Displacement of Aphytis chrysomphali by Aphytis melinus, parasitoids of the California red scale, in the Iberian Peninsula

Juan Ramon Boyero, Jose Miguel Vela, Eva Wong, Carlos Garcia Ripoll, Maria Jesús Verdú, Alberto Urbaneja, Pilar Vanaclocha

Abstract


Parasitoids are the main natural enemies of the California red scale, Aonidiella aurantii (Maskell) and on occasion can regulate their populations. To increase their effectiveness, inoculative or augmentative releases of parasitoids are promoted. Previous to the implementation of any release strategy an important and necessary step is to acquire knowledge on the parasitoid fauna associated with this key phytophagous pest. Parasitoids were surveyed and quantified in Spanish citrus orchards between 2005 and 2009. Aphytis melinus DeBach (87.1%) resulted as the dominant species, followed by Aphytis chrysomphali (Mercet) (15.9%), Encarsia perniciosi (Tower) (2.4%) and Aphycus hederaceus (Westwood) (0.004%). Overall, higher levels of parasitism were recorded in fruit than in twigs. Scales in fruit were parasitized at similar levels by the different parasitoid species whereas E. perniciosi was more active in twigs. Data eventually reveal the recent displacement of A. chrysomphali by A. melinus. The implications of these results on the biological control of A. aurantii are discussed and this information will be useful in the decision of IPM strategies for this pest.

Keywords


biological control; Aonidiella aurantii; climatic conditions; Encarsia perniciosi

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References


Abdelrahman I, 1974. Growth, development and innate capacity for increase in Aphytis chrysomphali Mercet and A. melinus DeBach, parasites de California red scale, Aonidiella aurantii (Mask.), in relation to temperature. Aust J Zool 22: 213-230. http://dx.doi.org/10.1071/ZO9740213

Asplanato G, García-Marí F, 2002. Parasitismo de la cochinilla roja californiana Aonidiella aurantii (Homoptera: Diaspididae) en la zona citrícola sur de Uruguay. Bol SanVeg Plagas 28: 5-20.

Atkinson PR, 1977. Preliminary analysis of a field population of citrus red scale, Aonidiella aurantii (Maskell), and the measurement and expression of stage duration and reproduction for life tables. B Entomol Res 67: 65-87. http://dx.doi.org/10.1017/S0007485300010907

Chapin III FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Salal OE, Hobbie SE, Mack MC, Diaz S, 2000. Consequences of changing biodiversity. Nature 405: 234-242. http://dx.doi.org/10.1038/35012241

Dahms EC, Smith D, 1994. The Aphytis fauna of Australia. In: Advances in the study of Aphytis (Hymenoptera: Aphelinidae) (Rosen ed.). Intercept, Andover, pp: 245-255.

Davis AJ, Jenkinson, LS, Lawton JH, Shorrocks B, Wood S, 1998. Making mistakes when predicting shifts in species range in response to global warming. Nature 391: 783-786. http://dx.doi.org/10.1038/35842

DeBach D, Sisojevic P, 1960. Some effects of temperature and competition on the distribution and relative abundance of A. lingnanesis and A. chrysomphali (Hymenoptera: Aphelinidae). Ecology 41: 153-160. http://dx.doi.org/10.2307/1931948

DeBach P, Argyriou LC, 1967. The colonization and success in Greece of some imported Aphytis spp. (Hym. Aphelinidae) parasitic on citrus scale insects (Hom. Diaspididae). Entomophaga 12: 325-342. http://dx.doi.org/10.1007/BF02376919

DeBach P, Rosen D, Kennet CE, 1969. Biological control of coccids by introduced natural enemies. In: Biological control. Ed. Huffaker CB, Proceedings of AAS Symposium, Massachusetts, pp: 165-194.

Furness GO, Buchanan GA, George R, Richardson NL, 1983. A history of the biological control of red scale, Aonidiella aurantii on citrus in the lower Murray Valley of Australia. Entomophaga 28: 199–212. http://dx.doi.org/10.1007/BF02372170

García-Mercet R, 1912. Un parásito del "poll-roig". Bol R Soc esp Hist Nat 12: 125-140.

García-Mercet R, 1921. Fauna Ibérica. Himenópteros. Familia Encírtidos. Museo Nacional de Ciencias Naturales, Madrid. http://dx.doi.org/10.5962/bhl.title.10362

García-Mercet R, 1930. Los Afelínidos de Espa-a. Revista de Biología y Limnología 2: 29-106.

Hance T, van Baaren J, Vernon P, Boivin G, 2007. Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52: 107-126. http://dx.doi.org/10.1146/annurev.ento.52.110405.091333

Heraty J, Woolley J, Polaszek A, 2007. Catalog of the Encarsia of the World. University of California, Riverside. Available in http://www.faculty.ucr.edu/~heraty/Encarsia.cat.pdf. [01 March 2010].

Jacas JA, Urbaneja A, 2010. Biological control in citrus in Spain: From classical to conservation biological control. In: Integrated management of arthropod pests and insect borne diseases. (Ciancio A & Mukerji KG, eds.). Springer, NL, pp: 57-68.

Limón F, Meliá A, Blasco J, Moner P, 1976. Estudio de la distribución, nivel de ataque y parásitos de las cochinillas diaspinas Chrysomphalus dictyospermi Morgan y Parlatoria pergandii Comst. En cítricos de la provincia de Castellón. Bol Serv Plagas 2: 73-87.

Meliá A, Blasco J, 1980. Los cóccidos perjudiciales a los cítricos de Castellón, y sus parasitos. Fruits 35: 551-554.

Noyes JS, 2003. Universal Chalcidoidea Database. The Trustees of the Natural History Museum, London. Available in http://www.nhm.ac.uk/research-curation/research/projects/chalcidoids/. [01 March 2010].

Parmesan C, 2006. Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37: 637-369. http://dx.doi.org/10.1146/annurev.ecolsys.37.091305.110100

Parmesan C, Yohe G, 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42. http://dx.doi.org/10.1038/nature01286

Pimm SL, 2001. Entrepreneurial insects. Nature 411: 531-532. http://dx.doi.org/10.1038/35079206

Pina T, Martínez B, Verdú MJ, 2003. Field parasitoids of Aonidiella aurantii (Homoptera: Diaspididae) in Valencia (Spain). IOBC wprs Bulletin 26: 109-115.

Pina T, Verdú MJ, 2007a. Establecimiento y dispersión de Aphytis melinus y A. lingnanensis (Hym.: Aphlenidiae), dos parasitoides introducidos para el control de Chrysomphalus dictyospermi Morgan y Aonidiella aurantii (Maskell) (Hem.: Diaspididae) en cítricos de la Comunidad Valenciana. Bol San Veg Plagas 33: 311-320.

Pina T, Verdú MJ, 2007b. El piojo rojo de California, Aonidiella aurantii (Maskell), y sus parasitoides en cítricos de la Comunidad Valenciana. Bol San Veg Plagas 33: 357-368.

Rodrigo E, Troncho P, García-Marí F, 1996. Parasitoids (Hym.: Aphelinidae) of three scale insects (Hom.: Diaspididae) in a citrus grove in Valencia, Spain. Entomophaga 41: 77-94. http://dx.doi.org/10.1007/BF02893295

Rosen D, 1994. Fifteen years of Aphytis research – an update. In: Advances in the study of Aphytis (Hymenoptera: Aphelinidae) (Rosen D, ed.). Intercept, Andover, pp: 3-9.

Samways MJ, 1985. Relationship between red scale, Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae), and its natural enemies in the upper and lower parts of citrus trees in South Africa. B Entomol Res 75: 379-393. http://dx.doi.org/10.1017/S0007485300014498

Siscaro G, Longo S, Lizzio S, 1999. Ruolo degli entomofagi di Aonidiella aurantii (Maskell) (Homoptera: Diaspididae) in agrumeti siciliani. Phytophaga 9: 52.

Sorribas JJ, Rodríguez E, Rodrigo E, García-Marí F, 2008. Niveles de parasitismo y especies de parasitoides del piojo rojo de California Aonidiella aurantii (Hemiptera: Diaspididae) en cítricos de la Comunidad Valenciana. Bol San Veg Plagas 34: 201-210.

Sorribas J, Rodríguez R, García-Marí F, 2010. Parasitoid competitive displacement and coexistence in citrus agroecosystems: linking species distribution with climate. Ecol Appl 20: 1101-1113. http://dx.doi.org/10.1890/09-1662.1

Tena A, Llácer E, Urbaneja A, 2013a. Biological control of a non-honeydew producer mediated by a distinct hierarchy of honeydew quality. Biol Control 67: 117-122. http://dx.doi.org/10.1016/j.biocontrol.2013.07.018

Tena A, Pekas A, Wäckers FL, Urbaneja A, 2013b. Parasitoids depend on non-host honeydew producers to cover their energetic needs. Ecol Entomol 38: 278-289. http://dx.doi.org/10.1111/een.12018

Urbaneja A, Catalán A, Tena A, Jacas JA, 2014. Gestión integrada de plagas y enfermedades de cítricos. Instituto Valenciano de Investigaciones Agrarias, Valencia. Available in http://www.gipcitricos.es. [21 January 2014].

Vacas S, Vanaclocha P, Alfaro C, Primo J, Verdú MJ, Urbaneja A, Navarro-Llopis V, 2012. Mating disruption for the control of Aonidiella aurantii Maskell (Hemiptera: Diaspididae) may contribute to increased effectiveness of natural enemies. Pest Manag Sci 68: 142-148. http://dx.doi.org/10.1002/ps.2239

Van Nouhuys S, Lei G, 2004. Parasitoid–host metapopulation dynamics: the causes and consequences of phenological asynchrony. J Anim Ecol 73: 526-535. http://dx.doi.org/10.1111/j.0021-8790.2004.00827.x

Vanaclocha P, Urbaneja A, Verdú MJ, 2009. Mortalidad natural del piojo rojo de California, Aonidiella aurantii, en cítricos de la Comunidad Valenciana y sus parasitoides asociados. Bol San Veg Plagas 35: 59-71.

Vanaclocha P, Vacas S, Alfaro C, Primo J, Verdú MJ, Navarro-Llopis V, Urbaneja A, 2012. Life history parameters and scale cover surface area of Aonidiella aurantii are altered in a mating disruption environment: implications for biological control. Pest Manag Sci 68: 1092-1097. http://dx.doi.org/10.1002/ps.3273

Vanaclocha P, Papacek D, Monzó C, Verdú MJ, Urbaneja A, 2013a. Intra-guild interactions between the parasitoid Aphytis lingnanensis and the predator Chilocorus circumdatus: implications for the biological control of armoured scales. Biol Control 65: 169-175. http://dx.doi.org/10.1016/j.biocontrol.2013.02.008

Vanaclocha P, Vidal-Quist C, Oheix S, Montón H, Planes L, Catalán J, Tena A, Verdú MJ, Urbaneja A, 2013b. Acute toxicity in laboratory tests of fresh and aged residues of pesticides used in citrus on the parasitoid Aphytis melinus. J Pest Sci 86: 329-336. http://dx.doi.org/10.1007/s10340-012-0448-8

Viggiani G, 1990. Endoparasites. In: Armored scale insects, their biology, natural enemies and control. Vol 4B (Rosen D, ed.). Elsevier, Amsterdam, pp: 121-132.

Viggiani G, 1994. The Aphytis fauna of the West Palearctic region, with notes on their role in biological control. In: Advances in the study of Aphytis (Hymenoptera: Aphelinidae) (Rosen D, ed.). Intercept, Andover, pp: 335-347.

Yu DS, Luck RF, Murdoch WW, 1990. Competition, resource partitioning and coexistence of an endoparasitoid Encarsia perniciosi and an ectoparasitoid Aphytis melinus of the California red scale. Ecol Entomol 15: 469-480. http://dx.doi.org/10.1111/j.1365-2311.1990.tb00830.x




DOI: 10.5424/sjar/2014121-5266