Impact of the Invasive Argentine Ant in Citrus Agroecosystems: Effects on the Diversity and Frequency of Native Ant Species Foraging on Tree Canopy
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Area and Experimental Design
2.2. Ant Sampling and Identification
2.3. Data Analysis
3. Results
3.1. Ant Communities
3.2. Seasonal Patterns
4. Discussion
4.1. Ant Community Structure
4.2. Seasonal Patterns
4.3. Implications for Citrus Pest Management
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Appendix A
Appendix B
Appendix C
References
- Kenis, M.; Auger-Rozenberg, M.A.; Roques, A.; Timms, L.; Péré, C.; Cock, M.J.W.; Settele, J.; Augustin, S.; Lopez-Vaamonde, C. Ecological effects of invasive alien insects. Biol. Invasions 2009, 11, 21–45. [Google Scholar] [CrossRef]
- McGlynn, T.P. The worldwide transfer of ants: Geographical distribution and ecological invasions. J. Biogeogr. 1999, 26, 535–548. [Google Scholar] [CrossRef]
- Wetterer, J.K. Geographic origin and spread of cosmopolitan ants (Hymenoptera: Formicidae). Halteres 2015, 6, 66–78. [Google Scholar]
- Holway, D.A.; Lach, L.; Suarez, A.V.; Tsutui, N.D.; Case, T.J. The causes and consequences of ant invasions. Annu. Rev. Ecol. Syst. 2002, 33, 181–233. [Google Scholar] [CrossRef] [Green Version]
- Wetterer, J.K.; Wild, A.L.; Suarez, A.V.; Roura-Pascual, N.; Espadaler, X. Worldwide spread of the Argentine ant, Linepithema humile (Hymenoptera: Formicidae). Myrmecol. News 2009, 12, 187–194. [Google Scholar]
- Ward, P.S. Distribution of the introduced Argentine ant (Iridomyrmex humilis) in natural habitats of the lower Sacramento valley and its effects on the indigenous ant fauna. Hilgardia 1987, 55, 1–16. [Google Scholar] [CrossRef] [Green Version]
- Hölldobler, B.; Wilson, E.O. The Ants; Springer: Berlin/Heidelberg, Germany, 1990. [Google Scholar]
- Cammell, M.E.; Way, M.J.; Paiva, M.R. Diversity and structure of ant communities associated with oak, pine, eucalyptus and arable habitats in Portugal. Insectes Soc. 1996, 43, 37–46. [Google Scholar] [CrossRef]
- Carpintero, S.; Reyes-López, J. The role of competitive dominance in the invasive ability of the Argentine ant (Linepithema humile). Biol. Invasions 2008, 10, 25–35. [Google Scholar] [CrossRef]
- Gao, Y.; Reitz, S.R. Emerging themes in our understanding of species displacements. Annu. Rev. Entomol. 2016, 62, 165–183. [Google Scholar] [CrossRef]
- Rice, E.S.; Silverman, J. Propagule pressure and climate contribute to the displacement of Linepithema humile by Pachycondyla chinensis. PLoS ONE 2013, 8, e56281. [Google Scholar] [CrossRef] [Green Version]
- Lach, L.; Hooper-Bùi, L.M. Consequences of ant invasions. In Ant Ecology; Lach, L., Parr, C., Abbott, K., Eds.; University Press: Oxford, UK, 2010; pp. 261–286. [Google Scholar]
- Oliveras, J.; Bas, J.M.; Casellas, D.; Gómez, C. Numerical dominance of the Argentine ant vs native ants and consequences on soil resource searching in Mediterranean cork-oak forests (Hymenoptera: Formicidae). Sociobiology 2005, 45, 1–16. [Google Scholar]
- Walters, A.C. Invasion of the Argentine ants (Hymenoptera, Formicidae) in South Australia: Impacts on community composition and abundance of invertebrates in urban parklands. Austral Ecol. 2006, 31, 367–376. [Google Scholar] [CrossRef]
- Rowles, A.D.; O’Dowd, D.J. Impacts of the invasive Argentine ant on native ants and other invertebrates in coastal scrub in south-eastern Australia. Austral Ecol. 2009, 34, 239–248. [Google Scholar] [CrossRef]
- Devenish, A.J.M.; Gomez, C.; Bridle, J.R.; Newton, R.J.; Summer, S. Invasive ants take and squander native seeds: Implications for native plant communities. Biol. Invasions 2019, 21, 451–466. [Google Scholar] [CrossRef] [Green Version]
- Menke, S.B.; Ward, P.S.; Holway, D.A. Long-term record of Argentine ant invasions reveals enduring ecological impacts. Ecology 2018, 99, 1194–1202. [Google Scholar] [CrossRef] [PubMed]
- Cerdá, X.; Palacios, R.; Retana, J. Ant community structure in citrus orchards in the Mediterranean Basin: Impoverishment as a consequence of habitat homogeneity. Environ. Entomol. 2009, 38, 317–324. [Google Scholar] [CrossRef] [Green Version]
- FAO. Citrus Fruit Fresh and Processed. Statistical Bulletin 2016; Food and Agriculture Organization of the United Nations: Rome, Italy, 2017. [Google Scholar]
- Pekas, A.; Tena, A.; Aguilar, A.; Garcia-Marí, F. Spatio-temporal patterns and interactions with honeydew-producing Hemiptera of ants in a Mediterranean citrus orchard. Agric. For. Entomol. 2011, 13, 89–97. [Google Scholar] [CrossRef]
- Zina, V.; Branco, M.; Franco, J.C. Ant community associated to citrus canopy in Southern Portugal over a century after the invasion by the Argentine ant. Phytoparasitica 2017, 45, 183–200. [Google Scholar] [CrossRef]
- Samways, M.J. Community structure of ants (Hymenoptera: Formicidae) in a series of habitats associated with citrus. J. Appl. Ecol. 1983, 20, 833–847. [Google Scholar] [CrossRef]
- Queiroz, J.M.; Oliveira, P.S. Tending ants protect honeydew-producing whiteflies (Homoptera: Aleyrodidae). Environ. Entomol. 2001, 30, 295–297. [Google Scholar] [CrossRef] [Green Version]
- Buckley, R.; Gullan, P. More aggressive ant species (Hymenoptera: Formicidae) provide better protection for soft scales and mealybugs (Homoptera: Coccidae, Pseudococcidae). Biotropica 1991, 23, 282–286. [Google Scholar] [CrossRef]
- Franco, J.C.; Silva, E.B.; Carvalho, J.P. Cochonilhas-Algodão (Hemiptera, Pseudococcidae) Associadas Aos Citrinos em Portugal; ISA Press: Lisbon, Portugal, 2000. [Google Scholar]
- Gullan, P.J. Relationships with ants. In Soft Scale Insects—Their Biology, Natural Enemies and Control; Ben-Dov, Y., Hodgson, C.J., Eds.; Elsevier Science: Amsterdam, The Netherlands, 1997; pp. 351–377. [Google Scholar]
- Bodenheimer, F.S. Citrus Entomology in the Middle East with Special References to Egypt, Iran, Irak, Palestine, Syria, Turkey; Dr. W. Junk Publishers: The Hague, The Netherlands, 1951. [Google Scholar]
- Ben-Dov, Y. Relationships with ants. In Armored Scale Insects—Their Biology, Natural Enemies and Control; Rosen, D., Ed.; Elsevier: Amsterdam, The Netherlands, 1990; pp. 339–343. [Google Scholar]
- Martínez-Ferrer, M.T.; Grafton-Cardwell, E.; Shorey, H.H. Disruption of parasitism of the California red scale (Homoptera: Diaspididae) by three ant species (Hymenoptera: Formicidae). Biol. Control. 2003, 26, 279–286. [Google Scholar] [CrossRef]
- Franco, J.C.; Garcia-Marí, F.; Ramos, A.P.; Besri, M. Survey of the situation of citrus pest management in Mediterranean countries. IOBC WPRS Bull. 2006, 29, 335–346. [Google Scholar]
- OPMP. A National Road Map for Integrated Pest Management. United States Department of Agriculture, Office of Pest Management Policy. 2018. Available online: https://www.ars.usda.gov/arsuserfiles/opmp/ipm%20road%20map%20final.pdf (accessed on 10 August 2020).
- Martins, M.N. Une fourmi terrible envahissant l’Europe (Iridomyrmex humilis Mayr). Brotéria Series Zoologia 1907, 6, 101–102. [Google Scholar]
- Coutinho, M.P. A “formiga-argentina” “Iridomyrmex humilis” Mayr “var. arrogans” Santschi. B Minist. Agric. 1929, 11, 95–116. [Google Scholar]
- Robinson, E.J.H. Polydomy: The organization and adaptive function of complex nest system in ants. Curr. Opin. Insect. Sci. 2014, 5, 37–43. [Google Scholar] [CrossRef] [Green Version]
- Heller, N.E.; Sanders, N.J.; Gordon, D.M. Linking temporal and spatial scales in the study of an Argentine ant invasion. Biol. Invasions 2006, 8, 501–507. [Google Scholar] [CrossRef] [Green Version]
- McGlynn, T.P. The ecology of nest movement in social insects. Annu. Rev. Entomol. 2012, 57, 291–308. [Google Scholar] [CrossRef] [Green Version]
- Koop, E.; Sobral, M.; Soares, T.; Woerner, M. Os Solos do Algarve e as Suas Características; Vista Geral Direcção Regional de Agricultura do Algarve: Faro, Portugal, 1989. [Google Scholar]
- Chong, C.S.; Hoffmann, A.A.; Thomson, L.J. Commercial agrochemical applications in vineyards do not influence ant communities. Environ. Entomol. 2007, 36, 1374–1383. [Google Scholar] [CrossRef]
- King, J.R.; Porter, S.D. Evaluation of sampling methods and species richness estimators for ants in upland ecosystems in Florida. Environ. Entomol. 2005, 34, 1566–1578. [Google Scholar] [CrossRef] [Green Version]
- Gotelli, N.J.; Colwell, R.K. Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 2011, 4, 379–391. [Google Scholar] [CrossRef] [Green Version]
- Martínez-Ferrer, M.T.; Campos-Rivela, J.M. Diversity, spatial distribution, and sampling for ant management decision-making in integrated pest management programs in citrus groves. Entomol. Exp. Appl. 2017, 162, 251–260. [Google Scholar] [CrossRef] [Green Version]
- Dunn, R.R.; Guénard, B.; Weiser, M.D.; Sanders, N. Geographic gradients. In Ant Ecology; Lach, L., Parr, C.L., Abbott, K.L., Eds.; Oxford University Press: Oxford, UK, 2010; pp. 38–58. [Google Scholar]
- Collingwood, C.; Prince, A. A guide to ants of continental Portugal (Hymenoptera: Formicidae). B Soc. Port. Entomol. 1998, 5, 1–49. [Google Scholar]
- Gómez, K.; Espadaler, X. Hormigas Ibéricas. 2007. Available online: http://www.hormigas.org (accessed on 15 November 2016).
- IBM Corp. IBM SPSS Statistics for Windows, Version 25.0; IBM Corp: Armonk, NY, USA, 2017. [Google Scholar]
- R Studio Team. RStudio: Integrated Development for R; RStudio Inc.: Boston, MA, USA, 2015. [Google Scholar]
- Van den Brink, P.J.; Van den Brink, N.W.; Ter Braak, C.J.F. Multivariate analysis of ecotoxicological data using ordination: Demonstrations of utility on the basis of various examples. Australas J. Ecotox. 2003, 9, 141–156. [Google Scholar]
- Van den Brink, P.J.; Ter Braak, C.J.F. Principal response curves: Analysis of time-dependent multivariate responses of biological community to stress. Environ. Toxicol. Chem. 1999, 18, 138–148. [Google Scholar] [CrossRef]
- Del Toro, I.; Ribbons, R.R.; Shannon, L.P. The little things that run the world revisited: A review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecol. News 2012, 17, 133–146. [Google Scholar]
- Vanaclocha, P.; Monzó, C.; Gómez, K.; Tortosa, D.; Pina, T.; Castañera, P.; Urbaneja, A. Hormigas (Hymenoptera: Formicidae) presentes en el suelo de los cítricos de la provincia de Valencia. Phytoma 2005, 171, 14–24. [Google Scholar]
- Alvis, L.; Garcia-Marí, F. Identification and abundance of ants (Hymenoptera: Formicidae) in citrus trees from Valencia (Spain). IOBC WPRS Bull. 2006, 29, 111–116. [Google Scholar]
- Urbaneja, A.; Garcia-Marí, F.; Tortosa, D.; Navarro, C.; Vanaclocha, P.; Bargues, L.; Castañera, P. Influence of ground predator on the survival of the Mediterranean fruit fly pupae, Ceratitis capitata, in Spanish citrus orchards. BioControl 2006, 51, 611–626. [Google Scholar] [CrossRef]
- La Pergola, A.; Alicata, A.; Longo, S. Survey of the ants (Hymenoptera, Formicidae) in citrus orchards with different types of crop management in Sicily. Control Citrus Fruit Crop. IOBC WPRS Bull. 2008, 38, 233–237. [Google Scholar]
- Calabuig, A.; Garcia-Marí, F.; Pekas, A. Ants in citrus: Impact on the abundance, species richness, diversity and community structure of predators and parasitoids. Agric. Ecosyst. Environ. 2015, 213, 178–185. [Google Scholar] [CrossRef]
- Wetterer, J.K.; Wetterer, A.L.; Hebard, E. Impact of the Argentine ant, Linepithema humile on the native ants of Santa Cruz Island, California. Sociobiology 2001, 38, 709–721. [Google Scholar]
- Arnan, X.; Andersen, A.N.; Gibb, H. Dominance-diversity relationships in ant communities differ with invasion. Glob. Chang. Biol. 2018, 24, 4614–4625. [Google Scholar] [CrossRef]
- Abril, S.; Gómez, C. Ascertaining key factors behind the coexistence of the native ant species Plagiolepis pygmaea with the invasive Argentine ant Linepithema humile (Hymenoptera: Formicidae). Sociobiology 2009, 53, 559–568. [Google Scholar]
- Roura-Pascual, N.; Bas, J.M.; Hui, C. The spread of the Argentine ant: Environmental determinants and impacts on native ant communities. Biol. Invasions 2010, 12, 2399–2412. [Google Scholar] [CrossRef]
- Human, K.G.; Gordon, D.M. Behavioral interactions of the invasive Argentine ant with native ant species. Insectes Soc. 1999, 46, 159–163. [Google Scholar] [CrossRef]
- Holway, D.A. Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 1999, 80, 238–251. [Google Scholar] [CrossRef]
- Blight, O.; Provost, E.; Renucci, M.; Tirard, A.; Orgeas, J. A native ant armed to limit the spread of the Argentine ant. Biol. Invasions 2010, 12, 3785–3793. [Google Scholar] [CrossRef]
- Castro-Cobo, S.; Carpintero, S.; Reyes-López, J.L.; Sergio, F.; Angulo, E. Humans and scavenging raptors facilitate Argentine ant invasion in Doñana National Park: No counter-effect of biotic resistance. Biol. Invasions 2019, 21, 2221–2232. [Google Scholar] [CrossRef]
- Way, M.J.; Cammell, M.E.; Paiva, M.R.; Collingwood, C.A. Distribution and dynamics of the Argentine ant Linepithema (Iridomyrmex) humile (Mayr) in relation to vegetation, soil conditions, topography and native competitor ants in Portugal. Insect Soc. 1997, 44, 415–433. [Google Scholar] [CrossRef]
- Rust, M.K.; Reierson, D.A.; Paine, E.; Blum, L.J. Seasonal activity and bait preferences of the Argentine ant (Hymenoptera: Formicidae). J. Agric. Urban Entomol. 2000, 17, 201–212. [Google Scholar]
- Davidson, D.W. Resource discovery versus resource domination in ants: A functional mechanism for breaking the trade-off. Ecol. Entomol. 1998, 23, 484–490. [Google Scholar] [CrossRef]
- Centorame, M.; Lancia, A.; Mori, E.; D’Eustacchio, D.; Fanfani, A. Could Linepithema humile (Hymenoptera, Formicidae) influence ant community composition? A preliminary study in a natural area in Italy. Redia 2017, 100, 89–94. [Google Scholar]
- Sanders, N.J.; Barton, K.E.; Gordon, D.M. Long-term dynamics of the distribution of the invasive Argentine ant, Linepithema humile, and native ant taxa in northern California. Oecologia 2001, 127, 123–130. [Google Scholar] [CrossRef] [PubMed]
- Parker, I.M.; Simberloff, D.; Lonsdale, W.M.; Goodell, K.; Wonham, M.; Kareiva, P.M.; Williamson, M.H.; Von Holle, B.; Moyle, P.B.; Byers, J.E.; et al. Impact: Toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1999, 1, 3–19. [Google Scholar] [CrossRef]
- Mestre, L.; Piñol, J.; Barrientos, J.A.; Espadaler, X. Differential ant exclusion from canopies shows contrasting top-down effects on community structure. Oecologia 2016, 180, 193–203. [Google Scholar] [CrossRef]
- Diaz, M.; Abril, S.; Enriquez, M.L.; Gómez, C. Assessment of the Argentine ant invasion management by means of manual removal of winter nests in mixed cork oak and pine forests. Biol. Invasions 2014, 16, 315–327. [Google Scholar] [CrossRef]
- Carvalho, J.P.; Ilharco, F.A.; Ferreira, M.A.; Carvalho, M.U.P. Manual de Pragas e Sintomas do Ataque de Insectos e Ácaros em Citrinos; Estação Agronómica Nacional: Oeiras, Portugal, 1999. [Google Scholar]
- James, D.G.; Stevens, M.M.; O’Malley, K.J. The impact of foraging ants on populations of Coccus hesperidum L. (Hem., Coccidae) and Aonidiella aurantii (Maskell) (Hem., Diaspididae) in an Australian citrus grove. J. Appl. Ent. 1997, 121, 257–259. [Google Scholar] [CrossRef]
- James, D.G.; Stevens, M.M.; O’Malley, K.J.; Faulder, R.J. Ant foraging reduces the abundance of beneficial and incidental arthropods in citrus canopies. Biol. Control 1999, 14, 121–126. [Google Scholar] [CrossRef]
- Smith, D.; Beattie, G.A.C.; Broadley, R. Citrus Pests and Their Natural Enemies: Integrated Pest Management in Australia; Desert Oak Publishing Services: Brisbane, Australia, 1997. [Google Scholar]
- Calabuig, A.; Garcia-Marí, F.; Pekas, A. Ants affect the infestation levels but not the parasitism of honeydew and non-honeydew producing pests in citrus. Bull. Entomol. Res. 2014, 104, 405–417. [Google Scholar] [CrossRef]
- Benfradj, N.; Vettraino, A.M.; Tomassini, A.; Bruni, N.; Vannini, A.; Boughalleb-M’Hamdi, N. Citrus gummosis incidence and role of ants (Lasius grandis) and snails (Helix aspersa) as vectors of the disease in Tunisia. For. Pathol. 2018, 48, e12423. [Google Scholar] [CrossRef]
- Buczkowski, G.; Mothapo, N.P.; Wossler, T.C. Let them eat termites—Prey-baiting provides effective control of Argentine ants, Linepithema humile, in a biodiversity hotspot. J. Appl. Entomol. 2018, 142, 504–512. [Google Scholar] [CrossRef]
Subfamily | Number of Specimens | Number of Orchards in Which Each Ant Species Was Found | ||||||
---|---|---|---|---|---|---|---|---|
Uninvaded Orchards (N = 12) | Invaded Orchards (N = 12) | Uninvaded Orchards (N = 12) | Invaded Orchards (N = 12) | |||||
Ant Species | ||||||||
N | % | N | % | N | % | N | % | |
Dolichoderinae | ||||||||
Linepithema humile | 0 | 0 | 5153 | 86.37 | 0 | 0 | 12 | 100 |
Tapinoma madeirense | 22 | 0.44 | 0 | 0 | 2 | 16.67 | 0 | 0 |
Tapinoma nigerrimum | 835 | 16.82 | 2 | 0.03 | 8 | 66.67 | 1 | 8.33 |
Tapinoma simrothi | 32 | 0.64 | 7 | 0.12 | 6 | 50.00 | 1 | 8.33 |
Formicinae | ||||||||
Camponotus gestroi | 0 | 0 | 1 | 0.02 | 0 | 0 | 1 | 8.33 |
Camponotus lateralis | 6 | 0.12 | 0 | 0 | 1 | 8.33 | 0 | 0 |
Camponotus micans | 25 | 0.50 | 0 | 0 | 1 | 8.33 | 0 | 0 |
Camponotus sylvaticus | 12 | 0.24 | 3 | 0.05 | 4 | 33.33 | 1 | 8.33 |
Formica cunicularia | 24 | 0.48 | 0 | 0 | 2 | 16.67 | 0 | 0 |
Lasius grandis | 2099 | 42.28 | 0 | 0 | 10 | 83.33 | 0 | 0 |
Plagiolepis pygmaea | 1159 | 23.35 | 783 | 13.12 | 10 | 83.33 | 12 | 100 |
Plagiolepis schmitzii | 224 | 4.51 | 3 | 0.05 | 7 | 58.33 | 2 | 16.67 |
Myrmicinae | ||||||||
Aphaenogaster senilis | 4 | 0.08 | 0 | 0 | 2 | 16.67 | 0 | 0 |
Crematogaster auberti | 41 | 0.83 | 4 | 0.07 | 2 | 16.67 | 1 | 8.33 |
Crematogaster scutellaris | 33 | 0.66 | 1 | 0.02 | 4 | 33.33 | 1 | 8.33 |
Crematogaster sordidula | 56 | 1.13 | 9 | 0.15 | 3 | 25.00 | 1 | 8.33 |
Messor barbarus | 4 | 0.08 | 0 | 0 | 3 | 25.00 | 0 | 0 |
Pheidole pallidula | 388 | 7.82 | 0 | 0 | 8 | 66.67 | 0 | 0 |
Total Number of Specimens (N) | 4964 | 5966 | ||||||
Species Richness (S) | 16 | 10 |
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Zina, V.; Branco, M.; Franco, J.C. Impact of the Invasive Argentine Ant in Citrus Agroecosystems: Effects on the Diversity and Frequency of Native Ant Species Foraging on Tree Canopy. Insects 2020, 11, 785. https://doi.org/10.3390/insects11110785
Zina V, Branco M, Franco JC. Impact of the Invasive Argentine Ant in Citrus Agroecosystems: Effects on the Diversity and Frequency of Native Ant Species Foraging on Tree Canopy. Insects. 2020; 11(11):785. https://doi.org/10.3390/insects11110785
Chicago/Turabian StyleZina, Vera, Manuela Branco, and José Carlos Franco. 2020. "Impact of the Invasive Argentine Ant in Citrus Agroecosystems: Effects on the Diversity and Frequency of Native Ant Species Foraging on Tree Canopy" Insects 11, no. 11: 785. https://doi.org/10.3390/insects11110785
APA StyleZina, V., Branco, M., & Franco, J. C. (2020). Impact of the Invasive Argentine Ant in Citrus Agroecosystems: Effects on the Diversity and Frequency of Native Ant Species Foraging on Tree Canopy. Insects, 11(11), 785. https://doi.org/10.3390/insects11110785