Evolutionary change in flight-to-light response in urban moths comes with changes in wing morphology.

Moths and other insects are attracted by artificial light sources. This flight-to-light behaviour disrupts their general activity focused on finding resources, such as mating partners, and increases predation risk. It thus has substantial fitness costs. In illuminated urban areas, spindle ermine moths Yponomeuta cagnagella were reported to have evolved a reduced flight-to-light response. Yet, the specific mechanism remained unknown, and was hypothesized to involve either changes in visual perception or general flight ability or overall mobility traits. Here, we test whether spindle ermine moths from urban and rural populations-with known differences in flight-to-light responses-differ in flight-related morphological traits. Urban individuals were found to have on average smaller wings than rural moths, which in turn correlated with a lower probability of being attracted to an artificial light source. Our finding supports the reduced mobility hypothesis, which states that reduced mobility in urban areas is associated with specific morphological changes in the flight apparatus.

Integrating learning into animal range dynamics under rapid human-induced environmental change.

Human-induced rapid environmental change (HIREC) is creating environments deviating considerably from natural habitats in which species evolved. Concurrently, climate warming is pushing species' climatic envelopes to geographic regions that offer novel ecological conditions. The persistence of species is likely affected by the interplay between the degree of ecological novelty and phenotypic plasticity, which in turn may shape an organism's range-shifting ability. Current modelling approaches that forecast animal ranges are characterized by a static representation of the relationship between habitat use and fitness, which may bias predictions under conditions imposed by HIREC. We argue that accounting for dynamic species-resource relationships can increase the ecological realism of range shift predictions. Our rationale builds on the concepts of ecological fitting, the process whereby individuals form successful novel biotic associations based on the suite of traits they carry at the time of encountering the novel condition, and behavioural plasticity, in particular learning. These concepts have revolutionized our view on fitness in novel ecological settings, and the way these processes may influence species ranges under HIREC. We have integrated them into a model of range expansion as a conceptual proof of principle highlighting the potentially substantial role of learning ability in range shifts under HIREC.

Occasional long-distance dispersal may not prevent inbreeding in a threatened butterfly.

BACKGROUND: To set up successful conservation measures, detailed knowledge on the dispersal and colonization capacities of the focal species and connectivity between populations is of high relevance. We developed species-specific nuclear microsatellite molecular markers for the grayling (Hipparchia semele), a butterfly endemic to Europe and of growing conservation concern in North-West Europe, and report on its population genetics, in a fragmented, anthropogenic landscape in Belgium. Our study included samples from 23 different locations nested in two regions and additional historical samples from two locations. We assessed contemporary, long-distance dispersal based on genetic assignment tests and investigated the effect of habitat loss and fragmentation on the population genetic structure and genetic variation using data of nine microsatellite loci. RESULTS: Detected dispersal events covered remarkably long distances, which were up to ten times larger than previously reported colonisation distances, with the longest movement recorded in this study even exceeding 100 km. However, observed frequencies of long-distance dispersal were low. Our results point to the consequences of the strong population decline of the last decades, with evidence of inbreeding for several of the recently sampled populations and low estimates of effective population sizes (Ne) (ranging from 20 to 54 individuals). CONCLUSIONS: Our study shows low frequencies of long-distance dispersal, which is unable to prevent inbreeding in most of the local populations. We discuss the significance for species conservation including future translocation events and discuss appropriate conservation strategies to maintain viable grayling (meta) populations in highly fragmented, anthropogenic landscapes.

Range expansion, habitat use, and choosiness in a butterfly under climate change: Marginality and tolerance of oviposition site selection.

Poleward range shifts under climate change involve the colonization of new sites and hence the foundation of new populations at the expanding edge. We studied oviposition site selection in a butterfly under range expansion (Lycaena dispar), a key process for the establishment of new populations. We described and compared the microhabitats used by the species for egg laying with those available across the study sites both in edge and in core populations. We carried out an ecological niche factor analysis (ENFA) to estimate (1) the variety of microhabitats used by the butterfly for egg laying (tolerance) and (2) the extent to which these selected microhabitats deviated from those available (marginality). Microhabitat availability was similar in edge and core populations. Ambient temperature recorded at the site level above the vegetation was on average lower at core populations. In contrast with what is often assumed, edge populations did not have narrower microhabitat use compared to core populations. Females in edge populations even showed a higher degree of generalism: They laid eggs under a wider range of microhabitats. We suggest that this pattern could be related to an overrepresentation of fast deciding personalities in edge populations. We also showed that the thermal time window for active female behavior was reduced in edge populations, which could significantly decrease the time budget for oviposition and decrease the threshold of acceptance during microhabitat selection for oviposition in recently established populations.

The decline of butterflies in Europe: Problems, significance, and possible solutions.

We review changes in the status of butterflies in Europe, focusing on long-running population data available for the United Kingdom, the Netherlands, and Belgium, based on standardized monitoring transects. In the United Kingdom, 8% of resident species have become extinct, and since 1976 overall numbers declined by around 50%. In the Netherlands, 20% of species have become extinct, and since 1990 overall numbers in the country declined by 50%. Distribution trends showed that butterfly distributions began decreasing long ago, and between 1890 and 1940, distributions declined by 80%. In Flanders (Belgium), 20 butterflies have become extinct (29%), and between 1992 and 2007 overall numbers declined by around 30%. A European Grassland Butterfly Indicator from 16 European countries shows there has been a 39% decline of grassland butterflies since 1990. The 2010 Red List of European butterflies listed 38 of the 482 European species (8%) as threatened and 44 species (10%) as near threatened (note that 47 species were not assessed). A country level analysis indicates that the average Red List rating is highest in central and mid-Western Europe and lowest in the far north of Europe and around the Mediterranean. The causes of the decline of butterflies are thought to be similar in most countries, mainly habitat loss and degradation and chemical pollution. Climate change is allowing many species to spread northward while bringing new threats to susceptible species. We describe examples of possible conservation solutions and a summary of policy changes needed to conserve butterflies and other insects.

Comment on "Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances".

Van Klink et al (Reports, 24 April 2020, p. 417) argue for a more nuanced view of insect decline, and of human responsibility for this decline, than previously suggested. However, shortcomings in data selection and methodology raise questions about their conclusions on trends and drivers. We call for more rigorous methodology to be applied in meta-analyses of ecological data.

Urbanization drives cross-taxon declines in abundance and diversity at multiple spatial scales.

The increasing urbanization process is hypothesized to drastically alter (semi-)natural environments with a concomitant major decline in species abundance and diversity. Yet, studies on this effect of urbanization, and the spatial scale at which it acts, are at present inconclusive due to the large heterogeneity in taxonomic groups and spatial scales at which this relationship has been investigated among studies. Comprehensive studies analysing this relationship across multiple animal groups and at multiple spatial scales are rare, hampering the assessment of how biodiversity generally responds to urbanization. We studied aquatic (cladocerans), limno-terrestrial (bdelloid rotifers) and terrestrial (butterflies, ground beetles, ground- and web spiders, macro-moths, orthopterans and snails) invertebrate groups using a hierarchical spatial design, wherein three local-scale (200 m × 200 m) urbanization levels were repeatedly sampled across three landscape-scale (3 km × 3 km) urbanization levels. We tested for local and landscape urbanization effects on abundance and species richness of each group, whereby total richness was partitioned into the average richness of local communities and the richness due to variation among local communities. Abundances of the terrestrial active dispersers declined in response to local urbanization, with reductions up to 85% for butterflies, while passive dispersers did not show any clear trend. Species richness also declined with increasing levels of urbanization, but responses were highly heterogeneous among the different groups with respect to the richness component and the spatial scale at which urbanization impacts richness. Depending on the group, species richness declined due to biotic homogenization and/or local species loss. This resulted in an overall decrease in total richness across groups in urban areas. These results provide strong support to the general negative impact of urbanization on abundance and species richness within habitat patches and highlight the importance of considering multiple spatial scales and taxa to assess the impacts of urbanization on biodiversity.

Patterns of host use by brood parasitic Maculinea butterflies across Europe.

The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Personality traits influence contest outcome, and vice versa, in a territorial butterfly.

Holding a territory is often crucial in order to acquire key resources, including mating partners. However, few studies have investigated the role of animal personality in the context of territorial conflicts and how the contest outcome itself may influence personality traits. We studied personality in male Speckled wood butterflies, Pararge aegeria, before and after territorial contests for sunspot territories. Before interactions, boldness decreased with age, while activity and exploration were only influenced by ambient conditions. Neither age nor morphology did influence the probability to win contests, but winners were more active and more explorative than losers and, moreover, males that received a red wing mark were more likely to be winners. Butterflies that lost a contest showed pronounced behavioural changes. Mean boldness increased and its repeatability was disrupted, while no such change was detected in winners. The observed boldness increase in losers may be explained by a 'desperado effect', though its implication for successive contests remains unknown. Given that territoriality is expected to have important consequences for reproductive success, our results suggest that personality traits may indirectly contribute to individual fitness by influencing the ability to gain access to mate-location patches.

Adaptive learning in non-social insects: from theory to field work, and back.

We review the evidence that learning affects fitness in non-social insects. Early accounts date back from the 1970s and were based on field-based observational and experimental work, yet exploration of the ways in which various forms of learning increase fitness remains limited in non-social insects. We highlight the concerns that arise when artificial laboratory settings, which do not take the ecology of the species into account, are used to estimate fitness benefits of learning. We argue that ecologically-relevant experimental designs are most useful to provide fitness estimates of learning, that is, designs that include: firstly, offspring of wild-caught animals producing newly established stocks under relevant breeding conditions, combined with common-garden and reciprocal transplant experiments; secondly, the spatio-temporal dynamics of key ecological resources; and thirdly, the natural behaviours of the animals while searching for, and probing, resources. Finally, we provide guidelines for the study of fitness-learning relationships in an eco-evolutionary framework.

Increased body size along urbanization gradients at both community and intraspecific level in macro-moths.

Urbanization involves a cocktail of human-induced rapid environmental changes and is forecasted to gain further importance. Urban-heat-island effects result in increased metabolic costs expected to drive shifts towards smaller body sizes. However, urban environments are also characterized by strong habitat fragmentation, often selecting for dispersal phenotypes. Here, we investigate to what extent, and at which spatial scale(s), urbanization drives body size shifts in macro-moths-an insect group characterized by positive size-dispersal links-at both the community and intraspecific level. Using light and bait trapping as part of a replicated, spatially nested sampling design, we show that despite the observed urban warming of their woodland habitat, macro-moth communities display considerable increases in community-weighted mean body size because of stronger filtering against small species along urbanization gradients. Urbanization drives intraspecific shifts towards increased body size too, at least for a third of species analysed. These results indicate that urbanization drives shifts towards larger, and hence, more mobile species and individuals in order to mitigate low connectivity of ecological resources in urban settings. Macro-moths are a key group within terrestrial ecosystems, and since body size is central to species interactions, such urbanization-driven phenotypic change may impact urban ecosystem functioning, especially in terms of nocturnal pollination and food web dynamics. Although we show that urbanization's size-biased filtering happens simultaneously and coherently at both the inter- and intraspecific level, we demonstrate that the impact at the community level is most pronounced at the 800 m radius scale, whereas species-specific size increases happen at local and landscape scales (50-3,200 m radius), depending on the species. Hence, measures-such as creating and improving urban green infrastructure-to mitigate the effects of urbanization on body size will have to be implemented at multiple spatial scales in order to be most effective.

Body-size shifts in aquatic and terrestrial urban communities.

Body size is intrinsically linked to metabolic rate and life-history traits, and is a crucial determinant of food webs and community dynamics1,2. The increased temperatures associated with the urban-heat-island effect result in increased metabolic costs and are expected to drive shifts to smaller body sizes 3 . Urban environments are, however, also characterized by substantial habitat fragmentation 4 , which favours mobile species. Here, using a replicated, spatially nested sampling design across ten animal taxonomic groups, we show that urban communities generally consist of smaller species. In addition, although we show urban warming for three habitat types and associated reduced community-weighted mean body sizes for four taxa, three taxa display a shift to larger species along the urbanization gradients. Our results show that the general trend towards smaller-sized species is overruled by filtering for larger species when there is positive covariation between size and dispersal, a process that can mitigate the low connectivity of ecological resources in urban settings 5 . We thus demonstrate that the urban-heat-island effect and urban habitat fragmentation are associated with contrasting community-level shifts in body size that critically depend on the association between body size and dispersal. Because body size determines the structure and dynamics of ecological networks 1 , such shifts may affect urban ecosystem function.

Flight-induced transgenerational maternal effects influence butterfly offspring performance during times of drought.

Maternal condition can generate resource-related maternal effects through differential egg provisioning that can negatively affect offspring performance especially when offspring growth occurs in stressful or sub-optimal environments. Using the Speckled Wood butterfly, Pararge aegeria (L.) we tested the hypothesis that repeated periods of intensive flight during female oviposition affects egg provisioning and reduces offspring performance when larval development occurs under stressful conditions on drought stressed host plants. We investigated whether (after controlling for egg size) maternal age and flight treatment resulted in changes in egg provisioning and whether this contributed to variation in offspring traits across life stages. Age-related changes in maternal condition were found to generate resource-related maternal effects that influenced offspring traits across all life stages. Flight-induced changes in maternal egg provisioning were found to have direct consequences for offspring development in the egg and larval stages. There were significant interactive effects between maternal age and flight on larval development and growth. Compared to offspring from forced flight mothers, offspring from control (no forced flight) mothers that hatched from eggs laid early in the oviposition period (i.e. by younger mothers) had shorter larval development times and heavier pupal masses, suggesting that offspring from mothers in relatively good condition may be able to buffer some of the costs associated with growth on drought stressed host plants. Our multi-factor study demonstrates the importance of considering the various, and often interacting, mechanisms by which maternal effects may influence offspring performance in stressful environments.

Timing of Breeding in an Ecologically Trapped Bird.

In human-modified environments, organisms may prefer to use habitats where their reproductive performance is lower compared to alternative options. Many such ecological traps occur in seasonally changing environments. Although the timing of breeding has been shown to impact reproductive performance in a variety of organisms, it has never been considered as a potential mechanism underlying ecological traps. We address this issue with a migratory bird, the red-backed shrike, breeding in a human-modified, farmland-forest landscape. Shrikes prefer breeding in forest clear-cuts where their reproductive performance is lower than in less attractive farmland. We compared brood size and quality of early (first broods) and delayed breeders (replacement broods) between the two habitats. We found a stronger seasonal decrease in reproductive performance in preferred forest clear-cuts than in farmland. Food resources were slightly more abundant in forest than in farmland at the beginning of the season but depleted more steeply in forest by the end of the breeding season. By contrast, the phenotypic quality of breeders did not decline over the course of the season in either habitat. This is the first report that the timing of breeding relative to the seasonal change in key resources may play a significant role in explaining low reproductive performance in ecological traps.

Ecotypic differentiation matters for latitudinal variation in energy metabolism and flight performance in a butterfly under climate change.

Life histories of organisms may vary with latitude as they experience different thermal constraints and challenges. This geographic, intraspecific variation could be of significance for range dynamics under climate change beyond edge-core comparisons. In this study, we did a reciprocal transplant experiment between the temperature-regimes of two latitudes with an ectotherm insect, examining the effects on energy metabolism and flight performance. Pararge aegeria expanded its ecological niche from cool woodland (ancestral) to warmer habitat in agricultural landscape (novel ecotype). Northern males had higher standard metabolic rates than southern males, but in females these rates depended on their ecotype. Southern males flew for longer than northern ones. In females, body mass-corrected flight performance depended on latitude and thermal treatment during larval development and in case of the southern females, their interaction. Our experimental study provides evidence for the role of ecological differentiation at the core of the range to modulate ecophysiology and flight performance at different latitudes, which in turn may affect the climatic responsiveness of the species.

The Urban Heat Island and its spatial scale dependent impact on survival and development in butterflies of different thermal sensitivity.

Climate alteration is one of the most cited ecological consequences of urbanization. However, the magnitude of this impact is likely to vary with spatial scale. We investigated how this alteration affects the biological fitness of insects, which are especially sensitive to ambient conditions and well-suited organisms to study urbanization-related changes in phenotypic traits. We monitored temperature and relative air humidity in wooded sites characterized by different levels of urbanization in the surroundings. Using a split-brood design experiment, we investigated the effect of urbanization at the local (i.e., 200 × 200 m) and landscape (i.e., 3 × 3 km) scale on two key traits of biological fitness in two closely related butterfly species that differ in thermal sensitivity. In line with the Urban Heat Island concept, urbanization led to a 1°C increase in daytime temperature and an 8% decrease in daytime relative humidity at the local scale. The thermophilous species Lasiommata megera responded at the local scale: larval survival increased twofold in urban compared to rural sites. Urbanized sites tended to produce bigger adults, although this was the case for males only. In the woodland species Pararge aegeria, which has recently expanded its ecological niche, we did not observe such a response, neither at the local, nor at the landscape scale. These results demonstrate interspecific differences in urbanization-related phenotypic plasticity and larval survival. We discuss larval pre-adaptations in species of different ecological profiles to urban conditions. Our results also highlight the significance of considering fine-grained spatial scales in urban ecology.

Flight Morphology, Compound Eye Structure and Dispersal in the Bog and the Cranberry Fritillary Butterflies: An Inter- and Intraspecific Comparison.

Understanding dispersal is of prime importance in conservation and population biology. Individual traits related to motion and navigation during dispersal may differ: (1) among species differing in habitat distribution, which in turn, may lead to interspecific differences in the potential for and costs of dispersal, (2) among populations of a species that experiences different levels of habitat fragmentation; (3) among individuals differing in their dispersal strategy and (4) between the sexes due to sexual differences in behaviour and dispersal tendencies. In butterflies, the visual system plays a central role in dispersal, but exactly how the visual system is related to dispersal has received far less attention than flight morphology. We studied two butterfly species to explore the relationships between flight and eye morphology, and dispersal. We predicted interspecific, intraspecific and intersexual differences for both flight and eye morphology relative to i) species-specific habitat distribution, ii) variation in dispersal strategy within each species and iii) behavioural differences between sexes. However, we did not investigate for potential population differences. We found: (1) sexual differences that presumably reflect different demands on both male and female visual and flight systems, (2) a higher wing loading (i.e. a proxy for flight performance), larger eyes and larger facet sizes in the frontal and lateral region of the eye (i.e. better navigation capacities) in the species inhabiting naturally fragmented habitat compared to the species inhabiting rather continuous habitat, and (3) larger facets in the frontal region in dispersers compared to residents within a species. Hence, dispersers may have similar locomotory capacity but potentially better navigation capacity. Dispersal ecology and evolution have attracted much attention, but there are still significant gaps in our understanding of the mechanisms of dispersal. Unfortunately, for many species we lack detailed information on the role of behavioural, morphological and physiological traits for dispersal. Our novel study supports the existence of inter- and intra-specific evolutionary responses in both motion and navigation capacities (i.e. flight and eye morphology) linked to dispersal.

Nectar resource limitation affects butterfly flight performance and metabolism differently in intensive and extensive agricultural landscapes.

Flight is an essential biological ability of many insects, but is energetically costly. Environments under rapid human-induced change are characterized by habitat fragmentation and may impose constraints on the energy income budget of organisms. This may, in turn, affect locomotor performance and willingness to fly. We tested flight performance and metabolic rates in meadow brown butterflies (Maniola jurtina) of two contrasted agricultural landscapes: intensively managed, nectar-poor (IL) versus extensively managed, nectar-rich landscapes (EL). Young female adults were submitted to four nectar treatments (i.e. nectar quality and quantity) in outdoor flight cages. IL individuals had better flight capacities in a flight mill and had lower resting metabolic rates (RMR) than EL individuals, except under the severest treatment. Under this treatment, RMR increased in IL individuals, but decreased in EL individuals; flight performance was maintained by IL individuals, but dropped by a factor 2.5 in EL individuals. IL individuals had more canalized (i.e. less plastic) responses relative to the nectar treatments than EL individuals. Our results show significant intraspecific variation in the locomotor and metabolic response of a butterfly to different energy income regimes relative to the landscape of origin. Ecophysiological studies help to improve our mechanistic understanding of the eco-evolutionary impact of anthropogenic environments on rare and widespread species.

A database on the distribution of butterflies (Lepidoptera) in northern Belgium (Flanders and the Brussels Capital Region).

In this data paper, we describe two datasets derived from two sources, which collectively represent the most complete overview of butterflies in Flanders and the Brussels Capital Region (northern Belgium). The first dataset (further referred to as the INBO dataset - http://doi.org/10.15468/njgbmh) contains 761,660 records of 70 species and is compiled by the Research Institute for Nature and Forest (INBO) in cooperation with the Butterfly working group of Natuurpunt (Vlinderwerkgroep). It is derived from the database Vlinderdatabank at the INBO, which consists of (historical) collection and literature data (1830-2001), for which all butterfly specimens in institutional and available personal collections were digitized and all entomological and other relevant publications were checked for butterfly distribution data. It also contains observations and monitoring data for the period 1991-2014. The latter type were collected by a (small) butterfly monitoring network where butterflies were recorded using a standardized protocol. The second dataset (further referred to as the Natuurpunt dataset - http://doi.org/10.15468/ezfbee) contains 612,934 records of 63 species and is derived from the database http://waarnemingen.be, hosted at the nature conservation NGO Natuurpunt in collaboration with Stichting Natuurinformatie. This dataset contains butterfly observations by volunteers (citizen scientists), mainly since 2008. Together, these datasets currently contain a total of 1,374,594 records, which are georeferenced using the centroid of their respective 5 × 5 km² Universal Transverse Mercator (UTM) grid cell. Both datasets are published as open data and are available through the Global Biodiversity Information Facility (GBIF).