Abstract
This study addresses the diversity of deep soil beetles on the old continental island of Madagascar. We highlight Coleoptera as the only order of insects repeatedly occupying the deep soil (=endogean) habitat. We describe and illustrate soil flotation technique used during our fieldwork in Madagascar in December 2019. We focus on the method’s high-output and mobile technicalities. We document 51 deep soil samples, each about 20 litres in volume, taken by us in varying Malagasy localities (Andringitra, Road RN7, Ankaratra, Andasibe) and habitats (primary forest versus grassland). We provide a preliminary illustrated overview of 1,430 deep soil beetles of Madagascar sampled by us. They include representatives of Carabidae (Anillini, Reicheiina), Leiodidae, Staphylinidae (Aleocharinae, Euaesthetinae, Osoriinae, Paederinae, Pselaphinae, Scydmaeninae), Scarabaeidae, Tenebrionidae and Curculionidae. We emphasize the significant disparity between collecting 1,430 adult endogean beetles and only about a dozen of their larvae, all belonging to Scydmaeninae.
References
Andújar, C., Faille, A., Pérez-González, S., Zaballos, J.P., Vogler, A.P. & Ribera, I. (2016) Gondwanian relicts and oceanic dispersal in a cosmopolitan radiation of euedaphic ground beetles. Molecular Phylogenetics and Evolution, 99, 235–246. https://doi.org/10.1016/j.ympev.2016.03.013
Andújar, C., Pérez-González, S., Arribas, P., Zaballos, J.P., Vogler, A.P. & Ribera, I. (2017) Speciation below ground: Tempo and mode of diversification in a radiation of endogean ground beetles. Molecular Ecology, 26 (21), 6053–6070.
https://doi.org/10.1111/mec.14358
Arribas, P., Andújar, C., Hopkins, K., Shepherd, M. & Vogler, A.P. (2016) Metabarcoding and mitochondrial metagenomics of endogean arthropods to unveil the mesofauna of the soil. Methods in Ecology and Evolution, 7, 1071–1081.
https://doi.org/10.1111/2041-210X.12557
Arribas, P., Andújar, C., Salces-Castellano, A., Emerson, B.C. & Vogler, A.P. (2020) The limited spatial scale of dispersal in soil arthropods revealed with whole-community haplotype-level metabarcoding. Molecular Ecology, 30 (1), 48–61.
https://doi.org/10.1111/mec.15591
Bouchard, B., Bousquet, Y., Davies, A.E., Alonso-Zarazaga, M.A., Lawrence, J.F., Lyal, C.H.C., Newton, A.F., Reid, C.A.M., Schmitt, M., Ślipiński, S.A. & Smith, A.B.T. (2011) Family-group names in Coleoptera. ZooKeys, 88, 1–972.
https://doi.org/10.3897/zookeys.88.807
Cambefort, Y. (1987) Insectes Coléoptères Aulonocnemidae. Faune de Madagascar, 69, 1–87.
Clarke, D.J. (2018) Systematics, natural history, and evolution of the saw-lipped rove beetles (Euaesthetinae): progress and prospects for future research. In: Betz, O., Irmler, U. & Klimaszewski, J. (Eds.), Biology of Rove Beetles (Staphylinidae). Springer, Cham, pp. 81–114.
https://doi.org/10.1007/978-3-319-70257-5_6
Coiffait, H. (1979) Insectes Coléoptères: Staphylinides Oxytelidae Osoriinae. Faune de Madagascar, 51, 1–136.
Dajoz, R. (1980) Coléoptères de Madagascar, III. Nouveaux Staphylinides de la sous-famille des Osoriinae. Bulletin de la Société Entomologique de France, 85, 123–130.
Deharveng, L. & Bedos, A. (2018) Diversity of terrestrial invertebrates in subterranean habitats. In: Moldovan, O.T., Kováč, Ľ. & Halse, S. (Eds.), Cave Ecology. Springer, Cham, pp. 107–172.
https://doi.org/10.1007/978-3-319-98852-8_7
Drees, C., Matern, A., Reimann, T. & Assmann, T. (2010) The dark side of relict species biology: cave animals as ancient lineages. In: Habel, J.C. & Assmann, T. (Eds.), Relict Species: Phylogeography and Conservation Biology. Springer, Berlin and Heidelberg, pp. 91–103.
https://doi.org/10.1007/978-3-540-92160-8
Dudley, R. & Pass, G. (2018) Wings and powered flight: Core novelties in insect evolution. Arthropod Structure and Development, 47 (4), 319–321.
https://doi.org/10.1016/j.asd.2018.06.006
Fancello, L., Hernando, C. & Leo, P. (2009) The endogean beetle fauna of the Marganai-Oridda-Valle del Leni area (SW Sardinia), with description of seven new species of Staphylinidae Leptotyphlinae (Coleoptera). Zootaxa, 2318, 317–338.
Faille, A., Casale, A., Balke, M. & Ribera, I. (2013) A molecular phylogeny of alpine subterranean Trechini (Coleoptera: Carabidae). BMC Evolutionary Biology, 13 (248), 1–16.
https://doi.org/10.1186/1471-2148-13-248
Faille, A. & Lecoq, J.C. (2018) Oedichirus spelaeus n. sp., the first cave dwelling beetle from Madagascar (Coleoptera: Staphylinidae: Paederinae). Journal of Cave and Karst Studies, 80, 13–18.
https://doi.org/10.4311/2017LSC0112R2
Franz, H. (1986) Monographie der Scydmaeniden (Coleoptera) von Madagaskar (mit Ausschluß der Cephenniini). Denkschriften der Österreichischen Akademie der Wissenschaften, Mathematisch-Naturwissenschaftliche Klasse, 125, 1–393.
Fresneda, J., Grebennikov, V.V. & Ribera, I. (2011) The phylogenetic and geographic limits of Leptodirini (Insecta: Coleoptera: Leiodidae: Cholevinae), with a description of Sciaphyes shestakovi sp.n. from the Russian Far East. Arthropod Systematics and Phylogeny, 69, 99–123.
Giachino, P.M. (2008) New genera and species of Anillini (Coleoptera Carabidae Bembidiini) from Madagascar and Seychelles Islands, with notes about their origin and distributions. Bollettino del Museo Civico di Storia Naturale di Verona, Botanica Zoologia, 32, 91–136.
Giachino, P.M. (2015) New Anillini from South Africa, Tanzania, Madagascar and Seychelles Islands (Coleoptera: Carabidae, Bembidiini). Fragmenta Entomologica, 47, 15–31.
https://doi.org/10.4081/fe.2015.130
Giachino, P.M. & Vailati, D. (2010) The subterranean environment. Hypogean life, concepts and collecting techniques. L’ambiente sotterraneo. Vita ipogea, concetti e tecniche di raccolta. WBA Handbooks 3. World Biodiversity Association, Verona, 130 pp.
Giller, P.S. (1996) The diversity of soil communities, the “poor man’s tropical rainforest.” Biodiversity and Conservation, 5 (2), 135–168.
https://doi.org/10.1007/BF00055827
Goulet, H. & Huber, J.T. (1993) Hymenoptera of the World: An identification guide to families. 1894/E. Agriculture Canada, Ottawa, 688 pp.
http://esc-sec.ca/wp/wp-content/uploads/2017/03/AAFC_hymenoptera_of_the_world.pdf
Grebennikov, V.V. (2010) First Alaocybites weevil (Insecta: Coleoptera: Curculionoidea) from the Eastern Palaearctic: a new microphthalmic species and generic relationships. Arthropod Systematics & Phylogeny, 68, 331–365.
Grebennikov, V.V., Bulirsch, P. & Magrini, P. (2009) Discovery of Antireicheia in Cameroon with description of four new species and discussion on phylogeny and distribution of endogean Reicheiina (Coleoptera: Carabidae: Scaritinae: Clivinini). Zootaxa, 2292 (1), 1–14.
https://doi.org/10.11646/zootaxa.2292.1.1
Grebennikov, V.V. & Newton, A.F. (2008) Minute larvae of Leptotyphlinae (Coleoptera: Staphylinidae): description of three genera with discussion on the monophyly and phylogenetic position of the subfamily as inferred from larval morphology. Zootaxa, 1817 (1), 49–58.
https://doi.org/10.11646/zootaxa.1817.1.5
Guzik, M.T., Austin, A.D., Cooper, S.J.B., Harvey, M.S., Humphreys, W.F., Bradford, T., Eberhard, S.M., King, R.A., Leys, R., Muirhead, K.A. & Tomlinson, M. (2010) Is the Australian subterranean fauna uniquely diverse? Invertebrate Systematics, 24, 407–418
https://doi.org/10.1071/IS10038
Hlaváč, P. & Baňař, P. (2017) The Pselaphinae (Coleoptera: Staphylinidae) of Madagascar. VII. Description of Madastiger robustus gen. and sp. nov. from Central Madagascar. Zootaxa, 4311 (3), 435–440.
https://doi.org/10.11646/zootaxa.4311.3.9
Hlaváč, P., Oromi, P. & Bordoni, A. (2006) Catalogue of troglobitic Staphylinidae (Pselaphinae excluded) of the World. Subterranean Biology, 4, 19–28.
Hlaváč, P., Perreau, M. & Čeplík, D. (2017) The subterranean beetles of the Balkan peninsula. ČZU, Praha, 267 pp.
Hoch, H. (2002) Hidden from the light of day: Planthoppers in subterranean habitats (Hemiptera: Auchenorrhyncha: Fulgoromorpha). Denisia, 4 (176), 139–146.
Holdhaus, K. (1954) Die Spuren der Eiszeit in der Tierwelt Europas. Wagner, Innsbruck, 493 pp., 52 tabs.
Jałoszyński, P. (2020) Taxonomy of ‘Euconnus complex’. Part XX. Madagassoconnus Franz and Oneila Peringuey placed as subgenera of Euconnus Thomson (Coleoptera, Staphylinidae, Scydmaeninae). Zootaxa, 4747 (2), 327–338.
https://doi.org/10.11646/zootaxa.4747.2.5
Janák, J. (2013) Revision of the southern African species of the genus Typhloleleupius Fagel, 1964 (Coleoptera: Staphylinidae: Paederinae). Acta Entomologica Musei Nationalis Pragae, 56, 203–210.
Janák, J. & Makranczy, G. (2016) Description of a blind and flightless species of Thinobius from South Africa (Coleoptera: Staphylinidae: Oxytelinae). Acta Entomologica Musei Nationalis Pragae, 56, 203–210.
Jeannel, R. (1954) Les Psélaphides de Madagascar. Mémoires de l’Institut Scientifique de Madagascar, E: Entomologie, 4, 139–344.
Jeannel, R. (1957) Révision des Bembidiides endogés d’Afrique et de Madagascar (Anillini, Coleoptera Caraboidea). Annales du Musée Royal du Congo Belge, 52, 1–68.
Jeannel, R. (1960) Révision des Psélaphides malgaches. Bulletin de l’Académie Malgache, 36 (1958), 31–216.
Jeannel, R. (1963) Monographie des “Anillini”, Bembidiides endogés (Coleoptera Trechidae). Mémoires du Museum National d’Histoire Naturelle, Paris (A), 28, 33–204.
Juberthie, C., Delay, B. & Bouillon, M. (1980a) Sur l’existence d’un milieu souterrain superficiel en zone non calcaire. Comptes Rendus de l’Académie des Sciences, 290, 49–52.
Juberthie, C., Delay, B. & Bouillon, M. (1980b) Extension du milieu souterrain en zone non calcaire: description d’un nouveau milieu et de son peuplement par les Coleóptères troglobies. Mémoires de Biospéologie, 7, 19–52.
Leleup, N. (1965) La faune entomologique cryptique de l’Afrique intertropicale. Musée Royal de l’Afrique Centrale, Annales, Serie in-8°, Sciences Zoologiques, 141, i–ix + 1–186.
Loìpez, H. & Oromiì, P (2010) A pitfall trap for sampling the mesovoid shallow substratum (MSS) fauna. Speleobiology Notes, 2, 7–11.
https://doi.org/10.5563/spbn.v2i0.19
Kühnelt, W. (1963) Soil-inhabiting arthropoda. Annual Review of Entomology, 8, 115–136.
https://doi.org/10.1146/annurev.en.08.010163.000555
Maddison, D.R., Kanda, K., Boyd, O.F., Faille, A., Porch, N., Erwin, T.L. & Roig-Juñent, S. (2019) Phylogeny of the beetle supertribe Trechitae (Coleoptera : Carabidae): Unexpected clades, isolated lineages, and morphological convergence. Molecular Phylogenetics and Evolution, 132, 151–176.
https://doi.org/10.1016/j.ympev.2018.11.006
Morrone, J.J. & Hlaváč, P. (2017) Checklist of the micro- and anophthalmic soil-dwelling weevils of the world (Coleoptera: Curculionidae). Zootaxa, 4239 (1), 1–102.
https://doi.org/10.11646/zootaxa.4239.1.1
Orgiazzi, A., Bardgett, R.D., Barrios, E., Behan-Pelletier, V., Briones, M.J.I., Chotte, J-L., De Deyn, G.B., Eggleton, P., Fierer, N., Fraser, T., Hedlund, K., Jeffery, S., Johnson, N.C., Jones, A., Kandeler, E., Kaneko, N., Lavelle, P., Lemanceau, P., Miko, L., Montanarella, L., Moreira, F.M.S., Ramirez, K.S., Scheu, S., Singh, B.K., Six, J., van der Putten, W.H. & Wall, D.H. (2016) Global Soil Biodiversity Atlas. European Commission, Publications Office of the European Union, Luxembourg, 176 pp.
Orousset, J. (1988) Insectes Coléoptères Staphylinidae Euaesthetinae. Faune de Madagascar, 71, 1–208.
Osella, G. (1977) Revisione della sottofamiglia Raymondionyminae (Coleoptera, Curculionidae). Memorie del Museo Civicodi Storia Naturale di Verona, 2 Serie, Sezione Scienze della Vita, 1, 1–162.
Pace, R. (1999) Insectes Coléoptères Staphylinidae Aleocharinae. Faune de Madagascar, 89, 1–261.
Pace, R. (2008) Aleocharinae (Insecta, Coleoptera, Staphylinidae) de Madagascar. Zoosystema, 30, 555–577.
Peck, S.B. (1990) Eyeless arthropods of the Galapagos Islands, Ecuador: composition and origin of the cryptozoic fauna of a young, tropical, oceanic archipelago. Biotropica, 22, 366–381.
https://doi.org/10.2307/2388554
Rémillet, M. (1973) Aperçu sur la faune souterraine à Madagascar. In: Livre du Cinquantenaire de l’Institut de Spéléologie «Emile Racovitz». Editions de l’Académie Roumaine des Sciences, Bucharest, pp. 135–160.
Rétaux, S., & Casane, D. (2013) Evolution of eye development in the darkness of caves: Adaptation, drift, or both? EvoDevo, 4 (1), 1–12.
https://doi.org/10.1186/2041-9139-4-26
Sabella, G., Viglianisi, F.M. & Petralia, E. (2012) Catalogue of malgasy genera of Pselaphinae Latreille, 1802 and first data on the diversity of Pselaphid beetles population in the Amber Mountain National Park, Northern Madagascar (Coleoptera Staphylinidae). Biodiversity Journal, 3, 429–444.
Schawaller, W. & Purchart, L. (2012) Nanocaecus hlavaci gen. & sp. nov. - first record of the tribe Gnathidiini (Coleoptera: Tenebrionidae: Diaperinae) from the Socotra Archipelago. Acta Entomologica Musei Nationalis Pragae, Supplement 2, 303–314.
Shelef, O., Helman, Y., Friedman, A.L.L., Behar, A. & Rachmilevitch, S. (2013) Tri-party underground symbiosis between a weevil, bacteria and a desert plant. PLoS ONE, 8 (11), e76588.
https://doi.org/10.1371/journal.pone.0076588
Shin, S., Clarke, D.J., Lemmon, A.R., Lemmon, E.M., Aitken, A.L., Haddad, S., Farrell, B.D., Marvaldi, A.E., Oberprieler, R.G. & McKenna, D.D. (2017) Phylogenomic data yield new and robust insights into the phylogeny and evolution of weevils. Molecular Biology and Evolution, 35, 823–836.
https://doi.org/10.1093/molbev/msx324
Smetana, A. (1986) Chionotyphlus alaskensis n.g., n.sp., a Tertiary relict from unglaciated interior Alaska (Coleoptera, Staphylinidae). Nouvelle Revue d’Entomologie, Nouvelle Série, 3, 171–187.
Struyve, T. (2018) On the soil dwelling Staphylinidae of Northwest Spain (Coleoptera). Belgian Journal of Entomology, 72, 1–59.
Švec, Z. (2004) New taxa of the tribes Pseudoliodini and Scotocryptini from Madagascar and the Ivory Coast (Coleoptera, Leiodidae, Leiodinae). Acta Musei Moraviae, Scientiae Biologicae, 89, 53–95.
Thayer, M.K., Newton, A.F. & Chatzimanolis, S. (2012) Prosolierius, a new mid-Cretaceous genus of Solieriinae (Coleoptera: Staphylinidae) with three new species from Burmese amber. Cretaceous Research, 34, 124–134.