Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-05-21T09:29:56.163Z Has data issue: false hasContentIssue false

Temperature-dependent development, survival and reproduction of Apanteles hemara (Nixon) (Hymenoptera: Braconidae) on Spoladea recurvalis (F.) (Lepidoptera: Crambidae)

Published online by Cambridge University Press:  18 February 2020

M. K. Agbodzavu*
Affiliation:
Zoology Department, Jomo Kenyatta University of Agriculture and Technology (JKUAT), P.O. Box 62000-00200 Nairobi, Kenya Plant Health Unit, International Centre of Insect Physiology and Ecology (ICIPE), P. O. Box 30772-00100, Nairobi, Kenya
Z. Osiemo-Lagat
Affiliation:
Zoology Department, Jomo Kenyatta University of Agriculture and Technology (JKUAT), P.O. Box 62000-00200 Nairobi, Kenya
M. Gikungu
Affiliation:
Zoology Department, Jomo Kenyatta University of Agriculture and Technology (JKUAT), P.O. Box 62000-00200 Nairobi, Kenya
S. Ekesi
Affiliation:
Plant Health Unit, International Centre of Insect Physiology and Ecology (ICIPE), P. O. Box 30772-00100, Nairobi, Kenya
K. K. M. Fiaboe
Affiliation:
Plant Health Unit, International Centre of Insect Physiology and Ecology (ICIPE), P. O. Box 30772-00100, Nairobi, Kenya International Institute of Tropical Agriculture, P. O. Box. 2008 (Messa), Cameroon
*
Author for correspondence: M. K. Agbodzavu, Email: agbodzavu@gmail.com

Abstract

The temperature-dependent development of Apanteles hemara (Nixon), a larval endoparasitoid of the devastating amaranth pest Spoladea recurvalis (F.) was studied in the laboratory at six constant temperatures (10, 15, 20, 25, 30 and 35 °C), a photoperiod of 12L:12D and a relative humidity of 60–70%. Developmental time decreased significantly with increasing temperature within the range of 15–30 °C. The parasitoid's pupal mortality, successful parasitism rate, adult emergence rate and longevity, sex ratio and fecundity were affected by temperature. The population of A. hemara failed to develop at 10 and 35 °C. The development threshold (Tmin) and the thermal constant (K) were calculated by the linear model while the lethal temperature (Tmax) was determined by the Lactin-1 model. The estimated values of Tmin, Tmax and K by the two models were 10.3 °C, 35.0 °C and 185.18 DD respectively for the total immature development. The estimated value of the optimum temperature using the Taylor model was 30.8 °C. This is the first study to report on the effect of temperature on the developmental parameters of A. hemara giving an insight into its biology. The implications of these findings for the use of A. hemara in biological control are discussed.

Type
Research Paper
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abram, PK, Brodeur, J, Urbaneja, A and Tena, A (2019) Nonreproductive effects of insect parasitoids on their hosts. Annual Review of Entomology 64, 259276.CrossRefGoogle ScholarPubMed
Agbodzavu, K, Lagat, ZO, Gikungu, M, Akutse, K, Ekesi, S and Fiaboe, KK (unpublished data). Diversity, distribution, seasonality and alternative hosts of amaranth lepidopteran defoliators and their associated natural enemies in two agro-ecological zones of Kenya.Google Scholar
Argov, Y and Rossler, Y (1996) Introduction, release and recovery of several exotic natural enemies for biological control of the citrus leaf miner, Phyllocnistis citrella, in Israel. Phytoparasitica 24, 3338.CrossRefGoogle Scholar
Berndt, LA and Wratten, SD (2005) Effects of alyssum flowers on the longevity, fecundity, and sex ratio of the leafroller parasitoid Dolichogenidea tasmanica. Biological Control 32, 6569.CrossRefGoogle Scholar
Bhattacherjee, N and Ramdas Menon, M (1964) Bionomics, biology and control of Hymenia recurvalis (Fabricius) (Pyralidae: Lepidoptera). Indian Journal of Entomology 26, 176183.Google Scholar
Cardona, C and Oatman, E (1971) Biology of Apanteles dignus (Hymenoptera: Braconidae), a primary parasite of the tomato pinworm. Annals of the Entomological Society of America 64, 9961007.CrossRefGoogle Scholar
Cardona, C and Oatman, E (1975) Biology and physical ecology of Apanteles subandinus Blanchard (Hymenoptera: Braconidae), with notes on temperature responses of Apanteles scutellaris Muesebeck and its host, the potato tuberworm. Hilgardia 43, 151.CrossRefGoogle Scholar
Chang, JC and Ramasamy, S (2016) Transcriptome analysis in the Beet Webworm, Spoladea recurvalis Fabricius (Lepidoptera: Crambidae). Insect Science 25, 3344.CrossRefGoogle Scholar
Chow, A and Heinz, KM (2005) Using hosts of mixed sizes to reduce male-biased sex ratio in the parasitoid wasp, Diglyphus isaea. Entomologia Experimentalis et Applicata 117, 193199.CrossRefGoogle Scholar
Clarke-Harris, D and Fleischer, SJ (2003) Sequential sampling and biorational chemistries for management of lepidopteran pests of vegetable amaranth in the Caribbean. Journal of Economic Entomology 96, 798804.CrossRefGoogle ScholarPubMed
Clarke-Harris, D, Fleischer, S, Fuller, C and Bolton, J (2004) Evaluation of the efficacy of new chemistries for controlling major lepidoptera pests on vegetable amaranth in Jamaica. CARDI Review 4, 1219.Google Scholar
Dannon, EA, Tamò, M, van Huis, A and Dicke, M (2010) Functional response and life history parameters of Apanteles taragamae, a larval parasitoid of Maruca vitrata. BioControl 55, 363378.CrossRefGoogle Scholar
Esmat, H, Wedad, K and Neama, A (2017) Effects of photoperiod on the immature developmental time of Apanteles galleriae Wilkinson (Hymenoptera: Braconidae). Journal of Agricultural Science and Food Technology 3, 16.Google Scholar
Ghahari, H, Fischer, M and Tobias, VI (2012) A study on the Braconidae (Hymenoptera: Ichneumonoidea) from Guilan province, Iran. Entomofauna 33, 317324.Google Scholar
Hentz, MG, Ellsworth, PC, Naranjo, SE and Watson, TF (1998) Development, longevity, and fecundity of Chelonus Sp. nr. curvimaculatus (Hymenoptera: Braconidae), an egg-larval parasitoid of pink bollworm (Lepidoptera: Gelechiidae). Environmental Entomology 27, 443449.CrossRefGoogle Scholar
Hoddle, MS, Warner, K, Steggall, J and Jetter, KM (2014) Classical biological control of invasive legacy crop pests: new technologies offer opportunities to revisit old pest problems in perennial tree crops. Insects 6, 1337.CrossRefGoogle ScholarPubMed
Houndekon, VA, De Groote, H and Lomer, C (2006) Health costs and externalities of pesticide use in the Sahel. Outlook on Agriculture 35, 2531.CrossRefGoogle Scholar
Htwe, AN, Takagi, M and Takasu, K (2008) Development of Myanmar strain of Cotesia vestalis (Hymenoptera: Braconidae) on its host Plutella xylostella (Lepidoptera: Plutellae) at different temperatures. Journal-Faculty of Agriculture Kyushu University 53, 441446.Google Scholar
James, B, Atcha-Ahowé, C, Godonou, I, Baimey, H, Goergen, G, Sikirou, R and Toko, M (2010) Gestion integree des nuisibles en production maraichere: guide pour les agents de vulgarisation en Afrique de l'Ouest. Ibadan: Nigeria Institut international d'agriculture tropicale (IITA), 120p.Google Scholar
Jervis, MA and Copland, MJW (1996) The Life Cycle. London, UK: Chapman & Hall.Google Scholar
Jiang, N, Sétamou, M, Ngi-Song, AJ and Omwega, CO (2004) Performance of Cotesia flavipes (Hymenoptera: Braconidae) in parasitizing Chilo partellus (Lepidoptera: Crambidae) as affected by temperature and host stage. Biological Control 31, 155164.CrossRefGoogle Scholar
Kahuthia-Gathu, R (2011) Invasion of amaranth and spinach by the spotted beet webworm Hymenia species in Eastern Province of Kenya. Jomo Kenyatta University reports. Nairobi, Kenya, 5p.Google Scholar
Kernasa, O, Suasa-ard, W and Charernsom, K (2008) Citrus leafminer, Phyllocnistis citrella Stainton (Lepidoptera: Phyllocnistidae) and its natural enemies. Kasetsart Journal: Natural Science 42, 238245.Google Scholar
Lee, S-K, Kim, J, Cheong, S-S, Kim, Y-K, Lee, S-G and Hwang, C-Y (2013) Temperature-dependent development model of hawaiian beet webworm Spoladea recurvalis Fabricius (Lepidoptera: Pyraustinae). Korean Journal of Applied Entomology 52, 512.CrossRefGoogle Scholar
Llacer, E, Urbaneja, A, Garrido, A and Jacas, J (2006) Temperature requirements may explain why the introduced parasitoid Quadrastichus citrella (Hymeoptera: Eulophidae) failed to control Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Spain. BioControl 51, 439452.CrossRefGoogle Scholar
Macharia, I (2015) Pesticides and health in vegetable production in Kenya. BioMed Research International 2015, 10.CrossRefGoogle ScholarPubMed
Mathieu, A, Dumont, Y, Chiroleu, F, Duyck, P-F, Flores, O, Lebreton, G, Reynaud, B, Quilici, S (2014) Predicting the altitudinal distribution of an introduced phytophagous insect against an invasive alien plant from laboratory controlled experiments: case of Cibdela janthina (Hymenoptera: Argidae) and Rubus alceifolius (Rosaceae) in La Réunion. BioControl 59, 461471.CrossRefGoogle Scholar
Maumbe, BM and Swinton, SM (2003) Hidden health costs of pesticide use in Zimbabwe's smallholder cotton growers. Social Science & Medicine 57, 15591571.CrossRefGoogle ScholarPubMed
Mohamad, F, Mansour, M and Ramadan, A (2015) Effects of biological and environmental factors on sex ratio in Ascogaster quadridentata Wesmael (Hymenoptera: Braconidae), a parasitoid of Cydia pomonella L. (Torticidae). Journal of Plant Protection Research 55, 151155.Google Scholar
Mohamed, SA, Overholt, WA, Wharton, RA and Lux, SA (2006) Effect of temperature on developmental time and longevity of Psyttalia cosyrae (Hymenoptera: Braconidae). Biocontrol Science and Technology 16, 717726.CrossRefGoogle Scholar
Murillo, H, Hunt, DW and VanLaerhoven, SL (2012) Fecundity and life table parameters of Campoletis sonorensis (Hymenoptera: Ichneumonidae), an endoparasitoid of the cabbage looper Trichoplusia ni Hübner (Lepidoptera: Noctuidae), under laboratory conditions. Biocontrol Science and Technology 22, 125134.CrossRefGoogle Scholar
Neven, LG (2000) Physiological responses of insects to heat. Postharvest Biology and Technology 21, 103111.CrossRefGoogle Scholar
Othim, STO, Agbodzavu, KM, Kahuthia-Gathu, R, Akutse, KS, Muchemi, S, Ekesi, S and Fiaboe, KKM (2017) Performance of Apanteles hemara (Hymenoptera: Braconidae) on two Amaranth Leaf-webbers: Spoladea recurvalis and Udea ferrugalis (Lepidoptera: Crambidae). Environmental Entomology 46, 12841291.CrossRefGoogle Scholar
Pande, Y (1972) Some observations on the Bionomics of Hymenia recurvalis F. (Lepid., Pyralidae) feeding on Trianthema monogyna and Amaranthus viridis in India. Zeitschrift für Angewandte Entomologie 72, 362366.Google Scholar
Papp, J (1996) Braconid wasps from the Cape Verde Islands (Hymenoptera, Braconidae). 1. Cheloninae, Exothecinae, Homolobinae, Microgastrinae, Rogadinae. Boletim do Museu Municipal do Funchal (História Natural) 48, 197216.Google Scholar
Paredes-López, O (2018) Amaranth Biology, Chemistry, and Technology. London, New York: CRC Press, 223p.CrossRefGoogle Scholar
Peter, C and Balasubramanian, R (1984) New records of parasites of Hymenia recurvalis (Lepidoptera: Pyralidae) on Amaranthus. Entomon 2, 7172.Google Scholar
Peter, C and David, B (1990) Biology of Apanteles machaeralis Wilkinson (Hymenoptera: Braconidae) a parasite of Diaphania indica (Saunders) (Lepidoptera: Pyralidae). Proceedings: Animal Sciences 99, 353362.Google Scholar
Qiu, B, Zhou, Z-S, Luo, S-P and Xu, Z-F (2012) Effect of temperature on development, survival, and fecundity of Microplitis manilae (Hymenoptera: Braconidae). Environmental Entomology 41, 657664.CrossRefGoogle Scholar
Qureshi, SR, Quan, W-L, Zhou, R-Q, Zhu, F and Wang, X-P (2017) Thermal effects on development and adult longevity of endoparasitoid Chelonus murakatae Munakata (Hymenoptera: Braconidae). Environmental Science and Pollution Research 24, 49264931.CrossRefGoogle Scholar
R Core Team (2017) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/Google Scholar
Ramalho, FS, Wanderley, PA, Malaquias, JB, Fernandes, FS, Nascimento, AR and Zanuncio, JC (2011) Effect of temperature on the reproduction of Bracon vulgaris Ashmead (Hymenoptera: Braconidae), a parasitoid of the cotton boll weevil. Anais da Academia Brasileira de Ciências 83, 10211030.CrossRefGoogle Scholar
Rebaudo, F, Struelens, Q and Dangles, O (2017) Modelling temperature-dependent development rate and phenology in arthropods: the devRate package for r. Methods in Ecology and Evolution 9, 11441150.CrossRefGoogle Scholar
Rechav, Y (1978) Biological and ecological studies of the parasitoid Chelonus inanitus (Hym.: Braconidae) in Israel. Entomophaga 23, 95102.CrossRefGoogle Scholar
Régnière, J (1984) A method of describing and using variability in development rates for the simulation of insect phenology. The Canadian Entomologist 116, 13671376.CrossRefGoogle Scholar
Roy, M, Brodeur, J and Cloutier, C (2002) Relationship between temperature and developmental rate of Stethorus punctillum (Coleoptera: Coccinellidae) and its prey Tetranychus mcdanieli (Acarina: Tetranychidae). Environmental Entomology 31, 177187.CrossRefGoogle Scholar
Santiago, P, Tenbergen, K, Vélez-Jiménez, E and Cardador-Martínez, M (2014) Functional attributes of amaranth. Austin Journal of Nutrition and Food Sciences 2, 1010.Google Scholar
Şengonca, Ç and Peters, G (1993) Biology and effectiveness of Apanteles rubecula Marsh. (Hym., Braconidae), a solitary larval parasitoid of Pieris rapae (L.) (Lep., Pieridae). Journal of Applied Entomology 115, 8589.Google Scholar
Stiling, P (1993) Why do natural enemies fail in classical biological control programs? American Entomologist 39, 3137.CrossRefGoogle Scholar
Taylor, F (1981) Ecology and evolution of physiological time in insects. The American Naturalist 117, 123.CrossRefGoogle Scholar
Tiwari, N and Tanwar, R (2001) Biocontrol agents of sugarcane pests: their bioecology, mass production and field application. In Upadhyay, RK, Mukerji, KG and Chamola, BP (eds.), Biocontrol Potential and its Exploitation in Sustainable Agriculture. University of Delhi, Delhi, India, Springer, pp. 189213.CrossRefGoogle Scholar
Uçkan, F and Erginin, E (2003) Temperature and food source effects on adult longevity of Apanteles galleriae Wilkinson (Hymenoptera: Braconidae). Environmental Entomology 32, 441446.CrossRefGoogle Scholar
Vance, AM (1931) Apanteles Thompsoni Lyle: A Braconid Parasite of the European Corn Borer. Beltsville: US Department of Agriculture, 28p.Google Scholar
Van Steenis, M (1994) Intrinsic rate of increase of Lysiphlebus testaceipes Cresson (Hym.; Braconidae), a parasitoid of Aphis gossypii Glover (Hom., Aphididae) at different temperatures. Journal of Applied Entomology 118, 399406.CrossRefGoogle Scholar
Varma, G, Rataul, H, Shenhmar, M, Singh, S and Jalali, S (1991) Role of inundative releases of egg parasitoid Trichogramma chilonis Ishii in the control of Chilo auricilius Dudgeon on sugarcane. Journal of Insect Science (India) 4, 165166.Google Scholar
Wohlfarter, M and Addison, P (2014) Life table study of Anagyrus Sp. nr. pseudococci (Girault) (Hymenoptera: Encyrtidae) on its host, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). African Entomology 22, 250256.CrossRefGoogle Scholar
Zamani, AA, Talebi, A, Fathipour, Y and Baniameri, V (2007) Effect of temperature on life history of Aphidius colemani and Aphidius matricariae (Hymenoptera: Braconidae), two parasitoids of Aphis gossypii and Myzus persicae (Homoptera: Aphididae). Environmental Entomology 36, 263271.CrossRefGoogle Scholar