Periodical Cicadas Research Articles

Cytogenetic characterization of periodical cicadas (Hemiptera: Cicadidae: Magicicada)

The periodical cicadas of the genus Magicicada Davis, 1925 inhabiting eastern United States are characterized by a long juvenile period of 17 or 13 years and periodical mass emergence of adults. In this genus, only seven species are distinguished and are distributed into three species groups, Decim, Cassini and Decula. We performed comparative cytogenetic study of all seven Magicicada species, and 6 of them were explored for the first time. The techniques used included standard chromosome staining, differential chromosome staining techniques (C-banding, AgNOR-banding and fluorochrome DAPI-staining) and FISH (fluorescence in situ hybridization) with 18S rDNA and (TTAGG)n-telomeric probes. All these species have holokinetic chromosomes, like other Hemiptera. Karyotypes of all species appeared to be remarkably conserved with 2n = 19/20 (18 + X0/XX) (male/female); one very large pair of autosomes and all other chromosomes constituting a decreasing size series; X chromosomes were indistinguishable, at least, at mitotic metaphases. The nucleolus organizer regions (NORs) revealed on one of the medium-sized chromosome pairs in all species and were shown to coincide with the rDNA clusters revealed by FISH. In all species, very small blocks of C-heterochromatin were variously located on chromosomes clearly using DAPI but less distinctly by C-banding. The chromosomes of all the species studied were confirmed to contain the "insect type" motif of telomeres (TTAGG)n.

Hybridization selects for prime-numbered life cycles in Magicicada: An individual-based simulation model of a structured periodical cicada population.

We investigate competition between separate periodical cicada populations each possessing different life‐cycle lengths. We build an individual‐based model to simulate the cicada life cycle and allow random migrations to occur between patches inhabited by the different populations. We show that if hybridization between different cycle lengths produces offspring that have an intermediate life‐cycle length, then predation acts disproportionately to select against the hybrid offspring. This happens because they emerge in low densities without the safety‐in‐numbers provided by either parent population. Thus, prime‐numbered life cycles that can better avoid hybridization are favored. However, we find that this advantage of prime‐numbered cycles occurs only if there is some mechanism that can occasionally synchronize emergence between local populations in sufficiently many patches.

Self-organizing cicada choruses respond to the local sound and light environment.

Periodical cicadas exhibit an extraordinary capacity for self‐organizing spatially synchronous breeding behavior. The regular emergence of periodical cicada broods across the United States is a phenomenon of longstanding public and scientific interest, as the cicadas of each brood emerge in huge numbers and briefly dominate their ecosystem. During the emergence, the 17‐year periodical cicada species Magicicada cassini is found to form synchronized choruses, and we investigated their chorusing behavior from the standpoint of spatial synchrony.Cicada choruses were observed to form in trees, calling regularly every five seconds. In order to determine the limits of this self‐organizing behavior, we set out to quantify the spatial synchronization between cicada call choruses in different trees, and how and why this varies in space and time.We performed 20 simultaneous recordings in Clinton State Park, Kansas, in June 2015 (Brood IV), with a team of citizen‐science volunteers using consumer equipment (smartphones). We use a wavelet approach to show in detail how spatially synchronous, self‐organized chorusing varies across the forest.We show how conditions that increase the strength of audio interactions between cicadas also increase the spatial synchrony of their chorusing. Higher forest canopy light levels increase cicada activity, corresponding to faster and higher‐amplitude chorus cycling and to greater synchrony of cycles across space. We implemented a relaxation‐oscillator‐ensemble model of interacting cicadas, finding that a tendency to call more often, driven by light levels, results in all these effects.Results demonstrate how the capacity to self‐organize in ecology depends sensitively on environmental conditions. Spatially correlated modulation of cycling rate by an external driver can also promote self‐organization of phase synchrony.

Evaluation of Organically Acceptable Methods to Control Periodical Cicada (Hemiptera: Cicadidae) Oviposition Injury on Nonbearing Apple Trees

Abstract Broad-spectrum insecticides are the standard control method used in tree fruit orchards to control periodical cicadas (Magicicada spp.) and to reduce associated oviposition injury to woody...

An augmented wood-penetrating structure: Cicada ovipositors enhanced with metals and other inorganic elements

Few insect species are as popular as periodical cicadas (Magicicada spp.). Despite representing an enormous biomass and numbers that exceed 370/m2 during mass emergences, the extended time period of the underground nymphal stages (up to 17 years) complicates investigations of their life history traits and ecology. Upon emergence, female cicadas mate and then use their ovipositors to cut through wood to lay their eggs. Given the ability to penetrate into wood, we hypothesized that the ovipositor cuticle is augmented with inorganic elements, which could increase hardness and reduce ovipositor fracturing. We used scanning electron microscopy and energy dispersive x-ray spectroscopy to evaluate the material properties of ovipositors of four cicada species, including three species of periodical cicadas. We found 14 inorganic elements of the cuticle, of which P, Ca, Si, Mg, Na, Fe, Zn, Mn, Cl, K, and S show the highest concentrations (%wt) near the apex of the ovipositor, where other structural modifications for penetrating wood are present. To the best of our knowledge, this is the first report of metal deposits in the cuticle of true bugs (Hemiptera, >80,000 described species).

Drought-induced Suppression of Female Fecundity in a Capital Breeder

Human-induced global climate change is exerting increasingly strong selective pressures on a myriad of fitness traits that affect organisms. These traits, in turn, are influenced by a variety of environmental parameters such as temperature and precipitation, particularly in ectothermic taxa such as amphibians and reptiles. Over the past several decades, severe and prolonged episodes of drought are becoming commonplace throughout North America. Documentation of responses to this environmental crisis, however, is often incomplete, particularly in cryptic species. Here, we investigated reproduction in a population of pitviper snakes (copperhead, Agkistrodon contortrix), a live-bearing capital breeder. This population experienced a severe drought from 2012 through 2016. We tested whether declines in number of progeny were linked to this drought. Decline in total number offspring was significant, but offspring length and mass were unaffected. Reproductive output was positively impacted by precipitation and negatively impacted by high temperatures. We hypothesized that severe declines of prey species (e.g., cicada, amphibians, and small mammals) reduced energy acquisition during drought, negatively impacting reproductive output of the snakes. Support for this view was found using the periodical cicada (Magicicada spp.) as a proxy for prey availability. Various climate simulations, including our own qualitative analysis, predict that drought events will continue unabated throughout the geographic distribution of copperheads which suggests that long-term monitoring of populations are needed to better understand geographic variation in drought resilience and cascading impacts of drought phenomena on ecosystem function.

Genes acting in longevity-related pathways in the endoparasitoid, Pteromalus puparum.

Among insects, lifespans vary over a broad range, from the short-lived mayflies to the 17-year periodical cicadas. Generally, lifespans are determined by a phase in life, the reproductive lifespan, which varies among species. Numerous pathways, such as the insulin/insulin-like growth factor signaling pathway, the target of rapamycin pathway and the mitogen-activated protein kinase/extracellular signal-regulated kinases pathways, influence aging and lifespan. Components of these pathways were identified as lifespan-related genes, including genes mediating growth, metabolism, development, resistance, and other processes. Many age-related genes have been discovered in fruit flies, honeybees, and ants among other insect species. Studies of insect aging and longevity can help understand insect biology and develop new pest management technologies. In this paper, we interrogated the new Pteromalus puparum genome, from which we predicted 133 putative lifespan-related genes based on their homology with known lifespan-related genes of Drosophila melanogaster. These genes function in five signaling pathways and three physiological processes. The conserved domain structures of these genes were predicted and their expression patterns were analyzed. Amino acid sequence alignments and domain structure analysis indicate that most components remain conserved across at least six insect orders. The data in this paper will facilitate future work on parasitoid lifespans, which may have economic value in biocontrol programs.

Periodical cicada emergence resource pulse tracks forest expansion in a tallgrass prairie landscape

AbstractUnderstanding factors that influence resource pulses is an important aspect of ecosystem ecology. We quantified below‐ to aboveground energy and nutrient fluxes during the 2015 periodical cicada emergence from forest habitats in a tallgrass prairie matrix and compared results to our prior studies of the 1998 emergence in the same watershed. We estimated 35.2 million cicadas emerged across 159 ha in 2015, almost 2× more than the 19.6 million across 98 ha in 1998. The 2015 emergence resulted in below‐ to aboveground fluxes of 9.4 metric tons of ash‐free dry mass and 1.12 metric tons of N, both ~2× greater than 1998. This corresponds to 59 kg C/ha and 7 kg N/ha in and adjacent to forested areas in 2015. Increased emergence in 2015 was a result of spatial expansion of cicadas, not higher densities. Periodical cicadas are expanding with forest habitats in this region. Cicadas expand into and oviposit in ~40% of available forest habitat during each emergence. Accordingly, we predict the 2032 emergence will span ~245 ha. Our study demonstrates how human alterations to a landscape, in this case forest expansion linked to fire suppression and reduced grazing, can alter the magnitude and extent of a resource pulse.

Psychoactive plant- and mushroom-associated alkaloids from two behavior modifying cicada pathogens.

Entomopathogenic fungi routinely kill their hosts before releasing infectious spores, but a few species keep insects alive while sporulating, which enhances dispersal. Transcriptomics- and metabolomics-based studies of entomopathogens with post-mortem dissemination from their parasitized hosts have unraveled infection processes and host responses. However, the mechanisms underlying active spore transmission by Entomophthoralean fungi in living insects remain elusive. Here we report the discovery, through metabolomics, of the plant-associated amphetamine, cathinone, in four Massospora cicadina-infected periodical cicada populations, and the mushroom-associated tryptamine, psilocybin, in annual cicadas infected with Massospora platypediae or Massospora levispora, which likely represent a single fungal species. The absence of some fungal enzymes necessary for cathinone and psilocybin biosynthesis along with the inability to detect intermediate metabolites or gene orthologs are consistent with possibly novel biosynthesis pathways in Massospora. The neurogenic activities of these compounds suggest the extended phenotype of Massospora that modifies cicada behavior to maximize dissemination is chemically-induced.

The Enhanced Indispensability Argument, the circularity problem, and the interpretability strategy

Within the context of the Quine-Putnam indispensability argument, one discussion about the status of mathematics is concerned with the `Enhanced Indispensability Argument', which makes explicit in what way mathematics is supposed to be indispensable in science, namely explanatory. If there are genuine mathematical explanations of empirical phenomena, an argument for mathematical platonism could be extracted by using inference to the best explanation. The best explanation of the primeness of the life cycles of Periodical Cicadas is genuinely mathematical, according to Baker (2005, 2009). Furthermore, the result is then also used to strengthen the platonist position (e.g. Baker 2017a). We pick up the circularity problem brought up by Leng (2005) and Bangu (2008). We will argue that Baker's attempt to solve this problem fails, if Hume's Principle is analytic. We will also provide the opponent of the Enhanced Indispensability Argument with the so-called 'interpretability strategy', which can be used to come up with alternative explanations in case Hume's Principle is non-analytic. \end{abstract}

Evolutionary Hysteresis and Ratchets in the Evolution of Periodical Cicadas.

It has been previously hypothesized that the perfectly synchronized mass emergence of periodical cicadas (Magicicada spp.) evolved as a result of a switch from size-based to age-based emergence. In the former case, cicada nymphs emerge immediately (at the first opportunity) on reaching maturity, whereas in the latter case, nymphs wait in order to emerge at a specific age. Here we use an individual-based model to simulate the cicada life cycle and to study the evolution of periodicity. We find that if age-based emergence evolves in a constant abiotic environment, it typically results in a population that is protoperiodic, and synchronous emergence of the whole population is not achieved. However, perfect periodicity and synchronous emergence can be attained, if the abiotic environment changes back and forth between favorable and unfavorable conditions (hysteresis). Furthermore, once age-based emergence evolves, generally it can only be invaded by other age-based emergence strategies with longer cycle lengths (evolutionary ratchet). Together, these mechanisms promote the evolution of long periodic life cycles and synchronous emergence in the Magicicada. We discuss how our results connect to previous theories and recent phylogenetic studies on Magicicada evolution.

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 2yr 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.

YAN KANG, The Linsly School, Wheeling, WV, 26003. Ovipositing Seventeen-Year Cicadas (Magicicada septendecim) prefer certain tree species, branch diameters and branch surface positions in a planted campus savanna habitat.

Previous research shows seventeen-year periodical cicadas feed on tree roots as nymphs and adult females oviposit on branches resulting in scars. Most studies evaluating periodical cicada oviposition preferences were conducted in mature forests sites. In this study oviposition preferences were evaluated on a planted savanna habitat at the Linsly campus. While nymphs feed underground on roots of a variety of tree species, where do females oviposit on above-ground branches? Initial observations suggested oviposition scar distribution was not random. This study’s objective was to evaluate periodical cicada oviposition preferences regarding tree species, branch diameter and branch aspect in a savanna landscape that included non-native trees. During the fall of 2018 eight trees representing eight species were chosen and for each tree five branches within 3m of the ground were studied as replicates. Within 100 cm standard sampling lengths of the branch, total oviposition scarring length, average ovipositon scar length, diameter of branch at the scar, and scar aspect were measured. Ovipositing cicadas showed some species preferences, but used angiosperm species such as the Japanese Scholar Tree, Black Oak, Silver Maple and Red Mulberry heavily regardless of their native or non-native status. White Pine was not used at all. Periodical cicadas favored branches 0.7 to 0.35 cm in diameter. Most tree branches had oviposition scars on bottom surfaces, but some heavily utilized trees had scars on the top and the side, suggesting competition for preferred lower spaces during egg-laying. These patterns suggest females may be selecting oviposition sites to maximize egg survival.

A Hybrid Model for the Population Dynamics of Periodical Cicadas.

In addition to their unusually long life cycle, periodical cicadas, Magicicada spp., provide an exceptional example of spatially synchronized life stage phenology in nature. Within regions ("broods") spanning 50,000-500,000 km[Formula: see text], adults emerge synchronously every 13 or 17 years. While satiation of avian predators is believed to be a key component of the ability of these populations to reach high densities, it is not clear why populations at a single location remain entirely synchronized. We develop nonlinear Leslie matrix-type models of periodical cicadas that include predation-driven Allee effects and competition in addition to reproduction and survival. Using both analytical and numerical techniques, we demonstrate the observed presence of a single brood critically depends on the relationship between fecundity, competition and predation. We analyze the single-brood, two-brood and all-brood equilibria in the large life span limit using a tractable hybrid approximation to the Leslie matrix model with continuous time competition in between discrete reproduction events. Within the hybrid model, we prove that the single-brood equilibrium is the only stable equilibrium. This hybrid model allows us to quantitatively predict population sizes and the range of parameters for which the stable single-brood and unstable two-brood and all-brood equilibria exist. The hybrid model yields a good approximation to the numerical results for the Leslie matrix model for the biologically relevant case of a 17-year life span.

Special Issue on “Biological Networks”

Networks of coordinated interactions among biological entities govern a myriad of biological functions that span a wide range of both length and time scales—from ecosystems to individual cells, and from years (e.g., the life cycle of periodical cicadas) to milliseconds (e.g., allosteric enzymeregulation[...]

Competition and Stragglers as Mediators of Developmental Synchrony in Periodical Cicadas.

Periodical cicadas are enigmatic organisms: broods spanning large spatial ranges consist of developmentally synchronized populations of 3-4 sympatric species that emerge as adults every 13 or 17 years. Only one brood typically occupies any single location, with well-defined boundaries separating distinct broods. The cause of such synchronous development remains uncertain, but it is known that synchronous emergence of large numbers of adults in a single year satiates predators, allowing a substantial fraction of emerging adults to survive long enough to reproduce. Competition among nymphs feeding on tree roots almost certainly plays a role in limiting populations. However, due to the difficulty of working with such long-lived subterranean life stages, the mechanisms governing competition in periodical cicadas have not been identified. A second process that may affect synchrony among periodical cicadas is their ability to delay or accelerate their emergence as adults by 1 year and accelerate it by 4 years (stragglers). We develop a nonlinear Leslie matrix-type model that describes cicada dynamics accounting for predation, competition, and stragglers. Using numerical simulations, we identify conditions that generate dynamics in which a single brood occupies a given geographical location. Our results show that while stragglers have the potential for introducing multiple sympatric broods, the interaction of interbrood competition with predation-driven Allee effects creates a system resistant to such invasions, and populations maintain developmental synchrony.

The periodical cicada four-year acceleration hypothesis revisited and the polyphyletic nature of Brood V, including an updated crowd-source enhanced map (Hemiptera: Cicadidae: Magicicada).

The periodical cicadas of North America (Magicicada spp.) are well-known for their long life cycles of 13 and 17 years and their mass synchronized emergences. Although periodical cicada life cycles are relatively strict, the biogeographic patterns of periodical cicada broods, or year-classes, indicate that they must undergo some degree of life cycle switching. We present a new map of periodical cicada Brood V, which emerged in 2016, and demonstrate that it consists of at least four distinct parts that span an area in the United States stretching from Ohio to Long Island. We discuss mtDNA haplotype variation in this brood in relation to other periodical cicada broods, noting that different parts of this brood appear to have different origins. We use this information to refine a hypothesis for the formation of periodical cicada broods by 1- and 4-year life cycle jumps.

Triplicate parallel life cycle divergence despite gene flow in periodical cicadas

Periodical cicadas comprise three species groups containing three pairs of 13- and 17-year life cycle species showing parallel divergence, along with a more anciently diverged 13-year species (Magicicda tredecim). The mechanism and genetic basis of this parallel divergence is unknown. Here we use orthologous transcriptome sequences to explore the demographic processes and genomic evolution associated with parallel life cycle divergence. The three 13- and 17-year species pairs have similar demographic histories, and the two life cycles diverged 200,000–100,000 years ago. Interestingly, these life cycle differences have been maintained despite substantial gene flow between 13- and 17-year species within species groups, which is possible during co-emergences. Sequence divergence between 13- and 17-year species in each species group (excluding M. tredecim) is minimal, and we find no shared divergent single-nucleotide polymorphisms (SNPs) or loci associated with all instances of life cycle divergence. The two life cycles may be controlled by highly limited genomic differences.

Urbanization disrupts latitude-size rule in 17-year cicadas.

Many ectotherms show a decrease in body size with increasing latitude due to changes in climate, a pattern termed converse Bergmann's rule. Urban conditions—particularly warmer temperatures and fragmented landscapes—may impose stresses on development that could disrupt these body size patterns. To test the impact of urbanization on development and latitudinal trends in body size, we launched a citizen science project to collect periodical cicadas (Magicicada septendecim) from across their latitudinal range during the 2013 emergence of Brood II. Periodical cicadas are long‐lived insects whose distribution spans a broad latitudinal range covering both urban and rural habitats. We used a geometric morphometric approach to assess body size and developmental stress based on fluctuating asymmetry in wing shape. Body size of rural cicadas followed converse Bergmann's rule, but this pattern was disrupted in urban habitats. In the north, urban cicadas were larger than their rural counterparts, while southern populations showed little variation in body size between habitats. We detected no evidence of differences in developmental stress due to urbanization. To our knowledge, this is the first evidence that urbanization disrupts biogeographical trends in body size, and this pattern highlights how the effects of urbanization may differ over a species’ range.

A specialized fungal parasite (Massospora cicadina) hijacks the sexual signals of periodical cicadas (Hemiptera: Cicadidae: Magicicada)

Male periodical cicadas (Magicicada spp.) infected with conidiospore-producing (“Stage I”) infections of the entomopathogenic fungus Massospora cicadina exhibit precisely timed wing-flick signaling behavior normally seen only in sexually receptive female cicadas. Male wing-flicks attract copulation attempts from conspecific males in the chorus; close contact apparently spreads the infective conidiospores. In contrast, males with “Stage II” infections that produce resting spores that wait for the next cicada generation do not produce female-specific signals. We propose that these complex fungus-induced behavioral changes, which resemble apparently independently derived changes in other cicada-Massospora systems, represent a fungus “extended phenotype” that hijacks cicadas, turning them into vehicles for fungus transmission at the expense of the cicadas’ own interests.