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Survey of Entomopathogenic
Nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) in Rio Grande do Sul State, Brazil
ARTIGO
Survey of Entomopathogenic Nematodes (Rhabditida: Heterorhabditidae,
Steinernematidae) in Rio Grande do Sul State, Brazil
Carla R.C. Barbosa-Negrisoli1, Mauro S. Garcia1, Claudia Dolinski2*, Aldomario S.
Negrisoli Jr.1, Daniel Bernardi1 & Fioravante J. dos Santos3
Laboratório de Biologia de Insetos e Controle Biológico, Universidade Federal de Pelotas, P.O. Box 354, 96010-900,
Pelotas (RS) Brazil.
2
Laboratório de Fitopatologia e Entomologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, 28013-602,
Campos de Goytacazes (RJ) Brazil.
3
Laboratório de Solos, Universidade Federal de Pelotas.
*Corresponding author: [email protected]
1
Recebido para publicação em 18 / 04 / 2010. Aceito em 17 / 11 / 2010.
Editado por Luiz Carlos C.B. Ferraz
Summary - Barbosa-Negrisoli, C.R.C., M.S. Garcia, C. Dolinski, A.S. Negrisoli Jr., D. Bernardi & F.J. Santos.
2010. Survey of entomopathogenic nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) in Rio Grande
do Sul State, Brazil.
Entomopathogenic nematodes (EPNs) have been found in different ecosystems. It is generally accepted
that natural habitats have the highest probability of the occurrence of native species suitable for mass release
against local pests, because they are adapted to the climate and other population regulators. The introduction
of exotic EPNs may have a negative impact on the native non-target organisms. Therefore, it is important to
determine the occurrence of native EPNs in a particular area, and this study aimed to search for EPN species
in Rio Grande do Sul State, Brazil. From the 121 soil samples collected, 15.7 % contained EPNs (9.9 %
steinernematids and 5.8 % heterorhabditids). Steinernema feltiae, S. rarum and S. riobrave were isolated for the first
time in the country. Steinernema rarum and Heterorhabditis bacteriophora were the most common EPNs found
(73.6 %). The data showed highest prevalence of EPNs in the north-northeast regions, in sandy soils, at
temperatures up to 25 ºC, from 700 to 1,100 m of altitude. H. bacteriophora and S. rarum were recorded at sea
level. Although the number of samples collected was not sufficient to be representative of all the species that
occur in this region of Brazil, the current data are expected to be important for use in local pest control
programs.
Key words: Heterorhabditis, Steinernema, occurrence, abiotic factors.
Resumo - Barbosa-Negrisoli, C.R.C., M.S. Garcia, C. Dolinski, A.S. Negrisoli Jr., D. Bernardi & F.J. Santos.
2010. Isolamento de nematóides entomopatogênicos (Rhabditida: Heterorhabditidae, Steinernematidae) no
Estado do Rio Grande do Sul, Brasil.
Nematoides entomopatogênicos (NEPs) estão presentes em vários ecossistemas. Em habitats naturais é
maior a probabilidade de ocorrência de espécies nativas, que podem ser mais adequadas para liberações
inundativas contra pragas locais devido à adaptação ao clima e a outros reguladores populacionais. A introdução
de NEPs exóticos pode ter um impacto negativo nos nematoides nativos. Portanto, este estudo teve como
objetivo amostrar áreas nativas do Estado do Rio Grande do Sul, Brasil, para se conhecer as espécies de NEPs
ali existentes. De 121 amostras de solo coletadas, 15,7 % continham NEPs (9,9 % esteinernematídeos e 5,8 %
heterorrabditídeos). Steinernema feltiae, S. rarum e S. riobrave foram isoladas pela primeira vez no país. Steinernema
rarum e Heterorhabditis bacteriophora foram os NEPs mais comumente encontrados (73,6 %). A maior incidência
de NEPs foi obtida nas regiões norte e nordeste, em solos arenosos, até 25 ºC, e entre 700 a 1.100 m de
Nematologia Brasileira 189
Piracicaba (SP) Brasil
Carla R.C. Barbosa-Negrisoli, Mauro S. Garcia, Claudia Dolinski, Aldomario S. Negrisoli Jr., Daniel Bernardi & Fioravante J. dos Santos
altitude. H. bacteriophora e S. rarum foram registrados ao nível do mar. Embora o número de amostras coletadas
não fosse suficiente para descrever todas as espécies de NEPs ocorrentes no Estado, os dados obtidos deverão
ser úteis em programas futuros de biocontrole de pragas locais.
Palavras-chaves: Heterorhabditis, Steinernema, ocorrência, fatores abióticos
Introduction
Entomopathogenic nematodes (EPNs) of the
genera Steinernema and Heterorhabditis (Rhabditida:
Steinernematidae, Heterorhabditidae) are
cosmopolitan, being present in soils and sediments in
several ecosystems, limited by water availability. They
move through the pores and water film that cover
soil particles traveling short distances, depending on
environmental conditions, in their search for a host to
feed and reproduce on (Treonis & Wall, 2005). EPNs
have an important role in controlling various soil insect
species (Kaya, 1990), and they are frequently detected
in most terrestrial habitats either in natural, agricultural
or other disturbed soils (Hominick, 2002).
Various searches of EPNs have been carried out
in natural habitats throughout the world, as previously
summarized by Hominick (2002). In Brazil, EPNs
were found in the states of Minas Gerais (MolinaAcevedo et al., 2005), Rondônia (Dolinski et al., 2008)
and Piauí (Barbosa-Negrisoli et al., 2007), among
others.
As a result of these studies, new species of EPNs
have being described worldwide and investigation
dealing with their population dynamics are crucial to
understand their persistence, distribution and effect
on local insect populations (Hominick & Reid, 1990).
In addition, climate parameters such as precipitation,
relative humidity, air and soil temperature influence
persistence of EPNs in the soil (Mrácek et al., 2005).
Natural habitats present a higher probability of
occurrence of native species, serving as an important
source in relation to biodiversity and use in biocontrol
(Stock & Gress, 2006). These species can be more
suitable to mass release against local pests due to their
adaptation to the local climate and other population
regulators (Bedding, 1990). In addition, many countries
consider that the introduction of exotic EPNs may
result in negative impact on the native non-target
organisms (Bathon, 1996; Dolinski & Moino Jr., 2006).
The present study aimed to determine the
190 Vol. 34(4) - 2010
occurrence and prevalence of the genera Heterorhabditis
and Steinernema in different areas of Rio Grande do
Sul State (RS), Brazil, in relation to abiotic factors such
as habitat, altitude, and soil (type, texture, and
temperature).
Material and Methods
Soil sampling was done in the regions of Central
Depression (CD), Central Plateau (CP), Coastal Plain
(CTP), Medium Plain (MP) and South Plain (SP),
comprising agronomic crops, pastures and native
forests cultivated in RS, covering an area of
approximately 150.000 km2.
Soil samples were collected by hoeing and
shoveling to a depth of 15 to 20 cm, and each sample
consisted of ten 100 g-sub-samples. The sub-samples
were mixed in buckets, placed in plastic bags and
transported in Styrofoam boxes to keep them at 20 º
to 25 ºC (Kaya & Stock, 1997). Each bag was labeled
with: date, place, associated habitat, altitude,
geographical position (latitude and longitude) and soil
temperature taken at 20cm depth. The sampling route
was planned to comprise the different RS regions,
and the number of samples for each region was taken
at random.
In the laboratory, soil samples were wetted with
distilled water when necessary, up to field capacity.
According to the modified methodology of Bedding
& Akhurst (1975), each sample was divided into two
plastic containers (14 x 14 x 7 cm), to which ten last
instar larvae of Galleria mellonella (Lepidoptera:
Pyralidae) were added. Containers were closed and
inverted so that the insects were in full contact with
soil. The containers were kept at room temperature
(25 ± 3 ºC) and after seven days, the dead larvae with
infection symptoms by EPNs were superficially
disinfested with sodium hypochlorite at 0.1%, placed
in a dry chamber (9 cm Petri dish with filter paper)
and incubated in a germination chamber at 25 ºC,
RH 70 ± 10 % and 12 h photophase. After three
Survey of Entomopathogenic Nematodes (Rhabditida: Heterorhabditidae, Steinernematidae) in Rio Grande do Sul State, Brazil
Results and Discussion
days, the larvae were transferred to modified White
traps (White, 1927) for harvesting of infective juveniles
(IJs). Parasitism was confirmed through the Koch’s
postulates, and the nematodes were multiplied for five
generations in G. mellonella larvae. The isolates were
identified using the morphometrics of IJs and males
(Nguyen & Smart, 1995) and molecular technique
(Dolinski et al., 2008).
The sufficiency of samples was determined by
collector curve or logarithmic regression analysis, from
the cumulative curve of additional species adapted
from Santana & Souto (2006). In order to determine
the relationship of the abiotic factors with the incidence
of EPNs, the percentage (P) of isolated EPNs for
each observed variable [regions, habitats, altitudes and
soils (type, granulometry and temperature)] was
calculated through the relationship between the
number of positive EPN samples and total number
of samples. Also, the total percentage isolation (TP)
was obtained through the relationship between the
total positive samples with nematodes and the total
collected samples, as follows: P = (number of positive
samples in each variable / number of samples taken
in that variable) x 100, and TP = 100 (total number
of positive samples / total number of samples) x
100.
From the 121 soil samples collected, 19 (15.7 %)
were EPN positive (Figure 1, Table 1). EPNs have
been isolated all over the world and the available data
of their prevalence, i.e., percentage of samples that
are positive, can vary drastically, as pointed out and
discussed by Hominick (2002). This variation is largely
due to the fact that they are aggregated, rather than at
random, in distribution, thus requiring a great sampling
effort (= size of sample area, number of samples,
size of samples) and the use of a combination of
extraction techniques to provide that the losses may
be kept to a minimum. The prevalence can also vary
with time, as the existence of local dominant and
comparatively rare EPN species is already well
established; many samples are necessary to recover all
species occurring in a determined region, if this is
accepted as possible. Habitat type and other factors
can also affect the prevalence. In Brazil, previous
attempts to correlate the occurrence of EPNs with
abiotic factors are not available.
Steinernema rarum (36.8 %) and Heterorhabditis
bacteriophora (31.6%) were the most common species
followed by Steinernema sp. (10.4 %), H. amazonensis
(5.2 %), S. feltiae (5.2 %), S. glaseri (5.2 %), and S.
riobrave (5.2 %). Two Steinernema isolates could not be
1
Steinernema sp.
0
1
1
5
0
0
7
36.8
S. riobrave
0
0
0
1
0
0
1
5.2
S. glaseri
1
0
1
4
0
0
6
31.6
S. rarum
% of positive samples (Prevalence)
25.00
25.00
6.97
34.20
33.33
0.00
-
S. feltiae
2
1
2
13
1
0
19
15.7
H. amazonensis
8
4
43
38
3
25
121
H. bacteriophora
Central Depression
Central Plateau
Coastal Plain
Medium Plain
South Plain
Others
Total
TP1
Total number of positive samples
Regions
Total number of samples
Table 1 - Occurrence of entomopathogenic nematodes in different regions of Rio Grande do Sul State, Brazil.
0
0
0
1
0
0
1
5.2
0
0
0
1
0
0
1
5.2
0
0
0
0
1
0
1
5.2
1
0
0
1
0
0
2
10.4
Total percentage.
Figure 1 - Geographic location of the sites from where entomopathogenic nematodes were isolated in Rio Grande do Sul State,
Brazil: Central Depression (CP), Central Plateau (CP), Coastal Plain (CP), Medium Plane (MP) and South Plain (SP).
identified as they did not multiply in G. mellonella. This
study revealed for the first time in Brazil the occurrence
of S. feltiae, S. rarum and S. riobrave. S. rarum was first
isolated in the Province of Córdoba, Argentina
(Doucet, 1986). H. bacteriophora is considered
cosmopolitan (Hominick, 2002) and has been found
in other regions of Brazil, such as in the states of
Pernambuco (Poinar, 1990) and São Paulo
(Vasconcelos et al. 2004). S. glaseri was first recorded
in Brazil in the state of São Paulo, as a parasite of
eggs of Migdolus fryanus, a sugarcane soil pest (Pizano
et al., 1985). H. amazonensis, so far only found in Brazil,
it was originally described from the state of
Amazonas (Andaló et al., 2006).
The EPNs were found in all parts of RS, but most
frequently in the north-northeast region (MP – Medium
Plateau and Above) (Table 1). Despite the fact that
Brazil is considered a tropical country, RS has a
temperate climate, favoring the occurrence of
192 Vol. 34(4) - 2010
steinernematids (Salas-Luévano, 2001), as also reported
in Ireland, where they form 98 % of the insectparasitic nematofauna (Griffin et al., 1991).
Heterorhabditids prevail most in tropical regions
(Roman & Beavers, 1982; Hominick & Briscoe, 1990;
Hara et al. 1991). In Brazil, several authors mentioned
a higher number of heterorhabditids adapted to mild
and hot environments, for example in the states of
Amazonas (Andaló et al., 2006), Minas Gerais (MolinaAcevedo et al., 2005), Rio de Janeiro (C. Dolinski,
UENF, personal observation), Rondônia (Dolinski et
al., 2008), and São Paulo (Fowler, 1988).
Entomopathogenic nematodes were present in
7.69 % to 18.18 % of samples from vegetables, forest,
native pastures, fruit trees and corn crop, and between
21.42 % and 25.00 % of samples within forest,
soybean and tobacco (Table 2). Mrácek et al. (1999)
observed higher frequency of EPNs (> 50%) in areas
with fruit trees, forests and pastures. In agricultural
S. feltiae
S. glaseri
S. riobrave
Steinernema sp
0.0
0.0
0.0
0.0
0.0
16.66
25.00
12.50
7.69
66.66
16.66
21.42
25.00
18.18
-
S. rarum
0
0
0
0
0
1
1
1
1
2
3
3
3
4
19
15.7
H. amazonensis
3
1
1
1
15
3
6
4
8
13
3
18
14
12
22
121
H. bacteriophora
Rice
Oat
Sugarcane
Area under Fallow
Beans
Fruit trees 1
Tobacco
Forest trees (generic)
Horticultural plants 2
Wheat
Native pasture
Forest trees (identified)
Soybean
Corn
Total
TP 4
% of positive samples
Crop
Number of positive samples
Table 2 - Occurrence of entomopathogenic nematodes as sampled in different crops of Rio Grande do Sul State, Brazil.
0
0
0
0
0
0
0
1
1
1
0
1
1
1
6
0
0
0
0
0
1
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
0
0
1
2
1
1
1
7
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
1
1
0
2
Orange, apple and vine.
Splash, potato, pea, watermelon, strawberry, radish and cucumber.
3
Acacia, eucalyptus and pine.
4
Total percentage.
1
2
habitats, the occurrence was lower than 50 % in corn
crop and pasture. Our results differed from the ones
obtained by Mrácek et al. (2005), regarding to the
Czech Republic, who observed a higher prevalence
in fruit trees in relation to native pasture. The same
authors observed low prevalence (10 – 32 %) in
managed apple orchard, cereals and managed pasture;
intermediate prevalence (36.4 – 50 %) in corn crop,
vineyard, and acacia and cowpea plant; high prevalence
(57 – 80 %) in non-managed apple orchard and native
pasture. In the same country, a higher frequency was
observed of S. feltiae (35.9 %), prevailing in pasture
and forests (Mrácek et al., 1999); this was also seen in
the UK and Holland, where the species occupied
pasture and refuge areas (Hominick et al., 1995).
Regarding the soil type, a high incidence of EPNs
was observed in Vertisols (udert) and Alisols (udult)
(100 %), followed by Nitosols (kandiudult) (33.33 %)
and Latosols (undox) (32.14 %) (Table 3). As for
granulometry, heterorhabditids (85.7 %) and
steinernematids (58.4 %) were predominant in sandy
soils (68.4 %) (Table 4). Due to the large diversity, the
soil type has not been a factor related to the prevalence
of EPNs. However, in agreement with the results of
this study, in the Brazilian state of Minas Gerais,
Molina-Acevedo et al. (2005) observed higher EPN
prevalence (66.6 %) in soil with higher sand
proportion (yellow-red Latosol) than in soil with high
clay content (purple Latosol, dark-red Latosol and
yellow-red Podzolic). Similarly, higher prevalence was
observed in light soils in the Czech Republic (Mrácek
et al., 2005), in Hawaii (Hara et al., 1991) and Ireland
(Blackshaw, 1988).
The isolated EPNs were grouped in three soil
temperature ranges (Table 5). In the samples in which
the temperature was below 20ºC (11.76 %) and above
25ºC (11.11 %) there was a higher prevalence of
EPNs. S. feltiae was the only species isolated in the
1
H. amazonensis
S. rarum
S. feltiae
S. glaseri
S. riobrave
Steinernema sp
2
9
1
4
1
1
1
0
19
15.7
H. bacteriophora
21
28
9
35
3
1
1
24
121
% of positive samples (P)
Argisoil
Latosoil
Luvisoil
Neosoil
Nitosoil
Vertisoil
Alisoil
Others
Total
TP1
Soil type
Table 3 - Occurrence of entomopathogenic nematodes in Rio Grande do Sul State, Brazil according to the different types of soil.
9.50
32.14
11.11
11.42
33.33
100
100
0
-
1
3
0
1
0
1
0
0
6
0
1
0
0
0
0
0
0
1
1
3
0
3
0
0
0
0
7
1
0
0
0
0
0
0
1
0
0
0
0
1
0
0
0
1
0
0
1
0
0
0
0
0
1
0
1
0
0
0
0
1
0
2
Total percentage.
Table 4 - Soil granulometry and correspondent geographic location of the positive samples for entomopathogenic nematodes
(isolates) found in Rio Grande do Sul State, Brazil.
Entomopathogenic nematodes
Isolate
Soil granulometry
Sand(%)
Silt (%)
Clay (%)
Latitude
Longitude
H. bacteriophora
RS33
RS56
RS57
RS58
RS88
RS107
55.3
62.9
63.7
63.1
37.3
67.0
23.8
21.7
25.0
26.2
22.8
19.5
20.9
12.8
11.4
11.7
39.8
13.5
-31º48’9,7’’
-28º19’45"
-28º15’06,8"
-28º15’06,8"
-28º56’41,5"
-32º06’49,7"
-52º25’5,8"
-51º05’17,0"
-51º29’46,4"
-51º29’46,4"
-53º38’54,4"
-53º08’02,6"
H. amazonensis
RS72
84.2
9.7
6.0
-30º15’39"
-54º58’13,1"
S. rarum
RS47
RS55
RS70
RS89
RS90
RS102
RS106
60.0
35.5
51.0
68.6
59.0
59.6
96.0
18.9
17.1
29.0
19.2
17.6
27.4
0.4
21.1
47.4
20.0
12.5
23.4
12.9
4.4
-27º28’28,5"
-28º19’43,1"
-30º44’30,4"
-31º23’59,6"
-31º20’20,1"
-28º50’14"
-30º10’48"
-52º54’13’7"
-51º05’17,8"
-55º06’11,6"
-52º40’48"
-52º52’32"
-52º51’36,9"
-50º12’35,9"
S. feltiae
RS76
57.4
31.2
11.3
-29º38’56,9"
-54º40’40,1"
S. glaseri
RS38
8.3
21.2
70.5
-28º01’40"
-52º14’00,6"
S. riobrave
RS59
6.9
22.5
70.6
-28º14’59,9"
-51º30’16,1"
Steinernema sp.
RS69
RS92
17.5
18.2
56.3
50.8
26.2
31.0
-30º53’55,4"
-31º00’15,3"
-54º51’31,7"
-52º58’49,1"
samples where the soil temperature was above 25 ºC.
In general, the prevalence of Heterorhabditis sp. is
negatively correlated to high temperatures and
194 Vol. 34(4) - 2010
positively to low ones (Prasad et al., 2001). However,
due to the absence of a suitable model, there is
controversy concerning the importance of this factor
1
H. amazonensis
S. rarum
S. feltiae
S. glaseri
S. riobrave
Steinernema sp
8
10
1
19
15.7
H. bacteriophora
68
44
9
121
< 20
20 – 25
> 25
Total
TP1
Soil temperature (ºC)
Table 5 - Occurrence of entomopathogenic nematodes in Rio Grande do Sul State, Brazil, in relation to the soil temperatures.
11.76
2.27
11.11
-
3
3
0
6
1
0
0
1
2
5
0
7
0
0
1
1
1
0
0
1
1
0
0
1
0
2
0
2
Total percentage.
1
H. amazonensis
S. rarum
S. feltiae
S. glaseri
S. riobrave
Steinernema sp
2
5
2
2
0
0
3
0
5
0
0
19
15.7
H. bacteriophora
42
29
7
9
5
0
14
2
6
0
3
121
1 – 100
100 – 200
200 – 300
300 – 400
400 – 500
500 – 600
600 – 700
700 – 800
800 – 900
900 – 1,000
1,000 – 1,100
Total
TP1
Altitude (m.s.l.)
Table 6 - Occurrence of entomopathogenic nematodes found in Rio Grande do Sul State, Brazil, according to different altitudes.
4.76
17.24
28.57
22.22
0
0
21.42
0
83.33
0
0
-
1
1
0
1
0
0
0
0
3
0
0
6
0
1
0
0
0
0
0
0
0
0
0
1
1
1
1
1
0
0
2
0
1
0
0
7
0
1
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
0
0
0
0
1
0
0
0
0
0
0
0
0
1
0
0
1
0
1
1
0
0
0
0
0
0
0
0
2
Total percentage.
in the population dynamics of EPNs, and whether
they interfere or not in incidence (Hominick & Briscoe,
1990; Puza & Mrácek, 2005).
With regard to altitude, EPNs were more prevalent
between 800 and 900 m (83.33 %) followed by 200
to 300 m (28.57 %), and at sea level from 1 to 100 m
(4.76 %) only H. bacteriophora and S. rarum were found
(Table 6). No influence of altitude on the occurrence
of EPNs was apparent from some previous studies
(Shishiniova et al., 1997; Mrácek et al., 2005). Despite
this, in Spain, Campos-Herrera et al. (2007) found
higher prevalence of EPNs from 501 to 800 m of
altitude and below 500 m no nematode was detected.
In the Hawaiian islands, Hara et al. (1991) collected 95
% of heterorhabditids at sea level (100 m), these
nematodes prevailing locally in relation to the
cumulative number of species
5
Observed
Log. (Observed)
4
3
y = 1.9194Ln(x) - 4.3879
2
R2 = 0.7488
1
0
1
7
13
19
25
31
37
43
49
55
61
67
73
79
85
91
97 103 109 115
121
number of samples
Figure 2 - Sample sufficiency for entomopathogenic nematode isolated in Rio Grande do Sul State, Brazil.
steinernematids. In our study, S. riobrave occurred at
827 m high, but Stock & Gress (2006) recorded it at
1,400 m; in opposition, S. feltiae was only present in
samples collected at low altitude, as also reported by
Roman & Beavers (1982) in Puerto Rico.
The number of samples collected in the present
study was not sufficient to represent all the EPNs that
may occur in RS, as the collector curve (Figure 2) was
not asymptotic, based on Colwell et al. (2004).
Therefore, additional investigation dealing with the
prevalence, abundance and other ecological aspects
related to EPNs occurring in the Rio Grande do Sul
State are strongly suggested.
Acknowledgements
The authors thank Dr. Márcio Voss from Embrapa
Trigo, Passo Fundo (RS) Brazil for his help with soil
sampling. C.R.C. Barbosa-Negrisoli received a
scholarship from Conselho Nacional de Pesquisa e
Desenvolvimento Tecnológico (CNPq).
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