Urban soil compaction reduces cicada diversity
© Moriyama and Numata. 2015
Received: 29 May 2015
Accepted: 27 June 2015
Published: 1 August 2015
Urbanization converts animal habitats into globally homogeneous environments. Consequently, urban communities have low diversity and are often dominated by a few species. However, proximate environmental factor(s) causing community degradation have rarely been identified among diverse and co-varying urban parameters.
The present study addresses the recent loss of cicada diversity in Osaka, Japan, where cicada communities are overwhelmed by a single species, Cryptotympana facialis. A field survey across an urban-forest gradient revealed that the trend of decreasing cicada diversity toward the urban core was mostly associated with the soil hardness among the environmental variables examined. Simultaneously, the proportion of C. facialis increased with soil hardness, although this effect was partially mitigated in forest patches. Newly hatched nymphs of C. facialis exhibited greater burrowing ability than that in other native species.
These findings identify soil compaction due to urbanization as a possible cause of cicada diversity loss, as it impedes the passage of nymphs to underground nests. This impact of urban soil compaction may influence ecosystem functioning of soil-dwelling arthropods and their trophically associated animals.
Urbanization brings about radical changes in animal habitats, contributes to the extirpation of local populations and community collapse, and consequently disrupts ecosystem function and service delivery [9, 13, 55]. Understanding urban degradation of biotic and abiotic community processes has become an increasingly urgent conservation concern [30, 36].
It is generally accepted that animal diversity decreases toward urban cores compared to rural surroundings [11, 14, 38]. Simultaneously, urban areas are usually dominated by a limited number of species, which are referred to as “urban exploiters” [4, 37]. Urban landscapes are characterized by extensive habitat fragmentation, a high proportion of impervious ground surfaces, compacted soil, locally hot and dry climatic conditions, and elevated pollution levels [13, 36, 46]. It is difficult to use correlative analyses to discriminate a proximate factor for community change from co-varying parameters because diverse environmental parameters interact and vary with urbanization processes . Moreover, responses to urbanization are highly species- or community-specific [10, 32, 53, 61]. Thus, studies aiming to identify a causal process responsible for biodiversity loss should be based on the life cycle traits and physiological or behavioral characteristics of individual species.
Until now, research on urban ecology has been developed largely for vertebrate species e.g., birds and mammals, and arthropods have received less attention in spite of their advantages regarding ethical and experimental practicability [30, 34]. Cicadas are a conspicuous insect group, especially in warm temperate and tropical zones, due to their large bodies and species-specific calling songs [2, 15, 43]. Because a change in cicada communities can easily be recognized by ordinary citizens as an acoustic change, it is an important index of biodiversity. In Japan, cicada communities have experienced substantial changes, mainly in urbanized areas . A striking instance is that in Osaka City—during the extensive urban growth in the last few decades of the 20th century, the cicada community became overwhelmed by a single native cicada, Cryptotympana facialis, which had previously comprised a minor population [40, 45, 59]. It has brought new social problems such as loud noise of calling songs and destruction of optical fiber cables .
In the present study, we investigated the influence of environmental parameters on cicada community structures along an urban-forest gradient in Osaka Prefecture, with a particular focus on urban soil compaction. While cicada nymphs grow on the underground roots of trees, adults and their eggs spend all their time on aboveground parts of trees [15, 43]. Hence, newly hatched nymphs confront the critical challenge of passing through the ground surface barrier and reaching suitable roots in a brief time [19, 23, 39]. Thus, we hypothesized that soil compaction in urban areas might be a proximate cause of diversity loss in the cicada community. We therefore compared burrowing ability among nymphs of native cicada species under standardized experimental conditions in addition to field observation of cicada diversity. The results suggested that degradation of the cicada community resulting from C. facialis domination had been administered by urban soil compaction.
Materials and methods
Osaka City is the most economically developed city in western Japan. It is located in the center of Osaka Prefecture, and surrounded by several suburban cities, including Sakai, Higashi-Osaka, and Mino. The outline of the prefecture is largely formed by mountain forest. We selected 13 sampling sites along this urban-forest gradient (Additional file 1: Table S1). Each site was assigned to one of three patch categories: a small park (0.49 − 3.74 ha), large park (25.5 − 106.7 ha), or continuous forest zone. Three to six sampling plots were defined in each site, except for small urban parks, in which only one plot was defined. The boundaries of each plot (at least two sides of a quadrangle) were defined by pavements, trails, steep slopes, or other apparent discontinuity of vegetation. The other sides were arbitrarily determined, and the area of each plot was 152.3 m2 on average (35.5 − 415.3 m2).
Collection of cicada exuviae
By collecting exuviae of final instar nymphs, we recorded the number and species of cicadas that had emerged from the sampling plots, i.e. C. facialis, Graptopsaltria nigrofuscata, Meimuna opalifera, Platypleura kaempferi, Hyalessa maculaticollis, and Tanna japonensis. Exuviae of these cicadas are conspicuous, steady for a long time, and have often used for community assessments (e.g. [45, 59]). Before the emergence period of adult cicadas, exuviae remaining from the previous year were removed. We visited each site to collect exuviae at least two times between 9 August and 25 September 2008. At each visit, we thoroughly rummaged through the sampling plot for all exuviae, some of which had fallen to the ground, and the others stayed on tree branches or trunks at heights of up to several meters. Thus, differences in visibility of exuviae among sites seemed to have negligible effects on results. A minor portion of exuviae may have been blown off or grabbed by a passerby in the sampling intervals. Nevertheless, we found a considerable number of exuviae at every site in consistent with auditory species information. Therefore, it is presumed that most exuviae were collected with the least sampling bias for species among sites. The species of the exuviae were identified according to Hayashi and Saisho . The diversity of the cicada community was evaluated using Shannon’s diversity index H .
Environmental variables included in the model analyses for cicada community structures
Small park, large park, forest
Percentage of impervious area in 1-km radius
Altitude at the site (m)
Slope of the ground (°)
Index of Yamanaka's soil hardness meter (mm)
Percentage of canopy coverage in 30-m radius
Shannon’s index (H)
Number of trees per 100 m2
We evaluated the effects of environmental parameters on cicada community structures under a generalized linear mixed model (GLMM) framework. Diversity indices (square-rooted) and proportions of a given species were fitted to a model that assumed a Gaussian or binomial error structure, with an identity or logit link function, respectively. In the latter variable, individual random effects were taken into account to avoid overdispersion. Model comparisons were performed by a chi-square test of deviance reduction.
We performed single variable analyses using each environmental variable. Quadratic terms were also evaluated in these models, and used in the further analyses if their effects were significant. In multi-variable analyses, all possible two-way interactions were considered. Some explanatory variables showed high correlation coefficients (Additional file 3: Table S3). To limit the effects of multicollinearity, the models omitted the altitude variable, whose variance inflation factor exceeded 10. We selected a parsimonious model based on the Akaike’s information criterion and then a stepwise backward procedure . Finally, the levels in a factorial variable were merged when it was not significantly different from the original model. All statistical analyses were conducted using R 3.1.2 .
Adult females of four species, i.e. C. facialis, G. nigrofuscata, M. opalifera, and P. kaempferi, were collected in Osaka Prefecture between July and September in 2006–2007. The methods of egg collection and maintenance have been described in detail [40, 42]. Captured adult females were individually caged in a plastic pot (9 cm diameter, 12 cm depth), and allowed to lay their eggs into squared Albizia timber sticks (6 × 6 × 130 mm). These sticks were kept outdoors in a net hung on the tree branch at the campus of Osaka City University. Approximately one month before completion of embryonic development, sticks were transferred to a laboratory at 25.0 ± 1.0 °C under 16 h light and 8 h dark cycles, and hydrated at intervals of 2–5 days to induce hatching . Nymphs leaving the sticks were used for burrowing experiments described below within 30 min.
The soil was collected on the campus of Osaka City University (Additional file 2: Table S2), passed through a 5-mm-mesh sieve, and dehydrated at 110 °C for 12–24 h. A grading analysis revealed that the soil type was sand with median grain diameter of 354 μm and coefficient of uniformity of 6.13. Burrowing arenas were created with cylindrical polystyrene containers (150 mm diameter, 90 mm height) filled with a mixture of 1200 g dried soil and 120 g distilled water (9.1 %), unless otherwise noted. The soil was compressed to final heights of 50, 55, 60, and 65 mm, to obtain four decreasing levels of soil compactness, 1.36, 1.23, 1.13, and 1.04 g/ml, respectively. In further experiments, the water content was increased to 150 g (11.1 %), or the soil was mixed with vermiculite (Nittai, Osaka, Japan). The compositions of the dried soil, vermiculite and distilled water were 880, 136, and 120 g (dry mass content of vermiculite was 13.4 %), or 320, 374, and 120 g (53.9 %), respectively. These mixtures had approximately the same volume as the 1200 g soil containing 120 g water before compression. In these experiments, the soil mixture was compressed to a height of 55 mm.
Ten nymphs were released on one of these burrowing arenas. The arenas were kept at 25.0 °C, and closed with a lid to prevent desiccation except during observation. Nymphs usually tried to enter the soil from small cracks on the surface. In well-compacted soil with flat surface, however, we often found newly-made tiny holes after nymphs had entered the soil. In the present study, nymphs that disappeared from the soil surface were considered to have burrowed. Although we recorded the number of burrowed nymphs every 15–30 min for 3 h, the scores at 60 min were compared among species as an ecologically relevant scale, because the previous study showed that no nymphs survive on the ground for more than 1 h in the field . The effects of species and soil conditions on burrowing rates were examined using GLMM assuming a binomial error structure with a logit link function, considering individual variation as a random effect. When the species term had a significant effect, we performed pairwise comparisons with a Bonferroni adjustment.
Cicada community change across the urban-forest gradient
Despite the general trend across the urban-forest gradient, variations in species composition within a site were not negligible. Then, we combined data from all sampling plots, and performed model analyses using the environmental parameters listed in Table 1. Some variables used in this study varied with urbanization, and showed high correlation with each other (Additional file 3: Table S3). For example, imperviousness of the ground surface, the most relevant urbanization indicator, was positively correlated with soil hardness, but negatively correlated with altitude, slope, and canopy coverage. These trends seemed to reflect the fact that urbanization has progressed in low, flat regions, and is characterized by open habitats and compacted soil.
Single-variable analyses for cicada diversity index and proportion of Cryptotympana facialis
Shannon's H (square root)
Proportion of C. facialis
Coefficient ± SE
Coefficient ± SE
Patch type (SP, F)a
−0.780 ± 0.174
9.08 ± 1.72
−0.642 ± 0.138
9.87 ± 2.01
−0.013 ± 0.002
0.187 ± 0.031
3.0e −3 ± 0.5e−3
−0.083 ± 0.021
0.050 ± 0.012
−0.785 ± 0.195
−0.079 ± 0.009
1.14 ± 0.14
0.013 ± 0.003
−0.165 ± 0.032
0.024 ± 0.018
−0.246 ± 0.277
−0.229 ± 0.104
3.28 ± 1.51
Parsimonious models for cicada diversity, abundance, and the proportion of Cryptotympana facialis
Coefficient ± SE
Shannon's H (square root)
2.15 / 7.31
2.15 ± 0.18
−0.079 ± 0.009
Proportion of Cryptotympana facialis
−18.7 ± 2.18
0.89 ± 0.11
Patch type (small & large park, forest)a
3.44 ± 0.74
Comparison of burrowing ability
Compared to urban soil, forest soil contains more heterogeneous materials with a porous nature and higher water content. When the water content was elevated from 9.1 to 11.1 %, burrowing rate increased in both C. facialis and G. nigrofuscata (Fig. 3B). Species and water content had significant effects (P < 0.001, GLMM), but there was no significant interaction effect (P > 0.05), indicating that water content affected burrowing success similarly in these two species. Finally, the soil was mixed with vermiculite to mimic litter-containing porous soil. Burrowing rate increased with vermiculite content in both species (Fig. 3C). Like water content, the species and vermiculite content had significant effects (P < 0.001), but their interaction did not (P > 0.05). Therefore, in all soil conditions tested, the burrowing rate of C. facialis nymphs never fell below those of the other native cicada species.
The present study revealed the possible involvement of soil hardness in the species distribution of cicadas. It has been shown that geographical distributions of cicadas are influenced by several abiotic factors, such as temperature [16, 42, 51, 60], humidity , and light . Several authors have pointed out the possible relevance of soil properties to species distribution or abundance of cicadas, although their causal relationships have not been verified [5, 12, 18, 26]. For soil-dwelling arthropods, such as ants [17, 21], digger wasps [33, 47, 54], tiger beetles , and larvae of May beetles , soil characteristics play an important role in determining species-specific distribution patterns. Especially, soil hardness is strongly related to underground activities, and therefore an appropriate digging ability appears to have been selected according to the requirements of the particular habitat [33, 47, 54]. Cicadas spend much time underground during their nymphal period . Once settled in underground nests, they are less mobile, and have relatively low mortality until emergence from the soil [19, 23]. However, considerable mortality occurs at the transition stage, in which tiny nymphs just after hatching from tree branches try to penetrate the ground surface to seek a suitable rootlet. Nymphs on the ground suffer extremely high risk of predation and desiccation unless they escape into the soil [19, 22, 23, 39]. The present study revealed that the distribution pattern of C. facialis associated with hard soil surface is consistent with its higher burrowing ability in the newly hatched stage. These findings suggest that soil hardness at the ground surface is a critical abiotic factor affecting the success of burrowing, and consequent colonization of cicadas.
We found that soil hardness was elevated in parallel with urbanization across the study sites. Soil in urbanized areas has generally been subjected to extensive tillage and compression during construction processes, repeated vehicle and foot traffic, loss of plant litter input, and changes in hydrology [20, 29, 46]. Consequently, urban soil shows non-porous compaction, low water content, low organic matter content, low water retention capacity, high pH, and high metal content. Such soil modifications can become a driving force in altering the soil arthropod community [35, 44, 52]. In the mid-20th century, G. nigrofuscata, M. opalifera, and P. kaempferi accounted for large portions, whereas the population of C. facialis accounted for a minor portion, of the cicada community in Osaka City . In the present survey, the diversity of the community in this region was extremely poor due to exclusive domination by C. facialis. During the late 20th century, rapid and extensive urbanization proceeded in Osaka, and seems to have rendered the soil compacted and hardened to states that are unusual in nature. The resultant urban soil is likely to have favored colonization of C. facialis due to its higher burrowing ability. We conclude, therefore, that soil compaction derived from extensive urbanization may have served as a proximate factor accounting for the time-course of the drastic change in the cicada community.
Two formerly common species, P. kaempferi and M. opalifera, were not found in Osaka City in the present survey, suggesting their possible local extirpation. The other previously common native species, G. nigrofuscata, barely persisted in this area, and populated more semi-urban areas than the former two species, although all three of these species were shown to have similar burrowing ability. G. nigrofuscata is the most prevalent lowland species in the main island of Japan , and formed the largest population in Osaka City before the extensive urbanization . Therefore, the higher ability of G. nigrofuscata to exploit lowland environments, except with regard to soil hardness, may be responsible for the current distribution patterns. In other words, soil compaction may place a similar burden across these species, and consequently species having smaller population sizes may be more susceptible to urbanization-driven extirpation.
The present findings raise the question of why C. facialis, in spite of its higher burrowing ability, accounted for only a minor portion of the cicada community before the extensive urbanization. Nymphs of C. facialis exhibited better burrowing ability in all soil conditions tested here, which included conditions mimicking soft, hydrated, or highly porous forest soil (Additional file 2: Table S2). Thus, it is unlikely that soil properties in less urbanized areas adversely affect the burrowing success of C. facialis. One possibility is that population growth of C. facialis had previously been limited by some environmental factor(s) negatively correlated with urbanization. In urban areas, air temperature is locally increased due to heat island effects, whereas humidity is decreased. We previously demonstrated that embryonic development of C. facialis requires greater thermal accumulation, and that the recent warming in Osaka was a prerequisite for its colonization in this area . Moreover, eggs of C. facialis show higher desiccation tolerance than those of G. nigrofuscata . These developmental and physiological characteristics of C. facialis that are favored by a hot, dry climate may have prevented its population growth before the advent of the urban climate.
Another possibility is that interspecific competition had suppressed C. facialis population growth. Cicadas usually exploit a wide range of plant species for feeding and oviposition [27, 62], and thus several species often share the same host tree. In the present study, exuviae of C. facialis were often found on the most prevalent tree species, such as Z. serrata, P. yedoensis, C. camphora, and G. biloba. These tree species are known to be exploited by the formerly common native species . Adult cicadas are well known to show segregation patterns with sympatric competitors in terms of time [5, 56], microhabitat conditions [50, 51, 57], and acoustic characteristics [50, 56]. Crowding in the underground nymphal stage also has adverse effects [22, 63]. The observed negative influence of the forest patch on C. facialis in the model analyses may reflect inappropriate climate conditions and/or elevated competition pressure by the other species that came from surrounding source populations.
The present study demonstrated that the decline in cicada diversity due to C. facialis domination across an urban-forest gradient is best predicted by soil hardness. We have also showed that the burrowing ability of newly hatched nymphs is remarkably higher in C. facialis than in other native species, which have decreased with urbanization. These consistent findings highlighted soil compaction as a proximate cause of cicada community degradation. The impact on community structures demonstrated here is predicted to be shared by diverse taxonomic groups across cities, because of the global homogeneity of urban environments , and because of the common importance of soil hardness among soil-dwelling arthropods [33, 47, 54]. Identification of proximate factors may also contribute to designing feasible and effective actions for biodiversity conservation . Cicadas play a substantial role in ecosystem function, such as nutrient flux from underground to aboveground [1, 5, 64, 66], and are important resources for vertebrate predators [28, 31]. Therefore, maintaining a variety of cicada species with different body sizes and emergence periods is expected to support diverse animals.
We thank Muneki Mitamura for technical advice on soil analyses. Our thanks are also due to Dmitry L. Musolin for critical reading of the manuscript and Elizabeth Nakajima for linguistic corrections. This study was financially supported in part by a research grant from the Convention for the Uemachi-Daichi Mild Hope Zone to MM.
- Aoki C, Lopes FS, de Oliveira AMR, de Souza FL, Marques MR. Nutrient flux associated with the emergence of Quesada gigas Olivier (Hemiptera: Cicadidae) in an urban ecosystem. Neotrop Entomol. 2011;40:436–9.PubMedView ArticleGoogle Scholar
- Beamer R. Studies on the biology of Kansas Cicadidae. Univ Kansas Sci Bull. 1928;18:155–263.Google Scholar
- Begon M, Harper JL, Townsend CR. Ecology: individuals, populations and communities. 3rd ed. London: Wiley-Blackwell; 1996.View ArticleGoogle Scholar
- Blair RB, Launer AE. Butterfly diversity and human land use: species assemblages along an urban gradient. Biol Conserv. 1997;80:113–25.View ArticleGoogle Scholar
- Callaham Jr MA, Whiles MR, Meyer CK, Brock BL, Charlton RE. Feeding ecology and emergence production of annual cicadas (Homoptera: Cicadidae) in tallgrass prairie. Oecologia. 2000;123:535–42.View ArticleGoogle Scholar
- Cornelisse T, Hafernik J. Effects of soil characteristics and human disturbance on tiger beetle oviposition. Ecol Entomol. 2009;34:495–503.View ArticleGoogle Scholar
- Crawley MJ. Statistics: an introduction using R. West Sussex: John Wiley & Sons; 2005.View ArticleGoogle Scholar
- Cyranoski D. 2007; Flying insects threaten to deafen Japan. Nature. 2014;448:49073.Google Scholar
- Dearborn DC, Kark S. Motivations for conserving urban biodiversity. Conserv Biol. 2010;24:432–40.PubMedView ArticleGoogle Scholar
- Denys C, Schmidt H. Insect communities on experimental mugwort (Artemisia vulgaris L.) plots along an urban gradient. Oecologia. 1998;113:269–77.View ArticleGoogle Scholar
- Faeth SH, Bang C, Saari S. Urban biodiversity: patterns and mechanisms. Ann NY Acad Sci. 2011;1223:69–81.PubMedView ArticleGoogle Scholar
- Glinski RL, Ohmart RD. Factors of reproduction and population densities in the Apache cicada (Diceroprocta apache). Southwest Nat. 1984;29:73–9.View ArticleGoogle Scholar
- Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, et al. Global change and the ecology of cities. Science. 2008;319:756–60.PubMedView ArticleGoogle Scholar
- Hansen A, Knight R, Marzluff J. Effects of exurban development on biodiversity: patterns, mechanisms, and research needs. Ecol Appl. 2005;15:1893–905.View ArticleGoogle Scholar
- Hayashi M, Saisho Y. The Cicadidae of Japan. Tokyo: Seibundo Shinkosha; 2011. (in Japanese)Google Scholar
- Heath JE, Hanegan JL, Wilkin PJ, Heath MS. Adaptation of the thermal responses of insects. Am Zool. 1971;11:147–58.Google Scholar
- Holway D, Suarez A, Case T. 2002; Role of abiotic factors in governing susceptibility to invasion: a test with Argentine ants. Ecology. 2011;83:1610–9.View ArticleGoogle Scholar
- Irwin M, Coelho J. Distribution of the Iowan brood of periodical cicadas (Homoptera: Cicadidae: Magicicada spp.) in Illinois. Ann Entomol Soc Am. 2000;93:82–9.View ArticleGoogle Scholar
- Ito Y, Nagamine M. Why a cicada, Mogannia minuta Matsumura, became a pest of sugarcane: an hypothesis based on the theory of “escape”. Ecol Entomol. 1981;6:273–83.View ArticleGoogle Scholar
- Jim CY. Soil compaction as a constraint to tree growth in tropical and subtropical urban habitats. Environ Conserv. 1993;20:35–49.View ArticleGoogle Scholar
- Johnson RA. Habitat segregation based on soil texture and body size in the seed-harvester ants Pogonomyrmex rugosus and P. barbatus. Ecol Entomol. 2000;25:403–12.View ArticleGoogle Scholar
- Karban R. Opposite density effects of nymphal and adult mortality for periodical cicadas. Ecology. 1984;65:1656–61.View ArticleGoogle Scholar
- Karban R. Evolution of prolonged development: a life table analysis for periodical cicadas. Am Nat. 1997;150:446–61.PubMedView ArticleGoogle Scholar
- Kato M. The Biology of the Cicadas. Tokyo: Iwasaki Shoten; 1956 (In Japanese.).Google Scholar
- Katovich K, Levine SJ, Young DK. Characterization and usefulness of soil-habitat preferences in identification of Phyllophaga (Coleoptera: Scarabaeidae) larvae. Ann Entomol Soc Am. 1998;91:288–97.View ArticleGoogle Scholar
- Kim K, Kim JG. Soil habitat characteristics of cicada nymph in an urban apartment garden. J Korea Soc Environ Restor Technol. 2011;14:47–55.Google Scholar
- Kim TE, Oh SY, Chang E, Jang Y. Host availability hypothesis: complex interactions with abiotic factors and predators may best explain population densities of cicada species. Animal Cells Syst (Seoul). 2014;18:143–53.View ArticleGoogle Scholar
- Koenig W, Liebhold A. Effects of periodical cicada emergences on abundance and synchrony of avian populations. Ecology. 2005;86:1873–82.View ArticleGoogle Scholar
- Kozlowski TT. Soil compaction and growth of woody plants. Scand J For Res. 1999;14:596–619.View ArticleGoogle Scholar
- Magle SB, Hunt VM, Vernon M, Crooks KR. Urban wildlife research: past, present, and future. Biol Conserv. 2012;155:23–32.View ArticleGoogle Scholar
- Marcello GJ, Wilder SM, Meikle DB. Population dynamics of a generalist rodent in relation to variability in pulsed food resources in a fragmented landscape. J Anim Ecol. 2008;77:41–6.PubMedView ArticleGoogle Scholar
- Mata L, Goula M, Hahs AK. Conserving insect assemblages in urban landscapes: accounting for species-specific responses and imperfect detection. J Insect Conserv. 2014;18:885–94.View ArticleGoogle Scholar
- McCorquodale DB. Soil softness, nest initiation and nest sharing in the wasp, Cerceris antipodes (Hymenoptera: Sphecidae). Ecol Entomol. 1989;14:191–6.View ArticleGoogle Scholar
- McIntyre N. Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am. 2000;93:825–35.View ArticleGoogle Scholar
- McIntyre NE, Rango J, Fagan WF, Faeth SH. Ground arthropod community structure in a heterogeneous urban environment. Landsc Urban Plan. 2001;52:257–74.View ArticleGoogle Scholar
- McKinney ML. Urbanization, biodiversity, and conservation. Bioscience. 2002;52:883–90.View ArticleGoogle Scholar
- McKinney ML. Urbanization as a major cause of biotic homogenization. Biol Conserv. 2006;127:247–60.View ArticleGoogle Scholar
- McKinney ML. Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst. 2008;11:161–76.View ArticleGoogle Scholar
- Moriyama M, Numata H. Induction of egg hatching by high humidity in the cicada Cryptotympana facialis. J Insect Physiol. 2006;52:1219–25.PubMedView ArticleGoogle Scholar
- Moriyama M, Numata H. Comparison of cold tolerance in eggs of two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata, in relation to climate warming. Entomol Sci. 2009;12:162–70.View ArticleGoogle Scholar
- Moriyama M, Numata H. Desiccation tolerance in fully developed embryos of two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata. Entomol Sci. 2010;13:68–74.View ArticleGoogle Scholar
- Moriyama M, Numata H. A cicada that ensures its fitness during climate warming by synchronizing its hatching time with the rainy season. Zoolog Sci. 2011;28:875–81.PubMedView ArticleGoogle Scholar
- Myers JG. Insect singers: a natural history of the cicadas. London: George Routledge and Sons; 1929.Google Scholar
- Norton BA, Thomson LJ, Williams NSG, McDonnell MJ. The effect of urban ground covers on arthropods: An experiment. Urban Ecosyst. 2014;17:77–99.View ArticleGoogle Scholar
- Numata H, Shiyake S. Cicadas living in urban areas: an influence of warming? Tokyo: Kaiyusha; 2007. (in Japanese)Google Scholar
- Pickett STA, Cadenasso ML, Grove JM, Boone CG, Groffman PM, Irwin E, et al. Urban ecological systems: scientific foundations and a decade of progress. J Environ Manage. 2011;92:331–62.PubMedView ArticleGoogle Scholar
- Potts S, Willmer P. Abiotic and biotic factors influencing nest-site selection by Halictus rubicundus, a ground-nesting halictine bee. Ecol Entomol. 1997;22:319–28.View ArticleGoogle Scholar
- R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014. [http://www.R-project.org/]
- Raupp MJ, Shrewsbury PM, Herms DA. Ecology of herbivorous arthropods in urban landscapes. Annu Rev Entomol. 2010;55:19–38.PubMedView ArticleGoogle Scholar
- Sanborn AF, Breitbarth JH, Heath JE, Heath MS. Temperature responses and habitat sharing in two sympatric species of Okanagana (Homoptera: Cicadoidea). West North Am Nat. 2002;62:437–50.Google Scholar
- Sanborn AF, Heath JE, Phillips PK, Heath MS, Noriega FG. Thermal adaptation and diversity in tropical ecosystems: evidence from cicadas (Hemiptera, Cicadidae). PLoS One. 2011;6, e29368.PubMed CentralPubMedView ArticleGoogle Scholar
- Santorufo L, van Gestel CAM, Rocco A, Maisto G. Soil invertebrates as bioindicators of urban soil quality. Environ Pollut. 2012;161:57–63.PubMedView ArticleGoogle Scholar
- Sattler T, Duelli P, Obrist MK, Arlettaz R, Moretti M. Response of arthropod species richness and functional groups to urban habitat structure and management. Landsc Ecol. 2010;25:941–54.View ArticleGoogle Scholar
- Srba M, Heneberg P. Nesting habitat segregation between closely related terricolous sphecid species (Hymenoptera:Spheciformes): key role of soil physical characteristics. J Insect Conserv. 2012;16:557–70.View ArticleGoogle Scholar
- Srivastava DS, Vellend M. Biodiversity-ecosystem function research: is it relevant to conservation? Annu Rev Ecol Evol Syst. 2005;36:267–94.View ArticleGoogle Scholar
- Sueur J. Cicada acoustic communication: potential sound partitioning in a multispecies community from Mexico (Hemiptera: Cicadomorpha: Cicadidae). Biol J Linn Soc. 2002;75:379–94.View ArticleGoogle Scholar
- Sueur J, Aubin T. Is microhabitat segregation between two cicada species (Tibicina haematodes and Cicada orni) due to calling song propagation constraints? Naturwissenschaften. 2003;90:322–26.PubMedView ArticleGoogle Scholar
- Tada A. Bearing capacity. In: Physical measurements in flooded rice soils: the Japanese methodologies. Los Baños: International Rice Research Institute; 1987. p. 55–61.Google Scholar
- Takakura KI, Yamazaki K. Cover dependence of predation avoidance alters the effect of habitat fragmentation on two cicadas (Hemiptera: Cicadidae). Ann Entomol Soc Am. 2007;100:729–35.View ArticleGoogle Scholar
- Toolson EC. Comparative thermal physiological ecology of syntopic populations of Cacama valvata and Tibicen bifidus (Homoptera: Cicadidae): Modeling fitness consequences of temperature variation. Integr Comp Biol. 1998;38:568–82.View ArticleGoogle Scholar
- Turrini T, Knop E. A landscape ecology approach identifies important drivers of urban biodiversity. Glob Chang Biol. 2015;21:1652–67.PubMedView ArticleGoogle Scholar
- White J. Resource partitioning by ovipositing cicadas. Am Nat. 1980;115:1–28.View ArticleGoogle Scholar
- White J, Lloyd M, Zar JH. Faulty eclosion in crowded suburban periodical cicadas: populations out of control. Ecology. 1979;60:305–15.View ArticleGoogle Scholar
- Yang LH. Periodical cicadas as resource pulses in North American forests. Science. 2004;306:1565–7.PubMedView ArticleGoogle Scholar
- Yang LH. Periodical cicadas use light for oviposition site selection. Proc Royal Soc B. 2006;273:2993–3000.View ArticleGoogle Scholar
- Yang L. Pulses of dead periodical cicadas increase herbivory of American bellflowers. Ecology. 2008;89:1497–502.PubMedView ArticleGoogle Scholar
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