Original articleA comparative study of the fauna associated with nest mounds of native and introduced populations of the red wood ant Formica paralugubris
Introduction
Red wood ants (RWA) are typical in Central and Northern Europe, where seven species of Formica s.s. or the F. rufa group are known [1]. In contrast to other ants, these species are mostly associated with coniferous trees and require cold climates [2]. In the southern portion of their distribution area, their presence is limited to higher altitudes [[3], [4], [5], [6]]. In Italy, the species of Formica s.s. are widespread along the Alpine chain, and only the more thermophilic Formica pratensis Retzius, 1783 naturally occurs at more southern locations in the Apennine mountains [7], although its exact distribution is still unknown. In the mid-twentieth century, nests of several alpine RWA species, such as F. paralugubris Seifert, 1996, F. polyctena Förster, 1850, and F. aquilonia Yarrow, 1955, were repeatedly introduced to the Apennines as biocontrol agents for forest insect pests, and in some cases, viable populations established and started to spread [[8], [9], [10]]. Their impact on the arthropod fauna inhabiting the newly occupied area has been demonstrated [9]. All RWA species are known to profoundly affect local communities, from plants to vertebrates, due to their predatory ability, dominant status, and capacity to modify the physical properties of the habitats they colonize [1,[11], [12], [13]]. The large aboveground nest mound is one distinguishing characteristic of these ants. They are formed to maintain stable humidity and temperature in the nest chambers, and often contrast with harsh external conditions [[14], [15], [16]]. For example, in F. polyctena mounds, the difference between the nest and air temperature during the winter can exceed 20 °C [17]. In cold habitats, this microclimatic stability may turn the RWA mounds into “warm islands”, which can be attractive for a wide array of organisms [18,19]. More in general, that ant nests can provide shelter, food and favorable physical conditions for many litter animals has been established for several ant species [e.g. 20,21,22,23,24].
The invertebrate fauna hosted in RWA nest mounds, assessed in multiple studies, includes a broad range of taxa: isopods, spiders, mites, nematodes, springtails and a long list of insects, from flies to several beetle species [[25], [26], [27], [28]]. More than 120 obligate myrmecophilous species have been found in RWA nest mounds, as well as several other species that occasionally inhabit nests because of their combined and often favorable moisture, pH and temperature conditions [19]. Myrmecophily can be defined as the partial or complete dependence on ant colonies by non-ant species [29]. This relationship can be based upon parasitic, commensal or even mutualistic interactions [30,31]. Thus far, more than ten thousand myrmecophilous arthropods are known, and they have evolved numerous strategies to inhabit or have access to ant nests [[32], [33], [34]], such as chemical camouflage, morphological mimicry and pheromonal attractors [[35], [36], [37]].
In this study, we analyze the invertebrate fauna hosted in the nest mounds of F. paralugubris, a highly polydomous and polygynous RWA species [38]. Since this species was one of the most often introduced into the Italian peninsula [10], we focus our study on the comparison of the nest myrmecophiles from native and introduced populations. Ant translocation involved the movement of entire nest mounds [8], and this likely translocated all the associated fauna as well. The main aims of this study are: i) to confirm that nest mounds can be attractive for the soil fauna, both in the native and imported populations, by comparing assemblages inhabiting nest mounds and soil; ii) to identify potentially myrmecophilous species not previously described in the literature; iii) to compare soil and nest fauna across sites and evaluate if this difference supports the hypothesis of species relocation. We focused on springtails (Hexapoda, Collembola) and oribatid mites (Acari, Oribatida), which were used in previous studies as common representative taxa of the mesofauna inhabiting RWA nest mounds [[39], [40], [41], [42]]. Among microarthropods, springtails and oribatid mites constitute two of the most species-rich taxa of the soil ecosystem [43]. Although quite distant phylogenetically, the two groups share several ecological and behavioral features because of their adaptation to similar ecological niches. Both groups feed on litter and soil micro-organisms and graze on fungi, and thereby affect the dispersion of saprophytic and mycorrhizal species and control fungal populations [[44], [45], [46], [47]]. Their community structure is modulated by several natural factors, including plant diversity, litter quality and meta-population dynamics. However, these two key groups are also sensitive to anthropogenic factors such as land use, soil tillage, environmental pollution, physical disturbance and fire [[48], [49], [50], [51]].
Section snippets
Study area and sampling design
The sampling was carried out between June and August 2017. Samples of nest material and soil were collected from three sites, one in the Alps in the Giovetto di Paline Nature Reserve (abbreviated as GP, 45° 57′57″N, 10° 7′48″E), and two in the Apennines, in the Abetone forest (abbreviated as AB, 44° 08′50″N, 10° 40′24″ E) and the Campigna Biogenetic Nature Reserve (abbreviated as CA, within the Foreste Casentinesi, Monte Falterona e Campigna National Park, 43° 52′00″N, 11° 44′14″E) (Fig. 1).
Results
The estimate of nest density was similar among sites (AB ~ 13 nests/ha, CA ~ 12 nests/ha, GP ~ 12 nests/ha). We collected a total of 32 springtail species (11 in GP, 21 in CA and 16 in AB) belonging to 21 genera, 122 oribatids (49 in GP, 39 in CA and 51 in AB) belonging to 62 genera, 53 morphospecies of other arthropods, 2 morphospecies of Annelida (Haplotaxida) belonging to the Enchytraeidae and Lumbricidae families, and one nematode morphospecies. Of the 53 morphospecies of arthropods, 39
Richness and diversity of soil and nest fauna
The predictions that higher species richness would be found in nest mounds of F. paralugubris than in the surrounding soil was confirmed for oribatids, but not for springtails. As for this latter group, the presence of red wood ants is known not to be a determining factor affecting their occurrence (see Lenoir et al. [40] for a study with F. polyctena). However, little is known about the difference in richness and diversity between ant nests and the surrounding soil. Conversely, for oribatids,
Conclusions
In conclusion, this is the first study to include an introduced population in a comparative analysis of the nest-associate fauna in red wood ants. We confirmed that RWA nests are hotspots for arthropod biodiversity, particularly for oribatid mites. We found several potentially myrmecophilous species that preferred the nest habitat instead of soil, though the symbiotic relationships with ants should be further investigated to verify myrmecophily. We used for the first time a comparative approach
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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