Parnassius Smintheus Research Articles

Extremes of snow and temperature affect patterns of genetic diversity and differentiation in the alpine butterfly Parnassius smintheus.

Weather is an important short-term, local driver of population size and dispersal, which in turn contribute to patterns of genetic diversity and differentiation within species. Climate change is leading to greater weather variability and more frequent extreme weather events. While the effects of long-term and broad-scale mean climate conditions on genetic variation are well studied, our understanding of the effects of weather variability and extreme conditions on genetic variation is less developed. We assessed the influence of temperature and snow depth on genetic diversity and differentiation of populations of the alpine butterfly, Parnassius smintheus. We examined the relationships between a suite of variables, including those representing extreme conditions, and population-level genetic diversity and differentiation across 1453 single nucleotide polymorphisms, using both linear and gravity models. We additionally examined effects of land cover variables known to influence dispersal and gene flow in this species. We found that extreme low temperature events and the lowest recorded mean snow depth were significant predictors of genetic diversity. Extreme low temperature events, mean snow depth and land cover resistance were significant predictors of genetic differentiation. These results are congruent with known effects of early winter weather on population size and habitat connectivity on dispersal in P. smintheus. Our results demonstrate the potential for changes in the frequency or magnitude of extreme weather events to alter patterns of genetic diversity and differentiation.

Immigration allows population persistence and maintains genetic diversity despite an attempted experimental extinction.

Widespread fragmentation and degradation of habitats make organisms increasingly vulnerable to declines in population size. Immigration is a key process potentially affecting the rescue and persistence of populations in the face of such pressures. Field research addressing severe demographic declines in the context of immigration among interconnected local populations is limited owing to difficulties in detecting such demographic events and the need for long-term monitoring of populations. In a 17-subpopulation metapopulation of the butterfly, Parnassius smintheus, all adults observed in two adjacent patches were removed over eight consecutive generations. Despite this severe and long-term reduction in survival and reproduction, the targeted populations did not go extinct. Here, we use genetic data to assess the role of immigration versus in situ reproduction in allowing the persistence of these populations. We genotyped 471 samples collected from the targeted populations throughout the removal experiment at 152 single nucleotide polymorphisms. We found no reduction in the genetic diversity of the targeted populations over time, but a decrease in the number of loci in Hardy-Weinberg equilibrium, consistent with a high level of immigration from multiple surrounding populations. Our results highlight the role of connectivity and movement in making metapopulations resilient to even severe and protracted localized population reductions.

Population extinction and metapopulation synchrony: a reassessment

Synchronous dynamics of populations reduces metapopulation persistence. Thus, determining sources of synchrony is important for understanding metapopulations and biodiversity patterns in response to environmental disturbance. Previously, we found that the experimental extinction of two contiguous subpopulations of the butterfly Parnassius smintheus, increased synchrony among nearby subpopulations relative to distant controls. We hypothesized that increased synchrony was caused by either 1) a Moran‐like effect where the loss of immigrants simultaneously reduced the abundance of surrounding subpopulations or 2) an increase in dispersal among subpopulations surrounding the extinction. Reestablishment following extinction allowed for discrimination of these hypotheses. Additional data and new analyses using 24‐years of population growth in 12 nearby and control subpopulations before, during and after the experimental extinction show that our initial result was wrong. The ‘increase' in synchrony seen during the extinction was due to synchrony being low among treatment subpopulations during the pre‐extinction period, rather than an increase due to the experimental extinction. Lower synchrony among treatment subpopulations prior to extinction may have been due to less dispersal among treatment than among control subpopulations during the pre‐extinction period. Population crashes inducing synchrony (a Moran effect) during the extinction and post‐extinction periods also appear to have had greater and more lasting effects on synchrony for treatment than control subpopulations. Theoretical models show that local population extinction can increase synchrony in metapopulations, particularly for tightly regulated populations, but further experiments are needed to test this hypothesis.

Early Evidence for Sexually Dimorphic, Ultraviolet Eyespots in Parnassius Smintheus, Doubleday, [1847

Early Evidence for Sexually Dimorphic, Ultraviolet Eyespots in Parnassius Smintheus, Doubleday, [1847

Spatial variation in early‐winter snow cover determines local dynamics in a network of alpine butterfly populations

Snow cover is an extremely variable but critical component of alpine environments. We use long term population data on multiple small populations of the alpine butterfly Parnassius smintheus, combined with high‐resolution satellite imagery of meadows, to show a strong link between fine‐scale spatial and temporal variation in early‐winter snow cover and annual change in butterfly population size, accounting for up to 80 percent of the variation in annual population change. Snow cover in early winter for each meadow is the best predictor of annual adult population change, despite being estimated for a relatively short time‐window in late November. We identify a means by which subpopulation response to a local, short‐term weather variable can be assessed over a large spatial extent, but also at a resolution relevant to the biology and local dynamics of this alpine species.

Inclusion of trophic interactions increases the vulnerability of an alpine butterfly species to climate change

Climate change is expected to have significant and complex impacts on ecological communities. In addition to direct effects of climate on species, there can also be indirect effects through an intermediary species, such as in host-plant interactions. Indirect effects are expected to be more pronounced in alpine environments because these ecosystems are sensitive to temperature changes and there are limited areas for migration of both species (i.e. closed systems), and because of simpler trophic interactions. We tested the hypothesis that climate change will reduce the range of an alpine butterfly (Parnassius smintheus) because of indirect effects through its host plant (Sedum sp.). To test for direct and indirect effects, we used the simulations of climate change to assess the distribution of P. smintheus with and without Sedum sp. We also compared the projected ranges of P. smintheus to four other butterfly species that are found in the alpine, but that are generalists feeding on many plant genera. We found that P. smintheus gained distributional area in climate-only models, but these gains were significantly reduced with the inclusion of Sedum sp. and in dry-climate scenarios which resulted in a reduction in net area. When compared to the more generalist butterfly species, P. smintheus exhibited the largest loss in suitable habitat. Our findings support the importance of including indirect effects in modelling species distributions in response to climate change. We highlight the potentially large and still neglected impacts climate change can have on the trophic structure of communities, which can lead to significant losses of biodiversity. In the future, communities will continue to favour species that are generalists as climate change induces asynchronies in the migration of species.

Demographic fluctuations lead to rapid and cyclic shifts in genetic structure among populations of an alpine butterfly, Parnassius smintheus.

Many populations, especially in insects, fluctuate in size, and periods of particularly low population size can have strong effects on genetic variation. Effects of demographic bottlenecks on genetic diversity of single populations are widely documented. Effects of bottlenecks on genetic structure among multiple interconnected populations are less studied, as are genetic changes across multiple cycles of demographic collapse and recovery. We take advantage of a long-term data set comprising demographic, genetic and movement data from a network of populations of the butterfly, Parnassius smintheus, to examine the effects of fluctuating population size on spatial genetic structure. We build on a previous study that documented increased genetic differentiation and loss of spatial genetic patterns (isolation by distance and by intervening forest cover) after a network-wide bottleneck event. Here, we show that genetic differentiation was reduced again and spatial patterns returned to the system extremely rapidly, within three years (i.e. generations). We also show that a second bottleneck had similar effects to the first, increasing differentiation and erasing spatial patterns. Thus, bottlenecks consistently drive random divergence of allele frequencies among populations in this system, but these effects are rapidly countered by gene flow during demographic recovery. Our results reveal a system in which the relative influence of genetic drift and gene flow continually shift as populations fluctuate in size, leading to cyclic changes in genetic structure. Our results also suggest caution in the interpretation of patterns of spatial genetic structure, and its association with landscape variables, when measured at only a single point in time.

Direct estimates of metapopulation capacity from dispersal show high interannual variability, but little effect of recent forest encroachment on network persistence

CONTEXT: Habitat loss and isolation are leading threats for biodiversity. Alpine habitat throughout the world is being lost and fragmented by forest encroachment. Previous analysis of forest encroachment from 1952 to 1993 in a population network along Jumpingpound Ridge, Alberta, Canada showed a 78% loss in meadow area, resulting in an estimated 41% reduction in dispersal of the alpine butterfly Parnassius smintheus. OBJECTIVES: Here, we pursue three questions. First, has forest encroachment continued since 1993? Second, if so, has it affected butterfly dispersal? And third, have any changes altered estimates of metapopulation persistence of this species? METHODS: The area of each meadow and distance between each pair of meadows were determined in GIS using aerial photographs taken in 1952, 1993, 1999, 2008, and 2012. Mark-recapture (1995–2015) and landscape data were used to estimate annual butterfly dispersal and network persistence. RESULTS: Alpine meadows along Jumpingpound Ridge continued to be fragmented by encroaching forest showing a decrease in area and increase in the amount of forest between them. Annual dispersal parameters varied over the study, but the only consistent response to forest encroachment was an increase in male dispersal distance within meadow habitat. Estimates of metapopulation capacity also varied greatly among years due to variability in dispersal. The network was predicted to persist based on nearly all estimates. CONCLUSIONS: Metapopulation capacity is a potentially powerful tool for conservation, but interannual variability in dispersal hampers its utility under realistic conditions and could result in erroneous conclusions regarding metapopulation persistence. The 7 km long network of 18 subpopulations of Parnassius smintheus along the Jumpingpound Ridge and Cox Hill is currently at little risk of extinction due to forest encroachment.

UV-induced anthocyanin in the host plant Sedum lanceolatum has little effect on feeding by larval Parnassius smintheus

Climate change has resulted in shorter periods of snow cover in alpine meadows, increasing the duration of UV exposure. We established the relationship between increased exposure to UV light and anthocyanin pigment levels in host plant Sedum lanceolatum and tested whether increased exposure changed the feeding behavior of its herbivore Parnassius smintheus. Anthocyanin concentrations were significantly greater in plants exposed to UV. Under field conditions, we found a preference of P. smintheus caterpillars for plants with slightly above average levels of anthocyanin; however, no-choice feeding experiments in which larvae ranging from 1 to 3 days old were placed on UV-rich and UV-low plants showed no difference in feeding. These results indicate that the reduction of snow cover in alpine meadows will change the pigment profile of plants, but these changes may have little effect on herbivory.

Dispersing male Parnassius smintheus butterflies are more strongly affected by forest matrix than are females.

Dispersal is a central aspect of the ecology, evolution, and conservation of species. Predicting how species will respond to changing environmental conditions requires understanding factors that produce variation in dispersal. We explore one source of variation, differences between sexes within a spatial population network. Here, we compare the dispersal patterns of male and female Parnassius smintheus among 18 subpopulations over 8 years using the Virtual Migration Model. Estimated dispersal parameters differed between males and females, particularly with respect to movement through meadow and forest matrix habitat. The estimated dispersal distances of males through forest were much less than for females. Observations of female movement showed that, unlike males, females do not avoid forest nor does forest exert an edge effect. We explored whether further forest encroachment in this system would have different effects for males and females by fitting mean parameter estimates to the landscape configuration seen in 1993 and 2012. Despite differences in their dispersal due presumably to both habitat and physiological differences, males and females are predicted to respond in similar ways to reduced meadow area and increased forest isolation.

Climate and extreme weather independently affect population growth, but neither is a consistently good predictor

AbstractClimate change involves changes in mean temperature and precipitation as well as increases in extreme weather events; thus, determining how species will respond to climate change requires understanding how organisms respond to change in both mean and extreme conditions. Previously, we have shown that the growth of 21 interconnected populations of the alpine butterfly, Parnassius smintheus, is affected by prevailing climatic conditions during its overwintering period. More recently, we have shown that population growth is affected by extreme weather events during early overwintering. Here, we compare the descriptive and predictive abilities of models based on climate, weather, and their combination. We found that both climate‐ and weather‐based models explain significant, but independent, variation in year‐to‐year changes in population abundance; the combination of both was not better than either individual model. None of the models showed consistently good predictive ability. The climate model was accurate in predicting relatively small changes in year‐to‐year abundance, but not large changes. In contrast, the weather model was poor at predicting small changes in abundance, but accurately predicted large changes. Our results indicate that a more mechanistic approach, linking specific conditions to vital rates and population growth, will be needed to predict population responses to changing abiotic conditions.

Pivotal effect of early‐winter temperatures and snowfall on population growth of alpineParnassius smintheusbutterflies

AbstractGeographic range shifts in species’ distributions, due to climate change, imply altered dynamics at both their northern and southern range limits, or at upper and lower elevational limits. There is therefore a need to identify specific weather or climate variable(s), and life stages or cohorts on which they act, and how these affect population growth. Identifying such variables permits prediction of population increase or decline under a changing climate, and shifts in a species’ geographic range. For relatively well studied groups, such as butterflies, geographic range shifts are well documented, but weather variables and mechanisms causing those shifts are not well known. The Holarctic butterfly genusParnassius(Papilionidae) inhabits northern and alpine environments subject to variable and extreme weather. As such,Parnassiusspecies are vulnerable not only to long‐term changes in average conditions but especially to short‐term extreme weather events. We use population growth estimates for the alpine butterfly,Parnassius smintheus, from 21 populations in the Rocky Mountains of Canada over a 20‐yr interval combined with techniques of machine learning (randomForests) and parametric modeling to identify the important weather variables determining population growth. We do this to determine the seasons and life stages ofP. smintheusmost affected by climate change. Extreme minimum and maximum temperatures in November, in combination with November snowfall, affect annual population growth most, more so than do mean temperatures in November, and more so than weather at any other time of year. Populations decline both in years with low extreme minimum temperatures in November and especially in years with high extreme maximum temperatures in November, indicating that overwintering eggs are particularly vulnerable to early‐winter weather. Snowfall ameliorates the negative effects of extreme temperatures, particularly for extreme warm events. Results provide insight into biological mechanisms by which overwintering eggs might be affected by early winter weather. Short‐term extreme weather in November, acting on a single pivotal life stage (egg) is a far better predictor of population change of alpineP. smintheusbutterflies than is the general index of climate, the Pacific Decadal Oscillation.

Connectivity rescues genetic diversity after a demographic bottleneck in a butterfly population network

Demographic bottlenecks that occur when populations fluctuate in size erode genetic diversity, but that diversity can be recovered through immigration. Connectivity among populations and habitat patches in the landscape enhances immigration and should in turn facilitate recovery of genetic diversity after a sudden reduction in population size. For the conservation of genetic diversity, it may therefore be particularly important to maintain connectivity in the face of factors that increase demographic instability, such as climate change. However, a direct link between connectivity and recovery of genetic diversity after a demographic bottleneck has not been clearly demonstrated in an empirical system. Here, we show that connectivity of habitat patches in the landscape contributes to the maintenance of genetic diversity after a demographic bottleneck. We were able to monitor genetic diversity in a network of populations of the alpine butterfly, Parnassius smintheus, before, during, and after a severe reduction in population size that lasted two generations. We found that allelic diversity in the network declined after the demographic bottleneck but that less allelic diversity was lost from populations occupying habitat patches with higher connectivity. Furthermore, the effect of connectivity on allelic diversity was important during the demographic recovery phase. Our results demonstrate directly the ability of connectivity to mediate the rescue of genetic diversity in a natural system.

Persistence in a Two-Dimensional Moving-Habitat Model.

Environmental changes are forcing many species to track suitable conditions or face extinction. In this study, we use a two-dimensional integrodifference equation to analyze whether a population can track a habitat that is moving due to climate change. We model habitat as a simple rectangle. Our model quickly leads to an eigenvalue problem that determines whether the population persists or declines. After surveying techniques to solve the eigenvalue problem, we highlight three findings that impact conservation efforts such as reserve design and species risk assessment. First, while other models focus on habitat length (parallel to the direction of habitat movement), we show that ignoring habitat width (perpendicular to habitat movement) can lead to overestimates of persistence. Dispersal barriers and hostile landscapes that constrain habitat width greatly decrease the population's ability to track its habitat. Second, for some long-distance dispersal kernels, increasing habitat length improves persistence without limit; for other kernels, increasing length is of limited help and has diminishing returns. Third, it is not always best to orient the long side of the habitat in the direction of climate change. Evidence suggests that the kurtosis of the dispersal kernel determines whether it is best to have a long, wide, or square habitat. In particular, populations with platykurtic dispersal benefit more from a wide habitat, while those with leptokurtic dispersal benefit more from a long habitat. We apply our model to the Rocky Mountain Apollo butterfly (Parnassius smintheus).

A priori prediction of an extreme crash in 2015 for a population network of the alpine butterfly, Parnassius smintheus

Prediction provides important validation for scientific hypotheses and models. We update an existing model and present a priori predictions for the growth of a network of 21 populations of the butterfly Parnassius smintheus based on previous population size and climate during the overwintering period. The model predicts that the extremely warm, dry winter of 2015 in the Rocky Mountains will result in a network‐wide crash. All populations are expected to show extreme negative growth. Ten of 21 populations are expected to have less than one individual and the 95% confidence intervals of 17 of 21 populations are predicted to overlap zero in 2015. Given the unprecedented nature of climate change, these predictions represent the best estimate based on our understanding of the effects of climate and density‐dependence for the population growth for this species. If the predictions prove to be valid, it provides strong support for the predictive ability of the current model and the negative impact of extreme climatic events for the persistence of populations and ultimately species.

Predicting the effects of forest encroachment for Sedum lanceolatum and Rhodiola integrifolia at a subalpine ecotone

The elevation of treeline is rising in many areas throughout the world. Encroachment of forest into alpine regions fragments habitats and causes changes in microhabitat potentially altering the density and distribution of species. Our study investigates two species of alpine Crassulaceae, Sedum lanceolatum and Rhodiola integrifolia, as part of a larger project determining the effects of forest encroachment in the front ranges of the Rocky Mountains. Previous studies of S. lanceolatum showed a decrease in its density, but an increase in herbivory by larvae of the butterfly Parnassius smintheus with increasing distance from the treeline. To better understand the potential impact of forest encroachment on these species and the microhabitat associations of the plant species, we counted their abundance and determined soil depth, soil type, and dominant rock type in 8417 quadrats of 1 m2 area spaced at 10 m intervals throughout 17 alpine meadows along Jumpingpound Ridge, AB, Canada. Using a geographic information system we extracted slope, aspect, elevation, and distance from treeline for each quadrat. S. lanceolatum was abundant in these meadows and its density was influenced by all factors examined, predominantly through effects on soil moisture. Its positive association with treeline was primarily at high elevation in meadows with west-facing aspects. R. integrifolia had a more restricted distribution and relatively low density; it was most abundant in gravelly soils with north-facing aspects and little slope. Comparing the distribution of each species to a model predicting future forest encroachment indicates that both will lose habitat to forest encroachment. R. integrifolia is predicted to lose 31 % of its current habitat area. S. lanceolatum, which occurs across a broader range of microhabitats, is predicted to lose 19 % of its current habitat area to forest encroachment. These losses will negatively affect P. smintheus, but the overall impacts of forest encroachment on the butterfly are predicted to be minimal.

Ten years of abundance data within a spatial population network of the alpine butterfly, Parnassius smintheus

Spatial‐population networks (metapopulations sensu lato) have distinct properties from isolated populations. Within a population network, the abundance, persistence, and dynamics of local populations are affected by other populations within the network. Similarly, the abundance of local populations within the network has a strong effect on the dynamics and persistence of the entire network. In this data paper, we present ten years (1995–2004) of local‐population abundance and seven years of dispersal data within a spatial‐population network consisting of 21 local populations of the Rocky Mountain Apollo butterfly, Parnassius smintheus. Populations were located within alpine meadows above the treeline (≈2100 m) along Lusk (51.01° N, 114.97° W) and Jumpingpound Ridges (50.95° N, 114.91° W) in the front ranges of the Rocky Mountains in Alberta, Canada. Mark–recapture methods were used to monitor all populations in 1995 and 1996, and most populations in 1997 and from 2001–2004. For these years, abundance was estimated using Craig's method. In other years, population size was estimated via Pollard transects and converted to a common estimate of abundance based on a statistical relationship between transect counts and Craig's estimate. We present multiple estimates of abundance for most populations over the adult flight season each year, and the observed number of emigrants and immigrants over the flight season for populations in years where mark–recapture was conducted. These data should be useful in synthetic studies of factors affecting local‐population abundance within spatial‐population networks, landscape genetics, spatial‐population dynamics, and the persistence of spatial‐population networks.

Identifying Rare Montane Meadow Parnassian Butterfly Populations Across Grand Teton National Park, Wyoming

The pristine, protected ecosystem of Grand Teton National Park (GRTE) is the ideal location to study the relationships between butterfly populations and the habitats on which these insects depend. Two montane meadow butterfly species, Parnassius clodius and Parnassius smintheus, were investigated in this study to identify patterns of habitat occupancy relating to variables across GRTE and into the surrounding territory of Bridger–Teton National Forest (BTNF). Population dynamics of P. clodius have been intensively studied by our research group over several consecutive years in one isolated population in Grand Teton National Park. However, little has been investigated regarding the Parnassian butterflies’ population range across the GRTE ecosystem. For this study, presence-absence butterfly surveys were conducted across 45 meadow sites in preferred habitat during the Parnassius flight season (June – July 2013). We found that P. clodius occupied 80% of the meadows surveyed, which was far greater than was originally predicted. P. smintheus, the more rare Parnassian butterfly in the GRTE ecosystem, was only found at 9% of the meadows surveyed. Understanding population ranges and habitat limits of these butterfly populations will be useful for managers and scientists within GRTE, and will assist conservation efforts for other related Parnassian species that are threatened or endangered worldwide due to habitat loss and climate change.

Variability in winter climate and winter extremes reduces population growth of an alpine butterfly

We examined the long-term, 15-year pattern of population change in a network of 21 Rocky Mountain populations of Parnassius smintheus butterflies in response to climatic variation. We found that winter values of the broadscale climate variable, the Pacific Decadal Oscillation (PDO) index, were a strong predictor of annual population growth, much more so than were endogenous biotic factors related to population density. The relationship between PDO and population growth was nonlinear. Populations declined in years with extreme winter PDO values, when there were either extremely warm or extremely cold sea surface temperatures in the eastern Pacific relative to that in the western Pacific. Results suggest that more variable winters, and more frequent extremely cold or warm winters, will result in more frequent decline of these populations, a pattern exacerbated by the trend for increasingly variable winters seen over the past century.

Mating failure of female Parnassius smintheus butterflies: a component but not a demographic Allee effect

AbstractFemale mating success affects the ecology, evolution, and conservation of species. From a population dynamic perspective, female mating failure occurring due to low population density potentially translates into negative population growth, resulting in population extinction. Despite the implications, there have been surprisingly few comprehensive studies of both the causes and the population level effects of female mating failure for insects. Herein, we examined the mating success of female Parnassius smintheus Doubleday (Lepidoptera: Papilionidae) butterflies and its effects on population growth. Using mark‐recapture data amassed from 17 interconnected populations over 12 years, we assessed whether yearly female mating success varied with local population density, and whether population growth varied with mating success. We found that there was increased female mating failure at low population density – a component Allee effect. However, this effect did not result in a demographic Allee effect. We found that population growth was greatest at lowest densities and that there was no relationship between female mating success and population growth. These results along with a growing number of studies indicate that demographic Allee effects are much less common than component effects, and they may be relatively uncommon for insects in nature.