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Home , Araripe, Caatinga, Didymiaceae, Echinosteliales, Ibiapina, Itapipoca

ISSN 1809-127X (online edition) © 2010 Check List and Authors Chec List Open Access | Freely available at www.checklist.org.br Journal of species lists and distribution

n Myxomycetes, state of , northeastern pecies S

1 2 2* of

, Antônia Aurelice Aurélio Costa istribuitio D ists

L Maria Helena Alves and Laise de Holanda Cavalcanti 1 Universidade Federal do Piauí, Campus Ministro Reis Velloso. Avenida São Sebastião, 2819. CEP 64202-020. Parnaíba, PI, Brazil. raphic 2 Universidade Federal de , Centro de Ciências Biológicas, Departamento de Botânica, Laboratório de Myxomycetes. Avenida Professor g [email protected] Moraes Rego s/n. CEP 50670–901. Cidade Universitária. Recife, PE, Brazil. eo * Corresponding author. E-mail: G n

o Abstract:

2 otes Thirty , fouris one genera of the andleast 215 explored species of ofthe Myxomycetes nine states in arethis present ofin the northeastern , with Brazil, records covering of 27 N 83 % of families, all subclasses and orders recognized for these microorganisms. Ceará, with an area of 148,825,602 km species, distributed across 13 genera, occurring in a humid forest environment of the southern mesoregion. The dominant vegetation type is the Caatinga (dry, tree-shrub deciduous vegetation), with patches of (savanna-like vegetation), Carrasco (montane deciduous shrub vegetation) and fragments of Pluvio-nebular northernTropical Subperennial and northwestern Forest mesoregions. and Pluvial TheTropical specimens Subdeciduous obtained Forest. were depositedIn order to at better the UFP document Herbarium. the diversity of myxomycetes in that state, specimens were collected from the field betweenComatricha 2002-2007, Crateriumin Ceará’s and Metatrichia increase the number of genera which comprise Ceará’s myxobiota to 16. denudata, EighteenCraterium species leucocephalum were recorded,, occurring panicea in the, B. Caatinga melanospora vegetation, and the intermedium records of , Metatrichia vesparia, rigidum and P. tenerum

are new records for Ceará, increasing the number of species known to occur in the state to 37.

Introduction The state of Ceará is located on the northeastern region of Brazil, bordered by the Atlantic Ocean to the north, the 2002;woody Araújo plants etare al strongly influenced by topography, type state of Pernambuco to the south, the states of Rio Grande isof estimated soil, and, particularly,in around 600 by species, rainfall (Lemosand approximately and Rodal do Norte and Paraíba to the east, and the state of Piauí to . 1998). The woodyet al flora of the Caatinga the west. With a predominantly Warm Tropical Semiarid frequent families are Cactaceae, Caesalpinaceae, Fabaceae, Euphorbiaceae1/3 of them are and endemic Mimosaceae, (Leal mainly. 2003). represented The most by Caesalpinia pyramidalis Mimosa microregionsclimate, in this (IPECE state, 2007). five phytogeographical units are and Croton (Araújo et al. recognized, with seven mesoregions divided into 33 The destruction of Tul. their and several natural species habitat of due to 1998). Ceará’s northwestern mesoregion presents varied Forest,vegetation, the Thorny including Deciduous the Pluvio-nebular Forest, and the Tropical Open anthropogenic activities has strongly threatened the ShrubbySubperennial Caatinga Forest, (IPECE the Pluvial 2007). ThisTropical mesoregion Subdeciduous holds degradationflora and the leads fauna not of only the Caatinga, to the soil with erosion some and species the already extinct and others endangered. This vegetation areas representative of the Caatinga bioma classified risk, but also to genetic erosion and loss of in different levels of biological importance, taking into biodiversity. (Vellosoaccount, etbesides al. 2002). the degree In Ceará’s of endanger northern for mesoregion, fauna and flora the The establishment of conservation units of the elements, their extension and viability of conservation tobiodiversity document of the the species Caatinga present is indicated in the as areas one ofmentioned the steps to be taken to curb the problem. As such, it is necessary predominant vegetation is the Shrubby Caatinga (dense or northeastern Brazil, where this occurs. Subperennialopen), and one Forest, can also and find the small Cerrado. fragments In Ceará’s of the southern Pluvio- aboveWith as extremely regards to important, the Caatinga across the microbiota, nine states the of mesoregion,nebular Tropical which Subperennial also holds extremelyForest, the important Pluvial Tropical areas, a smaller predominance of the Caatinga (IPECE 2007; information is scarce but the fewet published al. 2006). studies Only reveal two Vellosothe vegetation et al. 2002). is similar to the aforementioned, with publicationsan abundance addressand diversity the of myxomycetes bryophytes, basidiomycetes that occur in Ceará,and myxomycetes mentioning the (Cavalcanti presence of 27 species in fragments as wellThe as Caatinga succulent vegetation plants (Cactaceae is characterized and Bromeliaceae). by the presence of thorny deciduous, small-bulk woody species, of humid forest in the of Cariri (Alves and that the density and dominance of the herbaceous and Cavalcanti 1996; Cavalcanti and Putzke 1998). This Floristic and phyto-sociological studies have revealed paper gathers all the known occurring species for Ceará myxobiota, collected between 1994 and 2007, and it aims Check List | Volume 6 | Issue 4 | 2010 555 Alves et al. | Myxomycetes, state of Ceará, northeastern Brazil ecology of myxomycetes, particularly those occurring into provide extremely a baseline important with biological respect to areas, the biodiversity situated across and different mesoregions of Ceará.

Materials And Methods Study area Ceará is one of the nine states in the Brazilian northeast, 2

Figure 1. Representation of the families of recorded Myxomycetes for with an area of 148,825,602 km , which is equivalent the state of Ceará, northeastern Brazil. to 9.57 % of the region. The predominant climate is the typeWarm is Tropical the Caatinga, Semiarid, across occurring its different in 68 physiognomies, % of the total Calcareous species (Physaraceae and Didymiaceae) sucharea of as the the state Arboreal (IPECE 2007). Caatinga, The thedominant Dense vegetation Shrubby Caatinga, and the Open Shrubby Caatinga. Other types of etrepresent al 45 % of the known total for the state (37 spp.); this value is quite close to the one found by Estrada-Torres vegetation are found in the different mesoregions, such group. (2009) of species in a study characteristic carried out of in aridthe arid or region semiarid of as the Cerrado (savanna-like vegetation), the Carrasco Mexico (49 %), supporting the existence of a particular (montane deciduous shrub vegetation), andet fragments al The occurrence record of Physarum rigidum is the of Pluvio-nebular Tropical Subperennial Forest and the environments. DataPluvial Collection Tropical and Sub-deciduous Identification Forest (Araujo . 1998). which was recently listed by Parente et al The specimens reported in the current study were second report of this species for the Caatinga vegetation collected between 2002 and 2007, in the other species in this genus with records in Ceará. (2009) are forwidely the of Graça, Pacujá, , , and Sobral, distributedSerra da Capivara across theNational country, Park, except in the for state P. tenerum of Piauí., with The a located on northern and northwestern mesoregions (Amazonas), one in the southern region (Rio Grande do characteristics (Table 1). known occurrence in only one state in the northern region of For Ceará, the with collection, distinct herborization vegetational and and storage altitudinal of the states of the northeast (, Pernambuco, ), as Sul), one in the southeastern region (São Paulo) and three specimens, the methodology described by Cavalcanti reportedBadhamia by Cavalcanti panicea is(2002), documented Maimoni-Rodella from only (2002) two (1974) was used. Species identification was based on recordsand Putzke from (2002). northeastern Brazil, occurring in Morro do Lister (1925), Martin and Alexopoulos (1969),et Farr al. (1976), Chapéu, in a Caatinga area of Bahia, and in a fragment of Nannenga-Bremekamp (1991) and Lado and Pando with(1997). respect The toclassification the indication system of the by binomials Martin and authors (1983) et al. 2006). This species was collected ofwas the adopted species. and Lado (2001, 2005-2010) was followed inAtlantic the Forest of Sobral, in the where state thereof Pernambuco is a predominance (Cavalcanti of Dried specimens representing the studied material 2002; Cavalcanti were deposited at the UFP Herbarium. The binomials of the aforementioned taxa for Ceará were updated and an the TheCaatinga second vegetation largest (Tables group 1-2), of but species it was belongs found in to a annotated list of the species was generated. thehumid Stemonitaceae environment. (Figure 1), which corresponds to

Results And Discussion approximatelyStemonaria, Stemonitis 30 % of andthe knownStemonitopsis total for referred the northeast to the (Cavalcanti 2002). In the current study, besides the genera Up to the present moment, the occurrence of seven Comatricha, mesoregion,families, 13 in genera excursions and 27carried species out ofin myxomycetesthe microregion is withCrato only region one (Alves specimen and Cavalcanti collected on 1996; dead Cavalcanti wood, in and an known in the state of Ceará, all recorded in the southern Putzke 1998), there is also the occurrence of of Pacujá (Table 2). The sporocarps of this inof the Cariri current (Alves study and in Cavalcanti the northern 1996; and Cavalcanti northwestern and arboreal and open shrubby Caatinga environment in the Putzke 1998). With the addition of the records obtained features that do not correspond to any species currently in the state of Ceará, distributed across 16 genera with describedspecimen arein the well-conserved genus. and contain morphological mesoregions, thereComatricha are now, 37 species and known Metatrichia. to occur The Trichiaceae, with the genera Arcyria, Hemitrichia, Eight species Arcyria Metatrichia and Perichaena denudatafirst records, Badhamia of melanospora, B. panicea, Craterium leucocephalum, areDidymium new references intermedium for Ceará:, Metatrichia across the three mesoregions,, represent occurring 20 in% humid of the totalforests of vesparia, Physarum rigidum and P. tenerum (Table 2). known species of Ceará’s myxobiota (37 spp.), distributed The majority of the species belong to the Physaraceae, Stemonitaceae and Trichiaceae, while Ceratiomyxaceae, theas wellCeará as are in characterized the typical Caatinga by a worldwide vegetation distribution, (Figure 1; Cribrariaceae, Didymiaceae and Reticulariacae are andTables are 1-2). present Most in differentof the Trichiaceae ecosystems species across theknown Brazilian from represented by, at most, three species each (Figure 1). Arcyria insignis and A. magna

northeast (Cavalcanti 2002). Check List | Volume 6 | Issue 4 | 2010 556 Alves et al. | Myxomycetes, state of Ceará, northeastern Brazil

rosea and, more rarely, in the Caatinga, with records in eight of one record collected in humid forests in Ceará’s southern et al. mesoregion.var. are notable records since they are known only by fruticulosa, one of the four species which the nine states comprising the region (Cavalcanti constitute the family Ceratiomyxaceae, is cosmopolitan 2008). This species, previously known only from the Crato, and has a worldwide distribution (Rojas et al. 2008). In the in Ceará’s southern mesoregion (Cavalcanti and Putzke Brazilian northeast, it often occurs in humid forest areas 1998), was collected in an arboreal and open shrubby Caatinga environment, in the municipality of Pacujá, in Table 1. Ceará’s northwestern mesoregion (Tables 1-2).

Physical features and vegetationMunicipality of the municipalitiesAltitude (m) whereLongitude the myxobiota (w) wasLatitude explored (s) (CearáVegetation state, northeastern1 Brazil). Crato 426 PNTSF Graça TDF/OSC 39°24’34” 7°14’03” Ibiapina 878 PNTSF 179 40°45’51” 4°06’35” Itapipoca 108 OSC 40°52’16” 3°54’26” Pacujá 150 TDF/OSC 39°34’36” 3°29’37” Reriutaba 147 TDF/OSC 40°41’15” 4°03’16” Sobral OSC 40°39’25” 4°02’18” 69 40°14’54” 3°39’35” 1. PNTSF= Pluvio-Nebular Tropical Subperennial Forest; TDF= Thorny Deciduous Forest and OSC= Open Shrubby Caatinga. Table 2. Myxomycetes recorded from Ceará state, northeastern Brazil. * First record from Ceará. ** Cited as Dyctidium cancellatum (Batsch) T.Macbr.; *** Cited as Comatricha typhoides (F.H.Wigg.) Rostaf.

Mesoregion/Municipalities Taxa northwest north south graça ibiapina pacujá reriutaba sobral itapipoca crato CERATIOMYXACEAE Ceratiomyxa fruticulosa (O. F. Müll.) T. Macbr. + + CRIBRARIACEAE Cribraria cancellata + C. tenella Schrad. + Cribraria sp. (Batsch) Nann.-Bremek.** + DIDYMIACEAE (Pers.) Gray + D. intermedium J.Schröt.* + D. iridis (Ditmar) Fr. + PHYSARACEAE Badhamia affins Rostaf. + B. macrocarpa (Ces.) Rostaf. + B. melanospora Speg.* + B. panicea (Fr.) Rostaf.* + Craterium leucocephalum (Pers. ex J.F.Gmel.) Ditmar* + septica + + Physarum album + + P. compressum (L.) Alb. F.H.Wigg. and Schwein. + P. nucleatum Rex (Bull.) Chevall. + P. rigidum + P. stellatum (Massee) G.W.Martin + P. tenerum (G.Lister)Rex* G.Lister* + RETICULARIACEAE Dictydiaethalium plumbeum (Schumach.) Rostaf. + STEMONITACEAE Comatricha sp. + Stemonaria irregularis + S. longa + Stemonitis axifera (Bull.) (Rex) T.Macbr. Nann.-Bremek., R. Sharma and Y. Yamam. + S. flavogenita (Peck) E.Jahn Nann.-Bremek. , R. Sharma and Y. Yamam. + S. herbatica + S. pallida Wingate + S. splendens PeckRostaf. + + Stemonitopsis typhina + TRICHIACEAE Arcyria cinerea (Bull.) (F.H.Wigg.)Pers. Nann.-Bremek.*** + + + A. denudata + A. insignis Kalchbr. + A. magna (L.) rosea Wettst.* Rex + Hemitrichia calyculataand Cooke + + + + H. serpulavar. + + + + Metatrichia vesparia (Speg.) M.L.Farr + Perichaena (Scop.) depressa Rostaf. ex Lister + + + (Batsch) Nann.-Bremek. ex G.W. Martin and Alexop.* 08 07 02 01 27 Lib. TOTAL 03 03 Check List | Volume 6 | Issue 4 | 2010 557 Alves et al. | Myxomycetes, state of Ceará, northeastern Brazil

In the Brazilian northeast, the family Cribrariaceae is Estrada-Torres, A., D.W. Basanta, E.Fungal Conde Diversity and C. Lado. 2009. Myxomycetes associated with dryland ecosystems Flora Neotropica. of the Tehuacán-Cuicatlán Monograph 16. Valley New represented by 14 species, which represent nearly 30 % of Biosphere Reserve, Mexico. 36: 17-56. the recognized total for the family (Cavalcanti 2002;Cribraria Lado Farr,IPECE, M.L. Insti 1976.tuto deMyxomycetes. Pesquisa e Estratégia Econômica do Ceará. 2007. CearáYork, New em mapas, York Botanical 1.2.5. Unidades Garden. Fitoecológicas 304 p. . Electronic database cancellata2005-2010). and Alves C. tenella and Cavalcanti associated (1996), with the and humid Cavalcanti forest Captured on 25 inand the Putzke municipality (1998) of reportCrato. Both the species occurrence are characterized of February 2010. by a wide distribution across the Northeast with only a few accessible. at Nomenmyx http://www2.ipece.ce.gov.br/atlas/. - A nomenclatural Taxabase of Myxomycetes. records reported from the south and southeastern Lado, C. 2001 221Cuadernos p. de Trabajo de Flora Micológica Ibérica 16. Madrid: Consejo Superior deAn Investigaciones on-line nomenclatural Científicas, information Real Jardín systemBotánico. of 2002). Eumycetozoa of BrazilIn the (Cavalcanti current study, 2002; only Maimoni-Rodella one specimen from 2002; the Putzke family Lado,eumycetozoa.com. C. 2005-2010. Captured on 25 February 2010. was obtained, which was collected in the municipality . ElectronicMyxomycetes database accessible I. Ceratiomyxales, at http://www.nomen. Echinosteliales, of Graça, located on the region of the Caatinga, but in , . Flora Micologica Ibérica Lado,p. C. and F. Pando. 1997. , v.Ecologia 2. Berlim: e ConservaçãoCramer. 323 da Caatinga. a humid environment, on a dead fallen trunk, near a Leal, I.R., M.Tabarelli and J.M.C. Silva. (ed.). 2003. Recife: Editora Universitária da UFPE. 882 p. ofwaterfall, much in damaged the place sporocarps, known as thus “Bica only do Mazagão” allowing Lemos, J.R. and M.J.N. Rodal. 2002.Acta Fitossociologia Botanica Brasilica do componente [Mazagão springlet] (Tables 1-2). The Cribrariaspecimen), consisted but the lenhoso de umA monograph trecho da vegetaçãoof the de caatinga no Parque Nacional SerraMuseum da Capivara,of Natural Piauí, History. Brasil. 16(1): 23-42. characteristics of the peridial net are quite distinct from Lister, A. 1925. . 3a. ed., London: British confident identification to genus ( 296 p. state of Ceará. Maimoni-Rodella, R.C. 2002. Biodiversidade e distribuição de the other two species with a known occurrence for the 220mixomicetos In em ambientes naturais e antropogênicos no Brasil: Acknowledgments: This study was partially supported by Programa J.M.T.espécies Carneiro ocorrentes (ed.). Biodiversidade, nas Regiões Sudeste conservação e Centro-Oeste; e uso sustentávelp. 217- da flora do E.L. Brasil Araújo, A.N. Moura, E.V.S.B. Sampaio, L.M.S. Gestinari and

Biodiversidade PPBio grants from Conselho Nacional de Desenvolvimento . Recife: Universidade FederalThe Myxomycetes Rural de Pernambuco, Sociedade Botânica do Brasil. LiteratureCientífico e Tecnológico Cited - CNPq, and Federal University of Piauí – UFPI. Martin, G.W. and C.J. Alexopoulos. 1969. The. Iowa genera City: of MyxomycetesUniversity of Iowa Press. 561 p. (Arecaceae). Acta Botanica Brasilica Martin, G.W., C.J. Alexopoulos andA M.L. guide Far. to temperate 1983. Myxomycetes. Araújo,Alves, M.H. F.S., andE.V.S.B. L.H. Sampaio, Cavalcanti. M.A. 1996. Figueiredo, Myxomycetes M.J.N. Rodal em palmeiras and A.G. . Iowa City: University of Iowa Press. 561 p. 10(1): 1-7. Nannenga-Bremekamp, N.E. 1991. Revista Brasileira de Botânica 21 ,Bristol: Biopress Physaraceae, Limited. 409Physarum p. rigidum Fernandes. 1998. Composição florística da vegetação Memórias de carrasco, do Parente,Distribution M.P.M, M.F.A. extension Bezerra and andnew L.H.records. Cavalcanti. Check List 2009. Myxomycetes, InstitutoNovo Oriente, de Biociências CE. (2): 105-116. (G. Lister) G. Lister:In Cavalcanti, L.H. 1974. Mixomicetos novos para Pernambuco. 5(4): 759-762. Acta Botanica1(1): Brasilica 315-328. Putzke,Carneiro J. 2002. (ed.). Myxomycetes Biodiversidade, na Região conservação Sul do eBrasil; uso sustentável p. 221-223 da Cavalcanti, L.H. and J. Putzke. 1998. Myxomycetes da Chapada do floraE.L. Araújo, do Brasil A.N. Moura, E.V.S.B. Sampaio, L.M.S. Gestinari and J.M.T. (Crato-CE). 12(3): 257-265. Cavalcanti, L.H. 2002. Biodiversidade e distribuiçãoIn de mixomicetos em . Recife: Universidade Federal Rural2008. de Pernambuco,Microhabitat ambientes naturais e antropogênicos no Brasil: espécies ocorrentes andSociedade niche Botânica separation do inBrasil. species of Ceratiomyxa. Mycologia nasBiodiversidade, Regiões Norte conservação e Nordeste; e uso p. sustentável 209-216 da E.L. flora Araújo, do Brasil A.N.. Rojas, C., M. Schnittler, D. Biffi and S.L. Stephenson. Moura, E.V.S.B. Sampaio, L.M.S. Gestinari and J.M.T. Carneiro, (ed.). 2002. Ecorregiões: 100(6): Proposta843-850. para o Bioma Caatinga. Recife: Universidade Federal Rural de Pernambuco, Sociedade Velloso, A.L, E.V.S.B. Sampaio and F.G.C. Pareyn. ofBotânica Piauí, Northeast do Brasil. Brazil. Check List Recife: Associação Plantas Cavalcanti, L.H., M.P.M.P. Ponte and M. Mobin. 2006. Myxomycetes, State do Nordeste; Instituto de Conservação Ambiental The Nature Bezerra. 2008. Occurrence and distribution 2(2): 70-74. of the Ceratiomyxales Conservancy do Brasil. 76 p. Cavalcanti,(Myxomycetes) L.H., A.C.C. in northeastern Bezerra, A.A.A. Brazil. Costa, Brazilian I.N. Ferreira Archives and of Biology M.F.A. and Technology

51: 971-980. Received: May 2010 Costa, A.A.A., J.C.G. Tenório, I.N. Ferreira and L.H. Cavalcanti. 2009. Revised: August 2010 ActaMyxomycetes Botanica Brasilicade Floresta Atlântica: novas referências de Trichiales, Accepted: August 2010 Liceales e Stemonitales para o Estado da Paraíba, Nordeste do Brasil. Published online: October 2010 23(2): 313-322. Editorial responsibility: Matias J. Cafaro

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