Evaluating hill prairie quality in the Midwestern United States using Auchenorrhyncha (Insecta: Hemiptera) and vascular plants: a case study in implementing grassland conservation planning and management

In this study a habitat quality index based on Auchenorrhyncha (Insecta: Hemiptera) species composition was used to investigate the index’s ability in discriminating hill prairie quality along a gradient of disturbance, based on the Illinois Natural Areas Inventory grading criteria; whether this index differs from other vegetation-based measures of quality; and examine the relationships between Auchenorrhyncha and vegetation integrity and diversity. Auchenorrhyncha and vascular plants were sampled from 14 Illinois glacial-drift hill prairies representing a range in quality. Insects and plants were sampled from late July through August, 2007 and analyzed using univariate and multivariate analyses. Results from this study showed that Floristic Quality Index, Auchenorrhyncha Quality Index, as well as other Auchenorrhyncha and plant diversity and integrity index values are greater in high, followed by mid, then low quality hill prairie remnants. Also, these analyses showed that perennial C4 grasses are strongly associated with prairie Auchenorrhyncha. These data suggest that judicious used of prescribed burning or brush removal may be needed to prevent woody-encroachment from eliminating prairie vegetation and Auchenorrhyncha on low quality sites; and restoration of perennial C4 grasses on low quality sites are needed to support more prairie Auchenorrhyncha fauna. Reintroductions of conservative (i.e., prairie-dependent and fire-sensitive) Auchenorrhyncha may also be needed to improve Auchenorrhyncha integrity on mid and low quality sites but these reintroductions need to be used in combination with reduced burn management or the inclusion of unburned refugia to reduce the extirpation of these fire-sensitive insects.     

Community Associations of Chalk Grassland Leafhoppers (Hemiptera: Auchenorrhyncha): Conclusions for Habitat Conservation

Due to their confinement to specific hostplants or restricted habitat types, Auchenorrhyncha have the potential to make suitable biological indicators to measure the quality of chalk grassland under different management practices for nature conservation. The Auchenorrhyncha data from a study designed to identify the factors influencing the invertebrate diversity of chalk grasslands in southern England was used to evaluate the potential use of this group of insects as biological indicators. Between 1998 and 2002 altogether 81 chalk grassland sites were sampled. Vegetation structure and composition were recorded, and Auchenorrhyncha were sampled at each site on three occasions in each of two seasons using a ‘Vortis’ suction sampler. Auchenorrhyncha assemblages were then linked to the different grassland plant communities occurring on chalk soils according to the British National Vegetation Classification (NVC). Altogether 96 Auchenorrhyncha species were recorded during the study. Using data on the frequency and dominance of species, as is commonly done for plant communities, it was possible to identify the preferential and differential species of distinct Auchenorrhyncha assemblages. Significant differences between the Auchenorrhyncha assemblages associated with the various chalk grassland plant communities of the NVC were observed down to a level of sub-communities. We conclude that data on Auchenorrhyncha assemblages can provide valuable information for the setting of conservation management priorities, where data on floristic composition alone may not be sufficient, providing additional information on aspects of vegetation structure and condition.     

Habitat Diversity in the Conservation of the Grassland Auchenorrhyncha (Homoptera: Cercopidae,Cicadellidae, Cixidae,Delphacidae) of Northern Britain

Definition of northern British grassland Auchenorrhyncha habitats was carried out using a classification based on analysis of data from 351 sites, involving 121 species, located between Greater Manchester and northern Scotland. Ten habitats were identified showing little influence of geographical position and exhibiting a basic upland-lowland trend. Other factors influencing habitat and species assemblage distribution were soil water, vegetation structure and land cover. An analysis of the species data with satellite-derived land cover data indicated that the lowland covers of tilled land, coast and urban and the upland covers of heath grassland and shrub heath were most important in affecting both species and assemblage distribution. The large-scale survey of grassland sites provided new information on both the ecology and distribution of individual Auchenorrhyncha species. Some were limited to specific habitat types but a considerable number were generalist species found in most or all of the 10 habitat types but showing preferences within upland to lowland or wet to dry site gradients. The ability to generate a subtle grassland Auchenorrhyncha habitat classification with large-scale survey results from standardised and reproducible sampling increases the potential for using habitat diversity for the conservation of grassland Auchenorrhyncha. Habitat preservation would also ensure that species richness (biodiversity) is maintained and that the habitats of rare species are conserved.     

Long‐term population trends in three grassland insect groups: a comparative analysis of 1951 and 2009

Development of farming practices has caused drastic changes in European agricultural landscapes during the past 50 years. As a consequence of these changes, insect diversity is widely expected to decline. We performed a comparative analysis with long‐term data of three insect groups: Auchenorrhyncha, Heteroptera and Orthoptera. In 2009, we revisited nine grassland sites in northern Germany that were originally sampled in 1951 using the same techniques and during a similar time frame. We found that the insect community exhibited no consistent trends between years. Species richness of Auchenorrhyncha and Heteroptera increased on plot level as well as on landscape level but remained unchanged for Orthoptera. Abundance of Auchenorrhyncha and Orthoptera significantly decreased, while Heteroptera increased. There is a strong trend towards homogeneity in community composition for Heteroptera and a weak one for Auchenorrhyncha. The frequency and abundance of species preferring disturbed and/or eutrophic habitats increased, whereas the number of species preferring low‐productive habitats declined. This trend is especially pronounced in Auchenorrhyncha. Generalistic species were more abundant in relative proportions as well as in absolute numbers. We hypothesize that these trends arise from alterations of Central European landscapes because of agricultural intensification over the last several decades.     

The Auchenorrhyncha fauna of peat bogs in the Austrian part of the Bohemian Forest (Insecta,Hemiptera)

The first overview on the Auchenorrhyncha fauna of peat bogs of the Austrian Bohemian Forest is presented. Seven oligotrophic peat bog sites were studied in 2011 by suction sampler (“G-Vac”) and 93 Auchenorrhyncha species (with 7465 adult specimens) were recorded. Eleven species (about 18 % of the individuals) are tyrphobiontic or tyrphophilous. The relative species abundance plot is not very steep; the six most abundant species represent 50 % of the individuals. The most common species is Conomelus anceps (17 % of the individuals). Compared to the whole Austrian Auchenorrhyncha fauna, the fauna of peat bogs comprises distinctly more univoltine species and more species hibernating in nymphal stage. Densities of adult Auchenorrhyncha in peat bogs are low in spring (about 10–60 individuals per m²) and high in July, with up to 180 (±50) individuals per m². Disturbed peat bogs have higher species numbers and higher Auchenorrhyncha densities in total, but lower numbers and densities in peat bog specialists.     

Direct and indirect effects of climate change on insect herbivores: Auchenorrhyncha (Homoptera)

1. Novel manipulations of local climate were employed to investigate how warmer winters with either wetter or drier summers would affect the Auchenorrhyncha, a major component of the insect fauna of grasslands. Direct and indirect effects of climate manipulation were found.
2. Supplemented summer rainfall resulted in an increase in vegetation cover, leading to an increase in the abundance of the Auchenorrhyncha.
3. Summer drought, however, caused a decrease in vegetation cover, but this did not lead to a corresponding decrease in the abundance of the Auchenorrhyncha.
4. Egg hatch and the termination of nymphal hibernation occurred earlier in winter warmed plots; however, the rate of nymphal development was unaffected.     

The influence of fire on Illinois hill prairie Auchenorrhyncha (Insecta: Hemiptera) diversity and integrity

Prescribed burning has been important in maintaining the structure of plant communities in the tallgrass prairie. However, implementation of these burn regimes often overlooks responses of other taxa, particularly arthropods. In this study, the timing and frequency of burns were examined on one of the most diverse and abundant groups of herbivorous insects, Auchenorrhyncha. These insects are ideal candidates in understanding the effects of fire on prairie arthropods because they are among the most numerous invertebrate herbivores in the prairie and they have ecological characteristics that confer a wide range of responses to prescribed burning. A total of 19 Illinois hill prairies were sampled along the Mississippi and Sangamon Rivers in the summer of 2006 using a modified leaf-blower vacuum. These sites exhibited a wide range of burn management, from unburned to recently burned, and having been burned multiple times. Species richness, Auchenorrhyncha Quality Index (with and without abundance data) and the mean coefficient of conservatism (with and without abundance data) were calculated for each site. Results suggest that unburned sites supported the greatest number of species and had higher Auchenorrhyncha Quality Index and mean coefficient of conservatism values than sites undergoing burn management. In order for land managers to maintain the prairie Auchenorrhyncha community and conserve vascular plants, this study recommends infrequent rotational burning with a minimum of 3?C5?years; although additional studies are needed to determine the appropriate number of years between each burn.     

The Distribution of Grassland Auchenorrhyncha Assemblages (Homoptera: Cercopidae, Cicadellidae, Delphacidae) in Northern England and Scotland

The distribution of Auchenorrhyncha species assemblages on 174 grassland sites in northern England and Scotland was investigated using ordination and classification techniques. Altitude appeared to be the most important environmental variable influencing assemblage distribution but the effects of altitude on soil type and moisture, and on plant composition, either herbaceous or woody, and structure were likely to have been primary influences. The main differences between sites in the eight habitat groups of the classification were products of these soil and plant variables, with the geographical position of sites in the survey area having less of an effect on site classification. A considerable number of nationally and regionally rare and scarce species were recorded. The results indicate that Auchenorrhyncha could be used in site conservation based on invertebrate species assemblages and rare species distribution but that more information is required to assess both habitat diversity and species rarity. More survey work would also be required to identify appropriate site management procedures for the conservation of Auchenorrhyncha within an overall programme for terrestrial invertebrates.     

Succession changes in diversity and assemblages composition of planthoppers and leafhoppers in natural ancient peat bogs in Belarus

Succession has a strong influence on species diversity and composition of terrestrial ecosystems. Peat bogs are among them. They have a large area in Belarus compared to other Central European countries. While in several studies have analyzed the effects of succession on vegetation in peat bog ecosystems, the response of peatland insects to succession has not been investigated yet. To address this issue were sampled Auchenorrhyncha abundance and environmental parameters on the ancient and one of the largest natural peat bog along a successional gradient from the margin to the bog dome. The results provide evidence that succession of peat bogs has influence on planthoppers and leafhoppers abundance, diversity and species composition. Along the successional gradient from younger towards older successional stages an increase abundance of specialized peat bog species, chamebionts, oligophagous and monophagous was observed. On the contrary, the younger stages of natural peat bog succession offer favorable conditions to eurytopic, polyphagous and chortobiont planthoppers and leafhoppers. The highest abundance and species richness of Auchenorrhyncha were in the lagg zone followed by early stages of natural peat bog succession. The highest diversity was in the middle stages of succession. A determinant of Auchenorrhyncha diversity was the cover of ericaceous dwarf shrubs. Linear models shrub cover and number of plants species had a positive effect on planthoppers and leafhoppers diversity and a negative effect on their abundance. Amount of ericaceous dwarf shrubs within the peat bog could be as a measure of heterogeneity.     

Higher‐level phylogeny of the insect order Hemiptera: is Auchenorrhyncha really paraphyletic?

The higher‐level phylogeny of the order Hemiptera remains a contentious topic in insect systematics. The controversy is chiefly centred on the unresolved question of whether or not the hemipteran suborder Auchenorrhyncha (including the extant superfamilies Fulgoroidea, Membracoidea, Cicadoidea and Cercopoidea) is a monophyletic lineage. Presented here are the results of a multilocus molecular phylogenetic investigation of relationships among the major hemipteran lineages, designed specifically to address the question of Auchenorrhyncha monophyly in the context of broad taxonomic sampling across Hemiptera. Phylogenetic analyses (maximum parsimony, maximum likelihood and Bayesian inference) were based on DNA nucleotide sequence data from seven gene regions (18S rDNA, 28S rDNA, histone H3, histone 2A, wingless, cytochrome c oxidase I and NADH dehydrogenase subunit 4) generated from 86 in‐group exemplars representing all major lineages of Hemiptera (plus seven out‐group taxa). All combined analyses of these data recover the monophyly of Auchenorrhyncha, and also support the monophyly of each of the following lineages: Hemiptera, Sternorrhyncha, Heteropterodea, Heteroptera, Fulgoroidea, Cicadomorpha, Membracoidea, Cercopoidea and Cicadoidea. Also presented is a review of the major lines of morphological and molecular evidence for and against the monophyly of Auchenorrhyncha.     

Migration of leafhoppers (Homoptera: Auchenorrhyncha) into a new polder

Auchenorrhyncha of a new polder were sampled by different kinds of traps in four stations in new habitats, one station on the salt marsh and one just outside the polder. In the latter stations 20 species of Auchenorrhyncha were caught in numbers that declined during the four year study. The proportion of macropters of the common Streptanus sordidus was highest in the largest catches. In the polder proper 392 specimens of 13 species were caught, all had moved at least 1500 m, but some could be traced to origins at greater distances. The number of immigrants also declined during the study. The distribution of the leafhoppers over the trapping stations suggests that leafhoppers, although sometimes transported over great distances, as a rule quickly fall out once they are airborne. Probably only one species had founded a resident population in the new polder at the end of the study.     

An evaluation of methods for assessing the impacts of Bt‐maize MON810 cultivation and pyrethroid insecticide use on Auchenorrhyncha (planthoppers and leafhoppers)

1 Auchenorrhyncha (Planthoppers and Leafhoppers) are not only pests of many crops, but they are also nontarget organisms with respect to Bt‐protein expressing genetically modified plants. As herbivorous arthropods, planthoppers and leafhoppers ingest Cry proteins depending on their feeding behaviour. Consequently, they are directly exposed to these entomotoxic proteins and can also serve as a source of Cry protein exposure to predatory arthropods. Therefore, it is reasonable to use Auchenorrhyncha in the risk assessment of genetically modified crops. 2 During a 2‐year field study, we evaluated four different methods in terms of their feasibility to assess the impacts of plant‐incorporated protectants from Bt‐maize and of insecticide use on this group of arthropods. Visual assessment of plants, sweep netting, yellow traps and custom made sticky traps were utilized in field plots of Bt‐maize MON810, untreated near‐isogenic maize and insecticide‐treated near‐isogenic maize and were compared with respect to their capability to reflect the diversity and abundance of Auchenorrhyncha species. 3 Zyginidia scutellaris (Herrich‐Schäffer) (Cicadomorpha: Cicadellidae) represented more than 94% of all captured individuals in both years. The analysis of Z. scutellaris data showed no consistent differences between Bt‐maize MON810 and the untreated near isogenic hybrid, demonstrating no negative impact of MON810 on this species. Insecticide treatment, on the other hand, was not equivalent to the isogenic maize in terms of Z. scutellaris densities. Based on the collected data and on practical considerations, we recommend the combined use of transect‐wise sweep netting and sticky traps for the sampling of Auchenorrhyncha in maize.     

Seasonality of sap-sucking insects (Auchenorrhyncha, Hemiptera) feeding on Ficus (Moraceae) in a lowland rain forest in New Guinea

Sap-sucking insects (Auchenorrhyncha, Hemiptera) were sampled quantitatively from the foliage of 15 species of Ficus (Moraceae) in a lowland rain forest in Papua New Guinea. Continuous sampling throughout 12 months produced 61,777 individuals and 491 species. Two seasonality parameters, circular statistics and Lloyd's index, were calculated for 139 species with a sample size of more than 36 individuals. Most of the species were present in the adult stage for at least half of the year, and many of them continuously throughout the year. However, almost all species exhibited marked seasonal changes in abundance. The abundance peaks of species were scattered throughout most of the year, but more species reached their population maximum during the wet, especially early wet, season than during the dry season. Overall species richness and abundance of Auchenorrhyncha were also higher during the wet than the dry season. A significant correlation between seasonality and host specificity was revealed in the auchenorrhynchan community. In particular, species evenly distributed throughout the year had a tendency to feed on a larger number of Ficus species than seasonally more restricted species. The seasonality, and the seasonality versus specificity correlation, were independent of species abundance. Among the most abundant species (n > 300) there was a marginally significant negative correlation between abundance and host specificity, so that polyphagous species had, on average, larger populations than specialists. There was no similar correlation among rarer species. The Auchenorrhyncha comprises three feeding guilds, which were also analysed separately. The mesophyll-feeding guild exhibited more pronounced seasonality than the phloem- and xylem-feeders. This difference could be explained as a part of the overall correlation between seasonality and host specificity as mesophyll-feeders were significantly more host specific than the other two guilds. Received: 26 January 1998 / Accepted: 9 March 1998     

Morphology of arolia in Auchenorrhyncha (Insecta,Hemiptera)

The pretarsal arolium serves as an attachment device in many groups of insects, enabling them to walk efficiently on smooth surfaces, where claws alone do not provide sufficient foothold. The arolia of representatives of all major lineages of Auchenorrhyncha are described and illustrated, mainly using scanning electron microscopy and histology. Glands inside the lumen of the arolia are described for the first time in this group. It is shown that the morphology of arolia within Auchenorrhyncha differs considerably. Some of them are even distinctly bilobed. The cuticle of the contact zone is thickened and formed of branching chitinous rods. In some cases, two layers of rods oriented in different directions were found. An extended definition of “arolium” is proposed. J. Morphol. 275:1217–1225, 2014. © 2014 Wiley Periodicals, Inc.     

Using Auchenorrhyncha (Insecta: Hemiptera) to develop a new insect index in measuring North American tallgrass prairie quality

Auchenorrhyncha (i.e., leafhoppers, treehoppers, spittlebugs, and planthoppers) represent some of the most diverse groups of herbivorous insects in the tallgrass prairie biome, they have close associations with many native prairie grasses and forbs, and respond in predictable ways to changes in native grassland degradation. These attributes make Auchenorrhyncha ideal candidates in the development of a habitat quality index to measure tallgrass prairie quality. In this study we propose the development of a species-based habitat quality index called the Auchenorrhyncha quality index or AQI as a useful method in tracking the condition of tallgrass prairie quality. The AQI is computed by summing six ecological characteristics (i.e., host plant specificity, voltinism, overwintering microhabitat, wing length, habitat fidelity, and origin) for each Auchenorrhynchan insect encountered, yielding coefficient of conservatism (CC) values that range from 0 (habitat generalist/tolerant to disturbance) to 18 (habitat specific/intolerant to disturbance). These CC values are averaged and combined with species richness producing un-weighted by abundance AQI (AQI_w/outN) and weighted by abundance AQI (AQI_w/N). The performance of the AQI was evaluated by examining the effects of sampling intensity on this index using a sweep net and a vacuum apparatus from 10 sites located on the three main North American tallgrass prairie communities, wet-mesic, sand, and loess hill. Scientists and land managers can adequately sample Auchenorrhyncha from four transects using a vacuum. Also, the highest AQI values were found from loess hill and sand prairies, indicating that conservation efforts should focus on these prairie communities. Additional applications of the AQI may include: (1) discriminating prairie quality at various spatial scales; (2) testing hypotheses about the effects of disturbance on prairie habitat (e.g. prescribed burning); (3) using the AQI as a model in developing habitat quality indices based on other diverse groups of grassland insects; and (4) the AQI has the capacity to be readily modified in assessing the quality of other biomes. Ultimately, the AQI should be used in combination with other habitat quality indices based on other diverse groups of organisms, such as plants and other insects, to provide a more complete assessment of native habitat quality.     

DNA Barcodes for Nearctic Auchenorrhyncha (Insecta: Hemiptera)

Background

Many studies have shown the suitability of sequence variation in the 5′ region of the mitochondrial cytochrome c oxidase I (COI) gene as a DNA barcode for the identification of species in a wide range of animal groups. We examined 471 species in 147 genera of Hemiptera: Auchenorrhyncha drawn from specimens in the Canadian National Collection of Insects to assess the effectiveness of DNA barcoding in this group.

Methodology/Principal Findings

Analysis of the COI gene revealed less than 2% intra-specific divergence in 93% of the taxa examined, while minimum interspecific distances exceeded 2% in 70% of congeneric species pairs. Although most species are characterized by a distinct sequence cluster, sequences for members of many groups of closely related species either shared sequences or showed close similarity, with 25% of species separated from their nearest neighbor by less than 1%.

Conclusions/Significance

This study, although preliminary, provides DNA barcodes for about 8% of the species of this hemipteran suborder found in North America north of Mexico. Barcodes can enable the identification of many species of Auchenorrhyncha, but members of some species groups cannot be discriminated. Future use of DNA barcodes in regulatory, pest management, and environmental applications will be possible as the barcode library for Auchenorrhyncha expands to include more species and broader geographic coverage.     

Wing base structure supports Coleorrhyncha + Auchenorrhyncha (Insecta: Hemiptera)

The phylogenetic placement of the moss bugs (Insecta: Hemiptera: Coleorrhyncha) has been highly controversial. Many apparent morphological apomorphies support the close relationship between Coleorrhyncha and Heteroptera (=true bugs). However, a recent phylogenomic study strongly supported a sister group relationship between Coleorrhyncha and Auchenorrhyncha (planthoppers, leafhoppers, treehoppers, spittlebugs, and cicadas). To test these two alternative hypotheses, we examined the fore‐ and hindwing base structure of the only known extant macropterous species of Coleorrhyncha using binocular and confocal laser scanning microscopes and analyzed the data selected from the wing base phylogenetically. When full morphological data including the wing base characters were analyzed, the sister group relationship between Coleorrhyncha + Heteroptera was supported, agreeing with previous consensus based on morphology. In contrast, when only wing base characters were analyzed separately, the clade Coleorrhyncha + Auchenorrhyncha was recovered, in agreement with the result from the phylogenomic study. The membranous condition of the proximal median plate in the forewing was identified as a potential synapomorphy of the latter grouping, and the absence of the tegula was excluded as a potential synapomorphy of Coleorrhyncha and Heteroptera.     

The Use of Habitat Models in Conservation of Rare and Endangered Leafhopper Species (Hemiptera,Auchenorrhyncha)

For conservation of Auchenorrhyncha species, knowledge of their habitat requirements is essential. However, for most species there is no ‘quantitative’ knowledge that would allow e.g. spatially explicit predictions. Such predictions can be made by habitat models, which quantify the relationship between the environment and the occurrence of species. In two plot-based case studies – the endangered leafhopper Verdanus bensoni in mountainous grasslands and four endangered Auchenorrhyncha in urban brownfields – we used habitat models to quantify the habitat requirements of these five species and to exemplify their use for creating habitat suitability maps. In the first case study, the multivariate model showed that occurrence probabilities of the leafhopper V. bensoni increase with both decreasing nitrogen indicator values and decreasing tree cover. On urban brownfields, successional age was a driving factor for species’ occurrence. Site age largely determines a range of vegetation characteristics, which, in multivariate models, often replaced the variable age. Internal validation showed the robustness of all models. The models allow predictions of habitat quality under different management regimes (e.g. response to fertilization or abandonment for V. bensoni or to different turnover rates on brownfield sites). We discuss the application of habitat models in the conservation of Auchenorrhyncha, especially the use of habitat suitability maps.     

Diversity and temporal variations of the Hemiptera Auchenorrhyncha fauna in the Ajaccio region (France,Corsica)

Summary

During a one-year survey of the Auchenorrhyncha fauna in a maquis habitat of the Ajaccio region (Corsica), 37 species were listed including three alien species recorded in Europe in the last decades. The standard 658 bp mitochondrial COI barcode was obtained for 32 species, including 14 species never previously barcoded. Neighbor-joining analyses confirmed the delineation for all the species. However, comparisons with available sequences from mainland Europe showed that four species presented a significant intraspecific divergence (>3%), whereas a reduced interspecific divergence was found for another set of species. Complementary studies may therefore be necessary to better assess their taxonomic levels. Three species – Euscelis lineolata Brullé, 1832 (Cicadellidae), Philaenus spumarius (Linnaeus, 1758) (Aphrophoridae) and Latilica maculipes (Melichar, 1906) (Issidae) – accounted for up to 74.3% of the total insects collected. Although taxonomic interpretations using restricted sampling and COI sequences alone are not robust, the proportion of new sequences highlight the global lack of knowledge about the Auchenorrhyncha as a whole and the potentially presence of cryptic taxa in different clades.