INTRODUCTION

More than 5,000 species of aphids (Hemiptera: Aphididae) are described worldwide (Favret, 2020), with 384 species registered in Serbia. Yet, the expected number is about 550 (Petrović-Obradović et al., 2021). Aphids are small insects that produce honeydew (sugar-rich liquid), which is a result of excessive suction of plant sap from the phloem. Honeydew of aphids contains melesitosis (trisaccharide), which plays an important role in the interactions between aphids and ants (Yao, 2014). Certain species of ants collect, or “milk”, honeydew from aphids, providing the aphid colony protection from predators, such as ladybirds or lacewings and hymenopterous parasitoids such as Aphelinidae, Figitidae or Braconidae, exclusively the subfamily Aphidiinae (Way, 1963; Novgorodova & Gavrilyuk, 2012). Aphids derive many other benefits from ants; ants clean them of honeydew thus retaining the energy that aphids can use to feed and reproduce undisturbed. Ants promote apterous aphid forms, which again results in aphids saving their energy for other purposes. Ants build galleries in the earth around the aphid colonies providing them with both better protection and a microclimate.

Mutual relations between ants and other organisms are known as myrmecophily (Stadler & Dixon, 1999; Parker & Grimaldi, 2014; Saha et al., 2018). Homopterans are certainly the largest target group for aphid-associated ants (Way, 1963). The most researched is the cooperation between ants, aphids, and their relations with the aphids’ enemies; from the evolutionary and ecological aspect (Stadler & Dixon, 2005) or from the aspect of biological control application (Starý, 1966). Starý (1966) recognized three types of aphid-ant relationships: (1) constant, which is continuous, implying morphological adaptations in members of this mutualistic relationship; (2) temporary, occurring throughout all or almost all time in the season; (3) facultative, a most common situation, implying the accidental presence of ants in the colony and the lack of a serious mutualistic relationship with the aphids.

An interesting fact is that the number of recorded ant-aphid associations is relatively small. Hölldobler & Wilson (1990) explain this through the disproportionate number of species of both actors of the association in the northern and southern hemispheres; the highest diversity of ants in tropical regions, unlike aphids which are certainly more diverse in temperate regions. Siddiqui et al. (2019) suggest that the transition zones in which the two groups meet could be subtropical regions, and the diversity of ant-aphid associations may be the greatest. Although the exact number of ant-aphid associations is not known, Stadler & Dixon (1998) note that only one third to a quarter of all aphid species are ant attended, and among them, a small number are obligatory myrmecophiles. Some of the subterranean aphids, like many Pemphiginae, and many Lachninae, for example species from the genus Protrama Baker, are in an obligatory relationship with ants. Obligate myrmecophiles aphids are morphologically “modified” and prepared to live with ants. They usually have small cauda and small siphunculi. Around the dorsally placed anus there are many hairs, where droplets are kept until taken by ants. Ants promote production of apterae and in the genera Stomaphis Walker, they even make dispersal of aphids to other trees. A very common aphid, such as Aphis fabae Scopoli, is a facultative myrmecophile. However, ants do not visit aphids which produce plentiful wax, or have long siphunculi and cauda, or live in more or less closed galls, for example: Eriosoma lanigerum (Hausmann), Uroleucon Mordvilko, Prociphilus Koch, and others (Heie, 1980).

There are 17 ant subfamilies with about 13,500 described species worldwide (Bolton, 2018). The exact number of species that connect aphids is not known. The species from the subfamily Formicinae are the most numerous in mutual relations with their “protégés”, especially those included in the genera, Formica L. and Lasius Fabricius (Starý, 1966). Among Myrmicinae, Myrmica Latreille and Tetramorium Mayr also feed on aphid honeydew. The myrmecofauna of Serbia is composed of 141 species (Petrov, 2004). So far, there have been no published works on ants that attend aphid colonies for the territory of Serbia, and ex-Yugoslavia. The greatest contribution to the ant fauna on the territory of Serbia was by the myrmecologist Dr. Ivan Petrov (e.g., Petrov, 2000; 2004).

As aforementioned, both aphid and ant fauna have been well researched in Serbia. However, information on their interrelationships and trophic patterns, including aphids’ host plants is lacking. The primary goal of the current study is to present aphid-ant associations in Serbia during a period of almost 30 years of research on the ecology and diversity of aphids. Secondly, we expect this paper will provide a better insight into the faunistic complexes of the examined groups and serve as a platform in further research of ant and aphid interactions.

MATERIAL AND METHODS

Study area

Samples of ant-attended aphids were collected on the entire territory of Serbia, although predominantly in the north and southeastern parts (Fig. 1). Most of the samples were collected from lowland areas, both rural and urban, but also from higher altitudes such as Rajac mt at about 800 m above sea level (a.s.l.), Crna Trava at about 900 m a.s.l., Radan mt at about 1,000 m a.s.l. and Vlasinsko jezero (lake) at 1,250 m a.s.l. A detailed list of exploration sites with coordinates is provided in Table I. The collection within the research was conducted during two periods, from 1990 to 1997, and from 2016 to 2017.

Material collection

Specimens of aphids were collected by cutting infected parts of the plants, mainly leaves and twigs, and placing them in plastic boxes of 0.5 litre volume. The boxes, filled with sampled material, were then covered with a mesh cloth to prevent insects from escaping and to allow the boxes to be ventilated. Before covering the boxes, we picked up 10-20 adult specimens of aphids, both winged and wingless for later identification. Thus, collected aphid specimens were placed in 1.5 ml plastic tubes and conserved in 96% ethyl alcohol. Aphids were identified using identification keys (Blackman & Eastop, 2021). Worker ants were collected along with aphids in the field and placed in the same boxes with aphids. Once the ants were dead, by the same procedure as for aphids, they were preserved in 96% ethyl alcohol in 2 ml plastic microtubes. The ants were identified by Dr. Marko Karaman (Natural History Museum of Montenegro). The taxa names of aphids and ants have been adopted according to the Fauna Europaea online database (van Achterberg, 2013).

RESULTS

In the present study, 220 samples of 32 ant taxa and 74 aphid taxa were collected from 59 localities across Serbia. The results were presented in alphabetical order following ant scientific names; subfamily, genus, and species, respectively. The same was done for aphids and plants, while data on date of sampling are given chronologically.

Abbreviations for legators: [AS] A. Stojiljković, [MIM] M. Ilić Milošević, [ML] M. Lazarević, [MR] M. Ristić, [NM] N. Mladenović, [OPO] O. Petrović-Obradović, [SS] S. Stanković, [VŽ] V. Žikić and [ŽT] Ž. Tomanović.

Subfamily Dolichoderinae

Tapinoma sp. 1 – Aphis umbrella (Borner) on Malva sylvestris L., Niš, Deveti Maj, 18.05.2016, MR.

Tapinoma sp. 2 – Aphis umbrella on Malva sylvestris, Niš, Deveti Maj, 18.05.2016, MR.

Subfamily Formicinae

Camponotus (Myrmentoma) tergestinus Muller – Callaphis juglandis (Goeze) on Juglans regia L., Obedska bara, 07.06.1997, ŽT; Opovo, 23.06.1997, ŽT.

Camponotus (Colobopsis) truncatus (Spinola) – Brachycaudus cardui (L.) on Prunus domestica L., Prokuplje, Gornja Konjuša, 23.04.2016, MR.

Camponotus (Myrmentoma) piceus (Leach) – Aphis ruborum (Borner) on Rubus fruticosus L., Prokuplje, Gornja Konjuša, 29.05.2016, MR; – Brachycaudus cardui on Prunus avium L., Kruševac, Donji Stepoš, 01.05.2016, ML; – B. cardui on Prunus domestica, Prokuplje, Gornja Konjuša, 23.04.2013, MR.

Camponotus (Tanaemyrmex) aethiops (Latreille) – Lachnus sp. on Quercus cerris L., Prokuplje, Gornja Konjuša, 15.06.2016, MR.

Formica (Serviformica) balcanina Petrov & Collingwood – Aphis fabae Scopoli on Cirsium arvense (L.) Scop., Vlasinsko jezero (lake), 30.06.2016, SS; – Aphis sp. on Anthriscus sp., Vlasinsko jezero (lake), 30.06.2016, SS; – Chaetosiphon fragaefolii (Cockerell) on Fragaria vesca L., Kruševac, Donji Stepoš, 17.04.2016, ML; – Cavariella aegopodii (Scopoli) on Peucedanum officinalis L., Vlasinsko jezero (lake), 30.06.2016, SS; – Ctenocallis dobrovljanskyi Klodnitsky on Chamaecytisus heuffelii (Wierzb.), Vlasinsko jezero (lake), 28.07.2017, VŽ; – Dysaphis sorbi (Kaltenbach) on Sorbus aucuparia L., Sićevačka klisura, Sićevo, 11.06.2017, VŽ.

Formica (Serviformica) cinerea Mayr – Aphis fabae on Cirsium arvense, Niš, Pantelej, 28.07.2017, VŽ; – Brachycaudus sp. on Echium vulgare L., Majdanpek, Debeli Lug, 09.06.1990, OPO; – Symydobius oblongus (von Heyden) on Betula pendula Roth var. pendula, Vlasinsko jezero (lake), 21.07.1990, OPO.

Formica (Serviformica) cunicularia Latreille – Aphis fabae on Rumex patientia L., Niš, Deveti Maj, 15.04.2016, MR; – A. fabae on Bifora radians Bieb., Prokuplje, Gornja Konjuša, 29.05.2016, MR; – Aphis ruborum on Rubus fruticosus, Prokuplje, Gornja Konjuša, 29.05.2016, MR; – Brachycaudus cardui on Prunus cerasifera Ehrh., Vlasinsko jezero (lake), 22.05.2016, VŽ; – Cavariella aegopodii on Pastinaca hirsuta Pančić, Vlasinsko jezero (lake), 30.06.2016, SS; – Dysaphis plantaginea (Passerini) on Malus pumila Mill., Obedska bara, 07.06.1997, ŽT; Beograd, 01.08.1997, ŽT.

Formica (Serviformica) fusca L. – Cavariella aegopodii on Smyrnium perfoliatum L., Niš, Niška banja, 24.05.2016, VŽ.

Formica (Serviformica) gagates Latreille – Aphis fabae on Anthriscus sylvestris (L.) Hoffm., Niš, Niška banja, 14.05.2017, VŽ; – A. fabae on Rumex sp., Niš, Kamenički vis, 04.06.2017, NM; – Periphyllus sp. on Acer monspessulanum L., Niš, Gornji Matejevac, 21.05.2017, SS.

Formica (Serviformica) glauca Ruzsky – Aphis fabae on Hedera helix L., Prokuplje, Gornja Konjuša, 29.05.2016, MR.

Formica (Formica) pratensis Retzius – Aphis fabae on Anthriscus sylvaticus (L.) Hoffm., Prokuplje, Gornja Konjuša, 01.05.2016, MR; – A. fabae on Arctium lappa L., Pećinci, Ašanja, 15.06.1996, ŽT; – A. fabae on Galium mollugo L., Prokuplje, Gornja Konjuša, 23.04.2016, MR; – Brachycaudus cardui on Prunus cerasifera, Vlasinsko jezero (lake), 22.05.2016, VŽ; – Chaitophorus nigricantis Pintera, on Salix alba L., Majdanpek, Debeli Lug, 09.06.1990, OPO; – Chaitophorus vitellinae (Schrank) on S. alba, Majdanpek, Debeli Lug, 09.06.1990, OPO; – Ctenocallis dobrovljanskyi Klodnitsky on Chamaecytisus heuffelii, Vlasinsko jezero (lake), 28.07.2017, VŽ; – Myzus cerasi (Fabricius) on Prunus cerasus L., Prokuplje, Gornja Konjuša, 23.04.2016, MR; – Pterocomma sp. on Salix alba, Majdanpek, Debeli Lug, 09.06.1990, OPO; – Sipha maydis Passerini on Triticum aestivum L. subsp. aestivum, Suvobor, Rajac mt., 18.05.1990, OPO.

Formica (Raptiformica) sanguinea Latreille – Acaudinum centaureae (Koch) on Centaurea scabiosa L., Majdanpek, Debeli Lug, 09.06.1990, OPO.

Formica (Serviformica) rufibarbis Fabricius – Aphis baloticolla Szelegiewicz on Ballota nigra L., Beograd, 29.06.1996, ŽT; Stara Pazova, 10.06.1997, ŽT; – Aphis ulmariae Schrank on Filipendula ulmaria (L.) Maxim., Vlasinsko jezero (lake), 23.07.1990, OPO; – Macrosiphum rosae (L.) on Rosa sp., Beograd, 09.06.1997, ŽT; – Metopeurum fuscoviride Stroyan on Tanacetum vulgare L., Vlasinsko jezero (lake), 30.06.2016, VŽ; – Myzus cerasi on Prunus cerasus, Prokuplje, Gornja Konjuša, 23.04.2016, MR.

Lasius (Cautolasius) flavus (Fabricius) – Aphis serpylli Koch on Thymus praecox Opiz, Vlasinsko jezero (lake), 25.08.2017, VŽ.

Lasius (Dendrolasius) fuliginosus (Latreille) – Aphis vitalbae Ferrari on Clematis vitalba L., Prokuplje, Gornja Konjuša, 03.04.2016, MR; Gadžin Han, Ovsinjinac, 13.04.2016, MR; – Cavariella sp. on Salix sp., Obedska bara, 07.05.1995, ŽT; – Cavariella sp. on Salix sp., Obedska bara, 07.06.1997, ŽT; – Dysaphis reaumuri (Mordvilko) on Pyrus spinosa Forssk., Radan mt., 10.06.2017, VŽ; – Lachnus sp. on Quercus sp., Bor, Gornjane, 06.07.1990, OPO; – Pterocomma pilosum Buckton on Salix sp., Beograd, Ada Ciganlija, 23.03.1990, OPO.

Lasius (Lasius) alienus (Foerster) – Aphis crepidis (Börner) on Crepis biennis L., Ada, Mol, 23.06.1997, ŽT; – Aphis fabae on Papaver somniferum L., Obedska bara, 07.06.1997, ŽT; – A. fabae on unidentified plant, Titel, Vilovo, 10.06.1997, ŽT; – A. fabae on Rumex sp., Beograd, 10.06.1995, ŽT; – A. fabae on Tordylium maximum L., Niš, Pantelej, 20.05.2016, VŽ; – Aphis farinosa Gmelin on Salix sp., Majdanpek, Debeli Lug, 31.03.1990, OPO; – Aphis rumicis L. on Rumex sp., Smederevo, Lugavčina, 15.04.1990, OPO; – Aphis forbesi Weed on Fragaria vesca, Beograd, Višnjica, 12.08.1997, ŽT; – Aphis salviae Walker on Salvia nemorosa L., Kovačica, Uzdin, 22.06.2017, ŽT; – Aphis urticata Gmelin on Urtica dioica L., Beograd, Surčin, 01.05.1993, ŽT; Kovilovo, 15.06.1993, ŽT; Beograd, Dušanovac, 06.06.1995, ŽT; Pančevo, Omoljica, 13.06.1996, ŽT; Čenta, 20.06.1996, ŽT; Obedska bara, 07.06.1997, ŽT; Stara Pazova, 10.06.1997, ŽT; Opovo, Sefkerin, 23.06.1997, ŽT; – Aphis violae Schouteden on Viola tricolor L., Vlasinsko jezero (lake), 23.07.1990, OPO; – Brachycaudus cardui on Carduus acanthoides L., Zrenjanin, 20.06.1996, ŽT; Zrenjanin, Perlez, 13.06.1997, ŽT; Nova Crnja, 23.06.1997, ŽT; – Brachycaudus sp. on Stachys sp., Bor, Gornjane, 05.07.1990, OPO; – Chaitophorus nigricantis on Salix sp., Smederevo, Lugavčina, 31.03.1990, OPO; – Dysaphis plantaginea on Malus pumila, Obedska bara, 07.06.1997, ŽT; Beograd, 01.08.1997, ŽT; – Macrosiphum sp. on Tanacetum sp., Bor, Gornjane, 06.07.1990, OPO; – Phorodon humuli (Schrank) on Prunus cerasifera, Pančevo, Starčevo, 17.07.1996, ŽT; Beograd, Bečmen, 07.06.1997, ŽT; Stara Pazova, 10.06.1997, ŽT; Kovačica, 22.06.1997, ŽT; Beograd, 16.08.1997, ŽT; Prokuplje, Gornja Konjuša, 01.05.2016, MR; – Tetraneura sp. on Setaria verticillata (L.) P. Beauv., Beograd, 12.08.1997, ŽT.

Lasius (Lasius) brunneus (Latreille) – Aphis ruborum on Rubus caesius L., Beograd, Karaburma, 21.05.1990, OPO; – Aphis violae on Viola tricolor, Vlasinsko jezero (lake), 23.07.1990, OPO.

Lasius (Austrolasius) carniolicus Mayr – Geoica urticularia Passerini on Triticum aestivum subsp. aestivum (root), Inđija, 10.06.1997, ŽT.

Lasius (Lasius) emarginatus (Olivier) – Aphis fabae on Carduus acanthoides, Prokuplje, Gornja Konjuša, 29.05.2016, MR; – A. fabae on Digitalis grandiflora Miller, Tara, Derventa, 23.06.2016, SS; – A. fabae on Galium aparine L., Niš, Gornji Matejevac, 09.06.2016, VŽ; – Aphis podagrariae Schrank on Aegopodium podagraria L., Niš, Trošarina, 01.06.2016, SS; – Aphis pomi De Geer on Malus pumila., Prokuplje, Gornja Konjuša, 23.04.2016, MR; – Brachycaudus cardui on Prunus cerasifera, Kruševac, Donji Stepoš, 08.05.2016, ML; – Cavariella aegopodii on Smyrnium perfoliatum, Niš, Niška banja, 24.05.2016, VŽ; – Tetraneura sp. on Setaria verticillata (root), Beograd, 12.08.1997, ŽT.

Lasius (Lasius) niger (L.) – Aphis baloticolla on Ballota nigra, Beograd, 29.06.1996, ŽT; Stara Pazova, 10.06.1997, ŽT; – Aphis craccivora Koch on Medicago sativa L., Kovilovo, 10.05.1992, ŽT; Beograd, Surčin, 20.06.1995, ŽT; Žabalj, 20.06.1996, ŽT; – A. fabae on Althaea officinalis L., Sremski Karlovci, 10.06.1997, ŽT; – A. fabae on Malus pumila, Prokuplje, Gornja Konjuša, 29.05.2016, MR; – A. fabae on Rumex patientia, Niš, Deveti Maj, 15.04.2016, MR; Kraljevo, Maglič, 08.05.2016, ML; – A. fabae on Urtica urens L., Novi Bečej, Kumane, 20.06.1996, ŽT; – Aphis gossypii Glover on Althaea officinalis, Niš, Banja Topilo, 08.07.2017, VŽ; – Aphis lambersi (Börner) on Daucus carota L. (root), Tara, Derventa, 23.06.2016, VŽ; – Aphis pomi on Mespilus germanica L., Lebane, Konjino, 24.04.2016, SS; – Aphis spiraephaga Müller on Spirea media Fr. Schm., Beograd, Bečmen, 15.06.1996, ŽT; – Aphis umbrella on Althaea officinalis, Obrenovac, Mladost, 20.05.1990, OPO; – A. umbrella on Malva sp., Beograd, 17.04.1990, OPO; – Aphis urticata on Urtica dioica, Beograd, Surčin, 01.05.1993, ŽT; Kovilovo, 31.07.1993, ŽT; Beograd, Dušanovac, 13.06.1995, ŽT; Čenta, 20.06.1996, ŽT; Kikinda, 23.06.1997, ŽT; Prokuplje, Gornja Konjuša, 01.05.2016, MR; – Aphis vitalbae on Clematis vitalba, Niš, Deveti Maj, 06.04.2016, MR; – Brachycaudus sp. on Prunus persica (L.) Batsch, Žabalj 20.06.1996, ŽT; – Brachycaudus cardui on Carduus acanthoides, Zrenjanin, 20.06.1996, ŽT; Obedska bara, 07.06.1997, ŽT; Čenta, 10.06.1997, ŽT; Pančevo, 22.06.1997, ŽT; – B. cardui on Prunus cerasifera, Niš, Deveti Maj, 06.04.2016, MR; Kruševac, Donji Stepoš, 01.05.2016, ML; – Brachycaudus persicae Passerini, on Prunus persica, Beograd, 05.04.1990, OPO; – Cavariella aegopodii on Chaerophyllum hirsutum L., Perućac, 22.06.2016, VŽ; – Dysaphis ranunculi (Kaltenbach) on Ranunculus arvensis L., Čenta, 10.06.1997, ŽT; – Macrosiphum rosae on Rosa sp., Kruševac, Donji Stepoš, 11.04.2016, ML; – Microlophium carnosum (Buckton) on Urtica dioica, Niš, Deveti Maj, 18.05.2016, MR; – Myzus cerasi on Chrysanthemum sp. Beograd, 07.05.1996, ŽT; – M. cerasi on Prunus avium, Beograd, Dušanovac, 06.06.1995, ŽT; Beograd, Višnjica, 24.05.1997, ŽT; Obedska bara, 07.06.1997, ŽT; – M. cerasi on Prunus cerasifera, Kruševac, Donji Stepoš, 17.04.2016, ML; Kruševac, Donji Stepoš, 08.05.2016, ML; – Myzus persicae (Sulzer) on Capsicum annuum L., Smederevska Palanka, 09.05.1996, OPO; Čenta, 13.06.1997, ŽT; – M. persicae on Prunus persica, Beograd, 05.04.1990, OPO; Lebane, Konjino, 24.04.2016, SS; – Phorodon humuli on Prunus spinosa L., Niš, Deveti Maj, 17.04.2016, MR.

Lasius (Lasius) cf. niger (Linnaeus) – Brachycaudus cardui on Carduus acanthoides, Niš, Deveti Maj, 18.05.2016, MR.

Lasius (Lasius) paralienus Seifert – Aphis fabae on Agrostemma githago L., Prokuplje, Gornja Konjuša, 29.05.2016, MR; – A. fabae on Bifora radians, Prokuplje, Gornja Konjuša, 29.05.2016, MR; – A. fabae on Carduus acanthoides, Leskovac, 12.06.2017, AS; – A. fabae on Cirsium arvense, Leskovac, 19.07.2017, AS; – A. fabae on Matricaria chamomilla L.,Prokuplje, Gornja Konjuša, 29.05.2016, MR; – A. fabae on Xeranthemum annuum L., Prokuplje, Gornja Konjuša, 29.05.2016, MR; – Aphis gossypii on Ballota nigra , Niš, Deveti Maj, 18.05.2016, MR; – Aphis intybi Koch on Cichorium intybus L., Niš, Deveti Maj, 23.06.2016, MR; – Aphis ruborum on Rubus fruticosus, Prokuplje, Gornja Konjuša, 29.05.2016, MR; – Dysaphis pyri (Boyer de Fonscolombe) on Pyrus eleagnifolia Pallas, Radan mt., 10.06.2017, SS.

Lasius (Lasius) psammophilus Seifert – Aphis craccivora on Medicago sativa, Niš, Deveti Maj, 17.04.2016, MR; – Aphis fabae on Matricaria chamomilla, Prokuplje, Gornja Konjuša, 13.05.2016, MR; – A. fabae on Rubus sp., Kruševac, Donji Stepoš, 01.05.2016, ML; – A. fabae on Rumex patientia, Niš, Palilula, 28.04.2016, ML; – Aphis gossypii on Ballota nigra, Prokuplje, Gornja Konjuša, 23.04.2016, MR; – Aphis passeriniana (Del Guercio) on Salvia officinalis L., Niš, Deveti Maj, 06.04.2016, MR; – Aphis sambuci L. on Sambucus nigra L., Prokuplje, Gornja Konjuša, 23.04.2016, MR; – Myzus cerasi on Prunus avium, Kruševac, Donji Stepoš, 01.05.2016, ML; – M. cerasi on Prunus cerasus, Prokuplje, Gornja Konjuša, 23.04.2016, MR.

Lasius sp. 1 – Aphis fabae on Chenopodium album L., Prokuplje, Gornja Konjuša, 29.05.2016, MR.

Lasius sp. 2 – Aphis urticata on Urtica dioica, Prokuplje, Gornja Konjuša, 01.05.2016, MR.

Prenolepis nitens (Mayr ) – Anoecia corni (Fabricius) on Cornus sp., Beograd, 12.04.1990, OPO; Zemun, 09.04.1990, OPO; – Aphis fabae on Anthriscus sylvestris, Niš, Niška banja, 14.05.2017, VŽ; – A. fabae on Euonymus europaeus L., Beograd, Topčider, 13.05.1993, 03.05.1997, ŽT; Prokuplje, Gornja Konjuša, 02.04.2016, MR; – A. fabae on Galium mollugo, Prokuplje, Gornja Konjuša, 29.05.2016, MR; – A. fabae on Philadelphus coronarius L., Kruševac, Donji Stepoš, 16.04.2016, ML; – A. fabae on Rumex patientia, Kruševac, Donji Stepoš, 01.05.2016, ML; – Aphis hederae Kaltenbach on Hedera helix, Kruševac, Donji Stepoš, 11.04.2016, ML; Kruševac, Donji Stepoš, 01.05.2016, ML; Niš, Pantelej, 01.05.2016, VŽ; – Aphis pomi on Chaenomeles japonica (Thunb.) Lindley ex Spach, Kruševac, Donji Stepoš, 01.05.2016, ML; Kruševac, Donji Stepoš, 08.05.2016, ML; – Aphis ruborum on Rubus sp., Kruševac, Donji Stepoš, 01.05.2016, ML; – Aphis sambuci on Sambucus nigra, Niš, Deveti Maj, 17.04.2016, MR; Kruševac, Donji Stepoš, 01.05.2016, ML; – Aphis urticata on Urtica dioica, Žitište, 22.07.1997, ŽT; Kruševac, Donji Stepoš, 07.04.2016, ML; Gadžin Han, Ovsinjinac, 13.04.2016, MR; Kruševac, Donji Stepoš, 01.05.2016, ML; Prokuplje, Gornja Konjuša, 01.05.2016, MR; – A. urticata on Urtica sp., Smederevo, Lugavčina, 15.04.1990, OPO; – Aphis viburni Scopoli on Viburnum opulus L., Gadžin Han, Ovsinjinac, 13.04.2016, MR; – Aphis vitalbae on Clematis vitalba, Niš, Niška banja, 11.04.2016, MR; – Brachycaudus persicae on Prunus domestica, Smederevo, Lugavčina, 04.05.1990, OPO; – Chaetosiphon sp. on Lamium maculatum L., Beograd, Botanička bašta, 17.06.1997, ŽT; – Dysaphis sp. on Pyrus communis L., Beograd, Višnjica, 24.05.1997, ŽT; – Dysaphis sp. on P. communis, Obedska bara, 07.06.1997, ŽT; – Hyalopterus pruni (Geoffroy) on Prunus spinosa, Niš, Palilula, 28.04.2016, ML; – Lipaphis alliariae Müller on Alliaria petiolata (Bieb.) Cavara & Grande, Gadžin Han, Ovsinjinac, 13.04.2016, MR; – Macrosiphum rosae on Rosa canina L., Kruševac, Donji Stepoš, 08.05.2016, ML; – M. rosae on Rosa sp., Kruševac, Donji Stepoš, 01.05.2016, ML; – Periphyllus sp. on Acer campestre L., Gadžin Han, Ovsinjinac, 13.04.2016, MR; Periphyllus sp. on Acer monspessulanum, Niš, Niška Banja, 11.05.2016, MIM; – Phorodon humuli on Prunus cerasifera Niš, Deveti Maj, 17.04.2016, MR; Prokuplje, Gornja Konjuša, 01.05.2016, MR; – Thelaxes sp. on Quercus robur L., Radan mt. (1000 m a.s.l.), 12.06.2016, SS.

Subfamily Myrmicinae

Crematogaster schmidti (Mayr) – Aphis sambuci on Sambucus nigra, Prokuplje, Gornja Konjuša, 02.04.2016, 23.04.2016, MR; – Periphyllus sp. on Acer monspessulanum, Niš, Niška banja, 24.05.2016, VŽ; – Phorodon humuli on Prunus cerasifera Prokuplje, Gornja Konjuša, 01.05.2016, MR; – P. humuli on Prunus mahaleb L., Niš, Gornji Matejevac, 21.05.2017, SS.

Messor structor (Latreille) – Aphis umbrella on Malva neglecta Wallr., Crna Trava, 23.07.1990, OPO; – Myzus persicae on M. neglecta, Crna Trava, 23.07.1990, OPO.

Myrmica rubra (Linnaeus) – Cavariella aegopodii on Chaerophyllum hirsutum, Perućac, 22.06.2016, VŽ; – Pterocomma salicis (Linnaeus) on Salix sp., Vlasinsko jezero (lake), 24.07.1990, OPO.

Tetramorium caespitum (Linnaeus) – Aphis fabae on Beta vulgaris L. var. cicla, Leskovac, 26.05.2017, AS; – A. fabae on Cirsium arvense, Beograd, Surčin, 15.06.1993, ŽT; 21.07.1993, ŽT; Smederevska Palanka, 13.06.1997, ŽT; Opovo, 23.06.1997, ŽT; – Aphis taraxacicola (Börner) on Taraxacum sp., Beograd, Surčin, 03.04.1990, OPO.

In this survey, we counted 167 ant-aphid associations. Three species stand out as participants of most associations. Lasius niger forms 28 associations, almost 17% of the total number. This species is followed by Prenolepis nitens with 26 associations (15.57%) and its congener L. alienus, which makes 18 associations (10.78%). The percentage of ant-aphid associations is presented in Fig. 2, where only half of the ant species is presented because the other 16 species forming 1-2 associations with values less than 1.8% are not presented.

Ants were collected in 74 colonies of aphid species out of a total of 384 species registered in Serbia, which means that some aphid associations have not yet been documented. As a facultative myrmecophilous species, Aphis fabae was present in 43 samples in our study, this species is most frequently found in the present survey and makes up 38 associations. The second most frequent species in this research was Aphis urticata. It was collected 21 times forming only five associations. This is followed by Brachycaudus cardui (16 samples and 10 associations), Phorodon humuli (11 samples and 5 associations) and Myzus cerasi (10 samples and 7 associations). Other aphid species were sampled less than ten times.

DISCUSSION

This paper presents the first surveys of aphid-tending ants on the territory of Serbia, where their mutualistic relationships are presented through a complete association, plant-aphid-ant. The majority of the ants have been identified at the species level, except the four taxa belonging to the genera Lasius Fabricius and Tapinoma Förster. Of the three subfamilies presented here, Formicinae and Myrmicinae are listed with four genera each, while the subfamily Dolichoderinae is represented only by the genus Tapinoma.

The review of the literature has shown that there is no exact number of aphid species that are attended by each ant species. As already mentioned, some of the ant-aphid relationships are facultative, and therefore cannot always be registered (Starý, 1966). It is not entirely clear why this happens, but it is known that some species of ants show opportunistic behaviour in search of food and aphids. For example, it is shown that Lasius niger exhibits collective exploration of new territories and thus establishes relationships with various aphid species along the way (Devigne & Detrain, 2002). Usually, this species establishes the most numerous ant-aphid associations. For example, in a similar study, Novgorodova and Ryabinin, (2018) showed that L. niger was registered in associations with 103 species of aphids out of a total of 198 registered within the subfamily Aphidinae in the same survey. Lasius niger is one of the most common ants in Europe and the Balkans, often found as synanthropic species. This species has been observed in many countries and apparently has almost Holarctic distribution (AntWeb. Version 8.54.9. 2021). It is the most widespread species in Serbia (Petrov, 2002). On the other hand, Prenolepis nitenshas a somewhat narrower area and is mainly distributed in the Mediterranean region, although it is often found throughout the Balkan Peninsula (Seifert, 2007; Vesnić & Lelo, 2010). This species is also known as the European false honey ant and feeds mainly on sweet fruits, nectar and elaiosomes. In addition, P. nitens also obtains a substantial amount of sugar from different aphid species (Bregant, 1998). Prenolepis nitens often forms numerous associations with aphids. For example, in a similar survey conducted in Turkey, Akyürek et al. (2016) report L. alienus as one of the most common species forms associations with aphids along its two congeners (L. brunneus and L. turcicus Santschi). In the same survey, the most common aphid species attended by ants were Aphis fabae, A. spiraecola Patch, and Brachycaudus cardui. We have assumed that the reason for the abundance of A. fabae is that it is a polyphagous species (Petrović-Obradović, 2003; Blackman & Eastop, 2021) that is present everywhere, thus very often collected.

It was unexpected that some aphid taxa, such as Pterocomma Buckton, Geoica Hart, Tetraneura Hartig or Symidobius oblongus Von Heyden, were not abundant in the sampled material. These taxa are known as regularly visited by ants (Molnár et al., 2000), especially the species from the genera Geoica and Tetraneurathat are in permanent relationships with aphid tending ants (Pontin, 1978; Depa et al., 2020). Having in mind that species from the genera Geoica and Tetraneura live hidden, in the underground, or form galls, their concealment often led to them rarely being collected in the whole sample.

The coaction between ants and aphids is recognized as mutualism and is defined as an interaction between two species that is beneficial for both species (Bronstein, 2015). One might expect that aphid species attended by ants are thriving in comparison to others, however in some cases, for example between L. niger and A. fabae, when a different food is abundant ants often prey on aphids (Offenberg, 2001). A similar behaviour has been observed also in other aphid tending ant species, for example Formica rufa L. (Skinner, 1980). Nevertheless, the relationship between aphids and ants is widely present in nature and is one of the classic examples of mutualistic behaviour that often involves various adaptations driven by coevolution between the two groups.

Since this paper represents one of the first works on ant-aphid associations in Serbia, this is certainly not the definite number of aphids tended ants on the list. On the contrary, we assume that the number of ant and aphid species in associations is many times higher, primarily due to the lack of data, but also due to the flexible nature of mutual relations. Further research will greatly contribute to discovering the number of these interrelationships between the two groups of insects.

Acknowledgments

The authors are very grateful to Dr. Ivan Petrov for the identification of ants collected from 1990 to 1997, and Dr. Marko Karaman for the identification of ants collected from 2016-2017. We are also thankful to Dr. Lydia Mitits for the English language proofreading. This study was partially funded by the Ministry of Education, Science and Technological Development of the Republic of Serbia (Contract No. 451-03-68/2022-14/200178).

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