Flora of the State of Paraíba , Brazil : Loranthaceae Juss

The family Loranthaceae Juss., characterized by its parasitic habit, is rarely studied in Brazil. Current research provides a taxonomic survey of Loranthaceae in the State of Paraiba, northeastern Brazil, in which ten species belonging to four genera have been recorded: Passovia (one species), Psittacanthus (two species), Pusillanthus (one species) and Struthanthus (six species). Struthanthus concinnus Mart. was found for the first time in the state of Paraíba. A key to the species identification and taxonomic descriptions is presented, with images, geographic distribution and host data.


Introduction
Featuring more than 4000 parasite species among the angiosperms (NICKRENT et al., 1998), the order Santalales is included in the Loranthaceae group.It is mainly characterised as a hemiparasite with an economic importance associated to the damage it causes to plantations (CAZETTA; GALLETTI, 2003).The order Santalales is represented by several species known in Brazil as "ervas-de-passarinho" (mistletoes) and comprises 160 genera and approximately 2,200 species, currently comprising 18 families (NICKRENT et al., 2010).Among these families, Loranthaceae presents worldwide importance due to its representativeness with cosmopolitan distribution (TAINTER, 2002).
The "ervas-de-passarinho" [literally, bird´s plants] are so called because of the significant number of species, whose dispersal is mainly done by birds, with a close relationship between the plant group and birds (REID, 1991).When this relationship is upset by environmental changes, serious consequences occur, such as a sharp decrease in parasitic plants due to the loss of dispersers (ROBERTSON et al., 1999).
The family Loranthaceae comprises 700 species in 60 genera (KUIJT, 2007) and is abundant in the tropics, inhabiting a wide variety of hosts (TAINTER, 2002;LEAL et al., 2006).Although the first taxonomic analysis of the family was published in Die natürlichen Pflanzenfamilien by Adolf Engler (1897a, b and c), many divisions within the order have been added, where for a long time the Viscaceae had been included (NICKRENT et al., 2010).
Loranthaceae has been the target of several changes in its nomenclature.At first, Van Tieghem (1894) tallied 118 genera which Engler (1897a) synonymised under the genus Loranthus Jacq.Later, Danser (1929) proposed the basic framework for the current classification, dividing the family into three tribes: Nuytsieae, Elytrantheae and Lorantheae.Molecular studies carried out by Nickrent and Duff (1996), Nickrent et al. (1998) and more recently by Vidal-Russell and Nickrent (2008) and Nickrent et al. (2010) upheld the monophyly of Loranthaceae, with the Schoepfiaceae and Misodendraceae families as sister groups.The study by Nickrent et al. (2010) did not merely support the monophyly of Loranthaceae but also divided the family into tribes and sub-tribes.
Caires and Dettke (2014) reported eight species of Loranthaceae for the State of Paraíba, although the lack of publications on the taxonomy of the family for its flora constitutes a gap in the knowledge on the representativeness of mistletoes.
Current research presents a taxonomic survey of Loranthaceae for the state of Paraíba, Brazil, and aims to contribute towards in-depth knowledge on the richness and distribution of its genera and species in the region and on the flora of northeastern Brazil.

Study area
The state of Paraíba, Brazil, mainly lies on the Borborema Plateau (Planalto da Borborema), with the drought polygon constituting 98% of its territory.Geographic relief is in general quite different (AESA, 2006), featuring two large regions: the littoral, with predominant sandy coastal plains (restingas) on narrow beaches and fixed dunes (CARVALHO; OLIVEIRA-FILHO, 1993), and the interior, dominated by "caatinga" vegetation, characterized by thorny, deciduous, woody and herbaceous species of low height (SAMPAIO et al., 1995).

Taxonomic treatment
The morphologic analyses were based on specimens obtained in Paraíba during the study, complemented by examination of exsiccates deposited in the Herbarium Jaime Coelho de Moraes (EAN) and Herbarium Lauro Pires Xavier (JPB), both in the State of Paraíba, and by consulting types and original descriptions.The herbaria acronyms followed Thiers (2014) and taxonomic identifications for genus and species levels were based on specialised literature (ENGLER, 1897a;KUIJT, 1978KUIJT, , 1986KUIJT, , 2007KUIJT, , 2009;;REIF;ANDREATA, 2011) or by analysis of specimens deposited in the previously mentioned herbaria.
The descriptions were given following the model of the "Flora Fanerogâmica do Estado de São Paulo' (FFESP).The works of Hickey et al. (1973) and Weberling (1989) were adopted to standardize the morphological terms.An identification key was prepared for the species and also a set of data on the geographical distribution, flowering and/or fructification was provided.
Plants shrubs, sub-shrubs, and lianaceous or erect.Haustorial hemiparasites which insert themselves into the host's vascular system.Stem cylindrical to angular.Leaves simple, cross-opposite or distichously, rarely alternate or verticillate, eucamptodromous or acrodromous.Inflorescences composed of dyads, triads or monads grouped in spikes or racemes, found in the leaf axils or solitary.Flowers unisexual or bisexual, 4-5-6-merous, bracteates or not; epicalyx entirely in the form of a sheath; androecium isomerous, stamens epipetalous, stigma and style undivided.Berries monospermic.

Habitat and distribution
The plant densely infests the host, and more than one specimen may be found on the same host or on different hosts of the same species.The plants are characterised by epicortical roots, filaments with depressions accommodating anthers, which are basifixed, and also by the presence of rufousfurfuraceous scales.In the state of Paraíba, it was predominantly found in areas of the Atlantic Forest.It commonly occurs on fruit trees and ornamental plants, found mainly in urban spaces, especially on Terminalia catappa L. (Combretaceae).

Phenology
Flowered and fructified in February, April and September.

Habitat and distribution
Psittacanthus cordatus usually shows more than one specimen on a single host, but none in neighbouring plants.It is morphologically characterised as a plant devoid of epicortical roots, leaves sessile, crassous, base cordate, and by inflorescences in racemes of triads with the corolla intense orange.The species is common in "caatinga" areas and, in current research, it was found in the region called 'Cariri Paraibano', one of the driest areas of the state, with a predominance of the shrubby "caatinga".In Brazil, it is found in the states of Amazonas, Pará, Rondônia, Tocantins, Bahia, Ceará, Paraíba, Pernambuco, Piauí, Rio Grande do Norte, Sergipe, Goiás, Mato Grosso do Sul, Mato Grosso, Minas Gerais, Rio de Janeiro and São Paulo (CAIRES; DETTKE, 2014).The species was recently cited by Melo et al. (2011) for the state of Paraíba, Brazil.

Habitat and distribution
The species is recognizable, particularly, due to the trichotomous papillae on the branches, which characterize the specific epithet as well as by the 4merous flowers, smaller than 4 cm in length.Moreover, it presents inflorescences with contracted internodes, differentiating it from the other representatives of the family in Brazil.In the state of Paraíba, it was recorded only in more humid areas at altitudes above 500 m.This species was first treated in the genus Struthanthus as S. pubescens Rizzini (1980); recently Caires et al. (2012) included it in the genus Pusillanthus.In Brazil it has been found in the States of Bahia and Paraíba (CAIRES; DETTKE, 2014).

Phenology:
Flowered in June and July.
Plants glabrous or pilose; epicortical roots present or not along the stem, between the internodes or at the base of the branches.Stem erect or scandent, cylindrical or angular when young, when adult, generally with brown lenticels.Leaves opposite or sub-opposite, distichously, petiolate.Inflorescences in racemes, spikes, corymbs or glomerules of triads, bracteates, axillary to terminal.Flowers 0.5-1 cm in length, sessile pedicellate, unisexual or bisexual, corolla 4-6-merous; stamens longer than they are wide, male flowers bearing dimorphic stamens, 3 major and 3 minor alternating with each other, anthers versatile dorsifixed; female flowers with nectar glands encircling the atrophied gynoecium and androecium.Fruits elliptical, endosperm present.

Habitat and distribution
There are three reports on Struthanthus calobotrys in Brazil, including the type collected by Sellow in the state of Bahia.Morphologically, it is strongly characterised by epicortical roots, leaves with petioles of 1.5-2 cm in length, leaf blade strongly opaque, which often makes the stomata obvious to the naked eye, and a cylindrical axis of inflorescences.It is associated with areas of Atlantic Forest in the state of Paraíba, on the coast and in humid forest enclaves "brejos de altitude".The species is restricted to Brazil, only found in the states of Bahia and Paraíba (CAIRES; DETTKE, 2014).

Habitat and distribution
Occasional parasite usually found associated with coastal tableland "tabuleiro" vegetation.According to Reif and Andreata (2011), it is commonly characterized by inflorescences in spikes, stems densely lenticellate and leaves lanceolate.However, in current study, the leaf blade ovate with acuminate apex was also observed.The main distinctiveness lies in inflorescences in spikes of compressed axis, since the other species of the family studied have inflorescences with cylindrical or angular axis.

Habitat and distribution
The plants usually show more than one specimen per host, less frequently found in other neighbouring specimens, commonly associated with shaded areas.It is characterised by petioles 0.8-1 cm in length, compressed axis of inflorescence, and also by staminodes with compressed thecae.In the state of Paraíba, it has been reported in areas of the Atlantic Forest mainly in humid forest enclaves "brejos de altitude", in urban space.In Brazil, Struthanthus cuspidatus may be found in the States of Bahia, Paraíba, Pernambuco, Piauí, Minas Gerais and Rio de Janeiro (CAIRES; DETTKE, 2014).

Habitat and distribution
The plants are heavily branched, with branches protruding from the host, occupying almost the entire crown.Species easily recognised by presentation of leaf blade obovate, emarginated and acute apex, as well as by inflorescences in corymbs of triads and an abundance of epicortical roots along the branches.In Paraíba, it was recorded exclusively in "caatinga" regions.According to Krause (1922), it is frequently found on specimens of Rapanea Aubl.Stem flattened when young, cylindrical in adults, brown, with few lenticels; internodes 4.5-5 cm in length.Leaves cross-opposite to rarely sub-alternate, petiolate; petiole 1.5-2 cm in length; blade oblonglanceolate, (4-)6.5-7× 2.5-3 cm, apex acute to acuminate, base obtuse to cuneate, eucamptodromous, yellowish green, semi-coriaceous.Inflorescences in racemes of aggregate triads in the terminal portion of the branch, 6-7 cm in length, 4 pairs of triads per inflorescence, axis of inflorescence compressed to tetragonus, bracts acute-dentate with the middle bracts being larger than the lateral bracts.Flowers sessile, buds clavate; epicalyx green; corolla 6-merous, 0.4-0.5 cm in length, greenish, valvate; stamens-6, majors 0.6 × 0.1 cm, minors 0.4 × 0.1 cm, included; ovary inconspicuous with ca.0.1 cm in length; style cylindrical, 0.3-0.4cm in length.Fruit not observed.

Habitat and distribution
Plants with branches protruding from the host, but sparsely branched, presenting small volume and never reaching neighbouring hosts.As noted by Reif and Andreata (2011), the species is easily recognisable by leaf blades with an acute apex and acute-dentate bracts, the middle bracts being bigger in size than the lateral ones.In the study area, it is commonly found on rocky outcrops, also occurring in areas of Atlantic Forest and "caatinga".In Brazil, it has been recorded in the States of Acre, Bahia, Ceará, Paraíba, Mato Grosso, Goiás, Minas Gerais and Rio de Janeiro (CAIRES; DETTKE, 2014).

Phenology
Flowered in January and from August to November.

Conclusion
Ten species and four genera were reported for the state of Paraiba, with Struthanthus concinnus representing a new record for the state's flora.The main features used for the separation of the species comprised presence or absence of epicorticais roots, distribution of the lenticels in the branches, leaf apex format, types of inflorescences, and number of inflorescences per axil and position of anthers.The number of representatives found and the vegetative and reproductive morphological features highlighted for species recognition of Loranthaceae evidence the importance of current study for the family and also on other mistletoe groups in the State of Paraiba.

Figure 7 .
Figure 7. Struthanthus syringifolius. A. Habitat.B. Reproductive branch.C. Arrangement of triads.Plants semi-erect, sparsely branched and leaved.Epicortical roots found only at the base of the plant.