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Fungi Associated with Messor Ants on the Balkan Peninsula: First Biogeographical Data

1
Department of Zoology and Anthropology, Faculty of Biology, Sofia University, 1164 Sofia, Bulgaria
2
ELKH-ELTE-MTM Integrative Ecology Research Group, Biological Institute, Eötvös Loránd University, 1117 Budapest, Hungary
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(12), 1132; https://doi.org/10.3390/d14121132
Submission received: 26 November 2022 / Revised: 9 December 2022 / Accepted: 14 December 2022 / Published: 17 December 2022
(This article belongs to the Special Issue Biodiversity Research in Bulgaria)

Abstract

:
Ant nests’ relatively stable and long-lasting microhabitats present ideal living conditions for many uni- and multicellular organisms, whose relationships range from mutualistic to parasitic. Messor harvester ants inhabit arid and semi-arid open areas where their colonies consist of large numbers of individuals. Due to the high number of other organisms associated with harvester ants, their nests can be defined as islands for unique biota. Despite significant progress in research on ant-associated fungi in Europe, little is still known about the recently described ectoparasitic fungus Rickia lenoirii Santamaria, 2015 (Laboulbeniales), found on two species of ants of the genus Messor. Here we report for the first time the occurrence of the ectoparasitic ant-associated fungus R. lenoirii from three countries (Albania, Bulgaria, and continental Greece) and multiple localities in the Balkans. The fungus was detected on four ant host species—Messor structor (Latreille, 1798), M. wasmanni Krausse, 1910, M. hellenius Agosti & Collingwood, 1987, and M. mcarthuri Steiner et al., 2018 with the latter two representing new host records. Furthermore, spores of the widespread endoparasitic fungus of ants, Myrmicinosporidium durum Hölldobler, 1933 (Blastocladiomycota), were reported for the first time in Messor structor (Bulgaria). Images of the ant-associated Rickia lenoirii taken with a scanning electron microscope, a comparison with R. wasmannii, and a distribution map are also presented.

1. Introduction

Ants are well known as hosts of many parasitic organisms, including several endo- and ectoparasitic fungi [1,2]. To date, thirteen ant-parasitic fungal species have been reported in Europe [3,4]. Some of them are widespread, while others are known from only a few localities [5,6]. Four out of the thirteen myrmecoparasitic fungi are known to occur in the Balkans [7,8,9]. Three of them are ectoparasitic—Aegeritella tuberculata Balazy & J. Wisn., 1982 (Basidiomycota, Trichosporonales), Rickia wasmannii Cavara, 1899 and Laboulbenia camponoti S.W.T. Batra, 1963 (Ascomycota: Laboulbeniales), while the widespread fungus, Myrmicinosporidium durum Hölldobler, 1933 (Blastocladiomycota), is endoparasitic. The latter parasitizes a wide range of ant taxa [10,11]; the others are associated with specific genera. For example, the ectoparasitic Aegeritella tuberculata has been found on Lasius species [12,13,14,15] and less frequently on Formica [16,17,18], R. wasmannii and L. camponoti on Myrmica and Camponotus, respectively [3,19].
Rickia lenoirii Santam., 2015 was described from Aegina Island (Greece) and southern France (near Marseille), both findings being on Messor ants (M. wasmanni Krausse, 1910 and M. structor (Latreille, 1798)). It is the sixth species of the order Laboulbeniales known to parasitize ants, along with Dimorphomyces formicicicola (Speg.) I.I.Tav., Laboulbenia camponoti, L. ecitonis G.Blum, L. formicarum Thaxt., and Rickia wasmannii worldwide [6]. The description of R. lenoirii drew the attention of researchers, and the first distribution data in the Carpathian Basin (six localities in Hungary and one in Romania) were reported [20]. Since the first description and distribution records in the Carpathian Basin, no further data on the species have been available, unlike the other ant-associated species of the genus, R. wasmannii, for which a number of studies on distribution, hosts utilization, and its impact on ants have been carried out in the last decade.
The Balkan Peninsula has long been understudied in this regard, and we have only recently begun to understand the diversity of myrmecoparasitic fungi and their host preference in this region. Therefore, we started a survey to explore this unique ant-associated biota better. In this study, we searched for the presence of parasitic fungal species (mainly R. lenoirii and M. durum) on Messor ants in Albania, Bulgaria, and continental Greece.

2. Materials and Methods

The fungal-infested ants were collected during ant inventory surveys in Bulgaria, Albania, and Northern Greece. Samples were collected by hand-searching. The ant specimens were stored in ethanol, and detection of the fungi was done by microscopic examination. In preparation for the scanning electron microscopy (SEM), the ant specimens were dehydrated in a graded series of ethyl alcohol, then air-dried and glued on thin aluminum boards. They were gold-coated in a vacuum unit, and images were taken by SEM-TM4000 series. A distribution map of previously known and new localities of Messor-associated fungi was created with QGIS (v. 3.26.3).
Although the identification of the ant hosts follows the latest taxonomic revisions, three nest samples (one each from Albania, Greece, and Bulgaria) were left to a species group due to the small number of specimens examined (5 each) and the lack of material from Albania in the latest revision of the M. structor group [21]. Thus, the final species identification of these specimens will be postponed after further studies (also molecular). Nest samples with the infected ants were deposited in the Sofia University collection (BFUS) and in the private collection of SC and were labeled with unique collection numbers.
To determine Rickia lenoirii, thalli were removed with an insect needle and prepared on slides in Heinz-PVA. The specimens were determined based on the shape, size, and number of cells of the thallus, as well as the shape of the antheridia and perithecium, and compared with the original description and diagnostic characteristics [6] and those described in [20]. Similar to the samples from the Carpathian Basin in [20], the apex of the perithecia was, in most cases, less truncated than in the original description. Specimens of R. lenoirii are deposited in the personal collection of FB at Eötvös Loránd University.

3. Results

Fungal-infected workers of Messor ants in the study fields were detected in 15 nest samples—14 with Rickia lenoirii and one with spores of Myrmicinosporidium durum (Table 1). In addition to the new data on the little-known R. lenoirii, previously known ones are also summarized in the same table (Table 1) and a map (Figure 1). For the new data, information on both the host ant species and the number of infected specimens is included. Scanning electron microscope images of R. lenoirii on Messor ants (Figure 2) and of the other species of Rickia infecting ants, R. wasmannii (Figure 3), are presented. A Messor structor ant that is heavily parasitized with M. durum is shown in Figure 4.

4. Discussion

As a result of our study, two fungal species, Rickia lenoirii and Myrmicinosporidium durum were found to infect Messor ants. While the former is specific only to this ant genus, the latter fungus is a generalist with over 35 known host species among ants [8,10]. In this case, the discovery of M. durum in Messor ants is not unexpected, but the difficulty in detecting the infection due to the dark and thick cuticle of Messor ants may be the reason why this is the first time since the Portuguese report and why Messor structor has only now become known as a host (Figure 4).
Due to the relatively recent description of R. lenoirii, more data on the distribution, host species, and impact on them are still needed. The small thallus size of R. lenoirii (Figure 2) is the main reason for its late discovery. As can be seen from some of the data from our collections, infected ant individuals were present in collections long before the species was described.
The data on R. lenoirii in our study contribute novel biogeographic and ecological aspects. We report the first localities from the Balkans to the previously known ones of the fungus from southern France, Aegina Island, and the Carpathian Basin. We enlist 14 sites—2 in Albania, 1 in the continental part of Greece (Falakro Mt.), and 11 in Bulgaria (Table 1, Figure 1). The localities cover a wide altitudinal range from the Black Sea coast at 22 m a.s.l. (Bulgaria, Sinemorets) to nearly 1300 m a.s.l. (Albania, Korab Mt.). While Rickia wasmannii (Figure 3) is widespread, following the distribution of host species of the genus Myrmica in the Palaearctic, R. lenoirii is restricted to more southern parts of Europe, where ants of the genus Messor also occur. It should be noted that although R. wasmannii is widespread in Europe, its host spectrum is relatively narrow, parasitizing mainly Myrmica species that typically occur in moderately cool or moist microhabitats in a given region (e.g., M. gallienii Bondroit, 1920, M. scabrinodis, M. rubra Nylander, 1846, M. vandeli Bondroit, 1920, M. ruginodis Nylander, 1846) [22,23]. This is partly supported by a previous study showing a higher likelihood of R. wasmannii presence in habitats with low mean annual temperature and humidity in the Carpathian Basin, suggesting that climatic elements may significantly shape the distribution of this species [24]. Previously, [6,20] discussed that the distribution data on R. lenoirii so far have been found mainly near large bodies of water and that higher humidity might promote the presence of the fungus. However, most of the new localities from Bulgaria and Albania are far from large water bodies.
In our study, R. lenoirii was discovered on four ant hosts, as Messor hellenius and M. mcarthuri were added to the already known ones, M. structor and M. wasmanni. This confirms the close affiliation of this fungus to the ant genus but also indicates the potential for host range expansion after further exploration. Many species of Messor occur in the Balkans, and all of them prefer xerothermic biotopes. Despite unresolved taxonomic problems in some species groups, at least eight harvester ant species occur in the southeastern parts of the Balkans (Bulgaria, continental Greece, and the European part of Turkey), where more studies have been conducted [21,25,26,27]. For now, four of the known Messor species in the region have been found to be parasitized by R. lenoirii. Only M. structor reaches higher altitudes in the mountains, while the others (M. wasmanni, M. hellenius, and M. mcarthuri) are primarily lowland species. The other four Messor species, for which no records of infections are known so far, have habitat preferences in the Balkans like the latter. Furthermore, they are often sympatric. It would therefore be worthwhile to examine what habitat and climate factors might influence the occurrence of R. lenoirii, which infects Messor hosts with fundamentally different climate and habitat preferences.
In conclusion, the overlooked Rickia lenoirii seems to be more common than the small amount of data so far suggests, but its distribution is restricted in accordance with the range of Messor ant species, which are the most diverse in the Mediterranean region.

Author Contributions

Methodology, A.L.-G., S.C. and F.B.; validation, A.L.-G., S.C. and F.B.; investigation, A.L.-G., S.C. and F.B.; writing—original draft preparation, A.L.-G., S.C. and F.B.; writing—review and editing, A.L.-G., S.C. and F.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Science Fund of the Republic of Bulgaria, grant No. KP-06-N-51/6 from 11 November 2021.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We would like to thank Walter P. Pfliegler for his help in preparing the R. lenoirii specimens on slides and Stanila Arabadzhieva for the map of distribution.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. A map of previously known (in black) and new localities (in red) of Messor-associated fungi, Rickia lenoirii (squares) and Myrmicinosporidium durum (asterisks).
Figure 1. A map of previously known (in black) and new localities (in red) of Messor-associated fungi, Rickia lenoirii (squares) and Myrmicinosporidium durum (asterisks).
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Figure 2. A worker of Messor structor infected by the fungus Rickia lenoirii (a) and its mature thallus (b). The arrow in Figure 2a indicates the attachment location of the fungus from Figure 2b.
Figure 2. A worker of Messor structor infected by the fungus Rickia lenoirii (a) and its mature thallus (b). The arrow in Figure 2a indicates the attachment location of the fungus from Figure 2b.
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Figure 3. Rickia wasmannii on the Myrmica ant head (a) and its thalli (b). The arrow in Figure 3a indicates the attachment location of the fungi from Figure 3b.
Figure 3. Rickia wasmannii on the Myrmica ant head (a) and its thalli (b). The arrow in Figure 3a indicates the attachment location of the fungi from Figure 3b.
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Figure 4. A Messor structor ant with spores of Myrmicinosporidium durum. Scale: 1 mm.
Figure 4. A Messor structor ant with spores of Myrmicinosporidium durum. Scale: 1 mm.
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Table 1. Literature and new data on Messor-associated fungi.
Table 1. Literature and new data on Messor-associated fungi.
Rickia lenoirii Santam., 2015 (Figure 2)
CountryCollection dataLatitudeLongitudeAltitude
a.s.l. (m)
Ant Host, Number of Infected SpecimensSource, Collection Number
GreeceAegina Island37.750523.433728Messor wasmanni KrausseSantamaria & Espadaler 2015
FranceChâteau Gombert, near Marseille43.34975.4497141Messor structor (Latr.)Santamaria & Espadaler 2015
HungaryBudapest47.549519.0340118Messor structor (Latr.)Báthori et al. 2015
HungaryFarkasrét47.482218.9997239Messor structor (Latr.)Báthori et al. 2015
HungaryFerenc-hegy47.516419.0000153Messor structor (Latr.)Báthori et al. 2015
HungaryBalatonfüred46.964117.8136200Messor structor (Latr.)Báthori et al. 2015
HungaryRévfülöp46.833317.6334130Messor structor (Latr.)Báthori et al. 2015
HungaryBadacsony46.786317.4845106Messor structor (Latr.)Báthori et al. 2015
RomaniaHerkulesfürdő44.866822.3993398Messor structor (Latr.)Báthori et al. 2015
AlbaniaDibër, Radomirë, 02.07.2021, leg. A. Lapeva-Gjonova41.812720.48211275Messor sp. (structor group), 1 workerthis study, BFUS-ALG-000507
AlbaniaDibër, Zagrad, 02.07.2021, leg. A. Lapeva-Gjonova41.702120.50011191Messor structor (Latr.), 6 workersthis study, BFUS-ALG-000508
GreeceFalakro Mt., 27.06.2020, leg. A. Lapeva-Gjonova41.238524.0557942Messor sp. (structor group), 5 workersthis study, BFUS-ALG-000506
BulgariaOgrazhden Mt., Churilovo, 10.09.2021, leg. A. Lapeva-Gjonova41.460823.0067671Messor hellenius Agosti & Collingwood, 8 workersthis study, BFUS-ALG-000423
BulgariaThracian plain, Belozem, 17.08.2022, leg. A. Lapeva-Gjonova42.190025.0291143Messor mcarthuri Steiner et al., 5 workersthis study, BFUS-ALG-000615
BulgariaBesaparski hills, Trivoditsi, 15.04.2017, leg. A. Lapeva-Gjonova42.133624.4530191Messor structor (Latr.), 2 workersthis study, BFUS-ALG-000499
BulgariaMaleshevska Mt., Gorna Breznitsa, 27.03.2012, leg. A. Lapeva-Gjonova41.750723.1093484Messor structor (Latr.), 2 workersthis study, BFUS-ALG-000500
BulgariaVratsa karst Reserve, along Darvodeltsi river, 17.04.2016, leg. A. Lapeva-Gjonova43.178323.5775532Messor structor (Latr.), 5 workersthis study, BFUS-ALG-000502
BulgariaZemen gorge, Shegava river mouth, 08.05.2021, leg. I Georgiev42.393122.7103511Messor structor (Latr.), 2 workersthis study, BFUS-ALG-000504
BulgariaEastern Stara planina, Aytos, 19.06.2017, leg. A. Lapeva-Gjonova42.720027.2380263Messor wasmanni Krausse, 1 workerthis study, BFUS-ALG-000306
BulgariaSakar Mt., Radovets, 30.04.2011, leg. A. Lapeva-Gjonova41.927726.4602280Messor wasmanni Krausse, 3 workersthis study, BFUS-ALG-000501
BulgariaEastern Rhodopes Mt., Madzharovo, 04.06.2015, leg. A. Lapeva-Gjonova41.648925.8703134Messor wasmanni Krausse, 3 workersthis study, BFUS-ALG-000503
BulgariaDervent Heights, Golyam Dervent, 06.06.2021, leg. A. Lapeva-Gjonova42.003426.7422466Messor wasmanni Krausse, 2 workersthis study, BFUS-ALG-000505
BulgariaSouth Black sea coast, Sinemorets, 11.11.1997, leg. A. Lapeva-Gjonova42.060527.967922Messor wasmanni Krausse, 2 workersthis study, BFUS-ALG-000616
Myrmicinosporidium durum Hölldobler, 1933 (Figure 4)
CountryCollection DataLatitudeLongitudeAltitudeAnt Host, Number of Infected SpecimensSource, Collection Number
PortugalBaixo Alentejo---Messor barbarus (L.)Gonçalves et al., 2012
BulgariaVrachanska Mt., Lakatnik, 25.07.2014, leg. D. Gradinarov43.089423.4000460Messor structor (Latr.), 1 workerthis study, BFUS-ALG-000509
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Lapeva-Gjonova, A.; Csősz, S.; Báthori, F. Fungi Associated with Messor Ants on the Balkan Peninsula: First Biogeographical Data. Diversity 2022, 14, 1132. https://doi.org/10.3390/d14121132

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Lapeva-Gjonova A, Csősz S, Báthori F. Fungi Associated with Messor Ants on the Balkan Peninsula: First Biogeographical Data. Diversity. 2022; 14(12):1132. https://doi.org/10.3390/d14121132

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Lapeva-Gjonova, Albena, Sándor Csősz, and Ferenc Báthori. 2022. "Fungi Associated with Messor Ants on the Balkan Peninsula: First Biogeographical Data" Diversity 14, no. 12: 1132. https://doi.org/10.3390/d14121132

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