The Study on the Role of Entomopathogenic Fungal Endophytes in Controling the Cocoa Pod Borer (Conopomorpha cramerella (Snellen)) (Lepidoptera: Gracillariidae) on Cocoa Plant
Fungal endophytes are quite common in nature and some of them had been shown to have adverse effects against insects. The study aimed to isolate and identify of fungal endophytes from healthy pods of cocoa plant and to investigate their effects against the egg of cocoa pod borer (Conopomorpha cramerella (Snellen)) in the field as well as their endophytism on cocoa pods had been carried out. The results indicated that there were five fungal endophytes genera i.e., Trichoderma sp., Fusarium sp., Beauveria sp., Aspergillus sp. and one non-identified (mycelia sterilia) were found. All isolated endophytic fungus produced a negative effect on the survival of cocoa pod borer eggs but the greater effect were produced by Beauveria sp. and Aspergillus sp. treated in liquid form with the mean of 94 and 96% of egg mortality, respectively. Trichoderma sp., also produced a relatively high of 84 and 89% egg mortality for powder and liquid, respectively. Except Beauveria sp., Trichoderma sp., Fusarium sp. and Aspergillus sp. was found to penetrate in cocoa pod after two weeks of spraying. Beauveria sp., Trichoderma sp., Aspergillus sp. are endophytic fungus which provide potential biological control for cocoa pod borer.
to cite this article:
Nur Amin, La Daha and Nurariaty Agus, 2014. The Study on the Role of Entomopathogenic Fungal Endophytes in Controling the Cocoa Pod Borer (Conopomorpha cramerella (Snellen)) (Lepidoptera: Gracillariidae) on Cocoa Plant. Journal of Entomology, 11: 142-152.
Received: October 18, 2013;
Accepted: February 03, 2014;
Published: March 28, 2014
The Cocoa Pod Borer (CPB) Conopomorpha cramerella (Snellen) (Lepidoptera:
Gracillaridae) is one of the most important limiting factors to cocoa production
in Indonesia and Malaysia (Van Grinsven, 2003). Such
various control tactics as insecticide application, sanitation, pruning and
the use of ant predators had been practiced but not completely control obtained
indicating that a new control tactic needed to keep the pest population under
economic damage without an environmental negative impact produced.
In the course to seek an effective tactic control we come across that an interesting
issue is the presence of fungal endophytes fungi on various such plant species
as grasses and trees in various part of the world and the fungi seems to provide
a protection of the plant hosts against such attacks by insect herbivores and
pathogens. The term of endophyte was coined by the German scientist, Heinrich
Anton De Bary in 1884 and used to define fungi and bacteria occurring inside
plant tissues without causing any apparent symptoms in the host (Schulz
et al., 2006). In the last few years fungal endophytes have been
detected in hundreds of plants including such important agricultural commodities
as wheat (Larran et al., 2002), bananas (Amin,
1994), maize (Amin, 2013a) tree palm oil. A number
of authors have documented that the presence of endophytic fungi provide a protection
of the plant hosts against insect herbivore (Clement et
al., 2005), parasitic nematodes (Amin, 1994,
2013b; Elmi et al., 2000)
and plant pathogens (Dingle and Mcgee, 2003; Wicklow
et al., 2005). Other authors reported specifically the effects of
endophytic fungi of Trichoderma atroviride MT-20 and S-2 as well as Fo162
added to the soil at sowing significantly reduced the number of white fly Trialeurodes
vaporariorum, Aphis gossypii and Myzus persicae (Barahona,
2010). Variable effects however have sometimes been reported, e.g., Clement
et al. (2005) reported different effects on two aphids, bird-cherry
oat aphid, Rhopalosiphum padi (L.) and rose grass aphid, Metopopophium
dirhodum (Walker) and the wheat stem sawfly Mayetiola destructor
exposed to different wild barleys infected with Neotyphodium. Fewer studies
have explored this relationship in nongrass systems. However,
Jallow et al. (2004) reported drastic negative effects on larvae
of Helicoverpa armigera (Hubner) reared on tomato plants infected with
a nongrass endophyte, Acremonium strictum.
A such entomopathogens as Beauveria bassiana (Balsamo) Vuillemin (Ascomycota:
Hypocreales) has been reported as an endophyte on maize (Cherry
et al., 2004; Wagner and Lewis, 2000; Arnold
and Lewis, 2005), tomato (Leckie, 2002), in the cocoa,
Theobroma (Evans et al., 2003), (Mejia
et al., 2008), in oil palm (Amin et al.,
2008) and in bananas (Akello et al., 2007).
The mechanisms of insect control displayed by endophytic fungi was correlated
with toxin production (Lattanzio et al., 2006)
and the production of fungal metabolites (Bush et al.,
1997; Clay and Schardl, 2002). The traditional
mode of infection of such fungal entomopathogens as B. bassiana involves
spore deposition on the insect cuticle followed by formation of a germ tube
which through enzymatic and mechanical action penetrates the cuticle (Arnold
and Lewis, 2005). Once in the hemocoel, hyphal growth causes tissue damage
and nutrient depletion. Some entomopathogenic fungi are also known to produce
metabolites, but their involvement in insect toxicosis is still unknowed (Arnold
and Lewis, 2005).
Based on our experience in the last few years in South Sulawesi which one of
the most important cocoa production area in Indonesia, it is very oven that
there are some trees with pods found to be free from cocoa pod borer infestations
while the pods of other trees around suffer serious damage. Now a question arises
what make those pods free from cocoa pod borer or diseases damage? Might the
pods be associated with the presence of such endophytic microorganisms as fungi
and or bacteria. In order to answer the question the study had been carried
out with the aim to isolate the associated microorganism and then the trials
also made to investigate their effect on the cocoa pod borer.
MATERIALS AND METHODS
Isolation of fungal endophytes: Endophytic fungi were isolated according
the protocols described by Petrini (1986) which were
slightly modified based on preliminary tests. The health cocoa pods taken from
the field were washed twice in distilled water then surface sterilized by immersion
for 1 min in 70% (v/v) ethanol, 5 min in sodium hypochlorite (2.5 % (v/v) available
chlorine) and 30 seconds in 70% (v/v) ethanol and then washed three times in
sterilized distilled water for 1 min each time. After surface sterilization,
the samples were cut into 5-7 mm pieces and aseptically transferred to plates
containing Potato Dextrose Agar (PDA, pH 6.8, containing (g L-1):
potato 200; dextrose 20; agar 15.) which had been autoclaved for 15 min at 121°C
and then aseptically supplemented with 100 mg mL-1 of chloramphenicol
(Pfizer) to suppress bacterial growth. Aliquots from the third wash were plated
onto PDA to check that surface sterilization had been effective and they were
then incubated at 28°C. Any fungi present was isolated, purified and then
maintained at 4°C on PDA slopes for further identification. After 5 days
of incubation the grown fungi were identified with reference to Barnett
and Hunter (1998) and Dugan (2006).
Production of fungal endophyte in powder form: Such fungal endophyte
isolated as described previously propagated in rice medium containing chitin
(1.0 g). The rice medium that has been soaked for 3 h put into a flask 100 g
and autoclaved at 121°C for 30 min and after which by using a corkborer
(diameter 0.5 mm), five pieces of endophytic fungi were inoculated in once the
fungi started growing, the flask were shaken to assure an even fungal growth.
The grown fungi then incubated at 30°C for 48 h. The rice medium along with
the fungi then blended to produce a powder for further study.
Production of fungal endophyte in liquid form: The fungal grown obtained
propagated on Potato Dextrose Broth (PDB) containing 1 g chitin to 100 mL PDB
and autoclaved at 121°C for 30 min. By using a corkborer (diam. 0.5 mm),
five pieces of endophytic fungi were inoculated in the flask were shaken to
assure an even fungal growth. After 2 weeks the fungus in the flask filtered
with the use of Whatman paper No. 1 and the supernatant keep into the refrigerator
for use in further study.
The impacts of isolated fungal endophytes on the eggs of Cocoa Pod Borer
(CPB): The study was carried out to observe the impacts of fungal endophytes
application on the survival of CPB eggs. There were 6 fungal endophytes treatments
and with 3 replications were involved and 18 experimental units were then prepared
consequently. The experimental units consisted of a pod with naturally infested
eggs so 18 eggs infested pods were selected. The number of eggs on a pod samples
was recorded and then sprayed with 1x106 mL-1 suspension
of fungal conidia. The treatment was made every day for 3 days period. The eggs
were allowed to develop and after 1 week from the first application the eggs
were inspected and un hatch eggs then recorded. The percentage of un hatch eggs
were subsequently determined.
The study on the endophytisms of the fungal isolates: The study was
carried out to observe whether the fungal endophyte applied might be able to
penetrate into the treated pod. For each form (powder and liquid) of fungus,
18 pods consisted of 6 small, 6 moderate, 6 full size pods, respectively for
replication were selected from cocoa trees. The cocoa pods were sprayed with
a fungal endophyte with a conidial suspension of 1x mL-1. After two
weeks of application the treated pods were then harvested and fungal reisolation
then made with the same procedures as described in previous section.
RESULTS AND DISCUSSION
Isolation and identification of fungal endophyte isolates: The results
indicated that there were 5 genera of fungal endophytes isolated from healthy
pods of cocoa plants, i.e., Trichoderma sp., Fusarium sp.,
Aspergillus sp., Beauveria sp. and 1 (one) unidentified (mycelia
sterilia) (Fig. 1-5). In other study in
South Sulawesi in addition to Fusarium sp. and Aspergillus
sp., Curvularia sp., Geotrichum sp., Gliocladium sp.
and Colletotrichum sp., had been isolated from the health leaves of cocoa
plants which resistant to VSD disease (Amin et al.,
2014). A number of researches also reported the presence of endophytic fungi
in cocoa plants.
Hanada et al. (2010) isolated a number of genera
of fungal endophytes including Trichoderma, Fusarium from braches
and twigs tissues of cocoa trees in Brasil. They found that Trichoderma
and Fusarium showed a high level activity against Phytophthora palmivora,
the causal agent of the black pod rod disease of cocoa. The presence of Trichoderma
and Fusarium on the tissues of cocoa branches was also reported by
Rubini et al. (2005) and
Posada and Vega (2005) reported the establishment of entomopathogen Beauveria
bassiana as endophytes of cocoa plants if the fungus is inoculated in radicles
of seedlings. Three fungal endophyte isolated from healthy Theobroma cocoa
tissue and screened in vitro for antagonism against major pathogen of
cocoa (Mejia et al., 2008).
The impact of fungal endophytes on egg survival: The results indicated
that all fungal endophytes studied produced a negative effect on the egg survival
for both applied in powder and liquid form but a greater effects was recorded
in liquid one in which the means of egg mortality ranging from 63 to 96% if
the eggs treated with a liquid form compared to from 51 to 84% if treated with
a powder form, all the means of which are different significantly from that
of 10% produced by control (p = 0.05) (Table 1).
||Mean of egg mortality (%) treated with fungal endophytes in
a powder and liquid forms
|No. in the same column followed by same letters are not significantly
different, (p = 0.05, Tukeys test)
The means between fungal endophytes are not significantly different if they
applied in the powder forms but in the liquid form, Aspergillus seems
to produce the highest egg mortality (96%) is not significantly different from
that of produced by Beauveria and Trichoderma but significantly
different from that of produced by Fusarium and X isolate (p = 0.05)
(Table 1). In general, endophytic Trichoderma sp.,
Beaveria sp. and Aspergillus sp., seem to be an important mortality
factors for the cocoa pod borer egg which produced a relatively high mortality.
Endophytic Trichoderma sp., showed a similar effect if it were applied
in both powder and liquid forms with the mean of 84 and 89% egg mortality, respectively
while a greater high mortality for Beauveria sp. and Aspergillus
sp., application was only recorded in liquid forms with the mean of 94 and 96%,
respectively compared with only 51 and 64% if they applied in the powder form
The mode of action of how endophytic fungi might protect plants from such insect
herbivore attacks had been argued by many authors. Fungal endophytes grow systemically
in intercellular spaces of the above-ground plant tissues including seeds and
produce variety of alkaloids (Clay, 1998; Bultman
et al., 2003) or fungal metabolites (Bush
et al., 1997; Clay and Schardl, 2002). The
production of alkaloid substances by endophytes-containing plants might protect
the associated plants from herbivores due to antibiosis or feeding deterrence
mechanisms (Crawford et al., 2010). An antibiosis
substance is a toxic which might kill such victim as insects or microbial pathogens
if they contact with or consume the substance. Examples of toxin production
by endophytic fungi, notably those colonizing grasses are considerably abundant
in the literature. Azevedo et al. (2000) reviewed
that the protection of Canadian fir that against the spruce budworms resulted
from the production of toxic secondary metabolites by endophytic fungi. In Prestidge
and Gallagher (1988) and Pocasangre et al. (2000)
reported a relationship between the presence of the fungus A. lolii in
Lolium perenne and the growth, survival and feeding behaviour of Listronotus
bonariensis larvae. In this case, the reduction in insect attacks towards
infected plants was due to a strong toxin, lolitrem B, also toxic to mammals.
This toxin, once added to insect diets, reduced insect growth and survival.
Its assimilation occurs by ingestion but not by absorption through the insect
Arnold and Lewis (2005) specifically discussed mode
of action of Beauveria bassiana that the fungus deposits spore on the
insect cuticle followed by formation of a germ tube and through enzymatic and
mechanical action it penetrates the cuticle. Once in the hemocoel, hyphal growth
causes tissue damage and nutrient depletion. Mode of action of isolates fungal
endophytes on the eggs as found in the study might work in similar way.
The involvement of the enzymes in fungal endophyte mode of action as argued
by Arnold and Lewis (2005) is supported by other authors.
The production of chitinases by such endophytic fungi as Streptomyces
sp., were reported by Haggag and Abdallh (2012) and
Tang-Um and Niamsup (2012) and a number of fungal endophytes
including Trichoderma sp., Beauveria sp., and Aspergillus
sp. was reported by Matsumoto (2006).
Protease is an enzyme which capable of breaking down proteins while chitinase
is an enzyme which capable of breaking down or digest chitins. The insect exoskeleton
(insect cuticles) and egg shells (chorions) is mainly made of chitin and protein
components and if the insects or eggs come contact with the such endophytic
fungal product substances as digestive enzymes, the exoskeletons or chorions
will degraded consequently and by a combination with an antibiosis substances
will accelerate the dead of the insect or egg victim. In the case of the eggs,
the chemical substances produced by fungus might also enter directly through
the mycrophile, an egg hole for entrance of sperms.
It is assumed that the more rapidly action might take place depend on the such
amount of the fungal substances produced in a time as performed by liquid form
of fungal isolates studied which greatly reduced the egg survival compared to
powder form except for Trichoderma sp., isolate. The enzyme production
depend on such conditions as pH of culture, age of inoculums, type of fermentation,
submerged or solid (Matsumoto, 2006). The enzymatic activities
of Lecanicillium fungicola remarkably increased in liquid culture when
pH varied from acid to alkali. The chitinolytic activity in filamentous as B.
bassiana, Trichoderma harzianum, Aspergilus fumigates, Lecanicillium
lecanii, Metarhizium anisopliae, Fusarium generally increases
with culture time of incubation (Matsumoto, 2006). On
the other side that synthesis of secondary metabolites by the plant have been
shown to play an important roles in the interaction between plants and arthropods
(Dicke et al., 2003; Turlings
and Wackers, 2004; Van Poecke and Dicke, 2004;
Arimura et al., 2005). Adults white ply evaluate
the tactile and chemical cues of the plant surface after landing to determine
the suitability of a plant as shelter or as a feeding and/or oviposition host
(Walling, 2000). Changes in the synthesis of these cues
stimulated by Fo162 also influence the behaviour of the insect on the Cucurbitacea
plants hosts. The resulting effect increased plant fitness in a hostile environment
as reported by Howe and Schaller (2008).
Reisolation of fungal isolates treated: The results indicated that after
2 weeks, Trchoderma sp. and Fusarium sp., were able to penetrate
in the treated cocoa pods if fungus treated in both powder and liquid form.
Aspergilus sp. and X isolates on the other hand the penetration only
occurred if the fungus treated in the powder form and Beauveria sp. was
not detected in the pod for period of two weeks (Table 2).
It seems that Beauveria sp. might need more time in order to penetrate
in the pod since Posada et al. (2010) reported
that Beauveria bassiana is an endophyte in cocoa pods after two or three
months inoculation on the flowers. The ability of the associated fungus to penetrate
in the pod proofed that they could grow in the inter celuler of the pod and
showed the ability of endophytism and the cocoa pods are conducive for the growth
of naturally and inoculated fungal isolates consequently.
Indeed the research findings might over a great hope that endophytic fungus
studied i.e., Aspergillus sp., Beauveria sp. and Trichoderma
sp., seem to be potential for biological control agents of cocoa pod borer,
a destructive cocoa pest in the worldwide. If the fungus suspensions sprayed
on the cocoa pods, more than 90% the pod borer eggs might not be able to hatch
and the young larvae emerging from the remaining unhatch eggs will bore and
penetrate inside the pods and they will be then attacked or completely eliminated
by the endophytic fungus applied earlier. Thus to obtain the best result from
endophytic fungus application, the fungus should be sprayed as early as possible
or when the cocoa trees produce a small pods (less than one month old) to enable
the fungus colonized inside the pods.
||Reisolation of fungal endophyte isolate (%) in a powder and
When the pods gain a size of 9-10 cm in length (generally 3-4 months old),
a suitable size for egg oviposition by cocoa pod borer, an intensive spray will
be made but this is needed to be investigated.
It can be concluded that, Beauveria sp., Trichoderma sp. and
Aspergillus sp. are endophytic fungus which provide potential as biological
control agent for cocoa pod borer.
We would like to thank the Minister of the National Education and Culture,
Republic of Indonesia for the financial support provided for the study, under
the Contract of National Research Priority in Masterplan of acseleration and
Extention of Indonesian Economic Development 2011-2025. We also expand our thank
to the head of Hasanuddin University Research Institute for his valuable advice
during the study.
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