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Pattern of Richness and Distribution of Groundwater Copepoda (Cyclopoida: Harpacticoida) and Ostracoda in Romania: an Evolutionary Perspective

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Pattern of Richness and Distribution of Groundwater Copepoda (Cyclopoida: Harpacticoida) and Ostracoda in Romania: an Evolutionary Perspective See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/282942622 Pattern of richness and distribution of groundwater Copepoda (Cyclopoida: Harpacticoida) and Ostracoda in Romania: an evolutionary perspective ARTICLE in BIOLOGICAL JOURNAL OF THE LINNEAN SOCIETY · OCTOBER 2015 Impact Factor: 2.26 · DOI: 10.1111/bij.12686 READS 70 5 AUTHORS, INCLUDING: Sanda Iepure Angelica Feurdean Madrid Institute for Advanced Studies "Emil Racovita" Institute of Speleology 27 PUBLICATIONS 59 CITATIONS 53 PUBLICATIONS 781 CITATIONS SEE PROFILE SEE PROFILE Available from: Aurel Persoiu Retrieved on: 21 October 2015 Biological Journal of the Linnean Society, 2015, , –. With 6 figures. Pattern of richness and distribution of groundwater Copepoda (Cyclopoida: Harpacticoida) and Ostracoda in Romania: an evolutionary perspective SANDA IEPURE1,2*, ANGELICA FEURDEAN2,3, CARMEN BAD ALUT ßA 4,5, VIORICA NAGAVCIUC4,6 and AUREL PERSßOIU4 1Madrid Institute for Advanced Studies, IMDEA Water Institute, Technological Scientific Park of the University of Alcala, C/Punto Com, n° 2, 28805, Alcala de Henares, Madrid, Spain 2Institute of Speleology ‘Emil Racovitßa’, Romanian Academy, Clinicilor 5, 400006, Cluj-Napoca, Romania 3Senckenberg Biodiversity and Climate Research Centre (BiK-F), Senckenberganlage 25, 60325, Frankfurt, Germany 4Stable Isotope Laboratory, Sßtefan cel Mare University, Universitatßii 13, Suceava, 720229, Romania 5Department of Geography, Sßtefan cel Mare University, Universitatßii 13, Suceava, 720229, Romania 6Faculty of Forestry, Sßtefan cel Mare University, Universitatßii 13, Suceava, 720229, Romania Received 24 October 2014; revised 21 July 2015; accepted for publication 8 August 2015 It is assumed that the south-eastern Europe and especially the Romanian Carpathians were important regions for surface and underground invertebrates survival during glacial periods and acted as a source of post-glacial colonization processes. We analyzed data from 233 georeferenced records for 164 species of groundwater copepods and ostracods from Romania and used a comparative approach to recognize the determinants of the regional-scale richness, endemism, and distribution patterns, with a primary focus on species from the Carpathian Mountains. In addition, we examined the driving forces for the observed pattern of distribution and richness linked to contemporary (groundwater habitat fragmentation and heterogeneity, climate, vegetation) and historical (past climate and vegetation) environmental conditions. Our analyses showed that: (1) species richness was high, irrespective of habitat heterogeneity, in karst and non-karst areas; (2) the main driver accounting for high species richness in the karst landscape was the rainfall regime (> 1350 mm per year), whereas, in non-karst areas, it was woodland vegetation; and (3) there was significant species richness and richness of phyletic lineages in hypothetical forest glacial refugia of the Carpathian arc. The combination of the distribution pattern, diversification, and evolution of stygobite lineages provides reliable evidence for species persistence in the Romanian groundwater during Pleistocene. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 00, 000–000. ADDITIONAL KEYWORDS: Carpathian Mountains – endemism – forest – glacial refugia – karst frag- mentation – palaeoclimate – Pleistocene – vegetation cover. INTRODUCTION 2012) that further recolonized the northern Europe after the Late Glacial Maximum (LGM) (Taberlet et al., The ‘southerly refugial model’ states that, during glacial 1998; Hewitt, 2000, 2001, 2004; Rundle et al., 2002). periods, many terrestrial and aquatic organisms sur- Romania, by its geographical position during the vived in peri-Mediterranean refuges (e.g. the Iberian, Pleistocene glaciations south and east of the Italian, and Balkan peninsulas) (Schmitt & Varga, Fennoscandian and Alpine ice-sheets, have had a less colder climate (Onac & Lauritzen, 1996; Urdea, *Corresponding author. E-mail: [email protected] 2011), resulting in high regional biodiversity and the © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, , – 1 2 S. IEPURE ET AL. setting up of a speciation centre for several inverte- and heterogeneity, represent the primary driving brates (Schmitt & Varga, 2012). Furthermore, as a force behind increases in the range size and distribu- result of its location at the crossing of five out of the tion of such species (Castellarini et al., 2007a, b; 10 biogeographical provinces (alpine, continental, Galassi, Huys & Reid, 2009a; Galassi et al., 2009b; pannonian, Black Sea, and steppe), Romania has Zagmajster et al., 2014; Eme et al., 2014). In the pre- been documented as key geographical region and sent study, we used copepods and ostracods as target home to important extra-Mediterranean glacial refu- groups to infer the potential mechanisms responsible gia for subterranean invertebrates (Decu & Iliffe, for the present-day patterns of richness and distribu- 1983; Decu & Racovita, 1994; Ribera et al., 2010). In tion in subterranean habitats from the Carpathian particular, the Carpathian Mountains represent an Mountains. We compiled and mapped the occurrence ecological bridge connecting the fauna of western, patterns of 164 species and subspecies, providing central, eastern, and south-eastern Europe (Negrea updated distribution maps of species currently pre- & Boitan, 2001; Ribera et al., 2010; Ronikier, 2011; sent in the groundwater habitats of Romania. Next, Schmitt & Varga, 2012). Comparative phylogeo- we linked the observed pattern with contemporary graphical analyses on cave beetles from the Car- (groundwater habitat fragmentation and heterogene- pathian Mountains in Romania have provided ity, climate, vegetation) and historical (past climate significant insights into the factors driving the regio- and vegetation) environmental conditions. We inves- nal spatial pattern (Decu & Racovita, 1994; Ribera tigated whether the richness and distribution of obli- et al., 2010). These studies indicate that a high rich- gate groundwater copepods and ostracods is linked ness and rate of endemism resulted from small-scale to: (1) local geology and karst fragmentation; (2) pre- diversification, speciation, and long-term in situ spe- sent vegetation composition; and (3) past climate and cies survival during the Pleistocene cold periods. In vegetation conditions. We also tested whether the groundwater, the latest reviews of the literature hypothesis that the Carpathian Mountains in Roma- indicate a high level of diversity for several obligate nia functioned as an extra-Mediterranean refugial is crustaceans (Botosaneanu, 1986; Decu & Racovita, supported by evidence from the structural richness 1994; Moldovan et al., 2007a) that display phyletic and distribution patterns of groundwater copepods lineages with striking regional diversity and distri- and ostracods, highlighting the diversification and butions at the country level (Plesßa, 1956; Danielopol, evolution of specific stygobitic (obligate groundwater 1982; Negrea & Boitan, 2001; Iepure, 2007a, b). dwellers) lineages. However, the aspects related to regional factors driv- ing species distribution ranges and diversity remain less explored (Negrea & Boitan, 2001; Negrea & MATERIAL AND METHODS Negrea, 2003). The highest diversity among crustaceans in Roma- STUDY AREA nian groundwater is found in the copepods (class: Our study area was Romania (centred on 45° N, Copepoda; order: Cyclopoida and Harpacticoida) and 25° E), covering 238 391 km2. The country is located ostracods (class: Ostracoda; order: Podocopida), repre- in the south-eastern part of central Europe and is sented by more than 160 species and subspecies bounded by the Carpathian Mountains, the lower (Iepure, 2007a). These subterranean groups are highly course of the Danube (for a distance of 1075 km), specious and commonly subjected to genetic differenti- and the Black Sea (Fig. 1). The country exhibits ation and isolation, with allopatric and discontinuous great diversity in topography (altitudinal range from distributions as a result of vicariance or following sub- sea level to 2544 m a.s.l.), geological substrates, and sequent ancient drainage patterns (Galassi, 2001). climate. Furthermore, they have restricted dispersal capabili- The Carpathian Mountains form an arc in Roma- ties and are limited by the availability of space and nia, stretching between the border with Ukraine (to the fragmentary nature of groundwater habitats the north) and the Iron Gates near the border with (Stoch, 1995; Galassi, 2001; Stoch et al., 2009; Stoch & Serbia (to the south) (Fig. 1). The Mesozoic lime- Galassi, 2010). These characteristics make them a use- stones were strongly influenced by the Tertiary uplift ful proxy to test fundamental hypotheses related to of the Romanian Carpathian arc, which broke their the drivers shaping current distribution and richness unity and created isolated massifs (Onac & Cocean, patterns in subterranean habitats. 1996; Onac, 2000; Orasßeanu & Iurkiewicz, 2010). On The current synthesis on subterranean copepods the north-western flank of the Romanian Carpathi- and ostracods from Romania was initiated following ans lies the most important karst area of the coun- recent findings related to groundwater crustaceans try: the Apuseni Mountains (10 750 km2) (Fig. 1). in western and central Europe, indicating that cli- Here, intense fracturing has resulted in
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