Ascomycota in the litter of Inga edulis and Lafoensia pacari in an Atlantic Forest remnant in southeastern Bahia state, Brazil

Abstract

The Ascomycota population in the litter of Inga edulis and Lafoensia pacari trees was identified and its richness was evaluated. The collections were carried out from October 2018 to July 2019. Twenty fallen leaves were collected in different stages of decomposition. The leaf samples were carefully washed in running water and incubated in humid chambers. The fungal structures were mounted in PVLG resin and observed under a light microscope. The identification was done by consulting the specific literature. Distribution studies included richness, frequency, constancy, and similarity of the fungal populations. The total richness was 48 species and 36 genera corresponding to 58.33% in I. edulis and 60.41% in L. pacari. Most taxa had sporadic frequency and accidental constancy. There was low similarity between plant species. Ascomycota populations are well represented in Inga edulis and Lafoensia pacari litter. Richness, frequency, constancy, and similarity of these populations varied little in function of the collection date, climate and host plant. Lower richness observed in the second collection may reflect the effect of reduced humidity observed in that time of the year.

Full text

Rodriguésia 73: e00052021. 2022
http://rodriguesia.jbrj.gov.br
DOI: http://dx.doi.org/10.1590/2175-7860202273040
Abstract
The Ascomycota population in the litter of Inga edulis and Lafoensia pacari trees was identified and its richness
was evaluated. The collections were carried out from October 2018 to July 2019. Twenty fallen leaves were
collected in different stages of decomposition. The leaf samples were carefully washed in running water and
incubated in humid chambers. The fungal structures were mounted in PVLG resin and observed under a light
microscope. The identification was done by consulting the specific literature. Distribution studies included
richness, frequency, constancy, and similarity of the fungal populations. The total richness was 48 species and
36 genera corresponding to 58.33% in I. edulis and 60.41% in L. pacari. Most taxa had sporadic frequency
and accidental constancy. There was low similarity between plant species. Ascomycota populations are well
represented in Inga edulis and Lafoensia pacari litter. Richness, frequency, constancy, and similarity of these
populations varied little in function of the collection date, climate and host plant. Lower richness observed in
the second collection may reflect the effect of reduced humidity observed in that time of the year.
Key words: decomposing fungi, Fabaceae, Fungi, Lythraceae.
Resumo
A população de Ascomycota na serapilheira das árvores Inga edulis e Lafoensia pacari foi identificada
e avaliada a sua riqueza. As coletas foram realizadas no período de outubro de 2018 a julho de 2019.
Foram coletadas 20 folhas caídas em diferentes estágios de decomposição. As amostras de folhas foram
cuidadosamente lavadas em água corrente e incubadas em câmaras úmidas. As estruturas do fungo foram
montadas em resina PVLG e observadas ao microscópio de luz. A identificação foi realizada consultando a
literatura específica. A riqueza total foi de 48 espécies e 36 gêneros correspondendo a 58,33% em I. edulis e
60,41% em L. pacari. A maioria dos táxons possui freqüência esporádica e constância acidental. Houve baixa
similaridade entre as espécies de plantas. Inga edulis e L. pacari possuem grandes populações de Ascomycota
na separilheira delas. A riqueza, freqüência, constância e similaridade dessas populações variaram pouco
em função da época de coleta, clima e planta hospedeira. A baixa riqueza observada na segunda coleta pode
refletir o efeito da menor umidade observada naquela época do ano.
Palavras-chave: fungos em decomposição, Fabaceae, Fungi, Lythraceae.
Original Paper
Ascomycota in the litter of Inga edulis and Lafoensia pacari
in an Atlantic Forest remnant in southeastern Bahia state, Brazil
Priscila Silva Miranda1,5,7, Thaiana Santos Oliveira1,6, Edna Dora Martins Newman Luz2,
Maiara Araújo Lima dos Santos3 & José Luiz Bezerra4
1 UESC - State University of Santa Cruz, Postgraduate Course in Crop Science, Ilhéus, BA, Brazil.
2 Cocoa Research Center, Executive Committee of the Cocoa Crop Plan - CEPLAC, Ilhéus, BA, Brazil. ORCID: < https://orcid.org/0000-0003-1295-3960>.
3 Federal University of Pernambuco, Department of Mycology, Post Graduation in Fungi Biology, Recife, PE, Brazil. ORCID: < http://orcid.org/0000-0002-
7470-9405>.
4 UFRB - Federal University of Recôncavo da Bahia, Phytopathology CAPES/UFRB, Centro, Cruz das Almas, BA, Brazil. ORCID: < https://orcid.org/0000-
0002-7917-3400>.
5 ORCID: < https://orcid.org/0000-0001-6480-7805>
6 ORCID: < https://orcid.org/0000-0002-3508-9012>
7 Author for correspondence: miranda.priscila48@gmail.com

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Introduction
The Atlantic Forest is the most biodiverse
tropical forest in the world, with an estimated
20,000 plant species and 2,420 vertebrates,
including endemic and endangered species
(Rezende et al. 2018). Being considered as a
worldwide hotspot (Mittermeier et al. 2011).
Unfortunately, its diversity has been threatened by
anthropogenic actions since the discovery of Brazil,
with the extraction of brazilwood (Caesalpinia
echinata Lam.) (Sanquetta 2008). This biome
includes countless species of living organisms
some of which yet unknown to science (Paglia &
Pinto 2010).
The fragments of the Atlantic Forest have plant
and soil heterogeneity and diverse microclimatic
characteristics generating a large amount of organic
matter very rich in microorganisms (Marques et
al 2007; Santos et al. 2011). The organic matter
accumulated on the soil surface consists mainly of
dead plant material (leaves, wood, roots, branches,
fruits and flowers) and functions as a reservoir of
biodiversity organisms (Penna-firme & Oliveira
2017; Santa-Izabel & Gusmão 2018). In addition,
forest productivity can be estimated by the rate
of litter decomposition responsible for nutrient
cycling (Penna-Firme & Oliveira 2017).
Litter fungi along with other organisms
guarantee the cycling of nutrients, essential
for the nutrient balance in forest ecosystems
(Hättenschwiller et al. 2011). Fungi exhibit great
morphological and physiological adaptations to
this type of environment and their activity depend
on many ecological factors including temperature
and humidity at ground level (Marques et al. 2008).
A number of researchers studied the fungal
population in the Atlantic Forest litter seeking for
the relations of litter fungi to plant species, time
of the year and geographical location (Magalhães
et al. 2011; Costa & Gusmão 2015; Santos et al.
2017; Santa Izabel & Gusmão 2018; Grandi &
Silva 2003; Paulus et al. 2006; Morath et al. 2012).
The tree species Inga edulis Mart. (Fabaceae)
and Lafoensia pacari A. St.-Hil. (Lythraceae)
are widely distributed in tropical and subtropical
forests (Dias et al. 2010) and both are important
for restoring riparian forests and degraded areas
(Barbosa et al. 2017).
The mycobiota associated with litter of these
plants had not been studied and the main objective
of this research was to explore the Ascomycota
fungi associated with them and study their
population distribution.
Materials and Methods
Study area
Collections and analyses were carried out at
the Executive Committee of the Cocoa Farming Plan
- CEPLAC, of the Ministry of Agriculture - MAPA.
The area is located at km 22 of the Jorge Amado
highway, municipality of Ilhéus, Bahia, Brazil
(latitude: 14º47’20”S; longitude: 39º02’58”W).
This locality is inserted in the central corridor of the
Atlantic Forest, formed by the dense ombrophilous
forest, belonging to the neotropical zone (Veloso
et al. 1991). The climate in the region, according
to the Köppen classification, is of the Af type, hot
and humid tropical forest without a dry season,
with an average rainfall of 1,300 mm distributed
throughout the year, an average temperature of
23 °C and relative air humidity 80%. The soil of
the experimental area was classified as Nutrosolo
Háplico Eutroferrico as Santana et al. (2002).
Collection
The authors collected litter from two individuals
of Inga edulis (14°45’25”S and 39°14’23”W)
and two of Lafoensia pacari (14°45’26”S and
39°14’23”W) located in the experimental area H’ of
CEPEC/CEPLAC from October 2018 to July 2019.
They used 50 × 50 cm (0.25 m²) square frames to
mark areas under the trees to pick 20 leaves of each
plant species at different stages of decomposition.
The samples were transported to the Fungal
Diversity Laboratory of CEPLAC for processing. On
July 26, 2018, the climate conditions were: average
temperature 23.7 °C, 97 mm of rain in the month,
humidity of 85%; on March 12, 2019, were: average
temperature 25.5 °C, rain 125 mm/ in the month,
humidity 82% and on July 5, 2019, were: average
temperature 21.6 °C, rain 109 mm/ in the month,
humidity of 86%.
Samples processing
The samples were cleansed gently in plastic
sieves for one hour in tap water. After cleaning
the leaves were placed in moist chambers made
of plastic containers which were opened daily
for fifteen minutes for air renewal, according
to Castañeda-Ruiz et al. (2006). Stereoscopic
observation of the samples started 48 h after
incubation during 30 days.
Fungal characterization
Fungal structures (somatic, reproductive and
resistance structures) were mounted in permanent

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mounting medium (PVLG resin: polyvinyl alcohol
+ lactoglycerol) (Morton et al. 1993), between
microscope slides and coverslips. The preparations
were examined in a light microscope provided with
a photographic camera and a micrometric ocular.
The structures were interpreted, measured and
photographed. Species identification was achieved
through specific literature consultation.
Fungal population estimation
The variation of Ascomycota population
was based on estimation of richness, frequency,
constancy, and similarity of the species found.
Richness was defined as the total number of
species found in the collection sites and in each
plant species (Brower et al. 1998).
The calculation of frequency of occurrence
was based on the following formula:
F = n x 100/N
Where: n = number of samples in which a
species was found; N = total sample in each plant
species (2 plant species × 3 collections = 6).
Frequencies were classified according to
the classes proposed by Dajoz (1983), adapted
as: Sporadic, when found only in one collection;
Uncommon, when found in two collections;
Frequent, when found in three collections, but in
only one species; and Very Frequent, when found
in three collections and in both plant species.
To calculate constancy, the following formula
was used:
C = p.100/P
Where: p = number of collections in which
a fungal species was found; P = total number of
collections (three collections).
Constancy was classified as: Accidental,
when less than or equal to 33%, that is, present
in only one collection in this study; Accessory,
when greater than 50% and less than or equal to
66%, present in 2 collections; and Constant, when
greater than 66%, present in three collections.
The methodology was adapted from Cavalcanti &
Mobim (2004).
Similarity was obtained from the Sorensen
Index (Muller-Dombois 1981), using the following
formula:
S = 2c.100/a + b
Where: c = number of fungi common to both
plant species; a + b = number of fungi present on
the trees.
The three collections were compared
according to the following formula:
S = 3d.100/a + b + c
Where: d = number of fungi common to
the three collections; a + b + c = number of fungi
present in the collections.
The analyses were conducted in the PAST
3:01.
Results and Discussion
A total of 48 fungal taxa were identified
inserted in 37 genera. Inga edulis litter yieldd 28
taxa included in 18 genera and Lafoensia pacari
29 taxa in 26 genera. All taxa identified in the
present study are reported as decomposers of
plant substrates of various plant species and are
recorded in inventories on tropical regions (Santa
Izabel & Gusmão 2018; Monteiro et al. 2019)
and temperate regions (Hernández-Restrepo et al.
2017) in various regions of the world. Many studies
that have investigated saprobic fungi have revealed
new genera, species and records, especially when
tropical areas were investigated (Heredia-Abarca
et al. 2018; Cantillo et al. 2019; Pem et al. 2019;
Barbosa et al. 2020; Hyde et al. 2020).
Fungal species with frequency of occurrence
appeared in all collections (Tab. 1). The genus
Thozetella was prevalent in I. edulis litter and was
represented by eight species.
Taxa richness was 58.33% for the leaf litter
of I. edulis, and 60.41% for the leaf litter of L.
pacari (Fig. 1a), taxa richness was highest for L.
pacari (39.58%) in the first collection and for I.
edulis (37.50%) in the third collection. Lowest
richness was found for both plants in the second
collection (29.08 % for I. edulis and 25 % for L.
pacari) (Fig. 1b).
Regarding taxa richness, Marques et al.
(2008) studying a dense forest area and a sparse
forestry area in the Atlantic Forest of Bahia
observed higher richness in the dense area.
Other surveys also showed variations in richness
depending on the studied area and the amount of
collections made (Magalhães et al. 2011; Costa
& Gusmão 2015; Santos et al. 2017; Santa Izabel
Gusmão 2018). Polishook et al. (1996) studied
fungal richness in mixed leaf litter in forest
ecosystems, and concluded that fungi prefer certain
substrates. This fact was also observed by Hyde
& Alias (2000), who reported that different plant
parts (leaves, petioles, barks, among others) harbor
different fungi.
Sporadic taxa showed up in L. pacari
(58.62%) and in I. edulis (57.14%) (Tab. 2).
Uncommon taxa surged more in L. pacari
(24.13%) than in I. edulis (17.85%). Inga edulis

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Taxon
Inga edulis Lafoensia pacari
FO (%) FO (%)
Actinocymbe sp. 1.0 0.0
Beltrania rhombica Penz. 0.3 0.0
Beltraniella portoricensis (F. Stevens) Piroz. & S.D. Patil 0.3 0.3
Castanediella ramosa (Matsush.) 0.0 0.5
Ceratocladium sp. 0.0 0.3
Chaetopsina fulva Rambelli 0.0 1.0
Cladosporium aff. cladosporioides (Fresen.) G.A. de Vries 0.0 0.3
Cladosporium sp. 0.5 0.3
Clonostachys aff. rosea (Preuss) 0.3 0.3
Clonostachys aff. compactiuscula (Sacc.) D. Hawksw. & W. Gams 0.3 0.0
Coccomyces leptosporus Speg. 1.0 0.0
Colletotrichum gloeosporioides (Penz.) Penz. & Sacc. 0.0 1.0
Colletotrichum sp. (sexual morph) 0.3 0.0
Cryptophiale hamulata K.D. Hyde & McKenzie 0.0 0.3
Graphium sp. 0.5 0.0
Hansfordia pulvinata (Berk. & M.A. Curtis) S. Hughes 1958 0.0 0.3
Idriella lunata P.E. Nelson & S. Wilh. 0.3 0.0
Lauriomyces acerosus Somrith., Suetrong & E.B.G 0.0 0.5
Menispora britannica (M.B. Ellis) P.M. Kirk 1.0 0.3
Menisporopsis profusa Piroz. & Hodges 0.5 0.0
Menisporopsis theobromae S. Hughes 0.3 0.0
Metulocladosporiella sp. 0.0 0.3
Muyocopron corrientinum Speg 0.0 0.3
Nectria sp. 0.0 0.3
Neopestalotiopsis pernambucana Silvério, M.A.Q. Cavalc. & J.L. Bezerra 0.0 0.3
Ophioceras sp. 1.0 0.0
Ophiostoma sp. 0.0 0.3
Parasympodiella laxa (Subram. & Vittal) Ponnappa 0.0 0.5
Penicillium spp. 0.0 1.0
Periconia byssoides Pers. 0.3 0.0
Pestalotiopsis sp. 1.0 1.0
Pyrenochaeta sp. 0.0 1.0
Table 1 – Frequency of occurrence of fungi found in Inga edulis and Lafoensia pacari trees in an Atlantic Forest
remnant in Ilhéus city, Bahia State, Brazil.

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Taxon
Inga edulis Lafoensia pacari
FO (%) FO (%)
Sporidesmium tropicale M.B. Ellis 0.0 0.3
Sympodiella sp.0.0 0.3
Thozetella aff. submersa F.R. Barbosa & Gusmão 0.3 0.0
Thozetella buxifolia Allegr. Cazau, Cabello & Aramb 1.0 0.0
Thozetella cristata Piroz. & Hodges 1.0 0.3
Thozetella falcata B.C. Paulus, Gadek & K.D. Hyde 0.5 0.0
Thozetella havanensis R.F. Castañeda 1.0 0.0
Thozetella queenslandica B.C. Paulus, Gadek & K.D. Hyde 0.3 0.0
Thozetella radicata (E.F. Morris) Piroz. & Hodges 0.3 0.0
Thozetella sp. 0.3 0.3
Triposporium sp. 0.0 0.5
Vermiculariopsiella cf. cubensis (R.F. Castañeda) 0.3 0.0
Vermiculariopsiella pediculata (J.L. Cunn.) 0.3 0.5
Volutella sp. 0.0 0.0
Volutellonectria consors (Ellis & Everh.) 0.3 0.0
Zygosporium sp. 0.5 0.5
Total = 48
presented 21.42% frequent taxa and L. pacari
17.24 %. The species composition of frequent
taxa was different in the two plants: Menispora
britannica, Ophioceras sp., Thozetella buxifolia,
T. cristata and T. queenslandica were frequent taxa
in I. edulis, while Chaeptopsina fulva, Penicillium
spp., Pyrenochaeta sp., and Sympodiella sp.
were frequent in L. pacari. Only one taxon
(Pestalotiopsis sp.) was very common in all
collections and on both trees, accounting for 3.57%
and 3.44% richness in Inga edulis and Lafoensia
pacari, respectively.
As for taxa constancy in the trees, accidental
fungi collected one time in one collection
predominated (Fig. 2). In I. edulis, 57.14% of
the taxa were accidental, 17.85% accessory, and
25% constant. In L. pacari, 58.62% of the taxa
were accidental, 24.13% accessory, and 17.24%
constant. Santana et al. (2017) also observed a
greater occurrence of accidental species (61.54%)
in the Atlantic Forest fragment.
Santos et al. (2017) did a very accurate study
of the litter fungi in three tree species in a large
reserve of the Atlantic Forest in the municipality
of Una, Bahia and they found that 43.6% of the
taxa were constant.
Our results showing the predominance of
sporadic taxa fits those reported by many authors
in previous studies on litter fungi of the Atlantic
Forest (Barbosa et al. 2009; Magalhães et al. 2011;
Santos et al. 2017). Pestalotiopsis sp. was the only
very frequent species detected probably because it
is an extremely effective saprobe and endophyte
(Strobel & Daisy 2003; Jeewon et al. 2004;
Devarajan & Suryanarayanan 2006; Kruschewisky
et al. 2014). The predominance of accidental taxa
was reported by Magalhães et al. (2011) studying
three plant species in three areas in southern Bahia.
Marques et al. (2008) and Barbosa et al. (2009)
published similar results in other fragments of the
Atlantic Forest in Bahia. The authors concluded
that the rapid succession of litter fungi during
colonization in a humid chamber may cause the
overlook of some species. This fact was noted
also in the present study. Accidental fungi species
seems to be highly influenced by temperature and

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humidity, as well as, by litter decomposition stage.
Constant species appears to be less influenced by
these conditions and are perhaps more resistant to
climate changes (Lima & Sousa 2014; Costa &
Gusmão 2017).
Fungal similarity between plant species was
31.57% (Tab. 3), that is, of the 48 taxa identified
in the two trees, only the following nine fungi were
common: Beltraniella portoricensis, Cladosporium
sp., Clonostachys aff. rosea, Menispora britannica,
Pestalotiospsis sp., Thozetella cristata, Thozetella
sp., Vermiculariopsiella pediculata, and
Zygosporium sp. Comparing the three collections
a low similarity (26.82%) was found but by pairing
them a similarity above 50% was obtained.
Low similarity of fungal population was
expected since the host plants belonged to different
families. Studies show that the similarity index
is higher among plants of the same genus or
species than between different taxa (Maia 1983;
Polishook et al. 1996). Similar results were found
by Polishook et al. (1996) when studying the leaf
litter of Guarea guidonea Sleumer and Manilkara
bidentata Chev. The authors obtained fungal
similarity of 32 % and 26 %, respectively in two
different areas. Magalhães et al. (2011) obtained
a slightly higher similarity when comparing three
plant species (39.6%). According to Mueller-
Dombois & Ellenberg (1974), two communities
are considered similar when the Sorensen index is
higher than 50%. In Pernambuco, Assunção (2010)
also found similarity between the areas where she
collected banana endophytic fungi. Analyzing the
leaf litter of Caesalpinia echinata in two areas with
and without impact of air pollution in São Paulo,
Silva (2007) obtained a similarity index of 53.3%.
Of the taxa detected, 48 were asexual morphs
and only the following six were teleomorphic:
Actinocymbe sp., Colletotrichum sp., Muyocopron
corrientinum, Nectria sp., Ophioceras sp.,
Ophiostoma sp. Many of the asexual (conidial)
species were recorded in other studies (Cruz et al.
2007; Marques et al. 2008; Barbosa et al. 2009;
Magalhães et al. 2011; Santos et al. 2017; Monteiro
et al. 2019). The scarcity of teleomorphs of litter
Ascomycota detected now in I. edulis and L. pacari
Frequency Inga edulis (%) Lafoensia pacari (%)
Sporadic 16 57.14 17 58.62
Uncommon 5 17.85 7 24.13
Frequent 6 21.42 4 17.24
Very frequente 1 3.57 1 3.44
Richness/plant 28 100 29 100
Table 2 – Distribution of the taxa obtained in the plant species Inga edulis and Lafoensia pacari by frequency class.
Figure 2 – Taxa constancy in the litter of plant species
Inga edulis and Lafoensia pacari.
Figure 1 – a-b. Fungal richness of each plant species
– a. Inga edulis and Lafoensia pacari; b. between
collections 1, 2, and 3.
a
b

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occurs with other types of litter (Parungao et al.
2002; Duong et al. 2008; Santana et al. 2017).
These authors reported a vast majority of asexual
morphs of Ascomycota in litter.
Most species encountered in this work
were typical litter fungi such as: Beltrania
rhombica, Beltraniella portoricensis, Castanediella
ramose, Ceratocladium sp., Volutella sp., and
Volutellonectria consors. Other species correspond
to epifoliar pathogens or parasites of canopy leaves,
e.g., Actinocymbe sp., Hansfordia pulvinata,
Colletotrichum gloeosporioides and others.
Actinocymbe is an ascomycete belonging in the
Chaetothyriales which has never been reported
as a litter fungi since it is an epifoliar fungus.
Hansfordia pulvinata is a mycoparasite which
can be used as a biocontrol agent of several plant
patogenic ascomycetes. The finding of epifoliar
fungi in the litter of the studied plants implies
in alterations in the fungus metabolism (Pugh
et al. 1972). Many leaf pathogenic ascomycetes
complete their life cycle on the fallen leaves of
their hosts (Bowen et al. 2011).
Inga edulis and Lafoensia pacari have high
populations of Ascomycota in their litter. Richness,
frequency, constancy, and similarity of these
populations varied little in function of epoch of
collection, climate and host plant. Low richness
observed in the second collection may reflect the
effect of lower humidity observed in that time of
the year.
Acknowledgements
To Coordenação de Aperfeiçoamento de
Pessoal de Nível Superior (CAPES), for granting
the scholarship to the first (88882.451313/2019-
01) and second (88882.451314/2019-01) authors.
A research grant from the Conselho Nacional de
Pesquisas - CNPq (309340/2017-9) to the last
author is also acknowledged. We are also grateful
to the Executive Committee of the Cacao Crop
Plan (CEPLAC), for providing the Laboratory and
materials to conduct the fungal research.
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Plant species and collection Similarity (%)
Inga edulis and Lafoensia pacari 31.57
Collection 1 and collection 2 61.11
Collection 1 and collection 3 55.93
Collection 2 and collection 3 64.70
Collection 1, collection 2, and collection 3 26.82
Table 3 – Fungal similarity between the plant species Inga edulis and Lafoensia pacari, and between collections 1,
2, and 3.

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Area Editor: Dr. Anibal de Carvalho Junior
Received in February 04, 2021. Accepted in May 03, 2021.
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