The effects of a parasitoid wasp of a gall-making insect on host plant characteristics and the abundance of sharing host-plant herbivore
##plugins.themes.bootstrap3.article.sidebar##
Issue
Section
Articles
##plugins.themes.bootstrap3.article.main##
Abstract
Abstract. Triyogo A, Yasuda H. 2019. The effects of a parasitoid wasp of a gall-making insect on host plant characteristics and the abundance of sharing host-plant herbivore. Biodiversitas 20: 3499-3507. The present study has evaluated the indirect, top-down effects of a parasitoid wasp, Torymus beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae), of a gall-maker, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), on the characteristics of the chestnut tree, Castanea crenata Siebold & Zucc. (Fagales: Fagaceae), and the implications for other herbivores, the aphid, Myzocallis kuricola (Matsumura) (Homoptera: Aphididae). sharing the same host plant. In a field experiment, the behavior of D. kuriphilus larvae on chestnut tree was influenced by the T. beneficus as indicated by a small increment of gall volume. However, parasitism did not affect certain other leaf characteristics that were induced by the gall wasp. Here we show that the characteristics of chestnut tree induced by the gall-making wasp affected M. kuricola that subsequently attacked the chestnut tree. However, the hypothesis that top-down effects by natural enemies may affect other herbivores on chestnut tree through its influence on gall-making wasp was not supported in this study. This study shows that parasitism of a gall-maker does not affect the other herbivore sharing the same host plant. Furthermore, the top-down effects of the parasitoid's behavior on plants may have different effects on sharing host herbivores that attack galled plants.
##plugins.themes.bootstrap3.article.details##
References
Abbate C, Toscano S, Arcidiacono R, Romano D, Russo A, Mazzeo G. 2018. Induced responses of Bougainvillea glabra Choisy (Nyctaginaceae) against Phenacoccus peruvianus Granara de Willink (Hemiptera: Pseudococcidae) attack: preliminary results. Arthropod-Plant Interact 12: 41-48. https://doi.org/10.1007/s11829-017-9550-4
Aartsma Y, Bianchi FJ, van der Werf W, Poelman EH, Dicke M. 2017. Herbivore?induced plant volatiles and tritrophic interactions across spatial scales. New Phytol 216(4): 1054-1063. https://doi.org/10.1111/nph.14475
Bonaventure G, VanDoorn A, Baldwin IT. 2011. Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci 16:294–299. https://doi.org/10.1016/j.tplants. 2011.01. 006
Calderón-Cortés N, Uribe-Mú CA, Martínez-Méndez AK, Escalera-Vázquez LH, Cristobal-Pérez EJ, García-Oliva F, Quesada M. 2016. Ecosystem engineering and manipulation of host plant tissues by the insect borer Oncideres albomarginata chamela. J Insect Physiol 84: 128-136. https://doi.org/10.1016/j.jinsphys.2015.10.008
Cusumano A, Zhu F, Volkoff AN, Verbaarschot P, Bloem J, Vogel H, Dicke M, Poelman EH. 2018. Parasitic wasp?associated symbiont affects plant?mediated species interactions between herbivores. Ecol Lett 21(7): 957-967. https://doi.org/10.1111/ele.12952
Damman H (1989) Facilitative interactions between two lepidopteran herbivores of Asimina. Oecologia 78(2): 214-219
Da Silva SE, França JF, Pareja M. 2016. Olfactory response of four aphidophagous insects to aphid-and caterpillar-induced plant volatiles. Arthropod-Plant Inte 10(4): 331-340. https://doi.org/10.1007/s11829-016-9436-x
Erb M, Reymond P. 2019. Molecular interactions between plants and insect herbivores. Annu Rev Plant Bio 70: 527-557. https://doi.org/10.1146/annurev-arplant-050718-095910
Flaherty L, Quiring D. 2008. Plant module size and dose of gall induction stimulus influence gall induction and galler performance. Oikos 117(11): 1601-1608. https://doi.org/33410.HH/i.1600-0706.2008.l6555.x
Frago E, Mala M, Weldegergis BT, Yang C, McLean A, Godfray HCJ, Gols R, Dicke M. 2017. Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles. Nat Commun 8(1): p1860. https://doi.org/10.1038/s41467-017-01935-0
Gibbs M, Schönrogge K, Alma A, Melika G, Quacchia A, Stone GN, Aebi A. 2011. Torymus sinensis: a viable management option for the biological control of Dryocosmus kuriphilus in Europe?. BioControl 56(4): 527-538. https://doi.org/10.1007/s10526-340011-9364-8
Hare JD. 2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Ento 56: 161-180. https://doi.org/10.1146/annurev-ento-120709-144753
Hilker M, Meiners T. 2010. How do plants “notice” attack by herbivorous arthropods?. Biolo Rev 85(2): 267-280. doi:10.1111/j.1469-185X.2009.00100.x
Hunter MD, Price PW. 1992. Playing chutes and ladders: Heterogeneity and relative roles of bottom-up and top-down forces in natural communities. Ecology 73(3): 724-732
Karban R, Baldwin IT. 1997. Induced responses to herbivory. The University of Chicago press. 319p
Karban R. 2011. The ecology and evolution of induced resistance against herbivores. Func Eco 25(2): 339-347. https://doi.org/10.1111/j.1365-2435.2010.01789.x
Karban R, Myers JH. 1989. Induced plant responses to herbivory. Annu Rev Ecol Syst: 20(1): 331-348.
Kato K, Hijii N. 1993. Optimal clutch size of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Res Popul Ecol 35:1-14. https://doi.org/10.1007/BF02515640
Kato K, Hijii N. 1999. Mortality factors of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) after gall formation. Entomol Sci 2(4): 483-491
Kato K, Hijii N. 2001. Ovipositional traits of the chestnut gall wasp, Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Entomol Sci, 4(3): 295-299.
Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annual review of plant biology 53(1): 299-328. https://doi.org/ 10.1146/annurev.arplant.53.100301.135207
Mithöfer A, Boland W. 2012. Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63: 431-450. https://doi.org/10.1146/annurev-arplant-042110-103854
Miyashita K, Ito Y, Nakamura K, Nakamura M, Kondo M. 1965. Population dynamics of the chestnut gall wasp Drycosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). III. Five years of observation on population fluctuation. Appl Entomol Zool 9:42–52
Moriya S, Inoue K, Otake A, Shiga M, Mabuchi M. 1989. Decline of the chestnut gall wasp population, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) after the establishment of Torymus sinensis Kamijo (Hymenoptera: Torymidae). Appl Entomol Zool 24(2): 231-233.
Mumm R, Dicke M. 2010. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88(7): 628-667. https://doi.org/10.1139/Z10-032
Murakami Y. 1981. The Parasitoids of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) in Japan and the introduction of a promising natural enemy from China (Hymenoptera : Chalcidoidea). J Fat Agr 25(4): 167-174
Murakami Y, Tokuhisa E. 1985. Behavioural sequences of oviposition and host-feeding of Torymus (Syntomaspis) beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae), a native parasitoid of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Appl Entomol Zool 20(1): 43-49.
Murakami Y. 1988. Ecotypes of Torymus (Syntomaspis) beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae) with different seasonal prevalence of adult emergence. Appl Entomol Zool 23:81–87. http://doi.org/10.1303/aez.23.81
Murakami Y. 1997. Natural enemies of the chestnut gall wasp. approaches to biological control. Kyusyu University Press, Fukuoka. 308 pp (in Japanese)
Nakamura M, Miyamoto Y, Ohgushi T. 2003. Gall initiation enhances the availability of food resources for herbivorous insects. Func Ecol 17(6): 851-857
Ohgushi T. 2005. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36: 81-105. http://doi.org/10.1146/annurev.ecolsys. 36.091704. 175523
Ohgushi T, Craig TP, Price PW. 2007. Ecological communities: Plant mediation in indirect interaction webs. Cambridge University Press. Cambridge, UK
Ohgushi T, Schmitz OJ, Holt RD. 2012. Trait-mediated indirect interactions: Ecological and evolutionary perspectives. Cambridge University Press, Cambridge, UK
Oliveira DC, Isaias RMS, Fernandes GW, Ferreira BG, Carneiro RGS, Fuzaro L. 2016. Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J Insect Physiol 84: 103-113. https://doi.org/10.1016/j.jinsphys.2015.11.012
Otake A. 1980. Chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae): A preliminary study on trend of adult emergence and some other ecological aspects related to the final stage of its lifecycle. Appl Entomol Zool 15: 829-839
Ôtake A, Moriya S, Shiga M. 1984. Colonization of Torymus sinensis Kamijo (Hymenoptera: Torymidae), a parasitoid of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), introduced from China. Appl Entomol Zool 19: 111-114
Parkman P, Shepard M. 1981. Foliage consumption by yellow striped armyworm larvae after parasitisation by Euplectrus plathypenae. Fla Entomol 64: 192-194.
Peckarsky BL, Abrams PA, Bolnick DI, Dill LM, Grabowski JH, Luttbeg B, Orrock JL, Peacor SD, Preisser EL, Schmitz OJ, Trussell GC. 2008. Revisiting the classics: considering nonconsumptive effects in textbook examples of predator–prey interactions. Ecology 89(9): 2416-2425.
Piao CS, Moriya S. 1999. Oviposition of Torymus sinensis Kamijo (Hymenoptera: Torymidae) under natural conditions. Entomol Sci 2: 329–334
Poelman EH, Zheng SJ, Zhang Z, Heemskerk NM, Cortesero AM, Dicke M. 2011a. Parasitoid-spesific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proc Natl Acad Sci USA 108: 19647-19652. http://doi.org/10.1073/pnas.1110748108
Poelman EH, Gols R, Snoeren TA, Muru D, Smid HM, Dicke M. 2011b. Indirect plant?mediated interactions among parasitoid larvae. Ecol Lett 14(7): 670-676. http://doi.org/10.1111/j.1461-0248.2011.01629.x
Poelman EH, Dicke M. 2018. Insect?Plant Interactions Section III. Ecology and Evolution of Insect?Plant Interactions. Annual Plant Reviews book series, Volume 47: 309-337. https://doi.org/10.1002/9781119312994.apr0513
Powell JE. 1989. Food consumption by tobacco budworm (Lepidoptera: Noctuidae) larvae reduced after parasitizationy Microplitis demolitor or M. croceipes (Hymenoptera: Braconidae). J Econ Entomol 82(2): 408-411. http://dx.doi.org/10.1093/jee/82.2.408
Price PW, Bouton CE, Gross P et al. 1980 Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies Annu Rev Ecol Syst 11: 41-65. http://doi.org/10.1146/annurev.es.11.110180.000353
Quacchia A, Moriya S, Bosio G, Scapin I, Alma A. 2008. Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus. Biocontrol 53: 829-839. http://doi.org/10.1007/s13355-013-0194-2
Rani PU, Jyothsna Y. 2010. Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiol Plant 32(4): 695-701. https://doi.org/10.1007/s11738-009-0449-2
Schuman MC, Baldwin IT. 2016. The layers of plant responses to insect herbivores. Annu Rev Entomol 61: 373-394. http://doi.org/10.1146/annurev-ento-010715-023851
Schmitz OJ, Krivan V, Ovadia O. 2004. Trophic cascades: the primacy of trait?mediated indirect interactions. Ecol Lett 7(2): 153-163. http://doi.org/10.1111/j.1461-0248.2003. 00560.x
Stam JM, Kroes A, Li Y et al. 2014. Plant interactions with multiple insect herbivores: From community to genes. Annu Rev Plant Biol 65: 689-713. https://doi.org/10.1146/annurev-arplant-050213-035937
Stephens AE, Westoby M. 2015. Effects of insect attack to stems on plant survival, growth, reproduction and photosynthesis. Oikos 124(3): 266-273. https://doi.org/10.1111/oik.01809
Tewari S, Buonaccorsi JP, Averill AL. 2013. Impact of early season apical meristem injury by gall inducing tipworm (Diptera: Cecidomyiidae) on reproductive and vegetative growth of cranberry. J Econ Entomol 106(3): 1339-1348. https://doi.org/10.1603/EC12269
Tooker JF, Hanks LM. 2006. Tritrophic interactions and reproductive fitness of the prairie perennial Silphium laciniatum Gillette (Asteraceae). Environ Entomol 35: 537–545. http://dx.doi.org/10.1603/0046-225X-35.2.537
Triyogo A, Yasuda H. 2013. Effect of host-plant manipulation by a gall-inducing insect on abundance of herbivores on chestnut trees. Appl Entomol Zool 48(3): 345-353. https://doi.org/10.1007/s13355-013-0194-2
Van Loon JJA, de Boer JG, Dicke M. 2000. Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol Exp Appl 97: 219–227
Vijaya M, Rani PU. 2017. Defensive responses in Capsicum annuum (L) plants, induced due to the feeding by different larval instars of Spodoptera litura (F). Arthropod-Plant Inte 11(2): 193-202. https://doi.org/10.1007/s11829-016-9479-z
Wachi N, Abe Y. 2009. Taxonomic status of the oak gall wasp Callirhytis hakonensis Ashmead (Hymenoptera: Cynipidae), a candidate for native host of Torymus beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae), with a description of its sexual generation. pp 32–33 in: S. Moriya (ed.) A global serious pest of chestnut trees, Dryocosmus kuriphilus: yesterday, today and tomorrow. Proceedings of the Japan-Italy Joint International Symposium, Tsukuba, Japan, November 24–25, 2009
Xu H, Desurmont G, Degen T, Zhou G, Laplanche D, Henryk L, Turlings TC. 2017. Combined use of herbivore?induced plant volatiles and sex pheromones for mate location in braconid parasitoids. Plant Cell Environ 40(3): 330-339
Aartsma Y, Bianchi FJ, van der Werf W, Poelman EH, Dicke M. 2017. Herbivore?induced plant volatiles and tritrophic interactions across spatial scales. New Phytol 216(4): 1054-1063. https://doi.org/10.1111/nph.14475
Bonaventure G, VanDoorn A, Baldwin IT. 2011. Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci 16:294–299. https://doi.org/10.1016/j.tplants. 2011.01. 006
Calderón-Cortés N, Uribe-Mú CA, Martínez-Méndez AK, Escalera-Vázquez LH, Cristobal-Pérez EJ, García-Oliva F, Quesada M. 2016. Ecosystem engineering and manipulation of host plant tissues by the insect borer Oncideres albomarginata chamela. J Insect Physiol 84: 128-136. https://doi.org/10.1016/j.jinsphys.2015.10.008
Cusumano A, Zhu F, Volkoff AN, Verbaarschot P, Bloem J, Vogel H, Dicke M, Poelman EH. 2018. Parasitic wasp?associated symbiont affects plant?mediated species interactions between herbivores. Ecol Lett 21(7): 957-967. https://doi.org/10.1111/ele.12952
Damman H (1989) Facilitative interactions between two lepidopteran herbivores of Asimina. Oecologia 78(2): 214-219
Da Silva SE, França JF, Pareja M. 2016. Olfactory response of four aphidophagous insects to aphid-and caterpillar-induced plant volatiles. Arthropod-Plant Inte 10(4): 331-340. https://doi.org/10.1007/s11829-016-9436-x
Erb M, Reymond P. 2019. Molecular interactions between plants and insect herbivores. Annu Rev Plant Bio 70: 527-557. https://doi.org/10.1146/annurev-arplant-050718-095910
Flaherty L, Quiring D. 2008. Plant module size and dose of gall induction stimulus influence gall induction and galler performance. Oikos 117(11): 1601-1608. https://doi.org/33410.HH/i.1600-0706.2008.l6555.x
Frago E, Mala M, Weldegergis BT, Yang C, McLean A, Godfray HCJ, Gols R, Dicke M. 2017. Symbionts protect aphids from parasitic wasps by attenuating herbivore-induced plant volatiles. Nat Commun 8(1): p1860. https://doi.org/10.1038/s41467-017-01935-0
Gibbs M, Schönrogge K, Alma A, Melika G, Quacchia A, Stone GN, Aebi A. 2011. Torymus sinensis: a viable management option for the biological control of Dryocosmus kuriphilus in Europe?. BioControl 56(4): 527-538. https://doi.org/10.1007/s10526-340011-9364-8
Hare JD. 2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Ento 56: 161-180. https://doi.org/10.1146/annurev-ento-120709-144753
Hilker M, Meiners T. 2010. How do plants “notice” attack by herbivorous arthropods?. Biolo Rev 85(2): 267-280. doi:10.1111/j.1469-185X.2009.00100.x
Hunter MD, Price PW. 1992. Playing chutes and ladders: Heterogeneity and relative roles of bottom-up and top-down forces in natural communities. Ecology 73(3): 724-732
Karban R, Baldwin IT. 1997. Induced responses to herbivory. The University of Chicago press. 319p
Karban R. 2011. The ecology and evolution of induced resistance against herbivores. Func Eco 25(2): 339-347. https://doi.org/10.1111/j.1365-2435.2010.01789.x
Karban R, Myers JH. 1989. Induced plant responses to herbivory. Annu Rev Ecol Syst: 20(1): 331-348.
Kato K, Hijii N. 1993. Optimal clutch size of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Res Popul Ecol 35:1-14. https://doi.org/10.1007/BF02515640
Kato K, Hijii N. 1999. Mortality factors of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) after gall formation. Entomol Sci 2(4): 483-491
Kato K, Hijii N. 2001. Ovipositional traits of the chestnut gall wasp, Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Entomol Sci, 4(3): 295-299.
Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annual review of plant biology 53(1): 299-328. https://doi.org/ 10.1146/annurev.arplant.53.100301.135207
Mithöfer A, Boland W. 2012. Plant defense against herbivores: chemical aspects. Annu Rev Plant Biol 63: 431-450. https://doi.org/10.1146/annurev-arplant-042110-103854
Miyashita K, Ito Y, Nakamura K, Nakamura M, Kondo M. 1965. Population dynamics of the chestnut gall wasp Drycosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). III. Five years of observation on population fluctuation. Appl Entomol Zool 9:42–52
Moriya S, Inoue K, Otake A, Shiga M, Mabuchi M. 1989. Decline of the chestnut gall wasp population, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) after the establishment of Torymus sinensis Kamijo (Hymenoptera: Torymidae). Appl Entomol Zool 24(2): 231-233.
Mumm R, Dicke M. 2010. Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88(7): 628-667. https://doi.org/10.1139/Z10-032
Murakami Y. 1981. The Parasitoids of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae) in Japan and the introduction of a promising natural enemy from China (Hymenoptera : Chalcidoidea). J Fat Agr 25(4): 167-174
Murakami Y, Tokuhisa E. 1985. Behavioural sequences of oviposition and host-feeding of Torymus (Syntomaspis) beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae), a native parasitoid of Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae). Appl Entomol Zool 20(1): 43-49.
Murakami Y. 1988. Ecotypes of Torymus (Syntomaspis) beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae) with different seasonal prevalence of adult emergence. Appl Entomol Zool 23:81–87. http://doi.org/10.1303/aez.23.81
Murakami Y. 1997. Natural enemies of the chestnut gall wasp. approaches to biological control. Kyusyu University Press, Fukuoka. 308 pp (in Japanese)
Nakamura M, Miyamoto Y, Ohgushi T. 2003. Gall initiation enhances the availability of food resources for herbivorous insects. Func Ecol 17(6): 851-857
Ohgushi T. 2005. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Evol Syst 36: 81-105. http://doi.org/10.1146/annurev.ecolsys. 36.091704. 175523
Ohgushi T, Craig TP, Price PW. 2007. Ecological communities: Plant mediation in indirect interaction webs. Cambridge University Press. Cambridge, UK
Ohgushi T, Schmitz OJ, Holt RD. 2012. Trait-mediated indirect interactions: Ecological and evolutionary perspectives. Cambridge University Press, Cambridge, UK
Oliveira DC, Isaias RMS, Fernandes GW, Ferreira BG, Carneiro RGS, Fuzaro L. 2016. Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J Insect Physiol 84: 103-113. https://doi.org/10.1016/j.jinsphys.2015.11.012
Otake A. 1980. Chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae): A preliminary study on trend of adult emergence and some other ecological aspects related to the final stage of its lifecycle. Appl Entomol Zool 15: 829-839
Ôtake A, Moriya S, Shiga M. 1984. Colonization of Torymus sinensis Kamijo (Hymenoptera: Torymidae), a parasitoid of the chestnut gall wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), introduced from China. Appl Entomol Zool 19: 111-114
Parkman P, Shepard M. 1981. Foliage consumption by yellow striped armyworm larvae after parasitisation by Euplectrus plathypenae. Fla Entomol 64: 192-194.
Peckarsky BL, Abrams PA, Bolnick DI, Dill LM, Grabowski JH, Luttbeg B, Orrock JL, Peacor SD, Preisser EL, Schmitz OJ, Trussell GC. 2008. Revisiting the classics: considering nonconsumptive effects in textbook examples of predator–prey interactions. Ecology 89(9): 2416-2425.
Piao CS, Moriya S. 1999. Oviposition of Torymus sinensis Kamijo (Hymenoptera: Torymidae) under natural conditions. Entomol Sci 2: 329–334
Poelman EH, Zheng SJ, Zhang Z, Heemskerk NM, Cortesero AM, Dicke M. 2011a. Parasitoid-spesific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proc Natl Acad Sci USA 108: 19647-19652. http://doi.org/10.1073/pnas.1110748108
Poelman EH, Gols R, Snoeren TA, Muru D, Smid HM, Dicke M. 2011b. Indirect plant?mediated interactions among parasitoid larvae. Ecol Lett 14(7): 670-676. http://doi.org/10.1111/j.1461-0248.2011.01629.x
Poelman EH, Dicke M. 2018. Insect?Plant Interactions Section III. Ecology and Evolution of Insect?Plant Interactions. Annual Plant Reviews book series, Volume 47: 309-337. https://doi.org/10.1002/9781119312994.apr0513
Powell JE. 1989. Food consumption by tobacco budworm (Lepidoptera: Noctuidae) larvae reduced after parasitizationy Microplitis demolitor or M. croceipes (Hymenoptera: Braconidae). J Econ Entomol 82(2): 408-411. http://dx.doi.org/10.1093/jee/82.2.408
Price PW, Bouton CE, Gross P et al. 1980 Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies Annu Rev Ecol Syst 11: 41-65. http://doi.org/10.1146/annurev.es.11.110180.000353
Quacchia A, Moriya S, Bosio G, Scapin I, Alma A. 2008. Rearing, release and settlement prospect in Italy of Torymus sinensis, the biological control agent of the chestnut gall wasp Dryocosmus kuriphilus. Biocontrol 53: 829-839. http://doi.org/10.1007/s13355-013-0194-2
Rani PU, Jyothsna Y. 2010. Biochemical and enzymatic changes in rice plants as a mechanism of defense. Acta Physiol Plant 32(4): 695-701. https://doi.org/10.1007/s11738-009-0449-2
Schuman MC, Baldwin IT. 2016. The layers of plant responses to insect herbivores. Annu Rev Entomol 61: 373-394. http://doi.org/10.1146/annurev-ento-010715-023851
Schmitz OJ, Krivan V, Ovadia O. 2004. Trophic cascades: the primacy of trait?mediated indirect interactions. Ecol Lett 7(2): 153-163. http://doi.org/10.1111/j.1461-0248.2003. 00560.x
Stam JM, Kroes A, Li Y et al. 2014. Plant interactions with multiple insect herbivores: From community to genes. Annu Rev Plant Biol 65: 689-713. https://doi.org/10.1146/annurev-arplant-050213-035937
Stephens AE, Westoby M. 2015. Effects of insect attack to stems on plant survival, growth, reproduction and photosynthesis. Oikos 124(3): 266-273. https://doi.org/10.1111/oik.01809
Tewari S, Buonaccorsi JP, Averill AL. 2013. Impact of early season apical meristem injury by gall inducing tipworm (Diptera: Cecidomyiidae) on reproductive and vegetative growth of cranberry. J Econ Entomol 106(3): 1339-1348. https://doi.org/10.1603/EC12269
Tooker JF, Hanks LM. 2006. Tritrophic interactions and reproductive fitness of the prairie perennial Silphium laciniatum Gillette (Asteraceae). Environ Entomol 35: 537–545. http://dx.doi.org/10.1603/0046-225X-35.2.537
Triyogo A, Yasuda H. 2013. Effect of host-plant manipulation by a gall-inducing insect on abundance of herbivores on chestnut trees. Appl Entomol Zool 48(3): 345-353. https://doi.org/10.1007/s13355-013-0194-2
Van Loon JJA, de Boer JG, Dicke M. 2000. Parasitoid-plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomol Exp Appl 97: 219–227
Vijaya M, Rani PU. 2017. Defensive responses in Capsicum annuum (L) plants, induced due to the feeding by different larval instars of Spodoptera litura (F). Arthropod-Plant Inte 11(2): 193-202. https://doi.org/10.1007/s11829-016-9479-z
Wachi N, Abe Y. 2009. Taxonomic status of the oak gall wasp Callirhytis hakonensis Ashmead (Hymenoptera: Cynipidae), a candidate for native host of Torymus beneficus Yasumatsu et Kamijo (Hymenoptera: Torymidae), with a description of its sexual generation. pp 32–33 in: S. Moriya (ed.) A global serious pest of chestnut trees, Dryocosmus kuriphilus: yesterday, today and tomorrow. Proceedings of the Japan-Italy Joint International Symposium, Tsukuba, Japan, November 24–25, 2009
Xu H, Desurmont G, Degen T, Zhou G, Laplanche D, Henryk L, Turlings TC. 2017. Combined use of herbivore?induced plant volatiles and sex pheromones for mate location in braconid parasitoids. Plant Cell Environ 40(3): 330-339
Most read articles by the same author(s)
- ANANTO TRIYOGO, BUDIADI, S.M. WIDYASTUTI, SENA ADI SUBRATA, SUWITO SETYO BUDI, Abundance of ants (Hymenoptera: Formicidae) and the functional groups in two different habitats , Biodiversitas Journal of Biological Diversity: Vol. 21 No. 5 (2020)
- SRI RAHAYU, ANANTO TRIYOGO, SITI M. WIDYASTUTI, MUSYAFA’ MUSYAFA’, FIQRY ARDIANYAH, Pests and diseases on Falcataria moluccana trees in agroforestry systems with pineapple in East Java, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 22 No. 5 (2021)
- YUSUF ARDIAN SUTRISNO, ANANTO TRIYOGO, PRIYONO SURYANTO, Insect community in sengon (Falcataria moluccana) stands damaged by stem borers at various altitudes , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 6 (2022)
- ARINA DAMAYANTI, ANANTO TRIYOGO, MUSYAFA, Soil arthropod diversity in three different land management intensities of Wanagama Forest, Yogyakarta, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 3 (2023)