Diatom and Microarthropod Communities of Three Airfields in Estonia – Their Differences and Similarities and Possible Linkages to Airfield Properties

EUROPEAN JOURNAL OF ECOLOGY

EJE 2018, 4(2): 1-14, doi:10.2478/eje-2018-0008

Diatom and microarthropod communities of three airfields in Estonia – their differences and similarities and possible linkages to airfield properties

1 School of Natural Sci- Piret Vacht1, Annely Kuu2, Liisa Puusepp1,3, Tiiu Koff1,3, Sander Kutti2, Jane Raamets2, Liisa Küttim1,3 ences and Health, Tallinn University, Narva Rd 25, 10120, Tallinn, Estonia Corresponding author, ABSTRACT E-mail: [email protected] Even though airfields, which are often anthropologically modified natural areas, are continuously influenced by 2 School of Engineering, human activities, their soils are still dynamic ecosystems containing various habitats for microscopic groups of Tartu College of Tallinn organisms which are often ignored. In this exploratory study, the microarthropod fauna, Collembola (Hexapoda) University of Technology, and oribatid mites (Acari: Oribatida), and diatom (Bacillariophyta) flora were identified in three Estonian air- Puiestee 78, 51008, Tartu fields, both runway sides and snow-melting sites were investigated. The communities of these airfields shared 3 Institute of Ecol- approximately 10–60% of the species belonging to each studied bioindicator group. The shared species were ogy, Tallinn University, generally characteristic of a broad habitat spectrum. Communities were also characterized based on their species Uus-Sadama 5, 10120, richness and diversity and in relation to location and the purpose of different airfield areas (e.g. snow-melting Tallinn, Estonia sites vs. runway sides). Also, species indicative of a specific airfield or purpose of the area within the airfield were identified using Indicator Species Analysis. Some possible linkages between airfield properties and communities, e.g. airfield that had highest pollutant concentrations had also maintained high diversity and species richness, were noted. Despite the contamination levels the airfield soils had still maintained a functioning soil ecosystem.

KEYWORDS airfields, soil, Oribatida, Collembola, diatoms, bioindicators

INTRODUCTION et al. 2003). Research on urban microarthropod communities Civil aviation is a fast-growing industry driven by globalisa- are more common. The subjects range from roadside soils tion. Previously the environmental impacts of aircraft emis- (Eitminavičiūtė 2006a,b; Magro et al. 2013) to urban soil qual- sions (Moussiopoulos et al. 1997; Rissman et al. 2013), noise ity assessment (Santorufo et al. 2012). (Vanker et al. 2013), de-icing chemicals (Turnbull & Bevan Soil mites, including Oribatida (Acari), are considered 1995) and polycyclic aromatic hydrocarbons (Ray et al. 2008) fairly resistant towards anthropogenic activities (Skubała1997 ; have been studied. Also, airfield vegetation and wildlife studies Khalil et al. 2009; Santorufo et al. 2012), however their species are common (Servoss et al. 2000; Blackwell et al. 2008, 2009; specific response to various disturbances and environmental Belant et al. 2013; Fischer et al. 2013). However, in the con- changes make them valuable bioindicators (Paoletti & Bressan text of airport soils and anthropogenic soils in general, there 1996). Other soil microarthropods such as springtails (Hexapo- is less information (Pytka et al. 2003; Baran et al. 2004; Ray da: Collembola) and other mite orders are considered less sen- et al. 2008; McNeill & Cancilla 2009; Werkenthin et al. 2014). sitive towards traffic related environmental changes, though Even more scarcely studies on airfield soil biota have been con- this does not lessen their importance as potential bioindicators ducted. Among the few exceptions is a study exploring the mi- (Paoletti & Bressan1996 ; Eitminavičiūtė 2006a), e.g. when and croarthropod communities in the area of Orio al Serio Airport where other groups are only present in low numbers. Many in Bergamo, Italy (Migliorini et al. 2003) and another studying microarthropod species are also known for tolerating exposure the development of earthworm communities on translocated to heavy metals due to their accumulative properties, which

grassland turf from Manchester airport, United Kingdom (Butt makes them suitable for studying aviation related disturbances European Journal of Ecology

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(Van Straalen & Van Wensem 1986; Heikens et al. 2001). Dia- 1. MATERIAL AND METHODS toms, mostly known from their bioindication abilities in water (Dickman 1998), are so far less used for in soil ecological re- 1.1. Study sites search, but can still be considered as potential indicators of soil Three Estonian airfields (Fig. 1) were selected based on their habitat properties (van Kerckvoorde et al. 2000; Van de Vijver accessibility, aviation history, availability of background infor- et al. 2008; Heger et al. 2012; Vacht et al. 2014). mation and natural conditions for studying soil communities. Based on previous studies from urban areas and traf- The main characteristics of these three airfields are shown in fic related disturbances (Santorufo et al. 2012) the following Table 1. Based on the soil maps provided by Estonian Land -hypotheses were set: Although, microarthropod and diatom Board (http://geoportaal.maaamet.ee/est/Kaardiserver/Mul communities vary between the airfields the communities at lakaart-p96.html), the soils of Tallinn airfield range from Rendzi the studied airfields also share a substantial percentage of spe- Leptosols to Histosols. In Tartu the soils have been classified as cies which can be considered typical to areas affected by inten- Luvisols influenced by excess moisture (gleying) and in Pärnu sive traffic related disturbances such as airfields; Diatom and airfield as Gleysols. Since their classification, several decades microarthropod (Collembola and oribatid mites) species indic- ago, they have been subject to draining in various extent. ative of specific airfields and the purpose of different airfield The three airfields have experienced aviation - relat areas can be identified. ed disturbances in various extents. For example, Tallinn air- This pilot study aims (1) to describe and analyze the field today acts as the primary airfield in Estonia with highest microarthropod fauna and diatom flora of Tallinn, Tartu and passenger and aircraft movement numbers and also receives Pärnu airfields and their community parameters; (2) to identify intensive maintenance activities. Tartu airfield has low usage the extent of the shared community of each bioindicator group intensity but has been most recently (< 15 years) reconstruct- in comparison of the three airfields and the components of the ed, including partial removal and filling of soil. Pärnu airfield, ,shared community; (3) to attempt to identify whether the stud- on the other hand, is today only used for a few regional flights ied airfield soils have maintained their functionality based on but has been under extensive military use during the Soviet their biological properties. These aims were achieved. era (1940-1991) which may have resulted in high exposure to aviation related pollutants. Therefore, it is impossible to place the airfields on a clearly definable anthropogenic disturbance gradient.

Figure 1. Location of study sites in north-eastern Europe (A) and in Estonia (B) and general sampling design within the airfields (C) where TL1 and TL2 mark the sampling sites on slow-melting sites, and TL3 through TL8 mark the runway side sampling sites.

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Table 1. Characteristics of Tallinn, Tartu and Pärnu airfields lot et al. 2011; Souffreau et al. 2013; Lowe et al., 2014). The nomenclature follows Krammer & Lange-Bertalot (1988; 1991) with additions from newer taxonomic literature (e.g Compère, 2001; Lange-Bertalot et al. 2011). Soil parameters were measured to characterize the airfields in general, not to link them directly to soil communities, therefore, the soil samples from each airfields were pooled. These samples were analyzed at the Estonian Environ- mental Research Center with ICP-AES for Cu, Pb, Zn and Cd because these metals are considered most indicative of traffic- re lated pollution (Davis et al. 2001). Samples were also analysed

for total-N, P and K, Ca, Mg and pHKCl at the Estonian Agricul- -tural Research Centre. Soil organic matter and carbonate con tent was measured using loss-on-ignition method (prepASH®, Precisa). Soil microbial respiration rates (basal respiration) and Substrate Induced Respiration (SIR) were determined using 1.2. Sampling procedure and laboratory analysis of samples manometric respirometers (Oxitop®, WTW). Sampling was conducted in September, 2013, and repeated in September 2014. In addition to six sampling points at runway 1.3. Data analysis sides also two snow-melting sites were sampled from each air- Species data from two years of sampling were pooled for nu- field. Fig. 1 shows the general sampling design at each airfield. merical analyses. Communities were described by observed Because sampling at the airfields was to some extent restricted Collembola and oribatid mite abundance per sample, pres- (e.g the allowed time for sampling and the volume of soil re- ence-absence data was noted for diatoms. Because all mi- moved from the site) eight samples were collected for this ex- croarthropod communities from the same volume of soil were plorative study from each airfield each year (in total 48 samples identified and counted, only their observed species richness of each bioindicator group). A ø 5 cm soil auger was used to were calculated. Diatom communities were described based collect samples from 0-10 cm of topsoil (196 cm3) for microar- on rarefied species richness (Heck et al. 1975; Oksanen 2012). thropod (oribatid mites and springtails) and diatom extraction, All bioindicator groups were characterized based on communi- microbial measurements and soil chemical analysis. ty diversity (Shannon’s H). Also the Oribatida Collembola ratio Microarthropods were extracted using Berlese-Tull- (O/C) was calculated for each airfield. The number of repeti- gren funnel until samples were fully dry (at least 72 hours) tions for soil chemical and microbial analysis was limited due and stored in 90% ethanol. For clearing purposes 80% lactic to fieldwork restrictions and therefore this data was only ana- acid was used for oribatid mites. Samples were hand sorted lyzed using descriptive statistical methods to give an overview and identified by species. Keys by Fjellberg (1998; 2007) and on general soil characteristics. Hopkin (2007) were used to identify adult Collembola. The no- Kruskal-Wallis test, ANOVA, and average linkage clus- menclature follows Bellinger et al (1996-2018). For the identi- ter analysis based on Bray-Curtis dissimilarity were used to fication of adult oribatid mites keys by Weigmann (2006) and compare the communities of Tallinn, Tartu and Pärnu airfields Niedbala (2008) were used. The nomenclature follows Weig- and the different land uses within airfields (runway sides and mann (2006). snow-melting fields). Indicator Species Analysis (ISA) (Dufrene For diatom analysis soil samples (N = 24) were mixed & Legendre 1997; De Cáceres & Legendre 2009) together with and 2 cm3 of soil was extracted, then treated with 10% HCl and Monte Carlo randomization technique for testing the statistical

30% H2O2 while heating the samples to remove carbonates and significance (P < 0.05) of Indicator Values (IV) was used to iden- -organic matter. Samples were decanted and centrifuged to re- tify potential indicator species. Community parameter calcu move other unnecessary components. The solution (0.1 ml) lations, descriptive and generalising analyzes were conducted was transferred to cover glass, dried and fixed with Naphrax. using R programming environment (R Development Core Team Samples were examined under 600–1000 × magnification (us- 2014) with the ‘indicspecies’ (De Cáceres & Legendre 2009), ing immersion oil nd = 1.516). From each sample 300–500 ‘MASS’ (Venables & Ripley 2002) and ‘vegan’ (Oksanen 2013) valves were identified and counted along random transects. package, and IBM SPSS Statistics 20.0. Damaged valves were counted as a separate individual when more than half of the valve was intact. Diatoms were identified to species level and when this was impossible due to dam- 2. RESULTS ages, to genus level (Krammer & Lange-Bertalot 1988, 1991; Hamilton et al. 1992; Lange-Bertalot & Metzeltin 1996; Round 2.1. Soil properties & Bukhtiyarova1996 ; Lange-Bertalot & Metzeltin,1996 ; Lange- Although the soil maps provided by Estonian Land Board show Bertalot, 1997; Krammer, 2000; Compère, 2001; Lange-Berta- some differences between the three airfield soils and allof

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them have maintained some characteristics of the original soils community not shared by all studied airfields can be considered (e.g. higher carbonate content in Tallinn) they have all been af- site specific, possibly depending on the natural conditions (e.g. fected by aviation, airfield maintenance, and aviation related hydrological regime, soil development prior to aviation related construction activities e.g. draining, tilling, removal and filling. activities) and anthropogenic history (e.g. history and place- An overwhelming area of these soils can today be classified ment of the filling soil on site, type and quantity of de-icing as Technosols (IUSS Working Group WRB 2015), characterized chemicals) of each site. These site specific species included e.g. by a dense and tightly rooted mull type humus horizon that Bourletiella arvalis Fitch, 1863 (characteristic of Tartu airfield), contains various artifacts such as pieces of glass, aluminium, Micranurida pygmaea Börner, 1902 (characteristic of Pärnu air- plastic, paint and runway construction materials. Table 2 lists field) andFolsomia quadrioculata Tullberg, 1871 (characteristic the results from soil chemical analyses, including results from a of Tallinn airfield). previous study on Tallinn airfield soil (Keskküla 2011), and soil The list of all encountered species together with microbial parameter measurements. their abundance (per sample) at each airfield, separating between the runway sides and snow-melting sites is given in Ap- 2.2. Community properties pendix (Table A.1.). No significant differences were detected The results from community properties are shown in Table 3 in the species abundance in comparison of the three airfields. separating between the runway sides and snow-melting sites. In three-way ISA (Tallinn, Tartu and Pärnu airfield), springtails On Pärnu airfield the oribatid mites outnumbered the Col- were not significantly strong indicators of any of the airfields lembola (O/C ratio 3.0). In Tallinn the O/C ratio was 0.8 and in singularly, but as a combination M. affinis (IV = 0.87, P = 0.02) Tartu 0.5. and T. vulgaris (IV = 0.81, P = 0.011) were indicative of Pärnu and Tallinn airfields. 2.3. Collembola community composition On Family level, Neanuridae were significantly more In total 31 springtail species were identified, belonging to 22 abundant at snow-melting sites compared to runway sides (χ2 = genera. The most abundant species, forming 31% of the to- 5.715, df = 1, P = 0.017). The trend was opposite for Tomoceri- tal abundance, was Protaphorura armata Tullberg, 1869. The dae (χ2 = 6.611, df = 1, P = 0.01). Significant differences in spe- snow-melting sites of the three airfields shared five springtail cies abundance depending on the purpose of the airfield area species: Anurida granaria Nicolet, 1847, Metaphorura affinis (runway side or snow-melting sites) were rare, only a few spe- Börner, 1902, P. armata, Parisotoma notabilis Schaeffer, 1896 cies showed significant difference – e.g. T. vulgaris (χ2 = 6.611, and Ceratophysella sp. Runway sides shared 11 species, includ- df = 1, P = 0.01) and L. lanuginosus (χ2 = 7.689, df = 1, P = 0.006) ing almost all of those also found from snow-melting sites (ex- that were both only found on runway sides. Two-way ISA sup- cept Ceratophysella sp). In addition, the airfield runway sides ported the assumption that these two species can be consid- also shared Folsomia candida Willem 1902, Folsomia sexocula- ered significantly indicative of airfield runway sides (IV = 0.85,P ta Tullberg, 1871, Isotoma minor Schaeffer, 1896, Isotoma viri- = 0.011 and IV = 0.82, P = 0.017 respectively). The results from dis Bourlet, 1839, Isotomurus sp., Tomocerus vulgaris Tullberg, ISA, where the sites were divided into six groups (separating 1871 and Lepidocyrtus lanuginosus Gmelin, 1788. between airfields, their runway sides and snow-melting sites) An explorative average linkage cluster analysis re- showed that T. vulgaris (IV = 0.93, P = 0.01) and L. lanugino- vealed that based on the springtail communities the three air- sus (IV = 0.93, P = 0.003) are more specifically strongly and sig- fields cannot be distinguished from each-other. The part of the nificantly associated with the combination of Tallinn and Tartu runway sides. These species, however, can not be considered ideal indicators of these runway sides because they can also be Table 2. Results from soil chemical and microbial analysis. Heavy metal and oil found on other sites in addition to the two runway sides (A = product (C10-C40) concentration result ranges for Tallinn (*) are based on previ- 0.9459 and B = 0.9429 respectively) and they cannot be found ous research (Keskküla 2011), others are based on a single result from repreated measurements (N=10) or expressed as Mean ± SE as provided by the laboratory Table 3. Collembola, oribatid mites and diatom community parameters (observed species richness for Collembola and oribatid mites, rarefied species richness for diatoms and diversity expressed by Shannon’s H on the runway sides and snow- melting sites of Tallinn, Tartu and Pärnu airfields

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. though L. pannonica inhabited only runway side soils, no significant indicators were found that could identify different land use within airfields.

2.5. Diatom community composition In total 49 diatom species were identified belonging to 30 genera. The most abundant diatoms were Hantzschia amphioxys (Ehrenberg) Grunow, 1880 (26.1%), Aulacoseira granulata (Eh- renberg) Ehrenberg, 1843 (12.9%) and Luticola mutica (Kützing) Mann, 1990 (9.7%). The snow-melting sites shared five species, Figure 2. Average linkage cluster analysis of the oribatid mite samples collected from runways sides, abbreviation beginning with TL refer to Tallinn airfield, TR to which in addition to the three most abundant species were Tartu airfield and P to Pärnu airfield, numbers stand for sampling sites within the Fragilaria nitzschioides (Grunow) Lange-Bertalot, 2011 and airfield as shown on Fig.1. Navicula cari (Ehrenberg) Ehrenberg, 1836. The runway sides from all the sampled sites on Tallinn and Tartu runway sides (B of the three airfields shared eight species. These included the = 0.9167 for both). most abundant diatom species mentioned previously and also Pinnularia obscura (Krasske) Patrik & Reimer, 1966, N. cari, Hu- 2.4. Oribatida community composition midophila contenta (Grunow) Lowe et al., 2014 and F. nitzschi- In total 34 oribatid mite species were identified, belonging to oides. An explorative cluster analysis did not reveal notable sim- 22 genera. The majority of species found on airfield soils belong ilarities between the diatom communities of the three airfields, to suborder Brachypylina. The most abundant species were in comparison of the snow-melting sites and runway sides. Scheloribates laevigatus Koch, 1836 and Tectocepheus velatus There were 12 diatom species that were specific to velatus Michael, 1880. These two species made up 37% of the Pärnu airfield, including e.g. Fragilariforma virescens (Ralfs) total abundance, 19% and 18% respectively. While the snow- Williams & Round, 1988 and several species belonging to the melting sites of the three airfields shared only one oribatid mite Stauroneis genus. The list of all encountered species at each air- species, T. velatus velatus, the runway sides had five species field, separating between the runway sides and snow-melting incommon: Liebstadia pannonica Willmann, 1951, Platynothrus sites is given in Appendix (Table A.3.) peltifer Koch, 1839, S. laevigatus, Trichoribates incisellus Kram- The results from six-way ISA (separating between er, 1897 and T. velatus velatus. The list of all encountered spe- airfields, their runway sides and snow-melting sites) indicated cies together with their abundance (per sample) at each air- that Pinnularia lata (Brébisson) Rabehorst, 1853 (IV = 0.985 P field, separating between the runway sides and snow-melting = 0.016), Pinnularia borealis (Ehrenberg) Ehrenberg, 1843 (IV = sites at each airfield is given in Appendix (Table A.2.). 0.957 P = 0.041) and Diploneis finnica (Ehrenberg) Cleve, 1891 No significant differences in oribatid mite species (IV = 0.913 P = 0.027) are strongly and significantly associated abundance depending on the purpose of the airfield area (run- with the snow-melting sites of Pärnu airfield. These three spe- way side or snow-melting sites) or airfield were detected (P > cies can be used to indicate the snow-melting sites of Pärnu 0.05). The explorative average linkage cluster analysis showed airfield because they appear on all sampled sites (B = 1.0000) that at the snow-melting sites the oribatid mite communities and they are largely (but not completely) restricted to them were not differentiable based on the specific airfield. The com- (A=0.9706, A=0.9158 and A=0.8333 respectively). Also three munities belonging to the runway sides, however, formed a other diatom species – F. nitzschioides, L. mutica and D. finnica) distinct group together with the communities on the Tallinn air- were significantly (P > 0.05) linked to snow-melting sites of all field, and separated them from the communities of Tartu and the studied airfields. Pärnu (Fig. 2). No significant differences were observed in the abundance of oribatid mite species in comparison on runway sides and snow-melting sites nor in comparison of the three 3. DISCUSSION airfields. The concentrations of Pb and Zn were mildly elevated (Peter- Some site specific species such as Eupelops acromios sell et al. 1997) in Tallinn airfield. Pärnu airfield had elevated Hermann, 1804 and Nothrus silvestris Nicolet, 1855, character- Zn content compared to normal levels in the region. Levels of istic only of Tallinn airfield, andPunctoribates punctum Berlese, Cd were high on all airfields (Petersell et al. 1997). Neverthe- 1908, characteristic of Pärnu airfield, were encountered. When less, the concentration of measured heavy metals and oil prod- grouping the sites into six groups (separating between airfields, ucts (C10–C40) remained lower than the limits set by Estonian their runway sides and snow-melting sites) the ISA did not re- Environmental Ministry (Riigiteataja 2010; Pinedo et al. 2014). veal any oribatid mite species that were significantly indicative. While most soil parameters varied only moderately between In three-way ISA E. acromios was significantly indicative of Tal- the three airfields, elevated level of K was noted in Tallinn linn airfield (IV = 0.79, P = 0.01). S. laevigatus, T. velatus ve- and higher organic matter content in Tartu compared to the latus and Eupelops hygrophilus Knülle, 1954 were significantly other airfields. Overall, both K and organic matter content in (P < 0.04) linked to various combinations of two airfields. Even the humus horizon can be considered high (Kask & Niine 1997;

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Petersell et al. 1997). While in Tallinn the elevated K content is of the three airfields did not reveal any significant differences in ,likely linked to historic soil conditions, the high organic matter abundances, indicating that solely based on these parameters content in Tartu airfield soil is more of a mystery, possibly tied the airfields cannot be ranked according to their disturbance to characteristics of the filling soil used in some parts of the level. airfield. Soil pH values, varying from slightly acidic to neutral, The community similarity of different airfields and reflected the historic soil conditions, indicating also that the ad- airfield area purposes together with the number and percent- dition of construction and other aviation related substances has age of shared species suggest fairly homogeneous Collembolan not raised the soil pH as often occurs in soils under anthropo- communities. The typical airfield springtail community consists genic influence (Maechling et al. 1974). of A.granaria, M. affinis, P. armata, P. notabilis, and likely also The SIR results showed similar results as measured species belonging to Folsomia and Isotoma genera. from Estonian road-side grasslands (Vacht 2012), but exceeded Most of the oribatid mites found in this study (e.g. P. the levels measured from e.g. semi-coke heap habitats (Kalda punctum, S. laevigatus) are widespread eurytopic species, usu- et al. 2015). Basal respiration rate was higher than measured ally forming the main body of edaphic communities in most dis- from road-side soils (Vacht 2012). Soil basal respiration has turbed landscapes in Europe (Caruso et al. 2009). The species been shown to indicate toxicity effects (e.g. Pb, Zn, Cu) in soils composition of Oribatid mites resembled those of Lithuanian (Romero-Freire et al. 2016), but not in soils with high organic urban soils (Eitminavičiūtė 2006a,b) containing dominant T. ve- matter and carbonate content such as the soils encountered in latus velatus and S. laevigatus. The latter has also been found this study. Also the indicativeness of substrate induced respira- from the area of Orio al Serio Airport in Northern Italy (Migli- tion has been known to depend greatly on soil pH (Cheng & orini et al. 2003). The low abundance of Oppiella nova Oude- Coleman 1989). The elevated respiration rate in Pärnu may be mans, 1902 could be due to high soil pH as noted by previous related to the increased levels of oil products in the airfield soil studies (Eitminavičiūtė 2006a,b). Also typically moss-dwelling (Hund & Schenk 1994). (Smrž 1994) Scutovertex minutus Koch, 1835 was found from all Diatom and oribatid mite species richness (rarefied sites, however, only abundantly from one of the snow-melting species richness for diatoms) and diversity showed similar sites in Tartu (site TR1). Previously this species has been found trends in comparison of the three airfields. Collembolan diver- from the immediate proximity to the roads (Eitminavičiūtė sity varied greatly, showing no strong signs on indicativeness to 2006a,b) possibly showing its high tolerance towards de-icing airfield nor airfield area purpose. The oribatid mite and diatom agents and preference for hydric conditions. Some research community diversity were similar showing high diversity in the suggest the species has a high tolerance for fluctuating abiotic snow-melting sites of Tallinn airfield and lowest diversity in the soil parameters (e.g. moisture) (Smrž 1994). Also T. incisellus, runways sides of Tartu airfield. In Tallinn this difference could L. pannonica and Peloptulus phaenotus Koch, 1844 have been be caused by the nature of de-icing agents used, and in Tartu previously encountered in heavy metal contaminated soils (Ca- the decreased diversity could potentially be linked to recent ruso et al. 2009; Skubała & Zaleski 2012). Therefore, the com- runway construction work. munity that can be considered typical to airfields contains the Springtail communities were dominated by P. armata following species: T. velatus velatus, L. pannonica, P. peltifer, S. and P. notabilisi, which are known to inhabit highly disturbed laevigatus and T. incisellus. Compared to springtails the oribatid areas (Migliorini et al. 2003; Eitminavičiūtė 2006a,b). Collem- mite communities show more variability, especially in compari- bolans are considered as a relatively resistant group to anthro- son of different airfield area purposes. This is why in the future, pogenic disturbances (Bengtsson & Rundgren 1988; Haimi & especially the effects of airfield de-icing agents on oribatid mite Siira-Pietikäinen1996 ), however, their community composition communities should be studied in more detail. is known to respond to human-induced disturbances, especial- The dominant diatom species were the cosmopolitan ly by decreasing numbers of Isotomidae and Onychiuridae and H. amphioxys, A. granulata and L. mutica. All the studied air- increasing abundance of less demanding Entomobryidae and fields contained the same base soil community, that has also Neanuridae (Sousa et al. 2003; Magro et al. 2013). This study, previously been found from many soil habitats both in Estonia however, did not encounter a strong shift in most of these (Vacht et al. 2014) and elsewhere (Soare & Dobrescu 2010; groups in comparison of the three airfields nor in comparison Heger et al. 2012) that represent a tolerant algal community .of the snow-melting sites and runway sides. Only Neanuridae which has little bioindication value that is particular to airfields (e.g. A. granaria and M. pygmaea) were more abundant at Nevertheless, the shared species of the three airfields (e.g. F. the snow-melting sites, which may indicate that these areas nitzschioides, H. amphioxys, N. cari, L. mutica) can be expected present a suitable niche for these species. For Entomobryidae to be found on also other similar airfields. Also it is possible that (e.g. L. lanuginosus and L. cyaneus) the change in abundance some species (e.g. D. finnica) may indicate snow-melting sites was opposite, making it difficult to interpret either the runway mostly due to increased moisture, which are less suitable habi- sides nor snow-melting sites as the more demanding habitat. tats for microarthropod communities. This is one of the reasons Some studies also point out that epedaphic (Pernin et al. 2006) why microarthropods and diatoms should be considered as L. lanuginosus may be indifferent to soil contamination levels complementary bioindicator groups in soil ecological research. (Austruy et al. 2016). The comparison the Collembolan families The ISA revealed that in comparison of the three bioindicator

6 EUROPEAN JOURNAL OF ECOLOGY groups, diatoms and springtails were the most indicative on pollutants have maintained fully functional soil biological com- specific airfield or land use. Based on this, oribatid mites can be munities. Microarthropod and diatom community parame- considered fairly robust towards airfield related disturbances. ters show more similar variation than springtail communities Soil functionality is closely related to the concept of depending on the airfield and the purpose of the particular soil quality which in turn has the capability to sustain among airfield area. All three bioindicator groups had a substantial other things biotic communities (Gardi et al. 2002). All the air- percentage of species that can be considered typical to areas field soils are functional soils, containing a well adapted and affected by disturbances, in this case airfields. These species comparatively diverse community of diatoms, springtails and include springtails e.g. M. affinisand P. notabilis, oribatid mites oribatid mites. It has been noted on several occasions that us- T. velatus velatus, L. pannonica and T. incisellus, and diatoms F. ing bioindicators should be incorporated into evaluation of soil nitzschioides, H. amphioxys and L. mutica. functionality and quality of anthropogenic soils (Hartley et al. Collembola species L. lanuginosus and T. vulgaris 2008). The community composition found on these airfields were significantly indicative of airfield runway sides but no indicates that all main functional groups of microarthropods strong indicators of specific airfield were discovered. Oribatid are present, though fungal feeders were prominent (e.g. T. ve- mites were not indicative of different airfield purposes, only E. latus velatus, S. laevigatus). This means that the habitat must acromios was noted as indicative of Tallinn airfield. contain also sufficient food sources for all groups present.. Also Three diatom species, F. nitzschioides, Luticola mutica high ratio in Acarina/Collembola may suggest high soil quality and D. finnica, were significantly linked to airfield snow-melting because there are known to be less mites than springtails in sites. Also, many diatom species were specific to Pärnu airfield. degraded soils (Parisi et al. 2005). The results of the O/C ra- In conclusion, it is clear that despite aviation related tio indicates well that in an anthropogenic grassland such as disturbances these three airfields have maintained a functional airfields it is vital to include both oribatid mite and springtail soil biological community that has adapted well to these condi- identification due to the variation of the dominant group, to tions. Also, the shifts in O/C ratio and variation in the commu- receive a full overview of the microarthropod communities nity parameters of the three groups indicates the potential of before combining the data with diatom community data. The these three groups as complementary bioindicators of anthro- ratio reflects also the dominant soil process – humification over pogenic disturbances. Further studies are needed to confirm mineralization in Pärnu and mineralization over humification in the connections between these bioindicators and specific soil Tallinn and Tartu. The elevated O/C ratio ( >1 ) can be also con- parameters. sidered a measure of environmental stability (Bachelier 1986) which means Pärnu airfield can be considered as the most envi- Acknowledgements: We are grateful for financial support from ronmentally stable out of the three airfields studied. Tallinn University’s Centre of Excellence initiative “Studies of Natural and Man-made Environments” and “Natural Sciences and Sustainable Development”, and The Estonian Science 4. CONCLUSION Foundation. We are also grateful for The Hoogstraal Memorial While an overwhelming area of the three airfields show char- Acarology Student Fund, Tartu Cultural Endowment, and Eu- acteristics of Technosols, they also show properties of the ropean Social Fund’s Doctoral Studies and Internationalization natural soils which despite the moderately elevated levels of Program DoRa, carried out by Foundation Archimedes.

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APPENDIX

Table A1 Collembola

Tallinn Tartu Pärnu

Runway Snow-mel- Runway Snow-mel- Runway Snow-mel- sides ting sites sides ting sites sides ting sites Collembola Anurida granaria (Nicolet, 1847) 0.3 ± 0.2 1.0 ± 1.0 0.2 ± 0.2 3.0 ± 3.0 0.2 ± 0.2 0.5 ± 0.5 Bourletiella arvalis (Fitch, 1863) - - 0.2 ± 0.2 0.5 ± 0.5 - - Ceratophysella bengtssoni (Ågren, 1904) 4.7 ± 2.1 - - 3.0 ± 3.0 0.2 ± 0.2 1.5 ± 0.5 Ceratophysella sp. 2.3 ± 2.1 0.5 ± 0.5 3.0 ± 2.2 21.0 ± 20.0 0.3 ± 0.3 2.5 ± 2.5 Dicyrtomina sp. - 0.5 ± 0.5 - 0.5 ± 0.5 1.5 ± 1.5 - Folsomia candida (Willem, 1902) 3.5 ± 1.5 - 2.2 ± 1.8 8.5 ± 8.5 0.2 ± 0.2 0.5 ± 0.5 Folsomia fimetaria (Linnaeus, 1758) - - 0.5 ± 0.2 - 0.2 ± 0.2 0.5 ± 0.5 Folsomia quadrioculata (Tullberg, 1871) 0.2 ± 0.2 0.5 ± 0.5 - - - - Folsomia sexoculata (Tullberg, 1871) 3.8 ± 2.3 7.5 ± 5.5 0.7 ± 0.3 0.5 ± 0.5 3.3 ± 2.6 - Friesea sp. - - - 1.5 ± 1.5 - - Heteromurus nitidus (Templeton, 1835) 0.3 ± 0.2 - - - - - Hypogastrura sp. 2.7 ± 1.8 0.5 ± 0.5 0.5 ± 0.3 11.0 ± 11.0 - - Isotoma minor (Schaeffer, 1896) 5.2 ± 1.7 - 1.0 ± 0.7 31.5 ± 31.5 1.2 ± 0.5 2.0 ± 0.0 Isotoma viridis (Bourlet, 1839) 1.5 ± 0.9 - 1.2 ± 0.3 0.5 ± 0.5 0.7 ± 0.4 1.0 ± 1.0 Isotomurus palustris (Müller, 1776) 1.7 ± 0.6 - - - 0.2 ± 0.2 1.0 ± 0.0 Isotomurus sp. 1.8 ± 1.1 - 0.8 ± 0.5 - 0.3 ± 0.2 - Tomocerus vulgaris (Tullberg, 1871) 0.3 ± 0.2 - 1.5 ± 0.8 - - - Lepidocyrtus lanuginosus (Gmelin, 1788) 3.0 ± 1.5 - 2.5 ± 1.1 - 0.3 ± 0.2 - Metaphorura affinis (Börner, 1902) 2.3 ± 1.0 2.5 ± 2.5 7.5 ± 2.9 2.5 ± 2.5 0.5 ± 0.5 1.5 ± 1.5 Micranurida pygmaea (Börner, 1901) - - - - 0.2 ± 0.2 1.0 ± 1.0 Parisotoma notabilis (Schaeffer, 1896) 17.2 ± 7.5 2,5 ± 0.5 3.0 ± 1.9 1.5 ± 0.5 3.3 ± 1.7 1.0 ± 1.0 Proisotoma minuta (Tullberg, 1871) 0.3 ± 0.2 - 0.7 ± 0.5 35.0 ± 35.0 - 0.5 ± 0.5 Protaphorura armata (Tullberg, 1869) 1.7 ± 1.1 1.5 ± 1.5 4.7 ± 1.9 70.0 ± 70.0 0.2 ± 0.2 0.5 ± 0.5 Pseudisotoma sensibilis (Tullberg, 1876) - - 1.2 ± 1.2 - - 2.5 ± 2.5 - - Pseudosinella sexoculata (Schött, 1902) - - - 6.0 ± 6.0 Sminthurides schoetti (Axelson, 1903) - - - - 0.3 ± 0.3 - Sminthurides sp. - - - - 0.7 ± 0.4 - Sminthurinus aureus (Lubbock, 1862) 0.2 ± 0.2 - - 0.5 ± 0.5 - - Tomocerus vulgaris (Tullberg, 1871) 2.7 ± 0.9 - 3.2 ± 0.7 - 0.3 ± 0.3 - Willowsia buski (Lubbock, 1870) 1.2 ± 0.8 - 1.2 ± 1.0 - - - Xenylla sp. 2.2 ± 1.3 - 0.5 ± 0.3 1.0 ± 1.0 - -

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Table A2 Oribatid

Tallinn Tartu Pärnu Snow-melting Snow-melting Snow-melting Runway sides Runway sides Runway sides sites sites sites Oribatida Liochthonius brevis (Michael, 1888) - - - 4.0 ± 4.0 0.3 ± 0.3 1.0 ± 1.0 Liochthonius sellnicki (Thor, 1930) - - - - 0.5 ± 0.5 - Steganacarus (Atropacarus) sticulus (Koch, - - - - 0.5 ± 0.5 - 1836) Steganacarus (Tropacarus) carinatus 0.2 ± 0.2 - - - 0.2 ± 0.2 - (Koch, 1841) Rhysotrita ardua (Koch, 1841) - - - - 0.2 ± 0.2 - Platynothrus peltifer (Koch, 1839) 0.2 ± 0.2 - 0.7 ± 0.7 - 4.2 ± 2.1 1.0 ± 1.0 Nothrus silvestris (Nicolet, 1855) 0.2 ± 0.2 0.5 ± 0.5 - - - - Conchogneta traegardhi (Forsslund, 1947) 0.2 ± 0.2 - - - - - Oppiella nova (Oudemans, 1902) - - 0.8 ± 0.8 - 0.3 ± 0.2 - Oppiella translamellata (Willmann, 1923) 0.2 ± 0.2 - 0.8 ± 0.5 - - - Tectocepheus velatus velatus (Michael, 3.2 ± 1.5 2.0 ± 2.0 10.3 ± 5.3 18.0 ± 13.0 0.2 ± 0.2 - 1880) Scutovertex minutus (Koch, 1835) - 1.0 ± 1.0 - 23.5 ± 23.5 0.2 ± 0.2 - Eupelops tardus (Koch, 1835) 0.8 ± 0.5 - - - - - Eupelops acromios (Hermann, 1804) 1.7 ± 0.8 0.5 ± 0.5 - - - - Eupelops hygrophilus (Knülle, 1954) 3.3 ± 2.2 - - - 1.2 ± 0.6 4.0 ± 4.0 Eupelops occultus (Koch, 1835) - - 0.3 ± 0.3 - - - Peloptulus phaenotus (Koch, 1844) 0.3 ± 0.3 - - - 3.7 ± 2.1 1.0 ± 1.0 Liebstadia pannonica (Willmann, 1951) 0.2 ± 0.2 - 0.3 ± 0.3 - 0.3 ± 0.2 - Scheloribates laevigatus (Koch, 1836) 1.7 ± 1.7 - 14.8 ± 9.9 0.5 ± 0.5 4.7 ± 1.8 4.5 ± 3.5 Scheloribates latipes (Koch, 1844) 0.7 ± 0.7 - - - 0.5 ± 0.3 0.5 ± 0.5 Chamobates voigtsi (Oudemans, 1902) 0.2 ± 0.2 - - - - - Ceratozetes mediocris (Berlese, 1908) 0.2 ± 0.2 - - - - - Ceratozetes parvulus (Sellnick, 1922) 0.7 ± 0.5 - - - - - Ceratozetes gracilis (Michael, 1884) 0.2 ± 0.2 - - - - - Trichoribates incisellus (Kramer, 1897) 0.8 ± 0.5 - 0.7 ± 0.5 1.0 ± 1.0 0.2 ± 0.2 - Mycobates sarekensis (Trägårdh, 1910) - - 0.7 ± 0.7 0.5 ± 0.5 0.2 ± 0.2 - Mycobates tridactylus (Willmann, 1929) 0.2 ± 0.2 - - - - - Punctoribates punctum (Berlese, 1908) - - - - 0.2 ± 0.2 1.5 ± 1.5 Haplozetes vindobonesis (Willmann, 1935) 0.7 ± 0.7 - - - - - Peloribates longipilosus (Csiszár, 1962) 1.7 ± 1.7 - - - - - Galumna sp. 0.8 ± 0.3 - - - - - Galumna lanceata (Oudemans, 1900) 0.5 ± 0.5 - - - - - Galumna obvia (Berlese, 1914) 0.3 ± 0.3 - - - - - Pergalumna nervosa (Berlese, 1914) 0.7 ± 0.7 - - - - -

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Table A3 Diatom

Tallinn Tartu Pärnu Runway Snow-mel- Runway Snow-mel- Runway Snow-mel- sides ting sites sides ting sites sides ting sites Diatoms Achnanthes delicatula (Kützing) Grunow, 1880 - - - - - + Achnanthes hungarica (Grunow) Grunow, 1880 - - - - + - Actinella sp. (Lewis) Lewis, 1864 + - - - - - Amphipleura sp. (Kützing) Kützing, 1844 - - - - - + Aulacoseira granulata (Ehrenberg) Ehrenberg, 1843 + + + - + + Aulacoseira karelica (Mölder) Simonsen, 1979 + - - - - - Aulacoseira sp. (Ehrenberg) Thwaites, 1848 + - - + - - Caloneis sp. (Cleve) Cleve, 1894 - - - + - - Cocconeis fluviatilis (Wallace) Wallace, 1960 - - - - + - Cymbella affinis (Kützing) Kützing, 1844 - - + + - + Cymbella radiosa (Héribaud-Joseph) Héribaud-Joseph, + - - - - - 1903 Diploneis finnica(Ehrenberg) Cleve, 1891 - + - - - + Epithemia sp. Kützing, 1844 + - - - - + Epithemia turgida (Ehrenberg) Kützing, 1844 - - - + - + Eunotia paludosa Grunow 1862 - - + - - - Fragilaria nitzschioides (Grunow) Van Heurck 1881 + + + + + + Fragilaria sp. (Müller) Lyngbye, 1819 + - - - + - Fragilariforma virescens (Ralfs) Williams and Round, - - - - + - 1988 Gomphonema parvulus (Kützing) Kützing, 1849 + - - + - + Hantzschia amphioxys (Ehrenberg) Grunow, 1880 + + + + + + Humidophila contenta (Grunow) Lowe et al., 2014 + - + - + + Luticola mutica (Kützing) Mann, 1990 + + + + + + Luticola nivalis (Ehrenberg) Mann, 1990 - + - - - - Luticola venticosa (Kützing) Mann, 1990 + - - + - + Mastogloia sp. (Thwaites) Smith, 1856 - - - - - + Mayamaea sp. (Kützing) Lange-Bertalot, 1997 + + - - + + Navicula cari (Ehrenberg) Ehrenberg, 1836 + + + + + + Navicula cincta (Ehrenberg) Ralfs, 1861 - - - + + - Navicula subhamulata (Grunow) Grunow, 1880 + - - - + + Nitzschia alpina (Hustedt) Hustedt, 1943 + - - - + + Nitzschia amphibia (Grunow) Grunow, 1862 - - - + + + Nitzschia sp. Hassall, 1845 - - - + - - Pinnularia borealis (Ehrenberg) Ehrenberg, 1843 + + - - + + Pinnularia lata (Brébisson) Rabehorst, 1853 + - - - - + Pinnularia obscura (Krasske) Patrick and Reimer, 1966 + - - + + + Pinnularia rabenhorsti(Grunow) Krammer, 2000 - - - - + + Pinnularia sp. Ehrenberg, 1843 + - + - + - Pinnularia subcapitata Gregory, 1856 - - - - + - Pseudostaurosira sp. Williams and Round, 1988 - - - - - +

13 EUROPEAN JOURNAL OF ECOLOGY continued Table A3 Diatom

Sellaphora alastos (Hohn and Hellerman) Lange-Berta------+ lot and Metzeltin, 1996 Stauroforma exiguformis Flower, Jones and Round, - - - - - + 1996 Stauroneis kriegeri (Patrick) Patrick, 1945 - - - - + - Stauroneis sp. Ehrenberg, 1842 - - - - - + Staurosira construens var. venter (Ehrenberg) Hamil------+ ton, 1992 Staurosirella leptostauron (Ehrenberg) Williams and + + - - - + Round, 1987 Stephanodiscus sp. (Ehrenberg) Eherenberg, 1845 + - - - - + Suriella ovata Kützing, 1844 - - - - + - Tabellaria fenestrata (Lyngbye) Kützing, 1844 + - + - - + Ulnaria ulna (Kützing) Compère, 2001 - - - - - +

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EJE 2018, 4(2): 15-27, doi:10.2478/eje-2018-0009

Insights into the impacts of three current environmental problems on Amphibians

1 Department of Ecology Himangshu Dutta1 and Environmental Sci- ence, Assam University, Silchar, Assam, India. Pin: 788011 ABSTRACT Corresponding author, Global warming, light pollution and noise are common human-induced environmental problems that are es- E-mail: himangshu. [email protected] calating at a high rate. Their consequences on wildlife have mostly been overlooked, with the exception of a few species with respect to climate change. The problems often occur simultaneously and exert their negative effects together at the same time. In other words, their impacts are combined. Studies have never focused on more than one problem, and so, such combined effects have never been understood properly. The review ad- dresses this lacuna in the case of amphibians, which are a highly vulnerable group. It divides the overall impacts of the problems into seven categories (behaviour, health, movement, distribution, phenology, development and reproductive success) and then assesses their combined impact through statistical analyses. It revealed that amphibian calling is the most vulnerable aspect to the combined impacts. This could provide important input for conservation of amphibians.

KEYWORDS Amphibians, light, global warming, noise

INTRODUCTION Amphibians are good model organisms to assess the Amphibians play critical roles in food webs, and often link ter- potential impact of humans on biodiversity because of their restrial and aquatic ecosystems (Bickford et al.2010 ). They also trophic importance, environmental sensitivity, research tracta- affect ecosystem structure through soil burrowing and aquatic bility and impending extinction (Hopkins 2007). Therefore, the bioturbation, and provide ecosystem functions such as decom- present review has been undertaken to understand the composition and nutrient cycling through waste excretion (Hocking bined effects of three environmental problems (noise, light pol- & Babbitt 2014). However, these organisms are threatened by lution and global warming) on amphibians. several factors in the present times, and are declining at a fast- The review is the first-hand approach to make a com- er rate than birds and mammals (Stuart et al. 2004; Beebee & bined valuation of the overall impact of the three issues on Griffiths 2005). In fact, the global amphibian decline is a formi- amphibians. It understands the respective negative impacts of dable environmental problem of the late 20th century (Daszak the three issues on amphibians, and then divides the overall et al. 1999). Amphibians often have complex life histories; their impacts into seven categories (behaviour, health, movement, permeable skin fulfils several physiological functions and is distribution, phenology, development and reproductive suc- sensitive to the micro climatic conditions as well as to pollut- cess). Below I will provide a short overview of the relevance of ants. Because of these traits, amphibians are more sensitive to the three issues for biodiversity. human related environmental changes than other vertebrates, currently being in global decline (Kerby 2010). European Journal of Ecology European Journal of Ecology

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Noise Global warming Noise is an environmental force that alters the behaviour and The current trend of global warming is highly significant be- distribution of many wild vertebrates (Francis et al. 2012), and cause most of it is human-induced and taking place at an un- exerts selection pressure on acoustic signals (Ryan & Brenowitz precedented rate in the past 1,300 years (Whelan et al. 2008). 1985). It has the potential to severely affect wildlife (Brumm Greater heating effect of higher atmospheric levels of green- 2010). In fact, human induced acoustic environment is a selec- house gases like carbon dioxide, methane, nitrous oxide and tive force that alters communication patterns of many vocaliz- chlorofluorocarbons due to anthropogenic activities mainly ing anurans (Roca 2016). This is because a decrease in acoustic cause global warming (US EPA 2016). Annual worldwide emis- habitat due to anthropogenic noise acts as an environmental sion of such gases has continued to increase, reaching 49.5 bil- stressor on sensitive animal groups (Nelson et al. 2017). lion tonnes (Giga tonnes or Gt) of carbon dioxide equivalents

During the recent past, urbanization and develop- (CO2 eq) in 2010. This was the highest level till that date. The ment in the transport sector have increased the levels of noise rate of growth of such gases in the last decade (2000–2010) (Fuller et al. 2007). More powerful sources of noise, greater was double than the rate in any other decade since 1970 (Vic- geographical spread and mobility of noise sources, and a great- tor et al. 2014). Under these circumstances, heat-waves and er proportion of the day being exposed are important reasons wildfires have been projected to increase, whereas soil-mois- for this (Berglund & Lindvall 1995). Its intensity has also been ture availability is projected to decrease, due to greater evapo- increasing in many previously intensively developed regions ration (Engelbrecht et al. 2015). (Berglund & Lindvall 1995). Noise is expected to increase in the Biodiversity is impacted due to climate change and coming decades, but few studies have investigated the effects many species are likely to suffer declines or undergo extinc- of anthropogenic noise on anurans (Caorsi et al. 2017). tion (Foden et al.2013 ). It is because prominent environmental parameters of climate change such as temperature, solar radia- Light tion, humidity, cloud cover and precipitation have implications The rapid global increase in artificial lighting has transformed for biodiversity (Bickford 2010). nightscapes both in quantity and quality (Hölker et al. 2010). Such a change in the nocturnal environment is true pollution and exerts negative environmental and wildlife health impacts 1. MATERIAL AND METHODS (Cinzano 2002). Artificial light that alters the natural patterns of Scientific publications on the subject(s) were downloaded light and dark in ecosystems is known as ‘ecological light pol- from ‘Google Scholar’ using suitable search words such as lution’ (Longcore & Rich 2004). The linkage between economic ‘noise’, ‘global warming’, ‘light pollution’ and ‘amphibians’. activity, population increase and artificial light is evident in- sev Dutta (2018) had also used ‘Google Scholar’ to obtain scientific eral developing regions (Bennie et al. 2013). publications to review certain aspects of alien plant invasion. Artificial light at night exerts non negligible impacts However, in this case, information was also collected from a on fauna and flora (Aube´ 2015) and affects a wide variety of few reliable online sources to supplement the qualitative data taxonomic groups (Dananay 2013). It has been recently gain- obtained from the downloaded peer-reviewed articles. The ing attention in terms of its effects on diurnal and nocturnal literature was divided into proper subheads and organized. animals. Such impacts can extend up to population, commu- Thereafter, the combined effect of noise, light pollution and nity and ecosystem levels (Baker & Richardson 2006). This is global warming was assessed through categorization, followed because animals and ecosystems are severely affected when by tabulation. the natural cycle of light and darkness is altered by artificial light (Horváth et al. 2009). Artificial light has the potential to 1.1. Categorization alter individual behaviour as well as negatively affect biologi- I created seven categories (behaviour, health, movement, dis- cal rhythms, daily activity and reproduction (Raap et al. 2015). tribution, phenology, development and reproductive success), Blue-rich light at night has a greater capacity to alter circadian each of which represented a particular amphibian trait. The rhythm and photoperiod in the animal kingdom. Hence, blue- purpose was to convert qualitative information into empirical rich light exerts higher negative impacts on wildlife than yellow data through subsequent tabulation based on these categories light, which has lower ecological consequences (International and the three problems. These specific categories were se- Dark-Sky Association 2010). However, in addition to circadian lected because they comprehensively summarized the impacts clocks, night-time lighting also exerts negative effects on time of all the three issues. Thus, this categorization could be done partitioning and immigration/emigration of fauna (Gaston and only after understanding all the effects of the three issues on Bennie 2014). It also affects the social interactions and group amphibians. dynamics in several animals by altering individual activity patterns of individuals, reducing behavioural synchrony in social 1.2. Tabulation processes, affecting the communication between individuals The problems and the categories were subjected to two types and lowering social competence (Kurvers and Hölker 2015). of tabulation that gave rise to two tables (Tables 1 and 2). The first type was based on the seven affected categories. In this

16 EUROPEAN JOURNAL OF ECOLOGY type, the three problems were tabulated according to the re- decreased orientation towards the target signal under traffic spective categories they affected (Table 1). From Table 1, the noise (Bee & Swanson 2007). number of problems affecting each of the seven categories Anurans develop behavioural responses that enable could be obtained. the transmission of information and overcome masking of sig- The second type was based on the three problems. In nals in noisy conditions (Vargas-Salinas 2014). They cease to this type, the seven categories were tabulated according to the call, call faster or modify frequency or amplitude of calls in such respective problems that affected them (Table 2). From Table environments (Tennessen et al. 2014). This is evident in the 2, the number of categories affected by each of the three prob- males Bornean Rock frogs (Staurois parvus), which modify their lems could be obtained. Now, the three problems in Table 2 amplitude, pitch, repetition rate and duration of notes of ad- represented three distinct variables. The number of categories vertisement calls in noisy circumstances (Grafe et al.2012 ). It is affected by a variable (i.e., a problem) was considered as the in fact the plasticity in anuran vocalizations, which enables the value of that particular variable. Thus, there were three differ- maintenance of acoustic communication in traffic noise (Cun- ent variables, each of which had a particular value. Chi-square nington & Fahrig 2010). The Southern Brown Tree Frog (Litoria test was performed among the values of these variables. In ewingii) emits calls at elevated pitch levels under traffic noise other words, the test was performed among the number of (Parris et al. 2009). Such higher rates of vocalizations elevate amphibian traits affected by noise, light and global warming. amphibian aerobic metabolism up to 22 times, which in turn leads to physiological consequences and behaviour alterations. The latter effect hampers the breeding success. The collective 2. RESULTS impact affects the overall population growth and persistence. Greater vocal output triggered by noise can exert impacts at 2.1. Impacts of Noise both individual and the chorus-levels (Kaiser et al. 2010). The Cauca Poison frog Andinobates bombetes has been found to 2.1.1 Behaviour (Vocalizations) call more often, when traffic noise is lower (Vargas-Salinas & Noise interferes with anuran chorus, triggers changes in call Amézquita 2013). In case of Boana bischoffi and Boana lepto- rates and suppresses calls of one set of species, which in turn lineata, acoustic parameters are changed during or after the stimulates calling in other species (Sun & Narins 2005). Low- exposure to traffic noise. InBoana bischoffi, the advertisement frequency signals are more likely to get masked by anthropo- call rate decreases during road noise, and dominant frequen- genic noise (Vargas-Salinas 2014). Noise can even cause am- cy decreases over time. The call length of Boana leptolineata phibian male choruses to end before the arrival of the female changes, depending on the order of noise intensity (Caorsi et and thus reduce mating opportunities (Kaiser et al. 2010). In al. 2017). On the other hand, males of Pickersgill’s Reed frog addition, noise can cause deaths in amphibians. For instance, (Hyperolius pickersgilli) change temporal and spectral proper- female Wood Frogs (Lithobates sylvaticus) are unable to locate ties of calls during and after airplanes flyby (Kruger & Du Preez, male calls, in the presence of noise. Consequently, their move- 2016). Alterations in calling are also evident in Crawfish Frogs ment could be directed towards noisy roads and lead to ac- (Lithobates areolatus) (Engbrecht et al. 2015) as well as Gray cidents (Tennessen et al. 2014). In fact, roads result in severe Tree frog Hyla versicolor and Green Tree frog Rana clamitans effects on amphibians (Hoskin & Goosem 2010) because even (Cunnington & Fahrig 2012) in response to traffic noise. the most subtle road disturbances can exert profound impacts (Maynard et al. 2016). This is evident in female Cope’s Gray 2.1.2 Physiological effects Frogs (Hyla chrysoscelis), which exhibit greater latency and Noise exposure elevates stress hormone levels and induces im- munosuppressive effects in amphibians. Higher levels of noise

Table 1. Tabulation of affecting problems (Noise, Light and Global Warming) according to the affected amphibian categorical aspect

Affected aspect Affecting problems Remarks

1). Behaviour Noise, Light and Global Warming Amphibian mating calls are altered in response to all the three problems; Light affects foraging

2). Health Noise and Global Warming Noise triggers physiological changes; Global Warming exerts heat stress and triggers disease outbreaks

3). Movement Light Light impairs vision and hampers movement

4). Distribution Global Warming Global Warming changes species range

5). Phenology Global Warming Global warming changes timing of breeding

6). Development Global Warming Global Warming hampers larval development

7) Reproductive success Global Warming Global Warming negatively affects offspring survival

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Table 2. Tabulation of affected amphibian aspects/categories according to the affecting problems (Noise, Light and Global Warming)

No. of aspects χ2-test (among the number Names of affected categories/ Affecting problem affected by each of aspects affected by each aspects problem problem)

Noise Health, Behaviour 2

Light pollution Movement, Behaviour 2 χ2 = 3.2, df = 2, p > 0.05 Behaviour, Health, Distribution, Phenology, Develop- Global warming 6 ment and Reproductive success and stress hormone negatively affect the vocal sac colouration buildings. Certain anurans are also attracted to streetlamps at in the European Tree frog Hyla arborea, which in turn also af- night due to a greater availability of insects for hunting under fects sexual selection (Troïanowski et al. 2017). Noise has also illumination. On the contrary, the fossorial Red-backed Sala- been found to increase the secretion of stress-relevant glu- mander (Plethodon cinereus) forages less in brighter areas; cocorticoid hormone (corticosterone) in female Wood Frogs compared with darker areas, it also displays greater visual (Lithobates sylvaticus) and this can have substantial conse- threats in illuminated areas (Rich & Longcore 2006; Perry et quences even at the population-level (Tennessen et al. 2014). al. 2008). The preference for foraging site is not affected by In White’s tree frogs, Litoria caerulea, anthropogenic noise not light in Wood Frogs (Rana sylvatica), but Blue-spotted Sala- only increases corticosterone concentrations in circulations, manders (Ambystoma laterale) prefer deciduous litter in dark but also negatively affects the sperm count and viability. This and coniferous litter under greater illumination. Artificial light- proves that noise can change physiology and Darwinian fitness ing can also attract such salamanders to substrates that are not (Kaiser et al. 2015). usually preferred (Feuka et al. 2017).

2.1.3 Additional effects of noise 2.2.2 Vision and movement Noise, in the presence of light pollution, can disrupt the Orientation is the primary determinant of successful amphib- host-parasite interaction, as evident in the case of frog‐biting ian movements between habitats (Mazerolle & Vos 2006). midges (Corethrella spp.) and their túngara frog (Engystomops However, nocturnal car traffic emits light and noise that trig- pustulosus) hosts (McMahon et al. 2017). In addition, anthro- ger immobility in amphibians at the approach of the vehicles. pogenic noise causes acoustically communicating Marsh Frogs Consequently, amphibians become highly vulnerable to road (Pelophylax ridibundus) to leave burrows or change locomotion mortality (Mazerolle et al. 2005). Street lighting also increases (Lukanov et al. 2014). this risk by attracting migrating amphibians (van Grunsven et al. 2017). This is relevant in the case of pond-breeding amphib- 2.2. Impacts of Light ians, which move across the landscape to their breeding, sum- mering or hibernation grounds and thus, frequently encounter 2.2.1 Behaviour (Vocalizations and foraging) roads. In case of certain species (e.g., American toads Bufo Artificial light affects the calling behaviour in several amphibian americanus), the rate road mortality increases with an increase species in natural, mixed assemblages. The number of calling in traffic intensity, whereas in others, the mortality is greater individuals and call index decreases in frogs in response to the in lower (Spring peeper Pseudacris crucifer) or moderate (e.g., acute light input (Hall 2016). When frogs stop mating calls upon Ranid frogs) levels of traffic (Mazerolle 2004). In fact, several exposure, their reproductive capacity is reduced (Longcore & amphibians are killed by traffic on their way to reproduction Rich 2004; Chepesiuk 2009). The effect of light pollution is evi- sites during spring migration in Western Europe (van Grunsven dent in the male green frogs (Rana clamitans melanota), which et al. 2017). produce fewer advertisement calls and move more frequently A sudden increase in illumination due to artificial in the presence of artificial light, compared with ambient light lighting reduces the visual capability of frogs, which might re- conditions. Its behaviour is affected by artificial light in a man- quire hours to recover (Buchanan 1993). Frogs might also be ner that has the potential to reduce recruitment rates and thus attracted to light after such recovery (Jaeger & Hailman 1973). affect population dynamics (Baker & Richardson 2006). On the In addition, night lighting can stimulate phototactic behaviour, other hand, male tree frogs, Smilisca sila (Hylidae) emit fewer which inhibits movements of amphibians to and from breeding and less complex calls, and tend to call from more concealed areas (Longcore & Rich 2004). Further, alteration in the polar- sites, in the absence of illumination (Tuttle & Ryan 1982). ization of light due to human activities also affects amphibian Another behaviour affected by light is foraging, as movements as they have well-tuned polarized vision. Changes evident in certain nocturnal frogs, like Cane Toads (Bufo mari- in polarization occur due to interaction with human-made nus), which forage regularly under enhanced illumination near structures (Horváth et al. 2009).

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2.2.3 Additional effects of light also likely to expand distributions, as warming in the colder Light facilitates predation by visually orienting predators, and ranges creates scope for colonization. Inability to disperse hence, can increase their activities. Consequently, activities of causes species to lose range (Araujo et al. 2006). This is under- prey could be reduced due to a higher risk of predation. Diurnal stood from the fact that the suitable habitat of amphibians is and crepuscular predators could become facultative nocturnal likely to be shifted to higher altitudes and latitudes due to cli- predators under suitable lighting (Gaston et al. 2013). On the mate change in China (Duan et al. 2016). In central and western other hand, female Tungara frogs (Physalaemus pustulosus), South America, amphibians have also been predicted to under- under increased levels of light, become less selective about go a higher range contractions by 2071 due to climate change mate choice and tend to mate quickly and avoid predation risk (Lawler et al. 2010). In fact, changes in temperature patterns (Rand et al. 1997). have been associated with altitudinal range increase in amphibians after the retreat of Andean glaciers as well as in Malagasy 2.3. Impacts of Climate change massif (Seimon et al. 2007; Raxworthy et al. 2008). Moreover, global warming has brought about changes in patterns and in- 2.3.1 Population decline and extinctions tensity of El Nino Southern Oscillation, an event that impacts Decline and extinction of amphibian populations on account of biological productivity of the ocean, as well as community dis- climate change has taken place all over the world (Pounds et al. tribution near shores (Carey & Alexander 2003). 2006; Araujo et al. 2008; D’Amen & Bombi 2009). Species with a lower ability to disperse (Ochoa-Ochoa et al. 2012) and nar- 2.3.3 Phenological changes row tolerances for temperature and moisture (Olson & Saenz Phenology in some amphibian species has been altered by cli- 2013) are at a high risk. About 75% of amphibian and reptile mate and this is likely to expose them to fluctuating weather communities have declined in La Selva Costa Rica during the conditions (Olson & Saenz 2013). This is because reproduction last 35 years and climate-driven loss of leaf litter has been cited is closely linked to environmental cues and climate change can as a cause (Whitfield et al. 2007). A decline of 50% amphibian alter the timing of reproduction in many species (Blaustein population in Yellowstone National Park has been correlated 2010). Most temperate amphibian species remain inactive for a with temperature elevation and precipitation reduction over major part of the year. Upon subtle temperature and moisture the last 60 years (McMenamin et al. 2008). Unusual frost and increments, they immediately proceed to breed in water bod- weather conditions have led to the disappearance of amphib- ies. In such amphibians, global warming can induce early breed- ians in south-eastern Brazil (Heyer et al. 1998) and Costa Rica ing as temperatures increase (Araujo et al. 2006). (Crump et al. 1992) respectively, whereas droughts have caused The fact that global warming triggers earlier breeding population declines of Brazilian frogs in the Atlantic mountains in amphibians is evident from the changes in the phenology of (Weygoldt 1989). Fowler’s Toads (Anaxyrus fowleri), which is a late-breeding of According to Bickford et al. (2010), amphibians would spring (Green 2016). Amphibians have exhibited early breeding be adversely affected by the projected rapid climate change. in Japan (Kusano 2008) and New York (Gibbs and Breisch 2001) They state that within 50 years, the capacity of amphibians to and the fact is also evident in the newts of genus Triturus (Chad- adapt to climate change in Southeast Asia would be surpassed; wick et al. 2006). Although such preponed amphibian breeding indicating greater extinctions. However, up to 66 percent of am- has been recorded, the resulting consequences have not yet phibians identified by a study as highly vulnerable to climate been understood (Carey & Alexander 2003). change is not in the IUCN Red List of Threatened Species. These species have shown a sharp decline in the population or a 2.3.4 Behaviour (Mating) shrinking geographic range (Foden et al. 2013). Climate change Frequency of mating calls and mating success in amphibians even combines with other factors such as UV-B radiation and are influenced by temperature fluctuations (Gerhardt & Mudry contaminants and leads to complex implications that causes 1980). accelerated amphibian population declines and extinctions (Blaustein 2010). 2.3.5 Reproductive failure According to Foden et al. (2008), 52% of amphib- Amphibians are highly vulnerable to precipitation alterations as ian species are vulnerable to climate change due to special- water availability is necessary for the survival of their eggs and ized habitat requirements, limited dispersal ability and water- larvae (Araujo et al. 2006). Fluctuations in rainfall also affect dependent larvae. In this regard, amphibians depending on amphibian egg-laying (Caldwell 1987). Greater climatic fluctua- ephemeral ponds, coastal wetlands, arid and semi-arid sys- tions can also lead to seasons witnessing episodic mass mortal- tems, or alpine areas are at a high risk (Kundzewicz et al. 2007; ity or ‘bust’ years (Olson & Saenz 2013). IPCC 2007; Rios-López 2008; Brooks 2009). In addition, frogs that lay their eggs on land could experience heavy mortality arising due to lower soil moisture 2.3.2 Changes in distribution as well as elevated evaporation in dry and hot environments Due to climate change, the distribution of amphibians under- (Bickford et al. 2010). Early drying up of habitats due to changes goes changes (Munguı´a et al. 2012). Several amphibians are in climate results in mass mortality of eggs, tadpoles and meta-

19 EUROPEAN JOURNAL OF ECOLOGY morphosing individuals (Blaustein & Olson 1991). Moreover, because amphibian body temperatures are determined primar- this can also increase exposure to predators because when ily by heat exchange with air, water and/or soil or solar heat the water boundary recedes, amphibian refuge is lost (Olson & gained from the sun (Hutchison & Dupré 1992). Skin perme- Saenz 2013). Amphibians, depending on ephemeral ponds and ability, biphasic lifecycles and shell-less eggs are some features streams for reproduction, are the most vulnerable (Olson & that also make amphibians vulnerable to climatic changes (Car- Saenz 2013). In addition, warmer temperatures can also upset ey & Alexander 2003). Elevated temperatures can alter water sex-determination in some species (Eggert2004 ). regulation, oxygen uptake, emergence, mating, development, metamorphosis, growth and sex reversal in amphibians (Feder 2.3.6 Larval development & Burggren 1992). Larval gametogenesis and growth rates as well as post-meta- morphic growth rates dependent on temperature and thus, are 2.4.1 Combined effect of noise, light pollution and global affected by global warming (Beebee 1995; Carey et al. 2003). warming Increased water loss from bodies of metamorphosed amphib- Tabulation of the seven categories (behaviour, health, - move ians under higher temperatures, along with their inability to ment, distribution, phenology, development and reproductive produce concentrated urine, increases the risk of desiccation success) and the three problems, led to the assessment of the (Shoemaker et al. 1992). Global warming is also likely to influ- combined effects. When the three problems were tabulated ac- ence the availability of autotrophic food organisms consumed cording to the respective categories (i.e., traits) they affected, by several tadpoles due to the increase in primary production amphibian behaviour was found to be affected by all the three and nutrient cycling occurring due to increased temperatures issues. This was followed by health, which was affected by two (Meyer et al. 1999). problems (noise and global warming). All the remaining five Warming decreases the level of dissolved oxygen in traits were affected by only a single problem (Table 1). aquatic habitats that hampers embryonic and larval develop- When the seven categories were tabulated accord- ment and accelerates/suppresses hatching (Rome, Stevens and ing to their respective affecting problems, global warming was John-Alder 1992; Mills & Barnhart 1999). Moreover, under low found to affect six categories, whereas noise and light were oxygen levels, larvae tend to move to the water surface more found to affect two categories each. There was no significant frequently to collect air; consequently, lesser time is used for difference (χ2 = 3.2, df = 2, p > 0.05) in the number of amphibian foraging and growth and development is hampered (Wassersug categories affected by noise, light and global warming (Table 2). & Seibert 1975). The overall negative impacts of the three issues have been depicted in Fig. 1. 2.3.7 Incidence of diseases Climate change indirectly facilitates infectious disease epi- demics (Carey & Alexander 2003). It can alter the ranges of 3. DISCUSSION pathogens, hosts and vectors, as well as the mode of disease The literature survey and its analyses very well prove that noise, transmission and alter pathogen-host dynamics in amphibians light and global warming are multidimensional environmental (Blaustein et al. 2010). Global warming has already triggered forces that affect amphibians at different levels of the biological certain pathogen outbreaks that have led to mass extinctions organization. With greater urbanization and human develop- in the recent times (Pounds et al.2006 ). Monteverde Harlequin ment, their negative impacts are likely to intensify. Amphibians Frog (Atelopus sp.), Golden Toad (Bufo periglenes) and about exhibit moderate relative responses to water-borne toxins and 67% of approximately 110 species of genus Atelopus, endemic are not particularly sensitive to chemical contaminants (Kerby to the American tropics faced extinction due to Chytrid Fun- et al. 2010), but they are highly vulnerable to the three prob- gus (Batrachochytrium dendrobatidis). This has been linked lems discussed. An important drawback in this regard is the fact with rising temperatures due to global warming that shifted that alterations in amphibian distribution and community as- this pathogen to these areas, leading to outbreaks (Pounds et semblages under changing habitats due to human modification al. 2006). In fact, increasing temperatures in higher altitudes have not been understood (Kruger et al. 2015). are creating conditions optimum for the accelerated outbreaks The acoustic mode of communication makes an- of Batrachochytrium (Pounds et al. 2006). On the other hand, urans highly vulnerable to noise. This is because noise is an decrease in depths of water bodies due to climate change in- important determinant of such a communication, apart from creases exposure of amphibian embryos to ultraviolet (UV-B) the power generated from source of sound, environmental radiation, which in turn elevates infection risk by Saprolegnia features through which signals propagate, and receiver sensi- ferax causing greater egg mortality in amphibians (Kiesecker et tivity (Penna et al. 2013). In this regard, the acoustic adapta- al. 2001). tion hypothesis states that communication signals have been shaped by evolution in a manner that minimizes degradation 2.4. Direct impact of heat and maximizes contrast against the background noise (Vargas- Amphibians are ectothermic, and hence are affected directly or Salinas & Ame´zquita 2013). When such signals are obstructed indirectly by changes in their climate (Araujo et al. 2008). This is by noise, mating in amphibians is hampered. This is because

20 EUROPEAN JOURNAL OF ECOLOGY

Figure 1. Combined impact of the noise, light pollution and global warming in amphibians (Numbers in parentheses correspond to the serial numbers in Table 1)

the loud male sexual advertisement signals are required to cal requirements should be understood and noise production elicit responses from reproductive females, communicate with should be regulated according to their behaviour and needs in other males during interaction over calling sites and territories general. This could include strategies to reduce at particular (Vélez et al. 2013). In response to noise, frogs elevate their call seasons. However, an important obstruction in understanding amplitude, an aspect which requires further study (Schwartz & the effects of noise is limited knowledge about the hearing ca- Bee 2013). Noise also affects lizards in which sensitivity is influ- pacity of animals and characteristics of emitted sounds in natu- enced by changes in temperature and is usually the highest in ral environments (McGregor et al. 2013). their ranges of activity (Campbell 1969). Amphibians and reptiles have not evolved with arti- There is a necessity of adequate planning of develop- ficial night lighting, and hence, their physiology, behaviour and ment to avoid the negative effects of noise. If this could not be ecology are prone to the problem (Perry et al. 2008). Different achieved, noise control practices should be planned along with species exhibit different activity patterns under different light the development of infrastructure. An inventory of wildlife that conditions, and hence, alterations in lighting can increase or could be affected by noise should be prepared, their biologi- decrease competition among species. A native gecko species in

21 EUROPEAN JOURNAL OF ECOLOGY

Hawaii gets out-competed by another species during the pres- addition, greater knowledge of the environmental factors that ence of clustered insect distributions caused by lights (Petren enable organisms to get rid of winter dormancy will lead to a & Case 1996). Artificial night lighting can also cause disorien- greater understanding of long‐term phenological trends under tation in marine turtles during sea-finding (Tuxbury & Salmon climate change (Green 2016). 2005). Reptiles are also affected by climate change, but the Lights that match the normal, nocturnal spectra have implications of warming on reptiles have not been properly the least effects on anurans, and hence, should be used in am- studied (Araujo et al. 2006). Reptiles neither have the mobil- phibian habitats (Buchanan 2006). Trees can also be helpful in ity of birds nor are capable of regulating body temperature mitigating the impacts of excessive artificial lighting. In fact, the and are only able to move minimally under changing climates role of tree canopy with respect to light is evident in natural (US Geological Survey 2014). Climate change leads to up- ecosystems. This could be understood by the fact that changes ward migration and biased sex ratio in reptiles (Janzen 1994). in canopy coverage influence light penetration, which in turn Some reptiles have been projected to suffer severe decrease affects amphibian population dynamics in wetlands within for- in ranges between 2010 to 2099; for example, Plateau Striped ested biomes (Halverson et al. 2003). In fact, gradients arising Whiptail (Aspedoscelis velox), Arizona Black Rattlesnake (Cro- due to canopy cover over ponds influence the larval distribu- talus cerberus), Common Lesser Earless Lizard (Holbrookia tion among ponds (Skelly et al. 2002). Proper plantation of maculata) and Common Chuckwalla (Sauromalus ater) (US trees taking into consideration the topography of an area and Geological Survey 2014). Mitigation of climate change can only the source of light could be an efficient mitigation measure. In be achieved through the reduction of greenhouse gas emission addition, comprehensive investigations on the ecological light controlled through proper regulations. There is also a need pollution with the collaboration of physical scientists and en- to change attitudes on the interaction with and utilization of gineers are also required (Longcore & Rich 2004). Halfwerk & biological systems (Bickford et al. 2010). For the proper con- Slabbekoorn (2015) have suggested an integrated multimodal servation under climate change, critical habitats for amphibian approach in order to understand the complete ecological con- protection should be identified (Guisan et al. 2013). sequence of human activities on animal performance and per- When the combined effect of the three problems was ception. They have emphasized that more empirical studies considered, amphibian behaviour was identified as the most should be conducted on the covariance among sensory condi- vulnerable aspect. Calling was found to be at a high risk in this tions, such as, correlation between noise and light pollution. context because it was affected by all the three problems. This Global warming can severely affect amphibian fauna can have severe negative consequences in mating because because changes in temperature, precipitation, humidity and amphibian calls are crucial signals to attract mates and con- soil moisture affect their physiology, behaviour and ecology sequently reproduction would be affected (discussed earlier). of (Blaustein 2010). It also increases pathogen development This is a serious issue because reproduction is the main factor and survival rates, disease transmission and host susceptibility that efficiently maintains variation and inheritance and is the (Harvell et al. 2002). In fact, climate change has been promot- primary requisite of organic evolution (East 1918). ing infectious disease and eroding biodiversity; thus, reduction The fact that there was no significant difference in in greenhouse-gas concentrations is required (Pounds et al. the number of amphibian traits affected the three problems 2006). To add to this is the limited dispersal ability in amphib- indicated that the negative effect of global warming would not ians and reptiles, which makes these species further more vul- be the primary determining factor in determining the overall nerable to changes in climate (Araujo et al. 2006). Therefore, negative impact. In other words, the effect of light and noise future projected climate changes can pose challenges for the would not be negligible. On the contrary, a significant differ- surviving amphibian populations (Carey & Alexander 2003), ence would have indicated that global warming would be the leading to population declines and extinctions. In fact, lethal main determinant of the combined impact of the problems be- temperatures have already been measured in a number of am- cause it affected the highest number of amphibian traits. Thus, phibians across several habitats (Rome et al. 1992). The risk no problem should be neglected and mitigation measures of extinction is greater in higher elevation species as land or should be taken for all the three. However, while devising such habitat availability decreases with increase in altitude (Benning measures, habitat fragmentation should also be considered be- et al. 2002). Climate change has been projected to cause con- cause decrease in landscape connectivity due to fragmentation siderable damage to the Appalachian Mountains in US which is and habitat loss affects amphibian assemblage and reversal of a hotspot for salamander biodiversity (Milanovich et al. 2010). such changes is an important conservation strategy (Lehtinen The risk of extinction is higher in case of endemics et al. 1999). Moreover, there could be a number of ecological and restricted range species that have minimal or no space for consequences of fragmentation and habitat loss that could ac- upward movement or which are incapable of shifting upwards tually magnify the impacts of the above issues and vice versa. due to physiological effects of geographical gradients (Lawler In addition, there are anthropogenic activities that could have et al. 2009). However, direct causal relationships between am- their own consequences on amphibians. For instance, peat phibian declines and the correlated climate events need fur- mining changes the activity and movement of amphibians in ther research to be understood (Carey & Alexander 2003). In bog fragments. The ability of larger species to survive in such

22 EUROPEAN JOURNAL OF ECOLOGY disturbed environments is better than the smaller species, as existing anthropogenic activities should be taken into account. they are less sensitive to desiccation (Mazerolle 2001). Thus, An effective solution can be then be devised and amphibians it is understood that the problems are required be studied for can be conserved. the combined assessment of impacts to devise mitigation measures. However, while doing so, other ecological problems and Conflict of interest:The author declares no conflict of interest.

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EJE 2018, 4(2): 41-48, doi: 10.2478/eje-2018-0011

Trends of phanerophyte encroacher species along an aridity gradient on Kalahari sands, central Namibia

1 Faculty of Natural W.N. Hauwanga*1,2, B. McBenedict2 and B.J. Strohbach1 Resources and Spatial Sciences, Department of Natural Resource Management, Namibia ABSTRACT University of Science Poor rangeland management, especially overstocking and under-burning coupled with climate change on south- and Technology, P/Bag 13388, 13 Storch Street, ern African savannas, have brought about a serious ecological problem of bush encroachment. Bush encroach- Windhoek, Namibia. ment leads to many ecological implications such as extirpation or extinction of plant species and a colonisation Corresponding author, by opportunistic species leading to unwanted changes in plant species composition, structure and loss of spe- E-mail: willyhauwan- cies diversity. Furthermore, bush encroachment has a negative impact on the country’s progress in terms of [email protected] conservation efforts, economic stability and livelihood. Namibian livestock ranchers forego an estimated N$ 700 2School of public health, million loss yearly linked to bush encroachment. Studies focusing on particular bush encroacher species enable Department of Environ- the devise of ecologically sound management strategies by land manager, farmers and scientists for the preven- mental and Occupational tion and control of bush encroachment. Therefore, this study was undertaken to determine the main encroacher health, University of Namibia, P. O Box 2654, species and their relationship to the environmental factors along an aridity gradient on Kalahari sands in central Eliander Mwatale Street, Namibia. Results disclosed that Acacia erioloba E.Mey., Acacia mellifera (Vahl) Benth. ssp. dentines (Burch.) Oshakati West, Namibia. Brenan, Combretum collinum Fresen., Terminalia sericea Burch. Ex DC., Grewia spp., Bauhinia petersiana Bolle ssp. macrantha (Oliv.) Brummitt & J.H. Ross were the main encroacher species, and mean annual rainfall was the main environmental factor influencing their distribution. Nanophanerophyte from different encroacher species were recorded mainly from 400 mm to 500 mm mean annual rainfall, mesophanerophyte recorded from 280 mm to 450 mm, while microphanerophyte were widely distributed over the rainfall gradient. Bush encroachment was recorded at 440 mm mainly due to the poor rangeland management. Information from this study should be used as a baseline for conservation and restoration attempts towards savanna rangelands. KEYWORDS Bush encroachment, density, environmental factors, Kalahari sands, aridity gradient

© 2018 W.N. Hauwanga et al. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivs license INTRODUCTION competition from grasses coupled with increased soil moisture Southern African savannas are faced with a serious ecological availability culminates into survival and growth of woody plant problem of bush encroachment whereby the agricultural pro- seedlings into bush thickets. These corroborate with the widely ductivity gets affected. For example, studies have shown that documented trend of increasing woody plants with mean an- about 10–20 million ha in South Africa (Ward 2005), 3700000 nual rainfall on the savanna ecosystems (Scholes et al. 2002; ha in Botswana (Moleele et al. 2002) and 26 million ha in Na- Sankaran et al. 2005, Kgosikoma and Mogotsi 2013 and Archer mibia (De Klerk 2004) has been affected by bush encroach- et al. 2017). ment. According to Roques et al. (2001), De Klerk (2004) and Namibia is one of the southern African countries that Ward (2005), the main factors causing bush encroachment on is highly vulnerable to the adverse effects of bush encroach- southern African savannas are climate change and poor range- ment due to its high dependence on agriculture and tourism. land management especially overstocking and under-burning. According to Magwedere et al. (2012), agriculture supports Bush encroachment is basically the expansion of woody veg- about 70% of the Namibian population. However, only a small etation at the expense of the herbage vegetation in savanna percentage of the soil is suitable for crop farming (< 1%), lead- ecosystems. Savannas are characterised by unpredictable dry ing to livestock and wildlife farming dominating. This has re- and rainy seasons. This makes savannas rather unstable and sulted to a greater economic weight currently placed on the susceptible to bush encroachment since bush encroachment meat industry and the tourism sector in Namibia (Magwedere has been associated with inter-annual rainfall variability (An- et al. 2012). However, the meat industry and tourism sector

gassa and Oba 2008; Kulmatiski and Beard 2013). Reduced is threatened by loss of suitable habitants for animals due to European Journal of Ecology

41 EUROPEAN JOURNAL OF ECOLOGY bush encroachment. Bush encroachment leads to many eco- The present study successfully identified the relation- logical implications such as, extirpation or extinction of species, ship between several encroacher species and environmental for example, bush encroachment has been associated with the factors along the aridity gradient on Kalahari sands in central extinction of Gyps coprotheres in Namibia (De Klerk 2004). In Namibia. The Kalahari forms a clear south to north gradient of addition, bush encroachment leads to colonisation of savan- increasing mean annual precipitation of 150 mm per annum to nas by opportunistic species leading to unwanted changes in over 1200 mm per annum (Scholes et al. 2002). This gradient species composition and structure. Ratajczak et al. (2012) de- extends from the vineyards on the margins of the Orange River termined the consequences of woody encroachment on plant at Upington, South Africa to the north of the Congo River into species richness by performing a meta-analysis of 29 studies the south-east corner of Equatorial Gabon (Thomas 2002). The from 13 different grassland/savanna communities in North main aim of the study was to identify bush encroacher species, America. Ratajczak et al. (2012) results depicted a decrease their dominant life forms and their relation to environmental in the species richness with an increase in the woody plant factors along an aridity gradient on Kalahari sands in central encroachment in all 13 communities. Furthermore, bush en- Namibia. croachment has a negative impact on the country’s progress in terms of conservation efforts, economic stability and livelihood. This corroborates with De Klerk (2004) and Joubert et 1. MATERIALS AND METHODS al. (2008) who stated that the Namibian livestock ranchers forego an estimated N$ 700 million loss yearly linked to bush 1.1. Study sites encroachment. Kalahari is a sandy, largely semi-arid region that lies within Since the realisation of bush encroachment, several the southern African summer rainfall zone (Thomas and Shaw efforts have been directed to bush control. First by farmers and 1991; Scholes et al. 2002; Thomas 2002). According to Wang later by scientist, government and non-governmental organisa- et al. (2007), the Kalahari gradient is an ideal environment to tions. The Namibian government has declared the control of study changes in; ecosystem dynamics, vegetation composition bush encroachment as a national priority in its fifth National and structure, and nutrient cycles along a spatial precipitation Development Plan (NDP5). Several studies have been conduct- gradient without confounding soil effects. The significance of ed on bush encroachment in Namibia (Bester 1999; De Klerk the Kalahari transect is well known and acknowledged since it 2004; Zimmermann et al. 2008; Christian et al. 2010; Stafford has been designated as one of the International Geosphere– et al. 2017). Acacia mellifera and Dichrostachys cinerea con- Biosphere Program (IGBP) transects designed to address the secutively are the most widely distributed encroacher species global change questions at the regional scale (Kochet al. 1995; in the country and have the ability to change vegetation type Scholes and Parsons 1997; Privette et al. 2004). The present (De Klerk 2004). The latter led to their classification as the most study analysed the trends of encroacher species on Kalahari aggressive encroacher species in Namibia. These species can sands in central Namibia by exploring five sites, namely Mile change savannas consisting of various species to predomi- 46, Sonop, Waterberg, Sandveld and Ebenhaezer. All the study nantly either black thorn or sickle bush thickets (Bester 1999). sites fall within the extensive Kalahari sands and are dominated Other main encroacher species in Namibia are, Terminalia by the surface sediment of aeolian origin (Thomas and Shaw prunioides, Terminalia sericea, Colophospermum mopane, Aca- 1991). However, the study sites have different climatic condi- cia erubescens, Acacia fleckii and Acacia reficiense and Grewia tions (Table 1). flava (Bester 1999). Studies have encouraged turning bush harvest into a 1.2. Demarcation of plots and sampling big income generating industry (biomass commercialisation). Data used in the present study was collected from February According to Honsbein and Lindeque (2017), biomass commer- until April 2016. The demarcation of plots was done using mea- cialisation of the resultant biomass from bush encroachment suring tapes, and the GPS recording of each plot was taken. will have significant benefits of job creation in decentralised The study employed quantitative research design. Ten 50 m by parts of the country as well as economic growth. It is therefore 20 m plots were randomly demarcated using stratified random paramount to understand trends of encroacher species in the sampling design at Waterberg and Ebenhaezer. For Mile 46, So- country. Studies focusing on particular bush encroacher species nop and Sandveld, sampling was done on Biodiversity Observa- enable the devise of ecologically sound management strategies tion Network (BIOTA) plots (50 m by 20 m), which were also by land manager, farmers and scientists for the prevention and selected on a stratified random manner (Jürgens et al. 2010). control of bush encroachment. To generate information and According to Barbour et al. (1980) and Barbour et al. (1987), form a better view of bush encroachment in Namibia, the pres- stratified random design allows the fieldworker to locate the ent study identified bush encroacher species, their dominant samples randomly within each homogeneous region by subdi- life forms and their relation to environmental factors. Ward viding the survey area or any given stand into several homo- (2005) argued that multi-factorial experiments that includes geneous regions known as strata. Barbour et al. (1980) stated causal factors such as rainfall and soil nutrients are vital. that this design ensures that samples are dispersed through- out the entire surveyed area thus capturing key population

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Table 1: Main characteristics of the five selected study sites along an aridity gradient

Mean annual Mean annual Habitant type Study sites Latitude Longitude Altitude (m) rainfall (mm) temperature (°C)

Mile 46 18.301826 S 19.247311 E 1180 540 22.6 dry woodland savanna

Sonop 19.073818 S 18.903897 E 1236 500 23.1 dry woodland savanna

Waterberg 20.461330 S 17.208133 E 1550 450 18 Tree and Kalahari woodland savanna

Sandveld 22.043351 S 19.133903 E 1523 400 19.4 Camelthorn savanna

Ebenhaezer 23.216666 S 18.400000 E 1340 280 21.7 grassland and Acacia dominated savanna characteristics in the sample. Another advantage of stratified Growth forms used in the study were defined as follows: me- random sampling is that it does not compromise the concept sophanerophytes defined as all perennial woody plants with of random sampling (Barbour et al. 1980). a height from 8 m to 30 m, and microphanerophytes defined In each plot at each site, encroacher species were as all perennial woody plants with a height from 2 m to 8 m identified and counted. From each plot, a composite sample of as well as nanophanerophytes defined as all perennial woody surface soil was collected from a depth of 0–3 cm (Belsky et al. plants with a height between 25 cm and 2 m (Esten 1932; 1989, Collins et al. 1989, Stohlgren et al. 1998). This was done Raunkiaer 1934; Skarpe 1996). after the surface litter was removed. The composite sample was prepared by combining soil samples taken from the cor- ners and in the central point of the plot. The latter procedure 3. RESULTS was adapted in order to get soil sample that is a representative Acacia erioloba E.Mey., Acacia mellifera (Vahl) Benth. ssp. den- of the whole plot, hence accounting for short range spatial vari- tines (Burch.) Brenan, Combretum collinum Fresen., Terminalia ability (Collins et al. 1989). Top soil (4 kg) was collected from sericea Burch. Ex DC., Grewia spp., Bauhinia petersiana Bolle each plot using a garden shovel and placed in a Ziploc bag that ssp. macrantha (Oliv.) Brummitt & J.H. Ross were identified to was labelled accordingly. Samples were then sun-dried to halt be the main encroacher species at the five study sites along the biological activities and subjected to analysis at the Ministry of aridity gradient (nomenclature used in the present study fol- Agriculture Water and Forestry (MAWF) laboratory. The analy- lowed Klaassen and Kwembeya [2013]). Infraspecific taxa and sis focused on soil pH, texture, organic matter and electrical author citations were not repeated in the text. conductivity. Soil samples were also tested for important mac- ro elements, such as potassium, phosphorus, calcium, magne- 3.1. Environmental factors sium and sodium. Multivariate statistics specifically Nonmetric Multidimensional Scaling (NMS) was used to determine the encroacher species- environment relationship. NMS ordination procedure was 2. DATA ANALYSIS done using Sørensen (Bray-Curtis) distance measure. Number A Nonmetric Multidimensional Scaling (NMS) ordination using of runs used with real data was 200. After 500 number of itera- PC-Ord 6 (McCune et al. 2002; Hoand 2008) was used to deter- tions, a final solution was reached with a stress of 11.320 and mine the main environmental factors influencing the distribu- a final instability of 0.000001. A varimax Rotation of the results tion of encroacher species on Kalahari sands. The environmen- was requested. The resulting ordination graph was overlaid as tal data was overlaid as a biplot to indicate the environmental a biplot (Figure 1). The present study revealed that mean an- gradients of interest. The environmental factors used consisted nual rainfall was the main environmental factor influencing the of the following variables: mean annual rainfall, annual mini- distribution of encroacher species (Figure 1) on Kalahari sands. mum temperature, annual maximum temperature, humidity, G. bicolor, G. flava, A. mellifera and A. erioloba were also cor- pH, electrical conductivity, organic matter, phosphorus, potas- related with minimum annual temperature. sium, calcium, sodium, % sand, % clay and % silt. Encroacher species density was calculated based on 3.2. Density of main encroacher species a formula: D = N/A, where D is the density, N is the number Density per hectare of each of the main encroacher species of sampled encroacher species and A is the size of the plot was calculated and plotted to indicate their response to change from which encroacher species were sampled (Pielou 1975; in mean annual rainfall (Figure 2). According to Figure 2, A. Gotelli and Colwell 2011). Density of encroacher species was mellifera and A. erioloba showed overall similar trends of de- expressed in number per hectare. creasing species density with increasing mean annual rainfall. Encroacher species were categorised into three Slightly higher than expected A. mellifera density was recorded different life forms depending on their height and plotted. at 500 mm mean annual rainfall (Sonop). Furthermore, similar

43 EUROPEAN JOURNAL OF ECOLOGY . trends of increasing species density with increasing mean annual rainfall were recorded for C. collinum, Grewia spp and T. sericea. However, Grewia spp increase with mean annual rainfall up to 500 mm and drops drastically, whileT. sericea increase with mean annual rainfall up to 450 mm and decrease gradu- ally with mean annual rainfall. The density of B. petersiana fluctuated with increasing mean annual rainfall (Figure 2).

3.3. Encroacher species life form Encroacher species life forms were plotted. According to Fig- ure 3, a high number of nanophanerophytes from different encroacher species were recorded between 400 mm and 500 mm mean annual rainfall. B. petersiana had the highest nanophanerophytes at 540 mm and 450 mm respectively. Micro- phanerophytes were widely distributed over the rainfall gra- Figure 1: NMS result of main encroacher species illustrating a biplot dient. The highest number of microphanerophytes recorded overlaid with environmental factors belonged to A. mellifera at 280 mm followed by T. sericea at 450 mm. Mesophanerophytes of encroacher species were only .

Figure 2: Change in encroacher species density along an aridity gradient on Kalahari sands

44 EUROPEAN JOURNAL OF ECOLOGY

recorded from 280 mm to 450 mm, out of which T. sericea had to Mendelson et al. (2009), the studied low rainfall areas (Sand- the highest mesophanerophyte individuals (Figure 3). veld and Ebenhaezer) receive on average about 20 to 30 days of frost in a year, whereas high rainfall areas (Mile 46, Sonop and Waterberg) receive less than 5 days of frost in a year. Skarpe 4. DISCUSSION (1996) and Wakeling et al. (2012) stated that juveniles, short Acacia mellifera and A. erioloba generally showed similar shrubs and broad-leaved species cannot survive many days of trends of decreasing species density with increasing mean an- frost. nual rainfall. The low rainfall in the study was coupled with Rainfall has also been identified in other studies to annual minimum temperature, which limits the colonisation be the main environmental factor influencing the recruitment of these study areas by many woody plant species and other of A. mellifera and A. erioloba (Ernst et al. 1990; Barnes 1999; encroacher species. This significantly reduces the competition Joubert et al. 2017). The present study indicated that the stud- resulting inA. mellifera and A. erioloba species dominating ow- ied low rainfall areas are not bush encroached. This can be ing to their adaptability to harsh conditions. Another factor that attributed to the high mortality rate of species in low rainfall presumably contributed to the low density of C. collinum, T. areas. As stated by Barnes (1999), recruitment of seedlings can sericea, Grewia spp. and B. petersiana, and a high density of A. take place during an average rainfall year, however, mortality erioloba and A. mellifera in low rainfall areas is frost. According of seedlings mostly reach 100% before the next rain season; . hence, recruitment and survival of seedlings and saplings is more likely to be successful in years with above average rainfall. In addition, under low rainfall conditions, species grow much slower. Joubert et al. (2017) claimed that A. mellifera individuals are only likely to reach a height of approximately two meters at about 65 years. However, this growth rate can be improved under better environmental conditions such as mean annual rainfall above 400 mm. The annual minimum temperature associated with the low rainfall areas in the present study ostensi- bly contributed to the low recruitment and slow growth rate in low rainfall areas. This corroborates with Wakeling et al. (2012) who stated that savanna trees grow more slowly in cooler sites compared to warmer sites. The present study recorded a low density of A. erioloba compared to the density of A. mellifera in low rainfall areas. According to Seymour and Milton (2003), A. erioloba is less likely to be a primary encroacher species at any given area because it lacks the characteristics of a bush encroaching species. The predictions of a decrease in rainfall due to climate change (Midgley et al. 2005; Dirkx et al. 2008) suggests that the low rainfall areas are less likely to be bush encroached. Bush encroachment in low rainfall areas will be a highly slow process that can easily be detected and controlled before it threatens herbage production. Majority of encroacher species at low rainfall areas are microphanerophyte at 280 mm (Ebenhaezer) and mesophanerophyte at 400 mm, evidencing the slow recruitment rate and high mortality rate in low rainfall areas. The present study recorded a high abundance of nanophanerophyte of most encroacher species between 400 mm and 500 mm sug- gesting that areas that receives between 400 mm and 500 mm are more likely to experience bush encroachment. Trends of increasing species density with increasing mean annual rainfall were recorded for C. collinum, Grewia spp and T. sericea while B. petersiana density fluctuated with mean annual rainfall. This highlights the importance of rainfall in the distribution of plants on Kalahari sands as shown by Scholes et al. (2002). Encroacher species in high rainfall areas and in Figure 3: Change in encroacher species growth form along an aridity deeper soils areas are likely to have a significantly higher re- gradient cruitment, survival and growth rate, which makes high rainfall

45 EUROPEAN JOURNAL OF ECOLOGY areas susceptible to bush encroachment. Terminalia sericea, C. of grasses at 440 mm, consequently reducing competition on collinum and B. petersiana species give a definite preference seedlings and saplings. to deep Kalahari sand soils, and severe encroachment occurs locally under these habitat conditions. The highest density ofT. sericea was recorded at 440 mm, primarily due to poor range- 5. CONCLUSION AND RECOMMENDATIONS land management and especially due to fire suppression that The findings of the present study led to the conclusions that has been ongoing at that particular study site (Waterberg) since mean annual rainfall is the main environmental factor influenc- the 1980s (MET 2016). ing colonisation and distribution of main encroacher species on The result of this study suggests that under long Kalahari sands in central Namibia, primarily owed to its role in time fire suppression, T. sericea and B. petersiana are the most plant establishment, growth and survival. Poor rangeland man- dominant encroacher species. Terminalia sericea gains its com- agement such as fire suppression is one of the causative factors petitive advantage from its ability to depict different rooting of bush encroachment. It is therefore recommended that fire systems depending on the climatic conditions (Hipondoka and suppression on savannas should be limited, and information Versfeld 2006). Its tendency for deploying its roots near the from this study should be used as a baseline for conservation surface effectively enables it to compete for available soil wa- and restoration attempts towards the savanna rangelands. ter and nutrients with all other shallow rooted plants, such as grasses (Hipondoka and Versfeld 2006). This suggests that some Acknowledgement: We thank Dr. Wanke through OPTIMASS T. sericea species with tap roots are able to utilise deep wa- (Options for sustainable geo-biosphere feedback management ter, while some with shallow roots utilise water on and close to in Savanna systems under regional and global change) and the the surface. These give T. sericea an advantage to outcompete German Federal Ministry of Education and Research for fund- grasses and other phanerophytes. Conferring to Ferrar (1980), ing this research, SASSCAL (Southern African Science Service T. sericea species have developed morphological and physiolog- Centre for Climate Change and Adaptive Land Management) ical features resulting in low rates of transpiration even under for transport provision. We acknowledge Leena Naftal, Emma non-stress condition. The high density of B. petersiana at 440 Shidolo and Sherline Mukatu for the help rendered during data mm was mostly nanophanerophyte. Hence, it is logical to de- collection. duce that fire exclusion has significantly reduced the density

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APPENDIX 1 Table 2: Soil analysis results from the five selected study sites (M = Mile 46, S = So- nop, W = Waterberg, V = Sandveld and E = Ebenhaezer). For weather data please consult www.sasscalweathernet.org

Plots- PHw Ecw uS/cm OM % P ppm K ppm Ca ppm Mg ppm Na ppm Sand % Silt % Clay %

M1 6.25 212 1.1 0.6 38 339 57 0 96.2 2 1.8 M2 6.2 169 0.36 0.4 0 81 21 0 96.9 1.8 1.3 M3 6.35 226 1.08 1.5 77 595 82 0 94.3 3.6 2.1 M4 6.07 144 0.36 0.9 0 85 27 0 95.9 2.9 1.2 M5 6.32 218 1.16 0.6 0 25 14 0 93.6 2.7 3.7 M6 6.51 103 0.44 0 34 376 76 0 96.6 1.4 2 M7 6.22 182 0.95 1 29 525 76 0 96.3 2.3 1.4 M8 6.46 160 0.99 0.1 0 119 39 0 96.7 2.1 1.2 M9 6.05 142 0.5 0.3 0 90 30 0 96.8 2.3 0.9 M10 6.23 177 0.56 3.5 0 127 15 0 96.6 1.7 1.7 S1 5.65 232 0.78 3.6 21 179 32 0 95.6 3.5 0.9 S2 6.53 198 1.05 2.5 28 359 78 0 97.1 1.1 1.8 S3 5.98 127 0.35 0 21 57 14 0 96.7 1.3 2 S4 6.32 228 0.88 2.8 0 20 11 0 89.9 5.3 5 S5 6.69 215 0.78 5.2 38 489 82 0 97.2 1.6 1.2 S6 6.82 150 0.51 3.2 0 508 29 0 97.6 1.9 0.5 S7 5.76 200 0.45 0.3 30 201 43 0 93.8 4.6 1.6 S8 5.91 230 0.69 0.9 60 607 83 0 96.6 2.3 1.1 S9 6.86 217 0.41 0 55 642 91 0 97.5 1.3 1.2 S10 6.15 151 0.42 0.1 0 25 10 0 97.1 1.7 1.2 W1 5.33 337 2.76 37.2 262 3149 342 0 79.1 13.2 7.7 W2 5.26 182 1.72 16 15 331 69 0 91.6 4.7 3.7 W3 4.97 105 0.61 0 0 36 8 0 95.4 2.6 2 W4 5.32 283 0.75 0 20 39 10 0 93.9 5.1 1 W5 5.97 996 1 0 6 22 26 0 94.9 2.6 2.5 W6 5.06 167 1.13 0 2 14 22 0 94.5 4.3 1.2 W7 5.06 167 1.13 0 2 19 25 0 95.3 4 0.7 W8 4.5 135 0.76 21 44 29 6 0 92.8 6.1 1.1 W9 4.72 101 0.82 0 13 325 38 0 94.6 3.5 1.9 W10 5.39 620 1.92 30 163 675 322 0 95.2 4.1 0.7 V1 6.25 212 1.1 0.6 38 339 57 0 89.6 7.2 3.2 V2 6.76 236 0.76 0.5 43 201 60 0 90 6.9 3.1 V3 5.98 127 0.35 0 21 57 14 0 94.3 3.6 2.1 V4 5.81 169 0.36 0.4 0 81 21 0 94.9 4 1.1 V5 6.69 215 0.78 1 38 489 82 0 93.7 4 2.3 V6 6.65 226 1.08 1.5 77 595 82 0 92.8 5 2.3 V7 6.28 230 0.89 0.7 0 29 21 0 91.9 6.9 1.2 V8 6.36 144 0.63 0.9 0 85 27 0 94.2 2.3 3.3 V9 6.86 217 0.55 0 59 642 91 0 93.5 4.9 1.6 V10 6.53 151 0.42 0.3 0 25 10 0 95.1 3.2 1.7 E1 5.65 220 1.3 0.39 23 130 20 0 94.4 2.3 3.3 E2 6.55 132 1.1 0.9 0 239 63 0 94.8 4.2 1 E3 6.79 180 0.78 0.65 32 260 19 0 94.3 3.1 2.6 E4 6.6 126 1 2.8 40 325 56 0 95.2 2.1 2.7 E5 6.68 134 1.16 0.6 0 264 14 0 95.6 2.6 1.8 E6 6.51 103 0.44 0 34 376 76 0 96.8 2.3 0.9 E7 6.44 122 0.39 0 0 129 46 0 95.1 3.2 1.7 E8 6.46 160 0.99 0.1 0 119 39 0 94.2 4 1.8 E9 6.65 177 0.56 2.3 0 127 30 0 94 2.8 3.2 E10 6.37 100 1.22 0.64 29 300 69 0 93.7 3.3 3