Isoëtes sabatina ( Isoëtaceae Lycopodiophyta ), a new aquatic species from central Italy

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Isoëtes sabatina (Isoëtaceae, Lycopodiophyta), a new aquatic species from central Italy a

A. Troia & M. M. Azzella

b

a

Dipartimento di Biologia ambientale e Biodiversità, Università degli Studi di Palermo, Palermo, Italy b

Dipartimento di Biologia ambientale, La Sapienza Università, Roma, Italy Accepted author version posted online: 14 Mar 2013.Version of record first published: 08 Apr 2013.

To cite this article: A. Troia & M. M. Azzella (2013): Isoëtes sabatina (Isoëtaceae, Lycopodiophyta), a new aquatic species from central Italy, Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology: Official Journal of the Societa Botanica Italiana, DOI:10.1080/11263504.2013.782902 To link to this article: http://dx.doi.org/10.1080/11263504.2013.782902

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Plant Biosystems, 2013 http://dx.doi.org/10.1080/11263504.2013.782902

Isoe¨tes sabatina (Isoe¨taceae, Lycopodiophyta), a new aquatic species from central Italy A. TROIA1*, & M. M. AZZELLA2

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Dipartimento di Biologia ambientale e Biodiversita`, Universita` degli Studi di Palermo, Palermo, Italy and 2Dipartimento di Biologia ambientale, La Sapienza Universita`, Roma, Italy

Abstract The new species Isoe¨tes sabatina is described and illustrated. Morphological, anatomical, and ecological characters are given. It differs from the similar I. echinospora by several characters, such as megaspore ornamentation and size, microspore size, velum extension and form, and also for its ecology. A table showing the main differential characters of the new species compared with those of the other European aquatic species is presented. So far, the species is known from a single locality (Bracciano Lake, central Italy), having a peculiar ecology and within the Mediterranean bioclimate.

Keywords: Isoe¨taceae, Isoe¨tes, Italy, Lycopodiophyta, Mediterranean region, taxonomy

Introduction The genus Isoe¨tes in the Mediterranean area has been the subject of several studies in the last decade. Thanks to the results of investigations in the fields of cariology (e.g., Troia 2001; Peruzzi et al. 2003), morphology (e.g., Rolleri & Prada 2007; Bagella et al. 2011; Troia et al. 2012), and molecular systematics (Hoot et al. 2006; Bolin et al. 2008), a new key to the scarce macro-morphological variability of the genus has been found, allowing a better definition of the species concept in this group of organisms. Consequently, several new species have been discriminated or described in recent years (e.g., Cesca & Peruzzi 2001; Prada & Rolleri 2005; Ernandes et al. 2010; Troia & Raimondo 2010 [2009]; Bolin et al. 2011). During field investigations connected with a survey of the flora and vegetation of Italian volcanic lakes (Azzella 2012), in summer 2010, a population of Isoe¨tes was located in Bracciano Lake (Latium, central Italy) and reported as I. echinospora Durieu (Azzella & Ragogna 2011): it was the first report of this species in the Mediterranean region of peninsular Italy (Blasi & Frondoni 2011; Capotorti et al. 2012a), the nearest populations being in the Alps, ca. 500 km apart (Ferrarini et al. 1986).

Closer inspection of the plants and ecological considerations of their habitat showed that they differed in several aspects from I. echinospora. Analyses of living and dried plants and comparison with other aquatic Isoe¨tes species confirmed that this population represents a unique and previously undescribed species, which is here named and described. For description and nomenclature of megaspores and microspores, we followed Hickey (1986) and Musselman (2003), respectively.

Taxonomy Isoe¨tes sabatina Troia & Azzella, sp. nov. Figures 1 –8 Type: Italy. Lago di Bracciano (Roma), localita` Polline (UTM 33T 275.4667) at a depth of 1.2 m, on sandy substrate, 163 m a.s.l., 18 August 2010, leg. M.M. Azzella (holotype: FI; isotype: RO); same locality and data as above, leg. M.M. Azzella, July 2012 (paratypes: PAL, FI, RO). Differt ab Isoe¨tes echinospora macrosporarum ornamentatione magnitudineque, atque veli forma magnitudineque. Plants submerged in lakes (Figure 1). Stem (corm) bilobate (rarely trilobate). Leaves (15 – )20

Correspondence: M. M. Azzella, Dipartimento di Biologia ambientale, La Sapienza Universita`, P.le Aldo Moro 5, I-00185 Roma, Italy. Tel: þ 39 06 49912866. Fax: þ 39 06 49912420. Email: [email protected] q 2013 Societa´ Botanica Italiana

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Figure 3. I. sabatina. Transverse section of the leaf: AC, air chambers (those on the left are covered by translacunar diaphragms); C ¼ vascular bundle (with one intrastelar canal).

Figure 1. I. sabatina, general morphology and habit of the plant (the coin is ca. 22 mm in diameter).

(2 26), patent to erect, narrowly lanceolate, (6– )7 (2 9) cm long, 2 –3 mm wide at base, ca. 1 mm wide at mid-length. Subula semiterete, adaxially flat, abaxially convex. Leaf epidermis with irregularly striated cuticular ornamentation, “cuticular pegs” (sensu Prada & Rolleri 2005 ¼ “cun˜as cuticulares” sensu Rolleri & Prada 2007) well developed, evident as continuous longitudinal ridges (Figure 2). Four air chambers, with translacunar diaphragms, and one intrastelar canal (Figure 3); collenchymatous strands

Figure 2. I. sabatina. Holotype: surface view of the leaf epidermal cells (SEM image). Note the cuticular ornamentation (irregular striae), and the cuticular pegs well developed, evident as continuous longitudinal ridges.

and stomata absent. Velum covering ca. 3/4 – 4/5 of the sporangium, often with a “fenestra” (cf. Brunton & Britton 1996) (Figure 4). Ligule ca. 1 – 2 mm long, membranaceous, broadly triangular. Labium small, shorter than ligule. Megaspores (545 – )575 (2 645) mm in polar diameter (sample size ¼ 15), white, echinate in the distal surface, with peculiar adpressed elongate structures in the proximal surface (Figures 5, 6). Microspores (29– )30(2 33) mm long (sample size ¼ 30), laevigate, with irregular occasional spinules (Figures 7, 8). Etymology. The epithet refers to the ancient Latin name of the Lake Bracciano, “Lacus Sabatinus”, where the species has been found. Ecology. Bracciano Lake, the type locality, is located at an altitude of 164 m a.s.l. in the northern part of

Figure 4. I. sabatina. Adaxial face of the leaf base: lm, leaf margin (hyaline); li, ligula; ve, velum; fe, “fenestra” (window) in the velum, showing the sporangium surface.

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Isoe¨tes sabatina new species from Italy

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Figures 5–10. SEM images of megaspores and microspores. Figure 5. I. sabatina – Proximal view of a megaspore. Figure 6. I. sabatina – Megaspore (detail of the proximal surface). Figures 7 and 8. I. sabatina – Microspores. Figure 9. I. echinospora – Proximal view of a megaspore. Figure 10. I. echinospora – microspore. (Figures 5–8 from the holotype; Figures 9 and 10 from the herbarium specimen PAL 18619, “Dans le lac de Gue´ry, pre`s le Mont Dore, Puy-de-Dome, Dec. et rec. Durieu de Maisonneuve, 23 et 24 aouˆt 1861”).

the Latium Region (central Italy). The lake is one of the 12 volcanic lakes occurring in central-south Italy. It is a deep hardwater lake with a circular shape related to its volcanic origins. The Quaternary potassic volcanism in the Roman Province is related to the opening of the Tyrrhenian back-arc basin started during the Pliocene; in particular, the geological district in which lake Bracciano occurs was the site of intense volcanic activity beginning at about 600,000 years ago and continuing to ca. 90,000 years ago (Sottili et al. 2010). The aquatic flora of the lake has never been systematically studied before 2009 (Azzella 2012; Azzella et al. 2013). I. sabatina was found on the southeastern coast of the lake, on a sandy substrate at

a depth of 0.5 –1.5 m; owing to seasonal fluctuations of about 1 m, in the winter this depth increases up to 2.5 m. Here, I. sabatina grows in a coenosis characterized by the structural dominance of Juncus articulatus L. and Eleocharis acicularis (L.) Roem. & Schult., and the presence of other vascular plant species (Potamogeton perfoliatus L., P. crispus L., Myriophyllum spicatum L., Ranunculus tricophyllus Chaix s.l., Baldellia ranunculoides [L.] Parl.) and stoneworts (Chara aspera Dethard. ex Willd., C. hispida L. sensu Auct., C. vulgaris L., Nitella hyalina [DC.] C.Agardh). Owing to the dominance of Eleocharis acicularis and the presence of Baldellia ranunculoides, according to the Habitats Directive 92/43 EEC, the coenosis can be ascribed to the habitat

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3130 (Oligotrophic to mesotrophic standing waters with vegetation of the Littorelletea uniflorae and/or of the Isoe¨to-Nanojuncetea) (Biondi et al. 2009), never reported before in Bracciano Lake. In order to preserve the lake water from pollution, an O-ring collector connected with a sewage treatment plant was built around the lake in 1982 – 1984 (Mastrantuono et al. 2008); the water quality parameters during the last decades showed good nutrient status, and the lake was classified as oligomesotrophic (Margaritora et al. 2003). Nevertheless, an increase in the total nitrogen content of the surface waters has been reported (Catalani et al. 2006), and the wastewater treating system may be not sufficient to preserve the lake from eutrophic conditions. In July 2012, a specific survey of the physicochemical characteristic was conducted on the water near the Isoe¨tes population. We measured a maximum temperature of 28.58C, a conductivity of 560 mS cm21 at 208C, a pH of 8.9. Even if they are single-day measurements, they confirm the basic characteristics of the lake waters measured in winter 2010 using standardized methodologies (Legnani et al. 2005): alkalinity 3.3 meq l21, conductivity 482 mS cm21 at 208C, pH 8.0, total phosphorous 14.2 mg l21. Distribution. I. sabatina is only known so far from the locus classicus, in an area of about 700 m2 where about 1,000 mature individuals occur. It is possible that other populations may be found, within the same lake and/or in some of the other Italian volcanic lakes, which have similar chemical and hydrological characteristics (Margaritora 1992); nevertheless, the anthropogenic changes documented in the same lakes (Margaritora et al. 2003; Mastrantuono et al. 2008; Elwood et al. 2009; Azzella 2012), the ecology of aquatic Isoe¨tes species (generally needing clean and clear waters), and the field investigations made in Italian volcanic lakes by one of us (Azzella 2012) and by other researchers (e.g., Avena & Scoppola 1987; Scoppola et al. 1991; Iberite et al. 1995; Azzella & Scarfo` 2010) suggest that the known population of I. sabatina could be the only relic of a species more widely spread in the past. Conservation status. The single known population is potentially threatened by human activities: despite the presence of a Regional Natural Park and the absence of significant sources of organic wastes along the shores, local phenomena of water quality deterioration depend on some small inlets discharging into the lake and not connected to the sewage system, on some cultivated areas and on the intense recreational use of the sandy beaches (Mastrantuono et al. 2008). Considering its currently known range (less than 100 km2), the existence of only a single location, and the possible continuing decline of the

quality of habitat, the species can be ranked as Critically Endangered under red list criteria B1 (CR B1ab(iii); IUCN 2001). Thus, the presence of Isoe¨tes sabatina must be included in the biodiversity conservation policies recently suggested in the municipality and province of Rome (Blasi et al. 2008a, 2008b; Capotorti et al. 2013). Moreover, the Regional Park “Bracciano e Martignano” could play an important role in the protection of this endangered endemic species (Capotorti et al. 2012b) and ex situ programs of conservation could be applied to avoid the loss of biodiversity already highlighted in other Italian aquatic biotopes (see e.g. Croce et al. 2012), as suggested for other rare water ferns in the Mediterranean region (Ernandes & Marchiori 2012). Taxonomic and ecological observations. The systematic relationships of the new species are difficult to assess merely on the basis of anatomy and morphology, owing to parallel and convergent morphological evolution in the genus (Hickey 1986; Hoot et al. 2006; Bolin et al. 2008). The general morphology of the plant and of the spores, and the presence of a velum, suggest a link with I. echinospora, a widespread species typical of cold oligotrophic lakes in arctic and ˇ tvrtlı´kova´ alpine zones of northern hemisphere (C et al. 2012); however, morphological and ecological traits, as shown above, clearly differentiate the two species. In particular, I. echinospora has a small velum, covering 1/3 – 1/4 of the length of the sporangium (Prada 1983), cross section of the leaf more or less circular (Prada 1983), megaspore ornamentation echinate all over the surface (Prada 1983; Ferrarini et al. 1986), smaller megaspore (diameter [418] – 431.5 – [456] mm and 360 – 480 mm, respectively, according to Ferrarini et al. 1986; Prada, 1983), smaller microspore (length [24] – 27 –[30] mm and 24 – 26 mm, as above). To better compare the two species, in Figures 9 and 10, we show SEM images of I. echinospora spores, taken from a specimen collected in the locus classicus (according to Prada 1983) and kept in the Herbarium Mediterraneaum (PAL). In addition, Table I compares some morphological and ecological traits in all the European strictly aquatic species, including I. sabatina. Also ecological requirements of the new species appear unique (see Table I). The European aquatic Isoe¨ tes species normally occur in oligotrophic (total phosphorus , 20 mg l 21) and soft water (alkalinity ¼ 0.70 meq l21) (Voge 2004; Free et al. 2009). Indeed, the distinction between soft water and hard water is important to discriminate between lakes characterized by the presence or the absence of isoetid species (Vestergaard & Sand-Jensen 2000; Smolders et al. 2002). To the best of our knowledge,

Bioclimate (cf. RivasMartinez et al. 2004) Distribution area

Habitat

Microspore ornamentation Microspore size (mm): mean (min–max) Number of leaves: mean (min–max) Maximum leaf length (cm): mean (min–max)

Velum Corm lobes Collenchymatous strands Cuticular ornamentation Cuticular pegs Megaspore ornamentation Megaspore size (mm): mean (min–max)

Europe and N. America, usually N of 508N lat., extending southwards to Pyrenees, Alps

Cold soft water lakes

Europe, usually N of 508N lat., extending southwards to Pyrenees, Alps; circumboreal

Cold soft water lakes

Warm hard water lake

(8– 25)

Central Italy

(5– 20)

7 (6– 9)

(8– 40)

Boreal-temperate

(10–40)

20 (15–26)

(35–39)

Boreal-temperate

(24–26)

30 (29–33)

Laevigate/granulate

(530–700)

Partial (,1/3) 2 0 Discontinously striated Yes Cristate/reticulate

Isoe¨tes lacustris L.

Mediterranean

Laevigate/bacillate

(360–480)

575 (545 –645)

Laevigate/bacillate

Partial (,1/3) 2 3–2 (1) Smooth No Echinate

Isoe¨tes echinospora Durieu

Almost complete 2 (rarely 3) 0 Irregularly striated Yes Echinate/adpressed

I. sabatina Troia & Azzella

Pyrenees

Temperate

Mountain lakes

(4 –9)

(6–20)

(27–40)

Laevigate/granulate

(550–660)

[Partial] [2] [0] [Irregularly striated] [No] Echinate/cristate

Isoe¨tes creussensis Lazare & S. Riba ( ¼ I. brochonii sensu Auct.)

C-NW Spain

Temperate

Mountain lakes

10 (6 –15)

18 (5 –31)

28 (22–32)

Echinate

292 (231–385)

Complete 3 8 (10) Striated No Sparsely pustulate

Isoe¨tes asturicensis (M. Laı´nz) M. Laı´nz

NW Spain

Temperate

River beds

60 (26– 84)

37 (18– 72)

32 (27– 42)

Echinate

580 (485–731)

(Almost) complete 3 3 (4) Striated No Pustulate

Isoe¨tes fluitans M.I. Romero ( ¼ I. longissima sensu Auct.)

NW Italy (Po Plain)

Temperate

River beds

(30–100)

(90–100)

35 (30–40)

Laevigate/ granulate

566 (540 –610)

Absent 3 3 (6) Smooth No Baculate

Isoe¨tes malinverniana Ces. & De Not.

Table I. Synoptic comparison of European strictly aquatic Isoe¨tes species, based on data from different sources (Prada 1983; Ferrarini et al. 1986; Jermy & Akeroyd 1993; Romero et al. 2004; Romero & Real 2005; Rolleri & Prada 2007; Lazare & Riba 2010). For I. creussensis, some characters (in square brackets) were inferred from Rolleri & Prada (2007, sub “I. brochonii”).

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aquatic Isoe¨tes species were never found in waters with values of alkalinity similar to those recorded in Bracciano lake. In a recent work on I. malinverniana (Italy), the general link between low values of electrical conductivity and the presence of Isoetes species was confirmed, showing that an increase from ca. 100 to ca. 200 mS cm21 (in that case due to a nutrient enrichment of the water) may result in the local extinction of that species (Abeli et al. 2012). Further studies are in progress to improve our knowledge of the new species and shed light on its systematic relationships.

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Acknowledgements We thank the keepers of the herbaria FI, RO, and PAL for the loan of study material, Carmela Di Liberto (Dipartimento di Biologia ambientale e Biodiversita`, Universita` di Palermo) for the assistance with scanning electron microscopy, and two anonymous reviewers for their valuable comments and suggestions. Financial support from International Foundation Pro Herbario Mediterraneo and Fondazione per la Flora Italiana is gratefully acknowledged.

Note * Current affiliation: Dipartimento di Scienze e Tecnologie Biologiche Chimiche e Farmaceutiche, Universita` degli Studi di Palermo, via Archirafi 38, I-90123 Palermo, Italy. e-mail: [email protected]

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