EUROPEAN JOURNAL OF ENTOMOLOGYENTOMOLOGY ISSN (online): 1802-8829 Eur. J. Entomol. 113: 217–232, 2016 http://www.eje.cz doi: 10.14411/eje.2016.027 REVIEW

Dragonfl ies and damselfl ies () in urban ecosystems: A review

GIOVANNA VILLALOBOS-JIMÉNEZ, ALISON M. DUNN and CHRISTOPHER HASSALL

School of Biology, University of Leeds, Woodhouse Lane, LS2 9JT, Leeds, United Kingdom; e-mails: [email protected], [email protected], [email protected]

Key words. Odonata, urban ecology, city, anthropogenic stressors, odonates, dragonfl ies, damselfl ies, biodiversity, ecotoxicology, behaviour, life history, phenotypic variation, ecological traps, bioindicators

Abstract. The expansion of urban areas is one of the most signifi cant anthropogenic impacts on the natural landscape. Due to their sensitivity to stressors in both aquatic and terrestrial , dragonfl ies and damselfl ies (the Odonata) may provide in- sights into the effects of urbanisation on biodiversity. However, while knowledge about the impacts of urbanisation on odonates is growing, there has not been a comprehensive review of this body of literature until now. This is the fi rst systematic literature review conducted to evaluate both the quantity and topics of research conducted on odonates in urban ecosystems. From this research, 79 peer-reviewed papers were identifi ed, the vast majority (89.87%) of which related to studies of changing patterns of biodiversity in urban odonate communities. From the papers regarding biodiversity changes, 31 were performed in an urban-rural gradient and 21 of these reported lower diversity towards built up city cores. Twelve of the cases of biodiversity loss were directly related to the concentrations of pollutants in the water. Other studies found higher concentrations of pollutants in odonates from built-up catchments and suggested that odonates such as juncea and Platycnemis pennipes may be candidate indicators for particular contaminants. We conclude by identifying current research needs, which include the need for more studies regarding behavioural ecology and life-history traits in response to urbanisation, and a need to investigate the mechanisms behind diversity trends beyond pollution.

INTRODUCTION gate current research on the impacts of urbanisation using Urbanisation is one of the main drivers of ecosystem odonates as a model group. First, we will present a brief change. The expansion of urban areas is a main cause of overview on the impacts of urbanisation on terrestrial and many environmental stressors: (i) removal of native vege- freshwater ecosystems, then we conduct a systematic lite- tation leading to degradation and fragmentation of the nat- rature review regarding odonates in urban environments ural landscape, (ii) modifi cation of hydrological systems and outline the plausible effects on odonates, followed by through water extraction for human use, (iii) increase of the use of odonates as bioindicators, the conservation value local minimum temperature creating a “heat island” effect, of urban wetlands for odonates, a summary of evolution- and (iv) accumulation of pollutants to a point at which the ary strategies for to cope with urban stressors, and environment cannot fully process and degrade them, caus- fi nally we conclude by identifying research needs. ing eutrophication and affecting biogeochemical cycles THE EFFECTS OF URBAN STRESSORS ON (Grimm et al., 2008; McDonald, 2008). Moreover, the es- TERRESTRIAL AND FRESHWATER ECOSYSTEMS timated percentage of the world population living in urban areas now exceeds 50% (Grimm et al., 2008) and almost The wide range of impacts associated with urbanisation 60% will be living in urban areas by the year 2030 (Seto et indicates that it exerts a considerable effect on terrestrial al., 2012; Güneralp & Seto, 2013). Given the range of im- biodiversity. Most studies show that species richness and pacts and rapid growth of urban development, it is essen- evenness is reduced in highly urbanised regions, depend- tial that we understand in depth the implications for natural ing on the taxonomic group observed, degree of urbanisa- systems both in and around cities. Dragonfl ies and dam- tion, and spatial scale of analysis (McKinney, 2002, 2008). selfl ies (the Odonata) have been suggested as barometers For example, butterfl ies (Ruszczyk, 1987; Ruszczyk & for environmental change due to their sensitivity to other De Araujo, 1992; Blair & Launer, 1997) and ground ar- anthropogenic stressors such as climate change (Hassall, thropods (McIntyre et al., 2001) show this tendency. The 2015) and variation in quality (Clark & Samways, general pattern of biodiversity decrease in cities is prob- 1996). However, the impacts of urbanisation on odonates ably due to the fact that over 80% of land in city cores remain poorly understood. In this review, we will investi- is covered by buildings and pavements, with the remain-

Final formatted article © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice. An Open Access article distributed under the Creative Commons (CC-BY) license (http://creativecommons.org/licenses/by/4.0/).

217 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027 ing area used for lawns, , and shrubs (Blair & Launer, sensitivity to a range of urban stressors means that odo- 1997), thus fragmenting the landscape and homogenising nate communities have the potential to act as barometers vegetation composition (Blair & Launer, 1997; Faeth et al., of environmental change in urban areas, as has been dem- 2011; Faeth et al., 2012; McKinney, 2002). However, plant onstrated successfully in South Africa for habitat quality biodiversity peaks at intermediate levels of urbanisation, (Clark & Samways, 1996) and as has been suggested for perhaps due to the high numbers of species associated with climate change (Hassall, 2015). In this review we outline suburban gardens (McKinney, 2008). the stressors associated with urban environments that have Urban freshwaters have not been explored as much as the potential to affect odonates considerably across their terrestrial urban ecosystems, despite the high degree of life cycle. vulnerability that freshwaters exhibit to the pressures of AND AS A MODEL urbanisation (Paul & Meyer, 2001; Dudgeon et al., 2006). SYSTEM Urban streams, for example, are usually modifi ed to carry out storm water into natural streams, washing away in- Dragonfl ies and damselfl ies (the Odonata) are highly dustrial and human wastes, as well as road runoff (For- suitable model organisms for the study of urban ecosys- man, 2014). Streams are subjected to toxins, temperature tems because (a) they are sensitive to different stressors, change, siltation, organic pollutants, and the replacement such as pollutants (Ferreras-Romero et al., 2009) and tem- of riparian vegetation and substrate for rocks or concrete perature changes (Hassall & Thompson, 2008), therefore and, consequently, , molluscs, crustaceans, and an- can be a powerful tool to assess the general conditions of nelids tend to have decreased species richness and abun- the city environment; (b) they are aquatic as larvae and ter- dance (Paul & Meyer, 2001; Forman, 2008, 2014; Vaughan restrial as adults, hence can be used as bioindicators in both & Ormerod, 2012). The presence of organic pollution has aquatic and terrestrial habitats (Oertli, 2008); (c) they have been associated with increased abundance of chironomids an important role as predators, hence have a wide range and oligochaetes, making them the dominant members of of interactions with different organisms in both aquatic urban stream communities (Campbell, 1978; Seager & and terrestrial ecosystems (Knight et al., 2005); (d) they Abrahams, 1990; Paul & Meyer, 2001). are ideal for studying movement through the landscape, as Ponds are very frequent in parks and gardens for aes- their adult stage exhibits a high dispersal ability and are thetic purposes and to improve human well-being (For- very conspicuous (Conrad et al., 1999), and (e) their bio- man, 2014; Hassall, 2014), and are greatly infl uenced by a diversity, ecology and evolutionary biology is well-docu- variety of factors such as the land use of the surroundings, mented, providing a robust foundation for drawing general the runoff to the pond, subsurface groundwater fl ow, and conclusions (Córdoba-Aguilar, 2008). shoreline conditions (Forman, 2014). Parks and gardens are LITERATURE REVIEW heavily managed and fertilisers are commonly used, and due to their limited capacity for the processing of pollut- We conducted a literature review of the prior work re- ants and nutrients, ponds often suffer from eutrophication garding urbanisation and odonates, in order to evaluate with an accompanying decline in biodiversity (Forman, the potential of odonates as a model system for studying 2014). However, the relative isolation of urban ponds gen- urbanisation. During January–April 2014, we used stand- erates a substantial degree of habitat heterogeneity. Each ardised search terms with three online databases: Web of pond possesses its own physical, chemical, and hydrologi- Science, Scopus and ScienceDirect. The words “urban” cal features, facilitating the presence of a range of species and “Odonata OR dragonfl * OR damselfl *” were searched of specialised habitat requirements, hence increasing the in title, keywords and abstract (except in Web of Science, differentiation among these ecosystems and the landscape where the search was in Topic). Only peer-reviewed pa- diversity (β and γ diversity, respectively) (De Meester et pers including odonates in an urban environment were se- al., 2005). They also work as “stepping stones”, thus fa- lected, reviews were excluded. According to the nature of cilitating landscape connectivity and potentially acting as the study, each paper was classifi ed into one, two or three metapopulations (De Meester et al., 2005; Hassall, 2014). of the following categories: diversity (variables considered The biodiversity of odonates in urban areas is expected here were taxa richness, abundance, probability of occur- to be different from their rural counterparts, as is the case rence for creating habitat suitability models, diversity in- for other taxa. However, as already discussed, urbanisation dices such as Shannon-Wiener, etc.), toxicology (such as is a complex process that encompasses a wide range of se- physicochemical features of the water bodies and heavy lective pressures, and each of them is expected to have a metal concentration), behavioural ecology (dispersal, different impact on odonates according to the species and trophic dynamics), and life-history traits (reproduction, the life stages. Sensitive odonate species may be severely life growth). We went on to examine the references from affected by stressors such as contaminants from sewage the papers found in the standardised search and also added input, but generalist species are expected to tolerate these those to the analysis where appropriate. conditions, leading to decreased species richness. Moreo- The search returned a total of 79 papers, most of which ver, generalist species may exploit the resources avail- (65.82%) were published after 2004 (see Fig. 1, and Table able due to decreased interspecifi c competition, resulting S1 for a complete list of papers with categories). We were in high abundance of tolerant species. This variation in also interested in analysing geographical patterns in re-

218 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

Fig. 2. Map of urban odonate peer-reviewed publications found per country. Fig. 1. Urban odonate peer-reviewed publications found by year and category. Fragmentation search regarding odonates in urban ecosystems and found Fragmented landscapes with little vegetation cover and most studies were conducted in United States and Brazil, few water bodies may not provide suffi cient corridors to though plenty were from , South Africa, , facilitate dispersal, thus limiting odonate connectivity , and others (see Fig. 2). within cities (Chovanec et al., 2000; Watts et al., 2004; Of the 79 papers found, 71 (89.87%) investigated pat- Sato et al., 2008). Urban landscapes were found to function terns in biodiversity, of which 31 were executed in an ur- as barriers for calamorum, senega- ban-rural gradient or compared diversity in streams before lensis, and I. asiatica in Japan when the genetic differentia- and after the water fl ow reached an urbanised area. Of the tion among populations was analysed (Sato et al., 2008), studies regarding biodiversity in an urban-rural gradient, showing that the effect of fragmentation in urban areas is 21 reported less diversity in cities, and 12 cases of diversity consistent within at least three zygopteran species. These loss were related to pollutant concentration in the water results are also consistent between methods of dispersal (see Table 1). Below, we discuss the general trend within analysis: Watts et al. (2004) provide evidence from genetic these papers and give example studies to illustrate those techniques and a mark-release-recapture study that urban trends; a comprehensive list of studies and summaries of areas cause a strong negative effect in the dispersal of Coe- fi ndings can be found in the Supplementary Information nagrion mercuriale in UK. Although we did not fi nd any (Table S1). studies using odonates linking habitat selection and urban The effects of urban stressors on odonates landscapes, fragmentation may also affect habitat selection negatively by constraining access to optimal sites, as has Our results suggest that increasing urbanisation seems been shown in a study using two model species represent- to affect odonate diversity negatively, on the whole, as has ing territorial (van Langevelde, 2015). been shown in other groups (McKinney, 2008). However, urbanisation is a multi-faceted problem and the studies re- Vegetation removal and/or modifi cation viewed herein offer some perspectives on which aspects of Increased vegetation cover and biodiversity of plants urbanisation are having the greatest impacts on Odonata was associated with increased odonate richness and over- across their life cycle and how this may refl ect the biodi- all evenness in Austria (Chovanec et al., 2002), Germany versity loss in cities (see Fig. 3). It is worth mentioning that the stressors listed may not only have a considerable impact in a given stage of their life cycle, but the effects can also be transferred to other stages via carry-over effects (e.g. maternal effects from adult to larva, or persistence of impacts between life history stages from larva to adult), except when a decoupling mechanism interferes (for a de- tailed review see Stoks & Córdoba-Aguilar, 2012).

Table 1. Urban odonate peer-reviewed papers found related to di- versity. No urban-rural Less More No gradient diversity diversity change Urban odonate diversity 38 21 3 7 publications Fig. 3. Summary of drivers of odonate biodiversity in cities due to heavy management. Dashed lines represent hypothetical effects, Diversity related 412—1since no studies were found to investigate the association between to increased pollutants the specifi ed stressor and the corresponding trait(s) on odonates. 219 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

Table 2. Bioindicators of urbanisation. Response to Indicator taxon Urban stressor Reference urbanisation Aeshna spp. Tolerant Urban land use Brazner et al. (2007) Urban development Ferreras-Romero et al. (2009); Sensitive (deforestation and water pollution) Malherbe et al. (2010) Urban development Ischnura graellsii (Rambur, 1842) Tolerant Ferreras-Romero et al. (2009) (deforestation and water pollution) Urban development Anax parthenope (Selys, 1839) Tolerant Ferreras-Romero et al. (2009) (deforestation and water pollution) Urban development Aeshna mixta Latreille, 1805 Tolerant Ferreras-Romero et al. (2009) (deforestation and water pollution) Urban development Orthetrum cancellatum (Linnaeus, 1758) Tolerant Ferreras-Romero et al. (2009) (deforestation and water pollution) Urban development Tolerant Ferreras-Romero et al. (2009) (deforestation and water pollution) Aeshna juncea (Linnaeus, 1758) Tolerant Manganese, lead and nickel Girgin et al. (2010) Platycnemis pennipes (Pallas, 1771) Tolerant Cadmium, boron, iron and total hardness Girgin et al. (2010) fusca (Rambur, 1842) Tolerant Urban development (deforestation) Monteiro et al. (2013) Argia sp. Tolerant Urban development (deforestation) Monteiro et al. (2013) Argia modesta Selys, 1865 Sensitive Urban development (water pollution) Silva et al. (2010) Ischnura elegans (Vander Linden, 1820) Tolerant Urban development (water pollution) Solimini et al. (1997) Erythromma (= Cercion) lindenii (Selys, 1840) Tolerant Urban development (water pollution) Solimini et al. (1997)

(Goertzen & Suhling, 2013), France (Jeanmougin et al., may also exclude some specialist species that rely on par- 2014), and South Africa (Samways & Steytler, 1996; Pryke ticular plants, such as Aeshna viridis that only oviposits & Samways, 2009), among others. For example, Goert- on Stratiotes aloides (Dijkstra, 2006). However, it is worth zen & Suhling (2013) studied odonate diversity patterns mentioning that sensitivity to aquatic vegetation loss may in ponds across an urban-rural gradient using a multivari- vary across odonates, since not all species require aquatic ate approach and found that vegetation was not only one vegetation for oviposition. of the major drivers of alpha diversity, but also trampling Sewage discharge and stormwater runoff vegetation had a signifi cant negative effect. Other studies Sewage is formed primarily of domestic, commercial, have reported similar results, but suggested percentage and industrial waste. Wastewater is collected through the cover of submerged macrophytes was the main component sewage system and treated before releasing into freshwater. of vegetation affecting odonate diversity (Jeanmougin et However, sewer overfl ows are not uncommon, and some al., 2014). Additionally, indigenous plant species have also countries lack these facilities or treat wastewater only par- been highlighted as a key factor shaping odonate commu- tially (Rosa & Clasen, 2010) and in many occasions, treat- nities in urban wetlands, and leaving a strip of indigenous ment is not enough to remove all the contaminants (Paul & riparian vegetation of at least 20 m between the stream Meyer, 2001). edge and commercial plantations seems to facilitate the Several studies found in our literature search examined presence of sensitive odonate species such as Chlorolestes the effects of sewage input or “urban pollutants” in general tessellatus in South Africa (Samways & Steytler, 1996). rather than particular contaminants. In these cases, diver- The strong management of vegetation in terrestrial eco- sity was negatively related to sewage input (Solimini et al., systems in cities has a considerable impact on the adult 1997; Henriques-de-Oliveira et al., 2007), although most phase of odonates (Silva et al., 2010) because vegetation is of the papers from the search were focused on aquatic mac- one of the main cues used for habitat selection and it infl u- roinvertebrates and the overall group of odonates as bioin- ences a vast range of behaviours such as basking, forag- dicators rather than particular species. Urban pollution ing, roosting, sheltering, among others (Buchwald, 1992). was associated with increased abundance and dominance Removal or modifi cation of aquatic vegetation from urban of Libellulidae and other taxa (see Table 2), but decreased freshwater habitats also might have a considerable effect abundance of Gomphidae (Ferreras-Romero et al., 2009) on the behaviour of odonates not only on the adult phase, and overall evenness (Henriques-de-Oliveira et al., 2007). but throughout their life cycle. Adults use aquatic vegeta- However, it is worth mentioning that even though there tion as an oviposition substrate (Buchwald, 1992), often by are many tolerant species within Libellulidae and sensitive inserting eggs into submerged plant stems (Corbet, 1999). species in Gomphidae (Ferreras-Romero et al., 2009), the Once the eggs hatch, the larvae use the submerged plant sensitivity or tolerance of a stressor depends on the par- stems for perching, hiding from predators, and for sit-and- ticular species rather than a larger taxon, therefore caution wait ambush hunting (Buchwald, 1992). During emer- must be taken when considering libellulids or gomphids as gence, the larva climbs upwards out of the water along ver- bioindicators. tical plant stems and proceeds to full metamorphosis once Wastewater contains a wide variety of contaminants it leaves the water. The composition of plant communities ranging from metals, organic and inorganic fertilisers and

220 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027 pesticides to polychlorinated biphenyls (PCBs) and polycy- ODONATES AS BIOINDICATORS IN URBAN clic aromatic hydrocarbons (PAHs) (Paul & Meyer, 2001), ENVIRONMENTS forming a cocktail of pollutants which may affect odonate Aquatic biomonitoring programmes are aimed at evalu- larvae – and other aquatic macroinvertebrates – in a num- ating water quality and identify water pollution in an early ber of ways. First, high contents of organic matter and fer- stage before it leads to decreased environmental health and tilisers cause eutrophication, leading to algal and bacterial ultimately affects human health and the security of pub- blooms and decreasing levels of dissolved oxygen in water lic water supplies, which is particularly important in cities (Forman, 2008). Second, organic and inorganic contami- (Jones et al., 2010). Odonates have been used extensively nants from both sewage discharge and stormwater runoff as a bioindicator group of habitat quality (Clark & Sam- may be toxic for some species. For example, pesticide has ways, 1996; Sahlén & Ekestubbe, 2001; Foote & Rice Hor- been shown to increase mortality in odonate larvae and in nung, 2005; Subramanian et al., 2008; Clausnitzer et al., sublethal concentrations, it also increases fl uctuating asym- 2009; Dolný et al., 2011) and are one of the taxa included metry (e.g. Chang et al., 2007). A study looking at the life in the Biological Monitoring Working Party (BMWP) score history of Coenagrion puella under pesticide stress sug- system (Biological Monitoring Working Party, 1978). The gested that the sensitivity of life-history traits depends on BMWP score system has been used as a biological classifi - the type of pesticide and the exposure time, being increased cation system for river pollution surveys in UK since 1980 development time the only life-history trait which showed (Paisley et al., 2014). The revised BMWP system includes consistency across pesticide treatments in the long-term Calopterygidae, Platycnemididae, , Cord- exposure experiment (atrazine, carbaryl and endosulfan in ulegastridae, and Libellulidae (see Paisley et al., this case) (Campero et al., 2007). On the other hand, ex- 2014 for the scores of each group). However, some species posure of Ischnura elegans larvae to a pesticide (chlorpy- from these groups seem to be tolerant to urban stressors, rifos) decreased immune function signifi cantly, and adult such as Ischnura elegans, I. graellsii, Erythrodiplax fusca, heat stress caused a stronger decrease in immune function, among others (see Table 2). The presence of tolerant taxa indicating that temperature and pesticide stress interact in this system, as well as the absence of sensitive taxa such across metamorphosis (Janssens et al., 2014). Moreover, as vulgatissimus (Brooks, 2004), might result urban populations of C. puella larvae showed increased in a misleading BMWP score. For instance, if in a given activity levels when exposed to chlorpyrifos at 20° and freshwater habitat there are abundant odonates, but 50% of 24°C while showing decreased food intake under pesti- the abundance includes tolerant species such as I. elegans, cide stress at 24°C, compared to rural populations which the result would be a high BMWP score which might not showed decreased activity and food intake in all treatments indicate water quality appropriately. Conversely, if there (Tüzün et al., 2015). These results suggest that urban lar- were abundant G. vulgatissimus, the BMWP score would vae populations are locally adapted to higher contaminant be low, although the water quality in fact might be high. In levels (Tüzün et al., 2015). These studies are particularly order to reduce error using the current BMWP score sys- useful when analysing the impacts of urbanisation due to tem, we suggest that this system include sensitive species their multiple-stressor approach, which highlight the effect such as G. vulgatissimus and reduce the value of tolerant of interactions between urban stressors and contribute to a taxa. It has also been suggested that BMWP scores relying more integral understanding of urban ecosystems. on Odonata might be infl uenced by shifting distributions Certain contaminants such as PCBs and heavy met- under climate change (Hassall et al., 2010). als may bioaccumulate in tissues. There are 209 different types of PCBs, and the mid-chlorinated congeners (e.g. ECOLOGICAL TRAPS IN CITIES PCB-153 and PCB-138) have been found in high concen- Several studies have demonstrated that ecological traps trations among chironomids and dragonfl ies in an urban can arise for dragonfl ies within urban areas, reducing the riparian ecosystem in Beijing (Yu et al., 2013). Similar re- fi tness of urban populations (e.g. Horváth et al., 2007). The sults have been found with other organic persistent pollut- term “ecological trap” refers to situations in which unsuit- ants such as polybrominated diphenyl ethers (PBDEs) and able sites unable to sustain a population are preferred over hexachlorobenzene (HCB) in I. elegans larvae in several the suitable sites or the unsuitable habitats mimic the cues ponds across Flanders, Belgium (Van Praet et al., 2012). that species use for selecting ideal habitats, leading spe- Heavy metals may come from both sewage input and road cies to choose unsuitable habitats over the optimal sites runoff, and they also tend to accumulate in the exoskeleton for roosting, feeding, and mostly reproducing (Donovan of odonate larvae (Meyer et al., 1986). Although lead and & Thompson, 2001; Schlaepfer et al., 2002; Robertson & copper can cause deformities in other insects, e.g. Chirono- Hutto, 2006). Ecological traps are often induced by anthro- mus mentum (de Bisthoven et al., 1998), Aeshna juncea pogenic modifi cations of the environment (Schlaepfer et al., showed tolerance of high concentrations of manganese and 2002), hence urban locations could be used as model sites nickel, while Platycnemis pennipes showed a sensitivity to for studying ecological traps (Hale et al., 2015). Alongside cadmium, boron, and iron (Girgin et al., 2010), providing anthropogenically-modifi ed water bodies that might be evidence of their use as suitable candidates for biomonitor- sub-optimal for odonates (Hale et al., 2015), human activ- ing programmes. ity also produces a range of surfaces that refl ect polarised light to an equal or greater extent than water (Horváth et

221 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027 al., 1998). Since odonates (and other semi-aquatic insects) a major refuge for invertebrate species. Parks in South use polarised light as a cue for oviposition site selection, Africa have shown high odonate diversity, whereas alien such surfaces represent important ecological traps. For ex- plantation forests where Eucalyptus sp. was the most abun- ample, it was found in Brazil that the refl ectance of cars dant had the lowest odonate richness (Samways & Steytler, imitates the refl ectance pattern of ponds, encouraging the 1996). From a social perspective, increased biodiversity of presence of Pantala fl avescens in parking areas and even odonates in urban green areas such as botanical gardens causing them to oviposit on the cars’ surfaces, represent- and parks is also important because they help attract tour- ing an important energy loss (Van de Koken et al., 2007). ists and increase awareness of the role of wetlands (Leme- This behaviour has not only been observed in response to lin, 2007). cars (Watson, 1992; Gunther, 2003; Wildermuth & Hor- Additionally, urban ecosystems offer a vast diversity of váth, 2005; Blaho et al., 2014), but also to black plastic foil pond types, ranging from ornamental ponds to drainage (Wildermuth, 1998), crude oil ponds (Horváth et al., 1998) systems, each of these being subjected to different man- and grave stones (Horváth et al., 2007). According to agement plans (Hassall, 2014). This heterogeneity of pond Kokko & Sutherland (2001), this behaviour could produce types provides different hydrological and ecological con- an Allee effect in low population densities. In high densi- ditions which may promote a higher β and γ- diversity of ties where there is increased competition, most individuals odonates, not only generalist species (Goertzen & Suhling, would compete for the preferred but unsuitable habitats, 2013). Likewise, ponds are abundant mostly in suburban whereas the losing rivals would settle in the less preferred, areas in Central Europe (Willigalla & Fartmann, 2012), high-quality habitat. However, in low population densi- perhaps due to garden ponds. Garden ponds are also com- ties, the lack of competition will allow most individuals to mon in UK, between 2.5 and 3.5 million garden ponds are make poor decisions on choosing proper habitats, therefore estimated in UK (Davies et al., 2009), providing abundant decreasing population density even more and eventually aquatic habitats which facilitate connectivity and promote leading to extinction (Kokko & Sutherland, 2001; Schlaep- metapopulations (Hassall, 2014). fer et al., 2002). In spite of generalist species being abundant in cities, there are some specialist species that can also fi nd refuge in THE CONSERVATION VALUE OF URBAN WATER urban habitats. For example, the threatened damselfl y Coe- BODIES FOR ODONATES nagrion ornatum has been reported to inhabit drainage sys- Although most studies showed a decrease in biodiversity tems (Harabiš & Dolný, 2015), and golf courses in as a result of urbanisation, there is evidence suggesting that have demonstrated to serve as a refuge for endangered spe- urbanisation per se is not necessarily negative, but rather cies e.g. Leucorrhinia pectoralis, a dragonfl y considered the negative impacts on biodiversity arise from highly in- “near threatened” in the Appendix II of the Bern Conven- tensive management associated with urban environments. tion (Colding et al., 2009). Urban sites with a variety of vegetation composition, along An interesting case is presented by Ischnura gemina. with a proper management to minimise water pollution, This species is endemic to the Bay area, were found to host more diverse communities of dragon- USA, which is highly urbanised. Even though I. gemina fl ies and damselfl ies than those with limited vegetation di- has been able to survive despite the stressors in the region versity and increased water pollution (Colding et al., 2009; (Garrison & Hafernik, 1981a, b), populations are decreas- Goertzen & Suhling, 2013). For example, urban drainage ing and now it is threatened by urban development, in spite systems in The with low nutrient content of repatriation efforts (Hannon & Hafernik, 2007). This and rich vegetation have been shown to have compara- species is currently under protection, which is predicted to ble macroinvertebrate diversity to rural drainage systems benefi t the species under climate change scenarios as well (Vermonden et al., 2009). In the Austrian Danube River (Sánchez-Guillén et al., 2014). This situation represents an fl oodplain system located within the city limits of Vienna, important case study in urban invertebrate conservation not a water enhancement programme was implemented (which only for conservation biologists, but also for the regional consisted of restructuring the embankments of an artifi cial authorities and urban planners with whom conservationist island by creating shallow water areas, gravel banks, small must work, since I. gemina and other odonates, as previ- permanent backwaters and temporary waters) and showed ously discussed, are helpful indicators of habitat quality increased vegetation, odonate diversity and connectivity in and can work as “umbrella species” (Bried et al., 2007; the landscape in a long-term monitoring programme (e.g. Clausnitzer et al., 2009). This is particularly important in Chovanec et al., 2000, 2002). A study conducted in South cities because by meeting the conditions required for odo- Africa compared odonate diversity (and other invertebrate nates to survive, other species’ requirements will be met taxa) in natural and recovering forests and fynbos to alien as well (Bried et al., 2007), thus saving time and effort in pine plantations and botanical gardens rich in indigenous developing biodiverse, sustainable cities. They also work plants, and surprisingly the botanical gardens presented as “fl agship species” for wetlands due to their attractive- the highest species richness and abundance, especially ness (Lemelin, 2007), which may help attract visitors to compared with alien pine plantations (Pryke & Samways, urban green areas. 2009), providing evidence that botanical gardens represent

222 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

ADAPTING TO URBANISATION et al., 1998). Thus, there is no comprehensive knowledge regarding the diet of dragonfl ies and damselfl ies in cities. As we have mentioned throughout this review, some Given the fact that aquatic macroinvertebrate communities odonate species may be more tolerant of urban stressors. (i.e. prey) differ in cities from their rural counterparts (Az- In order to unravel the specifi c traits driving the success of rina et al., 2006), there might be a signifi cant impact on the species in urban ecosystems, some studies have examined energy fl ow in both aquatic and terrestrial habitats from the role of the life history of odonates in light of the stress- urban environments (Knight et al., 2005) and the poten- ors caused by urbanisation. For example, a study in Italy tial role for control of disease vectors in densely populated observed the life history patterns of Erythromma lindenii areas (Saha et al., 2012). Moreover, given the fact that and Ischnura elegans along an urban tract of a river and odonate larvae tend to bioaccumulate contaminants such suggested the key factors to allow these species to cope as heavy metals and PCBs that come from human activi- with organic pollution is a longer reproductive period, ab- ties, odonate larvae can transfer the contaminants to other sence of diapause, and tolerance of low oxygen concen- organisms via trophic interactions, either in aquatic or ter- tration (Solimini et al., 1997). Studies performed in Japan restrial ecosystems, that is, in the absence of a decoupling demonstrated that the life cycle of Sympetrum striolatum mechanism preventing the transfer of contaminants from imitoides was synchronised with the use of swimming larvae to adults (Yu et al., 2013). pools; this species laid eggs in autumn, the larvae hatched in mid-winter and most adults emerged before the pools Behaviour were drained and cleaned (Matsura et al., 1995; Matsura Research on behaviour in relation to urban odonate et al., 1998). However, the mechanisms underlying the life populations has focused on dispersal and the selection of history of these species in both studies are uncertain, i.e. oviposition sites, but a much wider suite of behavioural whether the species possessed pre-adaptations to urban traits would be expected to vary across urban-rural gradi- habitats or exhibit plastic responses that allow them to per- ents. Considering, for example, the different stressors from sist despite urban stressors. urban areas (reviewed above), it is common to fi nd tolerant However, the Odonata represent one group within which species in cities (i.e. urban adapters and exploiters; McKin- common garden rearing experiments using multiple stress- ney, 2002) such as I. elegans (Solimini et al., 1997). Urban ors have yielded considerable insights (Stoks et al., 2015). adapters and exploiters among invertebrates would be These studies allow the partitioning of genetic and envi- predicted to exhibit syndromes involving multiple behav- ronmental factors to investigate the relative contributions ioural responses such as increased boldness, that is, being of plasticity and adaptation, and have suggested that local willing to take more risks (Lowry et al., 2013) like those adaptation to temperature (Dinh Van et al., 2014; Aram- exhibited by vertebrates (e.g. song sparrows, Evans et al., bourou & Stoks, 2015) and pesticide stress (Tüzün et al., 2010). Only one study to our knowledge has investigated 2015) is common in odonates. Hence, studying phenotypic the behavioural response of odonates to urban stressors, variation in urban environments represents a great oppor- and found that exploration behaviour, activity, and food tunity for researchers in ecology and evolution to observe intake of C. puella larvae were affected by pesticide stress the complex, underlying processes of how species adapt to except for boldness, although urban populations in general new circumstances through the use of urban habitat patch showed increased activity rate compared to rural popula- networks as “natural experiments”. tions (Tüzün et al., 2015). Therefore, there is a current lack of studies regarding behavioural syndromes in odonates RESEARCH NEEDED and other invertebrates in response to other urban stressors While general patterns of diversity are well described and along urban-rural gradients and the ecological and evolu- some of the mechanisms underlying those patterns have tionary consequences of those syndromes. Further studies been quantifi ed, a number of important areas of research regarding odonate behavioural ecology could also provide are under-represented in the current literature. Below, we important insights into how odonates and other animals in- outline some of these key areas: teract with urban ecosystems and test for a generalisation Trophic interactions of urban evolutionary pressures across taxa. We found very few studies regarding trophic interactions Urban thermal ecology of odonates in cities, in spite of being considered key pred- Furthermore, we must consider that temperature in- ators in both aquatic and terrestrial ecosystems (Knight et creases in urban environments, creating a regional climate al., 2005). Some studies using turtles (Martins et al., 2010) change effect called “Urban Heat Island” (UHI, Grimm et and bats (Srinivasulu & Srinivasulu, 2005; Kalcounis- al., 2008). This temperature increase is most noticeable Rueppell et al., 2007) encountered odonates as prey, in during the night (Karl et al., 1988), and operates both in both urban and non-urban habitats. However, there is little terrestrial areas where pavements and rooftops absorb and information regarding how their role as predators changes radiate heat to increase the ambient air temperature, and in urban ecosystems. Possible intraguild predation has been in aquatic systems where heated runoff that passes over suggested, but not observed in detail (Agüero-Pelegrín & hot concrete and asphalt enters water bodies (Jones et al., Ferreras-Romero, 1994; Sacha, 2011). Other than that, it is 2012). Temperature is a major driver of odonate phenol- commonly known that they feed on chironomids (Matsura ogy (Hassall et al., 2007), polymorph frequency (Gosden

223 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027 et al., 2011), and body size (Hassall, 2013; Hassall et al., CONCLUSION 2014). Additionally, temperature has a great impact on To summarise, this review illustrates that odonate diver- many physiological processes, such as metabolism, res- sity is generally lower in built-up city cores than in sur- piration, muscular activity, immunology, development, rounding areas. However, with suitable management and reproduction, and – naturally – thermoregulation (i.e. pig- design, urban areas could increase diversity and landscape mentation, basking, wing-whirring) (Hassall & Thompson, connectivity, which has various promising implications 2008; Neven, 2000). Therefore, there may be phenological, for ecology, evolutionary biology, conservation biology morphological and physiological shifts in odonates caused and urban planning. While patterns in diversity are well- by the urban heat island effect, as well as interactions be- documented, there has been a lack of research into the tween these shifts. However, the effect of the UHI might behavioural, genetic, and life history processes that might not necessarily be negative. Most odonates are likely to tol- act as mechanisms to drive those diversity patterns. The erate such warm conditions due to their tropical evolution- literature reviewed here provides a strong case for the use ary origin (Pritchard & Leggott, 1987), although thermal of odonates as a model taxon in both the lab and fi eld for stress can be lethal if the temperatures exceed upper toler- the study of a wide range of phenomena related to urbani- ance thresholds. In fact, the UHI may facilitate dispersal sation. In order to achieve an integrated understanding of of odonates, as has been found in scale insects (Meineke urban ecosystems, we encourage further research, specifi - et al., 2013) and mosquitoes (Araujo et al., 2015). It has cally using odonates due to their versatility as bioindicators been suggested that cities in temperate regions may benefi t in both aquatic and terrestrial habitats. from the increased temperature, particularly during winter, although the UHI can also increase thermal and drought ACKNOWLEDGEMENTS. GV-J was supported by the Mexi- stress in tropical, subtropical and desert cities (Shochat et can National Council of Science and Technology (CONACYT) al., 2006). The UHI also has a great impact on freshwater through a doctoral scholarship. CH would like to acknowledge habitats. However, there is no research regarding these top- the support of an EU Marie Curie Fellowship. ics, hence we can only speculate at this point. REFERENCES Modifi ed hydrogeomorphology of freshwaters AGÜERO-PELEGRÍN M. & FERRERAS-ROMERO M. 1994: Dragonfl y Rivers and ponds are frequently subjected to human emergence from an artifi cial pond in the urban area of Cordoba, alterations mostly by increasing imperviousness, which Andalusia, southern Spain: A possible case of intraguild preda- increases temperature, decreases infi ltration of water and tion and competition between larvae. — Notul. Odonatol. 4: increases stormwater runoff drastically (for a detailed re- 57–60. view see Paul & Meyer, 2001). Sediment is also coarser ALVAREZ M. & PARDO I. 2007: Do temporary streams of Mediter- ranean islands have a distinct macroinvertebrate community? in urban water bodies as a result of alteration of sediment The case of Majorca. — Fundam. Appl. Limnol. 168: 55–70. supply and velocities, and also tends to accumulate high ARAMBOUROU H. & STOKS R. 2015: Warmer winters modulate metal contents such as lead, zinc, and cadmium (Paul & life history and energy storage but do not affect sensitivity to Meyer, 2001). The lack of natural substrate may interfere a widespread pesticide in an aquatic . — Aquat. Toxicol. with microhabitat use, habitat selection, and a variety of 167: 38–45. behaviours (e.g. sheltering, hunting). However, to our ARAUJO R.V., ALBERTINI M.R., COSTA-DA-SILVA A.L., SUESDEK L., knowledge no studies have yet been carried out on the im- FRANCESCHI N.C.S., BASTOS N.M., KATZ G., CARDOSO V.A., CAS- portance of fl ow regimes and sediment change to odonates TRO B.C., CAPURRO M.L. & ALLEGRO V.L.A.C. 2015: São Paulo within urban rivers and ponds. urban heat islands have a higher incidence of dengue than other urban areas. — Braz. J. Infect. Dis. 19: 146–155. Urban genomics AZRINA M.Z., YAP C.K., ISMAIL A.R., ISMAIL A. & TAN S.G. 2006: As mentioned previously, the intraspecifi c variation Anthropogenic impacts on the distribution and biodiversity of throughout an urban gradient may be driven via phenotypic benthic macroinvertebrates and water quality of the Langat plasticity or genetic adaptation. Other than studies look- River, Peninsular Malaysia. — Ecotoxicol. Environ. Saf. 64: 337–347. ing at dispersal (Watts et al., 2004; Sato et al., 2008), there BIOLOGICAL MONITORING WORKING PARTY 1978: Final Report: As- are no investigations to our knowledge that link genetics sessment and Presentation of the Biological Quality of Rivers to the phenotypic variation in urban odonate populations. in Great Britain. Unpublished Report. Thus, the underlying mechanisms that drive phenotypic BLAHO M., HERCZEG T., KRISKA G., EGRI A., SZAZ D., FARKAS A., variation of odonates in cities are not well-documented. TARJANYI N., CZINKE L., BARTA A. & HORVATH G. 2014: Unex- While one study has looked at population differentiation pected attraction of polarotactic water-leaving insects to matt across an urban landscape (Sato et al., 2008), there could black car surfaces: mattness of paintwork cannot eliminate be far greater insights through a combination of gene-fl ow the polarized light pollution of black cars. — PLoS ONE 9: models, cost surfaces, and corridor analyses to use odonate e103339, 11 pp. BLAIR R.B. & LAUNER A.E. 1997: Butterfl y diversity and human movement as an indicator of large-scale habitat connectiv- land use: Species assemblages along an urban gradient. — ity in cities. Modern advances in transcriptomics and me- Biol. Conserv. 80: 113–125. tabolomics also offer opportunities to explore the stressors BRACKEN B. & LEWIS C. 2004: Odonata of the Britannia Conserva- experienced by urban populations through the differential tion Area (Ottawa-Carleton County), Ontario. In Catling P.M., expression of genes (e.g. Chapman et al., 2009).

224 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

Jones C.D. & Pratt P. (eds): Ontario Odonata. Vol. 5. Toronto global assessment of an insect group. — Biol. Conserv. 142: Entomologists Association, Toronto, pp. 15–22. 1864–1869. BRANDT K. & BUCHWALD R. 2011: Importance of compensation CLETO FILHO S.E.N. & WALKER I. 2001: Effects of urban occupa- ponds for the Odonata fauna in the city of Oldenburg, Lower tion on the aquatic macroinvertebrate from a small stream of Saxony, Germany (Odonata). — Libellula 30: 111–132. Manaus, Amazonas State, Brazil. — Acta Amazon. 31: 69–89. BRAZNER J.C. , DANZ N.P., TREBITZ A.S., NIEMI G.J., REGAL R.R., COLDING J., LUNDBERG J., LUNDBERG S. & ANDERSSON E. 2009: HOLLENHORST T., HOST G.E., REAVIE E.D., BROWN T.N., HA- Golf courses and wetland fauna. — Ecol. Appl. 19: 1481–1491. NOWSKI J.M., JOHNSTON C.A., JOHNSON L.B., HOWE R.W. & CONRAD K.F., WILLSON K.H., HARVEY I.F., THOMAS C.J. & SHER- CIBOROWSKI J.J.H. 2007: Responsiveness of Great Lakes RATT T.N. 1999: Dispersal characteristics of seven odonate spe- wetland indicators to human disturbances at multiple spatial cies in an agricultural landscape. — Ecography 22: 524–531. scales: A multi-assemblage assessment. — J. Great Lakes Res. CORBET P.S. 1999: Dragonfl ies: Behavior and Ecology of Odo- 33: 42–66. nata. Harley Books, Martins, 830 pp. BRIED J.T., HERMAN B.D. & ERVIN G.N. 2007: Umbrella potential CÓRDOBA-AGUILAR A. 2008: Dragonfl ies and Damselfl ies: Model of plants and dragonfl ies for wetland conservation: a quantita- Organisms for Ecological and Evolutionary Research. Oxford tive case study using the umbrella index. — J. Appl. Ecol. 44: University Press, Oxford, 290 pp. 833–842. CRAVES J.A. & O’BRIEN D.S. 2013: The Odonata of Wayne Coun- BROOKS S. 2004: Field Guide to the Dragonfl ies and Damselfl ies ty, MI: Inspiration for renewed monitoring of urban areas. — of Great Britain and Ireland. 4th ed. British Wildlife Publish- Northeast. Nat. 20: 341–362. ing, Hook, 160 pp. DAVIES Z.G., FULLER R.A., LORAM A., IRVINE K.N., SIMS V. & GAS- BUCHWALD R. 1992: Vegetation and dragonfl y fauna – characteris- TON K.J. 2009: A national scale inventory of resource provision tics and examples of biocenological fi eld studies. — Vegetatio for biodiversity within domestic gardens. — Biol. Conserv. 101: 99–107. 142: 761–771. BURTON J.F. 1995: The fl ora and fauna of Elmstead Wood and DE BISTHOVEN L.J., POSTMA J.F., PARREN P., TIMMERMANS K.R. & Sundridge Park, Bromley, south-east London, in the 1940s, OLLEVIER F. 1998: Relations between heavy metals in aquatic with some earlier and later records. — Lond. Natl. 74: 83–112. sediments and in Chironomus larvae of Belgian lowland rivers CAMPBELL I. 1978: A biological investigation of an organically and their morphological deformities. — Can. J. Fish. Aquat. polluted urban stream in Victoria. — Marine Freshw. Res. 29: Sci. 55: 688–703. 275–291. DE MEESTER L., DECLERCK S., STOKS R., LOUETTE G., VAN DE CAMPERO M., OLLEVIER F. & STOKS R. 2007: Ecological relevance MEUTTER F., DE BIE T., MICHELS E. & BRENDONCK L. 2005: and sensitivity depending on the exposure time for two bio- Ponds and pools as model systems in conservation biology, markers. — Environ. Toxicol. 22: 572–581. ecology and evolutionary biology. — Aquat. Conserv. Marine CHANG X., ZHAI B., WANG M. & WANG B. 2007: Relationship be- Freshw. Ecosyst. 15: 715–725. tween exposure to an insecticide and fl uctuating asymmetry in DIJKSTRA K.D.B. 2006: Field Guide to the Dragonfl ies of Britain a damselfl y (Odonata, Coenagriidae). — Hydrobiologia 586: and Europe: Including Western Turkey and North-Western Af- 213–220. rica. British Wildlife Publishing, Milton on Stour, 320 pp. CHAPMAN R.W., MANCIA A., BEAL M., VELOSO A., RATHBURN C., DINH VAN K., JANSSENS L., DEBECKER S. & STOKS R. 2014: Warm- BLAIR A., SANGER D., HOLLAND A.F., WARR G.W. & DIDONATO ing increases chlorpyrifos effects on predator but not anti-pred- G.U.Y. 2009: A transcriptomic analysis of land-use impacts on ator behaviours. — Aquat. Toxicol. 152: 215–221. the oyster, Crassostrea virginica, in the South Atlantic Bight. DOLNÝ A., BÁRTA D., LHOTA S., RUSDIANTO & DROZD P. 2011: — Mol. Ecol. 18: 2415–2425. Dragonfl ies (Odonata) in the Bornean rain forest as indicators CHOVANEC A. 1994: Man-made wetlands in urban recreational of changes in biodiversity resulting from forest modifi cation areas – a habitat for ? — Landsc. Urban and destruction. — Trop. Zool. 24: 63–86. Plann. 29: 43–54. DOMBROVSKIY K.O. & KHARCHENKO T.A. 2005: Sanitary and hy- CHOVANEC A. & RAAB R. 1997: Dragonfl ies (Insecta, Odonata) drobiological state of Lake Zakitnya (Zaporozhye). — Hydro- and the ecological status of newly created wetlands: Examples biol. J. 41: 34–39. for long-term bioindication programmes. — Limnologica 27: DONOVAN T.M. & THOMPSON F.R. 2001: Modeling the ecological 381–392. trap hypothesis: A habitat and demographic analysis for mi- CHOVANEC A., SCHIEMER F., CABELA A., GRESSLER S., GRÖTZER C., grant songbirds. — Ecol. Appl. 11: 871–882. PASCHER K., RAAB R., TEUFL H. & WIMMER R. 2000: Construct- DUDGEON D., ARTHINGTON A.H., GESSNER M.O., KAWABATA Z.-I., ed inshore zones as river corridors through urban areas – the KNOWLER D.J., LÉVÊQUE C., NAIMAN R.J., PRIEUR-RICHARD A.- Danube in Vienna: Preliminary results. — Regul. Rivers Res. H., SOTO D., STIASSNY M.L.J. & SULLIVAN C.A. 2006: Fresh- Manag. 16: 175–187. water biodiversity: importance, threats, status and conservation CHOVANEC A., SCHIEMER F., WAIDBACHER H. & SPOLWIND R. 2002: challenges. — Biol. Rev. 81: 163–182. Rehabilitation of a heavily modifi ed river section of the Danube EDOKPAYI C.A., LAWAL M.O., OKWOK N.A. & OGUNWENMO C.A. in Vienna (Austria): Biological assessment of landscape link- 2004: Physico-chemical and macrobenthic faunal character- ages on different scales. — Int. Rev. Hydrobiol. 87: 183–195. istics of Kuramo Water, Lagos, southern Nigeria. — Afr. J. CLARK T.E. & SAMWAYS M.J. 1996: Dragonfl ies (Odonata) as in- Aquat. Sci. 29: 235–241. dicators of biotope quality in the Kruger National Park, South EVANS J., BOUDREAU K. & HYMAN J. 2010: Behavioural syndromes Africa. — J. Appl. Ecol. 33: 1001–1012. in urban and rural populations of song sparrows. — Ethology CLAUSNITZER V., KALKMAN V.J., RAM M., COLLEN B., BAILLIE 116: 588–595. J.E.M., BEDJANIČ M., DARWALL W.R.T., DIJKSTRA K.-D.B., DOW FAETH S.H., BANG C. & SAARI S. 2011: Urban biodiversity: pat- R., HAWKING J., KARUBE H., MALIKOVA E., PAULSON D., SCHÜTTE terns and mechanisms. — Ann. N. Y. Acad. Sci. 1223: 69–81. K., SUHLING F., VILLANUEVA R.J., VON ELLENRIEDER N. & WILSON FAETH S.H., SAARI S. & BANG C. 2012: Urban biodiversity: Pat- K. 2009: Odonata enter the biodiversity crisis debate: The fi rst terns, processes and implications for conservation. In: eLS. John Wiley & Sons, Chichester, http://www.els.net.

225 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

FERRERAS-ROMERO M., MARQUEZ-RODRIGUEZ J. & RUIZ-GARCIA A. HASSALL C. 2014: The ecology and biodiversity of urban ponds. 2009: Implications of anthropogenic disturbance factors on the — Wiley Interdisc. Rev. Water 1: 187–206. Odonata assemblage in a Mediterranean fl uvial system. — Int. HASSALL C. 2015: Odonata as candidate macroecological barom- J. Odonatol. 12: 413–428. eters for global climate change. — Freshw. Sci. 34: 1040–1049. FISCHER S., MARINONE M.C., FONTANARROSA M.S., NIEVES M. & HASSALL C. & THOMPSON D.J. 2008: The effects of environmental SCHWEIGMANN N.A. 2000: Urban rain pools: seasonal dynamics warming on Odonata: a review. — Int. J. Odonatol. 11: 131– and entomofauna in a park of Buenos Aires. — Hydrobiologia 153. 441: 45–53. HASSALL C., THOMPSON D.J., FRENCH G.C. & HARVEY I.F. 2007: FONTANARROSA M.S., TORRES P.L.M. & MICHAT M.C. 2004: Aquat- Historical changes in the phenology of British Odonata are re- ic insect communities of temporary pools and permanent ponds lated to climate. — Global Change Biol. 13: 933–941. in Buenos Aires City (Argentina). — Rev. Soc. Entomol. Ar- HASSALL C., THOMPSON D. & HARVEY I. 2010: The impact of gent. 63: 55–65. climate-induced distributional changes on the validity of bio- FOOTE A.L. & RICE HORNUNG C.L. 2005: Odonates as biological logical water quality metrics. — Environ. Monitor. Assess. 160: indicators of grazing effects on Canadian prairie wetlands. — 451–456. Ecol. Entomol. 30: 273–283. HASSALL C., KEAT S., THOMPSON D.J. & WATTS P.C. 2014: Berg- FORMAN R.T.T. 2008: Urban Regions: Ecology and Planning be- mann’s rule is maintained during a rapid range expansion in a yond the City. Cambridge University Press, New York, 408 pp. damselfl y. — Global Change Biol. 20: 475–482. FORMAN R.T.T. 2014: Urban Ecology: Science of Cities. Cam- HENRIQUES-DE-OLIVEIRA C., BAPTISTA D.F. & NESSIMIAN J.L. 2007: bridge University Press, New York, 464 pp. Sewage input effects on the macroinvertebrate community FUNK A., RECKENDORFER W., KUCERA-HIRZINGER V., RAAB R. & associated to Typha domingensis Pers in a coastal lagoon in SCHIEMER F. 2009: Aquatic diversity in a former fl oodplain: Re- southeastern Brazil. — Braz. J. Biol. 67: 73–80. mediation in an urban context. — Ecol. Engin. 35: 1476–1484. HORVÁTH G., BERNÁTH B. & MOLNÁR G. 1998: Dragonfl ies fi nd FUNK A., GSCHÖPF C., BLASCHKE A.P., WEIGELHOFER G. & RECKEN- crude oil visually more attractive than water: Multiple-choice DORFER W. 2013: Ecological niche models for the evaluation of experiments on dragonfl y polarotaxis. — Naturwissenschaften management options in an urban fl oodplain-conservation vs. 85: 292–297. restoration purposes. — Environ. Sci. Pol. 34: 79–91. HORVÁTH G., MALIK P., KRISKA G. & WILDERMUTH H. 2007: Eco- GARRISON R.W. & HAFERNIK J.E.J. 1981a: Distribution of Ischnu- logical traps for dragonfl ies in a cemetery: the attraction of ra gemina and a description of the andromorph female (Zygo- Sympetrum species (Odonata: Libellulidae) by horizontally ptera: Coenagrionidae). — Odonatologica 10: 85–92. polarizing black gravestones. — Freshw. Biol. 52: 1700–1709. GARRISON R.W. & HAFERNIK J.E.J. 1981b: Population structure of JANSSENS L., DINH VAN K. & STOKS R. 2014: Extreme tempera- the rare damselfl y, Ischnura gemina (Kennedy) (Odonata: Coe- tures in the adult stage shape delayed effects of larval pesticide nagrionidae). — Oecologia 48: 377–384. stress: A comparison between latitudes. — Aquat. Toxicol. 148: GIRGIN S., KAZANCI N. & DUGEL M. 2010: Relationship between 74–82. aquatic insects and heavy metals in an urban stream using JARA F.G., UBEDA C.A. & PEROTTI M.G. 2013: Predatory insects in multivariate techniques. — Int. J. Environ. Sci. Technol. 7: lentic freshwater habitats from northwest Patagonia: richness 653–664. and phenology. — J. Nat. Hist. 47: 2749–2768. GOERTZEN D. & SUHLING F. 2013: Promoting dragonfl y diversity JEANMOUGIN M., LEPRIEUR F., LOÏS G. & CLERGEAU P. 2014: Fine- in cities: major determinants and implications for urban pond scale urbanization affects Odonata species diversity in ponds of design. — J. Insect Conserv. 17: 399–409. a megacity (Paris, France). — Acta Oecol. 59: 26–34. GOSDEN T.P., STOKS R. & SVENSSON E.I. 2011: Range limits, large- JONES J.I., DAVY-BOWKER J., MURPHY J.F. & PRETTY J.L. 2010: scale biogeographic variation, and localized evolutionary dy- Ecological monitoring and assessment of pollution in rivers. In namics in a polymorphic damselfl y. — Biol. J. Linn. Soc. 102: Batty L.C. & Hallberg K.B. (eds): Ecology of Industrial Pol- 775–785. lution. Cambridge University Press, Cambridge, pp. 126–146. GRIMM N.B., FAETH S.H., GOLUBIEWSKI N.E., REDMAN C.L., WU J., JONES M., HUNT W. & WINSTON R. 2012: Effect of urban catch- BAI X. & BRIGGS J.M. 2008: Global change and the ecology of ment composition on runoff temperature. — J. Environ. Engin. cities. — Science 319: 756–760. 138: 1231–1236. GÜNERALP B. & SETO K.C. 2013: Futures of global urban expan- KALCOUNIS-RUEPPELL M.C., PAYNE V.H., HUFF S.R. & BOYKO A.L. sion: uncertainties and implications for biodiversity conserva- 2007: Effects of wastewater treatment plant effl uent on bat for- tion. — Environ. Res. Lett. 8: 014025, 10 pp. aging ecology in an urban stream system. — Biol. Conserv. GUNTHER A. 2003: Eiablage von Sympetrum vulgatum auf ein 138: 120–130. parkendes Auto (Odonata: Libellulidae). — Libellula 22: 19– KARL T.R., DIAZ H.F. & KUKLA G. 1988: Urbanization: Its detec- 23. tion and effect in the United States climate record. — J. Clim. HALE R., COLEMAN R., PETTIGROVE V. & SWEARER S.E. 2015: Re- 1: 1099–1123. view: Identifying, preventing and mitigating ecological traps KAROUNA-RENIER N.K. & SPARLING D.W. 2001: Relationships to improve the management of urban aquatic ecosystems. — J. between ambient geochemistry, watershed land-use and trace Appl. Ecol. 52: 928–939. metal concentrations in aquatic invertebrates living in storm- HANNON E.R. & HAFERNIK J.E. 2007: Reintroduction of the rare water treatment ponds. — Environ. Pollut. 112: 183–192. damselfl y Ischnura gemina (Odonata: Coenagrionidae) into an KNIGHT T.M., MCCOY M.W., CHASE J.M., MCCOY K.A. & HOLT urban park. — J. Insect Conserv. 11: 141–149. R.D. 2005: Trophic cascades across ecosystems. — Nature HARABIŠ F. & DOLNÝ A. 2015: Necessity for the conservation of 437: 880–883. drainage systems as last refugia for threatened damselfl y spe- KOKKO H. & SUTHERLAND W.J. 2001: Ecological traps in chang- cies, Coenagrion ornatum. — Insect Conserv. Div. 8: 143–151. ing environments: ecological and evolutionary consequences HASSALL C. 2013: Time stress and temperature explain continental of a behaviourally mediated Allee effect. — Evol. Ecol. Res. variation in damselfl y body size. — Ecography 36: 894–903. 3: 537–551.

226 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

KULKARNI A.S. & SUBRAMANIAN K.A. 2013: Habitat and seasonal MEYER W., HARISCH G. & SAGREDOS A.N. 1986: Biochemical distribution of Odonata (Insecta) of Mula and Mutha river ba- and histochemical aspects of lead exposure in dragonfl y lar- sins, Maharashtra, . — J. Threat. Taxa 5: 4084–4095. vae (Odonata: Anisoptera). — Ecotoxicol. Environ. Safety 11: KURY D. & CHRIST J. 2010: Odonata fauna and conservation in the 308–319. canton Basel-Stadt (NW Switzerland). — Mitt. Naturforsch. MONTEIRO C.D., COUCEIRO S.R.M., HAMADA N. & JUEN L. 2013: Gesellsch. Basel 12: 105–118. Effect of vegetation removal for road building on richness and LEMELIN R.H. 2007: Finding beauty in the dragon: The role of composition of Odonata communities in Amazonia, Brazil. — dragonfl ies in recreation and tourism. — J. Ecotour. 6: 139– Int. J. Odonatol. 16: 135–144. 145. MORENO P., FRANCA J.S., FERREIRA W.R., PAZ A.D., MONTEIRO I.M. LENDERS H.J.R., LEUVEN R.S.E.W., NIENHUIS P.H., DE NOOIJ & CALLISTO M. 2009: Use of the BEAST model for biomoni- R.J.W. & VAN ROOIJ S.A.M. 2001: BIO-SAFE: A method for toring water quality in a neotropical basin. — Hydrobiologia evaluation of biodiversity values on the basis of political and 630: 231–242. legal criteria. — Landsc. Urban Plann. 55: 121–137. MOSTERT K. 1998: Dragonfl ies (Odonata) in the agricultural land- LOWRY H., LILL A. & WONG B.B.M. 2013: Behavioural responses scape of South Holland. — Levende Natuur. 99: 142–149. of wildlife to urban environments. — Biol. Rev. 88: 537–549. MURDOCH D.A. 1989: The dragonfl ies of London’s East End, LUBERTAZZI M.A.A. & GINSBERG H.S. 2010: Emerging dragonfl y England, UK. — Lond. Natl. 68: 81–84. diversity at small Rhode Island (U.S.A.) wetlands along an ur- NEISS U.G., LENCIONI F.A.A., HAMADA N. & FERREIRA-KEPPLER banization gradient. — Urban Ecosyst. 13: 517–533. R.L. 2008: Larval redescription of maculatum LUNDE K.B. & RESH V.H. 2012: Development and validation of a Hagen in Selys, 1860 (Odonata: ) from macroinvertebrate index of biotic integrity (IBI) for assessing Manaus, Amazonas, Brazil. — Zootaxa 1696: 57–62. urban impacts to Northern California freshwater wetlands. — NELSON S.M. 2011: Response of stream macroinvertebrate assem- Environ. Monit. Assess. 184: 3653–3674. blages to erosion control structures in a wastewater dominated MAHATO M. & KENNEDY J.H. 2008a: Artifi cial substrate trans- urban stream in the southwestern U.S. — Hydrobiologia 663: fer technique to detect impact of urbanization on colonized 51–69. macroinvertebrates from a minimally impacted stream. — J. NEVEN L.G. 2000: Physiological responses of insects to heat. — Freshw. Ecol. 23: 205–212. Postharv. Biol. Technol. 21: 103–111. MAHATO M. & KENNEDY J.H. 2008b: Field experimental approach NUMMELIN M., LODENIUS M., TULISALO E., HIRVONEN H. & ALANKO to detect urban impact on Erpetogomphus designatus Hagen in T. 2007: Predatory insects as bioindicators of heavy metal pol- Selys larvae (Anisoptera: Gomphidae). — Odonatologica 37: lution. — Environ. Pollut. 145: 339–347. 13–28. OERTLI B. 2008: The use of dragonfl ies in the assessment and MAJUMDER J., DAS R.K., MAJUMDER P., GHOSH D. & AGARWALA monitoring of aquatic habitats. In Córdoba-Aguilar A. (ed.): B.K. 2013: Aquatic insect fauna and diversity in urban fresh Dragonfl ies and Damselfl ies: Model Organisms for Ecological water lakes of Tripura, Northeast India. — Midd. East J. Sci. and Evolutionary Research. Oxford University Press, Oxford, Res. 13: 25–32. pp. 79–95. MALHERBE W., WEPENER V. & VAN VUREN J.H.J. 2010: Anthropo- OSADA M. & TABATA S. 1992: Creation of natural ecosystem on genic spatial and temporal changes in the aquatic macroinver- the waterside space through inhabitant environment of dragon- tebrate assemblages of the lower Mvoti River, KwaZulu-Natal, fl ies: a case of Honmoku Public Park in Yokohama City, Japan. South Africa. — Afr. J. Aquat. Sci. 35: 13–20. — Tech. Bull. Fac. Hortic. Chiba Univ. 46: 35–45. MARTINS F.I., DE SOUZA F.L. & DA COSTA H.T.M. 2010: Feeding PAISLEY M.F., TRIGG D.J. & WALLEY W.J. 2014: Revision of the habits of Phrynops geoffroanus (Chelidae) in an urban river in Biological Monitoring Working Party (BMWP) score system: Central Brazil. — Chelon. Conserv. Biol. 9: 294–297. Derivation of present-only and abundance-related scores from MATSURA T., KOMATSU K., NOMURA K. & OH’OTO M. 1995: Life fi eld data. — River Res. Appl. 30: 887–904. history of Sympetrum striolatum imitoides Bartenef at an out- PAUL M.J. & MEYER J.L. 2001: Streams in the urban landscape. — door swimming pool in an urban area (Anisoptera: Libelluli- Annu. Rev. Ecol. Syst. 32: 333–365. dae). — Odonatologica 24: 291–300. POULTON B.C., WILDHABER M.L., CHARBONNEAU C.S., FAIRCHILD MATSURA T., NOMURA K. & KOMATSU K. 1998: Ecological studies J.F., MUELLER B.G. & SCHMITT C.J. 2003: A longitudinal as- of odonate larvae living in artifi cial ponds in an urban area: sessment of the aquatic macroinvertebrate community in the Occurrence of larval Sympetrum striolatum imitoides and its channelized lower Missouri River. — Environ. Monit. Assess. life history in primary school swimming pools. — Jap. J. Ecol. 85: 23–53. 48: 27–36. PRINCIPE R.E. & CORIGLIANO M.D. 2006: Benthic, drifting and MCDONALD R.I. 2008: Global urbanization: can ecologists iden- marginal macroinvertebrate assemblages in a lowland river: tify a sustainable way forward? — Front. Ecol. Environ. 6: Temporal and spatial variations and size structure. — Hydro- 99–104. biologia 553: 303–317. MCINTYRE N.E., RANGO J., FAGAN W.F. & FAETH S.H. 2001: PRITCHARD G. & LEGGOTT M. 1987: Temperature, incubation rates Ground community structure in a heterogeneous and the origins of dragonfl ies. — Adv. Odonatol. 3: 121–126. urban environment. — Landsc. Urban Plann. 52: 257–274. PRYKE J.S. & SAMWAYS M.J. 2009: Recovery of invertebrate di- MCKINNEY M.L. 2002: Urbanization, biodiversity, and conserva- versity in a rehabilitated city landscape mosaic in the heart of a tion. — BioScience 52: 883–890. biodiversity hotspot. — Landsc. Urban Plann. 93: 54–62. MCKINNEY M.L. 2008: Effects of urbanization on species rich- PUJOL-LUZ J.R. 1987: The adaptation of dragonfl ies to urban envi- ness: A review of plants and animals. — Urban Ecosyst. 11: ronment in Rio De Janeiro, Brazil 1. The dragonfl ies of Mini- 161–176. Horto Sylvio Potsch. — Notul. Odonatol. 2: 167–168. MEINEKE E.K., DUNN R.R., SEXTON J.O. & FRANK S.D. 2013: RIVERA RONDÓN C.A., ZAPATA A.M., PÉREZ D., MORALES Y., Urban warming drives insect pest abundance on street trees. — OVALLE H. & ALVAREZ J.P. 2010: Caracterización limnológica PLoS ONE 8: e59687, 7 pp. de humedales de la planicie de inundación del Río Orinoco (Orinoquía, Colombia). — Acta Biol. Colomb. 15: 145–166.

227 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

RIZZONI M., GUSTAVINO B., FERRARI C., GATTI L.G. & FANO E.A. SINCLAIR K.A., XIE Q. & MITCHELL C.P.J. 2012: Methylmercury in 1995: An integrated approach to the assessment of the environ- water, sediment, and invertebrates in created wetlands of Rouge mental-quality of The Tiber River in the urban area of Rome Park, Toronto, Canada. — Environ. Pollut. 171: 207–215. – a mutagenesis assay (micronucleus test) and an analysis of SMITH R.F. & LAMP W.O. 2008: Comparison of insect commu- macrobenthic community structure. — Sci. Total Environ. 162: nities between adjacent headwater and main-stem streams in 127–137. urban and rural watersheds. — J. North Am. Benthol. Soc. 27: ROBERTSON B.A. & HUTTO R.L. 2006: A framework for under- 161–175. standing ecological traps and an evaluation of existing evi- SOLIMINI A.G., TARALLO G.A. & CARCHINI G. 1997: Life history dence. — Ecology 87: 1075–1085. and species composition of the damselfl y assemblage along the ROSA G. & CLASEN T. 2010: Estimating the scope of household urban tract of a river in central Italy. — Hydrobiologia 356: water treatment in low- and medium-income countries. — Am. 21–32. J. Trop. Med. Hyg. 82: 289–300. SRINIVASULU B. & SRINIVASULU C. 2005: Diet of the black-bearded RUSZCZYK A. 1987: Distribution and abundance of butterfl ies in tomb bat Taphozous melanopogon Temminck, 1841 (Chiro- the urbanization zones of Porto Alegre, Brazil. — J. Res. Lepi- ptera: Emballonuridae) in India. — Zoos’ Print J. 20: 1935– dopt. 25: 157–178. 1938. RUSZCZYK A. & DE ARAUJO A.M. 1992: Gradients in butterfl y spe- STEYTLER N.S. & SAMWAYS M.J. 1995: Biotope selection by adult cies diversity in an urban area in Brazil. — J. Lepidopt. Soc. male dragonfl ies (Odonata) at an artifi cial lake created for in- 46: 255–264. sect conservation in South-Africa. — Biol. Conserv. 72: 381– SACHA D. 2011: How many dragonfl ies are there in your garden 386. pond? — Notul. Odonatol. 7: 66–67. STOKS R. & CÓRDOBA-AGUILAR A. 2012: Evolutionary ecology of SAHA N., ADITYA G., BANERJEE S. & SAHA G.K. 2012: Predation Odonata: A complex life cycle perspective. — Annu. Rev. En- potential of odonates on larvae: Implications for bio- tomol. 57: 249–265. logical control. — Biol. Contr. 63: 1–8. STOKS R., DEBECKER S., VAN K.D. & JANSSENS L. 2015: Integrat- SAHLÉN G. & EKESTUBBE K. 2001: Identifi cation of dragonfl ies ing ecology and evolution in aquatic toxicology: Insights from (Odonata) as indicators of general species richness in boreal damselfl ies. — Freshw. Sci. 34: 1032–1039. forest lakes. — Biodiv. Conserv. 10: 673–690. SUBRAMANIAN K.A., ALL S. & RAMACHANDRA T.V. 2008: Odonata SAMRAOUI B., DEBELAIR G. & BENYACOUB S. 1992: A much-threat- as indicators of riparian ecosystem health, a case study from ened lake: Lac des Oiseaux in Northeastern Algeria. — Envi- Southwestern Karnataka, India — Fraseria (N.S.) 7: 83–95. ron. Conserv. 19: 264–267. SUH A.N. & SAMWAYS M.J. 2005: Signifi cance of temporal chang- SAMWAYS M.J. & STEYTLER N.S. 1996: Dragonfl y (Odonata) dis- es when designing a reservoir for conservation of dragonfl y tribution patterns in urban and forest landscapes, and recom- diversity. — Biodiv. Conserv. 14: 165–178. mendations for riparian management. — Biol. Conserv. 78: SUHLING F., MARTENS A., LEIPELT K.G., SCHUETTE C. & HOPPE- 279–288. DOMINIK B. 2009: Dragonfl y fauna of Braunschweig, Germany SÁNCHEZ-GUILLÉN R.A., MUÑOZ J., HAFERNIK J., TIERNEY M., ROD- – distribution patterns and trends of a city’s dragonfl y fauna RIGUEZ-TAPIA G. & CÓRDOBA-AGUILAR A. 2014: Hybridization (Odonata). — Braunschw. Naturk. Schr. 8: 449–476. rate and climate change: are endangered species at risk? — J. TÜZÜN N., DEBECKER S., OP DE BEECK L. & STOKS R. 2015: Urbani- Insect Conserv. 18: 295–305. sation shapes behavioural responses to a pesticide. — Aquat. SAITO Y. & OWADA M. 2005: Dragonfl ies (Odonata) of the Toki- Toxicol. 163: 81–88. wamatsu Imperial Villa, Tokyo, Central Japan. — Mem. Natn. UBONI C., BRESSI N. & COLLA A. 2006: An urban population of Sci. Mus. (Tokyo) 39: 431–438. Cordulegaster heros Theischinger, 1979 in Italy. — Att. Mus. SATO M., KOHMATSU Y., YUMA M. & TSUBAKI Y. 2008: Population Civ. Stor. Nat. Trieste 53: 207–211. genetic differentiation in three sympatric damselfl y species in VAN DE KOKEN A.F., MATOS F.A.R. & MARTINS R.L. 2007: Behav- a highly fragmented urban landscape (Zygoptera: Coenagrioni- ior of Pantala fl avescens (Odonata, Anisoptera, Libellulidae) dae). — Odonatologica 37: 131–144. and waste of reproductive investment in urban areas. — Bol. SCHLAEPFER M.A., RUNGE M.C. & SHERMAN P.W. 2002: Ecologi- Mus. Biol. Mello Leitao (N.S.) 21: 7–18. cal and evolutionary traps. — Trends Ecol. Evol. 17: 474–480. VAN LAAR V. 1999: Recolonization of lowland streams in the SCOLOZZI R. & GENELETTI D. 2011: Spatial rule-based assessment Gelderse Vallei by the banded agrion Calopteryx splendens. — of habitat potential to predict impact of land use changes on Entomol. Ber. (Amsterdam) 59: 109–114. biodiversity at municipal scale. — Environ. Manag. 47: 368– VAN LANGEVELDE F. 2015: Modelling the negative effects of land- 383. scape fragmentation on habitat selection. — Ecol. Informatics SEAGER J. & ABRAHAMS R.G. 1990: The impact of storm sewage 30: 271–276. discharges on the ecology of a small urban river. — Wat. Sci. VAN PRAET N., COVACI A., TEUCHIES J., DE BRUYN L., VAN GOSSUM Tech. 22: 163–171. H., STOKS R. & BERVOETS L. 2012: Levels of persistent organic SETO K.C., GÜNERALP B. & HUTYRA L.R. 2012: Global forecasts pollutants in larvae of the damselfl y Ischnura elegans (Odona- of urban expansion to 2030 and direct impacts on biodiversity ta, Coenagrionidae) from different ponds in Flanders, Belgium. and carbon pools. — Proc. Natn. Acad. Sci. 109: 16083–16088. — Sci. Total Environ. 423: 162–167. SHOCHAT E., WARREN P.S., FAETH S.H., MCINTYRE N.E. & HOPE VAUGHAN I.P. & ORMEROD S.J. 2012: Large-scale, long-term D. 2006: From patterns to emerging processes in mechanistic trends in British river macroinvertebrates. — Global Change urban ecology. — Trends Ecol. Evol. 21: 186–191. Biol. 18: 2184–2194. SILVA D.D.P., DE MARCO P. & RESENDE D.C. 2010: Adult odonate VERMONDEN K., LEUVEN R.S.E.W., VAN DER VELDE G., VAN KATWIJK abundance and community assemblage measures as indicators M.M., ROELOFS J.G.M. & JAN HENDRIKS A. 2009: Urban drain- of stream ecological integrity: A case study. — Ecol. Indicat. age systems: An undervalued habitat for aquatic macroinverte- 10: 744–752. brates. — Biol. Conserv. 142: 1105–1115. WATSON J.A.L. 1992: Oviposition by exophytic dragonfl ies on ve- hicles. — Notul. Odonatol. 3: 137.

228 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

WATTS P.C., ROUQUETTE J.R., SACCHERI J., KEMP S.J. & THOMPSON WILLIGALLA C., MENKE N. & KRONSHAGE A. 2003: Importance of D.J. 2004: Molecular and ecological evidence for small-scale rain storage reservoirs for nature conservation – example of isolation by distance in an endangered damselfl y, Coenagrion dragonfl ies in the city of Münster/Westphalia. — Natursch. mercuriale. — Mol. Ecol. 13: 2931–2945. Landschaftspl. 35: 83–89. WILDERMUTH H. 1998: Dragonfl ies recognize the water of rendez- WILSON K.D.P. 1997: The odonate faunas from two vous and oviposition sites by horizontally polarized light: A streams, with details of site characteristics and developmental behavioural fi eld test. — Naturwissenschaften 85: 297–302. threats. — Odonatologica 26: 193–204. WILDERMUTH H. & HORVÁTH G. 2005: Visual deception of a male YU J., WANG T., HAN S., WANG P., ZHANG Q. & JIANG G. 2013: Libellula depressa by the shiny surface of a parked car (Odo- Distribution of polychlorinated biphenyls in an urban riparian nata: Libellulidae). — Int. J. Odonatol. 8: 97–105. zone affected by wastewater treatment plant effl uent and the WILLIGALLA C. & FARTMANN T. 2009: The Odonata fauna of the transfer to terrestrial compartment by invertebrates. — Sci. rain-storage ponds in the city of Mainz, Rhineland-Palatinate, Total Environ. 463–464: 252–257. Germany. — Libellula 28: 117–137. Received February 25, 2015; revised and accepted January 27, 2016 WILLIGALLA C. & FARTMANN T. 2012: Patterns in the diversity of Published online February 15, 2016 dragonfl ies (Odonata) in cities across Central Europe. — Eur. J. Entomol. 109: 235–245.

Table S1. Summary of publications considered in the analysis and the categories in which they were included. Reference Studied group Location Habitat type Variables Categories Results summary Agüero- Anax imperator, Crocothemis erythraea, Sympetrum fonscolombii Pelegrín & Urban Taxa richness, abundance, and Trithemis annulata were found. T. annulata was the most Odonates Spain Diversity Ferreras- pond exuviae dry weight, sex ratio abundant and male exuviae were heavier. There were slightly more Romero (1994) males than females. Taxa richness, abundance, Taxa richness was higher in undisturbed riparian land use in all Alvarez & Aquatic Temporary Spain community assemblage, fl ow Diversity aquatic invertebrates including odonates; Abundance was related Pardo (2007) macroinvertebrates streams permanence, riparian land use to fl ow permanence, independent from land use. Physicochemical features In all aquatic invertebrates including odonates, upstream pollution upstream (undisturbed) and Azrina et al. Aquatic Diversity indices were signifi cantly lower than downstream, where urban Malaysia River downstream (highly urbanised) (2006) macroinvertebrates Toxicology pollution was discharged. Diversity measurements were also sites, taxa richness and correlated with pollution indices. abundance, BMWP scores Highly Bracken & urbanised Fifty species of odonates encountered, which represents 47.2% Odonates Canada Taxa richness Diversity Lewis (2004) Conservation of the county richness. area Brandt & Taxa richness A total of 28 species of odonates was recorded, 21 of them were Buchwald Odonates Germany Ponds Diversity and abundance native from the area. (2011) Birds, fi sh, Human disturbance factors amphibians, aquatic (agriculture, urban development, Non-stressor variables were a better predictor of diversity than Brazner Coastal Diversity macroinvertebrates, USA contaminants), non-stressor human disturbance factors; fi sh (Ambloplites rupestris) and Aeshna et al. (2007) wetlands Toxicology wetland vegetation, variables (vegetation, watershed), spp. were the strongest indicators of urban development. and diatoms taxa richness Woodland A total of 210 species of higher plants; 24 species of mammals, Plants and United and parkland reptiles and amphibians; 82 species of birds; 101 species of Burton (1995) Taxa richness Diversity animals Kingdom (now golf- lepidopterans, and some more records of other insect orders, course) including odonates. Richness was considerably high; all amphibians found were included Chovanec Amphibians and Artifi cial Austria Taxa richness and abundance Diversity in the Red List of Endangered Species and the odonate species (1994) odonates urban pond were native from the area. Chovanec & Canals and Overall odonate diversity had increased since the implementation Odonates Austria Taxa richness and abundance Diversity Raab (1997) urban pond of the canal system and creation of artifi cial pond. Shallow sites without direct connection to the main river (Danube) Plants, odonates, River- Chovanec Taxa richness, abundance, were rich in odonates, amphibians, and riparian vegetation. The amphibians, Austria fl oodplain Diversity et al. (2000) community assemblage new presence of Ischnura pumilio demonstrates the connectivity reptiles, waterfowl systems facilitated by the new landscape. Ponds were inhabited mostly by amphibians and odonates, whereas Odonates, River- Chovanec Taxa richness, abundance, fi sh richness was related to connectivity. New fl oodplain system amphibians Austria fl oodplain Diversity et al. (2002) community assemblage facilitated migration paths for amphibians and dragonfl ies, but no and fi sh systems suitable breeding sites were found. Water quality measurements, Cleto Filho & Aquatic Diversity Water quality was lower in streams with urban input, which Brazil Streams taxa richness, diversity and Walker (2001) macroinvertebrates Toxicology negatively affected overall diversity, including odonates. similarity indices Golf-course Taxa richness in golf courses Species composition was not signifi cantly different between Colding et al. Amphibians Sweden and off- and off-course ponds, diversity Diversity ponds. Leucorrhinia pectoralis, an endangered species, was found (2009) and odonates course ponds and similarity indices exclusively in golf course ponds. Craves & Lotic and len- Ninety species of odonates encountered within a highly-urbanised Odonates USA Taxa richness and abundance Diversity O’Brien (2013) tic aterbodies county. Dombrovskiy Aquatic Taxa richness, abundance, Diversity Both diversity and saprobic indices were inversely related. & Kharchenko Urban lake macroinvertebrates diversity and saprobic indices Toxicology Zygopterans were the dominant predators. (2005) Low diversity in all sampling sites, elevated pollution rates. Edokpayi Aquatic Water quality measurements, Diversity Nigeria Lagoon BOD and TDB content were signifi cantly different among sites. et al. (2004) macroinvertebrates taxa richness and diversity index Toxicology No anisopterans were found. Physicochemical features, ecolo gi cal quality and land use Species composition was negatively related to physicochemical Ferreras- upstream (undisturbed) and Diversity values and modifi cation of land use. Communities in sites less Romero Odonates Spain River downstream (highly urbanised) Toxicology affected by human impact were dominated by semivoltine et al. (2009) sites, taxa richness, abundance, anisopterans. IBMWP scores Meteorological parameters, taxa The highest richness of adults was recorded during the warmer Fischer et al. Urban rain Aquatic insects Argentina richness and abundance along Diversity months; immatures were out of phase. Most ponds accounted less (2000) pools seasons than 25% of the recorded taxa. Only two odonate taxa recorded. 229 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

Table S1 (continued). Reference Studied group Location Habitat type Variables Categories Results summary Temporary, Odonate richness was higher where fl oating vegetation was found. urban Fontanarrosa Taxa richness in temporary pools was not signifi cantly different Aquatic insects Argentina pools and Taxa richness and diversity index Diversity et al. (2004) from permanent ponds, but overall diversity was lower. Only four permanent, odonate taxa recorded. rural lagoons Taxa richness, abundance, Aquatic molluscs, River- Molluscs and dragonfl ies were positively affected; fi sh showed no Funk et al. and species composition was dragonfl ies Austria fl oodplain Diversity change. Dragonfl ies had increased taxa richness and abundance, (2009) assessed before and after a water and fi sh systems but no signifi cant change in species composition. enhancement scheme Reptiles, amphi- River- Most of the species selected had a higher probability of being Funk et al. Probability of occurrence with bians, fi sh, snails Austria fl oodplain Diversity found in connected conditions. Odonate species included in the (2013) connected and isolated conditions and odonates systems model were Leucorrhinia pectoralis and Ophiogomphus cecilia. Diversity Dispersal was mostly local, but potential for larger dispersal Garrison Behavioural Urban park was detected. Constant population size, short life span, quick & Hafernik Ischnura gemina USA Population dynamics ecology creek maturation rate, slightly more males than females; one satellite (1981b) Life-history population found. traits Garrison Diversity Urban park Range is limited to small urban area, may have adapted to & Hafernik Ischnura gemina USA Geographic range Behavioural creek disturbance. Andromorphic female was described. (1981a) ecology Heavy metal concentration related Girgin et al. Diversity Aeshna juncea was a good bioindicator for Mn, Pb, and Ni; Aquatic insects Turkey Streams to taxa richness, abundance and (2010) Toxicology Platycnemis pennipes for Cd, B, Fe, and total hardness. diversity index Habitat variables (human Goertzen disturbance, vegetation, substrate Vegetation increased taxa richness and evenness, but decreased & Suhling Odonates Germany Ponds types, percentage of detritum, Diversity dominance. Human disturbance was not a signifi cant factor. (2013) mud, etc.) related to taxa richness, abundance, diversity indices Diversity Reintroduction of the endangered damselfl y was successful only Hannon & Population size, survivorship, Behavioural Ischnura Urban park one year. Reintroduced males moved longer distances than the Hafernik USA longevity, oviposition, ecology gemina creek ones recorded in 1979 and 1983, before their local extinction. No (2007) and dispersal Life-history oviposition observed at the end of the year. traits Richness increased in site with less sewage input, but Aquatic Taxa richness, abundance, evenness decreased; trichopterans and ephemeropterans were Henriques- macroinvertebrates community assemblage, diversity Diversity characteristic of these sites. Abundance was positively related to de-Oliveira Brazil Lagoon associated to and similarity indices in sites with Toxicology sewage input; chironomids and oligochaetes were present in such et al. (2007) Typha domingensis urban sewage input sites. Micrathyria spp. and Miathyria sp. were found exclusively in the site with less sewage input. Relation of richness and abundance Taxa richness peaked in early summer in ponds surrounded by Jara et al. Predatory aquatic with hydroperiod of the ponds, forest. Presence of fi sh did not alter taxa richness signifi cantly. Argentina Pools Diversity (2013) insects physical features, vegetation and The most frequent odonate species were Rhionaeschna variegata presence of fi sh and Cyanallagma interruptum Taxa richness, abundance, Dipterans, coleopterans, and lepidopterans were more abundant Kalcounis- Urban community structure (insects and Diversity Insectivorous upstream; odonates were more abundant downstream. Rueppell USA stream bats) and foraging behaviour (bats) Behavioural bats and insects Wastewater effl uent affected bat community structure, but not their et al. (2007) system related to wastewater treatment ecology foraging behaviour. plant effl uent Karouna- Zn and Cu concentrations in odonates were signifi cantly higher in Metal concentrations in Renier & Aquatic Stormwater watersheds with commercial development. All concentrations were USA invertebrates, sediments, and water Toxicology Sparling macroinvertebrates ponds below lethal for fi sh diet. No differences in sediments and water in relation to watershed land use (2001) concentration. Taxa richness, relative abundance, Kulkarni & Community assemblage was signifi cantly different among land diversity and similarity indices, Subramanian Odonates India River Diversity use types and season, presenting high diversity and abundance in and community assemblage along (2013) urbanised regions during the post monsoon season. different land use types Lotic and Kury & Christ Taxa richness A total of 42 species encountered, including two endangered Odonates Switzerland lentic Diversity (2010) and abundance (Gomphus pulchellus and Gomphus simillimus). waterbodies The BIO-SAFE biodiversity assessment method was developed Higher plants, based on several species of rivers and their fl oodplains, including odonates, Taxa richness, diversity, 14 species of odonates. This method was tested in different Lenders butterfl ies, fi sh, The River protection status using Diversity ecotopes from urban fl oodplains, and showed that ecotope et al. (2001) amphibians, Netherlands fl oodplains BIO-SAFE method saturation (TES) and the actual ecotope importance (ATEI) scores reptiles, birds must be taken into account to gain insight in the value of ecotopes and mammals for endangered species. Lubertazzi Community assemblage, taxa Richness and evenness did not differ signifi cantly between urban & Ginsberg Odonates USA Ponds richness, and diversity indices Diversity and rural sites; many species were more commonly found in urban (2010) along an urban-to-rural gradient sites with fi sh. The Index of Biotic Integrity (IBI) was developed using percent Physicochemical features, habitat Ephemeroptera, Odonata, and Trichoptera (EOT); EOT richness; Lunde Aquatic variables (vegetation composition, Diversity percent Tanypodinae/Chironomidae; Oligochaeta richness; & Resh USA Ponds macroinvertebrates substrate, urbanisation percentage), Toxicology percent Coleoptera; and predator richness. This method was (2012) taxa richness and abundance negatively related to percentage of urbanisation and showed no signifi cant bias with environmental gradients. Mahato & Aquatic Physicochemical features, Diversity Abundance was signifi cantly higher in the urban stream, no Kennedy USA Streams macroinvertebrates taxa richness and abundance Toxicology differences in richness. Two odonate taxa found. (2008a) Mahato & Erpetogomphus Survival, head width, total width, Life-history No survival in three sites (all of them in summer, two in spring). Kennedy USA Ponds designatus wing pad length and wet weight traits Growth rate was signifi cantly higher in one of the urbanised sites. (2008b) Majumder Taxa richness, abundance, Aquatic insects India Lakes Diversity Hemipterans and odonates had the highest taxa richness. et al. (2013) diversity indices Community assemblage in the main stem and its tributaries Physicochemical features, was signifi cantly different due to abundance of chironomids Malherbe Aquatic South River and Diversity taxa richness, abundance, and oligochaetes and low water quality. The polluted river et al. (2010) macroinvertebrates Africa tributaries Toxicology and community assemblages had decreased sensitive taxa such as Atyidae, Naucoridae, Gomphidae and Leptoceridae.

230 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

Table S1 (continued). Reference Studied group Location Habitat type Variables Categories Results summary Phrynops Chironomus sp. was the most frequent and abundant prey; Martins geoffroanus Behavioural Brazil River Composition of stomach contents odonate larvae, molluscs, fi sh and plants were present as et al. (2010) (Chelidae) ecology well. and its prey Diversity A total of 11 species were found, Sympetrum striolatum Behavioural imitoides was abundant in all pools, since chironomids (their Matsura Taxa richness, abundance, Odonates Japan Swimming pools ecology prey) are very abundant. Females lay their eggs directly on et al. (1998) life-history traits Life-history water and eggs hatch before other dragonfl y species, which traits also increases their abundance. Sympetrum striolatum imitoides was the most abundant in Matsura Diversity all pools, which fed on chironomid larvae. They emerge in Swimming Taxa richness and abundance, et al. Odonates Japan Life-history May-June and deposit eggs directly on water in October, pools survival, predation (1995) traits coinciding with non-use period of the pools. Male established their territory for 1–18 days. A total of 32 species were found. Erythrodiplax basifusca and Monteiro Taxa richness, abundance and Argia sp. were associated with deforested streams, hence et al. Odonates Brazil Streams community assemblage with Diversity could potentially be used as bioindicators for deforestation (2013) and without riparian vegetation from creation of new roads. Community assemblage allowed site classifi cation in four Moreno Taxa richness, abundance, and categories: natural, altered, highly altered and degraded. Aquatic River and et al. Brazil community assemblage using Diversity Sites in the degraded category were near urban sites. macroinvertebrates tributaries (2009) BEAST method Calopterygidae and Gomphidae represented non-impacted sites. Waterbodies in meadows, Taxa richness and density were negatively related to turbidity Mostert The arable land, Taxa richness, population and positively related to riparian vegetation. Natural areas Odonates Diversity (1998) Netherlands nature reserves, density, water turbidity were the most diverse. However, richness was higher in urban recreational areas sites than in agricultural areas. and urban areas Murdoch United Lotic and lentic A total of 11 species were found, fi ve of them were probably Odonates Taxa richness Diversity (1989) Kingdom waterbodies breeding. Neiss Microstigma Brazil Pond Not defi ned Diversity The larval description of the species was made. et al. (2008) maculatum Taxa richness, abundance, Wastewater input increased fl ow and abundance, but community assemblage, hydrology decreased conductivity and taxa richness. Tributary Nelson Aquatic Diversity USA Drainage features (velocity, depth, width) communities, which were associated with high conductivity, (2011) macroinvertebrates Toxicology and water quality measurements were taxa-rich compared with other groups and tended to before and after a treatment plant contain odonates and a variety of dipteran and beetle taxa. Heavy metal concentration in All demonstrated to be good indicators for heavy metal Nummelin Predatory aquatic dragonfl ies, antlions, waterstriders pollution, although ants were the least effective. Waterstriders Ponds Toxicology et al. (2007) insects and ants, both polluted and control displayed high levels of Fe and Mn; antlions and odonates for sites Fe and Cd; antlions and ants for Pb and Mn. Osada & Taxa richness and abundance, Diversity Odonate richness increased after improvement of the pond, Odonates and Tabata Japan Pond succession (hydrophytes) and Behavioural aquatic plants established there as well. Five distribution aquatic plants (1992) dispersal (odonates) ecology patterns were described. One third of the taxa collected belonged to the sensitive EPOT insect orders (Ephemeroptera, Plecoptera, Odonata, Poulton Aquatic Water quality metrics, taxa Diversity and Trichoptera). However, Trichoptera abundance decreased USA River et al. (2003) macroinvertebrates richness and diversity indices Toxicology downstream, next to a large city, whereas Oligochaeta relative abundance increased. Water quality metrics were particularly low downstream as well. Marginal fauna was more diverse than in benthos and Biomass, taxa richness, Principe & drift. Rural sites had higher biomass and abundance, yet Aquatic and diversity indices Corigliano Argentina River Diversity urban sites showed higher richness. Odonates were mostly macroinvertebrates in rural (2006) representative of marginal fauna, both in urban and rural sites, and urban sites except for Aeshna sp., which was only found in urban sites. Natural and recovering forests (riverine and non- Taxa richness and abundance, Pines had low taxa richness and abundance. Gardens Pryke & Plants and South riverine), natural species accumulation curves, provided refugees in urban areas for invertebrate diversity. Samways Diversity invertebrates Africa and recovering non-parametric estimators of Odonates and lepidopterans were more commonly found in (2009) fynbos, botanical richness, community assemblage fynbos and botanical gardens. gardens and alien pine plantations Pujol-Luz Urban water Taxa richness Twenty species of odonates were found, Odonates Brazil Diversity (1987) cisterns and abundance mostly during the month of November. Most systems showed low levels of pH, nutrients Rivera Physicochemical features, Algae, zooplankton and ions. Dominant algae were Bacillariophyceae Rondón River-fl oodplain community assemblage, taxa Diversity and aquatic Colombia and Zygnemaphyceae; coleopterans, odonates and et al. systems richness, abundance, Toxicology macroinvertebrates ephemeropterans were the most abundant in all communities, (2010) and diversity indices and were more diverse in substrates rich in leaf litter. Community assemblage, Rizzoni Aquatic Micronucleus frequency increased towards the city centre, diversity indices, taxa richness, Diversity et al. macroinvertebrates Italy River as well as invertebrate biomass, but diversity decreased. biomass and micronucleus Toxicology (1995) and Vicia faba Only two odonate taxa were reported. frequency Three species were found at fi rst, Aeshna cyanea was Sacha Garden Taxa richness, abundance, the most abundant. After a year, the other species were Odonates Diversity (2011) pond and population size outcompeted or eliminated by predation. Abundance grew up to 1 individual per litre. Saito & Garden A total of 18 species were enlisted, including the rare Owada Odonates Japan Taxa richness and abundance Diversity pond damselfl y Ceriagrion nipponicum. (2005) A description of the vegetation composition and structure Samraoui Plants, odonates Taxa richness and vegetation Algeria Lake Diversity was made, as well as an inventory of 45 bird species and 23 et al. (1992) and birds composition odonates.

231 Villalobos-Jiménez et al., Eur. J. Entomol. 113: 217–232, 2016 doi: 10.14411/eje.2016.027

Table S1 (continued). Reference Studied group Location Habitat type Variables Categories Results summary Environmental data, taxa A river through richness and abundance, Samways plantation forests, Industrial areas were the second lowest taxa richness, but had the South species accumulation curves, & Steytler Odonates residential areas, Diversity highest abundance in anisopterans. Parks, on the other hand, were Africa non-parametric estimators (1996) parklands, and the highest in zygopteran richness and abundance. of richness, community industrial areas assemblage

Rice paddies, Diversity No signifi cant differences in genetic diversity in urban and rural Sato et al. Zygoptera Japan natural and Genetic variability Behavioural populations. However, genetic differentiation was signifi cantly higher (2008) man-made ponds ecology in urban populations, meaning that dispersal is limited.

Muscardinus avellanarius, Sitta europaea, Probability of occurrence Scolozzi Erinacaeus according to their breeding, Habitat suitability models were used for mapping the impact & Geneletti europaeus, Italy Valley Diversity survival, dispersal, habitat of urban land use. (2011) Lanius collurio, unsuitability and hostility Rana synklepton esculenta, and Calopteryx virgo Physicochemical features, Argia modesta was abundant upstream; taxa richness and Silva et al. ecological quality, taxa Diversity Odonates Brazil River abundance were affected by seasonality and lack of riparian (2010) richness and abundance Toxicology vegetation. up- and downstream MeHg concentration in sediment, water and invertebrates was Methylmercury concentration higher in the newest (urban) wetlands. Odonates were signifi cantly Sinclair Invertebrates Canada River in sediment, water and Toxicology greater in wetlands equal to or less than 2 years old. Odonate MeHg et al. (2012) invertebrates concentrations from new and old wetland were not signifi cantly different. Community assemblage, Taxa richness and diversity were lower in urban sites. However, Smith & taxa richness, abundance, urban sites had high similarity in both headwater and main-stem Lamp Aquatic insects USA Streams diversity and similarity Diversity communities, unlike rural sites. The unique headwater taxa in urban (2008) indices in urban and rural headwater streams belonged only to Odonata (Ischnura spp. and watersheds Calopteryx maculata) and Diptera (Aedes and Odontomyia). Damselfl y assemblage was mostly formed by generalist species Diversity Water quality metrics, found in lentic habitats. Ischnura elegans and Erythromma Solimini Toxicology Zygoptera Italy River community assemblage (= Cercion) lindenii were the most abundant in highly polluted et al. (1997) Life-history and life-history traits wetlands, presenting a longer reproductive period, absence of traits diapause, and tolerance of low oxygen concentration. Srinivasulu & All studied samples contained mostly insects and , including Bats and Forest caves Composition Behavioural Srinivasulu India odonates. Forest bats presented opportunistic feeding behaviour, their prey and urban sites of faecal pellets ecology (2005) while urban ones were selective with their prey. Steytler & Diversity Stenotopic species were highly sensitive to changes in sunlight, South Artifi cial Biotope preference, Samways Odonates Behavioural water fl ow and vegetation structure. Yet, taxa richness increased Africa park pond taxa richness (1995) ecology over 100% after the creation of the pond. Taxa richness, community Taxa richness doubled after implementation of the reservoir. The Suh & Stream assemblage, habitat variables South most important factors determining species assemblage were Samways Odonates in an urban (shade, vegetation structure Diversity Africa vegetation structure and composition, percentage shade, submerged (2005) reservoir and composition, substrate, vegetation, water fl ow and amount of open water. etc.) A total of 51 species were found. Sympetrum pedemontanum, Coenagrion pulchellum, Ischnura pumilio and Sympetrum danae Suhling Species richness, Lotic and lentic had declined, although species like fusca, Gomphus et al. Odonates Germany abundance and population Diversity waterbodies vulgatissimus, Ophiogomphus cecilia, Orthetrum brunneum and (2009) trends Orthetrum coerulescens had increased in a period of almost 30 years. A population of Cordulegaster heros was found in an urban stream, Uboni et al. Cordulegaster Italy Stream Not defi ned Diversity where it co-occurs with Cordulegaster bidentata and Calopteryx (2006) heros virgo. Eggs laid, occurrence P. fl avescens occurrence was positively related to the amount of Van de Pantala frequency, amount of cars Behavioural cars found in the parking area. There was also a preference towards Koken Brazil Parking areas fl avescens in the parking area, ecology light coloured cars. Oviposition was recorded on the hood surfaces, et al. (2007) light/dark car ratio which represents an energy loss for the females. C. splendens had disappeared around 1970 due to pollution and van Laar Calopteryx The Streams Population density Diversity deforestation. After mitigation measures, the species recolonised (1999) splendens Netherlands the area, including urban sites. Diversity Genetic differentiation was signifi cant throughout sampling area, Watts et al. Coenagrion United River Genetic variability Behavioural thus species is mostly sedentary. Urban areas made a barrier effect (2004) mercuriale Kingdom ecology and limited their dispersal. Willigalla & Central Taxa richness is positively related to city size, but decreases towards Fartmann Odonates Cities Taxa richness and city area Diversity Europe city centres. (2012) Willigalla & Taxa richness, abundance, A total of 32 species were recorded. Richness increased in suburban Rain-storage Fartmann Odonates Germany community assemblage Diversity ponds and was positively related to pond size. Similarity index was ponds (2009) and similarity index negatively related to distance between ponds.

Willigalla Rain-storage A total of 27 species were recorded. Exposure to sunlight and Odonates Germany Taxa richness Diversity et al. (2003) ponds vegetation structure defi ned odonate diversity.

Wilson Taxa richness and Two sites were particularly rich in Gomphidae and Macromiidae Odonates Streams Diversity (1997) abundance species. Zooplankton presented the highest PCB levels, followed by Zooplankton Polychlorinated biphenyl Yu et al. soil-dwelling invertebrates. Chironomids and odonates had high and aquatic China River (PCB) concentration in Toxicology (2013) concentrations of mid-chlorinated congeners (PCB-153 and PCB- macroinvertebrates invertebrates 138).

232