Differential Susceptibility of Wild and Cultivated Blueberries to an Invasive Frugivorous Pest

  • Cesar Rodriguez-Saona
  • Kevin R. Cloonan
  • Fernando Sanchez-Pedraza
  • Yucheng Zhou
  • M. Monica Giusti
  • Betty Benrey


Highbush blueberry is a crop native to the northeast USA that has been domesticated for about 100 years. This study compared the susceptibility of wild and domesticated/cultivated highbush blueberries to an invasive frugivorous pest, the spotted wing drosophila (Drosophila suzukii). We hypothesized that: 1) cultivated fruits are preferred by D. suzukii for oviposition and better hosts for its offspring than wild fruits; and, 2) wild and cultivated fruits differ in physico-chemical traits. Fruits from wild and cultivated blueberries were collected from June through August of 2015 and 2016 from 10 to 12 sites in New Jersey (USA); with each site having wild and cultivated blueberries growing in close proximity. The preference and performance of D. suzukii on wild and cultivated blueberries were studied in choice and no-choice bioassays. In addition, we compared size, firmness, acidity (pH), total soluble solids (°Brix), and nutrient, phenolic, and anthocyanin content between wild and cultivated berries. In choice and no-choice bioassays, more eggs were oviposited in, and more flies emerged from, cultivated than wild blueberries. Cultivated fruits were 2x bigger, 47% firmer, 14% less acidic, and had lower °Brix, phenolic, and anthocyanin amounts per mass than wild fruits. Levels of potassium and boron were higher in cultivated fruits, while calcium, magnesium, and copper were higher in wild fruits. These results show that domestication and/or agronomic practices have made blueberries more susceptible to D. suzukii, which was associated with several physico-chemical changes in fruits. Our study documents the positive effects of crop domestication/cultivation on an invasive insect pest.


Highbush blueberry Vaccinium corymbosum Spotted wing drosophila Drosophila suzukii Preference-performance Physical attributes Fruit chemistry 



We thank the technical assistance of Matthew Strom, Evan Gunn, Robert Holdcraft, and Vera Kyryczenko-Roth, and two anonymous reviewers for their comments on an earlier version of the manuscript. We also wish to thank the blueberry growers who allowed us access to their farms and to adjacent wild sites. This research was supported by funds from the USDA NIFA Specialty Crop Research Initiative (SCRI) program (No. 2015-51181-24252), the New Jersey Blueberry and Cranberry Research Council, and hatch projects NJ08192 and NJ08140.


  1. Altieri MA, Nicholls CI (2003) Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems. Soil Tillage Res 72:203–211CrossRefGoogle Scholar
  2. Asplen MK, Anfora G, Biondi A, Choi D-S, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchison WD, Isaacs R, Jiang Z-L, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton V, Yu Y, Zappala L, Desneux N (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494CrossRefGoogle Scholar
  3. Atallah J, Teixeira L, Salazar R, Zaragoza G, Kopp A (2014) The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species. Proc R Soc Lond B Biol Sci 281:20132840CrossRefGoogle Scholar
  4. Ballman ES, Drummond FA (2017) Infestation of wild fruit by Drosophila suzukii surrounding Maine wild blueberry fields. J Agr Urban Entomol 33:61–70CrossRefGoogle Scholar
  5. Bellamy DE, Sisterson MS, Walse SS (2013) Quantifying host potentials: indexing postharvest fresh fruits for spotted wing drosophila, Drosophila suzukii. PLoS ONE 8:e61227CrossRefGoogle Scholar
  6. Benrey B, Callejas A, Rios L, Oyama K, Denno RF (1998) The effects of domestication of Brassica and Phaseolus on the interaction between phytophagous insects and parasitoids. Biol Control 11:130–140CrossRefGoogle Scholar
  7. Burrack HJ, Fernandez GE, Spivey T, Kraus DA (2013) Variation in selection and utilization of host crops in the field and laboratory by Drosophila suzukii Matsumara (Diptera: Drosophilidae), an invasive frugivore. Pest Manag Sci 69:1173–1180CrossRefGoogle Scholar
  8. Chen YH, Gols R, Benrey B (2015) Crop domestication and its impact on naturally selected trophic interactions. Annu Rev Entomol 60:35–58CrossRefGoogle Scholar
  9. Córdova-Campos O, Adame-Álvarez RM, Acosta-Gallegos JA, Heil M (2012) Domestication affected the basal and induced disease resistance in common bean (Phaseolus vulgaris). Eur J Plant Pathol 134:367–379CrossRefGoogle Scholar
  10. Culliney TW, Pimentel D (1986) Ecological effects of organic agricultural practices on insect populations. Agric Ecosyst Environ 15:253–256CrossRefGoogle Scholar
  11. Cuny MA, Shlichta GJ, Benrey B (2017) The large seed size of domesticated lima beans mitigates intraspecific competition among seed beetle larvae. Front Ecol Evol 5.
  12. Dalton DT, Walton VM, Shearer PW, Walsh DB, Caprile J, Isaacs R (2011) Laboratory survival of Drosophila suzukii under simulated winter conditions of the Pacific northwest and seasonal field trapping in five primary regions of small and stone fruit production in the United States. Pest Manag Sci 67:1368–1374CrossRefGoogle Scholar
  13. Darwin C (1868) The variation of animals and plants under domestication. London: John Murray. 1st ed, 1. Volume 1Google Scholar
  14. Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418:700–707CrossRefGoogle Scholar
  15. Doebley JF, Gaut BS, Smith BD (2006) The molecular genetics of crop domestication. Cell 127:1309–1321CrossRefGoogle Scholar
  16. Draper A, Galletta G, Jelenkovic G, Vorsa N (1987) Duke' highbush blueberry. HortScience 22:320Google Scholar
  17. Dróżdż P, Šėžienė V, Pyrzynska K (2018) Mineral composition of wild and cultivated blueberries. Biol Trace Elem Res 181:173–177CrossRefGoogle Scholar
  18. Eck P, Childers NF (1966) Bluebberry culture. Rutgers University Press, New BrunswickGoogle Scholar
  19. Ehlenfeldt MK (2009) Domestication of the highbush blueberry at Whitesbog, New Jersey, 1911-1916. Acta Hortic 810:147–152CrossRefGoogle Scholar
  20. Evans L (1993) Crop evolution, adaptation, and yield. Cambridge University Press, CambridgeGoogle Scholar
  21. Gallardo RK, Zhang Q, Dossett M, Polashock J, Rodriguez-Saona C, Vorsa N, Edger PP, Ashrafi H, Babiker E, Finn CE, Iorizzo M (2018) Breeding trait priorities of the blueberry industry in the United States and Canada. HortScience 53:1021–1028CrossRefGoogle Scholar
  22. Gepts P (2004) Crop domestication as a long-term selection experiment. In: Janick J (ed) Plant breeding reviews. Wiley, New York, pp 1–44Google Scholar
  23. Giovanelli G, Buratti S (2009) Comparison of polyphenolic composition and antioxidant activity of wild Italian blueberries and some cultivated varieties. Food Chem 112:903–908CrossRefGoogle Scholar
  24. Giusti MM, Wrolstad RE (2001) Characterization and measurement of anthocyanins by UV-visible spectroscopy. In: Wrolstad RE (ed) Current protocols in food analytical chemistry. Wiley, New York, pp F1.3.1–F1.3.13Google Scholar
  25. Hammer K (1984) Das domestikationssyndrom. Die Kulturpflanze 32:11–34CrossRefGoogle Scholar
  26. Hancock J (2001) Blueberry characteristics range among the varieties. The Fruit Growers News, May Issue, pp. 36–37Google Scholar
  27. Hardin JA, Kraus DA, Burrack HJ (2015) Diet quality mitigates intraspecific larval competition in Drosophila suzukii. Entomol Exp Appl 156:59–65CrossRefGoogle Scholar
  28. Harlan JR (1971) Agricultural origins: centers and noncenters. Science 174:468–474CrossRefGoogle Scholar
  29. Harlan JR (1992) Crops and man. Crop Science Society of America, MadisonGoogle Scholar
  30. Hauser M (2011) A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification. Pest Manag Sci 67:1352–1357CrossRefGoogle Scholar
  31. Hedin PA, Jenkins JN, Collum DH, White WH, Parrott WL, MacGown MW (1983) Cyanidin-3-β-glucoside, a newly recognized basis for resistance in cotton to the tobacco budworm Heliothis virescens (Fab.) (Lepidoptera: Noctuidae). Cell Mol Life Sci 39:799–801CrossRefGoogle Scholar
  32. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  33. Hernandez-Cumplido J, Giusti MM, Zhou Y, Kyryczenko-Roth V, Chen YH, Rodriguez-Saona C (2018) Testing the ‘plant domestication-reduced defense’ hypothesis in blueberries: the role of herbivore identity. Arthropod Plant Interact 12:483–493. CrossRefGoogle Scholar
  34. Horneck DA, Miller RO (1998) Determination of total nitrogen in plant tissue. In: Kalra YP (ed) Handbook and reference methods for plant analysis. CRC Press, New York, pp 75–83Google Scholar
  35. Huang C-YL, Schulte E (1985) Digestion of plant tissue for analysis by ICP emission spectroscopy. Commun Soil Sci Plant Anal 16:943–958CrossRefGoogle Scholar
  36. Ioriatti C, Walton V, Dalton D, Anfora G, Grassi A, Maistri S, Mazzoni V (2015) Drosophila suzukii (Diptera: Drosophilidae) and its potential impact to wine grapes during harvest in two cool climate wine grape production regions. J Econ Entomol 108:1148–1155CrossRefGoogle Scholar
  37. Jaramillo SL, Mehlferber E, Moore PJ (2015) Life-history trade-offs under different larval diets in Drosophila suzukii (Diptera: Drosophilidae). Physiol Entomol 40:2–9CrossRefGoogle Scholar
  38. Kalt W, McDonald JE, Ricker RD, Lu X (1999) Anthocyanin content and profile within and among blueberry species. Can J Plant Sci 79:617–623CrossRefGoogle Scholar
  39. Kareiva P, Watts S, McDonald R, Boucher T (2007) Domesticated nature: shaping landscapes and ecosystems for human welfare. Science 316:1866–1869CrossRefGoogle Scholar
  40. Kinjo H, Kunimi Y, Ban T, Nakai M (2013) Oviposition efficacy of Drosophila suzukii (Diptera: Drosophilidae) on different cultivars of blueberry. J Econ Entomol 106:1767–1771CrossRefGoogle Scholar
  41. Lattanzio V, Lattanzio VM, Cardinali A (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. In: Imperato F (ed) Phytochemistry: advances in research. Research Signpost, Kerala, pp 23–67Google Scholar
  42. Lee JC, Bruck DJ, Curry H, Edwards D, Haviland DR, Van Steenwyk RA, Yorgey BM (2011) The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii. Pest Manag Sci 67:1358–1367CrossRefGoogle Scholar
  43. Lee JC, Dreves AJ, Cave AM, Kawai S, Isaacs R, Miller JC, Van Timmeren S, Bruck DJ (2015) Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae). Ann Entomol Soc Am 108:117–129CrossRefGoogle Scholar
  44. Lee JC, Dalton DT, Swoboda-Bhattarai KA, Bruck DJ, Burrack HJ, Strik BC, Woltz JM, Walton VM (2016) Characterization and manipulation of fruit susceptibility to Drosophila suzukii. J Pest Sci 89:771–780CrossRefGoogle Scholar
  45. Liebhold AM, Tobin PC (2008) Population ecology of insect invasions and their management. Annu Rev Entomol 53:387–408CrossRefGoogle Scholar
  46. Little CM, Chapman TW, Moreau DL, Hillier NK (2017) Susceptibility of selected boreal fruits and berries to the invasive pest Drosophila suzukii (Diptera: Drosophilidae). Pest Manag Sci 73:160–166CrossRefGoogle Scholar
  47. Lu H, Zhang J, K-b L, Wu N, Li Y, Zhou K, Ye M, Zhang T, Zhang H, Yang X (2009) Earliest domestication of common millet (Panicum miliaceum) in East Asia extended to 10,000 years ago. Proc Natl Acad Sci 106:7367–7372CrossRefGoogle Scholar
  48. Mainland CM (2012) Frederick V. Coville and the history of North American highbush blueberry culture. Int J Fruit Sci 12:4–13CrossRefGoogle Scholar
  49. Mainland CM, Ehlenfeldt MK (2017) Celebrating the 100th anniversary of highbush blueberry domestication–the contribution by Frederick Vernon Coville and Elizabeth Coleman White. Acta Hortic 1180:135–142CrossRefGoogle Scholar
  50. Marshall DA, Spiers JM, Stringer SJ (2008) Blueberry splitting tendencies as predicted by fruit firmness. HortScience 43:567–570Google Scholar
  51. McCormick J (1979) The vegetation of the New Jersey pine barrens. In: Forman RTT (ed) Pine barrens: ecosystem and landscape. Academic Press Inc., New York, pp 229–243Google Scholar
  52. Meyer RS, DuVal AE, Jensen HR (2012) Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops. New Phytol 196:29–48CrossRefGoogle Scholar
  53. Mirnezhad M, Romero-González RR, Leiss KA, Choi YH, Verpoorte R, Klinkhamer PG (2010) Metabolomic analysis of host plant resistance to thrips in wild and cultivated tomatoes. Phytochem Anal 21:110–117CrossRefGoogle Scholar
  54. Moore J (1965) Improving highbush blueberries by breeding and selection. Euphytica 14:39–48Google Scholar
  55. Nation (2001) Insect physiology and biochemistry. CRC Press, Boca RatonCrossRefGoogle Scholar
  56. Pelton E, Gratton C, Guédot C (2017) Susceptibility of cold hardy grapes to Drosophila suzukii (Diptera: Drosophilidae). J Appl Entomol 141:644–652CrossRefGoogle Scholar
  57. Phelan PL, Mason JF, Stinner BR (1995) Soil-fertility management and host preference by European corn borer, Ostrinia nubilalis (Hübner), on Zea mays L.: a comparison of organic and conventional chemical farming. Agric Ecosyst Environ 56:1–8CrossRefGoogle Scholar
  58. Revadi S, Lebreton S, Witzgall P, Anfora G, Dekker T, Becher PG (2015) Sexual behavior of Drosophila suzukii. Insects 6:183–196CrossRefGoogle Scholar
  59. Rivera MJ, Rodriguez-Saona C, Jennings DE, Koppenhöfer AM (2015) Assessing the impact of cultivation and plant domestication of highbush blueberry (Vaccinium corymbosum) on soil properties and associated plant-parasitic nematode communities. Soil Biol Biochem 88:25–28CrossRefGoogle Scholar
  60. Rodriguez-Saona LE, Wrolstad RE (2001) Extraction, isolation, and purification of anthocyanins. In: Wrolstad RE (ed) Current protocols in food analytical chemistry. Wiley, New York, pp F1.1.1–F1.1.11Google Scholar
  61. Rodriguez-Saona C, Vorsa N, Singh AP, Johnson-Cicalese J, Szendrei Z, Mescher MC, Frost CJ (2011) Tracing the history of plant traits under domestication in cranberries: potential consequences on anti-herbivore defences. J Exp Bot 62:2633–2644CrossRefGoogle Scholar
  62. Rosenthal JP, Dirzo R (1997) Effects of life history, domestication and agronomic selection on plant defence against insects: evidence from maizes and wild relatives. Evol Ecol 11:337–355CrossRefGoogle Scholar
  63. Schaefer HM, Rentzsch M, Breuer M (2008) Anthocyanins reduce fungal growth in fruits. Nat Prod Commun 3:1267–1272Google Scholar
  64. Slinkard K, Singleton VL (1977) Total phenol analysis: automation and comparison with manual methods. Am J Enol Vitic 28:49–55Google Scholar
  65. Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol Lett 9:354–371CrossRefGoogle Scholar
  66. Szczepaniec A, Widney SE, Bernal JS, Eubanks MD (2013) Higher expression of induced defenses in teosintes (Zea spp.) is correlated with greater resistance to fall armyworm, Spodoptera frugiperda. Entomol Exp Appl 146:242–251CrossRefGoogle Scholar
  67. Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14CrossRefGoogle Scholar
  68. Tochen S, Dalton DT, Wiman N, Hamm C, Shearer PW, Walton VM (2014) Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry. Environ Entomol 43:501–510CrossRefGoogle Scholar
  69. Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157CrossRefGoogle Scholar
  70. Turcotte MM, Turley NE, Johnson MT (2014) The impact of domestication on resistance to two generalist herbivores across 29 independent domestication events. New Phytol 204:671–681CrossRefGoogle Scholar
  71. Warburton ML, Wilkes G, Taba S, Charcosset A, Mir C, Dumas F, Madur D, Dreisigacker S, Bedoya C, Prasanna B, Xie CX, Hearne S, Franco J (2011) Gene flow among different teosinte taxa and into the domesticated maize gene pool. Genet Resour Crop Evol 58:1243–1261CrossRefGoogle Scholar
  72. Whitehead SR, Turcotte MM, Poveda K (2017) Domestication impacts on plant–herbivore interactions: a meta-analysis. Philos Trans R Soc B 372:20160034CrossRefGoogle Scholar
  73. Wink M (1988) Plant breeding: importance of plant secondary metabolites for protection against pathogens and herbivores. Theor Appl Genet 75:225–233CrossRefGoogle Scholar
  74. Yamasaki M, Wright SI, McMullen MD (2007) Genomic screening for artificial selection during domestication and improvement in maize. Ann Bot 100:967–973CrossRefGoogle Scholar
  75. Yardım EN, Edwards CA (2003) Effects of organic and synthetic fertilizer sources on pest and predatory insects associated with tomatoes. Phytoparasitica 31:324–329CrossRefGoogle Scholar
  76. Zhou Y, Giusti MM, Parker J, Salamanca J, Rodriguez-Saona C (2016) Frugivory by brown marmorated stink bug (Hemiptera: Pentatomidae) alters blueberry fruit chemistry and preference by conspecifics. Environ Entomol 45:1227–1234CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of EntomologyRutgers University P.E. Marucci CenterChatsworthUSA
  2. 2.Departamento de ParasitologiaUniversidad Autónoma Agraria Antonio NarroSaltilloMexico
  3. 3.Department of Food Science and TechnologyThe Ohio State UniversityColumbusUSA
  4. 4.Laboratory of Evolutionary Entomology, Institute of BiologyUniversity of NeuchâtelNeuchâtelSwitzerland

Personalised recommendations