New records of Annonaceae in the Northeast Brazil

This study reports nine new records of Annonaceae for the states of Alagoas, Ceará, Paraíba and Pernambuco, in Northeastern Brazil: Duguetia lanceolata A.St.-Hil., D. ruboides Maas & He, D. sooretamae Maas, Guatteria tomentosa Rusby, Hornschuchia bryotrophe Nees, Pseudoxandra lucida R.E.Fr., Trigynaea duckei (R.E.Fr.) R.E.Fr.., Unonopsis guatterioides (A.DC.) R.E.Fr., and Xylopia ochrantha Mart. Descriptions, taxonomical and distributional comments, photos of diagnostic characters, geographic distribution maps and two identification keys, one of the genera of Annonaceae occurring in the Atlantic Forest and Caatinga and another for the new Duguetia records, are provided.


Introdution
Annonaceae is a pantropical family of flowering plants, with its highest richness and genus-level endemism in the Neotropical region (Doyle & Le Thomas, 1997;Chatrou, Rainer & Maas, 2004). It comprises about 2500 species distributed in 109 genera (Rainer & Chatrou, 2006;Chatrou, Turner, Klitgaard, Maas & Utteridge, 2018;Chaowasku et al., 2018aChaowasku et al., , 2018b. In Brazil, approximately 385 species and 30 genera are recorded, most of which occur in lowland tropical wet forest, such as those in the Atlantic Forest domain (Chatrou et al., 2004;BFG, 2018). However, some species of the family also grow in drier areas, as those found in the Caatinga.
The family is characterized as shrubs or trees; with simple, alternate leaves, generally distichous; absence of stipules; trimerous flowers, with one whorl of sepals and two whorls of petals; stamens and carpels usually numerous; and apocarpous to syncarpous fruits (Kessler, 1993). Among Annonaceae genera present in Brazil, Xylopia Aubl. Xylopia (ca. 200 spp.) is the only pantropical genus of the family, identified by the dehiscent fruit with six types of aril morphology, usually forming a complete ring around the micropyle, and the presence of sarcotesta on the seeds in many species, structure unknown in other Annonaceae (Stull et al., 2017;Johnson & Murray, 2020). Duguetia (95 spp.) presents African and Neotropical species, being recognized by the presence of stellate hairs, scales or both in young twigs, leaves and reproductive organs, and woody-fleshy syncarpous fruits (Maas, Westra & Chatrou, 2003;Bazante & Alves. 2017). Guatteria (ca. 180 spp.) is restricted to the Neotropics and recognized by pedicels with suprabasal articulation and apocarpous fruits (Maas et al., 2015;Maas et al. 2019). Like the last one, Pseudoxandra R.E.Fr., Unonopsis R.E.Fr., and Hornschuchia Nees. are also restricted to the Neotropical region. Pseudoxandra (24 spp.) is characterized by leaves with adaxially raised midrib, pedicels with 3-5 bracts, and imbricate petals . Unonopsis (48 spp.) also presents an adaxially raised midrib, but differs by pedicels with two bracts and valvate petals (Maas, Westra & Vermeer, 2007).
i i Hornschuchia (10 spp.) is restricted to the Atlantic Forest of eastern and southern of the Brazil and identified by flower buds long-conic, linear petals and presence of few stamens (Johnson & Murray, 1995). Trigynaea Schltdl. (8 spp.) is very similar morphologically to Hornschuchia, but is differentiated by flower buds globose to ovoid, ovate to elliptic petals, and by generally presenting triplinerved leaves at the base (Johnson & Murray, 1995).

Materials and Methods
Monthly excursions were carried out between 2016 and 2018 in areas in the Atlantic Forest, Caatinga domains, and in enclaves of Cerrado surrounded by Caatinga, presents in the states of Alagoas, Ceará, Paraíba, Pernambuco and Rio Grande do Norte. However, none of the taxa presented here have been registered for Rio Grande do Norte. Collected samples were processed according to Peixoto & Maria (2013) and incorporated into UFP herbarium, with duplicates sent to PEUFR. Apart from the field excursions, the following herbarium were analyzed: EAC, EAN, HUEFS, HVASF, IPA, JPB, MAC, PEUFR, UFP, UFRN (acronyms follow Thiers, 2018). Identifications were based on the specialized literature (Dias, 1988;Johnson & Murray, 1995;Maas et al., 2015). Morphological comparisons were conducted with type specimens and images available online at Jstor (https://plants.jstor.org/) and Brazilian Flora Online (http://reflora.jbrj.gov.br/reflora/herbarioVirtual/).
The morphological descriptions are based on the measurements of the specimens in the study area, following the terminology of Harris & Harris (2001). They are included here because morphological variations were observed in some new records, better discussed in the topics of taxonomic notes.
In addition, the descriptions provide additional data about a little-known family in Northeast Brazil. Geographic coordinates in decimal degrees and UTM projection were obtained using herbarium material and the SpeciesLink database (http://www.splink.org.br). Maps were prepared using the software QGIS.org (2017).

Results and Discussion
During a study of the richness of Annonaceae in Northeastern Brazil, we found nine species of the genera presented above that had never been reported to the states of Alagoas, Ceará, Paraíba and Pernambuco: Duguetia lanceolata A.F.C.P., D. ruboides Maas  Based on the importance of documenting species' distributions and their distribution patterns, morphological and ecological profile, in addition to increasing the floristic knowledge for making conservation decisions, we hereby discuss these new records.
Distribution notes: Duguetia lanceolata is endemic to Brazil and previously described as occurring in the Cerrado and Atlantic Forest domains, in lowland to montane forests from Goiás, in the Central-West region, to Rio Grande do Sul, in the Southern region (Maas, Kamer, Mello-Silva & Rainer, 2001). The species has been recorded for the Cerrado domain in Ceará, in semideciduous and subperennial forests in elevations of 760 m (Maas, Maas-Van de Kamer, Mello-Silva & Rainer, 2001;BFG, 2018). We hereby confirm the occurrence of this species in the Atlantic Forest domain in Pernambuco, in the Caatinga in Alagoas, and in Atlantic Forest enclaves (Brejos de Altitude) and Cerrado vegetation within the Caatinga domain in Ceará and Paraíba.

Duguetia ruboides
Distribution notes: Duguetia ruboides is endemic to Brazil and previously believed to be restricted to the Amazon and Cerrado domains in the states of Maranhão, Pará and Piauí BFG, 2018). Recently, this species was recorded in Alagoas, but no voucher specimen or reference was cited (BFG, 2018). We could not confirm the occurrence record for Alagoas, but the distribution has now been extended to mountainous areas of the Caatinga in the states of Ceará and Paraíba, and to the Atlantic Forest in Pernambuco.
Distribution notes: Duguetia sooretamae was considered endemic to the state of Espírito Santo, restricted to a coastal muçununga forest region (forests with sparse tree cover in sandy, wet soils) at Reserva Natural Vale BFG, 2018). Here, we present its first record in the Northeast region, in the state of Paraíba, in an area with restinga vegetation in sandy soil.
Distribution notes: Guatteria tomentosa occurs from Central America to Southeast Brazil, almost covering the whole distribitional range. In Brazil, this species was earlier reported from the Amazon and Atlantic Forest domains in the states of Acre, Amazonas, Bahia, Espírito Santo, and Minas Gerais in lowland, restinga, submontane and montane forests. (Maas et al., 2015;BFG, 2018). Here, it is first reported in Alagoas, from a collection in ombrophilous forest with clayey and sandy soil.
Taxonomic notes: The only voucher with fruit does not have monocarps, preventing its description. This species can be recognized for its long-persisting indument of erect, stiff hairs throughout the plant, pedicels 3.8-6.5 cm long, and by flower buds slightly pointed (Maas et al., 2015). The material examined in Alagoas presents some variations according to the description by Maas et al. (2015), with leaves sparsely covered with hairs below (vs densely covered with hairs below), and basal margins flat (vs. often revolute).
Distribution notes: Hornschuchia bryotrophe is endemic to Brazil and the most widely distributed species of the genus, with records from Bahia, Espírito Santo, Minas Gerais and Rio de Janeiro, in wet forest and sometimes on sandy soils (Johnson & Murray, 1995;BFG, 2018). It is now also recorded in Atlantic Forest remnants in Pernambuco, close to the coast, as most of the records of this species.
Distribution notes: Pseudoxandra lucida was previously reported throughout the Amazon region in Brazil and Guyana, in lowland forests in elevations up to 250 m BFG, 2018). It is registered here for the first time in the Atlantic Forest domain of Northeastern Brazil, from a collection in the state of Alagoas. The specimen was collected in dense montane ombrophilous forest, at elevation between 380-400 m.
Taxonomic notes: The species richness of Pseudoxandra grew considerably throughout the taxonomic treatments (Fries, 1937;Maas, Heusden, Koek-Noorman, van Setten & Westra, 1986;. As a result, complexes of similar species morphologically need to be further analyzed, as is the case of P. lucida and Pseudoxandra polyphleba (Diels) R.E.Fr. They share leaves densely to rather densely verruculose, glabrous, distance of marginal vein from margin 1-2 mm, and monocarps globose, with thin wall. But they differ mainly by the flowers, being larger and hairy in P. lucida, and small and glabrous in P. polyphleba . However, as in most collections of this genus, the only specimen collected in the study area does not have flowers. Thus, the voucher was identified as P. lucida by the coriaceous leaves (vs chartaceous), shiny above (vs not shiny), and monocarps with smooth surface in sicco (vs often shrivelled surface in sicco) . Furthermore, P. lucida resembles Pseudoxandra bahiensis Mass, which is endemic to Bahia, by the narrowly oblong-elliptic, densely verruculose leaves, with the leaf base sometimes presenting angular projections, and globose monocarps. The main difference between the two species is the thinner fruit wall, ca. 0.2 mm thick (vs 1.2-1.8 mm). The new record is also highly variable and slightly aberrant due to the long stipes, which usually are 4-10 mm long, being more similar to collections from Peru and Colombia  but fits with respect to all other characteristics.
Distribution notes: Trigynaea duckei is the species with the widest and most discontinuous distribution of the genus (Johnson & Murray, 1995;Lobão, 2017). It occurs in the Amazon and Caatinga domains of north and northeast of Brazil, in the states of Pará, Maranhão and Piauí, and then into Venezuela, Ecuador, Peru and Bolivia, in elevations between 60-1500 m (Johnson & Murray, 1995;BFG, 2018). The occurrence of this species in the state of Ceará is hereby confirmed. The specimen was collected in the interior of the Serra de Uruburetama forest, which is considered a 'Brejo de altitude' (Atlantic Forest remnants in higher elevations in the caatinga), with elevation of 928 m.
Taxonomic notes: Only a single voucher of this specimen was found in the study area, without flowers, with young fruits and seeds destroyed by insects, which made identification difficult. In addition, the voucher has morphological differences based on the literature (Johnson & Murray, 1995), such as the presence of 2-6 monocarps per fruit (vs 1-2), sessile (vs stipes 1.5-6 mm long), and 3-4 seeds per monocarp (vs 6-11). However, the specimen was recognized as Trigynaea duckei by leaves surface smooth, distinctly triplinerved, midrib flat above, internodal and apocarpous fruits with pedicel 2-5 mm long, calyx persistent into a cup-shaped, and monocarps finely warty.Trigynea, Bocagea A.St.-Hil. and Hornschuchia Nees form a clade within the Bocageeae tribe, and show some similarities as the sepals persistent on fruit, low numbers of stamens, and small torus diameter (Johnson & Murray, 1995). Among these two genera, Trigynaea is more similar to Hornschuchia for sharing small flowers with connate sepals and carunculate seeds. Considering the ten species of Hornschuchia, T. duckei is more similar to H. lianarum D. M. Johnson by fruiting pedicels 2-5 mm long, monocarps globose to ellipsoid and sessile (Johnson & Murray, 1995). It differs from that species by elliptic to narrowly-obovate leaves (vs ovate to broadly ovate), distinctly triplinerved (not triplinerved), monocarps apex umbonate (vs rounded) and finely warty (vs rugose).
Distribution notes: Unonopsis guatterioides has a wide distribution in the Amazon region of South America. It also occurs in other Brazilian regions, in the Amazon, Cerrado and Atlantic Forest domains (Maas et al. 2007). We hereby present the first record of the genus for the states of Alagoas and Pernambuco, collected in submontane ombrophilous forests, in elevations of 150-750 m.
Distribution notes: Xylopia ochrantha is endemic to Brazil and described as restricted to areas of restinga and ombrophilous forests in Bahia, Espírito Santo and Rio de Janeiro (Dias, 1988;BFG, 2018). According to BFG (2018), this species possibly occurs in Pernambuco, but no voucher or reference is cited. Here, we expand the geographic distribution of the species to the states of Alagoas and Pernambuco. It was collected in dense ombrophilous forest fragments and subperennial forests.
Taxonomic notes: This species is well defined by its cauliflory, a rare characteristic in Xylopia species in the Atlantic Forest, and by the dense indument of golden hairs in flowers and fruits (Dias, 1988). Only one other species of Xylopia presents cauliflory in the Atlantic Forest and Caatinga domains, X. decorticans Johnson & Lobão, which differs from X. ochrantha by the flaking bark in the twig branches and considerably larger leaves (9-24 cm long) (Lobão & Johnson, 2007;BFG, 2018).

Conclusion
According to the recent literature, 37 species of Annonaceae are recorded in the concerned states, with 23 species in Alagoas and Pernambuco, 20 in Ceará, and 18 in Paraíba. Duguetia, Guatteria and Xylopia were previously recorded in these states, unlike the other genera presented here (Pontes, Barbosa & Maas, 2004;Lyra-Lemos, Mota, Chagas & Silva, 2010;Nusbaumer et al., 2015;Bazante & Alves, 2017;BFG, 2018). According to our results, the diversity of Annonaceae is expanded in these states, now presenting 28 species in Alagoas and Pernambuco, 22 in Ceará, and 21 in Paraíba. Additionally, we present the first record of the genus Trigynaea in Ceará, Hornschuchia and Unonopsis in Pernambuco, and Pseudoxandra and Unonopsis in Alagoas.
With the exception of Guatteria tomentosa, Pseudoxandra lucida, Trigynaea duckei and Unonopsis guatterioides, all other new records are endemic to Brazil. Furthermore, we present the first record of P. lucida in the Atlantic Forest domain of Northeastern Brazil, and of Duguetia ruboides for the Caatinga and Atlantic Forest domains. These new records support a previously detected Amazonian-Atlantic Forest disjunction, with relicts of that connection through the Brejos de Altitude in the Brazilian Northeast (Andrade-Lima, 1953;Rizzini, 1963). Expanding the geographical distribution of Annonaceae species in the Northeast of Brasil helps to update information on endemism patterns, morphological characteristics and conservation status, all of which are essential in the creation of measures for species preservation and management (Mace, 2004). Thus, the new records presented here improve our understanding of the flora of Northeastern Brazil and they also reinforce the importance of keeping the collections up to date, since many identification errors were found and, as a result of this work, important contributions to the knowledge of these species are presented here. In addition, it also demonstrates the importance of better collection efforts in the Caatinga and Atlantic Forest remnants in the region, due to the fragmented and under-sampled vegetation.