Current temporal trends in moth abundance are counter to predicted effects of climate change in an assemblage of subarctic forest moths

Changes in climate are influencing the distribution and abundance of the world's biota, with significant consequences for biological diversity and ecosystem processes. Recent work has raised concern that populations of moths and butterflies (Lepidoptera) may be particularly susceptible to population declines under environmental change. Moreover, effects of climate change may be especially pronounced in high latitude ecosystems. Here, we examine population dynamics in an assemblage of subarctic forest moths in Finnish Lapland to assess current trajectories of population change. Moth counts were made continuously over a period of 32 years using light traps. From 456 species recorded, 80 were sufficiently abundant for detailed analyses of their population dynamics. Climate records indicated rapid increases in temperature and winter precipitation at our study site during the sampling period. However, 90% of moth populations were stable (57%) or increasing (33%) over the same period of study. Nonetheless, current population trends do not appear to reflect positive responses to climate change. Rather, time‐series models illustrated that the per capita rates of change of moth species were more frequently associated negatively than positively with climate change variables, even as their populations were increasing. For example, the per capita rates of change of 35% of microlepidoptera were associated negatively with climate change variables. Moth life‐history traits were not generally strong predictors of current population change or associations with climate change variables. However, 60% of moth species that fed as larvae on resources other than living vascular plants (e.g. litter, lichen, mosses) were associated negatively with climate change variables in time‐series models, suggesting that such species may be particularly vulnerable to climate change. Overall, populations of subarctic forest moths in Finland are performing better than expected, and their populations appear buffered at present from potential deleterious effects of climate change by other ecological forces.     

Tell me what you eat and I'll tell you when you fly: diet can predict phenological changes in response to climate change

Changes in phenology are correlated with climate change. However, we still struggle to understand the traits making species susceptible to climate change, and the implications of species' reactions for communities and food webs. Butterflies and moths are an ecologically important group that have shown pronounced phenological changes over the last decades. Tests using a > 150-year dataset from 566 European butterfly and moth species demonstrated that variation in phenological change was strongly related to traits describing plant-herbivore interactions (larval diet breadth, diet composition), and the life cycle. The results indicate that climate change related shifts in phenology are correlated with the seasonal availability and palatability of food plants. Lepidopterans feeding on herbaceous plants showed smaller shifts in flight periods but larger increases in voltinism than lepidopterans feeding on woody plants. Consequently, the effect of herbivorous lepidopterans may increase in herb-rich grassland ecosystems under warmer conditions, and not in forest ecosystems.     

Diel behavior in moths and butterflies: a synthesis of data illuminates the evolution of temporal activity

Lepidoptera (butterflies and moths) are one of the most taxonomically diverse insect orders with nearly 160,000 described species. They have been studied extensively for centuries and are found on nearly all continents and in many environments. It is often assumed that adult butterflies are strictly diurnal and adult moths are strictly nocturnal, but there are many exceptions. Despite the broad interest in butterflies and moths, a comprehensive review of diel (day-night) activity has not been conducted. Here, we synthesize existing data on diel activity in Lepidoptera, trace its evolutionary history on a phylogeny, and show where gaps lie in our knowledge. Diurnality was likely the ancestral condition in Lepidoptera, the ancestral heteroneuran was likely nocturnal, and more than 40 transitions to diurnality subsequently occurred. Using species diversity estimates across the order, we predict that roughly 75-85% of Lepidoptera are nocturnal. We also define the three frequently used terms for activity in animals (diurnal, nocturnal, crepuscular), and show that literature on the activity of micro-moths is significantly lacking. Ecological factors leading to nocturnality/diurnality is a compelling area of research and should be the focus of future studies.     

Mobility is related to species traits in noctuid moths

1. Mobility is important for the understanding of how species survive in fragmented landscapes and cope with increasing rates of habitat and climate change. However, mobility is a difficult trait to explore and is poorly known in most taxa. Species traits have been studied in relation to range shifts, extinction risks, and responses to habitat area and isolation, and have also been suggested as good estimators of mobility. Here we explore the relation between mobility and species traits in noctuid moths. 2. We sampled noctuid moths by an automatic light‐trap on an island far out in the Baltic Sea. We compared traits of the non‐resident species on the island with traits of a species pool of assumed potential migrants from the Swedish mainland. 3. Mobility was significantly related to adult activity period, length of flight period, and the interaction between host‐plant specificity and distribution area. Widely distributed host‐plant generalists were more mobile than host‐plant specialists with more restricted distribution, and species with an adult activity period in August to September moved to the island to a higher extent than species with an adult activity period in May to July. Our results remained qualitatively robust in additional analyses, after controlling for phylogeny and including all species recorded on the island, except for the trait ‘length of flight period’. 4. Our results highlight the importance of the relation between mobility and species traits. Noctuid moths with certain traits move over longer distances than earlier known. This finding is important to include when predicting range dynamics in fragmented and changing landscapes, and when conservation measures of species are devised.     

Investment in sensory structures,testis size,and wing coloration in males of a diurnal moth species: trade-offs or correlated growth?

For dioecious animals, reproductive success typically involves an exchange between the sexes of signals that provide information about mate location and quality. Typically, the elaborate, secondary sexual ornaments of males signal their quality, while females may signal their location and receptivity. In theory, the receptor structures that receive the latter signals may also become elaborate or enlarged in a way that ultimately functions to enhance mating success through improved mate location. The large, elaborate antennae of many male moths are one such sensory structure, and eye size may also be important in diurnal moths. Investment in these traits may be costly, resulting in trade‐offs among different traits associated with mate location. For polyandrous species, such trade‐offs may also include traits associated with paternity success, such as larger testes. Conversely, we would not expect this to be the case for monandrous species, where sperm competition is unlikely. We investigated these ideas by evaluating the relationship between investment in sensory structures (antennae, eye), testis, and a putative warning signal (orange hindwing patch) in field‐caught males of the monandrous diurnal painted apple moth Teia anartoides (Lepidoptera: Lymantriidae) in southeastern Australia. As predicted for a monandrous species, we found no evidence that male moths with larger sensory structures had reduced investment in testis size. However, contrary to expectation, investment in sensory structures was correlated: males with relatively larger antennae also had relatively larger eyes. Intriguingly, also, the size of male orange hindwing patches was positively correlated with testis size.     

Breathing some air into the single-species vacuum: multi-species responses to environmental change

Studies of ecological responses to climate change have often analysed species independently of each other, yet interactions between species are fundamental aspects of ecology. Mutshinda, O'Hara & Woiwod (2011) used light-trapping data for Lepidoptera (moths) to examine population responses to intraspecific effects and effects of winter rainfall and temperature. They show how Bayesian hierarchical models can analyse residual correlations among species' responses, illustrating an approach to account for and measure dependencies that are not fully explained by the candidate explanatory variables. A key result is that the responses of the different moth species did not appear to have strong residual correlation (Mutshinda, O'Hara & Woiwod 2011). These analyses provide an approach for synthesising across species and can better inform ecological responses to environmental change.     

An indicator highlights seasonal variation in the response of Lepidoptera communities to warming

The impacts of climate change on species and ecosystems are increasingly evident. While these tend to be clearest with respect to changes in phenology and distribution ranges, there are also important consequences for population sizes and community structure. There is an urgent need to develop ecological indicators that can be used to detect climate-driven changes in ecological communities, and identify how those impacts may vary spatially. Here we describe the development of a new community-based seasonal climate change indicator that uses national population and weather indices. We test this indicator using Lepidopteran and co-located weather data collected across a range of UK Environmental Change Network (ECN) sites. We compare our butterfly indicator with estimates derived from an alternative, previously published metric, the Community Temperature Index (CTI).First, we quantified the effect of temperature on population growth rates of moths and butterflies (Species Temperature Response, STR) by modelling annual variation in national population indices as a function of nationally averaged seasonal variation in temperature, using species and weather data independent of the ECN data. Then, we calculated average STRs for annually summarised species data from each ECN site, weighted by species’ abundance, to produce the Community Temperature Response (CTR). Finally, we tested the extent to which CTR correlated with spatial variation in temperature between sites and the extent to which temporal variation in CTR tracked both annual and seasonal warming trends.Mean site CTR was positively correlated with mean site temperature for moths but not butterflies. However, spatial variation in moth communities was well explained by mean site summer temperature and butterfly communities by winter temperature, respectively accounting for 74% and 63% of variation. Temporal variation in moth and butterfly CTR within sites did not vary with the mean annual temperature but responded to variation in the mean temperature of specific seasons. There were positive correlations between moth seasonal CTRs and seasonal temperatures in winter, spring and summer; and butterfly seasonal CTRs and seasonal temperatures in winter and summer. Butterfly CTR and CTI both correlated spatially and temporally with winter temperature.Our results highlight the need for seasonality to be considered when examining the impact of climate change on communities. Seasonal CTRs may be used to track the impact of changing temperatures on biodiversity and help identify potential mechanisms by which climate change is affecting communities. In the case of Lepidoptera, our results suggest that future warming may reassemble Lepidoptera communities.     

Leaf‐trait plasticity and species vulnerability to climate change in a Mongolian steppe

Climate change is expected to modify plant assemblages in ways that will have major consequences for ecosystem functions. How climate change will affect community composition will depend on how individual species respond, which is likely related to interspecific differences in functional traits. The extraordinary plasticity of some plant traits is typically neglected in assessing how climate change will affect different species. In the Mongolian steppe, we examined whether leaf functional traits under ambient conditions and whether plasticity in these traits under altered climate could explain climate‐induced biomass responses in 12 co‐occurring plant species. We experimentally created three probable climate change scenarios and used a model selection procedure to determine the set of baseline traits or plasticity values that best explained biomass response. Under all climate change scenarios, plasticity for at least one leaf trait correlated with change in species performance, while functional leaf‐trait values in ambient conditions did not. We demonstrate that trait plasticity could play a critical role in vulnerability of species to a rapidly changing environment. Plasticity should be considered when examining how climate change will affect plant performance, species' niche spaces, and ecological processes that depend on plant community composition.     

Invading and resident defoliators in a changing climate: cold tolerance and predictions concerning extreme winter cold as a range‐limiting factor

1. Winter temperatures in northern latitudes are predicted to increase markedly as a result of ongoing climate change, thus making the invasion of new insect defoliators possible. The establishment of new outbreak pest species may have major effects on northern ecosystems that are particularly sensitive to disturbances. 2. Effects of winter minimum temperatures under field and laboratory conditions were examined and limitations by minimum temperatures on future range expansion were investigated for invasive [Operophtera brumata (Lepidoptera: Geometridae)] and potentially invasive [Agriopis aurantiaria (Lepidoptera: Geometridae)] birch‐feeding forest pests. The results for the studied invasive and potentially invasive moths were compared with the parameters of the resident moth species Epirrita autumnata (Lepidoptera: Geometridae). 3. The results showed tolerated critical temperatures of the invader (O. brumata) and the resident (E. autumnata) were more similar (differing only by 1 °C), whereas the potential invader (A. aurantiaria) was much less tolerant of cold temperatures. Although describing different stages of overwintering, results were consistent between laboratory and field studies except for those at one field location, at which other abiotic conditions are suggested to have significant influence on moth egg survival. 4. Based on the present results and expected changes in winter temperatures over the next 30 years, the range expansion of an established invasive species may be predicted. No limitations were found regarding the possible future invasion of a new pest species to northern Fennoscandia. The importance of studying a species' whole overwintering period is highlighted and further studies devoted to the effects of other abiotic factors in addition to the effects of temperature are suggested.     

Life‐history traits and climatic responsiveness in noctuid moths

Emergence phenology has been shown to advance considerably in the past decades in many lepidopterans. Noctuid moths (Noctuidae) constitute a species‐rich family of lepidopterans with a large diversity of life history traits presumably driving climatic responsiveness. In our study we aim to assess the role of life‐history and ecological traits in climatic responsiveness of noctuid moths, whilst controlling for phylogenetic dependence. We used a long‐term dataset of European noctuid moths collected from a light‐trap in northeastern Hungary. As the study site is located at the intersection of several biogeographical zones harbouring a large number of noctuid moth species, our dataset provides a unique possibility to investigate the moths’ climatic sensitivity. To estimate the role of life‐history traits and ecological factors in driving lepidopterans’ response to climatic trends, we employed three proxies related to the species’ ecology (habitat affinity, food plant specialization and food type) and two robust types of life‐history traits (migration strategy and hibernation form). The degree of temporal shifts of various measures of emergence phenology was related to hibernation stage, food type and migration strategy. Large‐scale phylogenetic relatedness exerted little constraint in all models fitted on each measure of phenology. Our results imply that noctuid moths overwintering as adults exhibited greater degrees of phenological shifts than species hibernating as larvae or pupae. It implies that moths hibernating as adults are forced to suspend activity in our climate and the prolongation of autumn activity might be the result of increased plasticity in flight periods.     

Recent evidence for the climate change threat to Lepidoptera and other insects

Climate change is now estimated by some biologists to be the main threat to biodiversity, but doubts persist regarding which species are most at risk, and how best to adapt conservation management. Insects are expected to be highly responsive to climate change, because they have short life cycles which are strongly influenced by temperature. Insects also constitute the most diverse taxonomic group, carrying out biotic interactions of importance for ecological functioning and ecosystem services, so their responses to climate change are likely to be of considerable wider ecological significance. However, a review of recent published evidence of observed and modelled effects of climate change in ten high-ranking journals shows that comparatively few such studies have focused on insects. The majority of these studies are on Lepidoptera, because of the existence of detailed contemporary and historical datasets. These biases in published information may influence conclusions regarding the threat of climate change to insect biodiversity. Assessment of the vulnerability of insect species protected by the Bern Convention on the Conservation of European Wildlife and Natural Habitats also emphasises that most information is available for the Lepidoptera. In the absence of the necessary data to carry out detailed assessments of the likely effects of climate change on most threatened insects, we consider how autecological studies may help to illuminate the potential vulnerability of species, and draw preliminary conclusions about the priorities for insect conservation and research in a changing climate.     

History matters: ecometrics and integrative climate change biology

Climate change research is increasingly focusing on the dynamics among species, ecosystems and climates. Better data about the historical behaviours of these dynamics are urgently needed. Such data are already available from ecology, archaeology, palaeontology and geology, but their integration into climate change research is hampered by differences in their temporal and geographical scales. One productive way to unite data across scales is the study of functional morphological traits, which can form a common denominator for studying interactions between species and climate across taxa, across ecosystems, across space and through time-an approach we call 'ecometrics'. The sampling methods that have become established in palaeontology to standardize over different scales can be synthesized with tools from community ecology and climate change biology to improve our understanding of the dynamics among species, ecosystems, climates and earth systems over time. Developing these approaches into an integrative climate change biology will help enrich our understanding of the changes our modern world is undergoing.     

A diverse assemblage of moths feeding on aphid honeydew

Adult butterflies and moths (Lepidoptera) use their proboscises to feed on flower nectar and other types of liquid food. Aphids frequently secrete honeydew from their anuses, attracting various types of insects, such as ants. Adult lepidopterans are also known to feed on aphid honeydew. However, very few studies have clarified the species composition and morphology of moths feeding on aphid honeydew. In late June 2017, we found nocturnal moths sipping honeydew secreted by Shivaphis celti and Sitobion cornifoliae (Hemiptera: Aphididae) on leaves of Celtis sinensis (Cannabaceae) and Cornus kousa (Cornaceae), respectively, at the edge of a secondary forest in central Japan. The moths were observed to uncoil their proboscises and feed on honeydew on the leaves. No moths were observed to feed on honeydew directly from aphids. Nocturnal moths of 60 species (11 families) and 16 species (7 families) were collected from honeydew on Ce. sinensis and Co. kousa leaves, respectively. Eleven moth species were shared between the two types of honeydew. The most abundant species, Oncocera semirubella (Lepidoptera: Pyralidae), accounted for 44.7% of all individuals. The sex ratio of O. semirubella was female biased. Of the 65 moth species collected on aphid honeydew, 52.3% (34 species) have been previously reported to visit flowers. Moths visiting honeydew had relatively short proboscises and small body size. These results suggest that aphid honeydew is an important, accessible food resource for moths of small size.     

Environmental controls on the phenology of moths: predicting plasticity and constraint under climate change

Ecological systems have naturally high interannual variance in phenology. Component species have presumably evolved to maintain appropriate phenologies under historical climates, but cases of inappropriate phenology can be expected with climate change. Understanding controls on phenology permits predictions of ecological responses to climate change. We studied phenological control systems in Lepidoptera by analyzing flight times recorded at a network of sites in Finland. We evaluated the strength and form of controls from temperature and photoperiod, and tested for geographic variation within species. Temperature controls on phenology were evident in 51% of 112 study species and for a third of those thermal controls appear to be modified by photoperiodic cues. For 24% of the total, photoperiod by itself emerged as the most likely control system. Species with thermal control alone should be most immediately responsive in phenology to climate warming, but variably so depending upon the minimum temperature at which appreciable development occurs and the thermal responsiveness of development rate. Photoperiodic modification of thermal controls constrains phenotypic responses in phenologies to climate change, but can evolve to permit local adaptation. Our results suggest that climate change will alter the phenological structure of the Finnish Lepidoptera community in ways that are predictable with knowledge of the proximate physiological controls. Understanding how phenological controls in Lepidoptera compare to that of their host plants and enemies could permit general inferences regarding climatic effects on mid- to high-latitude ecosystems.     

Traits and climate are associated with first flowering day in herbaceous species along elevational gradients

Phenological responses to changing temperatures are known as “fingerprints of climate change,” yet these reactions are highly species specific. To assess whether different plant characteristics are related to these species‐specific responses in flowering phenology, we observed the first flowering day (FFD) of ten herbaceous species along two elevational gradients, representing temperature gradients. On the same populations, we measured traits being associated with (1) plant performance (specific leaf area), (2) leaf biochemistry (leaf C, N, P, K, and Mg content), and (3) water‐use efficiency (stomatal pore area index and stable carbon isotopes concentration). We found that as elevation increased, FFD was delayed for all species with a highly species‐specific rate. Populations at higher elevations needed less temperature accumulation to start flowering than populations of the same species at lower elevations. Surprisingly, traits explained a higher proportion of variance in the phenological data than elevation. Earlier flowering was associated with higher water‐use efficiency, higher leaf C, and lower leaf P content. In addition to that, the intensity of shifts in FFD was related to leaf N and K. These results propose that traits have a high potential in explaining phenological variations, which even surpassed the effect of temperature changes in our study. Therefore, they have a high potential to be included in future analyses studying the effects of climate change and will help to improve predictions of vegetation changes.     

Body size and activity times mediate mammalian responses to climate change

Model predictions of extinction risks from anthropogenic climate change are dire, but still overly simplistic. To reliably predict at‐risk species we need to know which species are currently responding, which are not, and what traits are mediating the responses. For mammals, we have yet to identify overarching physiological, behavioral, or biogeographic traits determining species' responses to climate change, but they must exist. To date, 73 mammal species in North America and eight additional species worldwide have been assessed for responses to climate change, including local extirpations, range contractions and shifts, decreased abundance, phenological shifts, morphological or genetic changes. Only 52% of those species have responded as expected, 7% responded opposite to expectations, and the remaining 41% have not responded. Which mammals are and are not responding to climate change is mediated predominantly by body size and activity times (phylogenetic multivariate logistic regressions, P < 0.0001). Large mammals respond more, for example, an elk is 27 times more likely to respond to climate change than a shrew. Obligate diurnal and nocturnal mammals are more than twice as likely to respond as mammals with flexible activity times (P < 0.0001). Among the other traits examined, species with higher latitudinal and elevational ranges were more likely to respond to climate change in some analyses, whereas hibernation, heterothermy, burrowing, nesting, and study location did not influence responses. These results indicate that some mammal species can behaviorally escape climate change whereas others cannot, analogous to paleontology's climate sheltering hypothesis. Including body size and activity flexibility traits into future extinction risk forecasts should substantially improve their predictive utility for conservation and management.     

Evaluation of pheromone-baited traps for winter moth and Bruce spanworm (Lepidoptera: Geometridae)

We tested different pheromone-baited traps for surveying winter moth, Operophtera brumata (L.) (Lepidoptera: Geometridae), populations in eastern North America. We compared male catch at Pherocon 1C sticky traps with various large capacity traps and showed that Universal Moth traps with white bottoms caught more winter moths than any other trap type. We ran the experiment on Cape Cod, MA, where we caught only winter moth, and in western Massachusetts, where we caught only Bruce spanworm, Operophtera bruceata (Hulst) (Lepidoptera: Geometridae), a congener of winter moth native to North America that uses the same pheromone compound [(Z,Z,Z)-1,3,6,9-nonadecatetraene] and is difficult to distinguish from adult male winter moths. With Bruce spanworm, the Pherocon 1C sticky traps caught by far the most moths. We tested an isomer of the pheromone [(E,Z,Z)-1,3,6,9-nonadecatetraene] that previous work had suggested would inhibit captures of Bruce spanworm but not winter moths. We found that the different doses and placements of the isomer suppressed captures of both species to a similar degree. We are thus doubtful that we can use the isomer to trap winter moths without also catching Bruce spanworm. Pheromone-baited survey traps will catch both species.     

Winter climate change,plant traits and nutrient and carbon cycling in cold biomes

It is essential that scientists be able to predict how strong climate warming, including profound changes to winter climate, will affect the ecosystem services of alpine, arctic and boreal areas, and how these services are driven by vegetation–soil feedbacks. One fruitful avenue for studying such changing feedbacks is through plant functional traits, as an understanding of these traits may help us to understand and synthesise (1) responses of vegetation (through ‘response traits’ and ‘specific response functions’ of each species) to winter climate and (2) the effects of changing vegetation composition (through ‘effect traits’ and ‘specific effect functions’ of each species) on soil functions. It is the relative correspondence of variation in response and effect traits that will provide useful data on the impacts of winter climate change on carbon and nutrient cycling processes. Here we discuss several examples of how the trait-based, response–effect framework can help scientists to better understand the effects of winter warming on key ecosystem functions in cold biomes. These examples support the view that measuring species for their response and effect traits, and how these traits are linked across species through correspondence of variation in specific response and effects functions, may be a useful approach for teasing out the contribution of changing vegetation composition to winter warming effects on ecosystem functions. This approach will be particularly useful when linked with ecosystem-level measurements of vegetation and process responses to winter warming along natural gradients, over medium time scales in given sites or in response to experimental climate manipulations.     

Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community‐level responses

Biological communities are shaped by complex interactions between organisms and their environment as well as interactions with other species. Humans are rapidly changing the marine environment through increasing greenhouse gas emissions, resulting in ocean warming and acidification. The first response by animals to environmental change is predominantly through modification of their behaviour, which in turn affects species interactions and ecological processes. Yet, many climate change studies ignore animal behaviour. Furthermore, our current knowledge of how global change alters animal behaviour is mostly restricted to single species, life phases and stressors, leading to an incomplete view of how coinciding climate stressors can affect the ecological interactions that structure biological communities. Here, we first review studies on the effects of warming and acidification on the behaviour of marine animals. We demonstrate how pervasive the effects of global change are on a wide range of critical behaviours that determine the persistence of species and their success in ecological communities. We then evaluate several approaches to studying the ecological effects of warming and acidification, and identify knowledge gaps that need to be filled, to better understand how global change will affect marine populations and communities through altered animal behaviours. Our review provides a synthesis of the far‐reaching consequences that behavioural changes could have for marine ecosystems in a rapidly changing environment. Without considering the pervasive effects of climate change on animal behaviour we will limit our ability to forecast the impacts of ocean change and provide insights that can aid management strategies.     

Current understanding of the development of sex attractant-based biocontrol in burnet moths

Burnet moths, also known as the family Zygaenidae, are a typical diurnal family of Lepidoptera. Some species are important insect pests in agriculture and forestry. The use of sex attractants is one of the most important measures in the integrated pest management of burnet moths because these attractants are highly efficient, do not cause pollution, and are convenient and harmless to natural enemies. The earliest information about sex pheromones in Zygaenidae was reported in 1972. To date, many studies have described sex pheromones and attractants of species in Zygaenidae. Here, we review a total of 22 sex attractant compositions identified for 57 species of Zygaenidae and compare the differences in the structures of sex attractants among these species. The application of sex attractants in seasonal monitoring showed that the main activity period of zygaenid moths is from May to September each year. However, there are few reports on the effects of sex attractants on mass trapping of members of the family Zygaenidae. The ratio and degradation of sex attractants and the trap color, shape and hanging height were considered the main factors influencing capture effectiveness. Directions for further study of burnet moths are also discussed.