Croton L. (Crotonoideae, Euphorbiaceae) in a protected area in Northeast Brazil

Abstract Croton is the largest genus of Crotonoideae Burmeist. (ca. 1200 species), with approximately 300 species distributed in all the phytogeographic domains in Brazil. The Chapada of Araripe Environmental Protection Area (CA-EPA) is one of the largest protected areas in northeastern Brazil and comprises many different types of vegetation. Considering the expressive representation of Croton in that northeastern region and its morphological complexity, we carried out a taxonomic study of the species occurring in the CA-EPA. The analysis of collections deposited in regional herbaria, together with field observations, revealed 18 Croton species, five of which had never been cited as occurring in the study area; seven of those taxa are endemic to the Brazilian semiarid region. Croton species were recorded in all of the vegetation types in the CA-EPA, especially in the “carrasco” and “caatinga” vegetation. The plants habits, the shapes of their stipules, extrafloral nectaries, indumenta, and staminate and pistillate sepals were important characteristics for their differentiation.


Introduction
Croton L., the largest genus of Crotonoideae (Euphorbiaceae), comprises almost 1,200 species throughout tropical regions of the world.Its representatives are recognized as sharing clear or colored latex, tectors or glandular trichomes, tectors trichomes can be simple, stellate to lepidote; leaves often with acropetiolar or basilaminar nectaries, Inflorescence thyrsus-like with staminate flowers in the distal portion of the branch and pistillate flowers in the proximal portion, trichomes on the receptacle, curved stamens in the floral buds, and corolla reduced or absent in pistillate flowers (Webster 1993;Berry et al. 2005).
Brazil is one of the centers of endemism of the genus Croton, with approximately 300 species distributed in all of its states and phytogeographic domains (Berry et al. 2005;Caruzo et al. 2020).Approximately 110 species are found in northeastern Brazil (ca.10% of the total diversity of the genus), with most of them occurring in the Caatinga domain (67) (Caruzo et al. 2020).Although Croton is one of the most taxonomically studied genera of the Crotonoideae family in Brazil (Secco et al. 2012), especially in the semiarid region (e.g., Carneiro-Torres 2009), there is still much to be discovered, as many new records and new species have recently been published (see Gomes et al. 2010;Carneiro-Torres et al. 2011;Rossine et al. 2020;Sodré & Silva 2022).
The high Croton richness and endemism in the Caatinga domain is relentlessly exposed to high levels of anthropic pressure.According to IBGE (2020), that domain showed continuous decreases in both grassland and forested vegetation cover between 2000 and 2018, with more than 35 thousand km² being impacted.Deforestation there has mainly been caused by harvesting firewood and pasture formation (MMA-Atlas 2007).Another worrying situation refers to the low number of legally protected areas in the Caatinga domain, especially in light of its significant territorial extension (Unidades de Conservação 2022).
The Chapada of Araripe Environmental Protection Area (CA-EPA) stands out as a sustainable-use conservation area occupying parts of three states in the Caatinga domain in northeastern Brazil.Despite having been established in 1997, the reserve still does not have a management plan and suffers from deforestation and degradation due to fire and pasture formation, resulting in ecosystem fragmentation (ICMBio 2015;Silva & Souza 2018).An increased knowledge of the occurrence and distribution of its biodiversity would help to identify target taxa for conservation, aid in establishing management strategies, allow the assessment of compliance with its conservation objectives, and help sustain human populations in the region without causing environmental degradation (Ragas 1995;Santos 2018).Loiola et al. (2015) surveyed the phanerogamic flora of Chapada of Araripe and listed 480 species of Angiosperms belonging to 79 families -especially Fabaceae Lindley (95 spp.), Rubiaceae Jussieu (28 spp.), Euphorbiaceae Jussieu (27 spp.), Bignoniaceae Jussieu (22 spp.), and Asteraceae Berchtold & Jan Presl (19 spp.).Croton was the most numerous genus in the entire survey (14 spp.), reflecting its expressive representation in areas of caatinga, cerrado, and humid forest vegetation (Cordeiro et al. 2015;Caruzo et al. 2020) -the vegetation types predominating in the CA-EPA.
The species list first presented for the CA-EPA (Loiola et al. 2015) was not, however, definitive, as some of the municipalities included within the reserve were not included in the survey -making it important to undertake a more detailed and inclusive taxonomic study of the area.Considering then the expressive representation of Croton in northeastern Brazil, the morphological complexity of the genus, and the lack of specific studies of that taxon in Chapada of Araripe, we undertook a study of the taxonomic and geographic distribution of Croton species occurring in the CA-EPA.
The characteristic climate of the CA-EPA region is hot tropical, with annual temperatures ranging between 23 and 27° C; the period between May and August is somewhat milder, with an average temperature of 21 to 25° C (IPECE 2009).The rainfall regime is irregular (varying from 700 to 1000 mm/year), with heavy concentrations of precipitation within just a few months of the year, with February being the wettest month.Elevations there can reach 850 to 1000 m a.s.l.The CA-EPA includes a number of different vegetation types: caatinga, carrasco, cerradão, cerrado, and humid forest (IBGE 2021).

Visits to herbaria and data collection
After an online survey of the digital platforms SpeciesLink (http:// inct.splink.org.br/) and Reflora Virtual Herbarium (http://reflora.jbrj.gov.br/), seven herbaria were selected for visitation or loan requests.The EAC, HCDAL, HUEFS, IPA, UFP, HST (non-indexed), and PEUFR herbaria (acronyms according to Thiers 2021) contained a considerable number of Croton exsiccates from the CA-EPA, and the EAC, HCDAL, HST, and PEUFR herbarium were visited.Exsiccates from the UFP herbarium (UFPE) were analyzed on loan.The other herbaria were not visited for health and safety reasons, due to the SARS-CoV-2 pandemic.

Species identifications and descriptions
Species identifications and descriptions were made based on consultations with specialists, the specialized literature (Carneiro-Torres 2009; Silva et al. 2010;Sodré et al. 2019;Rossine et al. 2021), and by comparison with standard collections.The descriptions were developed through morphological analyses of the specimens and complemented with information provided on the herbarium labels.If the herbarium specimens from the conservation area were not sufficient to provide detailed descriptions, they were complemented with material collected in the same domain and close to the study region.The terminologies used were based on Hickey (1973), Radford et al. (1974), Harris & Harris (2001), Webster et al. (1996) and Lucena & Sales (2006).Illustrations of the specimens analyzed are provided to demonstrate details of relevant morphological structures.Comments concerning the habitats and geographic distributions of the species were based on information contained on the herbarium labels, from digitized databases, and from the published literature.

Discussion
Regarding the collection effort in the CA-EPA region, Loiola et al. (2015) related the fact that the most collected municipalities are close to university campuses, such as the Universidade Regional do Cariri, in the state of Ceará, and the Universidade Vale do São Francisco (UNIVASF) and the Serra Talhada campus of Universidade Federal Rural de Pernambuco (UFRPE-UAST) in the state of Pernambuco, the presence of these research centers in nearby regions directly influences the collection effort in these municipalities.
All the vegetation types present in the CA-EPA harbor Croton species -predominantly in caatinga and carrasco vegetation.Croton heliotropiifolius and C. tricolor were recorded in all vegetation types present in the CA-EPA, which corroborates the wide distribution these species present in different domains (i.e.: Caatinga, Cerrado and Atlantic Forest), not only in the Northeast region but also other regions of Brazil (Caruzo et al. 2020).In contrast, C. betaceus and C. floribundus have records only in humid forest environments, which also corroborates the distribution data for these species, as both are generally found in Amazon Rainforest and Atlantic Forest areas (Caruzo et al. 2020).The Caatinga has the highest number of endemic species among the Seasonally Dry Tropical Forest and Woodland (SDTFW), as observed for Croton, since this domain comprises a high diversity and endemism for the genus in Brazil (Fernandes & Queiroz, 2018).
Of the 18 species of Croton found in the CA-EPA, only C. glandulosus and C. tricolor are on the international list of threatened species (IUCN, 2022); in the period of the study by Loiola et al. (2015) none of the 14 Croton species included in the survey had information about their conservation status recorded in an online database, which highlights the lack of studies, and also of dissemination related to this theme, which ends up making it even more difficult to implementation of conservation strategies aimed at these species and the environments in which they inhabit.
In the specieslink platform (specieslink.net/search),22 names accepted in Croton for the Chapada of Araripe area are listed, however in this list C. suassunae and C. sertanejus are not contemplated and, during the curse of the present work, it was elucidated that four species (C.ceanothifolius, C. cerinodentatus, C. luetzelburgii, C. sclerocalyx) were wrongly identified and do not occur in the study area.This highlights the importance of taxonomic work carried out by specialists in the groups and how it is crucial to consider that the survey, both in the field and in the herbarium, conducted with taxonomic expertise carried out by specialists, increases the chance of finding more realistic data with greater reliability in the identifications (Bebbera et al. 2010).
From a morphological point of view, the similarity between some species makes their taxonomic delimitations difficult.Croton echioides, and C. sertanejus stand out, for example, by having shrub habit, leaf blade with margins entire and extrafloral nectaries on the petiole.Easily diagnosed species, on the other hand, such as C. floribundus, C. jacobinensis, and C. triqueter, were also considered.

Figure 1 .
Figure 1.Map showing the location of the Chapada of Araripe Environmental Protection Area (CA-EPA).

Figure 3 .
Figure 3. Distribution map of Croton adamantinus and C. argyrophyllus in the CA-EPA.

Figure 4 .
Figure 4. Distribution map of Croton betaceus and C. blanchetianus in the CA-EPA.

Figure 5 .
Figure 5. Distribution map of Croton echioides in the CA-EPA.

Figure 9 .
Figure 9. Distribution map of Croton jacobinensis and C. limae in the CA-EPA.

13.Figure 11 .
Figure 11.Distribution map of Croton nepetifolius and C. pedicellatus in the CA-EPA.

Figure 12 .
Figure 12.Distribution map of Croton sertanejus in the CA-EPA.

Figure 13 .
Figure 13.Distribution map of Croton suassunae and C. tricolor in the CA-EPA.

occurrence in the study area, and conservation status:
(Sodré et al. 2019, Caruzo et al. 2020, 11.XII.1995,fl.,  A. M. Laurênio et al. 288 (PEUFR); Ibimirim, Serra Negra, proximidades do SítioOliveira, 22.III.1994,fl., fr., S. I. Silva, 351 (PEUFR).PIAUÍ: Canto do Buriti, Pajeú, 09.XII.1979,fl.,M.R. Dellaco, s.n.(PEUFR); Pedro IV, depois de Sertão de dentro, 01.III.1980, A. J. Castro et al.Croton grewioides is native to South America, occurring in Brazil, Bolívia and Peru.(Silva et al. 2010, Sodré et al. 2019, Riina et al. 2021); it occurs widely in all the states of the northeastern region of Brazil and can also be found in Minas Gerais State in southeastern Brazil(Sodré et al. 2019, Caruzo et al. 2020, Riina et al. 2021).The species was recorded in areas of caatinga and carrasco vegetation in the region and is frequently found along roadsides (Figure7).The species was classified as Least Concern in relation to its Extent of Occurrence (EOO) of 5,489,855.241km² and Area of Occupancy (AOO) of 924.000 km².Notes: Croton grewioides can be identified by the presence of obconic to cylindrical extrafloral nectaries on the margins of the leaf blade, and by the absence of stipules on mature branches.The species has a characteristic cinnamon scent, as noted by collectors on most herbarium specimen labels.

occurrence in the study area, and conservation status:
The conservation status of Croton tricolor was previously published in the IUCN Red List (2018) as Least Concern.