Discovery of Fusarium solani as a naturally occurring pathogen of sugarbeet root maggot (Diptera: Ulidiidae) pupae: Prevalence and baseline susceptibility

doi:10.1016/j.jip.2007.05.003

Journal of Invertebrate Pathology

Volume 97, Issue 1, January 2008, Pages 1-8

https://doi.org/10.1016/j.jip.2007.05.003 Get rights and content

Abstract

The fungus Fusarium solani (Mart.) Sacc. was discovered as a native entomopathogen of the sugarbeet root maggot, Tetanops myopaeformis (Röder), in the Red River Valley of North Dakota during the 2004 sugarbeet production season. This is the first report of a native pathogen affecting the pupal stage of T. myopaeformis. Forty-four percent of larvae collected from a field site near St. Thomas (Pembina Co.) in northeastern North Dakota during May and June of 2004 were infected with the entomopathogen. The mean LC₅₀ of F. solani, assessed by multiple-dose bioassays with laboratory-reared pupae, was 1.8 × 10⁶conidia/ml. After isolation and confirmation of pathogenicity, a pure isolate of the fungus was deposited in the ARS Entomopathogenic Fungal Collection (ARSEF, Ithaca, NY) as ARSEF 7382. Symptoms of F. solani infection included rapid pupal tissue atrophy and failure of adults to emerge. Transverse dissections of infected pupae revealed dense hyphal growth inside puparia, thus suggesting fungal penetration and pathogenicity. Mycelia emerged from pupae after host tissues were depleted. Exposure of older pupae to lethal concentrations caused rapid mortality of developing adults inside puparia. A second, more extensive field survey was conducted during the 2005 cropping season, and F. solani infection was observed in root maggots at most locations, although at lower levels (1–10%) of prevalence than in 2004. Aberrant timing or amounts of rainfall received could have caused asynchrony between pathogen and host during the second year of the experiment.

Introduction

The sugarbeet root maggot, Tetanops myopaeformis (Röder), is the most important insect pest of sugarbeet in the Red River Valley (RRV) of North Dakota and Minnesota. High infestations of this pest in the RRV are typically managed by using synthetic chemical insecticides, and up to two or three applications per growing season are not uncommon. Heavy reliance on these materials could eventually lead to the development of insecticide-resistant root maggot strains. Therefore, alternative control tools are needed to minimize producer dependence on conventional chemical insecticides.

Research on alternative T. myopaeformis control strategies utilizing microbial agents, particularly insect-pathogenic fungi, has met with some success. A native fungus, Syngliocladium tetanopsis Hodge, Humber, and Wozniak, was isolated from field-collected T. myopaeformis larvae and shown to be pathogenic to the insect (Hodge et al., 1998, Wozniak, 1999, Wozniak and Smigocki, 2001). Jonason et al. (2005) compared Metarhizium anisopliae (Metsch.) Sorok. and Beauveria bassiana (Balsamo) Vuillemin, and also evaluated several M. anisopliae strains for infectivity to T. myopaeformis larvae. They observed greater virulence against T. myopaeformis larvae in M. anisopliae than in B. bassiana, and found M. anisopliae isolate ATCC 62176 (MA1200) to result in the highest larval mortality among several isolates tested. Campbell et al., 2000, Campbell et al., 2006 tested M. anisopliae for potential as a root maggot mycoinsecticide under field conditions, and achieved encouraging results. They suggested that T. myopaeformis control via entomopathogenic fungi could be improved by using more virulent strains. While most research has focused on fungal control of T. myopaeformis larvae, the available body of literature lacks information regarding pathogen surveys on other life stages of the insect. This key insect pest could be especially vulnerable to infection during the pupal stage because pupae, being incapable of locomotion, are unable move through soil and rub off infective units of a pathogen prior to penetration.

Many Fusarium species are well-known pathogens of plants, insects, and humans. Although the systematic description of this genus is unresolved, Fusarium is unique because some isolates of the common phytopathogenic species (e.g., those associated with root rot diseases) also can infect subterranean insects. More than 13 Fusarium species are pathogenic to insects, and the group has a host range that includes Coleoptera, Diptera, Hemiptera, Hymenoptera, and Lepidoptera (Humber, 1992). Gupta et al. (1991) isolated the toxin beauvericin, a cyclodepsipeptide, from Fusarium. Those authors showed that beauvericin can kill 50% of Colorado potato beetle, Leptinotarsa decemlineata (Say), larval test populations at a 663-ppm dose. Beauvericin also is lethal to dipteran insects such as mosquitoes and blow flies (Tanada and Kaya, 1993). Venugopal et al. (1989) observed that epizootics of Fusarium caused mortality levels that were equal to or greater than predators and parasitoids in populations of the whitefly, Bemisia tabaci (Gennadius). Epizootics were suggested as being favored by high humidity, low temperatures, and availability of whitefly hosts; however, actual weather parameters were not presented in that report.

According to Humber (1992), Fusarium solani (Mart.) Sacc. is infectious to pupae of the dipteran family Anthomyiidae; however, this pathogen has not been previously reported as infecting T. myopaeformis at any stage of its life cycle. Observations reported herein focus on detection, isolation, and prevalence of F. solani in T. myopaeformis pupae collected from several field sites where sugarbeet had been grown the previous season. The objectives of research were to determine prevalence of F. solani epizootics via field surveys, describe disease progression in T. myopaeformis pupae under laboratory conditions, and quantify baseline susceptibility of pupae to F. solani.

Section snippets

Prevalence study—2004

A field site near St. Thomas (Pembina Co.) in northeastern North Dakota was selected for collections of T. myopaeformis pupae that had overwintered as larvae. The site was chosen based on the known occurrence of high T. myopaeformis infestations in the vicinity during the 2003 season. The field had been planted to sugarbeet in the year that preceded our collections, and potatoes were grown the year before sugarbeet. Spring wheat was growing on the site in 2004 during pupal collections. Major

Results

A total of 3600 pupae collected during the two field surveys were individually screened in this study. In 2004, F. solani prevalence fluctuated from 4% to 80% among pupal collection dates (Table 1). The average prevalence level of F. solani on T. myopaeformis pupae that year was 44%. In 2005, prevalence of F. solani (Table 2) ranged from <1% to 7% at St. Thomas, 6% at Lodema, and <1% at Cavalier. A 15-d incubation period was sufficient to allow mycelial egress from cadavers of infected

Discussion

This is the first report of infection of T. myopaeformis by F. solani, and it was confirmed by conducting two field surveys and laboratory screening. Pupae of T. myopaeformis infected by F. solani were found at the original site on all collection dates in 2004. Infected pupae also were present in 2005, although the frequency of infected insects was much lower than was observed in 2004. Laboratory studies demonstrated high virulence of isolate ARSEF 7382 to T. myopaeformis pupae. The high

Acknowledgements

We thank Dr. R.A. Humber of the U.S. Department of Agriculture—Agricultural Research Service Collection of Entomopathogenic Fungal Cultures (ARSEF, Cornell, University, Ithaca, NY), and J.A. Juba and Dr. D.M. Geiser of the Fusarium Research Center, Plant Pathology Department, Pennsylvania State University for identification and accession of fungal cultures. The assistance in disease surveys provided by R. Dregseth, C. Evensvold, C. Zander, B. McCamy, D. Miller, P. Burange, R.D. Adharapurapu, T.

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Recruitment of an insect and its nematode natural enemy by olfactory cues from a saprophytic fungus
2020, Soil Biology and Biochemistry
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Fusarium solani is large species complex of soilborne saprophytes, opportunistic plant parasites, and symbionts of insects such as ambrosia beetles that cultivate the fungus in their tunnels for nourishment (Egonyu and Torto, 2018). Entomopathogenic F. solani have been reported, but do not seem to be characteristic of the group (Barson, 1976; Majumdar et al., 2008). Wu et al. (2018) demonstrated that, while F. solani did not infect live Diaprepes root weevil larvae, the fungus readily colonized freeze-killed larvae.
Olfactory signals are critical for soil inhabitants to communicate and respond to the environment. In addition to the well-documented volatile cues from herbivores and herbivory-induced plants, attraction of both entomopathogenic nematodes (EPNs) and insect prey was recently shown to be induced by a saprophytic fungus Fusarium solani. Here, we used headspace solid-phase microextraction (HS-SPME) combined with gas chromatography-mass spectrometry (GC-MS), to identify two volatile organic compounds (VOCs), 1-pentanol and 1-octen-3-ol (octenol), from F. solani. In olfactometer bioassays, the infective juvenile stage of the EPN Steinernema diaprepesi was attracted to both VOCs. Although octenol was highly attractive to fungivorous Drosophila melanogaster fruit fly larvae, the non-fungivorous Diaprepes abbreviatus root weevil larvae were repelled by the compound. In soil microcosms, the VOCs delayed the infection of root weevil larvae by S. diaprepesi but facilitated S. diaprepesi infection of fly larvae. Presumably octenol attracted the flies and EPNs to a common locale, while provoking greater separation of EPNs and root weevils than occurred in the absence of the chemical. EPNs may have evolved to exploit these VOCs as a means of encountering fungivorous insects, whereas non-fungivorous arthropods may have evolved to avoid the compounds.
Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects
2020, Fungal Biology Reviews
The genus Fusarium is noted for including important plant pathogens and mycotoxin producers. Furthermore, many Fusarium lineages have been reported to be efficient in controlling insects and to exhibit promising characteristics for agricultural pest control such as causing high mortality rates and having fast action and abundant sporulation. In this review we present a survey of peer-reviewed papers published from 2000 to 2019, demonstrating the widespread pathogenicity of Fusarium to insects. This survey was made using search strings in a number of databases. We list the major complexes and species of Fusarium reported as entomopathogenic and highlight the features of interest for insect control as well as the advantages and implications of this practice. Out of a total of forty papers, at least 30 species and 273 isolates of Fusarium were reported as pathogenic to at least one species of insect. Ten complexes of Fusarium species harbor entomopathogenic fungi, of which F. incarnatum-equiseti, F. fujikuroi, F. oxysporum and F. solani (= Neocosmospora solani) species complexes represented the most abundant number of entomopathogenic strains. The entomopathogenic interactions of these fungi have received greater attention in recent years, but much remains to be explored, especially regarding the specificity of these fungi for the host insect, the production of undesirable secondary metabolites, and side-effect and safety tests organisms not targets. Detailed investigations in this regard will be crucial if we are to fully exploit the potential of Fusarium for controlling insect pests.
Isolation and structural elucidation of antifungal compounds from Ryudai gold (Curcuma longa) against Fusarium solani sensu lato isolated from American manatee
2019, Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology
Citation Excerpt :
However, no antifungal compound has been identified from the RD rhizomes. Fusarium solani sensu lato (FSSL) causes several diseases in human, animals, and plants (Nelson et al., 1994; Majumdar et al., 2008). According to our previous research, curcumin and demethoxycurcumin which are the major active constituents of turmeric showed the strong inhibitory effect on FSSL.
In a previous study, we reported that Curcuma longa strain Ryudai gold (RD) showed antifungal activity against Fusarium solani sensu lato (FSSL) among the different species and varieties of turmeric. The present study focused on isolation, identification and structural elucidation of antifungal compounds in RD. The ethyl acetate (EtOAc) fraction was eluted with n-hexane and EtOAc with gradually increasing the concentration of EtOAc (n-hexane:EtOAc; 100:0; 80:20; 60:40, 40:60, 20:80 and 0:100). The antifungal compounds were isolated from the most effective fraction by using silica gel, TOYOPEARL® HW-40F column, and high-performance liquid chromatography. Structural identification of the antifungal compounds was conducted using ¹H NMR, ¹³C NMR, and liquid chromatography-tandem mass spectrometry. The MeOH extract of the rhizome of RD inhibited the growth of FSSL in a concentration-dependent manner. The EtOAc fraction of the MeOH extract of RD demonstrated the highest antifungal activity against FSSL. The purified antifungal compounds were turmeronol B (1), turmeronol A (2), (E)-α-atlantone (3), dihydrobisdemethoxycurcumin (4), demethoxycurcumin (5) and curcumin (6). These six compounds showed concentration-dependent antifungal activity against FSSL. The concentration required for 50% growth inhibition (IC₅₀) of the four isolates of FSSL ranged from 116 to172, 127 to 185, 88 to 109, 90 to 112, 74 to 80 and 63 to 68 μM/L for turmeronol B, turmeronol A, (E)-α-atlantone, dihydrobisdemethoxycurcumin, demethoxycurcumin and curcumin, respectively. These results suggested that RD contained potential antifungal compounds that could be useful to control FSSL. The isolated compounds of RD can be a good source of natural antifungal agents or the lead compounds for the development of new synthetic drugs.
Phytochemical investigation and biological activities of Fusarium SP. An entomogenous fungus
2019, Biocatalysis and Agricultural Biotechnology
Citation Excerpt :
The genus of Fusarium is commonly known as a group of phytopathogenic fungi. However, it is now known that a large number of them act as entomopathogens, covering a wide range of hosts including Coleoptera, Diptera, Hemiptera, Homoptera, Hymenoptera and Lepidoptera (Majumbar et al., 2008). In the literature there are reports of the action of different strains of Fusarium on lepidoptera, such as F. chlamydosporum, F. equiseti, F. graminearum, F. moniliforme, F. oxysporum, F. poae, F. semitectum, F. sacchari, y F. solani.
Entomopathogenic fungi have an incredible capacity to produce biologically active metabolites. The present study was undertaken to evaluate the insecticidal activity of extracts, fractions and pure compounds from Fusarium sp. ARSEF 3300 entomopathogenic fungi against Spodoptera frugiperda Smith (Lepidoptera) and Ceratitis capitata Wiedemann (Diptera). Additionally, antimicrobial activity was determined against Staphylococcus aureus ATCC 6538 and Pseudomonas aeruginosa ATCC 27853. The culture media developed in the absence and presence of remains of the S. frugiperda insect were called fungus (H) and fungus-insect (HI), respectively. Volatile compounds in the extracts obtained with ethyl acetate were identified by GC-MS. Seven compounds of known chemical structure were isolated: cholesterol (1), campesterol (2), palmitic acid (3), cis-Oleic acid (4), stearic acid (5), ester propyl myristate (6) and cis-9, cis-12 Linoleic acid (7). The ethyl acetate extract of the HI supernatant of Fusarium sp., showed the highest ingestion dissuading activity in S. frugiperda (83% at 300 μg/g of diet) and the highest oviposition deterrence in C. capitata (50% at 50 μg/cm²). Extracts of H and HI supernatants from Fusarium sp. inhibited the growth of the P. aeruginosa (53.64% and 45.39%) and S. aureus (76.08% and 79.61%) at 400 μg/mL. Palmitic acid (46.23% and 38.59%), cis-Oleic acid (49.95% and 42.33%) and stearic acid (50.44% and 39.72%) showed the highest inhibition of growth and biofilm production in S. aureus at 100 μg/mL. Our results suggest the possible utilization of entomopathogenic fungal metabolites in the control of insect pests and human health.
The saprophytic fungus Fusarium solani increases the insecticidal efficacy of the entomopathogenic nematode Steinernema diaprepesi
2018, Journal of Invertebrate Pathology
Citation Excerpt :
Fusarium species are well-known saprophytic fungi that are abundant in soil (Teetor-Barsch and Roberts, 1983). Some Fusarium species are associated with insects, and some are reported to be entomopathogens (Barson, 1976; Majumdar et al., 2008). Except for a report by Navarro et al. (2014) that F. oxysporum might regulate Heterorhabditis sonorensis populations and reduce their survival, all research with respect to nematodes and Fusarium spp. has involved plant parasitic nematodes (Hallmann and Sikora, 1994; Siddiqui and Shaukat, 2003).
In two field surveys, high proportions of Galleria mellonella L. (Lepidoptera: Pyralidae) sentinel larval cadavers were infected by Fusarium solani without evidence of concomitant entomopathogenic nematode (EPN) or entomopathogenic fungus (EPF) reproduction. Because F. solani is not considered entomopathogenic, the survey suggested the possibility that F. solani competes with EPNs. We tested the hypotheses that F. solani attracts the EPN, Steinernema diaprepesi, to facilitate infection of Diaprepes root weevils (Diaprepes abbreviatus L.) and thereafter competes with the nematode in the insect cadaver. In two-choice olfactometer assays where one side was treated with F. solani mycelia and conidia, juvenile S. diaprepesi were attracted to the fungus, in either raw soil, or in autoclaved soil in the presence or absence of insects. However, this attraction was attenuated as the habitat became more complex, by using raw soil in combination with insect larvae. Fusarium oxysporum did not recruit the nematode. When soil microcosms were tested with F. solani conidia and S. diaprepesi, the concomitant infection increased the mortality of the insect (P = 0.02) to 83%, compared to 58% and 0% mortality when nematodes or fungi were individually applied, respectively. Concomitant inoculation also increased the number of cadavers that supported nematode reproduction and increased the population density of fungus in soil. The number of IJs entering the host insect was not affected by F. solani. These results support the possibility that F. solani can facilitate the insecticidal efficiency of S. diaprepesi in order to exploit the resources in the cadaver.
Fipronil enhanced natural occurrence of Fusarium solani (Hypocreales: Nectriaceae) on building infesting termite Heterotermes indicola Wasmann (Blattodea: Rhinotermitidae)
2018, Journal of Asia-Pacific Entomology
Citation Excerpt :
Sacc species (Roy et al., 2008; Strasser et al., 2010; Fernandes et al., 2012; Hatting, 2012). Among these species, F. solani is a naturally occurring pathogen and its virulence has been assessed against sugar beet root maggot pupae (Diptera), lepidopterans, coleopterans, homopterans, cockroaches (Blattodea), scorpions (Arachnida) and crustaceans (Teetor-Barsch and Roberts, 1983; Hose et al., 1984; Majumdar et al., 2008; Sun and Liu, 2008). This pathogenic infection in insects is established by conidia that contact with cuticle, germinate in favorable conditions and emit germ tube to invade the body through penetration.
The Southeast Asian subterranean termite, Heterotermes indicola Wasmann (Blattodea; Rhinotermitidae), is recognized as a building infesting lower termite species in urban environment. The extensive use of chemical termiticides against aerial mud tubes and underground nests of H. indicola beneath the buildings could not suppress its infestation; however, it enhanced the environmental contamination and insecticide resistance. In the present study, we tried to control termites using naturally occurring entomopathogenic fungi Fusarium solani (Mart.) Sacc., along with sublethal concentrations of termiticide fipronil in no-choice feeding pathogenecity bioassay for 20 days. Termite mortality after 20 days of continuous exposure to highest fungal treatment 1 × 10⁹ conidia/mL was 10% exclusively, whereas 100% mortality was calculated just after 16 days of concurrently exposure to 5 ppm of fipronil and highest rate of fungus 1 × 10⁹ conidia/mL. These results indicated that insecticidal stress declined the immune response of termites and reduced the repellency of termites against fungal conidia by breaching the primary defense mechanism (allogrooming). This co-application of F. solani at suitable sublethal concentrations of fipronil showed the promising potential against termites that may reduce the selection pressure of pesticides and resistance risk by targeted pests, but further investigations are necessary for developing field trials.

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Journal of Invertebrate Pathology

Abstract

Introduction

Section snippets

Prevalence study—2004

Results

Discussion

Acknowledgements

References (25)

Fungi: hyphomycetes

Lethal effects of Beauveria bassiana, Metarhizium anisopliae, and Paecilomyces fumosoroseus on the eggs of Tetranychus cinnabarinus (Acari: Tetranychidae) with a description of a mite egg bioassay system

Biol. Control.

A method of computing the effectiveness of an insecticide

J. Econ. Entomol.

Genetic variability within Fusarium solani species as revealed by PCR-fingerprinting based on PCR markers

Braz. J. Microbiol.

Control of sugarbeet root maggot with the fungus Metarhizium anisopliae

J. Sugar Beet Res.

Grower-adoptable formulations of the entomopathogenic fungus Metarhizium anisopliae (Ascomycota: Hypocreales) for sugarbeet root maggot (Diptera: Ulidiidae) management

Environ. Entomol.

Choosing and Using Statistics: A Biologist’s Guide

Statistical Methods in Biological Assay

Epidemiological concepts applied to insect epizootiology

Occurrence of Fusarium oxysporum Schlecht and its pathogenicity on guava scale Chloropulvinaria psidii Maskell (Hemiptera: Coccidae)

Curr. Sci.

Isolation of beauvericin as an insect toxin from Fusarium semitectum and Fusarium moniliforme var. subglutinans

Mycopathologia

Life history of the sugar-beet root maggot Tetanops myopaeformis (Röder) (Diptera: Otitidae) in southern Alberta

Can. Entomol.

Cited by (35)

Recruitment of an insect and its nematode natural enemy by olfactory cues from a saprophytic fungus

Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects

Isolation and structural elucidation of antifungal compounds from Ryudai gold (Curcuma longa) against Fusarium solani sensu lato isolated from American manatee

Phytochemical investigation and biological activities of Fusarium SP. An entomogenous fungus

The saprophytic fungus Fusarium solani increases the insecticidal efficacy of the entomopathogenic nematode Steinernema diaprepesi

Fipronil enhanced natural occurrence of Fusarium solani (Hypocreales: Nectriaceae) on building infesting termite Heterotermes indicola Wasmann (Blattodea: Rhinotermitidae)