Myrtaceae Juss. in restinga of Bahia: diversity, taxonomy, and distribution

ABSTRACT Myrtaceae has ca. 6,000 species, distributed into 140 genera with Pantropical distribution. The family is one of the five most representative flowering plants in species richness in Brazilian restinga and is also of great importance for the maintenance of the ecological cycles of this vegetation. However, few studies focus on Myrtaceae in restinga, mainly in the State of Bahia, which has the country's largest coastal extension. This study aims to present the first taxonomic study of Myrtaceae from the restinga of the State of Bahia, Brazil. A total of 10 field trips were performed from September 2016 to April 2019, and the most relevant herbaria of Brazil were consulted. A total of eight genera and 85 species of Myrtaceae were identified in the Bahian restinga. Myrcia was the most representative genus with 42 species, followed by Eugenia (23 spp.), Psidium (seven spp.), Campomanesia (five spp.), Myrciaria (four spp.), Neomitranthes (two spp.), and Blepharocalyx and Calycolpus (a single species each). Two of them represented new species to science, and four presented the first records to the studied area. The distribution patterns among the Brazilian biomes and the restinga phytophysiognomies are discussed, also a checklist, identification keys, and photographic plates are provided.


Introduction
Myrtaceae is the eighth most diverse family of angiosperms worldwide, with 6,000 species distributed into 140 genera (Lucas et  Myrteae is represented by 23 genera and 1,025 species in Brazil and are characterized by opposed leaves with translucid punctuations, white flowers (rarely pink, reddish to purple), petals free, 4-5 (rarely absent), stamens numerous (rarely fewer), ovary inferior, fruit berry with 1 to several seeds, with persistent or deciduous calyx; when the calyx is deciduous, it leaves a scar on the fruit ( ).This family is also of great importance for the maintenance of the ecological cycles of this vegetation, being an important food source for local fauna due to producing fruits throughout the year, especially on months with low availability of fleshy fruits produced by other plant families (Staggemeier et al. 2017).
Restinga comprises a mosaic of different phytophysiognomies with distinct floristic elements occurring over sandy deposits along the coast, mainly formed by marine regressions and transgressions during the quaternary period (Araujo & Henriques 1984;Araujo 1992).These sandy deposits are affected by the wind and sea-level oscillations, which is reflected in the phytophysiognomy diversity in restinga, including animal and plant richness (Araujo & Pereira 2009).Along the Brazilian coast, restinga discontinuously occurs over the coastal plains from ca. 4° N to 33° S, totalling 7,400 km in extension (IBGE 2004).
Even though Myrtaceae shows great diversity in Brazilian restinga, most of its current studies are restricted to checklists through generalist inventories ( Thus, this study presents the first taxonomic study of Myrtaceae from the restinga of the State of Bahia.A checklist, identification keys, photographic plates, taxonomic, biologic, and distribution comments of the species are presented.

Restinga and its phytophysiognomies in the State of Bahia
Restinga phytophysiognomies are discontinuously found along the coast of the State of Bahia throughout an extension of 1,120 km.Together, these phytophysiognomies form ecosystems associated with the Atlantic Forest biome bordered by mangroves, rivers, and forest patches along the Bahian coast (Martins 2012; Gomes & Guedes 2014; Matos et al. 2017).In some municipalities, such as Caravelas, Alcobaça, and Nova Viçosa, the restinga vegetation inhabits up to 20 km of inland coastal plains; in contrast to Itacaré and Ilhéus in which vegetation occupies narrow sand patches (Martin et al. 1980).

Restinga classification
To classify the restinga phytophysiognomies, we followed the definitions of Araujo & Pereira (2009) Phytophysiognomies identification occurred during field trips and by verifying the locality information on the labels from all analyzed specimens.Since most collectors used different classifications to name restinga phytophysiognomies over time, it was imperative to standardize all names that were grouped into the six phytophysiognomies: 1) DF, including the terms "forest of restinga" and "arboreal restinga"; 2) FRF, including "tall restinga with marshes" and "flooded restinga" (not observed during fieldwork, but recorded from the vast literature (Matos 2014; Thomas 2003; Dias & Soares 2008) and herborized specimens; 3) ST, including "open restinga", "restinga patches", "thickets and shrubs over dunes", "shrubby dunes", "herbaceous shrubby restinga", and "low restinga"; 4) DS, including "shrubby-arboreal restinga" and "dense shrubby restinga"; and 5) FS, including "shrubby restinga with marshes", "thickets and flooded herbaceous restinga", and "flooded thicket restinga".6) HPR, which had no evidence of Myrtaceae neither described in the literature nor on herborized or during field trips.Finally, for specimens with only the word "restinga" recorded as the phytophysiognomy of occurrence, we classified them as non-identifiable phytophysiognomy (NI).Additionally, we named "anthropized restinga" (AR) when the labels of the specimens indicated the terms "altered", "anthropized", "degraded", and "disturbed" restinga (see species distribution presented in Table 1).Taxonomy A total of 10 field trips, lasting from three to seven days each, were performed in seven municipalities of the State of Bahia (Conde, Ilhéus, Itacaré, Ituberá, Maraú, Mata de São João, and Una) from September 2016 to April 2019 (Fig. 2).Specimen collections were made following usual methods (Peixoto & Maia 2013) during walks in all different restinga phytophysiognomies.All specimens were processed, dried, and included in the Alexandre Leal Costa Herbarium (ALCB), with duplicates sent to the Universidade Estadual de Feira de Santana Herbarium (HUEFS).For taxa identification, we consulted specialized literature, besides analyzing type specimens, e-types, and their protologues.(2014).Measurements were taken from dried specimens and are presented as length x width.Species distribution was obtained from specimen labels, protologues, and online databases such as Flora e Funga do Brasil 2020, GBif (https://www.gbif.org/)and SpeciesLink (https:// specieslink.net).The distribution map was generated on QGIS (QGIS Development Team 2022).

Diversity of Myrtaceae in restinga of the State of Bahia
A total of eight genera and 85 species of Myrtaceae were identified in the restinga of Bahia, with ten of them endemic to this State, 45 species endemics to the Atlantic Forest biome, and six species endemics to restinga vegetation (Table 1

Distribution patterns
Four distribution patterns were identified within the Myrtaceae from restinga of Bahia state (Fig. 3): 49 species (58%) are endemic of the Atlantic Forest biome (AF); 17 species (19%) occur widely distributed in Brazil (WID); 16 species (19%) occur in the Atlantic Forest biome and Central Brazil, besides the Caatinga and Cerrado biomes (ACC); and three species (4%) occur disjunct between the Atlantic and Amazon Forests (AAM).
Previous floristic studies evidenced that restinga phytophysiognomies are colonized by plants from their surrounding biomes, such as the Atlantic Forest, Caatinga, Cerrado, and even the Amazon Forest.It reflects the species occurring among these Biomes and the low endemism rate found in restinga (Scarano 2002 M. neoregeliana, M. polyantha, Psidium brownianum, P. cattleyanum, and P. oligospermum).This pattern is probably related to the geographical proximity of the Bahian restinga to the Caatinga biome instead of the Cerrado Biome (Fig. 2).
Most species of Myrtaceae found in restinga of Bahia are endemic to the Atlantic Forest, similar to previous studies (Assis et al. 2004).This pattern is expected since most of the Brazilian restinga is associated with and heavily influenced by this biome (Cerqueira 2000).
The Atlantic Forest biome comprises more than half of the species of Myrtaceae from Brazil (692 spp.Eugenia punicifolia, Myrcia guianensis, M. splendens, M. tomentosa, Myrciaria floribunda, and Psidium guajava are widely distributed (WID) and occur in all Brazilian biomes, from humid to dry vegetation, bearing remarkable morphological plasticity in leaf size, texture, and indument.

Diversity of Myrtaceae among different restinga phytophysiognomies
Analyzing species distribution of Myrtaceae among restinga phytophysiognomies in the State of Bahia we could see that 68 species (45% of the total) are found in DF, with 31 species exclusive of this phytophysiognomy (Fig. 4).This result shows the importance of Myrtaceae for forested physiognomies within restinga dry forests (Assumpção & Nascimento 2000;Matos 2014).
Only six species were recorded in flooded restinga; four in the FRF phytophysiognomy, being Myrcia grazielae and Myrciaria glomerata restrict to it, and three species in the FS phytophysiognomy (Eugenia astringens, Myrcia neuwiedeana and M. splendens), with no exclusive species recorded.The low number of species occurring in flooded phytophysiognomies was also reported by Matos (2014), that showed soil flooding is a limiting factor for establishing species of Myrtaceae.
We have also noticed that some species of Myrtaceae occur in different portions of the Bahian restinga: 11 species (13%) are found in Northern restinga (above the municipality of Salvador), and 37 species (43%) only occur in southern restinga (below the municipality of Salvador) in the State of Bahia.Martin et al. (1980) and Matos (2014) pointed out that the floristic heterogeneity of northern and southern restinga in the State of Bahia might reflect   Key of Myrtaceae genera from restinga of Bahia (Fig. 5) Acta Botanica Brasilica, 2023, 37: e20220194 al. 2012; Govaerts et al. 2019) and two diversity centers, Australia and the Neotropics (Wilson et al. 2005).The tribe Myrteae comprises nine subtribes, 50 genera, and ca.2,500 species (Vasconcelos et al. 2017b; Lucas et al. 2019) and represents all the species diversity within this family in Brazil (Wilson et al. 2005; Lucas et al. 2007).This tribe is known for its taxonomic complexity due to the megadiverse genera Myrcia and Eugenia (Landrum & Kawasaki 1997), to its recent diversification age of ca.32.0 Ma, and mainly to the uniform floral morphology shared by its species (Biffin et al. 2010; Vasconcelos et al. 2017a; 2018).
, IBGE (2012), and Thomas (2003), and the nomenclature proposed by Dias & Soares (2008), as follows: 1) Non-Flooded restinga Forests (Dry Forests) (DF) (Fig. 1 A): occurring where the groundwater does not superficially surface, the soil is constantly humid during the dry season, and the upper layer comprises 15 to 20 m tall trees; 2) Flooded restinga Forests (FRF): occurring where the groundwater superficially surfaces most of the year, usually during the rainy season, and the upper layer comprises 15 to 20 m tall trees; 3) Shrub Thickets (ST) (Figure 1 B-C): occurring in mosaics of dense thickets, usually comprising different plant species of 4 to 6 m tall shrubs, interposed with open areas of white sand or herbaceous layer; 4) Non-Flooded Dense Shrubs (DS) (Fig. 1 D): showing relatively small shrubs (3 to 5 m tall), within a closed and dense physiognomy, mainly populated by species of Myrtaceae, without any interposed open area or with little herbaceous layer; 5) Flooded Dense Shrub/Herbs (FS) (Fig. 1 E-F): typically occurring in open areas alongside water streams in the coastal plain, surrounding lagoons and lakes where Cyperaceae and Poaceae are dominant; 6) Halophyte/ Psammophilous Reptant (HPR): herbaceous and subshrub formations, rhizomatous and reptant, mostly occurring alongside the coastal line influenced by higher tides.

Figure 2 .
Figure 2. A. Brazilian map.B. Coast of Bahia state; the highlighted municipalities are those sampled by collections.
; Castro et al. 2012; Fernandes & Queiroz 2015), corroborating our results (only six species).Of all species here classified as ACC, five of them only occur in the Atlantic Forest and Caatinga (Campomanesia ilhoensis, Eugenia schottiana, Myrcia arenaria, M. bergiana, and Myrciaria pilosa), two only occur in the Atlantic Forest and Cerrado (M.ilheosensis and M. racemosa), and nine occur in the Atlantic Forest, Caatinga and Cerrado (C.dichotoma, M. densa, M. multipunctata, M. loranthifolia, Acta Botanica Brasilica, 2023, 37: e20220194 or 58%, Proença et al. 2020), and recent Myrteae biogeographical reviews showed that the Atlantic Forest is the most likely ancestral area of the biggest genera, Myrcia and Eugenia, reflecting the great diversity of Myrtaceae in the Atlantic Forest (Santos et al. 2017; Mazine et al. 2018; Amorim et al. 2019).According to these recent studies, the main Myrteae lineages originated in the Atlantic Forest and later colonized the Amazon basin, Caatinga, Cerrado, Caribbean, and the Andes, which could explain species occurring among these biomes.For instance, Blepharocalyx eggersii, Eugenia excelsa and Myrciaria glomerata are disjunct distributed between the Atlantic and Amazon Forests.A total of 26 species of Myrtaceae from the restinga of Bahia also occur in the Espinhaço mountain range in several habitats (Campo Rupestre, Forests, Caatinga s.l., and Cerrado s.l.).This disjunction pattern has been recently recorded in the literature for other angiosperms groups (Alves et al. 2007; Lucresia et al. unpubl.res.).

Figure 3 .
Figure 3. Distribution pattern of Myrtaceae species found in restinga in the state of Bahia: WID -widely distributed in Brazil; AF -endemic of the Atlantic Forest biome; AAM -disjunction between the Atlantic and Amazon Forests; ACC -Atlantic Forest, Caatinga and Cerrado biomes.

Figure 10 .
Figure 10.A−B.Psidium guineense; A: immature fruit; B: young and old flowers (the petals and the stamens already fallen).C−E.P. oligospermum; C: inflorescence with young and old flowers, and bud; D: immature fruits; E: branches with leaves and fruits (A, B, D, E. J.D.O.Melo; C. T. Vieira).
climatic differences and the influence of different vegetation types.The northern Bahian coast is surrounded mainly by the Caatinga biome that presents a semiarid climate (Matos 2014; Matos et al. 2017), while the remaining coastal areas are not markedly dry (Martin et al. 1980; Cerqueira 2000) and is surrounded by the Atlantic Forest biome with great diversity and endemisms (Mori et al. 1981; 1983; Thomas et al. 1998; Amorim et al. 2005; Matos 2014).