Acceptance of two native myrmecophilous species, Platyarthrus hoffmannseggii (Isopoda: Oniscidea) and Cyphoderus albinus (Collembola: Cyphoderidae) by the introduced invasive garden ant Lasius neglectus (Hymenoptera: Formicidae) in Belgium

The myrmecophilous isopod Platyarthrus hoffmannseggii Brandt, 1833 and the myrmecophilous springtail Cyphoderus albinus Nicolet, 1842 are commonly found in nests of a wide range of ant species in Belgium. Here we report the first record of both myrmecophiles in nests of the invasive garden ant Lasius neglectus in the Citadelpark of Ghent, Belgium. Platyarthrus hoffmannseggii was found in two of the Lasius neglectus nests studied. In one of the two C. albinus was also discovered. In the localities where the invasive garden ant Lasius neglectus was introduced, as is also the case in the Citadelpark in Ghent, it out-competes all native ant species. This ant has a dramatic effect on the local native ant fauna. However, some of the myrmecophilous species associated with the native ant-fauna are less threatened as they are accepted by this invasive garden ant.


INTRODUCTION
In 1990 the invasive garden ant Lasius neglectus was first discovered and described from Budapest (Boomsma et al., 1990;Loon van et al., 1990).Since then, this polygynous, supercolonial and very competitive ant has been recorded at 93 localities in 15 countries all over Europe and nearby Asia (Schultz & Seifert, 2005;Espadaler & Bernal, 2006).Recently, more has been discovered about its distribution, origin, colony structure, ecology and behaviour at the sites where it was introduced (Seifert, 2000;Espadaler & Rey, 2001;Espadaler et al., 2004;Schultz & Seifert, 2005;Espadaler & Bernal, 2006).The source of the invasive garden ant is thought to be western Asia, most probably somewhere in the area between Asia Minor and Iran (Seifert, 2000;Schlick-Steiner et al., 2003;Schultz & Seifert, 2005).This ant is mainly introduced and spread by man: the transport of horticultural products is suggested to be the main vector for long distance dispersal (Seifert, 2000;Dekoninck et al., 2002;Tartally et al., 2004).This is certainly also the case for Belgium, where L. neglectus arrived before 1978 (Dekoninck et al., 2002).It has spread locally around its place of introduction: the Citadelpark in Ghent.In the microhabitats where this pest species settles, it out-competes other species of ants and produces huge nests.Also at other sites where this species was introduced in Europe, it out-competes native ant species, locally alters the structure and functioning of ecosystems and achieves pest status (Boomsma et al., 1990;Seifert, 2000;Tartally, 2000;Espadaler & Rey, 2001;Vöros & Gallé, 2002;Czechowska & Czechowski, 2003;Schlick-Steiner et al., 2003;Espadaler et al., 2004;Tartally et al., 2004;Schultz & Seifert, 2005;Espadaler & Bernal, 2006).The environmental factors determining the potential threat of L. neglectus to the native ant fauna and its spread in Belgium are the aims of the present study.
Many ant species have several guests in their nests (beetles, mites, crickets, woodlice, springtails, …).Some of these myrmecophilous species are ignored or tolerated; others are attacked (Hölldobler & Wilson, 1990).For most of these myrmecophilous species, information on their ecology, behaviour, live cycles and dispersal is lacking because they are difficult to observe and can only be found when specifically searched for.L. neglectus has a different colony structure from most other Lasius s. str., i.e., it is polygynous and constructs huge nests, possibly experiences more diverse conditions, offers more places for other species to survive in and routes for entering the nest, and thus in general offers more refuges for myrmecophiles than the smaller nests of monogynous species.Information on the nest fauna of L. neglectus in its original habitat is still lacking.However, Espadaler & Bernal (2006) give some indication of other animals associated with L. neglectus in Spain, where this ant was also introduced (Coleoptera: Clythra laeviscula Ratzeburg, 1837 (Chrysomelidae) larvae in a nest at Sant Cugat and one adult of Amphotis marginata (Fabricius, 1781) (Nitidulidae) in a nest of L. neglectus at Seva, Barcelona; Orthoptera: Myrmecophilus acervorum Panzer, 1799 in Bellaterra, Seva and Begues).
Another myrmecophilous species in nests of L. neglectus at the sites where it was introduced, is the isopod Platyarthrus schoblii Budde-Lund, 1885, which was recently recorded in nests of this ant in Budapest (Tartally et al., 2004).These authors suggest that this is the result of a joint introduction of the isopod and L. neglectus into Hungary, as P. schoblii is a new species for that country and only previously known from the Mediterranean region.In their study they recorded the presence of this isopod in 60% of the L. neglectus populations studied (Tartally et al., 2004).The other well-established representative of the myrmecophilous genus Platyrarthrus in Hungary, P. hoffmannseggii, was not found to co-occur with L. neglectus.P. hoffmannseggii is a widely distributed isopod in western-Europe that co-occurs with a great number of species from several genera of host ants (Vandel, 1962;Berg & Wijnhoven, 1997).Tartally et al., (2004) supposed that L. neglectus might also adopt P. hoffmannseggii in a relatively short time after introduction, as happened in the case of P. schoblii in Spain.There, the native P. schoblii was found together with the introduced and locally well established Argentine ant Linepithema humile (Tartally et al., 2004), which supports suggestion that this isopod is likely to be accepted by this new host species.
In Europe, C. albinus is widely distributed from Ireland via Norway and Mid-Finland, to Ukraine via Italy and until North Africa in the south, and up to Lebanon (Gisin, 1960;Salmon, 1964).Records cited by Salmon (1964) from North America (USA) (= Pseudosinella sp.cfr.Delamare Deboutteville (1948)), South America (Argentina) (= dubious record cfr.Mari Mutt & Bellinger, 1990), West Africa (Sierra Leone) and Micronesia (Marianen) need to be validated; they concern most probably other species.
In urban sites in Belgium, and the parks of the city of Ghent especially, P. hoffmannseggii is a commonly found myrmecophile in ant nests.It is assumed to have a wide range of hosts in Belgium and adjacent countries (Vandel, 1960;Berg & Wijnhoven, 1997;Dekoninck et al., 2003) and probably can also be found in a wide variety of habitats.
Recently an inventory of these two ant guests was undertaken in The Netherlands and Belgium.The major aims were to (1) gather all the records, (2) collect data on the hosts, (3) obtain information on the soil properties of the known localities and (4) gather information on their abundance and behaviour in ant nests.It was during this project that C. albinus and P. hoffmannseggii were recorded for the first time in nests of the invader garden ant, L. neglectus, in Ghent (Belgium).

MATERIAL AND METHODS
On 24.iv.2006five nests of Lasius neglectus in the Citadelpark were inspected for myrmecophilous guests.When checking the colonies for the presence of P. hoffmannseggii and C. albinus, nests were opened by turning over stones.Each time adults of the two species were carefully looked for by hand sorting and sifting of the sandy soil, plant debris and small stones.

RESULTS AND DISCUSSION
Adults of P. hoffmannseggii were found in two of five L. neglectus nests in the Citadelpark.In one of the two nests four adults and one juvenile of the springtail C. albinus were also observed.Specimens are stored in the collection of the RBINS, Royal Belgian Institute of Natural Sciences and the collection of the RUCA, Rijksuniversitair Centrum Antwerpen.The L. neglectus nests, where no myrmecophiles were found, were situated in less sunny conditions and perhaps this is why they lacked P. hoffmannseggii and C. albinus.
The habitat of C. albinus is characterised as follows: dry soil conditions, always found in the company of ants, regularly found in ant nests under stones; temperature range of soil between 6°C and 14°C; degree of moisture in the soil = 2-25% (volume); found from January to December (Bockemühl, 1956).In a soil sample taken at Spitzberg near Tübingen, C. albinus was found at a depth of 12 to 18 cm, when the temperature at the surface was 26°C.This species seems to be confined to a narrow temperature range (Bockemühl, 1956).
A preliminary list of the possible hosts in Belgium and The Netherlands (Berg & Dekoninck, unpubl. records) indicates a wide range of possible native hosts as already reported for elsewhere in Europe for both C. albinus (Delamare Deboutteville, 1948;Salmon, 1964;Vannier, 1971;Janssens, 1995;Henderickx & Vets, 2003) and P. hoffmannseggii (Vandel, 1962;Berg & Wijnhoven, 1997).We assume that P. hoffmannseggii and probably also C. albinus are common guests in ant nests in the parks of the city of Ghent and they have no particular preference for any particular species of ant.We assume that this was also the case in the Citadelpark before the arrival of the invasive garden ant.As this invasive species has out-competed almost all other ant species, the only possible nests for both myrmecophilous species are now the supercolonies of L. neglectus.
How both myrmecophilous species are able to locate and colonize the nests of their new hosts (and also other host nests) is unknown.Probably they produce eggs that are "recognized" or misidentified as ant eggs or larvae and brought to the nests, as is sometimes the case for other myrmecophilous species, such as butterflies (Elmes et al., 1991;Thomas et al., 1991) and beetles.This might be the case because Vannier (1971) observed Myrmica ruginodis workers transporting not only their larvae but also specimens of C. albinus deep into their nest when the nest was opened.
The suggestion that L. neglectus might adopt local myrmecophilous species (Tartally et al., 2004) is confirmed here.It is unknown if this is a quick process taking only several years or whether it takes much longer, because the first L. neglectus colony probably reached Ghent before 1978 (Dekoninck et al., 2002).The high percentage of nests with these myrmecophiles indicates it is a quick process.Donisthorpe (1927) mentions a similar case of the introduced ant (Wasmannia auropunctata Roger, 1863) hosting the native C. albinus in the hot-houses at Kew (Great Britain).The introduced pest ant species L. neglectus seems to be having a dramatic impact on the local ant fauna in Europe (Espadaler, 1999;Seifert, 2000;Espadaler & Rey, 2001;Dekoninck et al., 2002, Espadaler et al., 2004;Espadaler & Bernal, 2006).However, some myrmecophilous species seem to be able to adapt and colonize the nests of this introduced ant species.Probably for these species colonizing the nests of other ants is not a problem that threatens their survival.