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Population genetics of the wheat curl mite (Aceria tosichella Keifer) in Australia: implications for the management of wheat pathogens

Published online by Cambridge University Press:  26 October 2011

A.D. Miller*
Affiliation:
Department of Zoology, The University of Melbourne, Parkville, Victoria, 3010Australia School of Life and Environmental Sciences, Deakin University, Warrnambool, Victoria, 3280Australia
P.A. Umina
Affiliation:
Department of Zoology, The University of Melbourne, Parkville, Victoria, 3010Australia
A.R. Weeks
Affiliation:
Department of Genetics, The University of Melbourne, Parkville, Victoria, 3010Australia
A.A. Hoffmann
Affiliation:
Department of Zoology, The University of Melbourne, Parkville, Victoria, 3010Australia Department of Genetics, The University of Melbourne, Parkville, Victoria, 3010Australia
*
*Author for correspondence Fax: +61 3 8344 2279 E-mail: [email protected]

Abstract

The wheat curl mite (WCM), Aceria tosichella Keifer, is a polyphagous eriophyoid mite and the primary vector of wheat streak mosaic virus (WSMV) and five other viral pathogens in cereals. Previous research using molecular markers and a series of laboratory experiments found A. tosichella in Australia to consist of two genetically distinct lineages, which have broad overlapping distributions and differ in their ability to transmit WSMV under controlled conditions. This pattern of transmission also appears to be apparent in the field, whereby a strong association between WSMV detection and a single WCM lineage has been detected. In this study, we conduct a population genetic analysis and provide information on the genetic structure of the Australian viruliferous WCM lineage. We assessed genetic differentiation of 16 WCM populations using nine microsatellite markers. Strong evidence for extensive gene flow and low genetic structuring throughout the Australian wheatbelt was evident, with an exception for Western Australian and far north Queensland populations that appear to be genetically isolated. The data also indicate genetic patterns consistent with an arrhenotokous parthenogenetic mode of reproduction. Implications of these findings are discussed with reference to the management of WCM and associated cereal pathogens in Australia and overseas.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2011

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References

Amrine, J.W. & Stansy, T.A. (1994) Catalog of the Eriophyoidea (Acarina: Prostigmata) of the World. West Bloomfield, MI, USA, Indira Publishing House.Google Scholar
Anderson, N.H. & Morgan, C.V.G. (1958) Life-histories and habits of the clover mite, Bryobia praetiosa Koch, and the brown mite, B. arborea M. & A., in British Columbia (Acarina: Tetranychidae). The Canadian Entomologist 90, 2342.CrossRefGoogle Scholar
Appel, J.A., Bowden, R.L., Bockus, W.W. & Jardine, D. (2006) Preliminary 2006 Kansas wheat disease loss estimates. Kansas Cooperative Plant Disease Survey Report. Available online at http://www.ksda.gov/includes/document_center/plant_protection/Plant_Disease_Reports/2006KsWheatDiseaseLossEstimates.pdf (accessed September 2011).Google Scholar
Atkinson, T.G. & Grant, M.N. (1967) An evaluation of streak mosaic losses in winter wheat. Phytopathology 57, 188192.Google Scholar
Bell, G. (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. Berkley, CA, USA, University of California Press.Google Scholar
Borodina, E.E., Sukhareva, S.I., Shtein-Margolina, V.A., Evgrafova, L.P. & Krylov, A.V. (1982) Biological hosts of the agent of spot mosaic, a new viral disease of grasses. Mikrobiologicheskii Zhurnal 44, 3841.Google Scholar
Borsa, P. & Kjellberg, F. (1996) Experimental evidence for pseudo-arrhenotoky in Hypothenemus hampei (Coleoptera: Scolytidae). Heredity 76, 130135.CrossRefGoogle Scholar
Bowden, R.L., Brooks, H.L., Peterson, D.E. & Shroyer, J.P. (1991) Be a good neighbor: Control your volunteer wheat. Extension publication MF-1004. Kansas State University Agricultural Experiment Station and Cooperative Extension Service.Google Scholar
Brownstein, M.J., Carpten, J.D. & Smith, J.R. (1996) Modulation of non-templated nucleotide addition by tag DNA polymerase: Primer modifications that facilitate genotyping. Biotechniques 20, 10041106.CrossRefGoogle Scholar
Butlin, R., Schön, J. & Griffiths, H.I. (1998) Introduction to reproductive modes. pp. 124in Martens, K. (Ed.) Sex and Parthenogenesis: Evolutionary Ecology of Reproductive Modes in Non-marine Ostracods. Leiden, The Netherlands, Backhuys Publishers.Google Scholar
Capinera, J.L. (2008) Encyclopedia of Entomology. 2nd edn.Dordrecht, The Netherlands, Springer.CrossRefGoogle Scholar
Carew, M., Schiffer, M., Umina, P., Weeks, A. & Hoffmann, A. (2009) Molecular markers indicate that the wheat curl mite, Aceria tosichella Keifer, may represent a species complex in Australia. Bulletin of Entomological Research, 99(5), 479486.CrossRefGoogle ScholarPubMed
Carew, M.E., Goodisman, M.A.D. & Hoffmann, A.A. (2004) Species status and population genetic structure of grapevine eriophyoid mites. Entomologia Experimentalis et Applicata 111, 8796.CrossRefGoogle Scholar
Christian, M.L. & Willis, W.G. (1993) Survival of wheat streak mosaic-virus in grass hosts in Kansas from wheat harvest to fall wheat emergence. Plant Disease 77, 239242.CrossRefGoogle Scholar
Connin, R.V. (1956) The host range of the wheat curl mite, vector of wheat streak mosaic. Journal of Economic Entomology 49, 14.CrossRefGoogle Scholar
Coutts, B.A., Strickland, G.R., Kehoe, M.A., Severtson, D.L. & Jones, R.A.C. (2008) The epidemiology of wheat streak mosaic virus in Australia: case histories, gradients, mite vectors, and alternative hosts. Australian Journal of Agricultural Research 59, 844853.CrossRefGoogle Scholar
Crawford, N.G. (2010) SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources 10, 556557.CrossRefGoogle ScholarPubMed
Daly, J.C. & Gregg, P. (1985) Genetic variation in Heliothis in Australia: species identification and gene flow in the two pest species H. armigera (Hubner) and H. punctigera Wallengren (Lepidoptera: Noctuidae). Bulletin of Entomological Research 75, 169184.CrossRefGoogle Scholar
de Lillo, E. & Skoracka, A. (2010) What's “cool” on eriophyoid mites? Experimental and Applied Acarology 51, 330.CrossRefGoogle ScholarPubMed
del Rosario, M.S. & Sill, W.H. (1958) A method of rearing large colonies of an Eriophyid mite, Aceria tulipae (Keifer), in pure culture from single eggs or adults. Journal of Economic Entomology 51, 303306.CrossRefGoogle Scholar
del Rosario, M.S. & Sill, W.H. (1965) Physiological strains of Acreia tulipae (K.) and their relationships to the transmission of the wheat streak mosaic virus. Phytopathology 55, 11681175.Google Scholar
Denholm, I., Sawicki, M. & Farnham, A.W. (1985) Factors affecting resistance to insecticides in house-flies, Musca domestica L. (Diptera: Muscidae). IV. The population biology of flies on animal farms in south-eastern England and its implications for the management of resistance. Bulletin of Entomological Research 75, 143158.CrossRefGoogle Scholar
Dwyer, G.I., Gibbs, M.J., Gibbs, A.J. & Jones, R.A.C. (2007) Wheat streak mosaic virus in Australia: Relationship to isolates from the Pacific Northwest of the USA and its dispersion via seed transmission. Plant Disease 91, 164170.CrossRefGoogle ScholarPubMed
Ellis, M.H., Rebetzke, G.J. & Chu, P. (2003a) First report of Wheat streak mosaic virus in Australia. Plant Pathology 52, 808808.CrossRefGoogle Scholar
Ellis, M.H., Rebetzke, G.J., Mago, R. & Chu, P. (2003b) First report of Wheat streak mosaic virus in Australia. Australasian Plant Pathology 32, 551553.CrossRefGoogle Scholar
Endersby, N.M., McKechnie, S.W., Ridland, P.M. & Weeks, A.R. (2006) Microsatellites reveal a lack of structure in Australian populations of the diamondback moth, Plutella xylostella (L.). Molecular Ecology 15, 107118.CrossRefGoogle ScholarPubMed
Endersby, N.M., Ridland, P.M. & Hoffmann, A.A. (2008) The effects of local selection versus dispersal on insecticide resistance patterns: longitudinal evidence from diamondback moth (Plutella xylostella (Lepidoptera: Plutellidae)) in Australia evolving resistance to pyrethroids. Bulletin of Entomological Research 98, 145157.CrossRefGoogle ScholarPubMed
Frantz, A.C., Cellina, S., Krier, A., Schley, L. & Burke, T. (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? Journal of Applied Ecology 46, 493505.CrossRefGoogle Scholar
French, R. & Stenger, D.C. (2003) Evolution of wheat streak mosaic virus: Dynamics of population growth within plants may explain limited variation. Annual Review of Phytopathology 41, 199214.CrossRefGoogle ScholarPubMed
Frost, W.E. (1995) The ecology of cereal rust mite Abacarus hystrix (Nalepa) in irrigated perennial dairy pastures in South Australia. PhD thesis, The University of Adelaide, Adelaide, Australia.Google Scholar
Frost, W.E. & Ridland, P.M. (1996) Grasses. pp. 619629in Lindquist, E.E., Sabelis, M.W. & Bruin, J. (Eds) Eriophyoid Mites – Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier Science.CrossRefGoogle Scholar
Gibson, W.W. & Painter, R.H. (1957) Transportation by aphids of the wheat curl mite, Aceria tulipae (K.), a vector of the wheat streak mosaic virus. Journal of the Kansas Entomological Society 30, 147153.Google Scholar
Goudet, J. (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485486.CrossRefGoogle Scholar
Guillot, G. (2008) Inference of structure in subdivided populations at low levels of genetic differentiation-the correlated allele frequencies model revisited. Bioinformatics 24, 22222228.CrossRefGoogle ScholarPubMed
Guillot, G. (2009) On the inference of spatial structure from population genetics data. Bioinformatics 25, 17961801.CrossRefGoogle ScholarPubMed
Guillot, G. & Santos, F. (2009) A computer program to simulate multilocus genotype data with spatially autocorrelated allele frequencies. Molecular Ecology Resources 9, 11121120.CrossRefGoogle ScholarPubMed
Guillot, G., Estoup, A., Mortier, F. & Cosson, J.F. (2005) A spatial statistical model for landscape genetics. Genetics 170, 12611280.CrossRefGoogle ScholarPubMed
Halliday, R.B. & Knihinicki, D.K. (2004) The occurrence of Aceria tulipae (Keifer) and Aceria tosichella Keifer in Australia (Acari : Eriophyidae). International Journal of Acarology 30, 113118.CrossRefGoogle Scholar
Harvey, T.L. & Martin, T.J. (1988) Sticky tape method to measure cultivar effect on wheat curl mite population in wheat spike. Journal of Economic Entomology 81, 731734.CrossRefGoogle Scholar
Harvey, T.L., Seifers, D.L., Martin, T.J., Brown-Guedira, G. & Gill, B.S. (1999) Survival of wheat curl mites on different sources of resistance in wheat. Crop Science 39, 18871889.CrossRefGoogle Scholar
Harvey, T.L., Martin, T.J. & Seifers, D.L. (2000) Effect of nonviruliferous wheat curl mites on yield of winter wheat. Journal of Agricultural and Urban Entomology 17, 913.Google Scholar
Harvey, T.L., Seifers, D.L. & Martin, T.J. (2001) Host range differences between two strains of wheat curl mites (Acari: Eriophyidae). Journal of Agricultural and Urban Entomology 18, 3541.Google Scholar
Harvey, T.L., Martin, T.J. & Seifers, D.L. (2002) Wheat yield reduction due to wheat curl mite (Acari: Eriophyidae) infestations. Journal of Agricultural and Urban Entomology 19, 913.Google Scholar
Helle, W. & Sabelis, M.W. (Eds) (1985) Spider Mites: Their Biology, Natural Enemies and Control, vol. 1A (World Crop Pests). Amsterdam, The Netherlands, Elsevier.Google Scholar
Helle, W. & Wysoki, M. (1983) The chromosomes and sex-determination of some actinotrichid taxa (Acari), with special reference to Eriophyidae. International Journal of Acarology 9, 6771.CrossRefGoogle Scholar
Helle, W. & Wysoki, M. (1996) Arrhenotokous parthenogenesis. pp. 169–17 in Lindquist, E.E., Sabelis, M.W. & Bruin, J. (Eds) Eriophyoid Mites: Their Biology, Natural Enemies and Control, vol. 2. Amsterdam, The Netherlands, Elsevier.CrossRefGoogle Scholar
Hoffmann, A.A., Reynolds, K.T., Nash, M.A. & Weeks, A.R. (2008) A high incidence of parthenogenesis in agricultural pests. Proceedings of the Royal Society, Series B:Biological Sciences 275, 24732481.Google ScholarPubMed
Huelsenbeck, J.P. & Andolfatto, P. (2007) Inference of population structure under a Dirichlet process prior. Genetics 175, 17871802.CrossRefGoogle Scholar
Jiang, W., Garrett, K.A., Peterson, D.E., Harvey, T.L., Bowden, R.L. & Fang, L. (2005) The window of risk for emigration of Wheat streak mosaic virus varies with host eradication method. Plant Disease 89, 853858.CrossRefGoogle ScholarPubMed
Jost, l. (2008) Gst and its relatives do not measure differentiation. Molecular Ecology 17, 40154026.CrossRefGoogle Scholar
Lanoiselet, V.M., Hind-Lanoiselet, T.L. & Murray, G.M. (2008) Studies on the seed transmission of Wheat streak mosaic virus. Australasian Plant Pathology 37, 584588.CrossRefGoogle Scholar
Lester, L.J. & Selander, R.K. (1979) Population genetics of haplodiploid insects. Genetics 92, 13291345.CrossRefGoogle ScholarPubMed
Linquist, E.E. & Oldfield, G.N. (1996) Evolution of Eriophyoid Mites in Relation to their Host Plants. pp. 277300in Lindquist, E.E., Sabelis, M.W. & Bruin, J. (Eds) Eriophyoid Mites: Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier.CrossRefGoogle Scholar
Lindquist, E.E., Sabelis, M.W. & Bruin, J. (Eds) (1996) Eriophyoid Mites: Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier.Google Scholar
Liu, J., Lee, E.A., Sears, M.K. & Schaafsma, A.W. (2005) Wheat curl mite (Acari: Eriophyidae) dispersal and its relationship with kernel red streaking in maize. Journal of Economic Entomology 98, 15801586.CrossRefGoogle ScholarPubMed
Marshall, V.G. & Clayton, M.R. (2004) Biology and phenology of Cecidophyopsis psilaspis (Acari: Eriophyidae) on Pacific yew (Taxaceae). Canadian Entomologist 136, 695710.CrossRefGoogle Scholar
Mathys, G. (1957) Contribution a la connaissance de la systematique et de la biologie du genre Bryobia en Suisse romande. Bulletin de la Societe Entomologique Suisse 30, 190284.Google Scholar
Maynard Smith, J. (1978) The Evolution of Sex. Cambridge University Press, Cambridge.Google Scholar
Michalska, K., Skoracka, A., Navia, D. & Amrine, J.W. (2010) Behavioural studies on eriophyoid mites: an overview. Experimental and Applied Acarology 51, 3159.CrossRefGoogle ScholarPubMed
Murray, G. (2006) Update on wheat streak mosaic virus. Plant disease notes. New South Wales Department of Primary Industries, Australia.Google Scholar
Murray, G. & Wratten, K. (2005) Wheat streak mosaic virus. Plant disease notes. New South Wales Department of Primary Industries, Australia.Google Scholar
Nault, L.R. & Styer, W.E. (1969) The dispersal of Aceria tulipae and three other grass-infesting eriophyoid mites in Ohio. Annals of the Entomological Society of America 62, 14461455.CrossRefGoogle Scholar
Nyvall, R.F. (1999) Field Ccrop Diseases. 3rd edn.Ames, IA, USA, Iowa State University Press.Google Scholar
Oldfield, G.N., Hobza, R.F. & Wilson, N.S. (1970) Discovery and characterization of spermatophores in the Eriophyoidea (Acari). Annals of the Entomological Journal of America 63, 520526.CrossRefGoogle Scholar
Orlob, G.B. (1966) Feeding and transmission characteristics of Aceria tulipae Keifer as vector of wheat streak mosaic virus. Phytopathologische Zeitschrift 55, 218238.CrossRefGoogle Scholar
Ozman, S.K. & Goolsby, J.A. (2005) Biology and phenology of the eriophyid mite, Floracarus perrepae, on its native host in Australia, Old World climbing fern, Lygodium microphyllum. Experimental and Applied Acarology 35, 197213.CrossRefGoogle ScholarPubMed
Park, S.D.E. (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. PhD thesis. University of Dublin, Dublin, Ireland.Google Scholar
Peakall, R. & Smouse, P.E. (2006) GENALEX 6: genetic analysis in Excel. Population genetics software for teaching and research. Molecular Ecology Notes 6, 288295.CrossRefGoogle Scholar
Raymond, M. & Rousset, F. (1995) An exact test for population differentiation. Evolution 49, 12801283.CrossRefGoogle ScholarPubMed
Raymond, M., Callaghan, A., Fort, P. & Pasteur, N. (1991) Worldwide migration of amplified insecticide resistance genes in mosquitos. Nature 350, 151153.CrossRefGoogle Scholar
Robinson, M.T. & Hoffmann, A.A. (2000) Additional tests on the effects of pesticides on cryptic species of blue oat mite (Penthaleus spp.) and the redlegged earth mite (Halotydeus destructor). Australian Journal of Experimental Agriculture 40, 671678.CrossRefGoogle Scholar
Rousset, F. (1997) Genetic differentiation and estimation of gene ßow from F-statistics under isolation by distance. Genetics 145, 12191228.CrossRefGoogle Scholar
Rozen, S. & Skaletsky, H.J. (2000) Primer3 on the www for general users and for biologists programmers. pp. 365386in Krawetz, S. & Misener, S. (Eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ, USA, Humana Press.Google Scholar
Rugman-Jones, P.F., Weeks, A.R., Hoddle, M.S. & Stouthamer, R. (2005) Isolation and characterization of microsatellite loci in the avocado thrips Scirtothrips perseae (Thysanoptera: Thripidae). Molecular Ecology Notes 5, 644646.CrossRefGoogle Scholar
Sabelis, M.W. & Bruin, J. (1996) Evolutionary ecology: lifehistory patterns, food plant choice and dispersal. pp. 184201in Lindquist, M.W., Sabelis, M.W. & Bruin, J. (Eds) Eriophyoid Mites: Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands, Elsevier.Google Scholar
Sanchez-Sanchez, H., Henry, M., Cardenas-Soriano, E. & Alvizo-Villasana, H.F. (2001) Identification of wheat streak mosaic virus and its vector Aceria tosichella in Mexico. Plant Disease 85, 1317.CrossRefGoogle ScholarPubMed
Schwartz, M.K. & McKelvey, K.S. (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conservation Genetics 10, 441452.CrossRefGoogle Scholar
Schiffer, M., Umina, P., Carew, M., Hoffmann, A., Rodoni, B. & Miller, A. (2009) The distribution of wheat curl mite (Aceria tosichella Keifer) lineages in Australia and their potential to transmit wheat streak mosaic virus. Annals of Applied Biology 155, 371379.CrossRefGoogle Scholar
Seifers, D.L., Harvey, T.L., Martin, T.J. & Jensen, S.G. (1997) Identification of the wheat curl mite as the vector of the high plains virus of corn and wheat. Plant Disease 81, 11611166.CrossRefGoogle Scholar
Seifers, D.L., Martin, T.J., Harvey, T.L., Fellers, J.P. & Michaudm, J.P. (2009) Identification of the wheat curl mite as the vector of triticum mosaic virus. Plant Disease 93, 2529.CrossRefGoogle ScholarPubMed
Skoracka, A. & Kuczynski, L. (2004) Demography of the cereal rust mite Abacarus hystrix (Acari : Eriophyoidea) on quack grass. Experimental and Applied Acarology 32, 231242.CrossRefGoogle ScholarPubMed
Skoracka, A. & Kuczynski, L. (2006) Infestation parameters and morphological variation of the wheat curl mite Aceria tosichella Keifer (Acari: Eriophyoidea). pp. 330339in Gabrys, G. & Ignatowicz, S. (Eds) Advances in Polish Acarology. Warszawa, Poland, Wydawnictwo SGGW.Google Scholar
Slatkin, M. (1987) Gene flow and the geographic structure of natural populations. Science 236, 787792.CrossRefGoogle ScholarPubMed
Slykhuis, J.T. (1955) Aceria tulipae Keifer (Acarina, eriophyidae) in relation to the spread of wheat streak mosaic. Phytopathology 45, 116128.Google Scholar
Slykhuis, J.T. (1956) Wheat spot mosaic, caused by a mite transmitted virus associated with wheat streat mosaic. Phytopathology 46, 682687.Google Scholar
Slykhuis, J.T. (1976) Virus and virus like diseases of cereal crops. Annual Review of Phytopathology 14, 189210.CrossRefGoogle Scholar
Somsen, H.W. & Sill, W.H. Jr. (1970) The wheat curl mite, Aceria tulipae Keifer, in relation to epidemiology and control of wheat streat mosaic. Research Publication 162. Agricultural Experiment Station, Kansas State University of Agriculture and Applied Science Manhattan, 124.Google Scholar
Staples, R. & Allington, W.B. (1956) Streak of wheat in Nebraska and its control. University of Nebraska College of Agriculture Research Bulletin 178, 141.Google Scholar
Staples, R. & Allington, W.B. (1959) The efficiency of sticky traps in sampling population eriophyid mite Aceria tulipae (K.), vector of the wheat streak mosaic virus. Annals of the Entomological Journal of America 52, 159164.CrossRefGoogle Scholar
Sternlicht, M. & Goldenberg, S. (1971) Fertilization, sex ratio and post embryonic stages and the citrus bud mite Aceria sheldoni (Ewing) (Acari:Eriophyidae). Bulletin of Entomological Research 60, 391397.CrossRefGoogle Scholar
Thomas, J.A. & Hein, G.L. (2003) Influence of volunteer wheat plant condition on movement of the wheat curl mite, Aceria tosichella, in winter wheat. Experimental and Applied Acarology 31, 253268.CrossRefGoogle ScholarPubMed
Thomas, J.B., Conner, R.L. & Graf, R.J. (2004) Comparison of different sources of vector resistance for controlling wheat streak mosaic in winter wheat. Crop Science 44, 125126.CrossRefGoogle Scholar
Umina, P.A. & Hoffmann, A.A. (1999) Tolerance of cryptic species of blue oat mites (Penthaleus spp.) and the redlegged earth mite (Halotydeus destructor) to pesticides. Australian Journal of Experimental Agriculture 39, 621628.CrossRefGoogle Scholar
Weeks, A.R. & Hoffmann, A.A. (1999) The biology of Penthaleus species in southeastern Australia. Entomologia Experimentalis et Applicata 92, 179189.CrossRefGoogle Scholar
Weir, B. & Cockerham, C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 13581370.Google ScholarPubMed
Wrensch, D.L. & Ebbert, M.A. (1993) Evolution and Diversity of Sex Ratio in Insects and Mites. New York. USA, Chapman & Hall.CrossRefGoogle Scholar
Zane, L., Bargelloni, L. & Patarnello, T. (2002) Strategies for microsatellite isolation: a review. Molecular Ecology 11, 116.CrossRefGoogle ScholarPubMed