Nematology, 2011, Vol.

13(6), 721-728

Effect of nematophagous fungi on reproduction of

Meloidogyne enterolobii on guava (Psidium guajava) plants
Regina M.D. Gomes C ARNEIRO 1, , Leopoldo H IDALGO -D AZ 2 ,
Irene M ARTINS 1 , Karla Fernanda AYRES DE S OUZA S ILVA 1 ,
Mariana G UIMARES DE S OUSA 1 and Myrian S. T IGANO 1
1

Embrapa Recursos Genticos e Biotecnologia, Cx Postal 02372, CEP 70849-949, Braslia, DF, Brazil
2
Centro Nacional de Sanidad Agropecuaria, San Jos de las Lajas, Apartado 10, La Habana, Cuba
Received: 3 April 2010; revised: 5 November 2010
Accepted for publication: 8 November 2010; available online: 9 February 2011

Summary The root-knot nematode, Meloidogyne enterolobii, is a major disease of guava, Psidium guajava, in Brazil and other
countries. Egg-pathogenic fungi are considered potential biological control agents of root-knot nematodes and are associated with
suppression of Meloidogyne spp. Glasshouse experiments were conducted in order to evaluate the effect of the fungi Paecilomyces
lilacinus and Pochonia chlamydosporia on a population of M. enterolobii growing on guava plants. Guava seedlings of about 15-20
cm growing in plastic bags were inoculated with 10 000 eggs of M. enterolobii plant1 . Two months later, three isolates of P. lilacinus
and one isolate of P. chlamydosporia were inoculated in the infested plants. The effect of the treatments was evaluated 6 months
later. Although plant infection by nematodes was not attenuated, the number of eggs (g roots)1 fell significantly. The number of egg
masses infected with the fungi was inversely correlated with the number of eggs found in the roots. The most effective result (61.5%
of control) was obtained with the isolate CG1003 of P. chlamydoporia, which was originally isolated from eggs of M. enterolobii in
Brazil, followed by P. lilacinus (CG959 and CG1038) with about 40% of control. These fungi showed the ability to colonise healthy
guava roots in glasshouse experiments. These results suggest that P. chlamydosporia can be selected as a potential biological control
agent to be employed with other strategies in integrated management to control M. enterolobii on guava.
Keywords biological control, Paecilomyces lilacinus, Pochonia chlamydosporia, root-knot nematode.

The root-knot nematode Meloidogyne enterolobii Yang

& Eisenback, 1983 was described from a population obtained in China and isolated from a tree species (Enterolobium contortisiliquum Vell. Morong). This nematode was also reported from other regions in China and
Vietnam, but mainly isolated from guava (Psidium guajava L.) (Xu et al., 2004; Iwahori et al., 2010) and rhizome of arrowroot (Zhuo et al., 2010). More recently, it
has been suggested that M. enterolobii is a senior synonym of M. mayaguensis Rammah & Hirschmann, 1988
(EPPO, 2008), a species which had originally been described in Puerto Rico isolated from eggplant (Solanum
melongena L.) roots. The presence of this pathogen has
been increasingly detected in different geographical regions from a wide range of hosts, including crops carrying
genes of resistance to the main Meloidogyne spp. (Fargette
et al., 1996; Blok et al., 2002; Carneiro et al., 2006; Brito
et al., 2007). Considering the risk of introduction of this
Corresponding

pest into the European region, M. enterolobii was added

to the EPPO (2008) Alert List.
In Brazil, M. enterolobii was originally detected in
guava orchards in 2001 in Pernambuco and Bahia states
(Carneiro et al., 2001). Since then, this nematode has
been a matter of grave concern in the country because
it has been spreading rapidly, making the cultivation of
guava unviable in the heavily infested areas in northeastern Brazil (Carneiro et al., 2007). In five Brazilian
States, the total economic loss caused by M. enterolobii
has been estimated at US$ 61 million. The decimation of
the infested orchards has resulted in the loss of 3703 fulltime jobs. This study indicates the economic importance
of M. enterolobii to Brazil, which may increase further if
other guava-producing regions become infested and/or if
other crops become widely parasitised by this nematode
(Pereira et al., 2009). Several distressed growers are
using biological control, organic amendments and other

author, e-mail: recar@cenargen.embrapa.br

Koninklijke Brill NV, Leiden, 2011

Also available online - www.brill.nl/nemy

DOI:10.1163/138855410X545777
721

R.M.D.G. Carneiro et al.

methods to try to save their damaged guava plants, but

they are working without information from research.
In all recent surveys in Brazil, M. enterolobii has been
identified using esterase profile and molecular markers
(Carneiro et al., 2001; Siqueira et al., 2009). This nematode was also detected in native areas of the Atlantic Forest (Lima et al., 2005), suggesting that the species was not
introduced in Brazil from other countries, as was thought
at the time it was first detected (Carneiro et al., 2001).
Duponnois et al. (1995) tested the ability of two isolates
of the nematode-trapping-fungi Arthrobotrys oligospora,
isolated from Senegal, in capturing second-stage juveniles
(J2) of M. enterolobii, and obtained a significant reduction
in root-knot nematode populations on tomatoes in pot and
field experiments. Paecilomyces lilacinus (Thom) Samson
and Pochonia chlamydosporia Goddard have been identified as egg parasites and are associated with suppression of root-knot nematodes and cyst nematodes, and their
potential as biological control agents has been examined
(Jatala, 1986; Kerry, 2001; Atkins et al., 2003). However,
isolates differ in their pathogenicity to root-knot nematode eggs, their ability to grow in the rhizosphere and in
production of spores, as well as in their optimum temperature (Kerry et al., 1986). The fungus P. chlamydosporia is
able to produce chlamydospores so these spores were used
in the bioassays as inoculum. They present an advantage
over conidia in that they have sufficient food reserves to
enable the fungus to become established without adding
other energy sources (Kerry et al., 1993). In addition, the
host plant has a significant effect on the growth of the fungus in the rhizosphere (Bourne et al., 1996). It is imperative to identify the fungal isolates most suited to local
conditions and also those that extensively colonise the rhizospheres of locally grown crop cultivars. These fungi are
facultative parasites of nematodes and apparently common in root-knot nematode-infested soils, but it is only
recently that they have been isolated from M. enterolobii

egg masses from guava plants in Petrolina, Pernambuco

State (Arevalo et al., 2009).
Three accessions of Psidium friedrichsthalianium were
considered moderately resistant to M. enterolobii and
can be used as rootstock compatible with P. guajava cv.
Paluma in field conditions (Carneiro et al., 2007). Integrated and sustainable strategies for the control of rootknot nematodes on guava must be developed for specific
agricultural systems using resistance and biological control agents in order to maximise the potential of control.
This work aimed to evaluate in optimal conditions for
the fungi (sterilised soil), the effectiveness of P. lilacinus
and P. chlamydosporia isolated from M. enterolobii eggmasses and soil against this species of root-knot nematode
on guava roots in glasshouse conditions, and to determine
if these fungi can colonise the roots of this plant.

Materials and methods

E VALUATION OF NEMATOPHAGOUS FUNGI AGAINST
MELOIDOGYNE ENTEROLOBII
Three isolates of P. lilacinus and one isolate of P. chlamydosporia were evaluated (Table 1). These isolates
were obtained from the Culture Collection of Invertebrate
Fungi at Embrapa Recursos Genticos e Biotecnologia,
Braslia, Brazil. The isolates were cultured on potato
dextrose-agar (PDA) at 28 C. Chlamydospore and conidia
used as inoculum in the bioassays were produced in solidstate fermentation in plastic bags as described by Montes
de Oca (2004). For nematode inoculation, one population
of M. enterolobii obtained from guava, Petrolina, PE,
Brazil, was maintained on tomatoes cv. Santa Clara in
glasshouse conditions (25-30 C).
Three-month-old guava seedlings growing in 3 kg
plastic bags filled with steam sterilised soil mixture (50%
sand and 50% clay soils) were inoculated with 10 000
eggs (Pi ) extracted from tomato roots using the method

Table 1. Origin of the nematophagous fungus isolates.

Name
Pochonia chlamydosporia
Paecilomyces lilacinus
P. lilacinus
P. lilacinus

Isolate
CG1003
CG1004
CG959
CG1038

Locality

Host/Substrate

Petrolina, PE, Brazil

Petrolina, PE, Brazil
Colombia
Colombia

Meloidogyne enterolobii
M. enterolobii
Soil
Meloidogyne sp.

Origin
1
1
2
3

Origin: 1, isolates from the Culture Collection of Invertebrate Fungi from Embrapa Recursos Genticos e Biotecnologia; 2, isolate
obtained from a commercial product Biostat WP; 3, isolate obtained from a commercial product (Micos Plag WP).
722

Nematology

Effect of nematophagous fungi on Meloidogyne enterolobii on guava

described by Bonetti and Ferraz (1981). Two months

later, the fungus spores (conidia + chlamydospores) were
extracted from the colonised rice (19 days of incubation
at 25 C), quantified and suspended and applied in the
soil in order to obtain a homogeneous distribution of
the spores. The viable fungus concentrations were: 106
conidia (g soil)1 for P. lilacinus isolates and mainly
5000 chlamydospores (g soil)1 for the P. chlamydosporia
isolate. A control inoculated only with the nematode was
used. Treatments were replicated eight times (8 plants in
each treatment) and rearranged in a randomised complete
block design in a glasshouse. Six months after fungus
inoculation, trials were assessed by carrying out the
following evaluations:
Nematode population density
The root systems were carefully washed, blotted onto
paper to damp dry, and weighed. Galls and number of
egg masses produced by the nematode per root system
were counted. Gall Index (GI) was calculated according to
a scale proposed by Hartman and Sasser (1985) where 0 =
no galls, 1 = 1-2 galls, 2 = 3-10, 3 = 11-30, 4 = 31-100,
and 5 = over 100 galls. Eggs were extracted by triturating
in a blender for 1 min in 1% NaOCl, according to Bonetti
and Ferraz (1981). The number of eggs per root system
(final nematode population = Pf ) was counted in triplicate
in a Peters counting slide. This mean value was used to
determine the number of eggs g1 root.

After 100 days, the amount of fungus in the rhizosphere

was quantified by dilution plating on a semi-selective
medium (Chase et al., 1986; De Leij & Kerry, 1991) and
estimating the number of colony forming units (CFU) as
described by Kerry and Bourne (2002). The plants were
harvested and the root system carefully washed to remove
soil, then blotted dry and cut into small segments (1
cm) and mixed thoroughly; two 1 g subsamples of each
were taken at random. One root subsample was add to 9
ml of sterile 0.05% agar solution in a sterile pestle and
mortar, crushed enough to remove just the cortex cells
and a dilution range prepared (101 -103 ). Then, 0.2 ml
subsamples of each dilution were incubated at 25 C on
semi-selective medium for 2 weeks when the number of
CFUs was evaluated. The other subsample was used to
estimate root surface area for calculation of CFU cm2
according to Bourne et al. (1994).
S TATISTICAL ANALYSES
Analysis of variance was performed for the experiment
after a log(x + 1) transformation of the data for the eggs
(g roots)1 . The Scott-Knott (1974) test (P  0.05) was
used to evaluate differences among treatments. Pearson
correlation coefficients between colonised egg masses and
number of eggs (g roots)1 were calculated for each
genotype. All analyses were carried out using the SAS
statistical package (SAS Institute, 1988).

Percentage of egg masses colonised by the fungi

100 isolated egg masses were collected per treatment
from the guava roots washed with water and placed in
1% water agar with antibiotics (50 mg l1 of streptomycin
sulphate, chloramphenicol and chlortetracycline) in Petri
dishes. The number of colonised egg masses was determined after 72 h of incubation at 25 C.
ROOT COLONISATION
To assess the ability of nematode egg-parasitic fungi
to colonise the rhizosphere of healthy guava roots the
same isolates were used (Table 1). The fungus inocula
were produced as described above. Soil of each treatment
was mixed thoroughly with colonised rice of each isolate
separately for 106 conidia (g soil)1 for P. lilacinus and
5000 for P. chlamydosporia. Eight pots of 3 kg for each
treatment were filled with sterilised and inoculated soil
and planted with 90-day-old seedlings of guava. The
plants were maintained in glasshouse conditions at 2530 C.
Vol. 13(6), 2011

Results
Plants infected by the nematode in all treatments
showed symptoms such as stunted growth, general chlorosis and nutrient deficiency. The root systems were poorly
developed, severely infested, distorted by small and large
multiple galls and devoid of fine roots.
The effect of the four fungus isolates tested in the
treatment of infected guava plants significantly decreased
the number of eggs (g roots)1 of M. enterolobii, except
for the isolate CG959 of P. lilacinus, compared with the
untreated control. However, the infection caused by the
nematode, measured by the gall index, did not decrease
(Table 2). The isolate CG1003 of P. chlamydosporia
var. chlamydosporia (an isolate from M. enterolobii) was
the best to control this nematode, affecting reproduction
of the nematode with an estimated control of 61.53%
and colonising more than 70% of egg masses (Table 2).
Furthermore, the results revealed variation among the
P. lilacinus isolates, regarding their pathogenic activity
723

R.M.D.G. Carneiro et al.

Table 2. Effect of egg-parasitic fungi Pochonia chlamydosporia (Pc) and Paecilomyces lilacinus (Pl) on the reduction of populations
of Meloidogyne enterolobii.
Species-isolates

Pc-CG1003
Pl-CG1038
Pl-CG1004
Pl-CG959
Control

Weight of fresh roots

(g)

Gall index

Number of eggs
(g roots)1

Percentage of estimated
control

Number of parasitised
egg masses
(%)

253.70 a
246.60 a
208.25 b
263.62 a
223.85 b

5
5
5
5
5

2317.00 c
3727.50 b
3499.25 b
5964.62 a
6023.75 a

61.53
38.11
41.90
0.98
0.00

76.66 a
46.75 b
25.83 c
13.33 c
0.00*

Mean values (eight replicates) with different lower-case letters indicate significance at P < 0.05 according to the Scott and Knott
(1974) test.
Table 3. Root colonisation of nematophagous fungi Pochonia chlamydosporia (Pc) and Paecilomyces lilacinus (Pl) on guava roots
after 110 days, without nematodes, replicated four times.
Species-isolates
Pc-CG1003
Pl-CG1004
Pl-CG959
Pl-CG1038
Sterilised rice
Control

CFU (g roots)1
(n 103 )

CFU cm2 root

Host status

0.74
2.50
8.16
5.00
0.00
0.00

15.64
51.41
167.95
102.83

Poor
Poor
Moderate
Moderate

Host status: good host, >200 CFU cm2 root; moderate host, 100-200 CFU cm2 root; poor host, <100 CFU cm2 root (Kerry, 2001).

against M. enterolobii. Isolates of P. lilacinus presented

control between 0.98 and 41.9%. The parasitism of egg
masses was associated with a reduction in the number
of eggs (g roots)1 . For all isolates, the percentage of
colonised egg masses was negatively correlated with the
number of eggs (g roots)1 (R = 0.64; P = 0.09).
Analysing the differences in root weight, it seems that P.
chlamydosporia CG1003 and P. lilacinus (CG1038 and Pl
CG 959) promoted root growth compared with the control
(Table 2).
Psidium guajava was seen to be a poor or moderate
host for all the isolates tested in this study (Table 3). Any
isolate tested was able to grow extensively through the
healthy root surface of guava (more than 200 CFU cm2
of roots), according to Kerry and Bourne (2002).

Discussion
The soil-borne fungi P. chlamydosporia and P. lilacinus
have been implicated on a number of occasions in the
pathology of root-knot nematodes. They occur in a variety
724

of soils (Jatala, 1986; Kerry, 2001) and in the rhizosphere

of guava, parasitising eggs of M. enterolobii in Brazil
(Arevalo et al., 2009). Paecilomyces lilacinus is the most
tested biological control agent for nematodes and isolate
251 has been commercialised and registered for sale under
a number of different trade names for the control of
nematode pests in several countries (EPA, 2005; Kiewnick
& Sikora, 2006).
To understand and exploit P. chlamydosporia as
a means to regulate populations of root-knot nematodes it
is necessary to have detailed knowledge of ecological considerations, including the population dynamics of the fungus and nematode in the rhizosphere (Kerry, 2000). Kerry
and Bourne (2002) have shown that only 5% of biotypes
of P. chlamydosporia presented the characteristics considered essential for the control of root-knot nematodes;
hence, there is a need for careful selection of potential biological control agents. The three isolates studied in this
paper parasitised eggs of root-knot nematodes and caused
a significant reduction in nematode populations. However,
the control achieved was insufficient to reduce the gall
index (GI = 5.0) after six generations of root-knot nemaNematology

Effect of nematophagous fungi on Meloidogyne enterolobii on guava

todes on guava. Significant reduction in the multiplication

of M. arenaria was achieved with P. chlamydosporia after the first generation of the nematode on tomato. However, the control achieved was insufficient to prevent the
development of large nematode infestations in subsequent
generations (De Leij & Kerry, 1991). Hence, it is more
appropriate to determine the efficacy of biological control agents by comparing the extent of plant damage after
more than one generation of the nematode (De Leij et al.,
1993; Bourne et al., 1994; Bourne & Kerry, 1999). Similar
results were obtained by Coutinho et al. (2009) in all treatments in which the chlamydospores were incorporated on
tomato to control M. javanica, and a significant reduction
in the number of eggs (56-61%) was observed. Although
the number of galls fell in all treatments, the gall index
was very high (GI = 5.0), at more than 200 galls per plant.
Our results also revealed a variation among the P. lilacinus
isolates regarding pathogenic activity to the M. enterolobii
population. Variation among isolates of several species of
nematophagous fungi has been widely reported (Stirling
& Mankau, 1978; Nigh et al., 1980; Kerry et al., 1986;
Tiganomilani et al., 1995; Gunasekera et al., 2000). Only
the isolate of P. lilacinus obtained from soil (CG959) did
not cause significant reduction in nematode populations.
It seems that the isolates from eggs were more suppressive that the isolate collected from soil. The same was observed by Fans et al. (1991).
Pochonia chlamydosporia colonises the rhizosphere of
a wide range of crops and infects egg masses on the surface of the roots that protrude into the rhizosphere. Destruction of eggs and the subsequent control of nematode
populations depend on the effectiveness of this fungal invasion, which differs with plant species, nematode density and fungus isolates (De Leij et al., 1993; Bourne et
al., 1994; Puertas & Hidalgo, 2007). In the process of
P. chlamydosporia plant root colonisation, hyphae penetrate epidermal cells by means of apressoria and a hyphal
network is formed in epidermal and cortical cells. However, cortical cells seem to be the limit of fungal colonisation since no hyphae have been observed in the vascular
cylinder (Lopez-Llorca et al., 2002). Considering this, if
P. chlamydosporia cannot colonise the root cortex extensively, egg masses that remain within galled roots are not
colonised and the fungus provides poor control in situations where large galls are formed, such as in heavily infested soil and on highly nematode-susceptible crops (De
Leij & Kerry, 1991), such as the guava crop. Given this
high susceptibility of guava plants, forming big galls on
roots was considered an important aspect in determining
Vol. 13(6), 2011

the low biological control efficacy of fungi. Dactylella

oviparasitica Stirling & Mankau, which effectively controlled root-knot nematodes on peach, did not control the
same nematode on vines, on which the galls were approximately seven times the size (Stirling et al., 1979).
Pochonia chlamydosporia appeared to be more prevalent on galled than on non-galled roots. This may be due
to the leaching of more nutrients from nematode-damaged
than from undamaged tissue (De Leij & Kerry, 1991).
Paecilomyces lilacinus was also found more frequently on
galls (Hewlett et al., 1988), and the authors stressed the
importance of the root system in determining the spread
of the fungus and its efficacy as a biological control agent.
The poor and moderate capacity of our isolates in colonising guava roots (CFU) is probably related to the absence
of the nematode in our assay. Studies relying on CFU
counts have been criticised for failing to describe fungal population accurately, because fungi possess different life stages that are indistinguishable from each other
when they are colonies on agar plates (Kowalchuk, 1999).
On the other hand, isolates of P. chlamydosporia, which
are better competitors for nutrients and consequently better saprophytes (>CFU), can be poor parasites of plantparasitic nematodes. If the isolates depend more on the
presence of the nematodes for their nutrition, they may be
better biological control agents (Mauchline et al., 2004).
Natural soil application of nematophagous fungi for the
biological control of plant-parasitic nematodes often fails,
and in many cases it has been difficult to re-isolate the
agent delivered to the soil. A reason for these results could
be the inability of the fungi to proliferate in soil. Growth
of all fungi tested (P. chlamydosporia and P. lilacinus) was
inhibited in non-sterilised soil compared with sterilised
treatments (Monford et al., 2006). Nematophagous activity of P. chlamydosporia in natural and autoclaved soil on
tomato plants infested with M. javanica was evaluated. In
autoclaved soil, the reduction in the number of galls was
27.1% higher and the number of the eggs 22.1% higher
than in the non-autoclaved soil (Podest et al., 2009).
The present research made in optimal conditions for the
fungi (sterilised soil) indicated that egg-parasitic fungi on
their own cannot be used to control M. enterolobii populations on guava plants. More studies using naturally infested soil from guava production areas are necessary to
provide evidence that the introduction of native isolates
collected on egg masses of M. enterolobii can cause a reduction in the severity of damage caused by the nematode. Results indicated that a soil can be more receptive to its indigenous isolates than to non-indigenous iso725

R.M.D.G. Carneiro et al.

lates. Apparently, soil microbiota can determine the ability of nematophagous fungi to proliferate in soil (Monford et al., 2006). Perhaps in the future we will be able to
integrate biological control with other control measures
like moderately resistant rootstock on guava (Carneiro
et al., 2007). Current experience suggests that biological
control agents will not replace the other control measures
but, when integrated with resistant/tolerant crop cultivars,
they could play an important role in the development of
integrated control strategies in both developed and developing agriculture. The urgent need to reduce dependence
on nematicides should provide the necessary impetus for
the considerable amount of research and development still
required to ensure the successful use of integrated control
strategies, as has been suggested in other studies (Hidalgo
& Kerry, 2008).

References
A REVALO, J., H IDALGO -D AZ, L., M ARTINS, I., S OUZA,
J.F., C ASTRO, J.M.C., C ARNEIRO, R.M.D.G. & T IGANO,
M.S. (2009). Cultural and morphological characterization
of Pochonia chlamydosporia and Lecanicillium psalliotae
isolated from Meloidogyne mayaguensis eggs in Brazil.
Tropical Plant Pathology 34, 158-163.
ATKINS, S.D., H IDALGO -D AS, L., K ALISZ, H., M AUCHLINE,
T.H., H IRSCH, P.R. & K ERRY, B.R. (2003). Development
of a new management strategy for the control of rootknot nematodes (Meloidogyne spp.) in organic vegetation
production. Pest Management Science 59, 183-189.
B LOK, V.C., W ISHART, J., FARGETTE, M., B ERTHIER, K.
& P HILLIPS, M.S. (2002). Mitochondrial DNA differences
distinguishing Meloidogyne mayaguensis from the major
species of tropical root-knot nematodes. Nematology 4, 773781.
B ONETI, J.I.S. & F ERRAZ, S. (1981). Modificao do mtodo
de Hussey & Barker para extrao de ovos de Meloidogyne
exigua de razes de cafeeiros. Fitopatologia Brasileira 6, 553.
B OURNE, J.M. & K ERRY, B.R. (1999). Effect of the host
plant on the efficacy of Verticillium chlamydosporium as a
biological control agent of root-knot nematodes at different
nematode densities and fungal application rates. Soil Biology
and Biochemistry 31, 75-84.
B OURNE, J.M., K ERRY, B.R. & D E L EIJ, F.A.A.M. (1994).
Methods for the study of Verticillium chlamydosporium in the
rhizosphere. Journal of Nematology 26, 587-591
B OURNE, J.M., K ERRY, B.R. & D E L EIJ, F.A.A.M. (1996). The
importance of the host plant on the interaction between rootknot nematodes (Meloidogyne spp.) and the nemathophagous
fungus, Verticillium chlamydosporium (Goddard). Biocontrol
Science Technology 6, 539-548.
726

B RITO, J.A., S TANLEY, J.D., M ENDES, M.L., C ETINTAS, R.

& D ICKSON, D.W. (2007). Host status of selected cultivars
plants to Meloidogyne mayaguensis from Florida. Journal of
Nematology 36, 232-240.
C ARNEIRO, R.M.D.G., M OREIRA, W.A., A LMEIDA, M.R.A. &
G OMES, A.C.M.M. (2001). Primeiro registro de Meloidogyne
mayaguensis em goiabeira no Brasil. Nematologia Brasileira
25, 223-228.
C ARNEIRO, R.M.D.G., A LMEIDA, M.R.A., B RAGA, R.S.,
A LMEIDA, C.A. & G IORIA, R. (2006). Primeiro registro de
Meloidogyne mayaguensis parasitando plantas de tomate e pimento resistentes meloidoginose no estado de So Paulo.
Nematologia Brasileira 30, 81-86.
C ARNEIRO, R.M.D.G., C IROTTO, P.A., Q UINTANILHA, A.P.,
S ILVA, D.B. & C ARNEIRO, R.G. (2007). Resistance to
Meloidogyne mayaguensis in Psidium spp. accessions and
their grafting compatibility with P. guajava cv. Paluma.
Fitopatologia Brasileira 32, 281-284.
C HASE, A.R., O SBONE, L.S. & F ERGUSON, V.M. (1986). Selective isolation of entopathogenic fungi Beauveria bassiana
and Metarhizium anisopliae from an artificial potting medium. Florida Entomology 69, 285-292.
C OUTINHO, M.M., F REITAS, L.G., DALLEMORE -G IARETTA,
R., N EVES, W.S., L OPES, E.A. & F ERRAZ, S. (2009). Controle de Meloidogyne javanica com Pochonia chlamydosporia
e farinha de sementes de mamo. Nematologia Brasileira 33,
169-175.
D E L EIJ, F.A.A.M. & K ERRY, B.R. (1991). The nematophagous
fungus Verticillium clamydosporium as a potential biological
control agent for Meloidogyne arenaria. Revue de Nmatologie 14, 157-164.
D E L EIJ, F.A.A.M., K ERRY, B.R. & D ENNEHY, J.A. (1993).
Verticillium chlamydosporium as a biological control agent
for Meloidogyne incognita and M. hapla in pot and microplot tests. Nematologica 39, 115-126.
D UPONNOIS, R., M ATEILLE, T. & G UEYE, M. (1995). Biological characteristics and effects of two strains of Arthrobotrys
oligospora from Senegal on Meloidogyne species parasitizing
tomato plants. Biocontrol Science and Technology 5, 517-525.
EPA, US (Environmental Protection Agency) (2005). Paecilomyces lilacinus strain 251; exemption from the requirement of a tolerance. United States Federal Register 70,
19278-19283.
EPPO (2008). An emerging root-knot nematode, Meloidogyne
enterolobii: addition to the EPPO Alert List. EPPO Reporting
Service 5, 2008/105.
FARGETTE, M., P HILLIPS, M.S., B LOK, V.C., WAUGH, R. &
T RUDGILL, D.L. (1996). An RFLP study of relationships
between species, isolates and resistance-breaking lines of
tropical species of Meloidogyne. Fundamental and Applied
Nematology 19, 193-200.
G UNASEKERA, T.S., H OLLAND, R.J., G OLLINGS, M.R.,
B RISCOE, D.A., N EETHLING, D.C., W ILLIAMS, K.L. &
NAVALAINEN, K.M. (2000). Phenotypic and genetic characNematology

Effect of nematophagous fungi on Meloidogyne enterolobii on guava

terization of Paecilomyces lilacinus strains with biocontrol

activity against root-knot nematodes. Canadian Journal of
Microbiology 46, 775-783.
H EWLETT, T.E., D ICKSON, D.W., M ITCHELL, D.J. &
K ANNWISCHER -M ITCHELL, M.E. (1988). Evaluation of
Paecilomyces lilacinus as a biocontrol agent of Meloidogyne
javanica on tobacco. Journal of Nematology 20, 578-584.
H IDALGO -D AZ, L. & K ERRY, B.R. (2008). Integration of biological control with other methods of nematode management.
In: Ciancio, A. & Mukerji, K.G. (Eds). Integrated management and biocontrol of vegetable and grain crops nematodes.
Dordrecht, The Netherlands, Springer, pp. 29-49.
H IDALGO -D AZ, L., B OURNE, J.M., K ERRY, B.R. & RO DRGUEZ, M.G. (2000). Nematophagous Verticillium spp.
in soil infested with Meloidogyne spp. in Cuba: isolation
and screening. International Journal of Pest Management 46,
277-284.
I WAHORI, H., T RUC, N.T.N., BAN, D.V. & I CHINOSE, K.
(2009). First report of root-knot nematode Meloidogyne
enterolobii on guava in Vietnam. Plant Disease 93, 675.
[Abstr.]
JATALA, P. (1986). Biological control of plant parasitic nematodes. Annual Review of Phytopathology 24, 453-489.
K ERRY, B.R. (2000). Rhizosphere interactions and exploitation
of microbial agents for the biological control of plantparasitic nematodes. Annual Review of Phytopathology 38,
423-441.
K ERRY, B.R. (2001). Exploitation of the nematophagous fungus
Verticillium chlamydosporium Goddard for the biological
control of root-knot nematodes (Meloidogyne spp.). In: Butt,
T.M., Jackson, C. & Margan, N. (Eds). Fungi as biological
agents. Wallingford, UK, CABI Publishing, pp. 155-167.
K ERRY, B.R. & B OURNE, J.M. (2002). A manual for research
on Verticillium chlamydosporium, a potential biological
control agent for root-knot nematodes. Ghent, Belgium,
IOBC/WPRS, 84 pp.
K ERRY, B.R., I RVING, F. & H ORNSEY, J.C. (1986). Variation
between strains of the nematophagous fungus, Verticillium
chlamydosporium Goddard. I. Factors affecting growth in
vitro. Nematologica 32, 461-473.
K ERRY, B.R., K IRKWOOD, I.A., D E L EIJ, F.A.A.M., BARBA,
J., L EIDJENS, M.B. & B ROOKES, P.C. (1993). Growth and
survival of Verticillium chlamydosporium Goddard, a parasite
of nematodes in soil. Biocontrol Science and Technology 3,
355-365.
K IEWNICK, S. & S IKORA, R. (2006). Evaluation of Paecilomyces lilacinus strain 251 for the biological control of the
northern root-knot nematode Meloidogyne hapla Chitwood.
Nematology 8, 69-78.
KOWALCHUK, G.A. (1999). New perspectives towards analyzing fungal communities in terrestrial environments. Current
Opinions in Biotechnology 10, 247-251.
L IMA, I.M., D OLINSKI, C.M. & S OUZA, R.M. (2003). Disperso de Meloidogyne mayaguensis em goiabais de So Joo da
Vol. 13(6), 2011

Barra (RJ) e relato de novos hospedeiros dentre plantas invasoras e cultivadas. Nematologia Brasileira 27, 257-258.
L IMA, I.M., S OUZA, R.M., S ILVA, C.P. & C ARNEIRO,
R.M.D.G. (2005). Meloidogyne spp. from preserved areas of
Atlantic Forest in the State of Rio de Janeiro, Brazil. Nematologia Brasileira 29, 31-38.
L OPEZ -L LORCA, L.V., B ORDALLO, J.J., S ALINAS, J., M ON FORT, E. & L PEZ -S ERNA , M.L. (2002). Use of light and
scanning electron microscopy to examine colonization of
barley rhizosphere by the nematophgous fungus Verticillium
chlamydosporium. Mcron 33, 61-67.
M AUCHILINE, T.H., K ERRY, B.R. & H IRSCH, P.R. (2004). The
biocontrol fungus Pochonia chlamydosporia shows nematode
host preference at the infraspecific level. Mycology Research
108, 161-169.
M ONFORD, E., L OPEZ -L LORCA, L.V., JANSON, H.B. & S ALI NAS , J. (2006). In vitro soil receptivity assays to egg-parasitic
nematophagous fungi. Mycological Progress 5, 18-23.
M ONTES DE O CA, N. (2004). Buenas prcticas de fabricacin
para la obtencin de um bionematicida a partir de la cepa
IMI 187 de Pochonia chlamydosporia var. catenulata. Tesis
de Doctor em Ciencias Agrcolas, Universidad Agraria de La
Habana, Cuba, 152 pp.
N IGH, E.A., T HOMASON, I.J. & VAN G UNDY, S.D. (1980).
Identification and distribution of fungal parasites of Heterodera schachtii eggs in California, USA. Phytopathology 70,
884-889.
P EREIRA, F.O.M., S OUZA, R.M., S OUZA, P.M., D OLINSKI, C.
& S ANTOS, G.K. (2009). Estimativa do impacto econmico
e social direto de Meloidogyne mayaguensis na cultura da
goiaba no Brasil. Nematologia Brasileira 33, 176-181.
P ODEST, G.S., DALLEMOLE -G IARETTA, R., F REITAS, L.G.,
L OPES, E.A., F ERRAZ, S. & Z OOCA, R.J.F. (2009). Atividade nematfaga de Pochonia chlamydosporia em solo natural ou autoclavado sobre Meloidogyne javanica. Nematologia Brasileira 32, 191-193.
P UERTAS, A. & H IDALGO -D AZ, L. (2007). Influencia de
la planta hospedante y su interaccin con Meloidogyne
incognita sobre la efectividad de Pochonia chlamydosporia
var. catenulata. Revista de Proteccin Vegetal 22, 104-109.
SAS Institute (1988). SAS/STAT Users Guide, Release 6.03
edition. Cary, NC, SAS Institute, 1028 pp.
S COTT A.J. & K NOTT, M. (1974). A cluster analysis method
for grouping means in the analysis of variance. Biometrics
30, 507-512.
S IQUEIRA, K.M.S., F REITAS, V.M., A LMEIDA, M.R.A., S AN TOS , M.F.A., R ESENDE, F.O., T IGANO , M.S. & C ARNEIRO ,
R.M.D.G. (2009). Deteco de Meloidogyne mayaguensis em
goiabeira e mamoeiro no estado de Gois, usando marcadores
moleculares. Tropical Plant Pathology 34, 256-260.
S TIRLING, G.R. & M ANKAU, R. (1978). Parasitism of Meloidogyne eggs by a new fungal parasite. Journal of Nematology
10, 236-240.
727

R.M.D.G. Carneiro et al.

S TIRLING, G.R., M C K ERRY, M.V. & M ANKAU, R. (1979).

Biological control of root-knot nematodes (Meloidogyne
spp.) on peach. Phytopathology 69, 806-809.
T IGANOMILANI, M.S., C ARNEIRO, R.G., FARIA, M.R.,
F RAZO, H.S. & M CCOY, C.W. (1995). Isozyme characterization and pathogenicity of Paecilomyces fumosoroseus and
P. lilacinus to Diabrotica speciosa (Coleoptera: Chrysomelidae) and Meloidogyne javanica (Nematoda: Tylenchidae). Biological Control 5, 378-382.

728

X U, J., L IU, P., M ENG, Q. & L ONG, H. (2004). Characterization

of Meloidogyne species from China using isozyme, phenotypes and amplified mitochondrial DNA restriction fragment
length polymorphism. European Journal of Plant Pathology
110, 309-315.
Z HUO, K., H U, M.X., L IAO, J.L. (2010). First report of Meloidogyne enterolobii on arrowroot in China. Plant Disease 94,
271.

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