Research Article |
Corresponding author: Dariusz Skarżyński ( dariusz.skarzynski@uwr.edu.pl ) Academic editor: Wanda M. Weiner
© 2021 Dariusz Skarżyński, Adrian Smolis, Ľubomír Kováč, David Porco.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Skarżyński D, Smolis A, Kováč Ľ, Porco D (2021) A new European species of Ceratophysella (Collembola, Hypogastruridae) revealed by morphological data and DNA barcodes. ZooKeys 1021: 1-18. https://doi.org/10.3897/zookeys.1021.63147
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A new species, Ceratophysella stachi, from Denmark, Germany, Luxembourg, Norway, Poland, and Ukraine is described based on morphological data and DNA barcodes. It belongs to a small European group of species with type B chaetotaxy and strong tegumentary granulation with distinct fields of coarse granules: C. granulata Stach, 1949, C. lawrencei (Gisin, 1963), C. neomeridionalis (Nosek & Červek, 1970), C. scotica (Carpenter & Evans, 1899), and C. silvatica Rusek, 1964. It differs from all of them in the chaetotaxy of lateral parts of thoracic terga II–III (setae m6 present and one additional seta outside lateral sensillum m7 present or absent) that is exceptional within the whole C. armata-group. Notes on closely related species C. granulata are also given.
Springtails, integrative taxonomy, COI sequences, Ceratophysella stachi sp. nov., Ceratophysella granulata
Ceratophysella Börner, 1932, comprising 140 species (Bellinger et al. 1996–2021), is one of the largest collembolan genera within the family Hypogastruridae. Although the genus is considered cosmopolitan, the vast majority of species live in the temperate climatic zone of the northern hemisphere. Unfortunately, some of these species are insufficiently known, and there are doubts concerning their taxonomic status. One of these is Ceratophysella granulata Stach, 1949. This species was described from the Tatra Mountains (Polish Carpathians) by
Morphological analysis of available specimens designated as C. granulata (C. cf. granulata, Hypogastrura granulata) from Denmark, Germany, Hungary, Luxembourg, Norway, Poland (including syntypes and topotypes), Romania, Slovakia, Switzerland, and Ukraine from the collections of eight institutions (Table
A list of institutions and countries in which specimens are deposited, with abbreviations.
Abbreviation | Depository | Country |
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AF | Collection of Dr Arne Fjellberg | Norway |
DIBEC | Department of Invertebrate Biology, Evolution and Conservation, University of Wrocław | Poland |
PJSU | Department of Zoology, Institute of Biology and Ecology, Faculty of Science, Pavol Jozef Šafárik University, Košice | Slovakia |
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Hungarian Natural History Museum, Budapest | Hungary |
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Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Cracow | Poland |
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Muséum d’histoire naturelle, Geneva | Switzerland |
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Senckenberg Museum of Natural History, Görlitz | Germany |
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State Museum of Natural History, Ukrainian National Academy of Sciences, L’viv | Ukraine |
Species | Collecting data (all from Poland) | N | Published sequences |
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Ceratophysella granulata (= C. stachi sp. nov.) | Beskid Niski Mountains, Carpathians, litter of the Carpathian beech forest on the slopes of Ostra Góra near village Tylawa, at an altitude of 500 m a.s.l., 20.X.2009, leg. M. Furgoł | 2 | – |
Ceratophysella granulata | Tatra Mountains, Carpathians, litter of dwarf mountain pine shrubs on the slopes of the Gładkie Upłaziańskie, at an altitude of 1600 m a.s.l., 14.VIII.2009, leg. D. Skarżyński | 5 |
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Ceratophysella denticulata | Nizina Śląska Lowland, oak-hornbeam forest in Wrocław, 10.X.2009, leg. D. Skarżyński | 5 | – |
Ceratophysella cavicola | Karkonosze Mountains, Sudetes, old adit Krucze Skały near Karpacz, 650 m a.s.l, 6.VI.2009, leg. D. Skarżyński | 4 |
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Ceratophysella engadinensis | Wzgórza Trzebnickie Hills, peat bog near Twardogóra, 11.X.2009, leg. D. Skarżyński | 5 | – |
Specimens stored in alcohol were cleared in Nesbitt’s fluid (chloral hydrate, concentrated hydrochloric acid, distilled water), slide-mounted in a mixed medium (distilled water, gum arabic, glycerol, chloral hydrate), and studied using a Nikon Eclipse E600 phase contrast microscope. Figures were drawn using a camera lucida. A set of characters commonly used in the taxonomy of the genus (
Lysis of the tissues was carried out in 50 µl volume of lysis buffer and proteinase K incubated at 56 °C overnight. DNA extraction followed a standard automated protocol on 96-well glass fibre plates (
The material under study appeared to be taxonomically heterogeneous. Hungarian specimens (
Among the examined specimens that can be referred to C. granulata, two morphotypes were found, differing in the chaetotaxy of the lateral part of thoracic terga II–III, the size and shape of accessory boss near the postantennal organ, and the shape of mucro. Considering their clear morphological differentiation, both forms are treated as separate species. Thus, the form from the northwestern part of the Carpathians (Poland and Slovakia) was recognized (based on syntypes and topotypes) as C. granulata, whereas the form distributed in Norway through Denmark, Germany, Luxembourg, and the eastern part of Polish Carpathians to Ukraine (Fig.
Distribution of Ceratophysella stachi sp. nov. (black circles) and C. granulata (empty circles). Abbreviations: AKE – Akershus, B – Bieszczady Mts, BM – Beskid Mały Mts, BN – Beskid Niski Mts, BRA – Brandenburg, BS – Beskid Sądecki Mts, BW – Beskid Wyspowy Mts, BZ – Beskid Żywiecki Mts, CH - Čierna hora Mts, FUN – Funen, HES – Hesse, JUT – Jutland, L - Levočské vrchy Mts, LD – Lviv District, LT – Low Tatra Mts, LUX – Luxembourg, M – Muránska planina Plateau, MEC – Mecklenburg-West Pomerania, P – Pieniny Mts, S – Slovak Paradise, SAX – Saxony, SK – Slovak Karst, T – Tatra Mts, VES – Vestfold, VF – Veľká Fatra Mts.
The mean genetic divergence among the four Ceratophysella species included into the analysis was 24.2% (ranging from 19% to 28.2%), and their mean intraspecific variation was 0.5% (ranging from 0% to 0.6%). Similar values were found for both interspecific (mean 23% ranging from 21% to 24.4%) and intraspecific (1%) in C. stachi sp. nov., thus supporting the status of the new species (Table
Intraspecific and interspecific % of K2P distances in the targeted Ceratophysella species.
# | Species | Intraspecific distances | Interspecifc distances | ||||
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1 | 2 | 3 | 4 | 5 | |||
1 | C. cavicola | 0.2 | |||||
2 | C. denticulata | 0.6 | 26.6 | ||||
3 | C. engadinensis | 0.0 | 28.2 | 19.0 | |||
4 | C. granulata | 1.1 | 21.3 | 24.3 | 25.9 | ||
5 | C. stachi sp. nov. | 1.0 | 24.4 | 23.6 | 22.9 | 21.0 | – |
Ceratophysella granulata: Fjellberg, 1998: 41.
Holotype (DIBEC): female, Poland, Carpathians, Beskid Niski Mts, litter of the Carpathian beech forest on the slopes of Ostra Góra near Tylawa village, 500 m a.s.l., 20.X.2009, leg. M. Furgoł. Paratypes (DIBEC): 2 males, same data as holotype; male, juv., 14.V.2001, leg. A. Smolis, D. Skarżyński, other data same as holotype; 3 females, 5 males, juv., 14.V.2002, leg. A. Smolis, D. Skarżyński, other data same as holotype.
Denmark (AF, leg. A. Fjellberg) : female, Jutland, Himmerland, Rold Skov, Fagus liter, 20.III.1994, 94.024; Funen: 6 females, 2 males, Fiskerup Skov, forest stream, 24.III.1994, 94.076; female, Syltemade Adal, Fraxinus/Ulmus/Viburnum litter, 23.III.1994, 94.070. Germany (
Dedicated to Jan Stach, the excellent specialist in Collembola.
Body length 1–2 mm. Colour (in alcohol) bluish-gray to bluish-black. Tegumental granulation strong, with fields of especially coarse granules on head (large uniform field covering whole dorsal side except antennal bases), thoracic terga II–III (two large subaxial fields and two lateral ones of medium size, Fig.
Arrangement of setae on head typical for the genus, spine-like setae absent. Dorsal chaetotaxy of type B (Figs
Antennal segment IV with simple or lobed apical vesicle, subapical organite (or), microsensillum (ms), 7 (2 lateral, 5 dorsal) cylindrical, subequal sensilla and 15–25 slightly curved blunt-tipped sensilla in ventral field (Figs
Ocelli: 8 + 8. Postantennal organ 1.8–2.3 times as large as single ocellus; the former with four lobes, its anterior pair larger than posterior pair. Accessory boss large (equal to or only slightly smaller than posterior lobes of postantennal organ), often granulated (Fig.
Labrum with 5, 5, 4 setae; 4 prelabrals present. Maxillary head of C. armata type (
Tibiotarsi I, II, III with 19, 19, 18 setae, respectively, clavate setae absent. Claws with inner tooth and a pair of lateral teeth. Empodial appendage with broad lamelliform base and filiform apex reaching inner tooth or slightly beyond, ratio empodial appendage/ inner edge of claws = 0.4–0.7 (Fig.
Ventral tube with 4 + 4 setae. Furca well developed. Ratio dens + mucro/inner edge of claw III = 1.8–2.2, ratio dens/mucro = 1.7–2.2. Dens with uniform fine granules and 7 dorsal setae (2–4 inner setae modified) (Fig.
Anal spines yellowish, slightly curved, situated on high basal papillae, 1.1–1.7 times as long as inner edge of claws III (Fig.
The range of distribution of C. stachi sp. nov. appears to be relatively wide. It is known from Denmark (Jutland, Funen), Germany (Brandenburg, Hesse, Mecklenburg-West Pomerania, Saxony), Luxembourg, southern Norway (Akershus, Vestfold), Poland (Carpathians: Beskid Niski, Beskid Sądecki, Bieszczady mountains) and Ukraine (Lviv District) (Fig.
Ceratophysella stachi sp. nov. belongs to a small European branch of species of the C. armata-group, which have strong tegumentary granulation, with distinct fields of coarse granules: C. granulata, C. lawrencei (Gisin, 1963), C. neomeridionalis (Nosek & Červek, 1970), C. scotica (Carpenter & Evans, 1899), and C. silvatica. It differs from all of them in the chaetotaxy of the lateral parts of the thoracic terga II–III (setae m6 present and one additional seta outside lateral sensillum m7 present or absent vs setae m6 and additional setae absent) which is exceptional within the whole C. armata-group (both characters are found in the genus, but in other groups of species: formerly classified as Mitchellania Wray, 1953 and C. denticulata). The remaining differences between C. stachi sp. nov. and related species mentioned above are summarized in Table
Characteristics of Ceratophysella stachi sp. nov., C. granulata and related species. Based on
Species | d2 | oc2 | m6 | p3 | e/cl | Distribution | Habitat preferences |
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C. granulata 1 | − | − | − | + | 0.5–0.7 | Polish and Slovak Carpathians (Fig. |
Cold and humid places in the mountains: mosses in alpine zone, litter and mosses in dwarf mountain pine zone and deep gorges and caves in montane forests zone |
C. lawrencei | + | + | − | + | 0.5–1 | Austrian, Italian and Swiss Alps, Apennines, Polish Tatra Mts. | Litter, mosses on rocks in upper montane zone and above, caves |
C. neomeridionalis | + | + | − | - | 0.2–0.3 | Slovenian Dinaric Mts, Polish and Ukrainian Carpathians | Litter, mosses on rocks in montane zone |
C. scotica 2 | − | − | − | - | 0.7–1.1 | Belarus, Denmark, Finland, Germany, Great Britain, Ireland, Norway, Poland, Russia, Sweden, Ukraine | Hygrophilous and tyrphophilous species living in lowlands and mountains |
C. silvatica | + | − | − | - | 0.3–0.4 | Hungary, Italy, Poland, Romania, Slovakia, Ukraine | Litter, mosses on rocks in upland and mountain forests |
C. stachi sp. nov.3 | − | − | + | + | 0.4–0.7 | Denmark, Germany, Luxembourg, Norway, Poland, Ukraine (Fig. |
Litter and mosses in different types of forests in lowlands and mountains, also heathlands and bogs |
Ceratophysella granulata
Poland (Carpathians):
Specificaton of C. granulata morphology is provided by
Traditionally, the most commonly used method in the taxonomy of the genus Ceratophysella, as in other Collembola, is the analysis of morphological features (
We wish to thank Birgit Balkenhol (Senckenberg Museum of Natural History, Görlitz, Germany), Lászlo Dányi (Hungarian Natural History Museum, Budapest, Hungary), Arne Fjellberg (Norway), Igor Kaprus’ (State Museum of Natural History, Ukrainian National Academy of Sciences, L’viv, Ukraine), Peter Schwendinger (Muséum d’histoire naturelle, Geneva, Switzerland), and Wanda M. Weiner (Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Cracow, Poland), for the loan of the material. We also thank Harald Bruckner for searching for C. granulata in the collection of Natural History Museum in Vienna, Austria. We are grateful to Michał Furgoł (Poland) for collecting C. stachi sp. nov. for DNA barcoding. We also express our sincere thanks to Arne Fjellberg for inspiration to undertake the research. Anatoly Babenko (The Severtsov Institute of Ecology & Evolution, Russian Academy of Sciences, Moscow, Russia) and Arne Fjellberg kindly reviewed the manuscript.