Animal Cells and Systems, 2014 Vol. 18, No. 2, 143–153, http://dx.doi.org/10.1080/19768354.2014.906501
Host availability hypothesis: complex interactions with abiotic factors and predators may best explain population densities of cicada species Tae Eun Kima, Seung-Yoon Ohb, Eunmi Changc and Yikweon Jangd* a Department of Life Sciences, Ewha Womans University, Seoul 120-750, Republic of Korea; bSchool of Biological Sciences, Seoul National University, Seoul 151-747, Republic of Korea; cZiin Consulting Institute, Seoul 110-070, Republic of Korea; dDepartment of Life Sciences and Division of EcoScience, Ewha Womans University, Seoul 120-750, Republic of Korea
Advertisement calls of some cicadas are so loud that they are a nuisance to city-dwellers in Korea. We hypothesized that the densities of cicada species were directly correlated with the availability of host plant species. We conducted complete enumeration surveys of exuviae in Hyalessa fuscata, Cryptotympana atrata, Meimuna spp., and Graptopsaltria nigrofuscata in three representative habitats in Republic of Korea: metropolitan, suburban, and country. We measured resource-weighted density of each species based on the area and the number of trees, and used those values to calculate organism-weighted density, which measures the intensity of competition that an individual experiences sharing its host with others of its own species. H. fuscata was the dominant species in all three habitats. H. fuscata and C. atrata comprised a minimum of 75.2% of all cicadas across all habitats and sampling periods. Resource-weighted densities of H. fuscata and C. atrata were much higher in the metropolitan habitat than in the country habitat. Habitat was a significant factor for variations in organism-weighted densities in C. atrata and G. nigrofuscata, but it was not in Meimuna spp. and H. fuscata. Some of the results concerning the percentages of trees without exuviae and preferred plants seemed to support the host availability hypothesis in C. atrata, Meimuna spp. and G. nigrofuscata, but they may not in H. fuscata. The similarity between resource-weighted and organism-weighted densities suggests that factors other than host availability, speculatively abiotic factors and predators, may also account for the patterns of population densities in C. atrata and G. nigrofuscata. Keywords: Cryptotympana atrata; Graptopsaltria nigrofuscata; Hyalessa fuscata; host availability; Meimuna spp.; organism-weighted density; resource-weighted density
Introduction Male cicadas typically produce loud advertisement calls to attract female cicadas for mating. The cicada choruses typically occur during the day, but often extend late into the night especially in cities. There are several hypotheses that might explain uneven cicada densities across habitats: (1) favorable abiotic conditions, (2) low predation pressure, and (3) host plant availability. Abiotic factors influence the density of cicadas because these factors directly affect life history traits, such as survival rate, hatching, oviposition, habitat selection, and so on. Abiotic factors that might influence cicada density include light, temperature, humidity, and rainfall. Light condition was found to be a critical factor for oviposition site selection in periodical cicadas (Magicicada spp.; Yang 2006), and the photoperiod was suggested to affect hatching rate in Cryptotympana atrata (Sun et al. 2011). Although a causal effect of temperature on the density of cicada populations has not yet been established, temperature is implicated in the induction and termination of diapause, and also affects embryonic development in cicadas (Moriyama & Numata 2008). Hatching is induced by high humidity, and is important to the survival of the first
*Corresponding author. Email:
[email protected] Tae Eun Kim and Seung-Yoon Oh contributed equally to this work. © 2014 Korean Society for Integrative Biology
instar nymphs. This is because high humidity prevents desiccation and reduces the failure to dig successfully underground (Moriyama & Numata 2006). The low predation pressure hypothesis predicts that low predator densities are directly related to high densities of cicadas. Birds are known to be one of the most dominant predators for cicadas (Sazima 2009). There is a spatial synchrony between avian predators and periodical cicadas in eastern North America, and the emergence of periodical cicadas has significant demographic effects on key avian predators, mostly during or immediately after emergences (Koenig & Liebhold 2005). Furthermore, avian species richness has been observed to decline in relation to a gradient of increasing urbanization, as measured by localand landscape-level habitat features (Blair 1996; Melles et al. 2003). Thus, the low densities of avian species that prey on cicadas might explain high cicada densities. The host availability hypothesis predicts that the density of a given cicada species is directly correlated with the availability of that species’ host plant. Over 80% of all phytophagous hemipterans are monophagous or oligophagous, due to the high degree of tissue specialization in sucking roots (Bernays & Chapman 1994). In
ECOLOGY & POPULATION BIOLOGY
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(Received 14 January 2014; received in revised form 17 March 2014; accepted 17 March 2014)
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addition, the structure and shape of forests (Rodenhouse et al. 1997; Lin 2007) and the age of forests or trees (Clay et al. 2009; Yang & Karban 2009) affect the distribution and abundance of cicada species. Periodical cicadas in North America prefer to oviposit in some species of trees, such as Carya, Quercus, Ulmus, Acer, Cornus, and Fraxinus species, and do not prefer other tree species, such as Asimina triloba, Lindera benzoin, Robinia pseudoacacia, Rhus species, and conifers (Skeels 1907). Furthermore, preferences of tree species were different among three periodical cicada species (Williams & Smith 1991). Thus, the distribution of host plant species can affect the occurrence and dispersal of cicadas. We estimated both resource-weighted and organismweighted densities to determine the abundance of cicada species (Lewontin & Levins 1989; Begon et al. 2006). The resource-weighted density is the ratio of total population to total resource. However, the individuals are usually distributed unevenly in the resource, and the resource-weighted density may not reflect the density that typical individuals experience. Instead, in many cases, the resource consists of small patches within which individuals are uniformly distributed. The organismweighted density is the summation of the patch density for every individual divided by total population (Lewontin & Levins 1989). In essence, the organism-weighted density measures the intensity that an individual has to share its patch with other individuals. In this study, we investigated population densities of cicada species using enumeration of exuviae in three habitats in Korea: metropolitan, suburban, and country. If the host availability hypothesis is correct, the resourceweighted density of a cicada species should be high in habitats where available resource is abundant, whereas the organism-weighted density should be similar across habitats. The patch used to estimate organism-weighted density in this study was a tree. Thus, a difference in organism-weighted density between habitats may indicate that factors other than host availability may also contribute to densities of a species. We used percentage of trees without exuviae and percentage of the preferred trees as measures of resource for cicada juveniles. Methods Study species A mated female cicada lays eggs by stabbing her ovipositor inside the branch of a tree. The eggs hatch in the summer next year. The first-stage instars fall from the branch to the ground and go into the ground. They feed on the sap of the tree’s roots. Cicada larvae stay underground from 1 to 17 years, depending on species. The final-instar larvae make a tunnel to the surface and emerge from the ground. They climb the tree and molt on trunks, branches, or leaves.
There are 13 cicada species distributed on the Korean peninsula (Lee 2008). The morphology, life history, and distributions of all cicada species in Korea are well described (Lee 2005). In central Korean peninsula where this study was conducted, five species of the subfamily Cicadinae are typically found (Lee et al. 2012): Cryptotympana atrata Fabricius (Tribe Cryptotympanini), Hyalessa fuscata Distant (Tribe Sonatini), Graptopsaltria nigrofuscata Motschulsky (Tribe Polyneurini), Meimuna opalifera Walker (Tribe Cicadini), and Meimuna mongolica Distant (Tribe Cicadini). In this study, we combined M. opalifera and M. monoglica as Meimuna spp. for statistical analyses, because these two species were generally fewer than other species. Sampling localities Exuviae collection was conducted in three regions that differed in their degree of urbanization: metropolitan, suburban, and country. For the metropolitan habitat, we chose four localities in the city of Seoul, a city with a population of >10 million (Table 1). Seoul has limited forests, but has abundant high-rise buildings, roads, and residential complexes. The city of Gwacheon is a suburban, located south of Seoul. Because Gwacheon is surrounded by the Green Belt, a series of protected forests surrounding the capital region, development is restricted in the immediate vicinity. We chose four country localities in Gyeonggi Province surrounding Seoul: Yangpyeong, Pocheon, Gapyeong, and Yeoju. These country localities typically include large proportions of forested and agricultural areas. For replicates, we chose one to four sites within each locality for exuviae sampling. All sampling sites were located within a narrow latitudinal zone between 37°17′ and 37°54′ N. To limit bias in sample site selection, with respect to cicada species, we predetermined the sampling sites using Google map, selecting urbanized areas where landscaping trees typically occur. A sampling site was a contiguous area in which landscaping trees were planted. The sampling units for statistical analyses were the area of one such predetermined site and the trees included in that site, regardless of occurrence of cicada exuviae. Although we identified three habitat types for this study, landscape covers may be critical for cicada occurrence. Thus, to standardize the sampling localities across different habitat types, we restricted exuviae sampling to urbanized areas where landscaping trees were typically found, such as gardens of apartment complexes, schools, and parks. Thus, the immediate landscape surrounding sampling sites were quite similar across all three habitats. The standardization of landscapes surrounding samplings sites in all three localities were confirmed by the Geographic Information System (GIS) analysis. We analyzed the proportions of eight land cover types with radii
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Table 1. Sampling localities for the measurement of cicada density in this study. Habitat Metropolitan
Samsung Apgujeong Nonhyeon
Suburban
Daechi Jungang C1
Country
Jungang C7 Yangpyeong
Pocheon
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Site
Latitude (°N)
Longitude (°E)
Area (m2)
SS1 SS2 AG1 AG2 NH1 NH2 DC1 GC11 GC12 GC21 YP1 YP2 YP3 PC1 PC2 PC3 PC4 GP1 GP2 GP3 GP4 YJ1 YJ2 YJ3 YJ4
37°31′12″ 37°31′17″ 37°31′26″ 37°31′46″ 37°30′56″ 37°30′40″ 37°29′55″ 37°25′53″ 37°25′51″ 37°25′55″ 37°29′40″ 37°29′46″ 37°29′40″ 37°54′16″ 37°53′52″ 37°53′59″ 37°53′32″ 37°50′3″ 37°50′7″ 37°49′50″ 37°49′45″ 37°17′38″ 37°17′32″ 37°17′35″ 37°17′44″
127° 3′34.10″ 127° 3′44.35″ 127° 2′4.72″ 127° 1′57.39″ 127° 1′31.49″ 127° 0′37.81″ 127° 4′1.32″ 126°59′33.75″ 126°59′49.17″ 126°59′59.61″ 127°29′32.10″ 127°29′27.21″ 127°29′39.88″ 127°12′7.87″ 127°11′33.12″ 127°12′2.75″ 127°12′38.80″ 127°30′20.83″ 127°30′40.21″ 127°30′28.69″ 127°30′47.20″ 127°38′28.60″ 127°38′13.59″ 127°38′20.25″ 127°38′40.42″
1230 5825 7341 926 8203 1422 3673 1506 2015 4736 1813 3353 2532 13869 3380 1476 8213 3103 5085 3486 13261 13171 8039 1911 4339
Locality
Gapyeong
Yeoju
Note: All metropolitan localities are within the city of Seoul, and all suburban localities are within the city of Gwacheon, which is located south of Seoul. All country localities are found in the province of Gyeongi-do, which surrounds Seoul and Gwacheon.
of 100 m and 1000 m for each locality: city, road, agriculture, forest, grassland, wetland, wasteland, and water. GIS analysis was performed in ArcView™ (ESRI inc.; Redlands, CA, USA). The land cover data used in this analysis were from the Korean National Geographic Information Institute. The GIS analysis with 100 m radius showed that urban area dominated the landscape in all three habitats (Table 2). Agricultural field and forest occupied more than 23.1% of landscape in the country. However, the result of MANOVA showed that none of the three habitats differed in types of land cover in the 100 m radius (Wilk’s λ = 0.425;
F16,30 = 1.001, P = 0.481). With the 1000 m radius, the three habitats differed markedly in types of land cover (Table 2). Urban area was still dominant in the metropolitan habitat, with 65.2% of the total area being urban. In the suburban and country habitats, although the urban area still made up the largest percentages, forest area became increasingly common. In the country habitat, agricultural field composed a large percentage of the landscape. Accordingly, the results of MANOVA showed that habitat was a significant factor for differences in types of land cover when examined with a 1000-m radius (Wilk’s λ = 0.006; F16,30 = 21.466, P < 0.001). Thus, the sampling
Table 2. Percentages of land cover types for three habitats using the GIS analysis. Radius
Habitat
100 m
Metropolitan Suburban Country Metropolitan Suburban Country
1000 m
Urban 81.0 67.7 60.9 65.2 44.8 32.4
± ± ± ± ± ±
25.0 26.4 29.3 15.3 0.8 5.6
Road 13.1 1.0 6.5 14.7 11.7 6.0
±14.8 ± 1.4 ± 4.9 ± 1.5 ± 0.8 ± 2.1
Agriculture 0 1.5 10.2 0.1 4.9 22.4
± ± ± ± ± ±
0.0 2.6 14.0 0.3 1.9 5.6
Forest 0 9.5 11.9 1.3 27.4 22.4
± ± ± ± ± ±
0.0 13.5 23.9 1.5 1.4 11.1
Plain 4.8 7.4 8.6 5.1 8.6 8.8
± ± ± ± ± ±
11.2 5.3 13.2 4.7 1.0 4.5
Swamp 0.4 0 0 0.4 0.3 0
± ± ± ± ± ±
1.1 0.0 0.0 0.8 0.1 0.0
Empty 0.7 12.9 1.9 1.1 2.4 4.0
± ± ± ± ± ±
1.2 22.4 4.0 0.9 0.5 3.5
Watery
