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Yeast derivatives and wheat germ in the adult diet modulates fecundity in a tephritid pest

Published online by Cambridge University Press:  22 May 2018

L. Goane ,
P.M. Pereyra ,
F. Castro ,
M.J. Ruiz ,
M.L. Juárez ,
D.F. Segura  and
M.T. Vera
L. Goane*
Affiliation:
Facultad de Agronomía y Zootecnia, Cátedra de Terapéutica Vegetal (CTV), Universidad Nacional de Tucumán, Tucumán, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
P.M. Pereyra
Affiliation:
Instituto de Fisiología Animal, Fundación Miguel Lillo, Tucumán, Argentina
F. Castro
Affiliation:
Instituto de Fisiología Animal, Fundación Miguel Lillo, Tucumán, Argentina
M.J. Ruiz
Affiliation:
Facultad de Agronomía y Zootecnia, Cátedra de Terapéutica Vegetal (CTV), Universidad Nacional de Tucumán, Tucumán, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
M.L. Juárez
Affiliation:
Facultad de Agronomía y Zootecnia, Cátedra de Terapéutica Vegetal (CTV), Universidad Nacional de Tucumán, Tucumán, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina Unidad Ejecutora Lillo, Fundación Miguel Lillo, Tucumán, Argentina
D.F. Segura
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina Instituto de Genética “E.A. Favret”, CICVyA, Instituto Nacional de Tecnología Agropecuaria, Hurlingham, Argentina
M.T. Vera
Affiliation:
Facultad de Agronomía y Zootecnia, Cátedra de Terapéutica Vegetal (CTV), Universidad Nacional de Tucumán, Tucumán, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
*
*Author for correspondence Phone: +54 0381 4390003 Fax: +54 0381 4390040 E-mail: lugoane@gmail.com
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Abstract

Anastrepha fraterculus (Wiedemann), a pest of great economic importance in South America, needs urgently to be controlled by environmentally friendly methods such as the sterile insect technique for which mass rearing of insects is required. Because oogenesis takes place during the adult stage, mass-rearing facilities should provide the females a diet that maximizes egg production at the lowest cost. Accordingly, we investigated the effect of artificial protein sources in the adult diet (yeast derivatives of different cost but with similar amino acids profiles, and the addition of wheat germ) on fecundity. Additionally, we evaluated different ratios of yeast derivatives or wheat germ on ovary maturation, fecundity, and fertility as well as their association with the nutrient content of females. Females fed hydrolyzed yeast and yeast extract attained the highest fecundity level, and those fed brewer's yeast the lowest. Reducing the amount of hydrolyzed yeast, an expensive protein source, in the diet negatively affected fecundity and ovary maturation. Increasing the amount of brewer's yeast, a low-cost protein source, did not favor fecundity. The addition of wheat germ in the adult diet improved fecundity regardless of the yeast derivate considered. Percentage of egg hatch was not affected by the diet. Nutrient content of A. fraterculus females varied according to the adult diet provided and mating status. Our findings provide novel baseline information to understand the role of nutrition on reproductive performance of A. fraterculus females and are discussed in the context of resource allocation. They also provide valuable advances in the search for cost-effective adult diets at fruit fly mass rearing facilities.

Keywords

hydrolyzed yeastyeast extractbrewer's yeastproteinlipidsovary maturationAnastrepha fraterculus
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 2 , April 2019 , pp. 178 - 190
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Copyright
Copyright © Cambridge University Press 2018 

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References

Allinghi, A., Gramajo, C., Willink, E. & Vilardi, J. (2007) Induction of sterility in Anastrepha fraterculus (Diptera: Tephritidae) by gamma radiation. Florida Entomologist 90, 96–102.Google Scholar
Aluja, M., Piñero, J., Jácome, I., Díaz-Fleischer, F. & Sivinski, J. (2000) Behavior of flies in the genus Anastrepha (Trypetinae: Toxotrypanini). pp. 375–406 in Aluja, M. & Norrbom, A. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Aluja, M., Birke, A., Guillén, L., Díaz-Fleischer, F. & Nestel, D. (2011) Coping with an unpredictable and stressful environment: the life history and metabolic response to variable food and host availability in a polyphagous tephritid fly. Journal of Insect Physiology 57, 1592–1601.Google Scholar
Arrese, E.L. & Soulages, J.L. (2010) Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55, 207–225.Google Scholar
Balzarini, M.G., Gonzalez, L., Tablada, M., Casanoves, F., Di Rienzo, J.A. & Robledo, C.W. (2008) Infostat User´S Guide., Córdoba, Argentina, Editorial Brujas.Google Scholar
Bauerfeind, S.S. & Fischer, K. (2005) Effects of adult-derived carbohydrates, amino acids and micronutrients on female reproduction in a fruit-feeding butterfly. Journal of Insect Physiology 51, 545–554.Google Scholar
Bauerfeind, S.S., Fischer, K., Hartstein, S., Janowitz, S. & Martin-Creuzburg, D. (2007) Effects of adult nutrition on female reproduction in a fruit-feeding butterfly: the role of fruit decay and dietary lipids. Journal of Insect Physiology 53, 964–973.Google Scholar
Blagović, B., Rupčić, J., Mesarić, M., Georgiú, K. & Marić, V. (2001) Lipid composition of brewer's yeast. Food Technology and Biotechnology 39, 175–181.Google Scholar
Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Annals of Biochemistry 72, 248–254.Google Scholar
Canavoso, L.E., Jouni, Z.E., Karnas, K.J., Pennington, J.E. & Wells, M.A. (2001) Fat metabolism in insects. Annual Review of Nutrition 21, 23–46.Google Scholar
Carey, J.R., Harshman, L.G., Liedo, P., Müller, H.G., Wang, J.L. & Zhang, Z. (2008) Longevity-fertility trade-offs in the tephritid fruit fly, Anastrepha ludens, across dietary-restriction gradients. Aging Cell 7, 470–477.Google Scholar
Chang, C.L. (2004) Effect of amino acids on larvae and adults of Ceratitis capitata (Diptera: Tephritidae). Annals of the Entomological Society of America 97, 529–535.Google Scholar
Chang, C.L. (2009) Evaluation of yeasts and yeast products in larval and adult diets for the oriental fruit fly, Bactrocera dorsalis, and adult diets for the medfly, Ceratitis capitata, and the melon fly, Bactrocera curcurbitae. Journal of Insect Science 9, 1–9.Google Scholar
Chang, C.L. & Vargas, R.I. (2007) Wheat germ oil and its effects on a liquid larval rearing diet for oriental fruit flies (Diptera: Tephritidae). Journal of Economic Entomology 100, 322–326.Google Scholar
Chang, C.L., Vargas, R.I., Caceres, C., Jang, E. & Cho, I.K. (2006) Development and assessment of a liquid larval diet for Bactrocera dorsalis (Diptera: Tephritidae). Annals of the Entomological Society of America 99, 1191–1198.Google Scholar
Chang, C.L., Coudron, T.A., Goodman, C.L., Stanley, D.W., An, S. & Song, Q. (2010) Wheat germ oil in larval diet influences gene expression in adult oriental fruit fly. Journal of Insect Physiology 56, 356–365.Google Scholar
Chang, C.L., Coudron, T.A., Goodman, C.L. & Stanley, D.W. (2012) Larval dietary wheat germ oil influences age-specific protein expression in adults of the oriental fruit fly. Journal of Insect Physiology 58, 690–698.Google Scholar
Cheng, D., Chen, L., Yi, C., Liang, G. & Xu, Y. (2014) Association between changes in reproductive activity and D-glucose metabolism in the tephritid fruit fly, Bactrocera dorsalis (Hendel). Science Report 4, 1–9.Google Scholar
Christenson, L.D. & Foote, R.H. (1960) Biology of fruit flies. Annual Review of Entomology 5, 171–192.Google Scholar
Cladera, J., Vilardi, J.C., Juri, M., Paulin, L.E., Giardini, M.C., Gómez Cendra, P.V., Segura, D.F. & Lanzavecchia, S.B. (2014) Genetics and biology of Anastrepha fraterculus: research supporting the use of the sterile insect technique (SIT) to control this pest in Argentina. BMC Genetics 15, S12.Google Scholar
Cohen, A.C. (2004) Insect Diets: Science and Technology. Florida, USA, CRS Press.Google Scholar
Crawley, R.J. (2007) The R Book. Chichester, UK, Jhon Wiley & Sons.Google Scholar
Di Rienzo, J.A., Casanoves, F., Balzarini, M.G., Gonzalez, L., Tablada, M. & Robledo, C.W. (2017 a) InfoStat Versión 2017. Córdoba, Argentina, Grupo InfoStat, FCA, Universidad Nacional de Córdoba. Available online at http://www.infostat.com.ar.Google Scholar
Di Rienzo, J.A., Machiavelli, R. & Casanoves, F. (2017 b) Modelos Lineales Generalizados Mixtos en InfoStat. Córdoba, Argentina, Grupo InfoStat, FCA, Universidad Nacional de Córdoba. ISBN 978-987-42-4985-2.Google Scholar
Drew, R.A.I. & Yuval, B.I. (2000) The evolution of fruit fly feeding behavior. pp. 731–749 in Aluja, M. & Norrbom, A. (Eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behaviour. Boca Raton, FL, CRC Press.Google Scholar
Dyck, V.A., Hendrichs, J. & Robinson, A.S. (2006) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. Dordrecht, Netherlands, Springer Science & Business Media.Google Scholar
Fanson, B.G. & Taylor, P.W. (2012) Additive and interactive effects of nutrient classes on longevity, reproduction, and diet consumption in the Queensland fruit fly (Bactrocera tryoni). Journal of Insect Physiology 58, 327–334.Google Scholar
Fanson, B.G., Weldon, C.W., Pérez-Staples, D., Simpson, S.J. & Taylor, P.W. (2009) Nutrients, not caloric restriction, extend lifespan in Queensland fruit flies (Bactrocera tryoni). Aging Cell 8, 514–523.Google Scholar
Faraway, J.J. (2006). Extending the linear model with R: Generalized linear. Mixed Effects and Nonparametric Regression Models, 1. Florida, USA, CRC Press, Taylor & Francis Group.Google Scholar
Fischer, K., O'Brien, D.M. & Boggs, C.L. (2004) Allocation of larval and adult resources to reproduction in a fruit-feeding butterfly. Functional Ecology 18, 656–663.Google Scholar
Geister, T.L., Lorenz, M.W., Hoffmann, K.H. & Fischer, K. (2008) Adult nutrition and butterfly fitness: effects of diet quality on reproductive output, egg composition, and egg hatching success. Frontiers in Zoology 5, 10.Google Scholar
Grandison, R.C., Piper, M.D. & Partridge, L. (2009) Amino acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature 462, 1061–1064.Google Scholar
Gullan, P.J. & Cranston, P.S. (2014) The Insects: An Outline of Entomology. West Sussex, UK, John Wiley & Sons Ltd.Google Scholar
Hansen, M., Flatt, T. & Aguilaniu, H. (2013) Reproduction, fat metabolism, and life span: what is the connection? Cell Metabolism 17, 10–19.Google Scholar
Hernández-Ortiz, V., Canal, N.A., Salas, J.O.T., Ruíz-Hurtado, F.M. & Dzul-Cauich, J.F. (2015) Taxonomy and phenotypic relationships of the Anastrepha fraterculus complex in the Mesoamerican and Pacific Neotropical dominions (Diptera, Tephritidae). ZooKeys 540, 95–124.Google Scholar
Jácome, I., Aluja, M., Liedo, P. & Nestel, D. (1995) The influence of adult diet and age on lipid reserves in the tropical fruit fly Anastrepha serpentina (Diptera: Tephritidae). Journal of Insect Physiology 41, 1079–1086.Google Scholar
Jácome, I., Aluja, M. & Liedo, P. (1999) Impact of adult diet on demographic and population parameters of the tropical fruit fly Anastrepha serpentina (Diptera: Tephritidae). Bulletin of Entomological Research 89, 165–175.Google Scholar
Jensen, K., McClure, C., Priest, N.K. & Hunt, J. (2015) Sex-specific effects of protein and carbohydrate intake on reproduction but not lifespan in Drosophila melanogaster. Aging Cell 14, 605–615.Google Scholar
Jervis, M.A., Boggs, C.L. & Ferns, P.N. (2005) Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera. Ecological Entomology 30, 359–375.Google Scholar
Jervis, M.A., Ellers, J. & Harvey, J.A. (2008) Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annual Review of Entomology 53, 361–385.Google Scholar
Juárez, M.L., Devescovi, F., Břízová, R., Bachmann, G., Segura, D.F., Kalinová, B., Fernández, P., Ruiz, M.J., Yang, J., Teal, P.E.A., Cáceres, C., Vreysen, M.J.B., Hendrichs, J. & Vera, M.T. (2015) Evaluating mating compatibility within fruit fly cryptic species complexes and the potential role of sex pheromones in pre-mating isolation. ZooKeys 540, 125–155. Available online at http://dx.doi.org/10.3897/zookeys.540.6133.Google Scholar
Kaspi, R., Mossinson, S., Drezner, T., Kamensky, B. & Yuval, B. (2002) Effects of larval diet on development rates and reproductive maturation of male and female Mediterranean fruit flies. Physiological Entomology 27, 29–38.Google Scholar
Knipling, E.F. (1959) Screwworm eradication: concepts and research leading to the sterile male method. Smithsonian Institution Publication 4365, 409–418.Google Scholar
Kouloussis, N.A., Damos, P.T., Ioannou, C.S., Tsitsoulas, C., Papadopoulos, N.T. & Nestel, D. (2017) Age related assessment of sugar and protein intake of Ceratitis capitata in ad libitum conditions and modeling its relation to reproduction. Frontiers in Physiology 8, 271. Available online at http://doi.org/10.3389/fphys.2017.00271.Google Scholar
Lee, K.P. (2015) Dietary protein:carbohydrate balance is a critical modulator of lifespan and reproduction in Drosophila melanogaster: a test using a chemically defined diet. Journal of Insect Physiology 75, 12–19.Google Scholar
Lee, K.P., Simpson, S.J., Clissold, F.J., Brooks, R., Ballard, J.W.O., Taylor, P.W., Soran, N. & Raubenheimer, D. (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proceedings of the National Academy of Science of the United States of America 105, 2498–2503.Google Scholar
Leitão-Gonçalves, R., Carvalho-Santos, Z., Francisco, A.P., Fioreze, G.T., Anjos, M., Baltazar, C., Elias, A.P., Itskov, P.M., Piper, M.D.W. & Ribeiro, C. (2017) Commensal bacteria and essential amino acids control food choice behavior and reproduction. PLoS Biology 15, e2000862.Google Scholar
LeOra Software 2002–2003. Polo Plus. Probit and Logit Analysis. Version 1.Google Scholar
Levin, E., McCue, M.D. & Davidowitz, G. (2017) More than just sugar: allocation of nectar amino acids and fatty acids in a Lepidopteran. Proceedings of the Royal Society B 284, 20162126. Available online at http//dx.doi.org/10.1098/rspb2016.2126.Google Scholar
Liendo, M.C., Devescovi, F., Bachmann, G.E., Utgés, M.E., Abraham, S., Vera, M.T., Lanzavecchia, S.B., Bouvet, J.P., Gómez-Cendra, P., Hendrichs, J., Teal, P.E.A., Cladera, J.L. & Segura, D.F. (2013) Precocious sexual signalling and mating in Anastrepha fraterculus (Diptera: Tephritidae) sterile males achieved through juvenile hormone treatment and protein supplements. Bulletin of Entomological Research 103, 1–13.Google Scholar
Mastrangelo, T., Parker, A.G., Jessup, A., Pereira, R., Orozco-Dávila, D., Islam, A., Dammalage, T. & Walder, J.M. (2010) A new generation of X ray irradiators for insect sterilization. Journal of Economic Entomology 103, 85–94.Google Scholar
Morelli, R., Zamboni Costa, K., Martins Fagioni, K., Zamboni Costa, M.L., Do Nascimento, A.S., Meirelles de Azevedo Pimentel, R. & Melges Walder, J.M. (2012) New protein sources in adults diet for mass-rearing of Anastrepha fraterculus (Diptera:Tephritidae). Brazilian Archives on Biology and Technology 55, 827–833.Google Scholar
Nemny-Lavy, E. & Nestel, D. (2014) Protein requirements of the adult Ethiopian fruit fly Dacus ciliates. International Journal of Tropical Insect Science 34, S140–S147.Google Scholar
Nestel, D., Galun, R. & Friedman, S. (1985) Long-term regulation of sucrose intake by the adult Mediterranean fruit fly, Ceratitis capitata (Wiedemann). Journal of Insect Physiology 31, 533–536.Google Scholar
Nestel, D., Papadopoulos, N.T., Pascacio-Villafán, C., Righini, N., Altuzar-Molina, A.R. & Aluja, M. (2016) Resource allocation and compensation during development in holometabolous insects. Journal of Insect Physiology 95, 78–88.Google Scholar
Orr, C.W.M. (1964) The influence of nutritional and hormonal factors on the chemistry of the fat body, blood, and ovaries of the blowfly Phormia regina Meig. Journal of Insect Physiology 10, 103–119.Google Scholar
Ortiz, G. (1999) Potential use of the sterile insect technique against the South American fruit fly. pp. 121–130 in IAEA (Ed.) The South American Fruit fly, Anastrepha Fraterculus (Wied.): Advances in Artificial Rearing, Taxonomic status and Biological Studies. Vienna, Austria, IAEA Tech-Doc 1064.Google Scholar
Oviedo, A., Nestel, D., Papadopoulous, N.T., Ruiz, M.J., Prieto, S.C., Willink, E. & Vera, M.T. (2011) Management of protein intake in the fruit fly Anastrepha fraterculus. Journal of Insect Physiology 57, 1622–1630.Google Scholar
Papanastasiou, S.A., Nakas, C.T., Carey, J.R. & Papadopoulos, N.T. (2013) Condition-dependent effects of mating on longevity and fecundity of female medflies: the interplay between nutrition and age of mating. PLoS ONE 8, e70181. Available online at http//doi.org/10.1371/journal.pone.0070181.Google Scholar
Pascacio-Villafán, C., Williams, T., Sivinski, J., Birke, A. & Aluja, M. (2015) Costly nutritious diets do not necessarily translate into better performance of artificially reared fruit flies (Diptera: Tephritidae). Journal of Economic Entomology 108, 53–59.Google Scholar
Perez-Staples, D., Prabhu, V. & Taylor, P.W. (2007) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiological Entomology 32, 225–232.Google Scholar
Pinheiro, J.C. & Bates, D.M. (2000) Mixed-effects Models in S and S-Plus. New York, NY, Springer.Google Scholar
Raubenheimer, D. & Simpson, S.J. (1993) The geometry of compensatory feeding in the locust. Animal Behaviour 45, 953–964.Google Scholar
Simpson, S.J. & Raubenheimer, D. (1995) The geometric analysis of feeding and nutrition: a user's guide. Journal of Insect Physiology 41, 533–545.Google Scholar
Taylor, P.W., Perez-Staples, D., Weldon, C.W., Collins, S.R., Fanson, B.G., Yap, S. & Smallridge, C. (2011) Post-teneral nutrition as an influence on reproductive development, sexual performance and longevity of Queensland fruit flies. Journal of Applied Entomology 137, 113–125.Google Scholar
Teal, P.E., Gavilanez-slone, J.M. & Dueben, B.D. (2004) Effects of sucrose in adult diet on mortality of males of Anastrepha suspensa (Diptera: Tephritidae). Florida Entomology 87, 487–491.Google Scholar
Van Handel, E. (1965) Estimation of glycogen in small amounts of tissue. Annals of Biochemistry 11, 256–265.Google Scholar
Vera, M.T., Abraham, S., Oviedo, A. & Willink, E. (2007) Demographic and quality control parameters of Anastrepha fraterculus (Diptera: Tephritidae) maintained under artificial rearing. Florida Entomologist 90, 53–57.Google Scholar
Vera, M.T., Oviedo, A., Abraham, S., Ruiz, M.J., Mendoza, M., Chang, C.L. & Willink, E. (2014) Development of a larval diet for the South American fruit fly Anastrepha fraterculus (Diptera: Tephritidae). Journal of Tropical Insect Science 34, S73–S81.Google Scholar
Ziegler, R. & Van Antwerpen, R. (2006). Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology 36, 264–272.Google Scholar