Survival of mushrooms and termites upon pesticide exposure in the cocoa agro-ecosystem:  Post pesticide survival of mushrooms and termites in cocoa

Eric Asare Kumi; Silas Wintuma Avicor; Yahaya Bukari; Ishmael Amoako-Attah; Solomon Agyare; Mabel  Yeboah; Michael Wiafe-Kwagyan

doi:10.11594/jtls.13.01.01

Authors

Eric Asare Kumi Cocoa Research Institute of Ghana, Entomology Division
Silas Wintuma Avicor Cocoa Research Institute of Ghana, Entomology Division
Yahaya Bukari Cocoa Research Institute of Ghana, Plant Pathology Division
Ishmael Amoako-Attah Cocoa Research Institute of Ghana, Plant Pathology Division
Solomon Agyare Cocoa Research Institute of Ghana, Plant Pathology Division
Mabel Yeboah Cocoa Research Institute of Ghana, Plant Pathology Division
Michael Wiafe-Kwagyan University of Ghana Legon

DOI:

https://doi.org/10.11594/jtls.13.01.01

Keywords:

Agro-economy, Cocoa, Fungicides, Insecticides, Mushrooms, Termites

Abstract

Pesticides have become integral parts of cocoa cultivation for the management of insect pests and fungal pathogens which cause significant damage to the crop. However, continuous pesticides usage in the cocoa agro-ecosystem is of concern due to perceived adverse effects on non-target organisms. In this study, mushrooms and associated termites were used to elucidate the possible effect of insecticides and fungicides on non-target organisms in the cocoa agro-ecosystem. Vegetative phase of Pleurotus sajor-caju (Oyster mushroom), Volvariella volvacea (Paddy straw mushroom), Termitomyces globulus and Termitomyces robustus (Termite mushrooms) were subjected to concentrations of commercially formulated fungicides (metalaxyl 12 % + copper (I) oxide 60 % and cupric hydroxide 77 %) and insecticides (imidacloprid 20 % and bifenthrin 2.7 %) to observe their growth rates on Potato Dextrose Agar (PDA) medium. Worker termites, Macrotermes bellicosus, were also exposed to the pesticides in Petri dishes for 24 h to observe their mortality. The manufacturer’s recommended concentration of 245 ppm for bifenthrin completely inhibited mycelial growth of all the mushrooms and caused 100% mortality of termites. At 0.0245 ppm, the insecticide caused 60% mortality of termites, but it had no inhibitory effect on the mushrooms. Except P. sajor-caju, mycelial growth of all the other mushrooms were completely inhibited by metalaxyl + copper (I) oxide at the manufacturer’s recommended concentration of 2400 ppm. However, mycelial growth rate of the mushrooms at 0.24 ppm of the fungicide was similar to the control plates. This suggests that mushrooms could survive in the cocoa agro-ecosystem amidst pesticides at lower concentrations in cocoa soils.

References

Kumar K (2015) Role of edible mushroom as functional foods: A review. South Asian Journal of Food Technolo-gy and Environment 1(3&4): 211 – 218. doi:10.46370/sajfte.2015.v01i03and04.02.

Ache NT, Tonjock RK, Eneke ET B et al. (2019) Mush-room species richness, distribution and substrate speci-ficity in the Kilum-Ijim forest reserve of Cameroon. Jour-nal of Applied Biosciences 133: 13592 – 13617. doi:10.4314/jab.v133i1.11.

Marcot BG (2017) A review of the role of fungi in wood decay of forest ecosystems. U.S. Department of Agricul-ture, Forest Service, Pacific Northwest Research Station. Research Note PNW-RN-575. https://www.fs.fed.us/pnw/pubs/pnw_rn575.pdf. Ac-cessed date: 27th January, 2021.

Lakhanpal TN (2014) Mushroom biodiversity in India: Prospects and potential. Proceedings of the 8th Interna-tional Conference on Mushroom Biology and Mushroom Products (ICMBMP8). pp. 7 – 16. doi:10.2737/PNW-RN-575.

Pegler DN, Vanhaecke M (1994) Termitomyces of Southeast Asia. Kew Bulletin 49(4): 717 – 736. doi:10.2307/4118066.

Sangvichien E, Taylor-Hawksworth PA (2001) Termi-tomyces mushrooms: A tropical delicacy. Mycologist 15(1): 31 – 33. doi:10.1016/S0269-915X(01)80058-6.

Obodai M, Ferreira ICFR, Fernandes Â et al. (2014) Evaluation of the chemical and antioxidant properties of wild and cultivated mushrooms of Ghana. Molecules 19(12): 19532 – 19548. doi:10.3390/molecules191219532.

Koné NA, Soro B, Vanié-Léabo LPL et al. (2018) Diver-sity, phenology and distribution of Termitomyces species in Côte d’Ivoire. Mycology 9(4): 307 – 315. doi:10.1080/21501203.2018.1500498.

Seelan JSS, Yee CS, Fui FS et al. (2020) New species of Termitomyces (Lyophyllaceae, Basidiomycota) from Sa-bah (Northern Borneo), Malaysia. Mycobiology 48(2): 95 – 103. doi:10.1080/21501203.2018.1500498.

Aryal HP, Budathoki U (2016) Ethnomycology of Ter-mitomyces R. Heim in Nepal. Journal of Yeast and Fun-gal Research 7(4): 28 – 38. doi:10.5897/JYFR2015.0154.

Apetorgbor MM, Apetorgbor AK, Obodai M (2006) Indigenous knowledge and utilization of edible mush-rooms in parts of Southern Ghana. Ghana Journal of For-estry 19

& 20: 20 – 34. doi:10.4314/GJF.V19I1.36908.

Dandapat S, Kumar M, Ranjan R, Sinha MP (2019) Nu-tritional, hypoglycemic, and haematinic potentiality of ed-ible mushroom Pleurotus tuber-regium (Rumph. ex Fr.) Singer. Journal of Tropical Life Science 9(2): 195 – 207. doi:10.11594/jtls.09.02.08

Wisselink M, Aanen DK, van’t Padje A (2020) The lon-gevity of colonies of fungus-growing termites and the stability of the symbiosis. Insects 11: 527. doi:10.3390/insects11080527.

Ejomah AJ, Uyi OO, Ekaye SO (2020) Exposure of the African mound building termite, Macrotermes bellicosus, workers to commercially formulated 2,4-D and atrazine caused high mortality and impaired locomotor response. Plos One 15(3): e0230664. doi:10.1371/journal.pone.0230664.

Akpesse AAM, N’guessan GRY, Coulibaly T et al. (2019) Attacks and damage of termites (Insecta: Isoptera) in cocoa plantations (Theobroma cacao L.) of M’brimbo S. A. B Station (South Côte d’Ivoire). International Jour-nal of Advanced Research 7(1): 438 – 445. doi:10.21474/IJAR01/8347.

Sylvain TBC, Tenon C, Hortense BS (2019) Attacks of termites (Insecta: Isoptera) in cocoa farms (Theobroma cacao, L.) in Oumé (Côte d’Ivoire). International Journal of Current Research 11(9): 6899 – 6905. doi:10.24941/ijcr.36521.09.2019.

Asare R (2005) Cocoa agroforests in West Africa. A look at activities on preferred trees in the farming systems. Forest and landscape Denmark working papers No. 6, University of Copenhagen, Copenhagen.

Oke D, Odebiyi K (2007) Traditional cocoa-based agro-forestry and forest species conservation in Ondo State, Nigeria. Agriculture Ecosystems & Environment 122: 305 – 311. doi:10.1016/j.agee.2007.01.022.

Anglaaere CNL, Cobbina J, Sinclair FL, McDonald MA (2011) The effect of land use systems on tree diversity: farmer preference and species composition of cocoa-based agro-ecosystems in Ghana. Agroforestry Systems 81: 249 – 265. doi:10.1007/s10457-010-9366-z.

van Dijk H, Onguene NA, Kuyper TW (2003) Knowledge and utilization of edible mushrooms by local populations of the rain forest of South Cameroon. Ambio 32(1): 19 – 23. doi:10.1579/0044-7447-32.1.19.

Duguma B, Gockowski J, Bakala J (2001) Smallholder cacao (Theobroma cacao, Linn.) cultivation in agroforest-ry systems of west and central Africa: challenges and op-portunities. Agroforestry Systems 51: 177 – 188. doi:10.1023/A:1010747224249.

Leakey RRB, Tchoundjeu Z (2001) Diversification of tree crops: domestication of companion crops for poverty re-duction and environmental services. Experimental Agri-culture 37: 279 – 296. doi:10.1017/S0014479701003015.

Asare R (2006) A review on cocoa agroforestry as a means for biodiversity conservation. In: Paper presented at World Cocoa Foundation Partnership Conference, Brussels. 15.

Schroth G, Krauss U, Gasparotto L et al. (2000) Pests and diseases in agroforestry systems of the humid tropics. Agroforestry Systems 50: 199 – 241. doi:10.1023/A:1006468103914.

Flood J, Guest D, Holmes KA et al. (2004) Cocoa under attack. In: Flood J, Murphy R, eds. Cocoa Futures: A source book of some important issues facing the cocoa industry. Chinchina, Colombia: CABI-FEDERACAFE, USDA. 33 – 53.

N’Guessan FK, Coulibaly N (2000) Dynamique des populations de mirides et de quelques autres déprédateurs du cacaoyer dans la régionou est de la Côte d’lvoire (In French). Proceedings of the 13th International Cocoa Re-search Conference: 425 – 435. Cocoa Producers Alliance, Malaysia.

Sounigo O, Coulibaly N, Brun L et al. (2003) Evaluation of resistance of Theobroma cacao L. to mirids in Côte d’lvoire: results of comparative progeny trials. Crop Pro-tection 22: 615 – 621. doi:10.1016/S0261-2194(02)00244-2.

Babin R, Bisseleua H, Dibog L, Lumaret JC (2008) Rear-ing method and life table data for cocoa mirid bug Sahl-bergella singularis Haglund (Hemiptera: Miridae). Jour-nal of Applied Entomology 132: 366 – 374. doi:10.1111/j.1439-0418.2008.01273.x.

Adu-Acheampong R, Janice J, van Huis A et al. (2014) The cocoa mirid (Hemiptera: Miridae) problem: Evidence to support new recommendations on the timing of insecti-cide application on cocoa in Ghana. International Journal of Tropical Insect Science 34(1): 58 – 71. doi:10.1017/S1742758413000441.

Awudzi GK, Asamoah M, Owusu-Ansah F et al. (2016) Knowledge and perception of Ghanaian cocoa farmers on mirid control and their willingness to use forecasting sys-tems. International Journal of Tropical Insect Science 36: 22 – 31. doi:10.1017/S1742758415000247.

Adu-Acheampong R, Sarfo JE, Appiah EF et al. (2015) Strategy for insect pest control in cocoa. American Jour-nal of Experimental Agriculture 6(6): 416 – 423. doi:10.9734/AJEA/2015/12956.

Marelli JP, Guest DI, Bailey BA et al. (2019) Chocolate under threat from old and new cacao diseases. Phyto-pathology 109(8): 1331 – 1343. doi:10.1094/PHYTO-12-18-0477-RVW.

Antwi-Agyakwa AK, Osekre EA, Adu-Acheampong R, Ninsin KD (2015) Insecticide use practices in cocoa pro-duction in four regions in Ghana. West African Journal of Applied Ecology 23(1): 39 – 48.

Bateman R (2015) Pesticide use in cocoa: A guide for training administrative and research staff (3rd ed.). Inter-national Cocoa Organization (ICCO), London-UK. https://www.icco.org. Accessed date: 12th February 2019.

Valavanidis A (2018) Neonicotinoid insecticides. Banned by the European Union in 2018 after scientific studies concluded that harm honey bees. Scientific Reviews 37. https://www.chem-tox-ecotox.org/ScientificReviews. Ac-cessed date: 24th September, 2021.

Opoku IY, Appiah AA, Akrofi AY, Owusu GK (2000) Phytophthora megakarya: A potential threat to the cocoa industry in Ghana. Ghana Journal of Agricultural Science 33: 237 – 248. doi:10.4314/gjas.v33i2.1876.

Akrofi AY (2015) Phytophthora megakarya: a review on its status as a pathogen on cacao in West Africa. African Crop Science Journal 23(1): 67 – 87.

Pimentel D (1995) Amounts of pesticides reaching target pests: Environmental impacts and ethics. Journal of Agri-cultural and Environmental Ethics 8: 17 – 29. doi:10.1007/BF02286399.

Carriger JF, Rand GM, Gardinali PR et al. (2006) Pesti-cides of potential ecological concern in sediment from South Florida canals: An ecological risk prioritization for aquatic arthropods. Soil and Sediment Contamination 15: 21 – 45. doi:10.1080/15320380500363095.

Gill HK, Garg H (2014) Pesticide: Environmental impacts and management strategies. In: Solenski S, Larramenday ML, eds. Pesticides – Toxic effects. Intech Rijeka. 187 – 230. doi:10.5772/57399.

Norgrove L (2007) Effects of different copper fungicide application rates upon earthworm activity and impacts on cocoa yield over four years. European Journal of Soil Bi-ology 43: 303 – 310. doi:10.1016/j.ejsobi.2007.08.031.

Aminu FO, Edun TA (2019) Environmental effect of pesticide use by cocoa farmers in Nigeria. Journal of Re-search in Forestry, Wildlife & Environment 11(4): 153 – 163.

De Waard MA, Georgopoulos SG, Hollomon DW et al. (1993) Chemical control of plant diseases: problems and prospects. Annual Review of Phytopathology 31: 403 – 421. doi:10.1146/annurev.py.31.090193.002155.

Kwodaga JK, Odamtten GT, Owusu E, Akrofi AY, Wiafe-Kwagyan M (2017a) Effect of four copper-based fungicides on soil fungi in a cocoa farm at Tafo, Eastern Region, Ghana. Scientia Agriculturae 17(2): 55 – 76. doi:10.15192/PSCP.SA.2017.17.2.5576.

Addo-Forjour P, Gyamfi HG, Fei-Baffoe B, Akrofi AY (2013) Impact of copper-based fungicide application on copper contamination of cocoa plants and soils in the Ahafo Ano North District, Ashanti Region, Ghana. Ecol-ogy, Environment & Conservation 19(2): 303 – 310.

Tibuhwa DD, Kivaisi AK, Magingo FSS (2010) Utility of the macro-& micro - morphological characteristics used in classifying the species of Termitomyces. Tanzania Journal of Science 36: 31 – 45.

Yadav MK, Chandra R, Yadav SK, Dhakad PK, Sushree-ta NU (2017) Morphological characterization, identifica-tion and edibility test of edible mushrooms from Vindhya Forest of Northern India. Environment & Life Sciences 10(3): 246 – 248.

Tudses N (2016) Isolation and mycelial growth of mush-rooms on different yam-based culture media. Journal of Applied Biology & Biotechnology 4 (5): 33 – 36. doi:10.7324/JABB.2016.40505.

Alhajj MS, Qasem MAA, Jar El Nabi AR, Al-Mufarrej SI (2019) In-vitro antibacterial and antifungal effects of high levels of Chinese Star Anise. Brazilian Journal of Poultry Science 21(1): 1- 8. doi:10.1590/1806-9061-2016-0427.

Ye L, Karunarathna SC, Li H, Xu J, Hyde KD, Mortimer PE (2019) A survey of Termitomyces (Lyophyllaceae, Agaricales), including a new species, from a subtropical forest in Xishuangbanna, China. Mycobiology 47(4): 391 – 400. doi:10.1080/12298093.2019.1682449.

Vesala R, Niskanen T, Liimatainen K et al. (2017) Diver-sity of fungus-growing termites (Macrotermes) and their fungal symbionts (Termitomyces) in the semiarid Tsavo Ecosystem, Kenya. Biotropica 0(0): 1 – 11. doi: 10.1111/btp.12422.

Ackonor JB (1997) Preliminary findings on termites (Isoptera) associated with cocoa and coffee farms in Gha-na. International Journal of Tropical Insect Science 17 (3-4): 401 – 405. doi: 10.1017/S1742758400019251.

Kortei NK, Odamtten GT, Obodai M, Wiafe-Kwagyan M, Prempeh J (2018) Survey of mushroom consumption and the possible use of gamma irradiation for sterilization of compost for its cultivation in Southern Ghana. Agricul-ture & Food Security 7: 83. doi:10.1186/s40066-018-0235-8.

Obodai M, Amoa-Awua W, Odamtten GT (2010) Physi-cal, chemical and fungal phenology associated with com-posting of ‘wawa’ sawdust (Triplochiton scleroxylon) used in the cultivation of oyster mushrooms in Ghana. In-ternational Food Research Journal 17: 229 – 237.

Delgado-Ospina J, Molina-Hernández JB, Chaves-López C, Romanazzi G, Paparella A (2021) The role of fungi in the cocoa production chain and the challenge of climate change. Journal of Fungi 7: 202. doi:10.3390/jof7030202.

Shim JO, Chang KC, Lee YS et al. (2006) The fruiting body formation of Armillaria mellea on oak sawdust me-dium covered with ground raw carrots. Mycobiology 34: 206 – 208. doi:10.4489/myco.2006.34.4.206.

Lisboa DO, Evans HC, Araújo JPM et al. (2020) Monili-ophthora perniciosa, the mushroom causing witches’ broom disease of cacao: Insights into its taxonomy, ecol-ogy and host range in Brazil. Fungal Biology 124: 983 – 1003. doi:10.1016/j.funbio.2020.09.001.

Amoako-Attah I, Ali SS, Aime MC et al. (2020) Identifi-cation and characterization of fungi causing thread blight diseases on cacao in Ghana. Plant Disease 104(11): 3033 – 3042. doi:10.1094/PDIS-03-20-0565-RE.

Amoako-Attah I, Akrofi AY, Bin Hakeem R, Asamoah M, Kumi-Asare E (2016) White thread blight disease caused by Marasmiellus scandens (Massee) Dennis & Reid on cocoa and its control in Ghana. African Journal of Agricultural Research 11(50): 5064 - 5070. doi:10.5897/AJAR2016.11681.

Sharma S, Dewangen NK (2014) In vitro effect of insec-ticides on edible mushroom Agaricus bisporus. Journal of Industrial Pollution Control 30(2): 335 – 337.

Das N (2005) Heavy metals biosorption by mushrooms. Natural Product Radiance 4(6): 454 – 459.

Fosu-Mensah BY, Okoffo ED, Mensah M (2016) Syn-thetic pyrethroids pesticide residues in soils and drinking water sources from cocoa farms in Ghana. Environment & Pollution 5(1): 60 – 72. doi:10.5539/ep.v5n1p60.

Kwodaga JK, Odamtten GT, Owusu E, Akrofi AY (2017b) Influence of copper-based fungicides application on copper contamination of soils of cocoa farm at Akim Tafo, Eastern Region, Ghana. Ecology, Environment & Conservation 23(1): 165 – 172.

Yeoh BH, Lee CY, Tsunoda K (2006) Evaluation of several novel and conventional termiticide formulations against the Asian subterranean termite, Coptotermes gestroi (Wasmann) (Isoptera: Rhinotermitidae). In: Tsu-noda K. ed. Proceedings of the third conference of Pacific Rim Termite Research Group. Kyoto University, Kyoto, Japan. 79 – 83.

Mao L, Henderson G, Scherer CW (2011) Toxicity of seven termiticides on the Formosan and eastern subterra-nean termites. Journal of Economic Entomology 104: 1002 – 1008. doi:10.1603/EC11005.

Sapkota R, Stout MJ, Henderson G (2020) Residual effects of termiticides on mortality of Formosan subterra-nean termite (Isoptera: Rhinotermitidae) on substrates subjected to flooding. Journal of Economic Entomology 113(1): 367 – 374. doi:10.1093/jee/toz293.