Abstract
Competitive displacement is considered the most severe consequence of interspecific competition; if a superior competitor invades the habitat of an inferior species, the inferior species will be displaced. Most displacements previously reported among arthropods were caused by exotic species. The lack of investigation of displacement among native species may be due to their apparently harmonious coexistence, even if it is equivalent to an outcome of interspecific association. A seasonal change in the species composition of spider mites, from Panonychus ulmi to Tetranychus urticae, is observed in apple trees worldwide. Previous laboratory experiments have revealed amensal effects of T. urticae on P. ulmi via their webs. Using manipulation experiments in an orchard, we tested whether this seasonal change in species composition occurred as the result of interspecific competition between these spider mites. Invasion by T. urticae prevented an increase in P. ulmi densities throughout the experimental periods. Degree of overlap relative to the independent distribution on a leaf-surface basis (ω S) changed from positive to negative with increasing density of T. urticae. T. urticae invasion drove P. ulmi toward upper leaf surfaces (competitor-free space). The niche adjustment by P. ulmi occurred between leaf surfaces but not among leaves. Our findings show that asymmetrical competition between T. urticae and P. ulmi plays an important role in this unidirectional displacement and that the existence of refuges within a leaf produces the apparently harmonious coexistence of the mites and obscures their negative association.
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References
Belczewski R, Harmsen R (1997) Phylloplane fungi: an extrinsic factor of tetranychid population growth? Exp Appl Acarol 21:463–471
Belczewski R, Harmsen R (2000) The effect of non-pathogenic phylloplane fungi on life-history traits of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 24:257–270
Bonsall MB, Hassell MP (1997) Apparent competition structures ecological assemblages. Nature 388:371–373
Boykin LS, Campbell WV (1984) Wind dispersal of the twospotted spider mite (Acari: Tetranychidae) in North Carolina peanut fields. Environ Entomol 13:221–227
Brown MW, Hogmire HW, Schmitt JJ (1995) Competitive displacement of apple aphid by spirea aphid (Homoptera: Aphididae) on apple as mediated by human activities. Environ Entomol 24:1581–1591
Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5:302–315
Denno RF, McClure MS, Ott JR (1995) Interspecific interaction in phytophagous insects: competition re-examined and resurrected. Annu Rev Entomol 40:297–331
Dyer LA, Letourneau DK (1999) Trophic cascades in a complex terrestrial community. Proc Natl Acad Sci USA 96:5072–5076
Fleschner CA, Badgley ME, Ricker DW, Hall JC (1956) Air drift of spider mites. J Econ Entomol 49:624–627
Foott WH (1962) Competition between two species of mites. I. Experimental results. Can Entomol 94:365–375
Foott WH (1963) Competition between two species of mites. II. Factors influencing intensity. Can Entomol 95:45–57
Furuhashi K, Nishino M (1979) Effects of rainfall for the reproduction of citrus red mite, Panonychus citri McGregor. Bull Shizuoka Pref Citrus Exp Stn 15:29–36
González-Megías A, Gómez JM (2003) Consequences of removing a keystone herbivore for the abundance and diversity of arthropods associated with a cruciferous shrub. Ecol Entomol 28:299–308
Harrison S, Thomas CD, Lewinsohn TM (1995) Testing a metapopulation model of coexistence in the insect community on ragwort (Senecio jacobaea). Am Nat 145:546–562
Holt RD, Kotler BP (1987) Short-term apparent competition. Am Nat 130:412–430
Holt RD, Lawton JH (1993) Apparent competition and enemy-free space in insect host-parasitoid communities. Am Nat 142:623–645
Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520
Iwao S (1977) Analysis of spatial association between two species based on the interspecies mean crowding. Res Popul Ecol 18:243–260
Janssen A, Pallini A, Venzon M, Sabelis MW (1998) Behaviour and indirect interactions in food webs of plant-inhabiting arthropods. Exp Appl Acarol 22:497–521
Jeppson LR, Keifer HH, Baker EW (1975) Mites injurious to economic plants. University of California Press, Berkeley, Calif.
Kennedy GG, Smitley DR (1985) Dispersal. In: Helle W, Sabelis MW (eds) Spider mites: their biology, natural enemies and control, vol 1A. Elsevier, Amsterdam, pp 233–242
Kim D, Lee J (2003) Oviposition model of overwintered adult Tetranychus urticae (Acari: Tetranychidae) and mite phenology on the ground cover in apple orchards. Exp Appl Acarol 31:191–208
Kishimoto H (2002) Species composition and seasonal occurrence of spider mites (Acari: Tetranychidae) and their predators in Japanese pear orchards with different agrochemical spraying programs. Appl Entomol Zool 37:603–615
Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7:69–80
Lawson DS, Nyrop JP, Dennehy TJ (1996) Aerial dispersal of European red mites (Acari: Tetranychidae) in commercial apple orchards. Exp Appl Acarol 20:193–202
Lienk SE, Chapman PJ (1951) Influence of the presence or absence of the European red mite on two spotted spider mite abundance. J Econ Entomol 44:623
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
McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their roles in biological control. Annu Rev Entomol 42:291–321
McMurtry JA, Johnson HG (1966) An ecological study of the spider mite Oligonychus punicae (Hirst) and its natural enemies. Hilgardia 37:363–402
McMurtry JA, Scriven GT (1964) Studies on the feeding, reproduction, and development of Amblyseius hibisci (Acarina: Phytoseiidae) on various food substances. Ann Entomol Soc Am 57:649–655
Morimoto K, Furuichi H, Yano S, Osakabe M (2006) Web mediated interspecific competition among spider mites. J Econ Entomol 99:678–684
Morris RJ, Lewis OT, Godfray HCJ (2004) Experimental evidence for apparent competition in a tropical forest food web. Nature 428:310–313
Orrock JL, Fletcher RJ Jr (2005) Changes in community size affect the outcome of competition. Am Nat 166:107–111
Osakabe M (1988) Relationships between food substances and developmental success in Amblyseius sojaensis Ehara (Acarina: Phytoseiidae). Appl Entomol Zool 23:45–51
Osakabe M, Goka K, Toda S, Shintaku T, Amano H (2005) Significance of habitat type for the genetic population structure of Panonychus citri (Acari: Tetranychidae). Exp Appl Acarol 36:25–40
Putman W (1962) Life history and behaviour of the predacious mite Typhlodromus (T.) caudiglans Schuster (Acarina: Phytoseiidae) in Ontario, with notes on the prey of related species. Can Entomol 94:163–177
Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465
Rodriguez JG (1958) The comparative NPK nutrition of Panonychus ulmi (Koch) and Tetranychus telarius (L.) on apple trees. J Econ Entomol 51:369–373
Sabelis MW, Dicke M (1985) Long-range dispersal and searching behaviour. In: Helle W, Sabelis MW (eds) Spider mites. Their biology, natural enemies and control, vol 1B. Elsevier, Amsterdam, Oxford, New York, Tokyo, pp 141–160
Saito Y (1979) Study on spinning behaviour of spider mites. III.Responses of mites to webbing residues and their preferences for particular physical conditions of leaf surfaces (Acarina: Tetranychidae). Jpn J Appl Entomol Zool 23:82–91
Shorrocks B, Rosewell J, Edwards K (1984) Interspecific competition is not a major organizing force in many insect communities. Nature 310:310–312
Slone DH, Croft BA (1998) Spatial aggregation of apple mites (Acari: Phytoseiidae, Stigmaeidae, Tetranychidae) as measured by a binomial model: effects of life stage, reproduction, competition, and predation. Environ Entomol 27:918–925
Slone DH, Croft BA (2001) Species association among predaceous and phytophagous apple mites (Acari: Eriophyidae, Phytoseiidae, Stigmaeidae, Tetranychidae). Exp Appl Acarol 25:109–126
Sokal RR, Rohlf FJ (2000) Biometry, 3rd edn. Freeman, New York
Stewart AA (1996) Interspecific competition reinstated as an important force structuring insect herbivore communities. Trees 11:233–234
Tanaka M, Inoue K (1970) Fundamental studies on the utilization of natural enemies in citrus groves in Japan. II. The method of prediction of outbreaks of the citrus red mite, Panonychus citri (McG.). Bull Hort Res Sta Jpn Ser D 6:1–40
Toyoshima S (2003) A candidate of predatory phytoseiid mites (Acari: Phytoseiidae) for the control of the European red mite, Panonychus ulmi (Koch), (Acari: Tetranychidae) in Japanese apple orchards. Appl Entomol Zool 38:387–391
Tsagkarakou A, Navajas M, Lagnel J, Pasteur N (1997) Population structure in the spider mite Tetranychus urticae (Acari: Tetranychidae) from Crete based on multiple allozymes. Heredity 78:84–92
van Veen FJF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu Rev Entomol 51:187–208
van Veen FJF, van Holland PD, Godfray HCJ (2005) Stable coexistence in insect communities due to density- and trait-mediated indirect effects. Ecology 86:1382–1389
Acknowledgements
This study was partially supported by the 21st Century Centers of Excellence Program of Innovative Food and Environmental Studies Pioneered by Entomomimetic Sciences at Kyoto University. We thank Mr S. Abe, Ms M. Fukaya and Mr H. Sato of the Akita Fruit-Tree Experiment Station for kind help and encouragement.
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Communicated by Stefan Scheu.
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Osakabe, M., Hongo, K., Funayama, K. et al. Amensalism via webs causes unidirectional shifts of dominance in spider mite communities. Oecologia 150, 496–505 (2006). https://doi.org/10.1007/s00442-006-0560-7
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DOI: https://doi.org/10.1007/s00442-006-0560-7