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An analysis of mutualistic interactions between exotic ants and honeydew producers in the Yanbaru district of Okinawa Island, Japan

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Ecological Research

Abstract

Invasive exotic ants often have a mutualistic relationship with other insects excreting honeydew, and this is considered to play a key role in their invasion success. We investigated the multispecies association patterns between ants and hemipteran insects in the Yanbaru forests, Okinawa, Japan, an Asian biodiversity hotspot. We especially focused on roadside environments, which are the frontlines of invasion for exotic ants. We found that only a small number of herbaceous and pioneer plants were predominant on the roadsides. Four honeydew producers, Melanaphis formosana, Dysmicoccus sp. A, Heteropsylla cubana, and Sogata hakonensis, living on these roadside plants accounted for 94.9% of the total honeydew-producer aggregations observed. Only a few exotic ants, such as Technomyrmex brunneus and Anoplolepis gracilipes, were observed with these honeydew-producer aggregations, and densities of these ants and honeydew producers were often positively correlated. An ant exclusion experiment showed that exotic ant occurrence improved the survival of some of the hemipteran colonies. Interestingly, the abundance of native ants was not correlated with the abundance of honeydew producers, and the local density of Pheidole noda was negatively correlated with that of M. formosana. These findings, i.e., only a few ants, all exotic, tended to hemipteran honeydew producers despite the existence of many native ants, and the abundances of those exotic ants and those hemipteran insects had positive correlations, provide some insights into the mechanism of biological invasion and provide information for the management of exotic ants.

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References

  • Abbott KL, Green PT (2007) Collapse of an ant-scale mutualism in a rainforest on Christmas Island. Oikos 116:1238–1246

    Article  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19:716–723

    Article  Google Scholar 

  • Bach CE (1991) Direct and indirect interactions between ants (Pheidole megacephala), scales (Coccus viridis) and plants (Pluchea indica). Oecologia 87:233–239

    Article  Google Scholar 

  • Boer P, Vierbergen B (2008) Exotic ants in The Netherlands (Hymenoptera: Formicidae). Entomol Ber 68:121–129

    Google Scholar 

  • Bolger DT (2007) Spatial and temporal variation in the Argentine ant edge effect: implications for the mechanism of edge limitation. Biol Conserv 136:295–305

    Article  Google Scholar 

  • Bolton B (2007) Taxonomy of the dolichoderine ant genus Technomyrmex Mayr (Hymenoptera: Formicidae) based on the worker cast. Contrib Am Entomol Inst 35:1–150

    Google Scholar 

  • Braschler B, Lampel G, Baur B (2003) Experimental small-scale grassland fragmentation alters aphid population dynamics. Oikos 100:581–591

    Article  Google Scholar 

  • Clark DB (1982) The exotic ant Wasmannia auropunctata: autecology and effect on ant diversity and distribution on Santa Cruz Island, Galapagos. Biotropica 14:196–207

    Article  Google Scholar 

  • Davidson DW (1998) Resource discovery versus resource domination: a functional mechanism for breaking the trade-off. Ecol Entomol 23:484–490

    Article  Google Scholar 

  • Dunham AE, Mikheyev AS (2009) Influence of an invasive ant on grazing and detrital communities and nutrient fluxes in a tropical forest. Divers Distrib 16:33–42

    Article  Google Scholar 

  • Eguchi K (2001) A revision of the Bornean species of the ant genus Pheidole, Insecta: Hymenoptera: Formicidae: Myrmicinae. Tropics Monogr Ser 2:1–154

    Google Scholar 

  • Forys EA, Allen CR, Wojcik DP (2002) Influence of proximity and amount of human development and roads on the occurrence of the red imported fire ant in the lower Florida Keys. Biol Conserv 108:27–33

    Article  Google Scholar 

  • Fowler HG, Silva CA, Venticinque E (1993) Size, taxonomic and biomass distributions of flying insects in Central Amazonia: forest edge vs understory. Rev Biol Trop 41:755–760

    Google Scholar 

  • González-Hernández H, Johnson MW, Reimer NJ (1999) Impact of Pheidole megacephala (F) (Hymenoptera: Formicidae) on the biological control of Dysmicoccus brevipes (Cockerell) (Homoptera: Pseudococcidae). Biol Control 15:145–152

    Article  Google Scholar 

  • Grover CD, Dayton KC, Menke SB, Holway DA (2008) Effects of aphids on foliar foraging by Argentine ants and the resulting effects on other arthropods. Ecol Entomol 33:101–106

    Google Scholar 

  • Hansen DM, Müller CB (2008) Invasive ants disrupt Gecko pollination and seed dispersal of the endangered plant Roussea simplex in Mauritius. Biotropica 41:202–208

    Article  Google Scholar 

  • Helms KR, Vinson SB (2002) Widespread association of the invasive ant Solenopsis invicta with an invasive mealybug. Ecology 83:2425–2438

    Article  Google Scholar 

  • Hill M, Holm K, Terence V, Shah NJ, Matyot P (2003) Impact of the introduced yellow crazy ant Anoplolepis gracilipes on Bird Island, Seychelles. Biol Conserv 12:1969–1984

    Google Scholar 

  • Hoffmann BD, Andersen AN, Hill GJE (1999) Impact of an introduced ant on native rain forest invertebrates: Pheidole megacephala in monsoonal Australia. Oecologia 120:595–604

    Google Scholar 

  • Holway DA (1998) Effect of Argentine ant invasions on ground-dwelling arthropods in northern California riparian woodlands. Oecologia 116:252–258

    Article  Google Scholar 

  • Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233

    Article  Google Scholar 

  • Ikehara N (1979) Okinawa Syokubutsu Yagai Katuyou Zukan (Pictorial book of plants in Okinawa for field utilization), vol 3 (in Japanese). Shinsei Tosyo Syuppan, Naha

  • IUCN (2000) Conservation of Dugong (Dugong dugon), Okinawa Woodpecker (Sapheopipo noguchii) and Okinawa Rail (Gallirallus okinawae) in and around the Okinawa Island. The World Conservation Congress at its 2nd Session in Amman, Jordan, 4–11 October 2000

  • Kaplan I, Eubanks MD (2002) Disruption of cotton aphid (Homoptera: Aphididae)—natural enemy dynamics by red imported fire ants (Hymenoptera: Formicidae). Environ Entomol 31:1175–1183

    Article  Google Scholar 

  • Kaplan I, Eubanks MD (2005) Aphids alter the community-wide impact of fire ants. Ecology 86:1640–1649

    Article  Google Scholar 

  • Katayama M, Tsuji K (2010) Habitat differences and occurrence of native and exotic ants on Okinawa Island. Entomol Sci 13:425–429

    Article  Google Scholar 

  • King JR, Tschinkel WR (2007) Range expansion and local population increase of the exotic ant, Pheidole obscurithorax, in the southwestern United States (Hymenoptera: Formicidae). Fla Entomol 90:435–439

    Article  Google Scholar 

  • Lach L (2003) Invasive ants: unwanted partners in ant–plant interactions? Ann Missouri Bot Card 90:91–108

    Article  Google Scholar 

  • Le Breton J, Chazeau J, Jourdan H (2003) Immediate impacts of invasion by Wasmannia auropunctata (Hymenoptera: Formicidae) on native litter ant fauna in a New Caledonian rainforest. Austr Ecol 28:204–209

    Article  Google Scholar 

  • McClelland GTW, Jones IL (2009) The invasive ant fauna (Hymenoptera, Formicidae) of Laysan Island, Hawaiian Islands National Wildlife Refuge. Proc Hawaii Entomol Soc 41:37–46

    Google Scholar 

  • McGlynn TP (1999) The worldwide transport of ants: geographic distribution and ecological invasions. J Biogeogr 26:535–548

    Article  Google Scholar 

  • Nakamaru M, Beppu Y, Tsuji K (2007) Does disturbance favor dispersal? An analysis of ant migration using the colony-based lattice model. J Theor Biol 248:288–300

    Article  PubMed  Google Scholar 

  • Ness JH, Bronstein JL (2004) The effects of invasive ants on prospective ant mutualists. Biol Invasions 6:445–461

    Article  Google Scholar 

  • O’Dowd DJ, Green PT, Lake PS (2003) Invasion ‘meltdown’ on an oceanic island. Ecol Lett 6:812–817

    Article  Google Scholar 

  • Olson DM, Dinerstein E (1998) The global 200: a representation approach to conserving the earth’s most biologically valuable ecoregions. Conserv Biol 12:502–515

    Article  Google Scholar 

  • Passera L (1994) Characteristics of tramp species. In: Williams DF (ed) Exotic ants: impact and control of introduced species. Westview Press, Boulder, pp 23–43

    Google Scholar 

  • Pfeiffer M, Tuck HC, Lay TC (2008) Exploring arboreal ant community composition and co-occurrence patterns in plantations of oil palm Elaeis guineensis in Borneo and Peninsular Malaysia. Ecography 31:21–32

    Article  Google Scholar 

  • Phillips PA, Sherk CJ (1991) To control mealybugs, stop honeydew-seeking ants. Calif Agric 45:26–28

    Google Scholar 

  • R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org. Accessed 20 December 2009

  • Reimer N, Beardsley JW, Jahn G (1990) Pest ants in the Hawaiian Islands. In: Vander Meer RK, Jaffe K, Cedeno A (eds) Applied myrmecology. A world perspective. West View Press, Boulder, pp 40–50

    Google Scholar 

  • Samways MJ, Nel M, Prins AJ (1982) Ants (Hymenoptera: Formicidae) foraging in citrus trees and attending honeydew-producing Homoptera. Phytophylactica 14:155–157

    Google Scholar 

  • Sarty M, Abbott KL, Lester PJ (2007) Community level impacts of an ant invader and food mediated coexistence. Insect Soc 54:166–173

    Article  Google Scholar 

  • Stiles JH, Jones RH (1998) Distribution of the red imported fire ant, Solenopsis invicta, in road and powerline habitats. Landsc Ecol 335:335–346

    Article  Google Scholar 

  • Suarez AV, Bolger DT, Case TJ (1998) Effects of fragmentation and invasion on native ant communities in coastal southern California. Ecology 19:2041–2056

    Article  Google Scholar 

  • Sulaiman SFM (1997) Impact of weed management on ant density and fruit yield in the control of pineapple wilt disease. Acta Hortic 425:475–484

    Google Scholar 

  • Suwabe M (2009) Okinawa-hontou ni Okeru Ari no Gunsyû-Seitaigaku, Jiniteki Kakuran ga Gairai-Ari no Sinryaku ni Ataeru Eikyou (Community ecology of ants in the Okinawa Island. Effects of the anthropogenic disturbances on invansions by non-native tramp ants and on native ant community). PhD thesis, The United Graduate School of Agricultural Sciences, Kagoshima University (In Japanese)

  • Suwabe M, Ohnishi H, Kikuchi T, Kawara K, Tsuji K (2009) Difference in seasonal activity pattern between non-native and native ants in subtropical forest of Okinawa Island, Japan. Ecol Res 24:637–643

    Article  Google Scholar 

  • Tsuji K (2010) Unicolonial ants: loss of colony identity. In: Breed M, Moore J (eds) Encyclopedia of animal behavior. Academic Press, Oxford (in press)

  • Tsuji K, Tsuji N (1996) Evolution of life history strategies in ants: variation in queen number and mode of colony founding. Oikos 76:82–92

    Article  Google Scholar 

  • Wetterer JK, Espadaler X, Wetterer AL, Aguin-Pombo D, Franquinho-Aguiar AM (2006) Long-term impact of exotic ants on the native ants of Madeira. Ecol Entomol 31:358–368

    Article  Google Scholar 

  • Yamauchi K, Ogata K (1995) Social structure and reproductive systems of exotic versus endemic ants (Hymenoptera: Formicidae) of the Ryukyu Islands. Pacif Sci 49:55–68

    Google Scholar 

Download references

Acknowledgments

We thank Masami Hayashi for identification of Sogata hakonensis and Masakazu Sano for identifications of Aphis nasturtii, Metanipponaphis cuspidatae, and Melanaphis formosana. We also thank Alexander S. Mikheyev for his comments on our earlier manuscript. This study was supported in part by KAENHI (no. 21247006), a Young Investigator Research Grant from the University of the Ryukyus, and Mitsui and Co., Ltd. Environment Fund (no. 08R-B047). The Subtropical Field Science Center (Yona Field) of the University of the Ryukyus and the Yanbaru Wildlife Conservation Field Center of the Ministry of the Environment, Japan, also supported our work.

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Correspondence to Hirotaka Tanaka.

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Tanaka, H., Ohnishi, H., Tatsuta, H. et al. An analysis of mutualistic interactions between exotic ants and honeydew producers in the Yanbaru district of Okinawa Island, Japan. Ecol Res 26, 931–941 (2011). https://doi.org/10.1007/s11284-011-0851-2

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