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Ant–aphid relations in the south of Western Siberia (Hymenoptera: Formicidae; Hemiptera: Aphididae)

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Abstract

Aphids, the main suppliers of energy-rich honeydew, play an important role in the life of ants. However, the data on the trophobiotic ant–aphid associations in the majority of regions are still limited. We present the first data on the ant–aphid relations in the south of Western Siberia. Investigations were carried out in the most typical biotopes of forest-steppe and steppe zones in the territory of Novosibirsk and Kurgan regions (Russia) during 1993–2014. There were revealed 35 species of ants and 198 species of aphids. Detected 456 ant–aphid associations involved 28 ant species and 134 myrmecophilous aphids. Seven ant species were found to consume honeydew of 9 non-myrmecophilous aphids, scraping it from the plant. This behaviour is typical of subdominant and subordinate ants which do not protect their foraging areas. Ants associate with various numbers of aphid species. About 36% of ants attended aphid colonies of less than 5 species. The largest number of myrmecophilous aphids is associated with L. niger (Linnaeus, 1758) (103 species), Formica pratensis Retzius, 1783 (50), Formica rufa group (25–33), F. (Serviformica) fusca Linnaeus, 1758 (26) and F. (S.) cunicularia Latreille, 1798 (27). Different ants play unequal roles in the formation of trophobiotic interactions with aphids. Due to complex territorial and foraging behaviour, including high functional specialization among honeydew collectors, dominant ants of Formica s. str. are one of the leaders in this process. The role of L. niger and Formica ants of the subgenus Serviformica requires further detailed investigation.

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References

  • Addicott JF (1978) Competition for mutualists: aphids and ants. Can J Zool 56:2093–2096

    Article  Google Scholar 

  • Beckers R, Goss S, Deneubourg JL, Pasteels JM (1989) Colony size, communication and ant foraging strategy. Psyche 96:239–256

    Article  Google Scholar 

  • Blackman RL, Eastop VF (2006) Aphids on the World’s Shrubs and Herbaceous Plants. Wiley, Chichester, U.K. 1439 pp. (2 vols). IOP Publishing Aphidsonworldsplants. http://www.aphidsonworldsplants.info. Accessed 9 Jan 2017

  • Blüthgen N, Feldhaar H (2010) Food and shelter: how resources influence ant ecology. In: Lach L, Parr CL, Abbott KL (eds) Ant ecology. Oxford University Press, Oxford, pp 115–136

    Google Scholar 

  • Brian MV (1983) Social insect ecology and behavioural biology. Chapman & Hall, London

    Google Scholar 

  • Bristow CM (1984) Differential benefits from ant attendance to two species of Homoptera on New York ironweed. J Anim Ecol 53:715–726

    Article  Google Scholar 

  • Czechowski W, Radchenko A, Czechowska W (2002) The ants (Hymenoptera, Formicidae) of Poland. Museum and Institute of Zoology PAS, Warsaw

    Google Scholar 

  • Delabie JHC (2001) Trophobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotrop Entomol 30:501–516

    Article  Google Scholar 

  • Depa L, Mróz E, Bugaj-Nawrocka A, Orczewska A (2016) Do ants drive speciation in aphids? A possible case of ant-driven speciation in the aphid genus Stomaphis Walker (Aphidoidea, Lachninae). Zool J Linn Soc. https://doi.org/10.1111/zoj.12437

    Google Scholar 

  • Dixon AFG (1958) The escape responses shown by certain aphids to the presence of the coccinellid Adalia decempunctata (L.). Trans R Entomol Soc 10:319Р334

    Google Scholar 

  • Dlusskij GM (1967) Ants of genus Formica. Nauka, Мoscow. (In Russian)

    Google Scholar 

  • Dlusskij GM, Zryanin VA (2013) Keys for determination of ant species of genus Formica. In: Zakharov AA, Dlusskij GM, Goryunov DN et al (eds) Monitoring of ants Formica. KMK, Moscow, pp 52–60. (In Russian)

    Google Scholar 

  • Domisch T, Finer L, Neuvonen S, Niemela P, Risch AC, Kilpelainen J, Ohashi M, Jurgensen MF (2009) Foraging activity and dietary spectrum of wood ants (Formica rufa group) and their role in nutrient fluxes in boreal forests. Ecol Entomol 34:369–377

    Article  Google Scholar 

  • Favret C (2016) Aphid Species File. Version 5.0/5.0. IOP Publishing AphidSpeciesFile. http://Aphid.SpeciesFile.org. Accessed 22 June 2016

  • Frouz J, Jílková V, Sorvari J (2016) Contribution of wood ants to nutrient cycling and ecosystem function. In: Stockan JA, Robinson EJH (eds) Wood ant ecology and conservation. Cambridge University, Cambridge, pp 207–220

    Google Scholar 

  • Heie OE (1986) The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. III. Family Aphididae: subfamily Pterocommatinae & tribe Aphidini of subfamily Aphidinae. E.J. Brill/Scandinavian Science Press Ltd, Leiden

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Springer-Verlag, Berlin

    Book  Google Scholar 

  • Hölldobler B, Wilson EO (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. Norton & Company, New York

    Google Scholar 

  • Hosseini A, Hosseini M, Katayama N, Mehrparvar M (2017) Effect of ant attendance on aphid population growth and above ground biomass of the aphid’s host plant. Eur J Entomol 114:106–112

    Article  Google Scholar 

  • Ivanovskaja OI (1977) Aphids of the Western Siberia. Part 1 and 2. Nauka, Novosibirsk. (In Russian)

    Google Scholar 

  • Kanturski M, Karcz J, Kaszyca N, Depa Ł (2017) Perianal structures in myrmecophilous subterranean aphids (Insecta: Hemiptera: Aphididae)—Comparative morphology of trophobiotic organ with its first description in Lachninae. Arthropod Struct Dev 46(4):496–507

    Article  PubMed  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). Appl Entomol Zool 38:427–433

    Article  Google Scholar 

  • Lang C, Menzel F (2011) Lasius niger ants discriminate aphids based on their cuticular hydrocarbons. Anim Behav 82(6):1245–1254

    Article  Google Scholar 

  • Latibari MN, Moravvej G, Namaghi HS (2016) Investigation on the mutualistic interactions of ant species and the aphids, Cinara spp. (Hemiptera: Aphididae) on Pinus mugo trees in urban green space of Mashhad, Razavi Khorasan, Iran. Entomofauna 37:401–412

    Google Scholar 

  • Makarevich ON (2003) Liometopum microcephalum (Hymenoptera, Formicidae) in Nizhnee Pridneprovie. Vestn Zool 37:51–56. (In Ukrainian, Engl. abstr.)

    Google Scholar 

  • Mordvilko AK (1914) Fauna of Russia and Adjacent Countries. Insecta Hemiptera. vol 1, part 1. Imperatorskaya Akademiya Nauk, Petrograd. (In Russian)

    Google Scholar 

  • Mordvilko AK (1919) Fauna of Russia and adjacent countries. Insecta Hemiptera. vol 1, part 2. Imperatorskaya Akademiya Nauk, Petrograd. (In Russian)

  • Mordvilko AK (1929) Food plant catalogue of the Aphididae of USSR. Trudy po prikladnoy entomologii 14:1–100. (In Russian)

    Google Scholar 

  • Mordvilko AK (1936) Ants and aphids. Priroda 4:44–55. (In Russian)

    Google Scholar 

  • Newton JS, Glasier J, Maw HEL, Proctor HC, Foottit RG (2011) Ants and subterranean Sternorrhyncha in a native grassland in east-central Alberta, Canada. Can Entomol 143:518–523

    Article  Google Scholar 

  • Nixon GEJ (1951) The association of ants with aphids and coccids. Commonwealth Institute of Entomology, London

    Google Scholar 

  • Novgorodova TA (2002) Study of adaptations of aphids (Homoptera, Aphidinea) to ants: comparative analysis of myrmecophilous and non-myrmecophilous species. Entomol Rev 82(5):569–576

    Google Scholar 

  • Novgorodova ТА (2015) Organization of honeydew collection by foragers in different ant species (Hymenoptera, Formicidae): effect of colony size and species specificity. Eur J Entomol 112:688–697

    Google Scholar 

  • Novgorodova ТА, Gavrilyuk AV (2012) The degree of protection different ants (Hymenoptera: Formicidae) provide aphids (Hemiptera: Aphididae) against aphidophages. Eur J Entomol 109:187–196

    Article  Google Scholar 

  • Novgorodova T, Stekolshchikov A (2013) A contribution to the aphid (Insecta: Homoptera: Aphidinea) fauna of the Kurgan region. Zoosyst Ross 22:230–246

    Google Scholar 

  • Oliver TH, Leather SR, Cook JM (2008) Macroevolutionary patterns in the origin of mutualisms involving ants. J Evol Biol 21:1597–1608

    Article  CAS  PubMed  Google Scholar 

  • Quednau FV (2003) Atlas of the Drepanosiphini aphids of the world. Part II: Panaphidini Oestlund, 1923 Panaphidina Oestlund, 1923 (Hemiptera: Aphididae: Calaphidinae). The American Entomological Institute, Gainesville

    Google Scholar 

  • Radchenko AG (1994a) A Key to the identification of the ants of South Siberia. Trudy zapovednika “Daursky” 3:95–118. (In Russian)

    Google Scholar 

  • Radchenko AG (1994b) A key to the species of the genus Myrmica (Hymenoptera, Formicidae) in central and eastern Palaearctic. Zool Zh 73:130–145. (In Russian)

    Google Scholar 

  • Radchenko AG (1996) A key to the ant genus Camponotus (Hymenoptera, Formicidae) in Palaearctic Asia. Entomol Rev 76:430–437

    Google Scholar 

  • Radchenko A, Elmes A (2010) Myrmica (Hymenoptera, Formicidae) ants of the old wold. Natura optima dux Foundation, Warszawa

    Google Scholar 

  • Reznikova ZhI (1982) Interspecific communication between ants. Behaviour 80:84–95

    Article  Google Scholar 

  • Reznikova ZhI (1983) Interspecies inter-relations in ants. Nauka Press, Novosibirsk. (In Russian)

    Google Scholar 

  • Reznikova ZhI (1999) Ethological mechanisms of population density control in coadaptive complexes of ants. Russ J Ecol 30:187–192

    Google Scholar 

  • Seifert B (2000) A taxonomic revision of the ant subgenus Coptoformica Mueller, 1923 (Hymenoptera, Formicidae). Zoosystema 22:517–568

    Google Scholar 

  • Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interaction. Annu Rev Ecol Evol Syst 36:345–372

    Article  Google Scholar 

  • Stadler B, Dixon AFG (2008) A comparative analysis of morphological and ecological characters of European aphids and lycaenids in relation to ant-attendance. Oecologia 135:422–430

    Article  Google Scholar 

  • Stekolshchikov A, Novgorodova T (2013) New additions to the aphid fauna (Homoptera: Aphidinea) of Western Siberia (Homoptera: Aphidinea). Zoosyst Ross 22:63–68

    Google Scholar 

  • Styrsky JD, Eubanks MD (2007) Ecological consequences of interactions between ants and honeydew-producing insects. Proc R Soc B 274(1607):151–164

    Article  PubMed  Google Scholar 

  • Way MJ (1963) Mutualism between ants and honeydew producing Homoptera. Annu Rev Entomol 8:307–344

    Article  Google Scholar 

  • Yao I (2014) Costs and constraints in aphid-ant mutualism. Ecol Res 29:383–391

    Article  Google Scholar 

  • Zakharov AA (2015) Ants of forest communities, their life and role in the forest. KMK Scientific Press, Moscow. (In Russian)

    Google Scholar 

  • Zakharov AA, Dlusskij GM (2013) Brief essays about ant species of Formica. In: Zakharov AA, Dlusskij GM, Goryunov DN et al (eds) Monitoring of ants Formica. KMK, Moscow, pp 61–79. (In Russian)

    Google Scholar 

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Acknowledgements

We are grateful to A. Gavrilyuk and O. Yuzhkova for their help in material collection, A.V. Stekolshchikov (Zoological Institute RAS, St. Petersburg, Russia) for verification of the aphid identifications and specifying some aphid species and N. Vesnina (Novosibirsk State Pedagogical University, Novosibirsk) for help with the identification of host plants. We would also like to thank anonymous reviewers for their valuable comments on the manuscript and N. Murray for improving and checking the English of this manuscript. This study was supported by the Federal Fundamental Scientific Research Program (VI.51.1.10. No. 0311-2016-0004) and the Russian Foundation for Basic Research (No. 18-04-00849).

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  1. Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Frunze str. 11, Novosibirsk, 630091, Russia

    Tatiana A. Novgorodova & Artem S. Ryabinin

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  1. Tatiana A. Novgorodova
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  2. Artem S. Ryabinin
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The project was designed by TAN. Both authors collected the material (TAN: Novosibirsk Region, 1994–2014: TAN; Kurgan Region, 2006–2013: ASR). Data analysis was led by TAN; TAN and ASR wrote the paper.

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Correspondence to Tatiana A. Novgorodova.

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Handling Editor: Jouni Sorvari.

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Novgorodova, T.A., Ryabinin, A.S. Ant–aphid relations in the south of Western Siberia (Hymenoptera: Formicidae; Hemiptera: Aphididae). Arthropod-Plant Interactions 12, 369–376 (2018). https://doi.org/10.1007/s11829-017-9584-7

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