Intensive Biological Control in Spanish Greenhouses: Problems of the Success
Currently, biological control programs in greenhouse
crops involve the use, at the same time, several natural enemies
during the crop cycle. Also, large number of plant species grown in
greenhouses, among them, the used cultivars are also wide. However,
the cultivar effects on entomophagous species efficacy (predators and
parasitoids) have been scarcely studied. A new method had been
developed, using the factitious prey or host Ephestia kuehniella. It
allow us to evaluate, under greenhouse or controlled conditions
(semi-field), the cultivar effects on the entomophagous species
effectiveness. The work was carried out in greenhouse tomato crop. It
has been found the biological and ecological activities of predatory
species (Nesidiocoris tenuis) and egg-parasitoid (Trichogramma
achaeae) can be well represented with the use of the factitious prey
or host; being better in the former than the latter. The data found in
the trial are shown and discussed. The developed method could be
applied to evaluate new plant materials before making available to
farmers as commercial varieties, at low costs and easy use.
[1] J. C. Van Lenteren, "Success in biological control of arthropods by
augmentation of natural enemies,” in Biological control: measures of
success, G. Gurr and S. Wratten, Ed. Dordrecht, NL: Kluwer Acad.
Publ., 2000, pp. 77−103.
[2] J. van der Blom, "Applied Entomology in Spanish greenhouse
horticulture,” Proc. Neth. Entomol. Soc. Meet., vol. 21, pp. 9−17, 2010.
[3] E. Vila and T. Cabello, "Biosystems engineering applied to greenhouse
pest control,” in Biosystems engineering: biofactories for food
production in the XXI Century, I. Torres and R. Guevara, Ed. Berlin,
DE: Springer, 2014, pp. 99−128.
[4] T. Cabello and R. Cañero, "Technical efficiency of plant-protection in
Spanish greenhouses,” Crop Prot., vol. 13, pp. 153−159, 1994.
[5] T. Cabello and E. Vila, "Lucha biologica en invernaderos, consolidacion
del sistema,” Vida Rural, vol. 313, pp. 25−30, 2010.
[6] A. Janssen, A. Pallini, M. Venzon and M. W. Sabelis, "Behaviour and
indirect interactions in food webs of plant-inhabiting arthropods,” Exp.
Appl. Acarol., vol. 22, pp. 497−521, 1998.
[7] E. Yano, "Effects of intraguild predation and interspecific competition
among biological control agents in augmentative biological control in
greenhouses,” in Second Int. Symp. Biol. Control Arthropods, Davos,
2005, pp. 523−530.
[8] J. G. Messelink, C. M. J. Bloemhard, M. W. Sabelis and A. Janssen,
"Biological control of aphids in the presence of thrips and their
enemies,”. BioControl, vol. 58, pp. 45−55, 2013.
[9] J. A. Rosenheim and J.P. Harmon, "The influence of intraguild predation
on the suppression of a shared prey population: an empirical
reassessment,” in Trophic and guild interactions in biological control, J.
Brodeur and G. Boivin, Ed. Dordrecht, NL: Springer, 2006, pp. 1−20.
[10] J. M. Bergman and W. M. Tingey, "Aspects of interaction between plant
genotypes and biological control,” Bull. Entomol. Soc. Am., vol. 25, pp.
275−279, 1979.
[11] P. W. Price, "Ecological aspects of host plant resistance and biological
control: interactions among three trophic levels,” in Interactions of plant
resistance and parasitoids and predators of insects, D. J. Boethel and
R.D. Eikenbarry, Ed. Chichester, UK: Ellis Horwood, 1986, pp. 11−30.
[12] M. Thomas and J. Waage. Integration of biological control and hostplant
resistance breeding: a scientific and literature review. Gap, FR.:
Technical Centre for Agricultural and Rural Cooperation & CAB, 1996.
[13] A. M. Cortesero, J. O. Stapel and W. J. Lewis, "Understanding and
manipulating plant attributes to enhance biological control,” Biol.
Control, vol. 17, pp. 35–49, 2000.
[14] J. D. Hare, "Plant genetic variation in tritrophic interactions," in
Multitrophic Level Interactions, T. Tscharntke and B.A. Hawkins, Ed.
Cambridge, UK: Cambridge University Press, 2002, pp. 8−43.
[15] P. J. Ode, "Plant chemistry and natural enemy fitness: effects on
herbivore and natural enemy interactions,” Annu. Rev. Entornol., vol.
51, pp. 163−185, 2006.
[16] D. G. Bottrell, P. Barbosa, and F. Gould, "Manipulating natural enemies
by plant variety selection and modification: A realistic strategy?,” Annu.
Rev. Entomol., vol. 43: 347−367, 1998.
[17] T. Cabello, J. R. Gallego, F. J. Fernandez, M. Gamez, E. Vila, M. del
Pino and E. Hernandez-Suarez, "Biological control strategies for the South American tomato moth (Lep.: Gelechiidae) in greenhouse
tomatoes,” J. Econ. Entomol., vol. 105: 2085−2096, 2012.
[18] E. Vila, A. Parra, D. Beltran, J. R. Gallego, F. J. Fernandez and T.
Cabello, "IPM strategies in tomato crops in Spanish greenhouses,” IOBC
WPRS Bull., vol. 80, pp. 245−251, 2012.
[19] T. Cabello, Biologia de dos especies de Trichogramma (Hym.:
Trichogrammatidae) parasitas de Heliothis spp. (Lep.: Noctuidae) en
algodonero. Posibilidades de su empleo como agente de control.
Cordoba, ES: University of Cordoba, 1985.
[20] J. E. Belda and J. Lastres, "Reglamento especifico de Produccion
Integrada de tomate bajo abrigo,” Vida Rural, vol. 86, pp. 38−40, 1999.
[21] D. R. Dent and , M. P. Walton, Methodos in ecological and agricultural
entomology. Wallingford, UK: CAB Int., 1997.
[22] E. V. A. Gomide, E. F. Vilela, and M. Picanço, "Comparação de
procedimentos de amostragem de Tuta absoluta em tomateiro
estaqueado,” Neotrop. Entom., vol. 30, pp. 697−705, 2001.
[23] J. A. Sanchez, "Density thresholds for Nesidiocoris tenuis (Het.:
Miridae) in tomato crops,” Biol. Control, vol. 51, pp. 493−498, 2009.
[24] IBM, IBM SPSS Statistics for Windows, Armonk, NY: IBM Corp., 2012.
[25] A. G. Wheeler, "Predacious plant bugs (Miridae),” in Heteroptera of
economic importance, C.W. Schaefer and A. R. Panizzi, Ed. Boca
Raton, FL: CRC Press, 2000, pp. 657−693.
[26] J. A. Sanchez, "Zoophytophagy in the plantbug Nesidiocoris tenuis,”
Agric. For. Entomol., vol. 10, pp. 75−80, 2008.
[27] A. G. Wheeler and T. J. Henry, A synthesis of the holarctic Miridae
(Het.): distribution, biology, and origin, with emphasis on North
America. Lanham, MD: Entomol. Soc. Am., 1992.
[28] W. Rabitsch, "Alien true bugs of Europe (Insecta: Hem.: Het.),”
Zootaxa, vol. 1827, pp. 1−44, 2008.
[29] K. Valderrama, J. Granobles, E. Valencia and M. Sanchez, "Nesidiocoris
tenuis (Hem.: Miridae) predator in tobacco crops (Nicotiana tabacum),”
Rev. Colomb. Entomol., vol. 33, pp. 141−145, 2007.
[30] L. Ling-Rui, X. Ren-Feng, W. Xiao-Jing and Z. Fan-Rong, "Predation of
Nesidiocoris tenuis to Trialeurodes vaporariorum and Plutella
xylostella,” J. Agric. U. Hebei., vol. 2008-01, 2008.
[31] M. Perez-Hedo and A. Urbaneja, "Prospects for predatory mirid bugs as
biocontrol agents of aphids in sweet peppers,” J. Pest Sc. (publ. online),
2014.
[32] P. D. Lingren and D. A. Wolfenbarger, „Competition between
Trichogramma pretiosum and Orius insidiosus for caged tobacco
budworms on cotton treated with chlordimeform sprays,” Environ.
Entomol., vol. 5, pp. 1049−1052, 1976.
[33] K. Alrouechdi and J. Voegele, "Predation des Trichogrammes par les
Chrysopides,” Agronomie, vol. 1, pp. 187−189, 1981.
[34] C. Roger, D. Coderre, C. Vigneault and G. Boivin, "Prey discrimination
by a generalist Coccinellid predator: Effect of prey age or parasitism?,”
Ecol. Entomol., vol. 26, pp. 163-172, 2001.
[35] J. H. Brower and J. W. Press, "Interactions between the egg parasite
Trichogramma pretiosum (Hym.: Trichogrammatidae) and a predator,
Xylocoris flavipes (Hem.: Anthocoridae) of the almond moth Cadra
cautella (Lep.: Pyralidae),” J. Entomol. Sci., vol. 23, pp. 342−349, 1988.
[36] H. N. Oliveira, P. de Clercq, J. C. Zanuncio, D. Pratissoli and E.
Pedruzzi, "Nymphal development and feeding preference of Podisus
maculiventris (Het.: Pentatomidae) on eggs of Ephestia kuehniella
(Lep.: Pyralidae) parasitised or not by Trichogramma brassicae (Hym.:
Trichogrammatidae),” Braz. J. Biol., vol. 64, pp. 459−463, 2004.
[37] S. B. Vinson, "Nutritional Ecology of Insect Egg Parasitoids,” in Egg
parasitoids in agroecosystems with emphasis on Trichogramma, F. L.
Consoli, J. R. P. Parra and R. A. Zucchi, Ed. Dordrecht, NL: Springer,
2010, pp.: 25−55.
[38] J. P. Bournier, "Comportement de plusieurs sourches de Trichogrammes
vis-a-vis des oeuf d'Heliothis armigera (Lep.: Noctuidae) et de Chilo
partellus (Lep.: Pyralidae),” Les Colloques de l'INRA, vol. 9, pp. 85−96,
1982.
[39] G. D. Curl and P. P. Burbutis, "Host-preference studies with
Trichogramma nubilale,” Environ. Entornol., vol. 7, pp. 542−543, 1978.
[40] A.V. Navarajan, R. Dass, B. Parshad, "Influence of different host on
parasitism by Trichogramma chilonis and T. exiguum (Hym.:
Trichogrammatidae),” Z. ang. Entomol., vol. 92, pp. 160−l64, 1981.
[41] EPPO, "Side-effects on Trichogramma cacoeciae,” in EPPO Standars:
Guideline for the efficacy evaluation of plant protection products, Vol.
1. Paris, FR: European and Mediterranean Plant Protection Organization,
1999, pp. 165−172.
[42] T. Cabello, J. R. Gallego, F. J. Fernandez, D. de Scals, A. Rubio, S.
Salvatierra, A. Parra, "New simple methodology to evaluate the
insecticide side-effects on Trichogramma species (Hym.:
Trichogrammatidae) in greenhouse crops,” in Book of Abstracts of the
IXth Eur. Congr. Entomol., 2010, pp. 222.
[43] D. Pratissoli, U. Rodrigues-Vianna, H. Bolsoni-Zago and P. Luiz-
Pastori, "Capacidade de dispersão de Trichogramma em tomateiro
estaqueado,” Pesq. agropec. bras. Brasilia, vol. 40, pp. 613−616, 2005.
[44] S. M. Smith, "Biological control with Trichogramma: advances,
successes, and potential of their use,” Annu. Rev. Entomol., vol. 41, pp.
375−406, 1996.
[45] D. Gingras and G. Boivin, "Effect of plant structure, host density and
foraging duration on host finding by Trichogramma evanescens (Hym.:
Trichogrammatidae),” Environ. Entomol., vol. 31, pp. 1153−1157, 2002.
[1] J. C. Van Lenteren, "Success in biological control of arthropods by
augmentation of natural enemies,” in Biological control: measures of
success, G. Gurr and S. Wratten, Ed. Dordrecht, NL: Kluwer Acad.
Publ., 2000, pp. 77−103.
[2] J. van der Blom, "Applied Entomology in Spanish greenhouse
horticulture,” Proc. Neth. Entomol. Soc. Meet., vol. 21, pp. 9−17, 2010.
[3] E. Vila and T. Cabello, "Biosystems engineering applied to greenhouse
pest control,” in Biosystems engineering: biofactories for food
production in the XXI Century, I. Torres and R. Guevara, Ed. Berlin,
DE: Springer, 2014, pp. 99−128.
[4] T. Cabello and R. Cañero, "Technical efficiency of plant-protection in
Spanish greenhouses,” Crop Prot., vol. 13, pp. 153−159, 1994.
[5] T. Cabello and E. Vila, "Lucha biologica en invernaderos, consolidacion
del sistema,” Vida Rural, vol. 313, pp. 25−30, 2010.
[6] A. Janssen, A. Pallini, M. Venzon and M. W. Sabelis, "Behaviour and
indirect interactions in food webs of plant-inhabiting arthropods,” Exp.
Appl. Acarol., vol. 22, pp. 497−521, 1998.
[7] E. Yano, "Effects of intraguild predation and interspecific competition
among biological control agents in augmentative biological control in
greenhouses,” in Second Int. Symp. Biol. Control Arthropods, Davos,
2005, pp. 523−530.
[8] J. G. Messelink, C. M. J. Bloemhard, M. W. Sabelis and A. Janssen,
"Biological control of aphids in the presence of thrips and their
enemies,”. BioControl, vol. 58, pp. 45−55, 2013.
[9] J. A. Rosenheim and J.P. Harmon, "The influence of intraguild predation
on the suppression of a shared prey population: an empirical
reassessment,” in Trophic and guild interactions in biological control, J.
Brodeur and G. Boivin, Ed. Dordrecht, NL: Springer, 2006, pp. 1−20.
[10] J. M. Bergman and W. M. Tingey, "Aspects of interaction between plant
genotypes and biological control,” Bull. Entomol. Soc. Am., vol. 25, pp.
275−279, 1979.
[11] P. W. Price, "Ecological aspects of host plant resistance and biological
control: interactions among three trophic levels,” in Interactions of plant
resistance and parasitoids and predators of insects, D. J. Boethel and
R.D. Eikenbarry, Ed. Chichester, UK: Ellis Horwood, 1986, pp. 11−30.
[12] M. Thomas and J. Waage. Integration of biological control and hostplant
resistance breeding: a scientific and literature review. Gap, FR.:
Technical Centre for Agricultural and Rural Cooperation & CAB, 1996.
[13] A. M. Cortesero, J. O. Stapel and W. J. Lewis, "Understanding and
manipulating plant attributes to enhance biological control,” Biol.
Control, vol. 17, pp. 35–49, 2000.
[14] J. D. Hare, "Plant genetic variation in tritrophic interactions," in
Multitrophic Level Interactions, T. Tscharntke and B.A. Hawkins, Ed.
Cambridge, UK: Cambridge University Press, 2002, pp. 8−43.
[15] P. J. Ode, "Plant chemistry and natural enemy fitness: effects on
herbivore and natural enemy interactions,” Annu. Rev. Entornol., vol.
51, pp. 163−185, 2006.
[16] D. G. Bottrell, P. Barbosa, and F. Gould, "Manipulating natural enemies
by plant variety selection and modification: A realistic strategy?,” Annu.
Rev. Entomol., vol. 43: 347−367, 1998.
[17] T. Cabello, J. R. Gallego, F. J. Fernandez, M. Gamez, E. Vila, M. del
Pino and E. Hernandez-Suarez, "Biological control strategies for the South American tomato moth (Lep.: Gelechiidae) in greenhouse
tomatoes,” J. Econ. Entomol., vol. 105: 2085−2096, 2012.
[18] E. Vila, A. Parra, D. Beltran, J. R. Gallego, F. J. Fernandez and T.
Cabello, "IPM strategies in tomato crops in Spanish greenhouses,” IOBC
WPRS Bull., vol. 80, pp. 245−251, 2012.
[19] T. Cabello, Biologia de dos especies de Trichogramma (Hym.:
Trichogrammatidae) parasitas de Heliothis spp. (Lep.: Noctuidae) en
algodonero. Posibilidades de su empleo como agente de control.
Cordoba, ES: University of Cordoba, 1985.
[20] J. E. Belda and J. Lastres, "Reglamento especifico de Produccion
Integrada de tomate bajo abrigo,” Vida Rural, vol. 86, pp. 38−40, 1999.
[21] D. R. Dent and , M. P. Walton, Methodos in ecological and agricultural
entomology. Wallingford, UK: CAB Int., 1997.
[22] E. V. A. Gomide, E. F. Vilela, and M. Picanço, "Comparação de
procedimentos de amostragem de Tuta absoluta em tomateiro
estaqueado,” Neotrop. Entom., vol. 30, pp. 697−705, 2001.
[23] J. A. Sanchez, "Density thresholds for Nesidiocoris tenuis (Het.:
Miridae) in tomato crops,” Biol. Control, vol. 51, pp. 493−498, 2009.
[24] IBM, IBM SPSS Statistics for Windows, Armonk, NY: IBM Corp., 2012.
[25] A. G. Wheeler, "Predacious plant bugs (Miridae),” in Heteroptera of
economic importance, C.W. Schaefer and A. R. Panizzi, Ed. Boca
Raton, FL: CRC Press, 2000, pp. 657−693.
[26] J. A. Sanchez, "Zoophytophagy in the plantbug Nesidiocoris tenuis,”
Agric. For. Entomol., vol. 10, pp. 75−80, 2008.
[27] A. G. Wheeler and T. J. Henry, A synthesis of the holarctic Miridae
(Het.): distribution, biology, and origin, with emphasis on North
America. Lanham, MD: Entomol. Soc. Am., 1992.
[28] W. Rabitsch, "Alien true bugs of Europe (Insecta: Hem.: Het.),”
Zootaxa, vol. 1827, pp. 1−44, 2008.
[29] K. Valderrama, J. Granobles, E. Valencia and M. Sanchez, "Nesidiocoris
tenuis (Hem.: Miridae) predator in tobacco crops (Nicotiana tabacum),”
Rev. Colomb. Entomol., vol. 33, pp. 141−145, 2007.
[30] L. Ling-Rui, X. Ren-Feng, W. Xiao-Jing and Z. Fan-Rong, "Predation of
Nesidiocoris tenuis to Trialeurodes vaporariorum and Plutella
xylostella,” J. Agric. U. Hebei., vol. 2008-01, 2008.
[31] M. Perez-Hedo and A. Urbaneja, "Prospects for predatory mirid bugs as
biocontrol agents of aphids in sweet peppers,” J. Pest Sc. (publ. online),
2014.
[32] P. D. Lingren and D. A. Wolfenbarger, „Competition between
Trichogramma pretiosum and Orius insidiosus for caged tobacco
budworms on cotton treated with chlordimeform sprays,” Environ.
Entomol., vol. 5, pp. 1049−1052, 1976.
[33] K. Alrouechdi and J. Voegele, "Predation des Trichogrammes par les
Chrysopides,” Agronomie, vol. 1, pp. 187−189, 1981.
[34] C. Roger, D. Coderre, C. Vigneault and G. Boivin, "Prey discrimination
by a generalist Coccinellid predator: Effect of prey age or parasitism?,”
Ecol. Entomol., vol. 26, pp. 163-172, 2001.
[35] J. H. Brower and J. W. Press, "Interactions between the egg parasite
Trichogramma pretiosum (Hym.: Trichogrammatidae) and a predator,
Xylocoris flavipes (Hem.: Anthocoridae) of the almond moth Cadra
cautella (Lep.: Pyralidae),” J. Entomol. Sci., vol. 23, pp. 342−349, 1988.
[36] H. N. Oliveira, P. de Clercq, J. C. Zanuncio, D. Pratissoli and E.
Pedruzzi, "Nymphal development and feeding preference of Podisus
maculiventris (Het.: Pentatomidae) on eggs of Ephestia kuehniella
(Lep.: Pyralidae) parasitised or not by Trichogramma brassicae (Hym.:
Trichogrammatidae),” Braz. J. Biol., vol. 64, pp. 459−463, 2004.
[37] S. B. Vinson, "Nutritional Ecology of Insect Egg Parasitoids,” in Egg
parasitoids in agroecosystems with emphasis on Trichogramma, F. L.
Consoli, J. R. P. Parra and R. A. Zucchi, Ed. Dordrecht, NL: Springer,
2010, pp.: 25−55.
[38] J. P. Bournier, "Comportement de plusieurs sourches de Trichogrammes
vis-a-vis des oeuf d'Heliothis armigera (Lep.: Noctuidae) et de Chilo
partellus (Lep.: Pyralidae),” Les Colloques de l'INRA, vol. 9, pp. 85−96,
1982.
[39] G. D. Curl and P. P. Burbutis, "Host-preference studies with
Trichogramma nubilale,” Environ. Entornol., vol. 7, pp. 542−543, 1978.
[40] A.V. Navarajan, R. Dass, B. Parshad, "Influence of different host on
parasitism by Trichogramma chilonis and T. exiguum (Hym.:
Trichogrammatidae),” Z. ang. Entomol., vol. 92, pp. 160−l64, 1981.
[41] EPPO, "Side-effects on Trichogramma cacoeciae,” in EPPO Standars:
Guideline for the efficacy evaluation of plant protection products, Vol.
1. Paris, FR: European and Mediterranean Plant Protection Organization,
1999, pp. 165−172.
[42] T. Cabello, J. R. Gallego, F. J. Fernandez, D. de Scals, A. Rubio, S.
Salvatierra, A. Parra, "New simple methodology to evaluate the
insecticide side-effects on Trichogramma species (Hym.:
Trichogrammatidae) in greenhouse crops,” in Book of Abstracts of the
IXth Eur. Congr. Entomol., 2010, pp. 222.
[43] D. Pratissoli, U. Rodrigues-Vianna, H. Bolsoni-Zago and P. Luiz-
Pastori, "Capacidade de dispersão de Trichogramma em tomateiro
estaqueado,” Pesq. agropec. bras. Brasilia, vol. 40, pp. 613−616, 2005.
[44] S. M. Smith, "Biological control with Trichogramma: advances,
successes, and potential of their use,” Annu. Rev. Entomol., vol. 41, pp.
375−406, 1996.
[45] D. Gingras and G. Boivin, "Effect of plant structure, host density and
foraging duration on host finding by Trichogramma evanescens (Hym.:
Trichogrammatidae),” Environ. Entomol., vol. 31, pp. 1153−1157, 2002.
@article{"International Journal of Biological, Life and Agricultural Sciences:68144", author = "Carolina Sanchez and Juan R. Gallego and Manuel Gamez and Tomas Cabello", title = "Intensive Biological Control in Spanish Greenhouses: Problems of the Success", abstract = "Currently, biological control programs in greenhouse
crops involve the use, at the same time, several natural enemies
during the crop cycle. Also, large number of plant species grown in
greenhouses, among them, the used cultivars are also wide. However,
the cultivar effects on entomophagous species efficacy (predators and
parasitoids) have been scarcely studied. A new method had been
developed, using the factitious prey or host Ephestia kuehniella. It
allow us to evaluate, under greenhouse or controlled conditions
(semi-field), the cultivar effects on the entomophagous species
effectiveness. The work was carried out in greenhouse tomato crop. It
has been found the biological and ecological activities of predatory
species (Nesidiocoris tenuis) and egg-parasitoid (Trichogramma
achaeae) can be well represented with the use of the factitious prey
or host; being better in the former than the latter. The data found in
the trial are shown and discussed. The developed method could be
applied to evaluate new plant materials before making available to
farmers as commercial varieties, at low costs and easy use.
", keywords = "Cultivar Effects, Efficiency, Predators, Parasitoids.", volume = "8", number = "10", pages = "1123-5", }
