Hostname: page-component-76fb5796d-5g6vh Total loading time: 0 Render date: 2024-04-25T14:25:48.675Z Has data issue: false hasContentIssue false
  • English
  • Français

Ants affect the infestation levels but not the parasitism of honeydew and non-honeydew producing pests in citrus

Published online by Cambridge University Press:  13 November 2013

A. Calabuig ,
F. Garcia-Marí  and
A. Pekas
A. Calabuig*
Affiliation:
Instituto Agroforestal Mediterráneo (IAM), Universitat Politècnica de València, Camí de Vera s/n, 46022, València, Spain
F. Garcia-Marí
Affiliation:
Instituto Agroforestal Mediterráneo (IAM), Universitat Politècnica de València, Camí de Vera s/n, 46022, València, Spain
A. Pekas
Affiliation:
Instituto Agroforestal Mediterráneo (IAM), Universitat Politècnica de València, Camí de Vera s/n, 46022, València, Spain Biobest Belgium N.V., R&D Department, Ilse Velden 18, 2260 Westerlo, Belgium
*
*Author for correspondence Phone: +34651995119 Fax: +34963877331 E-mail: alteac@outlook.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Ants act simultaneously as predators and as hemipteran mutualists, and thereby may affect the composition and population dynamics of a wide arthropod community. We conducted ant-exclusion experiments in order to determine the impact of ants on the infestation levels and parasitism of three of the most important citrus pests of western Mediterranean citrus: the honeydew producer Aleurothrixus floccosus Maskell (woolly whitefly) and the non-honeydew producers Aonidiella aurantii Maskell (California red scale; CRS) and Phyllocnistis citrella (Staiton) (citrus leafminer). The study was conducted in three commercial citrus orchards, each one dominated by one ant species (Pheidole pallidula, Lasius grandis or Linepithema humile) during two consecutive growing seasons (2011 and 2012). We registered a significant reduction of the CRS densities on fruits in the ant-excluded treatment in the three orchards and in the two seasons, ranging from as high as 41% to as low as 21%. Similarly, the percentage of shoots occupied by A. floccosus was significantly lower in the ant-excluded plots in the orchards dominated by P. pallidula and L. humile. No significant differences were registered in the percentage of leaf surface loss caused by P. citrella between ant-allowed and ant-excluded treatments in any case. We found no significant differences in the percent parasitism between ant-allowed and ant-excluded treatments for honeydew and non-honeydew producing herbivores. These results suggest that: (i) ant management should be considered in order to reduce herbivore populations in citrus and (ii) mechanisms other than parasitism (e.g., predation) might explain the differences in herbivore infestation levels between treatments.

Keywords

Lasius grandisPheidole pallidulaLinepithema humileAonidiella aurantiiAleurothrixus floccosusPhyllocnistis citrella
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 4 , August 2014 , pp. 405 - 417
Copyright
Copyright © Cambridge University Press 2013 

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

Alvis, L. & Garcia-Marí, F. (2006) Identification and abundance of ants (Hymenoptera: Formicidae) in citrus trees from Valencia (Spain). IOBC-WPRS Bulletin 29(3), 111.Google Scholar
Alvis-Dávila, L. (2003) Identificación y abundancia de artrópodos depredadores en cultivos de cítricos valencianos. Memoria De Tesis Doctoral, Universidad Politécnica de Valencia, Spain.Google Scholar
Arnan, X., Cerdá, X. & Retana, J. (2012) Distinctive life traits and distribution along environmental gradients of dominant and subordinate mediterranean ant species. Oecologia 170(2), 489–500.Google Scholar
Bach, C.E. (1991) Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica). Oecologia 87(2), 233–239.Google Scholar
Bartlett, B. (1961) The influence of ants upon parasites, predators, and scale insects. Annals of the Entomological Society of America 54(4), 543–551.CrossRefGoogle Scholar
Bodenheimer, F.S. (1951) Citrus Entomology in the Middle East with Special References to Egypt, Iran, Irak, Palestine, Syria, Turkey. The Hague, Junk.Google Scholar
Buckley, R. (1987) Interactions involving plants, Homoptera, and ants. Annual Review of Ecology and Systematics 18, 111–135.Google Scholar
Buckley, R. & Gullan, P. (1991) More aggressive ant species (Hymenoptera: Formicidae) provide better protection for soft scales and mealybugs (Homoptera: Coccidae, Pseudococcidae). Biotropica 23(3), 282–286.Google Scholar
Carroll, C. & Janzen, D.H. (1973) Ecology of foraging by ants. Annual Review of Ecology and Systematics 4, 231–257.Google Scholar
Cerdá, X., Palacios, R. & Retana, J. (2009) Ant community structure in citrus orchards in the mediterranean basin: impoverishment as a consequence of habitat homogeneity. Environmental Entomology 38(2), 317–324.Google Scholar
Daane, K.M., Sime, K.R., Fallon, J. & Cooper, M.L. (2007) Impacts of Argentine ants on mealybugs and their natural enemies in California's coastal vineyards. Ecological Entomology 32(6), 583–596.CrossRefGoogle Scholar
Dao, H.T., Meats, A., Beattie, G.A.C., & Spooner-Hart, R. (2013) Ant-coccid mutualism in citrus canopies and its effect on natural enemies of red scale, Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae). Bulletin of Entomological Research 1–6, doi:10.1017/S0007485313000187.Google Scholar
DeBach, P. & Rosen, D. (1991) Biological Control by Natural Enemies. Cambridge, Cambridge University Press.Google Scholar
DeBach, P., Fleschner, C. & Dietrick, E. (1951) A biological check method for evaluating the effectiveness of entomophagous insects. Journal of Economic Entomology 44, 763–766.Google Scholar
Flanders, S.E. (1945) Coincident infestations of Aonidiella citrina and Coccus hesperidum, a result of ant activity. Journal of Economic Entomology 38(6), 711–712.CrossRefGoogle Scholar
Flanders, S.E. (1951) The role of the ant in the biological control of homopterous insects. The Canadian Entomologist 83(04), 93.CrossRefGoogle Scholar
Flanders, S.E. (1958) The role of the ant in the biological control of scale insects in California. Proceedings of the International Entomology Congress, Montréal 4, 579–584.Google Scholar
Font de Mora, R. (1923) Sobre la presencia de la hormiga argentina (Iridomyrmex humilis) en Valencia. Boletín de la Real Sociedad española de Historia natural 23, 77–78.Google Scholar
Garcia-Marí, F. (2012) Plagas de los cítricos. Gestión integrada en países de clima mediterráneo. Spain, Phytoma.Google Scholar
Garcia-Marí, F., Granda, C., Zaragoza, S. & Agustí, M. (2002) Impact of Phyllocnistis citrella (Lepidoptera: Gracillariidae) on leaf area development and yield of mature citrus trees in the mediterranean area. Journal of Economic Entomology 95(5), 966–974.Google Scholar
Garcia-Marí, F., Vercher, R., Costa-Comelles, J., Marzal, C. & Villalba, M. (2004) Establishment of Citrostichus phyllocnistoides (hymenoptera: Eulophidae) as a biological control agent for the citrus leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Spain. Biological Control 29(2), 215–226.Google Scholar
García-Mercet, R. (1923) Sobre la Icerya purchasi y la hormiga argentina. Bolletin De La Real Sociedad Española De Historia Natural 23, 14–15.Google Scholar
Haney, P., Luck, R. & Moreno, D. (1987) Increases in densities of the citrus red mite, Panonychus citri [Acarina: Tetranychidae], in association with the Argentine ant, Iridomyrmex humilis [Hymenoptera: Formicidae], in southern California citrus. Entomophaga 32(1), 49–57.Google Scholar
Heimpel, G.E., Rosenheim, J.A. & Mangel, M. (1997) Predation on adult Aphytis parasitoids in the field. Oecologia 110(3), 346–352.Google Scholar
Hölldobler, B. & Wilson, E.O. (1990) The Ants. Cambridge, Massachusetts, Belknap Press.Google Scholar
Holway, D.A., Lach, L., Suarez, A.V., Tsutsui, N.D. & Case, T.J. (2002) The causes and consequences of ant invasions. Annual Review of Ecology and Systematics 33, 181–233.CrossRefGoogle Scholar
Itioka, T. & Inoue, T. (1996 a) The role of predators and attendant ants in the regulation and persistence of a population of the citrus mealybug Pseudococcus citriculus in a Satsuma orange orchard. Applied Entomology and Zoology 31(2), 195–202.CrossRefGoogle Scholar
Itioka, T. & Inoue, T. (1996 b) The consequences of ant-attendance to the biological control of the red wax scale insect Ceroplastes rubens by Anicetus beneficus . Journal of Applied Ecology 33, 609–618.Google Scholar
Itioka, T. & Inoue, T. (1999) The alternation of mutualistic ant species affects the population growth of their trophobiont mealyhug. Ecography 22(2), 169–177.Google Scholar
James, D., Stevens, M. & O'Malley, K. (1997) The impact of foraging ants on populations of Coccus hesperidum L.(Hem., Coccidae) and Aonidiella aurantii (Maskell) (Hem., Diaspididae) in an Australian citrus grove. Journal of Applied Entomology 121(1–5), 257–259.Google Scholar
James, D.G., Stevens, M.M., O'Malley, K.J., & Faulder, R.J. (1999) Ant foraging reduces the abundance of beneficial and incidental arthropods in citrus canopies. Biological Control 14(2), 121–126.Google Scholar
Janzen, D.H. (1966) Coevolution of mutualism between ants and acacias in Central America. Evolution 20(3), 249–275.Google Scholar
Juan-Blasco, M., Tena, A., Vanaclocha, P., Cambra, M., Urbaneja, A. & Monzó, C. (2010) Efficacy of a micro-encapsulated formulation compared with a sticky barrier for excluding ants from citrus canopies. Journal of Applied Entomology 135(6), 467–472.Google Scholar
Kaneko, S. (2003) Different impacts of two species of aphid-attending ants with different aggressiveness on the number of emerging adults of the aphid's primary parasitoid and hyperparasitoids. Ecological Research 18(2), 199–212.Google Scholar
Kaplan, I. & Eubanks, M.D. (2005) Aphids alter the community-wide impact of fire ants. Ecology 86(6), 1640–1649.CrossRefGoogle Scholar
Karamaouna, F., Pascual-Ruiz, S., Aguilar-Fenollosa, E., Verdú, M., Urbaneja, A. & Jacas, J. (2010) Changes in predation and parasitism of the citrus leafminer Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae) populations in Spain following establishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae). Biological Control 52(1), 37–45.CrossRefGoogle Scholar
Karhu, K.J. (1998) Effects of ant exclusion during outbreaks of a defoliator and a sap-sucker on birch. Ecological Entomology 23(2), 185–194.Google Scholar
Katayama, N. & Suzuki, N. (2003) Bodyguard effects for aphids of Aphis craccivora Koch (Homoptera: Aphididae) as related to the activity of two ant species, Tetramorium caespitum Linnaeus (Hymenoptera: Formicidae) and Lasius niger L. (Hymenoptera: Formicidae). Applied Entomology and Zoology 38(3), 427–433.Google Scholar
Kidd, N. & Jervis, M. (1996) Population dynamics. pp. 316–317 in Jervis, M. & Kidd, N. (Eds) Insect Natural Enemies. Practical Approaches to their Study and Evaluation. London, UK, Chapman & Hall.Google Scholar
Martinez-Ferrer, M.T., Grafton-Cardwell, E.E. & Shorey, H.H. (2003) Disruption of parasitism of the California red scale (Homoptera: Diaspididae) by three ant species (Hymenoptera: Formicidae). Biological Control 26(3), 279–286.Google Scholar
McPhee, K., Garnas, J., Drummond, F. & Groden, E. (2012) Homopterans and an invasive red ant, Myrmica rubra (L.), in Maine. Environmental Entomology 41(1), 59–71.CrossRefGoogle Scholar
Mgocheki, N. & Addison, P. (2009) Interference of ants (Hymenoptera: Formicidae) with biological control of the vine mealybug Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). Biological Control 49(2), 180–185.Google Scholar
Mgocheki, N. & Addison, P. (2010) Spatial distribution of ants (Hymenoptera: Formicidae), vine mealybugs and mealybug parasitoids in vineyards. Journal of Applied Entomology 134(4), 285–295.Google Scholar
Monzó, C., Juan-Blasco, M., Pekár, S., Mollá, Ó., Castañera, P. & Urbaneja, A. (2013) Pre-adaptive shift of a native predator (Araneae, Zodariidae) to an abundant invasive ant species (Hymenoptera, Formicidae). Biological Invasions 15(1), 89–100.CrossRefGoogle Scholar
Moreno, D., Haney, P. & Luck, R. (1987) Chlorpyrifos and diazinon as barriers to Argentine ant (Hymenoptera: Formicidae) foraging on citrus trees. Journal of Economic Entomology 80(1), 208–214.Google Scholar
Murdoch, W.W., Luck, R.F., Swarbrick, S.L., Walde, S., Yu, D.S. & Reeve, J.D. (1995) Regulation of an insect population under biological control. Ecology 76(1), 206–217.Google Scholar
Nagy, C., Cross, J.V., & Markó, V. (2013) Sugar feeding of the common black ant, Lasius niger (L.), as a possible indirect method for reducing aphid populations on apple by disturbing ant-aphid mutualism. Biological Control 65, 24–36.CrossRefGoogle Scholar
Olotu, M.I., Plessis, H., Seguni, Z.S. & Maniania, N.K. (2012) Efficacy of the African weaver ant Oecophylla longinoda (Hymenoptera: Formicidae) in the control of Helopeltis spp. (Hemiptera: Miridae) and Pseudotheraptus wayi (Hemiptera: Coreidae) in cashew crop in Tanzania. Pest Management Science 69, 911–918.Google Scholar
Palacios, R., Martínez-Ferrer, M. & Cerdá, X. (1999) Composición, abundancia y fenología de las hormigas (Hymenoptera: Formicidae) en campos de cítricos de Tarragona. Boletín De Sanidad Vegetal.Plagas 25(2), 229–240.Google Scholar
Paris, C.I. & Espadaler, X. (2009) Honeydew collection by the invasive garden ant Lasius neglectus versus the native ant L. grandis. Arthropod-Plant Interactions 3(2), 75–85.Google Scholar
Pekas, A., Tena, A., Aguilar, A. & Garcia-Marí, F. (2010 a) Effect of Mediterranean ants (Hymenoptera: Formicidae) on California red scale (Hemiptera: Diaspididae) populations in citrus orchards. Environmental Entomology 39(3), 827–834.Google Scholar
Pekas, A., Tena, A., Aguilar, A. & Garcia-Marí, F. (2010 b) Influence of host size on parasitism by Aphytis chrysomphali and A. melinus (Hymenoptera: Aphelinidae) in Mediterranean populations of California red scale Aonidiella aurantii (Hemiptera: Diaspididae). Biological Control 55(2), 132–140.Google Scholar
Pekas, A., Tena, A., Aguilar, A. & Garcia-Marí, F. (2011) Spatio-temporal patterns and interactions with honeydew-producing hemiptera of ants in a Mediterranean citrus orchard. Agricultural and Forest Entomology 13(1), 89–97.Google Scholar
Pina, T., Verdú, M.J., Urbaneja, A. & Sabater-Munoz, B. (2012) The use of integrative taxonomy in determining species limits in the convergent pupa coloration pattern of Aphytis species. Biological Control 61(1), 64–70.Google Scholar
Piñol, J., Espadaler, X., Cañellas, N., Martínez-Vilalta, J., Barrientos, J.A. & Sol, D. (2010) Ant versus bird exclusion effects on the arthropod assemblage of an organic citrus grove. Ecological Entomology 35(3), 367–376.Google Scholar
Piñol, J., Ribes, E., Ribes, J. & Espadaler, X. (2012 a) Long-term changes and ant-exclusion effects on the true bugs (Hemiptera: Heteroptera) of an organic citrus grove. Agriculture Ecosystems and Environment. 158, 127–131.Google Scholar
Piñol, J., Espadaler, X. & Cañellas, N. (2012 b) Eight years of ant-exclusion from citrus canopies: effects on the arthropod assemblage and on fruit yield. Agricultural and Forest Entomology 14(1), 49–57.Google Scholar
Retana, J. & Cerdá, X. (1994) Agonistic relationships among sympatric mediterranean ant species (Hymenoptera: Formicidae). Journal of Insect Behavior 8(3), 365–380.CrossRefGoogle Scholar
Romeu-Dalmau, C., Espadaler, X. & Piñol, J. (2012) Abundance, interannual variation and potential pest predator role of two co-occurring earwig species in citrus canopies. Journal of Applied Entomology 136(7), 501–509.Google Scholar
Rosen, D. & DeBach, P. (1979) Species of Aphytis of the World (Hymenoptera: Aphelinidae). The Hague, Boston, London, Dr. W. Junk.Google Scholar
Rosumek, F.B., Silveira, F.A., de Neves, S.F., de Barbosa, U., Newton, P., Diniz, L., Oki, Y. & Cornelissen, T. (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160(3), 537–549 CrossRefGoogle ScholarPubMed
Samways, M. (1983) Community structure of ants (Hymenoptera: Formicidae) in a series of habitats associated with citrus. Journal of Applied Ecology 20(3), 833–847.CrossRefGoogle Scholar
Samways, M., Nel, M. & Prins, A. (1982) Ants (Hymenoptera: Formicidae) foraging in citrus trees and attending honeydew-producing Homoptera. Phytophylactica 14(4), 155–157.Google Scholar
Schaffer, B., Peña, J.E., Colls, A.M. & Hunsberger, A. (1997) Citrus leafminer (Lepidoptera: Gracillariidae) in lime: assessment of leaf damage and effects on photosynthesis. Crop Protection 16(4), 337–343.CrossRefGoogle Scholar
Seifert, B. (1992) A taxonomic revision of the Palaearctic members of the ant subgenus Lasius s. str. (Hymenoptera, formicidae). Abhandlungen Und Berichte Des Naturkundemuseums Görlitz 66, 1–67.Google Scholar
Soto, A., Ohlenschläger, F. & Garcia-Marí, F. (2001) Population dynamics and biological control of whiteflies Aleurothrixus floccosus, Dialeurodes citri and Parabemisia myricae (Homoptera: Aleyrodidae) in citrus orchards of Valencia (Spain). Boletín De Sanidad Vegetal. Plagas 95(1), 167–173.Google Scholar
Stadler, B. & Dixon, A.F. (2005) Ecology and evolution of aphid-ant interactions. Annual Review of Ecology, Evolution, and Systematics 36, 345–372.Google Scholar
Statgraphics (1994) Statistical Graphics System, Version 5.1 Plus. Rockville, MD, USA, Manugistics.Google Scholar
Steyn, J. (1954) The effect of the cosmopolitan Brown house ant (Pheidole megaecphala F.) on Citrus Red Scale (Aonidiella aurantii Mask.) at Letaba. Journal of the Entomological Society of Southern Africa 17(2), 252–264.Google Scholar
Styrsky, J.D. & Eubanks, M.D. (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proceedings of the Royal Society B: Biological Sciences 274(1607), 151–164.Google Scholar
Suckling, D.M., Peck, R.W., Stringer, L.D., Snook, K., & Banko, P.C. (2010) Trail pheromone disruption of Argentine ant trail formation and foraging. Journal of Chemical Ecology 36(1), 122–128.CrossRefGoogle ScholarPubMed
Townsend, G. & Heuberger, J. (1943) Methods for estimating losses caused by diseases in fungicide experiments. Plant Disease Reporter 27(17), 340–343.Google Scholar
Urbaneja, A., Muñoz, A., Garrido, A. & Jacas, J. (2004) Which role do lacewings and ants play as predators of the citrus leafminer in Spain. Spanish Journal of Agricultura Research 2(3), 377–384.CrossRefGoogle Scholar
Vanaclocha, P., Monzó, C., Gómez, K., Tortosa, D., Pina, T., Castañera, P. & Urbaneja, A. (2005) Hormigas (Hymenoptera: Formicidae) presentes en el suelo de los cítricos de la provincia de Valencia. Phytoma España: La Revista Profesional De Sanidad Vegetal (171), 14–25.Google Scholar
Vanek, S.J. & Potter, D.A. (2010) Ant-exclusion to promote biological control of soft scales (Hemiptera: Coccidae) on woody landscape plants. Environmental Entomology 39(6), 1829–1837.Google Scholar
Van Driesche, R.G. (1983) Meaning of percent parasitism in studies of insect parasitoids. Environmental Entomology 12(6), 1611–1622.Google Scholar
Van Mele, P. & Van Lenteren, J. (2002) Habitat manipulation for improved control of citrus leafminer and mite pests in a mixed orchard-ricefield landscape, Mekong Delta, Vietnam. Agriculture, Ecosystems and Environment 88(1), 35–48.CrossRefGoogle Scholar
Vercher, R., García Marí, F., Costa Comelles, J., Marzal, C. & Granda, C. (2000) Importación y establecimiento de parásitos del minador de hojas de cítricos Phyllocnistis citrella (Lepidoptera: Gracillariidae) Boletín De Sanidad Vegetal . Plagas 26(4), 577–590.Google Scholar
Völkl, W. (1992) Aphids or their parasitoids: who actually benefits from ant-attendance? Journal of Animal Ecology 61, 273–281.Google Scholar
Wäckers, F.L. (2005) Suitability of (extra-) floral nectar, pollen, and honeydew as insect food sources. pp. 17–74 in Wäckers, F.L. van Rijn, P.C.J. & Bruin, J. (Eds), Plant-Provided Food for Carnivorous Insects: A Protective Mutualism and its Applications. Cambridge University Press, Cambridge, UK.Google Scholar
Way, M.J. (1963) Mutualism between ants and honeydew-producing Homoptera. Annual Review of Entomology 8(1), 307–344.CrossRefGoogle Scholar
Yoo, H.J.S. & Holway, D.A. (2011) Context-dependence in an ant–aphid mutualism: direct effects of tending intensity on aphid performance. Ecological Entomology 36(4), 450–458.Google Scholar