Comparative thermal adaptation in cicadas (Hemiptera: Cicadidae) inhabiting Mediterranean ecosystems

The thermal responses of cicadas inhabiting the Mediterranean ecosystems in Europe, North America, South Africa, and Australia are investigated. A total of 37 species and two subspecies from 17 genera representing eight tribes and three subfamilies of cicadas are investigated. The analysis includes species that are restricted to the Mediterranean ecosystem as well as those which also inhabit additional environments. The data suggest that cicadas adapt to the climate type regardless of particular types of plants within the various Mediterranean communities. Similarly, cicada thermal responses are independent of body size or taxonomic affinities. There is a wider range of body temperatures for the maximum voluntary tolerance temperature than for heat torpor or minimum flight temperatures. This diversity seems to be determined by the subdivision of the habitat used and the behavior of the species. All species possess relatively elevated heat torpor temperatures adapting to the general thermal characteristics of the Mediterranean ecosystem. The data suggest that cicadas adapt to the Mediterranean climate type regardless of the diversity of particular types of plants within the various communities, of body size or of taxonomic position.     

Influence of altitude, habitat and microhabitat on thermal adaptation of cicadas from Southwest Texas (Hemiptera: Cicadidae)

The thermal responses of 12 cicada species inhabiting Big Bend National Park, Texas, USA are investigated to determine the influence of altitude, habitat and microhabitat. The park provides an opportunity to analyze the thermal responses in animals from a variety of habitats and altitudinal gradients within a limited geographic range. The data suggest that thermal responses of cicadas are adaptations to their specific habitats. No thermal responses are significantly correlated with body size. The maximum voluntary tolerance temperature (an upper behavioral thermoregulatory point) and heat torpor temperatures show significant correlations with altitude. Variability in thermal responses can also be related to the characteristics of the microhabitat selected or the behavioral pattern of a species.     

Feeding ecology and emergence production of annual cicadas (Homoptera: Cicadidae) in tallgrass prairie

The emergence phenology and feeding ecology of annual cicadas in tallgrass prairie are poorly documented. However, these large insects are abundant, and their annual emergence represents a potentially important flux of energy and nutrients from belowground to aboveground. We conducted a study at Konza Prairie Research Natural Area in eastern Kansas to characterize and quantify cicada emergence and associated energy and nutrient fluxes. We established emergence trap transects in three habitat types (upland prairie, lowland prairie, and riparian forest), and collected cicadas every 3 days from May to September. A subset of trapped cicadas was used for species- and sex-specific mass, nutrient, and stable isotope analyses. Five species were trapped during the study, of which three were dominant. Cicadetta calliope and Tibicen aurifera exhibited significantly higher emergence production in upland prairie than in lowland prairie, and were not captured in forested sites at all. T. dorsata emerged from all three habitat types, and though not significant, showed a trend of greater abundance in lowland grasslands. Two less abundant species, T. pruinosa and T. lyricen, emerged exclusively from forested habitats. Nitrogen fluxes associated with total cicada emergence were estimated to be ∼4 kg N ha^–1 year^–1 in both grassland habitats, and 1.01 kg N ha^–1 year^–1 in forested sites. Results of stable isotope analyses showed clear patterns of resource partitioning among dominant cicada species emerging from grassland sites. T. aurifera and C. calliope had δ¹³C and δ¹⁵N signatures indicative of feeding on shallowly rooted C₄ plants such as the warm-season grasses dominant in tallgrass prairie ecosystems, whereas T. dorsata signatures suggested preferential feeding on more deeply rooted C₃ plants. Received: 20 September 1999 / Accepted: 9 December 1999     

Energetics of emergence in the cicadas, Cyclochila australasiae and Abricta curvicosta (Homoptera: Cicadidae)

The final moult in cicadas marks a major transition in lifestyle and is a behaviour that makes the cicada vulnerable to predation. Consequently, emergence times are short and, we predict, therefore the rate of energy consumption would be high. Hence, we measured the energetic cost of emergence in Cyclochila australasiae (green grocer) and Abricta curvicosta (floury baker) cicadas during the final moult from nymph to adult cicada. Maximum energy expended whilst emerging was compared between the sexes and species. Even though C. australasiae take longer to emerge than A. curvicosta, the mass-specific cost of emergence is not different between the two species (C. australasiae: 11.34+/-2.55 J g(-1); A. curvicosta: 12.91+/-1.90 J g(-1)). The mass-specific metabolic rates of fully emerged adults of both species are approximately twice those of the nymphs and the maximum metabolic rate during emergence is about 1.5 times higher than the resting metabolic rate of emerged adults. Emergence times, as indicated by rates of oxygen consumption, are longer than expected and probably reflect limitations in the oxygen capacity of the cicadas during moulting.     

Comparative thermoregulation of sympatric endothermic and ectothermic cicadas (Homoptera: Cicadidae: Tibicen winnemanna and Tibicen chloromerus)

Measurements of body temperature in the field demonstrated that endothermic cicadas regulate body temperature by behavioral mechanisms as well as by endogenous heat production. Regression analysis suggests both endothermic and ectothermic species are thermoregulating. Body temperature of endothermically active cicadas without access to exogenous heat is approximately the same as the body temperature of basking cicadas. Tibicen winnemanna (Davis) raises body temperature in the field with the heat produced in flight or through the activation of the flight musculature without the act of flight. T. chloromerus (Walker) uses solar radiation to elevate body temperature to the level necessary for activity. The thermal responses of each species are related to its activity patterns with minimum flight temperature and shade-seeking temperatures significantly lower in the endothermic T. winnemanna. Heat torpor temperature appears to be related to the environment rather than behavior pattern. Endothermy in cicadas may serve to uncouple reproductive behavior from environmental constraints; to circumvent possible thermoregulatory problems; to permit the utilization of habitats unavailable to strictly ectothermic cicadas; to reduce predation; to optimize broadcast coverage and sound transmission; and to decrease possible acoustic interference. Accepted: 25 March 2000     

Evaporative cooling and endothermy in the 13-year periodical cicada,Magicicada tredecem (Homoptera: Cicadidae)

Summary The thermobiology of a cicada, Magicicada tredecem, from a warm, high humidity environment was investigated. Thoracic temperature (T_th) of M. tredecem in the field was strongly dependent on, and consistently higher than, ambient temperature (T_am), averaging 33.0±0.19°C on warm sunny days (T_am=28–29°C, rh=60–75%). Laboratory studies documented cuticle water fluxes high enough ( 5mg · cm^–2 · h^–1 in dry air at 40°C) to result in a significant degree of passive evaporative cooling, but the ability of M. tredecem to actively facilitate evaporative water loss during thermal stress is comparatively limited: water loss rates (WLR) of live M. tredecem at 40°C (dry air) were only 35–45% greater than those of dead cicadas. The limited ability of M. tredecem to facilitate transcuticular WLR is associated with limited surface distribution of the cuticular ducts through which water is actively extruded during evaporative cooling. In the laboratory, active extrusion of water had no appreciable effect on T_th, demonstrating that evaporative cooling was due largely to passive water flux through the highly permeable cuticle. The location of the abdominal pore tracts is such that extrusion of water through the ducts may preferentially cool the heart and perhaps other abdominal tissues. Long-term climatological data indicate that M. tredecem rarely encounters T_am levels high enough (i.e., above its apparent T_th setpoint of 34–35°C) to require evaporative cooling. Inactive M. tredecem can endothermically increase T_th. An hypothesis is proposed to account for the diversity of body temperature setpoints in cicadas.Abbreviations rh relative humidity - SOT standard operating temperature - T _am ambient temperature - T _b body temperature - T _sp body temperature setpoint - T _th thoracic temperature - TWF transcuticular water flux - WLR water loss rate     

Spermiogenesis in three species of cicadas (Hemiptera: Cicadidae)

Spermiogenesis in three species of cicadas representing one cicadettine (Monomatapa matoposa Boulard) and two cicadines (Diceroprocta biconica [Walker] and Kongota punctigera [Walker]) was investigated by light and electron microscopy. Although spermiogenesis was occurring in the testis of adult males of all species, earlier spermiogenic stages were observed in D. biconica only. While spermiogenesis was similar to that described for other insects, some differences were noted. For example granular material did not assemble around the centriole to form a centriolar adjunct but did accumulate in the cytoplasm of early spermatids adjacent to a region of the nuclear membrane where nuclear pores were aggregated. In late spermatids this material accumulated anterior to the mitochondrial derivatives in a developing postero‐lateral nuclear groove. While this material has been named the ‘centriolar adjunct’ by previous authors, its formation away from the centriole raises questions about its true identity. Second, during acrosome maturation an ante‐acrosomal region of cytoplasm develops. Although present in later spermatids, this region is lost in spermatozoa. Interspecific variations in chromatin condensation patterns and the number of microtubule layers encircling the spermatid nucleus during spermiogenesis were noted.     

Evolution and phylogeny of the New Zealand cicada genus Kikihia Dugdale (Homoptera: Auchenorrhyncha: Cicadidae) with special reference to the origin of the Kermadec and Norfolk Islands' species

Aim Determine the phylogeny and dispersal patterns of the cicada genus Kikihia in New Zealand and the origin of the Norfolk, Kermadec, and Chatham Island cicadas. Location New Zealand, Norfolk Island, Kermadec Islands and Chatham Island. Methods DNA sequences from 16 species and four soon to be described species of cicadas from New Zealand and Norfolk Island (Australia) were examined. A total of 1401 base pairs were analysed from whole genome extraction of three mitochondrial genes (cytochrome oxidase subunit II, ATPase6 and ATPase8). These DNA sequences were aligned and analysed using standard likelihood approaches to phylogenetic analysis. Dates of divergences between clades were determined using a molecular clock based on Bayesian statistics. Results Most species in the genus Kikihia diverged between 3 and 5 million years ago (Ma) coincident with a period of rapid mountain building in New Zealand. Cicada species on the Kermadec and Norfolk Islands invaded recently from New Zealand and are closely related to the New Zealand North Island species Kikihia cutora. Main conclusions Speciation in the genus Kikihia was likely due in large part to the appearance of new habitats associated with the rise of the Southern Alps, starting c. 5 Ma. Dispersal of Kikihia species within mainland New Zealand probably occurred gradually rather than through long‐distance jumps. However, invasion of Norfolk, the Kermadecs and Chatham Islands had to have occurred through long‐distance dispersal.     

Thermal adaptation in North American cicadas (Hemiptera: Cicadidae)

We determine and summarize the thermal responses for 118 species and subspecies of North American cicadas representing more than 50 years of fieldwork and experimentation. We investigate the role that habitat and behavior have on the thermal adaptation of the North American cicadas. There are general patterns of increasing thermal responses in warmer floristic provinces and increasing maximum potential temperature within a habitat. Altitude shows an inverse relationship with thermal responses. Comparison of thermal responses of species emerging early or late in the season within the same habitat show increases in the thermal responses along with the increasing environmental temperatures late in the summer. However, behavior, specifically the use of endothermy as a thermoregulatory strategy, can influence the values determined in a particular habitat. Subspecies generally do not differ in their thermal tolerances and thermal tolerances are consistent within a species over distances of more than 7600 km.     

A new genus and species of the subtribe Leptopsaltriina (Hemiptera: Cicadidae: Leptopsaltriini) from Vietnam,with a key to the genera of Leptopsaltriina

Vietanna Lee & Pham, gen. nov. and Vietanna hanoiensis Pham & Lee, sp. nov. are described based on a cicada specimen from Hanoi, Vietnam and placed in the subtribe Leptopsaltriina Moulton, 1923 of the tribe Leptopsaltriini Moulton, 1923 in the subfamily Cicadinae Latreille, 1802 (Hemiptera: Cicadidae). This new genus is morphologically similar to Tanna Distant, 1905 but distinguished from Tanna by the timbal cover exposing the inner part of timbal, the male abdominal epipleurite 3 with a distinct oblique linear fold, the male abdominal sternites without tubercle-like projections, and the aedeagus bifurcate at the apex. A key to the genera of Leptopsaltriina is provided.www.zoobank.org/urn:lsid:zoobank.org:pub:3B9CBC95-B54A-4BDE-A488-0DEAB69114BD.     

Behavioural and phylogeographic observations on Epipomponia nawai (Dyer, 1904): An East Asian moth (Lepidoptera; Epipyropidae) whose larvae are ectoparasitic on cicadas (Hemiptera; Cicadidae; Sonatini)

The lepidopteran family of the Epipyropidae contains currently 32 known species of moths with larvae that are parasitic on plant and leafhoppers as well as cicadas. This paper focuses on behavioural aspects of the final instar of the cicada parasite Epipomponia nawai (Dyer 1904) on the cicada Hyalessa maculaticollis (de Motschulsky 1866) and represents only the second report of the species from South Korea. This species is a new host for E. nawai in Korea, since in the past it had only been reported once from Meimuna opalifera and Oncotympana fuscata in Korea. Molecular relationships between specimens of E. nawai collected in China, Japan, and Korea were analysed. The Chinese haplotypes fell into two groups: one clearly related to the Korean haplotype, but the other tightly affiliated with the Japanese haplotype. The findings suggest two routes for the occurrence of E. nawai in mainland China. Once the host cicada was dead or too weak to move, the caterpillar crawled away from it, seeking a place to pupate. Very little is known about parasitic Lepidoptera and therefore any information on host species or behavioural aspects is of importance.     

Testing drivers of acoustic divergence in cicadas (Cicadidae: Tettigettalna)

Divergence in acoustic signals may have a crucial role in the speciation process of animals that rely on sound for intra-specific recognition and mate attraction. The acoustic adaptation hypothesis (AAH) postulates that signals should diverge according to the physical properties of the signalling environment. To be efficient, signals should maximize transmission and decrease degradation. To test which drivers of divergence exert the most influence in a speciose group of insects, we used a phylogenetic approach to the evolution of acoustic signals in the cicada genus Tettigettalna, investigating the relationship between acoustic traits (and their mode of evolution) and body size, climate and micro-/macro-habitat usage. Different traits showed different evolutionary paths. While acoustic divergence was generally independent of phylogenetic history, some temporal variables’ divergence was associated with genetic drift. We found support for ecological adaptation at the temporal but not the spectral level. Temporal patterns are correlated with micro- and macro-habitat usage and temperature stochasticity in ways that run against the AAH predictions, degrading signals more easily. These traits are likely to have evolved as an anti-predator strategy in conspicuous environments and low-density populations. Our results support a role of ecological selection, not excluding a likely role of sexual selection in the evolution of Tettigettalna calling songs, which should be further investigated in an integrative approach.     

Postembryonic development of the auditory system of the cicada Okanagana rimosa (Say) (Homoptera: Auchenorrhyncha: Cicadidae)

Cicadas (Homoptera: Auchenorrhyncha: Cicadidae) use acoustic signalling for mate attraction and perceive auditory signals by a tympanal organ in the second abdominal segment. The main structural features of the ear are the tympanum, the sensory organ consisting of numerous scolopidial cells, and the cuticular link between sensory neurones and tympanum (tympanal ridge and apodeme). Here, a first investigation of the postembryonic development of the auditory system is presented. In insects, sensory neurones usually differentiate during embryogenesis, and sound-perceiving structures form during postembryogenesis. Cicadas have an elongated and subterranian postembryogenesis which can take several years until the final moult. The neuroanatomy and functional morphology of the auditory system of the cicada Okanagana rimosa (Say) are documented for the adult and the three last larval stages. The sensory organ and the projection of sensory afferents to the CNS are present in the earliest stages investigated. The cuticular structures of the tympanum, the tympanal frame holding the tympanum, and the tympanal ridge differentiate in the later stages of postembryogenesis. Thus, despite the different life styles of larvae and adults, the neuronal components of the cicada auditory system develop already during embryogenesis or early postembryogenesis, and sound-perceiving structures like tympana are elaborated later in postembryogenesis. The life cycle allows comparison of cicada development to other hemimetabolous insects with respect to the influence of specially adapted life cycle stages on auditory maturation. The neuronal development of the auditory system conforms to the timing in other hemimetabolous insects.     

Ultrastructure and function of long and short sperm in Cicadidae (Hemiptera)

The cicada, Graptopsaltria nigrofuscata, produces two distinct sizes of sperm, as determined by either nuclear volume of early spermatids or nuclear length of mature sperm. Between both sperm, there is no difference in location of the acrosome and flagellum during spermiogenesis. The acrosome is covered by an anteacrosomal bleb, which is inserted in a common mass, spermatodesm, derived from cyst cells. Both kinds of sperm linked to the spermatodesm form sperm bundles, respectively. During copulation, the sperm bundles are transported from the vesicula seminalis of the male to the bursa copulatrix of the female. Morphometric analyses of the nuclear length revealed that the two kinds of sperm reach the bursa copulatrix in the same condition as that found in the vesicula seminalis. Once transferred inside the latter, the sperm bundles disintegrated to individual sperm within a few hours, and the tail components, such as the axoneme and mitochondrial derivatives, become separated from each other over time. The tail completely splits from the sperm nucleus 24 h after copulation. Fertile sperm accumulate in the spermatheca, the final storage organ, where only long sperm survived for any length of time. Fertilized eggs examined by vital staining contain only sperm with long nuclei.     

Sperm morphology in five species of cicadettine cicadas (Hemiptera: Cicadomorpha: Cicadidae)

Mature spermatozoa from five species of cicadas of the subfamily Cicadettinae (Quintilia wealei, Melampsalta leucoptera, Stagira simplex, Xosopsaltria thunbergi and Monomatapa matoposa) were examined by light and electron microscopy. In each species sperm are elongate, aggregated into organized bundles with their heads embedded in a homogenous matrix to form spermatodesmata, and exhibit polymegaly. The head of the sperm consist of an anteriorly positioned conical acrosome that has a tubular substructure and a deep, posterior invagination that forms the subacrosomal space (eccentrically positioned anteriorly). The acrosome is flattened anteriorly; posteriorly it extends along either side of the nucleus as two tubular processes that gradually decrease in diameter. The filiform nucleus tapers anteriorly and intrudes into the subscrosomal space. Posteriorly the nucleus has a lateral invagination that houses material of the so-called centriolar adjunct. Posterior to the centriolar adjuct and the nucleus are two crystalline mitochondrial derivatives and a centriole, respectively, the latter giving rise to the axoneme, which has a 9 + 9 + 2 arrangement of microtubules. In these respects the sperm are similar to those of platypleurine cicadas. However, some features seem unique to cicadettines, including the structural organization of an enlarged centriolar adjunct and the dimensions of the tails. The enlarged centriolar adjunct has a lamella-like substructure and can be considered a synapomorphic character in the Cicadettinae. It is, therefore, potentially useful in the separation of this subfamily from the Cicadinae. In addition, the great length of the sperm nucleus of long-headed sperm in M. matoposa could be a synapomorphy of this genus and related taphurine and cicadettine species.     

New Zealand cicadas of the genus Maoricicada (Homoptera: Tibicinidae)

Abstract

The genus Maoricicada Dugdale, 1972 includes 19 taxa, of which 15 are described here. Ten from the South Island mountains are described as new: M. alticola, M. clamitans, M. mangu gourlayi, M. m. multicostata, M. m. celer, M. nigra frigida, M. otagoensis otagoensis, M. o. maceweni, M. phaeoptera, and M. tenuis. The distributions of most taxa are mapped, their songs are represented by sonograms, and their known periods of emergence are recorded. Evidence of hybridisation is unknown. Most species are characteristic of open, unforested sites; M. nigra nigra and M. oromelaena occur close to the summer snowline, a zone not known to be inhabited by cicadas elsewhere in the world.     

Infectivity of resting spores of Massospora cicadina (Entomophthorales: Entomophthoraceae), an entomopathogenic fungus of periodical cicadas (Magicicada spp.) (Homoptera: Cicadidae)

Progeny of eastern oyster, Crassostrea virginica, introduced into France in 1992, were reared in IFREMER facilities to test their growth performances. During the summer of 1993, sporadic mass mortalities (80-90%) occurred among C. virginica spat reared in the IFREMER laboratories in La Tremblade (Charente Maritime, France) and Bouin (Vendée, France). Affected oysters presented mantle retraction and deposition of an anomalous conchiolin layer on the inner surface of the shell. The incidence of oysters with gross signs exceeded 80%. No obvious pathogen was identified in soft tissues by histology and transmission electron microscopy (TEM). However, histological examination showed the presence of anomalous basophilic round structures, 0.5-1 microm in diameter, in gill and mantle connective tissues. These extracellular Feulgen-negative structures reacted positively with the von Kossa stain. TEM examination on mantle and gill samples in diseased spat showed that the basophilic bodies consisted of concentric deposits of an amorphous substance interpreted as containing calcium. These observations may indicate that the mineralization process in spat shells was disturbed without exact determination of the cause. Based on the similarities of the gross signs to those reported in juvenile eastern oysters in the United States, we believe that the cause of the mortalities observed in France was probably the Juvenile Oyster Disease. Moreover, we report for the first time the detection of anomalous amorphous structures in gill and mantle connective tissues associated with mortalities and deposition of an anomalous conchioloin layer on the inner shell surface in C. virginica spat.     

Sperm morphology in four species of African platypleurine cicadas (Hemiptera: Cicadomorpha: Cicadidae)

Mature spermatozoa from four species of platypleurine cicadas (Albanycada albigera, Azanicada zuluensis, Platypleura capensis and P. hirtipennis) were examined by light and electron microscopy. The filiform sperm have a similar ultrastructure in all species but notable variations were found in sperm dimensions. All species produce more than one discrete length of nucleated, motile sperm, a form of polymorphism termed polymegaly. Polymegaly is expressed in two ways: sperm have bi- or trimodal head and tail lengths. The anterior parts of sperm heads are embedded in an elongate homogenous matrix forming a spermatodesm. The conical acrosome is deeply invaginated posteriorly, and sits on top of the nucleus. The acrosomal contents are differentiated internally with an electron-lucent central medulla and a denser cortex. The homogenously electron-dense nucleus is pointed anteriorly and is generally cylindrical, although posteriorly there is a lateral invagination that extends part-way along the nucleus. This invagination houses fine granular material of the centriolar adjunct. Vesicle-like elements that are associated with both the posterior nucleus and the centriolar adjunct are also found within the invagination. Immediately posterior of and adjoining the centriolar adjunct is a pair of mitochondrial derivatives that are elongated and extend for almost the entire length of the tail. The absence of accessory bodies in cicada sperm suggests that within the Cicadomorpha, the families Cicadidae and Cercopidae are closely affiliated.     

Biogeography and phylogeny of the New Zealand cicada genera (Hemiptera: Cicadidae) based on nuclear and mitochondrial DNA data

Aim Determine the geographical and temporal origins of New Zealand cicadas. Location New Zealand, eastern Australia and New Caledonia. Methods DNA sequences from 14 species of cicadas from New Zealand, Australia, and New Caledonia were examined. A total of 4628 bp were analysed from whole genome extraction of four mitochondrial genes (cytochrome oxidase subunits I and II, and ribosomal 12S and 16S subunits) and one nuclear gene (elongation factor‐1 alpha). These DNA sequences were aligned and analysed using standard phylogenetic methods based primarily on the maximum likelihood optimality criterion. Dates of divergences between clades were determined using several molecular clock methods. Results New Zealand cicadas form two well‐defined clades. One clade groups with Australian taxa, the other with New Caledonian taxa. The molecular clock analyses indicate that New Zealand genera diverged from the Australian and New Caledonian genera within the last 11.6 Myr. Main conclusions New Zealand was likely colonized by two or more invasions. One NZ lineage has its closest relatives in Australia and the other in New Caledonia. These invasions occurred well after New Zealand became isolated from other land masses, therefore cicadas must have crossed large bodies of water to reach New Zealand.     

Distribution of cicadas of the genus Lyristes (Hemiptera: Cicadidae) in the eastern Mediterranean area

The present study gives an updated overview on the distribution of species of the genus Lyristes Horváth, 1926 in the eastern Mediterranean area. Besides occurring in southern continental Europe, specimens of L. plebejus were also found along the southern Greek mainland and in the western Aegean island of Kithira. Moreover, the new data presented give L. gemellus as a new record for Greece (appearing only along most of the Anatolian coast) as well as for Cyprus. The genus seems to be absent from the Cyclades as well as from the islands of Crete and Karpathos. Therefore, the results revealed a faunal discontinuity between the Greek western and eastern islands in the Aegean Sea. Hence, the persistence of a deep sea barrier between these two groups of islands seems to explain the present distribution of Lyristes species, which is also in accordance with the paleogeography of the area and with the fact that dispersal to more geographically isolated islands might have been virtually impossible for species of this genus.