The forest, the cicadas and the holey fluxes: Periodical cicada impacts on soil respiration depends on tree mycorrhizal type.

The emergence of billions of periodical cicadas affects plant and animal communities profoundly, yet little is known about cicada impacts on soil carbon fluxes. We investigated the effects of Brood X cicadas (Magicicada septendecim, M. cassinii and M. septendeculain) on soil CO2 fluxes (RS ) in three Indiana forests. We hypothesized RS would be sensitive to emergence hole density, with the greatest effects occurring in soils with the lowest ambient fluxes. In support of our hypothesis, RS increased with increasing hole density and greater effects were observed near AM-associating trees (which expressed lower ambient fluxes) than near EcM-associating trees. Additionally, RS from emergence holes increased the temperature sensitivity (Q10 ) of RS by 13%, elevating the Q10 of ecosystem respiration. Brood X cicadas increased annual RS by ca. 2.5%, translating to an additional 717 Gg of CO2 across forested areas. As such, periodical cicadas can have substantial effects on soil processes and biogeochemistry.

Variation in Avian Predation Pressure as a Driver for the Diversification of Periodical Cicada Broods.

AbstractPeriodical cicadas live 13 or 17 years underground as nymphs, then emerge in synchrony as adults to reproduce. Developmentally synchronized populations called broods rarely coexist, with one dominant brood locally excluding those that emerge in off years. Twelve modern 17-year cicada broods are believed to have descended from only three ancestral broods following the last glaciation. The mechanisms by which these daughter broods overcame exclusion by the ancestral brood to synchronously emerge in a different year, however, are elusive. Here, we demonstrate that temporal variation in the population density of generalist predators can allow intermittent opportunities for new broods to invade, even though a single brood remains dominant most of the time. We show that this mechanism is consistent, in terms of the type and frequency of brood replacements, with the distribution of periodical cicada broods throughout North America today. Although we investigate one particularly charismatic case study, the mechanisms involved (competitive exclusion, Allee effects, trait variation, predation, and temporal variability) are ubiquitous and could contribute to patterns of species diversity in a range of systems.

Contaminant Removal from Nature's Self-Cleaning Surfaces.

Many organisms in nature have evolved superhydrophobic surfaces that leverage water droplets to clean themselves. While this ubiquitous self-cleaning process has substantial industrial promise, experiments have so far been unable to comprehend the underlying physics. With the aid of molecular simulations, here we rationalize and theoretically explain self-cleaning mechanisms by resolving the complex interplay between particle-droplet and particle-surface interactions, which originate at the nanoscale. We present a universal phase diagram that consolidates (a) observations from previous surface self-cleaning experiments conducted at micro-to-millimeter length scales and (b) our nanoscale particle-droplet simulations. Counterintuitively, our analysis shows that an upper limit for the radius of the droplet exists to remove contaminants of a particular size. We are now able to predict when and how particles of varying scale (from nano-to-micrometer) and adhesive strengths are removed from superhydrophobic surfaces.

Periodical Cicada Emergences Affect Masting Behavior of Oaks.

AbstractOaks (Quercus spp.) are masting species exhibiting highly variable and synchronized acorn production. We investigated the hypothesis that periodical cicadas (Magicada spp.), well known to have strong effects on the ecosystems in which they occur, affect acorn production of oaks through their xylem feeding habits as nymphs, the oviposition damage they inflict as adults during emergences, or the nutrient pulse resulting from the decomposition of their bodies following breeding. We found negative effects on acorn production during emergence years and the year following emergences and enhanced acorn production 2 years after emergence. We also found evidence indicating a significant effect of cicada emergences on spatial synchrony of acorn production by trees growing within the range of the same cicada brood compared with different broods. These results demonstrate that periodical cicadas act as a trophic environmental "veto" depressing acorn production during and immediately following emergences, after which the nutrient pulse associated with the cicada's demise enhances oak reproduction.

Multiple origins of interdependent endosymbiotic complexes in a genus of cicadas.

Bacterial endosymbionts that provide nutrients to hosts often have genomes that are extremely stable in structure and gene content. In contrast, the genome of the endosymbiont Hodgkinia cicadicola has fractured into multiple distinct lineages in some species of the cicada genus Tettigades To better understand the frequency, timing, and outcomes of Hodgkinia lineage splitting throughout this cicada genus, we sampled cicadas over three field seasons in Chile and performed genomics and microscopy on representative samples. We found that a single ancestral Hodgkinia lineage has split at least six independent times in Tettigades over the last 4 million years, resulting in complexes of between two and six distinct Hodgkinia lineages per host. Individual genomes in these symbiotic complexes differ dramatically in relative abundance, genome size, organization, and gene content. Each Hodgkinia lineage retains a small set of core genes involved in genetic information processing, but the high level of gene loss experienced by all genomes suggests that extensive sharing of gene products among symbiont cells must occur. In total, Hodgkinia complexes that consist of multiple lineages encode nearly complete sets of genes present on the ancestral single lineage and presumably perform the same functions as symbionts that have not undergone splitting. However, differences in the timing of the splits, along with dissimilar gene loss patterns on the resulting genomes, have led to very different outcomes of lineage splitting in extant cicadas.

Recurrent symbiont recruitment from fungal parasites in cicadas.

Diverse insects are associated with ancient bacterial symbionts, whose genomes have often suffered drastic reduction and degeneration. In extreme cases, such symbiont genomes seem almost unable to sustain the basic cellular functioning, which comprises an open question in the evolution of symbiosis. Here, we report an insect group wherein an ancient symbiont lineage suffering massive genome erosion has experienced recurrent extinction and replacement by host-associated pathogenic microbes. Cicadas are associated with the ancient bacterial co-obligate symbionts Sulcia and Hodgkinia, whose streamlined genomes are specialized for synthesizing essential amino acids, thereby enabling the host to live on plant sap. However, our inspection of 24 Japanese cicada species revealed that while all species possessed Sulcia, only nine species retained Hodgkinia, and their genomes exhibited substantial structural instability. The remaining 15 species lacked Hodgkinia and instead harbored yeast-like fungal symbionts. Detailed phylogenetic analyses uncovered repeated Hodgkinia-fungus and fungus-fungus replacements in cicadas. The fungal symbionts were phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, identifying entomopathogenic origins of the fungal symbionts. Most fungal symbionts of cicadas were uncultivable, but the fungal symbiont of Meimuna opalifera was cultivable, possibly because it is at an early stage of fungal symbiont replacement. Genome sequencing of the fungal symbiont revealed its metabolic versatility, presumably capable of synthesizing almost all amino acids, vitamins, and other metabolites, which is more than sufficient to compensate for the Hodgkinia loss. These findings highlight a straightforward ecological and evolutionary connection between parasitism and symbiosis, which may provide an evolutionary trajectory to renovate deteriorated ancient symbiosis via pathogen domestication.

One Hundred Mitochondrial Genomes of Cicadas.

Mitochondrial genomes can provide valuable information on the biology and evolutionary histories of their host organisms. Here, we present and characterize the complete coding regions of 107 mitochondrial genomes (mitogenomes) of cicadas (Insecta: Hemiptera: Auchenorrhyncha: Cicadoidea), representing 31 genera, 61 species, and 83 populations. We show that all cicada mitogenomes retain the organization and gene contents thought to be ancestral in insects, with some variability among cicada clades in the length of a region between the genes nad2 and cox1, which encodes 3 tRNAs. Phylogenetic analyses using these mitogenomes recapitulate a recent 5-gene classification of cicadas into families and subfamilies, but also identify a species that falls outside of the established taxonomic framework. While protein-coding genes are under strong purifying selection, tests of relative evolutionary rates reveal significant variation in evolutionary rates across taxa, highlighting the dynamic nature of mitochondrial genome evolution in cicadas. These data will serve as a useful reference for future research into the systematics, ecology, and evolution of the superfamily Cicadoidea.

How the Aridification of Australia Structured the Biogeography and Influenced the Diversification of a Large Lineage of Australian Cicadas.

Over the last 30 million years, Australia's landscape has undergone dramatic cooling and drying due to the establishment of the Antarctic Circumpolar Current and change in global CO$_{2}$ levels. Studies have shown that many Australian organisms went extinct during these major cooling events, while others experienced adaptive radiations and increases in diversification rates as a result of exploiting new niches in the arid zone. Despite the many studies on diversification and biogeography in Australia, few have been continent-wide and none have focused on a group of organisms adapted to feeding on plants. We studied 162 species of cicadas in the Australian Pauropsalta complex, a large generic lineage within the tribe Cicadettini. We asked whether there were changes in the diversification rate of Pauropsalta over time and if so: 1) which clades were associated with the rate change? 2) did timing of rate shifts correspond to known periods of dramatic historical climate change, 3) did increases in diversification rate along select lineages correspond to adaptive radiations with movement into the arid zone? To address these questions, we estimated a molecular phylogeny of the Pauropsalta complex using ${\sim}$5300 bp of nucleotide sequence data distributed among five loci (one mtDNA locus and four nDNA loci). We found that this large group of cicadas did not diversify at a constant rate as they spread through Australia; instead the signature of decreasing diversification rate changed roughly around the time of the expansion of the east Antarctic ice sheets ${\sim}$16 Ma and the glaciation of the northern hemisphere ${\sim}$3 Ma. Unlike other Australian taxa, the Pauropsalta complex did not explosively radiate in response to an early invasion of the arid zone. Instead multiple groups invaded the arid zone and experienced rates of diversification similar to mesic-distributed taxa. We found evidence for relictual groups, located in pre-Mesozoic habitat, that have not diversified and continue to reside on mesic hosts in isolated "habitat islands". Future work should focus on groups of similar ages with similar distribution patterns to determine whether this tempo and pattern of diversification and biogeography is consistent with evidence from other phytophagous insects.

No Transcriptional Compensation for Extreme Gene Dosage Imbalance in Fragmented Bacterial Endosymbionts of Cicadas.

Bacteria that form long-term intracellular associations with host cells lose many genes, a process that often results in tiny, gene-dense, and stable genomes. Paradoxically, the some of the same evolutionary processes that drive genome reduction and simplification may also cause genome expansion and complexification. A bacterial endosymbiont of cicadas, Hodgkinia cicadicola, exemplifies this paradox. In many cicada species, a single Hodgkinia lineage with a tiny, gene-dense genome has split into several interdependent cell and genome lineages. Each new Hodgkinia lineage encodes a unique subset of the ancestral unsplit genome in a complementary way, such that the collective gene contents of all lineages match the total found in the ancestral single genome. This splitting creates genetically distinct Hodgkinia cells that must function together to carry out basic cellular processes. It also creates a gene dosage problem where some genes are encoded by only a small fraction of cells while others are much more abundant. Here, by sequencing DNA and RNA of Hodgkinia from different cicada species with different amounts of splitting-along with its structurally stable, unsplit partner endosymbiont Sulcia muelleri-we show that Hodgkinia does not transcriptionally compensate to rescue the wildly unbalanced gene and genome ratios that result from lineage splitting. We also find that Hodgkinia has a reduced capacity for basic transcriptional control independent of the splitting process. Our findings reveal another layer of degeneration further pushing the limits of canonical molecular and cell biology in Hodgkinia and may partially explain its propensity to go extinct through symbiont replacement.

Introduction to the study of chromosomal and reproductive patterns in Paraneoptera.

This paper opens the themed issue (a monograph) "Aberrant cytogenetic and reproductive patterns in the evolution of Paraneoptera", prepared by a Russian-Bulgarian research team on the basis of long-term collaborative studies. In this first part of the issue, we provide the basic introductory information, describe the material involved and the methods applied, and give terminology and nomenclature of used taxonomic names.

An impressive new species of mugadina from queensland with notes on a congeneric species (cicadidae: cicadettinae: cicadettini).

This contribution details the morphology, distribution, and song characteristics of a new grass cicada species within the genus Mugadina Moulds, 2012, previously represented by only two much smaller species. The new species is M. superba sp. n. It occurs widely in central Queensland, occurring in a broad curved zone between the western desert areas and the eastern coast. Details of the morphology and the ticking calling songs presented are given, and detailed comparisons are made of morphology and songs between M. superba sp. n. and M. marshalli (Distant, 1911).

Checklist and provisional atlas of singing cicadas (Hemiptera: Cicadidae) of Bulgaria, based on bioacoustics.

BACKGROUND: The singing cicadas (Hemiptera: Cicadidae) of Bulgaria were poorly known. There are published records for 14 species: Cicada orni, Lyristes plebejus, Cicadatra atra, Cicadatra hyalina, Cicadatra persica, Cicadetta montana, Cicadetta mediterranea, Dimissalna dimissa, Oligoglena tibialis, Tympanistalna gastrica, Pagiphora annulata, Saticula coriaria, Tibicina haematodes and Tibicina steveni. NEW INFORMATION: Two species from this list were doubtful in the beginning of our study, since Tympanistalna gastrica is distributed in central and southern Portugal and Saticula coriaria is a north African species.We checked three major institutional collections housed in Sofia, Bulgaria: the National Museum of Natural History (SOFM), the Institute of Zoology (ZISB) and the Biology Faculty of Sofia University "St. Kliment Ohridski" (BFUS). We confirmed 11 of the species mentioned in literature, except Cicadetta mediterranea and found two additional species: Cicadatra platyptera and Cicadetta macedonica (the specimens in BFUS were bioacoustically confirmed).Based on this knowledge, we further investigated the singing cicadas of Bulgaria with the use of morphological and bioacoustic methods in the years 2008, 2009, 2010, 2012, 2016, 2018 and 2019. We were not able to confirm the presence of Cicadatra persica and Cicadetta mediterranea, but found three additional species: Cicadetta brevipennis s. lat., Cicadetta cantilatrix and Tettigettula pygmea. Using the bioacoustic methods, we also detected unknown singing patterns, which could belong to three or four additional taxa, which need to be described.The Bulgarian fauna of singing cicadas at the moment consists of 16 confirmed and 3-4 potential species.

A revision of the Australian cicada genus Punia Moulds, 2012 (Cicadidae: Cicadettinae: Cicadettini) with the description of four new species.

Punia minima (Goding Froggatt, 1904) from the Northern Territory is redescribed and the female described for the first time. Four new species found across the monsoonal north of Australia are documented: P. hyas sp.n., P. limpida sp.n., P. kolos sp.n. and P. queenslandica sp.n. A key to all five species is provided and their phylogenetic relationships discussed.

Homologous series by Nikolai Vavilov in the phylogeny of Homoptera.

The paper briefly discusses the most impressive examples of the Nikolai Vavilov's "Law of homologous series" in the evolution of one of the largest animal groups, homopterous insects, which comprise about 65,000 recent species in the world fauna. Different taxonomic and phylogenetic characters (morpho-anatomical, cytogenetic, reproductive and others) are considered at the taxonomic ranks of the order, suborder, superfamily and family.

A new species of Okanagana from the Walker Lane region of Nevada and California (Hemiptera: Auchenorrhyncha: Cicadidae).

Okanagana boweni sp. n. is described from the western margin of the Great Basin of North America. The new species is diagnosed from allopatric O. simulata Davis and sympatric O. utahensis Davis using morphological, bioacoustical, and molecular characters. The distribution of this new species coincides with the Walker Lane region that lies along the border of California and Nevada, USA. Based on geography, bioacoustics, morphology, and molecular phylogenetics, we hypothesize that O. boweni sp. n. is the allopatric sister species of O. simulata.

The effects of pulsed fertilization and chronic herbivory by periodical cicadas on tree growth.

Although many studies have investigated plant growth in the context of episodic herbivory and pressed resource availability, relatively few have examined how plant growth is affected by pulsed resources and chronic herbivory. Periodical cicada (Magicicada spp.) adults represent a pulsed detrital subsidy that fertilizes plants, and live cicada nymphs are long-lived root-feeding herbivores. Previous studies of cicada herbivory effects have been inconclusive, and previous studies of cicada-mediated fertilization did not examine effects on trees, or on a multiyear timescale. Here, we describe the results of a 3-yr experiment that factorially manipulated the presence and absence of cicada fertilization and herbivory in a population of 100 American sycamore (Platanus occidentalis) trees. We found that cicada fertilization strongly increased tree growth in the year of emergence, creating differences in tree size that persisted at least 2 yr later. By comparison, we did not detect reductions in tree growth associated with cicada herbivory in any year of this experiment. However, cicada herbivory reduced the densities of, and damage from, other aboveground herbivores. These results suggest that cicadas affect the size structure of forests over multiple years, and raise questions about how cicada-mediated fertilization and herbivory will affect tree growth over longer timescales.

An Identification key to the species of Auchenorrhyncha of Iranian fauna recorded as pests in orchards and a review on the pest status of the species.

An illustrated dichotomous identification key for a total of 54 Auchenorrhyncha species of Iran is presented. The studied species have been recorded as pests and vectors of diseases to fruit trees. Twenty nine records were contributed to Iranian orchards and 25 of which were from other parts of the world. Hence, the latter group can be considered as potential pests and vectors in Iran. Reviewing the published information on the former group suggests 12 species as pests (4, 2 and 6 species with significant, minor, and unknown recorded economic damage levels, respectively). The pest status of 14 recorded pest species were quite doubtful and 3 of them could not be present in Iran due to the lack of evidence or their limited distribution in other parts of the world. The 4 species which were recognized as well known and significantly important pests belonged to the families: Tropiduchidae (Ommatissus lybicus Bergevin, 1930), Cicadidae (Cicadatra alhageos (Kolenati, 1857)), and Cicadellidae (Hishimonus phycitis (Distant, 1908) and Neoaliturus haematoceps (Mulstant et Rey, 1855)). One species Orosanga japonicus is recording for the first time from Iran and added to the key.

Two new genera and five new species of Mugadina-like small grass cicadas (Hemiptera: Cicadidae: Cicadettini) from Central and Eastern Australia: comparative morphology, songs, behaviour and distributions.

Moulds (2012) established the genus Mugadina for two small cicadas, M. marshalli (Distant) and M. emma (Goding and Froggatt), both grass inhabiting species known from Queensland and New South Wales. Both species are notable for their relatively simple 'ticking' songs. Moulds further noted that there were at least two superficially similar genera of cicadas, but each with different genitalia. This paper describes two new genera of small (9-15 mm body lengths) and distinctive grass cicadas with genitalia that are very similar to those of Mugadina, but possess clear morphological, colour and calling song differences. The new genera are: Heremusina n. gen. with two known species namely H. udeoecetes n. sp. and H. pipatio n. sp.; the second new genus is Xeropsalta n. gen., containing four known species, X. thomsoni n. sp., X. aridula n. sp., X. rattrayi n. sp., and X. festiva n. comb. Heremusina n. gen. species are described from the Alice Springs area of Northern Territory and the Cloncurry area of northwest Queensland, from arid to semi arid habitats. The Xeropsalta n. gen. species are described from western, southwest and central Queensland, and from the Simpson and Strzelecki Deserts in northeastern South Australia and northwestern New South Wales, respectively, all locations in very arid to arid habitats, but close to seasonal (often irregular) rivers and lakes. X. festiva n. comb. occurs in semi arid habitats in southern and southeastern Australia.        Detailed taxonomic descriptions are provided of the new species, together with distributions, habitats, and the calling songs. The Heremusina species emit songs with short repetitive buzzing echemes, the echeme durations differing between each species. The Xeropsalta songs are notable for their complexity, containing multiple elements with rapid changes of amplitudes and temporal structures, rather atypical of the songs of most small grass dwelling cicadas. Detailed song structures distinguishing each of the species are illustrated and interpreted in each case in light of their respective taxonomic status.

Idiosyncratic Genome Degradation in a Bacterial Endosymbiont of Periodical Cicadas.

When a free-living bacterium transitions to a host-beneficial endosymbiotic lifestyle, it almost invariably loses a large fraction of its genome [1, 2]. The resulting small genomes often become stable in size, structure, and coding capacity [3-5], as exemplified by Sulcia muelleri, a nutritional endosymbiont of cicadas. Sulcia's partner endosymbiont, Hodgkinia cicadicola, similarly remains co-linear in some cicadas diverged by millions of years [6, 7]. But in the long-lived periodical cicada Magicicada tredecim, the Hodgkinia genome has split into dozens of tiny, gene-sparse circles that sometimes reside in distinct Hodgkinia cells [8]. Previous data suggested that all other Magicicada species harbor complex Hodgkinia populations, but the timing, number of origins, and outcomes of the splitting process were unknown. Here, by sequencing Hodgkinia metagenomes from the remaining six Magicicada and two sister species, we show that each Magicicada species harbors Hodgkinia populations of at least 20 genomic circles. We find little synteny among the 256 Hodgkinia circles analyzed except between the most closely related cicada species. Gene phylogenies show multiple Hodgkinia lineages in the common ancestor of Magicicada and its closest known relatives but that most splitting has occurred within Magicicada and has given rise to highly variable Hodgkinia gene dosages among species. These data show that Hodgkinia genome degradation has proceeded down different paths in different Magicicada species and support a model of genomic degradation that is stochastic in outcome and nonadaptive for the host. These patterns mirror the genomic instability seen in some mitochondria.

Simultaneous modelling of distributional patterns in a guild of eastern-Australian cicadas.

The distributions, with respect to habitat structure, of nine species of eastern-Australian cicadas have been shown to be non-random. The most striking consequence of this non-randomness is a marked inverse relationship between habitat breadth and habitat position (terms defined in text). Eight basic models and 12 derived models were used in conjunction with a canonical space to try to account for the ways in which the species of cicadas were distributed with respect to habitat. Several models produced results that were in reasonable agreement with the observed data. The most parsimonious of these corresponds to analytical results of other workers, such as Diamond's (1975) incidence curves, occurrence sequences (Schoener and Schoener 1983), and probability functions (Adler and Wilson 1985). The distributions of cicadas can be modelled by assuming that the species occupy sites independently of one another. These species of cicadas are unlikely to engage in interspecific competition, which is consistent with independence of distributions.