Occurrence and distribution of Perichaena ( Trichiaceae , Myxomycetes ) in the Brazilian Northeastern Region

Initially proposed by E. M. Fries in 1817, the genus Perichaena currently encompasses 34 species, with just under half (48%) being described between the years of 2000 and 2015, with type localities in countries of Africa, Asia, Europe, North, Central and South Americas (Novozhilov & Schnittler 2000; Wang et al. 2000; Yamamoto et al. 2002; Liu et al. 2007; Novozhilov et al. 2008; Estrada-Torres et al. 2009; Lado et al. 2009; 2014; Mitchell et al. 2011; Basanta et al. 2013; Ronikier et al. 2013; Lado 2015; Novozhilov & Stephenson 2015; Walker et al. 2015). In the Neotropics, where 16 species have already been noted, only P. calongei, P. megaspora and P. nigra have their type locality in South America (Lado & Basanta 2008; Lado et al. 2009; 2014; Ronikier et al. 2013). The genus is widely distributed in the Neotropical region, with records in 24 of the 31 countries where myxomycetes inventories have been conducted, with the greatest diversity being found in Mexico with 10 species, and Argentina and Ecuador, with six species each (Lado & Basanta 2008; Estrada-Torres et al. 2009; Lado et al. 2009; 2014; McHugh 2009; Rojas et al. 2013; Ronikier et al. 2013). The first record of the occurrence of a species of Perichaena in Brazil was based on a specimen of P. chrysosperma colABSTRACT The known distribution of Perichaena calongei, P. chrysosperma, P. corticalis, P. depressa, P. microspora, P. pedata and P. vermicularis in the nine states that comprise Brazil’s Northeast Region (1,548,672 km2) is presented herein, enhancing our understanding of the distribution of the genus Perichaena (Trichiaceae, Myxomycetes) in the Neotropics. This inventory encompasses a 100-year period (1914-2014), and analyzes material deposited in herbaria and collected by the authors. The collected material came from areas of thorny deciduous vegetation typical of the Caatinga biome and portions of savannah in the continent’s interior, rainforests, restingas (tropical moist broadleaf forests found along Brazil’s coastal spits) and mangroves of the Atlantic Forest biome along a coastal zone of approximately 3,000 km. Descriptions, illustrations, vegetational environments, microhabitats and distribution maps are given for each species. New records include Perichaena chrysosperma and P. depressa in the state of Maranhão, P. corticalis in the states of Bahia, Piauí, Rio Grande do Norte and Sergipe, P. calongei in the Northeast Region, and P. pedata in Brazil. This paper adds to the known types of macroclimates, elevation levels, vegetational environments and substrates for these species and provides a better understanding of their global distribution pattern.

The genus is widely distributed in the Neotropical region, with records in 24 of the 31 countries where myxomycetes inventories have been conducted, with the greatest diversity being found in Mexico with 10 species, and Argentina and Ecuador, with six species each (Lado & Basanta 2008;Estrada-Torres et al. 2009;Lado et al. 2009;2014;McHugh 2009;Rojas et al. 2013;Ronikier et al. 2013).The first record of the occurrence of a species of Perichaena in Brazil was based on a specimen of P. chrysosperma col-lected in the first decade of the 20 th century in the state of Santa Catarina, in the Southern Region of Brazil (Jahn 1902;Cavalcanti & Fortes 1994).Perichaena depressa has also been said to occur in the Southern Region of Brazil, having been found in the states of Santa Catarina and Rio Grande do Sul (Cavalcanti & Fortes 1995;Cavalcanti 2015).In the Northern Region, the first record of this genus was made near the end of the 20 th century based on a collection of an unidentified species found at the Maracá Ecological Station, in the state of Roraima (Cavalcanti et al. 1999); recently, P. longipes was described as occurring on aerial litter in the same state (Walker et al. 2015).In the Southeast Region, P. depressa, P. chrysosperma, P. microspora and P. vermicularis are all found in the states of São Paulo and Rio de Janeiro (Torrend 1915;Maimoni-Rodella & Gottsberger 1980;Hochgesand & Gottsberger 1996;Cavalcanti 2015).Perichaena depressa and P. vermicularis are known to occur in the Central-West Region from collections conducted in Cerrado environments at IBGE's Ecological Reserve in the Federal District (Carvalho et al. 2011). Recently, Araujo et al. (2015) documented P. calongei in Brazil for the first time, based on specimens collected in the National Forest of Silvânia, a conservation unit of Cerrado in the state of Goiás.
The first mention of the occurrence of Perichaena in the Brazilian Northeast Region was based on a specimen of P. chrysosperma collected early in the 20 th century in Belém da Cachoeira in the state of Bahia (Torrend 1915).The genus has been recorded in almost all states of the Northeast Region with the exception of Maranhão (Cavalcanti 1974a;2015;Cavalcanti & Marinho 1985;Góes & Cavalcanti 2002;Cavalcanti et al. 2006a;2006b;Alves et al. 2010;Bezerra et al. 2014).
Despite these records, additional information regarding the species of Perichaena in Brazil is sparse with only Cavalcanti (1974a) supplying information on the types of environment, microhabitats and seasonal variation of the species that occur in the state of Pernambuco: P. chrysosperma, P. depressa, P. corticalis, P. microspora and P. vermicularis.
Aiming to expand up on the existing knowledge of the geographic and ecosystem distribution of myxomycetes in the Neotropics, this study presents the species of Perichaena found in the different states of the Northeast Region of Brazil and provides the vegetational environments they occupy based on records made between the years of 1914 and 2014.

Study Region
One of South America's three major semi-arid areas is located in the Northeast Region of Brazil.It is characterized by low humidity, precipitation below evapotranspiration with irregular rainfall rhythms and extended periods of draught (Ab'Sáber 1999).Covering some 970,000 km 2 , it encompasses almost all of the Caatinga biome present in the states of Alagoas, Bahia, Ceará, Paraíba, Pernambuco, Piauí and Sergipe, with average rainfall below 800 mm/ year, an aridity index of up to 0.5 and high draught risk (MI 2005).Corresponding to climate, soil and topographical conditions, a wide variety of phytophisiognomies of xerophytic caatinga vegetation are found among the 1,113 municipalities of Brazil's semi-arid region (Prado 2003;Rodal et al. 2008)

Collection and identification
The following herbaria were consulted in order to verify the occurrence of species of Perichaena Fries in the nine states of the Northeast Region of Brazil: HUEFS, ICN, IPA, JPB, SP, TEPB, UB, UFBA, UFP, URM (Thiers 2014).Exsiccate identification was confirmed or redetermined and the binomials updated according to Lado (2015).The inventory was completed with specimens and samples of substrates collected by the authors between 1968 and 2014 (ca.200 study sites) in the states of Alagoas (AL), Bahia (BA), Ceará (CE), Maranhão (MA), Paraíba (PB), Pernambuco (PE), Piauí (PI), Rio Grande do Norte (RN) and Sergipe (SE) for preparing ca 6,500 moist chamber cultures (Härkönen 1981).Selected specimens were used to illustrate the sporocarps and taxonomically significant microstructures.Keys, illustrations and descriptions by Martin & Alexopoulos (1969); Farr (1976); Lado & Pando (1997) and Poulain et al. (2011) were used for species identification.Localities and corresponding geographical coordinates (based on field notes and exsiccate labels) were employed to construct distribution maps for the species using the QGIS 2.2 program.

Results and Discussion
In the six herbaria where exsiccates of Perichaena were found, 318 specimens of different levels of preservation and corresponding to seven species occurring in one or more states of Brazil's Northeast Region, were assessed.A list of voucher specimens, substrata and localities is provided in Tab.S1 in Supplementary material.We provide the first records of Perichaena chrysosperma and P. depressa for the state of Maranhão, P. corticalis for Bahia, Piauí, Rio Grande do Norte, and Sergipe, P. calongei for the Northeast Region, and P. pedata for Brazil.
Among the species of Perichaena recorded for Brazil's Northeast Region, P. depressa shows the widest distribution, with records in all states except Alagoas, while the remaining species were recorded from only one or two of the nine states.In this region of the country, these species are distributed amon g environments of savannah, steppical-savannah (=caatinga), rupestrian fields, highland and lowland forests, dense and open ombrophilous forests, semi-deciduous seasonal forests, riparian forests, coastal tablelands, restinga and mangrove forests, but they were most abundant in rainforests (Tab.1).In the several vegetational environments where they are found, on the most part, they sporulate on decomposing tree trunks, behaving also as corticolous, fimicolous, floricolous, foliicolous, lichenicolous, myceticolous and succulenticolous (Tab.2).
Perichaena, and the seven species of this genus that occur in the Northeast Region of Brazil, are described and commented on below.Perichaena Fr., Syst.Gasteromyc.: 11. 1817.
Described by Lado et al. (2009), P. calongei occurs in different localities distributed among the five states in northwestern Argentina in arid environments at high elevations; all specimens were obtained from the base of dead Puya sp.(Bromeliaceae) leaves, directly in the field or from moist chambers with a pH varying from neutral to slightly alkaline.The species was not found on other substrates or in cultures prepared with the remains of native plants from the same areas, which led the authors to conclude that microhabitat requirements are offered only by this type of Bromeliaceae.
Perichaena calongei is rare in Brazil, with only three records for the Northeast Region (this paper) and one for the National Forest of Silvânia (895-900 m), in the Central-West Region, found on decaying leaves and bark samples collected in a gallery forest and placed in moist chamber cultures (Araujo et al. 2015).Specimens were obtained from moist chambers assembled with lianas from the dense submontane ombrophilous forest in Bahia (RPPN Serra do Teimoso), bark of living trees on dense ombrophilous lowland forest (Saltinho Biological Reserve, PE) and with forest litter from Restinga forest (RPPN Estrela Forest), along the seashores of Rio Grande do Norte (Tabs.1-2).The data obtained in the present study increases the known types of macroclimates, elevations, vegetational environments and substrates for this  species and contributes to a better understanding of its global distribution pattern.
In Brazil's Northeast Region, P. chrysosperma can be found in natural environments as well as in urban parks, backyards and home gardens, sporulating in almost all months of the year, but reaching its peak in the rainy season (Cavalcanti 1974a).It is mostly lignicolous, however, it occupies other microhabitats as well, developing on the cortex of living trees, on ground litter and on succulent and plant inflorescences (Tab.2).It is distributed among different municipalities in the state of Bahia, Maranhão (first record), Paraíba, Pernambuco, Rio Grande do Norte and Sergipe, in pre-Amazonian forest environments, lowland dense ombrophilous forests, semi-deciduous seasonal forests, restinga forests, caatinga and rupestrian fields (Tab. 1).This is the first record of this species in a pre-Amazonian forest environment, as well as in an extremely dry environment such as the caatinga, in the microregion of Seridó Ocidental, in the state of Rio Grande do Norte.
In Brazil, the published records of this species were restricted to the Northeast Region, occurring in the states of Alagoas (Bezerra et al. 2014), Pernambuco (Farr 1960), Paraíba and Piauí (Cavalcanti 2015).The present study includes specimens collected in the Mesoregion of North Central Bahia (UFP 43420 and UFP 43447), and in the states of Sergipe and Rio Grande do Norte, in the wilderness of Seridó.In the environments in which it was recorded, P. corticalis occupies different microhabitats and can be lignicolous, foliicolous, corticolous or fimicolous in different types of vegetation from Caatinga (UFP 43428; UFP 43433 and UFP 43435), for which there were no previous occurrence records, to coastal rainforests (Tabs.1-2).
Despite its wide distribution in Brazil's northeast, the occurrence of P. depressa had not yet been recorded in the state of Maranhão, where it was collected in a pre-Amazonian rainforest environment, as well as in a steppical savannah environment with annual rainfall <500mm (municipality of Campo Formoso, BA) and in natural areas of Seridó, in Rio Grande do Norte.
Perichaena depressa is predominantly lignicolous (40% of the samples), however, it is also found in special microhabitats occasionally as a floricolous or a succulenticolous species, but it is also one of the two species of this genus present in the studied collections that is fimicolous in Brazil's Northeast Region (Tab.1).Penz. & Lister, in Penzig, Myxomyc. Fl. Buitenzorg 76. 1898.Fig. 3A-E.

Perichaena microspora
Hypothallus inconspicuous.Plasmodiocarp of varying length, sometimes reticulated, 250-350 μm diam., pink-salmon to ochraceous.Peridium simple, yellow, membranose, inner surface with grains of refused material close to the base of the sporocarp.Capillitium loose, yellowish-pink, filaments almost hyaline by transmitted With few records in European, Asiatic and North American countries, P. microspora is rare in the Neotropics, with known occurrences only in Cuba, Costa Rica and Brazil (Lado & Basanta 2008;Cavalcanti 2015).Torrend (1916) included P. microspora in his list of species for the state of Bahia.However, exsiccates were not located in the collection of the URM herbarium, where almost all collections made by him in Brazil were deposited.Exsiccate UFP 5070 was collected in Pernambuco in 1980 in a semi-deciduous seasonal forest environment, on dead leaves (Tabs.1-2) and identified in the same year by one of the authors.It was recorded in the Southeast Region for the first time by Cavalcanti (2015), based on an exsiccate deposited at the MA -fungi Herbarium, collected also in a semi-deciduous seasonal forest environment in the state of São Paulo by C. Lado & R. C. Maimoni-Rodella.(Lister & G. Lister) Lister ex E. Jahn, Ber. Deutsch. Bot. Ges. 36: 667. 1919.Fig. 3A, F-I.
The collection of the UFP herbarium has nine specimens of P. vermicularis, predominantly collected on the Laise de Holanda Cavalcanti, Andrea Carla Caldas Bezerra, David Itallo Barbosa, Leandro de Almeida Neves Nepomuceno Agra, Nestor Valente Powell, Vitor Xavier de Lima and Antônia Aurelice Aurélio Costa cortex of living trees and occasionally on dead tree trunks in parks and residential gardens (Tabs.1-2).The occurrence of P. vermicularis on the cortex of living trees has been recorded by different authors, such as Basanta (1998, on the cortex of Quercus ilex, Fagaceae) in Spain and by Cavalcanti (1974b) on Vochysia tucanorum (Vochysiaceae) and Aspidosperma tomentosum (Apocynaceae) in the cerrado of Emas, São Paulo.
The species is uncommon in the Northeast Region, with a few records in the municipalities of Recife and Olinda, in Pernambuco (Cavalcanti 1974a;Bezerra & Cavalcanti 2007) and in Lençóis, BA, in the Diamantina Plateau (Gusmão et al. 2005).In Pernambuco, all exsiccates were collected in an urban environment (Tab.1).Specimens collected on living tree trunks of Terminalia catappa (Combretaceae), in Olinda, PE, about 1 km from the coastline, showed small plasmodiocarps, with scanty capillitium and with spores of smaller diameter than normally described for the species, as also observed by Lado & Pando (1997).The remaining characteristics are typical for the species.In Bahia, it was found in the APA of Marimbus (HUEFS 84703), that encompasses a variety of ecosystems such as rupestrian fields, savannahs, steppical savannahs and seasonal forests, aside from marimbús, marsh-like environments into which most of the water of the Diamantina Plateau is drained (Tab.1).Aside from the Northeast Region, P. vermicularis has been known to occur towards the Central-West Region (Federal District) in an environment of Cerrado and in the Southeast Region (SP), in Atlantic Forest (Cavalcanti 2015).

Table 2 .
Microhabitats in which species of Perichaena Fr. occur in Brazil's Northeast Region