Effects of landscape structure and habitat type on a plant-herbivore-parasitoid community

The effects of local habitat and large-scale landscape factors on species diversity and species interactions were studied using the insect community in stems of the creeping thistle Cirsium arvense . Thistle abundance was higher in fallows than in crop fields and field margins, with fallows providing 67% of thistle abundance within 15 study areas on a landscape scale. Species richness of the herbivores was positively related with thistle abundance, parasitoid species richness was influenced by habitat type and was positively correlated with herbivore species richness. The abundance of herbivores and parasitoids was affected by local factors such as habitat type and host abundance, but also by landscape factors such as the percentage of non-crop area and the isolation of habitats. The infestation rate caused by the agromyzid Melanagromyza aeneoventris was positively related to percent non-crop area, whereas the parasitism rate of this fly increased with increasing habitat diversity on the landscape scale. For these two interactions and for total herbivore abundance, a scale-dependency of the landscape effects was found. The results emphasize that biological diversity and ecological functions within a plant-insect community are not only affected by local habitat factors but also by large-scale landscape characteristics. Hence, to improve future agri-environmental schemes for biodiversity conservation and biological control large-scale landscape effects and their scale-dependency should be considered.     

Differentiation of spring carabid beetle assemblages between semi‐natural habitats and adjoining winter wheat

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Humid grassland fallows promote spider diversity in a traditionally managed landscape

Agricultural intensification is an important driver of biodiversity decline. Regarding grassland ecosystems, traditionally managed hay meadows, as opposed to highly productive silage grassland, are often of high conservation value. Here, we compare spider assemblages among five grassland management regimes along an intensification gradient, ranging from long-term fallows (not farmed for ≥ 30 years) via traditionally managed hay meadows to high-intensity silage grassland. Humid long-term fallows harboured highest species richness and diversity, and their assemblages differed strongly from other management regimes. There was surprisingly little variation though among different types of hay meadows and silage grassland. We also included environmental parameters and land-cover types in the surroundings of study sites, indicating that spider assemblages were most strongly shaped by fallow-related parameters and the proportion of forests. The high spider diversity on fallows may result from their undisturbed vegetation structure, while management, regardless of frequency, may have detrimental effects. Our results demonstrate the high importance of unmanaged areas even in regions with an overall low land-use intensity, such as grassland ecosystems. We thus recommend the inclusion of temporal grassland fallows (unmanaged for 3-5 years) in agri-environmental schemes to increase landscape heterogeneity and preserve spider diversity.     

Missing the target? A critical view on butterfly conservation efforts on calcareous grasslands in south-western Germany

Butterflies are strongly declining on grassland habitats of Central Europe. Therefore, the success of conservation measures on high quality grassland habitats is controversially discussed. We compared the changes in butterfly diversity and community structure on six managed calcareous grasslands with eight unmanaged vineyard fallows. We obtained strong losses of species diversity and remarkable shifts of community compositions on both habitat types. However, the changes on vineyard fallows were only slightly more severe but more stochastic than on the calcareous grasslands. The shifts in community composition with respect to functional species traits were rather similar between the two different grassland types so that complex butterfly communities evolved into generalist-dominated ones. Connectivity was higher among vineyard fallows than among calcareous grasslands. Consequently, conservation measures on calcareous grasslands only partly achieved their goal to maintain the high species diversity and functional complexity still observed in the 1970s. The negative impacts of eutrophication and monotonisation of the landscape as well as climate change are affecting all habitats, independently from management concepts. Therefore, management on conservation sites can buffer against these effects, but is not sufficient for a full compensation.     

Response of Orthoptera assemblages to management of montane grasslands in the Western Carpathians

Montane grassy habitats in the Western Carpathians are relatively well preserved, maintain high species richness and are often important in accordance to the nature conservation policy in Europe. However, knowledge about the impact of farming on the habitat quality there is rather poor. The influence of various management types (permanent sheep pen, irregular grazing, mowing) on Orthoptera diversity and species determining assemblages of these habitats were analysed on 72 plots in Poľana Mts Biosphere Reserve. Altogether, 36 Orthoptera species (15 Ensifera, 21 Caelifera) were found, whereas the highest number of species was found on plots with irregular grazing (28 species), followed by plots with mown grass (17) and permanent sheep pens (14). All four measures of the assemblages’ diversity confirmed significant differences. Using Discriminant Function Analysis, correct classification rate of Orthoptera assemblages was unambiguous according to the type of management. Each form of the management harboured several characteristic species. Thus implications regarding the biodiversity conservation and grassland management were given.     

Effects of fen management and habitat parameters on staphylinid beetle (Coleoptera: Staphylinidae) assemblages in north-eastern Germany

Because fens have undergone dramatic declines in recent decades, an important question is which management regimes and habitat parameters are most effective in preserving fen biodiversity. The aim of the present study was to assess the effects of five different management regimes (intensive grassland, moist meadows, summer harvested sites, winter harvested sites, fallows) on staphylinid beetle assemblages. During the study period 5,989 individuals from 92 staphylinid beetle species were recorded. Species richness and abundance were highest on intensive grassland and fallows, and water level and vegetation height had significant impacts on the abundance of staphylinids. On winter-harvested sites species richness and abundance were lowest. In general, staphylinid beetles did not show pronounced variation among management regimes, while the environmental factors water level, vegetation height and top soil mineralisation seemed to have a larger structuring impact. The number of threatened species and the conservation index were highest on summer-harvested sites and fallows, representing fairly well-preserved fens. We conclude that summer harvest of reed beds or no management at all appears to be most beneficial for the conservation of staphylinid beetles.     

Butterfly diversity at the ecotone between agricultural and semi‐natural habitats across a climatic gradient

Aim Understanding the response of species to ecotones and habitat edges is essential to designing conservation management, especially in mosaic agricultural landscapes. This study examines how species diversity and composition change with distance from semi‐natural habitats, over ecotones into agricultural fields, and how within‐site patterns of community transition change across a climatic gradient and differ between crop types. Location A total of 19 sites in Israel where semi‐natural habitats border agricultural fields (wheat fields or olive groves) distributed along a sharp climatic gradient ranging between 100 and 800 mm mean annual rainfall. Methods  We performed butterfly surveys in 2006. We analysed species richness (α‐diversity), diversity, community nestedness and species turnover (β‐diversity) within sites and between sites (γ‐diversity). We also assessed where species of conservation concern occurred. Results In wheat sites, richness and diversity declined abruptly from ecotones to fields and remained homogenously poor throughout the fields, regardless of climate. In olive sites, despite the sharp structural boundary, richness and diversity remained high from the semi‐natural habitat to the grove margins and then declined gradually into groves. Species of conservation concern occurred across all habitats at olive sites, but none were found inside wheat fields or at their ecotones. The contrast in community structure between semi‐natural habitats and fields was affected by both climate and field type. Irrigation in arid regions did not augment species diversity. Main conclusions Our results indicate that consideration of crop type, within a climatic context, should receive high priority in biodiversity conservation in agricultural areas. In ‘hostile’ crops, such as wheat, we suggest favouring a combination of high‐intensity management and wide margins over less intensive management without margins, which may merely aid generalist butterfly species. The scarcity of butterflies in arid irrigated fields suggests a need to carefully assess the effects of irrigation and agrochemicals on species’ communities.     

Dynamic effects of ground-layer plant communities on beetles in a fragmented farming landscape

Vegetation effects on arthropods are well recognized, but it is unclear how different vegetation attributes might influence arthropod assemblages across mixed-agricultural landscapes. Understanding how plant communities influence arthropods under different habitat and seasonal contexts can identify vegetation management options for arthropod biodiversity. We examined relationships between vegetation structure, plant species richness and plant species composition, and the diversity and composition of beetles in different habitats and time periods. We asked: (1) What is the relative importance of plant species richness, vegetation structure and plant composition in explaining beetle species richness, activity-density and composition? (2) How do plant-beetle relationships vary between different habitats over time? We sampled beetles using pitfall traps and surveyed vegetation in three habitats (woodland, farmland, their edges) during peak crop growth in spring and post-harvest in summer. Plant composition better predicted beetle composition than vegetation structure. Both plant richness and vegetation structure significantly and positively affected beetle activity-density. The influence of all vegetation attributes often varied in strength and direction between habitats and seasons for all trophic groups. The variable nature of plant-beetle relationships suggests that vegetation management could be targeted at specific habitats and time periods to maximize positive outcomes for beetle diversity. In particular, management that promotes plant richness at edges, and promotes herbaceous cover during summer, can support beetle diversity. Conserving ground cover in all habitats may improve activity-density of all beetle trophic groups. The impacts of existing weed control strategies in Australian crop margins on arthropod biodiversity require further study.     

Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control

Agricultural intensification has resulted in a simplification of agricultural landscapes by the expansion of agricultural land, enlargement of field size and removal of non-crop habitat. These changes are considered to be an important cause of the rapid decline in farmland biodiversity, with the remaining biodiversity concentrated in field edges and non-crop habitats. The simplification of landscape composition and the decline of biodiversity may affect the functioning of natural pest control because non-crop habitats provide requisites for a broad spectrum of natural enemies, and the exchange of natural enemies between crop and non-crop habitats is likely to be diminished in landscapes dominated by arable cropland. In this review, we test the hypothesis that natural pest control is enhanced in complex patchy landscapes with a high proportion of non-crop habitats as compared to simple large-scale landscapes with little associated non-crop habitat. In 74% and 45% of the studies reviewed, respectively, natural enemy populations were higher and pest pressure lower in complex landscapes versus simple landscapes. Landscape-driven pest suppression may result in lower crop injury, although this has rarely been documented. Enhanced natural enemy activity was associated with herbaceous habitats in 80% of the cases (e.g. fallows, field margins), and somewhat less often with wooded habitats (71%) and landscape patchiness (70%). The similar contributions of these landscape factors suggest that all are equally important in enhancing natural enemy populations. We conclude that diversified landscapes hold most potential for the conservation of biodiversity and sustaining the pest control function.     

Even the Smallest Non-Crop Habitat Islands Could Be Beneficial: Distribution of Carabid Beetles and Spiders in Agricultural Landscape

Carabid beetles and ground-dwelling spiders inhabiting agroecosystems are beneficial organisms with a potential to control pest species. Intensification of agricultural management and reduction of areas covered by non-crop vegetation during recent decades in some areas has led to many potentially serious environmental problems including a decline in the diversity and abundance of beneficial arthropods in agricultural landscapes. This study investigated carabid beetle and spider assemblages in non-crop habitat islands of various sizes (50 to 18,000 square metres) within one large field, as well as the arable land within the field, using pitfall traps in two consecutive sampling periods (spring to early summer and peak summer). The non-crop habitat islands situated inside arable land hosted many unique ground-dwelling arthropod species that were not present within the surrounding arable land. Even the smallest non-crop habitat islands with areas of tens of square metres were inhabited by assemblages substantially different from these inhabiting arable land and thus enhanced the biodiversity of agricultural landscapes. The non-crop habitat area substantially affected the activity density, recorded species richness and recorded species composition of carabid and ground-dwelling spider assemblages; however, the effects were weakened when species specialised to non-crop habitats species were analysed separately. Interestingly, recorded species richness of spiders increased with non-crop habitat area, whereas recorded species richness of carabid beetles exhibited an opposite trend. There was substantial temporal variation in the spatial distribution of ground-dwelling arthropods, and contrasting patterns were observed for particular taxa (carabid beetles and spiders). In general, local environmental conditions (i.e., non-crop habitat island tree cover, shrub cover, grass cover and litter depth) were better determinants of arthropod assemblages than non-crop habitat island size, indicating that the creation of quite small but diversified (e.g., differing in vegetation cover) non-crop habitat islands could be the most efficient tool for the maintenance and enhancement of diversity of ground-dwelling carabids and spiders in agricultural landscapes.     

Effects of experimentally planting non-crop flowers into cabbage fields on the abundance and diversity of predators

Flowery field margins and intersowing of crops with flowers are used as management practices to promote arthropod biodiversity as well as biocontrol agents. Positive effects of enhancement (in abundance and species richness) of hymenopteran parasitoids on control of Lepidoptera pests have previously been demonstrated. However, effects on predatory arthropods, which may also serve as pest control agents, remain unclear. In an experimental study in cabbage fields we tested how sown flower strips on field margins and intersowing with cornflower affected the species richness, abundance and community composition of ground beetles and spiders. Furthermore, we investigated whether effects of flower margins are dependent on the distance from the field margins. We found that field margins generally harboured higher species richness, whereas effects on abundance were weaker. Intersown cornflower had positive effects on spider and ground beetle abundance, but affected species richness only weakly. Our results do not provide evidence for effects of distance from the flowery field margins on predator richness or abundance. Species composition was strongly affected by the habitat management actions. We conclude that habitat management practices like flower strips on field margins and intersowing with flowers, which are primarily added to attract and enhance parasitoids for pest control, also benefit biodiversity conservation in spiders and ground beetles. They also positively affect the abundance of these primarily predatory taxa, which adds to the biocontrol potential of non-crop flowering plants.     

Landscape-scale crop diversity interacts with local management to determine ground beetle diversity

Crop diversification and maintenance of semi-natural habitats (grasslands and field boundaries) are suggested to enhance farmland biodiversity, but the relative importance of these factors remains poorly known. We evaluated how crop diversity and availability of semi-natural grasslands at a landscape-scale interacted with local farming management (three management types from low to high intensity: ley < winter wheat < sugar beet) in their effect on ground beetle assemblages in southern Sweden. Ground beetle diversity increased with crop diversity either independently of local management (Simpson species diversity), or only in the less intensively managed habitats (rarefied species richness). While ground beetle diversity in leys tended to increase with field boundary length, no such relationship was observed in winter wheat or sugar beet fields. In contrast, the landscape proportions of leys and semi-natural grasslands did not affect ground beetle species richness and diversity. We conclude that (a) semi-natural grasslands and leys may not function as source habitats at a landscape-scale if they comprise a low proportion of the total land-use, while (b) increasing crop diversity is correlated to ground beetle richness and diversity in agricultural landscapes dominated by arable land. The beneficial effect of landscape-scale crop diversification on farmland biodiversity may depend on the general level of agricultural intensity of a region.     

Ground Beetle (Coleoptera: Carabidae) Assemblages of Restored Semi‐natural Habitats and Intensively Cultivated Fields in Northern China

Diversity of ground beetle (Coleoptera: Carabidae) assemblages and sub‐assemblages was compared between reafforested woodland, grassland, and intensively cultivated fields at Chongli County in Northern China. An array of eight pitfall traps per plot was used to sample the beetles on four replicate plots for each habitat. Replanted conifer woodland and semi‐natural grassland harbored very similar beetle assemblages. These had significantly lower rarefied species numbers than the distinctly different assemblages recorded in cultivated fields, with differences in alpha diversity being less pronounced for large and predatory species. Carabid activity‐density levels were higher in both woodland and grassland than in fields, with this trend being most pronounced for predatory and large species. To conserve high levels of gamma diversity, it is important to maintain a mosaic of agricultural areas and semi‐natural habitats. The latter also form a potential source for predatory species important in pest control. It appears that woodland‐specific species are rare in the study area, or they have not been able to reach and colonize the newly established woodland sites. It can also be concluded that morphological and ecological traits allow important insights into underlying ecological principles of overall diversity patterns.     

High effectiveness of tailored flower strips in reducing pests and crop plant damage

Providing key resources to animals may enhance both their biodiversity and the ecosystem services they provide. We examined the performance of annual flower strips targeted at the promotion of natural pest control in winter wheat. Flower strips were experimentally sown along 10 winter wheat fields across a gradient of landscape complexity (i.e. proportion non-crop area within 750 m around focal fields) and compared with 15 fields with wheat control strips. We found strong reductions in cereal leaf beetle (CLB) density (larvae: 40%; adults of the second generation: 53%) and plant damage caused by CLB (61%) in fields with flower strips compared with control fields. Natural enemies of CLB were strongly increased in flower strips and in part also in adjacent wheat fields. Flower strip effects on natural enemies, pests and crop damage were largely independent of landscape complexity (8–75% non-crop area). Our study demonstrates a high effectiveness of annual flower strips in promoting pest control, reducing CLB pest levels below the economic threshold. Hence, the studied flower strip offers a viable alternative to insecticides. This highlights the high potential of tailored agri-environment schemes to contribute to ecological intensification and may encourage more farmers to adopt such schemes.     

The succession of Staphylinidae (Coleoptera) after 15 years of conversion from conventional to organic farming

The results of a 15 years investigation after the conversion from conventional to organic farming are presented for the beetle family Staphylinidae. The aim of the study was to find general trends in the succession of assemblages, changes in the biodiversity and changes of dispersion for invading or retreating species. The succession of all fields studied are shifted in the same direction, which indicates an overall driving ecological factor after the conversion. However, individual fields showed a different speed within the succession. The number of species remained on the same level in the first 8 years but increased from the eighth to the 15th year. However, the species diversity on the organic fields were still lower than in the field margins. The conventionally farmed fields in 2001 before the conversion of the main study area was compared with adjacent conventionally farmed fields investigated 15 years later. This comparison showed that the species diversity was currently much lower there than 15 years before in the main study area. During the succession single species retreated from fields after the conversion and other species invaded the fields. In particular, species of open habitats and inquilines of mammals invaded the fields. It was concluded that organic farming had benefit effects on biodiversity, but a mosaic with field margins will enhance this effect.     

Are cladoceran diversity and community structure linked to spatial heterogeneity in urban landscapes and pond environments?

Biodiversity patterns in cladoceran communities were investigated in urban waterbodies in relation with residential land use, pond management, and waterbody environments. We evaluated species richness in the pelagic and littoral zones of eighteen waterbodies of a large Canadian city. Gamma diversity (26 species) observed at a small scale in the urban survey was important comparatively to large-scale surveys of lakes. Beta diversity ranged from 1 to 8 species among waterbodies. We tested if littoral species greatly contributed to regional diversity in urban waterbodies. Littoral species (Chydoridae, Ilyocryptidae, Macrothricidae, Polyphemidae) accounted for 58% of the total species pool. We distinguished five cladoceran assemblages associated to different waterbodies (temporary ponds, permanent lakes, and wetlands). Cladoceran communities were more diverse and variable in permanent lakes than in temporary ponds. Changes in cladoceran species assemblages among waterbodies were driven by variations in waterbody size and phosphorus enrichment, macrophyte and algal biomass, urban density, pond management practices, and the presence of potential predators as fish and macroinvertebrates. Our study indicates that both artificial ponds and lakes and natural wetlands are valuable habitats for the conservation of cladoceran biodiversity and rare endemic species in urban regions. Further research on pond management strategies promoting urban aquatic biodiversity should be undertaken.     

Disentangling the role of management,vegetation structure,and plant quality for Orthoptera in lowland meadows

Seminatural grasslands provide habitats for various species and are important for biodiversity conservation. The understanding of the diverse responses of species and traits to different grassland managenient methods is therefore urgently needed. We disentangled the role of grassland management (fertilization and irrigation), vegetation structure (biomass, sward height) and plant quality (protein and fiber content) for Orthoptera communities in lowland hay meadows in Germany. We found vegetation structure to be the most important environmental category in explaining community structure of Orthoptera (species richness, total individuals, fiinctional diversity and species composition). Intensively used meadows (fertilized, irrigated, high plant biomass) were characterized by assemblages with few species, low functional diversity, and low conservation value. Thereby, the relatively moderate fertilizer inputs in our study system of up to -75 kg N/ha/year reduced functional diversity of Orthoptera, while this negative effect of fertilization was not detectable when solely considering taxonomic aspects. We found strong support for a prominent role of plant quality in shaping Orthoptera communities and especially the trait composition. Our findings demonstrate the usefulness of considering both taxonomic and functional comp on ents (functio nal diversity) in biodiversity research and we suggest a stronger involvement of plant quality measures in Orthoptera studies.     

农业景观生物多样性与害虫生态控制

现代农业的一个重要特征就是人类对农田生态系统的干扰强度及频率不断增加,严重影响农业景观的结构及其生物多样性.农业景观结构的变化及其生物多样性的丧失,必然引起生态系统服务功能的弱化,不利于实施以保护自然天敌为主的害虫生态控制.农业的集约化经营导致自然生境破碎化,减少了农业景观的复杂性,使得作物和非作物变成一种相对离散化的生境类型和镶嵌的景观格局;破碎化的生境不仅会减少某些物种的丰度,还会影响物种之间的相互关系及生物群落的多样性和稳定性.非作物生境类型如林地、灌木篱墙、田块边缘区、休耕地和草地等,是一种比较稳定的异质化环境.非作物生境较少受到干扰,可以为寄生性和捕食性节肢动物提供适宜的越冬或避难场所以及替代猎物、花粉和花蜜等资源,因此,非作物生境有利于自然天敌的栖息和繁衍,也有利于它们迁入邻近的作物生境中对害虫起到调节和控制作用.景观的格局-过程-尺度影响农田生物群落物种丰富度、多度、多样性以及害虫与天敌之间的相互作用.从区域农业景观系统的角度出发,运用景观生态学的理论和方法来研究作物、害虫、天敌等组分在不同斑块之间的转移过程和变化规律,揭示害虫在较大尺度和具有异质性的空间范围内的灾变机理,可为利用农业景观生物多样性来保护农田自然天敌,实施害虫的区域性生态控制提供新的研究思路和手段.     

Does natural reforestation represent a potential threat to dung beetle diversity in the Alps?

Traditional agro-pastoral practices are in decline over much of the Alps, resulting in the complete elimination of livestock grazing in some areas. Natural reforestation following pastoral abandonment may represent a significant threat to alpine biodiversity, especially that associated with open habitats. This study presents the first assessment of the potential effects of natural reforestation on dung beetles by exploring the relationships between the beetle community (abundance, diversity, species turnover and assemblage structure) and the vegetation stages of ecological succession following pastoral abandonment. A hierarchical sampling design was used in the montane belt of the Sessera Valley (north-western Italian Alps). Dung beetles were sampled across 16 sampling sites set in four habitat types corresponding to four different successional stages (pasture, shrub, pioneer forest and beech forest) at two altitudinal levels. The two habitats at the extremes of the ecological succession, i.e. pasture and beech forest, had the greatest effect on the structure of local dung beetle assemblages. Overall, dung beetle abundance was greater in beech forest, whereas species richness, Shannon diversity and taxonomic diversity were significantly higher in pasture, hence suggesting this latter habitat can be considered as a key conservation habitat. Forests and pastures shared a lower number of species than the other pairs of habitats (i.e. species turnover between these two habitats was the highest). The two intermediate seral stages, i.e. shrub and pioneer forest, showed low dung beetle abundance and diversity values. Local dung beetle assemblages were also dependent on season and altitude; early-arriving species were typical of pastures of high elevation, whereas late-arriving species were typical of beech forests. It is likely that grazing in the Alps will continue to decrease in the future leading to replacement of open habitats by forest. This study suggests therefore that, at least in the montane belt, reforestation may have potentially profound and negative effects on dung beetle diversity. Maintaining traditional pastoral activities appears to be the most promising approach to preserve open habitats and adjacent beech forests, resulting in the conservation of species of both habitats.     

Landscape- and time-dependent benefits of wildflower areas to ground-dwelling arthropods

Wildflower areas are a popular agri-environment scheme to counteract agro-biodiversity loss. Yet, their benefits are controversially discussed. Since inconsistent benefits may be owed to landscape context and temporal dynamics, we applied a multi-year study to unravel effects of permanent and transient habitats on ground-dwelling arthropods in wildflower areas and cereal fields.Across three consecutive years, we studied activity density, species richness and community composition of rove beetles, carabid beetles and spiders in ten pairs of wildflower areas and cereal fields along independent gradients of proportions of permanent semi-natural habitats or transient wildflower areas.Arthropod responses to the proportions of permanent semi-natural habitats often followed a hump-shaped pattern, whereas transient wildflower areas seemed to drive linear responses. An interactive effect on rove beetle richness in wildflower areas implies that benefits were highest either at intermediate proportions of permanent semi-natural habitats or at lower proportions, but with additional availability of transient wildflower areas or in landscapes with low proportions of permanent semi-natural habitats, but high proportions of wildflower areas. However, ground-dwelling arthropod activity density or species richness did not systematically increase over the three study years.Our results suggest that both permanent and transient habitats differ in how they affect biodiversity, possibly due to different temporal continuity and resource diversity. Benefits of permanent semi-natural habitats seemed highest at an equilibrium between an increasing resource-related species pool and an increasing diversity dilution, whereas benefits of transient wildflower areas seemed to increase with resource complementarity and connectivity at the landscape scale. Nevertheless, both habitats seem to complement each other and considered in concert, seem to be most effective in promoting benefits of wildflower areas to ground-dwelling arthropods at intermediate landscape complexity. The substantial variation in diversity patterns among years with weather extremes, suggests that optimizing benefits of wildflower areas requires further multi-year studies.