The Open Plant Science Journal




(Discontinued)

ISSN: 1874-2947 ― Volume 11, 2019
RESEARCH ARTICLE

Compatibility of the Entomopathogenic Fungus Beauveria bassiana with Some Fungicides Used in California Strawberry



Surendra K. Dara*
University of California Cooperative Extension, 2156 Sierra Way, Ste C, San Luis Obispo, CA 93401, USA

Abstract

Background:

Entomopathogenic fungus Beauveria bassiana is pathogenic to several arthropod pests of strawberry in California and an important part of integrated pest management choices. However, fungicides applied for managing foliar and fruit diseases could interfere with the efficacy of B. bassiana.

Objective:

To determine the compatibility of some commonly used fungicides in strawberry with B. bassiana.

Method:

Laboratory assays were conducted using the larvae of the yellow mealworm, Tenebrio molitor. Mortality and infection caused by B. bassiana in T. molitor was compared in the presence and absence of seven fungicides that have different modes of action.

Result:

Mortality T. molitor larvaedue to B. bassiana was significantly affected in the presence of fungicides, myclobutanil (Rally) and captan (Captan). A significant reduction in the infection also occurred in the presence of captan, myclobutanil, and sulfur (Microthiol Disperss). Fenhexamid (Elevate) and pyraclostrobin + boscalid (Pristine) were the most compatible fungicides.

Conclusion:

Using certain fungicides with B. bassiana can be detrimental to the efficacy of the latter. However, certain fungicides are compatible with B. bassiana. These results help identify appropriate fungicides to be used when B. bassiana is applied for pest management.

Keywords: Beauveria bassiana, Fungicide, Compatibility, Strawberry.


Article Information


Identifiers and Pagination:

Year: 2017
Volume: 10
First Page: 29
Last Page: 34
Publisher Id: TOPSJ-10-29
DOI: 10.2174/1874294701710010029

Article History:

Received Date: 28/10/2016
Revision Received Date: 11/01/2017
Acceptance Date: 25/01/2017
Electronic publication date: 30/05/2017
Collection year: 2017

© 2017 Surendra K. Dara.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the University of California Cooperative Extension, 2156 Sierra Way, Ste C, San Luis Obispo, CA 93401, USA; Tel: 805-720-1700; Fax: 805-781-4316; E-mail: skdara@ucdavis.edu




INTRODUCTION

Several arthropod pests infest strawberry crop in California and cause a significant yield loss according to Zalom, Bolda, Dara, and Joseph [1Zalom FG, Bolda MP, Dara SK, Joseph S UC. UC IPM pest management guidelines: strawberry. University of California statewide integrated pest management program. Oakland: UC ANR Publication 3468 2014.]. Strawberry is an important commercial crop and the annual report from California Department of Pesticide Regulations [2California Department of Pesticide Regulation (CDPR) Summary of pesticide use report data 2014: indexed by commodity 2016. Available at: http://www.cdpr.ca.gov/docs/pur/pur14rep/comrpt14.pdf] indicates that large quantities of acaricides, fungicides, herbicides, and insecticides are applied to manage a variety of pests. Chemical acaricides and insecticides are mainly applied to manage the twospotted spider mite, Tetranychus urticae Koch and the western tarnished plant bug, Lygus hesperus Knight. Dara [3Dara SK. Twospotted spider mite and its management in strawberries. CAPCA Adviser 2015; 18(4): 56-8.-5Dara SK. Managing strawberry pests with chemical pesticides and non-chemical alternatives. Int J Berry Sci 2016; 1-13.
[http://dx.doi.org/10.1080/15538362.2016.1195311]
] demonstrated that entomopathogenic fungi such as Beauveria bassiana (Balsamo) Vuillemin, Isaria fumosorosea Wize, and Metarhizium brunneum Petch. can play an important role in integrated pest management (IPM) and promote sustainable agriculture. However, growers frequently apply fungicides to manage foliar and fruit diseases and the potential negative impact of these fungicides on the efficacy of entomopathogenic fungi is a concern for using these beneficial fungi for arthropod pest management. Sulfur and captan are the most widely used fungicides and in general, fungicide use surpasses that of acaricides and insecticides in California strawberries [2California Department of Pesticide Regulation (CDPR) Summary of pesticide use report data 2014: indexed by commodity 2016. Available at: http://www.cdpr.ca.gov/docs/pur/pur14rep/comrpt14.pdf]. Earlier studies by Moorhouse, Gillespie, Seller, and Charnley [6Moorhouse ER, Gillespie AT, Sellers EK, Charnley AK. Influence of fungicides and insecticides on the entomogenous fungus Metarhizium anisopliae, a pathogen of the vine weevil, Otiorhynchus sulcatus. Biocon Sci Tech 1992; 2(1): 49-58.
[http://dx.doi.org/10.1080/09583159209355217]
], Jaros-Su, Groden, and Zhang [7Jaros-Su J, Groden E, Zhang J. Effects of selected fungicides and the timing of fungicide application on Beauveria bassiana-induced mortality of the Colorado potato beetle (Coleoptera: Chrysomelidae). Biol Con 1999; 15(3): 259-69.
[http://dx.doi.org/10.1006/bcon.1999.0724]
], Luz, Netto, and Rocha [8Luz C, Netto MC, Rocha LF. In vitro susceptibility to fungicides by invertebrate-pathogenic and saprobic fungi. Mycopathologia 2007; 164(1): 39-47.
[http://dx.doi.org/10.1007/s11046-007-9020-0] [PMID: 17574540]
], and Brook [9Bruck DJ. Impact of fungicides on Metarhizium anisopliae in the rhizosphere, bulk soil and in vitro. BioControl 2009; 54(4): 597-606.
[http://dx.doi.org/10.1007/s10526-009-9213-1]
] evaluated the impact of some fungicides on the fungal growth and pest control efficacy of B. bassiana or other entomopathogenic fungi through invitro or potted plant studies in multiple crop or pest situations. However, no information specific to the fungicides used in California strawberries is available, especially after the release of some new fungicides in the recent years.

A laboratory study was conducted in 2012 to evaluate the compatibility of B. bassiana with seven fungicides that are commonly used in California strawberries. Results are expected to generate information to help growers make appropriate treatment decisions while choosing fungicides for disease management and B. bassiana for arthropod pest management in strawberry and other crops where these fungicides are used.

MATERIALS AND METHODS

The larvae of the yellow mealworm, Tenebrio molitor L. were used as the host insects to evaluate the pathogenicity of B. bassiana alone and in the presence of fungicides. A total of nine treatments including an untreated control were assessed in the study (Table 1). Medium sized T. molitor larvae of about 20 mm long were ordered from a commercial supplier (Fluker Farms, Port Allen, LA, USA) and kept at room temperature (26-27 oC) for two days prior to using them in the assay. Using the field application rates, 250 ml of each treatment liquid was prepared using deionized water and poured into separate spray bottles.

Table 1
List of treatments with active ingredients, Fungicide Resistance Action Committee (FRAC) mode of action groups, and field application rates.


One gallon plastic tubs with screening on the lid were used for treating T. molitor larvae. A clean paper towel was placed in the bottom of the tub and sprayed with about 5 ml of the respective fungicides in treatments [3Dara SK. Twospotted spider mite and its management in strawberries. CAPCA Adviser 2015; 18(4): 56-8.-9Bruck DJ. Impact of fungicides on Metarhizium anisopliae in the rhizosphere, bulk soil and in vitro. BioControl 2009; 54(4): 597-606.
[http://dx.doi.org/10.1007/s10526-009-9213-1]
]. Deionized water was used for the untreated control. Paper towels were allowed to dry before applying 5 ml of B. bassiana (Mycotrol-O). A carrot piece, approximately 3 cm long, was cut further into small pieces and placed in one end of the tub. Forty uniformly sized T. larvae were placed at the other end of the tub on the treated paper towel allowing them to crawl towards the food source and get more exposure to the treated surface. After a 24-hour exposure to the inoculum, larvae were transferred individually to 5 dram Plexiglas vials with the help of forceps. Each vial had a small piece of carrot and the larva was secured inside by covering the vial with a foam plug. Larvae were incubated at room temperature (26-27 oC), mortality was recorded daily for seven days, and additional pieces of carrots were placed as needed.

To determine the level of infection, cadavers of the larvae were surface sterilized in 3% sodium hypochlorite solution followed by rinsing in deionized water and incubating on a selective medium (oatmeal agar amended with dodine and crystal violet, according to Chase, Osborne, and Ferguson [10Chase AR, Osborne LS, Ferguson VM. Selective isolation of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae from an artificial potting medium. Fla Entomol 1986; 69(2): 285-92.
[http://dx.doi.org/10.2307/3494930]
]). Surface sterilization ensures that B. bassiana emerging from the cadavers is due to the infection and not saprophytic growth on the surface. Not all insects killed by the fungus show symptoms of infection and the level of infection measured in the study represents fungal sporulation from the cadavers.

Assays were repeated six times over a period of about 3 months. Data were analyzed using one-way analysis of variance. Percent mortality and infection were subjected to arcsine transformation and significant means were separated using Tukey’s HSD test.

RESULTS AND DISCUSSION

There was a significant difference (P < 0.00001) in the mortality and infection caused by B. bassiana (Mycotrol-O) in the presence of various fungicides (Fig. 1). Effect of the assay on the treatments was not statistically significant (P > 0.1). Most of the mortality occurred between 4 and 5 days after the larvae were incubated individually in the vials (Fig. 2). Captan (Captan) and myclobutanil (Rally) severely affected the mortality in T. molitor larvae, which was significantly less than the mortality caused by B. bassiana alone. Pyraclostrobin + boscalid (Pristine) and fenhexamid (Elevate) were the most compatible where B. bassiana caused 93 and 86% mortality, respectively, which was higher than 70% mortality caused by B. bassiana alone. The negative impact of cyprodinil + fludioxonil (Switch) and sulfur (Microthiol Disperss) was moderate compared to others.

Fig. (1)
Mortality and infection caused by Beauveria bassiana in Tenebrio molitor in the absence and presence of different fungicides. Bars with the same letters (lowercase for mortality and uppercase for infection) are not significantly different using Tukey’s HSD test (P < 0.00001).


When infection was compared, captan (~5%) and myclobutanil (~12%) had the highest impact followed by sulfur (~28%). The highest level of B. bassiana infection occurred in the presence of pyraclostrobin + boscalid (~85%) and fenhexamid (~80%). Infection from B. bassiana alone was about 66%. While mortality of the target pest is the primary objective in pest management, sporulation from the infected cadavers could help spread the inoculum in the crop habitat and promote longer control. So, the impact of fungicides on B. bassiana infection is also an important aspect to consider.

Jaros-Su, Groden, and Zhang [7Jaros-Su J, Groden E, Zhang J. Effects of selected fungicides and the timing of fungicide application on Beauveria bassiana-induced mortality of the Colorado potato beetle (Coleoptera: Chrysomelidae). Biol Con 1999; 15(3): 259-69.
[http://dx.doi.org/10.1006/bcon.1999.0724]
] studied the compatibility of B. bassiana with some fungicides used for potato disease management. They found out that copper hydroxide fungicide was less harmful to B. bassiana than chlorothalonil and mancozeb. These fungicides have multi-site contact activity against fungi, but differed in their compatibility with B. bassiana. Interaction between the fungicides and B. bassiana, and the resulting mortality of the Colorado potato beetle, Leptinotarsa decemlineata (Say) varied depending on application rates, intervals, and other factors. An earlier study by Loria, Galaini, and Roberts [11Loria R, Galaini S, Roberts DW. Survival of inoculum of the entomopathogenic fungus Beauveria bassiana as influenced by fungicides. Environ Entomol 1983; 12(6): 1724-6.
[http://dx.doi.org/10.1093/ee/12.6.1724]
] also reported the detrimental effect of mancozeb and metiram on B. bassiana. Chlorothalonil, which has a similar mode of action as mancozeb and metiram, and metalaxyl, which affects RNA polymerase were not harmful to B. bassiana.

Fig. (2)
Mean cumulative daily mortality in Tenebrio molitor caused by Beauveria bassiana in the absence and presence of difference fungicides.


In a more recent study, Shah, Ansari, Watkins, Phelps, Cross, and Butt [12Shah FA, Ansari MA, Watkins J, Phelps Z, Cross J, Butt TM. Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocon Sci Tech 2009; 19(7): 743-53.
[http://dx.doi.org/10.1080/09583150903100807]
] evaluated the effect of 15 fungicides on the conidial germination, mycelial growth, and virulence of B. bassiana, I. fumosorosea, Lecanicillium longisporum (Petch) Zare & Gams, and M. anisopliae (Metchnikoff) Sorokin. Some of these fungicides are similar to the ones used in the current study. Shah et al. infected the larvae of the waxmoth, Gallaria mellonella (L.) with commercial formulations of the entomopathogenic fungi and used single spore cultures from the cadavers in the study. Virulence of B. bassiana was not affected by any of the 15 fungicides, but conidial germination and mycelial growth were affected to varying levels. Compared to 100% conidial germination in the absence of any fungicides, there was 84, 80, 66, 37, 0, 0, and 0% germination in the presence of the label rates of quinoxyfen, azoxystrobin, fenhexamid, pyrimethanil, sulfur, myclobutanil, and captan, respectively. Mycelial growth was 1.04, 1.11, 1.92, 1.95, 1.96, 1.97, and 2.18 mm in the presence of myclobutanil, azoxystrobin, fenhexamid, captan, sulfur, pyrimethanil, and quinoxyfen, respectively, compared to 2.93 mm in the absence of any fungicide. In the current study, pyraclostrobin, (one of the active ingredients of Pristine) is similar to azoxystrobin, and cyprodinil (one of the active ingredients of Switch) is similar to pyrimethanil, which were used by Shah et al.

There are some variations between findings of the current study and those of Shal et al.’s. However, the highly negative impact of captan (Captan), myclobutanil (Rally), and sulfur (Microthiol Disperss) and the moderate impact of quinoxyfen (Quintec) in the current study were similar to what Shah et al. observed for conidial germination and mycelial growth. While fenhexamid moderately affected B. bassiana in Shah et al.’s study, it (Elevate) had no such impact in the current study. Shah et al. [12Shah FA, Ansari MA, Watkins J, Phelps Z, Cross J, Butt TM. Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocon Sci Tech 2009; 19(7): 743-53.
[http://dx.doi.org/10.1080/09583150903100807]
] reported variation in the inhibitory effect of the fungicides on different fungi. While captan appears to be detrimental to multiple entomopathogenic fungi, strobilurin fungicides, azoxystrobin and pyraclostrobin seem to be compatible with B. bassiana, but not with Metarhizium spp [9Bruck DJ. Impact of fungicides on Metarhizium anisopliae in the rhizosphere, bulk soil and in vitro. BioControl 2009; 54(4): 597-606.
[http://dx.doi.org/10.1007/s10526-009-9213-1]
, 12Shah FA, Ansari MA, Watkins J, Phelps Z, Cross J, Butt TM. Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocon Sci Tech 2009; 19(7): 743-53.
[http://dx.doi.org/10.1080/09583150903100807]
].

Kouassi, Coderre, and Todorova [13Kouassi M, Coderre D, Todorova SI. Effects of the timing of applications on the incompatibility of three fungicides and one isolate of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Deuteromycotina). J Appl Ent 2003; 127(7): 421-6.
[http://dx.doi.org/10.1046/j.1439-0418.2003.00769.x]
] evaluated the timing between the application of B. bassiana and metalaxyl, mancozeb, and cooper oxide against the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois). These fungicides inhibited the growth of B. bassiana in vitro and reduced the mortality of L. lineolaris when applied with or 2-4 days before the application of fungus. Compared to 84% mortality caused by B. bassiana alone, the mortality was 20, 25, and 30% from metalaxyl, mancozeb, and copper oxide, respectively, when they were applied 2-4 days earlier. These results are somewhat different from those observed by Jaros-Su, Groden, and Zhang [7Jaros-Su J, Groden E, Zhang J. Effects of selected fungicides and the timing of fungicide application on Beauveria bassiana-induced mortality of the Colorado potato beetle (Coleoptera: Chrysomelidae). Biol Con 1999; 15(3): 259-69.
[http://dx.doi.org/10.1006/bcon.1999.0724]
] and Loria, Galaini, and Roberts [11Loria R, Galaini S, Roberts DW. Survival of inoculum of the entomopathogenic fungus Beauveria bassiana as influenced by fungicides. Environ Entomol 1983; 12(6): 1724-6.
[http://dx.doi.org/10.1093/ee/12.6.1724]
] with metalaxyl, mancozeb, and copper hydroxide. However, Kouassi, Coderre, and Todorova [13Kouassi M, Coderre D, Todorova SI. Effects of the timing of applications on the incompatibility of three fungicides and one isolate of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Deuteromycotina). J Appl Ent 2003; 127(7): 421-6.
[http://dx.doi.org/10.1046/j.1439-0418.2003.00769.x]
] found that application of fungicides 2-4 days after the insects were treated with B. bassiana had a synergistic effect in the case of metalaxyl and copper oxide due to the insecticidal effect of these fungicides. The time interval of 2-4 days allowed B. bassiana infections in L. lineolaris along with additional mortality caused by the insecticidal effect of the fungicides.

Strobilurin fungicides are very popular and widely used in cropping systems around the world as reported by Bartlett, Clough, Godwin, Hall, Hamer, and Parr-Dobrzanski [14Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B. The strobilurin fungicides. Pest Manag Sci 2002; 58(7): 649-62.
[http://dx.doi.org/10.1002/ps.520] [PMID: 12146165]
]. Their compatibility with B. bassiana, as demonstrated in the current or other studies, is promising for the use of B. bassiana for pest management in cropping systems where such fungicides are used against plant pathogens. This is the first study evaluating the compatibility of B. bassiana with some of the fungicides commonly used in California strawberries. However, as some of these fungicides are used on other crops, these results are applicable wherever these fungicides are used. Results promote sustainable agriculture by providing an opportunity to use a non-chemical alternative to chemical insecticides or acaricides and address the concern of growers in selecting appropriate fungicides while using B. bassiana. Additional studies with other fungicides and different application intervals between B. bassiana and fungicides would be more useful to further evaluate their compatibility.

CONFLICT OF INTEREST

The author confirms that this article content has no conflict of interest.

ACKNOWLEDGEMENTS

Thanks to the technical assistance of Thomas Crottogini in conducting the assays.

REFERENCES

[1] Zalom FG, Bolda MP, Dara SK, Joseph S UC. UC IPM pest management guidelines: strawberry. University of California statewide integrated pest management program. Oakland: UC ANR Publication 3468 2014.
[2] California Department of Pesticide Regulation (CDPR) Summary of pesticide use report data 2014: indexed by commodity 2016. Available at: http://www.cdpr.ca.gov/docs/pur/pur14rep/comrpt14.pdf
[3] Dara SK. Twospotted spider mite and its management in strawberries. CAPCA Adviser 2015; 18(4): 56-8.
[4] Dara SK. IPM solutions for insect pests in California strawberries: efficacy of botanical, chemical, mechanical, and microbial options. CAPCA Adviser 2016a; 19(2): 40-6.
[5] Dara SK. Managing strawberry pests with chemical pesticides and non-chemical alternatives. Int J Berry Sci 2016; 1-13.
[http://dx.doi.org/10.1080/15538362.2016.1195311]
[6] Moorhouse ER, Gillespie AT, Sellers EK, Charnley AK. Influence of fungicides and insecticides on the entomogenous fungus Metarhizium anisopliae, a pathogen of the vine weevil, Otiorhynchus sulcatus. Biocon Sci Tech 1992; 2(1): 49-58.
[http://dx.doi.org/10.1080/09583159209355217]
[7] Jaros-Su J, Groden E, Zhang J. Effects of selected fungicides and the timing of fungicide application on Beauveria bassiana-induced mortality of the Colorado potato beetle (Coleoptera: Chrysomelidae). Biol Con 1999; 15(3): 259-69.
[http://dx.doi.org/10.1006/bcon.1999.0724]
[8] Luz C, Netto MC, Rocha LF. In vitro susceptibility to fungicides by invertebrate-pathogenic and saprobic fungi. Mycopathologia 2007; 164(1): 39-47.
[http://dx.doi.org/10.1007/s11046-007-9020-0] [PMID: 17574540]
[9] Bruck DJ. Impact of fungicides on Metarhizium anisopliae in the rhizosphere, bulk soil and in vitro. BioControl 2009; 54(4): 597-606.
[http://dx.doi.org/10.1007/s10526-009-9213-1]
[10] Chase AR, Osborne LS, Ferguson VM. Selective isolation of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae from an artificial potting medium. Fla Entomol 1986; 69(2): 285-92.
[http://dx.doi.org/10.2307/3494930]
[11] Loria R, Galaini S, Roberts DW. Survival of inoculum of the entomopathogenic fungus Beauveria bassiana as influenced by fungicides. Environ Entomol 1983; 12(6): 1724-6.
[http://dx.doi.org/10.1093/ee/12.6.1724]
[12] Shah FA, Ansari MA, Watkins J, Phelps Z, Cross J, Butt TM. Influence of commercial fungicides on the germination, growth and virulence of four species of entomopathogenic fungi. Biocon Sci Tech 2009; 19(7): 743-53.
[http://dx.doi.org/10.1080/09583150903100807]
[13] Kouassi M, Coderre D, Todorova SI. Effects of the timing of applications on the incompatibility of three fungicides and one isolate of the entomopathogenic fungus Beauveria bassiana (Balsamo) Vuillemin (Deuteromycotina). J Appl Ent 2003; 127(7): 421-6.
[http://dx.doi.org/10.1046/j.1439-0418.2003.00769.x]
[14] Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B. The strobilurin fungicides. Pest Manag Sci 2002; 58(7): 649-62.
[http://dx.doi.org/10.1002/ps.520] [PMID: 12146165]

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