sustainability

Article Response of Ground (Coleoptera: Carabidae) Communities to Effect of Urbanization in Southern Osaka: An Analytical Approach Using GIS

Jin-Wook Park 1 and Cheol Min Lee 2,*

1 Department of Landscape Architecture, Daegu Catholic University, 13-13 Hayang-ro, Hayang-eup, Gyeongsan-si, Daegu 38430, Korea; [email protected] 2 California Department of Food and Agriculture, 2710 Gateway Oaks Drive, Sacramento, CA 95833, USA * Correspondence: [email protected]; Tel.: +1-714-580-2234

Abstract: Urbanization involves the profound alteration of original habitats and causes habitat loss and biodiversity decline. This study aims to clarify the response of communities to the effect of urbanization in southern Osaka, Japan. In total, 2950 individuals from 53 species of ground beetle were collected in nine urban green areas. The categories of land use regarding the study sites were determined based on GIS data. The community index was not significantly different between areas. Urban areas and roads in land use mainly have a negative influence on ground . Paddies, fields, parks and green spaces, and open space were positively correlated with species richness of forest species and large-sized species, and open space was positively correlated   with species richness and the density of open land species. However, ground beetle communities in different areas of varying sizes did not group separately. These results suggest that changes in Citation: Park, J.-W.; Lee, C.M. paddies, fields, parks and green spaces, forests, and open space associated with the expanding urban Response of Ground Beetle area and road greatly influenced species composition, and the community structure remained similar. (Coleoptera: Carabidae) Communities to Effect of Urbanization in Southern Keywords: ground beetle; urbanization; land use; urban green area; GIS Osaka: An Analytical Approach Using GIS. Sustainability 2021, 13, 7134. https://doi.org/10.3390/ su13137134 1. Introduction Academic Editors: Volker Mauerhofer Urbanization drives global environmental changes and is one of the major anthro- and Ranjay K. Singh pogenic activities that impacts biodiversity and ecosystem processes [1–3]. Currently, 55% of the global human population lives in urban areas, and this trend is expected to continue Received: 2 May 2021 in the coming decades [4]. Urbanization has a significant impact on abiotic and biotic Accepted: 22 June 2021 factors in nature and leads to substantial changes in natural habitats with profound effects Published: 25 June 2021 on wildlife and their activity pattern, spatial distribution, phenology, productivity, and biotic interactions [5–7]. The diversity and community structure of wildlife will change Publisher’s Note: MDPI stays neutral significantly in urban habitats compared with rural ones [3,8–10]. with regard to jurisdictional claims in Ground beetles are useful bio-indicators because they are sufficiently varied both published maps and institutional affil- taxonomically and ecologically, abundant, and sensitive to the anthropogenic effect [11,12]. iations. Urbanization has a huge effect at various levels of the biological organization on ground beetles in urban habitats [13]. Ground beetles with large body sizes, predatory feeding habits, strict forest habitat requirements, and poor dispersal ability were most sensitive to urbanization [6]. Many studies have been conducted to clarify the relationships be- Copyright: © 2021 by the authors. tween ground beetle diversity and the effect of urbanization according to the urban–rural Licensee MDPI, Basel, Switzerland. gradient [8,14,15]. This article is an open access article There is a need for studies on the responses of ground beetle communities according distributed under the terms and to different areas and land use. To our knowledge, this is the first study to clarify the conditions of the Creative Commons response of ground beetles to the effect of urbanization using the GIS method. This study Attribution (CC BY) license (https:// was carried out in nine urban green areas in southern Osaka. We tested the following creativecommons.org/licenses/by/ questions: (1) How does the ground beetle community respond according to the area and 4.0/).

Sustainability 2021, 13, 7134. https://doi.org/10.3390/su13137134 https://www.mdpi.com/journal/sustainability Sustainability 2021, 13, x 2 of 13

Sustainability 2021, 13, 7134 response of ground beetles to the effect of urbanization using the GIS method. This2 study of 13 was carried out in nine urban green areas in southern Osaka. We tested the following questions: (1) How does the ground beetle community respond according to the area and landland use? use? (2) (2) Which Which species species are are more more vulnerable vulnerable to to the the effect effect of of urbanization? urbanization? (3) (3) Which Which environmentalenvironmental factorsfactors influenceinfluence positively,positively, or or negatively, negatively, the the ground ground beetle beetle community? community? Finally,Finally, we we propose propose an an alternative alternative to to improve improve ground ground beetle beetle diversity diversity in in urban urban areas. areas.

2.2. Materials Materials and and Methods Methods 2.1.2.1. Study Study Sites Sites OsakaOsaka Prefecture Prefecture is is the the second second largest largest metropolitan metropolitan area area in Japan, in Japan, and its and area its is area about is 2 1905about km 1905and km the2 and population the population is about is about 8.8 million 8.8 millio as ofn as April of April 2021. 2021. Osaka Osaka Prefecture Prefecture is surroundedis surrounded by by Mt. Mt. Izumikatsuragi, Izumikatsuragi, Mt. Mt. Iwawaki, Iwawaki, Mt. Mt. Kongo, Kongo, Mt. Mt. Iwahashiyama, Iwahashiyama, and and Mt.Mt. Ikoma.Ikoma. Yodo Yodo River River and and Yamato Yamato River River flow flow through through Osaka. Osaka. Many Many areas areas in inOsaka Osaka are arecomprised comprised of houses, of houses, apartments, apartments, and andother other buildings buildings (Figure (Figure 1). However,1). However, Osaka Osaka Prefec- Prefectureture has remnant has remnant forests forests between between mountain mountain areas and areas flatland and flatland areas, and areas, paddy and fields paddy in fieldssuburban in suburban areas. There areas. are Therealso large are urban also large green urban areas, green such as areas, urban such parks, as urbanurban forests, parks, urbantemples, forests, shrines, temples, university shrines, campuses, university etc. campuses, Urban green etc. areas Urban have green been areas fragmented have been by fragmentedurban areas by and urban separated areas and from separated other surroun from otherding surroundingnatural areas. natural However, areas. urban However, green urbanareas greenplay an areas important play an role important in maintaining role in maintainingwater and air water quality, and providing air quality, wildlife providing hab- wildlifeitat, and habitat, supporting and supportingmeta-populations meta-populations of regional offlora regional and fauna, flora andas well fauna, as recreational as well as recreationalareas for human areas forwellbeing human [2,16,17]. wellbeing The [2,16 urba,17].n Thegreen urban areas green should areas be shouldproperly be evaluated properly evaluatedto maintain to maintaintheir ecological their ecological value in the value urban in the ecosystem. urban ecosystem.

FigureFigure 1. 1.Map Map of of study study area. area.

WeWe chose chose nine nine urban urban green green areas areas in in southern southern Osaka Osaka (Figure (Figure2). 2) Suzunomiya. Suzunomiya park park (SU),(SU), Chayama Chayama parkpark (CH),(CH), Niwasiro park park (NI) (NI),, and and Kouzen Kouzen park park (KO) (KO) are are surrounded surrounded by byresidential residential areas, areas, apartment apartment complexes, complexes, and and roads. roads. Izumigaokaryokuchi Izumigaokaryokuchi (IZ), (IZ), Kurotori- Kuro- toriyamayama park park (KU), (KU), and and Koumyouike Koumyouike park park (KM) (KM) are are partially partially connected connected to naturalnatural habitats.habitats. TakasagoTakasago park park (TA) (TA) and and Umitonohureaihiroba Umitonohureaihiroba (UM) (UM) are are located located in in landfill landfill areas. areas. The The de-de- tailedtailed informationinformation ofof eacheach sitesite is is included included in in Table Table1. 1. The The nine nine urban urban green green areas areas were were classifiedclassified intointo threethree groupsgroups based on size: size: small small area area (<5 (<5 ha), ha), medium medium area area (>5 (>5 ha haand and <15 <15ha), ha), and and large large area area (>15 (>15 ha). ha).

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Figure 2. MapFigure of the 2. studyMap of sites. the SU:study Suzunomiya sites. SU: Suzunomiya park, CH: Chayama park, CH: park, Chayama TA: Takasago park, TA: park, Takasago IZ: Izumigaokaryokuchi, park, NI: NiwasiroIZ: park, Izumigaokaryokuchi, KU: Kurotoriyama NI: park, Niwasiro UM: Umitonohureaihiroba, park, KU: Kurotoriyama KO: park, Kouzen UM: park, Umitonohureaihiroba, KM: Koumyouike park. KO: Kouzen park, KM: Koumyouike park. 2.2. Survey and Ground Beetle Identification 2.2. Survey and Ground Beetle Identification The survey was carried out 18 times from April to December 2007 using pitfall traps in The surveynine was urban carried green out areas 18 times in southern from April Osaka. to December A plastic cup2007 (diameter using pitfall 7 cm, traps depth 10 cm) was in nine urban usedgreen to areas make ina southern trap without Osaka. using A plastic any bait, cup and (diameter five holes 7 cm, were depth made 10 to cm) avoid rainwater. was used to makeTen trapsa trap were without set 5 using m apart any in bait, a straight and five line holes in the were grassland made areato avoid and rain- another 10 traps in water. Ten trapsthe were forest set area 5 m for apart 7 days in ata straight each site. line As in some the grassland traps were area lost duringand another the survey 10 period, 346, traps in the forest321, area 357, 333,for 7 297, days 342, at each 345, 307,site. andAs some 297 traps traps were were collected lost during from the SU survey to KM, respectively. period, 346, 321,The 357, ground 333, 297, beetle 342, specimens 345, 307, and were 297 identified traps were using collected taxonomic from SU keys to [KM,18] to the level of respectively. Thespecies ground under beetle a stereoscopic specimens microscope. were identified using taxonomic keys [18] to the level of species under a stereoscopic microscope. 2.3. Body Size and Habitat Type 2.3. Body Size and HabitatThe body Type size of ground beetles was grouped into three size classes: small (<10.0 mm), The bodymedium size of ground (11.0–20.0 beetles mm), was and grouped large (>21.0 into mm)three basedsize classes: on Ueno small et al.(<10.0 [18]. In terms of mm), mediumhabitat (11.0–20.0 type, mm), the and ground large beetles (>21.0 weremm) classifiedbased on Ueno into twoet al. groups [18]. In based terms on of their location habitat type, thewhen ground collected. beetles Forest were species classifi wereed into mainly two groups recorded based in forests on their such location as broadleaf forests, when collected.pine Forest forests, species urban were forests, mainly and re secondarycorded in forests,forests whereassuch as broadleaf open land forests, species were mainly pine forests, urbanrecorded forests, on and riverbanks, secondary paddy forests, fields, whereas urban open green land areas, species and were urban mainly parks. If a species recorded on riverbanks,was recorded paddy in morefields, than urban one green habitat, areas, the and habitat urban where parks. the If a species species was was more frequent recorded in morewas than used. one Habitat habitat, type the was habitat determined where the based species on Ueno waset more al. [18 frequent], Lee [19 was], and Lake Biwa used. Habitat Museumtype was [20determined]. based on Ueno et al. [18], Lee [19], and Lake Biwa Museum [20]. 2.4. Land Use Analysis 2.4. Land Use AnalysisThe land use data were collected from a 1:5000 scale map published in 2001 by the The land Geospatialuse data were Information collected Authority from a 1:5000 of Japan. scale The map patterns published of the in surrounding2001 by the environment of survey routes in nine urban green areas were analyzed using GIS. There is no standard Geospatial Information Authority of Japan. The patterns of the surrounding environment method or previous study that suggested an appropriate radius for considering the influ- of survey routes in nine urban green areas were analyzed using GIS. There is no standard ence of urbanization on ground beetle communities. A 1 km radius in the urban green method or previous study that suggested an appropriate radius for considering the influ- areas in southern Osaka included some natural habitats. A previous study suggested that ence of urbanization on ground beetle communities. A 1 km radius in the urban green a circle of 500 m radius was appropriate for considering the impact of urbanization on areas in southern Osaka included some natural habitats. A previous study suggested that ground [21]. The land use was classified into ten categories: paddy, field, park a circle of 500 m radius was appropriate for considering the impact of urbanization on and green space, forest, urban area, road, open space, river and pond, sea, and others. Sustainability 2021, 13, 7134 4 of 13

Table 1. Summary of study sites.

Coordinates Main Plants Study Site Acronym Year Area (ha) Cho/Dai/ City Facility Remark Latitude Longitude Subsite 1 Subsite 2 Machi

Lawn area around Near to SU 34.5284 135.4804 1976 Small Q. glauca grove deciduous trees such as Hatadaimyou Suzunomiya park (1.4) C. sinensis var, japonica, Hatanishimachi Sakai Playground and Ligustrum japonicum temple Lawn area near Chayama Small deciduous trees such as Surrounded by CH 34.4889 135.5186 1982 Q. glauca grove Chayamadai Sakai Playground park (4.4) L. tulipifera and Triadica residential areas sebifera Grassland area where the Takasago Around deciduous trees majority of herbs were TA 34.5379 135.4063 1979 Small such as Rhaphiolepis Takaishi Baseball landfill area park (4.8) indica var. umbellate Desmodium paniculatum ground and Hypochaeris radicata Secondary forest where Grassland where the majority of herbs were S. Izumigaokaryokuchi IZ 34.5029 135.5304 1982 Medium the majority of trees were Ueno Sakai Connected to (5.3) Q. serrata and Q. canadensis var. scabra and natural forests acutissima Juncus tenuis Lawn area near Niwasiro Around deciduous trees deciduous trees such as Surrounded by NI 34.4742 135.4975 1982 Medium such as Myrica rubra and Niwasirodai Sakai Baseball park (6.9) Albizia julibrissin and ground residential areas Q. glauca Ulmus parvifolia Around a secondary Partially Kurotoriyama surrounded by KU 34.4866 135.4438 1960 Medium forest where the majority Lawn area near a lake Kurotoricho Izumi Playground park (7.2) of trees were Q. serrata paddy fields and and Q. acutissima crop fields Grassland area where the Large Around a colony of majority of herbs were Landfill area Umitonohureaihiroba UM 34.6027 135.4256 2000 Chikkoyawatamachi Sakai Biotope near the mouth (15.8) Pittosporum tobira Trifolium repens and of Yamato River Digitaria ciliaris Grassland dominated by Tajihayahime Kouzen Large Acer Erigeron annuus and near KO 34.5012 135.4965 1982 Around an Miyayamadai Sakai Playground park (17.4) buergerianum grove deciduous trees such as temple’s private Liriodendron tulipifera and estate L. japonicum Grassland where the Large Second forest where the majority of herbs were Partially Koumyouike park KM 34.4610 135.4756 1987 majority of trees were Q. Artemisia indica Kurotoricho Izumi Artifical lake (33.4) var. connected to serrata and Q. acutissima maximowiczii and natural forests Pueraria lobata Sustainability 2021, 13, 7134 5 of 13

Sustainability 2021, 13, x 9 of 13 2.5. Data Analysis A one-way ANOVA was used to verify the differences in species richness and density of body size and habitat type, species diversity (H’), and species evenness (J’) between Study sites; SU: Suzunomiya park, CH: Chayama park, TA: Takasago park, IZ: Izumigaokaryokuchi, NI: Niwasiro park, different areas. The relationships between eight categories of land use and the ground KU: Kurotoriyama park, UM: Umitonohureaihiroba, KO: Kouzen park, KM: Koumyouike park. beetles index were examined using Pearson’s correlation analysis. Ground beetle com- Table 5. Pearson’s correlationmunities coefficient were between ordinated ground using beetles non-metric index and land multidimensional use category of nine scaling urban (NMDS). green areas. Singleton species occurring on one site were excluded from NMDS ordination. NMDS ordination, species diversity, and species evennessPark and were calculated using Vegan R package (ver.River 2.5-6). Community Index YearAll statistical Area (ha) analyses Paddy were Field performed Green usingForest R Urban 4.0.3 [Area22]. Road Open Space and Space Pond Species richness 3. Results All species 0.333 0.591 ** 0.234 0.305 −0.288 0.022 −0.900 *** −0.806 *** 0.702 *** 0.081 Body size A total of 2950 ground beetles representing 53 species were collected (Table2).Species Small 0.639richness *** 0.379 was the0.017 highest −0.235 at UM − (300.700 species) *** −0.490 near * the−0.612 mouth ** of−0.476 Yamato * 0.707 River *** and − the0.321 lowest Medium 0.287at TA0.527 (4 species) ** 0.215 in the landfill0.349 area−0.254 in Takaishi0.047 city.−0.891 Density *** −0.796 was *** the 0.675 highest *** at 0.125 IZ (59.76) Large 0.061and the 0.692 lowest *** at0.369 TA (1.24). 0.515 * Species 0.085 diversity 0.374 and−0.791 evenness *** −0.774 broadly *** 0.479ranged * from 0.265 1.12 to Habitat type 2.80 andfrom 0.42 to 0.89, respectively. Synuchus nitidus was the most abundant species, Forest species −0.654with *** 951 0.172 individuals 0.641 *** (32.2% 0.960 *** of all0.700 individuals). *** 0.841 *** S. dulcigradus−0.055 −0.077(20.9%) and−0.358Dolichus 0.831 halensis *** Open land species 0.644(10.1%) *** 0.562 were ** also−0.026 abundant. −0.089 Three −0.615 dominant ** −0.342 species −0.946 accounted *** −0.836 for *** 63.3% 0.913 of *** all individuals.−0.274 Density When body size was considered, 30 medium-sized species, 16 small-sized species, and All species 0.1277 large-sized −0.476 species−0.061 were0.262 found −0.306 (Table −20.231). Species −0.127 richness 0.175 of small-sized 0.040 species0.568 ** and Body size medium-sized species was the highest at NI (8) and UM (19), respectively, but the lowest Small −0.214at TA −0.630 (1 and *** 3, 0.060Figure 3 0.453). Species * 0.032 richness 0.033 of large-sized 0.195 species 0.442 * was−0.336 the highest 0.783 at *** KM Medium 0.399(5). However,−0.362 large-sized−0.196 0.024 species −0.567 were ** −0.467 not found * −0.310 in SU, CH,0.008 TA, or 0.307 NI. The density 0.306 of Large −0.336 0.694 *** 0.570 ** 0.658 *** 0.492 * 0.721 *** −0.493 ** −0.628 ** 0.139 0.283 small-sized species and medium-sized species was the highest at IZ (26.07 and 33.15) and Habitat type the lowest at TA (0.28 and 0.56). The density of large-sized species was the highest at KU Forest species −0.327 −0.692 *** 0.031 0.467 * 0.181 0.123 0.353 0.570 ** −0.490 * 0.819 *** Open land species 0.795(2.22). *** 0.471 In terms −0.155 of habitat −0.413 type, * −0.822 13 forest*** −0.597 species ** −0.841 and *** 40 − open0.742 *** land 0.947 species *** were−0.550 found. ** Species diversity (H’) 0.146Species 0.902 richness *** 0.411 of forest * 0.219 species −0.020 were the0.256 highest −0.749 at IZ *** and −0.874 KM *** (10) and0.580 the** lowest−0.222 at TA Species evenness (J’) 0.144(1). Species 0.901 *** richness 0.416 and*