Nematophagous fungi from Mexico with activity against the sheep ...
Nematophagous fungi from Mexico with activity against the sheep ...
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Artículo Original<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108<br />
<strong>Nematophagous</strong> <strong>fungi</strong> <strong>from</strong> <strong>Mexico</strong> <strong>with</strong> <strong>activity</strong><br />
<strong>against</strong> <strong>the</strong> <strong>sheep</strong> nematode Haemonchus contortus<br />
ACEVEDO-RAMÍREZ P.M.C. 1 , QUIROZ-ROMERO H. 1 , VALERO-COSS R.O. 2 ,<br />
MENDOZA-DE GIVES P. 2 and GÓMEZ J.L 3<br />
1<br />
Departamento de Parasitología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de<br />
México UNAM.<br />
2<br />
Laboratorio de Helmintología, CENID-Parasitología Veterinaria, Instituto Nacional de Investigaciones Forestales,<br />
Agrícolas y Pecuarias, Jiutepec, Morelos.<br />
3<br />
Departamento de Bioquímica, Facultad de Medicina, UNAM.<br />
ABSTRACT<br />
The use of nematophagous <strong>fungi</strong> (NF) is a biological control alternative for gastrointestinal parasitic<br />
nematodes (GIN) in ruminants. The aim to <strong>the</strong> present work was to isolate and to identify nematophagous<br />
<strong>fungi</strong> <strong>with</strong> potential predatory <strong>activity</strong> <strong>against</strong> Haemonchus contortus larvae (L 3<br />
) in some regions of<br />
<strong>Mexico</strong>. Two hundred and fifty-nine samples <strong>from</strong> <strong>the</strong> soil, roots and ovine, caprine, bovine and porcine<br />
feces were collected <strong>from</strong> diverse zones of <strong>the</strong> country. Samples were transferred into agar plates,<br />
sprinkling technique was carried out and H. contortus L 3<br />
were used to determine in vitro nematophagous<br />
<strong>fungi</strong> predatory effect. Plates were incubated at room temperature and were revised under a stereoscopic<br />
microscope at 7, 14 and 28 days. The taxonomic identification revealed <strong>the</strong> presence of seven species of<br />
nematophagous <strong>fungi</strong>: Arthrobotrys oligospora, A. musiformis, A. kirghizica, A. brochopaga, A. conoides,<br />
A. superba and Monacrosporium gephyropagum. This is <strong>the</strong> first report on <strong>the</strong> presence of A. kirghizica and<br />
M. gephyropagum in <strong>Mexico</strong>. All species had predatory effect <strong>against</strong> H. contortus L 3<br />
however, A. conoides<br />
and M. gephyropagum showed <strong>the</strong> highest predatory <strong>activity</strong> <strong>with</strong> 93% and 83%, respectively.<br />
Key words: <strong>Nematophagous</strong> <strong>fungi</strong>, Arthobotrys, Monacrosporium, Haemonchus contortus.<br />
RESUMEN<br />
El propósito del presente trabajo fue aislar e identificar hongos nematófagos con potencial actividad<br />
contra larvas 3<br />
de Haemonchus contortus en algunas regiones de México. Para ello se recolectaron 259<br />
muestras de suelos, raíces y excrementos de ovinos, caprinos, bovinos y porcinos en diferentes localidades<br />
del país. Estas muestras se transfirieron a placas Petri en delgadas capas y larvas 3<br />
de H. contortus se usaron<br />
para determinar “in vitro” efectos nematófagos predatorios de hongos. Las placas Petri se incubaron a<br />
temperatura ambiente y se revisaron bajo microscopio estereoscópico a los 7, 14 y 28 días. La taxonomía<br />
Recibido: 24 de Febrero de 2011. Aprobado: 08 de Mayo de 2001.<br />
Correspondencia: Av. Universidad 3000, Coyoacan, C.P. 04510, México D. F., México.<br />
Phone, fax : 52(55) 5622-5898.<br />
E-mail: hquiroz@unam.mx, pedromdegives@yahoo.com, perlacevedoram@hotmail.com<br />
103
P. M. C. ACEVEDO et al.<br />
reveló la presencia de 7 especies de hongos nematófagos Arthrobotrys oligospora, A. musiformis, A.<br />
kirghizica, A. brochopaga, A. conoides, A. superba y Monacrosporium gephyropagum. Este es el primer<br />
informe de A. kirghizica y M. gephyropagum en México. Todas las especies tuvieron efecto predatorio<br />
contra l 3<br />
de H. contortus, sin embargo, A. conides y M. gephyropagum mostraron la mayor actividad<br />
predatoria con un 93% y 83% respectivamente.<br />
Palabras clave: Nematophagus <strong>fungi</strong>, Arthrobotrys, Monacrosporium, Haemonchus contortus.<br />
INTRODUCTION<br />
Gastrointestinal nematode (GIN) control is<br />
based on <strong>the</strong> use of a <strong>the</strong>rapeutic chemical strategy;<br />
never<strong>the</strong>less, <strong>the</strong> periodical and irrational use<br />
of an<strong>the</strong>lmintics, sub<strong>the</strong>rapeutic doses administration<br />
and short periods of applications, as well as<br />
<strong>the</strong> scarce alternation of different family of drugs,<br />
have resulted in rapid appearance of parasites resistant<br />
to chemicals. Haemonchus is no <strong>the</strong> exception,<br />
<strong>the</strong>re are resistant strains to bencimidazoles, imidazathiazoles<br />
and macrocyclic lactones, specially<br />
to ivermectin (Campos et al,1992; 2001; Torres et<br />
al, 2003; Encalada-Mena et al, 2008). Thus, <strong>the</strong> use<br />
of nematophagous <strong>fungi</strong> is a biological control alternative<br />
for this parasite.<br />
Although in <strong>Mexico</strong>, some nematophagous <strong>fungi</strong><br />
species have been identified (Lappe and Ulloa,<br />
1982; Llerandi-Juarez and Mendoza de Gives,<br />
1998); it remains as fundamental to perform studies<br />
that allow to know adittional genera and species of<br />
nematophagous <strong>fungi</strong> <strong>with</strong> potential <strong>against</strong> GIN of<br />
ruminants. The aim of this work was to isolate and<br />
to identify nematophagous <strong>fungi</strong> <strong>from</strong> diverse substrates<br />
of several localities in <strong>Mexico</strong> <strong>with</strong> predatory<br />
<strong>activity</strong> <strong>against</strong> H. contortus third stage larvae.<br />
MATERIAL AND METHODS<br />
Area of study. Material collection (soil, roots,<br />
and ruminant and pig feces) was carried out <strong>from</strong><br />
September 2008 to June 2009 in several federal<br />
entities of <strong>Mexico</strong> (Morelos, Puebla, Veracruz,<br />
Estado de México, Guanajuato, Sinaloa, Hidalgo<br />
and Distrito Federal). Samples were collected and<br />
placed into polyethylene bags for shipment and<br />
process at <strong>the</strong> laboratory.<br />
Sampling of different substrates for <strong>the</strong> isolation<br />
of nematophagous <strong>fungi</strong>. Samples consisting<br />
of soil, roots and ovine, bovine and caprine feces<br />
were taken <strong>from</strong> <strong>the</strong> soil surface and <strong>from</strong> a depth<br />
of 5 cm. Samples were collected <strong>from</strong> different localities<br />
of <strong>Mexico</strong> (Table 1). The collected material<br />
was placed in separate sterile plastic bags, <strong>with</strong> its<br />
respective identification. They were sent to <strong>the</strong> laboratory<br />
of Helmintology at CENID-PAVET and to<br />
<strong>the</strong> Department of Parasitology at <strong>the</strong> Facultad de<br />
Table 1. Sampling collection site for predatory nematophagous <strong>fungi</strong> search<br />
Study areas<br />
Jardines del Cenid-Pavet, Jiutepec, Morelos<br />
Rancho Experimental Las Margaritas, Hueytamalco, Puebla<br />
Centro de Enseñanza, Investigación y Extensión en Ganadería Tropical<br />
(CEIEGT), Martínez de la Torre, Veracruz<br />
Centro de Enseñanza, Investigación y Extensión en Producción Agro-<br />
Silvo-Pastoril (CEiepasp), Chapa de Mota, Edo. de México<br />
Centro de Enseñanza, Práctica e Investigación en Producción y Salud<br />
Animal (CEPIPSA); facultad de Estudios Superiores Zaragoza; Tlapan<br />
San Miguel de Allende, Guanajuato<br />
Facultad de Veterinaria de la Universidad Autónoma de Sinaloa, Culiacán,<br />
Sinaloa<br />
Ixmiquilpan, Hidalgo<br />
Climate (García 1987)<br />
Semiwarm<br />
Warm tropical rain<br />
Warm tropical rain<br />
Template cool and log summer<br />
Template cool and long summer<br />
Dry, warm summer<br />
Dry, cool summer<br />
Dry, semiwarm<br />
104<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108
NEMATOPHAGOUS FUNGI AGAINST HAEMONCHUS CONTORTUS<br />
Medicina Veterinaria y Zootecnia de la Universidad<br />
Nacional Autónoma de México for fur<strong>the</strong>r analysis.<br />
Samples were stored at 4ºC until <strong>the</strong>ir processing<br />
(Su et al, 2007).<br />
<strong>Nematophagous</strong> <strong>fungi</strong> isolation. The soil<br />
sprinkling on water-agar plates technique described<br />
by Barron, 1977 was used to isolate nematophagous<br />
<strong>fungi</strong>. Chloramphenicol (500 mg/L) was added to<br />
<strong>the</strong> culture media to avoid bacteria growth. The assay<br />
was done by duplicate. Seven days after seeding,<br />
an aqueous suspension <strong>with</strong> an undetermined<br />
number of H. contortus larvae was added, <strong>the</strong>y<br />
were incubated at room temperature for ano<strong>the</strong>r<br />
7 days (Wyborn et al, 1969). For identification of<br />
fungal structure (rings, nets, conidia) as well as <strong>the</strong><br />
detection of trapped nematodes, a stereoscopic microscope<br />
was used for observation at 7, 14 and 28<br />
days of incubation.<br />
Taxonomic identification of nematophagous<br />
<strong>fungi</strong>. Fungi identification was carried out by<br />
observation of morphometric characteristics under<br />
a light microscope. The taxonomic identification<br />
codes published by Cooke and Godfrey (1964), Van<br />
Oorschot (1985) and Rubner (1996) were used.<br />
Sheep faecal cultures to obtain Haemonchus<br />
contortus infective larvae. For <strong>the</strong> obtainment of<br />
H. contortus larvae, fecal samples <strong>from</strong> a <strong>sheep</strong>,<br />
previously infected <strong>with</strong> H. contortus L 3,<br />
were used.<br />
Feces were collected and a coproculture prepared<br />
during 10 days at room temperature. Afterwards,<br />
larvae were collected using Baermann fondle were<br />
stored at 4ºC until <strong>the</strong>ir use (Hendrix, 1999).<br />
Evaluation of <strong>the</strong> in vitro trapping capability<br />
of nematophagous <strong>fungi</strong> <strong>against</strong> Haemonchus<br />
contortus third stage larvae. Each fungus species<br />
was grown into Petri dishes of 6 cm in diameter<br />
<strong>with</strong> agar-water medium. Plates were incubated<br />
for 3 weeks at room temperature (25-28°C). After<br />
this period, one hundred H. contortus infective<br />
larvae were placed on <strong>the</strong> surface of each plate<br />
and incubated for 5 days at room temperature.<br />
Ten replicates were made for each fungus species;<br />
besides, agar-water dishes <strong>with</strong>out fungus were<br />
placed and used as control. After 5 days, <strong>the</strong> surface<br />
of <strong>the</strong> Petri dishes were scrapped <strong>with</strong> a spatula<br />
and washed <strong>with</strong> distilled water and <strong>the</strong> liquid<br />
was collected into assay tubes and refrigerated for<br />
2 hours at 4ºC to allow larvae migrate to <strong>the</strong> tube<br />
bottom. The volume of <strong>the</strong> tubes was adjusted to 2<br />
mL where larvae were found. Ten aliquots of 20 µL<br />
were taken and <strong>the</strong> recovered larvae were counted<br />
<strong>with</strong> <strong>the</strong> aid of a stereoscopic microscope.<br />
Data interpretation. Statistical analyses.<br />
Recovered larvae were counted and a capture percentage<br />
was estimated. A non-parametric U-Mann-<br />
Witney test was carried out to identify trapping difference<br />
between species.<br />
RESULTS<br />
<strong>Nematophagous</strong> <strong>fungi</strong> identification: From<br />
Figure 1. Arthobotrys oligospora. A: conidia (40X). B. Trapped larva (40X)..<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108<br />
105
P. M. C. ACEVEDO et al.<br />
Figure 2. Arthobotrys misifprmis. A: conidia (40X). B. Three-dimensional networks (10X).<br />
Figure 3. Arthobotrys kirghizica. A: conidia (40X). B. Three-dimensional networks (10X).<br />
Figure 4. Arthobotrys brochopaga. A: conidia, constrictor rings (10X). B. Trapped Haemonchus contortus (40X).<br />
106<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108
NEMATOPHAGOUS FUNGI AGAINST HAEMONCHUS CONTORTUS<br />
Figure 5. Monacrosporium gephyropagum. A: conidia (40X). B: Scalariform net (40X).<br />
<strong>the</strong> total of 259 samples, in 29 (11.2%) it was<br />
possible to isolate nematophagous <strong>fungi</strong> belonging<br />
to 7 species. All species showed predatory effect<br />
<strong>against</strong> H. contortus infective larvae. In Table<br />
2, <strong>the</strong> number of collected samples that resulted<br />
positive to predatory nematophagous <strong>fungi</strong> and<br />
corresponding species is summarized.<br />
In Figures 1-7, <strong>the</strong> different nematophagous<br />
<strong>fungi</strong> identified in different study areas of <strong>Mexico</strong><br />
are shown. The majority of <strong>the</strong> positive samples<br />
for nematophagous <strong>fungi</strong> were <strong>from</strong> warm wea<strong>the</strong>r<br />
zones. In <strong>the</strong> temperate regions, positive samples<br />
were found only in <strong>the</strong> Distrito Federal. In <strong>the</strong> lat-<br />
Figure 6. Arthrobotrys superba conidia (40X).<br />
Figure 7. Arthrobotrys conoides A: conidia (40X). B: Trapped Haemonchus contortus in three-dimensional network<br />
(10X).<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108<br />
107
P. M. C. ACEVEDO et al.<br />
Figure 8. Haemonchus contortus larvae 3 (L 3<br />
) trapping percentage by nematophagous <strong>fungi</strong>. Different species of<br />
nematophagous <strong>fungi</strong> were in Petri dishes <strong>with</strong> agar-water (2%), at room temperature and after twenty-one days, 100 H.<br />
contortus L 3<br />
were added. Seven days later, <strong>the</strong> dishes were washed and <strong>the</strong> surface scrapped. Free larvae were collected<br />
and trapping percentage was calculated.<br />
Study<br />
areas<br />
Table 2. Nematophagus <strong>fungi</strong> isolation in different study areas<br />
Positives samples<br />
/ Total samples<br />
Species<br />
Samples<br />
1 1/10 Arthrobotrys<br />
Bovine feces colected garden<br />
oligospora (Figure 1)<br />
2 6/47 A. musiformis (Figure 2) Soil <strong>from</strong> garden, decaying soil<br />
<strong>from</strong> coffee, orange tree and mint<br />
pot<br />
3 6/33 A. oligospora<br />
A. musiformis<br />
A. kirghizica (Figure 3)<br />
Monacrosporium sp<br />
4 0/55<br />
5 2/34 Arthrobotrys sp<br />
A. brochopaga (Figure 4)<br />
6 40/9 A. oligospora<br />
Monacrosporium gephyropagum<br />
(Figure 5)<br />
A. superba (Figure 6)<br />
A. conoide (Figure 7<br />
7 4/25 No identified<br />
Soil <strong>from</strong> garden, decaying soil<br />
Decaying soil<br />
Sheep feces colected <strong>from</strong> soil<br />
Soil <strong>from</strong> garden<br />
Sheep feces <strong>with</strong> soil<br />
Soil <strong>from</strong> garden, compost<br />
Soil <strong>from</strong> garden<br />
Soil <strong>from</strong> garden<br />
8 1/15 A. oligospora Soil <strong>from</strong> garden<br />
Total 29/259 (11,2%) 7 different species<br />
ter region, four different species were identified<br />
and <strong>the</strong> highest quantity of samples <strong>with</strong> predatory<br />
nematophagous <strong>fungi</strong> was recorded. A. oligospora<br />
was <strong>the</strong> most frequent species observed, since it was<br />
found in several localities, followed by A. musiformis.<br />
A. brochopaga <strong>fungi</strong> (producer of constrictor<br />
rings) and A. kirghizica were identified in samples<br />
collected <strong>from</strong> Sinaloa and Veracruz, respectively.<br />
A. superba, A. conoides and Monacrosporium gephyropagum<br />
were recorded in <strong>the</strong> Distrito Federal.<br />
108<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108
NEMATOPHAGOUS FUNGI AGAINST HAEMONCHUS CONTORTUS<br />
Trapping capability of nematophagous <strong>fungi</strong>:<br />
All <strong>the</strong> <strong>fungi</strong> species shown predatory effect<br />
<strong>against</strong> H. contortus infective larvae. There was<br />
statistical difference in trapping capability between<br />
species (P < 0.05). All species were different to <strong>the</strong><br />
control; <strong>the</strong>re was no statistical difference between<br />
A. oligospora, A. kirghizica, A. brochopaga and A.<br />
musiformis, but A. conoides and M. gephyropagum<br />
statistically differed <strong>from</strong> all o<strong>the</strong>r species (P <<br />
0.05) <strong>with</strong> 94% and 83% trapping <strong>activity</strong> respectively.<br />
In Figure 8, trapping percentages of H. contortus<br />
L 3<br />
in different nematophagous <strong>fungi</strong> (NF)<br />
species at 28 days of NF culture are shown.<br />
DISCUSSION AND CONCLUSIONS<br />
There is a variety of predatory nematophagous<br />
<strong>fungi</strong> in <strong>Mexico</strong>. A. oligospora is a worldwide<br />
frequent species and has a high incidence in several<br />
entities in <strong>Mexico</strong>, followed by A. musiformis.<br />
Previously, <strong>the</strong>se <strong>fungi</strong> have been recorded in<br />
Morelos and in this study <strong>the</strong>y were also recorded<br />
in Veracruz, Hidalgo and Federal District. Arthrobotrys<br />
conoides was recorded in a locality near <strong>the</strong><br />
Ajusco, just as Lappe and Ulloa (1982) had already<br />
identified it in nearby places; hence this is a distribution<br />
zone for this fungus. This is <strong>the</strong> first record<br />
about <strong>the</strong> presence of A. kirghizica and Monacrosporium<br />
gephyropagum in <strong>Mexico</strong>. A. superba has<br />
been previously recorded in <strong>the</strong> State of Morelos<br />
(Llerandi-Juarez and Mendoza-de Gives, 1998);<br />
never<strong>the</strong>less, this is <strong>the</strong> first record made on this<br />
species in <strong>the</strong> Distrito Federal. All mentioned <strong>fungi</strong><br />
species showed in vitro predatory <strong>activity</strong> <strong>against</strong><br />
H. contortus infective stage.<br />
In comparison to o<strong>the</strong>r countries, in Germany, 9<br />
species of Arthrobotrys, 2 species of Monacrosporium,<br />
1 species of Duddingtonia, were identified;<br />
<strong>the</strong> large number of predatory nematophagous <strong>fungi</strong><br />
isolated might be due to <strong>the</strong> fluorescence technique<br />
that <strong>the</strong>y used (Saxena and Lysek, 1993). A. conoides,<br />
A. musiformis, A. oligospora and A. superba<br />
have been identified in Germany, Scotland and in<br />
this study, also A. gephyropagum and A. kirghizica<br />
and Drechslerella brochopaga (Sexena, 2008) were<br />
similarly recorded in Scotland and <strong>Mexico</strong> <strong>with</strong> <strong>the</strong><br />
difference that in Scotland A. gephyropaga and Dr.<br />
brochopaga were most frequent and in this study it<br />
was A. oligospora.<br />
In <strong>the</strong> province of Yunan, China, found 17 different<br />
species <strong>from</strong> 660 fecal samples (Su et al,<br />
2007), most of <strong>the</strong>m belonged to A. oligospora and<br />
A. musiformis, which coincides that <strong>the</strong>se species<br />
were <strong>the</strong> most frequently recorded.<br />
Kelly et al, (2009) collected 12 species of<br />
nematophagous <strong>fungi</strong> in 120 samples <strong>from</strong> Irish<br />
pastures. From <strong>the</strong>se, Monacrosporium cianopaga,<br />
Duddingtonia flagrans and D. coniospora were<br />
detected in fresh feces samples. In contrast, in<br />
<strong>the</strong> present study only four positive samples to A.<br />
oligospora and A. brochopaga were isolated <strong>from</strong><br />
bovine feces, and A. kirghizica was isolated <strong>from</strong><br />
ovine feces; never<strong>the</strong>less, it worth to mention that<br />
samples were collected <strong>from</strong> <strong>the</strong> soil; <strong>the</strong>refore,<br />
<strong>the</strong> presence of <strong>fungi</strong> on feces could have been a<br />
secondary contamination and not necessarily that<br />
<strong>the</strong>y had already been on <strong>the</strong>m, hence having<br />
passed through <strong>the</strong> digestive tract of <strong>the</strong> animals.<br />
No predatory nematophagous <strong>fungi</strong> were identified<br />
in ovine, caprine, bovine and porcine feces<br />
samples, probably because <strong>the</strong>y are pen confined<br />
animals and it coincides <strong>with</strong> <strong>the</strong> recorded by Larsen<br />
et al, (1994) who only observed a scarce number<br />
of <strong>fungi</strong> <strong>from</strong> ruminant feces.<br />
Predatory nematophagous <strong>fungi</strong> positive samples<br />
correspond, in <strong>the</strong>ir majority, to soil collected<br />
<strong>from</strong> <strong>the</strong> garden as decomposed matter or under<br />
ornamental or aromatic plants. By <strong>the</strong> number of<br />
positive samples, it can be concluded that nematophagous<br />
<strong>fungi</strong> are more widely distributed in<br />
warm humid zones, its presence decreases in temperate<br />
zones, although this must be taken <strong>with</strong><br />
caution.<br />
Gonzalez-Cruz et al, (1998) recorded a trapping<br />
percentage of 93.1% of M. gephyropagum <strong>against</strong><br />
Strongyloides papillosus, in contrast <strong>with</strong> <strong>the</strong><br />
present study where trapping <strong>activity</strong> was 84% for H.<br />
contortus L 3<br />
. Several species of Arthrobotrys genus<br />
have demonstrated to have around 80% trapping<br />
<strong>activity</strong> <strong>against</strong> H. contortus infective larvae; A.<br />
oligospora was <strong>the</strong> most active (Waller and Faedo,<br />
1993), which contrasted <strong>with</strong> <strong>the</strong> present study,<br />
since A. conoides resulted <strong>with</strong> a higher trapping<br />
percentage, followed by M. gephyropagum.<br />
It is concluded that in <strong>Mexico</strong> <strong>the</strong>re are<br />
nematophagous <strong>fungi</strong> <strong>with</strong> predatory effect<br />
<strong>against</strong> H. contortus L 3,<br />
<strong>from</strong> which A. conoides<br />
and M. gephyropagum had a high trapping<br />
percentage.<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108<br />
109
P. M. C. ACEVEDO et al.<br />
REFERENCES<br />
1. BARRON G. 1977. The nematode-destroying <strong>fungi</strong>.<br />
Canadian Biological Publications Ltd. Canada. 140 p.<br />
2. CAMPOS R, HERRERA D, QUIROZ R. 1992. Diagnóstico<br />
in vitro de Haemonchus contortus resistente al<br />
albendazol, fenbendazol, oxfendazol y febantel en tres<br />
rebaños ovinos Tabasco o Pelibuey. Vet Mex 23, 51-56.<br />
3. COOKE RC, GODFREY BES. 1964. A key to <strong>the</strong> nematode-destroying<br />
<strong>fungi</strong>. Transactions British Mycological<br />
Society. 47(1), 61-74.<br />
4. ENCALADA L, LÓPEZ M, MENDOZA P, LIÉBANO<br />
E, VÁZQUEZ V, VERA G. 2008. Primer informe en<br />
México sobre la presencia de resistencia a ivermectina<br />
en bovinos infectados naturalmente con nematodos<br />
gastrointestinales Vet. Méx. 39 (4).<br />
5. GARCÍA E. 1988. Modificaciones al sistema de clasificación<br />
climática de Köppen. (Para adaptarlo a la<br />
República Mexicana). 4a ed. México.<br />
6. GONZÁLEZ-CRUZ M, MENDOZA DE GIVES P,<br />
QUIROZ-ROMERO H. Comparison of <strong>the</strong> trapping<br />
abililty of Arthrobotrys robusta and Monacrosporium<br />
gephyropagum on infective larvae of Strongyloides<br />
papillosus. J. Helminthol. 1998; 72: 209-213.<br />
7. HENDRIX CM. 1999. Diagnóstico Parasitológico<br />
Veterinario. Harcourt-Brace. 2nd Ed. España.<br />
8. KELLY P, GOOD B, HANRAHAN J, FITZPATRICK<br />
R, WAAL T. 2009. Screening for <strong>the</strong> presence of nematophagous<br />
<strong>fungi</strong> collected <strong>from</strong> Irish <strong>sheep</strong> pastures.<br />
Vet. Parasitol. 165: 345-349.<br />
9. LAPPE P, ULLOA M. 1982. Hongos destructores de<br />
nematodos en algunos suelos de México. Bol. Soc.<br />
Mex. Mic. 17, 99-113.<br />
10. LARSEN M, FAEDO M, WALLER P. 1994. The<br />
potential of nematophagous <strong>fungi</strong> to control <strong>the</strong> freeliving<br />
stages of nematode parasites of <strong>sheep</strong>: survey<br />
for <strong>the</strong> presence of <strong>fungi</strong> in fresh faeces of grazing<br />
livestock in Australia. Vet. Parasitol. 53: 275-281.<br />
11. LLERANDI- JUÁREZ R, MENDOZA DE GIVES P.<br />
1998. Resistence of chamydospores of nematophagous<br />
<strong>fungi</strong> to <strong>the</strong> digestive processes of <strong>sheep</strong>. J. Helminthology.<br />
72: 209-213.<br />
12. RUBNER A. 1996. Revision of predacious Hyphomycetes<br />
in <strong>the</strong> Dactylella-Monacrosporium complex. Taxonomy.<br />
Studies in Micology. 39: 134 pp.<br />
13. SAXENA G, LYSEK G. 1993. Observation of nematophagous<br />
<strong>fungi</strong> in natural soils by fluorescence microscopy<br />
and <strong>the</strong>ir correlation <strong>with</strong> isolation. Mycol.<br />
Res. 97(8): 1005-1011.<br />
14. SAXENA G. 2008. Observations on <strong>the</strong> occurrence<br />
of nematophagous <strong>fungi</strong> in Scotland. Applied soil<br />
ecology. 39: 352-357.<br />
15. SU H, HAO Y, MO M, ZHANG K. 2007. The ecology<br />
of nematodo-trapping hyphomycetes in cattle dung<br />
<strong>from</strong> three plateau pastures. Vet. Parasitol. 144: 293-<br />
298.<br />
16. TORRES J, ROBERTS B, CANTO J, MARTÍNEZ<br />
C, RODRÍGUEZ J, CANUL L, COB L, TIRADO F,<br />
AGUILAR A. 2003. Prevalence of <strong>sheep</strong> herds <strong>with</strong><br />
gastrointestinal nematodes resistant to benzimidazoles,<br />
imidazothiales and macrocyclic lactones in Yucatan. V<br />
International Seminar of Animal Parasitology, Yucatan,<br />
<strong>Mexico</strong>. 48-52.<br />
17. VAN OORSCHOT C. 1985. Taxonomy of <strong>the</strong> Dactylaria<br />
complex V. A review of Arthrobotrys and allied<br />
genera. Studies in Micology, 26: 61-122.<br />
18. WALLER P, FAEDO M. The potential of nematophagous<br />
<strong>fungi</strong> to control <strong>the</strong> free-living stages of nematode<br />
parasites of <strong>sheep</strong>: screening studies. Vet. Parasitol.<br />
1993; 49: 285-297.<br />
19. WYBORN CHE, PRIEST D, DUDDINGTON CL.<br />
1969. Selective technique for <strong>the</strong> determination of<br />
nematophagous <strong>fungi</strong> in soils. Soil Bid. Eiochem. 1,<br />
101-102.<br />
Acknowledgements: Special thanks to CONACYT for <strong>the</strong><br />
scholarship granted to Perla Maria del Carmen Acevedo-<br />
Ramirez, to Dr. Enrique Liebano for to provide H. contortus<br />
L 3<br />
and to Ana Arana Contreras, Esau Villarreal Olvera,<br />
Karina Leon Lopez and Elvia Lopez Martinez for <strong>the</strong>ir kind<br />
collaboration in <strong>the</strong> collection and handling of samples.<br />
110<br />
Rev. Ibero-Latinoam. Parasitol. (2011); 70 (1): 101-108