Myxobiota of the Brazilian Atlantic Forest : species on oil palm tree ( Elaeis guineensis , Arecaceae )

Programa de Pós-Graduação em Ciências Biológicas, Centro de Ciências Biológicas (CCB), Universidade Federal de Pernambuco, Av. Prof. Moraes Rego s/n, Cidade Universitária, 50.670-90, Recife, PE, Brasil. Professor Titular, Departamento de Botânica, CCB, UFPE; Pesquisador CNPq 1A. Apoio financeiro: CNPq. Autor para correspondência: laise@pq.cnpq.br Abstract Elaeis guineensis Jacq. (Arecaceae), the oil palm tree, serves as a phorophyte for many different groups of organisms, some of which help decompose organic matter coming from the organs of the tree itself or from remains of other plants retained in leaf sheaths. To study the myxobiota of E. guineensis, we examined living and dead trunks, leaves, bracts and inflorescences in the Gurjaú Ecological Reserve, in the township of Cabo de Santo Agostinho, Pernambuco, Brazil. Incidence and species abundance were determined in three Atlantic forest fragments. The reported species are listed herein, followed the known distribution of each species in Brazil, and which of them occur on palm trees. All of the subclasses and five orders were recorded and 22 species were added to the list of myxomycetes associated with oil palm trees in Brazil. The highest incidence value was recorded on dead leaves. Ceratiomyxa fruticulosa (O. F. Müll.) T. Macbr., Arcyria cinerea (Bull.) Pers. and Physarum compressum Alb. & Schwein. were the most common species, while Hemitrichia serpula (Scop.) Rostaf. ex Lister showed the highest levels of abundance and incidence, thus confirming its preference for the substrates provided by palm trees.

Myxobiota of the Brazilian Atlantic Forest: Myxobiota of the Brazilian Atlantic Forest: Myxobiota of the Brazilian Atlantic Forest: Myxobiota of the Brazilian Atlantic Forest: Myxobiota of the Brazilian Atlantic Forest: s s s s species on oil palm pecies on oil palm pecies on oil palm pecies on oil palm pecies on oil palm tree ( tree ( tree ( tree ( tree (Elaeis guineensis

Introduction
The oil palm tree (Elaeis guineensis Jacq.) arrived in Brazil, where it spread rapidly and is popularly known as dendezeiro, with the African slaves during the colonial period.Although it is exotic, it has been integrated into both the landscape and the culture of northeastern Brazil.In addition to the traditional use of the oil obtained from its fruit pulp and almond in industry and cooking, the recent use of its oil as biofuel makes it economically very important.At present, it is also used as an ornamental tree in streets, parks, and plazas in Pernambuco and other states (Lorenzi et al. 1996).This species can be found in fragments of the Silva,C.F & Cavalcanti, L.H Atlantic Forest in the Northeast Region and it is included in the list of mystical-religious plants used in the Afro-Brazilian umbanda and candomblé religious rituals (Albuquerque 1997).
The oil palm tree serves as a phorophyte (primary substrate) for several different groups of living organisms, some of which, including myxomycetes, help decompose organic matter coming from organs of the tree itself or from remains of other plants that are retained by leaf sheaths that remains attached to the trunk after senescence.
To contribute to the knowledge on the microhabitats available to myxomycetes in the Atlantic Forest and continue the ongoing survey of specimens of this group associated with palm trees in Brazil, a study of the incidence of sporocarps on the different organs of individuals of Elaeis guineensis growing in fragments of Atlantic Forest was carried out.

Material and Methods
The incidence of myxomycetes on Elaeis guineensis along with the distribution and abundance of sporocarps on trunks, leaves, bracts, inflorescences, and fruits (living or dead) were analyzed in the Café (6.852 ha), Cuxio (118.457ha), and São Braz (37.068 ha) forests, in the Gurjaú Ecological Reserve (8º14'21,7"S and 35º03'00,4"W), municipality of Cabo de Santo Agostinho, in the humid forest subzone of the state of Pernambuco.
The material collected (63 specimens) was curated and representative exsiccates were deposited at the UFP Herbarium.Species identification used the keys and descriptions found in Martin & Alexopoulos (1969), Farr (1976), andLado &Pando (1997).The classification used follows that of Martin et al. (1983).
The incidence percentage per individual and plant organ serving as a substrate was calculated; abundance was evaluated for each species according to the criteria of Novozhilov et al. (2001), which is based on the relationship between the number of specimens for a given taxon and the total number of records of myxomycetes for the substrate analyzed.Accordingly, the species were placed into the following categories: R -rare (0.5-1%), Ooccasional (2-4%), C -common (5-7%), and Aabundant (over 7%).The following data were listed after the name of each species: abundance, number of records obtained for each organ (Bct-bract; Trktrunk; Lf -leaf; Ifl -inflorescence), and whether the organ was living (Lv) or dead (Dd). The
Five of the six orders and 50 % of the families recognized for this class by Martin et al. (1983) are represented among the 63 specimens collected in the present study.These records increase the number of species of myxomycetes reported on oil palm tree to 25, two of which, Ceratiomyxa sphaerosperma Boedijn and Didymium anellus Morgan, had never been recorded as occurring on any species of palm tree in Brazil.

List of taxa associated to Elaeis guineensis
Ceratiomyxomycetidae -This subclass comprises only the order Ceratiomyxales, with a single family and genus including four species (Lado 2001).Two species were recorded in this study.
(C) (4/LfDd, 1/IflDd) Cosmopolitan and widely distributed in Brazil, this species had already been recorded on palm trees in the states of Ceará and Piauí (Alves & Cavalcanti 1996;Mobin & Cavalcanti 2000;Cavalcanti & Mobin 2004).In this study, the specimens were found on dead leaves and inflorescences (Tabs.1-2); it was common on oil palm trees in the São Braz and Café Forests.

Ceratiomyxa sphaerosperma
(O) (2/IflDd) Predominantly tropical and rarely cited in Brazil, C. sphaerosperma has been reported to occur as a lignicolous species in the Atlantic and Amazonian forests (Farr 1985;Cavalcanti 2002;Cavalcanti et al. 2008).In this study, it was only recorded in the São Braz Forest, where it was occasionally found on dead inflorescences of oil palm trees (Tabs.1-2); both specimens were very typical.This is a new record on palm trees in Brazil.
(C) (1/TrkDd, 2/TrkLv, 1/IflDd, 1/LfDd) This is a cosmopolitan species distributed in all regions of Brazil that was found on palm trees in the states of Pernambuco, Ceará and Piauí (Pôrto et al. 1985;Alves & Cavalcanti 1996;Mobin & Cavalcanti 2001).This species presents great morphological variations and, in the studied material, the variation in sporocarp size is striking.However, these characteristics are typical of the species, which is common on oil palm trees, where it develops on several different organs (Tabs.1-2).
(O) (1/TrkLv, 2/LfDd) A cosmopolitan species, C. microcarpa is found in all regions of Brazil, but has only been reported to occur on palm trees in the state of Piauí (Mobin & Cavalcanti 1998;Cavalcanti & Mobin 2004).In this study it was occasionally found on oil palm trees (Tab.2) of the Café Forest, and the specimens analyzed, obtained on dead leaves and living trunks (Tab.1), presented the typical characteristics of this species.
Records of associations with palm tree species in Brazil: A. vulgare; M. flexuosa.

Didymium anellus
(C) (1/BctDd, 3/IflDd) Until 2005, this species had only been recorded in the state of São Paulo (Hochgesand & Gottsberger 1996).Cavalcanti et al. (2006) reported D. anellus for the first time in the Northeastern region.This is the first record of D. anellus on palm trees in Brazil.The characteristics of the sporocarps -long plasmodiocarps or globose, sessile sporangia-are typical of this species.All the specimens were collected in the São Braz Forest, where it was common on oil palm trees.
Distribution in Brazil: Southeast (SP), Northeast (PE).(R) (1/IflDd) Recorded in a few states in northern and northeastern Brazil, D. clavus was found solely on palm trees in Piauí, in savanna ("cerrado") and alluvial forest environments (Mobin & Cavalcanti 1999a, 2000;Cavalcanti & Mobin 2004).In this study, it was rare on oil palm trees and was recorded only on an inflorescence (Tabs.1-2) in the Cuxio Forest.
Records of associations with palm tree species in Brazil: A. vulgare; C. prunifera.
(O) (3/IflDd) The three specimens encountered on the inflorescences (Tab. 1) of a single oil palm tree in the Cuxio Forest clearly belong to the complex encompassing D. nigripes, D. bahiense, and D. iridis, yet they could not be identified to species because they lacked the columella typically found in such species.
(R) (1/IflDd) Although this species is rarely collected, it seems to be common in the Neotropical region, where it occurs on leaves and bark of living trees.Rarely collected in Brazil and on oil palm trees (Cavalcanti et al. 2006), a single specimen was found in this study, in the Café Forest, on inflorescences along with sporocarps of a member of Physarales (Tabs.1-2).Sporocarps were very typical, with conspicuous dark projections on the peridium.Only their pedicel size varied and it was longer than in the descriptions found in the literature.
Records of associations with palm tree species in Brazil: E. guineensis.
Records of associations with palm tree species in Brazil: A. vulgare; A. speciosa; M. flexuosa.
(C) (4/LfDd) This species is widely distributed throughout the world.In Brazil, this is the first record on oil palm trees, although it had already been encountered on palm trees in São Paulo and Piauí (Hochgesand & Gottsberger 1996;Mobin & Cavalcanti 1998, 2000;Cavalcanti & Mobin 2004).It was common on E. guineensis and was found exclusively on the leaves of individuals in the Cuxio and Café Forests (Tabs.1-2).
Records of associations with palm tree species in Brazil: A. vulgare; A. speciosa; M. flexuosa.
In this study, a single specimen was encountered on an oil palm tree, one of the few species found on living bract (Tabs.1-2).
Records of associations with palm tree species in Brazil: A. vulgare; M. flexuosa.
Records of associations with palm tree species in Brazil: A. speciosa; C. nucifera; E. guineensis; M. flexuosa.
(R) (1/LfDd) Widely distributed in Brazil, this species has been reported to occur on palm trees of the genus Astrocaryum in the states of São Paulo and Piauí, under the name P. nutans Pers.(Hochgesand & Gottsberger 1996;Mobin & Cavalcanti 1999a;Cavalcanti & Mobin 2004).Rare on oil palm trees (on which it is recorded for the first time), a single Silva,C.F & Cavalcanti, L.H specimen was obtained on a dead leaf in the Café Forest.The sporocarps of this specimen were quite typical (Tabs.1-2).
Records of associations with palm tree species in Brazil: A. vulgare; Astrocaryum sp.
Records of associations with palm tree species in Brazil: A. speciosa.

Physarum compressum
(C) (5/IflDd ) Common on palm trees, with records in different states and regions, P. compressum is one of the four species that had been previously cited as occurring on oil palm trees in Brazil (Pôrto et al. 1985).It was found in the Café and São Braz Forests, predominately on inflorescences (Tab.1), confirming its place in the floricolous group, as observed among the Zingiberales by Schnittler & Stephenson (2002) in Ecuador, Costa Rica, and Puerto Rico.The form of the sporocarps varied considerably, yet within what should be expected for this species.
Records of associations with palm tree species in Brazil: C. nucifera; E. guineensis; Mauritia vinifera Mart.

Physarum crateriforme
(R) (1/IflDd) Rare in Brazil and on the studied substrate, this is its first record on oil palm trees, although it had already been found on unidentified palm trees in Pernambuco (Pôrto et al. 1985).The only specimen obtained was collected in the São Braz Forest, on a dead inflorescence, with very typical sporangia (Tabs.1-2).

Physarum gyrosum
(R) (1/TrkLv) Reported only in Pernambuco, P. gyrosum had not yet been observed on palm trees in Brazil, and it occurred rarely on oil palm trees in this study.The specimen was typical of this species, one of the few that sporulated on living trunks (Tab.1).
(R) (1/LfDd) This species, which occurs in all regions of the country, was observed on palm trees in the states of São Paulo, Ceará, and Piauí (Hochgesand & Gottsberger 1996;Alves & Cavalcanti 1996;Mobin & Cavalcanti 1998, 1999a;Cavalcanti & Mobin 2004).Frequent in other areas of the Atlantic forest, mainly as a lignicolous species, it was rare on oil palm trees, being collected only once in the Café Forest, on dead leaves (Tabs.1-2).
Records of associations with palm tree species in Brazil: A. vulgare; M. flexuosa.
(O) (2/LfDd) Physarum viride was occasionally encountered on oil palm trees and this is the first record of its occurrence on this kind of substrate.It is cited on other palm trees in the states of Amazonas, Piauí, and São Paulo (Farr 1985;Hochgesand & Gottsberger 1996;Mobin & Cavalcanti 1999a;Cavalcanti & Mobin 2004).
The two specimens analyzed, collected on dead leaves in the Café Forest (Tab.1), had the characteristics of var.aurantium (Bull.)Lister as referred to by Lado (2001)  Stemonitomycetidae -This subclass comprises only one order (Stemonitales) and one family (Stemonitaceae), with 16 genera and 202 species (Lado 2001).In this study, the three species found on E. guineensis belong to genera Stemonitis and Stemonitopsis.(O) (2/LfDd) Cosmopolitan and widely distributed throughout the different regions of Brazil, this species was found solely on palm trees in Piauí (Mobin & Cavalcanti 1998, 1999b;Cavalcanti & Mobin 2004).Cavalcanti et al. (2006) mentions S. fusca in the Gurjaú Ecological Reserve, on different substrates.In this study, this species was occasionally encountered on oil palm trees, and the fruiting bodies of one of the specimens collected on leaves in the Café Forest, had the characteristics of S. fusca var.nigrescens (Rex) Torrend, currently listed as a synonym of S. fusca by Lado (2001).

Stemonitis fusca
Records of associations with palm tree species in Brazil: A. vulgare; C. prunifera; M. flexuosa.

Stemonitis splendens
(R) (1/TrkLv) This cosmopolitan species is widely distributed in Brazil, with records in a different number of states, and in the Gurjaú Ecological Reserve (Cavalcanti et al. 2006).In this study, it was rare on oil palm trees, and was collected on living trunk in the Café Forest (Tabs.1-2).The characteristics of its fruiting bodies are typical of this species, already reported to grow on palm trees in the state of Piauí (Mobin & Cavalcanti 1998, 1999b;Cavalcanti & Mobin 2004), but not yet on oil palm trees.
Records of associations with palm tree species in Brazil: M. flexuosa.
(R) (1/ Trk Lv) Widely distributed in Brazil, this cosmopolitan species has been reported to occur on palm trees in the state of Piauí under the name Comatricha typhoides (Bull.)Rostaf.(Mobin & Cavalcanti 1998;Cavalcanti & Mobin 2004).Although it is cited by Cavalcanti et al. (2006) in the Gurjaú Ecological Reserve as sporulating on different substrates, S. typhina was rare on the oil palm trees analyzed in this study, and was collected on one living trunk (Tabs.1-2).
Records of associations with palm tree species in Brazil: A. vulgare; A. speciosa; M. flexuosa.
Species incidence and abundance in the microhabitat: The incidence of myxomycetes on E. guineensis was found to be high (40-80%).On the individuals studied, sporocarps were distributed over almost all of the organs analyzed, except for fruits (Tab.1).When comparing the myxobiota found on three savanna and alluvial forest palm tree species in the Sete Cidades National Park, Cavalcanti & Mobin (2004) concluded that leaves are the most common organ for myxomycete occurrence on A. vulgare, C. prunifera, and M. flexuosa.On oil palm trees, incidence was higher on leaves, although it did not differ much from that on inflorescences.
The association of A. cinerea, H. serpula, P. chrysosperma, and P. compressum with palm trees does not seem to be occasional, as they are mentioned by almost all the authors who have examined the relationship between myxomycetes and species in the family Arecaceae.In the Sete Cidades National Park, Mobin & Cavalcanti (1998, 2000) observed 70% incidence on C. prunifera (savanna) and 100% on M. flexuosa (alluvial forest), although they only obtained 34 and 98 specimens, respectively (16-26 species).When comparing the list of species associated to these palm trees, we observed that between 50% and 60% of those recorded on A. speciosa and M. flexuosa were present on the oil palm trees analyzed.
Species richness can be considered high for the oil palm trees analyzed; however, the species recorded are mostly rare or occasional (Tab.2).As shown by Pôrto et al. (1985), Alves & Cavalcanti (1996), Mobin & Cavalcanti (1998, 1999a, 2000) and Silva,C.F & Cavalcanti, L.H Cavalcanti & Mobin (2004), H. serpula and A. cinerea are frequently associated with palm trees in northeastern Brazil.In the Ecological Reserve of the Atlantic Forest studied in the present study, H. serpula showed the highest levels of abundance and incidence on oil palm trees, confirming they prefer association with palm trees.

Table 1 -
Incidence of myxomycetes on the different organs of Elaeis guineensis Jacq., based on data colleted in the Gurjaú Ecological Reserve, Pernambuco State, Brazil.Note: Dd = dead, Lv = living.

Table 2 -
Abundance of 24 species of myxomycetes on different organs of Elaeis guineensis Jacq.(Gurjaú Ecological Reserve, Pernambuco state, Brazil) in the synonymy given for P. viride.Myxobiota of Atlantic Florest: species on Elaeis guineensis Collected on dead leaves in the São Braz Forest, this specimen was colonized by fungi.Identification was limited to the genus level, although it was clearly different from the other species of Physarum studied.