Abstract
Dispersal can be an essential factor affecting the biological control of pests. Tetranychus urticae Koch (Acari: Tetranychidae) is a cosmopolitan and polyphagous species that may reach the pest status in many cropping systems including clementine orchards, where it may be found both in the trees and the associated flora. In a previous study, we demonstrated that the use of a ground cover of Festuca arundinacea Schreber (Poaceae) offered a better regulation of T. urticae populations than traditional alternatives (bare soil, multifloral wild cover). Therefore, we decided to study the ambulatory dispersal of mites crawling up and down tree trunks in a clementine mandarin orchard grown in association with a F. arundinacea cover for one season. The highest ambulatory migration rate was upward from the cover to the canopy. Multivariate regressions showed that the dynamics of T. urticae populations in the trees was strongly related to that of Phytoseiidae mites, their main natural predators. Surprisingly, canopy populations were not related to those on the ground cover or to those dispersing from it. When T. urticae individuals collected from the ground cover, the tree trunk, and the canopy were subjected to molecular analyses, the optimal number of genetic clusters (demes) was two. One cluster grouped individuals dispersed from the ground cover (e.g. collected on tree trunks) and 27.5 % of individuals collected in the ground cover. The second cluster grouped all the individuals collected from trees and 72.5 % of those collected in the cover. Interestingly, none of the individuals collected from the tree canopies was grouped with the first deme. This result may be taken as indicative that grass-adapted T. urticae individuals are unable to satisfactorily colonize and establish on the trees and provides evidence that host adaptation can hamper dispersal and establishment of the ground cover deme on trees, contributing to a better natural regulation of this pest species in citrus.
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Abad-Moyano R, Pina T, Dembilio O, Ferragut F, Urbaneja A (2009) Survey of natural enemies of spider mites (Acari: Tetranychidae) in citrus orchards in Eastern of Spain. Exp Appl Acarol 47:49–61. doi:10.1007/s10493-008-9193-3
Agrawal AA, Vala F, Sabelis MW (2002) Induction of preference and performance after acclimation to novel hosts in a phytophagous spider mite: adaptive plasticity? Am Nat 159:553–565. doi:10.1086/339463
Aguilar-Fenollosa E, Ibáñez-Gual MV, Pascual-Ruiz S, Hurtado M, Jacas JA (2011a) Effect of ground-cover management on spider mites and their phytoseiid natural enemies in clementine mandarin orchards (I): bottom-up regulation mechanisms. Biol Control 59:158–170. doi:10.1016/j.biocontrol.2011.06.013
Aguilar-Fenollosa E, Ibáñez-Gual MV, Pascual-Ruiz S, Hurtado M, Jacas JA (2011b) Effect of ground-cover management on spider mites and their phytoseiid natural enemies in clementine mandarin orchards (II): top-down regulation mechanisms. Biol Control 59:171–179. doi:10.1016/j.biocontrol.2011.06.012
Aguilar-Fenollosa E, Pascual-Ruiz S, Hurtado-Ruiz M, Jacas JA (2011c) Efficacy and economics of ground cover management as a conservation biological control strategy against Tetranychus urticae in clementine mandarin orchards. Crop Prot 30:1328–1333. doi:10.1016/j.cropro.2011.05.011
Aguilar-Fenollosa E, Pina T, Gómez-Martínez MA, Hurtado MA, Jacas JA (2012) Does host adaptation of Tetranychus urticae populations in clementine orchards with a Festuca arundinacea cover contribute to a better natural regulation of this pest mite? Entomol Exp Appl 144:181–190. doi:10.1111/j.1570-7458.2012.01276.x
Agut B, Gamir J, Jacas JA, Hurtado M, Flors V (2014) Different metabolic and genetic responses in citrus may explain relative susceptibility to Tetranychus urticae. Pest Manag Sci 70:1728–1741. doi:10.1002/ps.3718
Agut B, Gamir J, Jaques JA, Flors V (2015) Tetranychus urticae-triggered responses promote genotype-dependent conspecific repellence or attractiveness in citrus. New Phytol 207:790–804. doi:10.1111/nph.13357
Akaike H (1973) Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika 60:255–265. doi:10.1093/biomet/60.2.255
Alonzo H (2002) State-dependent habitat selection games between predators and prey: the importance of behavioral interactions and expected lifetime reproductive success. Evol Ecol Res 4:759–778
Bailly X, Migeon A, Navajas M (2004) Analysis of microsatellite variation in the spider mite pest Tetranychus turkestani (Acari: Tetranychidae) reveals population genetic structure and raises questions about ecological factors. Biol J Linnean Soc 82:69–78. doi:10.1111/j.1095-8312.2004.00316.x
Begon M, Harper JL, Townsend CR (1996) Ecology: individuals, populations and communities. Blackwell Science Ltd., Oxford
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows™ pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Montpellier: Université de Montpellier II
Bolker B, Holyoak M, Krivan V, Rowe L, Schmitz O (2003) Connecting theoretical and empirical studies of traitmediated interactions. Ecology 84:1101–1114. doi:10.1890/0012-9658(2003)084[1101:CTAESO]2.0.CO;2
Broström G, Holmberg H (2011) glmmML: generalized linear models with clustering. R package version 0.81-8
Carbonnelle S, Hance T, Migeon A, Baret P, Cros-Arteil S, Navajas M (2007) Microsatellite markers reveal spatial and genetic structure of Tetranychus urticae (Acari: Tetranychidae) populations along a latitudinal gradient in Europe. Exp Appl Acarol 41:225–241. doi:10.1007/s10493-007-9068-z
Clotuche G, Mailleux AC, Fernandez AA, Deneubourg JL, Detrain C, Hance T (2011) The formation of collective silk balls in the spider mite Tetranychus urticae Koch. PLoS ONE 6:e18854. doi:10.1371/journal.pone.0018854
Clotuche G, Navajas M, Mailleux AC, Hance T (2013) Reaching the ball or missing the flight? Collective dispersal in the two-spotted spider mite Tetranychus urticae. PLoS ONE 8:e77573. doi:10.1371/journal.pone.0077573
Croft BA, Jung C (2001) Phytoseiid dispersal at plant to regional levels: a review with emphasis on management of Neoseiulus fallacis in diverse agroecosystems. Exp Appl Acarol 25:763–784. doi:10.1023/A:1020406404509
Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J, Grbić M, Clarkh RM, Feyereisen R, Van Leeuwen T (2013) A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc Nat Acad Sci PNAS 110:E113–E122. doi:10.1073/pnas.1213214110
Dingle H (1996) Migration. The biology of life on the move. Oxford University Press, Oxford
Dunley JE, Croft BA (1992) Dispersal and gene flow of pesticide resistance traits in phytoseiid and tetranychid mites. Exp Appl Acarol 14:313–326. doi:10.1007/BF01200570
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x
Fellous S, Angot G, Orsucci M, Migeon A, Auger P, Olivieri I, Navajas M (2014) Combining experimental evolution and field population assays to study the evolution of host range breadth. J Evol Biol 27:911–919. doi:10.1111/jeb.12362
Ferragut F, Santonja MC (1989) Taxonomía y distribución de los ácaros del género Tetranychus Dufour 1832 (Acari: Tetranychidae) en España. Bol San Veg Plagas 15:271–281
Fox J, Andronic L, Ash M, Boye T, Calza S, Chang A, et al (2009) Rcmdr: R Commander. R package version 1.5-4
Fry JD (1990) Trade-offs in fitness on different hosts: evidence from a selection experiment with a phytophagous mite. Am Nat 136:569–580. doi:10.1086/285116
Ge C, Sun J-T, Cui Y-N, Hong X-Y (2013) Rapid development of 36 polymorphic microsatellite markers for Tetranychus truncatus by transferring from Tetranychus urticae. Exp Appl Acarol 61:195–2012. doi:10.1007/s10493-013-9684-8
Grafton-Cardwell EE, Granett J, Normington SM (1991) Influence of dispersal from almonds on the population dynamics and acaricide resistance frequencies of spider mites infesting neighboring cotton. Exp Appl Acarol 10:187–212. doi:10.1007/BF01198650
Grbić M, van Leeuwen T, Clark RM, Rombauts S, Rouze P, Grbić V, Osborne EJ et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479:487–492. doi:10.1038/nature10640
Gutiérrez J (1985) Mounting techniques. In: Helle W, Sabelis M (eds) Spider mites: their biology, natural enemies and control, vol 1A. Elsevier Science Publishers, Amsterdam, pp 351–353
Hardman JM, Jensen KI, Franklin JL, Moreau DL (2005) Effects of dispersal, predators (Acari: Phytoseiidae), weather, and ground cover treatments on populations of Tetranychus urticae (Acari: Tetranychidae) in apple orchards. J Econ Entomol 98:862–874. doi:10.1603/0022-0493-98.3.862
Hardman JM, Franklin JL, Bostanian NJ, Thistlewood HMA (2011) Effect of the width of the herbicide strip on mite dynamics in apple orchards. Exp Appl Acarol 53:215–234. doi:10.1007/s10493-010-9397-1
Ilias A, Vontas J, Tsagkarakou A (2014) Global distribution and origin of target site insecticide resistance mutations in Tetranychus urticae. Insect Biochem Molec Biol 48:17–28. doi:10.1016/j.ibmb.2014.02.006
Jaques JA, Aguilar-Fenollosa E, Hurtado-Ruiz MA, Pina T (2015) Food web engineering to enhance biological control of T. urticae by phytoseiid mites in citrus. In: Carrillo D, Moraes GJ, Peña JE (eds) Prospects for biological control of plant feeding mites and other harmful organisms. Progress in biological control, vol 19. Springer, Dordrecht, pp 251–269. doi:10.1007/978-3-319-15042-0_10
Kennedy GG, Smitley DR (1985) Dispersal. In: Helle W, Sabelis MW (eds) Spider mites: their biology, natural enemies and control, vol 1A. Elsevier Science Publishers, Amsterdam, pp 233–242
Lee S, Tsao R, Peterson C, Coats JR (1997) Insecticidal activity of monoterpenoids to western corn rootworm (Coleoptera: Chrysomelidae), twospotted spider mite (Acari: Tetranychidae), and house fly (Diptera: Muscidae). J Econ Entomol 90:883–892. doi:10.1093/jee/90.4.883
Li J, Margolies DC (1994) Responses to direct and indirect selection on aerial dispersal behaviour in Tetranychus urticae. Heredity 72:10–22. doi:10.1038/hdy.1994.2
Li T, Chen X-L, Hong XY (2009) Population genetic structure of Tetranychus urticae and its sibling Species species Tetranychus cinnabaribus (Acari: Tetranychidae) in China as inferred from microsatellite data. Ann Entomol Soc Am 102:674–683. doi:10.1603/008.102.0412
Lima SL (2002) Putting predators back into behavioral predator-prey interactions. Trends Ecol Evol 17:70–75. doi:10.1016/S0169-5347(01)02393-X
Luttbeg B, Kerby JL (2005) Are scared prey as good as dead? Trends Ecol Evol 20:416–418. doi:10.1016/j.tree.2005.05.006
Magalhães S, Forbes MR, Skororacka A, Osakabe M, Chevillon C, McCoy KD (2007) Host race formation in the Acari. Exp Appl Acarol 42:225–238. doi:10.1007/s10493-007-9091-0
Margolies DC (1995) Evidence of selection on spider mite dispersal rates in relation to habitat persistence in agroecosystems. Entomol Exp Appl 76:105–108. doi:10.1111/j.1570-7458.1995.tb01950.x
Margolies DC, Kennedy GG (1985) Movement of the twospotted spider mite, Tetranychus urticae, among hosts in a corn-peanut agroecosystem. Entomol Exp Appl 37:55–61. doi:10.1111/j.1570-7458.1985.tb03452.x
Marinosci C, Magalhães S, Macke E, Navajas M, Carbonell D, Devaux C, Olivieri I (2015) Effects of host plant on life-history traits in the polyphagous spider mite Tetranychus urticae. Ecol Evol 5:3151–3158. doi:10.1002/ece3.1554
McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their roles in biological control. Annu Rev Entomol 42:291–321. doi:10.1146/annurev.ento.42.1.291
Nachman G (1988) Regional persistence of locally unstable predator/prey populations. Exp Appl Acarol 5:293–318. doi:10.1007/BF02366099
Navajas MJ, Thistlewood HMA, Lagnel J, Hughes C (1998) Microsatellite sequences are under-represented in two mite genomes. Insect Mol Biol 7:249–256. doi:10.1111/j.1365-2583.1998.00066.x
Navajas M, Tsagkarakov A, Lagnel J, Perrot-Minnot MJ (2000) Genetic differentiation in Tetranychus urticae (Acari: Tetranychidae): polymorphism, host races or sibling species? Exp Appl Acarol 24:365–376. doi:10.1023/A:1006432604611
Navajas M, Perrot-Minnot MJ, Lagnel J, Migeon A, Bourse T, Cornuet JM (2002) Genetic structure of a greenhouse population of the spider mite Tetranychus urticae: spatio-temporal analysis with microsatellite markers. Insect Mol Biol 11:157–165. doi:10.1046/j.1365-2583.2002.00320.x
Nishimura S, Hinomoto N, Takafuji A (2003) Isolation, characterization, inheritance and linkage of microsatellite markers in Tetranychus kanzawai (Acari: Tetranychidae). Exp Appl Acarol 31:93–103. doi:10.1007/s10493-005-0410-z
Pascual-Ruiz S, Aguilar-Fenollosa E, Ibáñez-Gual V, Hurtado-Ruiz MA, Martínez-Ferrer MT, Jacas JA (2014a) Economic threshold for Tetranychus urticae (Acari: Tetranychidae) in clementine mandarins Citrus clementina. Exp Appl Acarol 62:337–362. doi:10.1007/s10493-013-9744-0
Pascual-Ruiz S, Gómez-Martinez MA, Ansaloni T, Segarra-Moragues JG, Sabater-Muñoz B, Jacas JA, Hurtado-Ruiz MA (2014b) Genetic structure of a phytophagous mite species affected by crop practices: the case of Tetranychus urticae in clementine mandarins. Exp Appl Acarol 62:477–498. doi:10.1007/s10493-013-9755-x
Peacor SD, Werner EE (2001) The contribution of trait mediated indirect effects to the net effects of a predator. Proc Nat Acad Sci PNAS 98:3904–3908. doi:10.1073/pnas.071061998
Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? Effects of intimidation and consumption in predator-prey interactions. Ecology 86:501–509. doi:10.1890/04-0719
Price PW (1984) Insect ecology. Wiley, New York
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Relyea RA (2003) How prey respond to combined predators: a review and an empirical test. Ecology 84:1827–1839. doi:10.1890/0012-9658(2003)084[1827:HPRTCP]2.0.CO;2
Rousset F (2008) GENEPOP 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x
Sabater-Muñoz B, Pascual-Ruiz S, Gómez-Martínez MA, Jacas JA, Hurtado MA (2012) Isolation and characterization of polymorphic microsatellite markers in Tetranychus urticae and cross amplification in other Tetranychidae and Phytoseiidae species of economic importance. Exp Appl Acarol 57:37–51. doi:10.1007/s10493-012-9529-x
Sih A (1987) Prey refuges and predator-prey stability. Theor Popul Biol 31:1–12. doi:10.1016/0040-5809(87)90019-0
Smitley DR, Kennedy GG (1988) Aerial dispersal of the two-spotted spider mite (Tetranychus urticae) from field corn. Exp Appl Acarol 5:33–46. doi:10.1007/BF02053815
Strong WB, Slone DH, Croft BA (1999) Hops as a metapopulation landscape for tetranychid phytoseiid interactions: perspectives of intra- and interplant dispersal. Exp Appl Acarol 23:581–597. doi:10.1023/A:1006208218771
Uesugi R, Osakabe MH (2007) Isolation and characterization of microsatellite loci in the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Mol Ecol Notes 7:290–292. doi:10.1111/j.1471-8286.2006.01583.x
Uesugi R, Kunimoto Y, Osakabe M (2009a) The fine-scale genetic structure of the two-spotted spider mite in a commercial greenhouse. Exp Appl Acarol 47:99–109. doi:10.1007/s10493-008-9201-7
Uesugi R, Sasawaki T, Osakabe M (2009b) Evidence of a high level of gene flow among apple trees in Tetranychus urticae. Exp Appl Acarol 49:281–290. doi:10.1007/s10493-009-9267-x
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York. doi:10.1007/978-0-387-21706-2
Walzer A, Moder K, Schausberger P (2009) Spatiotemporal within-plant distribution of the spider mite Tetranychus urticae and associated specialist and generalist predators. Bull Entomol Res 99:457–466. doi:10.1017/S0007485308006494
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. doi:10.2307/2408641
Weldon PJ, Carroll JF, Kramer M, Bedoukian RH, Coleman RE, Bernier UR (2011) Anointing chemicals and hematophagous arthropods: responses by ticks and mosquitoes to Citrus (Rutaceae) peel exudates and monoterpene components. J Chem Ecol 37:348–359. doi:10.1007/s10886-011-9922-7
Wybouw N, Zhurov V, Martel C, Bruinsma KA, Hendrickx F, Grbić V, van Leeuwen T (2015) Adaptation of a polyphagous herbivore to a novel host plant extensively shapes the transcriptome of herbivore and host. Mol Ecol. doi:10.1111/mec.13330
Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer. doi:10.1007/978-0-387-87458-6
Acknowledgments
To M.A. Gómez-Martínez (UJI) for advice on molecular biology techniques. This research was partially funded by the Spanish Plan Nacional R + D (AGL2008-05,287-C04/AGR and AGL2011-30538-C03-01). JGS-M was supported by a “Ramón y Cajal” postdoctoral contract from MICINN.
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Formerly known as J. A. Jacas.
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Aguilar-Fenollosa, E., Rey-Caballero, J., Blasco, J.M. et al. Patterns of ambulatory dispersal in Tetranychus urticae can be associated with host plant specialization. Exp Appl Acarol 68, 1–20 (2016). https://doi.org/10.1007/s10493-015-9969-1
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DOI: https://doi.org/10.1007/s10493-015-9969-1