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© 2017 J. Cramer in Gebr. Borntraeger Verlagsbuchhandlung, Stuttgart, www.borntraeger-cramer.de
Germany. DOI: 10.1127/nova_hedwigia/2017/0410 0029-5035/2017/0410 $ 8.25
Nova Hedwigia
published online April 2017 PrePub Article
C
New and interesting Laboulbeniales from Panama and
neighboring areas
Danny Haelewaters1,2*, Sarah J.C. Verhaeghen1, Tómás A. Ríos
Gonzáles3, Juan A. Bernal Vega4 and Rosa V. Villarreal Saucedo5
1 Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University,
Cambridge, Massachusetts 02138, U.S.A.
2 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge,
MA 02138, U.S.A.
3 Programa Centroamericano de Maestría en Entomología, Universidad de Panamá,
Panamá
4 Museo de Peces de Agua Dulce e Invertebrados, Universidad Autónoma de Chiriquí,
0427, David, Chiriquí, Panamá
5 Herbario, Universidad Autónoma de Chiriquí, 0427, David, Chiriquí, Panamá
With 3 gures and 2 tables
Abstract: We present 33 new records of Laboulbeniales from Central American countries on hosts
of the orders Blattodea, Coleoptera, and Diptera. Twenty-seven records are new for Panama. These
are Amorphomyces ophioglossae on Ophioglossa sp.; Chitonomyces hyalinus on Laccophilus pictus;
Ch. simplex on Laccophilus fasciatus and L. pictus; Dimeromyces homophoetae on Capraita sp.;
Eucantharomyces calleidae on Calleida aurata; Gloeandromyces pageanus sp. nov. on Trichobius
dugesioides; G. streblae on Trichobius spp.; Herpomyces chaetophilus on Periplaneta americana;
Hesperomyces virescens on Azya orbigera, Brachiacanthini gen. & sp. indet., Cycloneda sanguinea,
and Epilachna mexicana; Kleidiomyces hoplandriae on Hoplandria sp.; Laboulbenia bruchii on
Neolema sp.; L. coccinellidicola sp. nov. on Exochomus childreni and Exochomus sp. 1; L. disenochi on
Platynus purpurellus; L. ecitonis on Ecitophya sp.; L. flabelliformis on Asphaera transversofasciata;
L. fuliginosa and L. idiostoma on Altica bimarginata; L. perplexa and L. punctata on Galerita sp.;
L. skelleyi on Ischyrus sp. and Pselaphacus sparsus; L. systenae on Systena sp.; L. trogacti on
Carpelimus sp.; Neohaplomyces medonalis on Medinina gen. & sp. indet. and Paederinae gen. &
sp. indet.; Nycteromyces streblidinus on Trichobius joblingi; Peyritschiella protea on Platydracus
prasinvariegatus; Rhachomyces longissimus on Platynus lyratus; and Stichomyces conosomatis on
Sepedophilus sp. The number of species of Laboulbeniales in Panama is raised to 78. An alphabetical
parasite-host list of Panamanian Laboulbeniales is given. Additionally, the following new records
are presented for neighboring areas: Chitonomyces paradoxus on Laccophilus proximus from the
Bahamas; Gloeandromyces nycteribiidarum on Trichobius yunkeri from Costa Rica; Herpomyces
*Corrsponding author: dhaelewaters@fas.harvard.edu
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paranensis on Archimandrita tessellata from Colombia and Costa Rica; Hesperomyces palustris on
Coleomegilla maculata from Cuba; Laboulbenia fallax on Gyretes sp. from Trinidad; L. flabelliformis
on Asphaera nobilitata from Trinidad; L. funeralis on Gyrinus sp. from Costa Rica; and L. systenae
on Systena basalis from Haiti and on S. s-littera from Trinidad. Archimandrita, Azya, Capraita,
Epilachna, Ischyrus, and Trichobius are reported as new host genera for Laboulbeniales. Illustrations
are given for 16 species.
Key words: Ascomycota, Central America, ectoparasites, insect-fungus interactions, new species,
taxonomy.
Introduction
Recent study of the genus Laboulbenia Mont. & C.P.Robin in Panama yielded five
species that were for the first time reported for the country, including the newly
described L. tortilis J.A.Bernal & R.Kirschner This study (Villarreal et al. 2010)
initiated collecting insects and screening them for the presence of Laboulbeniales
by local students at the Universidad Autónoma de Chiriquí (Jennifer Castillo, Betty
Espinosa, Laura Gaitán, Leila Gonzalez, Katerine Gutierrez). It also initiated the
collaboration of DH (Pfister Lab, Harvard University) with JB and RV (Universidad
Autónoma de Chiriquí), of which this manuscript is the first physical output.
In this contribution, we provide details for 27 species of Laboulbeniales, all of which
represent new records for Panama. New records of Laboulbeniales are also reported
from the following countries: Bahamas, Colombia, Costa Rica, Cuba, Haiti and Trini-
dad and Tobago.
Most of these parasites and their hosts have been reported elsewhere in Central or South
America. However, we also found thalli of Gloeandromyces on the bat fly Trichobius
dugesioides Wenzel, 1966 (Diptera, Streblidae) and Laboulbenia Mont. & C.P.Robin
on ladybirds (Coleoptera, Coccinellidae) of the genus Exochomus Redtenbacher, 1843.
These specimens did not fit any of the descriptions in the literature available to us and
thus are described as new species, G. pageanus and L. coccinellidicola.
Materials and methods
The first source for our collections were dried insect specimens at entomological collections of
the American Museum of Natural History in New York (AMNH), Harvard University Museum
of Comparative Zoology in Cambridge, MA (MCZ); Museo de Peces de Agua e Invertebrados
(MUPADI); and Tupper Center of the Smithsonian Tropical Institute, in Ancon, Panama (STRI). DH
and SJCV carefully screened insects under dissecting microscopes at 50× magnification.
Second, insects were collected in the field by all authors and students using pitfall traps, aquatic nets,
entomological nets, or mistnets (for capturing bats), and by hand. Insects were stored in 70–95%
ethanol for transport to the laboratory where they were screened under 50× magnification. Parasitized
insects were separated from the uninfected ones and permanently stored in 95% ethanol.
Laboulbeniales thalli were transferred using a Minuten Pin (BioQuip #1208SA, Rancho Dominguez,
CA) and embedded in Amann solution (Benjamin 1971) with the help of a drop of Hoyer’s medium
(30 g arabic gum, 200 g chloral hydrate, 16 mL glycerol, 50 mL ddH20), as described by Haelewaters
et al. (2015b). Microscopic slides are deposited at FH (Farlow Herbarium, Harvard University),
MIUP (Museo de Invertebrados de la Universidad de Panamá), and UCH (Universidad Autónoma
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de Chiriquí). For Laboulbeniales removed from host specimens deposited at STRI, all "b" slides are
deposited at MIUP, the other ones at FH.
Observations and measurements of fungal specimens were made at the Pfister Lab using an Olympus
BX40 light microscope with Olympus XC50 digital camera and MicroSuite Special Edition software
3.1 (Soft Imaging Solutions GmbH). Images were optimized (with LEVELS and BRIGHTNESS/
CONTRAST tools) and cropped in Adobe Photoshop CS Version 8.0 (San Jose, California).
Finally, fungal material was found in unidentified microscopic slides from Roland Thaxter, whose
entire collection has been deposited at FH [except for co-types, which are deposited at the Muséum
National d’Histoire Naturelle in Paris, France (PC)]. The examination of these slides led to the
discovery of some unpublished records, which are presented and discussed in this paper.
Using the modified Extract-N-Amp Plant PCR Kit as outlined in Haelewaters et al. (2015a), we
isolated DNA, amplified the ribosomal small subunit (SSU) gene, and obtained a partial sequence
from H. virescens thalli removed from a specimen of Coccinellidae. The sequence was deposited
in GenBank (KX533512).
Taxonomy
Amorphomyces ophioglossae Thaxt., Proc. Am. Acad. Arts Sci. 48: 167 (1912).
Fig. 1A
Known distribution and hosts: Described on Ophioglossa (?) cava (Sharp, 1876)
from Argentina (Thaxter 1912) and since then only reported from Guatemala on an
unidentified staphylinid (Thaxter 1931).
new records from central america: PANAMA. On Ophioglossa sp. (Coleoptera, Staphylinidae,
Aleocharinae), Potrerillos Arriba (Chiriquí), i.2012, leg. J.Castillo & B.Espinosa, det. T.Ríos, in coll.
MUPADI, D.Haelew. 1001b (FH).
remarKs: Amorphomyces ophioglossae is closely related to A. minusculus Thaxt.,
which occurs on the same host genus. However, in female thalli of A. ophioglossae
the perithecial apex is distinctly suffused with dark brown on one side (Santamaría
2000, figs 18 & 26), which is obvious in the material we obtained.
Chitonomyces hyalinus Thaxt., Mem. Am. Acad. Arts Sci. 12: 291 (1896).
≡ Heimatomyces hyalinus Thaxt., Proc. Am. Acad. Arts Sci. 27: 31 (1892).
= Heimatomyces marginatus Thaxt., Proc. Am. Acad. Arts Sci. 27: 34 (1892).
= Chitonomyces marginatus (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 289 (1896).
Known distribution and hosts: Chitonomyces hyalinus was described [as Heimatomyces
hyalinus] on Laccophilus maculosus Say, 1823 (Coleoptera, Dytiscidae, Laccophilinae)
from Connecticut, U.S.A. (Thaxter 1892) and since then found only a few times on
Laccophilus spp.: in Grenada, Trinidad (Thaxter 1924), Brazil (Rossi & Bergonzo
2008), and New York, U.S.A. (Goldmann & Weir 2012). Recently Chitonomyces
marginatus was shown to be synonymous with C. hyalinus (Goldmann & Weir 2012).
The former has been found on Laccophilus spp. and Hydroporus spurius LeConte,
1855 in the U.S.A. and Jamaica (Thaxter 1892, 1924).
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new records from central america: PANAMA. On female Laccophilus pictus Laporte, 1835, NE
of Santa Fe (Veraguas), Río Mulabá, 24.viii.2006, rock pools, leg. and det. D.Post, in coll. STRI
(SYNOPTIC STRI-ENT 0 107 823), D.Haelew. 891a–b (FH, MIUP).
remarKs: The observed thalli fit the description of the"morphospecies" Ch. marginatus
(Thaxter 1896), which was synonymized with Ch. hyalinus (Goldmann & Weir
2012). The issues of position specificity and position-induced polymorphisms have
recently received a lot of attention, especially for species occurring on aquatic hosts.
Thirteen morphospecies of Chitonomyces Peyr. on L. maculosus were studied using
both phylogenetic and ecological data, resulting in synonomies and the recognition
of six species following the phylogenetic species concept (Goldmann & Weir 2012).
We found Ch. hyalinus together with Ch. simplex (slide D.Haelew. 891c) on the same
host specimen. Chitonomyces hyalinus was found along the margin of the left elytron
(between bristles), while Ch. simplex was found at the tip of the right elytron. Rossi
and Bergonzo (2008) also found this combination on Laccophilus fasciatus in Brazil,
but they also found up to five other position-specific morphospecies on this host.
Chitonomyces paradoxus (Peyr.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 287 (1896).
≡ Heimatomyces paradoxus Peyr., Sitzb. k. Akad. Wissensch., Math.-naturwiss. Cl. 68: 251 (1873).
= Heimatomyces unciger Thaxt., Proc. Am. Acad. Arts Sci. 30: 478 (1895).
= Chitonomyces unciger (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 288 (1896).
= Chitonomyces truncatus Speg., Anales Mus. Nac. Hist. Nat. Buenos Aires 27: 47 (1915).
Known distribution and hosts: On Laccophilus spp. (Coleoptera, Dytiscidae,
Lacco-philinae) from many countries, in Europe, North and Central America,
and Asia (Santamaría 2001). Most recently it was found on Laccophilus hyalinus
(De Geer, 1774) in Belgium (De Kesel & Werbrouck 2008), Laccophilus spp.
in Sweden (Huggert & Eriksson 2010), L. maculosus in New York, U.S.A.
(Goldmann & Weir 2012), and Laccophilus poecilus Klug, 1834 in Turkey (Rossi
2016). Chitonomyces truncatus, a synonym of Ch. paradoxus, was described
from Italy (Spegazzini 1915). Goldmann & Weir (2012) synonymized it with
Ch. unciger, based on the combination of molecular and ecological data.
Chitonomys unciger was described on L. maculosus from Connecticut, U.S.A.
(Thaxter 1895), and later found on Laccophilus spp. from Florida, U.S.A. and
China (Thaxter 1924).
new records from central america: BAHAMAS. On female Laccophilus proximus Say, 1823,
West End (Grand Bahama Island), 12.v.1953, leg. E.B.Hayden, in coll. AMNH, D.Haelew. 295a
(FH 00313437).
remarKs: Chitonomyces paradoxus is recognized by its compact habitus, the more
or less triangular cell h, and the perithecial outgrowth, which is pointed obliquely
upwards and tapering distally to a rounded point. Thaxter (1924) pointed out that
there is considerable morphological variation in this species, and Majewski (1994)
and Santamaría (2001) described three morphological forms on the three European
Laccophilus hosts [L. hyalinus, L. minutus (Linnaeus 1758), L. poecilus Klug, 1834].
However, in America (as well as in Asia) many more species serve as host to this
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species, which makes it hard to define its specific limits.
Chitonomyces simplex Thaxt., Mem. Am. Acad. Arts Sci. 12: 292 (1896).
≡ Heimatomyces simplex Thaxt., Proc. Am. Acad. Arts Sci. 27: 30 (1892).
= Heimatomyces uncinatus Thaxt., Proc. Am. Acad. Arts Sci. 27: 33 (1892).
= Chitonomyces uncinatus (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 291 (1896).
Known distribution and hosts: Reported from Laccophilus spp. (Coleoptera,
Dytiscidae, Laccophilinae) in Brazil, Grenada, Guatemala, Trinidad, and the U.S.A.
(Thaxter 1896, 1924, Rossi & Bergonzo 2008, Goldmann & Weir 2012).
new records from central america: PANAMA. On Laccophilus fasciatus Aubé, 1838, El Copé
Road, 1 km N of Pan-American Highway (Coclé), 29.viii.2006, roadside ditch, leg. and det. D.Post,
in coll STRI (SYNOPTIC STRI-ENT 0 107 818), D.Haelew. 888b (MIUP). On female L. pictus
Laporte, 1835, NE of Santa Fe (Veraguas), Río Mulabá, 24.viii.2006, rock pools, leg. and det. D.Post,
in coll. STRI (SYNOPTIC STRI-ENT 0 107 823), D.Haelew. 891c (FH).
remarKs: Thalli of C. simplex were removed from the tip of the right elytron from
both L. fasciatus and L. pictus. This is the growth position of the "typical" Ch.
simplex, with which Ch. uncinatus was recently synonymized (Goldmann & Weir
2012). Chitonomyces uncinatus occurs on the left-hand side of sternites 4–5 of male
host specimens only. The most distinctive feature of these two morphospecies is
the curvature of the perithecium; in Ch. simplex the perithecium curves away from
the primary appendage, in Ch. uncinatus it curves toward the primary appendage.
Despite consistent morphological differences, both species are recognized as a single
phylogenetic species (Goldmann & Weir 2012).
Dimeromyces homophoetae Thaxt., Proc. Am. Acad. Arts Sci. 50: 19 (1914).
Known distribution and hosts: Reported on Omophoita aequinoctialis (Linnaeus,
1758) [as Homophoeta] (Coleoptera, Chrysomelidae, Galerucinae) of Grenada,
Guatemala, and Trinidad (Thaxter 1914), and on Omophoita octoguttata (Fabricius,
1775) [as Homophoeta] from Argentina (Spegazzini 1917).
new records from central america: PANAMA. On Capraita sp. (Coleoptera, Chrysomelidae,
Galerucinae), Potrerillos Abajo (Chiriquí), N8°38'55.48"W 82°28'14.10", 648 m a.s.l., 20.vii.2016,
abandoned orange plantation, leg. Y.Aguirre, J.Bernal & D.Haelewaters, det. T.Ríos, in coll. MUPADI,
D.Haelew. 1105a–b (FH). Same data, D.Haelew. 1106a–b (UCH).
remarKs: To date, 11 species of Dimeromyces Thaxt. on Chrysomelidae have been
described (Haelewaters & Rossi 2015, Rossi et al. 2016). Dimeromyces homophoetae
is easily distinguished from the others by the pointed terminal cell of the primary
appendage of the female thallus (Thaxter 1924). Dimeromyces bubalinus W.Rossi et
al. shares this character but has a very different perithecial tip, with symmetrically
divergent, curved outgrowths (Rossi et al. 2015).
Eucantharomyces calleidae Thaxt., Proc. Am. Acad. Arts Sci. 35: 418 (1900).
Fig. 1B
Known distribution and hosts: Only known from Calleida spp. [misspelled as
"Callida"] in Suriname and Venezuela (Thaxter 1908).
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new records from central america: PANAMA. On Calleida aurata Motschulsky, 1864 [as
C. "anypterygioides"] (Coleoptera, Carabidae, Harpalinae), Cerro Picacho (Panamá), N8°38'W
80°03', 800 m a.s.l., 21.vi.1992, leg. and det. H.P.Stockwell, in coll. STRI (STOCKWELL STRI-
ENT 0 043 594), D.Haelew. 871a (FH).
remarKs: Eucantharomyces Thaxt. currently contains 29 species (Thaxter 1895,
Santamaría 2006, Rossi & Ponziani 2008). All of its members parasitize ground beetles
(Coleoptera, Carabidae). For species delineation features of the compound antheridium
and perithecium are used. For example, the number of antheridial cells and rows and the
spore apex remnant serve as diagnostic characters, as well as details of the perithecial
wall cells (e.g. with corrugations). However, despite Thaxter’s (1908) suggestion that
the number of antheridial cells for each row is constant, this is not a very reliable
character (Santamaría 1994, 2006). Eucantharomyces calleidae is recognized by the
structure of the base of the thallus: cells I and II of the receptacle are (sub-)equal and
lie next to each other. Cell III extends downward, hence covering the posterior side
of the upper half of cell II.
Gloeandromyces nycteribiidarum (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 16: 113
(1931). Fig. 1C
≡ Stigmatomyces nycteribiidarum Thaxt., Proc. Am. Acad. Arts Sci. 52: 702 (1917).
Known distribution and hosts: Described on Megistopoda aranea (Coquillett, 1899)
[as Pterellipsis aranea] (Diptera, Streblidae, Trichobinae), parasitic on Artibeus
jamaicensis grenadensis [as A. grenadensis] (Mammalia, Chiroptera, Phyllostomidae)
from Grenada (Thaxter 1931).
new records from central america: COSTA RICA. On male Trichobius yunkeri Wenzel, 1966
(Diptera, Streblidae, Trichobinae), Santa Rosa National Park (Guana-caste), 5.iii.2012, parasitic on
female Pteronotus parnellii (Mammalia, Chiroptera, Phyllostomidae), 2012CR296, leg. and det.
T.Hiller, in coll. MCZ, slide D.Haelew. 946a (FH). Same data, D.Haelew. 947a (FH).
RemarKs: Gloeandromyces Thaxt. includes only two species, G. nycteribiidarum
(Thaxt.) Thaxt. and G. streblae (Thaxt.) Thaxt. Gloeandromyces nycteribiidarum
was first described on a bat fly, which, however, was misidentified as a nycteribiid fly.
This explains the epithet reference, while the host belongs to the family Streblidae.
Because bat flies are blood-sucking ectoparasites of bats (Mammalia, Chiroptera), the
Laboulbeniales parasitizing these hosts can be considered hyperparasites.
The two species in the genus Gloeandromyces can be differentiated based on their total
length, perithecial features, and the way they attach to the host, which is by a rhizoidal
haustorium in G. nycteribiidarum or a blackened foot in G. streblae (Thaxter 1931).
The Costa Rican material represents the second report only for G. nycteribiidarum.
Gloeandromyces pageanus Haelew., sp. nov. Fig. 1D
MycoBank number MB 819381.
diagnosis: Different from the other species in the genus by its peculiar perithecial
bulbous outgrowths and finger-like projections.
types: PANAMA. On female Trichobius dugesioides Wenzel, 1966 (Diptera, Streblidae, Trichobinae),
collected in Gamboa (Colón), 26.vi.2016, parasitic on female Trachops cirrhosus (Mammalia,
eschweizerbart_xxx
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Chiroptera, Phyllostomidae), leg. R.Page et al., det. T.Hiller, D.Haelew. 1093a (HOLOTYPE, 6 mature
thalli, prescutum and scutum, FH). On female T. dugesioides, Gamboa (Colón), 24.vi.2016, parasitic
on male Trachops cirrhosus, leg. R.Page et al., det. T.Hiller, D.Haelew. 1092a (PARATYPE, 1 mature
thallus, prescutum, FH). Same data, D.Haelew. 1091a (PARATYPE, 1 mature thallus, right-hand side
thorax, FH). On male T. dugesioides, Gamboa (Colón), 2.vii.2016, parasitic on Trachops cirrhosus,
leg. R.Page et al., det. T.Hiller, D.Haelew. 1094a (PARATYPE, 4 mature thalli, right prescutum, FH).
On female T. dugesioides, same data, D.Haelew. 1098a (PARATYPE, 1 mature thallus, thorax, FH).
etymology: Referring to Dr. Rachel Page (Smithsonian Tropical Research Institute),
mammologist, collaborator, and Principal Investigator at the Bat Lab in Gamboa.
Description: thallus: 195–257 µm long from foot to perithecial tip. Irregularly colored
reddish, darker at the basal cell of the appendage, the perithecial bulbous outgrowth,
and the finger-like projections; upper part of cell III and cells VI and VII tinged
with orange. receptacle: Cell I anteriorly curved, longer than broad, with divergent
margins, 45–74 ×31–44 µm (above), carrying cells II and VI. Cell II trapezoidal,
slightly broader than long. Cell III isodiametrical, with rounded lower anterior
margin. appendage: Basal cell 7–10 ×11–13 µm, pentagonal, with parallel anterior
and posterior margins, carrying two very short branches of dichotomously dividing
cells; final cells antheridial. perithecium: Cell VI obliquely positioned between cells
II and VII, broadly triangular, lower margin rounded, broader than long. Perithecium
113–139 × 43–52 µm (not including bulbous outgrowth), obclavate, anterior margin
with a short and bulbous outgrowth at lower third; halfway at the posterior side two
finger-like projections obliquely directed upwards, up to 46 µm in length; neck well
distinguished, upper half of posterior side with two very short bulbous outgrowths, the
upper one slightly smaller and darkly pigmented; tip undifferentiated, blunt. Ascospores
bicellular, 30–35 × 3–5 µm.
remarKs: Its perithecial bulbous outgrowth and finger-like projections separate the
new species from the two known species in the genus Gloeandromyces (Thaxter 1917,
1931). These characteristics are stable, and have been observed in all studied specimens.
Gloeandromyces pageanus shares with G. streblae a simple, blackened foot.
The host for G. pageanus, Trichobius dugesioides, is also reported for G. streblae in
Panama. On most of the host specimens, we removed thalli of both parasite species
(Table 1). Gloeandromyces pageanus was always found on the thorax, while G. streblae
occurs mostly on the wings (Table 1). While G. pageanus seems limited to the thorax
(based on the available material), G. streblae has no positional restrictions; we have
observed this species on the thorax, legs, and wings. On one bat fly, both species co-
occurred on the right prescutum. This confirms that the two taxa are separate species.
Gloeandromyces streblae (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 16: 113 (1931).
Fig. 1G
≡ Stigmatomyces streblae Thaxt., Proc. Am. Acad. Arts Sci. 52: 700 (1917).
Known distribution and hosts: Described on Strebla wiedemanni Kolenati, 1856 [as
S. vespertilionis] (Diptera, Streblidae, Streblinae) from Venezuela.
new records from central america: PANAMA. On male Trichobius dugesioides (Diptera,
Streblidae, Trichobinae), Bohio (Panama Canal Zone), 29.ix.2013, parasitic on female Trachops
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Table 1. Overview of all bat fly-associated Laboulbeniales discussed in this paper, with information
of bat species, bat fly species, and position on the bat fly host from where thalli were removed.
Bat host Bat fly host Position on bat fly D.Haelew. # Parasite species Country
Pteronotus
parnellii Trichobius
yunkeri mouth parts 946a Gloeandromyces
nycteribiidarum Costa Rica
Pteronotus
parnellii Trichobius
yunkeri ventral head 947a Gloeandromyces
nycteribiidarum Costa Rica
Carollia
perspicillata Trichobius
joblongi left protibia 1066a Nycteromyces
streblidinus Panama
Pteronotus
parnellii Trichobius
yunkeri left wing 1067a Gloeandromyces
streblae Panama
Trachops
cirrhosus Trichobius
dugesioides right mesofemur 1068a Gloeandromyces
streblae Panama
Carollia
perspicillata Trichobius
joblingi
wings 1071a Gloeandromyces
streblae Panama
head & left
metafemur 1071b Nycteromyces
streblidinus
Carollia
castanea Trichobius
joblingi left profemur 1088a
Gloeandromyces
streblae
Nycteromyces
streblidinus
Panama
Trachops
cirrhosus Trichobius
dugesioides
right-hand side
thorax 1091a Gloeandromyces
pageanus Panama
lateral margin right
wing 1091c Gloeandromyces
streblae
Trachops
cirrhosus Trichobius
dugesioides prescutum 1092a Gloeandromyces
pageanus Panama
Trachops
cirrhosus Trichobius
dugesioides
prescutum &
scutum 1093a Gloeandromyces
pageanus Panama
lateral margin right
wing 1093c Gloeandromyces
streblae
Trachops
cirrhosus Trichobius
dugesioides right prescutum 1094a
Gloeandromyces
pageanus
Gloeandromyces
streblae
Panama
Trachops
cirrhosus Trichobius
dugesioides thorax 1098a Gloeandromyces
pageanus Panama
cirrhosus (Mammalia, Chiroptera, Phyllostomidae), P_0191, leg. and det. T.Hiller, in coll. MCZ,
D.Haelew. 1068a (FH). On male Trichobius joblingi Wenzel, 1966, Bohio (Panama Canal Zone),
2015, parasitic on female Carollia perspicillata (Mammalia, Chiroptera, Phyllostomidae), P_3935,
leg. and det. T.Hiller, in coll. MCZ, D.Haelew. 1071a (FH). On female Trichobius yunkeri Wenzel,
1966, Isla Barro Colorado (Panamá Oeste), 19.iv.2014, parasitic on female Pteronotus parnellii
(Mammalia, Chiroptera, Phyllostomidae), WP1_344, leg. and det. T.Hiller, in coll. MCZ, D.Haelew.
1067a (FH). On male T. joblingi, Gamboa (Colón), 13.vi.2016, parasitic on male Carollia castanea
(Mammalia, Chiroptera, Phyllostomidae), leg. R.Page et al., det. T.Hiller, D.Haelew. 1088a (FH).
On female T. dugesioides, Gamboa (Colón), 24.vi.2016, parasitic on male Trachops cirrhosus, leg.
R.Page et al., det. T.Hiller, D.Haelew. 1091c (FH). On female T. dugesioides, Gamboa (Colón),
26.vi.2016, parasitic on female Trachops cirrhosus, leg. R.Page et al., det. T.Hiller, D.Haelew. 1093c
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9
(FH). On male T. dugesioides, Gamboa (Colón), 2.vii.2016, parasitic on Trachops cirrhosus, leg.
R.Page et al., det. T.Hiller, D.Haelew. 1094a (FH).
RemarKs: The material from Panama represents only the second report for this species.
When Thaxter (1917) described G. streblae, he did not mention a bat host species.
However, S. wiedemanni typically parasitizes the common vampire bat Desmodus
rotundus (Mammalia, Chiroptera, Phyllostomidae) (Dick 2013). The host species for
G. streblae belong to two subfamilies: Streblinae (Strebla) and Trichobinae
(Trichobius). This seems to suggest a less strict host relationship for this species.
More data are required to understand the host specificity dynamics for this and other
species infecting bat flies.
Herpomyces chaetophilus Thaxt., Proc. Am. Acad. Arts Sci. 38: 12 (1902).
Known distribution and hosts: On Periplaneta spp. (Blattodea, Blattidae, Blattinae)
in "the Amazon", Mauritius, Peninsular Malaysia, and Zanzibar (Thaxter 1902, 1931,
Sugiyama & Mochizuka 1979). Only recently the fungus was discovered on Periplaneta
americana (Linnaeus, 1758) in Massachusetts, U.S.A. (Wang et al. 2016a).
new records from central america: PANAMA. On Periplaneta americana, Bágala (Chiriquí),
ix.2012, leg. Y.Saldaña, det. R.Santanach, in coll. MUPADI, D.Haelew. 932a (UCH). On P. americana,
Gamboa (Colón), 183 Harding Avenue, N 9°06'58.64", W 79°41'52.89", 15.vii.2016, apartment floor,
leg. and det. D.Haelewaters, in coll. MUPADI, D.Haelew. 1097a (FH).
RemarKs: Herpomyces chaetophilus is easily distinguished from other species in
the same genus for the following characters: (1) its solitary perithecium, with the tip
bending anteriorly and (2) the absence of a cellular upgrowth (or "shell-like shield";
Thaxter 1908) at the base of the perithecium.
This record is the first for Central America. Herpomyces chaetophilus is now known
from North, Central, and South America, Africa, and Asia. Wang et al. (2016a)
hypothesized that H. chaetophilus was somehow introduced with P. americana
to the United States, most likely after Thaxter’s time, who did not record it from
North America during his extensive studies. In the light of the recent records from
Massachusetts, U.S.A. (Wang et al. 2016a) and Panama (this paper) it will be interesting
to demonstrate routes of invasion by performing population genetics.
Herpomyces paranensis Thaxt., Proc. Am. Acad. Arts Sci. 38: 19 (1902). Fig. 1E
Known distribution and hosts: Herpomyces paranensis was described on Blaberus sp.
[as Blabera] from Brazil, and since then only found in Mexico on another unidentified
species of Blaberus Serville, 1831 (Thaxter 1902, 1908).
new records from central america: COLOMBIA. On Archimandrita tessellata Rehn, 1903
(Blattodea, Blaberidae, Blaberinae), no locality, 3.vi.1889, leg. Sleight, det. Bacon, in coll. AMNH,
D.Haelew. 615a (FH). COSTA RICA. On A. tessellata, Santa Rosa National Park (Guanacaste),
xi.2012, leg. A.R.Deans, det. L.M.Roth, in coll. MCZ, D.Haelew. 609c (FH).
RemarKs: This marks the first record of this fungus after more than a century.
Archimandrita Saussure, 1893 is a new host genus for this fungus. It belongs to the
same subfamily (Blaberinae) as Blaberus. This implies that the host specificity of H.
paranensis is not restricted to genus but (at least) to subfamily.
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Hesperomyces palustris W.Rossi & A.Weir, Fungal Biol. 117: 812 (2013). Fig. 1F
Known distribution and hosts: Only known from Coleomegilla maculata (DeGeer,
1775) (Coleoptera, Coccinellidae, Coccinellinae) in Ecuador (holotype) and Costa
Rica (Goldmann et al. 2013).
new records from central america: CUBA. On C. maculata, Viñales (Pinar del Río), 27–31.1951,
leg. P.Vaurie, det. G.H.Dieke, in coll. AMNH, D.Haelew. 379a–b (FH).
remarKs: Hesperomyces coleomegillae W.Rossi & A.Weir and H. palustris were
recently described as two phylogenetic species, each with two morphospecies on
precise positions of the host body (= position specificity; Goldmann et al. 2013). Both
species are the only ones of about 2,100 described species of Laboulbeniales for which
molecular analyses were used to back up the morphological observations.
Hesperomyces palustris has two morphotypes, one on the legs and one on the margins
of the elytra. Our material was collected from the margin of the right elytron and is
consistent with the morphotype description from this area.
Hesperomyces virescens Thaxt., Proc. Am. Acad. Arts Sci. 25: 264 (1891).
≡ Stigmatomyces virescens (Thaxt.) Thaxt., Proc. Am. Acad. Arts Sci. 29: 106 (1894).
Known distribution and hosts: Described on Chilocorus stigma (Say, 1835) [as
C. bivulnerus] (Coccinellidae, Coccinellinae, Chilocorinae) from California, U.S.A. It is a
widespread species known from all continents except Antarctica, hosted by several genera
of Coccinellidae (Santamaría et al. 1991, Ceryngier et al. 2012). Most recent records were
found on the globally invasive Harmonia axyridis (Pallas, 1773) in Argentina, Austria,
Canada, France, Slovakia, and South Africa (Haelewaters et al. 2017).
New records from central America: PANAMA. On Epilachna mexicana (Guérin-Méneville,
1842) (Coleoptera, Coccinellidae, Epilachninae), Volcán (Chiriquí), N8°47'23.47"W 82°38'44.93",
20.vii. 2015, leg. J.Bernal & S.Verhaeghen, det. D.Haelewaters, in coll. MCZ, D.Haelew. 930a
(FH). On Azya orbigera Mulsant, 1850 (Coleoptera, Coccinellidae, Coccidulinae), Potrerillos Abajo
(Chiriquí), N8°38'55.48"W 82°28'14.10", 648 m a.s.l., 19.vii.2015, abandoned orange plantation,
leg. M.Fuentes, L.Gonzalez, D.Haelewaters, R.Villarreal & S.Verhaeghen, det. D.Haelewaters, in
coll. MCZ, D.Haelew. 925a (FH). Same data, 20.vii.2016, leg. Y.Aguirre, J.Bernal & D.Haelewaters,
det. D.Haelewaters, in coll. MUPADI, D.Haelew. 1103a (FH). Same data, D.Haelew. 1104a
(FH). Same data, 21.vii.2016, leg. J.Bernal, L.Gonzalez, M.Fuentes, J.Trejos & R.Villarreal, det.
D.Haelewaters, in coll. MUPADI, D.Haelew. 1109a (FH). On Brachiacanthini gen. & sp. indet.
(Coleoptera, Coccinellidae, Scymninae), 6 km S of Ipetí (Panamá), 350 m a.s.l., 8.xi.1992, leg.
A.R.Gillogly, det. R.G.Boothe, in coll. STRI (STOCKWELL STRI-ENT 0 059 403), D.Haelew.
881a (FH). On Cycloneda sanguinea (Linnaeus, 1763) (Coleoptera, Coccinellidae, Coccinellinae),
Volcán, Urbanización La Florida (Chiriquí), N8°47'23.47"W 82°38'44.93", 20.vii.2015, leg. J.Bernal
& S.Verhaeghen, det. D.Haelewaters, in coll. MCZ, isolate D.Haelew. 929a.
Fig. 1. A. Amorphomyces ophioglossae (D.Haelew. 1001b). B. Eucantharomyces calleidae (D.Haelew.
871a), with cells I, II, and III of the receptacle labeled. C. Gloeandromyces nycteribiidarum (D.Haelew.
947a). D. Gloeandromyces pageanus sp. nov. (D.Haelew. 1092a), with indication of cells I, II, III,
VI, and the perithecium (p). E. Herpomyces paranensis (D.Haelew. 609c). F. Hesperomyces palustris
(D.Haelew. 379b). G. Gloeandromyces streblae (D.Haelew. 1096a). H. Neohaplomyces medonalis
(D.Haelew. 895a). Scale bars = 50 µm.
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RemarKs: Hesperomyces virescens was already known from many representatives of
three subfamilies within Coccinellidae: Chilocorinae, Coccinellinae, and Scymninae.
The new findings from Panama add two subfamilies to the host range of H. virescens:
Coccidulinae (Azya orbigera) and Epilachninae (Epilachna mexicana). The observed
infection prevalence of H. virescens on A. orbigera was 4.5% in 2015 (18–19 Jul,
n = 110). We went back to Potrerillos Abajo in 2016, and collected 4 specimens of
A. orbigera infected with H. virescens, marking a prevalence of 12.2% (19–21 Jul,
n = 41). However, thallus density on A. orbigera is extremely low, with 1–3 thalli per
host specimen.
An SSU rDNA sequence (isolate D.Haelew. 929a) from thalli removed from C. san-
guinea is available in GenBank with accession number KX533512. It is 99–100%
similar (100% query cover) to publicly available sequences of H. virescens from
Cheilomenes propinqua (Mulsant, 1850), H. axyridis, and Olla v-nigrum (Mulsant,
1866), confirming its identity as H. virescens. Not enough thalli were available on this
host specimen to also make microscope slides.
Kleidiomyces hoplandriae Thaxt., Proc. Am. Acad. Arts Sci. 25: 264 (1891).
Known distribution and hosts: Reported on Hoplandria spp. (Coleoptera,
Staphylinidae, Aleocharinae) from Ecuador, Grenada, and Trinidad (type) (Thaxter
1931, Bernardi et al. 2014).
New records from central america: PANAMA. On Hoplandria sp., Gamboa (Colón), Pipeline
Road KM7, 20.v-11.vi.1996, leg. S.Lingafelter, det. J.S.Ashe, in coll. STRI (SYNOPTIC STRI-ENT
0 108 324), D.Haelew. 910a–b (FH, MIUP).
remarKs: Kleidiomyces hoplandriae was described on Hoplandria "carinicollis",
which "appear[s] not to be valid" according to Frank (1982). Also the host for the
Ecuadorian material, Hoplandria "rossii", seems an undescribed species. Both species
names cannot be found in the Zoological Record (http://www.organismnames.com/).
Laboulbenia bruchii (Speg.) Thaxt., Proc. Am. Acad. Arts Sci. 50: 23 (1914).
Fig. 3A
≡ Sphaleromyces bruchii Speg., An. Mus. Nac. Hist. Nat. Buenos Aires 23: 195 (1912).
Known distribution and hosts: Reported in many countries in the Americas on
species of the genera Lema Fabricius, 1798 and Neolema Monrós, 1951 (Coleoptera,
Chrysomelidae, Criocerinae). Currently it is known in Argentina, Brazil, Ecuador,
French Guiana, Guatemala, Mexico, and Trinidad (Spegazzini 1912, Thaxter 1914,
Proaño Castro & Rossi 2008). Recently, De Kesel et al. (2011) reported L. bruchii for
the first time on the African continent (in Togo).
New records from central america: PANAMA. On Neolema sp., La Reserva Forestal de Fortuna
(Chiriquí), 9.i.2016, close to dam, leg. J.Bernal, D.Haelewaters, T.Ríos & R.Villarreal, det. T.Ríos,
in coll. MUPADI, D.Haelew. 986a (UCH). Same data, D.Haelew. 987a–b (FH).
RemarKs: This species is recognized primarily by its cell IV forming a protrusion,
which grows besides and slightly beyond the insertion cell. In this characteristic
L. bruchii is allied to L. bilobata Haelew. & W.Rossi, L. macarthurii Balazuc [formerly
eschweizerbart_xxx
13
L. papuana Thaxt.], and L. rhinoceralis Thaxt. All four species have hosts in the
Criocerinae subfamily (Lema, Neolema). However, L. bilobata is obviously completely
different because of the monstruous growth of cell VI (Haelewaters & Rossi 2015). The
perithecium of L. rhinoceralis carries two short apical horn-like projections (Thaxter
1914), which are absent in L. bruchii. Thaxter (1914) wrote about L. macarthurii:
"This species is so closely related to L. bruchii that I have hesitated to separate it
specifically, and it may prove to be merely a well marked variety when a large series
becomes available for examination".
Also Laboulbenia hottentotae Thaxt. occurs on insects of the genus Lema (in Zanzibar).
However, the thallus is always typically anteriorly curved and its cell IV does not form
a protrusion (Thaxter 1914).
Laboulbenia coccinellidicola Haelew., sp. nov. Fig. 2A–C
MycoBank number MB 819382.
Diagnosis: Separated from other species of Laboulbenia by (1) the crenulation on the
anterior margin of the receptacle up to cell VII, (2) the punctation pattern of cells II
through VII, (3) its simple inner and outer appendages, (4) the presence of a single
antheridium, and (5) Coccinellidae as hosts.
types: PANAMA. On Exochomus childreni Mulsant, 1850 (Coleoptera, Coccinellidae, Chilocorinae),
collected in Reserva Forestal De Fortuna (Chiriquí), "Cont. Div. Trail", 1300 m a.s.l., 18.i.1992, leg.
H.P.Stockwell, det. T.Ríos, in coll. STRI (STOCKWELL STRI-ENT 0 059 457), D.Haelew. 885a
(HOLOTYPE, 1 mature thallus, margin elytral tips, FH); ISOTYPES D.Haelew. 885b (1 submature
thallus, right elytron, MIUP), 885c (1 submature and 1 mature thallus, left elytron, FH), and 885d (1
mature thallus, left elytron, FH). On Exochomus sp. 1, Parque Nacional Darién (Darién), N7°45.5'
W77°41', 460 m a.s.l., 3–9.vi.1996, leg. H.P.Stockwell, det. T.Ríos, in coll. STRI (STOCKWELL
STRI-ENT 0 059 297), PARATYPES D.Haelew. 878a (4 mature thalli, right elytron, FH) and
878b (1 submature and 8 mature thalli, left elytron, FH). On E. childreni, La Mesa (Coclé), N8°37'
W80°07', 850 m a.s.l., 3.ii.1997, leg. H.P.Stockwell, det. T.Ríos, in coll. STRI (STOCKWELL
STRI-ENT 0 059 299), PARATYPE D.Haelew. 879a (1 juvenile thallus, tip of elytra, FH). On
Exochomus sp. 1, El Valle (Coclé), 750 m a.s.l., 17.v.1973, leg. H.P.Stockwell, det. T.Ríos, in coll.
STRI (STOCKWELL STRI-ENT 0 059 343), PARATYPE D.Haelew. 880a (4 juvenile thalli,
right elytron, FH). On Exochomus sp. 1, Reserva Natural Punta Patiño (Darién), N8°16'W 78°18',
0–50 m a.s.l., 12.xii.2004, leg. D.M.Windsor, det. T.Ríos, in coll. STRI (STOCKWELL STRI-ENT
0 070 120), PARATYPE D.Haelew. 884a (4 juvenile thalli, right elytron, FH).
etymology: Referring to the host family Coccinellidae, since this is the first report of
the genus Laboulbenia on this beetle family.
description: thallus: 183 µm long from foot to perithecial tip, straight; cell I, cell V,
and the perithecial tip hyaline to light brown colored, the rest of the thallus irregularly
brown, with the posterior margin of cells III and IV and the anterior margin of the
perithecial venter very dark brown. Anterior margin of the foot and of cells I, II, VI,
and VII crenulated. Cells II through VII punctate. receptacle: Cell I rectangular, up to
2× longer than broad, 27 × 16 µm. Cell II longer than broad, with divergent margins,
septum II–VI strongly oblique. Cells III and IV of similar length, rectangular, 1.5 ×
longer than broad. Cell V: at the inner-upper corner of cell IV, septum IV–V oblique,
strongly curved. Insertion cell: very dark, thickest in the middle, marking a strong
constriction at the posterior margin. appendage: Outer appendage consisting of a
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14
simple branch, up to 294 µm, composed of cells gradually more elongate; basal cell
rectangular, strongly curved posteriorly, 19 × 8 µm. Inner appendage consisting of a
simple branch, up to 173 µm, similar to the outer appendage but shorter, bearing a single,
short antheridium at the anterior side of the suprabasal cell; basal cell squarrish, less
than half as long than basal cell of outer appendage. perithecium: Cell VI obliquely
positioned, slightly broader than long, 10–14 × 14–17 µm. Perithecium 91–120 ×
24–32 µm, elongate, nearly symmetrical except for the anteriorly curved apex, with
prominent and rounded posterior lips, both of which subtend a conspicuous papilla;
posterior pre-ostiolar spot very conspicuous, black, opaque.
RemarKs: The genus Laboulbenia is the largest genus of Laboulbeniales. Over 600
species have been described – Dictionary of the Fungi mentions 593 species (Kirk et
al. 2008), and 30 new species were described since 2010 alone (Villarreal et al. 2010,
Rossi 2011, Rossi & Kirk-Spriggs 2011, De Kesel & Haelewaters 2014, Haelewaters
& Yaakop 2014, Haelewaters & Rossi 2015, Rossi et al. 2015, 2016, Wang et al.
2016b). Laboulbenia has a very wide host range, however L. coccinellidicola is the
first species on Coccinellidae. Thus far, this family was only known to host species in
the genus Hesperomyces Thaxt.
Fig. 2. A–C. Laboulbenia coccinellidicola sp. nov. A. Mature thallus (D.Haelew. 878a), with indication
of receptacle cells I through V, the basal cell of the perithecium (VI), the perithecium itself (p), the
inner appendage (ia) with the single antheridium (arrowhead), and the outer appendage (oa). B. Detail
of punctation on cells II through VII (D.Haelew. 878b). C. Detail showing crenulation at anterior
margin of receptacle up to cell VII (D.Haelew. 878c). Scale bars = 50 µm.
eschweizerbart_xxx
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The combination of the ornamentation of the basal part of the thallus (crenulation
of anterior cell margins and receptacular punctation), the simple inner and outer
appendages, and the single antheridium make this a well-distinguished species.
Laboulbenia disenochi Thaxt., Proc. Am. Acad. Arts Sci. 38: 34 (1902). Fig. 3B
Known distribution and hosts: Described from several species of Blackburnia Sharp,
1878 (Coleoptera, Carabidae, Platyninae) in Hawaii (Thaxter 1902). Colla (1926) also
reported it from an unidentified carabid on the Canary Islands but this record is doubtful
(Arndt & Santamaría 2004). Thaxter (1902) lists as hosts: Blackburnia optata (Sharp,
1903) [as Brosconymus, misspelled as "Brosconegneus"] and B. agonoides (Sharp,
1903), B. fracta (Sharp, 1903), and B. sulcipennis [all as Disenochus].
new records from central america: PANAMA. On Platynus purpurellus Liebherr, 1992
(Coleoptera, Carabidae, Platyninae), Parque Internacional La Amistad (Chiriquí), Sendero Panamá
Verde, 14.i.2016, under bark of logs, leg. D.Haelewaters, det. T.Ríos, in coll. MUPADI, D.Haelew.
1004a–b (FH).
remarKs: Laboulbenia disenochi parasitizes Platynus purpurellus in Panama, which
is an extension to the known host range. Both host genera Blackburnia and Platynus
Bonelli, 1810 belong to the subtribe Platynina sensu stricto within the Platynini tribe
(Coleoptera, Carabidae, Platyninae).
The most obvious observable difference from the type series (illustrated in Thaxter
1908) is the well-distinguished tip of the perithecium. However, the placement of cell
V, the blackening of the perithecial tip (and the hyaline area around the ostiole), and
the darkened branches of the appendage are illustrative of L. disenochi.
Laboulbenia ecitonis G.Blum, Centbl. Bakt. ParasitKde, Abt. II 62: 301 (1924).
Fig. 3E
Known distribution and hosts: Reported from Brazil (type), Costa Rica, and Ecuador.
Hosts are diverse, including Eciton Latreille, 1804 ants (Hymenoptera, Formicidae),
Sternocoelopsis [misspelled as Stenocobelopsis in Blum (1924) and Thaxter (1931)]
auricomus Reichensperger, 1923 (Coleoptera, Histeridae), Ecitophya gracillima
Mann, 1925 (Coleoptera, Staphylinidae, Aleocharinae), and uropodid mites (Acari,
Mesostigmata, Uropodidae) (Blum 1924, Reichensperger 1935, Rossi 1991).
New records from central america: PANAMA. On Ecitophya sp. (Coleoptera, Staphylinidae,
Aleocharinae), Cana Biological Station (Darién), N7°45'18"W77°41'6", 500–550 m a.s.l., 3.vi.1996,
army ant column, leg. J.S.Ashe & R.Brooks, det. J.S.Ashe, in coll. STRI (SYNOPTIC STRI-ENT
0 108 232), D.Haelew. 903a–c (MIUP). Same data, in coll. STRI (SYNOPTIC STRI-ENT 0 108
233), D.Haelew. 904a–d (FH).
RemarKs: Laboulbenia ecitonis is a plurivorous species that occurs on phylogenetically
unrelated hosts. Other examples are Laboulbenia polyxena W.Rossi et al. (Rossi et al.
2016) and Rickia berlesiana (Bacc.) Paoli (Thaxter 1931). While most Laboulbeniales
are strictly host specific, the explanation for this phenomenon lies in the fact that
these unrelated hosts occupy the same ecological niche (e.g. ant nests), in which
opportunities exist for Laboulbeniales to become transmitted from one host to another
(De Kesel & Haelewaters 2014, Pfliegler et al. 2016, Rossi 2011). Such opportunities
eschweizerbart_xxx
16
can ultimately lead to speciation through reproductive isolation. Examples for this
are Laboulbenia littoralis De Kesel & Haelew. and L. slackensis Cépède & F.Picard,
which are morphologically closely related but have phylogenetically diverse hosts (De
Kesel & Haelewaters 2014).
Our material follows the description for L. ecitonis well. In all thalli observed, cells
II–VI of the receptacle are dark colored, as in the Ecuadorian thalli described by Rossi
(1991). Pigmentation, however, is not a good parameter for species delineation.
Laboulbenia fallax Thaxt., Proc. Am. Acad. Arts Sci. 35: 176 (1899).
Known distribution and hosts: Known on species of Gyretes Brullé, 1835 (Coleoptera,
Gyrinidae, Gyrininae) from the "Amazon River", Brazil, and Panama only (Thaxter 1899).
new records from central america: TRINIDAD. On Gyretes sp., Verdant Vale (Tunapuna-Piarco),
no date, no collector, Thaxter No. 2912, slide 10301 (FH). On Gyretes sp., Sangre Grande, no date,
no collector, Thaxter No. 2886, slide 10302 (FH).
RemarKs: Thaxter designated slide FH 2912 as the "type" but he never published it
formally. This might have been part of the intended sixth volume of his monograph.
The monstrous development of cell V, resulting in an elongated lobe along the posterior
margin of the perithecium is characteristic for a few species only: L. fallax, L. rotundata
Thaxt., and L. satanas Balazuc, all parasitizing members of Gyrinidae. Laboulbenia
satanas carries horn-like outgrowths at its perithecial apex (Balazuc 1973), while the
apex in L. fallax is undifferentiated. As for L. rotundata, this species is deeply darkened,
contrary to L. fallax, and possesses two minute, tooth-like projections at the perithecial
tip (Thaxter 1905, 1908).
Laboulbenia flabelliformis K.Sugiy. & T.Majewski, Trans. Mycol. Soc. Japan 28:
127 (1987).
Known distribution and hosts: Described on Alticini sp. (Coleoptera, Chrysomelidae,
Galerucinae) from Peru (Sugiyama & Majewski 1987) and since then unreported.
new records from central america: PANAMA. On Asphaera transversofasciata (Jacoby, 1880)
(Coleoptera, Chrysomelidae, Galerucinae), Bugaba (Chiriquí), no date, no collector, Thaxter No.
1773, in coll. MCZ, slides 10505 and 10506 (FH). TRINIDAD. On Asphaera nobilitata Fabricius,
1787 (Coleoptera, Chrysomelidae, Galerucinae), Port of Spain, 1913, no collector, Thaxter No. 2472,
slides 10501 through 10504 (FH).
remarKs: This species is recognized by the following characteristics: (1) cells III and
IV of the receptacle are undivided, (2) cell V is free from the perithecium, and (3)
the appendage bears very long branchlets. The record from Trinidad is a confirmation
of the personal communication by R.K.Benjamin in Sugiyama & Majewski (1987).
Although he never formally described this fungus, Thaxter had tentatively named it
"Laboulbenia asphaerae" on his slide mounts, after the host genus.
Laboulbenia fuliginosa Thaxt., Proc. Am. Acad. Arts Sci. 50: 28 (1914). Fig. 3D
Known distribution and hosts: Only known from the original description on Altica
sp. [as Haltica] (Coleoptera, Chrysomelidae, Galerucinae) from Cuba, Guatemala,
Haiti, and Jamaica (Thaxter 1914).
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new records from central america: PANAMA. On Altica bimarginata Say, 1824, Boquete,
Parque Internacional La Amistad (Chiriquí), Sendero Los Quetzales, 13.xii.2015, leg. K.Castillo,
det. T.Ríos, in coll. MUPADI, D.Haelew. 974a (FH). Same data, D.Haelew. 981a–c (UCH). Same
data, D.Haelew. 972c (FH) and 972f (UCH).
RemarKs: Laboulbenia fuliginosa was portrayed as a "very ordinary looking species" by
Thaxter (1914). We agree that there are very few outstanding morphological characters
to describe this species. Most diagnostic features are: (1) cells IV and V are equal in
length, (2) insertion cell marks a strong constriction on the posterior margin of the
thallus, and (3) the basal cell of the outer appendage separated from its outermost
branch by an oblique black septum. In the 25 thalli that we studied, the outermost
branch of the outer appendage was always broken above the darkened septum, which
apparently is typical for this species (Thaxter 1914).
Laboulbenia funeralis Thaxt., Proc. Am. Acad. Arts Sci. 48: 208 (1912).
Known distribution and hosts: Described on Gyrinus sp. (Coleoptera, Gyrinidae,
Gyrininae) from Argentina. It has been reported on species of the genus Gyrinus
Geoffroy, 1762 and its subgenus Neogyrinus Hatch, 1925 in Bolivia, Brazil, Ecuador,
Paraguay, and the U.S.A. (Balazuc 1971, Weir & Rossi 2001, Proaño Castro & Rossi
2008, Rossi & Bergonzo 2008).
new records from central america: COSTA RICA. On Gyrinus sp., Cartago, 1910, no collector,
Thaxter No. 2039, slide 10118 (FH).
RemarKs: This new finding fills the gap between the North American and South
American records.
Laboulbenia idiostoma Thaxt., Proc. Am. Acad. Arts Sci. 50: 28 (1914). Fig. 3C
Known distribution and hosts: Described on Macroaltica [as Haltica] jamaicensis
(Fabricius, 1792) (Coleoptera, Chrysomelidae, Galerucinae) from Haiti (Thaxter 1914)
and subsequently reported on Altica spp. in India, Indonesia (Bali), Japan, Malaysian
Borneo, Peninsular Malaysia, Sierra Leone, and Thailand (Balazuc 1988, Kauk &
Mukerji 1995).
new records from central america: PANAMA. On Altica bimarginata Say, 1824 (Coleoptera,
Chrysomelidae, Galerucinae), Boquete, Parque Internacional La Amistad (Chiriquí), Sendero Los
Quetzales, 13.xii.2015, leg. K.Castillo, det. T.Ríos, in coll. MUPADI, D.Haelew. 972b (FH).
remarKs: Diagnostic for L. idiostoma are (1) cell IV, which is large, bending the
insertion cell and appendages inwards, and (2) the perithecium with two distinctive
rounded apical lobes (Thaxter 1914). Also characteristic for this species is the position
on the host body; thalli are restricted to the antennae (Thaxter 1914, Kaur & Mukerji
1995). The thalli on slide D.Haelew. 972b were removed from the right antenna.
The host insect bearing L. idiostoma was also infected with L. fuliginosa on its pronotum
(D.Haelew. 972c) and left elytron (D.Haelew. 972f).
Laboulbenia perplexa Thaxt., Proc. Am. Acad. Arts Sci. 38: 49 (1902). Fig. 3F
Known distribution and hosts: Described on Galerita (Galerita) carbonaria Mannerheim,
1837 (Coleoptera, Carabidae, Harpalinae) from Brazil and not reported since.
eschweizerbart_xxx
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new records from central america: PANAMA. On Galerita sp., Potrerillos Arriba (Chiriquí),
23.ii.2011, leg. J.Castillo & B.Espinosa, det. T.Ríos, in coll. MUPADI, D.Haelew. 999a–b (FH).
Same data, D.Haelew. 1230a–b (FH).
RemarKs: This is the second report of this species after over a hundred years.
Laboulbenia perplexa has a series of morphological characters that clearly separate
it from other species. The color pattern is unambiguous: cell I of the receptacle, the
(short) basal cells of the perithecium, and the perithecial tip are hyaline, contrasting
to the rest of the thallus, which is colored orange-brown. Also other features make
this a peculiar species: cell II is short and pentagonal, with two oblique upper septa,
separating it from cells III and VI. Septa III–IV and IV–V are positioned very obliquely
and nearly parallel. The appendages are composed of three branches, one arising from
the outer basal cell, two from either side of the inner basal cell. The perithecium is
erect and has slightly spiraled wall cells.
Closely related species are L. fusiformis Thaxt., L. punctata Thaxt., and L. subpunctata
Thaxt., all of which occur on Galerita spp. in Central and South America. Laboulbenia
fusiformis has a punctate perithecium and is much larger than L. perplexa. Thaxter
(1908) reported a total length of 1.65 mm for L. fusiformis (compared to 500 µm for
L. perplexa). Other differences between these two species are the much more elongate
receptacle and the color pattern (Thaxter 1908: Plate LXIV, fig. 4). Among other
differences, L. punctata and L. subpunctata have a punctate perithecium, with dark,
rounded to irregular spots up to its entire length in the case of the former, or only in
the lower half in the case of the latter.
The Brazilian host specimen from which the type collection of L. perplexa was removed
(Thaxter No. 960), was also host for L. fusiformis and L. subpunctata. As positions on
the host body are given: for L. fusiformis prosternum, for L. perplexa prothorax and
elytra, and for L. subpunctata head and prothorax (dorsal and ventral) (Thaxter 1908).
We observed a double infection on our Panamanian host specimen: thalli of L. perplexa
were removed from the pronotum (D.Haelew. 999b) and the left mesofemur (D.Haelew.
999a), while L. punctata thalli were removed from the clypeus (D.Haelew. 999c).
Thaxter (1908) doubted about the separation of L. fusiformis and L. perplexa. The above-
mentioned differences between these two species may be part of the morphological
plasticity or could even be (partly) due to nutritional gain from growing on different
positions. Molecular data will be needed to solve this issue.
Laboulbenia punctata Thaxt., Proc. Am. Acad. Arts Sci. 35: 197 (1899). Fig. 3G
Known distribution and hosts: Described on Galerita sp. (Coleoptera, Carabidae,
Harpalinae) from Venezuela and "South America". It has been reported on Galerita
(Galerita) moritzi Mannerheim, 1837 in Colombia (Thaxter 1908) and on Galerita
sp. in Argentina (Thaxter 1912).
new records from central america: PANAMA. On Galerita sp., Potrerillos Arriba
(Chiriquí), 23.ii.2011, leg. J.Castillo & B.Espinosa, det. T.Ríos, in coll. MUPADI,
D.Haelew. 999c (FH).
RemarKs: The most distinctive character of this species is the punctation of the
perithecium. Also L. subpunctata also has a perithecium with dark spots, but only in the
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lower fifth of rarely the lower half. In L. punctata, the spots are present through halfway
of the perithecium or more. Another, more subtle, difference lies in the antheridia,
which are elongate and straight in L. punctata while short and bent in L. subpunctata.
Our material agrees with Thaxter’s (1908) description and drawing of L. punctata.
Thaxter (1899, 1908) mentions the head as position of L. punctata on the host body.
This corresponds to the position of thalli on our Panamanian host specimen (clypeus).
Laboulbenia skelleyi W.Rossi & Bergonzo, Aliso 26: 6 (2008).
Known distribution and hosts: Described on Pselaphacus rubricatus (Herbst, 1799)
(Coleoptera, Erotylidae, Tritominae) from Brazil (Rossi & Bergonzo 2008), and
found on other species in Pselaphacus Percheron, 1835 in Costa Rica and Ecuador
(Barragán et al. 2013).
new records from central america: PANAMA. On Pselaphacus sparsus Guerin, 1956 (Coleoptera,
Erotylidae, Tritominae), Davíd, campus of Universidad Autónoma de Chiriquí (Chiriquí),
N8°38'55.48" W82°28'14.10", 648 m a.s.l., 26.vii.2016, Botanical Garden, leg. R.Villarreal &
participants of workshop "Hongos Asociados a Insectos", det. T.Ríos, in coll. MUPADI, D.Haelew.
1116a–b (UCH). Same data, D.Haelew. 1116a–b (FH). On Ischyrus sp. (Coleoptera, Erotylidae,
Tritominae), Humedales las Lagunas de Volcan (Chiriqui), 27.vii.2016, leg. R.Villarreal & participants
of workshop "Hongos Asociados a Insectos", det. T.Ríos, in coll. MUPADI, D.Haelew. 1118a (UCH).
remarKs: Seven species of Laboulbenia are reported from Erotylidae: L. encaustis
K.Sugiy. & T.Majewski, L. erotylidarum Haelew., L. mycotreti W.Rossi, L. nesitidis
Balazuc (Balazuc 1975), L. parvula Thaxt. (but see discussion in Haelewaters &
Yaakop 2014), L. scaphidomorphi Speg., and L. skelleyi (Colla 1926, Haelewaters &
Yaakop 2014, Rossi 2011, Rossi & Bergonzo 2008, Spegazzini 1915, Sugiyama &
Majewski 1987). Our material unmistakenly belongs to L. skelleyi. The single outer
appendage and forked inner appendage (above its suprabasal cells) in combination
with the blackened perithecial tip and hyaline apex separate this species from the other
ones on erotylid hosts.
In the thalli from Panama, receptacle cells I and II are distinctly crenulated at the anterior
margin. Even the youngest thalli among our studied material showed this crenulation.
This feature is also observable in the Brazilian material (Rossi & Bergonzo: fig. 21)
The host genus from Humedales las Lagunas de Volcan, Ischyrus Lacordaire, 1842,
belongs in the same subfamily as the only other known host genus for this parasite
(Pselaphacus). Ischyrus represents a new host genus for Laboulbeniales.
Laboulbenia systenae Speg., An. Mus. Nac. Hist. Nat. Buenos Aires 29: 568 (1917).
Known distribution and hosts: Described on Systena testaceovittata (Clark, 1865)
(Coleoptera, Chrysomelidae, Galerucinae) from Argentina (Spegazzini 1917), and since
then only reported on S. s-littera (Linnaeus, 1758) from Bolivia and Brazil (Weir &
Rossi 2001, Rossi & Bergonzo 2008).
new records from central america: HAITI. On Systena basalis J.DuVal, 1856 (Coleoptera,
Chrysomelidae, Galerucinae), 1913, leg. W.M.Mann, Thaxter No. 2489, slide 10671 (FH). Same
data, Thaxter No. 2490, slide 10672 (FH). PANAMA. On Systena sp., Potrerillos Abajo (Chiriquí),
N8°38'55.48"W82°28'14.10", 648 m a.s.l., 6.i.2016, abandoned orange plantation, leg. J.Bernal,
eschweizerbart_xxx
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Fig. 3. Different species of Laboulbenia. A. L. bruchii (D.Haelew. 987a), with indication of cell IV
forming a protrusion, cell V, and the basal cell of the perithecium (VI). B. L. disenochi (D.Haelew.
1004b). C. L. idiostoma (D.Haelew. 972b). D. L. fuliginosa (D.Haelew. 972c). E. L. ecitonis
(D.Haelew. 904b). F. L. perplexa (D.Haelew. 1230b), with indication of cells III, IV, and V, the
inner appendage (ia), and the outer appendage (oa). G. L. punctata (D.Haelew. 999c) with typically
punctated perithecium. Scale bars: A, C, D = 50 µm; B, E–G = 100 µm.
D.Haelewaters & R.Villarreal, det. T.Ríos, in coll. MUPADI, D.Haelew. 997a–b (FH) and 997c
(UCH). On Galerucinae sp. (Coleoptera, Chrysomelidae), Isla Barro Colorado (Panamá Oeste),
N9°9'53.01"W79°50'11.25", 1.vii.2015, high grasses, leg. D.Haelewaters & S.J.C.Verhaeghen, det.
D.Haelewaters, in coll. MCZ, TRINIDAD. On Systena s-littera, Port of Spain, 1913, no collector,
Thaxter No. 2469C, slide 10661 (FH).
RemarKs: Laboulbenia systenae is closely related to L. homophoetae (Speg.) Thaxt.
and L. sima W.Rossi et al., both of which occur on Chrysomelidae. Specifically,
L. homophoetae is reported from different genera in the Alticini and Galerucini
tribes (Galerucinae), but L. sima was only recently described on Phyllotrupes sp.
(Galerucinae, Alticini) (Haelewaters & Rossi 2015, Rossi et al. 2016).
The three species share the following characters: (1) cells III and IV are undivided
and (2) the general structure of the appendages. Laboulbenia sima is easily separated
based on the perithecial apex with large, spreading lips (Rossi et al. 2016). Laboulbenia
systenae differs from L. homophoetae in its less slender habitus and spindle-shaped
perithecium with spiraled wall cells. Thaxter (1914) stressed the morphological
plasticity of L. homophoetae. It is possible that L. homophoetae and L. systenae are
conspecific, as previously suggested by Weir & Rossi (2001) and Rossi & Bergonzo
(2008).
Laboulbenia trogacti W.Rossi, Mycologia, 103: 193 (2011).
Known distribution and hosts: Laboulbenia trogacti is only known from the type
collection in Ecuador, on Trogactus spp. (Coleoptera, Staphylinidae, Oxytelinae).
new records from central america: PANAMA. On Carpelimus sp. (Coleoptera, Staphylinidae,
Oxytelinae), Río Caldera (Chiriquí), N8°38'55.0"W 82°23'52.1", 360 ± 13 m a.s.l., 30.xii.2011, leg.
and det. Y.Aguirre, in coll. MUPADI, D.Haelew. 982a (FH). Same data, D.Haelew. 988a (UCH).
RemarKs: Many specimens of Carpelimus sp. were collected at the banks of Río Caldera
(Aguirre & Bernal 2014); out of 102 individuals, only two bore Laboulbeniales thalli.
Although slide D.Haelew. 988a consisted of a single juvenile thallus only, we were
able to easily identify it based on the following characters (Rossi 2011): (1) cells I
and II are typically long and slender; (2) cells IV and V are separated by a vertical
septum, and cell V is slightly darker; and (3) the basal portion of the outer appendage
consists of two superimposed cells separated by a oblique septum. Especially the
latter feature is unique in the genus Laboulbenia and thus diagnostic for L. trogacti.
The thalli on slide D.Haelew. 982a are different in general habitus. They remind
closely of L. trogacti, however with the perithecium being strictly ovoid, abruptly
narrowing to the distinctive, asymmetrical tip, ending in two rounded lips, the
posterior of which is more prominent and carries a small tooth. Conforming to the
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description by Rossi (2011), the posterior lip is subtended by a small blackish area,
but in the Panamanian material there is also a darker region at the anterior side,
although smaller and less profound.
Neohaplomyces medonalis R.K.Benj., El Aliso 3: 190 (1955). Fig. 1H
Known distribution and hosts: Described on Medon sp. (Coleoptera, Staphylinidae,
Paederinae) from California (holotype) and Arizona, U.S.A. (Benjamin 1955) and
since then found on Medon spp. in Greece, Spain, and Turkey and on Thinocharis sp.
(Coleoptera, Staphylinidae, Paederinae) in Madagascar (Santamaría & Girbal 1987,
Santamaría & Rossi 1999).
new records from central america: PANAMA. On Medonina gen. & sp. indet. (Coleoptera,
Staphylinidae, Paederinae), 20 km N of Gualaca (Chiriquí), N8°39'0"W82°12'0", 1200 m a.s.l.,
10.vi.1995, leg. R.Anderson, det. A.Newton & M.Thayer, in coll. STRI (SYNOPTIC STRI-ENT
0 108 079), D.Haelew. 897a–b (FH). On Paederinae gen. & sp. indet. (Coleoptera, Staphylinidae),
Cana Biological Station (Darién), N7°45'18"W 77°41'6", 530 m a.s.l., 9.xi.1996, leg. J.S.Ashe &
R.Brooks, det. J.S.Ashe, in coll. STRI (SYNOPTIC STRI-ENT 0 108 056), D.Haelew. 895a (FH).
RemarKs: Based on the available material (1 mature and several immature thalli), we
believe the fungus belongs to N. medonalis. The only noticable differences with the
description in Benjamin (1955) are the perithecium (not inflated below the middle)
and the number of rows of antheridial cells (3). Neohaplomyces cubensis R.K.Benj. is
distinctly smaller in total length, its cell I is narrower than cell II, and its perithecium is
posteriorly colored brown immediately below the apex. Neohaplomyces neomedonalis
R.K.Benj. is different from the other two species in the genus in its cell I, which forms
a typical protuberance at the upper posterior corner, and the antheridium with its nearly
vertical rows of antheridial cells.
Nycteromyces streblidinus Thaxt., Proc. Am. Acad. Arts Sci. 52: 654 (1917).
Known distribution and hosts: Described on Strebla wiedemanni Kolenati, 1856 [as
S. vespertilionis] (Diptera, Streblidae, Streblinae) from Venezuela (Thaxter 1917).
New records from central america: PANAMA. On male Trichobius joblingi Wenzel, 1966
(Diptera, Streblidae, Trichobinae), Bohio (Panama Canal Zone), 2015, parasitic on female Carollia
perspicillata (Mammalia, Chiroptera, Phyllostomidae), P_3949, leg. and det. T.Hiller, in coll. MCZ,
D.Haelew. 1066a (FH). On male T. joblingi, Bohio (Panama Canal Zone), 2015, parasitic on female
Carollia perspicillata, P_3935, leg. and det. T.Hiller, in coll. MCZ, D.Haelew. 1071b (FH). On male
T. joblongi, Gamboa (Colón), 13.vi.2016, parasitic on male Carollia castanea (Mammalia, Chiroptera,
Phyllostomidae), leg. R.Page et al., det. T.Hiller, D.Haelew. 1088a (FH).
RemarKs: The genus Nycteromyces Thaxt. is monotypic, with a single species N. stre-
blidinus that was described in 1917 and has not been reported since that time. The
material from Panama extends the known host range of Nycteromyces to the streblid
subfamily Trichobinae.
Nycteromyces bears a superficial resemblance to Polyandromyces Thaxt. Both genera
are dioecious, with separate male and female thalli, and monotypic. However, both the
male and female thalli of Nycteromyces are clearly distinguished from Polyandromyces
coptosomatis Thaxt. The male thallus carries multiple antheridia in a unilateral row
and ends with a dome-shaped cell, which holds a pointed tooth. The female thallus is
eschweizerbart_xxx
23
a reduced form compared to Polyandromyces, with the receptacle consisting of two
cells only, the second of which carries both the perithecium and appendage.
Two specimens of T. joblongi carried a double infection with Gloeandromyces streblae
(Table 1). For slide D.Haelew. 1071b, thalli of N. streblidinus were removed from the
head and left metafemur, while those of G. streblae were taken from the wings. For
slide D.Haelew. 1088a, thalli of both species were removed from the left profemur.
We found both species co-occurring on T. joblingi collected from Carollia bats in
multiple occasions (Haelewaters et al. unpublished records). It could be that the
roosting habits of these bats facilitate spore transmission of Laboulbeniales (sensu
Patterson et al. 2007).
Peyritschiella protea Thaxt., Proc. Am. Acad. Arts Sci. 35: 427 (1900).
Known distribution and hosts: Peyritschiella protea is widespread in Europe but less
common on other continents, with reports in Algeria (Maire 1920), Tibet (Lee et al.
2006), and the U.S.A. (Thaxter 1908, Haelewaters et a. 2015b). Hosts are Anotylus
Thomson, 1859; Bledius Samouelle, 1819; Manda Blackwelder, 1952; Oxytelus
Gravenhorst, 1802; Planeustomus Jacquelin du Val, 1857; Styloxys Gozis, 1886
(Coleoptera, Staphylinidae, Oxytelinae); and Philonthus Stephens, 1829 (Coleoptera,
Staphylinidae, Staphylininae).
new records from central america: PANAMA. On Platydracus prasinvariegatus (Bernhauer,
1921) (Coleoptera, Staphylinidae, Staphyliniae), Isla Barro Colorado (Panamá Oeste), Atta colombica
external debris pile, 12.x.1998, leg. K.Buchard, WR 2460 (FI).
RemarKs: The genus Platydracus Thomson 1858 has been mentioned as host for
Rhachomyces philonthinus Thaxt. (Balazuc 1982), but not for P. protea. This represents
the first report of this fungus in Central America.
Rhachomyces longissimus (Thaxt.) Thaxt., Mem. Am. Acad. Arts Sci. 12: 361 (1896).
≡ Acanthomyces longissimus Thaxt., Proc. Am. Acad. Arts Sci. 28: 176 (1893).
= Rhachomyces mattiroloi Colla, Mem. Reale Accad. Naz. Lincei, Cl. Sci. Fis. 6: 188 (1926).
Known distribution and hosts: Described on Dyscolus [as Colpodes] evanescens
(Bates, 1882) (Coleoptera, Carabidae, Platyninae) from Guatemala (Thaxter 1896).
Since then found in Colombia on Dyscolus [as Colpodes] reflexus (Chaudoir, 1859)
(Thaxter 1908); in Costa Rica [as R. mattiroloi] on an unidentified carabid from Costa
Rica (Colla 1926); in Cuba on Platynus medius (Darlington, 1937) (Balazuc 1977); in
Ecuador on Dyscolus (Hydrodyscolus) asphaltinus (Chaudoir, 1878), D. purpuratus
Reiche, 1842, and D. subviolaceus (Chaudoir, 1842); in Jamaica on Platynus cinchonae
(Darlington, 1934) (Proaño Castro & Rossi 2008); and in Mexico on Mexisphodrus
profundus Barr, 1966 (Vigna Taglianti & Rossi, 1998).
new records from central america: PANAMA. On Platynus lyratus (Chaudoir, 1879), Boquete,
Parque Internacional La Amistad (Chiriquí), Sendero Los Quetzales, 13.xii.2015, leg. K.Castillo,
det. T.Ríos, in coll. MUPADI, D.Haelew. 975b (FH) and 975c (UCH).
RemarKs: A number of different host genera have been reported for R. longissimus:
Dyscolus Dejean, 1831, Platynus Bonelli, 1810, and Mexisphodrus Barr, 1965.
However, all three belong to the same subtribe Platynina sensu stricto within the
eschweizerbart_xxx
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Platynini tribe (Coleoptera, Carabidae, Platyninae), suggesting a high degree of host
specificity of this fungus.
The Panamanian host specimen carried a double infection with Laboulbenia sp.
(slide D.Haelew. 975a). A single juvenile thallus of Laboulbenia sp. was found on
the prosternum, while the thalli of R. longissimus were removed from sternites and
the left metafemur and -tibia. Also in the Ecuadorian material double infections were
found with L. flagellata Peyr. (Proaño Castro & Rossi 2008).
Rhachomyces longissimus is the second-largest species of the Laboulbeniales
(Santamaría et al. 2016). In the original description, Thaxter (1893) mentions that the
receptacle slightly exceeds 1 mm in length. Later, he refers to it as the largest species
of the genus with a length up to 2 mm (Thaxter 1908). Colla (1926) even reports a
thallus of 3.5 mm [as R. mattiroloi]. The largest species of the order is Laboulbenia
kunkelii (Giard) Thaxt., which measures between 2 and 4 mm in total length (Giard
1892, Sugiyama and Phanichapol 1984).
Stichomyces conosomatis Thaxt., Proc. Am. Acad. Arts Sci. 37: 38 (1901).
= Stichomyces europaeus T.Majewski, Acta Mycol. 9: 121 (1973).
Known distribution and hosts: Stichomyces conosomatis is a widespread species that
is largely restricted to beetles in the genus Sepedophilus Gistel, 1856 (Coleoptera,
Staphylinidae, Tachyporinae), with reports from various European countries (Belgium,
Great Britain, Greece, Italy, The Netherlands, Poland, and Spain), Africa (Algeria),
America (Ecuador, the U.S.A.), and Asia (Japan) (Bernardi et al. 2014, Castaldo et
al. 2004, Haelewaters et al. 2012, 2015b, Majewski 2008). The parasite is also known
from Portugal on Speonemadus algarvensis Reboleira et al. (Coleoptera, Leiodidae,
Cholevinae) (Reboleira et al. 2017).
New records from central america: PANAMA. On Sepedophilus sp., Tierras Altas District, 27.
7 km W of Volcán (Chiriquí), N8°51'48"W82°44'36", 17.vi.1996, Finca Hartmann, leg. J.S.Ashe &
R.Brooks, det. J.S.Ashe, in coll. STRI (SYNOPTIC STRI-ENT 0 108 276), D.Haelew. 908a (FH).
remarKs: Until the discovery of the fungus on the cholevine beetle Speonemadus
algarvensis, this fungus had only been reported on Sepedophilus spp. The Portugese
record, however, came from a cave, which may account for the unusual host. Just like
in ant nests and salt marshes, phylogenetically unrelated hosts can come into close
contact in subterrenean caves and provide opportunities for Laboulbeniales parasites
to transmit from one to the other host (= host shift, De Kesel &Haelewaters 2014).
Discussion
In this contribution, we provide details for 27 species, all of which represent new records
for Panama. We reveal the presence of the following genera in Panama for the first time:
Amorphomyces Thaxt., Chitonomyces, Gloeandromyces, Neohaplomyces R.K.Benj.,
Nycteromyces, and Stichomyces Thaxt. With these new records, the total number of the
Laboulbeniales in Panama rises to 78, of which 40 are species of Laboulbenia (Table
2). This updated number of Laboulbeniales reported from Panama is still rather low.
eschweizerbart_xxx
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Table 2. Parasite-host list of Panamanian Laboulbeniales.
Species Host species Province Reference
1Amorphomyces ophioglossae Thaxt. Ophioglossa sp. Chiriquí This paper
2Chitonomyces hyalinus Thaxt. Laccophilus pictus Veraguas This paper
3Chitonomyces simplex Thaxt. Laccophilus pictus Veraguas This paper
Laccophilus fasciatus Coclé This paper
4Dimeromyces aulacophorae Thaxt. "Plataxantha sp." Thaxter 1908
5Dimeromyces homophoetae Thaxt. Capraita sp. Chiriquí This paper
6Eucantharomyces calleidae Thaxt. Calleida aurata [as
C. "anypterygioides"] Panamá This paper
7Eucantharomyces euprocti Thaxt. Euproctus quadrini Chiriquí Thaxter 1900
8Gloeandromyces pageanus Haelew. Trichobius dugesioides Colón This paper
9Gloeandromyces streblae (Thaxt.)
Thaxt. Trichobius dugesioides Panama Canal
Zone This paper
Trichobius joblongi Panama Canal
Zone This paper
Trichobius yunkeri Panamá Oeste This paper
10 Herpomyces chaetophilus Thaxt. Periplaneta americana Chiriquí This paper
Periplaneta americana Colón This paper
11 Herpomyces periplanetae Thaxt. Periplaneta sp. Panamá Thaxter 1902
Periplaneta americana Panamá Haelewaters
unpublished
Periplaneta
australasiae Panamá Haelewaters
unpublished
12 Herpomyces tricuspidatus Thaxt. "Large winged roach" Thaxter 1902
13 Hesperomyces coccinelloides
(Thaxt.) Thaxt. Scymnus tardus Panamá Oeste Thaxter 1931
14 Hesperomyces virescens Thaxt. Azya orbigera Chiriquí This paper
Epilachna mexicana Chiriquí This paper
Brachiacanthini gen. &
sp. indet. Panamá This paper
Cycloneda sanguinea Chiriquí This paper
15 Histeridomyces acriti Thaxt. Acritus near
simpliculus Panamá Oeste Thaxter 1931
16 Ilytheomyces elegans Thaxt. Ilythea sp. Bocas del Toro Thaxter 1917,
1931
17 Ilytheomyces lingulatus Thaxt. Ilythea sp. Bocas del Toro Thaxter 1917,
1931
18 Ilytheomyces major Thaxt. Ilythea sp. Bocas del Toro Thaxter 1917,
1931
19 Ilytheomyces manubriolatus Thaxt. Ilythea sp. Bocas del Toro Thaxter 1917,
1931
20 Ilytheomyces panamensis Thaxt. Ilythea sp. Bocas del Toro Thaxter 1917,
1931
21 Kleidiomyces furcillatus (Thaxt.)
Thaxt. Aleochara repetita Panamá Thaxter 1901
[as Monoico-
myces furcilla-
tus], 1908, 1931
22 Kleidiomyces hoplandriae Thaxt. Hoplandria sp. Colón This paper
23 Laboulbenia anchonoderi Thaxt. Anchonoderus
subaeneus Chiriquí Thaxter 1899,
1908
24 Laboulbenia bruchii (Speg.) Thaxt. Neolema sp. Chiriquí This paper
25 Laboulbenia catascopi Thaxt. Catascopus fascialis Thaxter 1908
Callida quadrispora Chiriquí Thaxter 1908
eschweizerbart_xxx
26
26 Laboulbenia cephaloleiarum Balazuc
& Demaux Cephaloleia sp. Balazuc 1988
27 Laboulbenia chiriquensis Thaxt. Callida scintillans Chiriquí Thaxter 1899,
1908
28 Laboulbenia coccinellidicola
Haelew. Exochomus childreni Chiriquí This paper
Coclé This paper
Exochomus sp. 1 Coclé This paper
Darién This paper
29 Laboulbenia colpodis Thaxt. Colpodes chiriquinus Chiriquí Thaxter 1899,
1908
30 Laboulbenia coptoderae Thaxt. Coptodera championi Thaxter 1893,
1896
31 Laboulbenia crispata Thaxt. Hippelates sp. Bocas del Toro Thaxter 1917
32 Laboulbenia cristata Thaxt. Paedereus luridiventris Chiriquí Thaxter 1908
33 Laboulbenia decipiens Thaxt. Galerita sp. Chiriquí Villarreal et al.
2010
34 Laboulbenia disenochi Thaxt. Platynus purpurellus Chiriquí This paper
35 Laboulbenia drakei R.K.Benj. Rhagovelia sp. Panama Canal
Zone Benjamin 1967
36 Laboulbenia drepanalis Thaxt. Gyretes acutangulus Chiriquí Thaxter 1899,
1908
37 Laboulbenia ecitonis Blum Ecitophya sp. Darién This paper
Ecitophya sp. Darién This paper
38 Laboulbenia fallax Thaxt. Gyretes acutangulus Chiriquí Thaxter 1899,
1908
39 Laboulbenia flabelliformis K.Sugiy.
& T.Majewski Asphaera
transversofasciata Chiriquí This paper
40 Laboulbenia flagellata Peyr. Coptodera championi Chiriquí Thaxter 1908
Platynus spp. Chiriquí Villarreal et al.
2010
41 Laboulbenia fuliginosa Thaxt. Altica bimarginata Chiriquí This paper
42 Laboulbenia guerinii C.P.Robin Gyretes acutangulus Chiriquí Thaxter 1908
43 Laboulbenia idiostoma Thaxt. Altica bimarginata Chiriquí This paper
44 Laboulbenia metrionae Balazuc Agroiconota judaica Balazuc 1978
45 Laboulbenia mexicana Thaxt. Galerita americana Chiriquí Thaxter 1908
46 Laboulbenia minima Thaxt. Calleida aurata [as C.
onypterigioides]Chiriquí Thaxter 1908
Calleida pallidipennis Thaxter 1893,
1896, 1902
47 Laboulbenia pachytelis Thaxt. Pachyteles
seriatoporus Chiriquí Thaxter 1908
48 Laboulbenia perplexa Thaxt. Galerita sp. Chiriquí This paper
49 Laboulbenia philonthi Thaxt. Philonthus sp. Haelewaters et
al. 2015b
50 Laboulbenia polyphaga Thaxt. Bradycellus
circumdatus Chiriquí Thaxter 1908
51 Laboulbenia pseudomasei Thaxt. [as
pseudomasci]Platynus spp. Chiriquí Villarreal et al.
2010
52 Laboulbenia punctata Thaxt. Galerita sp. Chiriquí This paper
53 Laboulbenia rhagoveliae R.K.Benj. Rhagovelia uncinata Panama Canal
Zone Benjamin 1967
54 Laboulbenia rigida Thaxt. Platynus sp. Chiriquí Villarreal et al.
2010
55 Laboulbenia scaphidomorphi Speg. Scaphidomorphus
bosci Spegazzini
1915
eschweizerbart_xxx
27
56 Laboulbenia skelleyi W.Rossi &
Bergonzo Ischyrus sp. Chiriquí This paper
Pselaphacus sparsus Chiriquí This paper
57 Laboulbenia subpunctata Thaxt. Galerita sp. Chiriquí Villarreal et al.
2010
Galeritini gen. & sp.
indet. Panamá Oeste Haelewaters
unpublished
58 Laboulbenia systenae Speg. Systena sp. Chiriquí This paper
59 Laboulbenia tenera T.Majewski Paratrechus sp. Chiriquí Villarreal et al.
2010
Platynus sp. Chiriquí Villarreal et al.
2010
60 Laboulbenia tortilis J.A.Bernal &
R.Kirschner Platynus sp. Chiriquí Villarreal et al.
2010
61 Laboulbenia trogacti W.Rossi Carpelimus sp. Chiriquí This paper
Carpelimus sp. Chiriquí This paper
62 Laboulbenia usingeri R.K.Benj. Rhagovelia uncinata Panama Canal
Zone Benjamin 1967
63 Mimeomyces atropurpureus (Thaxt.)
Thaxt. Quedius graciliventris Chiriquí Thaxter 1900,
1908 [as
Sphaleromyces
atropurpureus]
Quedius basiventris Chiriquí Thaxter 1900,
1908 [as
Sphaleromyces
atropurpureus]
64 Mimeomyces chiriquensis (Thaxt.)
Thaxt. Quedius flavicaudus Chiriquí Thaxter 1901,
1908 [as
Sphaleromyces
chiriquensis]
65 Neohaplomyces neomedonalis
R.K.Benj. Paederinae gen. & sp.
indet. Darién This paper
Medonina gen. & sp.
indet. Chiriquí This paper
66 Nycteromyces streblidinus Thaxt. Trichobius joblongi Panama Canal
Zone This paper
67 Peyritschiella lampropygi Thaxt. Lampropygus analis Chiriquí Thaxter 1931
68 Peyritschiella protea Thaxt. Platydracus
prasinvariegatus Panamá Oeste This paper
69 Peyritschiella vulgata (Thaxt.)
I.I.Tav. Philonthus
flavolimbatus Thaxter 1900,
1908 [as
Dichomyces
vulgatus]
70 Rhachomyces longissimus (Thaxt.)
Thaxt. Platynus lyratus Chiriquí This paper
71 Rickia nutans Thaxt. "Large passaloid
beetle" Thaxter 1926
72 Stemmatomyces panamensis Thaxt. Aeolus sp. Panamá Oeste Thaxter 1931
73 Stichomyces conosomatis Thaxt. Sepedophilus sp. Chiriquí This paper
74 Stigmatomyces caribbeus Thaxt. Discocerina sp. Bocas del Toro Thaxter 1917
75 Stigmatomyces constrictus Thaxt. Oscinis sp. Bocas del Toro Thaxter 1917,
1931
Siphonella sp. Bocas del Toro Thaxter 1917,
1931
76 Stigmatomyces drapetis Thaxt. Drapetis rectinerva Bocas del Toro Thaxter 1917,
1931
77 Stigmatomyces ochtheroideae Thaxt. Ochtheroidea sp. Bocas del Toro Thaxter 1931
78 Stigmatomyces recurvatus Thaxt. Paralimna ciliata Bocas del Toro Thaxter 1931
eschweizerbart_xxx
28
In comparison, both in Brazil and Ecuador more than 100 species of Laboulbeniales
have been reported (Rossi & Bergonzo 2008, Rossi et al. 2016). However, as mentioned
before in exploratory papers in both tropical and temperate regions, presently low
numbers of records represent the interest of investigators, rather than the true diversity.
Examples are Bolivia (< 50 species, Weir & Rossi 2001), French Guyana (25 species,
Rossi & Ponziani 2008), The Netherlands (40 species, Haelewaters et al. 2012), and
many countries on the African continent.
We report the presence of Laboulbenia perplexa in Panama, a morphologically very
striking species (Fig. 3F). While it does not occur on a rare host genus (Galerita
Fabricius, 1801), the Panamanian record is only the second – after Thaxter’s (1902)
type from Brazil. In this contribution, we also present other records of species that have
not been observed by laboulbeniologists for a hundred years or more: Dimeromyces
homophoetae (last reported in 1917), Eucantharomyces calleidae (1908), Herpomyces
paranensis (1908), Laboulbenia fallax (1899), L. fuliginosa (1914), and L. punctata
(1912).
A special case are the Laboulbeniales described on bat flies (Diptera, Hippoboscoidea,
Nycteribiidae and Streblidae). These flies are specialized ectoparasites of bats that live
on the fur and on wing membranes where they suck blood from their host. Bat flies
are hosts to three genera of Laboulbeniales: Arthrorhynchus Kolenati (limited to the
Eastern Hemisphere, on Nycteribiidae) and the neotropical genera Gloeandromyces
and Nycteromyces (on Streblidae). Until the records presented in this paper, only
the type collection was known of the species in Gloeandromyces and Nycteromyces.
However, many more records from different countries and descriptions of new species
are awaiting publication (Haelewaters, unpublished). These data provide a new exciting
direction for Laboulbeniales research, with the formulation and testing of hypotheses
about parasitism, host specificity, speciation, and population dynamics.
Acknowledgements
This paper was only possible through collaboration with many researchers, collaborators, curators,
and friends. For curatorial support: Annette Aiello (Smithsonian Tropical Research Institute, Panama),
Lee H.Herman (American Museum of Natural History), Tina A.Hofmann (Herbario UCH), Philip
D.Perkins (Harvard Museum of Comparative Zoology), Ruth Salass (American Museum of Natural
History), and Genevieve Tocci (Farlow Herbarium, Harvard University). For blattodean informations:
Heidi Hopkins (Ithaca College). For advice and sharing material: Thomas Hiller (University of Ulm,
Germany) and Walter Rossi (University of L’Aquila, Italy). For facilitating fieldwork in Gamboa,
Panama: Rachel A.Page (Smithsonian Tropical Research Institute, Gamboa, Panama). For assistance
with field applying for collecting and export permits: Orlando Cáceres (Centro de Investigaciones
Micológicas, CIMi). For assistance with fieldwork in Chiriquí, Panama between 2012 and 2016:
Yussef Aguirre, Jennifer Castillo, Kayla Castillo Sánchez, Betty Espinosa, María Fuentes, Leila
González, Joel Trejos (Universidad Autónoma de Chiriquí, Panama), Christopher H.Chen (Harvard
College), and Lany Valdés Rodríguez (Universidad de Panamá). We acknowledge the following
funding sources: Travel Grants from the David Rockefeller Center for Latin American Studies (to
DH); Theodore Roosevelt Memorial Grant from the American Museum of Natural History (to DH);
Sistema Nacional de Investigacion (SNI, to JB), an initiative of SENACYT, Panama‘s Secretaria
Nacional de Ciencia, Tecnología e Innovacion; SENACYT provided funding for the international
workshop "Hongos Asociados a Insectos: Un Aporte al Conocimiento de la Biodiversidad" in July
2016 (No. APY-GC-2015-57) (to RV) and supports TR in his "Programa Centroamericano de Maestría
eschweizerbart_xxx
29
en Entomología" at the University of Panama. Finally, we thank Walter Rossi (University of L’Aquila,
Italy) and Sergi Santamaría (Universitat Autònoma de Barcelona, Spain) for reviewing the paper.
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Manuscript submitted December 5, 2016; accepted January 31, 2017.
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