Andressa C. Z.

Machado (35-49)

doi: 10.31976/0104-038321v280002 SEÇÃO 1

BIONEMATICIDES IN BRAZIL: AN
EMERGING AND CHALLENGING MARKET
REVISÃO ANUAL DE PATOLOGIA DE PLANTAS
COPYRIGHT© REVISÃO ANUAL DE PATOLOGIA DE PLANTAS
2017 1
Andressa C. Z. Machado

ABSTRACT RAPP
Management of plant parasitic nematodes in Brazil is a challenge and bione-
REVISÃOare
maticides ANUAL DE PATOLOGIA
an important DE Integrated
tool in the PLANTAS Nematode Management in sev-
eral crops. There are 47 commercial bionematicides with 11 microorganisms as ac-
tive ingredient available for growers in Brazil; Bacillus spp. are the main biological
Nenhuma parteagents,
control desta but
publicação
fungi are poderá ser reproduzida
also important for nematodesemmanagement.
prévia Bionemat-
autorização, poricides
escrito, do editor.
reached 82% of the total market of nematicides in 2019/2020 in Brazil and,
in soybean, they represented 90% of the area treated with nematicides. Although,
the use of bionematicides is considered an emerging market worldwide, some chal-
RAPP -lenges
REVISÃOinvolveANUAL DE use
the correct PATOLOGIA DE PLANTAS
and formulation of organisms with different modes
SGAS of902
action, difficulties
Bloco B Salasin102
laboratory
e 103 culturing, and the existence of non-regulated bi-
onematicides,
ECONOMICALLYEdifício Athenas Asa Sul which do not ensure the quality, the purity, and the efficiency in the
nematode control under field conditions, leading to lack of control and discredit of
IMPORTANTBrasíliathisDF Brasil
tool. Considering the Brazilian biodiversity richness, a universe of new macro-
NEMATODES INCEP and microorganisms can be explored, as well as the metabolites produced by these
70390-020
organisms as the active ingredient of bionematicides. Expectations of an increase in
BRAZILSite SBF: www.sbfito.com.br
this market are optimistic and may materialize in light of the increasing demand for
biological
Site RAPP: products in Brazil.
rappsbf.weebly.com
KEYWORDS: biological control, management, nematodes, biopesticides

In the last decades, nematodes had gained tode, Pratylenchus brachyurus, the soybean cyst
a prominent position in Brazilian agriculture among nematode, Heterodera glycines (parasitize only soy-
the main diseases that attack economically im- bean) and the reniform nematode, Rotylenchulus
portant crops,Publicado
such as soybean, cotton,
no Brasil and coffee reniformis (MACHADO 2014). In coffee crops, M. ex-
(MACHADO 2014). Information provided by the Bra- igua, M. incognita and M. paranaensis are the main
zilian Nematological Society realize that nematodes nematode species causing extensive losses (OLIVEI-
cause about US$ 6.5 billion of yield losses in Brazil- RA & ROSA 2018). Sugarcane is parasitized and dam-
ian agriculture annually; considering only the soy- aged by M. incognita, M. javanica, P. brachyurus,
bean crops, these losses correspond to US$ 3 billion and P. zeae (DINARDO-MIRANDA 2014), while M.
(considering 1 dollar = R$ 5.3). enterolobii is a concern for fruit trees as guajava
For some crops, as soybean, cotton, Diagramação:
and (Psidium guajava) and acerola (Malpighia emargi-
maize, main nematode species are two root-knot nata) and vegetables (CARNEIRO 2003; PINHEIRO,
Gráfica Diagrama
nematodes, M. incognita and M. javanica (this sec- 2017).
ond not parasitize cotton), the root-lesion nema- Symptoms involve in general the stunting of

1
Instituto de Desenvolvimento Rural do Paraná – IAPAR/EMATER, Londrina, PR, 86047-902, Brazil. Corresponding author: Andressa
C. Z. Machado. E-mail: andressa_machado@idr.pr.gov.br.

RAPP
RAPP- -Volume
Volume25,
28,2017
2022 III35
 Andressa C. Z. Machado (35-49)

plants, chlorosis and falling of leaves, flower abor- health/biostimulants/state-of-the-industry-ex-

tion and lower yields. In the root system, the attack clusive-survey-results-on-biological-products/)
of root-knot nematodes is easy to recognize, since showed that the increasing demand for biological
they incite the formation of enlarged nodes known products are driving by consumers that require
as galls, but symptoms associated to the attack of lower pesticide residues, followed by the environ-
Pratylenchus spp. and other nematode species are mental laws, favorable regulatory framework, and
often unspecific and involve basically dark or ne- demand from farmers who are complying new
crotic lesions in roots, easily confounded with fungi purchasing strategies from large grocery retail-
or bacteria parasitism (FERRAZ & BROWN 2016). ers. These aspects are noticeable by the numbers
In addition to the significant damages and presented in this survey: 58% of the companies
yield losses caused by different nematode species, interviewed say that they are integrating biologi-
difficulties in management of these pathogens lead cal products into their portfolios and another 21%
to the great concern on plant-parasitic nematodes are looking to develop or offer biological prod-
in Brazil. Management is done mainly by the use ucts.
of resistant cultivars, the adoption of crop rotation The global pesticide market registered an
with non-hosts, or with the application of chem- amount of US$ 57.561 billion in 2018. The global
ical or biological nematicides (MACHADO 2016; biopesticide market represents a small portion of
MACHADO et al. 2016; ARITA et al. 2020; SILVA et this, since in 2018 its value was around US$ 3.14
al. 2020). billion, but the expected increase of this market
Unfortunately, few options of resistant cul- will be around 14% from 2019 to 2024 (AGROPAG-
tivars are available for growers and some of them ES 2019). The Latin America biopesticide market
could not be recommended for the different agri- represented US$ 305.1 million in 2017; Brazil
cultural areas in Brazil, due to the climatic restric- was the largest market, with US$ 103.5 million in
tions. Crop rotation is also constrained by the high 2017, increasing to US$ 200 million in 2019/2020
level of polyphagia observed in most of the nema- (CAMPOS 2021).
tode species, as P. brachyurus and M. incognita. In Brazilian biopesticide market was estimat-
addition, non-hosts options include non-commer- ed in about US$ 340 million in 2021, but projec-
cial plant species, as Crotalaria spectabilis, which tions are that biopesticides have the potential
reduce the chance of the grower adopting this to increase 107% until 2030, reaching about US$
management tool (SILVA et al. 2020). 700 million (FRAGA 2021). This market is repre-
Chemical and biological nematicides are sented by 41% of insecticides, 24% of fungicides,
good options for nematode management, espe- and 35% of nematicides; soybean, sugarcane, and
cially when other management tools are not avail- maize represent 75% of the biopesticide market
able or are difficult to be used. Despite the great in Brazil (FRAGA 2021). Specifically for soybean,
importance of nematodes in Brazil, few chemical more than 2.5 million hectares of this crop in Bra-
molecules are registered in the Brazilian Ministry of zil were treated with bionematicides in the crop-
Agriculture, Livestock and Food Supply for the use ping season of 2018/2019 (DIAS 2020).
in nematode infested fields (AGROFIT 2021). Until In relation to Brazilian nematicide mar-
this moment, we have 12 active ingredients, which ket, bionematicides were used in 90% of the area
corresponds to 29 commercial products, registered cropped with soybean and treated with nemati-
for the control of nematodes. On the contrary, we cides in 2019/2020; seed treatment represented
have 11 biological agents and 47 commercial prod- 70% of the total bionematicide application in soy-
ucts recommended for nematode management bean. Together with other crop species, the use of
(AGROFIT 2021). bionematicides in Brazil reached 82% of the total
market of nematicides in 2019/2020 (DIAS 2020).
BIONEMATICIDE MARKET The main organisms used in commercial products
Biological control as an important tool in in Brazil with nematicide action are bacteria, es-
the Integrated Nematode Management is a reality pecially Bacillus spp., and fungi, as Purpureocil-
in Brazil and worldwide nowadays. A global scale lium (=Paecilomyces) lilacinum, Pochonia chlam-
poll (https://www.agribusinessglobal.com/plant- ydosporia, and Trichoderma spp. (AGROFIT 2021).

36 RAPP - Volume 28, 2022

 Andressa C. Z. Machado (35-49)

MAIN BIONEMATICIDES IN BRAZIL: ORGANISMS todes, acting on different stages of the nematode
AND MODE OF ACTION development (KAVITHA et al. 2012; HU et al. 2017).
Bacillus spp. In Brazil, Bacillus spp. are The growth of the bacteria around the roots leads
present in almost 60% of the commercial bione- to an alteration in the composition of the root ex-
maticides (Table 1) (AGROFIT 2021). From 27 bi- udates, causing an interference in the recognizing
onematicides containing Bacillus spp., B. amylo- process by the nematodes, since they are attracted
liquefaciens are present in 10 of them, B. subtilis in direction to roots by the chemical compounds
in eight, as a single active ingredient, and three in of the root exudates from the host plant (HU et al.
mixture with B. licheniformis, followed by B. firmus 2017).
(3), B. velezensis (2), and B. methylotrophicus (1). Bacillus spp. are important plant growth
These bacteria colonize the rhizosphere and promoters (plant growth promoting rhizobacteria).
develop associated to roots, stimulated by root ex- Through the endophytic colonization of the roots,
udates, where they form a physic-chemical barrier they induce the production of growth regulators,
composed by bacterial cells and metabolites pro- specially phytohormones, which improve plant de-
duced by them (HASHEM et al. 2019); this barri- velopment (SANTOS et al. 2018). Besides, these bac-
er avoids nematode penetration into roots (Figure teria can also act as resistance inducers (Figure 1),
1). In addition, some isolates produce substances activating genes involved in the Systemic Induced
through their metabolism that are toxic to nema- Resistance (SIR) (CHOUDHARY & JOHRI 2009).

Table 1. List of bionematicides registered for use in Brazil, according to Agrofit (2021).
Biological Commercial Concentration Biological target Company
agent product
Pasteuria nishi- 1 x 1010 endospores Syngenta Proteção de Cultivos
Clariva PN Heterodera glycines
zawae / mL Ltda.
Pasteuria nishi- 1 x 1010 endospores Syngenta Proteção de Cultivos
Clariva PN BR Heterodera glycines
zawae / mL Ltda.
Pratylenchus brachyurus,
Bacillus firmus Andril Prime 4 x 109 CFU / g BASF S.A.
Meloidogyne javanica
Meloidogyne javanica,
Bacillus firmus Oleaje Prime 4 x 109 CFU / g BASF S.A.
Pratylenchus brachyurus
Meloidogyne javanica,
Bacillus firmus Votivo Prime 4 x 109 CFU / g BASF S.A.
Pratylenchus brachyurus
Pratylenchus brachyurus,
Bacillus amylo- Sumitomo Chemical do Brasil
Aveo EZ 6.1 x 1010 CFU / mL Meloidogyne incognita
liquefaciens Representações Ltda
Heterodera glycines
Bacillus amylo- Heterodera glycines, Meloidogyne Sumitomo Chemical do Brasil
Lumialza 6.1 x 1010 CFU / mL
liquefaciens incognita, Pratylenchus brachyurus Representações Ltda
Meloidogyne incognita, Meloidogyne
Bacillus amylo- 1 x 1010 endospores Sumitomo Chemical do Brasil
Trunemco javanica, Pratylenchus brachyurus,
liquefaciens / mL Representações Ltda
Rotylenchulus reniformis
Meloidogyne incognita, Vittia Fertilizantes e Biológicos
Bacillus subtilis Baci-Attack 1 x 108 CFU / mL
Meloidogyne javanica S.A.
Meloidogyne incognita, Vittia Fertilizantes e Biológicos
Bacillus subtilis Baci-Guard 4 x 108 CFU / mL
Meloidogyne javanica S.A.
Meloidogyne javanica, Meloidogyne
incognita, Meloidogyne exigua, Me- Vittia Fertilizantes e Biológicos
Bacillus subtilis Biobaci 1 x 108 CFU / mL
loidogyne paranaensis, S.A.
Pratylenchus zeae
Bacillus amylo- Vittia Fertilizantes e Biológicos
Nema-Attack 3 x 109 CFU / mL Meloidogyne incognita
liquefaciens S.A.
Bacillus amylo- Vittia Fertilizantes e Biológicos
Nema-Guard 3 x 109 CFU / mL Meloidogyne incognita
liquefaciens S.A.

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 Andressa C. Z. Machado (35-49)

Table 1. Continued
Biological Commercial Concentration Biological target Company
agent product
Heterodera glycines,
Bacillus amylo- Vittia Fertilizantes e Biológicos
No-Nema 3 x 109 CFU / g Meloidogyne incognita, Meloidogyne
liquefaciens S.A.
javanica, Pratylenchus brachyurus
Bacillus 3.5 x 1011 endo- Biotrop Soluções Biológicas e
Bionema Meloidogyne incognita
velezensis spores / L Participações Ltda
Biotrop Soluções Biológicas e
Bacillus subtilis Furatrop 1.9 x 1012 CFU / L Meloidogyne javanica
Participações Ltda
Biotrop Soluções Biológicas e
Bacillus subtilis Nematrop 1.9 x 1012 CFU / L Meloidogyne javanica
Participações Ltda
Biotrop Soluções Biológicas e
Bacillus subtilis Promobio 1.9 x 1012 CFU / L Meloidogyne javanica
Participações Ltda
Biotrop Soluções Biológicas e
Bacillus subtilis Paladyo 1.9 x 1012 CFU / L Meloidogyne javanica
Participações Ltda
Bacillus 3.5 x 1011 endo- Biotrop Soluções Biológicas e
Rudder Meloidogyne incognita
velezensis spores / L Participações Ltda
Bacillus amylo- Meloidogyne incognita, Meloidogyne
Boneville 1 x 1010 CFU / g Koppert do Brasil Holding Ltda
liquefaciens javanica, Pratylenchus brachyurus
Bacillus amylo- Meloidogyne incognita, Meloidogyne
Chevelle 1 x 1010 CFU / g Koppert do Brasil Holding Ltda
liquefaciens javanica, Pratylenchus brachyurus
Bacillus amylo- Meloidogyne incognita, Meloidogyne
Veraneio 1 x 1010 CFU / g Koppert do Brasil Holding Ltda
liquefaciens javanica, Pratylenchus brachyurus
Nemacontrol / Pratylenchus brachyurus / Simbiose Indústria e Comércio
Bacillus amylo- 5 x 109 CFU / mL
Nemacontrol Pratylenchus brachyurus de Fertilizantes e Insumos Mi-
liquefaciens 1 x 1010 CFU / mL
Super Meloidogyne javanica crobiológicos Ltda
Bacillus methy- Onix / Onix Meloidogyne javanica, Lallemand Soluções Agrobi-
1 x 109 CFU / g
lotrophicus OG* Pratylenchus brachyurus ológicas Ltda
Rizos / Rizos Meloidogyne javanica, Lallemand Soluções Agrobi-
Bacillus subtilis 3 x 109 CFU / mL
OG* Pratylenchus brachyurus ológicas Ltda
Bacillus licheni-
1 x 1011 + 1 x 1011 Meloidogyne incognita,
formis + Bacil- Presence FMC Química do Brasil Ltda
CFU / g Pratylenchus brachyurus
lus subtilis
Meloidogyne incognita, Meloidogyne
Bacillus licheni-
1 x 1011 + 1 x 1011 javanica, Meloidogyne graminicola,
formis + Bacil- Quartzo FMC Química do Brasil Ltda
CFU / g Meloidogyne exigua, Pratylenchus
lus subtilis
brachyurus, Radopholus similis
Bacillus li-
cheniformis + Profix / Pro- Agrivalle Brasil Indústria e Co-
1 x 1010 + 1 x 1010 + Meloidogyne incognita,
Bacillus subtilis fix-A / Profix-B mércio de Produtos Agrícolas
1 x 109 CFU / g Pratylenchus brachyurus
+ Paecilomyces / Profix-C S.A.
lilacinus
Paecilomyces Agrobiológica Sustentabilidade
ATIALY 1 x 105 CFU / g Meloidogyne incognita
lilacinus S.A.
Paecilomyces
BN40.001/19* 7.5 x 109 CFU / g Meloidogyne incognita Ballagro Agro Tecnologia Ltda
lilacinus
Paecilomyces Meloidogyne incognita, Meloidogyne
Nemat 7.5 x 109 CFU / g Ballagro Agro Tecnologia Ltda
lilacinus javanica, Pratylenchus brachyurus
Paecilomyces
Nettus* 7.5 x 109 CFU / g Meloidogyne incognita Ballagro Agro Tecnologia Ltda
lilacinus
Paecilomyces Purpureonyd
6.5 x 107 CFU / g Meloidogyne incognita TZ Biotech Ltda
lilacinus FR 25
Pochonia 5.2 x 107 chlamydo-
Rizotec Meloidogyne javanica Rizoflora Biotecnologia Ltda
chlamydosporia spores / g

38 RAPP - Volume 28, 2022

 Andressa C. Z. Machado (35-49)

Table 1. Continued
Biological Commercial Concentration Biological target Company
agent product
Pochonia PC-ATTACK / Vittia Fertilizantes e Biológicos
1 x 106 CFU / mL Meloidogyne javanica
chlamydosporia PC-GUARD S.A.
Pochonia Vittia Fertilizantes e Biológicos
RIZO-TURBO 1 x 106 CFU / mL Meloidogyne javanica
chlamydosporia S.A.
Trichoderma Trianum DS /
1 x 108 CFU / g Pratylenchus brachyurus Koppert do Brasil Holding Ltda
harzianum Trianum WG
Trichodermil
Trichoderma SC 1306/ Trich-
2 x 109 conidia / mL Pratylenchus zeae Koppert do Brasil Holding Ltda
harzianum odermil Super
SC 1306
Trichoderma TRICHO-TUR- 1 x 1010 conidia / Vittia Fertilizantes e Biológicos
Pratylenchus brachyurus
harzianum BO mL S.A.
*Bionematicide with approved use on organic agriculture.

Figure 1. Main modes of action of different biological control agents on nematodes.

RAPP - Volume 28, 2022 39

 Andressa C. Z. Machado (35-49)

Pasteuria nishizawae. Only two bionemati- Trichoderma spp. There are four bionemat-
cides are registered in Brazil with P. nizhizawae as icides with T. harzianum as the active ingredient
the active ingredient (Table 1) (AGROFIT 2021). This registered for nematode control in Brazil (Table 1).
species is recommended for the control of H. gly- Pratylenchus brachyurus and P. zeae are the biolog-
cines, since the bacteria in this genus are character- ical targets for all these bionematicides (AGROFIT
ized as obligatory parasites of nematodes with high 2021), and this can be attributed to the high capaci-
specificity. For instance, P. nishizawae is a parasite of ty of Trichoderma spp. to induce resistance in plants.
H. glycines, P. penetrans of Meloidogyne spp., and P. The colonization of roots by Trichoderma spp. in-
thornei of Pratylenchus spp. (PRESTON et al. 2003); duces physiological changes in plants that lead to
no bionematicide is available with this last two spe- the activation of defense mechanisms (Figure 1).
cies in its composition. This specificity could be con- So, plants try to stop the endophytic colonization
sidered as an advantage in comparison to non-se- of Trichoderma spp. through the reinforcement of
lective chemical nematicides that interfere on the the cell walls and through the accumulation of an-
micro and meso fauna present in the soil ecosystem, timicrobial compounds and reactive oxygen species
but also as a challenge to use Pasteuria spp. as a bi- (MARTÍNEZ-MEDINA et al. 2013). After this initial
ological control agent (ORR et al. 2020). defense, the expression of defense genes returns to
The formulation of the two bionematicides the pre-infectional levels, allowing the development
is composed by bacterial spores, a resistant struc- of the fungus as an avirulent endosymbiont (MASU-
ture that allows the survival of this microorganism NAKA et al. 2011).
under unfavorable conditions. These spores adhere After the attack of a biotrophic pathogen, as
to the cuticle of nematodes during its moving in the the sedentary nematodes, the plant local reaction
soil (Figure 1), remaining dormant until the nema- is the programed cell death, called hypersensitive
tode initiates the parasitism. So, a germinative tube reaction, followed by a systemic response that pre-
penetrates the cuticle and grows into the nematode vents the infection of healthy tissues not infected by
body, where the bacteria extract the nutrients nec- the nematode; this response is known as Systemic
essary to its development (DAVIES et al. 1988). Col- Acquired Resistance (SAR) and is mediated by sali-
onizing the interior of the nematode, Pasteuria spp. cylic acid (MARTÍNEZ-MEDINA et al. 2017). For her-
compromise the nematode reproduction, since the bivores, necrotrophic pathogens, and migratory en-
reproductive system can be completely damaged doparasitic nematodes, the plant reaction is called
by the bacteria (DAVIES et al. 2011). A number of Systemic Induced Resistance (SIR) and is regulat-
approximately 40 bound endospores that effective- ed by jasmonic acid and ethylene (LEONETTI et al.
ly encumber a nematode juvenile prevents root 2014). During the feeding, Pratylenchus spp. induce
infection (STIRLING 1984), but more than 100 en- cytoplasmic streaming and rarely cell death, but
dospores may bind to the cuticle of the nematode, their migration into roots induces cell death along
suppressing the infection of plants by this pathogen the migration path (MATHEW & OPPERMAN 2020).
(PRESTON et al. 2003). The resistance induced by Trichoderma spp.
The spores used in the formulation increase can generate a priming effect, which allow that the
the shelf life of the bionematicides and allow the resistance mechanisms are activated more quick-
survival of the bacteria between the cropping sea- ly and effectively when the plant is challenged by
sons. However, it is difficult to develop protocols for different pathogens, as a “collection” of different
Pasteuria spp. propagation outside of the nematode stresses (PASCHOLATI et al. 2019). The priming ef-
host that allow the production of endospores for fect generated by Trichoderma spp. was reported to
field application. Besides, as spores are immobile be transgenerational, i.e., when parental plants are
and Pasteuria spp. do not have saprophytic abilities, pre-conditioned, plants from the next generation
the efficiency of bionematicides formulated with showed the same level of resistance to nematodes
these microorganisms is dependent on the presence without fitness costs (MEDEIROS et al. 2017).
of the mobile forms of the nematode, the juveniles, In addition to this effect, Trichoderma spp.
that are the main stage used by these bacteria to can also produce toxic compounds to nematodes
initiate its parasitism (PRESTON et al. 2003). that reduce hatching and cause mortality of juve-

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 Andressa C. Z. Machado (35-49)

niles in in vitro studies, can prevent nematode pen- LA-LÓPEZ et al. 2013). Its endophytic behavior in
etration by the colonization of roots that leads to some plant species can also result in activation of
competition for feeding sites (VARGAS et al., 2009), plant defense mechanisms against soil-borne patho-
and can parasitize nematode eggs and juveniles gens, as nematodes (MACIÁ-VICENTE et al. 2009).
(ZHANG et al., 2017). The best formulations should use chlam-
ydospores of P. chlamydosporia, since conidia and
Purpureocillim lilacinum. This is an oppor- hyphal fragments are sensitive and show lower
tunistic fungus that parasites eggs, juveniles, and survival rates in comparison to chlamydospores,
adults of different nematode species (Figure 1). that are resistance structures specialized for sur-
There are six bionematicides available in Brazil with vival (DALLEMOLE-GIARETTA et al. 2011). These
this fungus in their composition, five of them formu- resistance structures have food reserves to allow
lated exclusively with P. lilacinum and one formulat- the establishment of the fungus without the addi-
ed in mixture with Bacillus spp. (Table 1). The main tion of supplementary energy sources (MAUCHLINE
biological targets are Meloidogyne spp. (AGROFIT et al. 2002), on the contrary of conidia and hyphal
2021) and several studies showed that the efficien- fragments, that can get into fungistasis if no sup-
cy of control conferred by P. lilacinum on sedentary plementary energy source is provided (KERRY et al.
nematodes can reach 70% (DALLEMOLE-GIARETTA 1993). In this regard, to improve the performance
et al. 2012). The chitinolytic ability of this fungus is of P. chlamydosporia in relation to the control of M.
responsible to the success in its parasitism, which javanica, Escudero et al. (2016) associated chitosan
initiates with the infection of eggs and sedentary as a supplementary energy source to fungi suspen-
females by the fungal hyphae that secrete extra- sion containing hyphal fragments and obtained an
cellular enzymes, as chitinases and proteases, de- increase in the infectivity and efficacy of the fungus
grading the eggshells and the cuticle of the female in the suppression of nematode populations, in in
body. Hyphae absorb the cellular content from eggs vitro experiments.
and sedentary females, acquiring essential nutrients
for their development and reproduction (MORTON CHALLENGES IN THE DEVELOPMENT OF BIOLOGI-
et al. 2004). The egg masses deposited by Meloi- CAL BIOPESTICIDES
dogyne spp. sedentary females can be completely In Brazil, the development of a biological
parasitized by P. lilacinum, which leads to alterations product takes around five years, and the cost esti-
in the embryogenic development of the juveniles in- mated is about US$ 7 million. The process is initi-
side eggs and to unhatched eggs (AHMED & MONJIL ated with the research of novel biological agents, a
2019). step that involves the identification of these organ-
Purpureocillium lilacinum also produces isms, the establishment of protocols for fermenta-
toxic substances to migratory nematodes, as P. tion process, previous in vitro evaluations against
brachyurus. Although not completely character- different biological targets, and the identification of
ized, these substances immobilize the juveniles and metabolites generated by the organism during its
prevent their penetration into roots (KHAN et al. fermentation. The next step is the production and
2006). This fungus also induces resistance in plants, formulation of the product, which involves the en-
through salicylic acid- or jasmonic acid-triggered re- hancement of the multiplication process of the or-
sponses (GHAHREMANI et al. 2019), as detailed for ganism, the development of a quality control proto-
Trichoderma spp. col, and the evaluation of performance and stability
of the formulation (MARRONE 2019).
Pochonia chlamydosporia. Only three bi- After this, the formulation follows to field
onematicides are available in Brazil composed by P. evaluations, when studies are conducted under
chlamydosporia (Table 1). The mode of action of this greenhouse and field conditions to determine the
fungus (Figure 1) is quite similar to that described efficacy in large scale and, if necessary, to indicate
to P. lilacinum (ESCUDERO et al. 2016; PODESTÁ et formulation adjustments. The final step analyzes the
al. 2016) and it is also a saprophytic species in the security of the product and finalize with the approv-
absence of plants and nematode hosts (MANZANIL- al and register of the new product; for this, com-

RAPP - Volume 28, 2022 41

 Andressa C. Z. Machado (35-49)

panies must generate dossiers containing studies present, the product can be lost by drift or run-off;
that ensure the security of the formulation, that are so, formulations should contain additives, as surfac-
submitted to the governmental regulators (in Brazil: tants or adjuvants to ensure the efficacy of control.
Brazilian Ministry of Agriculture, Livestock and Food Nevertheless, some additives can be bioincompati-
Supply (MAPA), Brazilian Health Regulatory Agency ble and this is one of the reasons why several prod-
(ANVISA), and Brazilian Institute of Environment and ucts with living organisms do not contain these sub-
Renewable Natural Resources (IBAMA)), that can stances (SKRABANIA 2019).
give the permission or deny the registration of the Another challenge is the high cost of invest-
new biopesticide (MARRONE 2019). ment required for research and development of
Although, all these steps need to be trans- formulations that ensure the survival of the biolog-
posed by companies to register a new bionemati- ical control agent under unfavorable conditions of
cide. Brazil has a modern regulatory apparatus, in storage and application in the field, as well as that
agreement with international guidelines and regula- ensure compatibility under mixture with other ag-
tions. For example, we have specific pioneering leg- ricultural products. In addition, the stability of the
islation on the evaluation of microbiological prod- formulation to degradation by UV light can also be
ucts for phytosanitary use (RDCs 194 and 195/2002 challenging. It is important because the majority of
– ANVISA; IN 95/2020 - MAPA). According to the Na- crops in Brazil are cultivated under the conventional
tional Bioinput Program (PNB), there is a clear public tillage, which represents 45% of the soil cultivation
policy for financing production and use of biological system (IBGE 2017) and involves soil disturbance;
inputs in Brazil, offering credit lines and financing of the soil is exposed until the establishment of the
up 30% of the capital costs invested in the construc- next crop and sowing is often done in dry soil con-
tion of biofactories (GAZZONI 2021). ditions, reducing the chances of a biological control
However, although the government incen- agent to establish itself properly. One of the ways to
tives and the fact that several new bionematicides protect the organism in the formulation is by using
are available for growers in Brazil, some challenges microencapsulation techniques that improve stabil-
need to be transposed and new alternatives should ity and can be used to control the rate of release of
be evaluated. The first challenge to be addressed the organism (BULLOCK 2019).
is the training and capacitation of distributors and Moisture and temperature can be critical
growers in the correct use of the different biological factors influencing the survival of fungal and bacte-
control agents. Companies in Brazil are investing in rial agents. Under dry conditions, the metabolism of
studies to guarantee more precise positioning of the some organisms is reduced to allow their survival in a
bionematicides in each crop and under the different dormant state, as the survival specialized structures
Brazilian edaphoclimatic conditions. CropLife Brasil of some fungi, as the chlamydospores produced by
(CLB) provided a website (https://croplifebrasil.org/) P. chlamydosporia (MASSOLA JÚNIOR 2018). Anoth-
with general information on technical aspects of the er strategy for survival is the sporulation of some
biological control and all the regulatory processes bacteria, as Bacillus spp., in which the bacterial ge-
involved in the registration of biological products in nome is sequestered in the spore (or endospore),
Brazil, that helps technicians, companies, and grow- a survival structure, until the environmental condi-
ers to develop and use biological control agents. tions return to adequate levels for germination of
Besides, the understanding on the mode of this spore (McKENNEY et al. 2013). Therefore, if en-
action of the different biological control agents (Fig- vironmental conditions are unfavorable to biological
ure 1), ensure that they will be used for the specific control agents, they can go into dormancy and nem-
target and under the best formulation and applica- atodes present in the soil will penetrate roots and
tion technology to allow maximum efficiency. The develop normally until the organisms return to the
inclusion of bionematicides in the precision agricul- normal activity, leading to lower and/or inconsistent
ture programs could also enhance the efficiency of efficacy compared to chemical nematicides, readily
the biological control agent (FARIA JUNIOR 2017). available in the soil.
Even when the biological control agent is applied In addition, for bionematicides formulated
correctly in the site where the biological target is with bacterial endospores, as those composed by

42 RAPP - Volume 28, 2022

 Andressa C. Z. Machado (35-49)

Bacillus spp. and Pasteuria spp., the difficulties in In addition to the inherent aspects of the
inducing the production of endospores in in vitro commercial bionematicides, as formulation, which
cultures in large scale for field application is a chal- could impact directly in the shelf life of these prod-
lenge. Sequencing of the genomes of these bacteria ucts, some strategies can be adopted by growers
could help in the identification of their metabolic to guarantee better results when using bionemati-
capabilities and limitations to optimize the in vitro cides in tropical and subtropical climates. In Brazil,
multiplication. Besides, bioinformatic tools could bionematicides are applied mainly through seed
help in the selection of isolates of parasitic bacteria treatment and, to a lesser extent, in furrow and via
more aggressive in the attachment, infection, and drench (MACHADO et al. 2016). In crops like cotton,
germination in different species of plant-parasitic bacteria are the preferred agents to be used as seed
nematodes (PRESTON et al. 2003). treatment, especially those from the genus Bacillus,
Another important challenge to the biologi- while fungi are applied in furrow (MACHADO 2021).
cal control market of nematodes in Brazil is the ex- This strategy could be a good option con-
istence of non-regulated bionematicides, without sidering that cotton monoculture during the sum-
registration in the Brazilian Ministry of Agriculture, mer season is the main production system in Brazil
Livestock and Food Supply. These bionematicides do (LAMAS et al. 2016), with intense soil disturbance
not ensure the quality, the purity, and the efficien- that could interfere in the survival of biological or-
cy on the nematode control under field conditions, ganisms. The use of spore-forming bacteria as seed
leading to lack of control and discredit of this tool. treatment in this situation could increase the effi-
Moreover, the on-farm technology, when the grow- ciency of control, since endospores are survival
er produces the biological control agent in his farm structures which allow bacteria to survive under
with low or no control of inoculum and fermentation unfavorable conditions. On the other hand, in the
process, can result in the contamination and repro- in-furrow application in fields where cover crops
duction of other microorganisms that can be patho- are used in mid-season, fungi could also be applied
genic to the crops, harmful to the environment, and at sowing, or in the debris following desiccation of
also to the applicator. Brazilian government must the cover crop prior to cotton or another main crop,
legislate laws to regularize this situation through when soil moisture and temperatures are regulated
strict quality control rules to ensure the credibility by the mulch, allowing the establishment and devel-
of this management tool (FARIA JUNIOR 2017). opment of fungi (MACHADO, 2021). Cover crops and
crop rotation could also improve the organic matter
CHALLENGES IN THE USE OF BIONEMATICIDES IN content of soils, that is important to the establish-
TROPICAL AND SUBTROPICAL CLIMATES ment of the biological agent.
Tropical and subtropical climates represent In soybean fields, bionematicides are used
an additional challenge for the use of biological con- essentially as seed treatment and few options to in
trol agents, especially due to the high temperatures furrow applications are available (AGROFIT 2021).
which often are inadequate to the survival of the However, Silva et al. (2020) emphasized that the
organism. Under these climates, several nematode seed treatment with bionematicides as the only tool
species can be present together in the same field to manage nematodes in soybean fields does not
and this is limiting when species-specific organisms provide the necessary protection against the dam-
are used in the biological control, as Pasteuria spp. ages caused by nematodes, mainly when soil nema-
Warm climates also allow nematode population den- tode populations are high. On the other hand, under
sities to increase significantly during the cropping field conditions, when fungi agents were applied in
season (GRECO & DI VITO 2009). In the Brazilian Cer- furrow in the cover crops succeeding soybean for
rado region, temperatures do not vary greatly be- the management of P. brachyurus, yields increased
tween seasons and crops are subsequently cropped 180 kg per hectare in comparison with plots that re-
in the field, allowing nematodes to reproduce con- ceived only the cover crop treatment (SILVA et al.
tinuously in the presence of the host and favorable 2020). The organic matter delivered by the cover
soil moisture content and optimal temperatures for crops also favor the development of microorgan-
their development. isms that can parasitize eggs and even the cyst of

RAPP - Volume 28, 2022 43

 Andressa C. Z. Machado (35-49)

H. glycines, positively impacting the management of gressive to coffee plants than M. paranaensis, whose
this important nematode in soybean crops. For the management must include a resistant cultivar allied
management of root-knot nematodes in soybean, with other management tools to avoid the damages
fungi are preferred, since the main target of the caused by this nematode. Therefore, studies should
fungal-based bionematicides is Meloidogyne spp. also contemplate M. incognita and M. paranaensis
(AGROFIT 2021). Greenhouse experiments have to validate the results obtained for M. exigua.
been showing that these organisms reduce around
60% of the root-knot nematode populations, in con- FUTURE PROSPECTS
trolled environment; however, under fields condi- Despite the expansion of the bionematicide
tions, the efficacy of fungi used as seed treatment in market in Brazil, few minor crops are contemplated
soybean is variable (SILVA et al. 2020). in the development of new products. For instance,
Despite the promising results found for cot- we have regional problems with nematode species
ton and soybean, the management of nematodes different from the main targets of bionematicides
in perennial crops, like coffee, is difficult because (Table 1), as M. paranaensis in coffee (OLIVEIRA &
plants remain in the field for several years; in trop- ROSA 2018), M. enterolobii in guajava, acerola, and
ical and subtropical climates, where temperature is vegetables (CARNEIRO 2003; PINHEIRO 2017), the
not a limiting factor to the development of nema- rice complex of root-knot nematodes, including M.
todes, it is expected to occur high increases in the graminicola (MATTOS et al. 2017), the yam nema-
nematode populations during the crop cycle. Unfor- todes P. coffeae and Scutellonema bradys (PINHEIRO
tunately, few studies are conducted with other pe- et al. 2016), the red-ring coconut nematode Bur-
rennial crops and bionematicides except coffee. saphelenchus cocophilus (WARWICK 2001), or the
In studies conducted under greenhouse con- aerial and bulb nematodes Aphelenchoides spp. and
ditions, bionematicides were used to manage the Ditylenchus dipsaci (MEYER et al. 2017; PINHEIRO et
most damaging nematode species to coffee planta- al. 2014). All of them are difficult to manage with
tions in Brazil, M. paranaensis, but none of the eval- resistant cultivars or crop rotation and any chemi-
uated bionematicides were effective in reducing the cal nematicide is available for the control of these
nematode population, although the application of targets (AGROFIT 2021). Bionematicides could be
P. lilacinum in furrow allowed better development an excellent option for the management of these
of plants (ARITA et al. 2020). Under field conditions, nematodes, especially in organic farms. Companies
cover crops or green manures intercropped with should invest some efforts to include these “mi-
coffee plants could improve the management of nor nematode species” as biological targets of the
nematodes, due to the organic matter and the fa- bionematicides, improving yields and fruit quality
vorable microclimate for the establishment of bio- where other management tools are unavailable or
logical control agents. fail.
The mixture of biological control agents could Besides, from 47 commercial bionematicides
also improve the efficacy of the biological control of recommended for nematode management in Brazil,
nematodes in coffee plants. Under greenhouse con- we have only 11 biological agents, in which Bacillus
ditions, Tolardo (2018) observed that the mixture spp. correspond to 60% of them (AGROFIT 2021).
of Bacillus subtilis + B. methylotrophicus + Tricho- The difficulty in discovering new chemical molecules
derma asperellum demonstrated similar efficiency and the costs associated with the development of
to reduce M. exigua population densities than that chemical nematicides make this poor explored uni-
obtained with the use of resistant cultivars. In a field verse of macro- and microorganisms attractive,
experiment, effective control of M. exigua was also especially for small companies (MARRONE 2019).
observed by Arpini et al. (2018), when a bionemati- Several microorganisms are reported to be effec-
cide formulated with the mixture of B. subtilis and B. tive against plant parasitic nematodes under in vi-
licheniformis (Quartzo®) was applied at high dosages tro conditions, but only a few of them are successful
twice (200 g of the commercial product per hectare biocontrol agents, mainly because of the difficulties
per application) at intervals of 60 days. However, it in laboratory culturing, or to access strains from col-
is important to emphasize that M. exigua is less ag- lections or soils, or due to the low effectiveness in

44 RAPP - Volume 28, 2022

 Andressa C. Z. Machado (35-49)

nematode control (SIDDIQUI & MAHMOOD 1996). of secondary metabolites, as alkaloids and steroids,
An alternative is the use of metabolites of these or- which can be toxic to nematodes (CARVALHO et al.
ganisms as the active ingredient of bionematicides. 2015).
However, not all natural biochemicals are regulated In addition to the search for new biologi-
as biopesticides; for this to happen, the substance cal control agents, long-term field studies must be
needs to have a non-toxic mode of action to the pest conducted to demonstrate the correct interval for
or pathogen, as the resistance inducers. Substances application of bionematicides, considering the wide
with a toxic mode of action to nematodes are regu- discrepancies found in climates, soil types, and crop
lated as chemicals (MARRONE 2019). systems between different Brazilian agricultural ar-
Some microorganisms have been studied eas. Besides, there is no concise and reliable infor-
and explored for nematode control worldwide, as mation on the effect of mixtures of different micro-
Myrothecium verrucaria, a fungus that compose the organisms, whether in the same bionematicide or in
bionematicide DiTera® (Valent BioSciences) and Bur- different products applied together or in rotation.
kholderia rinojensis, the bacteria from Majestene® After several years of research with bionematicides,
(Marrone Bio Innovations) (MARRONE 2019). Both results from the IDR´s Nematology laboratory led
bionematicides are not available for Brazilian grow- to believe that not necessarily bionematicides that
ers, but these organisms could be collected, isolat- have more than one organism in their composition
ed, and studied by local companies. are better than those that contain only one in their
The saprophyte bacteria Pseudomonas spp. formulation. It could be explained by the proper iso-
are used as active ingredients of biopesticides late used as active ingredient, which can be more
around the world and some species, as P. fluo- aggressive against the nematode itself, or more ag-
rescens, P. aeruginosa, and P. protegens have already ile in colonization of the substrate or root surface
demonstrated their potential in the nematode con- as a saprophyte or endophyte gaining an adaptive
trol. The mode of action involves the destruction of advantage, or even producing more toxic substanc-
the egg masses, interferences in the hatching, and es in its secondary metabolism that allow it to have
the cleavage of the ethylene precursor, which inhibit a higher nematicide effect.
the production of this hormone that is important in Considering the Brazilian biodiversity rich-
the development of galls in roots infected by Meloi- ness, this universe of new macro- and microorgan-
dogyne spp. (GLAZER et al. 1985; SEENIVASAN et al. isms can be explored for the development of new
2012; TAVAKOL-NORABADI et al. 2014). bionematicides. Expectations of an increase in this
Bacillus thuringiensis is also a potential or- market are optimistic and can attract small compa-
ganism to be used in the management of nema- nies, startups, and large investors to supply this in-
todes. The Cry proteins, that are pore-forming tox- creasing biological control market in Brazil.
ins used as insecticides, produced by this bacterium
have been demonstrated their potential to reduce REFERENCES
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