The Importance of Fluvial Habitats for Amphibian Conservation in the Mediterranean Climate

Basic and Applied Herpetology 31 (2017) 5-16

The importance of fluvial habitats for amphibian conservation in the Mediterranean climate

Wouter de Vries1, Adolfo Marco2,*

1 Asociación Ambor, Carretera Constantina - El Pedroso km. 1, 41450 Constantina, Sevilla, Spain. 2 Doñana Biological Station, CSIC, C/Américo Vespucio s/n, 41092 Sevilla, Spain.

*Correspondence: Phone: +34 606252802, E-mail: [email protected]

Received: 19 October 2016; returned for review: 21 December 2016; accepted 17 March 2017.

The importance of standing water habitat for amphibians is widely known and recognized. How- ever, in some arid or semiarid zones the availability of these temporal habitats is uncertain and fluvial habitats could play a very important role for amphibian conservation. For example, in the Mediterranean region many fluvial habitats have a temporary character, lacking predatory fish populations and hosting diverse amphibian communities. To compare the relative importance of various fluvial and still water habitats, we studied the breeding amphibian community over a wide area from 2006 to 2008 in southwestern Spain. All amphibian species found in the area were present in lotic habitats and the highest amphibian diversity was found in temporary stream habitats. Fluvial habitats were among the most important habitats used for reproduction by eight amphibian species of conservation concern, whereas for seven species a significant positive selection was found towards one or several fluvial habitat types as reproduction habitats. The conservation of fluvial habitats including rigorous impact assessments and management programs can be very important for the conservation of endangered amphibians in these semi-arid areas.

Key words: amphibians; aquatic habitat; conservation; diversity; ﬂuvial habitat; Mediterranean region.

Amphibians are declining worldwide zar, 2003) and might be essential for re- and need urgent protection and restora- gional biodiversity (Semlitsch Bodie, tion of their main habitats (Blaustein 1998; Williams et al., 2004). In Europe, Kiesecker, 2002; Stuart et al., 2004; stream habitats are important for several Blaustein Dobson, 2006). The right eval- amphibian species (e.g. Pleguezuelos et uation of the use of different aquatic habi- al., 2002; Creemers Van Delft, 2009) and tats by amphibians is necessary for the also in other regions streams can be of design and implementation of conserva- high value for some species (e.g. Kroll et tion strategies for this highly threatened al., 2008; Welsh Hodgson, 2008; Grant et vertebrate group. Many field studies point al., 2009). However, streams and rivers are out that ponds and pools are the most im- usually unsuitable habitats for most am- portant amphibian habitats on temperate phibian species, mainly because of strong regions (GÜnther, 1996; Semlitsch Body, currents and high predation risk by fishes. 1998; Snodgrass et al., 2000; Beja Alca- Several studies in Britain have demon-

DOI: http://dx.doi.org/10.11160/bah.56 DE VRIES & MARCO strated the high value of pond habitats amphibian community. An exhaustive compared to rivers, streams and ditches evaluation of the relative importance of (e.g. Biggs et al., 2000; Wood et al., 2003; ﬂuvial habitats for amphibians is still lack- Williams et al., 2004). In the Mediterranean ing. Studies of aquatic communities within region, temporary ponds are also valuable entire catchment areas are scarce and so habitats for a wide range of freshwater far do not include amphibians (e.g. Biggs fauna including amphibians (Boix i Mas- et al., 2000; Williams et al., 2004). We inves- afret, 2002; Beja Alcazar, 2003; Díaz- tigated the entire amphibian community Paniagua et al., 2005, 2006). However, in in a typical Mediterranean zone, surveying arid and semiarid zones of the Mediterra- all amphibian species breeding in all types nean region, temporary ponds can be of available aquatic habitats, in order to scarce, strongly impacted by human activi- obtain a comparative view of the relative ties and with a very short hydroperiod. In importance of lentic and lotic habitats for this scenario, streams and rivers that can the overall amphibian biodiversity as well also have a temporary character could as for endangered species. play an important ecological role for the

Figure 1: Map of the Sierra Norte de Sevilla Natural Park (southwestern Spain) and its location within the Iberian Peninsula, showing the main rivers and streams and all the waterbodies sampled for amphibians. Open stars correspond to lentic habitats and black stars correspond to lotic habitats. The vast majority of the sampled sites are inside the limits of the Natural Park and only few of them are in the external buﬀer zone.

6 FLUVIAL HABITATS FOR AMPHIBIAN CONSERVATION

Materials and Methods irregular precipitation of around 750 mm annually with maximum in winter Study sites (Consejería de Medio Ambiente, 2005). To evaluate the relative importance of Previous studies have recorded the pres- fluvial habitats on amphibian abundance ence of at least 12 amphibian species and diversity we selected the Sierra Norte (Pleguezuelos et al., 2002; De Vries et al., de Sevilla Natural Park (SNSNP, 177 484 2009). For a detailed description of the ar- ha, Fig. 1) and adjacent non-protected sur- ea, see Menor Cuenca (2008) and De roundings. This area is located in the Sier- Vries et al. (2009). ra Morena range in the north of the prov- The 301 lotic aquatic habitats selected ince of Seville (southwestern Spain) and for the study (Fig. 1) were classified in presents a high diversity and availability three different categories: rivers, streams of freshwater ecosystems along with a sig- and ephemeral streams (Table 1). The riv- nificant amphibian diversity. The climate ers in the area are less than 10 m wide and is typically Mediterranean with mean tem- seasonal, normally with running water in peratures between 18.6 and 26.1 ºC in Au- autumn, winter and spring, and lack of gust and 4.3 to 13 ºC in January, and an flowing water during the summer with

Table 1: Number of sampled sites (N), number of sites with amphibian presence (NA), number of amphibian breeding sites (NB) and number of sites sampled during the breeding period of each species, regardless of whether such species was detected or not. Ssal: Salamandra salamandra; Pwal: Pleurodeles waltl; Tpyg: Triturus pygmaeus; Lbos: Lissotriton boscai; Acis: Alytes cisternasii; Dgal: Discoglossus galganoi; Pibe: Pelodytes ibericus; Pcul: Pelobates cultripes; Bspi: Bufo spinosus; Ecal: Epidalea calamita; Hmer: Hyla meridionalis; Pper: Pelophylax perezi. Habitat N NA NB Ssal Pwal Tpyg Lbos Acis Dgal Pibe Pcul Bspi Ecal Hmer Pper type

River 131 97 85 97 73 63 51 37 102 41 40 73 42 42 43

Stream 137 112 101 112 104 72 101 66 137 61 78 102 59 72 59

Ephemeral 33 29 23 29 21 21 26 21 21 17 15 21 21 26 21 stream

Pond 114 86 81 86 77 51 61 40 81 53 52 76 48 52 50

Ephemeral 55 51 45 51 43 21 45 23 52 30 34 43 40 48 40 pond Intact 13 13 9 13 13 13 13 13 13 13 13 2 2 2 4 cistern Broken 20 19 14 18 18 18 18 18 18 18 18 18 4 4 4 cistern Well & 13 13 8 13 13 13 13 13 13 13 13 13 2 2 2 spring Swimming 14 7 5 13 12 9 7 6 14 5 7 13 5 6 5 pool

Trough 10 6 4 7 5 5 5 3 6 4 3 5 2 4 6

7 DE VRIES & MARCO natural permanent pools remaining. These stock density and occurrence period, and systems host a fish community of Cyprini- on cleaning frequency. Where livestock is dae and introduced exotic species (Prenda absent (at least during part of the year) or et al., 2006), and the introduced red swamp has no access to the entire pond area, there crayfish (Procambarus clarkii) as the most is usually vegetation of the genera important large aquatic amphibian preda- Callitriche, Potamogeton and sometimes Cha- tors (e.g. Cruz Rebelo, 2005). Depending ra, Typha and Juncus. on the year and the amount of shadow, the Data collection and analysis rivers can support dense aquatic vegetation with Ranunculus sp. in late winter Data on amphibians were recorded and spring. After strong rainfall, water during three consecutive years (2006-08) levels can rise several meters for a few using standard methods for amphibian days. Depending on the meteorological surveys (Heyer et al., 1994; Glandt, 2011). and hydrological conditions, migrating Sampling included calling surveys, sur- fish go upstream for spawning or alterna- veys on land near the water bodies, visual tively adults stay in the lower areas. With survey in or at the water, net sampling in exception of short periods following heavy water and terrestrial surveys near the wa- rainfall, streams have slow flowing water terbodies for metamorphs. Precipitation that usually forms series of interconnected during the study years was normal, with ponds and pools during the amphibian- 2006 being slightly wetter and 2007 and breeding period and dry out in summer, 2008 drier years, with annual rainfall of consequently lacking a permanent fish 659.4 354.3 and 505.2 mm, respectively, at community. After heavy rainfall, aquatic San Pablo airport, 60 kilometres from the vegetation is removed by the torrent. Dur- study area (average ± SD of annual precip- ing the study years, we observed that itation data in the period 1973-2008 = 543.3 ephemeral streams had running water for ± 201.0 mm). a few days or weeks, with small tempo- For each amphibian species, only data rary pools < 1 m2 surface formed naturally from the sites that were sampled with ap- by the water running along these streams. propriate conditions to detect these species The 239 lentic aquatic habitats selected (suitable observation method, as well as (Fig. 1, Table 1) were classified in seven appropriate time of the year, sampling different categories: ponds (permanent or technique and weather and hydrological long-lasting temporary pools), ephemeral conditions at the site during samplings) ponds (including flooded areas that can were used in the analysis. Due to im- hold water for a few weeks to months), portant phenological differences in the stone cisterns (either intact or broken, fur- reproduction of different species, the field ther on referred to as cistern), wells and surveys were distributed throughout the springs, artificial swimming pools and autumn, winter and early spring of every troughs. The amount and diversity of study year. The studied localities were aquatic vegetation in each site is highly widely distributed over the natural park variable and mainly depends on the live- area (Fig. 1) including three main basins

8 FLUVIAL HABITATS FOR AMPHIBIAN CONSERVATION

(the river Huéznar in the centre of the Oklahoma, USA) were performed for each Park, the river Viar in the west part and amphibian species comparing the ob- the river Retortillo in the east part) and served frequencies of sites of each habitat many secondary basins. Study sites were with successful breeding with the ex- defined as isolated water bodies or stretch- pected frequency if the selection were ran- es of 500 meters of length along a perma- dom. For each chi-square analysis, the nent or temporary running water habitat. habitat categories where the expected fre- Data on ephemeral streams, streams and quency was lower than 5 were excluded rivers were grouped per stretch of 500 me- from this analysis. Similar chi-square anal- ters using the software ArcView 3.2 (ESRI, yses were conducted pooling all data from Redlands, California, USA), resulting in either lentic of lotic habitats together. The approximately 500 to 1000 m2 of surface Bonferroni correction for multiple compar- area per site. isons was applied. We calculated the di- For each site, the species, number of versity of breeding amphibians on each individuals at each developmental stage, type of habitat using the Shannon index type of aquatic habitat and geographic (Krebs, 1989). For this calculation, the coordinates (GPS eTrex®, Garmin, Olathe, abundance of each species on each type of Kansas, USA) were registered. Eleven am- habitat was considered as the percentage phibian species had been widely found of sites of each habitat with evidence of throughout the area in previous studies breeding activity of the selected species in (De Vries et al., 2009). Moreover, the Iberian any of the three study years. parsley frog (Pelodytes ibericus) is consid- Considering the results of the chi- ered rare and with a discontinuous distri- square tests to evaluate the relative im- bution. The European treefrog (Hyla portance of each type of habitat, four cate- molleri) has been sporadically described for the gories were defined to indicate the value area (Pleguezuelos et al., 2002; Reques et of fluvial habitats for each amphibian spe- al., 2006). We registered for each species, year cies in the study area: 0: no statistically and type of habitat the number of breed- significant selection of fluvial habitats and ing localities considering only the presence < 25% of breeding sites corresponding to of eggs, larvae or metamorphs. fluvial habitats; 1: > 25% of breeding sites All statistical analyses were calculated corresponding to fluvial habitats but no using the presence or absence of each spe- statistically significant selection of any flu- cies on each sampled site. We calculated vial habitat type; 2: statistically significant the percentage of locations of each habitat (P < 0.05) selection of any of the three fluvial type with the presence of each amphibian habitat types; and 3: highly significant (P < species. We proceeded similarly for each 0.001) selection of any of the three fluvial species considering together all the lentic habitat types. or lotic habitats. In order to evaluate the Results relative importance of each type of habitat for each amphibian species, chi-square Reproduction of amphibians was de- tests (STATISTICA, Statsoft Inc., Tusla, tected in 375 out of 540 sampled sites

9 DE VRIES & MARCO

- - - - - 4 + 1 + N/A Pper 88.094 11.951 0.0005 < 0.0001

- - - - 4 + + 1 + cantly avoided, avoided, cantly N/A ﬁ 1.617 0.203 Hmer 20.295 0.0004

- - - 4 + = + + N/A Bc 7.025 41.604 0.0080 < 0.0001

- 3 + + = = 1 + s ) comparing the observed and ex- ) comparing the observed and N/A N/A B 7.677 12.139 0.0069 0.0056 P

- - - 3 + + 1 + cance ( ﬁ N/A N/A Pcu 9.380 22.813 0.0022 < 0.0001 cantly preferred, –: habitat signi –:cantly preferred, habitat

ﬁ

= = NA N/A N/A N/A N/A N/A N/A N/A Pibe

analysed because of the low sample size. For species abbre- species For size. sample low the of because analysed al

- - + + 1 + N/A N/A N/A N/A Dg 7.300 0.0069

erent types of habitats, as well as in lentic versus lotic habitats. Bold habitats. lentic versus lotic in as well as habitats, types of erent

- - - - 4 + + 1 + ﬀ N/A Aci 73.061 74.919 < 0.0001 < 0.0001

- 1 = + 1 = = N/A N/A Lb 2.400 0.121 1.833 0.176

- - 3 = + 1 = = N/A N/A 2.525 0.112 Tpyg 13.286 0.0041

- - - 2 + 1 + N/A N/A N/A Pw 47.449 11.578 0.0007 < 0.0001 ) analyses, degrees including of freedom (d.f.) signi and 2

- - 3 + + + 1 = sal S N/A N/A 1.409 0.235 28.023 < 0.0001

e analyses pointing to a preference for lotic habitats. +: habitat signi habitat +: habitats. lotic for a preference pointing to e analyses ic

tat

2 2

st P P Χ Χ bi i

d.f. d.f. erence between observed and expected frequencies, N/A: not not N/A: frequencies, and expected observed between erence Lotic Pond River Lentic Stream ﬀ Cistern ha tat Eph. pond S Eph. stream

cant di son ﬁ

ri Results of the chi-square ( chi-square the of Results a lotic e 2: mp l o Lentic vs. vs. Lentic b All habitats a C T di the in species amphibian each of occurrence of frequencies pected characters indicate thos signi =: no 1. Table see viations, 10 FLUVIAL HABITATS FOR AMPHIBIAN CONSERVATION

(Table 1). The community of amphibians mon toad (Bufo spinosus) and P. perezi, and breeding at each site as well as species di- significantly avoided by four species: the versity varied according to the habitat type sharp-ribbed salamander (Pleurodeles (Table 2). The 12 species present in the area waltl), the pygmy newt (Triturus pygmaeus), were recorded breeding in both fluvial and the spadefoot toad (Pelobates cultripes) still water habitats. Ten species had more and the natterjack toad (Epidalea than 25% of their observations in lotic hab- calamita), which preferred in lentic habitats itats and six species were more common in (Table 2). The chi-square test also showed fluvial than in stagnant water ecosystems. significant differences on habitat selection Lotic habitats were especially important by the southern treefrog (Hyla meridional- for the Iberian midwife toad (Alytes cister- is) but there was no differences in selection nasii), the Iberian painted frog (Discoglossus between lentic and lotic habitats (Table 2). galganoi) and the green frog (Pelophylax pere- Pelodytes ibericus was rare and the sample size zi) (Fig. 2). did not permit a chi-square analysis, alt- Fluvial habitats were significantly pre- hough its frequency in each type of habitat ferred for breeding by five species: the suggests that it prefers lentic habitats common salamander (Salamandra sala- (Table 2). The only species for which no mandra), A. cisternassi, D. galganoi, the com- significant preference for any habitat type

Figure 2: Percentage of breeding sites of each amphibian species corresponding to lotic and lentic habitats. For species abbreviations, see Table 1.

11 DE VRIES & MARCO was recorded was the Iberian newt ity to use fluvial as well as still water habi- (Lissotriton boscai) (Table 2). Fluvial habitats tats, allowing survival of populations dur- were of high importance for one vulnera- ing successive years with low water tables ble and six nearly threatened species and absence of ponds, even of temporary (Table 3). ones. Fortuna et al. (2006) suggested that a The amphibian diversity was especially network of a large number of different high in all fluvial habitats and in the types of temporary aquatic habitats is a ponds, whereas lower species diversity key factor for a favourable conservation values were found for smaller or artificial status of amphibian populations, and Beja ecosystems (Fig. 3). Temporary streams Alcazar (2003) showed that conserva- had the highest diversity index followed tion of amphibian assemblages in tempo- by ponds. rary ponds on Mediterranean farmlands requires networks of ponds with diverse Discussion hydroperiods. Our results indicate that In the Mediterranean region, the high temporary fluvial habitats in the Mediter- species diversity and abundance of am- ranean region are also important in this phibians might be explained by their abil- respect, which is in accordance with the

Table 3: Importance of lotic habitats in the SNSNP for amphibians according to their legal protection in Spain and the European Union (EU) and to their conservation status at European, national (i.e. Spain) and regional (i.e. Andalusia) levels. For explanation of the ﬂuvial habitat importance categories, see Materials and Methods. For species abbreviations, see Table 1. SP: species with Spe- cial Protection level in Spain according to the Spanish legislation (Real Decreto 139/2011, de 4 de febrero 2011), IV: species of community interest that require strict protection according to Habitat Directive of the European Union (Directive 92/43/EEC). c As Triturus marmoratus. d,e,f LC: of Least Concern, NT: Near Threatened, VU: Vulnerable, DD: Data Deﬁcient. Species Importance of Legal protection Conservation status lotic habitats Spain EU European1 National3 Regional4 Pwal 0 SP NT NT NT Ssal 2 NT NT5 Lbos 2 SP NT NT Tpyg 1 SP IV NT2 VU VU6 Acis 3 SP IV NT NT NT Dgal 2 SP IV Pcul 1 SP IV NT NT NT Pibe 0 SP DD NT Bspi 2 Bcal 2 SP IV Hmer 1 SP IV NT NT Pper 3 1According to Temple Cox (2009); 2according to Arntzen et al. (2009); 3according to Pleguezuelos et al. (2002); 4according to Franco Ruiz Rodríguez de los Santos (2001) and Reques et al. (2006); 5as Salamandra salamandra morenica; 6eastern populations, as Triturus marmoratus pygmaeus.

12 FLUVIAL HABITATS FOR AMPHIBIAN CONSERVATION

Figure 3: Shannon index of amphibian species diversity in each type of aquatic habitat.

findings of Wood et al. (2003), who stressed and our study areas had similar site occu- the necessity of preserving temporary pancy, though for most species it was low- aquatic habitats for the conservation of er at SNSNP. Both studies indicate a high amphibians. Fluvial habitats regularly value of ponds as amphibian habitat, but form a part of such networks of temporary at the same time several species in SNSNP waterbodies in the Mediterranean region. had similar or even higher site occupancy Various studies indicate a positive cor- in fluvial habitats. Díaz-Paniagua et al. relation between hydroperiod and am- (2006) demonstrated a high importance of phibian diversity (e.g. Snodgrass et al., temporary and permanent ponds and 2000; Beja Alcazar, 2003; Díaz- lakes in Doñana in southwestern Spain. Paniagua et al., 2006). In these studies, as Seven amphibian species were recorded well as in the present ones, it is observed breeding in the few fluvial habitats studied that the long-lasting, but not permanent, there, with averages of 3.9 species per site waterbodies were the most valuable for for slow-flowing waters and 1.5 species the amphibians. Our study shows also the per site for fast-flowing streams. Our data additional value that fluvial habitats with are in accordance with those of Díaz- long but not permanent hydroperiods Paniagua (1990) and Díaz-Paniagua et al. have, indicating that for the conservation (2006), who observed a high importance of of amphibian communities within ecosys- especially long-lasting temporary habitats tems, measures should be directed at both for most species, and also of ephemeral still water and fluvial temporary habitats. habitats for E. calamita and fluvial habitats Beja Alcazar (2003) observed am- for A. cisternasi. We observed a remarka- phibians in 53 out of 57 ponds (ephemeral, bly low occurrence and importance of temporal and permanent) in a lowland ephemeral ponds for D. galganoi com- area in a Natural Park in southwestern pared to the aforementioned studies con- Portugal. Species occurring in both their ducted in Doñana; the ephemeral micro-

13 DE VRIES & MARCO habitat used by this species during the pre- conservation value that Mediterranean sent study consisted mainly of inundations fluvial habitats have for amphibians. Med- along streams banks. iterranean temporary lotic ecosystems Fluvial ecosystems in the Mediterrane- should be considered for listing on the Eu- an climate are considered suitable aquatic ropean Habitat Directive because of their habitats for all the species found in this high importance to amphibians. study except E. calamita in southwestern Acknowledgement Europe (e.g. Barbadillo et al., 1999; Re- ques, 2000; Salvador 2009). In the present This study was possible thanks to the study, we have quantified the high im- good cooperation with the Natural Park portance of such fluvial habitats for am- Sierra Norte de Sevilla (Consejería de Me- phibian communities in a typical Mediter- dio Ambiente) and landowners in the area. ranean ecosystem in years with normal We especially appreciate the support from precipitation. The inter-annual variations the Directora Conservadora I. Cuenca and in hydroperiod contribute to the long-term other members of the Natural Parks’ staff conservation of the amphibian community (A. Menor, L.M. Platero) for facilitating by enhancing habitat for different species authorizations and stimulating studies on in different years (Jakob et al., 2003). At the herpetology within the Park. Furthermore, species level, our data indicate that fluvial we had great help and information on val- habitats in the Mediterranean region are of uable areas or literature on amphibians high importance for one Vulnerable and from J. Llorente, F. Ugía, A. García, M.C. six Nearly Threatened species (Table 3). Perez, P. Carmona (ACPES), N. Selva and For seven out of nine species of conserva- J. Kielgast. We are thankful to Jim Foster tion concern (i.e. T. pygmaeus, L. boscai, A. for improving the language in the English cisternasii, D. galganoi, P. cultripes, E. manuscript. calamita and H. meridionalis), which require References special protection according to the Spanish Arntzen, J.W.; Jehle, R.; Bosch, J.; Miaud, C.; legislation (Real Decreto 139/2011, de 4 de Tejedo, M.; Lizana, M.; Martínez-Solano, febrero 2011) fluvial habitat is important or I.; Salvador, A.; García-París, M.; Recuero even the preferred habitat. For six species Gil, E.; Sá-Sousa, P. Márquez R. (2009). of European Community Interest (Annex Triturus marmoratus. The IUCN Red List of IV of the European Habitats Directive Threatened Species 2009: e.T59477A11949129. 92/43/EEC), fluvial habitat is among their Barbadillo. L.J.; Lacomba, J.I.; Pérez-Mellado, important habitats in our study area, being V.; Sancho, V. LÓpez-Jurado, L.F. (1999). the most important one for A. cisternasii Anfibios y Reptiles de la Península Ibérica, Ba- leares y Canarias. GeoPlaneta, Barcelona, and D. galganoi. For A. cisternasii, a glob- Spain. ally Nearly Threatened Iberian endemism, Blaustein, A.R. Dobson, A. (2006). Extinc- the fluvial habitats were of highest, almost tions: A message from the frogs. Nature 439: unique importance in the SNSNP, as in 143-144. other Mediterranean ecosystems (Beja et Blaustein, A.R. Kiesecker, J.M. (2002). Com- al., 2009). Thus, our study indicates the high plexity in conservation: lessons from the

14 FLUVIAL HABITATS FOR AMPHIBIAN CONSERVATION

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