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Podostemaceae in Southern Brazil

This study provides a taxonomic treatment of the Podostemaceae family in southern Brazil. Podostemaceae is the largest family of strictly aquatic angiosperms. The center of family richness is the equatorial region of South America. Taxonomic studies are still scarce in Brazil. For southern Brazil there are six genera and 10 species recognized. Dichotomous key and illustrations are presented for species identification.


Introduction
Podostemaceae is distributed in rivers in tropical regions of the world and some temperate zones of North America and Asia (Tavares 1997), being the largest family of exclusively aquatic Angiosperms, with 50 genera and approximately 270 species (Philbrick & Novelo 2004). The plants of this family are aquatic herbs, that vary in size, and have unusual morphology for flowering plants. They have simple anatomical features, and generally are very distinct when compared to other groups of aquatic Angiosperms (Ameka et al. 2002). The representatives of this family grow on rocky substrates, in rivers with strong currents. Exceptionally they may occur in lentic ecosystems (Irgang et al. 2003). The life cycle is very singular when compared to other families of Angiosperms, especially because of the need to flower and fruit in synchrony with water-level fluctuations (Tavares et al. 2006). In periods when the rivers have low water levels, some of the plants or even the entire population begins the reproductive process, up to fruit maturity and seed dispersal (Imaichi et al. 2004;Tavares et al. 2006).
Due to their form, sometimes like lichens or bryophytes, the position of Podostemaceae has always been controversial (Tavares 1997) and the phylogenetic relationship discussed (Kita & Kato 2001). Different classification systems always had difficulty in relating the family to other taxonomic groups. When recognized as a family, it was initially placed among the monocots (Richard 1816;Martius & Zuccarini 1822). Lindley (1830) was the first to recognize Podostemaceae as a dicotyledonous family. Warming (1888) considered Podostemaceae related to Saxifragaceae. Cronquist (1981) included the family in the monotypical order Podostemales, subclass Rosidae. Cusset & Cusset (1988), studying the African Podostemaceae, established for the family the exclusive class Podostemopsida. Recently, the classification system APG III (2009) included the family in the order Malpighiales, having as a sister group Hypericaceae and affinities with Clusiaceae and Callophyllaceae. The species with neotropical distribution were recently investigated in a phylogenetical study (Tippery et al. 2011) and the clade clusioid, from the order Malpighiales in which Podostemaceae is included, presented for the first time well resolved phylogeny (Ruhfel et al. 2011). Mello, A.S., Tavares, A.S. & Trevisan, R. Despite the wide distribution and richness of the species, taxonomic studies of Podostemaceae in Brazil are still scarce, although there have been some important recent contributions (Philbrick & Bove 2008;Bove et al. 2011). Tulasne (1863), in the Flora brasiliensis, recognized 15 genera and 30 species. Van Royen (1951, 1953, 1954 did taxonomic treatments for the Americas. The taxonomic decisions of Van Royen represented higher levels of richness and grade of endemism for the South American taxa than those recognized by Philbrick & Bove (2010). Tavares (1997) studied Podostemaceae from some rivers in the Amazon, associating taxonomy with ecological concepts. Aona & Amaral (2006) studied the taxonomy of the family for the state of São Paulo. For the state of Santa Catarina Van Royen & Reitz (1971) indicated the ocurrence of five genera and 13 species. Furthermore, the studies of Pontirolli (1955) and Tur (1975Tur ( , 1988Tur ( , 1997Tur ( , 1999 for Argentina and Paraguay are references for taxonomic studies in southern Brazil, especially because of shared species in the watersheds. New genera and species have being recently described, mainly for Brazil and Argentina (Tur 2003, Philbrick et al. 2005, Philbrick & Bove 2008. Bove (2010) listed 17 genera and 87 species for Brazil. The scarcity of collections, few field studies, and unrepresentative and poorly preserved exsicatae in the collections favor controversial opinions on the taxonomy of the family (Philbrick & Novelo 1995). However, some herbaria from southern Brazil have good collections of Podostemaceae, comprising the most of the states of Paraná, Santa Catarina, and Rio Grande do Sul.
This study aims to present a taxonomic treatment of the species of Podostemaceae occurring in southern Brazil.

Material and Methods
For the taxonomic treatment we followed classical methodology, including a review of the specialized literature, herbarium material, and field expeditions from 2008 to 2010, in which the main rivers of the all important watersheds in southern Brazil were visited. We collected 60 specimens which were included in the collection of the herbarium of Universidade Federal de Santa Catarina, FLOR.
About 300 exsicatae were examined from different herbaria: FLOR, FURB, HAS, HBR, HURG, ICN, LP, MBM, PACA, UPCB, HUCS, from southern Brazil and CTES and LP, from Argentina (siglas according to Thiers 2010). Part of the type material was not analyzed, because it is deposited in European herbaria; however, images of type material available at the sites of the main herbaria were consulted. The morphological characterization of the vegetative and reproductive structures is according to the terminology used for the family. We accepted the synonymization of Van Royen (1951, 1953, 1954, Tur (1997Tur ( , 1999, Tavares (1997) and Philbrick & Novelo 2004.

Apinagia yguazuensis was treated by Van Royen & Reitz (1971) as A. fucoides in Santa
Catarina. However, analysis of specimens from Paraguay and Argentina, associated with new collections from the state, confirmed A. yguazuensis as the taxon occurring in southern Brazil.
The species shows high phenotypic plasticity, varying in size and shape of leaves. Observations on populations occurring in the states of Santa Catarina and Rio Grande do Sul showed that A. yguazuensis lives in streams of low to medium depth and has narrow stems, smaller leaves with yellow to light green coloration. The collection L. Smith & R. Reitz 13927 (HBR) has wider stems and leaves, terminations dichotomous, filiform and tiny. This morphological variability was also observed by Fontana (2008) within a population.
Apinagia yguazuensis can be considered a rare species in southern Brazil, being proposed as vulnerable (VU) by Philbrick & Bove (2010), according to IUCN criteria. This species is distributed in the basins of the Paraná, Iguaçu and Uruguay rivers, in the states of Paraná, Santa Catarina and Rio Grande do Sul. It also occurs in Paraguay, Paraná River, and in Argentina, in the basins of the Uruguay and Paraná rivers.

Marathrum azarensis
This species was cited by Bove (2010) for the state of Paraná, although the material referred to by the author had been collected in the Paraná River, in Paraguay, far from the border with Brazil (Fontana 2007). The collection A.S. Mello & A. Nuernberg 584 (FLOR) in the municipality of Abelardo Luz, Santa Catarina, is in effect the first and only record of the species in Brazil. Marathrum azarensis is hardly recognizable in the field because of its small size and lack of stem. The leaves are flattened, dorsiventral, rosulate, with thick petiole, endings filiform, coloration generally light green and reddish margin.  Fig. 3 a-d Herbs, variable size. Leaves 5.5-35 cm × 3-15 cm, adaxial surface rough, nerves prominent on the adaxial face, with remarkable papillae, abaxial face glabrous. Monochasium spiciform, simple ou branched, 4-23 cm long; rachis 5.5-17.5 cm long; bracts c. 5 mm × 2 mm, in the inflorescence branches. Flowers numerous; spathella 5-8 mm; pedicel 1-2 cm long; tepals 5-10, 5-9 mm long; anthers extrorse, obtuse or emarginate, basifixed, 2-3 mm. Capsule 3.5-4.5 mm long, 8-10 ribbed; pedicel up to 3.5 cm long in ripe fruit. Mourera aspera was collected in southern Brazil in only a few areas in northwestern Paraná. This species has a very restricted area of distribution, so far, only in the basins of the Paraná and Iguaçú rivers. Although Van Royen & Reitz (1971) presented a taxonomic treatment and indicated its possible occurrence in the state of Santa Catarina, there are no herbarium records or field observations that confirm the occurrence of the species in that state. Mourera aspera has the largest leaves and flowers of the southern Podostemaceae. The most striking morphological features are the size and shape of leaves, inflorescence a spiciform monochasium, pink flowers, and the rough papillae that cover the adaxial surface of leaves, composed of a set of siliceous cells.

Mourera
In southern Brazil, the species was collected in rivers of the watershed of the Paraná River, in the western portion of the state. In addition to Paraná, this species occurs in the states of Bahia, Espírito Santo, Goiás, Mato Grosso, Minas Gerais, São Paulo, and Rio de Janeiro. It is also found in Argentina and Paraguay.
Podostemum is the genus with the most species in southern Brazil, including five species. The most striking feature of the genus is the presence of an andropodium, a structure that bears the base of two stamens with anthers. Despite all available literature and the species of the genus being the most common and well reprepresented in collections in austral South America, the taxonomy is still controversial. The monograph on Podostemum (Philbrick & Novelo 2004) used phylogenetic analysis based only on morphological characters and presented a new proposal for the treatments of Van Royen (1954), Van Royen & Reitz (1971) and Tur (1988Tur ( , 1997Tur ( , 1999. According to Van Royen (1954), the genus has 12 species in south Brazil and Van Royen & Reitz (1971) cited the occurrence of seven species in Santa Catarina. In contrast, Philbrick & Novelo (2004) justified that the species recognized by Van Royen (1954) are, in fact, local forms of species with greater distribution. Those authors recognized only four species (Podostemum comatum Hicken, P. distichum (Cham.) Wedd., P. muelleri Warm. and P. rutifolium Warm.) and added P. irgangii Philbrick & Novelo.

Podostemaceae in Southern Brazil
This study was innovative, but it led to a discussion concerning their taxonomic conclusions, requiring intensification of taxonomic studies. The genus Crenias Spreng, treated by Van Royen & Reitz (1971)  Herbs of variable size. Roots 0.8-2 mm wide. Stem dimorphic, twisted, little branched, 2-115 cm long when vegetative and 1.5-2 cm long when reproductive. Leaves 2-20 cm long, dichotomously divided, divisions appearing in two dimensions; apex of endings elongate, rounded to acute; petiole flattened; stipules amplexicaulis, with 2(-3) triangular teeth, 0.2-1.5 mm long. Flowers growing on short stalks arising from the roots; pedicel 0.5-1.5 cm; tepals 3, linear to filiform, andropodium 1-3 mm long; ovary ellipsoid, 1-2.7 mm long; stigmas entire, filiform, 1-1.5 mm. Capsule 2 mm long, 2 valves unequal, 3(-5) ribs on each valve. Podostemum comatum is rare in southern Brazil, despite its wide dispersion area in the three states. The herbarium collections are limited and usually incomplete, especially the dimorphic stems, often collected separately and treated as distinct species. During field work it was not possible to collect this species in Santa Catarina, requiring intensified new sampling. In the municipality of Telêmaco Borba, Paraná, a population was found with stems over one meter in length, a fact never reported before in the literature.
Podostemum comatum is distributed in the states of Paraná, Santa Catarina and Rio Grande do Sul. It also occurs in the state of São Paulo and in Argentina, Paraguay and Uruguay. Figs. 5b-d, 6a-c Herbs. Roots prostrate, flattened, 0.6-2.9 mm wide. Monomorphic stems, older rigid, dark and twisted, 0.4-600 mm long. Leaves peciolate, compound, inserted perpendicularly on the stem axis, distichous, variable forms, when verticillate, 2 or 3 axes from which arise leaflets; when dichotomous, 2-8 dichotomic divisions emerging in three dimensions, last divisions of leaves in V or U shape, apex acute, 0.2-15 cm long; stipules emerging as an extension of the sheath navicular-shaped, persistent, hard and darkened in older stems, 0.2-1.4 mm long, 2-7 teeth of different sizes, triangular, lateral larger than the central, 0.05-0.3 mm long. Flowers 1-5 per stem; tepals 3, 2 lateral and 1 at the bifurcation of the andropodium; andropodium 0.3-5.2 mm long; ovary reddish, 6-8 ribs, stigmas entire. Capsule bivalvar, 3-4 ribs per valve.   Podostemum distichum is the most common species, with the greatest dispersion area in southern Brazil, occurring preferentially in waterways on the South Brazilian Plateau, forming dense communities with P. comatum, P. muelleri, P. rutifolium and Tristicha trifaria. In field works we realized that it is common at higher altitudes. P. distichum has the highest morphological variability within the genus, with little-or much-divided leaves, verticillate or not and stems short or long. It differs from other species by the leaf divisions arising in three dimensions. Philbrick & Novelo (2004) synonymized P. atrichum, P. arguirense, P. glaziovianum, P. schenckii and P. warmingii under P. distichum. However, the phylogenetic approach of Moline et al. (2006), including morphological and molecular characters, indicated that the proposed complex should be carefully studied. The analysis of collections and field work were crucial to note this complexity. Although we are accepting the proposal made by Moline et al. (2006), it is necessary to intensify work and it will probably be given new taxonomic positions.
In Brazil, Podostemum distichum is widely distributed over the three southern states, as well as São Paulo and Minas Gerais. It also occurs in Argentina, in the basins of the Uruguay River and Paraná rivers, in Paraguay and Uruguay. Figs. 6d-g, 7a-b Herbs. Roots prostrate, rounded, 0.2-2.1 mm wide. Monomorphic stems, prostrate or erect, 1-42 mm long. Leaves distichous, divided, divisions of the leaves verticillate, 1-5 cm long; whorls uniformly arranged, 5-14 whorls per leaf, 6-11 leaflets per whorl, 3.1-7.2 mm long, apex acute. Petioles 0.2-0.4 mm long; base symmetric, perpendicular to the axis of the stem, hard; stipules in two forms, hard, symmetric, persistent, dark in older stems; first type located at the base of the leaf insertion on the stem, with two lobes, 0.7-1.1 mm long, subamplexicaulis, protruding 0.4-0.6 mm from the stem; second type appearing above the insertion of the petiole; teeth 4-9, 0.2-0.5 mm long. Flowers 1-7 per stem, solitary; tepals 3, linear, sometimes curved, 2 lateral, 0.6-2mm long and 1 at the bifurcation of the andropodium, 0.4-1.5 mm long; andropodium 0.3-1.7 mm × c. 4.5 mm. Ovary 0.8-2.1 mm × 0.8-1.6 mm; stigmas 2, entire, 0.4-1.6 mm. Capsule 1.2-2.2 × 0.9-1.7 mm; peduncle 1-6 mm long.   Podostemum irgangii is the unique species of the genus with two kinds of stipules. Another striking feature is the even distribution of the verticillate whorls. However, identification of Podostemum irgangii and P. distichum may be grossly mistaken. P. irgangii has two forms of stipules and its leaves are usually evenly verticillate. Moreover, in communities where both species occur together, Podostemum irgangii usually has stems and leaves darker and harder. Among the criteria used for diagnosis of the species, stipules and uniform verticillate division of the leaflets were not present in all populations analyzed. Some populations have one or more divisions of the leaves in which the leaflets are inserted irregularly. Likewise, some individuals had smooth stems and the stipules were inserted only above the petiole. Although some populations of Podostemum irgangii are easily identified, the morphological variability found, mainly in rivers when associated with Podostemum distichum, indicates the need for increasing collections. Podostemum irgangii is the only species of the genus endemic to southern Brazil. It was considered to be vulnerable (VU) by Philbrick & Bove (2010). In the present study it is recorded for the first time in Rio Grande do Sul. It occurs only in rivers located in the western portion of the Araucaria Plateau, which compound the basins of the Iguaçú and Uruguay rivers. Due to the large loss of habitats and the small area of distribution, the species is in serious danger of extinction. Warm. Kongel. Danske Vidensk. Selsk. Skr., Naturvidensk. Math. Afd. ser. 6, 4: 445, 480 (t. 16-17). 1888Warm. Fam. Podostem. 3: 1, 38, pl. 16, 17. 1888 Figs. 7c-e Herbs. Roots prostrate, 0.3-8mm wide. Monomorphic stems. Leaves usually sessile, simple, entire or with 1-4 divisions dichotomic, 0.1-34 mm × 0.2-1.5 mm; blades linear to spatulate, divisions dichotomic emerging in two dimensions; base of the leaves flattened, asymmetric, wider than the blade, obliquely inserted on the stem, flexible or hard; stipule simple, asymmetric, forming a visible tooth only on one side, entire or slightly emaginate flattened, persistent and hardened in older stems. Flowers 1-10 per stem; tepals 3, 2 latera 0.5-1.9 mm long and 1 at the bifurcation of the andropodium 0.1-1.3 mm long; andropodium 0.1-3 mm long; ovary 0.8-2.3 × 0.6-1.8 mm, 6-8 ribs; stigmas entire. Capsule 1-2.7 mm × 0.9-1.9 mm; 6-8 ribs, 3-4 per valve.

Podostemum müelleri
Podostemum müelleri is recognized by the enlarged base of the leaves and the stipules consisting of a tooth and only visible on one side. Podostemum müelleri presents wide distribution in the southern states of Brazil, as wel as São Paulo and Goiás. It also occurs in Argentina, Paraguay and Uruguay. Leaves distichous, entire to 5 times dichotomized or lobed, 1.5-20 mm long, spatulate; apex rounded, obtuse or acute, 0.9-2.1 mm long; base of the leaves symmetric; stipules 0.01-0.4 mm long, persistent, hardened and darkened in older stems, 2 teeth triangular and flattened, 0.05 mm long. Flowers 1-5 per stem; tepals 3, apex acute, 2 lateral 0.6-1.7 mm long and 1 at the bifurcation of the andropodium 0.2-1.2 long; ovary reddish pink, 8-10 ribs, 0.4-2.1 × 0.4-1.5 mm; stigmas entire. Capsule 1.2-2.3 mm × 0.8-1.6 mm; 8-10 ribs, 4-5 per valve. Podostemum rutifolium is recognized by very small leaves, blade spatulate, apex obtuse, rarely acute. The stems usually are diminute, inserted in opposite way along the roots. The stems and leaves are prostrate. In areas where it is dominant, it forms dense populations. Philbrick & Novelo (2004) propose two subspecies for P. rutifolium: P. rutifolium subsp. rutifolium, occurring in austral South America and P. rutifolium subsp. ricciforme to Central America. Both subspecies are differentiated only by leaf size and disjunct occurrence. In the present study we do not consider any of the subspecies, since leaf size is not a significant character in the circumscription of taxa in this family.
Podostemum rutifolium is common in southern Brazil, mainly in rivers in the states of Rio Grande do Sul and Santa Catarina. It also occurs in Argentina, Paraguay, and Uruguay.
The genus belongs to the subfamily Tristichoideae, recognized by Engler (1930) and considered by many authors as a different family, because it is characterized by the absence of spathella before anthesis and by having whorls that involve all floral parts. Recent works on the biogeography of Tristicha (Kita & Kato 2004) suggested that this genus had originated in Africa and dispersed to other continents, following a reverse path of the other species of the family.  specimens of Podostemum. This species is easily recognized in the fertile condition by large pedicels and three tepals involving the ovary. The tristichous phyllotaxy also assists in the identification.

5.1
Tristicha trifaria is widely distributed in southern Brazil, occurring mainly in communities with species of Podostemum. The species is the only one in the family that has a Pantropical distribution, occurring also in Africa. However, biogeographic analyses (Kita & Kato 2004) indicate that there are possibly two different species, one confined to the African continent and the other to the Americas.