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Acta Mycologica
ORIGINAL RESEARCH PAPER
A new report on Hesperomyces
coleomegillae (Ascomycota, Laboulbeniales)
parasitism of Coleomegilla maculata
(Coleoptera, Coccinellidae) in Brazil
Carlos Antonio Inácio1*, Hagabo Honorato de Paulo2, Jonas
Dias Almeida2, Jessica Rembinski2, Elen Lima Aguiar Menezes2,
Alessandra Carvalho Silva3
1 Department of Entomology and Plant Pathology, Universidade Federal Rural do Rio de Janeiro,
BR 465, Km 7, University Campus, Rural Zone, Seropédica, RJ, CEP 23851-970, Brazil
2 Department of Entomology and Plant Pathology, Rural University of Rio de Janeiro, UFRRJ, BR
465, Km 7, University Campus, Rural Zone, Seropédica, RJ, CEP 23851-970, Brazil
3 Embrapa Agrobiology, BR 465, Km 7, Ecology Site, Rural Zone, Seropédica, RJ, CEP 23981-355,
Brazil
* Corresponding author. Email: inacio@ufrrj.br
Abstract
For the rst time, the genus Hesperomyces has been reported to infect Coleomegilla
maculata in laboratory mass rearing in Brazil. alli were found growing on several
parts of this ladybird species, including the head, elytra, legs, and abdomen. Infested
adults died aer 60 days.
Keywords
host–parasitic interaction; Laboulbeniomycetes; ectoparasitic fungi; 12-spotted
ladybird; biotrophic parasites; tropical fungi
Introduction
e order Laboulbeniales (Fungi: Ascomycota) comprises about 2,200 species in 141
genera [1] and was previously included in Basidiomycota and/or Zygomycota. Recent
studies based on molecular data conrmed that Laboulbeniales are members of As-
comycota [2]. ey are biotrophic ectoparasites of arthropods, and beetles (Insecta:
Coleoptera) and ies (Insecta: Diptera) are their most common hosts [3–5]. ese fungi
are specialized and develop by forming a multicellular thallus in the tegument of living
arthropods [6–8]. Seven species of Laboulbeniales parasitize ladybirds (Coleoptera,
Coccinellidae) [6]: six species of the genus Hesperomyces (H. chilomenes axt., H.
coccinelloides axt., H. coleomegillae W. Rossi & A. Weir, H. papuanus T. Majewski &
K. Sugiy., H. palustris W. Rossi & A. Weir, and H. virescens axt.) and one Laboulbenia
species (L. coccinellidicola Haelew.) [6,9]. An eighth species, H. hyperaspidis axt., was
brought into synonymy with H. virescens based on morphological characteristics [10],
although this decision might have been premature [6].
Coleomegilla maculata DeGeer (Coleoptera: Coccinellidae), the 12-spotted ladybird,
is widely distributed in natural and managed ecosystems in North, Central, and South
American regions, including Brazil [11–14]. It is primarily an aphidophagous insect,
but its diet may include other insects (e.g., scales, psyllids, eggs, and neonate larvae of
Lepidoptera and Coleoptera). us, this ladybird is considered an important agent for
crop pest control [15–17]. Coleomegilla maculata adults are known to be hosts for H.
coleomegillae and H. palustris in Ecuador, Costa Rica, and Cuba. e rst observation
of C. maculata acting as a host for Hesperomyces (H. palustris) occurred in 1951 in Cuba
DOI: 10.5586/am.1117
Publication history
Received: 2018-02-25
Accepted: 2018-11-21
Published: 2019-04-18
Handling editor
Malgorzata Ruszkiewicz-
Michalska, Institute for
Agricultural and Forest
Environment, Polish Academy of
Sciences, Poland
Authors’ contributions
HH: collected and examined
the material, drafted the
manuscript; JD and JR:
examined the material,
prepared the gure; contributed
to manuscript preparation; AS:
wrote the manuscript; EM: wrote
the manuscript and identied
ladybird species; CA: examined
and identied the material,
wrote the manuscript
Funding
The authors acknowledge
CAPES, CNPq, and FAPERJ for
funds supporting this research.
Competing interests
No competing interests have
been declared.
Copyright notice
© The Author(s) 2019. This is an
Open Access article distributed
under the terms of the
Creative Commons Attribution
License, which permits
redistribution, commercial and
noncommercial, provided that
the article is properly cited.
Citation
Inácio CA, de Paulo HH, Almeida
JD, Rembinski J, Menezes ELA,
Silva AC. A new report on
Hesperomyces coleomegillae
(Ascomycota, Laboulbeniales)
parasitism of Coleomegilla
maculata (Coleoptera,
Coccinellidae) in Brazil. Acta
Mycol. 2019;54(1):1117. https://
doi.org/10.5586/am.1117
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2 of 7© The Author(s) 2019 Published by Po lish Botanical Socie ty Acta Mycol 5 4(1) :1117
Inácio et al. / A r eport on Hesperomyces parasitism of Coleomegilla maculata
[9]. Coleomegilla maculata adults were found with H. palustris and H. coleomegillae
thalli in Costa Rica and Ecuador [18].
e Brazilian Laboulbeniales fungi have not yet been thoroughly investigated.
ere is a record of Laboulbenia ecitonis Blum from the Eciton, or army ant, genus
(Hymenoptera: Formicidae, Ecitoninae) in Curitiba, State of Paraná [7,19]. Data in
previous literature indicates that nearly 100 species of laboulbenialean fungi have been
recorded in Brazil, the majority of which have been found on beetles [20,21]. In addition,
Rossi and Bergonzo [21] documented the occurrence of 13 Laboulbeniales species in
Brazil – all but one associated with beetles. e exception was H. coccinelloides, found
on a ladybird, Diomus seminulus (Mulsant), in the State of Ceará.
is work aims to report Hesperomyces infecting C. maculata adults in mass-rearing
laboratory conditions in Seropédica, Rio de Janeiro, Brazil.
Material and methods
A colony matrix of C. maculata was reared in a climate-controlled laboratory (25°C
±1°C, 60% ±10% RH, and 12-hour photoperiod) at the Integrate Pest Management
Center (CIMP) of the Department of Entomology and Plant Pathology (DEnF) of the
Universidade Federal Rural do Rio de Janeiro (UFRRJ) on the Seropédica campus in
RJ, Brazil.
is colony originated from adults collected from the organic farm Fazendinha
Agroecológica Km 07, also known as Integrated System of Agroecological Produc-
tion (SIPA) in the municipality of Seropédica, RJ (22°45'24" S, 43°40'29" W) in 2010
[22]. Adults and larvae were reared continuously and fed ad libitum on living larvae
of Drosophila melanogaster Meigen (Diptera: Drosophilidae). e ospring of adults
collected in this farm were introduced annually in the colony matrix to maintain the
vigor of the colony. e eld adults were separated from those of the colony matrix
and held in plastic containers.
Adults were stored in disposable 1-liter transparent plastic containers sealed with
organza to enable gas exchange. Due to the diculty in visually determining the sex
[23], six adults were kept per container; however, when mating had not been observed
in a 24-hour period, random exchanges among containers of some individuals were
performed to ensure the presence of at least one viable pair per container. Filtered water
was provided using cotton wool placed in plastic bottle caps. e larvae of C. maculata
were individually kept in 20-mL glass vials closed with hydrophilic cotton from the
second instar until adulthood.
From September to December 2015 and January to
May 2016, C. maculata adults (6 months to 1-year old)
with yellowish structures in some parts of their integu-
ment were observed in the colony matrix at CIMP. Each
individual was observed under a dissecting microscope
in the Laboratory of Mycology (DEnF, UFRRJ). Examin-
ing these adults revealed that the visible structures were
thalli of Laboulbeniales fungi. eir position on the host
integument was recorded (Tab. 1 ).
To identify the parasite, the thalli were gently removed
from the host’s cuticle using a needle as well as dissect-
ing and optical microscope techniques. e thalli were
mounted on permanent slides stained with cotton-blue/
lactoglycerol or oxin/KOH glycerol. Measurements
and pictures were taken using an Olympus BX41 optical
microscope with a digital camera and micrometer. e
following morphological characteristics were determined:
total length from foot to perithecial tip, length from foot
to tip of uppermost antheridium, length and width of perithecium, and length and
width of ascospores. Both the Philco-Hitachi TM 1000 electron microscope, located
at the Health and Sciences Biological Institute – ICBS/UFRRJ (Seropédica campus),
and Evo LS 10 (Carl Zeiss), located at EMBRAPA Agrobiology (Seropédica, RJ), were
Tab. 1 Number of mature thalli of H. colleomegillae on dierent
body parts of several host individuals.
Body part Number of thalli* % of thalli
Head 25 8.9
Leg 44 16.0
orax 46 30.1
Abdomen 61 22.0
Elytra 64 23.0
Total 281 100.0
* Taken from 50 naturally infected individuals.
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Inácio et al. / A r eport on Hesperomyces parasitism of Coleomegilla maculata
utilized for some measurements, and pictures were acquired. Identication of the
fungal parasite followed de Kesel [24] and Goldmann et al. [18]. Sampled material and
voucher slides were deposited at the Phytopathological Herbarium Verlande Duarte
Silveira (DEnF/UFRRJ), UFRJ.
Results
e fungus was identied in the genus Hesperomyces, described by axter in 1891
(Ascomycota, Laboulbeniomycetes, Laboulbeniales) [25].
Hesperomyces coleomegillae W. Rossi & A. Weir (Fig. 1)
Material examined. Brazil, Rio de Janeiro, Seropédica: main campus of UFRRJ, inside a
building of CIMP, coordinates 22°46'10" S, 43°41'38" W, on elytra of the ladybird Coleome-
gilla maculata DeGeer, November 14, 2015, H. H. Paulo No. 3 (UFRRJ – 12.305).
e fungus formed ascomata on several parts of C. maculata adults, including the
prothorax, mesothorax, and head (antennae and mouthparts, such as palpi); however,
formation primarily occurred on the elytra (dorsal part) (Fig. 1A–G). e fore, middle,
and hind legs and abdomen also exhibited infection (Tab . 1 ). Ascomata showed the
following characters: length from foot to top of perithecium: up to 770 μm; length
from foot to tip of uppermost antheridium: 108–156 μm; perithecium: 92–563(–670)
× 34–80(–96) μm, showing apical outgrowths (26–36 μm) (Fig. 1J–L); ascospores:
68–96 × 5–6 μm, hyaline, one-septate, spindle-shaped, with thick a mucilaginous layer
(Fig. 1L) (Tab. 2 ).
Discussion
is paper reports the rst record of living C. maculata adults hosting Hesperomyces
in laboratory mass-rearing in Brazil, originating from specimens collected in the eld.
Eggs and larvae were never infected, which was expected as Laboulbeniales fungi
only infect living adults [4,6]. is fungus was identied as H. coleomegillae based on
morphological characters described in previous literature [18] (also see Tab. 2 ).
It has already been reported that species in the genus Hesperomyces parasitize C.
maculata adults; specically, H. coleomegillae in Central America (Costa Rica) and H.
palustris in Costa Rica, Cuba, and Ecuador [18,26].
Laboulbeniales fungi do not have a free-living stage, and the propagation of their
sticky ascospores is triggered or promoted by the activity of the host (grooming,
copulation, or other contact) [4,6,27]. A number of factors may have led the ladybird
colony to become infected with H. coleomegillae. It is likely that a eld-collected adult
bearing mature thalli (having passed unnoticed by the collector) was enough to initi-
ate propagation among the adults in the rearing containers. In addition, when mating
had not been observed within 24 hours, there was random exchanges of individuals
among the containers until the presence of at least one viable pair per container was
observed. However, new adult collections should be carried out on the same farm to
more accurately detect natural infection of C. maculata by Hesperomyces species.
Individual Cycloneda sanguinea (Linnaeus), Eriopis connexa (Germar), Harmonia
axyridis (Pallas), and Hippodamia convergens Guerin-Meneville adults have also been
reported to occur at SIPA [13,28,29], and H. virescens axt. has been reported to infect
adult lady beetles of the above species in other countries [6,25]. erefore, new records
of species in Hesperomyces on wild populations of these lady beetles in Brazil should
be expected. However, based on studies by Cottrell and Riddick [30] and Riddick [31]
the chances of transmission taking place from H. virescens-infected H. axyridis to C.
maculata adults at SIPA are likely low. ese authors demonstrated that intraspecies
transmission of this fungus in H. axyridis was common, whereas interspecies transmis-
sion of H. axyridis to Coccinella septempunctata L. and Olla v-nigrum (Mulsant), as well
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Inácio et al. / A r eport on Hesperomyces parasitism of Coleomegilla maculata
Fig. 1 (A–G) Body parts of Coleomegilla maculata infected by Hesperomyces. (A) Pronotum and dorsal part of the elytra of C.
maculata with thalli (bar: 1 mm). (B,C) Legs and prosternum of C. maculata with ascomata (bar: 500 µm). (D–F) Pictures obtained
from a scanning electron microscope (SEM). (D) Detail of the fungus on the head and pronotum of C. maculata (bar: 5 mm).
(E) Infection on leg (bar: 600 µm). (F) Detail of infection of tibia (bar: 600 µm). (G) Detail of infection, mainly of femur (bar:
600 µm). (H–L) Hesperomyces structures. (H) Detail of young antheridium with appendages (bar: 15 µm). (I) Apical outgrowth
of perithecia (bar: 100 µm). (J,K) Perithecia (bar: 100 µm). (L) Ascospores (bar: 20 µm).
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Inácio et al. / A r eport on Hesperomyces parasitism of Coleomegilla maculata
as from O. v-nigrum to both C. septempunctata L. and H. convergens Guerin-Meneville,
was notably uncommon. e same authors [30,31] did not observe infection of C.
maculata adults aer connement with H. axyridis aer placed in a vial and tumbled
on a vial roller for 1 h.
In general, Laboulbeniales fungi cause little or no harm to their arthropod hosts
and do not seem to kill them [32–35]. However, there are indications that species in
the genus Hesperomyces deviate from this because of the penetrating haustorium in
the exoskeleton of their hosts, and some negative eects on hosts have been reported
[36,37]. Hosts with high numbers of thalli, such as those from H. virescens on H.
axyridis with more than 100 thalli (sometimes >400 thalli), on the outer parts of their
body (e.g., elytra, eyes, antennae, mouthparts, and/or legs) may no longer be able to y,
mate, or detect their prey [6,37]. In this study, it was observed that 100% of naturally
colonized adults died aer 60 days and the number of eggs laid by infected adults was
aected compared to noninfected adults of the same age. It was also observed that C.
maculata adults under 6 months of age were not infected by H. coleomegillae. is
result suggests that older adults may be more susceptible to infection by this species.
Additional research is needed to support this hypothesis.
Tab. 2 Comparison of morphological characters (in µm) of Hesperomyces species associated with Coccinellidae (Coleoptera)
reported from Central and South America.
Species Country
Length
from foot to
perithecial tip
Length from
foot to tip of
uppermost
antheridium
Length and
width of
perithecium
Perithecial
outgrowth
Length and
width of
ascospores
H. coccinelloides1Panama 120–240 - 24–30 ×
85–110
35–40 -
H. coleomegillae2Costa Rica,
Ecuador
370–600 130–150 55–70 ×
210–350
27–33 75–77
H. hyperaspidis3Trinidad
Tobago
180 - 25 × 110 20 -
H. palustris2Costa Rica,
Ecuador
(355)400–675 105–130 55–70 ×
245–355
50–70 -
H. coleomegillae4Brazil Up to 770 108–156 34–80(–96) ×
92–563(–670)
26–36 68–96 × 5–6
1 axter [38] (host: Scymnus tardus Mulsant); 2 Goldmann et al. [19] (host: Coleomegilla maculata); 3 axter [38] (host: Hyperaspis
sp.); 4 present study (host: Coleomegilla maculata).
Acknowledgments
e second author acknowledges CAPES for grants supporting his master’s degree program. e
authors are obliged to Karinne Moura de Freitas (EMBRAPA Agrobiologia) and Jose Antonio
(UFRRJ /ICBS) for their technical assistance with electron microscope; C. A. Inácio is grateful to
the Foundation for Aid Research in the State of Rio de Janeiro (FAPERJ) and National Council
for Scientic and Technological Development (CNPq).
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