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We characterized the entomopathogenic fungal species, Conoideocrella luteorostrata (Zimm.) D. Johnson, G.H. Sung, Hywel-Jones & Spatafora (Hypo-creales: Clavicipitaceae), on the elongate hemlock scale, Fiorinia externa Ferris (Hemiptera: Diaspididae), infesting Fraser fir Christmas tree, Abies fraseri (Pursh) Poir (Pinaceae). Fraser fir Christmas t...
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... have been reports of several natural enemies, including predators, parasitoids, and entomopathogenic fungi, feeding on or attacking F. externa in the last 65 yr (Davidson & McComb 1958;McClure 1977aMcClure , b, c, 1978McClure , 1979Lambdin et al. 2005;Lynch et al. 2006;Mayer et al. 2008;Marcelino et al. 2009a, b;Abell & Driesche 2012). However, only a few have shown potential to be used as biological control agents (Table 1). ...Context 2
... parasitism can cause a decrease in parasitism rate and equilibrium in host density (Ives 1992). There have been 5 entomopathogenic fungal species reported from F. externa in the USA (Table 1). So far, only 1, Colletotrichum fioriniae (Marcelino & Gouli) Pennycook (Phyllachorales: Phyllachoraceae) was found to be effective. ...Context 3
... far, only 1, Colletotrichum fioriniae (Marcelino & Gouli) Pennycook (Phyllachorales: Phyllachoraceae) was found to be effective. However, C. fioriniae was reported to cause endophyticity towards plants ( Marcelino et al. 2009 a, b; Table 1; JAP Marcelino, personal communication). The objectives of this study are: (1) morphological and molecular characterization of entomopathogenic fungal species, C. luteorostrata from scale insect species, F. externa; (2) morphological diagnostics of F. externa and its comparison with 2 closely related species, F. fioriniae and F. phantasma; and (3) a comprehensive review of potential natural enemies of F. externa. ...Context 4
... conducted a comprehensive review of natural enemies of F. externa in this study and elaborated on the need for a new natural enemy of F. externa in the USA (Table 1). There are 12 identified and 1 unidentified predator species reported from 3 families (Coccinellidae, Miridae, and Neuroptera) in F. externa infested areas in the USA (Table 1). ...Context 5
... conducted a comprehensive review of natural enemies of F. externa in this study and elaborated on the need for a new natural enemy of F. externa in the USA (Table 1). There are 12 identified and 1 unidentified predator species reported from 3 families (Coccinellidae, Miridae, and Neuroptera) in F. externa infested areas in the USA (Table 1). This includes 8 ladybird beetles (Table 1). ...Context 6
... are 12 identified and 1 unidentified predator species reported from 3 families (Coccinellidae, Miridae, and Neuroptera) in F. externa infested areas in the USA (Table 1). This includes 8 ladybird beetles (Table 1). Only 4 were found feeding on F. externa, including Chilocorus kuwanae Silvestri (Coleoptera: Coccinellidae), Cybocephalus nipponicus Endrödy-Younga (Coleoptera: Cybocephalidae), Rhyzobius lophanthae (Blaisdell) (Coleoptera: Coccinellidae), and Scymnillus horni (Gordon) (Coleoptera: Coccinellidae). ...Context 7
... 4 were found feeding on F. externa, including Chilocorus kuwanae Silvestri (Coleoptera: Coccinellidae), Cybocephalus nipponicus Endrödy-Younga (Coleoptera: Cybocephalidae), Rhyzobius lophanthae (Blaisdell) (Coleoptera: Coccinellidae), and Scymnillus horni (Gordon) (Coleoptera: Coccinellidae). Chilocorus kuwanae is an introduced species and was found established in the USA (Table 1). Cybocephalus nipponicus was imported, mass-reared, and released to control F. externa in the USA (Table 1). ...Context 8
... kuwanae is an introduced species and was found established in the USA (Table 1). Cybocephalus nipponicus was imported, mass-reared, and released to control F. externa in the USA (Table 1). There was no noticeable reduction in F. externa population in the presence of these predators (see the column of category for potential in Table 1). ...Context 9
... nipponicus was imported, mass-reared, and released to control F. externa in the USA (Table 1). There was no noticeable reduction in F. externa population in the presence of these predators (see the column of category for potential in Table 1). Three parasitoid species have shown parasitism for F. externa (Table 1). ...Context 10
... was no noticeable reduction in F. externa population in the presence of these predators (see the column of category for potential in Table 1). Three parasitoid species have shown parasitism for F. externa (Table 1). Prospaltella sp. was reported by one of the earliest studies and might be a misidentification of Encarsia citrina (Craw) ( Table 1). ...Context 11
... parasitoid species have shown parasitism for F. externa (Table 1). Prospaltella sp. was reported by one of the earliest studies and might be a misidentification of Encarsia citrina (Craw) ( Table 1). Aphytis aonidiae (Mercet) and E. citrina were reported multiple times in the literature and have shown potential to control F. externa (Table 1). ...Context 12
... sp. was reported by one of the earliest studies and might be a misidentification of Encarsia citrina (Craw) ( Table 1). Aphytis aonidiae (Mercet) and E. citrina were reported multiple times in the literature and have shown potential to control F. externa (Table 1). Ten fungi have been recovered from F. externa including 4 entomopathogenic fungi (Beauveria bassiana (Bals.-Criv.) ...Context 13
... Berk. [Myriangiaceae]), 1 endophyte, and 5 phytopathogens (Table 1), with 1 isolate of phytopathogen, Colletotrichum fioriniae (Marcelino & Gouli) Pennycook (Glommerellaceae) showing higher entomopathogenic potential for F. externa (Table 1). We categorized the natural enemies based on their control potential and concluded that 2 parasitoids, A. aonidiae and E. citrina, and 1 entomopathogenic fungus, C. fioriniae were the most effective in reducing the population of F. externa (Table 1). ...Context 14
... Berk. [Myriangiaceae]), 1 endophyte, and 5 phytopathogens (Table 1), with 1 isolate of phytopathogen, Colletotrichum fioriniae (Marcelino & Gouli) Pennycook (Glommerellaceae) showing higher entomopathogenic potential for F. externa (Table 1). We categorized the natural enemies based on their control potential and concluded that 2 parasitoids, A. aonidiae and E. citrina, and 1 entomopathogenic fungus, C. fioriniae were the most effective in reducing the population of F. externa (Table 1). ...Context 15
... 1 endophyte, and 5 phytopathogens (Table 1), with 1 isolate of phytopathogen, Colletotrichum fioriniae (Marcelino & Gouli) Pennycook (Glommerellaceae) showing higher entomopathogenic potential for F. externa (Table 1). We categorized the natural enemies based on their control potential and concluded that 2 parasitoids, A. aonidiae and E. citrina, and 1 entomopathogenic fungus, C. fioriniae were the most effective in reducing the population of F. externa (Table 1). However, the effectiveness of A. aonidiae alone is not enough and E. citrina population is asynchronous with that of F. externa in the USA (Table 1). ...Context 16
... categorized the natural enemies based on their control potential and concluded that 2 parasitoids, A. aonidiae and E. citrina, and 1 entomopathogenic fungus, C. fioriniae were the most effective in reducing the population of F. externa (Table 1). However, the effectiveness of A. aonidiae alone is not enough and E. citrina population is asynchronous with that of F. externa in the USA (Table 1). In addition, both parasitoid species showed density-dependent parasitism causing a decrease in parasitism rate and an equilibrium in host density (Table 1). ...Context 17
... the effectiveness of A. aonidiae alone is not enough and E. citrina population is asynchronous with that of F. externa in the USA (Table 1). In addition, both parasitoid species showed density-dependent parasitism causing a decrease in parasitism rate and an equilibrium in host density (Table 1). On the other hand, the entomopathogenic fungus, C. fioriniae shows plasticity in host choice from plants to insects (Table 1). ...Context 18
... addition, both parasitoid species showed density-dependent parasitism causing a decrease in parasitism rate and an equilibrium in host density (Table 1). On the other hand, the entomopathogenic fungus, C. fioriniae shows plasticity in host choice from plants to insects (Table 1). ...Context 19
... the USA, extensive work has been conducted to isolate entomopathogenic fungi to be used as biocontrol agents against F. externa and from which fungal strains in 10 genera (Beauveria, Botrytis, Colletotri- chum, Cordyceps, Fusarium, Phialophora, Lecanicillium, Mycosphaer- ella, Myriangium, and Nectria) have been recovered (Marcelino 2007;Marcelino et al. 2009a, b; Table 1). Among them, only 1 species of Colletotrichum, C. fioriniae, showed high pathogenicity against F. externa with mortality rates of 55% or higher (Table 1). ...Context 20
... the USA, extensive work has been conducted to isolate entomopathogenic fungi to be used as biocontrol agents against F. externa and from which fungal strains in 10 genera (Beauveria, Botrytis, Colletotri- chum, Cordyceps, Fusarium, Phialophora, Lecanicillium, Mycosphaer- ella, Myriangium, and Nectria) have been recovered (Marcelino 2007;Marcelino et al. 2009a, b; Table 1). Among them, only 1 species of Colletotrichum, C. fioriniae, showed high pathogenicity against F. externa with mortality rates of 55% or higher (Table 1). However, C. fioriniae has been identified as a causal agent of disease in economically important crops, including blueberries, eggplants, hazelnuts, hemp, and Satsuma mandarin among others ( Pszczółkowska et al. 2016;Sezer et al. 2017;Xu et al. 2018;Szarka et al. 2020; Table 1) restricting its use as a biocontrol agent. ...Context 21
... them, only 1 species of Colletotrichum, C. fioriniae, showed high pathogenicity against F. externa with mortality rates of 55% or higher (Table 1). However, C. fioriniae has been identified as a causal agent of disease in economically important crops, including blueberries, eggplants, hazelnuts, hemp, and Satsuma mandarin among others ( Pszczółkowska et al. 2016;Sezer et al. 2017;Xu et al. 2018;Szarka et al. 2020; Table 1) restricting its use as a biocontrol agent. ...Context 22
... far, all attempts to control F. externa have been in vain due to scale cover that protects it against insecticides, natural enemies, and adverse climatic conditions ( Marcelino et al. 2009a; Table 1). The use of insecticides has been associated with increased scale insect populations and outbreaks (Luck & Dahlsten 1975;Frank 2012). ...Context 23
... insecticide applications to Fraser fir that disregard the conservation of natural enemies may lead to their successful off-site dispersal. Predators are generalist and feed indiscriminately on different pest species, thereby reducing their effectiveness (Table 1). However, parasitoids are usually species-specific ( Ahmed et al. 2017). ...Context 24
... parasitoids are usually species-specific ( Ahmed et al. 2017). In general, parasitoids along with other natural enemies have been shown to be ineffective in controlling F. externa (Abell & Van Driesche 2012 ; Table 1), a phenomenon attributed to asynchrony between armored scales and their parasitoids, triggered by overlapping F. externa generations (Table 1). Current management practices and future research should incorporate the use of entomopathogenic fungi or extracts of secondary metabolites with insecticidal properties that are compatible with parasitoids to maximize natural Fraser fir pest control during harvest and shipment. ...Context 25
... parasitoids are usually species-specific ( Ahmed et al. 2017). In general, parasitoids along with other natural enemies have been shown to be ineffective in controlling F. externa (Abell & Van Driesche 2012 ; Table 1), a phenomenon attributed to asynchrony between armored scales and their parasitoids, triggered by overlapping F. externa generations (Table 1). Current management practices and future research should incorporate the use of entomopathogenic fungi or extracts of secondary metabolites with insecticidal properties that are compatible with parasitoids to maximize natural Fraser fir pest control during harvest and shipment. ...Similar publications
The internal transcribed spacer 2 (ITS2) is one of the best-known universal DNA barcode regions. This short nuclear region is commonly used not only to discriminate taxa, but also to reconstruct phylogenetic relationships. However, the efficiency of using ITS2 in these applications depends on many factors, including the family under study. Pinaceae...
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... Furthermore, a number of entomopathogenic fungi can infect and exert a detrimental effect on scale insects. Besides the best known entomopathogens, such as species of Akanthomyces/Lecanicillium, which are commonly reported to haunt populations of Coccidae [51,52], new species have been characterized in recent years for their pathogenicity to these pests [53][54][55][56]. Moreover, species in certain fungal genera that are frequently reported to establish an endophytic association with plants, such as Fusarium and Cladosporium, could play an ecological role in the containment of scale insects [51,57,58]. ...
Insects possess an effective immune system, which has been extensively characterized in several model species, revealing a plethora of conserved genes involved in recognition, signaling, and responses to pathogens and parasites. However, some taxonomic groups, characterized by peculiar trophic niches, such as plant-sap feeders, which are often important pests of crops and forestry ecosystems, have been largely overlooked regarding their immune gene repertoire. Here we annotated the immune genes of soft scale insects (Hemiptera: Coccidae) for which omics data are publicly available. By using immune genes of aphids and Drosophila to query the genome of Ericerus pela, as well as the transcriptomes of Ceroplastes cirripediformis and Coccus sp., we highlight the lack of peptidoglycan recognition proteins, galectins, thaumatins, and antimicrobial peptides in Coc-cidae. This work contributes to expanding our knowledge about the evolutionary trajectories of immune genes and offers a list of promising candidates for developing new control strategies based on the suppression of pests' immunity through RNAi technologies.
... Since 2019, the fungus Conoideocrella luteorostrata, has been independently confirmed from EHS infested Fraser fir (Abies fraseri) Christmas trees originating from Michigan, North Carolina, and Virginia, United States of America (Urbina & Ahmed, 2022; this study). The entomopathogenic fungus, previously known as Torrubiella luteorostrata and Paecilomyces cinnamomeus, has also been reported from Japan, Thailand, Indonesia, Cuba, Ghana and Russia (Gavrilov-Zimin & Borisov, 2020;Hywel-Jones, 1993;Luangsa-ard et al., 2008;Petch, 1923;Saito et al., 2012;Samson, 1974, p. 62) and is presumed native to Thailand based on the historic occurrence of C. luteorostrata and other Conoideocrella species (Luangsa-ard et al., 2008). ...
... isolates from this study. However due to the reduced length, sequences deposited by Urbina & Ahmed (2022) were excluded from phylogenetic analysis. ...
... Our discovery of the naturally occurring epizootic of Conoideocrella luteorostrata on elongate hemlock scales is promising since these insects are an economically significant pest on Christmas tree farms and do not currently have a commercially available fungal biocontrol option. A recently published independent survey by Urbina & Ahmed (2022) supports the relatively recent expansion of this fungus across EHS populations impacting Christmas tree production in VA, NC, and MI. We expanded on the current understanding of the U.S. population of C. luteorostrata with a mycological investigation that included bioassays using 105 and is also made available for use under a CC0 license. ...
The entomopathogenic fungus Conoideocrella luteorostrata , which is known to infect armored scale insects and whiteflies in Thailand and Japan, has been recently found causing natural epizootics in elongate hemlock scales (EHS) in Christmas tree farms in the eastern United States. The fungus was isolated from mycosed EHS, but not from the surrounding Fraser fir needles, which suggests that the life cycle is restricted to the insect host. This fungus is a promising candidate for biocontrol of EHS since it infects scales naturally and when applied under lab conditions, thus confirming pathogenicity of Conoideocrella luteorostrata against EHS, an essential first step in developing it as a biocontrol. Comparisons of multiple locus sequence data generated from isolates spanning multiple sites in North Carolina support a single clonal strain impacting United States EHS populations. Our results suggest that this biocontrol fungus merits further investigation and development as an agent targeting EHS in Christmas tree farms and surrounding hemlock forests.
... Conoideocrella luteorostrata, also known as Torrubiella luteorostrata and Paecilomyces cinnamomeus, has been reported from Japan (Saito et al., 2012), Thailand (Johnson et al., 2009), andRussia (Gavrilov-Zimin &Borisov, 2020). This species was not reported in the United States until a concurrent, recently published study reported isolating this fungus from EHS encountered during plant inspections (Urbina & Ahmed's 2022). The genus Conoideocrella was created from some members of the genus Torrubiella which separated into their own phylogenetic clade and share morphological traits including elongated conical-shaped perithecia and planar stromata (Johnson et al., 2009). ...
Elongate hemlock scales (Fiorinia externa) are insects that are parasitic to hemlock, spruce, fir, and pine trees, and which have been introduced into the US from their native range in Japan. They cause major economic damage to Christmas tree farmers because they are difficult to control with chemical pesticides and they reduce the salability and exportability of trees. We have documented the first population of the entomopathogenic fungus Conoideocrella luteorostrata in the United States. This fungus is known to infect scale insects in Japan and Thailand, but we have obtained isolates causing a widespread natural epizootic in the crawler stage of the insect throughout multiple sites in Virginia and North Carolina. The objectives of my study were to characterize the evolutionary history and morphology of this population, survey associated fungi and insects in the environment, and assess its potential as a biocontrol agent for Fiorinia externa. Genetic sequences of several isolates of C. luteorostrata from different sites at multiple loci were identical, suggesting a clonal population with a single introduction event. The fungus could be isolated from insect cadavers, but not from the surrounding fir needles, suggesting that the life cycle is restricted to the insect host. No fungal infections were observed on other Fraser fir associated arthropods found in our survey, including insect predators/parasitoids of Fiorinia externa. When elongate hemlock scale nymphs were treated with fungal spores, the fungus could be cultured from the surface-sterilized symptomatic cadavers weeks later. This fungus is a promising candidate for biocontrol of elongate hemlock scale since it specifically infects elongate hemlock scale under natural Christmas tree farm conditions and is not a plant pathogen. This project could be further developed through pathogenicity bioassays with treatments of C. luteorostrata in the laboratory and in the field.
The entomopathogenic fungus Conoideocrella luteorostrata has recently been implicated in natural epizootics among exotic elongate hemlock scale (EHS) insects in Christmas tree farms in the eastern United States. Since 1913, C. luteorostrata has been reported from various plant feeding Hemiptera in the southeastern United States, but comprehensive morphological and phylogenetic studies of U.S. populations are lacking. The recovery of multiple strains of C. luteorostrata from mycosed EHS in North Carolina provided an opportunity to conduct pathogenicity assays and morphological and phylogenetic studies to investigate genus- and species-level boundaries among the Clavicipitaceae. Pathogenicity assays confirmed that C. luteorostrata causes mortality of EHS crawlers, an essential first step in developing this fungus as a biocontrol. Morphological studies revealed that conidia aligned with previous measurements of the Paecilomyces-like asexual state of C. luteorostrata, with conidiophore morphology consistent with historical observations. Additionally, a Hirsutella-like synanamorph was observed in select C. luteorostrata strains. In both a four-locus, 54-taxon Clavicipitaceae-wide phylogenetic analysis including D1-D2 domains of the nuclear 28S rRNA region (28S), elongation factor 1 alpha (EF1-α), DNA-directed RNA polymerase II subunit 1 (RPB1), and DNA-directed RNA polymerase II subunit 2 (RPB2) and a two-locus, 38-taxon (28S and EF1-α) phylogenetic analysis, all three Conoideocrella species were resolved as strongly supported monophyletic lineages across all loci and both methods (maximum likelihood and Bayesian inference) of phylogenetic inference except for 28S for C. tenuis. Despite the strong support for individual Conoideocrella species, none of the analyses supported the monophyly of Conoideocrella with the inclusion of Dussiella. Due to the paucity of RPB1 and RPB2 sequence data, EF1-α provided superior delimitation of intraspecies groupings for Conoideocrella and should be used in future studies. Further development of C. luteorostrata as a biocontrol against EHS will require additional surveys across diverse Hemiptera and expanded pathogenicity testing to clarify host range and efficacy of this fungus.
