Research Article |
Corresponding author: Enrique Baquero ( ebaquero@unav.es ) Academic editor: Louis Deharveng
© 2024 Enrique Baquero, Rafael Jordana, Floren Fadrique.
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:
Baquero E, Jordana R, Fadrique F (2024) Two new species of Collembola (Arthropoda, Hexapoda) from Cova Urbana, a cave under a city. Subterranean Biology 49: 163-184. https://doi.org/10.3897/subtbiol.49.120956
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The Collembola fauna of the Cova Urbana located under the city of Tarragona (Spain) is studied, and the climatic characteristics of the cave, its partial geomorphology and its planimetry are presented. For the first time in this cave, some specimens of Collembola have been captured and studied, and two new species for science belonging to the genera Coecobrya and Pygmarrhopalites are described and illustrated. In addition, a specimen of the genus Arrhopalites probably belonging to another new species has been studied, but it could not be described because only one specimen was available. The presence of so few specimens and only four species is attributed to the absence of organic matter from percolation and detritus (oligotrophic cave).
Arrhopalitidae, cave fauna, Entomobryidae, new species, troglobionts, urban cave
The “Cova Urbana de Tarragona” (Fig.
This cavity, excavated in a small core of dolomites from the Jurassic period, has developed through a stratification joint, expanded by the corrosion of water from the phreatic level marked by the base level of the Mediterranean. There are also some samples of water circulation under hydrostatic pressure. Subsequent graviclastic processes have created rooms of notable volume, with the consequent chaos of resulting blocks. The chemolithogenic process is very small, taking into account the development of the cavity: it is limited to the base of the entrance shafts and first rooms. The enormous volume of water in the cavity is of phreatic origin and the analyzes carried out by the “Societat d’Investigacions Espeleológiques” show a very low level of chlorides and sodium, so it is ruled out that there may be contact or leaks of seawater, given its proximity (
The climatic conditions of the cavity are exceptional, with a very high-temperature range along the cave (between 20.1 °C and 21.9 °C.) and a relative humidity that is also very high (HR 97.9), a logical consequence of the evaporation of water from the cavity. The concentration of ambient oxygen varies according to the area: from 18.7% to 20.5%, although in one of the Roman galleries half-clogged by debris, 17.2% was recorded. The measurements were carried out with a Hibok C‑315 digital thermo-hygrometer and a Hibok P2‑250 digital oximeter.
A priori, the biological condition of this cavity could be described as almost azoic in terms of troglobitic fauna, considering the faunal richness of relatively nearby cavities. The Cova Urbana is a very mineral cavity, that is, being without contact with the outside, there is no organic, vegetal, or animal matter inside, which could facilitate the formation of a trophic chain: the scarcity of fauna may be motivated due by the poor ecological conditions (limited availability of food) of this underground habitat and the geological isolation of the cavity (
Springtails are the most representative troglobitic fauna of the cavity, and for this reason, sampling has focused on their capture. They have only been found –and after many attempts– in the Maginet Room (Fig.
After the preliminary sorting to separate the Neelipleona and Symphypleona from other Collembola, some representative specimens of each species were selected and mounted in Hoyer’s medium for observation under a microscope, and some specimens were cleared in Nesbitt’s fluid. The remaining samples were stored in 70% ethyl alcohol. The slides were observed under two microscopes: an Olympus BX51‑TF (Olympus Group, Tokyo, Japan) with multiple viewing and phase contrast and a Zeiss model Axio Imager.A1 with differential interference contrast (DIC). For measurements, a U-DA drawing attachment UIS (Universal Infinity System) and a scale calibrated with a slide by Graticules Ltd., Cambridge, UK (1 mm divided in 100 parts) were used. For SEM (Scanning Electron Microscopy) the specimens were dehydrated using a series of ethyl alcohol followed by critical-point drying in CO2, then mounted on aluminum SEM stubs, and coated in an Argon atmosphere with 16 nm gold in a sputter-coater Emitech Ltd., Strovolos, Chipre, model K550. SEM observations were made with a FE-SEM Zeiss model Sigma 300 VP (Zeiss, Oberkochen, Germany).
The terminology for Pygmarrhopalites Vargovitsh, 2009 used in descriptions follows
Abd abdomen or abdominal segment I–VI
al anterolateral s-chaeta
as anterosubmedial s-chaeta
Ant antennal or antenna/ae
a.s.l. above sea level
Mc macrochaeta/ae
mes mesochaeta
mic microchaeta
ms microsensillum/a
PAO postantennal organ
psp pseudopore
Th thorax, or thoracic segments
MZNA Museum of Zoology at the University of Navarra, Pamplona, Spain
Throughout three samplings, four species belonging to the Collembola group have been found, and one mite specimen (possibly due to accidental presence). Regarding the Collembola, in addition to the two species described, a single specimen of Arrhopalites sp., and 17 specimens of Folsomia candida, a cosmopolitan species present in many biotopes in addition to in caves, where it sometimes causes problems due to transporting fungi from the outside that alter the ecosystem were also collected.
Class Collembola Lubbock, 1873
Order Entomobryomorpha Börner, 1913
Family Entomobryidae Schäffer, 1896 sensu Godeiro et al. 2023
Subfamily Entomobryinae Schäffer, 1896 sensu Godeiro et al. 2023
Genus Coecobrya Yosii, 1956
Holotype • female on slide, Spain: Tarragona city, Tarragona province, Cova Urbana, geographic coordinates 41.114193, 1.248222, 15 m a.s.l. (the entrance is in an urban area), 6/vii/2022, dark zone of the cave, by aspirator (MZNA code 782957). Paratypes • same data as holotype, three females on two slides (MZNA codes 782958, 782972 to 782973), 10 in ethyl alcohol (MZNA codes 782961 to 782970) and one mounted on stub for SEM observation (MZNA code 782971) • 29/vii/2022, two females on slide (MZNA codes 782972 to 782973), and two specimens in ethyl alcohol (code samples 782987 to 783988) • 1/vii/2023, 10 specimens in ethyl alcohol (code samples 782975 to 783985) and one mounted on stub for SEM observation (MZNA code 782971). All Floren Fadrique leg (BIOSP, Associació Catalana de Biospeleologia). Specimens deposited in MZNA.
Habitus
as in Fig.
Antennae
(Figs
Head. Clypeal and labral areas in Fig.
Legs. Legs devoid of scales, covered with ordinary ciliated chaetae of various lengths, mic not seen. Coxa of leg I with one proximal psp and two chaetae posteriorly; coxa of leg II with eight chaetae in anterior row, two chaetae in posterior row and one proximal psp; coxa of leg III without proximal psp. Trochanteral organ with 15 smooth, straight, unequal spine-like chaetae (Fig.
Ventral tube
(Fig.
complex. Tenaculum with four large teeth and one ciliated chaeta. Manubrium covered with ciliated chaetae, and seven smooth chaetae on two rows on posterior side. Manubrial plate with two pseudopores and two ciliate chaetae, one each side. Dens without spines, annulated and covered with ciliated chaetae on both sides, and 2 + 2 basal smooth posterior chaetae. Distal smooth part of dens similar in length to mucro. Mucro falcate, basal spine long, nearly reaching the tip of the mucronal tooth (Fig.
Dorsal chaetotaxy
(Fig.
The specimens were captured in the dark area of the cave (Sala Maginet), in the deep and isothermal area of the cavity, very close to the aerial end of the cave (from here, the route is underwater), on wood with fungus. After placing a cheese bait during 15 days on that same wood, only specimens of the Folsomia candida species were captured.
The new species is named after the name of the cavity where it was found, Cova Urbana, which in turn is so named because its entrance is in the heart of a city.
The new species differs morphologically from other known Coecobrya species by presenting four internal teeth of claw. To the best of our knowledge, Coecobrya montana (Imms, 1912) sensu Zhang, Deharveng & Chen, 2009 from India, C. submontana Stach, 1960 from Afghanistan, C. troglobia Jantarit & Nilsai, 2021 (in
Suborder Appendiciphora Bretfeld, 1986
Superfamily Katiannoidea Bretfeld, 1994
Family Arrhopalitidae Stach, 1956
Genus Pymarrhopalites Vargovitsh, 2009
Holotype • female on slide, Spain: Tarragona city, Tarragona province, Cova Urbana, geographic coordinates 41.114193, 1.248222, 15 m a.s.l. (the entrance is in an urban area), 6/vii/2022, dark zone of the cave, by aspirator (MZNA code 782954). Paratypes • same data as holotype, three specimens on slide (MZNA codes 782955 and 782986), and one mounted on stub for SEM observation (MZNA code 782953). All Floren Fadrique leg (BIOSP, Associació Catalana de Biospeleologia). Specimens deposited in MZNA.
Female. Body not pigmented; length (holotype): head, 0.23 mm; body 0.62 mm.
Head. Eyes 1 + 1, unpigmented. Clypeal area, row a: 2 + 2 and an axial chaeta; row b: 2 + 2; row c: 2 + 2; row d: 4 + 4; row e: 5 + 5; row f: 4 + 4. Inter-antennal area, row α: 2 + 2; row β: 1 + 1 and an axial chaeta; rows A and C: 2 + 2 and an axial chaeta; row B: 1 + 1 and an axial chaeta; row D: 2 + 2 chaeta. Lateral chaetae of rows C and D are not spine-like (Fig.
Pygmarrhopalites sietae sp. nov. A head chaetotaxy B Ant I–II (* means that this chaeta has been observed only in one specimen) C Ant III (the arrows point to chaetae that are noticeably thinner than the others and the sensory organ are included in a rectangle with the chaetae in black) Ant IV (the arrow points to the knobbed subapical organite). Scale bar: 0.05 mm.
Antenna
(Fig.
Legs. (Figs
Great abdomen
(Fig.
Abd VI. Sixth abdominal segment: a0 not bifurcate, and none of the other circum-anal chaetae broadened, winged or serrated; anal appendage with long fringes or brush‑like along final two thirds (Fig.
Ventral tube with 1 + 1 subapical chaetae.
Tenaculum with two apical chaetae on the corpus, three teeth, and a basal process on each ramus (Fig.
The specimens were only captured near the main siphon of the Maginet Room (Fig.
The name of the new species is dedicated to the association that maintains the cavity and organizes the visits, the Societat d’Investigacions Espeleològiques de Tarragona (SIET).
There are only two previously described species that share the presence of only one eye, absence of spine-like chaetae on posterior head, presence of papilla on Ant III, the number and position of spines/spine-like on dens (203 for external/anterior/internal) and a similar shape of anal appendage: P. furcatus (Stach, 1945) and P. ornatus (Stach, 1945). P. furcatus has not tooth on the claw of leg 1, a long filament on empodium of leg 3, and the anal appendice simply bifurcate; P. ornatus has not tooth on empodium of leg 1 and the filament on empodium of leg 3 is longer than in the new species; both species have the proximal spine (IIpe) on external dens strong and articulate, while in the new species is only a spine-like chaeta. The three descriptions of P. ornatus (
One female dehydrated on stub (for SEM observation), Spain: Tarragona city, Tarragona province, Cova Urbana, geographic coordinates 41.114193, 1.248222, 15 m a.s.l. (the entrance is in an urban area), 6/vii/2022, dark zone of the cave, by aspirator (MZNA code 782956). Floren Fadrique leg (BIOSP, Associació Catalana de Biospeleologia). Specimen deposited in MZNA.
Sixth abdominal segment description: three spines per side on the dorsal valve and one on each of lateral; broadened, winged, and sometimes serrated circumanal chaetae (A1–3, Av1’, Av1 and Av3) (Fig.
All descriptions of the small abdomen of A. caecus mention 2 + 2 cuticular spines per side (two in dorsal valve and two in lateral valves) (e.g.
This work demonstrates the need for collaboration between different institutions, on this occasion two associations related to caving and natural or cultural heritage, and a university. The interdisciplinary work has made it possible to make available to those interested the topography of an interesting cave located in the center of a large city (135 000 inhabitants) belonging to the Catalonian Community, advances in the knowledge of the biocenosis of this cave, and the description of two new species for the fauna. It is once again demonstrated that the isolation of Collembola species that live in relatively close caves has caused their speciation into different species. Also that the low availability of organic matter means that the abundance of fauna in the caves is low and, as on this occasion, that human beings can be important in directing the distribution of fauna in the caves.
We are deeply indebted to Jakub Sternalski (Department of Invertebrate Zoology, Institute of Systematics and Evolution of Animals, Polish Adademy of Sciences) by the loan of the specimens of Sinella montana and Sinella submontana (Stach Collection) for comparation. The third author would like to express his deep gratitude to Josep Lluís Almiñana and Josep Maria Plana (SIET) for their collaboration in carrying out this study, especially for their work as guides during the sampling in the cavity. We acknowledge the constructive comments made by Robert S. Vargovitsh and an anonymous reviewer; their suggestions helped considerably to improve the present contribution.