Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-27T20:01:44.578Z Has data issue: false hasContentIssue false
  • English
  • Français

An analysis of using entomopathogenic nematodes against above-ground pests

Published online by Cambridge University Press:  09 March 2007

S. Arthurs ,
K.M. Heinz  and
J.R. Prasifka
S. Arthurs*
Affiliation:
Biological Control Laboratory, Department of Entomology, Texas A&M University, College Station, TX 77843–2475, USA
K.M. Heinz
Affiliation:
Biological Control Laboratory, Department of Entomology, Texas A&M University, College Station, TX 77843–2475, USA
J.R. Prasifka
Affiliation:
Biological Control Laboratory, Department of Entomology, Texas A&M University, College Station, TX 77843–2475, USA
*
*Present address: USDA-ARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, WA 98951, USA Fax: (509) 454 5646 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Applications of entomopathogenic nematodes in the families Steinernematidae and Heterorhabditidae have traditionally been targeted against soil insects. Nonetheless, research over the last two decades highlights the potential of such agents against above-ground pests under certain circumstances. A general linear model was used to test for patterns in efficacy among 136 published trials with Steinernema carpocapsae Weiser, the most common species applied against foliar and other above-ground pests. The focus was on field and greenhouse assessments, rather than laboratory assays where relevant ecological barriers to infection are typically removed. The model showed differences in nematode treatment efficacy depending on the pests’ target habitat (bore holes > cryptic foliage > exposed foliage) and trial location (greenhouse > field studies). Relative humidity and temperature during and up to 8 h post-application were also predicted to influence rates of nematode infection obtained. Conversely, spray adjuvants (both wetting agents and anti-desiccants) and nematode dosage applied (both concentration and use of consecutive applications 3–4 days apart) did not explain a significant amount of variance in nematode performance. With reference to case studies the model is used to discuss the relative importance of different factors on nematode efficacy and highlight priorities for workers considering using entomopathogenic nematodes to target pests in novel environments.

Type
Research Article
Information
Bulletin of Entomological Research , Volume 94 , Issue 4 , August 2004 , pp. 297 - 306
Copyright
Copyright © Cambridge University Press 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bari, M.A. & Kaya, H.K. (1984) Evaluation of the entomogenous nematode Neoaplectana carpocapsae (= Steinernema feltiae) Weiser (Rhabditida, Steinernematidae) and the bacterium Bacillus thuringiensis Berliner var. kurstaki for suppression of the artichoke plume moth (Lepidoptera, Pterophoridae). Journal of Economic Entomology 77, 225–229.Google Scholar
Baur, M.E., Kaya, H.K., Gaugler, R. & Tabashnik, B. (1997a) Effects of adjuvants on entomopathogenic nematode persistence and efficacy against Plutella xylostella. Biocontrol Science and Technology 7, 513–525.Google Scholar
Baur, M.E., Kaya, H.K. & Tabashnik, B.E. (1997b) Efficacy of a dehydrated steinernematid nematode against black cutworm (Lepidoptera: Noctuidae) and diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology 90, 1200–1206.Google Scholar
Baur, M.E., Kaya, H.K., Tabashnik, B.E. & Chilcutt, C.F. (1998) Suppression of diamondback moth (Lepidoptera: Plutellidae) with an entomopathogenic nematode (Rhabditida: Steinernematidae) and Bacillus thuringiensis Berliner. Journal of Economic Entomology 91, 1089–1095.Google Scholar
Bedding, R.A. & Miller, L.A. (1981) Disinfesting blackcurrant cuttings of Synanthedon tipuliformis, (Lepidoptera, Sesiidae) using the insect parasitic nematode, Neoaplectana bibionis (Nematoda, Steinernematidae). Environmental Entomology 10, 449–453.Google Scholar
Begley, J.W. 1990. Efficacy against insects in habitats other than soil. pp. 215–231 in Gaugler, R. & Kaya, H.K. (Eds) Entomopathogenic nematodes in biological control. Boca Raton, Florida, CRC Press.Google Scholar
Bélair, G., Vincent, C. & Chouinard, G. (1998) Foliar sprays with Steinernema carpocapsae against early season apple pests. Journal of Nematology 30, 599–606.Google Scholar
Bélair, G., Vincent, C., Lemire, S. & Coderre, D. (1999) Laboratory and field assays with entomopathogenic nematodes for the management of oblique banded leafroller Choristoneura rosaceana (Harris) (Tortricidae). Journal of Nematology 31, 684–689.Google Scholar
Ben-Yakir, D., Efron, D., Chen, M. & Glazer, I. (1998) Evaluation of entomopathogenic nematodes for biocontrol of the European corn borer, Ostrinia nubilalis, on sweet corn in Israel. Phytoparasitica 26, 101–108.CrossRefGoogle Scholar
Bong, C.J.F. (1986) Field control of Heliothis zea (Boddie) (Lepidoptera: Noctuidae) using an insect parasitic nematode. Insect Science and its Application 7, 23–25.Google Scholar
Bong, C.J.F. & Sikorowski, P.P. (1983) Use of the DD136 strain of Neoaplectana carpocapsae Weiser (Rhabditida: Steinernematidae) for the control of corn earworm (Lepidoptera: Noctuidae). Journal of Economic Entomology 76, 590–593.Google Scholar
Broadbent, A.B., Olthof, T.H.A. (1995) Foliar application of Steinernema carpocapsae (Rhabditida, Steinernematidae) to control Liriomyza trifolii (Diptera, Agromyzidae) larvae in chrysanthemums. Environmental Entomology 24, 431–435.CrossRefGoogle Scholar
Brown, I.M. & Gaugler, R. (1997) Temperature and humidity influence emergence and survival of entomopathogenic nematodes. Nematologica 43, 363–375.Google Scholar
Cabanillas, H.E., Poinar, G.O. & Raulston, J.R. (1994) Steinernema riobravis n-sp (Rhabditida, Steinernematidae) from Texas. Fundamental and Applied Nematology 17, 123–131.Google Scholar
Campbell, J.F. & Gaugler, R. (1993) Nictation behavior and its ecological implications in the host search strategies of entomopathogenic nematodes (Heterorhabditidae and Steinernematidae). Behaviour 126, 155–169.Google Scholar
Chamberlin, H.C. & Dutky, S.R. (1958) Tests of pathogens for the control of tobacco insects. Journal of Economic Entomology 51, 560CrossRefGoogle Scholar
Copping, L.G. & Menn, J.J. (2000) Biopesticides: a review of their action, applications and efficacy. Pest Management Science 56, 651–676.3.0.CO;2-U>CrossRefGoogle Scholar
Cossentine, J.E., Banham, F.L. & Jensen, L.B. (1990) Efficacy of the nematode Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) against the peachtree borer, Synanthedon exitosa (Lepidoptera: Sesiidae) in peach trees. Journal of the Entomological Society of British Columbia 87, 82–84.Google Scholar
Cross, J.V., Solomon, M.G., Chandler, D., Jarrett, P., Richardson, P.N., Winstanley, D., Bathon, H., Huber, J., Keller, B., Langenbruch, G.A. & Zimmerman, G. (1999) Biocontrol of pests of apples and pears in northern and central Europe: 1. Microbial agents and nematodes. Biocontrol Science and Technology 9, 125–149.CrossRefGoogle Scholar
Deseö, K.V. & Miller, L.A. (1985) Efficacy of entomogenous nematodes, Steinernema spp. against clearwing moths, Synanthedon spp, in north Italian apple orchards. Nematologica 31, 100–108.Google Scholar
Ehlers, R.U. (1996) Current and future use of nematodes in biocontrol: practice and commercial aspects with regard to regulatory policy issues. Biocontrol Science and Technology 6, 303–316.CrossRefGoogle Scholar
Eidt, D.C. & Dunphy, G.B. (1991) Control of spruce budmoth, Zeiraphera canadensis Mut. and Free. in white spruce plantations with entomopathogenic nematodes, Steinernema spp. Canadian Entomologist 123, 379–385.Google Scholar
Fife, J.P., Derksen, R.C., Ozkan, H.E. & Grewal, P.S. (2003) Effects of pressure differentials on the viability and infectivity of entomopathogenic nematodes. Biological Control 27, 65–72.CrossRefGoogle Scholar
Finney, J.R. & Walker, C. (1979) Assessment of a field trial using the DD-136 strain of Neoaplectana sp. for the control of Scolytus scolytus. Journal of Invertebrate Pathology 33, 239–241.CrossRefGoogle Scholar
Forschler, B.T. & Nordin, G.L. (1988) Suppression of carpenterworm, Prionoxystus robiniae (Lepidoptera, Cossidae), with the entomophagous nematodes, Steinernema feltiae and Steinernema bibionis. Journal of the Kansas Entomological Society 61, 396–400.Google Scholar
Friedman, M.J. (1990) Commercial production and development. pp. 153–172 in Gaugler, R. & Kaya, H.K. (eds) Entomopathogenic nematodes in biological control. Boca Raton, Florida, CRC Press.Google Scholar
Fujiie, A. & Yokoyama, T. (1998) Effects of ultraviolet light on the entomopathogenic nematode, Steinernema kushidai and its symbiotic bacterium, Xenorhabdus japonicus. Applied Entomology and Zoology 33, 263–269.Google Scholar
Fuxa, J.R. (1987) Ecological considerations in the use of entomopathogens in IPM. Annual Review of Entomology 32, 225–251.Google Scholar
Gan-Mor, S. & Matthews, G.A. (2003) Recent developments in sprayers for application of biopesticides – an overview. Biosystems Engineering 84, 119–125.CrossRefGoogle Scholar
Gaugler, R. (1988) Ecological considerations in the biological control of soil-inhabiting insects with entomopathogenic nematodes. Agriculture Ecosystems and Environment 24, 351–360.CrossRefGoogle Scholar
Gaugler, R. & Campbell, J.F. (1991) Selection for enhanced host-finding of scarab larvae (Coleoptera, Scarabaeidae) in an entomopathogenic nematode. Environmental Entomology 20, 700–706.Google Scholar
Gaugler, R., Bednarek, A. & Campbell, J.F. (1992) Ultraviolet inactivation of heterorhabditid and steinernematid nematodes. Journal of Invertebrate Pathology 59, 155–160.Google Scholar
Georgis, R. (1990) Formulation and application technology. pp. 173–191 in Gaugler, R. & Kaya, H.K. (eds) Entomopathogenic nematodes in biological control. Boca Raton, Florida, CRC Press.Google Scholar
Georgis, R. & Dunlop, D.B. (1994) Water dispersable granule: a novel formulation for nematode-based bioinsecticides. pp. 31–36Proceedings of the Brighton Crop Protection Conference–pests and diseases, vol. 2. British Crop Protection Council, Farnham, Surrey EnglandGoogle Scholar
Georgis, R., Hague, N.G.M. (1988) Field-evaluation of Steinernema feltiae against the web-spinning larch sawfly Cephalcia lariciphila. Journal of Nematology 20, 317–320.Google Scholar
Georgis, R., Hague, N.G.M. (1991) Nematodes as biological insecticides. Pesticide Outlook 2, 29–32.Google Scholar
Glazer, I. & Navon, A. (1990) Activity and persistence of entomoparasitic nematodes tested against Heliothis armigera (Lepidoptera, Noctuidae). Journal of Economic Entomology 83, 1795–1800.Google Scholar
Glazer, I., Klein, M., Navon, A. & Nakache, Y. (1992) Comparison of efficacy of entomopathogenic nematodes combined with antidesiccants applied by canopy sprays against three cotton pests (Lepidoptera, Noctuidae). Journal of Economic Entomology 85, 1636–1641.Google Scholar
Grewal, P.S., Selvan, S. & Gaugler, R. (1994) Thermal adaptation of entomopathogenic nematodes–niche breadth for infection, establishment, and reproduction. Journal of Thermal Biology 19, 245–253.Google Scholar
Grewal, P.S., Gaugler, R. & Shupe, C. (1996) Rapid changes in thermal sensitivity of entomopathogenic nematodes in response to selection at temperature extremes. Journal of Invertebrate Pathology 68, 65–73.Google Scholar
Hara, A.H., Kaya, H.K., Gaugler, R., LeBeck, L.M. & Mello, C.L. (1993) Entomopathogenic nematodes for biological control of the leafminer, Liriomyza trifolii (Dipt, Agromyzidae). Entomophaga 38, 359–369.Google Scholar
Harris, M.A., Begley, J.W. & Warkentin, D.L. (1990) Liriomyza trifolii (Diptera, Agromyzidae) suppression with foliar applications of Steinernema carpocapsae (Rhabditida, Steinernematidae) and abamectin. Journal of Economic Entomology 83, 2380–2384.Google Scholar
Head, J., Palmer, L.F., Walters, K.F.A. (2002) Development of an integrated control strategy for leafminers in leafy salads with potential for extrapolation to other cropping systems. IOBC/WPRS Bulletin 25, 97–100.Google Scholar
Hominick, W.M., Reid, A.P., Bohan, D.A. & Briscoe, B.R. (1996) Entomopathogenic nematodes: biodiversity, geographical distribution and the convention on biological diversity. Biocontrol Science and Technology 6, 317–331.Google Scholar
Jansson, R.K., Lecrone, S.H. & Gaugler, R. (1993) Field efficacy and persistence of entomopathogenic nematodes (Rhabditida, Steinernematidae, Heterorhabditidae) for control of sweet-potato weevil (Coleoptera, Apionidae) in southern Florida. Journal of Economic Entomology 86, 1055–1063.Google Scholar
Jaques, R.P. (1967) Mortality of five apple insects induced by nematode DD136. Journal of Economic Entomology 60, 741–743.Google Scholar
Kain, D.P. & Agnello, A.M. (1999) Pest status of American plum borer (Lepidoptera: Pyralidae) and fruit tree borer control with synthetic insecticides and entomopathogenic nematodes in New York State. Journal of Economic Entomology 92, 193–200.CrossRefGoogle ScholarPubMed
Kaya, H.K. (1985) Entomogenous nematodes for insect control in IPM systems. pp. 283–302Biological control in agricultural IPM systems Hoy, M.A., Herzog, D.C. (eds) New YorkAcademic Press.Google Scholar
Kaya, H.K. (1990) Soil ecology. pp. 93–115Gaugler., R., Kaya, H.K.Entomopathogenic nematodes in biological control Boca Raton, Florida CRC Press.Google Scholar
Kaya, H.K. (1993) Entomogenous and entomopathogenic nematodes in biological control. pp. 565–591Evans, K., Trudgill, D.L., Webster, J.M. (eds) Plant parasitic nematodes in temperate agriculture Wallingford, Oxon CAB International.Google Scholar
Kaya, H.K. & Brown, L.R. (1986) Field application of entomogenous nematodes for biological control of clear-wing moth borers in alder and sycamore trees. Journal of Arboriculture 12, 150–154.Google Scholar
Kaya, H.K. & Gaugler, R. (1993) Entomopathogenic nematodes. Annual Review of Entomology 38, 181–206.CrossRefGoogle Scholar
Kaya, H.K. & Reardon, R.C. (1982) Evaluation of Neoaplectana carpocapsae for biological control of the western spruce budworm, Choristoneura occidentalis–ineffectiveness and persistence of tank mixes. Journal of Nematology 14, 595–597.Google ScholarPubMed
Kaya, H.K. & Stock, S.P. (1997) Techniques in insect nematology. Manual of techniques in insect pathology pp. 281–324San Diego, California Academic Press.Google Scholar
Kaya, H.K., Hara, A.H. & Reardon, R.C. (1981) Laboratory and field-evaluation of Neoaplectana carpocapsae (Rhabditida, Steinernematidae) against the elm leaf beetle (Coleoptera, Chrysomelidae) and the western spruce budworm (Lepidoptera, Tortricidae). Canadian Entomologist 113, 787–793.Google Scholar
Kaya, H.K., Joos, J.L., Falcon, L.A. & Berlowitz, A. (1984) Suppression of the codling moth (Lepidoptera, Olethreutidae) with the entomogenous nematode, Steinernema feltiae (Rhabditida, Steinernematidae). Journal of Economic Entomology 77, 1240–1244.CrossRefGoogle Scholar
Klein, M.G. (1990) Efficacy against soil-inhabiting insect pests. Entomopathogenic nematodes in biological control 195–214Gaugler, R., Kaya, H.K. (eds) Boca Raton, Florida CRC Press.Google Scholar
Koppenhofer, A.M., Kaya, H.K. & Taormino, S.P. (1995) Infectivity of entomopathogenic nematodes (Rhabditida, Steinernematidae) at different soil depths and moistures. Journal of Invertebrate Pathology 65, 193–199.Google Scholar
Kung, S.P., Gaugler, R. & Kaya, H.K. (1991) Effects of soil-temperature, moisture, and relative-humidity on entomopathogenic nematode persistence. Journal of Invertebrate Pathology 57, 242–249.Google Scholar
Lacey, L.A. & Unruh, T.R. (1998) Entomopathogenic nematodes for control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae): Effect of nematode species, concentration, temperature, and humidity. Biological Control 13, 190–197.CrossRefGoogle Scholar
Legaspi, J.C., Legaspi, B.C. & Saldana, R.R. (2000) Evaluation of Steinernema riobravis (Nematoda: Steinernematidae) against the Mexican rice borer (Lepidoptera: Pyralidae). Journal of Entomological Science 35, 141–149.CrossRefGoogle Scholar
Lello, E.R., Patel, M.N., Matthews, G.A. & Wright, D.J. (1996) Application technology for entomopathogenic nematodes against foliar pests. Crop Protection 15, 567–574.CrossRefGoogle Scholar
Liu, J., Poinar, G.O. & Berry, R.E. (2000) Control of insect pests with entomopathogenic nematodes: the impact of molecular biology and phylogenetic reconstruction. Annual Review of Entomology 45, 287–306.Google Scholar
Macvean, C.M., Brewer, J.W. & Capinera, J.L. (1982) Field-tests of anti-desiccants to extend the infection period of an entomogenous nematode, Neoaplectana carpocapsae (Rhabditida, Steinernematidae), against the Colorado potato beetle (Coleoptera, Chrysomelidae). Journal of Economic Entomology 75, 97–101.Google Scholar
Mason, J.M. & Wright, D.J. (1997) Potential for the control of Plutella xylostella larvae with entomopathogenic nematodes. Journal of Invertebrate Pathology 70, 234–242.CrossRefGoogle Scholar
Mason, J.M., Matthews, G.A. & Wright, D.J. (1998) Screening and selection of adjuvants for the spray application of entomopathogenic nematodes against a foliar pest. Crop Protection 17, 463–470.Google Scholar
Mason, J.M., Matthews, G.A. & Wright, D.J. (1999) Evaluation of spinning disc technology for the application of entomopathogenic nematodes against a foliar pest. Journal of Invertebrate Pathology 73, 282–288.Google Scholar
Miller, L.A. & Bedding, R.A. (1982) Field testing of the insect parasitic nematode, Neoaplectana bibionis [Nematoda, Steinernematidae] against currant borer moth, Synanthedon tipuliformis [Lep, Sesiidae] in blackcurrants. Entomophaga 27, 109–114.Google Scholar
Nachtigall, S. & Dickler, E. (1992) Experiences with field applications of entomoparasitic nematodes for biological control of cryptic living insects in orchards. Acta Phytopathologica et Entomologica Hungarica 27, 485–490.Google Scholar
Neter, J., Kutner, M.H., Nachtsheim, C.J. & Wasserman, W. (1996) Applied linear statistical models 3rd edn. 1408 pp. Boston, McGraw-Hill.Google Scholar
Nickle, W.R. & Shapiro, M. (1994) Effects of eight brighteners as solar-radiation protectants for Steinernema carpocapsae, All strain. Journal of Nematology 26, 782–784.Google Scholar
Nilsson, U. & Gripwall, E. (1999) Influence of application technique on the viability of the biological control agents Verticillium lecanii and Steinernema feltiae. Crop Protection 18, 53–59.Google Scholar
Parrella, M.P. (1987) Biology of Liriomyza. Annual Review of Entomology 32, 201–224.Google Scholar
Poinar, G.O. (1990) Taxonomy and biology of Steinernematidae and Heterorhabditidae. Entomopathogenic nematodes in biological control pp. 23–61Gaugler, R., Kaya, H.K. (eds) Boca Raton, Florida CRC PressGoogle Scholar
Richter, A.R. & Fuxa, J.R. (1990) Effect of Steinernema feltiae on Spodoptera frugipera and Heliothis zea (Lepidoptera: Noctuidae) in corn. Journal of Economic Entomology 83, 1286–1291.Google Scholar
SAS Institute (1999) SAS/STAT ® user's guide version 8. 3884 pp. Cary, North Carolina SAS Institute IncGoogle Scholar
Shannag, H.K. & Capinera, J.L. (1995) Evaluation of entomopathogenic nematode species for the control of melonworm (Lepidoptera, Pyralidae). Environmental Entomology 24, 143–148.Google Scholar
Shapiro, M., Mclane, W. & Bell, R. (1985) Laboratory evaluation of selected chemicals as antidesiccants for the protection of the entomogenous nematode, Steinernema feltiae (Rhabditidae, Steinernematidae), against Lymantria dispar (Lepidoptera, Lymantriidae). Journal of Economic Entomology 78, 1437–1441.Google Scholar
Shapiro, D.I., Glazer, I. & Segal, D. (1997) Genetic improvement of heat tolerance in Heterorhabditis bacteriophora through hybridization. Biological Control 8, 153–159.Google Scholar
Simons, W.R. & Poinar, G.O. (1973) Ability of Neoaplectana carpocapsae (Steinernematidae: Nematoda) to survive extended periods of desiccation. Journal of Invertebrate Pathology 22, 228–230.Google Scholar
Smits, P.H. (1996) Post-application persistence of entomopathogenic nematodes. Biocontrol Science and Technology 6, 379–387.Google Scholar
Spaull, V.W. (1992) On the use of a methylcellulose polymer to increase the effectiveness of a Heterorhabditis species against the sugarcane stalk borer, Eldana saccharina. Fundamental and Applied Nematology 15, 457–461.Google Scholar
Unruh, T.R. & Lacey, L.A. (2001) Control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae), with Steinernema carpocapsae: effects of supplemental wetting and pupation site on infection rate. Biological Control 20, 48–56.Google Scholar
Vincent, C.Bélair, G. (1992) Biocontrol of the apple sawfly, Hoplocampa testudinea, with entomogenous nematodes. Entomophaga 37, 575–582.Google Scholar
Wardlow, L. (2002) EPNs do it again. Grower 31, 16–17.Google Scholar
Welch, H.E. (1958) Test of a nematode and an associated bacterium for the control of the Colorado potato beetle, Leptinotarsa decemlineata (Say). Annual Report of the Entomological Society of Ontario 88, 53–54.Google Scholar
Welch, H.E. & Briand, L.J. (1961a) Field experiment on the use of a nematode for the control of vegetable crop insects. Proceedings of the Entomological Society of Ontario 91, 197–202.Google Scholar
Welch, H.E. & Briand, L.J. (1961b) Test of the nematode DD-136 and an associated bacterium for the control of the Colorado potato beetle, Leptinotarsa decemlineata (Say). Canadian Entomologist 93, 759–763.Google Scholar
Williams, E.C., MacDonald, O.C. (1995) Critical factors required by the nematode Steinernema feltiae for the control of the leafminers Liriomyza huidobrensis, Liriomyza bryoniae and Chromatomyia syngenesiae. Annals of Applied Biology 127, 329–341.Google Scholar
Williams, E.C., Walters, K.F.A. (1994) Nematode control of leafminers: efficacy, temperature and timing. pp. 1079–1084Proceedings of the Brighton Crop Protection Conference–pests and diseases vol. 2. British Crop Protection CouncilFarnham, Surrey, UK.Google Scholar
Williams, E.C., Walters, K.F.A. (2000) Foliar application of the entomopathogenic nematode Steinernema feltiae against leafminers on vegetables. Biocontrol Science and Technology 10, 61–70.Google Scholar
Yamanaka, K., Seta, K. & Yasuda, M. (1986) Evaluation of the use of entomogenous nematode, Steinernema feltiae (Str. Mexican) for the biological control of the fall webworm, Hyphantria cunea, (Lepidoptera: Arctiidae). Japanese Journal of Nematology 16 26Google Scholar