Research Article |
Corresponding author: Javier I. Arbea ( jarbeapo@gmail.com ) Academic editor: Ľubomír Kováč
© 2021 Javier I. Arbea, Virginia García López, Francisco Javier Soria, Pedro Abellán.
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:
Arbea JI, López VG, Soria FJ, Abellán P (2021) Collembola from Hundidero-Gato Cave in Southern Spain, with the description of a new species of Entomobrya Rondani, 1861 (Collembola, Entomobryidae). Subterranean Biology 38: 77-90. https://doi.org/10.3897/subtbiol.38.66254
|
This paper deals with some Collembola from a cave at La Sierra de Grazalema (Málaga). In total, eight species of springtails were found. Two may represent new species but there is insufficient material available to prepare full descriptions (one species in the genus Ceratophysella, one in Hypogastrura), one species (Folsomides cf. ayllonensis) is identified to species, but differences from the nominal species suggest further studies may indicate the Grazalema populations represent a distinct form, and one other is described as new to science, Entomobrya virginiae Arbea, sp. nov. The new species is characterized by no sexual dimorphism in colour pattern, 5 central macrochaetae on Abd II and 4 macrochaetae on Abd III. For the identification and description of the new species, the set of characters proposed by
Arthropoda, biospeleology, Entomobryidae, Entomobrya, taxonomy
The Hundidero-Gato system, within the Subbaetic Mountain range (Southern Spain), is a hydrogeological system composed by more than 10 km of galleries. This cave, located between the municipalities of Montejaque and Benaoján in the province of Málaga (Andalusia, Spain), has two mouths: the first one is Hundidero, which acts as a sink, and the other one, which is called Gato, where the complex drains. The system harbours a wide variety of subterranean environments, including an old subterranean river course, subterranean lakes, broad chambers and galleries (
The information about the subterranean biology in this system is scarce and fragmented (
There are few references on the cave-dwelling Collembola in the Subbaetic System. Only nine species have been recorded in some caves from Sierra de las Nieves, Sierra de Almijara and Sierra de Tejeda (
The Hundidero-Gato system is located in the northeast extreme of Sierra de Líbar, within the mountain range of Ronda, in the northwest of the province of Málaga. In this cave we can find three characteristic types of karstification: the first floor corresponds to a first stage, while the lower floor is always flooded; the middle floor is the most relevant as it corresponds with the speleological trek and it is the most developed.
Due to the extension of the system, we have limited the study area to the most accessible part at the entrance. The coordinates of Hundidero are 36°43'39"N, 5°14'19"W, about 558 m above the sea level. The entrance of the cave has a width of 10 m and a height of approximately 60 m, and 400 m of depth accessible on foot.
We used baited pitfall traps to collect invertebrates, which were placed in some areas of the cave that were susceptible to harbor fauna. For the pitfall traps we used clinical analysis cans (volume 150 ml), which were buried and filled with a modification of Turquin´s liquid (
Two areas were sampled: the entrance to the cave, which covers about 400 m from the mouth to the first lake, and the area called gallery, a ledge located after about 20 m from the lake, about 20 m in the vertical of the wall, corresponding to the deepest area that was sampled. In total, sixteen pitfall traps were placed: four in semi-darkness (twilight) and four in total darkness in the entrance area; and five traps in soil with guano and three in soil without guano in gallery. The sampling was carried out in 2016 (both the entrance and gallery) and 2018 (only the entrance), and the traps were placed in the dates that the Natural Park of Sierra the Grazallema allowed us. The traps were in the cave for one week. The entry seasons established by the Park was governed by the activity of the bats, allowing us access from mid-March to mid-April and later from mid-August to mid-November, in order to not disturb the breeding and wintering periods of the bats.
Some specimens were cleared in Nesbitt’s fluid and were mounted in Hoyer’s medium for compound microscope observation in phase constrast. Figures were drawn with a camera lucida.
Chaetotaxy schemes in Entomobrya follow
Abbreviations used: Abd = abdominal segment; Ant = antennal segment; as = sensilla; mc = mesochaeta(e); Mc = macrochaeta(e); psp = pseudopore; Th = thoracic segment; MNCN = National Museum of Natural Sciences at Madrid, Spain; MZUN = Museum of Zoology, University of Navarra, Spain.
Cueva del Gato, twilight zone, 27-III-2016, 1 ♀
The single individual collected apparently represents an undescribed species similar to C. norensis Cassagnau, 1965, characterized by A-type of chaetotaxy (p1 chaeta shorter than p2 chaeta on Abd IV), dens with 6 chaetae, the basal chaeta more than twice as long as the others, retinaculum with 4+4 teeth, tibiotarsi with one pointed tenent hair, claw with one internal tooth and two lateral teeth, filament of empodium 2/3 as long as the inner edge of claw, Ant IV with trilobed apical bulb and 7 thin sensilla, slender anal spines 1.5 times the long of the claws and 1.8 mm length. The species is dark blue and does not show characters typically present in cave-adapted species.
Additional material is needed to confirm the identity of the species.
Cueva del Gato, twilight zone, 27-III-2016, 1 juv.
The single individual collected appears to represent a new species similar to H. vernalis (Carl, 1901), characterized by tibiotarsi with one slightly knobbed tenent hair, empodium with broad basal lamella, dorso-lateral parts of Th II–III with m6 chaeta, Ant IV with trilobed apical bulb and 7 sensillae, dens with 6–7 chaetae, 2.7 times as long as mucro, PAO nearly the same size as an ommatidium, anal spines minute, on high papillae, coarse body granulation (8 granules between the p1 chaetae of Abd V) and 1 mm length. The species is grey-blue and does not show characters typically present in cave adapted species.
Additional material is needed to confirm the identity of the species.
New Sierra de Grazalema (Málaga) record.
Cueva del Gato, twilight zone, 27-III-2016, 16 ex; dark zone, 14-IV-2016, 1 ex, 13-XI-2016, 2 ex, 4-X-2018, 25 ex; cave galleries, 14-IV-2016, 1 ex, 30-IX-2016, 1 ex.
Edaphic and troglophilous, guanophilous species. This is a common European species in the caves of the Iberian Peninsula (Spain and Portugal) and the Balearic Islands (
New Sierra de Grazalema (Málaga) record.
Cueva del Gato, twilight zone, 27-III-2016, 3 ex, 16-VIII-2018, 1 ex.
This is a cosmopolitan species known to occur in dry habitats, surface leaf litter or lichens on rocks (
New Sierra de Grazalema (Málaga) record.
Cueva del Gato, dark zone, 30-IX-2016, 1 ex.
The species lacks pigment, but has 5+5 eyes. The juvenile (0.5 mm) examined differ from F. ayllonensis, as original description (
The physical distance (≈690 km) and morphological differences between the Grazalema and Ayllón populations suggest they may represent distinct species, but additional material from Sierra de Grazalema will be needed to determine if the morphological differences noted here are fixed.
Topography of Hundidero-Gato system and locations where the Collembola were sampled. Modified from
Sistema Hundidero-Gato, Benaoján-Montejaque, Málaga (Sierra de Grazalema Natural Park, Spain), 36°43'39"N, 5°14'19"W, 558 m a.s.l.
Holotype female on slide, Sistema Hundidero-Gato, Benaoján-Montejaque, Málaga (Spain), dark zone, 23-VIII-2018, leg. Virginia García López; 80 paratypes, same data as holotype: 12 females, 4 males and 4 juveniles on slide (11 from twilight and 9 from dark zone) and 60 ex. in a tube with ethyl alcohol (20 from twilight and 40 from dark zone). Deposited in MNCN (holotype and paratypes in slides) and MZUN (paratypes in alcohol).
The name is dedicated to Virginia García López, who captured the specimens.
Body
length 1.80 mm, excluding antennae (mean 16 ex., Table
Measurements of E. virginiae sp. nov. (in micrometers), average from 16 specimens.
Holotype | Mean | Min. | Max. | |
---|---|---|---|---|
Ant I | 129 | 131 | 87 | 179 |
Ant II | 308 | 312 | 225 | 469 |
Ant III | 326 | 317 | 230 | 437 |
Ant IV | 313 | 319 | 253 | 437 |
Ant | 1076 | 1078 | 795 | 1522 |
Head | 377 | 344 | 267 | 446 |
Ant/Head ratio | 2,85 | 3,13 | 2,54 | 3,81 |
Th II | 230 | 216 | 161 | 322 |
Th III | 170 | 144 | 92 | 184 |
Abd I | 175 | 123 | 55 | 175 |
Abd II | 170 | 161 | 92 | 221 |
Abd III | 156 | 134 | 74 | 184 |
Abd IV | 533 | 486 | 377 | 671 |
Abd IV/III ratio | 3,42 | 3,78 | 2,80 | 5,60 |
Abd V | 138 | 112 | 92 | 138 |
Abd VI | 87 | 76 | 51 | 97 |
Body | 2036 | 1795 | 1353 | 2323 |
Manubrium | 368 | 347 | 285 | 483 |
Dens | 469 | 430 | 354 | 561 |
Claw | 77 | 71 | 58 | 86 |
Empodium | 47 | 47 | 37 | 58 |
Tenent hair | 85 | 79 | 63 | 86 |
Head. Eight eyes, GH smaller than EF. Antennae length 1.08 mm, 3.13 times the length of the head (n = 16, Table
Entomobrya virginiae Arbea, sp. nov. 4 head chaetotaxy 5 Th II chaetotaxy 6 Abd II–III chaetotaxy 7 Abd IV chaetotaxy. Symbols: open circle = Mc that could be absent in male and juvenile specimens but present in females; closed circle = Mc that are always present; black chaetae-like = sensilla; black circles with a cross line = pseudopores; long chaetae = bothriotricha.
Thorax
(Fig.
Abdomen
(Figs
Entomobrya virginiae Arbea, sp. nov. 8 labrum 9 labial papilla E 10 tip of Ant IV 11 labral papillae 12 tip of dens and mucro 13 manubrial plate (open circles = Mc; gray circles = pseudopores) 14 trochanteral organ 15 claw and empodium of leg III; Scale bars: 0.02 mm (8, 12–15), 0.01 mm (9–11).
Legs. Trochanteral organ with 15–16 smooth chaetae in V-shaped and 7–8 lateral smooth chaetae (Fig.
For the identification of the species of Entomobrya we must consider a combination of colour pattern and dorsal macrochaetotaxy. It has been shown that species with the same colour pattern can have a different chaetotaxy (
Differences of E. virginiae sp. nov. among the similar species of Entomobrya by colour pattern and/or macrochaetotaxy of Th II and Abd II–III tergites. The species share: Mc S’0 on H3 area of head absent; Th II with 2 Mc on T1 area; Abd III with 1/1 Mc on A3/A5 areas; Abd IV without unpair chaetae on A7 and A9 areas and the trichobothrium at the level T2 and T4. U = unknown character. Differences with E. virginiae sp. nov. in bold. References: 1,
E. achuteygai | E. atrocincta Europe | E. atrocincta North America | E. atteneri | E. benaventi | E. fainae | E. gazmirae | E. grimanesae | E. guayarminae | E. maroccana | E. melitensis | E. multifasciata | E. nigrocincta | E. numidica | E. cf. quinquelineata Canary Islands | E. vergarensis | E. virginiae sp. nov. | |
Ch.1 H1 (Head) An2–An3 | 3 | 2 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | U | 3 | 3 | 3 | 3 | 3 | 3 |
Ch.2 H2 A5–A7 | 2 | 1 | 1(2) | 2–3 | 1 | 1 | 2 | 1 | 1 | 1 | U | 1 | 1 | 1 | 1 | 3 | 2 |
Ch.3 H4 S1–S3–S4 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | 2 | U | 3(2) | 2 | 3 | 3 | 3 | 3 |
Ch.4 H5 Ps2–Ps3–Ps5 | 2 | 2(3) | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | U | 2 | 2 | 3 | 2 | 3 | 2 |
Ch.5 Labral papillae: smooth papillae (1), with some projections (2) | 2 | 1 | 2 | 2 | 2 | 1 | 1 | 2 | 1 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
Ch.6 Length of lateral process subequal to labial papilla E (1) or shorter than labial papilla E (2) | 2 | U | U | 1 | 1 | 1 | 2 | 1 | 1 | U | U | 1 | U | U | 2 | U | 1 |
Ch.7 eyes G&H size = E&F (1), < E&F (2) | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
Ch.8 apical antennal retractile bulb absent (0), lobe simple (1), bilobed (2) | 2 | 1 | 1–2 | 2 | 2 | 2 | 1(0) | 2 | 2 | 1 | 2 | 1–2 | 2 | 2 | 2 | 2 | 1 |
Ch.9 T2 chaetae number a5, m4–m5 | 4 | 3 | 3 | 4 | 3 | 3 | 4 | 4 | 4 | 3 | 3 | 3 | 3 | 3 | 4 | 3 | 4(3) |
Ch.10 T2 chaeta a5’ | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1(0) |
Ch.11 Claw internal teeth 3(3), 4(4) | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 4 | 3 | 4 | 4 | 4 | 4 | 4 | 4 |
Ch.12 Claw dorsal tooth absent (0), basal (1), internal teeth level (2) | 1 | 2 | 2 | 1 | 1 | 2 | 1 | 2 | 2 | 2 | 0 | 1 | 2 | 1 | 1 | 2 | 2 |
Ch.13 A1 Abd II a2–a3 | 2 | 2 | 2(1) | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 |
Ch.14 A2 Abd II m3 series chaetae number | 3 | 3 | 2(3) | 4 | 3 | 3 | 3 | 3 | 3 | 3 | 3 | 2–3 | 2 | 3 | 3 | 3 | 3 |
Ch.15 A4 Abd III above m2 chaetae number | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 1 | 2 | 2 | 2 | 2 |
Ch.16 A6 Abd IV A1–D1 chaetae number | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Ch.17 A7 Abd IV A2–E1 chaetae number | 4 | 4 | 1(4) | 4 | 3 | 3 | 4 | 2 | 0 | 0 | 0 | 2–3 | 2 | 2 | 2(3) | 3 | 3–4 |
Ch.18 A8 unpair chaeta A04 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 0 |
Ch.19 A8 Abd IV A4a–C2a chaetae number | 3 | 3 | 3 | 3 | 3 | 4 | 3 | 3 | 3 | 3 | 4 | 3 | 3 | 3 | 3–4 | 5 | 3 |
Ch.20 A9 Abd IV A5–B5 chaetae number | 2 | 3 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
Ch.21 A10 Abd IV A6–B6 chaetae number | 2 | 3 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 | 2 |
Ch.22 Manubrial plate chaetae number | 5 | 3–4 | 3–4 | 4–6 | U | 4–6 | 6–7 | 4 | 4 | U | 4 | 4 | 4 | 4 | 3–4 | 4 | 4 |
Ch.23 Sexual dimorphism in colour present (1) or absent (0) | U | 0 | 1 | 0 | 1 | 0 | U | 0 | U | 0 | 0 | 0 | 1 | 0 | 0 | 0 | 0 |
Number of differences in relation to E. virginiae sp. nov. | 4 | 5 | 1 | 3 | 5 | 4 | 5 | 3 | 4 | 5 | 5 | 2 | 8 | 5 | 5 | 5 | – |
References | 4 | 2 | 1,3 | 4 | 5 | 4 | 4 | 4 | 4 | 2 | 2 | 2,4 | 2,4 | 2 | 4 | 2 |
New Sierra de Grazalema (Málaga) record.
Cueva del Gato. 9-VIII-2018, 2 ex. in twilight and 11 ex. in dark zone; 16-VIII-2018, 4 ex. in twilight and 11 ex. in dark zone; 23-VIII-2018, 3 ex. in twilight zone; 30-VIII-2018, 2 ex. in dark zone; 16-IX-2018, 8 ex. in dark zone; 20-IX-2018, 16 ex. in twilight zone; 4-X-2018, 25 ex. in twilight and 39 ex. in dark zone.
Known species from the Canary Islands and the southeastern part of the Iberian Peninsula. This troglophilous species is relatively common in subterranean habitats (
New Sierra de Grazalema (Málaga) record.
Cueva del Gato. 9-VIII-2018, 21 ex. in twilight zone; 16-IX-2018, 23 ex. in dark zone; 20-IX-2018, 6 ex. in twilight zone; 4-X-2018, 5 ex. in twilight and 11 ex. in dark zone.
This is a cosmopolitan species widely distributed in Europe and North America. Occurs on the surface and in upper layers of different moist soils and in their low vegetation. Occasionally appears in caves from Spain (
The number of springtails collected is higher in dark zone (58% of all Collembola collected), but the twilight zone proved to be the most richness – of the eight species recorded in this study, we recorded seven in the twilight and only five in the dark zone (Figs
Four of the eight species were represented by only one to four specimens (Fig.
To thank the Department of Zoology of the University of Seville for their unconditional and essential support for the surveys and the authorities responsible for the “Sierra de Grazalema Natural Park”, as well as the “Consejería de Agricultura, Ganadería, Pesca y Desarrollo Sostenible, Junta de Andalucía” that provided the authorizations and permits for the execution of the work. Also thank our friend Toni Pérez Fernández for directing us to the underground world. The authors also would like to thank Enrique Baquero and Aron Katz who provided excellent comments and suggestions that improved this manuscript.