Defining the importance of landscape metrics for large branchiopod biodiversity and conservation: the case of the Iberian Peninsula and Balearic Islands

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ArticleTitle _{Defining the importance of landscape metrics for large branchiopod biodiversity and conservation: the case} of the Iberian Peninsula and Balearic Islands

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Journal Name Hydrobiologia

Corresponding Author Family Name Sala

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Division GRECO, Institute of Aquatic Ecology

Organization University of Girona

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Author Family Name Alonso

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Organization Instituto de Acuicultura de Torre de la Sal, CSIC

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Division Department of Ecology

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Phone Fax Email URL ORCID Schedule Received 23 December 2016 Revised 20 June 2017 Accepted 30 June 2017

Abstract _{The deficiency in the distributional data of invertebrate taxa is one of the major impediments acting on the} bias towards the low awareness of its conservation status. The present study sets a basic framework to understand the large branchiopods distribution in the Iberian Peninsula and Balearic Islands. Since the extensive surveys performed in the late 1980s, no more studies existed updating the information for the whole studied area. The present study fills the gap, gathering together all available information on large branchiopods distribution since 1995, and analysing the effect of human population density and several landscape characteristics on their distribution, taking into consideration different spatial scales (100 m, 1 km and 10 km). In overall, 28 large branchiopod taxa (17 anostracans, 7 notostracans and 4

spinicaudatans) are known to occur in the area. Approximately 30% of the sites hosted multiple species, with a maximum of 6 species. Significant positive co-occurring species pairs were found clustered together, forming 4 different associations of large branchiopod species. In general, species clustered in the same group showed similar responses to analysed landscape characteristics, usually showing a better fit at higher spatial scales.

Keywords (separated by '-') _{Anostraca - Co-occurrences - Land cover - Notostraca - Rarity - Spinicaudata}

Footnote Information Electronic supplementary material The online version of this article (doi:10.1007/s10750-017-3293-1)

contains supplementary material, which is available to authorized users.

Guest editors: Federico Marrone, D. Christopher Rogers, Paola Zarattini & Luigi Naselli-Flores / New Challenges in Anostracan Research: a Tribute to Graziella Mura

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C H A L L E N G E S I N A N O S T R A C A N R E S E A R C H 1

2

Defining the importance of landscape metrics for large

3

branchiopod biodiversity and conservation: the case

4

of the Iberian Peninsula and Balearic Islands

5 Jordi Sala .Ste´phanie Gasco´n.David Cunillera-Montcusı´.Miguel Alonso. 6 Francisco Amat.Luis Cancela da Fonseca.Margarida Cristo.

7 Margarita Florencio.Juan Garcı´a-de-Lomas.Margarida Machado. 8 Maria Rosa Miracle.Alexandre Miro´.Jose´ Luis Pe´rez-Bote. 9 Joan Lluı´s Pretus.Florent Prunier.Javier Ripoll .Juan Rueda.

10 Marı´a Sahuquillo.Laura Serrano .Marc Ventura .David Verdiell-Cubedo. 11 Dani Boix

12 Received: 23 December 2016 / Revised: 20 June 2017 / Accepted: 30 June 2017

13 ÓSpringer International Publishing AG 2017

14 Abstract The deﬁciency in the distributional data of 15 invertebrate taxa is one of the major impediments 16 acting on the bias towards the low awareness of its 17 conservation status. The present study sets a basic 18 framework to understand the large branchiopods 19 distribution in the Iberian Peninsula and Balearic 20 Islands. Since the extensive surveys performed in the 21 late 1980s, no more studies existed updating the 22 information for the whole studied area. The present

23 study ﬁlls the gap, gathering together all available

24 information on large branchiopods distribution since

25 1995, and analysing the effect of human population

26 density and several landscape characteristics on their

27 distribution, taking into consideration different spatial

28 scales (100 m, 1 km and 10 km). In overall, 28 large

29 branchiopod taxa (17 anostracans, 7 notostracans and

30 4 spinicaudatans) are known to occur in the area.

31 Approximately 30% of the sites hosted multiple

32 species, with a maximum of 6 species. Signiﬁcant

33 positive co-occurring species pairs were found

clus-34 tered together, forming 4 different associations of

35 large branchiopod species. In general, species

clus-36 tered in the same group showed similar responses to

37 analysed landscape characteristics, usually showing a

38 better ﬁt at higher spatial scales.

A1 Electronic supplementary material The online version of

A2 this article (doi:10.1007/s10750-017-3293-1) contains

supple-A3 mentary material, which is available to authorized users. A4 Guest editors: Federico Marrone, D. Christopher Rogers, Paola A5 Zarattini & Luigi Naselli-Flores / New Challenges in A6 Anostracan Research: a Tribute to Graziella Mura

A7 J. Sala (&) S. Gasco´n D. Cunillera-Montcusı´ A8 D. Boix

A9 GRECO, Institute of Aquatic Ecology, University of A10 Girona, Girona, Spain

A11 e-mail: js.genoher@gmail.com

A12 M. Alonso J. L. Pretus

A13 Department of Ecology, University of Barcelona, A14 Barcelona, Spain

A15 F. Amat

A16 Instituto de Acuicultura de Torre de la Sal, CSIC, A17 Castello´n, Ribera de Cabanes, Spain

A18 L. C. da Fonseca

A19 Laborato´rio Marı´timo da Guia, MARE– Marine and A20 Environmental Sciences Centre, Cascais, Portugal

A21 L. C. da Fonseca

A22 CTA - Centro de Cieˆncias e Tecnologias da A´ gua,

A23 Universidade do Algarve, Faro, Portugal

A24 M. Cristo

A25 FCT, Universidade do Algarve, Faro, Portugal

A26 M. Cristo M. Machado

A27 CCMar, Universidade do Algarve, Faro, Portugal AQ1

123

Journal : Medium 10750 Dispatch : 5-7-2017 Pages : 18

Article No. : 3293 h LE h TYPESET

MS Code : HYDR-D-16-01181 h CP4 h DISK4

Hydrobiologia

DOI 10.1007/s10750-017-3293-1

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39 Keywords _{Anostraca Co-occurrences Land} 40 cover Notostraca Rarity Spinicaudata

41 Introduction

42 Large branchiopods are a key faunal group of 43 crustaceans characteristic of temporary aquatic sys-44 tems (with few exceptions) which can be found across 45 all continents (Brendonck et al., 2008). Although 46 nowadays nearly 600 species of large branchiopods 47 are known worldwide (Rogers et al.,2015), a large part 48 of them are known only from a few localities ([50% of 49 the species are known from B10 localities in the case 50 of anostracans; Rogers, 2013), indicating that the 51 faunal group harbours a large amount of biodiversity, 52 and that the knowledge of the group is still far from 53 being complete (Rogers et al.,2015). This is also the 54 case in the western Mediterranean, where descriptions 55 of new species are still being performed (e.g. Alonso 56 & Garcı´a-de-Lomas, 2009; Korn et al., 2010; 57 Machado & Sala,2013; Boix et al.,2016) and some 58 efforts to describe the distribution of large bran-59 chiopods are made at regional (e.g. Machado et al., 60 1999; Boix,2002; Samraoui & Dumont,2002; Culioli 61 et al., 2006; Marrone & Mura, 2006; Miracle et al., 62 2008; Prunier & Saldan˜a, 2010; Rodrı´guez-Flores

63 et al., 2016) and national level (e.g. Alonso, 1985;

64 Thie´ry, 1987; Defaye et al., 1998; Mura,1999; Van

65 den Broeck et al., 2015a; Marrone et al.,2016). The

66 effects of environmental factors on the distribution of

67 large branchiopods are largely known, particularly

68 those related to habitat characteristics (e.g. salinity,

69 turbidity, temperature, surface, depth, altitude,

vege-70 tation cover; Alonso, 1998; Boven et al., 2008;

71 Nhiwatiwa et al.,2011; Gasco´n et al.,2012; Horva´th

72 et al.,2013; Sahuquillo & Miracle,2013; Stoch et al.,

73

2016). Moreover, some spatial variables at regional 74 level are also known to affect species distribution,

75 such as the closeness of sites (which can be related to

76 dispersal or shared environmental characteristics;

77 Nhiwatiwa et al.,2011; Horva´th et al.,2013), climatic

78 gradients (Stoch et al.,2016) or habitat fragmentation

79 (Gasco´n et al., 2012). The sensitivity of large

80 branchiopods to all this range of environmental and

81 spatial variables makes them especially interesting as

82 biological indicators of the conservation status of

83 temporary wetlands (e.g. Sahuquillo & Miracle,2015;

84 Van den Broeck et al.,2015b; Lumbreras et al.,2016).

85 However, the effects of changes in land use and the

86 fragmentation and loss of habitats have been less

87 explored on large branchiopods, although these factors

88 are recognized as some of the main threats to global

89 biodiversity. In the case of the Mediterranean region,

90 larger biodiversity losses are expected in future

A28 M. Florencio

A29 Estacio´n Biolo´gica de Don˜ana, CSIC, Seville, Spain

A30 M. Florencio

A31 Departamento de Ecologia, Instituto de Cieˆncias A32 Biolo´gicas, Universidade Federal de Goia´s, Goiaˆnia, A33 Goia´s, Brazil

A34 J. Garcı´a-de-Lomas

A35 Research Group on Ecology and Dynamics of Aquatic A36 Ecosystems, University of Ca´diz, Ca´diz, Spain

A37 M. R. Miracle J. Rueda M. Sahuquillo A38 Instituto Cavanilles de Biodiversidad y Biologı´a A39 Evolutiva, University of Valencia, Burjassot, Valencia,

Spain

A40 A. Miro´ M. Ventura

A41 Integrative Freshwater Ecology Group, Center for A42 Advanced Studies of Blanes, Spanish Research Council A43 (CEAB-CSIC), Blanes, Girona, Catalonia, Spain

A44 J. L. Pe´rez-Bote

A45 Zoology Unit, University of Extremadura, Badajoz, Spain

A46 F. Prunier J. Ripoll

A47 Asociacio´n de Educacio´n Ambiental El Bosque Animado, A48 Co´rdoba, Spain

A49 J. Rueda

A50 Department of Microbiology and Ecology, University of A51 Valencia, Burjassot, Valencia, Spain

A52 M. Sahuquillo

A53 Direccio´n General de Medio Natural, Generalitat A54 Valenciana, Valencia, Spain

A55 L. Serrano

A56 Department of Plant Biology and Ecology, University of A57 Sevilla, Seville, Spain

A58 D. Verdiell-Cubedo

A59 Asociacio´n Columbares, Murcia, Spain AQ2

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91 scenarios, due to the sensitivity of its ecosystems to 92 drivers of biodiversity change, especially those related 93 to land-use change and introduction of exotic species 94 (Sala et al.,2000; Underwood et al.,2009). Although 95 temporary ponds were so far only minimally impacted 96 by traditional agricultural uses, their disappearance 97 and degradation have been highly intensified during 98 the last 50 years, due to infrastructure and urban 99 development, and intensification of agricultural activ-100 ity (Gallego-Fernańdez et al., 1999; Rhazi et al., 101 2012). This increasing degradation and loss of habitats 102 (Belk, 1998; Zacharias & Zamparas, 2010) strongly 103 impact large branchiopod populations, leading to 104 greater distances between remaining populations, 105 eventually leading to the loss of local populations 106 (Eder & Ho¨dl, 2002) and even some species on the 107 regional scale (Martens & De Moor, 1995; Mura, 108 1999; De Roeck et al.,2007). Therefore, the landscape 109 structure surrounding the wetlands should be taken 110 into account when evaluating the factors affecting 111 large branchiopods assemblages, since some land-112 scape characteristics are known to have great impor-113 tance for biotic communities, such as landscape 114 heterogeneity or land-use types, acting at several 115 spatial scales (Weibull et al.,2000; Hall et al.,2004; 116 Hartel & von Wehrden,2013). The evaluation of these 117 landscape characteristics for the conservation of the 118 large branchiopod assemblages has been seldomly 119 carried out, but the type of land use is known to affect 120 assemblage structure of passive dispersers (Hall et al., 121 2004), as well as some species at different spatial 122 scales (Angeler et al., 2008), whereas for other 123 species, the land use surrounding the wetland was 124 shown to be irrelevant (Angeler et al.,2008; Horva´th 125 et al.,2013). To this end, the integration of landscape 126 characteristics will improve large branchiopod con-127 servation programs at regional and national level, and 128 they will help to better understand the drivers of 129 biodiversity change linked to future scenarios of 130 global change.

131 The main goal of this article is to describe the 132 overall biodiversity patterns of the large branchiopods 133 present in the Iberian Peninsula and Balearic Islands, 134 establishing a general overview for the conservation of 135 this faunal group in this area. Additionally, we aim to 136 determine if the biodiversity patterns detected are 137 similar across the entire study area, and to investigate 138 the role of land use, landscape structure, population 139 density and protected area networks on the large

140 branchiopod species distribution. These will set a

141 basic framework to understand their distribution and

142 will allow us to assess whether there are particular

143 factors affecting this faunal group that should be taken

144 into consideration in the evaluation of their

conserva-145 tion status.

146 Materials and methods

147 Study area

148 The Iberian Peninsula and the Balearic Islands are

149 situated in the western Mediterranean, and cover an

150 area of about 587,000 km2. The area is shared by

151 several countries (Spain, Portugal, Andorra, France

152 and Gibraltar), although the scope of this study

153 focusses only on Spain and Portugal. The climate

154 types present in the study area are mainly arid and

155 temperate climates, with cold climates circumscribed

156 to the higher peaks in the mountain ranges (Peel et al.,

157

2007; AEMET & IM,2011). Arid climate is restricted 158 mostly to southeastern Spain, although there are some

159 areas in northeastern (Ebro valley), central (southern

160 Meseta and Extremadura) and southwestern

(Alen-161 tejo) Iberian Peninsula, and Balearic Islands (southern

162 Majorca, and the islands of Ibiza and Formentera) with

163 this type of climate. Temperate climates are divided

164 into those with dry summer (which comprises the

165 majority of the area of the Iberian Peninsula, from the

166 western Atlantic coast to the Mediterranean sea,

167 excluding the arid southeastern Spain) or without dry

168 season (restricted to the northern Iberian Peninsula–

169 Cantabrian coast, northern Meseta and the Iberian and

170 Pyrenees mountain ranges).

171 Species distribution

172 All known bibliographical and unpublished large

173 branchiopod records from the Iberian Peninsula and

174 Balearic Islands were compiled (dating back to 1916),

175 and geographically referenced to the maximum

pos-176 sible resolution whenever possible (see Online

177 Resource 1 for bibliographical references). This

178 allowed to create the checklist of the large

bran-179 chiopod fauna, and the global distribution in the

180 Iberian Peninsula and Balearic Islands (see Online

181 Resource 2). However, as it is unreliable to relate old

182 records to present-day landscape metrics, all analyses

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183 were limited to records from 1995 onwards. Moreover, 184 some records were not considered for the study of the 185 biodiversity patterns due to particularities in the 186 biology or in the taxonomic resolution of different 187 taxa. Thus, the exotic invasive Artemia franciscana 188 Kellogg, 1906 was not considered as this species 189 competitively displaces the autochthonous species of 190 Artemia. Records of parthenogenetic strains of 191 Artemiawith undefined ploidy were also not consid-192 ered, because parthenogenetic strains with different 193 ploidies (i.e. diploid and tetraploid) were considered 194 as two different taxa, as recent studies suggest that 195 they could be related to different bisexual Artemia 196 species (Munõz et al.,2010; Asem et al.,2016). In the 197 case of genus Triops, we considered all species of the 198 genus as one taxon, due to the difficulties to allocate 199 the bibliographical records of this genus to the 6 200 existing species present in the Iberian Peninsula (Korn 201 et al., 2006,2010); at this moment, syntopic occur-202 rences of different species of Triops have not been 203 recorded in the Iberian Peninsula or the Balearic 204 Islands.

205 For each species, the number of occurrences in the 206 study area allowed to determine their rarity with rank– 207 frequency curves following Siqueira et al. (2012). The 208 inﬂection point of the curve classiﬁed the species as 209 common (those at the left side of the curve) or rare 210 (those at the right side of the curve; in this case those 211 that were present in less than 50 sites; see Online 212 Resource 3). Moreover, those species that contributed 213 with less than 1% to the total occurrences were 214 considered very rare (in this case, those that were 215 present in less than 15 sites).

216 Biodiversity metrics were calculated using two 217 different approaches. In one hand, for each site species 218 richness and composition was recorded in order to 219 describe biodiversity patterns across the whole study 220 area. We considered co-occurring species as those 221 species that were recorded in the same site, but not 222 necessarily at the same time (i.e. syntopic species). 223 However, data on synchronic species (i.e. those 224 species that were recorded at the same time in the 225 same site) appear in Online Resource 4. On the other 226 hand, for each UTM 100 km grid square we calculated 227 the number of sites with presence of large bran-228 chiopods, the mean species richness per site, the total 229 species richness in each grid square and the percentage

230 of sites that showed co-occurring species.

Seventy-231 seven UTM 100 km grid squares had presence of large

232 branchiopods in the Iberian Peninsula and Balearic

233 Islands, but only those with more than 5 sites were

234 included in the analyses (39 out of 77).

235 Landscape metrics

236 Landscape metrics were calculated considering

237 human population density (DP, based on local

admin-238 istrative units), protection status (N2000, Natura 2000

239 network areas), land cover (CORINE land cover) and

240 landscape structure. We assigned to each site the

241 corresponding population density of the local

admin-242 istrative units (LAUs) where it was located. LAUs, as

243 well as their corresponding population, were obtained

244 from 2011 population census (European Statistical

245 System, 2011). Natura 2000 network areas (EEA,

246

2015) were used as the protection category for the 247 studied region instead of other national protected areas

248 due to its high representativeness of biodiversity

249 (Rosati et al., 2008; Abellań & Sańchez-Fernańdez,

250

2015). Sites that were in a Natura 2000 network area 251 were classiﬁed as Protected. Land covers were

clas-252 siﬁed in 6 categories based on CORINE Land Cover

253 inventories (EEA, 2006): artiﬁcial surfaces (AS),

254 forests and semi-natural areas (FS), irrigated

agricul-255 tural areas (IA), non-irrigated agricultural areas (nIA),

256 wetland areas (W) and water bodies, although this last

257 category was not used to test its effects on the biotic

258 assemblages. Then, for each site, we calculated the

259 relative percentage of surface occupied by each

260 category using 3 different spatial scales (circular areas

261 were constructed using 100 m, 1 km and 10 km radius

262 distances to the central point of each site as centroid).

263 We used ArcMap GIS 10.0 to process all datasets and

264 calculate landscape metrics (ESRI, 1999). Finally,

265 following Weibull et al. (2000), landscape diversity

266 (Ldiv) was calculated as a measure of landscape

267 structure using the Shannon diversity index,

268 Ldiv = -pi ln(pi), where pi is the proportion of

269 habitat i in the circular areas used for calculating the

270 land covers. In the case of the UTM grid square

271 approach, we calculated the mean values of the

272 relative percentage of surface occupied by each

273 category of land covers and landscape diversity for

274 all the sites present at each grid square.

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275 Data analysis 276 Species associations

277 Species associations were explored using two different 278 approaches: (1) co-occurrence analysis and (2) clas-279 sification analysis. The co-occurrence analysis 280 allowed us to identify significant co-occurring species, 281 either with positive or negative co-occurrences. 282 Moreover, the effect size (i.e. the difference between 283 expected and observed frequency of co-occurrence) 284 was also obtained in order to quantify the strength of 285 the pattern. In the second approach, a non-hierarchical 286 cluster approach was used to identify species assem-287 blages. Partitioning around medoids (PAM) was the 288 classification technique chosen to cluster species into 289 groups, since it has been pointed out as more robust 290 than more classical approaches like k-means cluster-291 ing (Borcard et al., 2011). Sørensen similarity was 292 used as the similarity measure. The number of groups 293 tested representing existing species assemblages was 294 from 2 to 16 (number of large branchiopod species 295 minus 1, only considering the species with more than 5 296 occurrences). Silhouette widths of the resulting groups 297 were obtained to examine group membership’s appro-298 priateness, as well as the overall classification result 299 using the Rousseeuw quality index. The silhouette 300 width ranges between -1 and 1, and it is a measure of 301 the degree of membership of an object to its cluster, 302 negative values indicating misclassified objects. Co-303 occurrence analysis was performed using package 304 ‘‘cooccur’’ (Griffith et al., 2016), and PAM analysis 305 was performed using package ‘‘cluster’’ (Maechler 306 et al.,2016).

307 Species and landscape metrics

308 Hierarchical partitioning was used to identify the 309 relationship’s sign (positive or negative) and the 310 relative magnitude of the effects of the landscape 311 metrics tested at different scales (areas of 100 m, 1 km 312 and 10 km radius). This method assesses the indepen-313 dent, joint and total contribution (relative inﬂuence) of 314 each predictor variable by averaging a measure of 315 goodness-of-ﬁt over all possible models that include 316 that predictor variable. Therefore, it is less susceptible 317 to multicollinearity problems than are the single-318 model approaches when looking for the ‘‘best’’ model

319 (Logan, 2010). In order to evaluate whether the

320 magnitude of the contribution of a variable is

signif-321 icant (Z C 1.65 at the 95% level), a randomization

322 procedure was used in which the independent

contri-323 butions of each predictor variable were compared to

324 distributions of such contributions generated by

325 repeated randomizations of the data matrix (number

326 of randomizations = 100). While a binomial family

327 error was speciﬁed for the species hierarchical

parti-328 tioning and randomization procedures, a Poisson

329 family error was used for species richness analyses.

330 When over- or under-dispersion was detected, P values

331 were corrected using quasi-likelihood model (Logan,

332

2010). The sign of the relationship between species 333 presence–absence or richness data and landscape

334 metrics was assessed with generalized linear models

335 (GLM) using all environmental variables as

predic-336 tors. To assess the model goodness-of-ﬁt, we

337 employed the squared Pearson correlation coefﬁcient

338 between observed and predicted values. Hierarchical

339 partitioning and randomizations were carried out

340 using package ‘‘hier.part’’ (Walsh & Mac Nally,

341

2013).

342 Biodiversity and landscape metrics

343 Conditional inference tree (CIT) models were used to

344 assess the relationship between biodiversity (response

345 variables: mean species richness per site, the total

346 species richness in each UTM 100 km grid square and

347 the percentage of sites with co-occurrences) and

348 landscape metrics (explanatory variables: DP,

349 N2000, AS, FS, IA, nIA, W, Ldiv) in the 3 tested

350 spatial scales (100 m, 1 km and 10 km radius). This

351 type of regression displays a binary tree, built by a

352 process known as binary recursive partitioning, which

353 gives a very clear picture of the structure of the data,

354 and provides a highly intuitive insight into the kinds of

355 interactions between variables (Crawley,2002). CIT

356 are not affected by over-ﬁtting and are unbiased with

357 regard to the types of explanatory variables used

358 (Hothorn et al.,2006; Strobl et al.,2007). CIT models

359 were developed using the ‘‘party’’ package for R

360 (Hothorn et al., 2006). Three models, one for each

361 biodiversity metric, were run with the different spatial

362 scales.

363 All statistical analyses were run using R 3.0.1 (R

364 Core Team,2013).

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365 Results

366 In total, 1808 bibliographical and unpublished records 367 of large branchiopods in the Iberian Peninsula and the 368 Balearic Islands were obtained (see Online Resource

369 1), corresponding to 1167 different sites (i.e. water

370 bodies). One hundred seventy sites had only records

371 before 1995 (Fig.1), and were used only for the

372 overall distribution of species (see Online Resource 2

373 for distribution maps with all records), leaving 997

Records before 1995 Records from 1995 onwards Artemia salina

Branchinectella media

Tanymastix stagnalis part. Artemia (tetraploid)

Linderiella sp.

Artemia franciscana Branchinecta ferox Branchinecta orientalis

Branchipus cortesi Branchipus schaefferi Chirocephalus diaphanus

Lepidurus apus Leptestheria mayeti Linderiella baetica

Maghrebestheria maroccana Phallocryptus spinosus Streptocephalus torvicornis

Tanymastix sp. Tanymastigites lusitanica Triops spp. part. Artemia (diploid)

Cyzicus grubei

Fig. 1 Distribution maps of all records of large branchiopods before 1995, of all records from 1995 onwards, and of the different large branchiopod taxa present in Iberian Peninsula and Balearic Islands from 1995 onwards

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374 sites to use for analyses. The records were scattered all 375 across the Iberian Peninsula and the Balearic Islands, 376 but they were more frequent in the southern regions 377 (Andalusia, Alentejo and Algarve) than in the central 378 and northern ones, with the exception of Catalonia 379 (Fig.2A). There are still some regions (Navarra, 380 Cantabria and several northern Portuguese districts) 381 without records of large branchiopods.

382 Twenty-eight taxa have been recorded to date in the 383 Iberian Peninsula and Balearic Islands: 17 anostracans 384 (one of them the invasive exotic Artemia franciscana), 385 7 notostracans and 4 spinicaudatans. Seven taxa can be 386 considered common ([50 sites) (Table1), although 387 we considered all Triops spp. together, and within this 388 group there are some species with restricted distribu-389 tions (e.g. T. emeritensis Korn & Pe´rez-Bote, 2010,

390 with two known sites; Korn et al.,2010). Fifteen taxa

391 can be considered rare (\50 sites); within this group,

392 11 taxa are extremely rare, being in less than 15 sites

393 (Table 1). To our knowledge, Cyzicus tetracerus

394 (Krynicki, 1830) is the only taxon that has not been

395 captured again since 1983 (Alonso, 1996), so it was

396 not present in further analyses. The majority of the

397 taxa are considered as Trans-Iberian species with wide

398 distributions across the western Palaearctic, although

399 there are also a large number of Iberian endemic

400 species (10 species, of which 4 can be considered as

401 extremely rare). Spinicaudatans, notostracans and

402 extremely rare anostracans tended to co-occur

fre-403 quently with other species, with the exception of

404 Tanymastigites lusitanica Machado & Sala, 2013,

405 usually found alone (Table1). Approximately 30% of no. sites < 11 31 mean S < 1.15 total S < 3 % sites < 15 A B C D

Fig. 2 Geographical patterns of large branchiopod assem-blages. A Number of sites within each UTM 100 km grid square. B Mean species richness (S) per site recorded in each UTM 100 km grid square. C Total species richness (S) recorded

in each UTM 100 km grid square. D Percentage of sites with more than 1 species in each UTM 100 km grid square. In all panels, only UTM grid squares with more than ﬁve sites are shown

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406 sites presented co-occurrence of large branchiopod 407 species, with decreasing site frequencies when number 408 of co-occurring species increased (see Online 409 Resource 4). A maximum of 6 species were found 410 co-occurring together in 2 different sites in SW Iberian 411 Peninsula (in Andalusia and Algarve), followed by 5 412 species found in 7 sites (Andalusia, Extremadura and 413 Alentejo) and 4 species found in 34 sites (Andalusia, 414 Extremadura, Algarve, Alentejo and Valencia). 415 The UTM 100 km grid square approach showed 416 that the general biodiversity patterns were geograph-417 ically heterogeneous in the study area (Fig.2).

418 Number of sites with large branchiopods

419 (mean = 23.3; range 6–125; Fig. 2A) had high values

420 in SW and NE Iberian Peninsula, similarly to the

421 pattern found for the total species richness per UTM

422 grid square (mean = 4.6; range 1–11; Fig.2C). In the

423 case of the mean species richness per site

424 (mean = 1.4; range 1.0–2.2; Fig. 2B), high values

425 were also more common in SW Iberian Peninsula, but

426 there were also some UTM grid squares with high

427 values in the eastern part of the Peninsula and in the

428 Balearic Islands. The percentage of sites with

co-429 occurrences within a UTM grid square (mean = 26.8;

Table 1 Taxa of large branchiopods found in the Iberian Peninsula and Balearic Islands from 1995 onwards in decreasing order of occurrence

Taxon Abbreviation No. sites Rarity General

distribution

Co-occurrences with other spp. (%)

Chirocephalus diaphanusPre´vost, 1803 CHR_DIA 377 C T 38.2

Branchipus schaefferiFischer, 1834 BCH_SCH 293 C T 22.9

Triopsspp. TRP_SPP 241 C – 79.7

Tanymastix stagnalis(L., 1758) TAN_STA 169 C N 64.5

Branchipus cortesiAlonso & Jaume, 1991 BCH_COR 111 C EN 77.5

Streptocephalus torvicornis(Waga, 1842) STR_TOR 62 C T 71.0

Cyzicus grubei(Simon, 1886) CYZ_GRU 60 C EN 95.0

Maghrebestheria maroccanaThie´ry, 1988 MAG_MAR 23 R S 100.0

Artemia salina(L., 1758) ART_SAL 20 R T 25.0

Branchinectella media(Schmankewitsch, 1873) BRT_MED 18 R T 22.2

Artemia franciscanaKellogg, 1906 ART_FRA 16 – EX –

Tanymastixsp. TAN_SP 15 R EN 46.7

Phallocryptus spinosus(Milne-Edwards, 1840) PHC_SPI 9 RR T 44.4

Tanymastigites lusitanicaMachado & Sala,2013 TAG_LUS 9 RR EN 11.1

parthenogenetic Artemia (tetraploid) ART_PAT 8 RR T 12.5

Branchinecta orientalisSars, 1901 BRN_ORI 8 RR T 50.0

parthenogenetic Artemia (diploid) ART_PAD 7 RR T 57.1

Lepidurus apus(L., 1758) LEP_APU 7 RR T 14.3

Leptestheria mayeti(Simon, 1885) LPT_MAY 4 RR M 100.0

Branchinecta ferox(Milne-Edwards, 1840) BRN_FER 3 RR T 66.7

Linderiellasp. LIN_SP 3 RR EN 100.0

Linderiella baeticaAlonso & Garcı´a-de-Lomas,2009 LIN_BAE 1 RR EN 100.0

Cyzicus tetracerus(Krynicki, 1830) CYZ_TET 0 RR T –

For each taxon, number of sites, rarity class, general distribution in the study area (adapted from Abella´n et al.,2005) and percentage

of sites where each taxon co-occurred with any other taxa. Note that Triops spp. is a heterogeneous group that includes 6 species, 4 of them endemic from the Iberian Peninsula (1 of them extremely rare)

Ccommon, EN endemic species, EX exotic species, M Mediterranean species, N northern species (present in Europe and the Iberian

Peninsula, but not in north Africa), R rare, RR extremely rare, S southern species (present in north Africa and the Iberian Peninsula, but not in Europe north of the Pyrenees), T Trans-Iberian species (present in Europe, the Iberian Peninsula and north Africa)

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430 range 0.0–67.4; Fig.2D) was especially high in SW, 431 whereas lower values were observed in the NE and 432 some areas in the SE Iberian Peninsula.

433 The probabilistic co-occurrences analysis showed 434 some species pairs with significant positive associa-435 tions (e.g. Branchipus cortesi Alonso & Jaume, 1991 436 and Tanymastix stagnalis (L., 1758); Cyzicus grubei 437 (Simon, 1886) and Triops spp.; Fig. 3), whereas other 438 pairs had significant negative co-occurrences (e.g. 439 Branchipus schaefferi Fischer, 1834 and Chiro-440 cephalus diaphanus Pre´vost, 1803; T. stagnalis and 441 B. schaefferi; C. diaphanus and T. stagnalis; Fig.3). 442 The partitioning around medoids (PAM) analysis 443 obtained similar results, clustering together the species 444 that showed positive co-occurrences (Fig. 4). How-445 ever, the global average silhouette width (ASW; a 446 measure of how well the species are clustered) was 447 quite low, indicating that in general the affinity among 448 the species in each cluster was not very strong. PAM 449 analysis classified the species in four significant 450 groups: group 1 (including Artemia salina (L., 1758)

451 and the diploid parthenogenetic Artemia), group 3

452 (including B. cortesi, T. stagnalis and

Maghrebesthe-453 ria maroccana Thie´ry, 1988), group 4 (including

454 Streptocephalus torvicornis (Waga, 1842), Triops

455 spp., C. grubei, C. diaphanus and B. schaefferi) and

456 group 6 [including the halophilous Branchinectella

457 media (Schmankewitsch, 1873) and Phallocryptus

458 spinosus (Milne-Edwards, 1840)]. Group 1 had the

459 highest ASW, whereas group 4 had the lowest ASW,

460 pointing that the species in this cluster were not tightly

461 grouped.

462 Overall, hierarchical variation partitioning showed

463 signiﬁcant effects of landscape metrics on large

464 branchiopods at several spatial scales. In general, the

465 best ﬁt was observed at the largest spatial scale

466 (10 km). In the case of species richness, although the

467 proportion of the variation explained was low, the

468 presence of non-irrigated agriculture (nIA) revealed

469 positive relationships at lower spatial scales (100 m

470 and 1 km), whereas forests and semi-natural

vegeta-471 tion (FS) showed signiﬁcant positive relationship at

Fig. 3 Pairwise combinations of large branchiopod species in the Iberian Peninsula and Balearic Islands determined by probabilistic co-occurrence analysis. Circles indicate signiﬁcant co-occurrences, and the size of

the circlesrepresents the

effect sizes of the

association. Only signiﬁcant co-occurrences are shown. White circles in white

backgroundpositive

co-occurrences; black circles in

grey backgroundnegative

co-occurrences.

Abbreviations of species are

the same as in Table1

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472 the lowest spatial scale (100 m) but negative relation-473 ships at larger scales (Fig.5). At the largest spatial 474 scale, presence of wetlands and landscape diversity 475 (Ldiv) showed a positive relationship, and population 476 density showed a negative relationship.

477 In the case of group 1 of PAM analysis, the 478 proportion of the variation explained was relatively 479 high, especially for the diploid parthenogenetic 480 Artemia. Wetlands (W) and population density (DP) 481 had significant positive relationships on the distribu-482 tion of both taxa at different scales, whereas the rest of 483 metrics had low relation (Fig.5). For group 3 of PAM 484 analysis, composed by an assemblage characteristic of 485 the SW Iberian Peninsula, protected areas (N2000) 486 and Ldiv (especially at large spatial scales) showed 487 significant positive relationships on the distribution of 488 B. cortesi and T. stagnalis. FS and nIA showed 489 different effects depending of the spatial scale anal-490 ysed, being negative at larger scales and positive at 491 smaller ones (Fig.5). In contrast, the group 4 of PAM 492 analysis (Fig.5) was characterized by significant 493 positive relationships of nIA, especially at small 494 spatial scales, although the proportion of the variation 495 explained was relatively low. Also, the distribution of

496 some species was deﬁned by being outside of

497 protected areas (C. diaphanus, S. torvicornis and

498 Triopsspp.). Interestingly, B. schaefferi was positively

499 related to population density (DP), artiﬁcial surfaces

500 (AS), irrigated agriculture (IA), FS and nIA, whereas

501 Chirocephalus diaphanus was negatively related to

502 DP, IA and Ldiv. The group 6 of PAM analysis was

503 composed of Branchinectella media and

Phallocryp-504 tus spinosus, two characteristic species of saline

505 endorrheic wetlands, and their distribution were

506 explained by being positively related to N2000, Ldiv

Fig. 4 Silhouette plots showing the partition around medoids (PAM) analysis results. Different colours indicate different groups. Average silhouette width of the overall analysis is indicated at the bottom of the plot. j stands for the

number of the cluster; nj

indicates the number of species within each cluster j;

aveieCjsicorresponds to the

average silhouette width for each cluster. Abbreviations of species are the same as in

Table1

c

Fig. 5 Plots showing species richness (S) and species groups of PAM analysis (groups 1, 3, 4, 6 and the rest of species not clustered in any group of PAM analysis) in the three spatial scales (100 m, 1 km and 10 km). The first column shows the ﬁt of the binomial models calculated as the Pearson’s correlation between observed and expected values (white bars), whereas the rest of columns show the independent contribution of the landscape metrics obtained from the hierarchical partitioning (grey bars indicate positive effects while black bars indicate negative effects). Only signiﬁcant relationships detected after

the randomization process are shown (see ‘‘Materials and

methods’’ section for more details). Abbreviations of species are

the same as in Table1, and those of landscape metrics appear in

Materials and methods

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GR

OUP 1

GR

OUP 3

GR

OUP 4

GR

OUP 6

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507 (mainly at small spatial scales), nIA and W (both at 508 large spatial scales), while FS had negative significant 509 relationship on them (Fig.5). The rest of the species 510 formed a heterogeneous group of extremely rare 511 species that did not cluster significantly in PAM 512 analysis. Therefore, there was not a common pattern in 513 the landscape metrics affecting the species distribu-514 tions, although DP had negative significant relation-515 ships on the distribution of all species except 516 Lepidurus apus(L., 1758), whereas nIA had positive 517 significant relationships at larger scales with the

518 exception of the tetraploid parthenogenetic Artemia

519 (Fig.5).

520 Wetland and non-irrigated agriculture land covers

521 were the only factors that were related to the

522 biodiversity metrics at the UTM 100 km grid square

523 approach. Signiﬁcantly higher values of mean species

524 richness per site at a spatial scale of 1 km radius

525 (Fig.6A) were found in UTM grid squares with high

526 values of wetland land cover (more than 6.9 ha), and

527 also in non-irrigated agriculture land cover (more than

528 177.4 ha). Similar results were obtained for total

Fig. 6 Signiﬁcant results of the conditional inference trees between biodiversity and landscape metrics for each UTM 100 km grid square at each spatial scale. A Mean species richness per site at a spatial scale of 1 km radius. B Total species richness per UTM grid square at a spatial scale of 1 km radius.

C Total species richness per UTM grid square at a spatial scale of 10 km radius. D Percentage of sites with co-occurrences at a spatial scale of 1 km radius. Abbreviations of landscape metrics

appear in ‘‘Materials and methods’’ section

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529 species richness per UTM grid square at a spatial scale 530 of 10 km radius (Fig.6C), and for the percentage of 531 sites with co-occurrences at a spatial scale of 1 km 532 radius (Fig.6D). In the case of total species richness 533 per UTM grid square at a spatial scale of 1 km radius 534 (Fig.6B), signiﬁcantly higher values were found only 535 in UTM grid squares with high values of wetland land 536 cover (more than 2.4 ha).

537 Discussion

538 This work represents an exhaustive update of the 539 distribution and the biodiversity patterns of the large 540 branchiopod fauna of the Iberian Peninsula and 541 Balearic Islands, similarly to other studies in neigh-542 bouring countries (e.g. Defaye et al., 1998; Mura, 543 1999; Van den Broeck et al., 2015a; Marrone et al., 544 2016). Since the major works by Alonso 545 (1985, 1996, 1998) on Iberian and Balearic large 546 branchiopods, six new species were described (L. 547 baetica, Tanymastigites lusitanica, Triops baeticus 548 Korn, 2010, T. gadensis Korn & Garcı´a-de-Lomas, 549 2010, T. vicentinus Korn, Machado, Cristo & Cancela 550 da Fonseca, 2010 and T. emeritensis; Alonso & 551 Garcı´a-de-Lomas,2009; Korn et al.,2010; Machado 552 & Sala,2013), 2 more are currently being described 553 (Linderiella sp. and Tanymastix sp.), 1 is new for the 554 Iberian Peninsula (Triops simplex Ghigi, 1921; Korn 555 et al., 2010) and an exotic species was recorded all 556 along the Peninsula (Artemia franciscana; Amat et al., 557 2005). To date, the number of species found in the 558 study area, 28 species, is similar to neighbouring 559 countries (e.g. 22 species in Morocco (Thie´ry,1986; 560 Amat et al., 2005; Boix et al., 2016; Korn & 561 Hundsdoerfer, 2016), and 25 in Italy (Cottarelli & 562 Mura, 1983; Mura, 1999; Marrone & Mura, 2006; 563 Mura et al., 2006; Scanabissi et al., 2006; Alfonso, 564 2017)) and slightly higher than others [e.g. 19 species 565 both in Tunisia (Ben Naceur et al., 2013; Marrone 566 et al.,2016) and Algeria (Samraoui & Dumont,2002; 567 Samraoui et al.,2006; Ghomari et al.,2011), and 18 568 species in France (Nourisson & Thie´ry,1988; Defaye 569 et al.,1998; Amat et al.,2005; Rabet et al.,2005)]. The 570 taxa with high occurrences were species common in 571 the western Palaearctic (C. diaphanus, B. schaefferi, T, 572 stagnalis, S. torvicornis), together with two Iberian 573 endemics (B. cortesi, C. grubei) widely distributed 574 mainly in the western Peninsula. Also, the genus

575 Triops had high occurrences, but paradoxically it is

576 one of the taxa that gathers more uncertainties about

577 its distribution due to recent taxonomical

modiﬁca-578 tions (until 2006 it was considered as only one species,

579 T. cancriformis(Bosc, 1801); Korn et al.,2006,2010),

580 that difﬁcult the allocation of all previous

biblio-581 graphical records to the 6 species present in the Iberian

582 Peninsula. A detailed study of the identities,

distribu-583 tions and conservation status of the genus Triops in the

584 Iberian Peninsula (especially in the northern and

585 eastern regions) and Balearic Islands is therefore

586 strongly recommended. For the extremely rare

587 species, monitoring and conservation programs should

588 be mandatory, due to their low occurrences, in some

589 cases with the major part of their localities outside

590 protected areas. A paradigmatic case is the anostracan

591 Linderiella baeticaAlonso & Garcı´a-de-Lomas,2009,

592 of which the only known remaining population is

593 critically endangered by urbanization (Garcı´a de

594 Lomas et al., 2016), and that urgent measures are

595 needed to avoid extinction. However, surveillance and

596 monitoring programs should be also regarded for not

597 so rare species, because their populations could be

598 declining rapidly, even at supranational scales. This is

599 the case of the autochthonous species of genus

600 Artemia, which are also of great concern. The

601 abandonment of the salterns, together with the

expan-602 sion of the invasive A. franciscana, are leading to the

603 decline and loss of populations of native species

604 through competition and displacement (Amat et al.,

605

2007; Redo´n et al.,2015), and there is an urgent need 606 to update the distributional data and to assess the

607 conservation status of the Mediterranean brine

608 shrimps at national level or higher in order to evaluate

609 the extent of damage to their populations (Mura et al.,

610

2006).

611 Four large branchiopod associations were detected

612 which corresponded in part to those already described

613 by Alonso (1998). Two associations were

character-614 istic of saline habitats: group 1 is a characteristic

615 association with Artemia present mainly in salterns,

616 whereas group 6 contained the halophile species

617 Phallocryptus spinosus and Branchinectella media,

618 which is also present in other areas with steppic

619 habitats (e.g. Samraoui et al., 2006; Marrone et al.,

620

2016). The other two associations were characteristic 621 of freshwater temporary waterbodies. Group 3 is a

622 characteristic association from the SW Iberian

Penin-623 sula with B. cortesi, T. stagnalis and sometimes M.

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624 maroccana, partly described in Cancela da Fonseca 625 et al. (2008). This association is partly similar to the 626 one observed in Morocco, where M. maroccana 627 usually also appears with Tanymastix affinis Daday, 628 1910 and sometimes with B. schaefferi (Thie´ry,1991; 629 Van den Broeck et al.,2015a). Group 4 corresponds to 630 an association that coincides partly with the one 631 described by Alonso (1998), but probably corresponds 632 to two different groups due to the fact that several 633 species of genus Triops are included in this group. In 634 this sense, an association with B. schaefferi, Triops 635 spp. and sometimes S. torvicornis, is present in the arid 636 climates of the north and the east of the Peninsula, and 637 in the Balearic Islands, whereas an association with C. 638 diaphanus, C. grubei and Triops spp. is characteristic 639 of the south of the Iberian Peninsula.

640 The necessity of increasing our knowledge on large 641 branchiopod ecology should not be restricted only to 642 species or population level, but they should also 643 encompass higher levels of organization. The func-644 tioning of biodiversity patterns at different spatial 645 scales must be taken into account for improving 646 conservation actions, because disturbances are scale 647 dependent (Caro,2010). In general, our study detected 648 that land use had an effect on the species richness and 649 distribution of large branchiopods. However, not all 650 the species were affected by the same landscape 651 metrics. These results are in concordance with those 652 observed by Angeler et al. (2008), with T. cancri-653 formisbeing affected by irrigated agriculture at large 654 spatial scale, whereas Branchinecta orientalis was not. 655 In contrast, other studies found no effects of land use 656 on large branchiopod communities (e.g. Horva´th et al., 657 2013; Mabidi et al., 2016). We found that species 658 clustered together were similarly affected by the same 659 landscape metrics, but that different clusters were 660 affected by different landscape metrics, which could 661 partially explain those contrasting results. Agricultural 662 (irrigated and non-irrigated) and wetland land covers 663 were the metrics that affected to more species (positive 664 or negative, and with different magnitudes). It is 665 known that agricultural land use around temporary 666 ponds can have important effects on their biota (Rhazi 667 et al.,2001; O’Neill et al.,2016), although traditional 668 agricultural practices are a key factor for temporary 669 pond conservation (Bagella et al., 2016). This is in 670 concordance with the positive relationships that 671 showed the non-irrigated agriculture on the majority 672 of large branchiopod species. Similarly, it is known

673 that the extent of wet areas or the pond density also

674 inﬂuences invertebrate and plant assemblages (e.g.

675 Boix et al.,2008; Bagella et al.,2010). It is interesting

676 to note that the majority of the relationships had a

677 better ﬁt at larger spatial scales, in accordance with the

678 results found by Angeler et al. (2008), suggesting that

679 management at larger scales have also to be taken into

680 account for the conservation of large branchiopods.

681 Moreover, biodiversity metrics were inﬂuenced by

682 the presence of wetlands and/or land use linked to

non-683 irrigated agricultural practices, especially at larger

684 scales. Our results showed that wetlands, ﬂoodplains

685 and surrounding areas in the Iberian Peninsula (e.g.

686 Guadiana, Don˜ana, Ca´diz and Emporda` wetlands)

687 presented high values of large branchiopod species

688 richness at different spatial scales, probably due to the

689 heterogeneity of the water body types that could host

690 different communities. Moreover, these areas were

691 also important for the presence of rare and/or Iberian

692 endemic species. The importance of this kind of

693 habitats for the biodiversity of large branchiopods has

694 also been observed in other regions (e.g. Eder et al.,

695

1997; Timms & Sanders, 2002; Waterkeyn et al., 696

2009; Nhiwatiwa et al., 2014; Stoch et al., 2016). 697 However, land-use analyses also revealed that

tempo-698 rary water bodies in non-irrigated agricultural

land-699 scapes not linked directly to large wetland areas also

700 hosted a large amount of biodiversity. Traditional,

701 non-intensive agricultural practices are compatible

702 with the existence of highly biodiverse temporary

703 ponds (e.g. Grillas et al.,2004; Robson & Clay,2005),

704 even in areas where temporary ponds are human-made

705 and the presence of natural temporary water bodies is

706 very rare (e.g. Verdiell-Cubedo & Boix, 2014). The

707 large branchiopod fauna associated to these habitats is

708 usually very rich, and they host multiple species (e.g.

709 Boven et al., 2008; Cancela da Fonseca et al.,2008;

710 Prunier & Saldan˜a, 2010; Marrone et al., 2016;

711 Alfonso, 2017). However, these habitats are rapidly

712 declining due to intensiﬁcation of agricultural

prac-713 tices, changes in land use and population growth (e.g.

714 Underwood et al.,2009; Rhazi et al.,2012), affecting

715 the biotic populations linked to these habitats (e.g.

716 Euliss Jr. & Mushet,1999; Beja & Alcazar,2003; Van

717 den Broeck et al.,2015a).

718 Since the extensive surveys performed by Alonso

719 (1985, 1996, 1998) in the Iberian Peninsula and

720 Balearic Islands during the last quarter of the twentieth

721 century, no more studies exist updating the

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722 information for the whole study area. In this sense, the 723 present study represents a new step on the knowledge 724 of large branchiopod distribution in this area, not only 725 because it gathers all available information on the 726 distribution of this taxonomic group (historical records 727 and new observations), but also because it analyses the 728 effect of several landscape characteristics on its 729 distribution, detailing the spatial scale at which its 730 inﬂuence is noticeable for large branchiopods pres-731 ence. All this information would be highly valuable 732 for land stakeholders under future conservation 733 scenarios.

734 Acknowledgements We dedicate this paper to the memory of

735 Prof. Graziella Mura that inspired many of us with her

736 passionate approach to these interesting organisms. We also

737 dedicate this study to the memory of our co-author Prof. Maria

738 Rosa Miracle, who was an admired and stimulating researcher in

739 the Iberian limnology. We want to sincerely thank all people that

740 selﬂessly supplied us with large branchiopod records. We also

741 thank two anonymous reviewers for providing valuable

742 comments to an earlier version of the manuscript. MF is

743 supported by a grant from the Brazilian Conselho Nacional de

744 Desenvolvimento Cientı´ﬁco e Tecnolo´gico—CNPq (401045/

745 2014-5), program Cieˆncia sem Fronteiras. DC-M held a grant

746 from the Spanish Ministry of Education, Culture and Sport

747 (FPU014/06783).

748 References

749 Abellań, P. & D. Sańchez-Fernańdez, 2015. A gap analysis

750 comparing the effectiveness of Natura 2000 and national

751 protected area networks in representing European

752 amphibians and reptiles. Biodiversity and Conservation 24:

753 1377–1390.

754 Abellań, P., D. Sańchez-Fernańdez, J. Velasco & A. Millań,

755 2005. Assessing conservation priorities for insects: status

756 of water beetles in southeast Spain. Biological

Conserva-757 tion 121: 79–90.

758 AEMET & IM, 2011. Iberian climate atlas. Air temperature and

759 precipitation (1971-2000). Agencia Estatal de

Meteo-760 rologı´a & Instituto de Meteorologia de Portugal, Madrid.

761 Alfonso, G., 2017. Diversity and distribution of large

bran-762 chiopods (Branchiopoda: Anostraca, Notostraca,

Spini-763 caudata) in Apulian ponds (SE Italy). The European

764 Zoological Journal 84: 172–185.

765 Alonso, M., 1985. A survey of the Spanish Euphyllopoda.

766 Miscel la`nia Zoolo`gica 9: 179–208.

767 Alonso, M., 1996. Crustacea. Branchiopoda. In Ramos, M. A.,

768 et al. (eds), Fauna Ibe´rica, Vol. 7. Museo Nacional de

769 Ciencias Naturales, CSIC, Madrid.

770 Alonso, M., 1998. Las lagunas de la Espan˜a peninsular.

Lim-771 netica 15: 1–176.

772 Alonso, M. & J. Garcı´a-de-Lomas, 2009. Systematics and

773 ecology of Linderiella baetica n. sp. (Crustacea,

774

Branchiopoda, Anostraca, Chirocephalidae), a new species

775

from southern Spain. Zoosystema 31: 807–827.

776

Amat, F., F. Hontoria, O. Ruiz, A. J. Green, M. I. Sa´nchez, J.

777

Figuerola & F. Hortas, 2005. The American brine shrimp as

778

an exotic invasive species in the western Mediterranean.

779

Biological Invasions 7: 37–47.

780

Amat, F., F. Hontoria, J. C. Navarro, N. Vieira & G. Mura, 2007.

781

Biodiversity loss in the genus Artemia in the Western

782

Mediterranean Region. Limnetica 26: 387–404.

783

Angeler, D. G., O. Viedma, S. Sa´nchez-Carrillo & M. A´

lvarez-784

Cobelas, 2008. Conservation issues of temporary wetland

785

Branchiopoda (Anostraca, Notostraca: crustacea) in a

786

semiarid agricultural landscape: what spatial scales are

787

relevant? Biological Conservation 141: 1224–1234.

788

Asem, A., A. Eimanifar & S.-C. Sun, 2016. Genetic variation

789

and evolutionary origins of parthenogenetic Artemia

790

(Crustacea: Anostraca) with different ploidies. Zoologica

791

Scripta 45: 421–436.

792

Bagella, S., S. Gasco´n, M. C. Caria, J. Sala, M. A. Mariani & D.

793

Boix, 2010. Identifying key environmental factors related

794

to plant and crustacean assemblages in Mediterranean

795

temporary ponds. Biodiversity and Conservation 19:

796

1749–1768.

797

Bagella, S., S. Gasco´n, R. Filigheddu, A. Cogoni & D. Boix,

798

2016. Mediterranean temporary ponds: new challenges

799

from a neglected habitat. Hydrobiologia 782: 1–10.

800

Beja, P. & R. Alcazar, 2003. Conservation of Mediterranean

801

temporary ponds under agricultural intensiﬁcation: an

802

evaluation using amphibians. Biological Conservation

803

114: 317–326.

804

Belk, D., 1998. Global status and trends in ephemeral pool

805

invertebrate conservation: implications for Californian

806

fairy shrimp. In Witham, C. W., et al. (eds.), Ecology,

807

Conservation, and Management of Vernal Pool

Ecosys-808

tems – Proceedings from a 1996 Conference. California

809

Native Plant Society, Sacramento: 147–150.

810

Ben Naceur, H., A. Ben Rejeb Jenhani & M. S. Romdhane,

811

2013. Morphometric characterization of adult Artemia

812

(Crustacea: Branchiopoda) populations from costal and

813

inland Tunisian salt lakes. African Invertebrates 54:

814

543–555.

815

Boix, D., 2002. Aportacio´ al coneixement de la distribucio´

816

d’anostracis i notostracis (Crustacea: Branchiopoda) als

817

Paı¨sos Catalans. Butlletı´ de la Institucio´ Catalana

d’His-818

to`ria Natural 70: 55–71.

819

Boix, D., S. Gasco´n, J. Sala, A. Badosa, S. Brucet, R.

Lo´pez-820

Flores, M. Martinoy, J. Gifre & X. D. Quintana, 2008.

821

Patterns of composition and species richness of crustaceans

822

and aquatic insects along environmental gradients in

823

Mediterranean water bodies. Hydrobiologia 597: 53–69.

824

Boix, D., J. Sala, D. Escoriza & M. Alonso, 2016. Linderiella

825

jebalaesp. nov. (Crustacea: Branchiopoda: Anostraca), a

826

new species from the Rif mountains (northern Morocco).

827

Zootaxa 4138: 491–512.

828

Borcard, D., F. Gillet & P. Legendre, 2011. Numerical Ecology

829

with R. Springer, New York.

830

Boven, L., B. Vanschoenwinkel, E. R. De Roeck, A. Hulsmans

831

& L. Brendonck, 2008. Diversity and distribution of large

832

branchiopods in Kiskunsa´g (Hungary) in relation to local

833

habitat and spatial factors: implications for their

conser-834

vation. Marine and Freshwater Research 59: 940–950. AQ3

Hydrobiologia