Profitability in livestock farming is
adversely affected due to different types of parasitic and vector borne
infections (Imran et al. 2018;
Rashid et al. 2019; Zafar et al. 2019) and gastrointestinal
nematodes (GINs) is one of the major impediments. The most common method for
control of GINs is the use of synthetic anthelmintics. The development of resistance in parasites to
several families of anthelmintics (Leathwick et al. 2001; Ijaz
et al. 2018) has posed a threat in
affective chemotherapeutic parasite control. In the last two decades, resistance has developed
rapidly throughout the world and increasing incidents of anthelmintic
resistance (AR) in Brazil, Argentina, New Zealand, USA, and the UK have been
reported (Waghorn et al. 2006; Stafford et al. 2007). This
increased prevalence of AR and the issue of drug residues in animal products
(Manzoor et al. 2019) have provided a spur for research into
‘alternative/novel’ approaches for control of GINs. The search for novel
approaches is not only driven by AR but also by the need for techniques that
are feasible for application by resource-poor farmers in non-commercial
subsistence farming systems. The utilization of nematophagous fungi (NF), which
parasitise nematodes, is one of such alternatives to control the nematode
population (Khattak et al. 2018).
Various species of NF have been
identified as potential biological control agents to decrease the infection
level of GINs in ruminants (Chandrawathani et al. 2004; Waller et al.
2004). These NF belong to all major taxonomic groups but the majority belongs
to phylum Ascomycetes (Gams et al. 1998). All
NF can be divided into two major groups i.e., predacious and
endoparasitic, which are further categorized based on killing or trapping
behavior. The predacious fungi construct extensive hyphal structures in their
surrounding environment that produce adhesive traps or nets at intervals that
trap and kill the nematode. In contrast, the endoparasitic NF produces
encysting spores that adhere to and penetrate the
egg-shell or conidia that are ingested and grow within the nematode (Basualdo et
al. 2000).
Surveys for documentation of
NF in the faecal environment have been conducted in various countries of the
globe like; Australia (Larsen et al. 1994), Brazil (Saumell et al.
2000), Iran (Ghahfarokhi et al. 2004), Malaysia (Chandrawathani et al.
2002), New Zealand (Skipp et al. 2002) and South Africa (Durand et al.
2005). As far as literature could be ascertained, In Pakistan, no survey to
check the prevalence of naturally occurring NF has been conducted. Keeping in
view the significance of NF in control of GINs and no availability of data from
Pakistan, this study has been planned with objectives to document the species
of naturally occurring NF present on pastures in hilly areas. To check the
effect of temperature and rainfall on the prevalence of NF, the seasonal
variation was also estimated in the current study. This study will provide
baseline data on prevalent species of NF and will help in designing a biological
control program.
The samples were collected in both the Summer
and Winter seasons for three years to record the maximum number of naturally
occurring NF in hilly areas. Faecal and soil samples were collected from sheep
farms to isolate all naturally occurring NF in the study area. Information
obtained was recorded in the form of the frequency of occurrence.
Study area
Pakistan is
a country with varying climatic
conditions having four seasons annually i.e., Winter,
Spring, Summer, and Autumn. It also has a
variety of terrain conditions, mountains,
hills, arid lands, and desserts. This study was carried out in the hilly area (District Manshera) to
check the difference in the natural occurrence of NF in Summer
and Winter Winterseasons for three consecutive years. District Mansehra is mainly a hilly area located in Khyber
Pakhtunkhwa, Pakistan. It is located 34.6744° N and 73.3709° E at an altitude of 1,088 meters above sea
level. The annual rainfall (1445 mm) is concentrated in the Summer.
The climate of the region is rainy in the Summer and
dry in Winter. The estimates of temperatures and rain falls during these
seasons have been mentioned in Table 1. The average annual temperature in the
region falls around 22.5°C.
During each season, a total of 150 random samples were collected (5 g
each) from small ruminant livestock farms. Faecal material was acquired
directly from the rectum of animals and the ground after wearing gloves. Some soil along faecal deposit area was also collected as
naturally occurring NF from the soil surrounding the faecal culture enters the
faecal material to predate the larvae. After collection, all the samples
were pooled into one big container and mixed to maximize the chances of
isolation of NF. All containers were clearly and completely labeled (location,
animal, date of collection) and samples were brought to the laboratory at the
Department of Parasitology, the University of Agriculture Faisalabad within 12
h after collection.
In the laboratory, the collected samples were homogenized thoroughly. Out
of the homogenized faecal material, 10 samples (2 g each) were crumpled and
cultivated on individual Petri dishes comprising 2% water agar with nematode
larvae as bait (1000 larvae/Petri dish). Petri dishes were then enclosed and
retained at 21–26°C for 3 weeks. Petri dishes were examined underneath the
stereomicroscope weekly to check any fungal growth.
The NF cultured on the Petri plates were then isolated and refined in
pure cultures for identification procedure. First, they were shifted to clean
water agar plates and L3 from mixed infection of GINs
were added to the Petri plates as a source of bait ensuring eminent
proliferation. After growth on water agar Petri plates, conidia were then
shifted to cornmeal (2%) agar plates and net development was encouraged by the
addition of L3 of GINs to pure cultures for identification. The identification was carried out based on
morphological features (as the morphology of conidiophores and conidial size in
the micro-culture) and trapping structure produced by the fungus on nematode
infected culture. This was achieved primarily by following the explanations of Subramanian (1963), Cooke and Godfrey (1964),
Cooke and Dickinson (1965), Schenck et al. (1977), van Oorschot (1985), Gams (1988), Liu and Zhang (1994)
and Rubner (1996).
A total of
21 NF belonging to seven different genera were observed. The maximum number of
species from genus Arthrobotrys was recorded
(n=7) followed by genus Dactylaria (n=5) and Nematoctonus (n=4). Name of
individual NF species and their total frequency of occurrence along with different infection structures observed in Summer and Winter seasons have been presented in Table 2 and
3 respectively.
The samples collected (n=150/sampling)
in Summer 2013, 2014 and 2015, showed total
frequencies of n = 166, n=142 and n= 145, respectively. In Summer
2013 the occurrence of NF with different infection structures Table 1: Avergae temperature and rainfall of district Mansehra, Pakistan
|
Seasons |
Summer |
Winter |
|||||
|
June |
July |
August |
September |
December |
January |
February |
|
|
Avg. Temperature (°C) |
28 |
26.7 |
25.3 |
23.9 |
10 |
8 |
9.8 |
|
Min. Temperature (°C) |
21.3 |
21.3 |
20.4 |
18 |
4.2 |
2.6 |
4.3 |
|
Max. Temperature (°C) |
34.8 |
32.2 |
30.3 |
29.9 |
15.9 |
13.4 |
15.3 |
|
Precipitation /Rainfall (mm) |
91 |
302 |
266 |
113 |
55 |
90 |
127 |
Adopted from: https://en.climate-data.org (Anonymous, n.
d)
Table 2: Frequency
of occurrence of nematophagous fungi out of collected
samples from Jabba farm, Mansehra,
KPK, Pakistan in Summer 2013-2015
|
Nematphagus Fungi |
Predatory mechanism |
Frequency in Summer 2013 |
Frequency in Summer 2014 |
Frequency in Summer 2015 |
Total Frequency |
|
Arthrobortrys robusta |
Adhesive nets |
21 |
17 |
18 |
56 |
|
A. conoides |
Adhesive nets |
12 |
9 |
9 |
30 |
|
A. dactyloides |
Constricting rings |
4 |
5 |
6 |
15 |
|
A. brochopaga |
Adhesive spores |
5 |
6 |
4 |
15 |
|
A.
cladodes |
Adhesive nets |
18 |
9 |
22 |
49 |
|
A. oligospora |
Adhesive nets |
27 |
19 |
16 |
62 |
|
A. musiformis |
Adhesive nets |
8 |
4 |
3 |
15 |
|
Cystopage lateralisa |
Adhesive mycelia |
1 |
0 |
1 |
2 |
|
Dactylaria candida |
Non-constricting rings |
2 |
1 |
1 |
4 |
|
D. haptospora |
Conidia with adhesive branches |
3 |
0 |
1 |
4 |
|
D. leptospora |
Conidia with adhesive branches |
4 |
6 |
1 |
11 |
|
D. pyriformis |
Conidia with adhesive branches |
3 |
1 |
2 |
6 |
|
D. sclerohypha |
Conidia with adhesive branches |
1 |
2 |
0 |
3 |
|
D. heterospora |
Conidia with adhesive branches |
1 |
0 |
0 |
1 |
|
D. leptospora |
Non-constricting rings |
1 |
1 |
1 |
3 |
|
Harpsporium anguillulae |
Ingested conidia |
17 |
15 |
12 |
44 |
|
Monacrosporium spp. |
Adhesive nets |
1 |
3 |
1 |
5 |
|
Nematoctonus campylosporus |
Conidia with adhesive knobs |
3 |
2 |
0 |
5 |
|
N. robustus |
Adhesive conidia |
7 |
3 |
6 |
16 |
|
N. haptocladus |
Conidia with adhesive knobs |
2 |
0 |
1 |
3 |
|
N. tylosporus |
Conidia with adhesive knobs |
1 |
0 |
2 |
3 |
|
Total frequency |
142 |
103 |
107 |
352 |
Table
3: Frequency of
occurrence of nematophagous fungi out of collected
samples from Jabba farm, Mansehra,
KPK, Pakistan in Winter 2013-2016
|
Nematphagus Fungi |
Predatory mechanism |
Frequency in Winter 2013-2014 |
Frequency in Winter 2014-2015 |
Frequency in Winter 2015-2016 |
Total Frequency |
|
A. robusta |
Adhesive nets |
8 |
7 |
4 |
19 |
|
A. conoides |
Adhesive nets |
1 |
3 |
6 |
10 |
|
A. dactyloides |
Constricting rings |
0 |
1 |
2 |
3 |
|
A. brochopaga |
Adhesive spores |
2 |
0 |
1 |
3 |
|
A.
cladodes |
Adhesive nets |
1 |
2 |
1 |
4 |
|
A. oligospora |
Adhesive nets |
6 |
4 |
8 |
18 |
|
A. musiformis |
Adhesive nets |
0 |
1 |
3 |
4 |
|
Adhesive mycelia |
0 |
0 |
0 |
0 |
|
|
D. candida |
Non-constricting rings |
3 |
1 |
0 |
4 |
|
D. haptospora |
Conidia with adhesive branches |
0 |
0 |
0 |
0 |
|
D. leptospora |
Conidia with adhesive branches |
1 |
0 |
1 |
2 |
|
D. pyriformis |
Conidia with adhesive branches |
1 |
3 |
4 |
8 |
|
D. sclerohypha |
Conidia with adhesive branches |
2 |
1 |
2 |
5 |
|
D. heterospora |
Conidia with adhesive branches |
0 |
0 |
1 |
1 |
|
D. leptospora |
Non-constricting rings |
0 |
1 |
0 |
1 |
|
H. anguillulae |
Ingested conidia |
5 |
2 |
7 |
14 |
|
Monacrosporium spp |
Adhesive nets |
1 |
2 |
2 |
5 |
|
N. campylosporus |
Conidia with adhesive knobs |
1 |
0 |
0 |
1 |
|
N. robustus |
Adhesive conidia |
0 |
0 |
5 |
5 |
|
N. haptocladus |
Conidia with adhesive knobs |
0 |
0 |
3 |
3 |
|
N. tylosporus |
Conidia with adhesive knobs |
0 |
0 |
4 |
4 |
|
Total frequency |
32 |
28 |
54 |
114 |
were; Adhesive nets (n
= 87), Constricting rings (n = 4), Adhesive spores (n = 5), Adhesive mycelia (n
= 1), Non-constricting rings (n = 3), Conidia with adhesive branches (n = 12),
Ingested conidia (n = 17), Conidia with adhesive knobs (n = 6) and Adhesive
conidia (n = 7). A. oligospora
(n = 27), A. robusta
(n = 21), A. cladodes (n = 18), Harpsporium anguillulae (n = 17) were
the top four most frequent species. Moreover, second replication of the trial
was carried out in Summer of 2014. Out of the total
frequency, the occurrence of NF with different infection structures were;
adhesive nets (n = 61), constricting rings (n = 5), adhesive spores (n = 6),
adhesive mycelia (n = 0), non-constricting rings (n = 2), conidia with adhesive
branches (n = 9), ingested conidia (n = 15), conidia with adhesive knobs (n =
2) and adhesive conidia (n = 3), which also shows that NF with adhesive nets
were most prevalent and adhesive mycelia were least prevalent as they were
absent in this area. Although less frequent than 2013 Arthrobotrys (n =
69) was still the most predominant genus whereas, A. oligospora (n = 19), A. robusta (n
= 17), H. anguillulae
(n = 15) and Arthrobortrys conoides
(n = 9), were the top four most frequent species at Jaba farm, Mansehra in Summer of 2014. In Summer of 2015, the occurrence of NF with
different infection structures at this farm were; adhesive nets (n = 69),
constricting rings (n = 6), adhesive spores (n = 4), adhesive mycelia (n = 1),
non-constricting rings (n = 2), conidia with adhesive branches (n = 4),
ingested conidia (n = 12), conidia with adhesive knobs (n = 3) and adhesive
conidia (n = 6), which shows that NF with adhesive nets were predominant during
all three Summers and adhesive mycelia were least. A. oligospora (n = 16), A. robusta (n
= 18), A. cladodes (n = 22) and H. anguillulae
(n = 12), were the top four most frequent species in Summer
of 2015. Detailed results have been presented in Table 2.
The samples collected from Jabba farm (n=150/sampling)
during Winter 2013–14, 2014–15 and
2015–16 showed total frequencies
of 50, 40 and 95 (Table 3). Out of the total frequency, the occurrence of NF
with different infection structures at this farm were; adhesive nets (n = 17),
adhesive spores (n = 2), non-constricting rings (n = 3), conidia with adhesive
branches (n = 4), ingested conidia (n = 5), conidia with adhesive knobs (n =
1). The NFs with adhesive nets were most prevalent and constricting rings,
adhesive mycelia and adhesive conidia were least prevalent as they were absent
at this sampling instance. Arthrobotrys (n
= 18) was the most predominant genus
whereas, A. robusta
(n = 8), A. oligospora
(n = 6), H. anguillulae
(n = 5) and Dactylaria candida (n =
3), were the top four most frequent species at Jaba farm, Mansehra in Winter of 2013–2014.
In the next trial replication of Winter 2014–2015, NF with different infection
structures were; adhesive nets (n = 19), constricting rings (n = 1),
non-constricting rings (n = 2), conidia with adhesive branches (n = 4), and
ingested conidia (n = 2). The NFs with adhesive nets were most prevalent and
adhesive spores, adhesive mycelia, conidia with adhesive knobs and adhesive
conidia were absent in this area sampling. Arthrobotrys
(n = 18) was the most predominant
genus whereas, A. oligospora
(n = 4), A. robusta
(n = 7), Dactylaria pyriformis (n
= 3) and Arthrobortrys conoides (n =
3), were the top four most frequent species out of all. The frequency of
occurrence of NF with different infection structures in Winter
2015–16 were; adhesive nets (n =
24), constricting rings (n = 2), adhesive spores (n = 1), conidia with adhesive
branches (n = 8), ingested conidia (n = 7), conidia with adhesive knobs (n = 7)
and adhesive conidia (n = 5). NF with adhesive nets was most prevalent and
adhesive mycelia, non-constricting rings were not observed in this area. Arthrobotrys (n = 25) was the most predominant genus out of
all, whereas, A. oligospora
(n = 8), H. anguillulae
(n = 7), Arthrobortrys conoides (n =
6) and Nematoctonus robustus (n = 5),
were the most frequently observed species.
Discussion
Nematode trapping fungi are considered to be a useful
biological tool against parasitic nematodes in cattle and sheep (Larsen 2000;
Flores-Crespo et al. 2001). The Arthrobotrys genus is distributed
worldwide and is known for controlling nematodes by its predatory activity
(Dalla Pria et al. 1991; Naves and Campos 1991; Nordbring-Hertz et al.
2011). The NFs belonging to this genus utilizes two different carbon sources,
one in organic matter as a saprophyte and the other from the predatory activity
against nematodes, which makes it adaptable to different habitats (Wachira et
al. 2009). This ability of fungus produces a very little impact on the environment
when used as a biological control agent on livestock farms.). In vitro
testing of H. anguillulae on faecal cultures and agar media has shown
that these fungi are capable of reducing the number of free-living larval
stages significantly (Nansen et al.
1988; Waller and Faedo 1993; Mendoza-de Gives and Vazquez-Prats 1994; Mendoza-de
Gives et al. 1992, 1994). Charles et al. (1996) also evaluated the
efficacy of H. anguillulae in Brazil. He conducted an invitro assay to
estimate its efficacy in which he targeted H. contortus and percetage
reduction of 99.5% was observed at a dose rate of 300,000 conidia per gram of
faeces. Abovementioned and various other studies throughout the world showed
significant effect of nematophagous
fungi against gastro intestinal
nematodes making it a considerable candidate for developmental
strategies for control of nematodes.
In this
present study, various species of NFs were locally isolated in Mansehra and it
was found that they were isolated more abundantly in the soil/faeces collected
in Summer as compared to Winter, which was influenced
by climatic conditions. In a tropical climate, the development of pre-parasitic
forms of trichostrongylid nematodes of sheep on pasture occurs in a few days.
Thus, the rapid colonization of faeces by NF would be important in the natural
control of these parasites.
Overall, the
highest frequency of these NF was observed in the Summer
season, and a low frequency was observed in the Winter season. This may be
because NF propagates more efficiently in hot humid conditions as compared to
low temperatures and dry conditions. The optimum temperature recorded for the
growth of NF is 25°C (Anamika 2015). It has been reported that the consequent
development of adhesive networks around nematodes, was significantly slower at
the lower temperatures (5–10°C) than the
higher temperatures (15–30°C). The
colonization of the nematode by trophic hyphae is affected by temperature. At
temperatures below 15°C, it has been observed that the development of tropic hyphae
is reduced (Belder and Jensen 1994). The high prevalence of A. oligospora isolated from livestock
farms has also been reported (Mahoney and strongman 1994). In accordance with
Saumell et al. (2000), who reported the high prevalence of Arthrobotrys species in Brazil, the mean
annual temperature of the location chosen for sampling was 18.5°C, which is
similar to the annual temperature (20°C) in the present study area. High prevalence of A. oligospora, A. conoides, and A. robusta have
also been reported in Iraq and Oman (Muhsin and Kasim 1998).
The ideal
temperature range for the growth and development of the majority of the NF has
been found between 15–30°C (Cooke 1963; Pandey 1973; Grønvold et al. 1985). The temperature of the study
falls close to the ideal temperature of fungal growth this could be the reason
for a high frequency of NF recorded during the present study. The largest number
of isolates was retrieved from faeces at the
beginning of the rainy season (during Summer). During
this period of the year, the average minimum as well as maximum temperature is
increased.Under these conditions, NF became abundant. In the rainy months,
the invasion of the faeces by an abundance of free-living nematodes would
facilitate the colonization of predatory fungi. When nematodes are infected by
NF, they maintain their motility for some time thus facilitating dispersal. The
presence of a larger number of isolates of NF in rainy months was also reported
in the organic matter of the soil, where sheep pastured. Fungi, which form
adhesive nets, were predominant during the dry season. However, A.
oligospora, among the predatory fungi, was isolated in every sampling,
demonstrating their abundance in the environment and their capacity to colonize
faeces and develop in both the wet and dry months. Adhesive net-forming fungi
A. oligospora ,
which were the most abundant predatory species in the dry months, may resist
drying out, as was observed by (Gray and Bailey 1985).
Conclusion
For the treatment of nematode infections in livestock
and to prevent the spread of larvae in the environment, these NF may be
directly administered to animals. This may provide a strategy for the control
of further environmental contamination by the nematode larvae. In vitro studies are pivotal to select
effective NF before their application in the field. However, in vitro studies may give an
overestimate about the efficacy of NF; as in these trials, the nematodes cannot
escape and reproduce as they have in the natural environment. Also, they have
limited physical space and less evaluation time. So, in vivo studies may
also be conducted for the proper estimation of the predatory activity.
Acknowledgments
Authors are highly thankful to Prof. Dr.
Sajjad-ur-Rehman, Director
Institute of Microbiology, University of Agriculture Faisalabad for his help in
the cultivation
and identification of fungi. We also acknowledge the support of the staff of
the Experimental Research Station, Jabba.
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