Major Factors Affecting the Distribution of Anuran Communities in the Urban, Suburban and Rural Areas of Shanghai, China

Xiaoxiao SHU,Wei ZHANG, Ben LI, Enle PEI, Xiao YUAN, Tianhou WANG*and Zhenghuan WANG*

1School of Life Science, East China Normal University, Shanghai 200062, China

2Shanghai Landscaping and City Appearance Administrative Bureau, Shanghai 200040, China

Major Factors Affecting the Distribution of Anuran Communities in the Urban, Suburban and Rural Areas of Shanghai, China

Xiaoxiao SHU1,Wei ZHANG1, Ben LI1, Enle PEI2, Xiao YUAN2, Tianhou WANG1*and Zhenghuan WANG1*

1School of Life Science, East China Normal University, Shanghai 200062, China

2Shanghai Landscaping and City Appearance Administrative Bureau, Shanghai 200040, China

There is a dearth of information on the effects of landscape and microhabitat variables on the distribution of anurans in areas of rapid urban development, in both tropical and subtropical regions. Therefore, we studied 24 wetlands sites from the center of Shanghai city, China extending outward to rural areas. Sampling was performed from May through July 2014. Urbanization was categorized by the proportion of hard ground cover. Transect sampling and‘calling’ surveys were used to investigated the richness and density of anurans; microhabitat factors were recorded simultaneously. One-way analysis of variance and Kruskal–Wallis tests were conducted to analyze differences of total density, species richness and density of individual anuran species in the three urbanization levels; redundancy analysis was carried out on the relationship between anuran density and environmental variables. Species richness was lowest in the areas where the proportion of hard ground cover was ＞ 80%, and the total density of anurans was highest in the areas where coverage of the hard ground cover was ＜ 30%. We recorded fve species belonging to four genera and four families and an individual anuran species that had varied representations in urban environments. Beijing gold-striped pond frogs (Pelophylax plancyi) and Zhoushan toads (Bufo gargarizans) appeared to be well adapted to the Shanghai metropolis. Large water environments and aquatic vegetation (foating-leaves and emergent vegetation) were indicators of the presence of Beijing gold-striped pond frogs. The density of black-spotted pond frog (Pelophylax nigromaculatus) was at the lowest density in the areas where hard ground coverage was ＞ 80%, and tended to prefer larger bodies of water. Hong Kong rice-paddy frogs (Fejervarya multistriata) and ornamented pygmy frogs (Microhyla achatina) both suffered severely from cropland loss due to urban development. Bare land around breeding grounds was important for Hong Kong rice-paddy frogs, since it usually chooses mud coast caves for hibernation.

subtropical regions, rapid urbanization, amphibian, habitat variable, breeding seasons

1. Introduction

Anurans are indicator species of the health of wetland ecosystems (Guzy et al., 2012), and are facing worldwide decline. The speed at which this decline in species richness and abundance is occurring is faster than that of birds and mammals (Stuart et al., 2004). This downtrend has happened for many reasons, with urban development being recognized as one of the main causes.

Urban development changes land-use patterns, increasing impervious surface cover with the widespread development of buildings and extensive complex road networks (McDonnell et al., 1997; Collins et al. 2000; McKinney, 2002), resulting in the fragmentation and loss of vital habitats and habitat corridors (Czech et al., 2000; McKinney, 2002; Miller and Hobbs, 2002). Complex road systems also cause a high mortality of anurans (Hels and Buchwald, 2001; Mazerolle, 2004). Anurans usually form metapopulations in urban environments, therefore, habitat connectivity is vital to their survival (Brown and Kodric-Brown, 1977), as their ability to migrate is relatively poor. All the above urbanization factors have a negative influence on amphibian species richness and anuran migration (Vos and Chardon, 1998; Rubbo and Kiesecker, 2005; Pautasso, 2007; Pillsbury and Miller, 2008; Vignoli et al., 2009).

On a microhabitat scale, aquatic and terrestrial habitats are both necessary for anurans to complete their life cycle. Urbanization, however, has led to the degradation of a diverse range of suitable habitats (Dodd and Smith, 2003; Stevens and Paszkowski, 2004). The urban heat island effect which occurs in urban areas has caused an increase not only in atmospheric temperatures but also local water temperatures, resulting in increased mortality rates of amphibian eggs (Bornstein, 1968; McDonnell et al., 1993; Corn and Muths, 2002; Grimm et al., 2008). Urban water environments are prone to heavy metal pollution and natural water are at risk of contamination due to runoff from the wide application of chemical fertilizers and pesticides, threatening larval survival (Semlitsch, 2000; Paul and Meyer, 2001; Boone and Bridges, 2003; Rubbo and Kiesecker, 2005). The habitat characteristics of artificial wetlands, such as the presence of predator fish also negatively affect the survival of breeding amphibians (Orizaola and Bra?a, 2006).

Only 1% of the research related to organismal distribution across urbanization gradients relates to amphibians and reptiles (McDonnell and Hahs, 2008). Studies on the effect of rapid urbanization on anurans in tropical and subtropical regions are rare (Hamer and McDonnell, 2008). Nearly 40% of China’s wetlands are under moderate and serious threat (An et al., 2008). Forest and agricultural areas around cities are being quickly replaced by residential buildings, roads and other constraining features (Fazal, 2000; Liu et al., 2003; Yoon, 2009). Urbanization has developed rapidly in the past few decades in China (Liu et al.,2003), especially in Shanghai, which is located along the Yangtze River estuary and is a commercial and financial center of mainland China. The Shanghai region experienced rapid economic and population growth, from 1982 to 1990; the Shanghai downtown area increased from 149.85 km2to 279.78 km2and continued to expand to 377.56 km2after 2000 (Song, 2003). From 1989 to 2013, the population of Shanghai had an average annual growth rate of 0.89%. The population density has grown from 2013 persons/km2to 3809 persons/km2(Shanghai statistical yearbook, 1989–2013), making it the city with the highest population density and the fastest growing urban development in China (Wang et al., 2014). According to terrestrial wildlife resource surveys in Shanghai, three anuran species disappeared between 2000 and 2013. Dramatic urban development may be responsible for the decline and disappearance of these anuran species (Xie et al., 2002).

Our research selected Shanghai, the largest city with the fastest urbanization in China as the study area, and we investigated the distribution patterns and major infuential factors on the anuran community within each urbanization level (urban, suburban and rural) (Matson, 1990; McDonnell and Pickett, 1990), which has been commonly applied to studies of urbanization impacts on avian populations (Clergeau et al., 1998, 2006; Melles et al., 2003; Crooks et al., 2004; Vignoli et al., 2013). This awareness should help implement and support effective protection strategies for amphibians.

2. Materials and Methods

2.1 Study AreaThe research study area was located in the city of Shanghai, China, a recognized subtropical region, and an area undergoing accelerated urbanization. Urban expansion infrastructure needs to meet a myriad of developmental demands, including new housing, commercial buildings, transport infrastructure, etc. Most researchers use ‘land-use’ or ‘land-cover’ as criteria for determining urbanization gradients (McDonnell and Hahs, 2008). This research used the proportion of hard ground cover within 2 km of the sample plot to define urbanization levels (Marzluff et al., 2001). “Hard ground cover” included residential or commercial buildings, roads networks and other impermeable strata, and sites with values ＞ 80% were defned as urban areas, between 30%–80% as suburban areas and ＜ 30% as rural areas. In this study, 24 sites were chosen from the city center to the outer rural perimeter (Figure 1). Eight study sites were located within each urbanization level (urban, suburban and rural). Site selection was based on two principles; first, sites must be at least 1 km apart to control data independence and second, sites had to be classified as a permanent or semi-permanent pond to qualify for investigation and ensure reliable data collection.

2.2 Anuran SamplingDuring the breeding seasons, May through July 2014, transect sampling (Harris and Burnham, 2002), and calling surveys (Weir et al., 2009) were conducted to evaluate the population size. Due to variation in sample plot accessibility, sample transect lengths were not always consistent. The mean sample transect length was 1113 m (standard error SE: 126 m), with a transect width of 5 m. Surveys were conductedat least 0.5 h after sunset and completed by 00:00. Air temperatures ranged from 18.7 oC–26.5 oC and water temperatures between 22.1 oC–26.7 oC, with wind speeds below 5.8 m/s.

2.3 Landscape CharacteristicsIn general, anurans tend to have poor dispersal ability (Semlitsch, 2000; Smith and Green, 2005), based on their limited distribution potential. Therefore, landscape characteristics were quantified within 1 km radius of each sample plot using Google Earth Pro (version 6.2.2.6613), which included water and cropland coverage.

2.4 Breeding Habitat CharacteristicsAs microhabitat variables, we selected water depth, pH and water salinity, aquatic vegetation coverage (floating-leaves vegetaion, emergent vegetation and submerged vegetation), argillaceous bank coverage, slopes and bare land coverage within 2 m of the sample plot. Water depth was measured using a 1.5 m tape, and five water depths were taken within 1 m of the water’s edge (Hazell et al., 2004), to obtain an averaged value. The AZ8685 Pen Type pH meter and the AZ8371 handheld salinometer (Frank Electronics Co., Ltd., Shenzhen, China) were used to measure pH and water salinity at the water surface, approximately 30 cm from the water’s edge (Hazell et al., 2004; Rubbo and Kiesecker, 2005). Visual estimation was used to determine aquatic vegetation coverage (Price et al., 2005; Clark et al., 2007), argillaceous bank coverage and bare land coverage. The pond slope was measured using a geological compass. Data of breeding habitat variables were collected during anuran surveys.

2.5 Statistical AnalysesThe Kolmogorov–Smirnov test was used to determine whether total density, species richness and density of targeted anuran species were normally distributed. Data were converted by arcsine transformation in order to conform to a normal distribution with homogeneity of variance.

One-way analysis of variance (ANOVA) followed by a post-hoc Tukey’s multiple comparison test was used to deduce differences of the density of Beijing gold-striped pond frogs and Zhoushan toads along the urbanization gradient, because they conformed to the assumed parameters. However, Kruskal–Wallis test, followed by post-hoc pairwise comparison tests were used to analyze density differences of Black-spotted pond frogs, Hong Kong rice-paddy frogs and ornamented pygmy frogs in each urbanization level, because they did not conform the assumed parameters. We conducted this statistical analyses using SPSS version 20.0.

Detrended correspondence analysis (DCA) was used to analyze the data of species-sample,and the gradient lengths of axis 1 were 2.641＜3; therefore, we conducted a redundancy analysis (RDA) involving five species and environmental variables to determine which environmental variables were the major influencing factors in the distribution of individual anuran species at breeding sites. RDA is an extension of multiple linear regression (Dodkins et al., 2005), which is a simple method to elucidate the relationship between species and environmental variables. The statistical signifcance of the RDA was evaluated by Monte Carlo permutation tests. We conducted this statistical analyses in Canoco 4.5.

3. Results

3.1 Distribution of the Anuran Community in the Urban-Suburban-Rural AreasAnuran species richness was signifcantly lowest in the areas where hard ground coverage was ＞ 80% (F2,21=8.749, P=0.002), but there was no signifcant difference between rural and suburban areas (Table 1). The anuran total density was signifcantly increased with decreasing urbanization degree (F2,21=7.429, P=0.004), and reached its peak where hard ground coverage was ＜ 30% (rural areas), there was no signifcant difference between urban and suburban areas (Table 1).

Each anuran species was found to have its own individual responses to urbanization. The density of the Hong Kong rice-paddy frogs (Kruskal–Wallis test: χ2=15.398, df=2, P＜0.001) and ornamented pygmy frogs (Kruskal-Wallis test: χ2=6.530, df=2, P=0.038) was significantly different between the three urbanization levels (Table 1); the density of Hong Kong rice-paddy frogs increased with decreasing urbanization degree and ornamented pygmy frogs were not present in the urban areas. The density of Black-spotted pond frogs were signifcantly the lowest in the areas where coverage of the hard ground cover was ＞ 80% (urban areas) (Kruskal–Wallis test: χ2=6.935, df=2, P=0.031), but no signifcant difference was noted between the suburban and rural areas (Table 1).

The density of the Beijing gold-striped pond frogs (F2,21=3.419, P=0.052) and Zhoushan toads (F2,21=0.340, P=0.716) did not reveal a signifcant difference between three urbanization levels (Table 1).

3.2 Factors Underlying Anuran Community DistributionIn the RDA analyses, the four axis explained 60.7% of the species variation. The percent of explained variation for the frst and second axis of RDA was 35.7% and 15.0%, respectively. Correlation betweenenvironmental variables, ordering axis and species variable ordering axis was 0.922 and 0.894, respectively (Table 2). According to Monte Carlo permutation tests of the RDA, explained variation of the first canonical axis had a significant effect on species (F=6.657, P=0.018), and all canonical axis was also have signifcant (F=1.773, P=0.039).

Water coverage, cropland coverage, emerged vegetation coverage and bare land coverage were significantly correlated to the first axis (Table 3, Figure 2), these environmental variables increased along the axis one from left to right; water coverage and bare land coverage were signifcantly correlated to the second axis (Table 3, Figure 2), and water coverage was increased along axis two from the bottom up; however, bare land was decreased along axis two from the bottom up.

Our results indicated that anurans had species-specifc requirements for habitat conditions and resources. The result of RDA shows that Black-spotted pond frogs were significantly positively associated with water coverage (Table 4, Figure 2), Beijing gold-striped pond frogs were positively associated with water coverage and aquatic vegetation coverage including floating-leaves and emerged vegetation (Table 4, Figure 2), cropland coverage and bare land coverage had signifcant infuence on the density of Hong Kong rice-paddy frogs (Table 4, Figure 2), and only cropland coverage had a signifcantly relationship with Ornamented pygmy frogs (Table 4, Figure 2). RDA analysis did not show any variable that significantly influenced the distribution of Zhoushan toads.

4. Discussion

This study found that a high level of urbanization has a negative effect on density and distribution of local anurans (Table 1); similar findings have been reported in other localities (Shirose et al. 2000; MacGregor-Fors et al., 2013). As urbanization levels increased, species richness decreased, and total species density reached a minimum where hard ground cover was ＞80%. Urbanization reduces habitat availability for anurans, and the decreased species richness in urban wetlands was attributable to the rarity of Hong Kong rice-paddy frogs and Ornamented pygmy frogs, which prefer cropland habitat (Table 4), we hypothesize that the disappearance of cropland habitat is the main reason for decline in species richness urban areas.

Figure 1 Location of study sites in Shanghai. The People’s square in Shanghai was served as the urban center in this study.

Figure 2 First and second axis of the RDA involving anuran species and environmental variables in Shanghai, Environmental variables (arrows) are: Water Coverage (WaterCov); Cropland Coverage (Cropland); Water depth (WaterDe); Slope; Water PH; Water salinity (WaterSa); Floating-leaves vegetation Coverage (FLVC); Emergent vegetation Coverage (EVC); Submerged vegetation Coverage (SVC); Argillaceous bank Coverage (Argillac); Bare land (Bare Lan). Species (acronyms) are: Black-spotted pond frog (BSPF); Beijing gold-strip pond frog (BGSPF); Hong Kong rice-paddy frog (HKRF); Ornamented pygmy frog (OPF); Zhoushan toad (ZT).

Individual anuran species have different responses to urbanization, and the infuence of urbanization on anurans is highly associated with the life history of the species and their sensitivity to environmental changes (Garden et al., 2006). Decreasing cropland coverage is the main limiting factor affecting the distribution of Hong Kong rice-paddy frogs and Ornamented pygmy frogs in the three urbanization levels (Table 4). This is consistent with the dispersal-dependent-decline hypothesis that

sedentary species can be extremely sensitive to habitat loss and habitat degradation, and paddy-associated frogs are sensitive to the loss of cropland habitats (Tsuji et al., 2011). From our research alone, it has been demonstrated that the rapid development of urban infrastructure and shrinkage of cropland reduce the optimum habitat of the Hong Kong rice-paddy frogs and ornamented pygmy frogs, causing their populations to undergo a dramatic decline. These may eventually become the first two threatened anuran species in the next decade. deMaynadier and Hunter (1999) showed that high-density vegetation growing on the edge of wetlands can provide food, shelter and migration and overwintering sites. However, bare land plays an important role in the survival of the Hong Kong rice-paddy frog (Table 4), since it can provide mud caves for hibernation sites (Wang et al., 2008). In the feld, we also observed that frogs hide in the mud caves when threatened.

Table 1 Species richness and anuran density in the three urbanization levels.

Table 2 Statistical characteristics of four ordination axis of the RDA.

Table 3 Correlation coeffcients between environmental variation and RDA ordination axis.

Table 4 Correlation coeffcients between environmental variables and fve anurans species.

High levels of urbanization hindered the distribution of the Black-spotted pond frog, and reduce their density. However, different from a similar study in Osaka-kobe (Japan) (Tsuji et al., 2011), our research noted that in Shanghai, the density and distribution of the Blackspotted pond frog was restricted by the size of the water area, which is important for their reproduction and larval development (Vignoli et al., 2009). Farmland ecosystems become restrictive habitat factors for the survival of Black-spotted pond frog in Osaka-Kobe (Tsuji et al., 2011). Differences in habitat selection may be associated with the different urban development patterns and local agricultural practices. Osaka-Kobe is a metropolitan area with paddy fields widely distributed in rural and urban zones (Tsuji et al., 2011), but the urbanization development of Shanghai is mainly diffused outward in a circular confguration, with no paddy felds in the interior urban environment. Different urbanization development models may contribute to different urbanization pressures on the same anurans, and Black-spotted pond frogs may change its habitat preferences in order to adapt to these different environmental stresses.

It has been reported that some anurans can adapt to urbanization (Rubbo and Kiesecker, 2005; Tsuji et al., 2011). According to our research, rapid urbanization has had little effect on the density and distribution of the Beijing gold-striped pond frogs and Zhoushan toads (Table 1). The Beijing gold-striped pond frog tended to choose a wetland ecosystem with abundant foating-leaves vegetation, such as water lilies (Nymphaea odorata) and duckweed (Spirodela polyrhiza). Emergent vegetation, such as the lotus fower (Nelumbo nucifera) and bulrush (Phragmites communis) were also potential indicators for the presence of the frog (Table 4). Aquatic vegetation is also a good indicator for in predicting anuran occurrence and larvae survival of North American amphibians (Skidds et al., 2007; Purrenhage and Boone, 2009), The density of aquatic vegetation affects all life-cycle stages of Beijing gold-striped pond frogs, providing shelter for larvae, spawning sites for adults and can also be used as a platform for resting and breathing (Egan and Paton, 2004; Skidds et al., 2007; Scheffers and Paszkowski, 2013). In addition, large-area water environmental play an important role in the reproduction and migration of Beijing gold-striped pond frogs.

5. Conservation Implications

Our research noted that highly urbanized areas have significant negative effects on the survival of some anurans, and a reasonable collocation of a variety of habitat characteristics which were benefcial to the frogs complete life history are critical for anurans conservation (Garcia-Gonzalez and Garcia-Vazquez, 2012).

According to our research, the survival of the Hong Kong rice-paddy frogs and Ornamented pygmy frogs was dependent on cropland habitat. Retaining this essential habitat is a critical conservation measures for these two anurans. In addition, terrestrial habitats such as reserves of bare land around artifcial wetlands are also important, as they can provide hibernation sites and shelter for Hong Kong rice-paddy frogs.

Large-area wetland ecosystems are more productive for the conservation of the Black-spotted pond frogs and Beijing gold-striped pond frog. The question of whether large ponds should be constructed or multiple small ponds interconnected to form a larger integrated water network is still a topic to be discussed and requires further research.

Ponds in urban areas attract visitors and allow for recreation, but also play an important role in the urban ecosystem and have irreplaceable ecological functions in the conservation of urban anurans (Shirose et al., 2000), providing an alternative permanent habitat for urban adaption. Carrier and Beebee (2003) noted that British urban and suburban areas with many good quality ponds provide excellent conditions for the common frogs (Rana temporaria). Maintaining floating-leaves vegetation and emergent vegetation in the urban ponds or establishing aquatic vegetation buffer strips along the shoreline of large lakes would be effective methods for towards the conservation of Beijing gold-striped pond frogs.

AcknowledgmentsWe thank T. WU for his guidance in sample region mapping. We appreciate the cooperation of the various urban park managers. This project was fully supported by research funding and permits from Shanghai Landscaping and City Appearance Administrative Bureau (Grant No. F131508).

An N., Gao N. Y., Liu C. E. 2008. Wetland degradation in China: Causes, evaluation, and protection measures. Chin J Ecol, 27: 821–828

Brown J. H., Kodric-Brown A. 1977. Turnover rates in insular biogeography: Effect of immigration on extinction. Ecology, 58: 445–449

Boone M. D., Bridges C. M. 2003. Effects of pesticides on amphibian populations. In Semlitsch R. D. (Ed.), Amphibian Conservation. Smithsonian Institution, Washington, DC, 152–167

Bengtsson G., Tranvik L. 1989. Critical metal concentrations for forest soil invertebrates. Water Air Soil Pollut, 47: 381–417

Czech B., Paul R. K., Patrick K. D. 2000. Economic Associations among Causes of Species Endangerment in the United States refect the integration of economic sectors, supporting the theory and evidence that economic growth proceeds at the competitive exclusion of nonhuman species in the aggregate. BioScience, 50: 593–601

Carrier J. A., Beebee T. J. C. 2003. Recent, substantial, and unexplained declines of the common toad Bufo bufo in lowland England. Biol Conserv, 111: 395–399

Clark P. J., Reed J. M., Tavernia B. G., Windmiller B. S., Regosin J. V. 2008. Urbanization effects on spotted salamander and wood frog presence and abundance for the study of amphibians and reptiles. University of Waterloo

Corn P. S., Muths E. 2002. Variable breeding phenology affects the exposure of amphibian embryos to ultraviolet radiation. Ecology, 83: 2958–2963

Collins J. P., Kinzig A., Grimm N. B., Fagan W. F., Hope D., Wu J. 2000. A new urban ecology. Am Sci, 88: 416–425

Clergeau P., Savard J. P. L., Mennechez G., Falardeau G. 1998. Bird abundance and diversity along an urban–rural gradient: A comparative study between two cities on different continents. Condor, 100: 413–425

Clergeau P., Croci S., Jokim?ki, J., Kaisanlahti-Jokim?ki, M. L., Dinetti M. 2006. Avifauna homogenisation by urbanisation: Analysis at different European latitudes. Biol Conserv, 127: 336–344

Crooks K. R., Suarez A. V., Bolger D. T. 2004. Avian assemblages along a gradient of urbanization in a highly fragmented landscape. Biol Conserv, 115: 451–462

deMaynadier P. G., Hunter M. L. 1999. Forest canopy closure and juvenile emigration by pool-breeding amphibians in Maine. J Wildl Manage, 63: 441–450

Dodd C. K., Smith L. L. 2003. Habitat destruction and alteration. Amphibian Conservation. Smithsonian Institution, Washington, 94–112

Dodkins I., Rippey B., Hale P. 2005. An application of canonical correspondence analysis for developing ecological quality assessment metrics for river macrophytes. Freshwater Biol, 50: 891–904

Egan R. S., Paton P. W. C. 2004. Within-pond parameters affecting oviposition by wood frogs and spotted salamanders. Wetlands, 24: 1–13

Fazal S. 2000. Urban expansion and loss of agricultural land-a GIS based study of Saharanpur City, India. Environ Urban, 12: 133–149

Grimm N. B., Faeth S. H., Golubiewski N. E., Redman C. L., Wu J., Bai X., Briggs J. M. 2008. Global change and the ecology of cities. Science, 319: 756–760

Garden J., Mcalpine C., Peterson A. N. N., Jones D., Possingham H. 2006. Review of the ecology of Australian urban fauna: a focus on spatially explicit processes. Austral Ecol, 31: 126–148

Garcia-Gonzalez C., Garcia-Vazquez E. 2012. Urban ponds, neglected Noah’s ark for amphibians. J Herpetol, 46: 507–514

Guzy J. C., Mccoy E. D., Deyle A. C., Gonzalez S. M., Halstead N., Mushinsky H. R. 2012. Urbanization interferes with the use of amphibians as indicators of ecological integrity of wetlands. J Appl Ecol, 49: 941–952

Hazell D., Hero K., Lindenmayer D., Cunningham R. 2004. A comparison of constructed and natural habitat for frog conservation in an Australian agricultural landscape. Biol Conserv, 119: 61–71

Hamer A. J., McDonnell M. J. 2008. Amphibian ecology and conservation in the urbanising world: A review. Biol Conserv, 141: 2432–2449

Hels T., Buchwald E. 2001. The effect of road kills on amphibian populations. Biol Conserv, 99: 331–340

Harris R. B., Burnham K. P. 2002. On estimating wildlife densities from line tramsect data. Curr Zool, 48: 812–818

Internet reference. Shanghai statistical yearbook, density of population 1989–2013. Retrieved from:

http://#cnki.net/kns55/navi/result.aspx?id=N2010040188&fle =N2010040188000080&foor=1

http://#cnki.net/kns55/navi/result.aspx?id=N2014090171&fle =N2014090171000021&foor=1

Liu J. Y., Liu M. L., Zhuang D. F., Zhang Z. X., Deng X. Z. 2003. Study on spatial pattern of land-use change in China during 1995–2000. Science in China Series D: Earth Sci, 46: 373–384

McKinney M. L. 2002, Urbanization, Biodiversity, and Conservation The impacts of urbanization on native species are poorly studied, but educating a highly urbanized human population about these impacts can greatly improve species conservation in all ecosystems. BioScience, 52: 883–890

Marzluff J. M., Bowman R., Donnelly R. 2001. A historical perspective on urban bird research: trends, terms, and approaches. Avian ecology and conservation in an urbanizing world. New York: Springer, 1–17

Miller J. R., Hobbs R. J. 2002. Conservation where people live and work. Conserv Biol, 16: 330–337

Mazerolle M. J. 2004. Amphibian road mortality in response to nightly variations in traffc intensity. Herpetologica, 60: 45–53

McDonnell M. J., Pickett S. T. A., Pouyat R. V. 1993. The application of the ecological gradient paradigm to the study of urban effects. Humans as components of ecosystems. New York:Springer, 175–189

MacGregor-Fors I., Ordo?ez O. H., Ortega-álvarez R. 2013. Urban croaking: Diversity and distribution of anurans in a neotropical city. Urban Ecosyst, 16: 389–396

Matson P. 1990. The use of urban gradients in ecological studies. Ecology, 71: 1231

McDonnell M. J., Hahs A. K. 2008. The use of gradient analysis studies in advancing our understanding of the ecology of urbanizing landscapes: Current status and future directions. Land Ecol, 23: 1143–1155

McDonnell M. J., Pickett S. T. A. 1990. The study of ecosystem structure and function along urban-rural gradients: An unexploited opportunity for Ecology. Ecology, 71: 1232–1237

McDonnell M. J., Pickett S. T. A., Groffman P., Bohlen P., Pouyat R. V., Zipperer W. C., Parmelee R. V., Carreiro M. M., Medley K. 1997. Ecosystem processes along an urban-rural gradient. Urban Ecosys, 1: 21–36

Melles S., Glenn S., Martin K. 2003. Urban bird diversity and landscape complexity. Species-environment associations along a multiscale habitat gradient. Conserv Ecol, 7: 271–279

Orizaola G., Bra?a F. 2006. Effect of salmonid introduction and other environmental characteristics on amphibian distribution and abundance in mountain lakes of northern spain. Anim Conserv, 9: 171–178

Pautasso M. 2007. Scale dependence of the correlation between human population presence and vertebrate and plant species richness. Ecol Lett, 10: 16–24

Porej D., Hetherington T. E. 2005. Designing wetlands for amphibians: The importance of predatory fish and shallow littoral zones in structuring of amphibian communities. Wetl Ecol Manag, 13: 445–455

Petranka J. W., Harp E. M., Holbrook C. T., Hamel J. A. 2007. Long-term persistence of amphibian populations in a restored wetland complex. Biol Conserv, 138: 371–380

Purrenhage J. L., Boone M. D. 2009. Amphibian community response to variation in habitat structure and competitor density. Herpetologica, 65: 14–30

Price S. J., Marks D. R., Howe R. W., Hanowski J. A. M., Niemi G. J. 2005. The importance of spatial scale for conservation and assessment of anuran populations in coastal wetlands of the western great lakes, USA. Landscape Ecol, 20: 441–454

Pillsbury F. C., Miller J. R. 2008. Habitat and landscape characteristics underlying anuran community structure along an urban-rural gradient. Ecol Appl, 18: 1107–1118

Paul M. J., Meyer J. L. 2001. Streams in the urban landscape. Annu Rev Ecol Syst, 32: 333–365

Rubbo M. J., Kiesecker J. M. 2005. Amphibian breeding distribution in an urbanized landscape. Conserv Biol, 19: 504–511

Stuart S. N., Chanson J. S., Cox N., Young B. E., Rodrigues A. S. L., Fischman D. L., Waller R. W. 2004. Status and trends of amphibian declines and extinctions worldwide. Science, 306: 1783–1786

Semlitsch R. D. 2000. Principles for management of aquaticbreeding amphibians. J Wildl Manage, 64: 5–31

Stevens C. E., Paszkowski C. A. 2004. Using chorus-size ranks from call surveys to estimate reproductive activity of the wood frog (Rana sylvatica). J Herpetol, 38: 404–410

Scheffers B. R., Paszkowski C. A. 2013. Amphibian use of urban stormwater wetlands: The role of natural habitat features. Landscape Urban Plan, 113: 139–149

Skidds D. E., Mitchell J. C. 2007. Habitat correlates of reproductive effort in wood frogs and spotted salamanders in an urbanizing watershed. J Herpetol, 41: 439–450

Shirose L., Dunn L., Barton D. R., Struger J., Bishop C. A., Shepherd D., Lang A. L. 2000. Contamination and wildlife communities in stormwater detention ponds in Guelph and the Greater Toronto Area, Ontario, 1997 and 1998, Part 1. Wildlife communities. Water Qual Res J Can, 35: 399–435

Smith A. M., Green D. M. 2005. Dispersal and the metapopulation paradigm in amphibian ecology and conservation: Are all amphibian populations metapopulations? Ecography, 28: 110–128

Song B. S. 2003. Urbanization, Suburbanization and Social Reconstruction–A Case Study of Shanghai. J East China Norm Univ (Philos Soc Sci), 35: 97–104

Tsuji M., Ushimaru A., Osawa T., Mitsuhashi H. 2011.Paddyassociated frog declines via urbanization: A test of the dispersaldependent-decline hypothesis. Landscape Urban Plan, 103: 318–325

Vasconcelos D., Calhoun A. J. K. 2006. Monitoring created seasonal pools for functional success: A six-year case study of amphibian responses, Sears Island, Maine, USA. Wetlands, 26: 992–1003

Vos C. C., Chardon J. P. 1998. Effects of habitat fragmentation and road density on the distribution pattern of the moor frog Rana arvalis. J Appl Ecol, 44–56

Vignoli L., Mocaer I., Luiselli L., Bologna M. A. 2009. Can a large metropolis sustain complex herpetofauna communities? An analysis of green space areas suitability in Rome, Anim Conserv, 12: 456–466

Vignoli L., Scirè S., Bologna M. A. 2013. Rural–urban gradient and land use in a millenary metropolis: How urbanization affects avian functional groups and the role of old villas in bird assemblage patterning. Web Ecol, 13: 49–67

Weir L. A., Fiske I. J., Royle J. A. 2009. Trends in Anuran Occupancy From Northem States of the Ametic: An Amphibian Monitoring Program. Herpetol Conserv Biol, 4: 389–402

Wang J. L., Xue W. J., Li N. B., Wang X. L., Jiang H. R., Xu H. F. 2008. Hibernation of Rana limnocharis in Shanghai farmland. Chin J Ecol, 10: 1289–1291

Wang Z., Zhou H. W., Chen G. Z., Gao H. 2014. Countermeasure to Control Shanghai Population Scale with Fast Growth Effectively. J Soc Sci, 2: 56–65

Xie Y. M., Huang Z. Y., Du D. C., Qin X. K., Ma J. F., Yu K., Yu W. D., Xu H. F. 2002. Shanghai terrestrial wildlife resources investigation report. Shanghai Municipal Forestry Administration

Yoon C. G. 2009. Wise use of paddy rice fields to partially compensate for the loss of natural wetlands. Paddy Water Environ, 7: 357–366

*Corresponding authors: Prof. Tianhou WANG, from East China Normal University, Shanghai, China, with his research focusing on wetland ecology and conservation biology; Dr. Zhenghuan WANG, from East China Normal University, Shanghai, China, with his research focusing on urban ecology and wildlife biology.

E-mail: thwang@bio.ecnu.edu.cn (Tianhou WANG); zhwang@bio.ecnu. edu.cn (Zhenghuan WANG)

Received: 26 November 2015 Accepted: 14 January 2016