ÁREA: BIOLOGÍA Y GENÉTICA

Entomopathogenic Fungi in Misiones Province: A Review

Hongos entomopatógenos en la provincia de Misiones: Revisión

 

Gustavo A. Bich^{1 *}, María L. Castrillo², Marilyn R. Silva¹, Gabriela V. Díaz², Laura L. Villalba², Pedro D. Zapata², y Martha G. Medvedeff^†1

¹ Laboratorio de Microbiología e Inmunología, Universidad Nacional de Misiones, Av. Mariano Moreno 1375, CP 3300, Posadas, Misiones, Argentina.
² Laboratorio de Biotecnología Molecular, Universidad Nacional de Misiones, Av. Mariano Moreno 1375, CP 3300, Posadas, Misiones, Argentina.
* E-mail: gustavobich@yahoo.com.ar

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Abstract

Entomopathogenic fungi (EPF) are microorganisms with a high specificity and the ability to infect and kill insects and consequently there has been great interest in the use of these fungi as biocontrol agents against many crop pests. The purpose of the present review was to update the available information about EPF in Misiones in order to expand the knowledge of biodiversity of this group and the potential use in biocontrol of pest. The broad literature in this subject was reviewed and synthesized. First we present a general view of taxonomical information of EPF and then, noteworthy studies conducted by several authors. As a result of this review, it was concluded that there are scarce studies on EPF in Misiones province compared to other provinces in Argentina and Brazil. The goal of this overview is to encourage the search and in-depth examination of the scientific knowledge of EPF in Misiones province.

Keywords: Review; Entomopathogenic fungi; Biodiversity; Biological control; Misiones.

Resumen

Los hongos entomopatógenos (HEP) son microorganismos altamente específicos que se alimentan de insectos y por ello existe un gran interés en el uso de estos hongos como control biológico para cultivos de interés agrícola. El propósito de esta revisión fue actualizar la información disponible sobre HEP en Misiones e incrementar el conocimiento de la biodiversidad de este grupo y su uso potencial en biocontrol de plagas. La amplia y dispersa bibliografía disponible sobre este tema fue minuciosamente revisada, organizada y sintetizada. Se presenta una visión general sobre la información taxonómica de los HEP, y luego se realiza una recopilación y análisis de los estudios publicados. Como resultado de esta revisión se puede concluir que existen escasos estudios de HEP en la provincia de Misiones comparado con otras provincias de Argentina o Brasil. La expectativa de esta revisión de los estudios de HEP es fomentar la búsqueda y profundización del conocimiento científico en el área.

Palabras clave: Revisión; Hongos entomopatógenos; Biodiversidad; Control biológico; Misiones.

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Introduction

The province of Misiones belongs to the Alto Parana Atlantic Forest, an ecoregion of the Atlantic Forest. It has a subtropical semi-deciduous forest with an annual rainfall of 1700-2200 mm, with no marked drought season ⁽¹⁾. The biota of the Atlantic Forest is extremely diverse, and the assessment of the current state of this region´s biodiversity is still poorly known ⁽²⁾. Although current research data are significant, there are not equivalent to the huge amount of unknown diversity and every accurate research will lead to a beneficial contribution.
Entomopathogenic fungi (EPF) are microorganisms of the Fungi kingdom, mainly present in Ascomycota and Basidiomycota phyla, but there are also some strains belonging to Chytridiomycota and Zygomycota phyla ⁽³⁾.
Ascomycota is the major phylum in the Fungi kingdom, including many important entomopathogenic fungi in their asexual (anamorphic) phase like Beauveria, Metarhizium, Lecanicillium, Nomuraea, or Paecilomyces = Isaria; or the sexual (teleomorphic) state, Cordyceps. Also, many of the asexual fungi in the Hypocreales order are under intensive study due to several traits favoring their use as biological insecticides, owing their ease of mass production, storage, virulence, and application ^{(4, 5)}.
Only a small number of members within the Basidiomycota phylum are true entomopathogens. This group of fungi is characterized by the development of reproductive spores, named basidiospores. Primarily Septobasidium and Uredinella genera are obligate pathogens of armored scale insects (Hemiptera). These fungi form a complex relationship with their hosts; they are parasitic on individual insects but may be mutualistic from the perspective of a population of insects ^{(6, 7)}.
Chytrids are fungi in the phylum Chytridiomycota. They inhabit freshwater ecosystems and produce zoospores with a single flagellum. The best-known insect pathogenic species belong to the genus Coelomomyces; all are obligate parasites of mosquitoes and other Dipterans and require crustacean alternate hosts to complete their life cycles ⁽⁸⁾.
The zygomycetes, in phylum Zygomycota, are characterized by the formation of sexual spores called zygospores. Most entomopathogens within the Zygomycota occur within the order Entomophthorales. Many species have worldwide distribution and are often responsible for wide-scale epizootics, affecting mainly species listed in the orders Hemiptera, Lepidoptera, Orthoptera and Diptera. The most common genera include Conidiobolus, Entomophaga, Entomophthora, Erynia, Pandora, Neozygites and Zoophthora. Most are obligate parasites possessing restricted host ranges; however, some species, such as Zoophthora radicans, have relatively wide host ranges ^{(3, 9)}.
The observation of major epizootics of fungal pathogens in natural populations of insects and other arthropods has encouraged intense interest in the use of EPF as biological control agents ⁽¹⁰⁾. Also, entomopathogenic Hyphomycetes have one of the widest spectra of host ranges among entomopathogens ⁽¹¹⁾. Therefore, EPF can be employed in biological control strategies ⁽¹²⁾.
Biological control with EPF is a promising alternative to chemical control; also biocontrol with entomopathogenic fungi might provide long-lasting insect control without damage to the environment or non-target organisms ⁽¹³⁾.
The available literature of studies on entomopathogenic fungi in Misiones province is rather scattered. Despite the importance of entomopathogenic fungi, for biodiversity and agriculture, there has been little attempt to synthesize an overview of the diversity of these microbes in Misiones. The purpose of the present review was to collate and update the available information about this group of fungi in Misiones province (Argentina) in order to expand the knowledge of its biodiversity.
In order to survey the knowledge of investigations on entomopathogenic fungi in Misiones, Argentina, we reviewed the existing information and synthesized the scattered literature on this subject.
The bibliography used and cited here was carefully searched and compiled from researches and scientific data of fungal genera and families in Misiones province from major online bibliographic and academic databases.

Studies on entomopathogenic fungi in Misiones

Misiones has a rich but extensively underexplored diversity of fungi affecting arthropods; many of these fungi have an important potential use in biological control. The biodiversity in the Atlantic Forest is the richest on the earth, but microbial biodiversity in both Brazilian and Argentinean forests remains very poorly explored in comparison with the plant and animal biodiversity ^{(14, 15)}.
One of the first investigations, involving EPF, cited for this region the teleomorphic fungi Cordyceps martialis (referred as C. submilitaris) in early last century (mentioned in Sosa-Gómez et al. ^[15]).
Trichomycetes is an interesting fungal group associated with living arthropods such as insects, millipedes, and crustaceans, growing extensively in the hind gut and some of them are reported to be of insects pathogens ^{(16, 17, 18, 19)}. The term "trichomycetes" is derived from the Greek word "tricho", meaning hair, in reference to the hair-like appearance of thalli in the host gut ⁽²⁰⁾. The fungal taxon Trichomycetes would include just two orders: Asellariales and Harpellales (Amoebidiales and Eccrinales were formerly included in this taxon) ⁽²¹⁾. Harpellales is the species-richest order in the Trichomycetes class. López- Lastra et al. ⁽¹⁶⁾ studied fourteen species of Trichomycetes (phylum Zygomycota) and found that five of them (Genistellospora homothallica, Harpella tica, Smittium culisetae, Smittium sp., and Stachylina sp.) came from Misiones. The importance of the increase knowledge of this group of fungi is to determine the potential use as biological control of some insect pest ⁽²⁰⁾. Some records reported that Smittium spp. caused moderate or high larval mortality in Anopheles, Aedes and Culex genera in the laboratory, but these rates have never been found on mosquitoes in the field ^{(22, 23)}. Regarding natural enemies of Culicidae (Diptera), these findings should be kept in mind, although further analyses are needed to evaluate the feasibility to use these fungi groups in biological control.
Entomophaga grylli, other member of Zygomycota, was isolated from the grasshopper Ronderosia bergi in Puerto Iguazú, Misiones ⁽²⁴⁾. This was a new record of EPF from the Entomophthorales order isolated from grasshoppers in this province. Fungi of the E. grylli pathotype or species complex are parasites of grasshoppers and locusts (Orthoptera), and their host range includes many economically important Orthoptera species worldwide. The species of the E. grylli complex are highly pathogenic and can cause important field epizootics ^{(5, 26)}.
Recent investigations related to pests in yerba mate (Ilex paraguariensis St. Hill.) and its biological control have studied and characterized different groups of EPF. Alves et al. ⁽²⁷⁾ and Formentini et al. ⁽²⁸⁾ emphasized the use of Beauveria bassiana and Z. radicans against some pests like Thelosia camina, Hylesia sp., Oligonychus yothersi, and Gyropsylla spegazziniana. Soils of yerba mate plantations from Misiones were sampled and evaluated with respect to the presence of EPF. Schapovaloff et al. ⁽²⁹⁾ found about 30 different strains of B. bassiana, M. anisopliae and Isaria sp., and proposed the evaluation of their potential as biological control against yerba mate pests. These authors considered B. bassiana against the main pest of yerba mate, Hedypathes betulinus (Coleoptera: Cerambycidae: Lamiinae) and found strains that caused mortality rates higher than 80%. These results agree with Leite et al. ⁽³⁰⁾, who evaluated suspensions of B. bassiana against adults of H. betulinus under field conditions and found mortality rates of 76%.
Furthermore, Bich et al. ⁽³¹⁾ presented a survey about the hyphomycetes in soils of different types of yerba mate plantations. The presence of different fungal genera was observed, but just one strain of an EPF among all, was identified as Paecilomyces lilacinus, usually reported as pathogen of nematodes. However, its potential as biological control remains to be determined a priori using in-vitro assays.
In 2013 Bich et al. ⁽³²⁾ evaluated the viability of spores of Beauveria sp. and Metarhizium sp. in three commonly used surfactants, and concluded that entomopathogenic formulations containing spore solutions with glycerin are considered preferable because they do not reduce spore viability and do not make foam.
These findings are important in the search of agents for biological control of pest in main crops of agronomical importance of Misiones.

Studies with EPF in places close to Misiones province

Several studies of EPF in other Argentinean provinces and Brazilian states near Misiones are discussed in this section.
The cicadellid leafhopper Sonesimia grossa is an important insect in agriculture because it causes considerable damage to crops as a vector of plant pathogens. These insects live in Tucumán and Misiones provinces ⁽³³⁾. Toledo et al. ⁽⁵⁾ isolated Clonostachys rosea and considered it as an EPF of S. grossa in Argentina. These authors also evaluated the pathogenicity of C. rosea against two species of Hemiptera in Tucumán (other than S. grossa). Even though they confirmed mortality rates, the evaluation against S. grossa remains to be estimated in a search for a potential biological control of this leafhopper-pest in Misiones.
In Paraná State (Brazil), Dalla Santa et al. ⁽³⁴⁾ analyzed in-vitro and in field conditions of Beauveria sp production and evaluated its pathogenicity against insects in Ilex paraguariensis. They found encouraging results that support that Beauveria sp can be considered to be an important biological control agent in yerba mate plantations.
Others species belonging to Entomophthorales order were reported in Corrientes province by Sosa-Gómez et al. ⁽³⁵⁾. These authors reported that Zoophthora radicans can cause important disease outbreaks among susceptible hosts like psyllids. Also, Z. radicans affect satisfactory homoptera such as Empoasca kraemeri in Santa Catarina State (Brazil) ⁽³⁶⁾.
Table 1 illustrates the published data on entomopathogenic fungi of Misiones, including the identification of hosts and publication references.

Table 1: Entomopathogenic fungi in Misiones province

Conclusions

So far, eleven EPF genera affecting eight insect genera have been cited for Misiones, most of them jeopardize species of agricultural importance. It should also be noted that many outstanding investigations remain to be done because there were no studies corresponding to the Chytridiomycota phylum. All these EPF are important microorganisms that could be tested and probably used in biological control of harmful pests of crops in Misiones.
Also, this overview exposes the minor and fragmentary existence of EPF studies made in Misiones compared to other Argentinean and Brazilian provinces. The results compiled here are the most inclusive and current listing of fungi affecting arthropods for this province. This review contains most of the existing literature scattered among many local, national, and international publications in di verse languages, and this is the first attempt to compile and to synthesize the knowledge of EPF from this province.
The goal of this overview is to encourage the search and in-depth examination of the scientific knowledge of EPF in Misiones province.

Acknowledgements

Bich and Castrillo have fellowships for doctoral studies of the Consejo Nacional de Investigaciones Científicas y Técnicas of Argentina (CONICET) and Comité Ejecutivo de Desarrollo e Innovación Tecnológica (CEDIT) de Misiones.

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Recibido: 18/08/2013
Aprobado: 16/07/2014.