Regional climate on the breeding grounds predicts variation in the natal origin of monarch butterflies overwintering in Mexico over 38 years

Addressing population declines of migratory insects requires linking populations across different portions of the annual cycle and understanding the effects of variation in weather and climate on productivity, recruitment, and patterns of long‐distance movement. We used stable H and C isotopes and geospatial modeling to estimate the natal origin of monarch butterflies (Danaus plexippus) in eastern North America using over 1000 monarchs collected over almost four decades at Mexican overwintering colonies. Multinomial regression was used to ascertain which climate‐related factors best‐predicted temporal variation in natal origin across six breeding regions. The region producing the largest proportion of overwintering monarchs was the US Midwest (mean annual proportion = 0.38; 95% CI: 0.36–0.41) followed by the north‐central (0.17; 0.14–0.18), northeast (0.15; 0.11–0.16), northwest (0.12; 0.12–0.16), southwest (0.11; 0.08–0.12), and southeast (0.08; 0.07–0.11) regions. There was no evidence of directional shifts in the relative contributions of different natal regions over time, which suggests these regions are comprising the same relative proportion of the overwintering population in recent years as in the mid‐1970s. Instead, interannual variation in the proportion of monarchs from each region covaried with climate, as measured by the Southern Oscillation Index and regional‐specific daily maximum temperature and precipitation, which together likely dictate larval development rates and food plant condition. Our results provide the first robust long‐term analysis of predictors of the natal origins of monarchs overwintering in Mexico. Conservation efforts on the breeding grounds focused on the Midwest region will likely have the greatest benefit to eastern North American migratory monarchs, but the population will likely remain sensitive to regional and stochastic weather patterns.     

Intra‐population variation in the natal origins and wing morphology of overwintering western monarch butterflies Danaus plexippus

Understanding the natal origins of migratory animals is critical for understanding their population dynamics and conservation. However, quantitative estimates of population recruitment from different natal habitats can be difficult to assess for many species, especially those with large geographic ranges. These limitations hinder the evaluation of alternative hypotheses about the key movements and ecological interactions of migratory species. Here, we quantitatively investigated intra‐population variation in the natal origins of western North American monarch butterflies Danaus plexippus using spatial analyses of stable isotope ratios and correlations with wing morphology. A map of hydrogen isotope values in western monarch butterfly wings (δ²H_m) was estimated using a transfer function that relates the δ²H_m values of monarch butterfly wing keratin to a long‐term dataset of precipitation isotope (δ²H_p) values across the western United States. Isotopic analyses of 114 monarch butterfly wings collected at four California overwintering locations indicated substantial individual variation in natal origins, with most recruitment coming from broad regions along the Pacific coast, the southwestern US and the northern intermountain region. These observed patterns may partially resolve and reconcile several past hypotheses about the natal origins of western monarch butterflies, while also raising new questions. More negative δ²H_m values (associated with longer migratory distance) were significantly correlated with larger forewing sizes, consistent with expectations based on the aerodynamic and energetic costs of long‐distance migration, while analyses of wing shape suggest potential differences in the movement behaviors and constraints observed in the western range, compared with previous observations in eastern North America. Taken together, the results of this study indicate substantial individual variation in the natal origins of overwintering western monarch butterflies, suggesting both local and long‐distance movement to overwintering sites.     

Patterns of parasitism in monarch butterflies during the breeding season in eastern North America

1. Migratory behaviour can result in reduced prevalence of pathogens in host populations. Two hypotheses have been proposed to explain this relationship: (i) ‘migratory escape’, where migrants benefit from escaping pathogen accumulation in contaminated environments; and (ii) ‘migratory culling’, where the selective removal of infected individuals occurs during migration. 2. In the host–parasite system between the monarch butterfly (Danaus plexippus Linn.) and its obligate protozoan parasite Ophryocystis elektroscirrha (OE), there is evidence to support both hypotheses, particularly during the monarchs' autumn migration. However, these processes can operate simultaneously and could vary throughout the monarchs' annual migratory cycle. Assessing the relative strength for each hypothesis has not previously been done. 3. To evaluate both hypotheses, parasite infection prevalence was examined in monarchs sampled in eastern North America during April–September, and stable isotopes (δ²H, δ¹³C) were used to estimate natal origin and infer migration distance. There was stronger support for the migratory escape hypothesis, wherein infection prevalence increased over the breeding season and was higher at southern latitudes, where the breeding season tends to be longer compared with northern latitudes. Little support was found for the migratory culling hypothesis, as infection prevalence was similar whether monarchs travelled shorter or longer distances. 4. These results suggest that migration allows individuals to escape parasites not only during the autumn, as shown in previous work, but during the monarchs' spring and summer movements when they recolonise the breeding range. These results imply a potential fitness advantage to monarchs that migrate further north to exploit parasite‐free habitats.     

Effects of climate on fall migration phenology of monarch butterflies departing the northeastern breeding grounds in Canada

Monarch butterflies (Danaus plexippus) undergo an iconic multi-generational migration, traveling thousands of kilometers from the summer breeding grounds in southern Canada to overwintering sites in central Mexico. This migration phenomena can be affected by climate change, which may have important implications on fitness and ultimately populations status. We investigated the long-term trends in fall migration phenology of monarchs using a 25-year dataset collected along the coast of Lake Erie in Ontario, Canada. We also investigated local long-term trends in weather covariates that have the potential to influence migration phenology at this site. Patterns in standardized daily counts of monarchs were compared with local weather covariates using two methods (i.e., monthly averages and moving windows) to assess difference in outputs between analytical approaches. Our results suggest that monarch migration timing (migration midpoint, average peak, first peak, and late passage) and weather covariates have been consistent over time, in direct contrast to a similar study in Cape May, New Jersey, which showed a significant increase in both fall temperature and a 16- to 19-day shift in monarch migration timing. Furthermore, our results differed between analytical approaches. With respect to annual variability in air temperature, our monthly average analysis suggested that for each degree increase in September air temperature, late season passage would advance 4.71 days (±1.59 SE, p = .01). However, the moving window analysis suggested that this result is likely spurious and found no significant correlations between migration timing and any weather covariates. Importantly, our results caution against extrapolating the effects of climate change on the migration phenology of the monarch across study regions and the need for more long-term monitoring efforts to better understand regional drivers of variability in migration timing.     

The fall migration flyways of monarch butterflies in eastern North America revealed by citizen scientists

The migration of monarch butterflies (Danaus plexippus) from Canada and the United States to overwintering sites in Mexico is one of the world’s most amazing biological phenomena, although recent threats make it imperative that the resources needed by migrating monarchs be conserved. The most important first step in preserving migration resources—determining the migration flyways—is also the most challenging because of the large-scale nature of the migration. Prior attempts to determine the flyways using mark-recapture techniques with wing tags gave some clues, but this important information has never been fully obtainable until now. In 2005 the citizen-science program, Journey North, initiated a project that asked participants to record sightings of overnight roosts of monarchs during their fall migration, and this project now provides an ideal way to illustrate the flyways used by monarchs on their way to Mexico, with the assumption that roost locations indicate migration routes. We used 3 years of this data to elucidate the flyways on a continent-wide scale, that revealed two distinct flyways, but only one appears to lead directly to Mexico. This main, ‘central’ flyway begins in the American Midwest states and southern Ontario, then continues south-southwest through the states of Kansas, Missouri, Oklahoma and Arkansas, and finally passes through Texas and northern Mexico. These data also highlighted a separate, smaller flyway along the eastern and coastal states, but there was a noticeable lack of roost sightings in this flyway at lower latitudes. Since there are few recoveries of marked monarchs in Mexico originating from coastal areas, we compared the timing of roost formation in this ‘eastern’ flyway with the main, central flyway. Roosts in the eastern flyway lagged behind the central roosts in timing, suggesting that monarchs traveling in this flyway have a reduced chance of making it to the Mexico wintering site. Combined, our evidence indicates that locations in the central flyway should be considered priority areas for conserving migration resources.     

Differences in phenotypic traits and migratory strategies between eastern North American monarch butterflies,Danaus plexippus (L.)

The eastern North American population of the monarch butterfly (Danaus plexippus plexippus) has different migratory routes. The majority fly to overwintering colonies in Mexico and others take an eastern route through Florida and Cuba. Monarchs migrating through Florida–Cuba do not overwinter and are mostly found nectaring and flying close to vegetation. This present study explores whether Florida–Cuba versus Mexican migrants differ in (1) phenotypic traits important for migration (e.g. wing size and condition, lipid and lean mass content, and reproductive status) and (2) migratory strategies. The monarch natal grounds (e.g. migrants versus residents) were determined through thin‐layer chromatography cardenolide fingerprint and stable isotopes (hydrogen δ²H and carbon δ¹³C). In addition, wing size and condition, lipid and lean mass, and reproductive status were determined. The results suggest that Mexican migrants are better suited for longer sustained flights and successful overwinter periods as a result of larger wings in better condition, reproductive diapause, and significant fat content. By contrast, Florida–Cuba migrants are more suited for shorter flights and opportunistic migratory strategies, given that their wings were in poor condition, as well as the active reproductive status of > 50% of these butterflies and their significantly low fat content. Eastern monarch migration is more complex and diverse than previously assumed. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Alpine biogeography of Parnassian butterflies during Quaternary climate cycles in North America

Growth of alpine glaciers during the Pleistocene had profound effects on montane landscapes in North America and the organisms now inhabiting alpine ecosystems. Biogeography of this region has often been viewed as a system of sky islands despite the fact that species richness patterns deviate from a strict island biogeographic model. One explanation is that alpine species are not in equilibrium because of late Quaternary geographic range shifts. Genetic data can provide evidence of nonequilibrium dynamics and the distributional shifts that occur during glaciation events in alpine landscapes. Using mitochondrial and nuclear sequence data, we examine the evolutionary history of butterflies in the Parnassius phoebus complex. We test explicit, alternative models of the biogeographic history of Parnassius smintheus and Parnassius behrii , including an equilibrium island model, ancestral radiation and fragmentation, an expanding alpine archipelago and an alpine archipelago refuge model. Our results support the alpine archipelago refuge model, in which alpine butterflies undergo population contraction during glacial climates followed by population expansion during interglacial phases. While butterflies can disperse between distant mountain ranges during glacial periods, gene flow is rare. We find evidence of recent connectivity between California and Colorado, population expansion events following deglaciation ∼20 000 years B.P., and small population sizes during the last glacial period. An analysis of lineage splitting suggests that morphological differences in P. smintheus and P. behrii are the result of late Pleistocene divergence (∼48 000 years B.P.) with limited gene flow. Our results demonstrate that spatially complex and nonequilibrium population dynamics influence alpine diversity patterns.     

Distribution of the monarch butterfly, Danaus plexippus (L.) (Lepidoptera: Nymphalidae), in western North America

The standard model for the migration of the monarch butterfly in western North America has hitherto been movement in the autumn to overwintering sites in coastal California, followed by a return inland by most individuals in the spring. This model is based largely on observational and limited tagging and recovery data. In this paper we test the model by plotting many years of museum and collection records on a monthly basis on a map of the region. Our plots suggest a movement of Oregon, Washington and other north-western populations of summer butterflies to California in the autumn, but movement of more north-easterly populations (e.g. from Idaho and Montana) along two pathways through Nevada, Utah and Arizona to Mexico. The more westerly of these two pathways may follow the Colorado River south as indicated by museum records and seasonal temperature data. The eastern pathway may enter northern Utah along the western scarp of the Wasatch Mountains and run south through Utah and Arizona. Further analysis of distributions suggests that monarch butterflies in the American West occur primarily along rivers, and there are observations indicating that autumn migrants often follow riparian corridors. More data are needed to test our new model; we suggest the nature of the data required.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 491–500.     

Are female monarch butterflies declining in eastern North America? Evidence of a 30-year change in sex ratios at Mexican overwintering sites

Every autumn the entire eastern North American population of monarch butterflies (Danaus plexippus) undergoes a spectacular migration to overwintering sites in the mountains of central Mexico, where they form massive clusters and can number in the millions. Since their discovery, these sites have been extensively studied, and in many of these studies, monarchs were captured and sexes recorded. In a recent effort to compile the sex ratio data from these published records, a surprising trend was found, which appears to show a gradual decline in proportion of females over time. Sex ratio data from 14 collections of monarchs, all spanning 30 years and totaling 69 113 individuals, showed a significant negative correlation between proportion of females and year (r = −0.69, p = 0.007). Between 1976 and 1985, 53 per cent of overwintering monarchs were female, whereas in the last decade, 43 per cent were female. The relationship was significant with and without weighting the analyses by sampling effort. Moreover, analysis of a recent three-year dataset of sex ratios revealed no variation among nine separate colonies, so differences in sampling location did not influence the trend. Additional evidence from autumn migration collections appears to confirm that proportions of females are declining, and also suggests the sex ratio is shifting on breeding grounds. While breeding monarchs face a number of threats, one possibility is an increase in prevalence of the protozoan parasite, Ophryocystis elektroscirrha, which recent evidence shows affects females more so than males. Further study will be needed to determine the exact cause of this trend, but for now it should be monitored closely.     

Ecological niches in sequential generations of eastern North American monarch butterflies (Lepidoptera: Danaidae): the ecology of migration and likely climate change implications

Eastern North American monarch butterflies (Danaus plexippus L.) show a series of range shifts during their breeding season. Using ecological niche modeling, we studied the environmental context of these shifts by identifying the ecological conditions that monarchs use in successive summer months. Monarchs use a consistent ecological regimen through the summer, but these conditions contrast strikingly with those used during the winter. Hence, monarchs exhibit niche-following among sequential breeding generations but niche-switching between the breeding and overwintering stages of their annual cycle. We projected their breeding ecological niche onto monthly future climate scenarios, which indicated northward shifts, particularly at the northern extreme of their summer movements, over the next 50 yrs; if both monarchs and their milkweed host plants cannot track these changing climates, monarchs could lose distributional area during critical breeding months.     

Spatial variation in demography and population growth rate: the importance of natal location

1. Understanding the pattern and magnitude of spatial variation in demography and population growth rate (lambda) is key to understanding the structure and dynamics of natural populations. However, such spatial variation is challenging to quantify. We use>20 years of individual life-history data to quantify small- and large-scale spatial variation in demography and lambda within a single population of red-billed choughs Pyrrhocorax pyrrhocorax on Islay, Scotland. Critically, we demonstrate a major importance of an individual's natal rather than current location in driving observed spatial variation. 2. Breeding success (the number of offspring fledged per breeding attempt) varied among individual chough nest sites but did not vary on a larger spatial scale across Islay. 3. The proportion of fledglings observed to survive to recruiting age varied markedly among individual nest sites and also varied more widely across Islay. Spatial capture-mark-recapture models defined two discrete geographical regions where fledgling survival differed significantly: choughs fledged in region 'BGE' were more likely to survive than choughs fledged in region 'CNSW' as both subadults and adults. 4. The asymptotic lambda attributable to breeding attempts in region BGE exceeded unity, and exceeded that attributable to breeding attempts in region CNSW. Relatively productive and unproductive regions therefore exist within this population. 5. Spatial variation in adult survival was better explained by an individual's natal region than the region where that individual settled to breed. Spatial variation in lambda would consequently have remained undetected had survival been measured across resident breeders rather than across individuals fledged in each region. Furthermore, breeding success was a weak predictor of a nest site's estimated productivity of recruits. 6. We therefore describe marked spatial variation in demography and lambda within a single population of a territorial vertebrate, mediated partly by long-term links between an individual's natal location and its subsequent life-history. Life-long monitoring of individuals of known origin may therefore be necessary to identify accurately subpopulations of intrinsically high and low lambda.     

Sources of variation for nutritional condition indices of the plasma of migratory lesser kestrels in the breeding grounds

Although published information on reference values for biochemical parameters in birds of prey has increased during the last years, little is known on their sources of variation. We used an insectivorous and small migratory raptor species, the lesser kestrel Falco naumanni, as a model. We looked for sources of variation of nutritional biochemical parameters (i.e. triglycerides, cholesterol, uric acid and urea) of both nestlings and adults. Reference values indicated that, as a rule, lesser kestrel showed more elevated triglycerides, urea and uric acid levels than other raptors. All analyzed factors except gender (i.e. year, colony, sampling time, presence/absence of a geolocator, body mass, laying date and capture date) reached significance for at least one biochemical parameter. In the morning, we found an important postprandial increase in the concentration of all biochemical parameters in nestlings, and uric acid and urea levels in adults. A positive relationship was detected between triglycerides and body mass in nestlings and adults. Although we did not find differences between blood biochemical parameters of the oldest and youngest chick of each brood, we found that cholesterol levels were lower in nestlings from larger broods. Coloration of tarsi (measured as brightness) was related to triglycerides and urea levels of nestlings and adults, respectively. The feeding habits of lesser kestrel probably explain the different levels and patterns of variation of metabolites in comparison to more carnivorous raptors eating mammals or birds.     

Nestedness and migratory status of avian assemblages in North America and Europe

We examine patterns of nestedness and species incidence for the resident and migrant components of avifaunas in North America and Europe. While all assemblages were significantly nested, there were no significant differences between North American and European avifaunas overall in nestedness or incidence. Residents did not differ from migrants in their adherence to a nested distribution, but did exhibit significantly higher incidences when continental affiliation was ignored.¶We develop a new nestedness index that examines each species' relative contribution to an assemblage's overall pattern of nestedness. The relative nestedness index exhibits a quadratic relationship with incidence such that species with low incidences and species with high incidences generally increase the overall level of nestedness, while species with intermediate incidence tend to decrease nestedness.     

Vulnerability of riparian ecosystems to elevated CO2 and climate change in arid and semiarid western North America

Riparian ecosystems, already greatly altered by water management, land development, and biological invasion, are being further altered by increasing atmospheric CO₂ concentrations ([CO₂]) and climate change, particularly in arid and semiarid (dryland) regions. In this literature review, we (1) summarize expected changes in [CO₂], climate, hydrology, and water management in dryland western North America, (2) consider likely effects of those changes on riparian ecosystems, and (3) identify critical knowledge gaps. Temperatures in the region are rising and droughts are becoming more frequent and intense. Warmer temperatures in turn are altering river hydrology: advancing the timing of spring snow melt floods, altering flood magnitudes, and reducing summer and base flows. Direct effects of increased [CO₂] and climate change on riparian ecosystems may be similar to effects in uplands, including increased heat and water stress, altered phenology and species geographic distributions, and disrupted trophic and symbiotic interactions. Indirect effects due to climate‐driven changes in streamflow, however, may exacerbate the direct effects of warming and increase the relative importance of moisture and fluvial disturbance as drivers of riparian ecosystem response to global change. Together, climate change and climate‐driven changes in streamflow are likely to reduce abundance of dominant, native, early‐successional tree species, favor herbaceous species and both drought‐tolerant and late‐successional woody species (including many introduced species), reduce habitat quality for many riparian animals, and slow litter decomposition and nutrient cycling. Climate‐driven changes in human water demand and associated water management may intensify these effects. On some regulated rivers, however, reservoir releases could be managed to protect riparian ecosystem. Immediate research priorities include determining riparian species' environmental requirements and monitoring riparian ecosystems to allow rapid detection and response to undesirable ecological change.     

Potential distributional shifts in North America of allelopathic invasive plant species under climate change models

Predictive studies play a crucial role in the study of biological invasions of terrestrial plants under possible climate change scenarios. Invasive species are recognized for their ability to modify soil microbial communities and influence ecosystem dynamics. Here, we focused on six species of allelopathic flowering plants—Ailanthus altissima, Casuarina equisetifolia, Centaurea stoebe ssp. micranthos, Dioscorea bulbifera, Lantana camara, and Schinus terebinthifolia—that are invasive in North America and examined their potential to spread further during projected climate change. We used Species Distribution Models (SDMs) to predict future suitable areas for these species in North America under several proposed future climate models. ENMEval and Maxent were used to develop SDMs, estimate current distributions, and predict future areas of suitable climate for each species. Areas with the greatest predicted suitable climate in the future include the northeastern and the coastal northwestern regions of North America. Range size estimations demonstrate the possibility of extreme range loss for these invasives in the southeastern United States, while new areas may become suitable in the northeastern United States and southeastern Canada. These findings show an overall northward shift of suitable climate during the next few decades, given projected changes in temperature and precipitation. Our results can be utilized to analyze potential shifts in the distribution of these invasive species and may aid in the development of conservation and management plans to target and control dissemination in areas at higher risk for potential future invasion by these allelopathic species.     

Life-history variation and adaptation in the historically mobile plant Arabidopsis thaliana (Brassicaceae) in North America

We used field-collected seeds of Arabidopsis thaliana (Brassicaceae) to simulate a colonization event of plants from diverse locations into a common environment to compare regionally "local" and "foreign" populations of this historically mobile species. Life history varied among regional groups, but most variation was found among populations within regions. While we found significant differences among populations and regional groups for important life-history characters, we did not find significant differences in performance of plants from different populations or regional groups. Rather, we found evidence that differences in life history contributed to the ability of plants from foreign regions to perform comparably to local Kentucky plants. Had plants from different regions not differed in the timing and size of reproduction, we would have seen that Kentucky (local) plants had higher total fitness via greater reproductive success of individuals that survived to reproduce and that Michigan plants would have had the lowest fitness. The populations are comparably adapted to the environment in Kentucky but through different combinations of life-history characters. Therefore, the life-history variation in this mobile species appears to contribute not to fitness differences among populations but rather to success in colonizing new locations.