Climatic warming increases voltinism in European butterflies and moths

Climate change is altering geographical ranges, population dynamics and phenologies of many organisms. For ectotherms, increased ambient temperatures frequently have direct consequences for metabolic rates, activity patterns and developmental rates. Consequently, in many insect species both an earlier beginning and prolongation of seasonal duration occurred in parallel with recent global warming. However, from an ecological and evolutionary perspective, the number of generations (voltinism) and investment into each generation may be even more important than seasonality, since an additional generation per unit time may accelerate population growth or adaptation. Using a dataset extending back to the mid-nineteenth century, I report changes in the voltinism of butterfly and moth species of Central Europe. A significant proportion of 263 multi-voltine species showed augmented frequency of second and subsequent generations relative to the first generation in a warm period since 1980, and 44 species even increased the number of generations after 1980. Expected ecological consequences are diverse. Since multi-voltinism has been linked to insect outbreaks they include an increase in the abundance of herbivorous pests of agriculture and forestry. However, disruption of the developmental synchrony associated with multi-voltinism and host plant phenology may also reduce fitness, potentially having unexpected consequences for species of conservation concern. The ability of species to adapt evolutionarily to a changing environment may be facilitated by increased voltinism.     

Projecting insect voltinism under high and low greenhouse gas emission conditions

We develop individual-based Monte Carlo methods to explore how climate change can alter insect voltinism under varying greenhouse gas emissions scenarios by using input distributions of diapause termination or spring emergence, development rate, and diapause initiation, linked to daily temperature and photoperiod. We show concurrence of these projections with a field dataset, and then explore changes in grape berry moth, Paralobesia viteana (Clemens), voltinism that may occur with climate projections developed from the average of three climate models using two different future emissions scenarios from the International Panel of Climate Change (IPCC). Based on historical climate data from 1960 to 2008, and projected downscaled climate data until 2099 under both high (A1fi) and low (B1) greenhouse gas emission scenarios, we used concepts of P. viteana biology to estimate distributions of individuals entering successive generations per year. Under the low emissions scenario, we observed an earlier emergence from diapause and a shift in mean voltinism from 2.8 to 3.1 generations per year, with a fraction of the population achieving a fourth generation. Under the high emissions scenario, up to 3.6 mean generations per year were projected by the end of this century, with a very small fraction of the population achieving a fifth generation. Changes in voltinism in this and other species in response to climate change likely will cause significant economic and ecological impacts, and the methods presented here can be readily adapted to other species for which the input distributions are reasonably approximated.     

Latitudinal clines in alternative life histories in a geometrid moth

The relative roles of genetic differentiation and developmental plasticity in generating latitudinal gradients in life histories remain insufficiently understood. In particular, this applies to determination of voltinism (annual number of generations) in short‐lived ectotherms, and the associated trait values. We studied different components of variation in development of Chiasmia clathrata (Lepidoptera: Geometridae) larvae that originated from populations expressing univoltine, partially bivoltine or bivoltine phenology along a latitudinal gradient of season length. Indicative of population‐level genetic differentiation, larval period became longer while growth rate decreased with increasing season length within a particular phenology, but saw‐tooth clines emerged across the phenologies. Indicative of phenotypic plasticity, individuals that developed directly into reproductive adults had shorter development times and higher growth rates than those entering diapause. The most marked differences between the alternative developmental pathways were found in the bivoltine region suggesting that the adaptive correlates of the direct development evolve if exposed to selection. Pupal mass followed a complex cline without clear reference to the shift in voltinism or developmental pathway probably due to varying interplay between the responses in development time and growth rate. The results highlight the multidimensionality of evolutionary trajectories of life‐history traits, which either facilitate or constrain the evolution of integrated traits in alternative phenotypes.     

Alternative life histories in the water strider Gerris lacustris: time constraint on wing morph and voltinism

The wing dimorphic water strider Gerris lacustris L. (Heteroptera: Gerridae) switches to a bivoltine life cycle under favorable climatic conditions. The switch in voltinism is accompanied by a reduction of wing development in the directly reproducing midsummer generation, while the diapausing generation has a high fraction of long‐winged individuals. We investigated whether the thermal energy (degree‐days) available in natural habitats constrains the combination of developmental pathway and wing morph. Offspring of G. lacustris were reared under quasi‐natural conditions at two temperature regimes to determine the thermal constant k required to complete adult development in either wing morph. The thermal constant for egg‐to‐adult development of the short‐winged morph was about 20% lower than of the long‐winged morph. Based on the results from the outdoor laboratory experiment, we calculated the total degree‐days necessary to complete the possible combinations of wing morph pattern and voltinism. Comparison of these estimates with the thermal energy actually available during the reproductive season of 2004 for various natural habitats (sun‐exposed field ponds and shaded forest ponds) suggests that voltinism as well as wing morph pattern is strongly limited by the number of degree‐days available in these habitats. On forest ponds, only univoltine life cycles were possible, whereas on field ponds temperature allowed bivoltine life cycles. However, only the eggs laid at the very beginning of the season had the potential to accumulate enough degree‐days to complete a bivoltine life cycle with both generations long‐winged. We conclude that thermal energy is the main environmental constraint limiting voltinism of populations in the two habitat types. Furthermore, the available thermal energy also seems to influence the determination of the seasonal wing pattern in G. lacustris.     

Historical and projected interactions between climate change and insect voltinism in a multivoltine species

Climate change can cause major changes to the dynamics of individual species and to those communities in which they interact. One effect of increasing temperatures is on insect voltinism, with the logical assumption that increases in surface temperatures would permit multivoltine species to increase the number of generations per year. Though insect development is primarily driven by temperature, most multivoltine insect species rely on photoperiodic cues, which do not change from year‐to‐year or in response to climate warming, to initiate diapause. Thus, the relationship between climate change and voltinism could be complex. We use a phenology model for grape berry moth, Paralobesia viteana (Clemens), which incorporates temperature‐dependent development and diapause termination, and photoperiod‐dependent diapause induction, to explore historical patterns in year‐to‐year voltinism fluctuations. We then extend this model to predict voltinism under varying scenarios of climate change to show the importance of both the quality and quantity of accumulated heat units. We also illustrate that increases in mean surface temperatures > 2 °C can have dramatic effects on insect voltinism by causing a shift in the ovipositional period that currently is subject to diapause‐inducing photoperiods.     

Explaining the sawtooth: latitudinal periodicity in a circadian gene correlates with shifts in generation number

Many temperate insects take advantage of longer growing seasons at lower latitudes by increasing their generation number or voltinism. In some insects, development time abruptly decreases when additional generations are fit into the season. Consequently, latitudinal ‘sawtooth’ clines associated with shifts in voltinism are seen for phenotypes correlated with development time, like body size. However, latitudinal variation in voltinism has not been linked to genetic variation at specific loci. Here, we show a pattern in allele frequency among voltinism ecotypes of the European corn borer moth (Ostrinia nubilalis) that is reminiscent of a sawtooth cline. We characterized 145 autosomal and sex‐linked SNPs and found that period, a circadian gene that is genetically linked to a major QTL determining variation in post‐diapause development time, shows cyclical variation between voltinism ecotypes. Allele frequencies at an unlinked circadian clock gene cryptochrome1 were correlated with period. These results suggest that selection on development time to ‘fit’ complete life cycles into a latitudinally varying growing season produces oscillations in alleles associated with voltinism, primarily through changes at loci underlying the duration of transitions between diapause and other life history phases. Correlations among clock loci suggest possible coupling between the circadian clock and the circannual rhythms for synchronizing seasonal life history. We anticipate that latitudinal oscillations in allele frequency will represent signatures of adaptation to seasonal environments in other insects and may be critical to understanding the ecological and evolutionary consequences of variable environments, including response to global climate change.     

A population model for diapausing multivoltine insects under asymmetric cannibalism

Pupa-eating cannibalism occurs naturally in several insect species. Byasa alcinous is a multivoltine species of Red-bodied Swallowtail butterfly found in East Asia, which diapauses as pupa over the winter and whose larvae cannibalize eggs and pupae. We investigate the effects on population dynamics of increasing the asymmetric cannibalistic attack rate of a general insect species in different environmental conditions. We do this by theoretically formulating a generalized system of univoltine and bivoltine larvae over two generations in the spring and summer months. We predict that a lack of resources over the summer can force the population to become entirely univoltine, unless the second-generation bivoltine larvae increase their cannibalistic attack rate, and consume the diapausing pupae from the first generation. The model shows that under extreme environmental conditions, the persistence of univoltine larvae is favoured when faced with the threat of extinction. The model also predicts the conditions for the coexistence of both univoltine and bivoltine larvae, and the degree to which they can both coexist, which decreases as the resource in the second generation increases. This work provides the grounding for future theoretical and experimental consideration of the role of cannibalism in determining insect voltinism.     

Western pine beetle voltinism in a changing California climate

1. Recent hot droughts in California resulted in ponderosa pine (Pinus ponderosa) mortality attributed to drought and western pine beetle (WPB, Dendroctonus brevicomis). While drought alone can cause tree death, direct warming effects on WPB are a contributing factor. Research on WPB generation timing (voltinism), however, is lacking.
2. We monitored WPB tree attacks and adult emergence timing at two California sites and developed a degree-day model from field-observed data. Historical, contemporary, and future temperatures for several California sites were used with the model to examine trends in WPB voltinism.
3. Field data showed a single summer and an overwinter generation at a northern California site. As summer temperatures increased beyond 1900–1980 averages, the predicted number of full and partial WPB generations by 2021 had increased from ~2 annual (one summer and one overwinter) generations historically to ~2.3 at two northern California sites and from ~2.3 to ~3.2 at two warmer California sites.
4. Historical and contemporary data suggest winter warming was not sufficient for an additional generation overwinter. Instead, increases in generations were driven by summer and fall temperatures.
5. Unconstrained increases in the number of future annual generations will be limited by complex, but not well understood, WPB thermal adaptations. Increased knowledge of temperature-driven WPB population growth will improve forest vegetation models aimed at predicting ponderosa pine mortality in a changing climate.

     

Life‐history traits related to diapause in univoltine and bivoltine populations of Ypthima multistriata (Lepidoptera: Satyridae) inhabiting similar latitudes

In most temperate insects, diapause strategies and voltinism generally exhibit latitudinal clines, supporting the concept that they represent adaptations to climate. In contrast, in the satyrine butterfly Ypthima multistriata Butler, local populations with different voltinism patterns are geographically intermingled, suggesting that life‐history traits related to diapause may differ even between geographically and phylogenetically close populations. In this study, we experimentally examined the critical photoperiod for diapause induction and the larval developmental period in two univoltine and two bivoltine populations of Y. multistriata, all of which inhabit virtually the same latitude (34.652–34.750°N). We found that the critical photoperiod for diapause induction was longer in the univoltine populations than in the bivoltine populations. Moreover, the larval period under the long day length treatment was different among populations in both sexes, although significant differences were also detected between populations with the same voltinism. These results indicate that in Y. multistriata, life‐history traits related to diapause can not be attributed merely to climatic conditions such as temperature or day length, which depend largely on latitude. Therefore, we suggest that biotic elements, such as leaf toughness, as well as abiotic elements should be taken into account in attempts to explain the enigmatic pattern of geographic variation in the diapause strategies of Y. multistriata.     

Effects of climate change and crop planting structure on the abundance of cotton bollworm,Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae)

The interactions between plants and insects play an important role in ecosystems. Climate change and cropping patterns can affect herbivorous pest insect dynamics. Understanding the reasons for population fluctuations can help improve integrated pest management strategies. Here, a 25‐year dataset on climate, cropping planting structure, and the population dynamics of cotton bollworms (Helicoverpa armigera) from Bachu County, south Xinjiang, China, was analyzed to assess the effects of changes in climate and crop planting structure on the population dynamics of H. armigera. The three generations of H. armigera showed increasing trends in population size with climate warming, especially in the third generation. The relative abundances of the first and second generations decreased, but that of the third generation increased. Rising temperature and precipitation produced different impacts on the development of different generations. The population numbers of H. armigera increased with the increase in the non‐Bacillus thuringiensis (Bt) cotton‐planted area. Asynchrony of abrupt changes existed among climate change, crop flowering dates, and the phenology of H. armigera moths. The asynchronous responses in crop flowering dates and phenology of H. armigera to climate warming would expand in the future. The primary factors affecting the first, second, and third generations of moths were T_mean in June, the last appearance date of the second generation of moths, and the duration of the third generation of moths, respectively. To reduce the harm to crops caused by H. armigera, Bt cotton should be widely planted.     

Adaptation to the new land or effect of global warming? An age-structured model for rapid voltinism change in an alien lepidopteran pest

1. Hyphantria cunea Drury invaded Japan at Tokyo in 1945 and expanded its distribution gradually into northern and south-western Japan. All populations in Japan were bivoltine until the early 1970s, at which time trivoltine populations appeared in several southern regions. Presently, H. cunea exists as separate bivoltine and trivoltine populations divided around latitude 36 degrees . In the course of this voltinism change, the mean surface temperature in Japan rose by 1.0 degrees C. 2. To determine whether and how this temperature increase might be responsible for the voltinism change, we constructed an age-structured model incorporating growth speed driven by actual daily temperature and detailed mechanisms of diapause induction triggered by both daily photoperiod and temperature. 3. The simulation result suggests that both the acceleration of the growth speed and the prolongation of diapause induction are necessary to cause changes in voltinism, regardless of temperature increase. We concluded that the H. cunea population changed its life-history traits as an adaptation parallel with its invasion into the south-western parts of Japan. 4. Though the temperature increase had little effect on the fitness and heat stress in bivoltine and trivoltine populations, the trivoltine life cycle has become advantageous at least in marginal regions such as Tokyo.     

Heterodynamic processes in Coccinella septempunctata L. (Coccinellidae: Coleoptera): a mini review

Among ladybirds, diapause has evidently been most studied in Coccinella septempunctata L. adults. Coccinella septempunctata (C‐7), the seven spot, has attracted attention both in Europe and the USA for being heterogeneous as to the induction of diapause. A polyphenic character of diapause is a prominent feature in C. septempunctata and this phenomenon generally and often generates voltinism heterogeneity within populations. A greater part of the C‐7 population shows an obligatory univoltine cycle, whereas a smaller proportion is facultatively polyvoltine. Coccinella s. bruckii in Japan is bivoltine, in which the first generation of adults aestivate while the second generation hibernates. This paper reviews this heterodynamic cycle and its importance in the life history of C‐7, as reported from different regions of the world. Heterogeneous voltinism and diapause smooth the progress of a portion of C‐7 populations to take benefit of aphids well into late summer and autumn. Understanding such variation and plasticity in the life history of this species can help in organizing proper biological control attempts using it as a biocontrol agent.     

The influence of planting date,transgenic Bt maize and hybrid relative maturity on European corn borer Ostrinia nubilalis (Lepidoptera: Crambidae) ovipositional patterns

A three year study was carried out at Hoytville and at Wooster, Ohio, USA from 2006 to 2008 to investigate the influence of planting date, transgenic maize and hybrid maturity on Ostrinia nubilalis (Hubner) population dynamics and oviposition patterns. Maize plants were planted in late April or early May, mid‐May and early June during each year. The moth flight pattern showed bivoltine generations during the three years. The first moth flight peaked in June, with the populations declining during July. The second moth flight peaked in August and declined towards the end of September or early October. Egg mass density did not differ significantly between transgenic and non‐transgenic maize of different maturities. Significant differences were observed, however, among planting dates, sampling dates, and sampling date × planting date interactions. Generally higher numbers of egg masses from second generation moths were deposited on late planted maize than middle and early plantings.     

Modelling as a tool for analysing the temperature‐dependent future of the Colorado potato beetle in Europe

A warmer climate may increase the risk of attacks by insect pests on agricultural crops, and questions on how to adapt management practice have created a need for impact models. Phenological models driven by climate data can be used for assessing the potential distribution and voltinism of different insect species, but the quality of the simulations is influenced by a range of uncertainties. In this study, we model the temperature‐dependent activity and development of the Colorado potato beetle, and analyse the influence of uncertainty associated with parameterization of temperature and day length response. We found that the developmental threshold has a major impact on the simulated number of generations per year. Little is known about local adaptations and individual variations, but the use of an upper and a lower developmental threshold gave an indication on the potential variation. The day length conditions triggering diapause are known only for a few populations. We used gridded observed temperature data to estimate local adaptations, hypothesizing that cold autumns can leave a footprint in the population genetics by low survival of individuals not reaching the adult stage before winter. Our study indicated that the potential selection pressure caused by climate conditions varies between European regions. Provided that there is enough genetic variation, a local adaption at the northern distribution limit would reduce the number of unsuccessful initiations and thereby increase the potential for spreading to areas currently not infested. The simulations of the impact model were highly sensitive to biases in climate model data, i.e. systematic deviations in comparison with observed weather, highlightening the need of improved performance of regional climate models. Even a moderate temperature increase could change the voltinism of Leptinotarsa decemlineata in Europe, but knowledge on agricultural practice and strategies for countermeasures is needed to evaluate changes in risk of attacks.     

Climate change and voltinism of Mythimna sequax: the location and choice of phenological models matter

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Genetic and phenotypic sources of life history variation along a cline in voltinism in the cricket Allonemobius socius

Clinal variation in life histories can be genetically based, resulting from selection imposed by different environments, or it may be due to the differential expression of phenotypically plastic traits. We examined the cline in voltinism in the egg-diapausing cricket Allonemobius socius, with populations spanning the switch from a univoltine to a bivoltine phenology. A common garden experiment was employed, using environments that mimicked photoperiod and temperature conditions found in the field. There were only small differences in development time among populations, and the difference in phenology observed in the field is likely due to clinal variation in the length of the growing season. We found large genetically-based differences in the reaction norm for egg diapause that were further magnified by environmental cues. The synergism of genetic and environmental effects was an example of cogradient selection. In the zone of transition between phenologies, voltinism appeared to be a conditional strategy, rather than a genetic polymorphism. First-generation females from this area can lay either direct-developing or diapause eggs depending on the likelihood that a second generation will have sufficient time to develop. For this species, the cline in voltinism is the result of a combination of environmental effects on development, and genetic and environmental influences on egg diapause propensity.     

Geographical variation in insect developmental period: effect of host plant phenology on the life cycle of the bruchid seed feeder shape Kytorhinus sharpianus

The voltinism of the bruchid Kytorhinus sharpianus Bridwell (Coleoptera: Bruchidae) and the phenology of its host plant Sophora flavescens Aiton (Leguminosae) were observed at four latitudes: Aomori (40°46' N), Obanazawa (38°37' N), Kujiranami (37°21' N) and Mitsuma (36°05' N) in northeastern Honshu (Japan). Kytorhinus sharpianus life cycle ranged from bivoltine and partially trivoltine in the south to univoltine and partially bivoltine in the north. Sophora flavescens started growing later in spring at higher latitudes. However, the relative growth rate was higher in the north (Aomori) than in the south (Mitsuma). In parallel with this, the first-generation of adult K. sharpianus appeared later at higher latitudes. When the four local populations were reared at 24 °C, L16:D8 and 65% r.h., males developed faster than females. The mean developmental time showed a saw-toothed latitudinal cline. The reversion in the latitudinal trend of variation corresponded to the change in the major type of life cycles from univoltine to bivoltine. Two heat units throughout the year and post-fruiting period were calculated as the sums of degree-days above the developmental threshold (12 °C) of K. sharpianus. Both heat units decreased in parallel with each other with increasing latitude. The greater growth rate of hosts in the northern population compensated for the smaller heat units. In addition, when the heat units were divided by the degree-days needed to complete development, the numerical value was the approximate number of generations observed in each locality.     

Developmental threshold, day-degree requirements and voltinism of the aphid predator Episyrphus balteatus (Diptera: Syrphidae)

Episyrphus balteatus is the dominant syrphid predator of aphids in the UK, reestablishment of populations each season is mainly by migration from warmer climes, as overwintering in this country is minimal with an uncertain level of success. The effects of temperature on the developmental rate of E. balteatus were investigated to determine the potential voltinism of this species in the UK. Estimates of the developmental threshold temperature from oviposition to adult emergence varied between 6.0d?C and 7.1d?C with a day-degree (DD) requirement of between 256 and 280 depending on the method of analysis used. Using the DD requirement derived from a weighted linear regression (261 DD above a threshold of 6.8d?C) in combination with the required value from adult emergence to first oviposition, suggests a total requirement of approximately 374 DD above 6.8d?C per generation. These data, together with climate records, indicate that one to three generations are possible each year, depending on the available DD and origin of the population. The advantages and limitations of different approaches and models used to estimate developmental thresholds and DD requirements are discussed.     

Forest defoliator outbreaks under climate change: effects on the frequency and severity of outbreaks of five pine insect pests

To identify general patterns in the effects of climate change on the outbreak dynamics of forest‐defoliating insect species, we examined a 212‐year record (1800–2011) of outbreaks of five pine‐defoliating species (Bupalus piniarius, Panolis flammea, Lymantria monacha, Dendrolimus pini, and Diprion pini) in Bavaria, Germany for the evidence of climate‐driven changes in the severity, cyclicity, and frequency of outbreaks. We also accounted for historical changes in forestry practices and examined effects of past insecticide use to suppress outbreaks. Analysis of relationships between severity or occurrence of outbreaks and detrended measures of temperature and precipitation revealed a mixture of positive and negative relationships between temperature and outbreak activity. Two moth species (P. flammea and Dendrolimus pini) exhibited lower outbreak activity following years or decades of unusually warm temperatures, whereas a sawfly (Diprion pini), for which voltinism is influenced by temperature, displayed increased outbreak occurrence in years of high summer temperatures. We detected only one apparent effect of precipitation, which showed Dendrolimus pini outbreaks tending to follow drought. Wavelet analysis of outbreak time series suggested climate change may be associated with collapse of L. monacha and Dendrolimus pini outbreak cycles (loss of cyclicity and discontinuation of outbreaks, respectively), but high‐frequency cycles for B. piniarius and P. flammea in the late 1900s. Regional outbreak severity was generally not related to past suppression efforts (area treated with insecticides). Recent shifts in forestry practices affecting tree species composition roughly coincided with high‐frequency outbreak cycles in B. piniarius and P. flammea but are unlikely to explain the detected relationships between climate and outbreak severity or collapses of outbreak cycles. Our results highlight both individualistic responses of different pine‐defoliating species to climate changes and some patterns that are consistent across defoliator species in this and other forest systems, including collapsing of population cycles.