Flora of Ceará, Brazil: Clusiaceae

Abstract The floristic-taxonomic survey of Clusiaceae is presented as part of the project “Flora of Ceará: knowing to conserve”. The study was based on the analysis of specimens deposited in national and international herbaria and observations of natural populations during field expeditions carried out from February, 2019 to March, 2020. The family is represented in Ceará by eight species distributed in four genera: Clusia, Garcinia, Symphonia and Tovomita. Clusia was the most representative with five species: C. ibiapabensis, C. melchiorii, C. nemorosa, C. nogueirae and C. panapanari. The other genera are represented by one species each: Garcinia gardneriana, Symphonia globulifera and Tovomita mangle. The species preferentially occur in humid environments such as Dense Ombrophilous Forest and near watercourses. Clusia ibiapabensis and C. nogueirae are endemic to Ceará, and C. melchiorii and S. globulifera are new records for the state. Only Clusia nemorosa and C. panapanari were recorded in conservations units. Identification keys, descriptions, taxonomic relationships, illustrations, and comments on the geographical distribution and phenology of the species are presented.


Introduction
Clusiaceae, included in the order Malpighiales, comprises 15 genera and about 800 species with tropical distribution, and is more diversified in the Neotropical region (Stevens 2001 onwards;Marinho et al. 2019).Its species can be found in a wide variety of environments, from wetter regions of tropical forests to xeromorphic environments (Gustafsson 2009(Gustafsson , 2010;;Marinho et al. 2020a).
The family is characterized as mainly trees, shrubs or hemiepiphytes, glabrous, evergreen, with secretory ducts; leaves simple, opposite, entire, secondary veins generally parallel and often united to an intramarginal vein; flowers solitary or in terminal or axillary inflorescence; flowers bisexual or unisexual, actinomorphic; sepals two to five (-numerous), free or united; petals four to eight, free; stamens four or more, free or fused in synandrium or staminal tube; nectariferous disc can be present or absent, staminodes can be present or absent in pistillate and staminate flowers, with or without resin secretion; ovary superior, 2-multilocular, with one to numerous ovules per locule, placentation usually axillary, rare parietal or basal; free or united styles, usually permanent on the fruit; fruit berry or fleshy capsule, with one to numerous seeds which are arillate or not (Stevens 2001(Stevens onwards, 2007;;Bittrich 2003).
In Ceará, Clusiaceae is mentioned only in regional floristic surveys, such as Loiola et al. (2015) in Chapada do Araripe, in the southern portion of the state; Loiola et al. (2020) in the catalog of angiosperm diversity in Ceará; Silveira et al. (2020a) in a field and herbarium survey of the phanerogamic flora of the Ubajara National Park, and Silveira et al. (2020b) in the flora of Serra de Baturité.In addition, two new species of Clusia Linnaeus (1753: 510) were recently described based on specimens from the Ibiapaba plateau, C. ibiapabensis A.C. Alencar & A.S. Farias-Castro (2020: 262) and C. nogueirae A.C. Alencar & A.S. Farias-Castro (2020: 260).As part of the project "Flora do Ceará: knowing to conserve", this study aimed to carry out a taxonomic treatment of Clusiaceae, with updates of identifications and geographic distribution of the species, using taxonomic descriptions, identification keys, illustrations and maps, as well as taxonomic and phenological comments, thus contributing to the knowledge of the group and the diversity of the flora of Ceará.

Material and Methods
The study was based on the analysis of specimens of Clusiaceae from the ALCB, ASE, EAC, HCDAL, HDELTA, HUEFS, HURB, HUVA, IPA, MO, NY, R, UEC and UFP herbaria collections (acronyms according to Thiers, continuously updated), and also from HST (not indexed, Recife, Pernambuco).Fresh material was collected during field expeditions carried out between February, 2019 and March, 2020.Author names follow Flora e Funga do Brasil 2020 (continuously updated) Project.Morphological terminology was based on Radford et al. (1974) and Harris & Harris (2001).Data on habits, habitat, phenology and popular names were obtained from exsiccate labels.When the samples collected in Ceará were insufficient for the description or illustration of the species, additional materials from other states were used.
Clusia melchiorii is endemic to Brazil, with records for the northeastern (Bahia and Pernambuco) and southeastern (Espírito Santo) regions (Marinho et al. 2020b).Clusia melchiorii is recorded here for the first time in Ceará, in areas of Dense Ombrophilous Forest (Fig. 1).

Clusia nemorosa
Clusia nemorosa was found throughout many phytophysiognomies and countries of South America, with records in Brazil, Guyana, French Guiana, Suriname and Venezuela (Tropicos 2020).In Brazil, it has records in all regions, except for the South (Nascimento Jr. & Alencar 2020).In Ceará, C. nemorosa was recorded at altitudes varying between 475-935 m, in Dense Ombrophilous Forest, Savanna, Steppic Savanna (Carrasco), Forested Savanna, transition areas of Steppic Savanna and Savanna and Semi-deciduous Seasonal Forest (Fig. 1).The species was collected in Ubajara National Park.
The species was collected with flowers in February, March, June, August, September, and October and with fruits in January, February, March, April, July, August, September, October, November, and December.

Clusia nogueirae
Rodriguésia 74: e01132022.2023 0.5 × 0.2 cm, resiniferous.Capsules 2-3.3 × 1.2-2.9cm, 5-valvar, oblong, elliptic or asymmetrical; sepals, petals and staminodes caducous, stigmas persistent.Seeds with aril present.C l u s i a n o g u e i r a e h a s a s p e c u l i a r characteristics since the staminate flower forms a conical, crateriform, circular synandrium, numerous compacted stamens, tiny and resincovered around a well-developed pistillode.It can be confused with C. ibiapabensis due to the general appearance of the branches, which are not carenate and not escrobiculate, but it differs by the number of stamens (ca.200 stamens fused in a synandrium vs. ≤ 35 free and clavate stamens in C. ibiapabensis).
The species was collected with flowers and fruits in January.
Garcinia gardneriana occurs in Brazil and, according to Mouzinho et al. (2022Mouzinho et al. ( , 2023)), the species is restricted to the Atlantic Forest.In Ceará, the species was recorded in Dense Ombrophilous Forest and Steppic Savana (Carrasco) (Fig. 6).
The species was collected with flowers in October and fruits in January, March, April, August, November, and December.
Garcinia gardneriana is known as Bacupari.The species has edible fruits that are consumed as juices or fresh, in addition to being a food source for capuchin monkeys and agouti (Guimarães et al. 2004).
Symphonia globulifera occurs in Argentina, Belize, Bolivia, Brazil, Caribbean, Colombia, Costa Rica, Ecuador, Guyana, French Guiana, Guatemala, Honduras, Madagascar, Mexico, Panama, Peru, Suriname and Venezuela (Tropicos 2020).In Brazilian territory, it has records for all regions of the country, with the exception of the South (Muniz 2020).In Ceará, the species was recorded in vegetation with fluvial-lacustrine influence in only one municipality (Fig. 7).
The species was collected with flowers in September.
Tovomita mangle can be distinguished from other species of Clusiaceae from Ceará by the few secondary veins (9-10 pairs) and small floral buds (0.6-0.11 cm long) totally covered by the sepals.The capsule fruit is similar to those of Clusia but has only one seed per locule.
Tovomita mangle is an endemic species of the Brazilian Atlantic Forest, often found in forest plains and Lowland Semi-deciduous Forest, and is generally associated with watercourses (Marinho et al. 2016).In Ceará, T. mangle was recorded only in highland environments in Dense Ombrophilous Forest (Fig. 7).
The species was collected with floral buds in September and October, and fruits in March.

Figure 4
Figure 4 -a-d.Clusia nemorosa -a.branch with cymes; b. staminate flower; c. stamen with lateral anther and connective exceeding the thecae; d. detail of the vein of the leaf abaxial surface.e-h.Clusia nogueirae -e.branch with floral buds; f. staminate flower; g. pistillode detail; h.detail of the vein of the leaf adaxial surface.(a-d.Loiola et al. 1950; e-h.Castro 2786).

Figure 5
Figure 5 -a-c.Clusia panapanari -a.branch with fruits; b. staminate flower; c. detail of the vein of the leaf adaxial surface.d-f.Garcinia gardneriana -d.branch with axillary flowers; e. side view of fruit; f. detail of the vein on the leaf adaxial surface.(a-c.Ferreira 113; d-f.Silveira (EAC 41636).

Identification key for Clusiaceae species in Ceará
. Clusia melchiorii and Symphonia globulifera are new records for Ceará, and C. ibiapabensis and C. nogueirae have so far only been recorded in the state of Ceará.Clusia nemorosa and C. panapanari are the species with the widest distribution in Ceará and both occur in the Ubajara National Park.There are few records of Clusiaceae species in conservation units, which demonstrates the need for studies that focus on the conservation status of the Clusiaceae family in the state of Ceará.In Ceará, the representatives of Clusiaceae occur, preferentially, in humid environments (Dense Ombrophilous Forest), and are generally registered in the mountains of Guaramiranga, Baturité and Maranguape.However, there were records in dry environments such as Savanna (Cerrado), Steppic Savanna (Carrasco) and in the Vegetation Complex of the Coastal Zone in the Lowland Semi-deciduous Forest = (Mata de Tabuleiro).Trees.Branches woody, not carenate, not escrobiculate, not striate.Petioles 0.5-1.2cm long, colleters absent.Leaf ................. 1. Clusia ibiapabensis 1. Clusia ibiapabensis A.C. Alencar & A.S. Farias-Castro, Phytotaxa 460(4): 262.2020.Figs.1; 2a-b; 3a-e