Corticolous myxobiota of the Pernambuco Center of Endemism, Brazil

Situated within the Atlantic Forest domain, the Centro de Endemismo Pernambuco (Pernambuco Center of Endemism) CEPE is regarded as a priority for biodiversity conservation worldwide. Covering an area of approximately 56,000 km2, it encompasses part of the states of Alagoas, Pernambuco, Paraíba and Rio Grande do Norte in northeastern Brazil. Here we present an identifi cation key to 73 species of Myxomycetes that compose the known corticolous myxobiota of the Dense Ombrofi lous Lowland Forest, Semideciduous Lowland Forest, Restinga Forest and Mangrove environments of CEPE. Specimens included here were found developed in natural conditions in the fi eld or obtained through moist chamber culture. Among the species found, Arcyria cinerea, Clastoderma debaryanum, Cribraria confusa, C. violacea and Echinostelium minutum were the most common; and Comatricha longipila, Licea pedicellata, Paradiachaeopsis longipes, Perichaena calongei and Stemonaria fuscoides were the most rare. Our data indicates that the species richness of corticolous myxomycetes in rainforests is lower than that of temperate forests. Th ese same data also suggest that taxonomic diversity (mean number of species per genus) is similar to, or higher than, that found in temperate regions of the world.


Introduction
Myxomycetes (Amoebozoa) are unicellular phagotrophic eukaryotes that prey on fungus and bacteria, and occur in terrestrial environments as haploid, uninucleated myxamoebae and swarm cells or as diploid multinucleated plasmodium that produce fungus-like fruiting bodies (Gray & Alexopoulos 1968).About one third of the species of Myxomycetes have worldwide distribution, but some seem to be restricted to the tropics and others to temperate regions (Stephenson et al. 2008).Studies of soil microbiota shows the importance of this group of organisms to the ecosystems where they occur, serving as regulators of microbial populations of bacteria, yeasts and fi lamentous fungi and in nutrient cycling and mineralization (Keller & Everhart 2010; Stephenson & Feest 2012).
Myxomycetes are classified into ecological groups according to the microhabitats where they develop and sporulate, being lignicolous and foliicolous myxomycetes the most well-known (Ing 1994).Corticolous myxomycetes inhabit the bark of living shrubs and trees.Species typical of this ecological group generally produce sporangia up to 1 mm in height and usually have protoplasmodia (≤ 0.5 mm), which have low mobility and are capable of responding rapidly to environmental conditions that induce sporulation (Everhart & Keller 2008).Species of this group are not distributed randomly among the different environments where they are recorded, and neither occur with the same abundance throughout the year since their trophic stages are strongly influenced by temperature, moisture and substrate pH as well food availability (Madelin 1984;Tran et al. 2006).There is no evidence of endemism among species of myxomycetes, but differences in myxobiota composition between different types of microhabitats have already been observed (Novozhilov et al. 1999;2003;2006;Stephenson et al. 2000;Schnittler 2001).
Studies performed in tropical forests, which are characterized by high levels of pluviosity and air humidity, suggests that their myxomycete diversity is lower than that observed in temperate forests, and with low corticolous species richness (Stephenson et al. 2004).Analysing the composition of the corticolous myxobiota from temperate moist forest in the Great Smoky Mountains National Park (GSMNP), Snell & Keller (2003) recorded 84 species from moist-chambers mounted with samples obtained from 25 trees.In urban environments of the province of Madrid, Spain, 37 species were documented from 81 moist-chamber cultures mounted with bark of living Quercus ilex (Fagaceae) (Basanta 1998).
Studies focusing on the corticolous myxobiota of Brazil were initiated by Cavalcanti (1974), who recorded 20 species on the bark of 300 trees of the Cerrado biome, of which 13 taxa were obtained through moist-chamber culture.Bezerra & Cavalcanti (2007)  Aiming to expand up on the existing knowledge of the ecosystem distribution of myxomycetes in the Neotropics, this paper presents 73 corticolous species found in different forest environments of the CEPE and provides a key for their identification, based on records made between the years of 1970 and 2016.

Collection and identification
Inventory was based on field collections, moist-chamber culture and specimens deposited in the herbaria UFP, URM and IPA, for which identifications were confirmed or redetermined, and binomials updated according to Lado (2015).The monographs of Martin   An identification key is presented for all the corticolous species recorded at CEPE.After the species and author names, numbers representing the localities where the species were recorded are given as superscripts.

Identification key (index number show occurrence places at CEPE -see Study area)
Acta Botanica Brasilica -30(4): 549-559.October-December 2016 Southeast (SP) regions of Brazil, occurring as corticolous in Caatinga, Cerrado, Atlantic Forest and Mangrove (Cavalcanti 2015); it is one of the first to sporulate, and its sporangium can be observed within two to three days after culture initiation.Some corticolous species that occur in CEPE have been rarely recorded in Brazil.Among these are Perichaena calongei, Physarum  Considering the myxobiota from REBIO Saltinho, one of the most humid environments among the 12 areas explored for myxomycetes in the CEPE, the present work documented 21 species (ca. of 44% of the species currently known from CEPE), occurring in 256 moist-chambers with bark of living trees.Although this is greater than the number of corticolous species observed by Stephenson et al. (2004) in the rainforest of the Maquipucuna Reserve in Ecuador (14 spp), it is lower than that encountered in temperate forests by Snell & Keller (2003), who reported 84 species and 24 genera (S/G = 3.5) from 418 moist chamber cultures and Everhart & Keller (2008), who recorded 46 species and 20 genera (S/G = 2.3) in 580 moist chambers.
The data presented herein are consistent with the observation that tropical corticolous myxobiota are less rich than those of temperate regions.However, the taxonomic diversity recorded at REBIO Saltinho (S/G = 2.3) and CEPE (S/G= 2.8), are equal to, or higher than, that of some temperate forests (e.g., Snell & Keller 2003;Everhart & Keller 2008).
listed ten species found on 20 specimens of Terminalia cattapa (Combretaceae), during 12 months of study in urban environments in Recife, Pernambuco.In Restinga of the Parque Estadual Dunas do Natal, Bezerra et al. (2007) obtained only 12 species from 200 moistchamber plates prepared with cortex of trees typical of this vegetation.Distributed along the latitude of 28°, the Atlantic Forest is the second largest Neotropical forest, and is considered a biodiversity hotspot with numerous endemic species of different taxa distributed among centers of Brazilian endemism, including Centro de Endemismo Pernambuco (CEPE) (Tabarelli et al. 2006).Currently, information on corticolous myxomycetes occurring in the northeastern part of the Atlantic Forest and its associated ecosystems are scarce (Silva & Cavalcanti 2010; Damasceno et al. 2011; Cavalcanti et al. 2014).

Figure 1 .
Figure 1.Localization of the Pernambuco Center of Endemism in the Northeastern Region of Brazil.

ResultsA
total of 73 species was recorded from the cortex of living trees and shrubs of CEPE.The species belong to Myxogastromycetidae and Stemonitomycetidae and represent five orders, encompassing members of Clastodermataceae, Echinosteliaceae, Dictydiaethaliaceae, Reticulariaceae, Liceaceae, Arcyriaceae, Trichiaceae, Physaraceae, Didymiaceae and Stemonitaceae.
gyrosum, Licea biforis and L. pedicellata, which have been recorded in Ombrophilous Forest of Biological Reserve in the municipality of Saltinho, and Comatricha longipila, Paradiachaeopsis longipes and Physarum decipiens, which were found in Restinga vegetation of Dunas do Natal State Park.Perichaena calongei was reported in Brazil for the first time by Araujo et al. (2015), who obtained it from moist chamber culture mounted with dead leaves and bark of living trees from Cerrado in the state of Goiás.This species was recorded for the first time in the Northeast Region in Ombrophilous Dense Submontane Forest of the Atlantic Forest in the state of Bahia, by moist-chamber culture mounted with lianas collected at Private Reserve of Natural Heritage (RPPN) Serra do Teimoso and, subsequently, at CEPE in Restinga of RPPN Mata Estrela in the state of Rio Grande do Norte (Cavalcanti et al. 2016).