Pilularia Minuta Durieu (Marsileaceae) Discovered in South-Eastern-Sicily: New Insights on Its Ecology, Distribution and Conservation Status

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Pilularia minuta Durieu (Marsileaceae) discovered in south-eastern-Sicily: new insights on its ecology, distribution and conservation status

Pietro Minissale , José Antonio Molina & Saverio Sciandrello

To cite this article: Pietro Minissale , José Antonio Molina & Saverio Sciandrello (2017): Pilularia minuta Durieu (Marsileaceae) discovered in south-eastern-Sicily: new insights on its ecology, distribution and conservation status, Botany Letters To link to this article: http://dx.doi.org/10.1080/23818107.2017.1357051

Published online: 07 Aug 2017.

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Download by: [University of Catania] Date: 07 August 2017, At: 05:12 Botany Letters, 2017 https://doi.org/10.1080/23818107.2017.1357051

Pilularia minuta Durieu (Marsileaceae) discovered in south-eastern-Sicily: new insights on its ecology, distribution and conservation status

Pietro Minissalea , José Antonio Molinab and Saverio Sciandrelloc

aDepartment of Biological, Geological and Environmental Sciences, University of Catania, Catania, Italy; bDepartment of Plant Biology II, Complutense University of Madrid, Madrid, Spain; cCentre for the Conservation and Management of Nature and Agroecosystems (CUTGANA), University of Catania, Catania, Italy

ABSTRACT ARTICLE HISTORY Pilularia minuta Durieu (Marsileaceae) is a rare and endangered Mediterranean species of Received 11 March 2017 temporary ponds. It occurs in different countries all around the Mediterranean Basin with a Accepted 13 July 2017 scattered distribution. In Italy, this species is known for Sardinia, Apulia and recently for western KEYWORDS Sicily. During a field investigation, the species was found in the Hyblaean Plateau (south- Distribution; endangered eastern Sicily). The aim of this work is to analyze the ecological features and conservation status species; Isoeto-Nanojuncetea; of P. minuta populations occurring in Sicily. The floristic composition of Pilularia minuta plant Mediterranean temporary communities were determined using the standard relevé method. Three spatially differentiated ponds; wetlands; Pilularia belts with specific floristic compositions emerged from the numerical analysis (UPGMA method, minuta Euclidean distance coefficient) and from canonical correspondence analysis (CCA), mainly correlated to the water level. Our results showed that temporary ponds mainly host amphibian vegetation belonging to the phytosociological class Isoëto-Nanojuncetea, which includes pioneering annual plant communities growing on periodically flooded soils. Most species belong to the Mediterranean element, with therophytes as the dominant life form. The floristic richness and diversity index of these plant communities increased from the inner belt towards the upper belt. Finally, a synthesis of all known localities of Pilularia minuta from the Mediterranean area is given, together with a new assessment of the risk status for Sicily and Italy.

Introduction Calatafimi (Trapani). In the framework of researches on the plant communities of the temporary ponds, car- Pilularia minuta Durieu (Marsileaceae) is a steno-Medi- ried out in protected areas or SCIs (Sites of Community terranean endemic (Rhazi, Grillas, and Rhazi 2010) and Importance) of SE Sicily (Minissale and Sciandrello one of the most emblematic species of Mediterranean 2016; Sciandrello et al. 2016), two new populations temporary ponds. It is known from several countries of Pilularia minuta were discovered in April 2015 and around the Mediterranean Basin (Christenhusz and March 2016 in the Hyblaean Plateau (Figure 1), in some Raab-Straube 2013). Its range is quite discontinuous. Up ponds on regularly inundated volcanic soils. The first one to now, it is found in Portugal (Algarve), Spain (Huelva, is located at Cozzo Fico, south of Mount Pancali (near Zamora, La Mancha and Menorca provinces (ANTHOS

Downloaded by [University of Catania] at 05:12 07 August 2017 Carlentini) at 360 m above sea level (a.s.l.) (2 ponds); the 2012)), southern France, Corsica, Greece, western and second one was found at Cozzo Ogliastri (near Sortino), northern Aegean islands, Cyprus, Croatia (Dalmatian at 385 m a.s.l. (10 ponds). The population discovered by coast) and Turkey (Izmir). It also occurs in Maghreb, e.g. Troia and Lansdown (2016) is about 200 km from the Morocco, Algeria, and recently it was found in Tunisia Hyblaean populations at about 200 m a.s.l., on siliceous (Daoud-Bouattour et al. 2009). soils derived from sedimentary rocks. In Italy, Pilularia minuta presence has been con- Pilularia minuta is considered an endangered spe- firmed for Sardinia and Apulia (Beccarisi, Ernandes, cies of the Mediterranean Region (Rhazi, Grillas, and and Zuccarello 2009; Bagella and Caria 2012; Mascia Rhazi 2010). Moreover, it is reported by the European et al. 2013). Its presence in Sicily was reported the first Red List of Vascular Plants with the same conservation time by Nicotra (1893) from Trapani but it was based status (Bilz et al. 2011). It is also in Annex I of Berne on a misidentification of his specimens (Troia and Convention (Council of Europe 1979). However, there Lansdown 2016). is still poor information about the habitat of P. minuta Recently, a small population of Pilularia minuta (Desfayes 2008; Silva, Pinto-Cruz, and Espírito-Sant was found in Sicily (Troia and Lansdown 2016), near 2008; Garcia Cardo 2011; Ernandes and Marchiori 2013;

Figure 1. Current known distribution of Pilularia minuta in Sicily (little dots). In grey is highlighted Syracuse province. Source: Authors.

Daoud-Bouattour et al. 2014), and the synecology of wood, where cows sustain the grassland which is the the small pillwort communities (Braun-Blanquet 1935; main matrix vegetation. Furthermore, Pyrus spinosa Paradis and Finidori 2005; Daoud-Bouattour et al. 2009). Forssk. and Sarcopoterium spinosum (L.) Spach are the The main objectives of this research are to: (1) provide most frequent shrubs. data about the habitat where P. minuta occurs in Sicily; Regarding conservation measures Cozzo Ogliastri is (2) analyze the floristic composition and some ecological a Site of Community Importance (ITA0900023 Cozzo parameters of the amphibian plant communities related Ogliastri), according to the European directive 92/43 to P. minuta; (3) evaluate the species diversity and define EEC. This area is well known for the occurrence of spatial patterns; (4) update the small pillwort distribu- Zelkova sicula Di Pasquale, Garfì and Quézel, a critically

Downloaded by [University of Catania] at 05:12 07 August 2017 tion (5) re-evaluate its conservation status at regional endangered narrow endemic species involved in special (Sicily) and national (Italy) scales. conservation measures (Garfì et al. 2011).

Material and Methods Methods Study area Our study was based on field surveys, as well as on the The surveyed territory, the northern part of the Hyblaean review of literature and herbarium specimens (Appendix Plateau, is flat, with Tertiary volcanic substrates, span- 1). For the risk assessment at the regional scale, the ning in age between 3 and 1.5 million years BP (Carbone IUCN protocol (IUCN 2001) was followed according 2011; De Beni et al. 2011). According to the bioclimatic to the most recent guidelines for its application (IUCN classification proposed by Rivas-Martinez (1993) and 2014). In particular, the IUCN criterion (B) was applied Rivas-Martínez, Penas, and Diaz (2004), the study area by estimating trends in the Area of Occupancy (AOO) is characterized by the lower mesomediterranean ther- using a 2 × 2 km2 grid (IUCN 2014). motype and lower dry ombrotypes (Bazan et al. 2015). In order to analyze the structure and floristic com- The average annual rainfalls and temperatures from position of the P. minuta populations during the period the closest thermo-pluviometric stations are: Cozzo from 2015 to 2016, 12 temporary ponds were desig- Fico-M. Pancali (717 mm, 17.5 °C, Carlentini); and nated (with presence of P. minuta) and 23 plots were Cozzo Ogliastri (916 mm, 16.1 °C, Sortino). Overall, sampled (Appendix 2), using vegetation transect for the plant landscape is a cork oak (Quercus suber L.) open each pond. Transects were laid perpendicular to the BOTANY LETTERS 3

margin of each ponds. Each transect consists of contig- Giardina, Raimondo, and Spadaro (2007); the life form uous 40 × 40 cm2, in which the floristic data was noted. of each taxon is taken from Pignatti (1982), while the Transect length varied from 40 cm to 80 cm, depend- chorological types are adapted from Brullo, Grillo, ing on the spatial extension of the hydro-hygrophilous and Guglielmo (1998). The syntaxonomical scheme plant communities observed. The floristic composition of the vegetation units follows Biondi et al. (2014) and cover of species in each plot were determined by (Appendix 3). using a scale from 0% to 100%. Numerical analysis (Cluster Analysis – UPGMA method, Euclidean distance coefficient) of plots/relevés was performed using Results and discussion the software package SYN-TAX 2000 (Podani 2001). Pilularia minuta in the zonation of the temporary Environmental gradients and plant communities were ponds examined with canonical correspondence analysis (CCA) using the “PC-ORD”, 6.08 software. CCA takes The cluster analysis shows five main groups (Figure 2) into account different quantitative data, such as pH, corresponding to different plant communities, each one conductivity, coverage (%), altitude, average annual with specific floristic compositions (Table 1) and related temperature (°C), average annual rainfall (mm), to different belts in the temporary pond. The inner belt water level in March (three water level intervals: level with a very long flooding period (from December– 1 = 1–10 cm, 2 = 10–20 cm, 3 = >20 cm) and number of January to March–April) is characterized by Callitriche species (N. sp.).Water pH, electrical conductivity (EC) brutia community (group 1, Figure 2) and by Eleocharis and total dissolved solids (TDS) were determined using palustris community (group 5) with a low presence of pH/conductivity meter SG23 SevenGoDuo. P. minuta. The intermediate belt with a long flooding Two indices were chosen to estimate diversity of period (from December–January to February–March) the plant communities identified by cluster analysis: is characterized by Isoetes longissima community (group (1) species richness of each vegetation cluster, cal- 4) with a moderate presence of P. minuta. The upper culated as the average number of species per plots belt with a moderate flooding period (from December– and (2) Shannon–Wiener’s index of diversity (H). January to February) is characterized by P. minuta The nomenclature is based on Conti et al. (2005) and community within which is possible to distinguish two Downloaded by [University of Catania] at 05:12 07 August 2017

Figure 2. Dendrogram resulting from cluster analysis of the plots (UPGMA method, Euclidean coefficient). Plant communities: 1. Callitriche brutia comm., 2. Pilularia minuta/Tillaea vaillantii subcomm., 3. Pilularia minuta/Juncus pygmaeus subcomm, 4. Isoetes longissima comm. 5. Eleocharis palustris comm. 4 P. MINISSALE ET AL.

sub-communities (group 2 – Pilularia minuta/Tillaea filiformis, and Eryngium pusillum. The phytosociologi- vaillantii, group 3 – Pilularia minuta/Juncus pygmaeus) cal relevés performed by Daoud-Bouattour et al. (2009) the latter being more abundant in shallower waters. for Tunisia, due to the strong floristic similarity, can be Our results showed that temporary ponds host attributed to this new association. amphibian vegetation. Most species belong to The classification of relevés (Junco pygmaei-Pilularie- Mediterranean element (44%), with the dominant life tum minutae) by means of cluster analysis, displayed two form corresponding to therophytes (65%). Lower val- well separated groups, each one with specific indicator ues were reached by hydrophytes (17%), geophytes (2%) species. The first sub-community (Rel. n. 6, 8, 10, 12, 20), and hemicryptophytes (2%). Of these species, 35% are related to natural ponds, is characterized by a peculiar included in the Italian Red Book (Conti 1997), three of floristic assemblage with S. laurentia, C. filiformis and I. which are classified as endangered (i.e. Isoetes longissima, longissima (subass. typicum), while the second one (Rel. Lythrum borysthenicum and Solenopsis laurentia), two as n. 2, 4, 22, 23), which grows in wet bottoms of drainage vulnerable (i.e. Pilularia minuta and Eryngium pusillum), ditches, is characterized by the presence of T. vaillan- and three as lower risk (i.e. Cicendia filiformis, Ranunculus tii (subass. Tillaetosum vaillantii). In western Sicily, P. lateriflorus and Tillaea vaillantii). Most species of these minuta was found in similar ecological conditions (Troia temporary ponds belong to the phytosociological class and Lansdown 2016). It grows on seasonal ponds associ- Isoeto-Nanojuncetea (Brullo and Minissale 1998), which ated with some species of the Isoeto-Nanojuncetea class, mainly includes pioneer annual plant communities that such as I. longissima, Myosotis sicula, Elatine macropoda, grow on periodically flooded soils. Similarly, most of Ranunculus peltatus, R. ophioglossifolius, and with other the recognized vegetation types can be ascribed to the species of Nasturtio-Glycerietalia, such as Alisma lanceo- class Isoeto-Nanojuncetea, with the exception of the helo- latum, Eleocharis palustris and Glyceria notata. phytic Eleocharis palustris community (group 5), which can be included in the class Phragmito-Magnocaricetea Community ecology and diversity (Appendix 3). Isoetes longissima community (group 4) can be referred to the association Isoeto velatae-Crassu- The CCA analysis clearly shows that the main discrimi- letum vaillantii Poiron and Barbero 1965 of the alliance nating factor is water level, a factor closely related to the Isoetion grouping Mediterranean early spring communi- flooding time (Figure 3). The plant communities with ties. Callitriche brutia community (group 1) is referable a longer flooding time are characterized by Callitriche to Ranunculo lateriflori-Callitrichetum brutiae Brullo brutia and Eleocharis palustris, all located in the right and Minissale 1998 of the alliance Menthion cervinae part of the diagram. The intermediate position is occu- of deeper waters. The floristic assemblage of Pilularia pied by Isoetes longissima plant community while P. minuta community (groups 2–3) can be referred to the minuta community (Pilularia minuta/Tillaea vaillantii alliance Cicendio-Solenopsion laurentiae typical of soils subcomm. and Pilularia minuta/Juncus pygmaeus sub- flooding by shallow/middle waters and drying in spring, comm.) is positioned in the upper left of the diagram described by Brullo and Minissale (1998). It is notewor- showing a moderate flooding time. thy that no association has been found in the literature The species richness of each pond ranges between regarding P. minuta, while it is well known the vegeta- 3 and 13 species (mean = 8). The floristic richness tion with P. globulifera L., vicariant species of western and diversity index of our plant communities increase

Downloaded by [University of Catania] at 05:12 07 August 2017 Europe (Szczęśniak et al. 2012) and characteristic spe- from the inner belt towards the less deep belt (Table 1, cies of Pilularietum globuliferae Tüxen 1955, belonging Figure 4). In fact, Callitriche brutia community (five to the class Littorelletea uniflorae Br.-Bl. and Tüxen ex plots) shows a low diversity with an average species rich- Westhoff, Dijk and Passchier 1946. ness of 5.4 and an average Shannon–Wiener diversity In the light of these considerations, we propose a index (H) of 1.2 (J 0.7), as well as the plots containing new association for the Mediterranean P. minuta plant Eleocharis palustris plant community (two plots), having communities: Junco pygmaei-Pilularietum minutae an average of four species and a H index of 0.8 (J 0.6). The ass. Nova hoc loco (Table 1, Rel. 8, cluster A12). This lesser deep ponds, characterized by moderate periods of annual vegetation grows on ponds and drainage ditches submersion, show an increase of species richness and on flat or slightly sloping surfaces, on clayey or clay- diversity index; in particular, I. longissima community ey-silty substrates, subject to periodic flooding within (seven plots) has an average of 8.7 species and a H index the thermo-Mediterranean or lower meso-Mediterra- of 1.4 (J 0.7) while Pilularia minuta and Juncus pygmaeus nean bioclimatic belts (Rivas-Martínez, Penas, and Diaz (nine plots) community averaged 9.8 species and a H 2004). The plant assemblage is mainly characterized by P. index of 1.7 (J 0.8). In the lowland ponds of Great Britain minuta and Juncus pygmaeus, with several hygrophilous under temperate climate, Williams et al. (1998) recorded species belonging to the Isoeto-Nanojuncetea class, such a mean number of six plant species per pond with a 0–25 as I. longissima, Lotus angustissimus, Lythrum hyssopi- species range in temporary ponds. Brose (2001) found folia, L.borysthenicum, Ranunculus lateriflorus, Mentha a mean number of nine plant species per pond with a pulegium, Tillaea vaillantii, Solenopsis laurentia, Cicendia range of 1–24 species on temporary ponds in Germany. BOTANY LETTERS 5 - ...... 5 9 5 1 3 5 10 90 85 16 10 0,7 1,5 0,5 0,7 386 916 7.36 0.26 0.13 40x40 ...... 5 5 5 3 – – 3 – 30 70 80 16 0,7 1,6 0,5 0,7 386 916 40x40 ...... 4 2 1 5 3 1 – 5 – 6 – 70 19 80 16 0,4 0,8 0,4 0,5 386 916 40x40 ...... 5 4 5 1 5 1 2 5 – 1 – – 10 70 10 18 90 10 17 20 20 13 0,8 2,0 0,7 0,8 360 717 40x40 ...... 4 5 5 2 6 60 17 85 17 10 50 10 0,3 0,7 0,3 0,4 360 717 6.89 0.30 0.15 40x40 ...... 5 1 4 5 5 1 5 1 2 5 – 5 – – 30 16 80 10 17 10 10 13 0,8 1,9 0,5 0,7 360 717 40x40 ...... 1 4 1 5 5 1 2 5 – 5 – – 10 50 20 14 85 10 17 30 12 0,7 1,3 0,6 0,8 360 717 40x40 ...... 4 5 5 1 3 5 80 11 80 16 15 0,8 2,2 0,7 0,8 386 916 6.62 0.26 0.14 40x40 ...... 4 7 1 3 5 – – 6 – 60 10 10 70 16 10 0,7 1,4 0,7 0,8 386 916 40x40 ...... 3 5 1 1 5 – 5 – – 1 20 20 50 90 10 30 16 30 11 20 0,8 1,9 0,6 0,8 386 916 40x40 ...... 3 5 1 5 – 5 – – 5 20 10 12 40 85 15 16 20 10 25 0,8 1,7 0,8 0,9 386 916 40x40 ...... 3 1 5 2 5 – 5 – – 5 10 40 10 30 80 10 16 10 10 0,8 2,1 0,8 0,9 386 916 40x40 ...... 3 8 5 1 5 – 5 – – 5 30 40 80 10 16 10 10 15 10 0,4 0,8 0,5 0,5 386 916 40x40 ...... 1 3 6 5 2 5 – 5 – 5 – 1 5 40 30 60 15 16 10 11 0,8 1,9 0,7 0,8 386 916 40x40 ...... 2 2 1 1 – 5 1 – 9 – 5 70 23 20 90 25 16 10 0,4 0,8 0,4 0,5 386 916 40x40 ...... 2 1 5 2 5 1 – 5 5 – – 5 60 22 40 85 30 16 10 0,8 2,0 0,7 0,9 386 916 40x40 ...... 2 4 5 2 1 1 7 10 70 10 90 16 10 0,6 1,2 0,6 0,7 384 916 8.33 0.23 0.11 40x40 ...... 2 2 1 5 2 2 1 1 1 20 60 85 10 16 15 10 0,8 1,9 0,6 0,8 384 916 8.44 0.38 0.19 40x40 Downloaded by [University of Catania] at 05:12 07 August 2017 ...... 1 2 1 3 1 – – 5 – 40 21 60 16 10 0,5 0,8 0,7 0,7 386 916 40x40 ...... 1 5 3 – – 6 – 5 30 60 15 90 17 20 10 0,5 1,2 0,5 0,6 360 717 40x40 ...... 5 1 3 7 5 10 40 13 80 17 20 20 10 0,4 0,7 0,7 0,6 360 717 7.07 0.81 0.40 40x40 ...... 1 3 3 5 3 50 10 50 16 0,7 1,5 0,4 0,6 384 916 8.33 0.23 0.11 40x40 ...... 1 1 2 5 3 6 1 60 20 70 16 10 0,6 1,1 0,5 0,6 384 916 8.45 0.39 0.19 40x40 ich. ex ich. ex chult. chrank) Litv. in Maevskÿ Litv. chrank) huill. cholz & S & Durieu T ( S S Durieu ther species ainfall (mm/year) S venness_e^H/ quitability_J Rel. number Rel. O L. resupinatum Trifolium Eleocharis palustris (L.) R oem. Plant communities Plant L. aquatilis Ranunculus Callitriche brutia Petagna Callitriche rea (side by side/cm) (side by A rea Boreau arenastrum Polygonum Durieu in Bory minuta Pilularia Car. Isoeto- N anojuncetea Car. R Juncus pygmaeus Coverage (%) Coverage sp.Spergularia L. angustissimus Lotus A ltitude (m a.s.l.) L. anagallis - aquatica Veronica L. hyssopifolia Lythrum med. (°C)T med. (Biv.) Guss. (Biv.) spicata Glyceria Lythrum borysthenicum Lythrum R L. Anthemis cotula DC. lateriflorus Ranunculus Water level classes* level Water Mentha pulegium L. pH Ochlopoa H. infirma (Kunth) Conducibility (m S ) Conducibility Brot. Juncus hybridus T D S (g/L) Willd. vaillantii Tillaea o. species N o. (L.) C. Presl Solenopsis laurentia S impson_1-D (L.) Delarbre filiformis Cicendia S hannon_H Eryngium pusillum L. E E Diagnostic species Diagnostic longissima BoryIsoetes & comm. 5. Eleo longissima comm. 4. Isoetes subcomm. / Juncus pygmaeus minuta 3. Pilularia subcomm. vaillantii minuta/Tillaea 2. Pilularia brutia comm. (23 plots). 1. Callitriche communities 1. Plant Table charis palustris comm. 1 = 1–10 cm; 2 10–20 cm; 3 >20 cm. classes (in March): level *Water sp17 sp2 sp18 sp3 sp19 sp4 sp5 sp20 sp6 sp21 sp7 sp22 sp8 sp23 sp9 sp10 sp11 sp12 sp13 sp14 sp15 sp16 sp1 6 P. MINISSALE ET AL. ant ( 2008 ) ant ánchez, and Medina ( 2007 ) ánchez, and Medina ( 2007 ) References annitsaros ( 1999 ) annitsaros anta ( 1962–63 ) anta anta ( 1962–63 ) anta Y orba in Daoud-Bouattour et al. ( 2009 ) et al. orba in Daoud-Bouattour ( 2009 ) icotra ( 1893 ) icotra ć ( 2015 ) ikoli enol et al. ( 2016 ) enol et al. enol et al. ( 2016 ) enol et al. his study his study roia and Lansdown ( 2016 ) and Lansdown roia S ( 1998 ); MeikleQuézel ( 1977 ) S Bazos and Bazos T Bagella and Caria ( 2012 ) Bagella and Caria ( 2004 ) Marchetti N T T 2009 ) ( and Zuccarello E rnandes, Beccarisi, N ( 1980 ) and Gustafsson Bothmer, von S nogerup, Mascia et al. ( 2013 ) Mascia et al. Paradis and Finidori ( 2005 ) and Finidori Paradis Bagella in Daoud-Bouattour et al. ( 2009 ) et al. Bagella in Daoud-Bouattour Mascia et al. ( 2013 ) Mascia et al. Mascia et al. ( 2013 ) Mascia et al. Daoud-Bouattour et al. ( 2009 ) et al. Daoud-Bouattour ( 2011 ) Cardo Garcia ( 2009 ) et al. in Daoud-Bouattour M. Porto Pinto-Cruz, and E spírito-S ilva, S ( 2009 ) et al. Molina in Daoud-Bouattour J. ( 1979 ) and Prelli Badré L. S Daoud-Bouattour et al. ( 2009 ) et al. Daoud-Bouattour ( 2009 ) et al. Daoud-Bouattour ( 2009 ) et al. Daoud-Bouattour Quézel & S Quézel et al. Bariego Hernández in Daoud-Bouattour P. 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Daoud-Bouattour Jiménez- S Delgado, 2016 1903 1993 2016 2016 2009 2002 1980 2009 2010 2008 2007 1979 2007 2009 2008 1854 1952 2009 2008 2006 > 30 years >10 years? 2003–2006 2006–2007 2003–2006 1990–1991 2006–2007 Last observation nineteenth century?nineteenth – Destroyed – >10 pools 2 pools Destroyed Destroyed 1 pool 1 pool 2 pools 3 pools – – – – Destroyed – 3 pools 20 pools- – 1 pool ca. 10 pools Destroyed ca. 12 pools – Population >10 pools 1 pool >3 pools Destroyed 1 pool Destroyed Destroyed 1 pool 3 pools 7 pools >10 pools A nse de Furnellu) A lbufereta ’ lmeto ( O lmeto bbasanta di A bbasanta irso e A ltopiano T our d’ T znalcazar) A ibatejo, Baixo A lentejo Baixo ibatejo, angone” iflet, western Mamora western iflet, T T rapani evilla anto, Mudjardjo, Les Issers, Msabia Issers, Les Mudjardjo, anto, gliastri, Melilli A lacati ejenane ab empio Downloaded by [University of Catania] at 05:12 07 August 2017 tagno di Corru s’Itiri” di Corru tagno iu S iddu” ercone” - R S Mura Dell’Unda,Mura e Porto rgiu rmaris, La Mola de Fornells, S La Mola de Fornells, A rmaris, outheast of ( evilla province rapani rasu, Frasseli, Padullelu, Padullelu, Frasseli, de S uartone, A rasu, Padule re – Kadifekale Cesme- Cozzo O Cozzo Carlentini Fico, Cozzo N ettuno T T Calatafimi, ardò, Lecce N ardò, Masseria Bellimento, Cres, R Cres, 2 islands (Psathoura) CI“Media valle del S CI“Media valle S CI“ CI“Giara di Gèsturi” S CI“Giara Pula, T Pula, rgosolo e Urzulei - S u di O liena, rgosolo “ S upramonte S CI Villanueva de la Jara Villanueva R do O bispo, Vila Montemor-o- N ovo Montblanc R oquehaute, Biot T - Mara Bosa, tra Capo costiera e zona “ E ntroterra S CI Site Garâa S Majen el Ma Gauthier) (mares E l Frîn – Zamora province Zamora E s Mola de Fornells, de Binissermenya, Verda Bassa Bou Ismaïl-Castiglione Djebel S S idi limane S south of R ommani Benslimane, S Huelva provinces Huelva S Cordóba, ea egean S ardinia ardinia ardinia ardinia ardinia ardinia – Izmir ( S myrna) Izmir S icily S icily Lazio S icily S icily A pulia Mediterranean coast Mediterranean A Lesvos S S S S S Castilla-La Mancha Castilla-La A lgarve A lgarve Hérault Maritime A lps Corsica S Region Mogods Kroumiria E l Kala region Kabylies Castilla Léon Castilla Menorca A lger region ran region O ran Gharb Mamora Meseta Coastal A ndalusia 1 2 3 4 5 6 7 8 9 38 37 36 30 31 27 28 29 32 33 34 35 26 25 24 23 22 15 16 17 18 19 20 21 13 14 11 12 10 No. urkey unisia Cyprus T Croatia Greece Portugal France Italy (from Daoud-Bouattour et al. [ 2009 ] modified). et al. Daoud-Bouattour (from minuta of Pilularia 2. Locations Table Country T A lgeria Morocco S pain BOTANY LETTERS 7

Figure 3. Canonical correspondence analysis (CCA) plot. Total variance (inertia) in the species data: 2.5529; Eigen values: axis 1 = 0.604; axis 2 = 0.498, Variance in species data % of variance explained 23.7 (axis 1), 19.5 (axis 2), Cumulative % explained 23.7 (axis 1) and 43.2 (axis 2). Plant communities: 1. Callitriche brutia comm. 2. Pilularia minuta/Tillaea vaillantii subcomm. 3. Pilularia minuta/Juncus pygmaeus subcomm. 4. Isoetes longissima comm. 5. Eleocharis palustris comm.

Della Bella et al. (2008) in a study on the macrophytic Distribution and re-evaluation of Pilularia minuta Downloaded by [University of Catania] at 05:12 07 August 2017 diversity of the Tyrrhenian coastal ponds (central Italy) conservation status in Italy recorded a mean number of nine plant species per pond The recently discovered populations in Sicily and Apulia with a 1–26 species range in temporary ponds. Bagella significantly extend its distribution area in Italy. In the et al. (2009) studied the Sardinian temporary ponds on Mediterranean Region, only the most arid south-eastern old volcanic soils and found a floristic richness rang- areas such as Egypt, Libya, Syria and Israel, are excluded ing between 9 and 56 related to eight distinct floristic (Tab. 2, Figure 5). assemblages, all linked to different ecological conditions. According to the European Red List of Vascular Plants Therefore, macroclimate is not so relevant to the total (Bilz et al. 2011), the species is considered EN B2ab(i, species richness, remaining similar at different latitude: ii, iii, iv, v) c(iv) (IUCN Red List Criteria – Europe). but, in the Mediterranean ponds, it is higher for a single According to Daoud-Bouattour et al. (2009), the rarity plot having generally a much smaller surface. In par- of Pilularia minuta in the Mediterranean area is not only ticular, in small ponds, microtopography and ecological based on the reduction of natural habitat (climatic change variations, due to water depth and flooding period, are and human activity at a local scale), but it also depends crucial ecological features influencing plant community on the tiny size of the species and its ephemeral biological distribution, as already stated by Santo and Arsénio cycle, which could make it rather difficult to find. (2005), Molina et al. (2011), and Caria et al. (2015). 8 P. MINISSALE ET AL.

Figure 4. Pilularia minuta locations: A. Cozzo Fico (Carlentini-Siracusa) flooded temporary ponds with Isoetes longissima comm.; B. Cozzo Ogliastri (Melilli-Siracusa) dry temporary ponds with Isoetes longissima comm. (middle belt) and with Juncus pygmaeus comm. (shallow belt); C-D. Pilularia minuta in its habitat. Downloaded by [University of Catania] at 05:12 07 August 2017

Figure 5. Location of Pilularia minuta populations around the Mediterranean Basin (black dots: existing populations; black stars: destroyed or misidentified populations); (from Daoud-Bouattour et al. (2009), updated). Numbers refer to Table 2.

According to the assessment made on the Italian AOO is 12 km2 (one location for Hyblaean territory, one populations (Mascia et al. 2013; Rossi et al. 2013), the location for Calatafimi territory) (Figure 1). According species is recorded in 46 sites (AOO – 124 km2 – 2 x to the IUCN categories and criteria (IUCN 2001), the 2 km2 grid) in Sardinia, and one site (AOO – 4 km2) major threats for the populations are “human intrusions in Apulia, was considered as vulnerable (VU B2ab iii), and disturbance” and “natural system modifications”. based on the criterion B. However, Mascia et al. (2013) Based on our data and considering the IUCN criterion highlighted for Sardinia a very fragmented distribution B as the best method to carry out the assessment, we and a progressive degradation of its habitat, especially in propose that this species should be considered as endan- areas with intense agricultural exploitation. In Sicily, the gered (EN) B2ab (ii) in Sicily (having a very small AOO, BOTANY LETTERS 9

the occurrence on two locations, and possible decline the effectiveness of the Natura 2000 network in Sicily of populations especially in the western Sicily site due in relation to these specific habitats, which are often to the agricultural practices). Moreover, considering neglected in conservation policies (Bagella, Caria, and the distance between the two main populations (about Filigheddu 2013). 200 km), we can state that the Sicilian distribution area of P. minuta is extremely fragmented. In Apulia, the spe- Disclosure statement cies was assessed as critically endangered (CR) B2ab (ii) (Ernandes and Marchiori 2013), basing on a very small No potential conflict of interest was reported by the authors. AOO, the occurrence of one location and possible population decline. In the light of these considerations: 1. Funding Extremely fragmented distribution on national territory This research was supported by grants from the CUTGANA and a very small overall AOO (well below the threshold (University of Catania). of 500 km of EN status); 2. Generally restricted locations in the Italian territory; 3. Probable decline of the species in many of the known areas; 4. Ongoing reduction Notes on contributors and disappearance of temporary ponds; 5. Changes in Pietro Minissale is a botanist lecturer and researcher in the land use (overgrazing and traditional agricultural activi- Department of Biological, Geological and Environmental ties); we propose to evaluate P. minuta also for the entire Sciences, Plant Biology Section, University of Catania. His Italian territory, as in the rest of its Mediterranean range, current research projects focus on plant biodiversity of the Mediterranean area. with the risk status endangered (EN) B2ab(ii, iii). Contribution: Data collection and interpretation, critical reading of the manuscript. Conclusions José Antonio Molina is a botanist and university professor in Our study revealed important data regarding the dis- the Department of Plant Biology II, Complutense University of Madrid. He is co-director of the Complutense Research tribution pattern and ecological requirements of P. Group FitoSoluM. His research lines are related to Ecology minuta, which are relevant issues for future conservation and Plant Taxonomy. measures for this emblematic and endangered species. Contribution: Data collection and interpretation, critical Moreover, as demonstrated by Bouahim et al. (2015) in reading of the manuscript. Morocco, our results highlight the need to plan concrete Saverio Sciandrello is a botanist in the Centre for conservation actions of this rare species and especially its the Conservation and Management of Nature and micro-habitat whose disappearance is mainly related to Agroecosystems (CUTGANA) University of Catania. His the landscape transformations (agriculture and pasture). current research projects focus on plant biodiversity of We can conclude with the following remarks: (a) the Mediterranean area with special attention to wetlands. Contribution: Data collection, data elaboration and interpre- P. minuta populations occur on soils with a moderate tation, critical reading of the manuscript. flooding time by waters with lower conductivity; (b) a new association (Junco pygmaei-Pilularietum minutae) characterized by P. minuta is proposed here; (c) P. minuta ORCID plant community shows the highest species richness and Pietro Minissale http://orcid.org/0000-0002-4047-4169 Downloaded by [University of Catania] at 05:12 07 August 2017 Shannon-Wiener index of the vegetation zonation in José Antonio Molina http://orcid.org/0000-0003-4348-6015 temporary ponds; (e) after a re-evaluation of the con- Saverio Sciandrello http://orcid.org/0000-0003-1132-5698 servation status of P. minuta in Italy, it is proposed as an endangered species for this territory; (f) considering the high natural value of the Sicilian localities (Cozzo References Ogliastri and Cozzo Fico ponds) for the presence of rare ANTHOS. 2012. Sistema de información de las plantas de and endangered plant species, such as P. minuta, Isoetes España [Plants Information System of Spain]. Real Jardín longissima, Juncus pygmaeus, Lythrum borysthenicum, Botánico, CSIC – Fundación Biodiversidad. Accessed Ranunculus lateriflorus, Solenopsis laurentia, Cicendia April 27, 2016. www.anthos.es filiformis, Eryngium pusillum, and being classified, Badré, F., and R. Prelli. 1979. “Additions à la flore ptéridologique des Alpes Maritimes [Additions to the according to Dir. 92/43/EEC, as priority habitat Pteridological Flora of the Maritime Alps].” Riviéra (3170*), the expansion of the nearby Site of Community Scientifique 1979 (1–2): 5–25. Importance “Cozzo Ogliastri” (ITA090024) is proposed Bagella, S., and M. C. Caria. 2012. “Diversity and Ecological in order to include the Cozzo Fico ponds (area currently Characteristics of Vascular Flora in Mediterranean excluded from any conservation measure). Similarly, Temporary Pools.” Comptes Rendus Biologies 335: 69–76. Bagella, S., M. C. Caria, E. Farris, and R. Filigheddu. 2009. Troia et al. (2016) for the Pilularia population from “Spatial-time Variability and Conservation Relevance of western Sicily, highlighted the deficiencies of the pro- Plant Communities in Mediterranean Temporary Wet tection of the wetland for which they advocated the Habitats: A Case Study in Sardinia (Italy).” Plant Biosystems creation of a N2000 site. These actions would increase 143 (3): 435–442. 10 P. MINISSALE ET AL.

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Appendix 3 Isoetetalia durieui Br.-Bl. 1936 Isoetion durieui Br.-Bl. 1936 Syntaxonomical scheme Isoeto velatae-Crassuletum vaillantii Poiron & Barbero 1965 Phragmito australis-Magnocaricetea Elatae Klika in Menthion cervinae Br.-Bl. ex Moor 1937 Klika & Novák 1941 Ranunculo lateriflori-Callitrichetum brutiae Brullo and Nasturtio officinalis-Glycerietalia fluitantis Pign. Minissale 1998 1953 Cicendio filiformis-Solenopsion laurentiae Brullo Glycerio fluitantis-Sparganion neglecti Br.-Bl. & Siss- and Minissale 1998 ing in Boer 1942 Junco pygmaei-Pilularietum minutae Minissale, Molina & Eleocharis palustris comm. Sciandrello ass. nova Isoeto-Nanojuncetea Br.-Bl. & R. Tx. ex Westhoff et al. Junco pygmaei-Pilularietum minutae tillaetosum vaillantii 1946 Minissale, Molina & Sciandrello subass. nova Downloaded by [University of Catania] at 05:12 07 August 2017