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

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Review

Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects Ana Carla da Silva SANTOS*, Athaline Gonc¸alves DINIZ, Patricia Vieira TIAGO, Neiva Tinti de OLIVEIRA Departamento de Micologia, Universidade Federal de Pernambuco, Av. Professor Moraes Rego 1235, Cidade
ria, Recife, Pernambuco, 50670-901, Brazil Universita

article info

abstract

Article history:

The genus Fusarium is noted for including important plant pathogens and mycotoxin pro-

Received 19 February 2019

ducers. Furthermore, many Fusarium lineages have been reported to be efficient in con-

Received in revised form

trolling insects and to exhibit promising characteristics for agricultural pest control

5 December 2019

such as causing high mortality rates and having fast action and abundant sporulation.

Accepted 6 December 2019

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

Keywords:

was made using search strings in a number of databases. We list the major complexes

Biocontrol

and species of Fusarium reported as entomopathogenic and highlight the features of inter-

Entomopathogenic fungi

est for insect control as well as the advantages and implications of this practice. Out of a

Fusarium fujikuroi species complex

total of forty papers, at least 30 species and 273 isolates of Fusarium were reported as

Fusarium incarnatum-Equiseti species

pathogenic to at least one species of insect. Ten complexes of Fusarium species harbor en-

complex

tomopathogenic fungi, of which F. incarnatum-equiseti, F. fujikuroi, F. oxysporum and F.

Fusarium oxysporum species complex

solani (¼ Neocosmospora solani) species complexes represented the most abundant number

Fusarium solani species complex

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. ª 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved.

1.

Introduction

Fusarium is a ubiquitous genus in nature with representatives found in the soil and in various other substrates such as

decomposing organic matter or in pathogenic or nonpathogenic associations with animals, plants and other organisms (Summerell et al., 2010; Walsh et al., 2010; Aoki, O’Donnell and Geiser, 2014; Sharma and Marques, 2018;

* Corresponding author. E-mail address: [email protected] (A. C. S. Santos). https://doi.org/10.1016/j.fbr.2019.12.002 1749-4613/ª 2019 British Mycological Society. Published by Elsevier Ltd. All rights reserved.

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

2

Torbati et al., 2018). Due to the importance of these fungi as plant pathogens and mycotoxin producers, most studies over more than 200 y of history have focused on isolates obtained from economically important diseased plants in commercial agricultural settings (Summerell and Leslie, 2011). However, other habitats and hosts, including natural ecosystems and diversified agroecosystems (Walsh et al., 2010; Leslie and Summerell, 2011; Laurence et al., 2015), clinical and veterinary samples (O’Donnell et al., 2010; Van Diepeningen et al., 2014; O’Donnell et al. 2016a) and insects (Freeman et al., 2013a, 2013b; Kasson et al. 2013; Aoki et al., 2018, 2019) have also been shown to be important sources for the investigation of Fusarium species. As these species are studied, the knowledge about the phylogeny, interactions and survival strategies deployed by Fusarium in ecosystems increases and becomes more amenable to practical exploitation (Summerell et al., 2010; Leslie and Summerell, 2011; Laurence et al., 2015). Fusarium and other well-established plant pathogenic genera have the ability to switch between different life style stages (Van Kan et al., 2014; De Silva et al., 2017) and to act on non-plant hosts (Perez-Nadales et al., 2014; Van Diepeningen and De Hoog, 2016), including several animals (O’Donnell et al., 2012, 2016a) and even other fungi (Torbati et al., 2018). Among animals, insects are most abundantly associated with Fusarium species. The reports of insectassociated Fusarium species published in the 50’s, 60’s and 70’s culminated in the publication in the early 80’s of a literature review concerning non-pathogenic and pathogenic relationships between Fusarium and insects (Teetor-Barsch and Roberts, 1983). Although these reports are not recent, it is only in the last few years that they have received serious attention. The investigation of Fusarium in insects has led to the discovery of new species (Freeman et al., 2013b; Aoki et al., 2018, 2019; Santos et al., 2019) and of several interesting interactions between Fusarium and insects (Freeman et al., 2013a; Kasson et al., 2013; O’Donnell et al., 2016b; Toki et al., 2016) demonstrating that fungi often solely studied as plant pathogens play additional roles in nature for which we do not know the ecological significance. Of the Fusarium-insect associations, those that are pathogenic have been highlighted by an increasing number of studies demonstrating the potential of little known and little explored Fusarium species as biological control agents of insects (see Table 1). However, the utilization of Fusarium species for the biological control of agriculturally important pest insects and as novel sources of insecticidal compounds has been limited in part due to the concern of inadvertently releasing phytopathogens and their toxins into the environment (O’Donnell et al., 2012). This concern is intensified by the fact that the identification and delimitation of Fusarium species is difficult, requiring a polyphasic approach integrating morphological, biological and phylogenetic markers for accurate identification (Summerell and Leslie, 2011). This is because morphological species recognition (MSR) historically used for identification of Fusarium species has been shown to be limited and has given rise to conflicting taxonomic schemes that greatly underestimate species diversity within the genus (Geiser et al., 2004; Leslie and Summerell, 2006; O’Donnell et al., 2010; Burgess, 2014).

A. C. da S. Santos et al.

On the other hand, although few investigations have been conducted in order to determine the spectrum of action of the entomopathogenic Fusarium species, studies have shown that some Fusarium isolates that caused high mortality to insects also showed specificity to the host and safe to the crop plants, since the ability to parasitize requires specific adaptations to the host (Kuruvilla and Jacob, 1980; Teetor-Barsch and Roberts, 1983; Mikunthan and Manjunatha, 2006; Lazo, 2012; Fan et al., 2014). In addition, molecular phylogenetic methods have better defined relationships between Fusarium species and become more accessible (Geiser et al., 2004; Watanabe et al., 2011). Thus, further investigation regarding the Fusarium species that attack insects should be conducted in order to improve our understanding of the host-Fusarium-environment interactions and use of these microorganisms of agronomic interest. In this review, we provide a survey of the main pathogenic species to insects and indicate the species complexes richest in entomopathogenic Fusarium lineages. We address the major topics concerning the use of entomopathogenic Fusarium species as biological control agents of insect pests, highlighting in this group the features of interest for insect control and advantages and challenges to apply these fungi in biological control.

2. Fusarium: contextualizing this versatile group of fungi The Fusarium (Nectriaceae, Hypocreales) group is remarkable for several reasons, including its genetic diversity, its wide geographic distribution and abundance in natural ecosystems and the diversity of its relationships with other organisms (Summerell and Leslie, 2011; Burgess, 2014; Torbati et al., 2018). However, this genus is known primarily for its roles as plant pathogens and as mycotoxin producers (Summerell and Leslie, 2011; O’Donnell et al., 2018). At least 80% of cultivated plant species are associated with a disease caused by a species of Fusarium (Leslie and Summerell, 2006), some of which cause devastating economic and sociological impacts for farmers and communities dependent on affected crops (Summerell and Leslie, 2011). Mycotoxins produced by Fusarium can contaminate food and feed and cause both acute and chronic toxic effects to humans and other animals, in a magnitude dependent on the mycotoxin type and the level and duration of exposure (Antonissen et al., 2014; O’Donnell et al., 2018). Beyond being toxic and/or carcinogenic and causing even death in case of prolonged exposure, these metabolites may have a role in plant disease, and may need to be regulated in commercial and international trade (Kvas et al., 2009; Summerell and Leslie, 2011). Fusarium has also emerged as a clinical and veterinary interest group (Van Diepeningen et al., 2014; O’Donnell et al., 2016a), responsible for infections that in humans range from superficial to life-threatening, deep and disseminated infections. The latter predominantly affects immunocompromised individuals in whom mortality approaches 100% (Wang et al., 2011; Van Diepeningen and De Hoog, 2016). Fusarium species have also been associated with animals such as spiders, insects, amphibians and reptiles

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

Species Complex Fusarium chlamydosporum species complex Fusarium fujikuroi species complex

Fusarium species

Target insect species

Type of mortality assessment

Mortality rate

Reference

F. chlamydosporum (4 isolates)

Samples of soil

Galleria mellonella (Lepidoptera: Pyralidae)a

Accumulated mortality in the 12 d

10e20%d

Ameen, (2012)

F. fujikuroi (1 isolate)

Planococcus ficus (Hemiptera: Pseudococcidae)

Mortality

40, 50 and 70% for each insect, respectively

Sharma et al., (2018)

F. moniliforme ¼ F. verticillioides (1 isolate) F. moniliforme ¼ F. verticillioides (1 isolate) F. moniliforme ¼ F. verticillioides (7 isolates) F. moniliforme [ F. verticillioides (1 isolate) F. nygamai (1 isolate)

Soil samples using a “Galleria bait method” Dalbulus maidis (Hemiptera: Cicadellidae) Samples of soil

Planococcus f
ıcus (Hemiptera: Pseudococcidae); Tenebrio molitor (Coleoptera: Tenebrionidae) Galleria mellonella (Lepidoptera: Pyralidae)b Galleria mellonella (Lepidoptera: Pyralidae)c Trialeurodes vaporariorum (Hemiptera: Aleyrodidae)b Galleria mellonella (Lepidoptera: Pyralidae)a

Accumulated mortality in 6 d Total mortality

30%

Accumulated mortality in 12 d

13e56%d

Ali-Shtayeh, Mara’I and Jamous, (2003)
n et al., Torres-Barraga (2004) Ameen, (2012)

Bemisia tabaci (Hemiptera: Aleyrodidae) Acythopeus curvirostris (Coleoptera: Curculionidae)

Bemisia tabaci (Hemiptera: Aleyrodidae)b Acythopeus curvirostris (Coleoptera: Curculionidae)b

Corrected mortality

42e76.7%f

Sain et al., (2019)

Total mortality

Sepasi et al., (2015)

F. proliferatum (2 isolates)

Zea mays

Schizaphis graminum (Hemiptera: Aphididae)a

Mortality per hour for 24 h

F. proliferatum (1 isolate)

Total mortality

97 and 100%

Tosi et al., (2015)

Total mortality

40%

Chehri, (2017)

F. proliferatum (1 isolate)

Unknown

Al-Ani et al., (2018)

Samples of soil

13 and 26%

Ameen, (2012)

F. subglutinans(1 isolate)

Aphis gossypii (Hemiptera: Aphididae) Tropidacris collaris (Orthoptera: Romaleidae) Soil samples using a “Galleria bait method”

Accumulated mortality in 20 d Accumulated mortality in 12 d Corrected total mortality Accumulated mortality in 10 d Accumulated mortality in 10 d

74.01%

F. sacchari (2 isolates)

Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae)b Dryocosmus kuriphilus (Hymenoptera: Cynipidae)b Tribolium confusum (Coleoptera: Tenebrionidae)c Tribolium confusum (Coleoptera: Tenebrionidae)a Galleria mellonella (Lepidoptera: Pyralidae)a Frankliniella occidentalis (Thysanoptera: Thripidae)a Ronderosia bergi (Orthoptera: Acrididae)b Galleria mellonella. (Lepidoptera: Pyralidae)c

Accumulated mortality in 6 d

F. proliferatum (2 isolates) F. proliferatum (1 isolate)

Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) Dryocosmus kuriphilus (Hymenoptera: Cynipidae) Unknown

83 and 62% for larvae and adult, respectively 83e99, 70e86 and 26e96%d for wingless, nymphs and larvae, respectively 100%

15.5e90.9f

€ zer, (2019) Demiro

58%

Pelizza et al., (2011)

18%

Ali-Shtayeh, Mara’I and Jamous, (2003)

F. verticillioides (1 isolate) Fusarium heterosporum species complex

Host/Substrate

F. heterosporum (1 isolate)

96.6%

Entomopathogenic Fusarium species

Ganassi et al., (2001)

Lazo, (2012)

(continued on next page)

3

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

Table 1 e Summary of host insects in which Fusarium species have been reported as entomopathogenic.

4

Species Complex Fusarium incarnatumequiseti species complex

Fusarium species F. equiseti (1 isolate) F. equiseti (1 isolate) F. equiseti (1 isolate) F. equiseti (1 isolate) F. equiseti (3 isolates)

F. incarnatum (1 isolate)

F. incarnatum (1 isolate) F. pallidoroseum ¼ F. incarnatum (1 isolate) F. pallidoroseum ¼ F. incarnatum (1 isolate) F. semitectum ¼ F. incarnatum (7 isolates) F. semitectum ¼ F. incarnatum(2 isolates) F. semitectum ¼ F. incarnatum (1 isolate)

Host/Substrate

Target insect species

Soil samples using a “Galleria bait method” Cephus cinctus (Hymenoptera: Cephidae) Samples of soil

Galleria mellonella (Lepidoptera: Pyralidae)a Cephus cinctus (Hymenoptera: Cephidae)b Galleria mellonella (Lepidoptera: Pyralidae)a Brahmina coriacea (Coleoptera: Scarabaeidae)c Bemisia tabaci (Hemiptera: Aleyrodidae)b

Mortality

Ceratothripoides claratris (Thysanoptera: Thripidae), Pseudococcus cryptus (Hemiptera: Pseudococcidae) and Bemisia tabaci (Hemiptera: Aleyrodidae)b Bemisia tabaci (Hemiptera: Aleyrodidae)b Culex quinquefasciatus (Diptera: Culicidae)c Lymantria obfuscata (Lepidoptera: Lymantridae)b Galleria mellonella (Lepidoptera: Pyralidae)c Ceratovacuna lanigera (Hemiptera: Aphididae)b Myzus persicae (Hemiptera: Aphididae)b Galleria mellonella (Lepidoptera: Pyralidae)a Aphis gossypii (Hemiptera: Aphididae)b

Accumulated mortality in 12 d Accumulated mortality in 6 d

Brahmina coriacea (Coleoptera: Scarabaeidae) Aphis gossypii (Hemiptera: Aphididae), mealybug (Hemiptera) and Bemisia tabaci (Hemiptera: Aleyrodidae) Ceratothripoides claratris (Thysanoptera: Thripidae)

Bemisia tabaci (Hemiptera: Aleyrodidae) Culex quinquefasciatus (Diptera: Culicidae) Lymantria obfuscata (Lepidoptera: Lymantridae) Soil samples using a “Galleria bait method” Ceratovacuna lanigera (Hemiptera: Aphididae) Unknown

Type of mortality assessment

Mortality rate 0%

Sun and Liu, (2008)

mortality

~34e80%e

mortality

16%

Wenda-Piesik et al., (2009) Ameen, (2012)

mortality

21.11%

Sharma et al., (2012)

mortality

100% for nymphs and 0e20% for adultsd,e

Anwar et al., (2017)

Corrected total mortality

0.0, 13.3 and 6.7% for each insect, respectively

Panyasiri et al. (2007)

Accumulated mortality in 144 h Total mortality

100% for nymphs and 0% for adults 4.41e24.97%e

Anwar et al., (2017) Mohanty et al., (2008)

Accumulated in 16 d Accumulated in 5e7 d Accumulated in 15 d Accumulated in 6 d

mortality

13e100%e

Munshi et al., (2008)

mortality

16e33%d,f

mortality

45.73 and 53.14%

Ali-Shtayeh, Mara’I and Jamous, (2003) Aswini et al. (2007)

mortality

18.11e62.66% for adults and 8.66e84.30% for nymphse 10e63%d

Asharani et al., 2009

Jayasimha et al., (2012)

Accumulated in 13 d Accumulated in 12 d Accumulated in 30 d Accumulated in 144 h

F. semitectum ¼ F. incarnatum (7 isolates) F. semitectum ¼ F. incarnatum (1 isolate)

Samples of soil

F. semitectum ¼ F. incarnatum (1 isolate)

Unknown

Amrasca biguttula (Hemiptera: Cicadellidae)b

Accumulated mortality in 6 d

FIESC 3 [ F. compactum (1 isolate) FIESC 16 [ F. sulawesiensis (1 isolate)

Dryocosmus kuriphilus (Hymenoptera: Cynipidae) Dactylopius opuntiae (Hemiptera: Dactylopiidae)

Dryocosmus kuriphilus (Hymenoptera: Cynipidae)b Dactylopius opuntiae (Hemiptera: Dactylopiidae)b

Total mortality

12.07e79.90% for nymph and 12.09e64.40% for adultse 6.67e83.34% for nymphs and 12.86e75.21% for adultse 60%

Confirmed mortalities

~32%

Unknown

Reference

Ameen, (2012)

Jayasimha et al. (2014)

Addario and Turchetti, (2011) ~ o et al., Carneiro-Lea (2017)

A. C. da S. Santos et al.

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

Table 1 (continued )

Dactylopius opuntiae (Hemiptera: Dactylopiidae)b

Confirmed mortalities

~38%

~ o et al., Carneiro-Lea (2017)

Dactylopius opuntiae (Hemiptera: Dactylopiidae)

Dactylopius opuntiae (Hemiptera: Dactylopiidae)b

Confirmed mortalities

8e66.66%d

~ o et al., Carneiro-Lea (2017)

Dactylopius opuntiae (Hemiptera: Dactylopiidae)

Dactylopius opuntiae (Hemiptera: Dactylopiidae)b

Corrected total mortality

75.34e88.98%d

Santos et al., (2016)

Dactylopius opuntiae (Hemiptera: Dactylopiidae)

Dactylopius opuntiae (Hemiptera: Dactylopiidae)b

Corrected total mortality

13.23e73.64%d

Velez et al., (2019)

Dryocosmus kuriphilus (Hymenoptera: Cynipidae)b

Total mortality

70%

Addario and Turchetti, (2011)

FIESC 28 [ F. coffeatum (1 isolate) FIESC species unspecified (1 isolate) FIESC species unspecified (1 isolate)

Dryocosmus kuriphilus (Hymenoptera: Cynipidae) and cynipid gall Dactylopius opuntiae (Hemiptera: Dactylopiidae) Coccus hesperidum(Hemiptera: Coccidae) Coccus hesperidum(Hemiptera: Coccidae)

Confirmed mortalities

~43%

Accumulated total mortality Corrected total mortality

91.33%

~ o et al., Carneiro-Lea (2017) Fan et al., (2014)

F. lateritium (1 isolate)

Soil Sample

F. oxysporum (1 isolate)

Eldana saccharina (Lepidoptera: Pyralidae) Soil samples using a “Galleria bait method” Samples of soil

Dactylopius opuntiae (Hemiptera: Dactylopiidae)b Coccus hesperidum(Hemiptera: Coccidae)b Matsucoccus matsumurae(Hemiptera: Coccoidea)a Spodoptera litura (Lepidoptera: Noctuidae)b Eldana saccharina (Lepidoptera: Pyralidae)b Galleria mellonella (Lepidoptera: Pyralidae)a Galleria mellonella (Lepidoptera: Pyralidae)a Brahmina coriacea (Coleoptera: Scarabaeidae)c Bemisia tabaci (Hemiptera: Aleyrodidae)b Trialeurodes vaporariorum (Hemiptera: Aleyrodidae)b Platypus quercivorus (Coleoptera: Platypodidae)c Galleria mellonella (Lepidoptera: Pyralidae)c Planococcus f
ıcus (Hemiptera: Pseudococcidae); Tenebrio molitor (Coleoptera: Tenebrionidae); Galleria mellonella (Lepidoptera: Pyralidae)b Galleria mellonella (Lepidoptera: Pyralidae)a

Fusarium lateritium species complex Fusarium oxysporum species complex

F. oxysporum (35 isolates) F. oxysporum (27 isolates) F. oxysporum (1 isolate) F. oxysporum (1 isolate) F. oxysporum (1 isolate) F. oxysporum (4 isolates) F. oxysporum (2 isolates) F. oxysporum (1 isolate)

Fusarium redolens species complex

F. redolens (1 isolate)

Brahmina coriacea (Coleoptera: Scarabaeidae) Aphis gossypii (Hemiptera: Aphididae) Carpophilus lugubris (Coleoptera: Nitidulidae) Platypus quercivorus (Coleoptera: Platypodidae) Soil samples using a “Galleria bait method” Planococcus f
ıcus (Hemiptera: Pseudococcidae)

Soil samples using a “Galleria bait method”

Corrected total mortality Mortality

53.67 and 83% for nymphs and adult female, respectively 5e100% for eggs and 57e92% for larvaee 0e53.3%e

Mortality

0e93.3%d

Anand and Tiwary, (2009) Baidoo and Ackuaku, (2011) Sun and Liu, (2008)

Accumulated mortality in 12 d Accumulated mortality in 30 d Accumulated mortality in 144 h Total mortality

10e76%d

Ameen, (2012)

85.96%

Sharma et al., (2012)

100% for nymphs and ~13.5e20% for adultse 97.5%

Anwar et al., (2017)

Accumulated mortality in 6e25 d Accumulated mortality in 6 d Mortality

52.83%

Mortality

26.7%

30 and 33% 50, 60 and 80% for each insect, respectively

Entomopathogenic Fusarium species

Liu et al., (2014)


n et al., Torres-Barraga (2004) Qi et al., (2011) Ali-Shtayeh, Mara’I and Jamous, (2003) Sharma et al., (2018)

Sun and Liu, (2008) (continued on next page)

5

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Dactylopius opuntiae (Hemiptera: Dactylopiidae)

FIESC 17 [ F. pernambucanum (1 isolate) FIESC 20 [ F. caatingaense (22 isolates) FIESC 20 [ F. caatingaense (4 isolates) FIESC 20 [ F. caatingaense (4 isolates) FIESC 25 [ F. nanum (2 isolates)

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Species Complex

Fusarium species

Fusarium sambucinum species complex

F. culmorum (1 isolate) F. graminearum (5 isolates) F. poae (1 isolate) F. pseudograminearum (1 isolate) F. sambucinum (1 isolate)

Fusarium solani species complex

F. keratoplasticum (2 isolates) F. solani (5 isolates) F. solani (2 isolates)

F. solani (18 isolates) F. solani (1 isolate) F. solani (1 isolate) F. solani (1 isolate) F. solani (1 isolate)

F. solani (1 isolate) F. solani (24 isolates) F. solani (1 isolate) F. solani (2 isolates)

F. solani (1 isolate)

Host/Substrate

Target insect species

Cephus cinctus(Hymenoptera: Cephidae) Samples of soil

Cephus cinctus (Hymenoptera: Cephidae)b Galleria mellonella (Lepidoptera: Pyralidae)a Galleria mellonella (Lepidoptera: Pyralidae)a Cephus cinctus (Hymenoptera: Cephidae)b Galleria mellonella (Lepidoptera: Pyralidae)a Tribolium confusum (Coleoptera: Tenebrionidae)c

Accumulated in 13 d Accumulated in 12 d Accumulated in 12 d Accumulated in 13 d Mortality

Samples of soil Cephus cinctus (Hymenoptera: Cephidae) Soil samples using a “Galleria bait method” Tribolium confusum and T. castaneum (Coleoptera: Tenebrionidae) Soil samples using a “Galleria bait method” Bemisia tabaci (Hemiptera: Aleyrodidae)and Ceratothripoides claratris (Thysanoptera: Thripidae)

Soil samples using a “Galleria bait method” Tetanops myopaeformis (Diptera: Ulidiidae) Bupalus piniaria (Lepidoptera: Geometridae) Platypus quercivorus (Coleoptera: Platypodidae) Cadaver of an insect not identified Brahmina coriacea (Coleoptera: Scarabaeidae) Samples of soil Bemisia tabaci (Hemiptera: Aleyrodidae) Planococcus f
ıcus (Hemiptera: Pseudococcidae)

Soil Sample

Type of mortality assessment

Mortality rate

Reference

mortality

~54e80%e

mortality

13e20%d

Wenda-Piesik et al., (2009) Ameen, (2012)

mortality

13%

Ameen, (2012)

mortality

~38e97%e 0%

Wenda-Piesik et al., (2009) Sun and Liu, (2008)

Total mortality

80 and 50%

Chehri, (2017)

Galleria mellonella (Lepidoptera: Pyralidae)c Ceratothripoides claratris (Thysanoptera: Thripidae), Pseudococcus cryptus (Hemiptera: Pseudococcidae) and Bemisia tabaci (Hemiptera: Aleyrodidae)b Galleria mellonella (Lepidoptera: Pyralidae)a Tetanops myopaeformis (Diptera: Ulidiidae)b Bupalus piniaria (Lepidoptera: Geometridae)b Platypus quercivorus (Coleoptera: Platypodidae)c Periplaneta americana (Blattodea: Blattidae)b

Accumulated mortality in 5e10 d Corrected total mortality

28e44%d,f

Ali-Shtayeh, Mara’I and Jamous, (2003) Panyasiri et al. (2007)

Brahmina coriacea (Coleoptera: Scarabaeidae)c Galleria mellonella (Lepidoptera: Pyralidae)a Bemisia tabaci (Hemiptera: Aleyrodidae)b Planococcus f
ıcus (Hemiptera: Pseudococcidae); Tenebrio molitor (Coleoptera: Tenebrionidae); Galleria mellonella (Lepidoptera: Pyralidae)b Heterotermes indicola (Blattodea: Rhinotermitidae)b

Accumulated mortality in 30 d Accumulated mortality in 12 d Accumulated mortality in 144 h Mortality

6.7e16.7, 0e56.7 and 23.3e76.7%d for each insect, respectively

Mortality

0e86.7%d

Sun and Liu, (2008)

Corrected total mortality Accumulated mortality in 10 d Accumulated mortality in 6e25 d Total mortality

>80%

Majumdar et al., (2008)

30.7%

iulyte_ et al., 2010 Pec

47.33%

Qi et al., (2011)

60, 100 and 50e60%g at summer, autumn and winter, respectively. 81.85%

Abdul-Wahid and Elbanna, (2012)

10e76%d

Ameen, (2012)

100% for nymphs and 0% for adults 30e60, 30e70 and 40e50%d for each insect, respectively

Anwar et al., (2017)

10%

Afza et al., 2018

Accumulated mortality in 20 d

Sharma et al., (2012)

Sharma et al., (2018)

A. C. da S. Santos et al.

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

Table 1 (continued )

F. solani (3 isolates) Fusarium tricinctum species complex

F. acuminatum (1 isolate) F. avenaceum (1 isolate) F. avenaceum (11 isolates) F. avenaceum (1 isolate) F. tricinctum (2 isolates)

Unknown

Fusarium sp. (11 isolates) Fusarium sp. (1 isolate) Fusarium sp. (1 isolate)

Endophytic of strawberry leaves Spodoptera frugiperda (Lepidoptera: Noctuidae) Cephus cinctus (Hymenoptera: Cephidae) Cephus cinctus (Hymenoptera: Cephidae) Soil samples using a “Galleria bait method” Dialeurodes citri (Aleyrodidae: Hemiptera) Soil samples using a “Galleria bait method” Soil samples using a “Galleria bait method” Platypus quercivorus (Coleoptera: Platypodidae) Mealybug (Hemiptera) of cotton field

Duponchelia fovealis (Lepidoptera: Crambidae)b Spodoptera frugiperda (Lepidoptera: Noctuidae)a Cephus cinctus (Hymenoptera: Cephidae)b Cephus cinctus (Hymenoptera: Cephidae)b Galleria mellonella (Lepidoptera: Pyralidae)a Sitophilus oryzae (Coleoptera: Curculionidae)b Galleria mellonella (Lepidoptera: Pyralidae)a Galleria mellonella (Lepidoptera: Pyralidae)a Platypus quercivorus (Coleoptera: Platypodidae)c Bemisia tabaci (Hemiptera: Aleyrodidae)b

Corrected total mortality Survival analysis

32%

Amatuzzi et al., (2018)

~30e52.4%d

Accumulated mortality in 13 d Accumulated mortality in 13 d Mortality

~25e60%e

0e26.7%d

Hernandez-Trejo et al., (2019) Wenda-Piesik et al., (2009) Wenda-Piesik et al., (2009) Sun and Liu, (2008)

Corrected total mortality Mortality

52.22e94.86%g

Batta, (2012)

0% for both isolates

Sun and Liu, (2008)

Mortality

0e93.3%d

Sun and Liu, (2008)

Accumulated mortality in 6e25 d Accumulated mortality in 144 h

40.33%

Qi et al., (2011)

100% for nymphs and 6.5e13% for adultse

Anwar et al., (2017)

~55e90%e

Entomopathogenic Fusarium species

Species in bold were identified using molecular data. Inoculation of fungus in the insect: a Immersion in spore suspension; b Spraying of spore suspension; c exposure or direct contact of the insect with fungal spores. For the cases in which the mortality rate was presented with variation: d Variation in the mortality rate for the different isolates tested; e Variation in mortality rate for different concentrations of spores tested; f Variation in mortality rate according to the evaluation time interval; g Variation in mortality rate for different types of treatment tested. Only the studies that conducted pathogenicity tests for more than one stage of life of the insect had the mortality rates presented for each phase.

7

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

F. solani (1 isolate)

8

(O’Donnell et al., 2012, 2016a). Among the animals, it is with insects that Fusarium is most abundantly associated (TeetorBarsch and Roberts, 1983) with an increasing number of papers reporting pathogenic Fusarium-insect associations (see Table 1) which result in the control of insect pests and will be addressed in this review. Over the past two decades, the knowledge of Fusarium species diversity and their evolutionary relationships has increased significantly due to the application of multilocus molecular phylogenetics and genealogical concordance phylogenetic species recognition (Aoki, O’Donnell and Geiser, 2014). These methods have shown that the identification of Fusarium species traditionally based on morphological characteristics favored the creation of taxonomic schemes that significantly underestimate species diversity within the genus and that the limited number of morphological characters separating species has given rise to species concepts that are too broad (Geiser et al., 2004). In addition, the morphological plasticity found in Fusarium in response to changes in the environment (Leslie et al., 2001, Leslie and Summerell, 2006) contributed to this problem. It is now widely accepted that taxa previously thought to represent species are actually complexes of species consisting of numerous distinct taxa (O’Donnell, 2000; O’Donnell et al., 2008; Schroers et al., 2016; Lombard et al., 2019a). Currently Fusarium comprises 16 to 23 species complexes and some monotypic lineages (Laurence et al., 2011; O’Donnell et al., 2013; Zhou et al., 2016; Sandoval-Denis et al., 2018). The number of complexes varies according to different criteria used for the definition of genus boundaries, which may be more restrictive, based on the phylogeny and morphological characteristics of the sexual morphs € fenhan et al., 2011; Lombard et al., 2015), or a wider in (Gra order to retain agriculturally and medically relevant species, such as those in the Fusarium solani species complex (FSSC) € fenhan et al., (Geiser et al., 2013) ¼ genus Neocosmospora (Gra 2011). Some of these complexes harbor phylogenetic species discovered via molecular phylogenetics that have not been formally described. Many of these are morphologically cryptic (Aoki, O’Donnell and Geiser, 2014; O’Donnell et al., 2015). In order to be precise when discussing these unnamed species, an informal nomenclature system has been adopted in five complexes of Fusarium species, including species of agronomic and clinical interest (Chang et al., 2006; O’Donnell et al., 2008, 2009, 2010; Schroers et al., 2009). Based on a Multilocus Sequence Typing scheme (MLST), this system classifies, within a complex of species, the phylogenetic species and their haplotypes, represented by Arabic numerals and lower case Roman letters, respectively (O’Donnell et al., 2015). Methodologies for studying sexual compatibility in Fusarium are well established (Klittich and Leslie, 1988; Covert
nyi et al., 2004), and may be useful for et al., 1999; Kere testing the degree of reproductive isolation among certain phylogenetic species, contributing to a more robust delimitation of them. Using a polyphasic approach, combining morphological, biological and molecular phylogenetic data and considering ecological aspects of the fungus is essential for the development of a successful Fusarium taxonomy model.

A. C. da S. Santos et al.

3. Which fusaria infect which insects and how virulent are they? Classic works by Wollenweber and Reinking (1935) and Gordon (1959, 1960) reported some species obtained from insects, although the number of these isolates has been small compared with the number of isolates recovered from plants. The reports on insect-associated Fusarium species published between 1950 and 1980 were gathered in a literature review published in the early 80’s, which addressed non-pathogenic and pathogenic relationships between Fusarium and insects (Teetor-Barsch and Roberts, 1983). In 2012 a large study based on multilocus sequence typing (MLST) assessed the phylogenetic diversity of Fusarium strains isolated from diverse insects and showed that insect-associated Fusarium species nested within 10 species complexes, of which eight included novel, putatively unnamed insecticolous species (O’Donnell et al., 2012). Recently Sharma and Marques (2018) have addressed insect-Fusarium pathogenic and mutualistic associations in a review, focusing on studies demonstrating the natural insect-pathogenicity under field conditions. Here, we provide a survey of peer-reviewed papers, published from 2000 to 2019, investigating Fusarium species for their pathogenicity to insects. These articles were retrieved from the databases using the key word “Fusarium”, combined with the terms “biological control of insects”, “entomopathogenic fungi”, or “pathogenic to insects”, as well as the names of the insect orders. Of these studies, only those who carried out pathogenicity tests against insects were considered and presented in this review (Table 1). We also list the species complexes to which they belong and highlight those that harbor the largest number of entomopathogenic species and strains, and the orders of insects most affected by representatives of these complexes. Forty peer-reviewed papers were evaluated, of which 12 were published between 2001 and 2009, and 28 published between 2010 and 2019. In these studies, pathogenicity tests were conducted against one or more species of insects, using fungi isolated from insects in most cases (Table 1). Some additional isolates obtained from soil and vegetables were shown to be entomopathogenic in tests with percentages of mortality ranging from 5 to 100% between different isolates against different insects (Ali-Shtayeh, Mara’I and Jamous, 2003; Ameen, 2012; Anand and Tiwary, 2009; Amatuzzi et al., 2018). Together, the 40 studies involved 273 isolates of Fusarium identified as belonging to at least 30 species. Only sixteen (40%) of these investigations used molecular tools for the identification of Fusarium species, and even among these, some have not considered the multilocus haplotype nomenclature used within some complexes to distinguish species that lack a Latin binomial. As the morphological recognition of species does not allow an accurate identification of Fusarium species (Leslie et al., 2001; Geiser et al., 2004), many fungi were identified as old species, which we now know correspond to broader taxa that contain several different species, such as the species complexes F. incarnatum-equiseti (O’Donnell et al., 2009; Xia et al., 2019), F. oxysporum (Laurence et al., 2014; Lombard et al., 2019a) and F. solani (Chang et al. 2006; O’Donnell, 2000; Schroers et al.

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

Entomopathogenic Fusarium species

2016; Sandoval-Denis and Crous, 2018; Sandoval-Denis et al., 2019). Fusarium species most frequently reported as entomopathogenic in the articles were F. solani (reported in 14 studies and pathogenic to 14 insect species), F. oxysporum (reported in nine studies and pathogenic to eight insect species), F. semitectum (reported in six studies and pathogenic to five insect species), F. equiseti (reported in five studies and pathogenic to four insect species) and F. proliferatum (reported in five studies and pathogenic to four insect species). The species with entomopathogenic representatives were distributed in ten complexes (Fig. 1), of which four stand out as the most frequently reported in the studies  Fusarium incarnatum-equiseti, Fusarium fujikuroi, Fusarium solani and Fusarium oxysporum species complexes, appearing in 19, 13, 15 and nine studies, respectively. These complexes also harbored the largest number of entomopathogenic isolates, of which 68 belonged to the F. incarnatum-equiseti species complex, 23 to the F. fujikuroi species complex, 64 to the F. solani species complex and 73 to the F. oxysporum species complex. O’Donnell et al. (2012) studied phylogenetic estimates of the diversity of Fusarium strains isolated from insects, but without determining their pathogenicity and showed that the species complexes most species rich in insect-associated lineages were the F. fujikuroi (eight species and 43 isolates from insects), the F. incarnatum-equiseti (15 species and 31 isolates from insects), the F. oxysporum (14 isolates from insects), the F. solani (eight species and 13 isolates from insects) and the F. tricinctum species complexes (five species and seven isolates from insects). In the articles evaluated, insects of the orders Hemiptera were prevalent hosts for members of the F. fujikuroi and F. incarnatum-equiseti species complexes, and insects of the orders Coleoptera and Hemiptera for members of the F. oxysporum and F. solani species complexes. Overall, considering all reports without distinguishing the Fusarium complexes, the order Hemiptera is the most frequently reported as a source of Fusarium isolation, followed by Coleoptera and Hymenoptera. Regarding pathogenicity, of the forty studies, sixteen tested Fusarium isolates against insects of the order Hemiptera, eleven against insects of the order Lepidoptera, seven against insects of the order Coleoptera, three against insects of the order Hymenoptera, two against insects of the orders Blattodea, Diptera and Thysanoptera, and one against insects of the orders and Orthoptera. For most cases moderate to high mortality rates were observed, as summarized in Table 1. The lowest percentages were recorded against insects of the orders Lepidoptera and Thysanoptera. It was possible to register an affinity to some orders of insects by members of the complexes of species most rich in entomopathogenic isolates. Most isolates of the F. incarnatum-equiseti species complex were tested against Hemiptera and Lepidoptera insects (Fig. 2). However, whereas mortality rates ranging from low to high have been recorded for insects of the order Hemiptera (Table 1), the pathogenicity against insects of the order Lepidoptera, in most cases, was low or even nonexistent (Ali-Shtayeh, Mara’I and Jamous, 2003; Sun and Liu, 2008; Ameen, 2012). The majority of the isolates of the F. fujikuroi species complex were tested against insects of the orders Coleoptera, Hemiptera and Lepidoptera (Fig. 2), with the highest mortality rates usually recorded against Coleoptera

9


n et al., and Hemiptera (Ganassi et al., 2001; Torres-Barraga 2004; Lazo, 2012; Sharma et al., 2018). Most of the isolates of the F. solani species complex have also been tested against members of the Coleoptera, Hemiptera and Lepidoptera orders (Fig. 2), with mortality rates ranging from low to high for the insects of each of the prevalent orders (Table 1). For members of the F. oxysporum species complex, the mortality rates recorded against Lepidoptera insects ranged from low to high (Ali-Shtayeh, Mara’I and Jamous, 2003; Sun and Liu, 2008; Baidoo and Ackuaku, 2011), and from moderate to high against insects of the orders Coleoptera and Hemiptera
n et al., 2004; Qi et al., 2011; Ameen, 2012; (Torres-Barraga Anwar et al., 2017; Sharma et al., 2018). The inoculation methodologies involved mainly the immersion of the insects in spore suspensions or spraying of spore suspensions on insects, and in some cases the direct contact with the fungus. As these data come from different studies using different species of insects and different isolates of Fusarium, it was not possible to establish a correlation between the methodology used and the efficacy of the treatment. However, Batta (2012) tested three types of fungus treatment against adults of Sitophilus oryzae infesting wheat grain, and found differences in the mean percentage mortality according to the methodology of inoculation, with the highest mean percentage mortality obtained by the direct spraying of S. oryzae with the conidial suspension before introduction of the treated adults into pots containing wheat grain. The lowest mean percentage mortality was obtained by spraying the inner surfaces of pots with the fungus conidial suspension before introducing the grain and insects. Variation in mortality rates was also recorded when one or more isolates were tested using different concentrations of spores (Ameen, 2012; Munshi et al., 2008; Wenda-Piesik et al., 2009, Baidoo and Ackuaku, 2011; Jayasimha et al., 2012) and when mortality was assessed at different time intervals (Ali-Shtayeh, Mara’I and Jamous, 2003). Sun and Liu (2008) observed intraspecific variation of the efficacy of the fungal species after evaluating the pathogenicity of 35 isolates of Fusarium oxysporum and 18 isolates of Fusarium solani against Galleria mellonella (Lepidoptera: Pyralidae), with variations in mortality from 0 to 93.3%, and 0e86.7% respectively.

4. Fusarium as biological control agents for insects: key characteristics and frontiers Given the entomopathogenic potential of Fusarium species, it is necessary to evaluate both the promising features and the negative implications of their use for the biological control of pest insects on agricultural crops, aiming at a more effective exploitation of these fungi, with safety and minimal environmental impacts. Fusarium strains have been reported to cause high mortality rates against insects (Ganassi et al.,
n et al., 2004; Munshi et al., 2008; Abdul2001; Torres-Barraga Wahid and Elbanna, 2012; Fan et al., 2014; Tosi et al., 2015; Anwar et al., 2017). In 21 of the 40 articles percentages of mortality above 80% were reported, and in 13 these percentages were above 90% (Table 1), highlighting the potential of these fungi for insect control. This entomopathogenic potential was initially overshadowed due to reports of Fusarium species

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

10

A. C. da S. Santos et al.

Fusarium species, (isolates number) and insect Orders

Species complexes

F. e quise ti (7) F. semitectum (19) F. inc arnatum (2) F. pallidoroseum (2) FIESC 3 = F. c ompa c tum (1)

100

F. inc arnatum-e quise ti sc

FIESC 16 = F. sulaw e sie nsis (1) FIESC 17 = F. pe rna mbuc a num (1) FIESC 2 0 = F. c a a t inga e nse (30) FIESC 25 = F. na num (2) FIESC 28 = F. c offe a tum (1)

100

F. gra mine arum (5) F. c ulmorum (1)

100

72

F. pse udogra mine a rum (1)

F. sambucinum sc

F. poa e (1)

99

F. sambucinum (1) 100

100 100

F. c hlamydosporum sc

F. c hlamydosporum (4) F. tric inc tum (2)

F. tric inc tum sc

F. acumina tum (1) F. a ve na c e um (13)

100

F. hete rosporum sc

F. hete rosporum (1)

100

F. prolife ra tum (7) F. moniliforme (9) F. fujikuroi (1)

100

F. fujikuroi sc

F. sac c ha ri (2) F. vertic illioide s (1)

100

100

100 100 99 100 0.04

F. subglutina ns (1) F. nyga mai (1) F. oxysporum sc

F. oxysporum (74)

F. redole ns sc

F. redole ns (1)

F. late ritium sc

F. late ritium (1) F. k e ra t opla stic um (2)

F. sola ni sc

F. sola ni (62) Legends insect Orders: Blattodea Coleoptera

Diptera

Hymenoptera

Orthoptera

Hemiptera

Lepidoptera

Thysanoptera

Fig. 1 e Maximum likelihood (ML) tree based on RPB1 and RPB2 sequences, showing Fusarium species and complexes that harbor entomopathogenic isolates. Symbols on the right indicate the orders of insects for which isolates of that fungal species were pathogenic.

or strains weakly pathogenic to insects and to the difficulty in isolating the true pathogen, since saprophytic strains of the same fungus colonize dead insects (Teetor-Barsch and Roberts, 1983). However, more recent investigations have revealed a high virulence and rapid action of these fungi (Addario and Turchetti, 2011; Liu et al., 2014). In some cases

a mortality of up to 40% in just 24 h was observed, reaching 100 % mortality by the 6th day (Lazo, 2012), of up to 99% after 12 h of application (Ganassi et al., 2001), and 100% after 144 h (Anwar et al., 2017). To optimize treatment efficiency, methods of application (e.g. spraying, dusting, dipping, felting) and concentrations of inocula, and the time of

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

Entomopathogenic Fusarium species

11

Fig. 2 e Graph illustrating the number of isolates from each Fusarium species complex tested against each insect order.

application should also be evaluated (Teetor-Barsch and Roberts, 1983). In some cases, different life stages of the same insect species are susceptible to the Fusarium species (Ganassi et al., 2001; Anand and Tiwary, 2009; Asharani et al., 2009; Jayasimha et al., 2012; Liu et al., 2014; Jayasimha et al., 2014; Sepasi et al., 2015). This allows the infection of non-feeding stages such as eggs and pupae, which are not accessible to non-fungal pathogens that need to be ingested to invade their hosts (Goettel et al., 2010; Hussain et al., 2012). This ability is due to the production of enzymes by the fungi, which enables them to infect insects directly through the integument, the first barrier against biological insecticides (Hussain et al., 2012). The enzymes involved in pathogenesis of insects are generally grouped into proteases, chitinases and lipases (Khan et al., 2012). Some Fusarium species have been reported as good producers of these enzymes (Bueno et al., 2009; AbdulWahid and Elbanna, 2012; Juntunen et al., 2015; Sopuruchukwu et al., 2015). However, the number of studies investigating the production of enzymes by Fusarium is still small, given that its ability to explore a wide range of substrates and hosts may be indicative of a poorly exploited biotechnological potential (Leslie et al., 2001; Summerell et al., 2010; Summerell and Leslie, 2011). After the process of infection and death of the host, under favorable environmental conditions, some entomopathogenic fungi grow out of the cadaver, and form sporulation structures and spores (Fig. 3) for dissemination to another host (Goettel et al., 2010). Tosi et al. (2015) observed in natural field conditions Fusarium proliferatum isolates involving the bodies of

larvae, pupae and adults of Dryocosmus kuriphilus (Hymenoptera: Cynipidae). In experiments using F. incarnatum-equiseti species complex isolates against the same insect species, the bodies of the insects infested by fungal mycelium (Addario and Turchetti, 2011) were frequently observed. Fan et al. (2014) reported mycelial growth of isolate of this complex on Coccus hesperidum (Hemiptera: Coccidae) under both field and laboratory conditions after application of spore suspension in pathogenicity tests. Macroconidia of Fusarium avenaceum were observed on the outer surfaces of Sitophilus oryzae (Coleoptera: Curculionidae) after three days of insect death and incubation under 20  1 C humidity conditions (Batta, 2012). After ten days of inoculation of F. verticillioides on thirdinstar nymphs of Ronderosia Berg (Orthoptera: Acrididae), conidiophores and conidia were observed growing from dead insects (Pelizza et al., 2011). The same occurred with nymphs of Schizaphis graminum (Hemiptera: Aphididae) after 18e24 h of the treatment with F. proliferatum (Ganassi et al., 2001). According to Santos et al. (2016) the abundant presence of these structures are considered advantageous for the biocontrol. Alternatively, if unable to find another host, many species form some type of resting stage capable of surviving periods of adverse conditions before forming or releasing a type of spore (Goettel et al., 2010). Persistence in the environment is a characteristic of interest for the selection of control microbial agents (Tiago et al., 2012). As facultative pathogens, entomopathogenic Fusarium species are likely to have an excellent survival potential in the field (Teetor-Barsch and Roberts, 1983). Several Fusarium species form long-term survival structures, such as chlamydospores, that can remain for years in

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

12

A. C. da S. Santos et al.

Fig. 3 e Fusarium sporulation emerging from different insects. A: Aleurocanthus woglumi; B: Dactylopius opuntiae; C: Aphis craccivora.

the soil or environment, including in adverse conditions (Leslie and Summerell, 2006). Among the Fusarium complexes most commonly reported in insects, the production of chlamydospores is variable, being generally abundant in F. solani species complex (Sandoval-Denis and Crous, 2018) and sparse to abundant, depending on the species, in F. incarnatum-equiseti species complex (Gerlach and Nirenberg, 1982; Santos et al., 2019; Xia et al., 2019), while most species included in F. fujikuroi species complex do not produce such a structure (Kvas et al., 2009). In the F. oxysporum species complex, there are species that formed chlamydospores abundantly and species that do not produce the structure (Lombard et al., 2019a). In addition to the significant characteristics for the biological control of insects mentioned above, the cultivation of Fusarium is simple and mass production should pose no difficulty. Another advantage is the possibility of increasing the virulence of entomopathogenic isolates, as has already been done with plant pathogenic Fusarium strains by genetic manipulation (Teetor-Barsch and Roberts, 1983). Moreover the high genetic variability naturally observed in Fusarium (Leslie and Summerell, 2006; Burgess, 2014) is a strategic advantage for biological control, because it widens the range of possibilities to be selected and employed in the control of insects, and consequently the chances of finding more efficient entomopathogens (Tiago et al., 2016). On the other hand, efforts to use Fusarium species in biological control have been limited by some factors, including the fact that they are potential producers of mycotoxins (O’Donnell et al., 2012, 2018) that can be highly toxic or carcinogenic (Strasser et al., 2000). Fusarium comprises producers of the most toxicologically important mycotoxins such as trichothecenes, deoxynivalenol, fumonisins, moniliformin and zearalenone (Antonissen et al., 2014; Nazari et al., 2015) which, on a large scale, can contaminate the environment with amounts harmful to health (Teetor-Barsch and Roberts, 1983; O’Donnell et al., 2012). On the other hand, while little is known about metabolites from fungal biological control agents, including those from commercialized mycoinsecticides, mycoherbicides and mycoparasites (Vey et al., 2001; Strasser et al., 2000), much has been learned about mycotoxins produced by Fusarium (Antonissen et al., 2014; O’Donnell et al., 2018) and the development of methods and tools to detect mycotoxins makes the selection of strains that are intrinsically poor toxin producers possible (Strasser

et al., 2000). In order for any entomopathogenic fungus to be registered as a microbial control agent, it must first undergo stringent testing for potential harmful effects on vertebrates, including mammals (Goettel et al., 2010). Some entomopathogenic fungi produce toxins insecticidal that may assist in pathogenesis and result in more rapid host death (Goettel et al., 2010). One of these metabolites is the beauvericin that has a strong insecticidal activity against a broad spectrum of insect pests (Wang and Xu, 2012) and has no significant health consequences to humans and animals, compared to other mycotoxins (Li et al., 2013). Several Fusarium species are able to produce beauvericin (Liuzzi et al., 2017), including members of the species complexes F. fujikuroi (Moretti et al., 2007; Liuzzi et al., 2017; O’Donnell et al., 2018), F. incarnatum-equiseti (Kosiak et al., 2005; O’Donnell et al., 2018), F. oxysporum (Song et al., 2009; Li et al., 2013; O’Donnell et al., 2018) and F. solani (Ekundayo and Oladunmoye, 2007), reinforcing their potential for control of insects. Another hurdle concerning the use of Fusarium in biological control is the chance of unintentionally releasing phytopathogens in mass into the environment (O’Donnell et al., 2012), since many species of the genus are known to cause diseases in plants (Summerell and Leslie, 2011; Burgess, 2014). Therefore, considering using Fusarium strains for control of insects, these should be studied for their host specificity. Specificity of entomopathogenic fungi varies widely between genera, within genera, and even among strains of a species. For biocontrol applications the isolate is more important than the species as a unit (Goettel et al., 2010), for this reason, the potential for interactions must be studied on a strain-bystrain basis (Leger et al., 2011). Some studies have indicated that Fusarium isolates that cause high mortalities in their insect host show a high host specificity and do not infect the crop plant (Kuruvilla and Jacob, 1980; Teetor-Barsch and Roberts, 1983; Mikunthan and Manjunatha 2006; Wenda-Piesik et al., 2009; Lazo, 2012; Fan et al., 2014). However, of the forty works reporting the pathogenicity of Fusarium strains to insects presented in this review, only five investigated the abil
n et al., ity of these strains to infect plants (Torres-Barraga 2004; Wenda-Piesik et al., 2009; Lazo, 2012; Fan et al., 2014; Sepasi et al., 2015), thus little is known about the actual host range of entomopathogenic Fusarium strains, a point that needs to be considered for determining their safety to nontarget organisms.

Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002

Entomopathogenic Fusarium species

Susceptibility assays using nontarget organisms should be also conducted as is done with other fungi used for biological control, considering the potential risk to non-targets organisms. This evaluation should involve laboratory studies initially, aiming at the selection of isolates unable to infect non-targets, even under optimal conditions for the fungus. The following steps, involving semi-field and field studies, in turn, may provide a more realistic prediction of the likelihood of these fungi being a threat can provide a more realistic prediction of the likelihood of these fungi represent an ecological risk (Roy and Pell, 2000). A critical point that needs to take a more important role in the research involving Fusarium in biological control is the identification of these fungi. In spite of molecular phylogenetic methods becoming more accessible (Watanabe et al., 2011), the studies published in the last two decades show that the identification of the most of the entomopathogenic Fusarium isolates is still made based only on morphological characteristics. This can result in loss of information and an inconsistent identification, since morphological approaches underestimate the diversity of species in the genus (Geiser et al., 2004). Although the taxonomy of Fusarium is considered complex, and the accurate identification and delimitation of species is laborious (Summerell and Leslie, 2011; Burgess, 2014) it is essential that the identification and characterization of these fungi be carried out by combining biological, ecological, morphological and molecular data whenever possible.

5.

13

2009, 2012). Recently, descriptions and Latin binomials have been attributed to most of these species (Lombard et al., 2019b; Sandoval-Denis et al., 2019; Xia et al., 2019), including species from insects (Freeman et al., 2013b; Aoki et al., 2018, 2019; Santos et al., 2019). It is believed, however, that genetic diversity in these groups is still under-sampled (O’Donnell et al., 2012; Sandoval-Denis and Crous, 2018). Therefore, studying insect-associated Fusarium species promise not only new insights into their ecology, but also advances in knowledge about the diversity and taxonomy of Fusarium. The pathogenicity of Fusarium has been reported against insects of the orders Blattodea, Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Orthoptera and Thysanoptera. Despite the increasing number of studies showing the potential of these fungi for the control of insects, few have investigated their specificity to the host insect, the production of undesirable secondary metabolites by them, or side-effect and safety tests with non-target organisms. Researchers should assess in depth these aspects for all strains of Fusarium that they consider using in biological control. Expanding our understanding of the host-Fusarium-environment interaction is necessary and will be decisive for the better exploration of those microorganisms of agronomic interest.

Declaration of Competing Interest None declared.

Conclusions Acknowledgments

In this study, we carried out a survey of forty papers published since 2001 reporting the pathogenicity of Fusarium to insects. These reports show that the genus includes many strong entomopathogenic agents with promising characteristics for the control of insects, in contrast to earlier views that the Fusarium relationships with insects were mostly opportunistic. The ability of Fusarium isolates to produce enzymes (Bueno et al., 2009; Abdul-Wahid and Elbanna, 2012; Juntunen et al., 2015; Sopuruchukwu et al., 2015) and toxins (Liuzzi et al., 2017; O’Donnell et al., 2018) that can assist in the penetration and death of insects and in view of the colonization of insects observed in the field (Tosi et al., 2015). This added the confirmation of Koch’s postulates performed in the laboratory, some resulting in high mortality rates (Table 1), shows that Fusarium-insect interactions are more diverse than previously thought and much remains to be explored. Most of the insect pathogens are located within four species complexes: F. incarnatum-equiseti, F. fujikuroi, F. solani and F. oxysporum. Since many species contained in these complexes are difficult to distinguish morphologically it is necessary to use other markers, especially the molecular ones, for accurate identification. However, most of the entomopathogenic Fusarium isolates have not received the appropriate taxonomic attention, as discussed in the above topics, so that a change in this direction is necessary. Complexes rich in entomopathogenic strains, such as F. incarnatum-equiseti and F. solani, initially comprised many phylogenetic species not described, designated by the haplotype nomenclature system (Chang et al., 2006; O’Donnell et al., 2008; O’Donnell et al.,

We thank the Conselho Nacional de Pesquisa (CNPq) and the ~ o de Aperfeic¸oamento de Pessoal de N
ıvel SupeCoordenac¸a rior (CAPES) e Brazil for scholarships for Ana Carla da Silva Santos and Athaline Gonc¸alves Diniz. We are grateful to Marlus Filipe Costa Nunes for his assistance in the preparation of drawings of the insects.

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Please cite this article as: Santos, Ana Carla da Silv et al., Entomopathogenic Fusarium species: a review of their potential for the biological control of insects, implications and prospects, Fungal Biology Reviews, https://doi.org/10.1016/j.fbr.2019.12.002