Joint Russian-Cyprus project by the Russian Foundation for Basic Research and Research & Innovation Foundation (project no. 19-54-25001) “The association of beetles and lichens as a factor in the evolutionary diversification of lichenophagous Coleoptera – applications for indication of Mediterranean ecosystems”

Participants

Russian team:

1. DrSc Maxim Nabozhenko (Precaspian Institute of biological resourses of Dagestan Federal Researche Centre of the Russian Academy of Sciences, Makhachkala); Web: https://www.zin.ru/animalia/coleoptera/eng/nabozhen.htm

https://entomodon.ru/structure/member/1

https://www.researchgate.net/profile/Maxim-Nabozhenko-2

2. Dr Ludmila Gagarina (Komarov Botanical Institute of the Russian Academy of Sciences, St Petersburg); Web:

https://www.binran.ru/en/sotrudniki/4973/

https://www.researchgate.net/profile/Ludmila-Gagarina

3. Postgraduate Ivan Chigray (Zoological Institute of the Russian Academy of Sciences, St Petersburg). Web:

https://www.zin.ru/animalia/coleoptera/rus/chigray.htm

http://entomodon.ru/structure/member/8

https://www.researchgate.net/profile/Ivan-Chigray

Cypriot team:

1. Dr, Assistant Professor Anna Papadopoulou (University of Cyprus, Department of Biological Sciences, Nicosia); Web:

https://annapapadopoulou.weebly.com

http://ucy.ac.cy/dir/en/component/comprofiler/userprofile/apapad08

https://www.researchgate.net/profile/Anna-Papadopoulou-6

2. Postgraduate Konstantinos Ntatsopoulos (University of Cyprus, Department of Biological Sciences, Nicosia); Web:

https://meelab.weebly.com/people.html

3. Postgraduate Loudmila Jelinscaia Lagou (University of Cyprus, Department of Biological Sciences, Nicosia).

https://www.researchgate.net/profile/Loudmila-Jelinscaia-Lagou

Aim of the project

The research is based on the hypothesis of the co-evolution of lichen-feeding beetles and lichens. We assume that the trophic specialization had a fundamental role in the evolutionary diversification of some largest groups of lichenophagous Coleoptera from the family Tenebrionidae and, possibly, of several other groups of beetles. Earlier, the interrelationships of lichenophagous beetles and their feeding lichens have not been studied, and until recently nothing was known about the existence of diverse and numerous group of beetles that feed exclusively on lichens (about 1000 species of Tenebrionidae in the Holarctic, hundreds species of xylobiontic weevils-lichenophagous of the tribe Otiorhynchini). Conservativeness in the structure of lichenophagous Tenebrionidae and their deep diversification due to widespread distribution in various landscapes and trophic specialization may be associated with archaic feeding of lichens. On the other hand, lichenophagous beetles can significantly affect the composition, structure, and projectivity of the covering of lichens sinusia, and therefore a correction for the impact of lichenophagous macroarthropods should always be made when using lichen-based indication in areas of their mass presence. The aim of our study is to establish the depth of the relationships between foliose, fruticose lichens (epiphytic, epilithic and epigeic) and lichen-feeding beetles for further substantiation of their coevolution, as well as the use of the obtained data and objects in bioindication. The following results will be obtained: the composition and structure of the taxocenes of lichen-feeding beetles in the forests and Mediterranean landscapes of Cyprus with one of the highest diversity of lichenophagous Tenebrionidae in Mediterranean region, trophic spectrum of lichen-feeding beetles, their diurnal and seasonal activity, new data on morphological adaptations of these beetles to feeding lichens and habitats on their sinusias, factors to reduce interspecific competition, the methods of lichen-indication will be improve taking into account the press of lichenophagous Coleoptera and the degree of anthropogenic impact. ITS of sequences from isidia and soredia from the surface of the body of lichenophagous beetles will be studied and a preliminary conclusion drawn on the participation or not participation of lichenophages in the transference of asexual reproduction structures. We will use DNA sequence data to reconstruct phylogenetic relationships of both the lichenophagous beetles (Coleoptera: Tenebrionidae: Helopini) and their host lichens and assess phylogenetic community structure (i.e., phylogenetic clustering vs. overdispersion) of the lichenophagous beetle communities, an approach that allows to distinguish between hypotheses of environmental filtering vs. competitive exclusion. The reconstructed phylogenies will also allow us to identify phylogenetic constraints in host choice, i.e. lichenophagous lineages that appear to be exclusively associated with certain lichen lineages, suggestive of co-evolution processes

Regions of research expeditions: Cyprus, Turkey, the Caucasus.

Results for the first year of the project (August 2019– July 2020)

The structure of the taxocene of lichen-feeding tenebrionids of the tribe Helopini in the central part of the Troodos ridge of Cyprus, in the forests with domination of Cyprus cedar (Cedrus brevifolia) is analysed for the first time. We established that beetles of one life-form feed on both foliose and fruticose epiphytic lichens, which is unusual for Mediterranean ecosystems. Knowledges on the composition and biocenotic relationships of Cyprus species of the genus Helops have been expanded. Two species with a helopioid life-form (feeding on fruticose epiphytic lichens) of the same genus (Helops) of the subtribe Helopina participate in the formation of one taxocene. Such taxocene structure was known in the Mediterranean ecosystems only for representatives of the genera of the subtribe Cylindrinotina (cylindrinotoid life-form, feeding on foliose lichens). A new accidentally introduced species of lichen-feeding beetles (from Europe to Cyprus) Helops caeruleus was registered In the Larnaca region in the gardens and a new data on distribution of Helopini from Cyprus are published, as well as catalogue of Helopini from Cyprus (Nabozhenko et al. 2020). The biocenotic relationships of the Middle Eastern species of the genus Odocnemis were established. Six new Middle Eastern species of lichen-feeding darkling beetles of the tribe Helopini tribe (Nabozhenko, 2019; Nabozhenko, Háva, 2020) and two new species of facultative lichenophages of the Tribe Blaptini (Chigray, 2020) were described as part of the revision of Asian lichenophagous tenebrionids. The differences between the two life forms in the damage of various parts of lichen thalli were revealed. Preliminary phylogenetic analysis using genetic markers of 18S rRNA 600 bp for 44 taxa, COI mDNA for 17 genera and MP20 nDNA for 8 genera revealed the polyphyly of the largest genera in the subtribe Cylindrinotina and monophyly of most genera in the subtribe Helopina.

Publications after the first year of the project

Nabozhenko M.V. 2019. New and little known species of lichenophagous Tenebrionidae (Coleoptera) of the tribe Helopini from Iran. Entomological Review. 99(7): 1026–1034. https://doi.org/10.1134/S0013873819070145

Chigray I., Ivanov A. 2020. A review of the genus Blaps (Coleoptera: Tenebrionidae) of Central and South Kazakhstan with description of two new species. Acta Zoologica Academiae Scientiarum Hungaricae. 66(2): 111–162. https://doi.org/10.17109/AZH.66.2.111.2020

Nabozhenko M.V., Háva J. 2020. To the knowledge of the Near East species of the genus Odocnemis Allard, 1876 (Coleoptera: Tenebrionidae: Helopini). Zootaxa. 4767(2): 319–331. https://doi.org/10.11646/zootaxa.4767.2.7

Nabozhenko M., Keskin B., Papadopoulou A. 2020. Two new species and new records of darkling beetles of the tribe Helopini from Turkey and Cyprus (Coleoptera: Tenebrionidae). Acta Entomologica Musei Nationalis Pragae. 60(2): 411–417. https://doi.org/10.37520/aemnp.2020.25

Results for the second year of the project (July 2020– July 2021)

In 2020-2021, four expeditions were carried out on the project topic:

1. July 2020: Caucasus - Karachay-Cherkessia, North Ossetia

2.March-April 2021: Turkey

3.May 2021: Cyprus

4. June 2021: Caucasus – Dagestan

The trophic relationships of alpine and forest species of Nalassus were identified in the Western and Central Caucasus. Two forest species Nalassus pharnaces and Nalassus brevicollis feed on physcioid epiphytic lichens, and the first species is probably a monophagous beetle and feeds on Phaeophyscia hirsuta (Mereschk.) exclusively on Fagus trunks, while N. brevicollis is polyphagous beetle and feeds on wide range of physcioid lichens Physcia tenella (Scop.) DC., Physconia disorta (With.) J. R. Launon, Physcia adscendens (Fr.) H. Olivier, Vulpicida juniperinus (L.) J.-E. Mattsson & M. J. Lai, Physcia stellaris (L.) Nyl., Phaeophyscia orbicularis (Neck.) Moberg) on various trees. Various alpine species, Nalassus dombaicus, N. alanicus, N. diteras, feed on epilithic parmelian lichens, namely Arctoparmelia separata (Th. Fr.) Hale. Living beetles of Nalassus kalashiani were found for the first time since the original description. The species inhabits the limestone upland steppe in the vicinity of Levashi village, adults hide in the soil in the roots of feather grass and Astragalus during the day, and feed on one species of epigeic lichens at night (in the process of identification). Thus, a narrow trophic specialization is observed only in isolated forest and mountain-steppe species; however, regularities have been revealed in the distribution of ecological groups with different trophic specialization. Since the majority of alpine species have allopatric ranges, there is no division of trophic niches. The aforementioned monophagous beetle Nalassus pharnaces sympatrically distributed with the closely related species Nalassus ludmilae in Abkhazia, the first species only on beeches, and the second only on fir trees. In this case, narrow trophic specialization can be interpreted as one of the factors of species diversification.

A new species of Odocnemis was found in Cyprus (Pano Panagia). It inhabits Pinus brutia at night and feeds on lichens Physcia adscedens. The following taxocenes of lichenophagous Tenebrionidae were found in Cyprus (hel – helopioid form of life, large beetles, feeding on fruticose lichens; cyl. – cylindrinotoid form of life, small beetles, feeding on foliose lichens): Helops glabriventris (hel) + Helops thoracicus (hel) + Raiboscelis cyprius (hel) (Cedrus brevifolis, Pinus brutia); Helops glabriventris (hel) + Raiboscelis cyprius (hel) (Pinus nigra, Pinus brutia); Helops glabriventris (hel) + Odocnemis intrusicollis (cyl) (Pinus nigra). A species of the cyl form of live was found as feeding on fruticose lichen Pseudevernia furfuracea together with Helops glabriventris, however, Odocnemis consumes only the reproductive organs isidia, while Helops feeds on thallus with damage to the upper cortical layer.

A sympatric habitat of two species of Helops was registered for the first time. Helops thoracicus is an older invader to the island and lives only in old cedar forests and in the surrounding old pine forests, while the widespread Helops glabriventris transferred on the island probably in the Messinian period (7.246–5.333 Ma) in the Miocene, widely expanded the range on Cyprus and is displacing an endangered autochthonous species.

Four new species of darkling beetles of the tribe Helopini were found in Turkey in 2021, two of them are herbivorous Catomus, while two other are lichen-feeding Turkonalassus and Armenohelops. The genus Entomogonus was researched in detail. This genus demonstrates a transition from forest humid to arid habitats and it is divided into three ecological groups, corresponding to subgenera: forest mesophylic lichenophages (Eutelogonus) mediterranean dry meadows (s. str.) or semi-desert (Delonurops) xerophylic phytophages. Lichen-feeding species inhabit coniferous forests in Western Anatolia and broadleaf woodlands in Eastern Anatolia, Iraq and Transcaucasia, where they feed on foliose lichens. They require specific habitat conditions, including the presence of host lichens on old large trees at low and medium elevations, large stones near trunks and sources of moisture, which are very rare in Eastern Mediterranean and therefore populations have very narrow ranges. Herbivorous species are distributed in upland xerophytic landscapes, semi-deserts and deserts in the Central Anatolia, Cyprus, Syria, Jordan and Transcaucasia. The change in trophic association allowed this group to occupy vast arid territories, however, anthropogenic activity caused a fragmentation of their ranges. Species of the nominotypical subgenus require large stones in combination with large herbaceous plants and small shrubs, sandstone soil and sources of moisture, which remain around ancient or medieval ruins and in very small areas between fields, resulting in highly fragmented ranges. Semi-desert species have less specific habitat requirements and can be found in highly degraded biotopes, but natural factors, such as moisture or sandy soil limit their ranges.

Publications after the second year of the project:

• Nabozhenko M.V. 2020. A new psammophilic species of the genus Catomus Allard, 1876 (Coleoptera: Tenebrionidae: Helopini) from the Negev Desert, Israel, with a key to all known species from the Near East. Israel Journal of Entomology. 50(2): 31–37. https://doi.org/10.5281/zenodo.3974456
• Ando K., Barclay M.V.L., Bologna A.M.A., Bouchard P., Bousquet Y., Chigray I.A., Drumont A.O.D., Egorov L.V., Horák J., Iwan D., Kami?ski M.J., Królik R., Kubisz D., Löbl I., Merkl O., Nabozhenko M.V., Nardi G., Nikitsky N.B., Novák V., Pollock D.A., Schawaller W., Schuh R., Soldati F., Telnov D., Young D.K. 2020. Catalogue of Palaearctic Coleoptera, Volume 5. Tenebrionoidea (D. Iwan, I. Löbl eds.). Leiden: Brill. xxiv, 945 pp. https://doi.org/10.1163/9789004434998
• Nabozhenko M.V., Mpamnaras A., Kalaentzis K. 2020. Contribution to the knowledge of Mediterranean lichen-feeding darkling beetles of the genus Stenohelops Reitter, 1922 (Coleoptera: Tenebrionidae). Zootaxa. 4896(2): 292–300. https://doi.org/10.11646/zootaxa.4896.2.10
• Chigray I.A. 2020. A new species of darkling beetles of the genus Blaps Fabricius, 1775 (Coleoptera: Tenebrionidae) from Turkmenistan and Iran. Caucasian Entomological Bulletin. 16(2): 311–318. https://doi.org/10.23885/181433262020162-311318
• Nabozhenko M.V., Keskin B., Nabozhenko S.V., Alpagut Keskin N., Papadopoulou A., Gagarina L.V., Ntatsopoulos K., Jelinscaia-Lagou L. 2021. The genus Entomogonus Solier, 1848 (Coleoptera: Tenebrionidae): distribution, reasons for habitat fragmentation and the pathway from forest lichenophages to semi-desert phytophages. In: International Tenebrionoidea Virtual Symposium VI (May 21–22, 2021), Book of Abstracts, 2021: 20–21. https://sites.google.com/view/tenebrionoidea/
• Chigray I.A. 2021. Problems of the subgeneric structure of the genus Blaps Fabricius, 1775 (Coleoptera: Tenebrionidae). In: International Tenebrionoidea Virtual Symposium VI (May 21–22, 2021), Book of Abstracts, 2021: 25. https://sites.google.com/view/tenebrionoidea/