Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-23T05:01:10.788Z Has data issue: false hasContentIssue false
  • English
  • Français

Microbial composition affects the performance of an artificial Tephritid larval diet

Published online by Cambridge University Press:  20 September 2017

P. Rempoulakis ,
S. Sela (Saldinger) ,
E. Nemny-Lavy ,
R. Pinto ,
A. Birke  and
D. Nestel
P. Rempoulakis*
Affiliation:
Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia Department of Entomology, Institute of Plant Protection, The Volcani Center, ARO, P. O. Box 15159, Rishon LeZiyyon 7528809, Israel
S. Sela (Saldinger)
Affiliation:
Microbial Food-Safety Research Unit, Department of Food Quality & Safety, Institute for Postharvest and Food Sciences, The Volcani Center, ARO, P. O. Box 15159, Rishon LeZiyyon 7528809, Israel
E. Nemny-Lavy
Affiliation:
Department of Entomology, Institute of Plant Protection, The Volcani Center, ARO, P. O. Box 15159, Rishon LeZiyyon 7528809, Israel
R. Pinto
Affiliation:
Microbial Food-Safety Research Unit, Department of Food Quality & Safety, Institute for Postharvest and Food Sciences, The Volcani Center, ARO, P. O. Box 15159, Rishon LeZiyyon 7528809, Israel
A. Birke
Affiliation:
Red de Manejo Biorracional de Plagas y Vectores, Clúster Científico y Tecnológico Biomimic®, Instituto de Ecología, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, Mexico
D. Nestel
Affiliation:
Department of Entomology, Institute of Plant Protection, The Volcani Center, ARO, P. O. Box 15159, Rishon LeZiyyon 7528809, Israel
*
*Author for correspondence: Tel: +61 02 98501314 Fax: +61 02 98504299 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The present study investigated the patterns of microorganisms in an artificial larval diet during Dacus ciliatus (Diptera; Tephritidae) larval development. Microbial population contents in the diet of total heterotrophic bacteria, yeast and molds, coliform and lactobacilli, and their dynamics during development, were monitored. Initially, the microbial composition in diet trays failing to produce viable pupae and in trays successfully producing pupae and adult flies was characterized. The failing diet trays contained large populations of lactobacilli that increased during larval development, and low populations of coliforms. In contrast, the successful diet showed an increasing population of coliforms and a low, or undetected, population of lactobacilli. To study the hypothesis that lactobacilli affect D. ciliatus larval development, we conducted controlled inoculation experiments in which Lactobacillus plantarum was added into fresh diet at the time of egg seeding. L. plantarum inoculated trays showed no production of D. ciliatus. Control trays without lactobacilli inoculation showed variable results. One tray successfully produced viable pupae and adults, and showed a slight and slow increase in the indigenous populations of lactobacilli. The second tray, however, failed to produce pupae and showed a fast increase of the indigenous lactobacilli to very high levels. Monitored pH trends in L. plantarum-inoculated diet showed a sharp pH decrease during the first 4 days of larval development from 5 to less than 4 units, while successful diet, producing viable D. ciliatus pupae and adults, showed a moderate pH drop during most of the larval development period. The paper discusses the possible ecological interactions between D. ciliatus larvae, the microbial content of the diet and the physical properties of the diet. The discussion also points out at the usefulness of this approach in understanding and managing mass production parameters of tephritid fruit flies industrial diets used for Sterile Insect Technique.

Keywords

larval mediumlactobacillicoliformsmass rearing
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 4 , August 2018 , pp. 434 - 441
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Alberti, M., Marzluff, J.M., Shulenberger, E., Bradley, G., Ryan, C. & Zumbrunnen, C. (2003) Integrating human into ecology: opportunities and challenges for studying urban ecosytems. Bioscience 53, 1169–1179.Google Scholar
Augustinos, A.A., Kyritsis, G.A., Papadopoulos, N.T., Abd-Alla, A.M.M., Cáceres, C. & Bourtzis, K. (2015) Exploitation of the medfly gut microbiota for the enhancement of sterile insect technique: use of Enterobacter sp. in larval diet-based probiotic applications. PLoS ONE 10, 1–17.CrossRefGoogle ScholarPubMed
Belda, E., Pedrola, L., Peretó, J., Martínez-Blanch, J.F., Montagud, A., Navarro, E., Urchueguía, J., Ramón, D., Moya, A. & Porcar, M. (2011) Microbial diversity in the midguts of field and lab-reared populations of the European corn borer Ostrinia nubilalis. PLoS ONE 6, e21751.CrossRefGoogle ScholarPubMed
Ben Ami, E., Yuval, B. & Jurkevitch, E. (2010) Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance. The ISME Journal 4, 28–37.Google Scholar
Calkins, C.O., Parker, A.G. (2005) Sterile insect quality. pp. 269–296 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique, Principles and Practice in Area-Wide Integrated Pest Management. Springer, Dordrecht, The Netherlands.CrossRefGoogle Scholar
Chan, H.T. & Jang, E.B. (1995) Diet pH effects on mass rearing of Mediterranean Fruit Fly (Diptera: Tephritidae). Journal of Economic Entomology 88(3), 569–573.Google Scholar
Cohen, A.C. 2015. Insect Diets : Science and Technology. 2nd edn. Boca Raton, FL, USA, CRC Presss.Google Scholar
Dimou, I., Rempoulakis, P. & Economopoulos, A.P. (2010) Olive fruit fly [Bactrocera (Dacus) oleae (Rossi) (Diptera: Tephritidae)] adult rearing diet without antibiotic. Journal of Applied Entomology 134, 72–79.Google Scholar
Economopoulos, A.P. & Zervas, G.A. (1982) The Quality Problem in Olive Flies Produced for SIT Experiments. Vienna, IAEA STI/PUB.Google Scholar
Ellis, J.L., Bannink, A., Hindrichsen, I.K., Kinley, R.D., Pellikaan, W.F., Milora, N. & Dijkstra, J. (2016) The effect of lactic acid bacteria included as a probiotic or silage inoculant on in vitro rumen digestibility, total gas and methane production. Animal Feed Science and Technology 211, 61–74.CrossRefGoogle Scholar
EPPO (2011) Data sheets on quarantine pests: Dacus ciliatus. Available at: https://www.eppo.int/QUARANTINE/insects/ Dacus_ciliatus/DACUCI_ds.pdf (accessed 23 May 2017).Google Scholar
Estes, A.M., Nestel, D., Belcari, A., Jessup, A., Rempoulakis, P. & Economopoulos, A.P. (2012) A basis for the renewal of sterile insect technique for the olive fly, Bactrocera oleae (Rossi). Journal of Applied Entomology 136, 1–16.Google Scholar
Inglis, G.D. & Cohen, A.C. (2004) Influence of antimicrobial agents on the spoilage of a meat-based entomophage diet. Journal of Economic Entomology 97, 235–250.Google Scholar
Jang, E.B. & Chan, H.T. (1993) Alleviation of acetic acid production during mass rearing of the Mediterranean fruit fly (Diptera: Tephritidae). Journal of Economic Entomology 86(2), 301–309.Google Scholar
Khaeso, K., Andongma, A.A., Soulyianonh, A., Zhu, J., Krutmuang, P. & Niu, C.-Y. (2017) Assessing the effects of gut bacteria manipulation on the development of the oriental fruit fly, Bactrocera dorsalis (Diptera; Tephritidae). Symbiosis, 1–9. https://doi.org/10.1007/s13199-017-0493-4Google Scholar
Konstantopoulou, M.A., Economopoulos, A.P. & Raptopoulos, D.G. (1999) Artificial rearing antimicrobials as selecting factors of Adh alleles in Bactrocera (Dacus) oleae (Diptera: Tephritidae). Journal of Economic Entomology 92, 563–568.Google Scholar
Konstantopoulou, M.A. & Raptopoulos, D. (2003) Alcohol dehydrogenase allele frequencies in Bactrocera oleae (Dipt., Tephritidae): Effect of ethanol addition in larval diet. Journal of Applied Entomology 127, 243–247.Google Scholar
Maklakov, A., Ishaaya, I., Freidberg, A., Yawetz, A., Horowitz, A.R. & Yarom, I. (2001) Toxicological studies of organophosphorous and pyrethroid insecticides for controlling the fruit fly Dacus ciliatus (Diptera: Tephritidae). Journal of Economic Entomology 94, 1059–1066.Google Scholar
Mello, A.F.S., Wayadande, A.C., Yokomi, R.K. & Fletcher, J. (2009) Transmission of different isolates of Spiroplasma citri to carrot and citrus by Circulifer tenellus (Hemiptera: Cicadellidae). Journal of Economic Entomology 102, 1417–1422.CrossRefGoogle ScholarPubMed
Mueller, U.G. & Sachs, J.L. (2015) Engineering microbiomes to improve plant and animal health. Trend in Microbiology 23, 606–617.CrossRefGoogle ScholarPubMed
Nemny-Lavy, E., Nestel, D. & Rempoulakis, P. (2016) Laboratory longevity and competitiveness of Dacus ciliatus Loew (Diptera: Tephritidae) following sub-sterilizing gamma irradiation. Bulletin of Entomological Research 106, 415–419.CrossRefGoogle ScholarPubMed
Nestel, D., Nemny-Lavy, E., Zilberg, L., Weiss, M., Akiva, R. & Gazit, Y. (2004) The fruit fly PUB: a phagostimulation unit bioassay system to quantitatively measure ingestion of baits by individual flies. Journal of Applied Entomology 128, 576–582.Google Scholar
Prosser, J.I., Bohannan, B.J.M., Curtis, T.P., Ellis, R.J., Firestone, M.K., Freckleton, R.P., Green, J.L., Green, L.E., Killham, K., Lennon, J.J., Osborn, A.M., Solan, M., Van Der Gast, C.J. & Young, J.P.W. (2007) The role of ecological theory in microbial ecology. Nature Reviews, Microbiology 5, 384–392.CrossRefGoogle ScholarPubMed
Rempoulakis, P., Afshar, N., Osorio, B., Barajas-Aceves, M., Szular, J., Ahmad, S., Dammalage, T., Tomas, U.S., Nemny-Lavy, E., Salomon, M., Vreysen, M.J.B., Nestel, D. & Missirlis, F. (2014a). Conserved metallomics in two insect families evolving separately for a hundred million years. Biometals 27, 1323–1335.Google Scholar
Rempoulakis, P., Dimou, I., Chrysargyris, A. & Economopoulos, A.P. (2014b) Improving olive fruit fly Bactrocera oleae (Diptera: Tephritidae) adult and larval artificial diets, microflora associated with the fly and evaluation of a transgenic olive fruit fly strain. International Journal of Tropical Insect Science 34, S114–S122.Google Scholar
Rempoulakis, P., Castro, R., Nemny-Lavy, E. & Nestel, D. (2015) Effects of radiation on the fertility of the Ethiopian fruit fly, Dacus ciliatus. Entomologia Experimentalis et Applicata 155, 117–122.CrossRefGoogle Scholar
Rempoulakis, P., Nemny-Lavy, E. & , Castro, R. & Nestel, D. (2016) Mating behaviour of Dacus ciliatus (Loew) [Diptera:Tephritidae]: comparisons between a laboratory and a wild population. Journal of Applied Entomology 140, 250–260.Google Scholar
Savino, F., Cordisco, L., Tarasco, V., Locatelli, E., Di Gioia, D., Oggero, R. & Matteuzzi, D. (2011) Antagonistic effect of lactobacillus strains against gas-producing coliforms isolated from colicky infants. BMC Microbiology 11, 157.Google Scholar
Sørensen, J.G., Addison, M.F. & Terblanche, J.S. (2012) Mass-rearing of insects for pest management: challenges, synergies and advances from evolutionary physiology. Crop Protection 38, 87–94.Google Scholar
StatSoft, Inc. 2011. STATISTICA, version 10. Tulsa, OK.Google Scholar
Tzanakakis, M. (2003) Seasonal development and dormancy of insects and mites feeding on olive: a review. Netherlands Journal of Zoology 52, 87–224.Google Scholar
Vandermeer, J.H. (2011) The Ecology of Agroecosystems. Boston, Jones & Bartlett Learning.Google Scholar
Vargas, R.I., Williamson, D.L., Chang, H. & Komura, M. (1984) Effects of larval diet pH on worker comfort and insect quality during mass production of Mediterranean fruit fly (Diptera: Tephritidae) in Hawaii. Journal of Environmental Science And Health A 19(5), 621–630.Google Scholar
Supplementary material: File

Rempoulakis et al supplementary material

Table S1

Download Rempoulakis et al supplementary material(File)
File 12.6 KB