Temperature mediated influence of mycotoxigenic fungi on the life cycle attributes of Callosobruchus maculatus F. in stored chickpea

doi:10.21203/rs.3.rs-1532248/v1

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Temperature mediated influence of mycotoxigenic fungi on the life cycle attributes of Callosobruchus maculatus F. in stored chickpea

https://doi.org/10.21203/rs.3.rs-1532248/v1

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Environmental factors (biotic and abiotic) are a major source of grain reserve depletion. Fungi and insect pests both damage grains synergistically in the store. Fungal and insect pest infestations pose nutritional damage to the stored food which becomes unpalatable for the consumer. There is a need to develop a timeline for synergistic damage caused by insect pest and mycotoxigenic fungi to manage them in stored products. For this purpose, interaction of mycotoxigenic fungi (Aspergillus flavus, Aspergillus niger, Penicillium digitatum and Alternaria alternata) along with C. maculatus (Fabricius) (Bruchidae: Coleoptera) was studied at wide range of temperature. Development of C. maculatus was observed on fungus inoculated and non-inoculated C. arietinum seeds under different temperatures. C. maculatus was found attracted for completion of its life cycle attributes (Fecundity, larval emergence, pupae and adults) in fungus inoculated grains. Population of C. maculatus was decreased by increase in temperature but high temperatures pose to more fungi developments. Meanwhile, more egg laying was observed at 27 ºC and 33 ºC. At tested temperatures, larval emergence was high as compared other checked life attributes. Infestation of A. flavus and A. niger was also increased with different life stages of C. maculatus at all checked temperatures. Penicillium digitatum and Alternaria alternata infestation were increased in the C. arietinum at 27 ºC and 30 ºC respectively. This study will help in measuring the control practices of fungi and insect pest infestations in stored chick pea in Pakistan.

Insect microbial interaction

C. maculatus

Growth parameters

Ecophysiological factors

Pakistan is fourth in chickpea (Cicer arietinum Linnaeus) production. It has high carbohydrate contents (62.34%) (El-adawy, 2002) and protein levels (23.67%) (Alajaji and El-Adawy, 2006; FAO, 2018). Pakistan faces considerable losses (15–55%) in chickpea crops during storage (Vanzetti et al., 2017). Contamination of stored commodities is mostly reported with microflora and insect infestations (Bhat, 1988; Delouche, 1980; Mills, 1986; Tuda, 1996). Mycotoxins are non-volatile secondary metabolites, produced by filamentous fungi which reduce the quality of stored food by damaging their physical appearance and chemical composition (Bräse et al., 2009). Mycotoxins mediated semiochemicals are considered as an indicator of rotten odor in grains and simulate interaction among insects and fungus species (Bennett and Inamdar, 2015; Bennett et al., 2012)

In stored commodities, the species of genus Aspergillus and Penicillium more proliferate due to high relative humidity and mycotoxins (Dawar et al., 2007; Kumar et al., 2009; Patil et al., 2012; Shukla et al., 2012). Aspergillus flavus contributed 64% of more aflatoxin production in C. arietinum seeds as compared to quality-added products of chickpea (Ramirez et al., 2018). There have been deleterious consequences of chick pea consumption contaminated with toxigenic fungi on human health and animals (Urooj et al., 2015).

The granivorous Callosobruchus maculatus F. (cowpea weevil)(Coleoptera: Chrysomelidae: Bruchidae) is the considerable causative agent of severe losses in seed germination, weight and nutritional level of legumes (Généfol et al., 2018; Staneva, 1982; Valencia et al., 1986). The C. maculatus can destroy dry beans in tropical and arid climatic zones, especially in stores (Tuda et al., 2006). Beetles can develop in the availability of reduced water and food quantity in storage ecosystems (Dongre et al., 1996). The penetration of storage fungi in stored commodities occurs due to the mishandling after harvest, presence of dust residues, cracks in seed coat because of mechanical handling and insects (Woloshuk and Martínez, 2012).

Temperature is also a fundamental aspect related to insect physiology (Ratte, 1984) and biochemistry (Downer and Kallapur, 1981). The various ranges of temperature affect the survival of Bruchidae species and insect activities (Giga and Smith, 1987; Miyatake et al., 2008; Soares et al., 2015). Development of bruchid beetles is highly responsive to ranges of temperature which are also responsible for fungal communities development in post-harvest practices (Kistler, 1995; Sautour et al., 2001; Umoetok Akpassam et al., 2017). The well-studied temperature variables for all pathogenic microbes are 15–37°C. The optimum temperature for growth of A. flavus is 37°C, while Penicillium species are also developed at lower temperatures i.e., from room temperature to 0°C (Asurmendi et al., 2015; Lahouar et al., 2016; Palou, 2014).

Current study is designed to interpret the relationship between fungi species (Penicillium digitatum, Aspergillus flavus, Aspergillus niger, Alternaria alternata) and population builup of C. maculatus in stored grains at different temperature ranges(25°C, 27°C, 33°C and 35°C) at constant humidity (70%). Current findings will be helpful in developing some IPM strategy for C. maculatus and fungal infestation in stored products

2.1. Insect culture

C. maculatus was cultured on presanitized chickpea grains under constant environmental conditions (25 ± 5°C and 55 ± 5% R.H.) to obtain a uniform population. Males and females were separated by using protocols of (Beck and Blumer, 2011).

2.2. Collection of chickpea

For experiment, we collected stored chickpea (kabuli variety) (not freshly harvested) from the retailors of four different selected locations (Fig. 1): Dg Khan, Lodhran, Muzaffargarh, and Multan kept at 25 ± 5°C and 55 ± 5% R.H. in Ecotoxicology Laboratory, Department of Entomology, Bahauddin Zakariya University (BZU) Multan, Pakistan (+ 30° 11' 52"N, + 71° 28' 11" E). All the samples were stored in autoclaved glass jars (round cylinderrical with dimensions of 32 x 23 x 23 cm) covered with aluminum foil and transferred directly to the mycological laboratory for fungus infestation via PDA (Potato Dextrose Agar)

2.3. Isolation of mycotoxigenic fungi

Isolation of fungi from C. maculatus and C. arietinum was performed in fungi research laboratory, Department of Plant Pathology, Bahauddin Zakariya University, Multan, Pakistan. Seven C. maculatus were made sterile with 2% solution of sodium hypochlorite, washed twice with distilled water, dried on blotter paper, crushed and placed on PDA (Potato Dextrose Agar) plate.The PDA plates were prepared by Potato 125 g, Dextrose 10 g and Agar 7.5 g in 500 ml distilled water. Five healthy-appearing grains of C. arietinum were collected from the stock. Grains were disinfected with 2% sodium hypochlorite, washed with distilled water twice, dried on blotting paper and placed on PDA plates for fungal growth observation (Bosly and Kawanna, 2014; Taylor and Sinha, 2009). All the isolation procedures were done in a horizontal laminar flow cabinet (Airstream® (LHG) (Lamboni and Hell, 2009). The isolation procedure for both insects and grains were replicated 10 times.

2.4. Identification of mycotoxigenic fungi

Identification of different fungi spp. performed at Plant Pathology Department of Bahuddin Zakariya University (BZU) Multan, Pakistan. Mycological evaluation through microscopic examination was done by staining the hyphae with methylene blue on glass slides from fresh fungi cultures (Morishita and Sei, 2006).

2.5. Purification of mycotoxigenic fungi

Purification was done to remove contamination of other microbes from fungi cultures. Stainless steel needles were used for the purification of fungi culture. Sterilized the needle on the spirit lamp and then needles were used to separate the piece of PDA containing required fungal species. Placed fungal spores on PDA plate in an incubator at 25°C and observed daily to check the culture purification (Ko et al., 2001).

2.6. Percentage of fungus

The rate of occurrence of specific fungus species in an isolated culture of insect and grains was determined by the following formula (Eq. 1) (Ahmad and Singh, 1991):

\(\text{F}\text{r}\text{e}\text{q}\text{u}\text{e}\text{n}\text{c}\text{y} \text{o}\text{f} \text{F}\text{u}\text{n}\text{g}\text{u}\text{s} \left(\text{\%}\right)=\) \(\frac{\text{T}\text{o}\text{t}\text{a}\text{l} \text{n}\text{o}. \text{o}\text{f} \text{s}\text{e}\text{e}\text{d}\text{s} \text{c}\text{o}\text{n}\text{t}\text{a}\text{i}\text{n}\text{i}\text{n}\text{g} \text{p}\text{a}\text{r}\text{t}\text{i}\text{c}\text{u}\text{l}\text{a}\text{r} \text{f}\text{u}\text{n}\text{g}\text{u}\text{s}}{\text{T}\text{o}\text{t}\text{a}\text{l} \text{n}\text{o}. \text{o}\text{f} \text{s}\text{e}\text{e}\text{d}\text{s} \text{u}\text{s}\text{e}\text{d}}\) X 100

2.7. Spore suspension

Fungi (A. flavus, A. niger, P. digitatum and A. alternata) isolated from C. arietinum and C. maculatus were used for spore suspension. The suspensions were prepared from 7 days of fresh cultures of fungus. Fungal spoers of mycotoxigenic fungi species were scraped with the help of glass slide by adding 20 ml autoclaved distilled water, and then solution was stirred in magnetic stirrer until conidia become separated from PDA. After agitation impurities of suspension were removed by filtering it through filter paper. The numbers of spores were counted under a light microscope through haemocytometer.

2.8. Inoculation of C. arietinum grains

Spore suspension was diluted to obtain 5 X 10³ spores/ml to inoculate C. arietinum. Autoclaved chickpea grains were inoculated with four different fungi by adding 3 ml of spore suspension per 100 g grains in glass jar (h = 5″,W = 3.2″) (Nesci and Montemarani, 2011).

2.9. Influence of temperature on growth of C. maculatus and mycotxigenic fungi

The normal prevailing temperature ranges (27, 30, 33 and 35°C) were tested for the growth of C. maculatus and mycotoxigenic fungi simultaneously, at 70% R.H. (Gillooly et al., 2002). All the selected temperatures and humidity were maintained in Laboratory climate chamber (MLR-352-PE).

2.10. Extent of fungi on life cycle of C. maculatus

Five pairs of surface-sterilized (2% sodium hypochlorite) adults were introduced into glass jar (Height = 5″,width = 3.2″) each containing 100 g inoculated C. arietinum in Ecotoxicology Laboratory, Department of Entomology, Bahauddin Zakariya University, Multan and removed after 24 hours (Tsai et al., 2007). All the experimental units were maintained in a growth chamber with four constant temperatures 27°C, 30°C, 33°C & 35°C and R.H. 70%. Cicer arietinum were checked for numbers of C. maculatus eggs, larvae, pupae and adults by dissecting grains along with growth of fungal species (Howe and Currie, 1964). Each treatment was replicated 4 times.

2.11. Statistical analysis

Incidence (%) of fungal species in C. maculatus adults and chickpea grains were analyzed via frequency equation. While, Chi square test and Two-Way ANOVA of the fungal isolation frequency were performed by subjecting data to a computational basaed software SPSS (SPSS VERSION 7.0). Variables (temperature, humidity and number of days) were compared through Duncans Multiple Range Test (DMRT) at 95%. Developmental activity of C. maculatus (dependent variable) correlated with constant humidity (70%), selected temperatures and fungal species (considered as independent variables) was calculated through software (SAS Institute, 2000).

3.1. Isolation of mycotoxigenic Fungi

3.1.1. From C. arietinum grains

C. arietinum grains were analyzed for fungal colonies, Aspergillus, Fusarium, Penicillium and Alternaria were prominent as seed spoilers. A. flavus, A. niger, A. alternata, P. digitatum and F. oxysporum were examined as dominant species from all localities sampled. C. arietinum was found to be highly infested with A. flavus (52.3) while A. alternata had the lowest frequency of colonies (8) among the four tested fungal species. Colonies of A. niger, P. digitatum and F. oxysporum, were found statistically similar, while A. flavus and A. alternata had a significant difference (F = 32.009; df = 4(20); P < 0.001) between fungal colony frequencies (Table 1).

Table 1

Mycotoxigenic fungi isolated from *C. arietinum* samples purchased from different locations of Punjab Pakistan.
Species	Multan (n = 75)	Muzaffargarh (n = 75)	Lodhran (n = 75)	DG khan (n = 75)	Total Isolates (n = 300)	Isolation Frequency SE(±)
A. flavus	72	28	27	30	157	52.3 ± 14.58a
A. niger	33	15	21	13	82	27.3 ± 6.00b
A.alternata	10	3	7	4	24	8 ± 2.11b
F. oxysporum	30	8	7	19	64	21.33 ± 7.20b
P. digitatum	30	11	11	14	66	22 ± 6.07b
Means within a column followed by the same letter are not significantly different from each other (SPSS software at 0.05).

3.1.2. From C. maculatus

Fungal growth observation from the body of C. maculatus revealed that A. flavus was found frequently (71.43) while A. alternata was the minimal fungal isolate from both adult stages was 4.64 (Table 2). Diversities of fungus are present on the body of C. maculatus but there is no association between gender of insect and types of fungus they are independent ( X² = 6.339^a; df = 4 ; P > 0.175)

Table 2

Isolation of fungi from both male and female adults of *C. maculatus.*
Species	No. of isolates			Isolation Frequency
	Female (n = 140)	Male (n = 140)	Total isolates (n = 280)	Isolation Frequency
A. flavus	98	102	200	71.43
A. niger	20	24	44	15.71
A. alternata	3	10	13	4.64
F. oxysporum	24	37	61	21.79
P. digitatum	32	26	58	20.7
(Chi square test at 0.05)

3.2. Identification of mycotoxigenic fungi

Fungal species isolated from C. arietinum and C. maculatus were identified at Plant Pathology Department of Bahuddin Zakariya University (BZU) Multan.

3.4. Interaction among mycotoxigenic fungi and C. maculatus in C. arietinum grains at different temperatures

3.4.1. Developmental period of C. maculatus

C. maculatus were tested for their life cycle attributes (egg,larvae, pupae and adult stages) on inoculated C. arietinum grains at four different temperatures (27 ºC, 30 ºC, 33 ºC, 35 ºC). C. maculatus population was significantly developed at all tested temperatures (F = 81.85; df = 3(60); P < 0.0001). As the temperature increased C. maculatus life period was shortened and at 35 ºC, the insect showed shortest life period. Meanwhile, intensification in temperature also increased the progress of A. flavus and A. niger in grains. The life period of C. maculatus was elapsed to 33 days (highest recorded days) at 30°C. Impact of Fungal growth was found non-significant with the life cycle attributes of C. maculatus (F = 1.03; df = 4(60); P = 0.4006) and all tested temperatures (F = 1.51; df = 12(60); P = 0.146) (Fig. 2).

3.4.2. Fecundity of C. maculatus

Oviposition rates of C. maculatus were significantly affected by all tested temperatures (F = 564.37; df = 3(60); P < 0.0001). The females of C. maculatus preferred inoculated C. arietinum more than sterilized C. arietinum grains for oviposition at all temperatures. At 27°C and 33°C, oviposition was 403.75 on C. arietinum grains inoculated with A. flavus and A. niger. Reduction in the oviposition occurs at 35°C in inoculated and control C. arietinum. P. digitatum inoculated grains exhibited a few oviposition (33.25). Oviposition rate was highly significant with relation to fungal inoculation (F = 192.23; df = 4(60); P < 0.0001) and temperature (F = 83.05; df = 12(60); P < 0.0001) (Fig. 3).

3.4.3. Incubation period

Incubation period of C. maculatus were not significantly (F = 0.40; df = 4(60); P = 0.80) influenced by interaction of fungi and temperature (F = 0.66; df = 12(60); P = 0.78). Highest incubation period was of 8.25 days at 27°C and also same number of days were observed in presence of all tested fungal species on C. arietinum. Temperature ranges exhibited highly significant (F = 35.93; df = 3(60); P < 0.0001) effect on the incubation period of C. maculatus. Increase in temperature was also decreased the incubation period of C. maculatus as observed in P. digitatum infested C. arietinum grains was shows shortest incubation period (3.5 days) at 35°C (Fig. 4).

3.4.4. Larval emergence of C. maculatus

Larvae of C. maculatus were highly influenced due to temperatures (F = 98.15; df = 3(60); P < 0.0001) and mycotoxigenic fungi (F = 104.49; df = 4(60); P < 0.0001) infestation in C. arietinum. Larvae emergence was lower than oviposition of C. maculatus in inoculated C. arietinum. Fungal prevalence in grains at different temperatures was decreased the larvae emergence. Moreover, opposite results for larvae emergence were observed in instances of non-inoculated (323 at 27°C) and A. niger inoculated (275.5 at 33°C) C. arietinum. The successive highest rate of larvae emergence was evaluated in C. arietinum infested with A. niger. Numbers of larvae emergence was also significantly affected because of interaction among fungi and temperatures (F = 19.38; df = 12(60); P < 0.0001). The results also indicated the lowest number of larvae emergence in P. digitatum infested C. arietinum at 35°C was 33.25 (Fig. 5).

3.4.5. Pupation of C. maculatus

The mycotoxigenic fungi (F = 153.97; df = 4(60); P < 0.0001), temperatures (F = 158.96; df = 3(60); P < 0.0001) and their interaction (F = 38.90; df = 12(60); P < 0.0001) exhibited highly significant effects towards pupation rate of C. maculatus. However, C. arietinum infested with P. digitatum and A. alternata shows the lowest pupation rate was 28.5 and 38 at 35°C. High numbers of pupae emerged at 27°C in inoculated and un-inoculated C. arietinum as compared to other temperatures and control (Fig. 6).

3.4.6. Adult emergence

Adult emergence of C. maculatus were inversely correlated with fluctuating temperatures (F = 202.02; df = 3(60); P < 0.0001), mycotoxigenic fungi (F = 97.95; df = 4(60); P < 0.0001) (F = 18.30; df = 4(60); P < 0.0001) and their interactions (F = 17.37; df = 12(60); P < 0.0001). Results demonstrated that, at 27°C maximum adults were emerged in inoculated and non-inoculated C. arietinum. However, the lowest adult emergence rate at 35°C in P. digitatum inoculated C. arietinum was 23 (Fig. 7).

Six-month storage of C. arietinum grains in different storage conditions face deterioration (26%) and weight loss (55.67%) because of C. maculatus infestation (Babu et al., 2020). C. arietinum with thin seed coat, large seed size, high carbohydrates and phenols were more susceptible to C. maculatus infestation (Swamy et al., 2020). Adults of C. maculatus enclosed mycotoxigenic fungi (Aspergillus, Penicillium, Fusarium and Alternaria) species inside the body, as previously suggested by (Kumari et al., 2011) in case of red flour beetle. In this study we observed that the proliferation of mycotoxigenic fungi in C. arietinum also increased due to C. maculatus infestation within storage ecosystem. The presence of both C. maculatus and mycotoxigenic fungi species significantly takes part in the deterioration of stored commodities (Allotey et al., 2010). Results revealed high frequencies of A. flavus and A. niger isolates from C. maculatus adults. On the other hand, similar results reported that infestation of mycotoxigenic fungi in Triticum aestivum observed beacuase of T. castaneum and Sitophilus granarius activities (Agrawal et al., 1957; Bosly and Kawanna, 2014). The presence of mycotoxigenic fungi in an insect’s body illustrates that insects were able to transfer fungal flora in grains. Red flour beetle had been associated with dissemination of mycotoxigenic fungi to their hosts (Bosly and Kawanna, 2014) and also observed in stored rice grains (Yun et al., 2018). C. maculatus larvae, pupae and adults were significantly affected by the infestation of mycotoxigenic fungi.

Insect pests have intrinsic ability to develop and reproduce to change in temperature and time progressively (Burges, 2008). Temperature is inversely interacting with growth rate of insects. Resuts explain that C. maculatus completed its life cycle on all tested fungus and temperature parameters. The progressive period of C. maculatus was shorter on all infested and non-infested C. arietinum at 35°C and 70% R.H. Shortest life period of Cadra cautella were demonstrated at 30°C and 70% R.H. (Burges and Haskins, 1965). Ahasverus advena also complete their life cycle on different concentrations of Aflatoxin B₁ infested grains and the shortest life cycle was observed at 30°C (Jacob, 1996; Zhao et al., 2018). Emergence of larvae was high at 27°C on sterilized C. arietinum as well as on C. arietinum infested with A. niger at 33°C. Similar results were observed in development of Trogoderma granarium on broken wheat grains at 35°C while maximum fecundity and larvae emergence was evaluated at 30°C (Riaz et al., 2014). The infestation of mycotoxigenic fungi was able to influence the development period of C. maculatus in stored grains under selected temperature ranges.

Longest development period of C. maculatus was analyzed 33 days at 30°C and more than 25 days at 27°C on inoculated and non-inoculated C. arietinum. C. maculatus showed an incubation period of more than 6 days at 30°C on all tested parameters. This is higher than other pests including Chilo partellus was showed shortest incubation period (4 days) at 30°C but a similar development period of more than 30 days was observed at 30°C at 80% R.H. (Tamiru et al., 2012). Maximum progress rate of A. flavus was noticed at 35°C (Mannaa and Kim, 2018). A. alternata shows maximum growth rate at 25°C on Glycine max (Oviedo et al., 2011). Meanwhile germination of Penicillium spp. was observed at 30°C at 75% humidity (Pasanen et al., 1991). Fusarium spp. was not showed any germination at temperature up to 25°C on G. max medium (Garcia et al., 2012) that’s why we do not select this species as the medium for C. maculatus growth on these temperature ranges.

Temperature influenced the fecundity of C. maculatus more than humidity. Temperature and suitable host preferences are the most considerable factors related to the development and oviposition of C. maculatus (Giga and Smith, 1987; Mam and Mohamed, 2015). The results presented maximum oviposition and larvae rate of C. maculatus on A. flavus inoculated C. arietinum at 27°C as well as on A. niger at 33°C. High numbers of larvae, pupae and adults were observed on sterilized C. arietinum. C. maculatus preferred A. flavus and A. niger infested C. arietinum more than control for oviposition. This is in contrast to; Corns infested with A. halophilicus were more suitable for the oviposition of P. interpunctella while a high development rate was observed at autoclaved corn (Abdel-Rahman H. A., 1969). T. stercorea showed minimum oviposition and maximum numbers of larvae on A. flavus at 30°C. Average oviposition rate of C. maculatus on the P. digitatum (33–209) was highest as compared to T. stercorea was lowest on P. purpurogenum (42). Minimum larvae emergence was observed in T. stercorea on P. purpurogenum (Jacob, 1988; Tsai et al., 2007) as the same results were also observed for C. maculatus on P. digitatum C. arietinum.

C. maculatus preferred to oviposit at 30°C and 35°C while maximum oviposition was observed at 30°C on sterilized C. arietinum (Chandrantha et al., 1987; Lale and Vidal, 2003). Researchers also found that A. advena and Cryptolestes ferrugineus were not able to oviposit on the A. flavus and A. niger isolates as observed in case of C. maculatus (David, 1974; Loschiavo and Sinha, 1966).

More than 70% of C. arietinum deteriorates because of mycotoxigenic fungi and C. maculatus in houses, markets and stores. All the identified fungi species are well known to produce mycotoxins and reduction in the nutritional value of C. arietinum. A reduced amount of fungal growth on non-infested autoclaved chickpea grains (control) was observed at all selected temperatures even in presence of weevil. Preventive measures for both pests should be applied at commercial levels on the tested temperatures ranges in stores, houses and markets.

C. maculatus was able to reproduce in both inoculated and non-inoculated grains on all selected temperatures.

Market stored chickpea grains were found with more than 50% frequency of mycotoxigenic fungi while this percentage increased to 70% when insects come in contact with the grains in storages

C. maculatus carr fungus in body and the relationship between both developed early at 35°C causing high quality damage of C. arietinum.

Acknowledgments

The research was supported by Bahhaudin Zakariya University Pakistan (Multan), Faculty of agriculture sciences and technology and funded by the Department of Entomology.

Competing interest

Authors declare no competing interest.

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No competing interests reported.

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Temperature mediated influence of mycotoxigenic fungi on the life cycle attributes of Callosobruchus maculatus F. in stored chickpea

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Abstract

Figures

1. Introduction

2. Materials And Methods

2.1. Insect culture

2.2. Collection of chickpea

2.3. Isolation of mycotoxigenic fungi

2.4. Identification of mycotoxigenic fungi

2.5. Purification of mycotoxigenic fungi

2.6. Percentage of fungus

2.7. Spore suspension

2.8. Inoculation of C. arietinum grains

2.9. Influence of temperature on growth of C. maculatus and mycotxigenic fungi

2.10. Extent of fungi on life cycle of C. maculatus

2.11. Statistical analysis

3. Results

3.1. Isolation of mycotoxigenic Fungi

3.1.1. From C. arietinum grains

3.1.2. From C. maculatus

3.2. Identification of mycotoxigenic fungi

3.4. Interaction among mycotoxigenic fungi and C. maculatus in C. arietinum grains at different temperatures

3.4.1. Developmental period of C. maculatus

3.4.2. Fecundity of C. maculatus

3.4.3. Incubation period

3.4.4. Larval emergence of C. maculatus

3.4.5. Pupation of C. maculatus

3.4.6. Adult emergence

4. Discussion

5. Conclusion

Declarations

References

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