Special Issue "Insect Pathology"

Guest Editor
Prof. Dr. Drion G. Boucias
Entomology and Nematology Department, University of Florida, Building 970, Natural Area Dr. (Steinmetz Hall), Gainesville, FL 32611, USA
Website: http://entnemdept.ifas.ufl.edu/cv/people/boucias/
E-Mail: pathos@ufl.edu
Interests: insect pathology; insect disease interactions; microbial metabolites; epizootiology; microbial control; structure-function relationships; symbiont/pathogen interactions

Dear Colleagues,

Insect Pathology is a broad topic that encompasses multiple disciplines that covers the biology of microbes that have a detrimental impact on the insect fitness. Over the past decades, progress has been made in elucidating .the mechanisms responsible for the ability of microbes (viruses, bacteria, fungi, protists, algae, nematodes) to infect and replicate within the insect host. Using a combination of histological and molecular approaches specific pathogenic determinants have been identified that dictate the infectivity, virulence, and specificity of various disease-causing agents. Fundamental studies on these insect-associated microbes have provided both products and strategies used in the management of insect pest populations. In this issue a combination of original articles and minireviews, written by insect microbiologists and entomologists, will address the properties that allow entomopathogens to recognize the insect host, to gain ingress through insect defense barriers, to replicate within the host, to egress from the host, and to persist and be transmitted to healthy conspecifics.

Prof. Dr. Drion G. Boucias
Guest Editor

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• insect pathology
• insect-disease interactions
• pathogenic determinants
• insecticidal toxins
• epizootiology
• insect defenses

Type of Paper: Article
Title: Compatibility, Efficacy and Virulence of Isaria Fumosorosea (Hypocreales: Cordycipitaceae) Blastospores with Agricultural Chemicals Used for Management of the Asian Citrus Psyllid Diaphorina Citri (Hemiptera: Psylloidea)
Authors: Pasco Avery, David Pick, Luis Aristizabal, James Kerrigan, Charles Powell, Michael Rogers and Steven Arthurs
Affiliation: Indian River Research and Education Center, 2199 South Rock Road, Fort Pierce, FL 34945-3138, USA; E-Mail: pbavery@ufl.edu
Abstract: Biorational insecticides are being increasingly emphasized for inclusion in integrated pest management programs for invasive insects. The entomopathogenic fungus Isaria fumosorosea can be used to help manage the Asian citrus psyllid with minimal impact on beneficial arthropods, but its effectiveness may be compromised by agrochemicals used to control concurrent pests. We evaluated the compatibility of I. fumosorosea blastospores with a range of spray oils and copper-based fungicides registered for use in citrus groves. Results showed a range of responses of the fungus to the different materials including compatibility and incompatibility. In some cases, the addition of oils with the blastospores increased the efficacy and virulence of the fungus when exposed to the psyllids, compared to either the oil or fungus alone. Our data show that care should be taken in selecting appropriate agrochemicals for tank-mixing with commercial formulations of entomopathogenic fungi for management of citrus pests. The practicality and future of using entomopathogenic fungi in the field for managing the invasive Asian citrus psyllid and other citrus pests will be discussed.

Type of Paper: Review
Title: Insects as Food for Plants
Authors: S. Behie and M.J. Bidochka
Affiliations: Department of Biology, Brock University, ST. Catharines, Canada; E-Mail: mbidochka@brocku.ca
Abstract: Many plants have evolved adaptations in order to survive in low nutrient environments. One of the more specialized adaptations in some plants to low nitrogen habitats is the ability to trap and digest insects, a high source of nitrogen. For example, insect carnivorous plants such as pitcher plants (families Nepenthaceae and Sarraceniaceae) are able to obtain substantial amounts of nitrogen from insects they ingest. Other plants form associations with mycorrhizal fungi that can provide soluble nitrogen from the soil. However, a specialized group of endophytic, insect pathogenic fungi (EIPF), particularly Metarhizium spp. and Beauveria bassiana, can provide host plants with insect derived nitrogen. These soil inhabiting fungi can infect a wide range of insect species and form endophytic associations with certain plant species. Subsequently, the fungus transfers insect derived nitrogen to the plant. Here the tripartite interactions between insect, EIPF and plant are examined. We provide a model for the evolution of insect and plant host ranges for EIPF interactions. We suggest that host plants would select for EIPF that have broad insect host ranges. On the other hand insect host specificity would be favoured in obligate insect pathogens that are non-endophytic. We also suggest that plant and EIPF form a symbiosis where in the fungus provides insect derived nitrogen in exchange for plant derived carbon sources.

Type of Paper: Review
Title: Hirsutellin A: a Paradigmatic Example of the Insecticidal Function of Fungal Ribotoxins
Authors: Elías Herrero-Galán, Lucía García-Ortega, Miriam Olombrada, Javier Lacadena, Álvaro Martínez-del-Pozo, José G. Gavilanes and Mercedes Oñaderra
Affiliations: Departamento de Bioquímica y Biología Molecular I, Facultad de Química, Universidad Complutense, 28040 Madrid, Spain; E-Mail: mos@bbm1.ucm.es
Abstract: The fungal pathogen Hirsutella thompsonii produces a insecticidal protein named hirsutellin A (HtA). On the basis of a extensive biochemical and structural characterization HtA has been considered to be a member of the ribotoxin group of proteins. Ribotoxins are a family of fungal extracellular ribonucleases which inactivate ribosomes by specifically cleaving a single phosphodiester bond located at the universally conserved sarcin/ricin loop of the large rRNA. The biological function of fungal ribotoxins has remained elusive. They were brought to light in the 1960’s during a screening program for new antibiotics and antitumor agents. Later on, in 2008 the discovery of hirsutellin A, a insecticidal protein, as a singular ribotoxin recalled the idea of the biological activity of this toxins as insecticidal agents. Further studies have demonstrated that the most representative member of the ribotoxin family, α-sarcin, also shows strong toxic action against insect cells. The determination of high resolution structures, the characterization of a large number of mutants and the use of different cell lines have been the tools used for the study of their mechanism of action at the molecular level. The aim of this review is to serve as a compilation of the facts that allow to identify HtA as a paradigmatic example of the insecticidal function of fungal ribotoxins.

Type of Paper: Review
Title: The Non-photosynthetic Algae Helicosporidium spp.: Emergence of a Novel Group of Insect Pathogens
Author: Aurélien Tartar
Affiliation: Nova Southeastern University, 3301 College Ave., Fort Lauderdale, FL 33314, USA; E-Mail: aurelien@nova.edu
Abstract: Since the original description of Helicosporidium parasiticum in 1921, members of the genus Helicosporidium have been reported to infect a wide variety of invertebrates but their characterization has remained dependent on occasional reports of infection. Recently, several new Helicosporidium isolates have been successfully maintained in axenic cultures. The ability to produce large quantity of biological material has led to very significant advances in the understanding of Helicosporidium biology and its interactions with insect hosts. In particular, the unique infectious process has been well documented; the highly characteristic cyst and its included filamentous cell have been shown to play a central role during host infection and have been the focus of detailed morphological and developmental studies. In addition, phylogenetic analyses inferred from a multitude of molecular sequences have demonstrated that Helicosporidium are highly specialized non-photosynthetic algae (Chlorophyta: Trebouxiophyceae), and represent the first described entomopathogenic algae. This review provides an overview of i) the morphology of Helicosporidium cell types, ii) the Helicosporidium life cycle, including the entire infectious sequence and its impact on insect hosts, iii) the phylogenetic analyses that have prompted the taxonomic classification of Helicosporidium as green algae, iv) the documented host range for this novel group of entomopathogens.

Type of Paper: Article
Title: Entomopathogenic Fungi as Epizootic Factor in the Forest Populations of Alien sucking Insects in North-eastern Region of the USA
Authors: Vladimir V. Gouli, Jose P. Marcelino, Svetlana Y. Gouli, Margaret Skinner and Bruce L. Parker
Affiliation: Entomology Research Laboratory, University of Vermont, Burlington, Vermont, 05405-0105, USA; E-Mail: vgouli@uvm.edu
Abstract: Mycological analyses of the most economically important alien sucking insects including elongate hemlock scale, Fiorinia externa Ferris (Hemiptera: Diaspididae); European fruit lecanium, Parthenolecanium corni Bouche, (Hemiptera: Coccidae); hemlock woolly adelgid, Adelgid tsugae Annand (Homoptera: Adelgidae) and pear thrips, Taeniothrips inconsequens Uzel (Thysanoptera: Thripidae) were conducted. All fungal cultures isolated from insects in the period of mass mortality were identified based on both traditional morphological characteristics and DNA analyses. The fungi were subdivided into three groups. The first group are included the specialized entomopathogenic species - Mariannaea sp. Myriangium duriaei Mont. & Berk., Myriangium sp., Hirsutella lecaniicola (Jaap) Petch, Hirsutella sp., Metarhiziopsis microspora, Beauveria bassiana (Balsamo-Crivelli) Vuillemin, Lecanicillium muscarium (Petch) Zare & W Gams, L. psalliotae (Treschow) Zare & Gams, Lecanicillum sp. Paecilomyces marquandii (Massee) Hughes, Isaria farinosa (Holmsk.) Fries, Isaria sp. and Colletotrichum acutatum subsp. fioriniae (Marcelino & Gouli) R.G. Shivas & Y.P. Tan. The second group are united the facultative entomopathogens – Rhinocladiella sp., Nectria sp., Botrytis sp., Fusarium sp., Phyalophora sp., Phoma sp.; and the third group - contaminants – Penicillium sp., Cladosporium sp., Scopulariopsis sp., Aspergillus sp., and Trichoderma spp. Local explosive epizootics provoking by specialized fungi – M. duriaei, H. lecaniicola, B. bassiana, Lecanicillium sp. and Mariannaea sp. were registered. Fungi M. microspora, P. marquandii and I. farinosa did not have significant importance as mortality insect factors. Experimental inoculation of insect in laboratory and field conditions using fungi B. bassiana and L. muscarium was resulted to mortality of insects from 45% to 95 % but the pest populations were re-established the high quantity after wintering. The fungi tested in field conditions are ecologically associated with soil and fungal propagules have limited possibility to persist in plant canopy, As a result the single local application of soil-dwelling B. bassiana and L. muscarium fungi cannot result to long-time suppression of insect population which permanently located in plant canopy.

Type of Paper: Review
Title: Long-term diagnostic investigations on the occurrence and incidence of insect pathogens in populations of the codling moth, Cydia pomonella L.
Authors: Gisbert Zimmermann, Alois M. Huger, Regina G. Kleespies
Affiliation: Julius Kühn-Institute, Federal Research Centre for Cultivated Plants, Institute for Biological Control, Heinrichstraße 243, D-64287 Darmstadt, Germany; E-Mail: regina.kleespies@jki.bund.de
Abstract: About 20,550 larvae, pupae, and adults of the codling moth, Cydia pomonella L, were diagnosed for pathogens during prognostic long-term investigations (1955-2011). Prevailing entomopathogens diagnosed in these studies were entomopathogenic fungi, especially Beauveria bassiana, and the microsporidium Nosema carpocapsae, the infection rates of which were determined in codling moth populations from various regions. Experiments revealed that the fecundity and fertility of microsporidia-infected female adults were significantly reduced compared to healthy ones. These studies are aimed at providing an overview on the ecology of C. pomonella and its natural insect pathogenic antagonists with regard to the development of new biocontrol strategies.

Type of Paper: Article
Title: The effect of Entomopathogenic fungus Aspergillus spp. on the European Honeybee, Apis mellifera ligustica (Hymenoptera : Apidae))
Authors: Robert K. Mensah ^1,3, Robert Spooner-Hart ² and Albert Basta ²
Affiliations: ¹. Australian Cotton Research Institute, NSW Department of Industry & Investments, Locked Bag 1000, Narrabri, Australia; E-Mail: robert.mensah@industry.nsw.gov.au
^2.Centre for Plants and the Environment, University of Western Sydney, Locked Bag 1797 Penrith South NSW 1797, Australia; E-Mail: r.spooner-hart@uws.edu.au
^3.Australian Cotton Catchment Communities Cooperative Research Centre (CRC), Locked Bag 1001, Narrabri, NSW Australia
Abstract: Entomopathogenic fungus when used as microbial control agents against pests in agroecosystems such as cotton may have potential to establish and spread in the environment. As a result, information on the effect of such entomopathogenic fungi on non-target organisms such as honeybee, Apis mellifera is important for registration as biopesticides. The effect of an entomopathogenic fungus, BC 639 (Aspergillus spp) against the European honeybee, A. mellifera was studied. Three methods of application namely direct dermal exposure to spores, acute oral toxicity and exposure of bees to fresh spore residues on filter paper in a petridish were used in these studies in the laboratory. In the direct dermal exposure and exposure of bees to spores on filter paper methods, the bees were exposed to 2.5 or 5.0 mL spray aliquots via a 118 Potter Precision Spray Tower. In the acute oral toxicity test, 2.5 or 5.0 ml fungal formulation was diluted in 50% honey syrup and fed to the bees. Mortality was recorded at 24, 48, 72 and 96 hours after treatment (HAT). The results showed the entomopathogen, itself, did not induce mortality in worker honey bees up to four days after they were exposed to the insecticide, whether by direct contact, contact with fresh residues or exposed to bees in simulated nectar. No fungal growth was observed on any dead honey bees seven days after application. In conclusion, the findings of this study indicate that BC 639 is a good candidate as a microbial control agent in the context of integrated pest management (IPM) program on agricultural crops.

Type of Paper: Article
Title: Abundance of Detected Haplotypes from Fifteen Isolates of Beauveria bassiana (Balsamo) Vuillemin (Ascomycota: Hypocreales) Found Naturally Infecting the Coffee Berry Borer Hypothenemus hampei (Coleoptera: Curculionidae) in Brazil
Authors: Richard Ian Samuels ^1,*, Verônica de Moraes ¹, Rozimar Campos Pereira ¹, Carlos Peres Silva ² and Maurício Bacci Jr. ³
Affiliations: ¹ Department of Entomology and Plant Pathology, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ 28013-600, Brazil; E-Mails: richard@uenf.br (R.I.S.); veronicade@bol.com.br (V.M.); rozimarcp@gmail.com (R.C.P.)
² Departamento de Bioquímica, Universidade Federal de Santa Catarina, CEP 88040-900, Florianópolis, Brasil; E-Mail: capsilva@ccb.ufsc.br
³ Department of Biochemistry and Microbiology, Center for the Study of Social Insects, São Paulo State University, Av. 24A, 1515, 13506-900, Rio Claro, SP, Brazil E-Mail: mbacci@rc.unesp.br
Abstract: The host-pathogen relationship of the coffee berry borer, Hypothenemus hampei, and the entomopathogenic fungus Beauveria bassiana was investigated by testing the virulence of 15 isolates found naturally infecting this insect in Brazil and from DNA sequence analysis of the ITS region. All isolates were considered to be virulent under laboratory conditions, with S50 values ranging from 2 to 4 days and cumulative mortalities at day 4 ranging from 46 to 100%. There appeared to be no relationship between virulence and geographical location or strain genotype. This finding suggesting that virulence was not a major characteristic determining dispersal of B. bassiana in the coffee berry borer. Phylogenetic analysis showed that the 15 studied isolates can be divided in two groups: group 1, composed of 12 isolates which were very closely related to each other, and another heterogeneous group (group 2) containing 3 isolates, more closely related to distinct B. bassiana strains which had been previously described in the literature. Both group 1 and group 2 strains were found infecting H. hampei individuals in the same geographic regions, suggesting that the coffee berry borer can be readily infected by a range of non-host specific B. bassiana isolates.

Type of Paper: Article
Title: Entomopathogenic Nematode (EPN) Prevalence and Diversity in Organic and Conventional Beef and Wheat Productions Systems in Oklahoma
Authors: Xandra Robideau *, Kyle Risser and Carmen Greenwood
Affiliations: Oklahoma State University, Department of Entomology and Plant Pathology, 127 Noble Research, Stillwater, OK 74078, USA; E-Mail: carmen.greenwood@okstate.edu
Abstract: Entomopathogenic nematodes (EPN) in the families Steinernematidae and Heterorhabditidae are obligate parasites of arthropods, exist naturally in soils worldwide, and have been used commercially to suppress soil-dwelling insect pests. Little is known about EPN diversity within Oklahoma. Oklahoma is home to 11 different ecoregions delineated by a pronounced precipitation gradient from east to west across the state. This study aimed to characterize EPN communities in organic versus conventional beef and wheat production systems within the same ecoregion. A combination of bioassay technique and molecular identification was used to identify EPN species. Soil samples were subjected to bioassay using G. mellonella to ascertain infection rates by EPN. EPN were identified, initially by infected G. mellonella symptoms. Based on these symptoms, appropriate primers were chosen to amplify regions of the ITS gene. These regions were then sequenced to confirm identification. The Heterorhabditis species identified was Heterorhabditis bacteriophora. The Steinernema species of EPN identified included: Steinernema feltiae, S. texanum, S. glaseri. S. carpocapsae, and S. riobrave. Within the organic and conventional fields, overall infection rates were 2.06% in organic wheat, 6.73% in conventional wheat, 7.33% in organic pasture, and 6.67% in conventional pasture. This study showed a higher incidence of EPN in organic wheat fields than conventional wheat fields and higher incidence in pastures than agricultural fields.

Type of Paper: Article
Title: A third way for entomophthoralean fungi to survive the winter: slow disease transmission between hibernating host
Authors: Jørgen Eilenberg, Lene Thomsen and Annette Bruun Jensen
Affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Thorvaldsensvej 40, DK 1871 Frederiksberg C., Denmark; E-Mail: Jei@life.ku.dk
Abstract: In temperate regions, insect pathogenic fungi face the challenge of surviving through the winter. Winter is a time when hosts are immobile, low in number or are present in a stage which is not susceptible to infection. Fungi from Entomophthoramycota have so far been known to survive the winter in two ways: either as (1) thick-walled resting spores released into environment from dead hosts, or as (2) structures inside the dead host (e.g., hyphal bodies). Here we report, from Danish environment, a third way to survive the winter, namely a slow progression and transmission of Entomophthora schizophorae in adult dipteran Pollenia hosts that hibernate in clusters in unheated roofs, wood etc. Fungus killed, sporulating flies were observed outside very early and very late in the season. By sampling adults at the time of their emergence from hibernation in late winter/early spring we documented that the fungus was naturally prevalent and killed flies after incubation. Experimentally we documented that even at a temperature of 5 o C, the fungus was able to maintain itself and in Pollenia cohorts for up to 90 days. From these observations the full winter cycle of this fungus is elucidated. The three types of winter survival are discussed in relation to benefits for fungus epidemic development and host-pathogen co-evolution.

Type of Paper: Article
Title: Potential Plant-Aphid-Fungal Associations Aiding Conservation Biological Control of Cereal Aphids in Argentina
Authors: César Salto ¹, Romina Manfrino ² and Claudia Lopez Lastra ³,*,
Affiliation: ¹ Instituto Nacional de Tecnología Agropecuaria (INTA). Área Investigación Agronomía. Protección Vegetal. Ruta Nacional 34, Km. 227. Rafaela (2300), Santa Fe, Argentina
² CONICET, INTA, Rafaela, Ruta Nacional 34, km 227, Santa Fe, Argentina
³ Centro de Estudios Parasitológicos and de Vectores (CEPAVE). UNLP-CONICET. Calle 2, nro 584. La Plata (1900), Buenos Aires, Argentina; E-Mail: claudia@cepave.edu.ar
Abstract: The overall goal of this study was to identify potential associations between aphids and plants as reservoirs of entomophthoroid fungi. A survey of native spontaneous vegetation that grows around wheat crops in 2 different locations was performed over 2 years, from April 2010 to April 2012 in Pampeana central region, Argentina. For each sample date was selected on a randomly basis five individuals of each vegetal species, from those plants were collected healthy and infected aphids. Aphid hosts were taxonomically identified as well as entomophthoroid fungi. The associations identified as favorable for inclusion in CBC strategies in borders of wheat crops are: Sonchus oleraceus (L.)/Hyperomyzus carduellinus (Theobald), Uroleucon sonchi (L.)/Pandora neoaphidis (Remaudière & Hennebert) Humber; Sonchus oleraceus (L.)/Hyperomyzus carduellinus (Theobald)/Zoophthora radicans (Brefeld) Batko; Lamium amplexicaule (L.)/Cryptomyzus korschelti Bôrner/P. neoaphidis, Z. radicans, Entomophthora planchoniana Cornu; Foeniculum vulgare (Miller)/Dysaphis apiifolia (Theobald)/Z. radicans; Morrenia brachystephana Griseb/ Aphis nerii Boyer de Fonscolombe/P. neoaphidis and Brassica rapa L./Brevicoryne brassicae (L.)/P. neoaphidis. The use of these plant species as alternative substrates for the aphid species mentioned before in conservation biological control strategies could be suitable, and one reason is because the aphids hosts are not pests for the wheat crop and they also could be alternative hosts for entomophthoroid fungi in borders of wheat crops.

Type of Paper: Review
Title: Grooming Behavior in Disease Defense Mechanism
Authors: Marianna Zhukovskaya ¹, Aya Yanagawa ²,* and Brian T. Forschler ^3
1 Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian
Academy of Scienses, Saint-Petersburg, 194223, Russia; E-Mail: mzhukovskaya@yahoo.com (M.Z.)
² Research Institute for Sustainable Humanosphere, Kyoto University, Uji 611-0011, Japan; E-Mail: ayanagawa@rish.kyoto-u.ac.jp (A.Y.)
³ Department of Entomology, University of Georgia, Athens, GA 30602, USA;
E-Mail: bfor@uga.edu (B.F.)
Abstract: Grooming behavior is a well-recognized behavior in many insects, however its mechanisms, functions and roles are obscure. In this paper, we review this behavior from disease prevention aspect and overview its physical function, role in disease defense against pathogenic infection and the neurophysiological mechanism in disease defense by grooming. This paper started with the general concept and functions of grooming behavior. Then the topic moved to disease defense by the behavior; the care of individuals (body surfaces) and colonies, and closed with neurobiological factors in grooming behavior. The intricate interactions of grooming behavior in physical, immunological and neurological mechanism were illustrated and it lightened the possibility of grooming behavior in opening a new ecological view in insect-pathogen interactions.

Type of Paper: Review
Title: Immune Signaling and Antimicrobial Peptide Expression in Lepidoptera
Authors: Ángel Casanova-Torres and Heidi Goodrich-Blair *
Affiliation: Bacteriology Department, University of Wisconsin-Madison, WI, USA; E-Mails: amcasanova@wisc.edu (A.C.-T.); hgblair@bact.wisc.edu (H.G.-B.)
Abstract: Many lepidopteran insects are agricultural pests that affect stored grains, food and fiber crops. These insects have negative ecological and economic impacts since they lower crop yield and control pesticides are expensive and can have off-target effects on pollinators. A better understanding of lepidopteran immunity will aid in identifying new targets for the development of specific insect pest management compounds. A fundamental aspect of immunity, and therefore a logical target for control, is the induction of antimicrobial peptide (AMP) expression. AMPs are small cationic peptides whose expression is induced in the presence of microbial immunogenic antigens. These peptides insert into and disrupt microbial membranes, thereby promoting pathogen clearance and insect survival. Pathways leading to AMP expression have been extensively studied in the Dipteran Drosophila melanogaster. However, Diptera are an important group of pollinators and pest management strategies that target their immune systems is not recommended. Recent advances have facilitated investigation of Lepidopteran immunity, revealing both conserved and derived characteristics. In this review we will highlight differences and similarities between Drosophila and Lepidopteran immune signaling pathways involved in AMP expression and how such comparative immunology could aid in developing pest management strategies that are specific to agricultural insect pests.