Abstract
We evaluated the effect of augmentative releases of Diachasmimorpha longicaudata (Ashmead), on the native parasitoid guild of Anastrepha spp. over a two year period in zones adjacent to mango commercial orchards in Chiapas, Mexico. We chose two 15 ha working zones, 15 km apart, harbouring fruit fly hosts of varying densities without chemical control. In 2013, parasitoids were released in zone “A” while zone “B” served as control. In 2014 zones were exchanged. As expected, releases of D. longicaudata significantly increased total parasitism, from around 0.5–5% to over 22%, but annual parasitism by native parasitoids was only significantly affected in zone “A”. The numbers of native parasitoids were higher in zone “A” in both years, and diversity (H′) was not affected by D. longicaudata releases in both zones. Our results suggest that releases of D. longicaudata affect the relative abundance but not the species richness of native parasitoids.

Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Aluja M (1993) Manejo integrado de moscas de la fruta. Mexico DF
Aluja M (1996) Future trends in fruit fly management. In: McPheron BA, Steck G (eds) Fruit fly pests: a world assessment of their biology and management. DelRay Beach, Florida, pp 309–320
Aluja M, Guillen J, Liedo P, Cabrera M, Rios E, de la Rosa G, Celedonio H, Mota D (1990) Fruit infesting tephritids (Dipt.: Tephritidae) and associated parasitoids in Chiapas, Mexico. BioControl 35:39–48
Aluja M, Montoya P, Cancino J, Guillén L, Ramírez-Romero R (2008) Control biológico de moscas de la fruta. In: Arredondo H y Rodríguez del Bosque LA (eds) Control biológico en México: una revisión de casos. Soc Mex de Control Biológico, DGSV/SAGARPA. Mexico, pp 292–222
Aluja M, Ovruski SM, Sivinski J, Córdova-García G, Schliserman P, Núñez-Campero SR, Ordano M (2013) Inter-specific competition and competition-free space in the tephritid parasitoids Utetes anastrephae and Doryctobracon areolatus (Hymenoptera: Braconidae: Opiinae). Ecol Entomol 38:485–496
Aluja M, Sivinski J, van Driesche R, Anzures-Dadda A, Guillén L (2014) Pest management through tropical tree conservation. Biodivers Conserv 23:831–853
Barney JN, Whitlow TH (2008) A unifying framework for biological invasions: the state factor model. Biol Invasions 10:259–272
Cancino J, Ruiz L, López P, Moreno FM (2010) Cría masiva de parasitoides. In: Montoya P, Toledo J, Hernández E (eds) Moscas de la fruta: Fundamentos y procedimientos para su manejo. SyG Editores, Mexico, pp 291–306
Cancino J, López-Arriaga F, Montoya P (2017) Packaging conditions for the field release of the fruit fly parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Austral Entomol. doi:10.1111/aen.12229
De Moraes CM, Mescher MC (2005) Intrinsic competition between larval parasitoids with different degrees of host specificity. Ecol Entomol 30:564–570
Frank JH (1998) How risky is biological control? Comment. Ecology 79:1829–1834
Garcıa-Medel D, Sivinski J, Díaz-Fleischer F, Ramírez-Romero R, Aluja M (2007) Foraging behavior by six fruit fly parasitoids (Hymenoptera: Braconidae) released as single- or multiple-species cohorts in field cages: Influence of fruit location and host density. Biol Control 43:12–22
Greathead DJ (1995) Benefits and risks of classical biological control. In: Hokkanen HMT, Lynch JM (eds) Biological control: benefits and risks. Cambridge University Press, Cambridge, pp 53–63
Harrisson KA, Pavlova A, Amos JN, Takeuchi N, Lill AJ, Radford Q, Sunnucks P (2013) Disrupted fine-scale population processes in fragmented landscapes despite large-scale genetic connectivity for a widespread and common cooperative breeder: the superb fairy-wren (Malurus cyaneus). J Anim Ecol 82(2):322–333
Heimpel GE, Asplen MK (2011) A “Goldilocks” hypothesis for dispersal of biological of control agents. BioControl 56:441–450
Hernández-Ortíz V, Guillén-Aguilar J, López L (2010) Taxonomía e identificación de moscas de la fruta de importancia económica en América. In: Montoya P, Toledo J, Hernández E (eds) Moscas de la fruta: fundamentos y procedimientos para su manejo. SyG Editores, Mexico, pp 49–80
Hilbe JM (2011) Negative binomial regression. 2nd edition. New York, USA
Hooper KR (2001) Research needs concerning non-target impacts of biological control introductions. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, pp 39–56
Howart FG (1983) Classical biocontrol: Panacea or Pandora’s box. Proc Hawaii Entomol Soc 24:239–244
Howart FG (1991) Environmental impacts of classical biological control. Annu Rev Entomol 36:485–509
Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170
Kindlmann P, Ameixa OMCC, Dixon AFG (2011) Ecological effects of invasive alien species on native communities, with particular emphasis on the interactions between aphids and ladybirds. BioControl 56:469–476
Leyva JL, Browning HW, Gilstrap FE (1991) Effects of host fruit species, size and color on parasitization of Anastrepha ludens (Diptera: Tephritidae) by Diachasmimorpha longicaudata (Hymenoptera: Braconidae). Environ Entomol 20:1469–1474
López M, Aluja M, Sivinski J (1999) Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biol Control 15:119–129
Mack RN (1996) Predicting the identity and fate of plant invaders: emergent and emerging approaches. Biol Conserv 78:107–121
Montoya P, Liedo P, Benrey B, Cancino J, Barrera JF, Sivinski J, Aluja M (2000) Biological control of Anastrepha spp. (Diptera: Tephritidae) in mango orchards through augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol Control 18:216–224
Montoya P, Celedonio H, Miranda H, Paxtian J, Orozco D (2002) Evaluación de sistemas de trampeo y atrayentes para la captura de hembras de Ceratitis capitata (Wied.) y otras moscas de la fruta (Diptera: Tephritidae) en la región del Soconusco Chiapas. Folia Entomol Mex 41:359–374
Montoya P, Cancino J, Zenil M, Santiago G, Gutiérrez JM (2007) The augmentative biological control component in the Mexican national campaign against Anastrepha spp. fruit flies. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests: from research to field implementation. Springer, Dordrecht, pp 661–670
Montoya P, Cancino J, Ruiz L (2012) Packing of fruit fly parasitoids for augmentative releases. Insects 3:889–899
Montoya P, Ayala A, López P, Cancino J, Cabrera H, Cruz J, Martinez AM, Figueroa I, Liedo P (2016) Natural parasitism in fruit fly populations in disturbed areas adjacent to commercial mango orchards in Chiapas and Veracruz, Mexico. Environ Entomol 42(2):328–337
Murillo FD, Liedo P, Nieto-López MG, Cabrera-Mireles H, Barrera JF, Montoya P (2016) First instar larvae morphology of Opiinae (Hymenoptera: Braconidae) parasitoids of Anastrepha (Diptera: Tephritidae) fruit flies. Implications for interspecific competition. Arthrop Struct Dev 45:294–300
O’Doherty R, Link JE (1993) Fruit flies in Belize, Central America. In: Aluja M, Liedo P (eds) Fruit flies, biology and management. Springer, New York, pp 35–57
Orlinski AD (2016) Work of the EPPO/IOBC panel on biological control agents. EPPO Bull 46:243–248
Paranhos BJ, Sivinski J, Stuhl C, Holler T, Aluja M (2013) Intrinsic competition and competitor-free-space influence the coexistence of parasitoids (Hymenoptera: Braconidae: Opiinae) of neotropical Tephritidae (Diptera). Environ Entomol 42:717–723
R statical program (2016) R version 3.3.1. The R Foundation for Statical Computing. http://www.r-project.org
Rogers P (1996) Disturbance ecology and forest management: a review of literature. General technical report INT-GTR-336. U.S. Department of Agriculture, Forest Service, Intermountain Research Station, Ogden, p 16
Roy HE, Handley LJ, Schönrogge K, Poland RL, Purse BV (2011) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? BioControl 56:451–468
Simberloff D, Stilling P (1996) How risky is biological control? Ecology 77:1965–1974
Sivinski JM, Calkins CO, Baranowski RM, Harris D, Brambila J, Diaz J, Bums RE, Holler T, Dodson D (1996) Suppression Caribbean fruit fly Anastrepha suspensa (Loew) Diptera: Tephritidae) population through releases of the parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Biol Control 6:177–185
Sivinski JM, Piñero J, Aluja M (2000) The distributions of parasitoids (Hymenoptera) of Anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biol Control 18:258–269
Sivinski J, Vulinec K, Aluja M (2001) Ovipositor length in a guild of a parasitoids (Hymenoptera: Braconidae) attacking Anastrepha spp. fruit flies (Diptera: Tephritidae) in southern Mexico. Ann Entomol Soc Am 94:886–895
Smith RL, Smith TM (2001) Ecología (traduced by Mezquiet FAE), 4ta edn. Pearson Educacion SA, Madrid
Thomas MB, Willis AJ (1998) Biocontrol—risky but necessary? Trends Ecol Evol 13:325–328
Torsten H, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
van Driesche RG, Bellow TS Jr, Elkinton JS, Ferro ND (1991) The meaning of percentage parasitism revisited: solutions to the problem of accurately estimating total losses from parasitism. Environ Entomol 20:1–17
van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634
Vargas RI, Long A, Miller NW, Delate K, Jackson CG, Uchida GK, Bautista RC, Harris EJ (2004) Releases of Psyttalia fletcheri (Hymenoptera: Braconidae) and sterile flies to suppress melon fly (Diptera: Tephritidae) in Hawaii. J Econ Entomol 97:1531–1537
Waage JK (2001) Indirect ecological effects in biological control: the challenge and the opportunity. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, pp 1–11
Wajnberg E, Scott JK, Quimby PC (eds) (2001) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford
Wang XG, Johnson MW, Deame KM, Yokoyama V (2009) Larger olive fruit size reduces efficiency of Psyttalia concolor, as a parasitoid of the olive fruit fly. Biol Control 49:45–51
Ward M (2016) The regulatory landscape for biological control agents. EPPO Bull 46:249–253
Wharton RA, Marsh PM, Sharkey AJ (eds) (1998) Manual para los géneros de la familia Braconidae (Hymenoptera) del Nuevo Mundo (ed en Español por Mercado I). International Society of Hymenopterists, Washington DC
Wong TTY, Ramadan MM, McInnis DO, Mochizuki N, Nishimoto JA, Herr JC (1991) Augmentative releases of Diachasmimorpha tryoni (Hymenoptera: Braconidae) to suppress a Mediterranean fruit fly (Diptera: Tephritidae) population in Kula, Maui, Hawaii. Biol Control 1:2–7
Wong TTY, Ramadan MM, Herr JC, McInnis DO (1992) Suppression of a Mediterranean fruit fly (Diptera: Tephritidae) population with concurrent parasitoid and sterile fly release in Kula, Maui, Hawaii. J Econ Entomol 85:1671–1678
Acknowledgements
We thank Cesar Galvez, Velisario Lopez and Alvaro Meza (Programa Moscafrut SAGARPA-IICA) for technical support and Javier Valle (ECOSUR) for statistical advice. This study was partially funded by the Programa Nacional de Moscas de la Fruta DGSV-SENASICA-SAGARPA and project 163431 of the SAGARPA-CONACYT sectorial funds.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Josep Anton Jaques Miret.
Rights and permissions
About this article
Cite this article
Montoya, P., López, P., Cruz, J. et al. Effect of Diachasmimorpha longicaudata releases on the native parasitoid guild attacking Anastrepha spp. larvae in disturbed zones of Chiapas, Mexico. BioControl 62, 581–593 (2017). https://doi.org/10.1007/s10526-017-9826-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-017-9826-8

