Stable isotopes for reliable identification of wild and mass-reared Queensland fruit flies in sterile insect technique programs

Abstract

Queensland fruit fly is one of the most economically important horticultural pests in Australia. Sterile insect technique (SIT) is now being reconsidered and upscaled to combat this pest so reliable discrimination of released sterile Q-flies from wild flies in monitoring traps is important for effective SIT operations. Stable isotopes provide a permanent chemical marker to discriminate sterile and wild flies when dye marking is unclear. In this study, we compared the isotopic ratios of carbon and nitrogen between Q-flies reared on different larval diets and wild flies collected from diverse locations in Australia and New Caledonia. Finally, we conducted a release–recapture study to corroborate differences in stable isotope C and N ratios in laboratory-reared and wild Q-flies. The δ15N values obtained from wild and laboratory Q-flies showed high variability that is likely related to the food source of the larval and/or adult stage and do not offer an effective means to discriminate between sterile and wild Q-flies. The δ13C values of examined wild Q-flies ranged from − 27.46 to − 24.37‰ VPDB, whereas those from laboratory-reared, released and recaptured Q-flies ranged from − 25.73 to − 19.26‰ VPDB. Differences in δ13C values resulted in 100% correct classification of wild flies and 96.88% correct classification of released flies. Measurements of intrinsic δ13C values offer a precise tool to discriminate between sterile and wild Q-flies in SIT programs, regardless of the composition of the larval or adult pre-release diets.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Availability of data and material

The datasets generated during the current study are available from the corresponding author on reasonable request.

Code availability

No custom code was used in this research.

References

  1. Adams M-O, Seifert CL, Lehner L, Truxa C, Wanek W, Fiedler K (2016) Stable isotope signatures reflect dietary diversity in European forest moths. Front Zool. https://doi.org/10.1186/s12983-016-0170-0

    Article  PubMed  PubMed Central  Google Scholar 

  2. 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. J Insect Physiol 57:1592–1601

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. Aluja M, Ordano M, Guillén L, Rull J (20120 Understanding long-term fruit fly (Diptera: Tephritidae) population dynamics: implications for area wide management. J Econ Entomol. 105: 823–836.

  4. Bateman MA (1991) The impact of fruit flies on Australian horticulture. 81 pp. Horticultural policy council report no. 3. Canberra: Department of Primary Industries.

  5. Bohlke J, Coplen TB (1995) IAEA TECDOC-825 Proceedings of a consultants meeting held in Vienna Austria 1–3. 1993.

  6. Botteon V, Costa MdLZ, Kovaleski A, Martinelli LA, Mastrangelo T (2018) Can stable isotope markers be used to distinguish wild and mass-reared Anastrepha fraterculus flies? PLoS ONE 13(12):e0209921. https://doi.org/10.1371/journal.pone.0209921

    Article  PubMed  PubMed Central  Google Scholar 

  7. Botteon V, Costa MdLZ, Kovaleski A, Martinelli LA, Mastrangelo T (2019) Isotopic discrimination and persistence of the 13C marker in adults of Anastrepha fraterculus (Diptera: Tephritidae) Brazilian-1 morphotype. Fla Entomol 102:336–346

    Article  Google Scholar 

  8. Cangussu JA, Zucoloto FS (1992) Nutritional value and selection of different diets by adult Ceratitis capitata flies (Diptera: Tephritidae). J Insect Physiol 38:485–491

    Article  Google Scholar 

  9. Christenson LD, Maeda S, Holloway JR (1956) Substitution of dehydrated for fresh carrots in medium for rearing fruit flies. J Econ Entomol 49:135–136

    Article  Google Scholar 

  10. Clarke AR, Powell KS, Weldon CW, Taylor PW (2011) The ecology of Bactrocera tryoni (Diptera: Tephritidae): what do we know to assist pest management? Ann Appl Biol 158:26–54

    Article  Google Scholar 

  11. Coplen TB (1995) Reporting of stable hydrogen, carbon and oxygen isotopic abundances – (Technical Report). Geothermics 24:708–712

    Article  Google Scholar 

  12. Coplen TB, Brand WA, Gehre M, Groning M, Meijer HAJ, Toman B, Verkouteren RM (2006) New Guidelines for δ13C Measurements. Anal Chem 78:2439–2441

    CAS  PubMed  Article  Google Scholar 

  13. Dawson TE, Brooks PD, Fundamentals of stable isotope chemistry and measurement. In: Unkovich M, (eds) (2001) Stable isotope techniques in the study of biological processes and functioning of ecosystems. Kluwer Academic Publisher, Dordrecht, pp 1–18

    Google Scholar 

  14. Deniro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    CAS  Article  Google Scholar 

  15. Dominiak BC, Schinagl L, Nicol H (2000) Impact of fluorescent marker dyes on emergence of sterile Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Gen Appl Entomol 29:45–47

    Google Scholar 

  16. Dominiak BC, Sundaralingam S, Jiang L, Fanson BG, Collins SR, Banos C, Davies JB, Taylor PW (2014) Evaluating irradiation dose for sterility induction and quality control of mass produced Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). J Econ Entomol 107:1172–1178

    CAS  PubMed  Article  Google Scholar 

  17. Dominiak BC, Sundaralingam S, Jiang L, Jessup AJ, Barchia IM (2010) Impact of marker dye on adult eclosion and flight ability of mass produced Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Aust J Entomol 49:166–169

    Article  Google Scholar 

  18. Dominiak BC, SundaralingamS JSL, Jessup A, Barchia I (2008) Production levels and life history traits of mass reared Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) during 1999/2002 in Australia. Plant Prot Q 23:131–135

    Google Scholar 

  19. Dominiak BC, Westcott AE, Barchia IM (2003) Release of sterile Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae), at Sydney, Australia. Aust J Exp Agric 43:519–528

    Article  Google Scholar 

  20. Drew R, Hooper G, Bateman M (1978) Economic fruit flies of the South Pacific Region. Oriental fruit fly working party, standing committee on agriculture, Canberra, 137 pp.

  21. Enkerlin W (2005) Impact of fruit fly control programmes using the sterile insect technique. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 651–676

    Google Scholar 

  22. Enkerlin W, Lopez L, Celedonio H (1996) Increased accuracy in discrimination between captured wild unmarked and released dye-marked adults in fruit fly (Diptera: Tephritidae) sterile released programs. J Econ Entomol 89:946–949

    Article  Google Scholar 

  23. Fanson BG, Sundaralingam S, Jiang L, Dominiak BC, D’Arcy G (2014) A review of 16 years of quality control parameters at a mass-rearing facility producing Queensland fruit fly, Bactrocera tryoni. Entomol Exp Appl 151:152–159

    Article  Google Scholar 

  24. FAO/IAEA/USDA (2019) Product quality control for sterile mass-reared and released tephritid fruit flies, Version 7.0. International Atomic Energy Agency, Vienna

  25. Finney GL (1956) A fortified carrot medium for mass-culture of the oriental fruit fly and certain other tephritids. J Econ Entomol 49:135–136

    Article  Google Scholar 

  26. Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  27. Gilchrist AS, Dominiak BC (2019) Using DNA markers and isotope marking to test the effectiveness of fluorescent dust marking during a sterile insect technique program targeting Bactrocera tryoni (Diptera: Tephritidae) in Australia. Crop Prot 120:109–112

    Article  Google Scholar 

  28. Groning M, International stable isotope reference materials. In: De Groot PA, (eds) (2004) Handbook of stable isotope analytical techniques. Elsevier, Amsterdam, pp 874–906

    Book  Google Scholar 

  29. Hancock DL, Hamacek EL, Lloyd AC, Elson-Harris MM (2000) The distribution and host plants of fruit flies (Diptera: Tephritidae) in Australia. DPI Publications, Brisbane, Australia

    Google Scholar 

  30. Hatch KA, Crawford MA, Kunz AW, Thomsen SR (2006) An objective means of diagnosing anorexia nervosa and bulimia nervosa using 15N/ 14N and 13C/12C ratios in hair. Rapid Commun Mass Spectrom 20:3367–3373

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. Hendrichs J (2000) Use of the sterile insect technique against key insect pests. Sustain Develop Int 2:75–79

    Google Scholar 

  32. Hendrichs J, Franz G, Rendon P (1995) Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. J Appl Entomol 119:371–377

    Article  Google Scholar 

  33. Hendrichs J, Katsoyannos BI, Papaj DR, Prokopy RJ (1991) Sex differences in movement between natural feeding and mating sites and tradeoffs between food consumption, mating success and predator evasion in Mediterranean fruit flies (Diptera: Tephritidae). Oecologia 86:223–231

    CAS  PubMed  Article  Google Scholar 

  34. Hendrichs J, Vreysen MJB, Enkerlin WR, Cayol JP (2005) Strategic options in using sterile insects for area-wide integrated pest management. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 563–600

    Google Scholar 

  35. Holder PW, Van Hale RJ, Frew R, George S, Armstrong KF (2020) Natal origin of the invasive biosecurity pest, brown marmorated stink bug (Halyomorpha halys: Penatomidae), determined by dual-element stable isotope-ratio mass spectrometry. Pest Manag Sci 76(4):1456–1463

    CAS  PubMed  Article  Google Scholar 

  36. Hood-Nowotny R, Harari A, Seth RK, Wee SL, Conlong DE, Suckling DM, Carpenter JE (2016) Stable isotope markers differentiate between mass-reared and wild Lepidoptera in sterile insect technique programs. Fla Entomol 99(sp1):166–176

    Article  Google Scholar 

  37. Hood-Nowotny R, Knols BGJ (2007) Stable isotope methods in biological and ecological studies of arthropods. Entomol Exp Appl 124:3–16

    CAS  Article  Google Scholar 

  38. Hood-Nowotny R, Mayr CL, Islam A, Robinson A, Caceres C (2009) Routine isotope marking for the Mediterranean fruit fly (Diptera: Tephritidae). J Econ Entomol 102:941–947

    CAS  PubMed  Article  Google Scholar 

  39. Hood-Nowotny R, Watzka M, Mayr L, Mekonnen S, Kapitano B, Parker A (2011) Intrinsic and synthetic stable isotope marking of tsetse flies. J Insect Sci (Online) 11:79. https://doi.org/10.1673/031.011.7901

    Article  Google Scholar 

  40. Hyodo F (2015) Use of stable carbon and nitrogen isotopes in insect trophic ecology. Entomol Sci 18:295–312

    Article  Google Scholar 

  41. Jacome I, Aluja M, Liedo P (1999) Impact of adult diet on demographic and population parameters of the tropical fruit fly Anastrepha serpentina (Diptera, Tephritidae) Bull Entomol Res. 89: 165–175.

  42. Jessup A, Cruickshank L (1999) Production quality assurance for tri-state sterile insect research program, 1 January to 30 June 1998. Horticultural research and development corporation, Gordon, NSW, Australia

    Google Scholar 

  43. Kellner CM, Schoeninger MJ (2007) A simple carbon isotope model for reconstructing prehistoric human diet. Am J Phys Anthropol 133:1112–1127

  44. Knipling EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462

    Article  Google Scholar 

  45. Knipling EF (1979) The Basic Principles of insect population suppression and management. ESA Agriculture Handbook No. 512. U.S. Department of Agriculture.

  46. Majumder R, Sutcliffe B, Taylor PW, Chapman TA (2019) Next-Generation Sequencing reveals relationship between the larval microbiome and food substrate in the polyphagous Queensland fruit fly. Sci Rep 9:14292

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  47. Majumder R, Sutcliffe B, Midgley DJ, Taylor PW, Chapman TA (2020) Fruit host-dependent fungal communities in the microbiome of wild Queensland fruit fly larvae. Sci Rep 10:16550

  48. Madeira F, Di Lascio A, Carlino P, Costantini ML, Pons X (2013) Change in carbon stable isotope ratios of the predatory bug Orius majusculus after dietary shifts. Entomol Exp Appl 148:287–296

    CAS  Article  Google Scholar 

  49. Mainali BP, Moadeli T, Ponton F, Taylor PW (2019) Comparison of gel larval diet with traditional lucerne chaff and carrot solid diets for rearing of Queensland fruit fly (Diptera: Tephritidae). J Econ Entomol 112:2278–2286

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  50. Meats A, Holmes HM, Kelly GL (2004) Laboratory adaptation of Bactrocera tryoni (Diptera: Tephritidae) decreases mating age and increases protein consumption and number of eggs produced per milligram of protein. Bull Entomol Res 94:517–524

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. Minagawa M, Wada E (1984) Stepwise enrichment of 15 N along food chains: further evidence and the relation between δ15 N and animal age. Geochim Cosmochim Acta 48:1135–1140

    CAS  Article  Google Scholar 

  52. Moadeli T, Taylor PW, Ponton F (2017) High productivity gel diets for rearing of Queensland fruit fly, Bactrocera tryoni. J Pest Sci 90:507–520

    Article  Google Scholar 

  53. Myers JH, Savoie A, van Randen E (1998) Eradication and pest management. Annu Rev Entomol 43:471–491

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. Norris KR (1957) A method of marking Calliphoridae (Diptera) during emergence from the puparium. Nature 15:309–315

    Google Scholar 

  55. O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336

    Article  Google Scholar 

  56. Opiyo MA, Hamer GL, Lwetoijera DW, Auckland LD, Majambere S, Okumu FO (2016) Using stable isotopes of carbon and nitrogen to mark wild populations of Anopheles and Aedes mosquitoes in South-Eastern Tanzania. PLoS ONE 11:e0159067. https://doi.org/10.1371/journal.pone.0159067d

    Article  PubMed  PubMed Central  Google Scholar 

  57. Perez-Staples D, Prabhu V, Taylor PW (2007) Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiol Entomol 32:225–232

    Article  Google Scholar 

  58. Ramírez-Santos EM, Rendón P, Ruiz-Montoya L, Toledo J, Liedo P (2016) Performance of a Genetically Modified Strain of the Mediterranean Fruit Fly (Diptera: Tephritidae) for Area-Wide Integrated Pest Management with the Sterile Insect Technique. J Econ Entomol 110(1):24–34

    Google Scholar 

  59. SAS Institute Inc. (2016) SAS/STAT User’s Guide Version 9.4, SAS Institute, Cary, NC, USA

  60. Schoell M, Faber E, Coleman ML (1983) Carbon and hydrogen isotopic compositions of the NBS 22 and NBS 21 stable isotope reference materials: An inter-laboratory comparison: Org Geochem. 5: 3–6.

  61. Schwarcz HP (1991) Some theoretical aspects of isotope paleodiet studies. J Archaeol Sci 18:261–275

  62. Steiner LF (1965) A rapid method for identifying dye-marked fruit flies. J Econ Entomol 58:374–375

    Article  Google Scholar 

  63. Sutherst RW, Collyer BS, Yonow T (2000) The vulnerability of Australian horticulture to the Queensland fruit fly, Bactrocera (Dacus) tryoni, under climate change. Aust J Agric Res 51:467–480

    Article  Google Scholar 

  64. Voigt CC, Rex K, Michener RH, Speakman JR (2008) Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia 157:31–40

  65. Vreysen MJB, Hendrichs J, Enkerlin WR (2006) The sterile insect technique as a component of sustainable area-wide integrated pest management of selected horticultural insect pests. J Fruit Ornam Plant Res 14:107–131

    Google Scholar 

  66. Wada E, Mizutani H, Minagawa M (1991) The use of stable isotopes for food web analysis. Crit Rev Food Sci Nutr 30:361–371

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  67. Wehi PM, Hicks BJ (2010) Isotopic fractionation in a large herbivorous insect, the Auckland tree weta. J Insect Physiol 56:1877–1882

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  68. Weldon CW (2005) Marking Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) with fluorescent pigments: pupal emergence, adult mortality and visibility and persistence of marks. Gen Appl Entomol 34:7–13

    Google Scholar 

Download references

Funding

This research was conducted as part of the SITplus collaborative fruit fly program. Project Raising Q-fly Sterile Insect Technique to World Standard (HG14033) is funded by the Hort Frontiers Fruit Fly Fund, part of the Hort Frontiers strategic partnership initiative developed by Hort Innovation, with co-investment from Macquarie University and contributions from the Australian Government.

Author information

Affiliations

Authors

Corresponding author

Correspondence to P. Rempoulakis.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Consent for publication

This research was conducted at Macquarie University, using funds from Hort Innovation. Both Macquarie University and Hort Innovation and all of the authors, consent to publication of this work.

Consent to participate

This research only involved research using insects. Consent to participate does not apply.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Jian J Duan.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Mainali, B., Andrew, A.S., Taylor, P.W. et al. Stable isotopes for reliable identification of wild and mass-reared Queensland fruit flies in sterile insect technique programs. J Pest Sci (2021). https://doi.org/10.1007/s10340-021-01383-2

Download citation

Keywords

  • Tephritidae
  • Bactrocera tryoni
  • SIT
  • Carbon
  • Nitrogen