Content uploaded by André Santiago
Author content
All content in this area was uploaded by André Santiago on May 11, 2015
Content may be subject to copyright.
Submitted 4 June 2014, Accepted 6 December 2014, Published online 15 December 2014
Corresponding Author: Roger Melo – e-mail – rogerfrmelo@gmail.com 790
The genera Ascobolus and Saccobolus (Ascobolaceae, Pezizales) in
Brazil
Melo RFR1, Miller AN3, Santiago ALCMA2 and Maia LC1
1 Universidade Federal de Pernambuco, Departamento de Micologia, Centro de Ciências Biológicas, Avenida da
Engenharia, s/n, 50740–600, Recife, Pernambuco, Brazil. rogerfrmelo@gmail.com
2 Illinois Natural History Survey, University of Illinois, 1816 S. Oak St., Champaign, IL 61820
3 Universidade Federal Rural de Pernambuco, Unidade Acadêmica de Serra Talhada, Fazenda Saco, sn., caixa postal
063, Serra Talhada, Pernambuco, Brazil
Melo RFR, Miller AN, Santiago ALCMA, Maia LC 2014 – The genera Ascobolus and Saccobolus
(Ascobolaceae, Pezizales) in Brazil. Mycosphere 5(6), 790–804, Doi 10.5943/mycosphere/5/6/9
Abstract
Coprophilous species of Ascobolus and Saccobolus from Brazil are poorly known. Fourteen
species were identified from fresh herbivore dung recently collected in Pernambuco, Northeastern
Brazil, and eight exsiccatti sets were revised from the Pe. Camille Torrend (URM) and Dárdano de
Andrade Lima (IPA) herbaria. Ascobolus elegans and S. beckii are reported for the first time in
South America, while Ascobolus americanus and Saccobolus saccoboloides are reported for the
first time in Brazil. Saccobolus infestans is neotypified. Information regarding the distribution and
substrate preference of these species is presented. Descriptions and plates are provided, along with
an identification key to all known species of Ascobolus and Saccobolus in Brazil.
Key words – Ascomycota – dung fungi – taxonomy
Introduction
Ascobolaceae comprises six genera and approximately 129 species, composed mainly of
saprobic species associated with herbivore dung (Kirk et al. 2008). The group contain species with
small, fleshy apothecia, usually with a furfuraceous or villose disk due to the protruding asci
bearing dark coloured ascospores in maturity, asci clavate to saccate, with dome-shaped or
truncated apices, opening by a conspicuous operculum, and ascospores free or united in a single
cluster, usually dark, in shades of red, purple or brown, with a smooth to strongly ornamented
episporium (Van Brummelen 1967). Representatives of Ascobolaceae are predominantly
coprophilous, but some species have been recorded in vegetable material and burnt substrates
(Richardson 2007).
Most species of Ascobolaceae belong to Ascobolus and Saccobolus, both genera occurring
worldwide and commonly found throughout the year (Richardson 2001b). Within the pigmented
spored genus that have flesh and excipula (formerly allocated in Ascoboloideae tribe), the former
contain free ascospores inside the asci, while the later have ascospores strongly cemented together
in clusters, even after their liberation.
In Brazil, the knowledge of these genera is still scarce. In compiling the fungi studied by
Batista and colleagues, da Silva & Minter (1995) mentioned only two typical coprophilous
ascomycetes, being Ascobolus notatus Batista & A.F. Vital one of them. During a visit to Brazil in
Mycosphere 5 (6): 790–804 (2014) ISSN 2077 7019
www.mycosphere.org Article Mycosphere
Copyright © 2014 Online Edition
Doi 10.5943/mycosphere/5/6/9
791
1998, Richardson (2001a) sampled herbivore dung and recorded A. immersus Pers., Saccobolus
citrinus Boud. & Torrend, S. depauperatus (Berk. & Broome) E.C. Hansen, S. truncatus Velen., S.
verrucisporus Brumm. and S. versicolor (P. Karst.) P. Karst. in Bonito and Pantanal of Rio Negro,
Mato Grosso do Sul, providing a brief description for these six species.
In the present work, Ascobolus and Saccobolus recorded in Brazil are discussed, along with
the recent new additions from fresh material collected in Pernambuco, Northeastern Brazil, herbaria
and bibliographic revision, and aspects regarding substrate preference and distribution.
Materials & Methods
Study area and sampling
Dung samples were collected from: 1) animal precincts on the campus of Universidade
Federal Rural de Pernambuco, Recife (8°00’54”S, 34°56’59”W), 2) in a Zoological Park at Reserva
Ecológica de Dois Irmãos, Recife (8°7’30”S, 34°52’30”W), 3) on farms close to the Instituto
Agronônico de Pernambuco (IPA) in Caruaru (8°01’59”S, 36°06’59”W) and in Serra Talhada
(7°54’59”S, 38°17’0.14”W), both located on Caatinga domain in the semi–arid region of
Pernambuco. Samples of cattle (Bos sp.), goat (Capra sp.) and horse (Equus sp.) dung were
collected in all areas, while samples of camel (Camelus bactrianus L.), llama (Lama glama L.),
deer (Cervus elaphus L), paca (Cuniculus paca L.) and waterbuck (Kobus ellipsiprymnus L.) dung
were available on the Zoo park at Dois Irmãos. Samples were collected in clean plastic bags, gently
air dried when necessary, taken to the laboratory and incubated in moist chambers at room
temperature (28 ± 2°C) for at least 60 days under alternating natural light and dark periods. The
specimen habit was observed directly from substrata under a stereomicroscope (Leica EZ4), and
apothecia in different stages of development were mounted in tap water, lactophenol with cotton
blue or Polyvinyl–Lacto–Glycerol (PVLG) for observation under light microscopy. Species were
identified based on morphology in different stages of development according to Van Brummelen
(1967), Bell (1983), Richardson & Watling (1997), Doveri (2004), Bell (2005) and Doveri (2014).
Shannon's diversity index was used as an estimator of species diversity in each substratum and in
the assemblage as a whole (Shannon 1948). A careful literature revision and a survey of national
herbaria were performed in order to access information regarding older records of the studied
genera in Brazil. Exsiccatti were requested in herbaria Pe. Camille Torrend (URM), Dárdano de
Andrade Lima (IPA), both in Pernambuco, Maria Eneyda P. Kaufmann Fidalgo (IBT), São Paulo,
Instituto Nacional de Pesquisas da Amazônia (INPA), Amazonas, Museu Paraense Emilio Goeldi
(MG), Minas Gerais, Instituto de Biociências, Universidade Federal do Rio Grande do Sul (INC),
Rio Grande do Sul, and Dimitri Sucre Benjamin (JBRJ), Rio de Janeiro, where all exsiccates
containing material of Ascobolus and Saccobolus collected in Brazil were searched and, if located,
taxonomically revised, with similar methodology. High resolution images of morphological
characters were taken with the aid of a BX51 Olympus microscope equipped with bright–field and
Nomarski interference optics. Permanent slides were mounted and deposited in URM (Pe. Camille
Torrend Herbarium, Universidade Federal de Pernambuco, Recife, Brazil).
Results
Fourteen species were identified from fresh material, showing apothecia fruiting directly on
dung, and another eight species from exsiccati containing relevant dry material from herbaria were
examined. An identification key to the coprophilous species of Ascobolus and Saccobolus in Brazil
is provided.
Key to species of Ascobolus and Saccobolus from Brazil
1. Ascospores free inside the asci in all stages of development .......................................................... 2
1. Ascospores firmly cemented together in all or some stage of development ................................... 6
792
2. Apothecia eugymnohymenial, large, usually visible with naked eye, up to 1500 μm diam. Disk
strongly furfuraceous ....................................................................................................... A. scatigenus
2. Apothecia cleistohymenial, smaller, up to 600 μm diam. Disk punctate to weakly furfuraceous .. 3
3. Apothecia opening on the telohymenial phase. Episporium with a pattern of subparallel crevices,
occasionally anastomosing ................................................................................................................. 4
3. Apothecia opening on the mesohymenial phase. Episporium smooth or finely granular,
sometimes with a few fissures ............................................................................................................. 5
4. Receptacle with a prominent, crenulate margin. Episporium with a regular pattern of longitudinal
fissures. Ascospores 10–15 × 6.5–7.5 μm ....................................................................... A. crenulatus
4. Receptacle with an acute, finely denticulate margin. Episporium with a regular pattern of fine,
closely spaced fissures. Ascospores 22–27.5 × 12–13.5 µm ........................................... A. levisporus
5. Ascospores more than 50 μm long, surrounded by a gelatinous sheath ........................ A.immersus
5. Ascospores smaller. Gelatinous sheath present or absent .............................................................. 6
6. Ascospores 32.5–37.5 × 15.5–17 μm ......................................................................... A.americanus
6. Ascospores 27.5–32 × 12.5–15 μm .................................................................................. A.elegans
7. Spore–clusters loose, visible in young asci only. Ascospores free at maturity ....... S.saccoboloides
7. Spore–clusters compact even after liberation. Spores firmly cemented even after liberation ........ 8
8. Spore–clusters with four rows of two longitudinally disposed spores and two longitudinal planes
of symmetry ........................................................................................................................................ 9
8. Spore–clusters with a different pattern of spore arrangement ...................................................... 12
9. Receptacle yellow to lemon–yellow. Ascospores with strongly truncate ends ................ S. citrinus
9. Receptacle golden–yellow to amber. Ascospores without strongly truncate ends ....................... 10
10. Receptacle strongly colored, in shades of ember. Ascospores 25–27.5 × 7.5–12.5 μm ... S. glaber
10. Receptacle weakly colored, in shades of yellow. Ascospores smaller, less than 20 μm long .... 11
11. Ascospores 13–20 × 8–9.5 μm. Spore–clusters becoming shorter at maturity ........... S. truncatus
11. Ascospores 11.5–12.5 × 5–7.5 μm. Spore–clusters not shortening at maturity ............ S. minimus
12. Spore–clusters with the axes of the spores at right angles to the axis of the package, with four
pairs united in a cylindrical cluster ..................................................................................... S. infestans
12. Spore–clusters with a different pattern of spore arrangement .................................................... 13
13. Spore–clusters with two rows of three and one row of two spores, where the axis of spores are
parallel to the axis of the cluster ................................................................................. S. verrucisporus
13. Spore–cluster with two rows of three and one row of two spores, where the two terminal pair of
spores are parallel to the axis of the cluster and the two median pairs are obliquely disposed ........ 14
14. Episporium thick, coarsely warted or reticulated. Ascospores 17.5–22.5 × 8.5–10 μm ... S. beckii
14. Episporium smooth to finely granular, sometimes with an incomplete network of fissures ...... 15
15. Spore–clusters 29–32 × 9.5–12 μm. Ascospores 11.5 × 6–6.5 µm ...................... S. depauperatus
15. Spore–clusters 38–48 × 16–20 μm. Ascospores 14.5–19 × 7–10 µm ........................ S. versicolor
Taxonomy
793
Ascobolus americanus (Cooke & Ellis) Seaver, North American Cup–fungi (Operculates) 85.1928.
Figs 1–3
≡ Ascobolus leveillei var. americanus Cooke & Ellis, Florule Finistère (Paris) 35. 1876.
= Ascobolus amoenus Oudem., Hedwigia 21(11). 1882.
Apothecia gregarious to scattered, sessile, semi–immersed or superficial, 250–600 × 150–500
μm, glabrous. Receptacle globose and closed at first, dark–yellow, becoming subglobose, yellow,
with undifferentiated margin. Disk red to dark–purple due to many exposed protruding thin asci
bearing mature ascospores. Hymenium well developed, 245–310 μm thick. Hypothecium thin,
composed of small oblong cells. Excipulum composed of subglobose and angular cells, (textura
angularis and textura globulosa), with well differentiated layers. Paraphyses filiform, simple or
branched, sometimes septate, hyaline, 2–3 μm thick, embedded in greenish–yellow substance in
some apothecia, easily observed when mounting in water. Asci 8–spored, clavate to cylindric–
clavate, with a short stalk, rounded above, 215–295 × 30–44.5 μm. Ascospores uniseriate,
becoming biseriate with maturation, ellipsoid, hyaline when young, becoming violet to brownish–
red in maturity, smooth to finely granular, 32.5–37.5 × 15.5–17 μm.
Habitat – Recorded on dung of blue wildebeest, camel, cattle, elephant, giraffe, goat, horse,
rabbit and muskrat.
Known distribution – Africa (South Africa), Europe (Netherlands), North America (U.S.A.,
Canada) and South America (Argentina, Peru, Venezuela). This is the first record from Brazil.
Material examined – Brazil, Pernambuco, Serra Talhada, Instituto Agronômico de
Pernambuco (IPA), on cattle dung, 30 May 2012, R.F.R. Melo (URM84600, 84601); on goat dung,
10 Jun 2011, R.F.R. Melo (URM84603); on horse dung: 23 Apr 2012, R.F.R. Melo (URM84602);
8 Sep 2011, R.F.R. Melo (URM84599).
Notes – This species is similar to A. elegans, and can be distinguished mainly by the size of
the ascospores (32.5–37.5 × 15.5–17 μm) and by a somewhat furfuraceous disk, with several
simultaneously protruding asci.
Ascobolus crenulatus P. Karst., Fungi Fenniae Exsiccati, 8(763), 1868. Figs 4–6
= Ascobolus viridulus W. Phillips & Plowr., Grevillea 8(47): 103, 1880.
Apothecia isolated, sessile, superficial, 0.5–0.6 mm diam., glabrous. Receptacle at first
globose, with undifferentiated disk, pale yellow to yellow, then hemispheric to lenticular, greenish–
yellow, and finally darker, in shades of dark yellow to amber colored with the ripening of
ascospores, with crenulated margin. Disk with violaceous to purplish punctuation due to the
coloured episporium of ascospores inside the protruding asci at maturity, weakly furfuraceous.
Hymenium well differentiated, 120–200 µm thick. Hypothecia poorly differentiated, composed of
small globose cells and hyphae, usually indistinct from the hymenium. Excipulum composed of
globose and subglobose cells (textura globosa), with poorly differentiated layers. Paraphyses
cylindric, simple or branched, septate, hyaline, 2.5–3 µm thick. Asci 8–spored, cylindric–clavate,
shortening towards the base to form a short stalk, rounded above, 135–145.5 × 12.5–15 µm.
Ascospores uniseriate when maturing, finally becoming irregularly biseriate, ellipsoid, hyaline
when young, becoming violaceous to pale red, with episporium presenting parallel fissures,
longitudinal to the spore main axis, occasionally anastomosing, 10–15 × 6.5–7.5 µm, sometimes
with unilateral mucilagenous substance.
Habitat – Recorded in vegetable material and in dung of deer, dog, goat, grouse, partridge,
pheasant, pigeon, porcupine, raven and rabbit.
Known distribution – Worldwide.
Material examined – Brazil, Pernambuco, Recife, Universidade Federal Rural de Pernambuco
(UFRPE), on goat dung, 23 Sep 2011, R.F.R. Melo (URM85922, 85923).
Notes – As suggested by the etymology of its specific epithet (lat. crenulatus = notched,
serrated), this species has, as a main distinguishing morphological character, receptacles with
crenulated margin. It represents a typical member of Van Brummelen's Ascobolus Section, with
794
episporium presenting a pattern of subparallel fissures, longitudinal with the spore main axis,
occasionally anastomosing. Despite being well distributed, it was recorded in Brazil only once, in
Pernambuco, fruiting on goat dung.
Ascobolus elegans J. Klein, Verh. zool.–bot. Ges. Wien 20: 566. 1870. Figs 7–8
≡ Ascophanus elegans (J. Klein) Sacc., Syll. fung. (Abellini) 10: 32. 1892.
≡ Dasyobolus elegans (J. Klein) Svrcek. Sb. nár. Mus. Praze 32B(2–4): 117. 1979.
Apothecia gregarious to scattered, sessile, usually superficial, 300–400 μm diam., glabrous.
Receptacle globose at first, greenish yellow, becoming subglobose andyellow at maturity, with
undifferentiated margin. Disk poorly distinct, with red to purple dots due to exposed protruding asci
bearing mature ascospores. Hymenium well developed, 200–250 μm thick. Hypothecium thin,
composed of small globular to subglobular cells. Excipulum composed of angular and subglobose
cells, becoming elongated next to the surface, (textura angularis, textura epidermoidea or textura
globulosa), with poorly differentiated layers. Paraphyses filiform, simple or branched, septate,
hyaline, 2.5–3 μm thick, embedded in greenish–yellow substance in some apothecia, easily
observed when mounted in water. Asci 8–spored, clavate, tapering towards the base to form a short
stipe, rounded above, 210–257.5 × 31–35.5 μm. Ascospores biseriate, ellipsoid, hyaline when
young, becoming violet to brownish–red in maturity, smooth to finely granular, 27.5–32 × 12.5–15
μm. Habitat – Recorded on dung of cattle, giraffe, goose, hare, horse, rabbit and zebra.
Known distribution – Europe (Denmark, Germany, Great Britain, Poland, Sweden) and North
America (U.S.A.). This is the first record from South America.
Material examined – Brazil, Pernambuco, Caruaru, Instituto Agronômico de Pernambuco
(IPA), on horse dung, 15 Jun 2011, R.F.R. Melo (URM84604, 84605).
Notes – Ascobolus elegans can be distinguished from other representatives of section
Dasyobolus by ascospore dimensions, smaller than A. americanus (Cooke & Ellis) Seaver and
larger than A. mancus (Rehm) Brumm., and by epispore ornamentation, smooth to finely granular
(Van Brummelen 1967).
Ascobolus immersus Pers., Neues Mag. Bot. 1: 115. 1794. Figs 9–11
≡ Dasyobolus immersus (Pers.) Sacc., Syll. fung. (Abellini) 11:421. 1895.
Apothecia usually scattered, sessile, 500–1200 μm diam., glabrous. Receptacle globose to
ovoid and closed at first, dark–yellow to greenish–brown, immersed to erumpent, becoming
subglobose to pyriform, yellow, superficial, without margin. Disk with ~3–7 exposed protruding
asci and its ascospores, easily observed in stereomicroscope. Hymenium composed of few exposed
asci. Hypothecium thin, composed of small isodiametric cells, poorly observable. Excipulum
composed of angular, subglobose or oblong cells, (textura angularis and textura globosa), with
layers poorly differentiated after maturation. Paraphyses filiform, simpleor branched, septate,
hyaline, 2–3μm thick, in greenish–yellow substance in some apothecia, easily observed when
mounted in water. Asci 8–spored, broadly clavate, with a short stalk, rounded above, 394–445 ×
107–130 μm, greatly elongated before spore liberation, reaching ~690–700 μm. Ascospores
biseriateor irregularly disposed in the asci, variable in morphology, oblong to ellipsoid, sometimes
subglobose, hyaline when young, becoming purple or violet, finally in shades of red to purplish–
brown, smooth or with one to few fissure lines, 57.5–62.5 × 30–35 μm, surrounded by a thick
gelatinous envelope.
Habitat – Recorded on dung of many herbivores.
Known distribution – Worldwide.
Material examined – Brazil, Pernambuco, Caruaru, Instituto Agronômico de Pernambuco
(IPA), on cattle dung, 17 Jun 2011, R.F.R. Melo (URM84606); Serra Talhada, Instituto
Agronômico de Pernambuco (IPA), on horse dung, 15 Jun 2011, R.F.R. Melo (URM84609);
Recife, Universidade Federal Rural de Pernambuco (UFRPE), on horse dung, 12 Sep 2011, R.F.R.
Melo (URM84607); 12 Mar 2012, R.F.R. Melo (URM84608); Recife, on guinea pig dung, 1 Dec
795
1947, Batista A.C. (URM653, IPA37905, IPA1129); Recife, Dois Irmãos, on rabbit dung, 1 Dec
1947, Pontual D. (URM646, IPA37903).
Notes – Ascobolus immersus is one of the most common fungi found fruiting on incubated
herbivore dung, being recorded worldwide. It can be easily recognized by its very large ascospores
(57.5–62.5 × 30–35 μm) surrounded by a conspicuous gelatinous envelope. In Brazil, this species
was recorded by Richardson (2001a), Batista et al. (1961), among other authors. No apothecia was
found on material reviewed under the labels URM653 and IPA37905, but well preserved apothecia
were found on material in the box number 1129 in IPA herbarium, along with the holotype of
Chaetomium brasiliense Bat & Pontual. Ascobolus cuniculorum A.C. Batista & Pontual was
proposed for specimens found on rabbit dung identified by Chaves Batista in Pernambuco, Brazil,
but was later synonymized under A. immersus Pers. by Van Brummelen (1967). No apothecia were
found on both exsiccati, available from two different herbaria. The holotype of A. cuniculorum
consisted of a single dry pellet of rabbit dung with several pseudothecia of Sporormiella minima
(Auersw.) S.I. Ahmed & Cain, but no apothecia could be found. Thus, based on the revision of the
aforementioned author, “Ascobolus cuniculorum A.C. Batista & Pontual” was nomenclaturally
superfluous when published, and should stand as a synonym of Ascobolus immersus Pers.
Ascobolus scatigenus (Berk. & M.A. Curtis) Brumm., Persoonia, Suppl. 1: 159. 1967. Figs 12–14
≡ Sphaeria scatigena Berk. & Broome, Annals and Magazine of Natural History 7: 452. 1861.
≡ Hypocopra scatigena (Berk. & Broome) Sacc., Sylloge Fungorum 1: 243. 1882.
≡ Coniochaeta scatigena (Berk. & Broome) Cain, Studies of Coprophilous Spaeriales in Ontario:
62. 1934.
≡ Ascobolus notatus A.C. Batista & A.F. Vital, Anais Soc. Biol. Pernambuco 13(2): 61. 1955.
=Ascobolus magnificus B.O. Dodge, Mycologia 4(4): 218. 1912.
Apothecia scattered to gregarious, sessile, superficial, 1.5–2.7 mm, glabrous. Receptacle
initially subglobular, white to pale luteous, exposing the disk during the beginning of development,
with undifferentiated hymenium, bearing immature asci, later becoming lageniform, cupulate and
finally scutellate, pale yellow, granular in texture, with involute, poorly differentiated margin. Disk
plane to slightly undulate, strongly furfuraceous, dark–red to black coloured due to many exposed
protruding thin asci bearing mature ascospores. Hymenium well differentiated, 190–215 µm thick.
Hypothecium composed of small, hyaline, globose cells, 5–10 µm thick. Excipulum composed of
small globose and subglobose cells (textura globulosa), hyaline, 50–75 µm thick.Paraphyses
abundant, cylindric, simples or occasionally branched, septate, hyaline, 2.5–3.5 µm diam., slightly
larger towards the apex, up to 6.5 µm diam., occasionally longer than the asci in the hymenium.
Asci 8–spored, cylindric–clavate, with a short stalk, rounded to slightly tapered above, with
prominent opercula, 175–225 × 17.5–30 µm. Ascospores uniseriate, ellipsoid, hyaline when young,
then violaceous to brownish–red, smooth or with one to a few oblique fissure, usually
inconspicuous, 22–24.5 × 10–15 µm.
Habitat – Recorded on dung of many herbivores.
Known distribution – Worldwide.
Material examined – Brazil, Pernambuco, Serra Talhada, Instituto Agronômico de
Pernambuco (IPA), on cattle dung, 16 Feb 2012, R.F.R Melo (URM85924); Recife, Universidade
Federal Rural de Pernambuco (UFRPE), on cattle dung, 19 Nov 2012, R.F.R Melo (URM85925);
Recife, on cattle dung, 1 Dec 1947, Vital A.F. (URM1976).
Notes – Ascobolus scatigenus has relatively large receptacles, usually visible on the substrate
with the unaided eye, on dung surface under incubation, or in situ. The eugymnohymenial
ascomata, furfuraceous disk, composed of protruding asci with ellipsoid ascospores (22–24.5 × 10–
15 μm), usually with a single to a few oblique fissures on its episporium, distinguishes this species.
It resembles A. castaneus, which differs by having different apothecium ontogeny, ascospores
smaller and smooth episporium. The exsiccate URM1976, labeled with the denomination
Ascobolus notatus A.C. Batista & A.F. Vital contains sessile apothecia, previously revised by van
Brummelen (1976) as A. scatigenus (Berk.) Brumm., comb. nov. in his monograph. The material
796
contains apothecia scattered, sessile, superficial, 900–1200 μm diam.; receptacle cup–shaped, with
somewhat involute margin; disk concave; hymenium ~200 μm thick; excipulum not clearly
observable due to the state of preservation of the apothecia; asci cylindric–clavate, 150–195.5 ×
17.5–23.5 μm; ascospores ellipsoid, 20–27.5 × 12.5–15 μm. The identification of A. scatigenus
sensu van Brummelen was confirmed. The name A .notatus A.C. Batista & A.F. Vital stands as a
synonym of A. scatigenus (Berk.) Brumm., comb. nov.
Saccobolus beckii Heimerl, Österr. Ascob.: 18. 1889. Figs 15–16
Apothecia gregarious or scattered, sessile, superficial, 400–650 μm diam, glabrous.
Receptacle globular at first, becoming pulvinate, light yellow, with undifferentiated margin. Disk
convex, dotted with black protruding tips of asci bearing ripe ascospore clusters. Hymenium 8.5–
12.2 μm. Hypothecium undifferentiated. Excipulum thin, composed of interwoven hyphae.
Paraphyses cylindric, simple, septate, hyaline, 2–3 μm thick. Asci 8–spored, clavate, tapering
towards the base, with a truncate apex and a short stipe, 150–165 × 41–45.5μm. Spore clusters
arranged in a pattern with two rows of three and one row of two spores, 50–55 × 18–22 μm, at the
apical portion inside the asci, surrounded by a thin gelatinous sheath. Ascospores ellipsoid, hyaline
when young, becoming dark–brown to black in maturity, with thick episporium composed of coarse
warts, 17.5–22.5 × 8.5–10 μm.
Habitat – Recorded from dung of cattle, deer, elephant and zebra. New additions on horse and
goat dung arepresented.
Known distribution – Africa (South Africa) and Europe (Austria, Bermuda, France, Germany,
Great Britain). This is the first record from South America.
Material examined – Brazil, Pernambuco, Caruaru, Instituto Agronômico de Pernambuco
(IPA), on goat dung, 3 Jan 2012, R.F.R. Melo (URM84612); Recife, Universidade Federal Rural
de Pernambuco (UFRPE), on goat dung, 7 Aug 2012, R.F.R. Melo (URM84610, 84611).
Notes – Saccobolus beckii can be easily distinguished by the ornamentation pattern of the
spore cluster and by its coarsely warted episporium (Van Brummelen, 1967, Bell, 1983).
Saccobolus citrinus Boud. & Torrend, Bull. Soc. mycol. Fr. 27(2): 131. 1911. Figs 17–19
Apothecia gregarious to scattered, sessile, superficial, 300–400 μm diam., glabrous.
Receptacle scuttelate, discoid, pulvinate or lenticular, light yellow to yellow when young,
becoming dark yellow to ochraceous with age, with undifferentiated margin. Disk convex, dotted
with black protruding tips of asci bearing ripe ascospore clusters. Hymenium poorly developed.
Hypothecium undifferentiated. Excipulum thin,composed of a palisade of cells inundifferentiated
layers. Paraphyses cylindric, simple, septate, hyaline, 2–3 μm thick, slightly enlarged at apex,
embedded in greenish–yellow substance in some apothecia, easily observed when mountedin water.
Asci 8–spored, clavate, tapering towards the base, with a truncate apex and a short stipe, 110–150 ×
30–33 μm. Spore clusters arranged in a pattern with four columns, each containing two spores,
47.5–55 × 15–20 μm, at the apical portion inside the asci, surrounded by a thin gelatinous sheath.
Ascospores biseriate, ellipsoid, hyaline when young, becoming brownish–red to purple in maturity,
with an ornamentation of fine isolated warts, 20–23 × 7.5–11 μm.
Habitat – Recorded on dung of many herbivores.
Known distribution – Worldwide.
Material examined – Brazil, Pernambuco, Serra Talhada, Instituto Agronômico de
Pernambuco (IPA), on cattle dung, 10 Oct 2011, R.F.R Melo (URM84613); 26 Dec 2011, R.F.R
Melo (URM84617); 1 Mar 2013, R.F.R Melo (URM84616); Recife, Universidade Federal Rural
de Pernambuco (UFRPE), on cattle dung, 3 Apr 2012, R.F.R Melo (URM84618); on goat dung, 15
Jun 2012, R.F.R Melo (URM84614, 84615).
Notes – Saccobolus citrinus is one of the most common species of the genus with the 2 × 4
spore–cluster pattern, easily found in dung of herbivores in damp chambers. The species can be
distinguished from S. glaber by the slightly smaller size of ascospores (20–23 × 8–10 µm), and the
truncated ends of the ascospores, as well as the lemon–yellow color of the apothecia.
797
Saccobolus depauperatus (Berk. & Broome) Rehm, Vidensk. Meddel. Dansk Naturhist. Foren.
Kjøbenhavn: 293. 1876. Figs 20–21
≡ Ascobolus depauperatus Berk. & Broome, Ann. Mag. nat. Hist., Ser. 3(15): 448. 1865.
Apothecia gregarious to scattered, sessile, superficial, up to 300 μm diam., glabrous.
Receptacle pulvinate, hyaline to pale violet, with undifferentiated margin. Disk convex, faintly
violet, dotted with dark purplish protruding tips of asci bearing ripe ascospore clusters. Hymenium
62.5 × 80 μm thick. Hypothecium poorly observable in material examined. Excipulum composed of
a very thin layer with globular and subglobular cells (textura globulosa). Paraphyses poorly
observable in material examined. Asci 8–spored, clavate, tapering towards the base, with a truncate
apex and a short stipe, 70–95.5 × 17.5–20 μm. Spore clusters arranged in a pattern with two rows of
three and with one row of two spores, 32.5–36.5 × 10–15 μm, sometimes asymmetrical. Ascospores
fusoid to ellipsoid, hyaline when young, becoming purplish–brown at maturity, smooth or with an
ornamentation of fine isolated warts, 11–15 × 5–7.5 μm.
Habitat – Recorded from dung of cattle, chamois, deer, elephant, elk, hare, horse, porcupine,
rabbit and sheep.
Known distribution – Africa (Morroco), Asia (Pakistan), Europe (Austria, Denmark, Faroe
Islands, Finland, France, Germany, Great Britain, Iceland, Italy, Netherlands, Poland, Spain,
Sweden), North America (Canada, U.S.A.), Oceania (Australia, New Zealand) and South America
(Argentina, Brazil, Ecuador, Venezuela).
Material examined – Brazil, Pernambuco, Serra Talhada, Instituto Agronômico de
Pernambuco (IPA), on cattle dung, 12 Sep 2011, R.F.R. Melo (URM84620); on goat dung, 16 May
2012, R.F.R. Melo (URM84619).
Notes – This is a common cosmopolitan species, rather variable in morphology, with small
apothecia that can be distinguished from S. minimus Velen. by its spore–cluster arrangement and
from S. versicolor (P. Karst.) P. Karst. by its smaller apothecia, asci and ascospores.
Saccobolus glaber (Pers.) Lambotte, Mém. Soc. roy. Sci. Liège, 14: 284. 1888. Figs 24–25
≡ Ascobolus glaber Pers. Neues Mag. Bot. 1: 115. 1794.
Apothecia usually scattered, sometimes gregarious, sessile, superficial, 350–800 μm diam.,
glabrous. Receptacle globose to subglobose at first, becoming pulvinate, in shades of ambar, with
undifferentiated margin. Disk convex, golden before asci ripening, later dotted with dark–purple to
black protruding tips of asci bearing ripe ascospore clusters. Hymenium 162.5–200 μm.
Hypothecium undifferentiated. Excipulum thin, composed of small subglobose cells. Paraphyses
cylindric, simple or branched near the apex, septate, hyaline, 3–3.5 μm thick, sometimes slightly
enlarged at apex, with yellow contents in some apothecia, easily observed when mounted in water.
Asci 8–spored, cylindric–clavate, 175.5–260 × 20–32 μm. Spore clusters arranged in a pattern with
four columns, each containing two spores, 52.5–57.5 × 20–21.5 μm, at the apical portion inside the
asci, surrounded by a thick gelatinous sheath, especially observable after spore cluster release.
Ascospores ellipsoid to slightly fusiform, sometimes asymmetrical, hyaline when young, becoming
purplish–brown in maturity, with rounded tips with an ornamentation of fine isolated warts, 25–
27.5 × 7.5–12.5 μm.
Habitat – Recorded from dung of bear, blue wildebeest, camel, cattle, deer, elephant, gnu,
horse, sheep and zebu.
Known distribution – Worldwide.
Material examined – Brazil, Pernambuco, Caruaru, Instituto Agronômico de Pernambuco
(IPA), on horse dung, 13 Jun 2012, R.F.R. Melo (URM84623); Serra Talhada, Instituto
Agronômico de Pernambuco (IPA), on cattle dung, 26 Dec 2011, R.F.R. Melo (URM84621);
Recife, Universidade Federal Rural de Pernambuco (UFRPE), on cattle dung, 3 Apr 2012, R.F.R.
Melo (URM84622); 7 Aug 2012, R.F.R. Melo (URM84624); 3 Feb 2013, R.F.R. Melo
(URM84625).
798
Notes – Saccobolus glaber resembles S. citrinus Boud. & Torrend in general morphology,
being distinguished by the color of receptacle, usually darker, in shades of amber, golden to dark
yellow, and for its slightly longer ascospores (25–27.5 µm) with rounded tips.
Saccobolus infestans (Bat. & Pontual) Brumm., Persoonia, Suppl. 1: 204. 1967. Figs 22–23
≡ Ascobolus infestans Bat. & Pontual, Bol. Secr. Agric. (Pernambuco) 15: 31. 1948.
Apothecia usually scattered, sometimes gregarious, sessile, superficial, 90–120 μm diam.,
glabrous. Receptacle globose to subglobose at first, becoming pulvinate, pale, with undifferentiated
margin. Disk convex, white before asci ripening, later dotted with violaceous protruding tips of asci
bearing ripe ascospore clusters. Hymenium ~75 μm thick. Hypothecium undifferentiated.
Excipulum thin, composed of small angular cells. Paraphyses cylindric, simple or branched near the
apex, septate, hyaline, 1–2.5 μm thick. Asci 8–spored, clavate, 75–110 × 14–20.5 μm. Spore
clusters arranged in a pattern with the axes of the spores at right angles to the axis of the cluster,
20–25.5 × 10–15 μm. Ascospores ellipsoid, hyaline when young, becoming brown in maturity, with
rounded tips, slightly roughened, 10–11 × 5–6 μm.
Habitat – Recorded from dung of donkey and horse.
Known distribution – Central America (Panama, Tahiti) and South America (Brazil,
Venezuela).
Material examined – (neotypus) Brazil, Pernambuco, Recife, Universidade Federal Rural de
Pernambuco (UFRPE), on horse dung, 6 Mar 2013, R.F.R. Melo (URM84632); (isoneotypus)
Recife, Universidade Federal Rural de Pernambuco (UFRPE), on horse dung, 6 Mar 2013, R.F.R.
Melo (URM84633).
Notes – Saccobolus infestans can be characterized by the unusual arrangement of its spore
cluster. It resembles S. geminatus in having spores transversely arranged in the cluster, but differs
in having smaller ascospores (10–11 × 5–6 μm) not firmly united in pairs. It was first described in
Brazil by Batista & Pontual (1948), from material collected on horse dung in Dois
Irmãos, Recife, Pernambuco, as Ascobolus infestans Bat. & Pontual. Despite the efforts, the
exsiccate containing the holotype, deposited in IPA herbarium, could not be found. The original
work where this name was proposed contained a short description and one picture, without
drawings. Thus, according to the Article 9.7 of the International Code of Botanical Nomenclature
(Melbourne Code), since there is material left from the holotype first designated, the recent material
collected on the same substrate (horse dung) and locality (Dois Irmãos, Recife) is designated here
as neotype (URM84632) and isoneotype (URM84633).
Saccobolus minimus Velen., Monogr. Discom. Bohem. (Prague) 1: 370. 1934. Fig 26
Apothecia scattered, sessile, superficial, 100–175 μm diam., glabrous. Receptacle pulvinate,
translucid light yellow to ochraceous, with undifferentiated margin. Disk convex, amber colored
before ascospore ripening, dotted with black protruding tips of mature asci bearing ascospore
clusters. Hymenium 45–65 μm. Hypothecium undifferentiated. Excipulum thin, composed of
globose cells on the lower part and by a palisade of cells on the upper part. Paraphyses cylindric to
filiform, simple, septate, hyaline, 1.5–2.5 μm thick, with yellow contents, easily observed when
mounting in water. Asci 8–spored, clavate, tapering towards the base, with a truncate apex and a
short stipe, 50–55.5 × 30–33 μm. Spore clusters compact, arranged in a pattern with four columns,
each one containing two spores,27.5–30 × 10–15 μm, at the apical portion inside the asci,
surrounded by a thin gelatinous sheath. Ascospores ellipsoid, hyaline when young, becoming
pinkish–violet to purplish–brown in maturity, smooth to finely punctate, 11.5–12.5 × 5–7.5 μm.
Habitat – Recorded from dung of camel, cow, deer, donkey, giraffe, goat, muskrat, sheepand
zebra.
Known distribution – Africa (Kenya, South Africa), Asia (Thailand), North America
(Canada, Hawaii, U.S.A.), Europe (Austria, Czech Republic, Germany, France, Italy, Poland,
799
Spain), Oceania (New Zealand) and South America (Ecuador, Puerto Rico). This is the first record
from Brazil.
Material examined – Brazil, Pernambuco, Serra Talhada, Instituto Agronômico de
Pernambuco (IPA), on goat dung, 7 Oct 2012, R.F.R. Melo (URM84626).
Notes – According to Van Brummelen (1967), despite being a cosmopolitan species, S.
minimus is rarely recorded due to its small size. It can be characterized by its ochraceous apothecia,
pattern of spore–cluster arrangement and small ascospores (11.5–12.5 × 5–7.5 μm).
Saccobolus saccoboloides (Seaver) Brumm., Persoonia, Suppl. 1: 168. 1967. Figs 27–30
≡Ascobolus saccoboloides Seaver, Mycologia 38(6): 640. 1946.
Apothecia scattered, superficial, sessile, 300–900 m in diam., glabrous. Receptacle
lenticular, yellow when readily mature, becoming amber with age, then finally dark–brown to
black. Disk dotted with a coppery staining due to the protruding tips of ripe asci. Hymenium well
developed, ~100 μm thick. Hypothecium undifferentiated. Excipulum composed of globose cells,
strongly cyanophilous. Paraphyses filiform, simple, septate, 2.5–3 µm in diam.at the base, filled
with yellowish contents (not observable in some mounting media). Asci 8–spored, clavate, with a
short stalk and truncate apex, 70–87.5 16–22 µm, stretching up to 120 µm long, with an easily
observable operculum after spore release. Spore clusters cemented in a very early stage of
development, assuming a pattern arrangement more or less regular, becoming free inside the
ascibefore liberation. Ascospores irregularly arranged after separation, ellipsoid to somewhat
fusoid, sometimes asymmetric, at first hyaline, becoming reddish brown when ripe, 12.5–16.5 5–
7.5 µm, with smooth episporium.
Habitat – Recorded from pig dung. New additions to camel, deer, llama and waterbuck dung
are presented.
Known distribution – Indonesia and New Guinea. This is the first record from Brazil.
Material examined – Brazil, Pernambuco, Recife, Horto Zoobotânico do Parque Estadual
Dois Irmãos, on deer dung, 11 Sep 2009, R.F.R. Melo (URM82289); 25 Nov 2009, R.F.R. Melo
(URM82293); on llama dung: 02 Oct 2009, R.F.R. Melo (URM82290); 07 May 2010, R.F.R.
Melo (URM82298); on camel dung: 05 Oct 2009 R.F.R. Melo (URM82291); 10 Dec 2009, R.F.R.
Melo (URM82294); 02 Feb 2010, R.F.R. Melo (URM82295); 05 Apr 2010, R.F.R. Melo
(URM82297); on waterbuck dung, 20 Nov 2009, R.F.R. Melo (URM82292); 10 Mar 2010, R.F.R.
Melo (URM82296).
Notes – Saccobolus saccoboloides represents an atypical member of the genus by the
tendency of ascospores to separate inside the asci, and was placed by Dodge & Seaver (1946) in
Ascobolus as A. saccoboloides Seaver. However, other characters, such as the tendency of a loose
spore cluster to form a somewhat regular pattern in young asci (four columns, each containing two
spores), apothecium development and asci morphology, support the current placement of this
species in Saccobolus.
Saccobolus truncatus Velen., Monogr. Discom. Bohem. (Prague): 370 (1934) Figs 31–33
Apothecia scattered, sessile, superficial, 200–275 μm diam., glabrous. Receptacle
semiglobular at first, becoming lenticular, light yellow, with undifferentiated margin. Disk convex,
light yellow, dotted with dark brown to black protruding tips of asci bearing ripe ascospore clusters.
Hymenium ~ 45μm thick. Hypothecium not clearly observed in material examined. Excipulum
thin, composed of globose cells on the lower part, and by a palisade of cells on the upper part.
Paraphyses cylindric to clavate, simple or more rarely branched, septate, hyaline, 1.5–3.5 μm thick,
slightly enlarged at the apex. Asci 8–spored, clavate, tapering towards the base, with a truncate
apex, 75–82.5 × 17.5–20 μm. Spore clusters elongated to compact, arranged in a pattern with four
columns, each containing two spores, 37.5–40 × 15.5–20 μm, becoming shorter with spore
maturation, to a point where the pattern of arrangement can not be distinguished, shortening to
27.5–30 μm long, surrounded by a thick gelatinous sheath. Ascospores ellipsoid, hyaline when
800
young, becoming purple to purplish–brown in maturity, smooth to finely punctate, sometimes with
fissures, 13–20 × 8–9.5 μm.
Habitat – Recorded from dung of cow, horse, partridge, rabbit, raven and sheep. New
addition to goat dung is presented.
Known distribution – Africa (Morroco), Asia (Thailand), Europe (Austria, Czech Republic,
Denmark, France, Germany, netherlands), North America (Canada, U.S.A.) and South America
(Brazil, Peru, Puerto Rico). This is the first record from northeastern Brazil.
Material examined – Brazil, Pernambuco, Serra Talhada, Instituto Agronômico de
Pernambuco (IPA), on cattle dung, 6 Oct 2012, R.F.R.Melo (URM84630,84631); 14 Oct 2012,
R.F.R.Melo (URM84627); Recife, Universidade Federal Rural de Pernambuco (UFRPE), on cattle
dung, 3 Apr 2012, R.F.R.Melo (URM84628, 84629).
Notes – Saccobolus truncatus presents small pale yellow apothecia, usually scattered,
resembling S. minimus Velen., but can be distinguished by the shape and size of ascospores, and by
the tendency of the spore–cluster to become shortened in maturity.
Saccobolus versicolor (P. Karst.) P. Karst., Acta Soc. Fauna Flora fenn. 2(6): 123. 1885. Fig 34
≡ Ascobolus versicolor P. Karst., Bidr. Känn. Finl. Nat. Folk 19: 79. 1871.
Apothecia gregarious to scattered, superficial, up to 300 μm diam., glabrous. Receptacle
pulvinate to lenticular, lilaceous, with undifferentiated margin. Disk convex, light violet, dotted
with purple protruding tips of asci bearing ripe ascospore clusters. Hymenium ~120 μm thick.
Hypothecium not clearly observed in material examined. Excipulum thin, composed of intertwined
hyphae and globose cells, barely observable in material examined. Paraphyses filiform, branched,
septate, hyaline, 2–3 μmthick, sometimes enlarged at the apex. Asci 8–spored, clavate, with a short
stipe and truncated apex, tapering towards the base, 90–130 × 25–33 μm. Spore Clustersarranged in
a pattern with two rows of three and one row of two spores, 50–57 × 18.5–22.5 μm. Ascospores
ellipsoid, violaceous to brown, smooth to finely roughened, 20–22.5 × 10–11.5 μm.
Habitat – Recorded from dung of camel, caribou, cattle, deer, goat, hare, horse, lemming,
mouse, muskrat, rabbit, reedbuck, sheep and steenbok. New addition to llama dung is presented.
Known distribution – Asia (China), Africa (Kenya), Europe (Austria, Belgium, Czech
Republic, Denmark, Finland, France, Germany, Great Britain, Italy, Netherlands, Norway, Sweden,
Switzerland, Poland, Romania, and Russia), North America (Canada, U.S.A), Oceania (New
Zealand) and South America (Brazil, Chile).
Material examined – Brazil, Pernambuco, Recife, Horto Zoobotânico do Parque Estadual
Dois Irmãos, on llama dung, 21 Aug 2009, R.F.R. Melo (URM82299).
Notes – Saccobolus versicolor shows great variability in its morphology. This species can be
characterized by its spore–cluster arrangement, episporium smooth to finely granular and ascospore
and spore cluster dimensions.
Unverified and doubtful species
Ascobolus epixylon
Name of unknown origin, not found in the literature. The species contained in this material at
URM herbarium (URM7181) has pulvinate stromata, not related with any Ascobolus species. The
exsiccate did not contained author names.
Ascobolus levisporus Speg., Anal. Mus. nac. Hist. nat. B. Aires 6: 307. 1898.
This species was only found in North and South America, and the type is in poor condition. It
resembles A. furfuraceus, being distinguished by its larger apothecia and spaced striations in the
episporium. It was first published by Spegazzini in Anales del Museo Nacional de Buenos Aires in
1899, recorded on cattle dung in La Plata, Argentina (Spegazinni, 1899), as “A. laevisporus Speg.”.
It occurs as a very rare species, being rarely described, apart from the known records.
801
Figures 1–34 – Ascobolus americanus. (1) Apothecium on dung (Bar = 200 µm), (2) mounted apothecium
(Bar = 100 µm) and (3) mature spores (Bar = 10 µm). A. crenulatus. (4) Apothecium on dung (Bar = 200
µm), (5) mature spores (Bar = 5 µm) and (6) asci (Bar = 20 µm). A. elegans. (7) Apothecium on dung (Bar =
400 µm) and (8) mature spores (Bar = 15 µm). A.immersus (9) Apothecium on dung (Bar = 750 µm), (10)
mounted apothecium (Bar = 250 µm) and (11) mature spores, with some visible fissures (Bar = 25 µm). A.
scatigenus. (12) Apothecium on dung (Bar = 750 µm), (13) mounted apothecium (Bar = 250 µm) and (14)
mature spores (Bar = 5 µm). Saccobolus beckii. (15) Apothecium on dung (Bar = 500 µm) and (16) spore–
cluster, with cracked episporium (Bar = 10 µm). S.citrinus. (17) Apothecium on dung (Bar = 250 µm), (18)
spore cluster (Bar = 10 µm) and (19) mounted apothecium (Bar = 50 µm). S. depauperatus. (20)
Apothecium on dung (Bar = 250 µm) and (21) mounted apothecium (Bar = 100 µm). S. infestans. (22)
Apothecium on dung (Bar = 500 µm) and (23) spore–clusters in different views (Bar = 20 µm). S. glaber.
(24) Apothecium on dung (Bar = 500 µm) and (25) mounted apothecium (Bar = 150 µm). S. minimus. (26)
Apothecium on dung (Bar = 150 µm). S. saccoboloides. (27) Apothecium on dung (Bar = 250 µm), (28)
mounted apothecium, with clearly observable paraphyses with yellowish contents (Bar = 50 µm), (29) free
spores (Bar = 15 µm) and (30) asci with spores assuming the spore cluster arrangement, just before its
disruption (Bar = 10 µm). S. truncatus. (31) Apothecium on dung (Bar = 500 µm), (32) mounted apothecium
(Bar = 50 µm) and (33) shortened spore cluster (Bar = 5 µm). S. versicolor. (34) mounted apothecium (Bar =
50 µm).
802
Ascobolus sp.
The exsiccate IPA37924, deposited in Dárdano de Andrade Lima herbarium in January 19th,
1948 contains a single dry pellet of frog dung, labeled "Ascobolus sp.". However, no apothecia
were found at the time of the last revision or in this study, and the possibility of identification of
this material remains lost with it.
Saccobolus verrucisporus Persoonia, Suppl. 1: 198. 1967.
Saccobolus verrucisporus var. longisporus S.C. Kaushal & Virdi, Willdenowia 16(1): 274. 1986.
During a survey of coprophilous fungi in Mato Grosso, Mid–west Brazil, Richardson (2001a)
recorded S. verrucisporus for the first time in Brazil. The material consisted of "very small
apothecia, 150–200 µm diam., with ~10–12 simultaneously protruding exposed asci; asci 125 × 29
µm; spore clusters 32–38 × 16 µm; ascospores 12.5–16 × 8–9.5 µm". It was deposited in his
personal collection under the code "MJR 62–63/98".
Discussion
From the recent survey carried out on dung fungi of domestic herbivores in Pernambuco
(goat, horse and cattle), the most common species was Saccobolus citrinus, recorded on almost
every sample brought to the laboratory, dominant on all three substrates studied (cattle, goat and
horse dung) and areas surveyed (Caruaru, Recife and Serra Talhada), followed by Ascobolus
immersus, fruiting soon upon incubation. Despite the lack of study at a national scale, these species
are most likely widespread on domesticated herbivore dung throughout Pernambuco in a
vegetational gradient that ranges from Atlantic Rainforests to semiarid Caatinga. Saccobolus
saccoboloides, despite being rare, was the dominant species on samples collected at the Zoological
Park in Dois Irmãos, Recife, by Melo et al. (2012). This species was recorded for the first time in
Brazil, confirming the need for additional studies on these fungi. Saccobolus versicolor, despite
being a common worldwide species, was poorly represented in the recent surveys, being recorded
only once. Along with S. saccoboloides, A. americanus are reported for the first time in Brazil.
Ascobolus elegans and S. beckii are reported for the first time in South America.
Regarding the substrate relationship, in general, species did not show a preference for
specific dung types in most records, contradicting previous statements in some works (Webster
1970, Ebersohn & Eicker 1991, Richardson 2007).The number of records, species richness, and
estimates of species diversity on each substrate and in each studied area is presented (Table 1).
Considering both genera, no clear substrate preference could be detected. Ascobolus and
Saccobolus are known generalists on herbivore dung (Van Brummelen 1967, Richardson 2001b,
Krug et al. 2004). Cattle dung had the highest number of records. Considering that S. glaber was
recorded throughout the three areas, the slightly higher number of records on cattle dung is worth
noticing. Ascobolus scatigenus, although scarcely recorded during the survey, was found on cattle
dung only from two different areas. Coincidently, species richness was equal among substrates.
These results indicates that community diversity was similar as well, slightly higher on cattle dung,
due to the abundance discrepancies among taxa.
The studied areas represented a gradient between Atlantic rainforest biome and semi–arid
Caatinga. Most records were obtained in Serra Talhada Municipality, which had the driest climate
and vegetation typical of Brazilian arid environments. The stressful condition of the studied
assemblages in this area, subjected to heavy droughts throughout the years of survey, is believed to
have suppressed the dominance of competitor species and increased the availability of niches,
improving the diversity along the community development (Pugh & Boddy 1988, Cooke & Whips
1993, Dix & Webster 1995). Most species had records somewhat evenly distributed along areas.
Ascobolus americanus was typically found in Serra Talhada. Considering the distribution of records
on different substrates in the same area, the relationship with the area itself can be deemed superior
than the substrate relationship. Recife had the highest species diversity, with three exclusive
species, A. crenulatus, S. infestans, and S. saccoboloides.
803
Table 1 Number of records, species richness and diversity of Ascobolus and Saccobolus
assemblages recorded from different dung types and in different areas in Pernambuco, Brazil.
Substrate
Area
Species
Cattle
Goat
Horse
Total
Caruaru
Recife
Serra
Talhada
Total
Ascobolus americanus
8
5
6
19
1
1
17
19
A. crenulatus
0
1
0
1
0
1
0
1
A. elegans
0
1
3
4
0
0
4
4
A. immersus
17
14
17
48
16
12
20
48
A. scatigenus
3
0
0
3
0
2
1
3
Saccobolus beckii
2
6
3
11
2
6
3
11
S. citrinus
25
15
20
60
21
18
21
60
S. depauperatus
1
3
1
5
2
0
3
5
S. glaber
10
1
4
15
6
6
3
15
S. infestans
0
0
1
1
0
1
0
1
S. minimus
2
1
2
5
2
2
1
5
S. saccoboloides
1
1
0
2
0
2
0
2
S. truncatus
6
0
1
7
1
4
2
7
Number of records (N)
75
48
58
181
51
55
75
181
Species Richness (S)
10
10
10
13
8
11
10
13
Species Diversity (H')
1.84
1.79
1.77
1.91
1.51
1.95
1.79
1.91
Acknowledgements
The authors would like to thank the “Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior” (CAPES) and the “Conselho Nacional de Desenvolvimento Científico e Tecnológico”
(CNPq–Ciência sem Fronteiras; INCT–Herbário Virtual da Flora e dos Fungos) for providing PhD
scolarships to the first author. L.C. Maia acknowledges the research fellowship and grants provided
by CNPq (INCT–HVFF, Protax, Sisbiota).
References
Batista AC, Pontual D. 1948 – Alguns fungos coprófilos de Pernambuco. Boletim da Secretaria de
Agricultura Indústria e Comércio do Estado de Pernambuco 15, 27-44.
Bell A. 1983 – Dung Fungi: An Illustrated Guide to Coprophilous Fungi in New Zealand. Victoria
University Press, Wellington.
Bell, A. 2005 – An illustrated guide to the coprophilous Ascomycetes of Australia. CBS
Biodiversity Series, Utrecht.
Cooke, RC, Whipps, JM. 1993 – Ecophysiology of Fungi. Blackwell Scientific Publications.
da Silva M, Minter DW. 1995 – Fungi from Brazil Recorded by Batista and Co–Workers.
Mycological Papers 169, 1–585.
Dix NJ, Webster J. 1995 – Fungal ecology. Chapman & Hall, London.
Dodge BO, Seaver FJ. 1946 – Species of Ascobolus for genetic study. Mycologia 38, 639–651.
Doveri F. 2004 – Fungi Fimicoli Italici. A.M.B.Fondazione Centro Studi, Livorno.
Doveri F. 2014 – An update on the genera Ascobolus and Saccobolus with keys and descriptions of
three coprophilous species, new to Italy. Mycosphere 5(1), 86–135.
Ebersohn C, Eicker A. 1991 – Coprophilous fungal species composition and species diversity on
various dung substrates of african game animals. Botanical Bulletin of Academia Sinica.
33, 8595.
Kirk PM, Cannon PF, Minter DW, Stalpers JA. 2008 – Dictionary of the Fungi. CABI,
Wallingford.
Krug JC, Benny GL, Keller, HW. 2004 – Coprophilous fungi. 467–499, in Mueller GM et al.
(eds.), Biodiversity of fungi. Inventory and monitoring methods. Elsevier Academic Press,
London.
804
Melo RFR, Bezerra JL,Cavalcanti MAQ. 2012 – Diversity of coprophilous Ascomycetes from
captive wild animals in Dois Irmãos State Park, Brazil. Nova Hedwigia 94, 153–162.
Pugh, GJF, Boddy L. 1988 – A view of disturbance and life strategies in fungi. Proceedings of the
Royal Society of Edinburgh 94B, 3–11.
Richardson MJ. 2001a – Coprophilous Fungi from Brazil. Brazilian Archives of Biology and
Technology 44, 283–289.
Richardson, M.J. 2001b – Diversity and occurrence of coprophilous fungi. Mycological Research
105, 387–402.
Richardson MJ. 2007 – The distribution and ocurrence of Ascobolaceae. Mycologia Montenegrina
10, 211–227.
Richardson MJ, Watling R. 1997 – Keys to Fungi on Dung. British Mycological Society,
Stourbridge.
Shannon CE. 1948 – A mathematical theory of communication. The Bell System Technical
Journal, 27, 379–423 and 623–656.
Spegazzini, C. 1899 – Fungi Argentini novi vel critici. Anales del Museo Nacional de Historia
Natural Buenos Aires 6: 81–365.
Webster J. 1970 – Presidential Address. Coprophilous fungi. Transactions of the Britsh
Mycological Society 54, 161–180.
Van Brummelen J. 1967 – A world monograph of the genera Ascobolus and Saccobolus. Persoonia,
Supplement 1, 1–260.
www.iapt-taxon.org – 2011.
www.indexfungorum.org – 2011.
