Naturwissenschaften

, Volume 97, Issue 3, pp 291–298 | Cite as

Molecular diagnosis of a previously unreported predator–prey association in coffee: Karnyothrips flavipes Jones (Thysanoptera: Phlaeothripidae) predation on the coffee berry borer

  • Juliana Jaramillo
  • Eric G. Chapman
  • Fernando E. Vega
  • James D. Harwood
ORIGINAL PAPER

Abstract

The coffee berry borer, Hypothenemus hampei, is the most important pest of coffee throughout the world, causing losses estimated at US $500 million/year. The thrips Karnyothrips flavipes was observed for the first time feeding on immature stages of H. hampei in April 2008 from samples collected in the Kisii area of Western Kenya. Since the trophic interactions between H. hampei and K. flavipes are carried out entirely within the coffee berry, and because thrips feed by liquid ingestion, we used molecular gut-content analysis to confirm the potential role of K. flavipes as a predator of H. hampei in an organic coffee production system. Species-specific COI primers designed for H. hampei were shown to have a high degree of specificity for H. hampei DNA and did not produce any PCR product from DNA templates of the other insects associated with the coffee agroecosystems. In total, 3,327 K. flavipes emerged from 17,792 H. hampei-infested berries collected from the field between April and September 2008. Throughout the season, 8.3% of K. flavipes tested positive for H. hampei DNA, although at times this figure approached 50%. Prey availability was significantly correlated with prey consumption, thus indicating the potential impact on H. hampei populations.

Keywords

Biological control Organic coffee Karnyothrips flavipes Hypothenemus hampei Gut-content analysis Kenya Predator–prey interactions 

Notes

Acknowledgements

We are very grateful to Mr. Charles Kamonjo (icipe) for technical assistance, Adenirin Chabi-Olaye (icipe) for statistical advice, Christian Borgemeister for helpful comments to an earlier version of the manuscript, and Steve Nakahara (USDA, ARS) for identifying the thrips. We thank Abel O. Mainya from Kisii Coffee Demonstration (Kenya) for kindly providing the coffee berries and for his help during the sampling period, Prof. Linda Field (Head of Insect Molecular Biology Group Rothamsted Research) and Prof. John A. Pickett (Head Department of Biological Chemistry, Rothamsted Research) and three anonymous reviewers who provided valuable comments on an earlier draft of the manuscript. This research was funded by the German Research Foundation—Deutsche Forschungsgemeinschaft (DFG). JDH and ECG are supported by the University of Kentucky Agricultural Experiment Station State Project KY008043. This is publication number 09-08-052 of the University of Kentucky Agricultural Experiment Station.

Supplementary material

114_2009_641_MOESM1_ESM.pdf (86 kb)
Supplementary Table 1 (PDF 71 kb)

References

  1. Ananthakrishnan TN (1979) Biosystematics of Thysanoptera. Annu Rev Entomol 24:159–183CrossRefGoogle Scholar
  2. Armbrecht I, Rivera L, Perfecto I (2005) Reduced diversity and complexity in the leaf-litter ant assemblage of Colombian coffee plantations. Conserv Biol 19:897–907CrossRefGoogle Scholar
  3. Armbrecht I, Gallego MC (2007) Testing ant predation on the coffee berry borer in shaded and sun coffee plantations in Colombia. Entomol Exp Appl 124:261–267CrossRefGoogle Scholar
  4. Bailey P, Caon G (1986) Predation of twospotted mite, Tetranychus urticae Koch (Acarina: Tetranychidae) by Haplothrips victoriensis Bagnall (Thysanoptera: Phlaeothripidae) and Stethorus nigripes Kapur (Coleoptera: Coccinellidae) on seed lucerne crops in South Australia. Aust J Zool 34:515–525CrossRefGoogle Scholar
  5. Barrera J (1994) Dynamique des populations du scolyte des fruits du cafeier Hypothenemus hampei (Coleoptera: Scolytidae), et lutte biologique avec le parasitoide Cephalonomia stephanoderis (Hymenoptera: Bethylidae) au Chiapas, Mexique. Dissertation. Université Paul Sabatier, Toulouse, FranceGoogle Scholar
  6. Borbón-Martinez MO (1989) Bioecologie d’un ravageur des baies de caféier. Hypothenemus hampei Ferr. (Coleoptera: Scolytidae) et de ses parasitoides au Togo. Dissertation, Université Paul Sabatier, Toulouse, FranceGoogle Scholar
  7. Bustillo AE, Cárdenas R, Posada FJ (2002) Natural enemies and competitors of Hypothenemus hampei (Ferrari) in Colombia. Neotrop Entomol 31:635–639CrossRefGoogle Scholar
  8. Chen Y, Giles KL, Payton ME, Greenstone MH (2000) Identifying key cereal aphid predators by molecular gut analysis. Mol Ecol 9:1887–1898CrossRefPubMedGoogle Scholar
  9. Childers CC, Nakahara S (2006) Thysanoptera (thrips) within citrus orchards in Florida: Species distribution, relative and seasonal abundance within trees, and species on vines and ground cover plants. J Insect Sci 6:45CrossRefGoogle Scholar
  10. Cohen AC (1995) Extra-oral digestion in predaceous terrestrial Arthropoda. Annu Rev Entomol 40:85–103CrossRefGoogle Scholar
  11. Collins FA, Whitcomb WH (1975) Natural enemies of the white peach scale, Pseudaulacaspis pentagona (Homoptera: Coccidae), in Florida. Florida Entomol 58:15–21CrossRefGoogle Scholar
  12. Damon A (2000) A review of the biology and control of the coffee berry borer Hypothenemus hampei (Coleoptera: Scolytidae). Bull Entomol Res 90:453–465CrossRefPubMedGoogle Scholar
  13. Decazy B (1990) Descripción, biología, ecología y control de la broca del cafeto Hypothenemus hampei (Ferrari). In: Conferencias conmemorativas 50 años de Cenicafé 1938–1988, pp. 133–139. CENICAFE, Chinchiná, ColombiaGoogle Scholar
  14. Ding-Xu L, Juan T, Zuo-Rui S (2007) Functional response of the predator Scolothrips takahashii to hawthorn spider mite, Tetranychus viennensis: effect of age and temperature. Biocontrol 52:41–61CrossRefGoogle Scholar
  15. Elliott N, Kieckhefer R, Kauffman W (1996) Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia 105:537–544CrossRefGoogle Scholar
  16. Folmer O, Black M, Hoeh WR, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299Google Scholar
  17. Fournier V, Hagler J, Daane K, de León J, Groves R (2008) Identifying the predator complex of Homalodisca vitripennis (Hemiptera: Cicadellidae): a comparative study of the efficacy of an ELISA and PCR gut content assay. Oecologia 157:629–640CrossRefPubMedGoogle Scholar
  18. Giovannucci D, Koekoek FJ (2003) The state of sustainable coffee: a study of twelve major markets. International Coffee Organization and International Institute of Sustainable Development, London, United Kingdom and Winnipeg, CanadaGoogle Scholar
  19. Greenstone MH, Hunt JH (1993) Determination of prey antigen half-life in Polistes metricus using a monoclonal antibody-based immunodot assay. Entomol Exp Appl 68:1–7CrossRefGoogle Scholar
  20. Greenstone MH, Rowley DR, Weber DC, Hawthorne DJ (2007) Feeding mode and prey detectability half-lives in molecular gut-content analysis: An example with two predators of the Colorado potato beetle. Bull Entomol Res 97:201–209CrossRefPubMedGoogle Scholar
  21. Hargreaves H (1935) Stephanoderis hampei Ferr., coffee berry borer in Uganda. East African Agric J 1:218–224Google Scholar
  22. Harwood JD, Desneux N, Yoo HYS, Rowley DL, Greenstone ML, Obrycki JJ, O’Neil RJ (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol Ecol 16:4390–4400CrossRefPubMedGoogle Scholar
  23. Harwood JD, Yoo HJS, Greenstone MH, Rowley DL, O’Neil RJ (2009) Differential impact of adults and nymphs of a generalist predator on an exotic invasive pest demonstrated by molecular gut-content analysis. Biol Inv 11:895–903CrossRefGoogle Scholar
  24. Harwood JD, Obrycki JJ (2005) Quantifying aphid predation rates of generalist predators in the field. Eur J Entomol 102:335–350Google Scholar
  25. Hoddle MS, Jones J, Oishi K, Morgan D, Robinson L (2001) Evaluation of diets for the development and reproduction of Franklinothrips orizabensis (Thysanoptera: Aeolothripidae). Bull Entomol Res 91:273–280PubMedGoogle Scholar
  26. Hoddle MS, Nakahara S, Phillips PA (2002) Foreign exploration for Scirtothrips perseae Nakahara (Thysanoptera: Thripidae) and associated natural enemies on avocado (Persea americana Miller). Biol Control 24:251–265CrossRefGoogle Scholar
  27. Howarth FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–508CrossRefGoogle Scholar
  28. Infante F, Mumford J, García-Ballinas A (2003) Predation by native arthropods on the African parasitoid Prorops nasuta (Hymenoptera: Bethylidae) in coffee plantations of Mexico. Florida Entomol 86:86–88CrossRefGoogle Scholar
  29. Jaramillo J (2008) Biology, ecology and biological control of the coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae: Scolytinae). Dissertation, Leibniz Universität Hannover, GermanyGoogle Scholar
  30. Jaramillo J, Borgemeister C, Baker PS (2006) Coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae): searching for sustainable control strategies. Bull Entomol Res 96:223–233CrossRefPubMedGoogle Scholar
  31. Jaramillo J, Chabi-Olaye A, Borgemeister C, Kamonjo C, Poehling HM, Vega FE (2009a) Where to sample? Ecological implications of sampling strata in determining abundance and impact of natural enemies of the coffee berry borer Hypothenemus hampei. Biol Control 49:245–253CrossRefGoogle Scholar
  32. Jaramillo J, Chabi-Olaye A, Poehling HM, Kamonjo Ch, Borgemeister C (2009b) Development of an improved laboratory production technique for coffee berry borer Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae, Scolytinae), using fresh coffee berries. Entomol Exp Appl 130:275–281CrossRefGoogle Scholar
  33. Jonsson M, Wratten SD, Landis DA, Gurr GM (2008) Recent advances in conservation biological control of arthropods by arthropods. Biol Control 45:172–175CrossRefGoogle Scholar
  34. Juen A, Traugott M (2007) Revealing species-specific trophic links in soil food webs: molecular identification of scarab predators. Mol Ecol 16:1545–1557CrossRefPubMedGoogle Scholar
  35. Kakimoto K, Inoue H, Hinomoto N, Noda T, Hirano K, Kashio T, Kusigemati K, Okajima S (2006) Potential of Haplothrips brevitubus (Karny) (Thysanoptera: Phlaeothripidae) as a predator of mulberry thrips Pseudodendrothrips mori (Niwa) (Thysanoptera: Thripidae). Biol Control 37:314–319CrossRefGoogle Scholar
  36. Karlin S, Altschul SF (1990) Methods for assessing the statistical significance of molecular sequence features by using general scoring schemes. Proc Natl Acad Sci USA 87:2264–2268CrossRefPubMedGoogle Scholar
  37. Karlin S, Altschul SF (1993) Applications and statistics for multiple high-scoring segments in molecular sequences. Proc Ntl Acad Sci USA 90:5873–5877CrossRefGoogle Scholar
  38. Larentzaki E, Powell G, Copland MJW (2007) Effect of cold storage on survival, reproduction and development of adults and eggs of Franklinothrips vespiformis (Crawford). Biol Control 43:265–270CrossRefGoogle Scholar
  39. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  40. Le Pelley RH (1968) Pests of coffee. Longmans Green and Co., LondonGoogle Scholar
  41. Lewis T (1973) Thrips: their biology, ecology and economic importance. Academic Press, London, UKGoogle Scholar
  42. Mound LA (2007) Thysanoptera (Thrips) of the world—a checklist. http://www.ento.csiro.au/thysanoptera/worldthrips.html (visited 25 October 2009)
  43. Mound LA, Marullo R (1996) The thrips of Central and South America: an introduction (Insecta: Thysanoptera). Memoirs on Entomology, International, vol. 6. Associated Publishers, Gainesville, Florida, USAGoogle Scholar
  44. Mound LA, Morris DC (2007) The insect Order Thysanoptera: classification versus systematics. Zootaxa 1668:395–411Google Scholar
  45. Nakano S, Fujimoto M, Sugimoto N (1999) Nucleic acid duplex stability: influence of base composition on cation effects. Nucleic Acids Res 27:2957–2965CrossRefPubMedGoogle Scholar
  46. Nyffeler M (1999) Prey selection of spiders in the field. J Arachn 27:317–324Google Scholar
  47. Payton ME, Greenstone MH, Schenker N (2003) Overlapping confidence intervals or standard error intervals: what do they mean in terms of statistical significance? J Insect Sci 3:34PubMedGoogle Scholar
  48. Pérez J, Infante F, Vega FE (2005) Does the coffee berry borer (Coleoptera: Scolytidae) have mutualistic fungi? Ann Entomol Soc Am 98:483–490CrossRefGoogle Scholar
  49. Perfecto I, Rice RA, Greenberg R, van der Voort ME (1996) Shade coffee: a disappearing refuge for biodiversity. Shade coffee plantations can contain as much biodiversity as forest habitats. Bioscience 46:598–608CrossRefGoogle Scholar
  50. Perfecto I, Vandermeer J, Hanson P, Cartin V (1997) Arthropod biodiversity loss and the transformation of a tropical agro-ecosystem. Biodivers Conserv 6:935–945CrossRefGoogle Scholar
  51. Pfannenstiel RS (2008) Spider predators of lepidopteran eggs in south Texas field crops. Biol Control 46:202–208CrossRefGoogle Scholar
  52. Pitkin BR (1976) A revision of the Indian species of Haplothrips and related genera (Thysanoptera: Phlaeothripidae). Bull Br Mus Nat Hist 34:223–280Google Scholar
  53. Priesner H (1960) A monograph of the Thysanoptera of the Egyptian desserts. Publications de L'institut du Desert D'Egypte, Cairo, EgyptGoogle Scholar
  54. Priesner H (1964) Ordnung Thysanoptera (Fransenflügler, Thripse). Bestimmungsbcher zur Bodenfauna Europas, Volume 2. Akademie-Verlag, Berlin, GermanyGoogle Scholar
  55. Richter A, Klein AM, Tscharntke T, Tylianakis JM (2007) Abandonement of coffee agroforests increases insect abundance and diversity. Agrof Syst 69:175–182CrossRefGoogle Scholar
  56. SAS Institute (1999) SAS/Stat user's guide. SAS Institute, Cary, NCGoogle Scholar
  57. Sheppard SK, Harwood JD (2005) Advances in molecular ecology: tracking trophic links through predator–prey food-webs. Funct Ecol 19:751–762CrossRefGoogle Scholar
  58. Sunderland KD, Axelsen JA, Dromph K, Freier B, Hemptinne JL, Holst NH, Mols PJM, Petersen MK, Powell W, Ruggle P, Triltsch H, Winder L (1997) Pest control by a community of natural enemies. Acta Jutlandica 72:271–326Google Scholar
  59. Symondson WOC (2002) Molecular identification of prey in predator diets. Mol Ecol 11:627–641CrossRefPubMedGoogle Scholar
  60. Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594CrossRefPubMedGoogle Scholar
  61. Teodoro A, Klein AM, Tscharntke T (2008) Environmentally mediated coffee pest densities in relation to agroforestry managements, using hierarchical partitioning analyses. Agri Ecosyst Environ 125:120–126CrossRefGoogle Scholar
  62. Traugott M, Bell JR, Broad GR, Powell W, Van Veen JF, Vollhardt IMG, Symondson WOC (2008) Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community. Mol Ecol 17:3928–3938CrossRefPubMedGoogle Scholar
  63. Tscharntke T, Bommarco R, Clough Y, Crist TO, Kleijn D, Rand TA, Tylianakis JM, van Nouhuys S, Vidal S (2007) Conservation biological control and enemy diversity on a landscape scale. Biol Control 43:294–309CrossRefGoogle Scholar
  64. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874CrossRefGoogle Scholar
  65. Vega FE, Mercadier G, Damon A, Kirk A (1999) Natural enemies of the coffee berry borer Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) in Togo and Côte d'Ivoire, and other insects associated with coffee beans. Afr Entomol 7:243–248Google Scholar
  66. Vega FE, Rosenquist E, Collins W (2003) Global project needed to tackle coffee crisis. Nature 435:343CrossRefGoogle Scholar
  67. von Ahsen N, Oellerich M, Schutz E (1999) Application of a thermodynamic nearest-neighbor model to estimate nucleic acid stability and optimize probe design: prediction of melting points of multiple mutations of apolipoprotein B-3500 and factor V with a hybridization probe genotyping assay on the LightCycler. Clin Chem 45:2094–2101Google Scholar
  68. Weber DC, Lundgren JG (2009) Assessing the trophic ecology of the Coccinellidae: their roles as predators and as prey. Biol Control 51:199–214CrossRefGoogle Scholar
  69. Zimmerman EC (1948) Insects of Hawaii. vol. 2, Apterygota to Thysanoptera. University of Hawaii Press, Honolulu, HawaiiGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Juliana Jaramillo
    • 1
    • 2
  • Eric G. Chapman
    • 3
  • Fernando E. Vega
    • 4
  • James D. Harwood
    • 3
  1. 1.International Centre of Insect Physiology and Ecology (ICIPE)NairobiKenya
  2. 2.Institute of Plant Diseases and Plant ProtectionUniversity of HannoverHannoverGermany
  3. 3.Department of EntomologyUniversity of KentuckyLexingtonUSA
  4. 4.Sustainable Perennial Crops Laboratory, US Department of AgricultureAgricultural Research ServiceBeltsvilleUSA

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