Floristic survey of Rubiaceae in the largest remnant of Cerrado in the metropolitan region of São Paulo, Brazil

Abstract

We present a floristic survey of the family Rubiaceae in Juquery State Park, a conservation unit that harbors the largest Cerrado area in the metropolitan region of São Paulo and is a refuge within the Atlantic Forest domain. The work was conducted using conventional methods in plant taxonomy, including fieldwork between 2020 and 2023, a literature survey, visits to herbaria, and requests for specimen loans. Previous articles revealed the high diversity of the family in the park, but no specific treatment had been published. In the present study, 35 species distributed in 15 genera were recorded in different phytophysiognomies, and Borreria (7 spp.), Palicourea (5 spp.), Coccocypselum (4 spp.), Psychotria (4 spp.), and Galianthe (3 spp.) are the richest. Four genera (Cordiera, Hexasepalum, Malanea and Mitracarpus) and 21 species are new records for this conservation unit. A dichotomous identification key and photos of the species are also provided. The diversity of Rubiaceae species in the study area is greater than previously recorded in broader surveys, and the mosaic formed by open and forest phytophysiognomies in the park probably contributes to this high level of diversity.

Key words: campo cerrado; campo sujo; neotropical flora; Palicoureeae; Spermacoceae

Resumo

Apresentamos um levantamento florístico da família Rubiaceae no Parque Estadual do Juquery, uma Unidade de Conservação que abriga a maior área de Cerrado da região metropolitana de São Paulo. O trabalho foi elaborado com base nos métodos convencionais em taxonomia vegetal: trabalho de campo com expedições de campo entre 2020 e 2023, levantamento bibliográfico, visita a herbários e pedidos de empréstimo de materiais. Estudos anteriores revelaram uma alta diversidade da família no parque, mas nenhum tratamento específico havia sido realizado. No presente estudo foram registradas 35 espécies em diversas fitofisionomias, que estão distribuídas em 15 gêneros, sendo Borreria (7 spp.), Palicourea (5 spp.), Coccocypselum (4 spp.), Psychotria (4 spp.), e Galianthe (3 spp.) os mais diversos. Também reportamos quatro gêneros (Cordiera, Hexasepalum, Malanea e Mitracarpus) e 21 espécies sem registro prévio para essa Unidade de Conservação. Uma chave dicotômica de identificação e fotos das espécies são apresentadas em conjunto a lista de espécies. A diversidade de espécies de Rubiaceae na área de estudo é maior do que já tinha sido registrada em levantamentos mais amplos, e o mosaico formado por fitofisionomias abertas e florestais presentes no Parque deve contribuir para essa alta diversidade.

Palavras-chave: campo cerrado; campo sujo; flora neotropical; Palicoureeae; Spermacoceae

Introduction

One of the largest flowering plant families is Rubiaceae, which comprises over 14,000 species within 620 genera distributed throughout the world, although it is most diverse in the Neotropics (Govaerts et al. 2023). With all sorts of habits, ranging from herbs and shrubs to small trees and canopy trees, identifying Rubiaceae is easy using the following diagnostic traits that are common in the family: leaves opposite, blades undivided with an entire margin, interpetiolar stipules present; flowers radially symmetric, corollas gamopetalous, stamen and petal number the same, and ovary inferior (Jung-Mendaçolli 2007; Delprete & Jardim 2012). The high diversity found in this family and its abundance and presence in all vegetation layers make Rubiaceae a good indicator in ecological and conservation studies (Delprete & Jardim 2012). Furthermore, the plants of this family have an intricate relationship with several pollinators and their fruits are a common food source for tropical fauna (Gentry & Emmons 1987; Bremer & Eriksson 2009). In Brazil, the family Rubiaceae is represented by 1,417 species within 128 genera; it occurs in every phytogeographic domain (Flora e Funga do Brasil 2023, continuously updated) and is especially diverse in the Amazon basin, Atlantic Forest, and Cerrado (Delprete & Jardim 2012).

The Brazilian Cerrado is widespread in the states as Goiás and Tocantins; however, it is also present in several other states and regions of the country (Eiten 1972). According to some estimates, the Cerrado used to cover ca. 3,500,000 ha of São Paulo in the 18^th century, which is about 14% of the state (Baitello et al. 2013). Currently, the remnants of the Cerrado in this state are small, fragmented, and surrounded by pasture, sugarcane and soy plantations, and urban areas (Durigan et al. 2007). Only a few of these remnants are protected as conservation units (Durigan et al. 2006; Rodrigues & Bononi 2008). As stated by Ratter et al. (2003), the Cerrado in São Paulo has a notably rich and heterogeneous flora compared to other states, including species that are rare or even absent in other areas.

The Cerrado consists mostly of savanna physiognomies and, therefore, the real richness occurs in the non-arboreal, herbaceous-subshrub stratum (Castro et al. 1999). However, phytosociological studies tend to focus on woody plants and neglect this other floristic component (Durigan et al. 2018). Several studies note that the family Rubiaceae is one of the most species-rich groups in herbaceous-subshrub and shrub-tree components of the Cerrado (Mantovani & Martins 1993; Batalha et al. 1997; Ratter et al. 1997; Batalha & Mantovani 2001; Tannus & Assis 2004; Ishara et al. 2008; Rossatto et al. 2008; Sasaki & Mello-Silva 2008; BFG 2015).

Considering the importance of Rubiaceae species for biodiversity conservation in fragments of native vegetation, and the high value of protected areas of the Cerrado in São Paulo state, this work includes a checklist of Rubiaceae for the largest Cerrado fragment in the São Paulo metropolitan region.

A dichotomous identification key, photos of species, and a discussion about some species determinations and comparisons with other savanna fragments in the state are also provided. Thus, this increases what is known about the Brazilian flora and the Cerrado in São Paulo and we expect it will contribute to the park’s management plan.

Material and Methods

Study area

We conducted this study in Juquery State Park (Parque Estadual do Juquery - PEJY; Fig. 1), a fully protected conservation unit in Franco da Rocha, São Paulo state, Brazil (23º19’ and 23º25’S, 46º45’and 46º35’W) (Secretaria de Infraestrutura e Meio Ambiente 2023a). The park’s grounds were formerly a farm that belonged to Dr. Franco da Rocha and later became home to the Franco da Rocha Hospital - Psychiatric Department. Even though it used to be a psychiatric hospital, the original vegetation cover survived because of low usage (Baitello et al. 2013).

The park was created in 1993 and its protected area is about 2,000 hectares. It is bordered to the north by the Juquery River valley, to the west by the Paiva Castro Dam, and to the south and east by the valleys of the Morro Grande or Morro do Juquery hill complex. The Juquery River basin integrates the Cantareira Water System, which is one of the most important water supply systems in São Paulo (Baitello et al. 2013).

The region where the park is can be defined as semi-mountainous, with the elevation varying between 730 and 950 m, including several deep valleys (Baitello et al. 2013). The average annual temperature is 20 ºC, there is no defined dry season, and the climate is classified as Cfb by the Köppen-Geiger classification system (Alvares et al. 2013).

Figure 1
Location of Juquery State Park in the city of Franco da Rocha, São Paulo state, Brazil. BR: Brazil; SP: São Paulo; FR: Franco da Rocha; CA: Caieiras. Black and white lines represent the boundaries between municipalities, yellow lines represent the road system, and crossed lines with ferrugineous color represent the railway system. The blue area depicts the Paiva Castro Dam. Map produced by Samantha F. Marcon with adaptation from São Paulo (2020).

Most of the vegetation cover consists of the following Cerrado phytophysiognomies: campo limpo (open fields) (Fig. 2a), campo sujo (fields with bushes and small scattered trees) (Fig. 2b), campo cerrado (fields with a greater number of bushes and trees) (Fig. 2c), and cerrado sensu stricto (a dominance of trees and shrubs, despite considerable herbaceous vegetation) (Coutinho 1978). The distinction between areas of campo cerrado and cerrado sensu stricto is not very clear in PEJY, and according Baitello et al. (2013) the areas of cerrado sensu stricto are rare and altered, so we decided to use only campo cerrado for these phytophysiognomies with a high number of woody individuals. In addition, the park has remnants of forest environments, such as forests at the bottom of valleys and riparian and gallery forests (Fig. 2d-f) (Baitello et al. 2013; Silva et al. 2018). It is also the largest Cerrado remnant in the São Paulo metropolitan region (Keller et al. 2021), which is an area composed by 39 municipalities and a population of almost 20 million inhabitants (Lima & Rueda 2018).

The park is open to the public to use for leisure and sports, as well as activities related to environmental education and the appreciation of nature (Secretaria de Infraestrutura e Meio Ambiente 2023b). However, previous studies (Silva et al. 2018; Keller et al. 2021) highlight the park’s vulnerability to anthropogenic pressure because its surroundings are extremely urbanized and influenced by a nearby penitentiary. Furthermore, there are records of invasive species and the indiscriminate use of fire (Baitello et al. 2013).

Floristic survey

We took four field trips to the park between 2020 and 2023. We visited the savanna and forest phytophysiognomies to collect fertile Rubiaceae individuals; when not available, we collected vegetative vouchers. All the collected material was processed according to Fidalgo & Bononi (1984) and deposited in the Federal University of São Paulo herbarium (HUFSP); duplicates were sent to the Forestry Institute of São Paulo (SPSF), São Paulo University (SPF), and Rio de Janeiro Botanical Garden (RB) herbaria (acronyms according to Thiers, continuously updated). We also analyzed Rubiaceae material collected in the park and previously deposited in HUFABC, HUFSP and SPSF, which added up to about 150 specimens. We used digital databases, such as Reflora (<reflora.jbrj.gov.br/>), SpeciesLink (<http://splink.cria.org.br/>) and JSTOR Global Plants (<https://plants.jstor.org/>), to find and analyze other material from the park, as well as for comparisons with other specimens and type material to confirm identifications. We verified the accepted names, synonyms, and authors using the International Plant Names Index database (<https://www.ipni.org/>) and Tropicos (2023a) (<https://tropicos.org>). All analyzed material is listed in Appendix S1 (available on supplementary material <https://doi.org/10.6084/m9.figshare.25645581.v1>).

We identified the plants by consulting literature about Rubiaceae, including Lewis & Oliver (1974), Costa & Mamede (2002), Gomes (2003), Jung-Mendaçolli (2007), Pereira (2007), Taylor et al. (2007), Cabral (2009), Silveira (2010), Souza et al. (2010), Cabral et al. (2011), Sousa et al. (2013), Zappi et al. (2014, 2017), Nepomuceno et al. (2018), Fonseca et al. (2020), and the Flora & Funga do Brasil platform. In addition, we consulted specialists to confirm or identify doubtful specimens (see Acknowledgements).

We observed and categorized the morphological data about the habits, stipules, leaves, flowers, and fruits in a spreadsheet. The characteristics are listed in Appendix S2 (available on supplementary material <https://doi.org/10.6084/m9.figshare.25645581.v1>). We prioritized vegetative traits over reproductive traits in the identification key. The terminology used is based on Radford et al. (1974) and Robbrecht (1988).

Results and Discussion

Thirty-five species of Rubiaceae, in 15 genera, were found in Juquery State Park (Tab. 1; Figs. 3-8). Of these, Borreria (7 spp.), Palicourea (5 spp.), Coccocypselum (4 spp.), Psychotria (4 spp.), and Galianthe (3 spp.) were the most diverse. In relation to habit, 23 species are herbs and subshrubs, while the others are trees or shrubs. Despite the great diversity of phytophysiognomies present in the park, most of the woody species were found in forest environments. In contrast, all species found in the savanna phytophysiognomies are herbs or subshrubs.

Previous general floristic surveys carried out in the park reported 17 species (Baitello et al. 2013) and 12 species (Keller et al. 2021) of Rubiaceae. The first was made in the different phytophysiognomies of the park, while the second focused on savanna grassland areas. In this work, we report four genera (Cordiera, Hexasepalum, Malanea and Mitracarpus) and 21 species with no previous records from the park, which corresponds to 62.8% of the species list.

Figure 2
a-f. Phytophysionogmies in Juquery State Park - a. campo limpo; b. campo sujo; c. campo cerrado; d. forest at the bottom of a valley with campo limpo in the foreground; e. riparian forest; f. gallery forest.

Table 1
Rubiaceae species found in PEJY, along with their respective habits, vegetation where they occur, confirmed distribution in Brazil, and selected voucher material.

Species	Habit	Vegetation	Confirmed distribution (according to Flora e Funga do Brasil)	Voucher
Bathysa australis K.Schum. (Fig. 3a-c)	Tree	Forest	Southern and Southeastern regions, plus Bahia and Federal District	I.C. Rossatto et al. 31 (HUFSP)
Borreria capitata (Ruiz & Pav.) DC. (Fig. 3d)	Herb	Campo sujo	All regions	I.C. Rossatto et al. 104 (HUFSP)
Borreria dasycephala (Cham. & Schltdl.) Bacigalupo & E.L.Cabral (Fig. 3e)	Herb	Forest	Southern region plus São Paulo	I.C. Rossatto et al. 12 (HUFSP)
Borreria runkii K.Schum.	Herb	Campo sujo	Mato Grosso, Mato Grosso do Sul and São Paulo	I.C. Rossatto et al. 24 (HUFSP)
Borreria schumannii (Standl. ex Bacigalupo) E.L.Cabral & Sobrado (Fig. 3f)	Sub-shrub	Forest	Northern, Midwest, Southern and Southeastern regions, plus Bahia and Maranhão	I.C. Rossatto et al. 39 (HUFSP)
Borreria tenella Cham. & Schltdl. (Fig. 4a-b)	Herb	Campo cerrado / campo sujo	Northern, Midwest, Southern and Southeastern regions, plus Bahia and Ceará	I.C. Rossatto et al. 74 (HUFSP)
Borreria verticillata G.Mey. (Fig. 4d)	Sub-shrub	Campo cerrado	All regions	I.C. Rossatto et al. 66 (HUFSP)
Borreria sp. (Fig. 4c)	Herb	Campo cerrado	-	I.C. Rossatto et al. 98 (HUFSP)
Coccocypselum condalia Pers. (Fig. 4e)	Herb	Ombrophilous forest	Midwest, Northeastern, Southern and Southeastern regions, plus Roraima and Tocantins	I.C. Rossatto et al. 53 (HUFSP)
Coccocypselum geophiloides Wawra (Fig. 4f)	Herb	Forest	Southern and Southeastern regions, plus Bahia	C.P. Bruniera et al. 1112 (HUFSP)
Coccocypselum hasslerianum Chodat (Fig. 4g-h)	Herb	Forest	Midwest, Southern and Southeastern regions, plus Alagoas, Bahia and Ceará	I.C. Rossatto et al. 42 (HUFSP)
Coccocypselum lanceolatum (Ruiz & Pav.) Pers. (Fig. 5a-b)	Herb	Forest / campo cerrado	Midwest, Northeastern, Southern and Southeastern regions, plus Tocantins	I.C. Rossatto et al. 11 (HUFSP)
Cordiera myrciifolia (K.Schum.) C.H.Perss. & Delprete (Fig. 5c-d)	Tree	Forest	All regions	I.C. Rossatto et al. 32 (HUFSP)
Declieuxia cordigera Mart. ex Zucc. var. cordigera (Fig. 5e-f)	Herb	Campo cerrado / Campo sujo	Midwest region, plus Bahia, Minas Gerais, São Paulo and Paraná	J.B. Baitello 1347 (SPSF)
Declieuxia cordigera var. angustifolia Müll.Arg. (Fig. 5g)	Herb	Campo cerrado / Campo sujo	Goiás, Mato Grosso, Minas Gerais, São Paulo, and Paraná	I.C. Rossatto et al. 2 (HUFSP)
Faramea latifolia (Cham. & Schltdl.) DC.	Tree/Shrub	Campo cerrado /forest	Rio de Janeiro	J.B. Baitello 1682 (SPSF)
Galianthe angustifolia (Cham. & Schltdl.) E.L.Cabral (Figs. 5h; 6a)	Sub-shrub	Campo cerrado / campo sujo	Midwest region, plus Minas Gerais, São Paulo and Paraná	I.C. Rossatto et al. 67 (HUFSP)
Galianthe liliifolia (Standl.) E.L.Cabral (Fig. 6b-c)	Sub-shrub	Campo cerrado / campo sujo	Federal District, Goiás, Minas Gerais and São Paulo	I.C. Rossatto et al. 68 (HUFSP)
Galianthe palustris (Cham. & Schltdl.) Cabaña Fader & E.L.Cabral (Fig. 6d-e)	Herb	Forest	Southern and Southeastern regions, plus Bahia	C.P. Bruniera et al. 1115 (HUFSP)
Hexasepalum radulum (Willd.) Delprete & J.H.Kirkbr. (Fig. 6f)	Herb	Forest	Northeastern, Southern, and Southeastern regions, plus Tocantins and Goiás	I.C. Rossatto et al. 26 (HUFSP)
Hexasepalum teres (Walter) J.H.Kirkbr. (Fig. 6g)	Herb/sub-shrub	Campo cerrado / campo sujo	All regions	I.C. Rossatto et al. 23 (HUFSP)
Malanea forsteronioides Müll.Arg.	Herb	Forest	Southern and Southeastern regions	I.C. Rossatto et al. 46 (HUFSP)
Mitracarpus hirtus (L.) DC.	Herb	Campo cerrado	All regions	J.B. Baitello & F.S. Peres 1459 (SPSF)
Palicourea forsteronioides (Müll.Arg.) C.M.Taylor (Fig. 6h-i)	Shrub	Forest	Minas Gerais and São Paulo	I.C. Rossatto et al. 37 (HUFSP)
Palicourea hoffmannseggiana (Roem. & Schult.) Borhidi (Fig. 6j-k)	Shrub	Forest	All regions	I.C. Rossatto et al. 38 (HUFSP)
Palicourea marcgravii A.St.-Hil. (Figs. 6l; 7a)	Tree/shrub	Forest	All regions	I.C. Rossatto et al. 43 (HUFSP)
Palicourea rigida Kunth (Fig. 7b-c)	Subshrub	Campo cerrado / campo sujo	All regions	I.C. Rossatto et al. 72 (HUFSP)
Palicourea sessilis (Vell.) C.M.Taylor (Fig. 7d)	Tree/shrub	Forest	Southern and Southeastern regions plus Bahia and Pernambuco	I.C. Rossatto et al. 6 (HUFSP)
Psychotria carthagenensis Jacq. (Fig. 7e-f)	Tree/shrub	Forest	All regions	I.C. Rossatto et al. 69A (HUFSP)
Psychotria laciniata Vell. (Fig. 7g)	Tree/shrub	Forest	Southern and Southeastern regions	I.C. Rossatto et al. 64 (HUFSP)
Psychotria stachyoides Benth. (Fig. 7h)	Shrub	Forest	Southern and Southeastern regions plus Bahia, Ceará and Goiás	I.C. Rossatto et al. 51 (HUFSP)
Psychotria suterella Müll.Arg. (Fig. 7i-j)	Tree/shrub	Forest	Southern and Southeastern regions	I.C. Rossatto et al. 30 (HUFSP)
Richardia brasiliensis Gomez (Fig. 7k-l)	Herb	Campo cerrado	All regions	I.C. Rossatto et al. 18 (HUFSP)
Richardia stellaris Steud. (Fig. 8a-b)	Herb	Campo cerrado	Southern and Southeastern regions plus Mato Grosso do Sul	I.C. Rossatto et al. 21 (HUFSP)
Rudgea gardenioides (Cham.) Müll.Arg. (Fig. 8c-e)	Tree	Forest	Southern and Southeastern regions	C.P. Bruniera et al. 1178 (HUFSP)
Sabicea brasiliensis Wernham (Fig. 8f-g)	Subshrub	Campo cerrado / campo sujo	Bahia, Federal District, Goiás, Minas Gerais, Mato Grosso, São Paulo, and Tocantins	C.P. Bruniera et al. 1125 (HUFSP)

Key to the Rubiaceae species in Juquery State Park

1. Stipules multifimbriate 2

2. Leaves appearing whorled because of the presence of brachyblasts 3

3. Inflorescence a glomerule 4

4. Leaf blade elliptic to ovate, hirsutullous, venation distinct on both sideBorreria capitata

4’. Leaf blade elliptic to oblong, glabrous, venation indistinct on both sidesBorreria verticillata

3’. Inflorescence a thyrse 5

5. Leaf blade filiform, secondary veins in 2-3 pairs, indumentum greenGalianthe angustifolia

5’. Leaf blade elliptic, secondary veins in 4-5 pairs, indumentum ferruginousGalianthe liliifolia

2’. Leaves opposite, without brachyblasts 6

6. Prostrate herbs 7

7. Leaf blade elliptic to ovate, membranaceous, pilose; flowers hexamerous; schizocarp with 3 mericarpsRichardia brasiliensis

7’. Leaf blade triangular to narrowly ovate, chartaceous, glabrous; flowers tetramerous; schizocarp with 4 mericarpsRichardia stellaris

6’. Erect herbs 8

8. Leaf blade elliptic to obovate, apex obtuse, rounded, or cuspidateGalianthe palustris

8’. Leaf blade elliptic, lanceolate or linear, apex acute or acuminate 9

9. Stipular lobes 3, the middle one wider and longer than the othersBorreria runkii

9’. Stipular lobes 5-11, same size 10

10. Glomerules axillary 11

11. Stem glabrousBorreria schumanni

11’. Stem pilose 12

12. Leaf blade membranousBorreria sp.

12’. Leaf blade chartaceous to coriaceous 13

13. Leaf blade coriaceous, secondary veins inconspicuous on both sides; corolla light pink to lilacHexasepalum teres

13’. Leaf blade chartaceous, secondary veins evident on both sides; corolla whiteHexasepalum radulum

10’. Glomerules terminal 14

14. Capsule-like fruit with transverse dehiscenceMitracarpus hirtus

14’. Capsule-like fruit with longitudinal dehiscence 15

15. Leaf blade lanceolate, chartaceous, glabrousBorreria dasycephala

15’. Leaf blade linear, membranaceous to coriaceous, glabrous to pubescentBorreria tenella

1’. Stipules entire or bifid 16

16. Herbs or subshrubs 17

17. Leaves sessile 18

18. Leaf blade ovate, base truncate to cordateDeclieuxia cordigera var. cordigera

18’. Leaf blade narrowly elliptic to elliptic, base acuteDeclieuxia cordigera var. angustifolia

17’. Leaves petiolate 19

19. Leaf blade chartaceous to coriaceous 20

20. Stem and branches glabrous; leaf blade elliptic, oblanceolate, obovate or ovate, glabrous; inflorescence pyramidal, with yellow flowersPalicourea rigida

20’. Stem and branches densely villous; leaf blade elliptical or ovate-lanceolate, lanate; inflorescence capitate, with white flowersSabicea brasiliensis

19’. Leaf blade membranaceous to chartaceous 21

21. Stipules triangular, foliaceousMalanea forsteronioides

21’. Stipules linear to triangular aristate, not foliaceous 22

22. Stem and leaves glabrous 23

23. Leaf blade cordiform, secondary veins in 6-9 pairsCoccocypselum geophiloides

23’. Leaf blade ovoid or lanceolate, secondary veins in 4-6 pairsCoccocypselum condalia

22’. Stem and leaves hirsute or velutinous 24

24’. Leaf blade with cordate to truncate base; inflorescence sessileCoccocypselum hasslerianum

24’. Leaf blade with cuneate, truncate, rounded, or asymmetrical base; inflorescence pedunculateCoccocypselum lanceolatum

16’. Trees or shrubs 25

25. Stipules entire 26

26. Stipules deciduous, exposing a ring of colletersPsychotria carthagenensis

26’. Stipules persistent 27

27. Stipules with dorsal appendages; stem with spongy barkRudgea gardenioides

27’. Stipules without appendages; stem with solid bark 28

28. Leaf blade coriaceousFaramea latifolia

28’. Leaf blade chartaceous to membranaceous 29

29. Terminal stipules ca. 2cm long, leaf-like; leaf blade with about 30 pairs of secondary veins; inflorescence pyramidalBathysa australis

29’. Terminal stipules up to 3mm long, triangular; leaf blade with about 7 pairs of secondary veins; female flowers solitary and male flowers in groups of 5-6Cordiera myrciifolia

25’. Stipules bifid 30

30. Inflorescence with pink to orange peduncle; flowers with orange to yellowish corolla with lilac or pink apexPalicourea marcgravii

30’. Inflorescence with green peduncle; flowers white or yellow 31

31. Inflorescence mainly axillary, sometimes terminal; fruit ellipsoid or obovoidPalicourea sessilis

31’. Inflorescence only terminal; fruit globose 32

32. Inflorescence sessile or subsessile 33

33. Leaf blade elliptic, glabrous, apex acute or usually acuminate, base cuneate; flowers sessile, with yellow corollaPsychotria laciniata

33’. Leaf blade elliptic to oblong, sometimes hirsutullous along the primary vein on the abaxial side, apex acuminate, base acute or cuneate; flowers subsessile, with white corollaPsychotria suterella

32’. Inflorescence pedunculate 34

34. Bracts poorly developed; inflorescence spike-likePalicourea forsteronioides

34’. Bracts well developed; inflorescence capitate or paniculate 35

35. Leaf blade elliptic, glabrous; inflorescence with green, purplish or white, glabrous bractsPalicourea hoffmannseggiana

35’. Leaf blade narrowly elliptic, pilose on both sides; inflorescence with green, sericeous bractsPsychotria stachyoides

Figure 3
a-c. Bathysa australis - a. vegetative branch; b. stipule; c. old inflorescence. d. Borreria capitata - flowering branch. e. Borreria dasycephala - flowering branch. f. Borreria schumannii - flowering branch.

Figure 4
a-b. Borreria tenella - a. stipule; b. terminal inflorescence. c. Borreria verticillata - flowering branch. d. Borreria sp. - flowering branch. e. Coccocypselum condalia - flowering branch. f. Coccocypselum geophiloides - vegetative branch. g-h. Coccocypselum hasslerianum. g. flowering branch; h. immature fruits and one blue mature fruit.

Figure 5
a-b. Coccocypselum lanceolatum -a. stipule; b. terminal inflorescence. c-d. Cordiera myrciifolia - c. masculine flowers; d. immature fruits. e-g. Declieuxia cordigera var. cordigera - e. terminal inflorescence; f. flowering branch; g. D. cordigera var. angustifolia. h. Galianthe angustifolia - leaves.

Figure 6
a. Galianthe angustifolia - terminal inflorescence. b-c. Galianthe liliifolia - b. habit; c. terminal inflorescence. d-e. Galianthe palustris - d. stipule; e. flowering branch. f. Hexasepalum radulum - flowering branch. g. Hexasepalum teres - flowering branch with immature fruits. h-i. Palicourea forsteronioides - h. terminal inflorescence; i. immature fruits. j-k. Palicourea hoffmannseggiana - j. flowering branch; k. immature fruits. l. Palicourea marcgravii - terminal inflorescence.

Figure 7
a. Palicourea marcgravii - immature fruits. b-c. Palicourea rigida - b. terminal inflorescence; c. inflorescence with red brown mature fruits. d. Palicourea sessilis - immature fruits. e-f. Psychotria carthagenensis - e. branch with terminal stipule and distal decidual stipule; f. inflorescence with immature fruits. g. Psychotria laciniata - purple mature fruits. h. Psychotria stachyoides - immature inflorescence. i-j. Psychotria suterella - i. flowering branch; j. purple mature fruit. k-l. Richardia brasiliensis - k. stipule; l. terminal inflorescence.

Figure 8
a-b. Richardia stellaris - a. habit; b. flower bud. c-e. Rudgea gardenioides - c. leaves; d. barky stem; e. stipule. f-g. Sabicea brasiliensis - f. flowering branch; g. red brown mature fruits.

Notes about species identifications

Although five other species were listed by Baitello et al. (2013), they were not included on our list because we did not collect them during the expeditions or find herbarium material of these taxa [Amaioua intermedia Mart., Galianthe peruviana (Pers.) E.L. Cabral, Manettia luteorubra Benth., Posoqueria acutifolia Mart. and Rudgea sessilis (Vell.) Müll. Arg.]. According to C.P. Bruniera (personal communication), Rudgea sessilis is sometimes confused with Palicourea sessilis, as noted for herbarium specimens, probably because of the narrow leaves of these species. P. sessilis has a wide distribution in eastern Brazil, is quite abundant in its range and commonly found in PEJY, so it is likely that the specimen listed by Baitello et al. (2013) as R. sessilis is P. sessilis.

We were not confident in the identifications of some loaned specimens because they did not agree with the literature and photographs of type material. This was the case for Borreria warmingii K. Schum., Declieuxia fruticosa (Willd.) Kuntze, Galianthe grandifolia E.L. Cabral, and Richardia schumanniiW.H. Lewis & Oliv. We redetermined them as Borreria tenella, Declieuxia cordigera, Galianthe liliifolia and Richardia stellaris, respectively, and discuss these decisions below.

Borreria tenella was determined based on the following: hirsute branches; leaf blades linear, membranous to coriaceous, with 3-4 pairs of secondary veins; and stipular sheath pubescent, with 6-8 lobes. However, B. warmingii has the following: glabrous branches; leaf blades linear, coriaceous, light green, with 2-3 pairs of secondary veins; and stipular sheath glabrous, with one larger central lobe and two smaller lateral lobes. Although B. tenella is classified as illegitimate (Tropicos 2023a), this name was maintained since the group that this species is in is constantly undergoing nomenclatural changes.

Declieuxia cordigera was determined because the analyzed material has the following: hirsutullous to pilose branches; non-decurrent stipules; leaf blades oblanceolate, ovate or narrowly elliptic to elliptic, coriaceous, base truncate, cordate or acute, adaxial surface glabrous, hirsute or hirsutullous, abaxial surface glabrous, hirsute or hirsutullous, secondary veins in 3-6 pairs; and corolla tubular-campanulate. The two varieties of D. cordigera were also identified; D. cordigera var. cordigera individuals have ovate leaf blades and D. cordigera var. angustifolia individuals have narrowly elliptic to elliptic leaf blades. On the other hand, D. fruticosa has the following: glabrous branches; decurrent stipules, which extend to the next node; leaf blades elliptic to ovate, membranous, glabrous, base obtuse to rounded, secondary veins in 5-7 pairs; and corolla hypocrateriform. After an analysis of material of the two species at the Reflora Virtual Herbarium and the types on JSTOR Global Plants, it became clear that the delimitation of these two species needs further study.

Galianthe liliifolia was determined due to the presence of a rusty indumentum that, according to Cabral (2009), is a striking feature of this species. In addition, it has leaves that are pseudoverticillate, with elliptic-lanceolate, hirsutullous, chartaceous blades, and a hirsute stipular sheath with 7-10 lobes. In turn, G. grandifolia has leaves that are opposite (rarely pseudoverticillate), with elliptic to lanceolate, subcoriaceous leaf blades, and a hirsute stipular sheath with 6-7 lobes.

Richardia stellaris was determined based on the key in Lewis & Oliver (1974), mainly because the stipular lobes are 5-7 mm long and the schizocarp has 4 glabrous mericarps. In contrast, R. schumannii has stipular lobes up to 2 mm long and a schizocarp with 4 mericarps that are scabrous at the apex.

Finally, Borreria sp. remained undetermined due to the scarcity of material; it was only found during one of the field expeditions.

Notes on diversity and occurrence data

Compared to other floristic surveys conducted in different Cerrado remnants in São Paulo (Mantovani & Martins 1993; Batalha et al. 1997; Batalha & Mantovani 2001; Tannus & Assis 2004; Ishara et al. 2008; Rossato et al. 2008; Sasaki & Mello-Silva 2008; Ishara & Maimoni-Rodella 2012; Cavassan & Weiser 2015), Borreria, Declieuxia, Palicourea and Richardia were present in all studies, but with different species compositions. Borreria was not as diverse, with up to three species in most studies, except for Sasaki & Mello-Silva (2008) who recorded five species, while we recorded seven species. Coccocypselum lanceolatum and Palicourea rigida were the only species recorded in all the surveys. Chiococca spp. and Tocoyena spp. are frequent in other localities but were not found in PEJY. Most of the species cited from forests, such as Bathysa australis, Coccocypselum condalia, C. hasslerianum, C. geophiloides and Rudgea gardenioides, were not recorded by the studies mentioned above. This is probably related to the heterogeneous landscape in PEJY, including savanna phytophysiognomies interspersed with forest formations. Most of the studies recorded an average of 15 Rubiaceae species, while we found about twice as many species. This is probably because we only focused on this family, while the others were general surveys.

Species of the tribe Spermacoceae (Borreria, Galianthe, Hexasepalum and Mitracarpus) prevail in the open formations in the park, which is consistent with statistics that demonstrate these genera have high species richness in the Cerrado domain (Miguel et al. 2020; Salas et al. 2020; Souza et al. 2020). The forest formations are dominated by species of the tribe Palicoureeae (mainly Palicourea and Psychotria, but also Rudgea) that are commonly found in humid vegetation (Tropicos 2023b).

Based on an analysis of the data in Flora e Funga do Brasil, all the species recorded in this study were confirmed to occur in São Paulo State, except for Faramea latifolia that has only been confirmed to occur in Rio de Janeiro state and possibly in São Paulo. Most of the species are native to the South and Southeast regions of Brazil, while others, such as Borreria verticillata, Cordiera myrciifolia, Hexasepalum teres, Palicourea hoffmannseggiana, P. marcgravii, P. rigida, Psychotria carthagenensis and Richardia brasiliensis, have wide distributions throughout the country. In contrast, Borreria runkii and Palicourea forsteronioides have more restricted distributions; B. runkii occurs in the states of Mato Grosso, Mato Grosso do Sul and São Paulo, and P. forsteronioides occurs only in the states of Minas Gerais and São Paulo.

Thus, the importance of the park is reinforced as a home to a megadiversity of species. Also, the role the park plays to conserve the Cerrado and Atlantic Forest flora is essential to ensure the maintenance of such heterogeneous and diverse biota (Baitello et al. 2013; Keller et al. 2021). We hope the knowledge provided here can be used to encourage conservation and preservation actions (Forzza et al. 2012), since the park is under constant anthropogenic pressure due to the increasing urbanization in its surroundings and illegal fires.

Acknowledgements

The authors thank the following: the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), for the scholarship granted to I.C.R. (grant 166590/2020-7); the Juquery State Park staff, for providing accommodations and help in the park, which allowed us to conduct this research; the Instituto Florestal, for providing the permits (Processo SMA 260108 - 002.298/2018); the HUFSP and Unifesp campus Diadema, for providing the infrastructure needed to conduct this work; the curators at SPSF and HUFABC, for the loans and donations; Victor Camargo Keller, for showing us new places in the park, helping with the identifications, and providing relevant suggestions related to the present work; João do Carmo, for helping with the identifications and for his suggestions on a previous version of this work; Javier Florentín, for helping identify the Spermacoceae materials; Letícia Dutra, for suggesting useful papers and helping with identifications; João Victor Schiavon, Samantha F. Marcon and Thaís Teixeira Conegiro, for their help during field trips; and Samantha F. Marcon, for making the map. We dedicated this work to João Batista Baitello, the greatest researcher of the Juquery State Park Flora, deceased in September 2023.

Data availability statement

In accordance with Open Science communication practices, the authors inform that raw data is available in the UNIFESP's data repository, which provides free access and guaranteed preservation: https://hdl.handle.net/20.500.12682/rdp/BMUUDK

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Edited by

• Area Editor:
  Dra. Maria Teresa Buril

Publication Dates

• Publication in this collection
  07 June 2024
• Date of issue
  2024

History

• Received
  12 July 2023
• Accepted
  03 Oct 2023