Diversity and distribution of Ludwigia (Onagraceae) in Paraíba State, Northeastern Brazil

This paper provides a taxonomic assessment and distribution details of the species of the genus Ludwigia L. (Onagraceae) for the Paraíba State, Northeastern Brazil. Six species were found: L. erecta (L.) H.Hara, L. helminthorrhiza (Mart.) H.Hara, L. hyssopifolia (G.Don) Exell, L. leptocarpa (Nutt.) H.Hara, L. nervosa (Poir.) H.Hara and L. octovalvis (Jacq.) P.H.Raven. Ludwigia nervosa was recorded for the first time in the studied area. Our taxonomic treatment comprises an identification key to the species. For each species, description, illustrations, taxonomic comments, flowering and fruiting data, geographic distribution map, and the conservation status for the studied area are provided. Among the recorded species, three were classified as “Near Threatened”, two as “Vulnerable” and one as “Critically Endangered”.

Morphological descriptions were prepared based on the analysis of material obtained during fi eld trips, supplemented by specimens from the above-mentioned institutions. Descriptive terminology of vegetative and reproductive structures followed studies of the family Onagraceae as well as the works of Radford et al. (1974) and Harris & Harris (2001). Additionally, we consulted the works of Rizzini (1977) for leaf typifying and Payne (1978) for indumentum. Abbreviations of names of the authors follow The International Plant Names Index (IPNI, continuously updated). Data on the species geographic distribution were retrieved from specialized literature and from labels on the material examined in the herbaria. Data on habitats, fl owering and fructifi cation are taken from the labels of the studied material.

Abbreviations
Conservation status was determined for each taxon at the local scale (Paraíba State, Brazil). Criteria and categories established by the International Union for Conservation of Nature (IUCN 2001) were followed.
The extent of occurrence (EOO) and area of occupancy (AOO) of each species was calculated using the software GeoCAT, available at http://geocat.kew.org/editor, based on distribution data retrieved from voucher labels and from the collections. Although no endemic taxon to Brazil was reported, the current study provided one new record of Ludwigia for the fl ora of the Paraíba State (L. nervosa (Poir.) H.Hara). Most species were reported from the Caatinga and Atlantic Rainforest domains, except for L. nervosa that showed a preferential distribution in the Atlantic Rainforest (Table 1).

Results
The conservation assessments revealed that three species are threatened: Ludwigia hyssopifolia and L. leptocarpa are considered as "Vulnerable" (VU) and L. nervosa as "Critically Endangered" (CR). The other species are not included on the list of threatened species. European Journal of Taxonomy 639: 1-24 (2020) yellow or white, deciduous; androecium isostemonous or diplostemonous, disposed in two series, epipetalous shorter than the episepalous, stamens inserted at the base of the epigynous disk together with the petals; hypanthium not extended above the ovary, cylindrical or angular, 4-5-carpellar, 4-5-locular, ovaries numerous, placentation axial, stigma capitate, globose, slightly lobular, the number of lobules corresponds to the number of locules; nectariferous disk generally plain or convex, on the ovary, nectary depressed, covered with indumentum of white trichomes. Fruit a capsule. Seeds small, numerous, unior pluriseriate in each locule, free or embedded in endocarp, generally with inconspicuous raphe, in some sections it may be expanded and equal in size to the body of the seed, or rarely expanded and wing-shaped (Ludwigia sect. Arborescentes Zardini & P.H.Raven).

Distribution
The genus Ludwigia is pantropical. It is the only genus of the subfamily Ludwigioideae, composed of 83 species grouped in 23 sections, considered the most distinct genus of Onagraceae. Ten sections are distributed in South America, fi ve in Africa, three in North America, three in Asia and two are not restricted to any continent. Main diversity centers are South America and North America (Wagner et al. 2007;Pesamosca & Boldrini 2015).

Habitat and phenology
In Paraíba State the species may be found on the banks of lakes, dams, rivers, close to waterfalls or on humid sites, associated with Caatinga or the Atlantic Rainforest. Flowering and fructifi cation occur between March and July and between December and January.

Conservation status (Paraíba State, Brazil)
The extent of occurrence (EOO) of Ludwigia erecta in the Paraíba State is 43 308.511 km 2 , exceeding the upper limit for Vulnerable status under the criterion B1. The species has an area of occupancy (AOO) of 124 km 2 , within the limit for Endangered status under the criterion B2; however, L. erecta is recorded from more than 5 locations, 33 in the Paraíba State, and there is currently no evidence of a particular threat to its habitat, and no decline in the populations. Despite the AOO that suggests it is in Endangered category, L. erecta is evaluated as Near Threatened (NT), due to its wide distribution in Paraiba State.

Note
Ludwigia erecta is mainly distinguished by its oblongoid, tetrangular capsule and pluriseriate seeds, which are not embedded in the endocarp. The name of the section Ludwigia sect. Pterocaulon to which the species belongs refered to its four-angled stems and capsules (Ramamoorthy 1979 (Vieira 2015;Torres et al. 2016).

Habitat and phenology
In the Paraíba State, it was collected in dams, temporary lakes, streams and rivers, linked to three mesoregions: Sertão, Agreste and Mata, associated with the Caatinga or Atlantic Rainforest. It produced fl owers all the year round and fruits between June and July and between October and November.

Conservation status (Paraíba State, Brazil)
The extent of occurrence (EOO) of Ludwigia helminthorrhiza in the Paraíba State is 23 582.060 km 2 , close to the upper limit for Vulnerable status under the criterion B1. Ludwigia helminthorrhiza has an area of occupancy (AOO) of 100 km 2 which could qualify the species for the Endangered status under the criterion B2. However, L. helminthorrhiza is present at more than 5 locations and no evidence of threats or decline was observed. Ludwigia helminthorrhiza is assessed as Near Threatened (NT) in the Paraíba State.

Note
The species diff ers from other species of the genus in the studied area by its exclusively aquatic habit. Furthermore, it has spongy pneumatophore roots, orbicular leaves, white corolla with a yellow spot at the base and capsules with uniseriate seeds fi rmly embedded in woody coherent endocarp. Ludwigia helminthorrhiza belongs to Ludwigia sect. Jussiaea (= former section Oligospermum (Micheli) H.Hara), characterized by seeds strongly embedded in a portion of the woody endocarp (Zardini & Raven 1992 glabrous; petals 4.5-5 × 2.8-3 mm, golden yellow, elliptic, with acute apex; hypanthium ca 8 mm long, 4-locular; style ca 2 mm long, stigma capitate; stamens 8, anthers globose; plain nectariferous disk with depressed nectaries, pilose, surrounding the base of each epipetalous stamens. Capsule 25-27 × 1.5-2 mm, cylindrical, slightly wide at the distal region, internally dimorphic, glabrous. Seeds smaller than 1 mm in length, fusiform, pluriseriate and not embedded in endocarp in the upper part of the capsule, uniseriate and embedded in endocarp in the lower section of the capsule, raphe non-infl ated, with diameter narrower than the body of the seed.

Habitat and phenology
In the study area, L. hyssopifolia occurs from the Sertão region to the Mata region. It is found on humid soil, in swampy environments, or close to water courses, associated with the Caatinga and the Atlantic Rainforest. Flowers occur from January to October and fruits from May to September.

Conservation status (Paraíba State, Brazil)
The extent of occurrence (EOO) of Ludwigia hyssopifolia is 14 285.685 km 2 , within the limit for the Vulnerable category (EOO less than 20 000 km²). The species' area of occupancy (AOO) is 80 km 2 , within the limit for the Endangered category (criterion B2: less than 500 km 2 ). However, L. hyssopifolia is recorded from more than 5 locations in the Paraíba State, and other conditions were not met to apply the criterion B2 (no evidence of populations fragmentation or decline, no threats or habitat loss). In the Paraíba State, the species falls under the category Vulnerable (VU), defi ned according to criterion B1ab(ii,iii) because only one record occurs in a conservation area, the Monumento Natural do Vale dos Dinossauros, in Sousa, the other locations where the species occurs are not protected areas and are aff ected by urban expansion.

Note
Most voucher specimens of L. hyssopifolia in the consulted herbaria are misidentifi ed as L. erecta. The two species are similar, with tetramerous fl owers with yellow petals, up to 5 mm long. However, the internaly dimorphic capsule with free pluriseriate seeds in the distal part and uniseriate seeds embedded in endocarp in the proximal part is the most important feature that distinguishes L. hyssopifolia from the others species. Dimorphism of the capsule characterizes Ludwigia sect. Fissendocarpa which is monospecifi c (Zardini & Raven 1992;Wagner et al. 2007).

Distribution
The species has a wide distribution in Neotropical region, from southeast USA to Argentina and Africa (Zardini & Raven 1997). and South (PR, RS, SC) Region (Lima et al. 2013;Vieira 2015).

Habitat and phenology
In Paraíba State, L. leptocarpa may be found on the banks of lakes and in the fl ooded areas, in the vegetation of Caatinga and Atlantic Rainforest. It is fl owering from September to December and fruiting in September.

Conservation status (Paraíba State, Brazil)
The extent of occurrence (EOO) of Ludwigia leptocarpa is 15 683.720 km 2 (within the limit for Vulnerable status under the criterion B1) and its area of occupancy (AOO) is 32 km2 (within the limit for Endangered status under the criterion B2). It is known from eight specimens representing a total of eight locations, within the threshold for Vulnerable under criterion B, no population has been recorded in a protected area. In the Paraíba State, the species falls under the category Vulnerable (VU), defi ned according to criterion B1ab(ii,iii).

Note
Ludwigia leptocarpa is characterized by a yellow pentamerous corolla, which is a unique feature within the genus, as all other species of the genus have a tetramerous yellow corolla or a pentamerous white corolla. Uniseriate seeds embedded in horseshoe-shaped endocarp are the most relevant characteristic of L. leptocarpa. The horseshoe-shaped endocarp is a diagnostic feature of Ludwigia sect. Seminuda, a section to which L. leptocarpa belongs (Zardini & Raven 1992;Wagner et al. 2007 Additional material examined BRAZIL -Bahia • Belmonte, Barrolândia, Estação Experimental "Gregorio Bondar" CEPLAC;13 May 1993;fl . and fr.;W. Thomas et al. s.n.;NY[9907].

Distribution
Ludwigia nervosa is distributed from South Mexico to Bolivia and Paraguay (Zardini & Raven 1997 (Vieira 2015).

Habitat and phenology
In the studied area, L. nervosa occurs only in the mesoregion Mata, in swampy environments, associated with Atlantic Rainforest vegetation. Flowers occur in February and May.

Conservation status (Paraíba State, Brazil)
The extent of occurrence (EOO) of Ludwigia nervosa is 0 km 2 and its area of occupancy (AOO) is 8 km 2 . According to the IUCN criteria, the species is assessed as Critically Endangered (CR) under criterion B1ab(i,ii,iii)+2ab(i,ii,iii). Ludwigia nervosa is only known from 2 specimens in Paraíba State, one of which was collected almost 50 years ago, and the second 30 years ago. The biome with which it is associated in Paraíba State is frequently degraded by the expansion of sugarcane monocultures, posing a potential threat to the species and possibly causing a continuous decline of its population.

Note
Ludwigia nervosa diff ers from other Ludwigia species in the studied area by its chartaceous leaves, high nectariferous disk and obconic tetrangular capsule with pluriseriate seeds not embedded in endocarp. Seed characteristics were retrieved from Zardini & Raven (1997 Ludwigia sect. Macrocarpon (Zardini & Raven 1992). Furthermore, it has petals with emarginated apex, 8-ribbed capsules, and pluriseriate seeds in the locule and not embedded in the endocarp.
According to Raven (1963), the species has a complex morphological variation. Specimens may be found varying in size, shape of leaf blades, density of branch and leaf indumentum, and in petal and fruit length (Duarte & Esteves 2001). Precisely for this reason, Raven (1963) Raven & Tai (1977) recognize only as a single species, since specimens of the two subspecies may be found on the same site. Thus, it is usual to fi nd both populations with typical individuals and populations with individuals intermediate in morphological characteristics between the two subspecies. Diff erences are maintained by autogamy (Raven & Tai 1977). In the study area, morphologically variable individuals were found. In this paper, the two distinct populations are treated as a single species, as suggested by Raven & Tai (1977).

Discussion
The genus Ludwigia is the richest in number of species of the family Onagraceae. Currently, 45 species of the genus Ludwigia are recorded in Brazil, of which nineteen species (39.6%) are endemic to the country (Vieira 2015), but only six species of the genus Ludwigia were found in the Paraíba State.
The identifi cation of Ludwigia species is complex, mainly due to the fact that most of them have uniform characters, sharing pattern of stem architecture and leaf morphology. On the other hand, characters associated with leaves and indumentum can be widely variable under diff erent environmental conditions, causing misinterpretations. Many species of the genus Ludwigia are amphibian and show phenotypic plasticity, with morphological features varying under diff erent environmental conditions, causing complications in their identifi cation (Dutartre et al. 2006).
In addition, there are other factors that make it even more diffi cult to identify Ludwigia species such as very easily detachable petals as well as autogamy detected in species (e.g., L. octovalvis), which may result in the establishment of intermediate individuals.
According to the literature, Ludwigia species are often associated with wetlands (Munz 1947;Oziegbe et al. 2011). In the study they were found occurring in rivers, streams, marshes, around ponds and weir as well as in water accumulated on rocky outcrops and in anthropized areas.
Characters most relevant for distinguishing of Ludwigia species recorded in the studied area were shape of the petals and fruits, arrangement of the ovules in locules, presence or absence of persistent endocarp tissue around the mature seeds, and last but not least, raphe size. Other researchers of the group also used some of these diagnostic features to separate species, as well as to delimitate distinct sections (e.g., Eyde 1978;Wagner et al. 2007). According to Eyde (1978) the most important distinguishing features in Ludwigia are the uniseriate or pluriseriate arrangement of the ovules and the presence or absence of persistent endocarp tissue around mature seeds; this author also found that seeds are embedded in endocarp only in taxa with uniseriate arrangement.
The present paper represents an important contribution to the knowledge of the Paraíba fl ora, especially for a better understanding of the delimitation of Ludwigia species, aiming to the development of future studies about the group beyond updating its geographical distribution in Paraíba state and northeastern Brazil.