Chronic speciation in periodical cicadas

Allochronic speciation and reproductive character displacement are two intuitively attractive models of speciation. The first proposes that changes in the timing of life cycles produce new species, whereas the second suggests that speciation is due to the exaggeration of sexual isolation in sympatric populations. Clear examples of either process in nature remain elusive, despite some extensive searches. Two recent studies of mtDNA markers and behaviour of periodical cicadas in North America have identified a new species of cicada that seems to provide good evidence for the involvement of both processes in its origin.     

Differential susceptibility of tree species to oviposition by periodical cicadas

Abstract 1. Periodical cicadas occur widely in deciduous forests of eastern North America and represent the largest insect emergences in the world. Their effects on forest community dynamics, via oviposition damage and root feeding, are potentially great but not well understood. If tree species vary in their susceptibility to cicada oviposition and root colonization, then periodical cicadas may affect ecological interactions among tree species and forest composition. 2. We measured oviposition damage on 63 tree species at 52 sites in southern Indiana, U.S.A. for two broods of periodical cicadas. We compared oviposition damage among different sites, habitats, and tree species. We also measured cicada emergence rates in mature and successional forest habitats and from beneath different tree species. 3. Certain tree species received significantly more oviposition damage than others, and the most and least damaged species were consistent between the two broods. For some species, oviposition damage varied between mature and successional sites. Despite the differences in oviposition rates among species, there was no difference in emergence rates from beneath different tree species, suggesting that initial differences in cicada density among tree species are not maintained through the nymphal life cycle. 4. Cicadas oviposited more at successional sites, but emerged more in mature forest stands, suggesting that successive generations of cicadas represent a shifting mosaic between forests of different ages. As tree species consistently vary in their susceptibility to oviposition damage, periodical cicadas could alter local competitive interactions and therefore affect forest dynamics.     

Acoustic adaptations of periodical cicadas (Hemiptera: Magicicada)

We studied the trade-off between traits that function in mate attraction and those that function in enemy avoidance by contrasting features of acoustic communication in cicadas differentially at risk to predators in the same environment. Two genera of North American cicadas were studied: Magicicada and Tibicen. Magicicada species of periodical cicadas, with 17-year life cycles, seek mates in dense aggregations of calling males that are made possible by the relative ineffectiveness of predators to control their numbers. During the breeding season, Magicicada are so abundant that they satiate their predators. From their relative freedom from predation, it is to be expected that traits for attracting mates are emphasized in Magicicada compared with the more solitary genus Tibicen , which reproduce at much lower densities. Males of solitary species are expected to sing more loudly and at low pitch because both features enhance long-distance transmission. These two features were confirmed by measurement. Magicicada septendecim appears to be the most divergent species, evolutionarily, in terms of an unusually sharply tuned sound resonating system, low resonant frequency, and quietness of its song that cannot be entirely explained by body size. These characteristics represent adaptations to the problem of communicating unambiguously to females at close range in a loud and heterogeneous sound environment. Sensitivity to predators, parasitoids, and congeneric species may also have shaped the evolution of their communication systems.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 15–24.     

Effects of local density on fecundity and mating speed for periodical cicadas

Summary This paper catalogues several different dichotomies that have all been termed r- and K-selection. The status of the concept of r- and K-selection is discussed and a more restricted usage of the terms is recommended.     

Evolution of prolonged development: a life table analysis for periodical cicadas

According to conventional wisdom, natural selection should favor early reproduction. Prolonged development of 13 and 17 yr has been difficult to explain for periodical cicadas. Earlier, I hypothesized that development may be long for periodical cicadas because fecundity increases as a function of longer development with little increased risk of mortality. In this article, I tested whether the fecundity was greater for 17-yr cicadas than for 13-yr cicadas and estimated the shape of the survivorship curve. A cohort of 17-yr cicadas was followed from 1979 through 1996. Most mortality occurred during the first 2 yr; thereafter mortality was uncommon. Across 17 yr, adult densities increased at five out of seven sites, and in no case did the change exceed three times. Seventeen-year adults had heavier ovaries than did 13-yr adults; this effect was greater for Magicicada cassini (1.80 times) than for Magicicada decim (1.16 times). For M. cassini, the extra fecundity associated with 17-yr development swamped the potential advantages of more frequent reproduction of 13-yr forms under most conditions. For M. decim, realistically low rates of mortality roughly matched the small effect of development on fecundity. Prolonged development in periodical cicadas may be explained adequately by the demographic hypothesis, although it may also reduce predation risk to adults or result from strong selection for large body size.     

Spatial variability in oviposition damage by periodical cicadas in a fragmented landscape

Effects of the periodical cicada (Magicicada spp.) on forest dynamics are poorly documented. A 1998 emergence of M. cassini in eastern Kansas led to colonization of a fragmented experimental landscape undergoing secondary succession. We hypothesized that per-tree rates of oviposition damage by cicadas would reflect: (1) distance from the source of the emergence, (2) patch size, and (3) local tree density. Ovipositing females displayed clear preferences for host species and damage incidence showed predictable spatial patterns. Two species (smooth sumac, Rhus glabra, and eastern red cedar, Juniperus virginiana) were rarely attacked, whereas others (rough-leaved dogwood, Cornus drummondii; slippery elm, Ulmus rubra; box elder, Acer negundo, and honey locust, Gleditsia triacanthos) were strongly attacked. The dominant early successional tree, dogwood, received on average the most attacks. As predicted, attacks per stem declined strongly with distance from the emergence source, and with local stem density (a "dilution" effect). Contrary to expectations, there were more attacks per stem on larger patches. Because ovipositing cicadas cut damaging slits in host tree branches, potentially affecting tree growth rate, competitive ability, and capacity to reproduce, cicada damage could potentially influence spatial variation in secondary succession.     

Life cycle replacement by gene introduction under an allee effect in periodical cicadas

Periodical cicadas (Magicicada spp.) in the USA are divided into three species groups (-decim, -cassini, -decula) of similar but distinct morphology and behavior. Each group contains at least one species with a 17-year life cycle and one with a 13-year cycle; each species is most closely related to one with the other cycle. One explanation for the apparent polyphyly of 13- and 17-year life cycles is that populations switch between the two cycles. Using a numerical model, we test the general feasibility of life cycle switching by the introduction of alleles for one cycle into populations of the other cycle. Our results suggest that fitness reductions at low population densities of mating individuals (the Allee effect) could play a role in life cycle switching. In our model, if the 13-year cycle is genetically dominant, a 17-year cycle population will switch to a 13-year cycle given the introduction of a few 13-year cycle alleles under a moderate Allee effect. We also show that under a weak Allee effect, different year-classes ("broods") with 17-year life cycles can be generated. Remarkably, the outcomes of our models depend only on the dominance relationships of the cycle alleles, irrespective of any fitness advantages.     

Evidence for paternal leakage in hybrid periodical cicadas (Hemiptera: Magicicada spp.)

Mitochondrial inheritance is generally assumed to be maternal. However, there is increasing evidence of exceptions to this rule, especially in hybrid crosses. In these cases, mitochondria are also inherited paternally, so "paternal leakage" of mitochondria occurs. It is important to understand these exceptions better, since they potentially complicate or invalidate studies that make use of mitochondrial markers. We surveyed F1 offspring of experimental hybrid crosses of the 17-year periodical cicadas Magicicada septendecim, M. septendecula, and M. cassini for the presence of paternal mitochondrial markers at various times during development (1-day eggs; 3-, 6-, 9-week eggs; 16-month old 1st and 2nd instar nymphs). We found evidence of paternal leakage in both reciprocal hybrid crosses in all of these samples. The relative difficulty of detecting paternal mtDNA in the youngest eggs and ease of detecting leakage in older eggs and in nymphs suggests that paternal mitochondria proliferate as the eggs develop. Our data support recent theoretical predictions that paternal leakage may be more common than previously estimated.     

Courtship in two species of periodical cicadas, Magicicada septendecim and Magicicada cassini

Courtship behaviour of two species of periodical cicadas, Magicicada septendecim and M. cassini, was studied in the field during the 1970, 1973, and 1974 emergences of these insects. In areas where both species were courting there were differences in both male and female courtship patterns, both in acoustic and behavioural components. Experiments with models showed that male M. septendecim were more likely to court crude models of females than were M. cassini males. When females were ‘courted’ with models that could imitate some of male courtship, they were more receptive when the models' ‘songs’ were those of conspecific males. Acoustic differences between species are probably used by females in mate selection, maintaining species separation even in areas where the two species overlap in both space and time.     

Resource pulses of dead periodical cicadas increase the growth of American bellflower rosettes under competitive and non-competitive conditions

This experiment investigates how pulsed nutrient resources interact with intraspecific competition to influence biomass production and nutrient use efficiency in the American bellflower (Campanulastrum americanum). The competitive environment of these plants was manipulated by growing plants alone or with neighboring conspecifics, and the occurrence of pulsed nutrient resources was manipulated through the addition of 17-year periodical cicada (Magicicada septendecim) carcasses in order to simulate naturally occurring pulsed resources in this system. The addition of cicada carcasses increased mean plant biomass by 61 % compared to non-supplemented plants, while competition decreased mean plant biomass by 44 % compared to plants grown without competition; these effects were additive. In comparison, nutrient use efficiency decreased in fertilized plants (cicada-supplemented plants showed 20 % greater foliage nitrogen concentrations compared to non-supplemented plants), but was not significantly affected by the plant’s competitive environment. In addition, cicada supplementation did not significantly increase the biomass asymmetry in competing pairs of plants. These results suggest that these plants increased their total nutrient uptake at a timescale commensurate with the pulsed increase in nutrient availability due to cicada carcass decomposition.     

Sexual dimorphism of motorneurons: Timbal muscle innervation in male periodical cicadas and homologous structures in females

Summary Treatment of cultured goldfish xanthophores by hormone (ACTH) or c-AMP induces not only pigment dispersion, but subsequent outgrowth of processes, and pigment translocation into these processes. These latter effects are shown to proceed as follows: First the edge of the cytoplasmic lamellae takes on a scalloped contour with numerous protrusions. These presumably serve as nucleation centers where short microfilament bundles are assembled, Later, the microfilament bundles elongate (grow), often resulting in an extension of the protrusions to become filopodia while the proximal end of the microfilaments penetrates into the thicker portion of the cellular process which now houses the pigment, i.e., the carotenoid droplets. Carotenoid droplets appear to migrate along the microfilament bundles, or cytoplasmic channels associated with them, into the filopodia. Finally, some of the filopodia become broader, thicker and laden with carotenoid droplets and are then recognized by light microscopy as pigmented cellular processes. The microfilaments have been shown to be actin filaments by their thickness, the size of their subunits, and decoration by heavy meromyosin. Evidence is presented which suggests that the growth of these actin filaments may come about by recruitment from short F-actin strands found in random orientation in adjacent areas.     

Geographic body size variation in the periodical cicadas Magicicada: implications for life cycle divergence and local adaptation

Seven species in three species groups (Decim, Cassini and Decula) of periodical cicadas (Magicicada) occupy a wide latitudinal range in the eastern United States. To clarify how adult body size, a key trait affecting fitness, varies geographically with climate conditions and life cycle, we analysed the relationships of population mean head width to geographic variables (latitude, longitude, altitude), habitat annual mean temperature (AMT), life cycle and species differences. Within species, body size was larger in females than males and decreased with increasing latitude (and decreasing habitat AMT), following the converse Bergmann's rule. For the pair of recently diverged 13‐ and 17‐year species in each group, 13‐year cicadas were equal in size or slightly smaller on average than their 17‐year counterparts despite their shorter developmental time. This fact suggests that, under the same climatic conditions, 17‐year cicadas have lowered growth rates compared to their 13‐years counterparts, allowing 13‐year cicadas with faster growth rates to achieve body sizes equivalent to those of their 17‐year counterparts at the same locations. However, in the Decim group, which includes two 13‐year species, the more southerly, anciently diverged 13‐year species (Magicicada tredecim) was characterized by a larger body size than the other, more northerly 13‐ and 17‐year species, suggesting that local adaptation in warmer habitats may ultimately lead to evolution of larger body sizes. Our results demonstrate how geographic clines in body size may be maintained in sister species possessing different life cycles.     

Red-winged blackbird predation on periodical cicadas (Cicadidae: Magicicada spp.): bird behavior and cicada responses

Summary Predation by red-winged blackbirds Agelaius phoeniceus L. on 13-year periodical cicadas (Magicicada spp.) and reactions by periodical cicadas to predators were studied during emergence of Brood XIX during summer of 1985 in northwestern Arkansas (USA). Emergences of periodical cicadas are classic examples of predator satiation due to high local densities of cicadas and birds are the major predators of adult periodical cicadas. Reactions of periodical cicadas to predators were assessed by recording behaviors exhibited by cicadas when approached in trees by a human hand during the 3-week period of peak adult densitics. Most male cicadas made a noise in association with escape behaviors when approached, and 50% of the females, which are silent, attempted escape behaviors. Observations of predation attempts on cicadas by red-winged blackbirds were made during the period of peak predation pressure. Red-winged blackbirds spent less time searching for cicadas over that 2-week period of increasing predation pressure, and became increasingly efficient at capturing cicadas. Handling time of cicadas by red-winged blackbirds increased by about 20 seconds over that period, as blackbirds spent more time consuming female cicadas. The flysquawk response, used only by male cicadas, was effective in deterring red-winged blackbirds; only 5% of the attacks by blackbirds were successful when that behavior was exhibited. All cicadas that remained motionless and silent when approached by blackbirds were captured and consumed. Because females remained inactive when approached more often than did males, blackbirds may have consumed more female cicadas. Changes that appeared in reactions of preiodical cicadas to the model predator and to the attacks of blackbirds reflect both changes in the sex ratio of the cicada populations and changes in behaviors of cicadas associated with mating and egg laying. The loud noise made by male periodical cicadas at mating centers did not appear to deter predation by blackbirds. Changes in the behavior of blackbirds that appeared to be in association with greater predation on female periodical cicadas relates directly to aspects of foraging theory, particularly predictions concerning more selective foraging during periods of abundant food resources.     

Reproductive character displacement and speciation in periodical cicadas, with description of new species, 13-year Magicicada neotredecem

Abstract. Acoustic mate-attracting signals of related sympatric, synchronic species are always distinguishable, but those of related allopatric species sometimes are not, thus suggesting that such signals may evolve to "reinforce" premating species isolation when similar species become sympatric. This hypothesis predicts divergences restricted to regions of sympatry in partially overlapping species, but such "reproductive character displacement" has rarely been confirmed. We report such a case in the acoustic signals of a previously unrecognized 13-year periodical cicada species, Magicicada neotredecim , described here as a new species (see Appendix). Where M. neotredecim overlaps M. tredecim in the central United States, the dominant male call pitch (frequency) of M. neotredecim increases from approximately 1.4 kHz to 1.7 kHz, whereas that of M. tredecim remains comparatively stable. The average preferences of female M. neotredecim for call pitch show a similar geographic pattern, changing with the call pitch of conspecific males. Magicicada neotredecim differs from 13-year M. tredecim in abdomen coloration, mitochondrial DNA, and call pitch, but is not consistently distinguishable from 17-year M. septendecim ; thus, like other Magicicada species, M. neotredecim appears most closely related to a geographically adjacent counterpart with the alternative life cycle. Speciation in Magicicada may be facilitated by life-cycle changes that create temporal isolation, and reinforcement could play a role by fostering divergence in premating signals prior to speciation. We present two theories of Magicicada speciation by life-cycle evolution: "nurse-brood facilitation" and "life-cycle canalization."     

Periodical cicadas

The evolution of periodicity and synchronicity of magical cicadas is studied by means of mathematical models. Received: 28 January 1999 / Revised version: 4 November 1999 / Published online: 3 April 2000     

Comparison of exclusion and imidacloprid for reduction of oviposition damage to young trees by periodical cicadas (Hemiptera: Cicadidae)

Insecticides are traditionally used to control periodical cicadas (Homoptera: Cicadidae) and to reduce associated injury caused by oviposition. However, research has shown that conventional insecticides have low or variable season-long efficacy in reducing injury caused by cicadas. New systemic neonicotinoid insecticides provide excellent levels of control against a variety of sucking insects. We compared the efficacy of a neonicotinoid insecticide, imidacloprid, and a nonchemical control measure, netting, to reduce cicada injury. Netted trees sustained very little injury, whereas unprotected trees were heavily damaged. Fewer eggnests, scars, and flags were observed on trees treated with imidacloprid compared with unprotected trees; however, the hatching of cicada eggs was unaffected by imidacloprid.     

Eicosanoids mediate nodulation reactions to bacterial infections in adults of two 17-year periodical cicadas,Magicicada septendecim and M. cassini

Nodulation is the first and quantitatively most important cellular defense reaction to bacterial infections in insects. Treating adults of the 17-year periodical cicadas, Magicicada septendecim and M. cassini, with eicosanoid biosynthesis inhibitors immediately prior to intrahemocoelic injections of the bacterium, Serratia marcescens, sharply reduced the nodulation response to bacterial challenges. Separate treatments with specific inhibitors of phospholipase A(2), cyclooxygenase, and lipoxygenase reduced nodulation, supporting our view that nodule formation is a multi-step process in which individual steps are separately mediated by lipoxygenase and cyclooxygenase products. The inhibitory influence of dexamethasone was apparent by 2 h after injection, and nodulation was significantly reduced, relative to control insects, over the following 14 h. The dexamethasone effects were reversed by treating bacteria-challenged insects with the eicosanoid-precursor polyunsaturated fatty acid, arachidonic acid. Low levels of arachidonic acid were detected in fat body phospholipids. These findings in adults of an exopterygote insect species with an unusual life history pattern broaden our hypothesis that eicosanoids mediate cellular immune reactions to bacterial infections in most, if not all, insects.     

Flight energetics and dispersal capability of the fire ant, Solenopsis invicta Buren

Experiments were conducted to estimate the flight capabilities of fire ant (Solenopsis invicta Buren) alates. These experiments were designed to: (1) quantify energetic expenditure during fixed flight; (2) characterize metabolic substrates of male and female alates; (3) estimate flight speed of male and female alates; and (4) quantify wingbeat frequency and water loss of females during flight. Flying males (in closed-system respirometry) increased metabolic rate approximately 38.4-fold over resting rate. Females increased metabolic rate approximately 51-fold (closed-system respirometry) and 48-fold (flow-through respirometry) over resting rate. Female alates had a mean respiratory quotient (RQ) of 0.999, indicating reliance on carbohydrates. The mean RQ of males was significantly lower (0.867). The flight speed of females on a circular flight mill averaged approximately 0.7 m s(-1), and increased with temperature but decreased with increasing body mass. The flight speed of males was 43% greater (approximately 1.0 m s(-1)) and increased linearly with temperature and increasing body mass. Female alates lost an average of 1.8 mg water h(-1) during flight. A simple energetics model, combined with previous work on the nutrient content of S. invicta and patterns of CO(2) release observed in this study, indicate that the flight capability of S. invicta female alates is limited to <5 km in the absence of wind.