Research Article |
Corresponding author: José G. Palacios-Vargas ( troglolaphysa@hotmail.com ) Academic editor: Oana Teodora Moldovan
© 2020 José G. Palacios-Vargas.
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:
Palacios-Vargas JG (2020) Acheroxenylla (Collembola, Hypogastruridae), first record from the Americas with description of a new species from a Peruvian cave. Subterranean Biology 34: 109-119. https://doi.org/10.3897/subtbiol.34.50673
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A new diagnosis for Acheroxenylla Ellis, 1976 is proposed, based on new characteristics recently discovered in other species of the genus. A new species living on guano from oil bird guacharo is described and illustrated and its Barcode Index Number (BIN) from BOLD System is given. A key for the identification of the four known species is also included.
Xenyllian group, cueva de Samuel, chaetotaxy, troglomorphy
After
In a recent expedition organized by Josiane Lips to collect cave fauna, several samples were collected in six caves from Rioja Province (northern Perú). They were processed by Berlese-Tullgren, hand collected and kept in alcohol. All of them were preserved in ethanol 96% at the Department of Entomology, Museo de Historia Natural, Universidad Mayor de San Marcos, Perú. Later the specimens of Collembola were sent to the Laboratorio de Ecología y Sistemática de Microartrópodos, Faculty of Sciences, Universidad Nacional Autónoma de México for study.
Among the Collembola, some specimens of Acheroxenylla were found. Five were preserved for molecular study and six were prepared in Hoyer’s solution. Later, they were studied under a contrast phase microscope Carl Zeiss mod. 465270-9906 and drawn with the aid of a camera lucida.
For the molecular study each of the five specimens were photographed and sent for sequencing with the standard COI–5P marker ("DNA barcode", Ratnasingham & Hebert, 2013) at the Canadian Centre for DNA Barcoding.
Abbreviations used in this paper are: Ant = antennal segment; Abd = abdominal segment; hr = anal valve setae; PAO = postantennal organ; Sgd = dorsal guard sensillum; Sgv = ventral guard sensillum; Th = thoracic segment; a = anterior row of setae; m = median row of setae; m’ = microsensillum; or = apical organ; p = posterior row of setae; S = sensillum; ss = sensorial seta; Tita = tibiotarsus.
Class Collembola Lubbock, 1870
Order Poduromorpha Börner, 1913
Family Hypogastruridae Börner, 1906
Small Hypogastruridae (from 0.5 to 1.3 mm). Setae not differentiated in macrosetae, only with smooth or slightly barbulate mesosetae and longer sensory setae. They are usually white, with dark or black color only under each eye, with possible bluish gray pigmentation all over the body. Antennae cylindrical about the same length as the head, with a simple or trilobed retractile papilla; Ant IV with a dorso-external microsensillum, a subapical sensorial organ and 4 cylindrical or oval sensilla: 3 external and one internal. Ant. III organ with 2 microsensilla hidden by or not by a tegumentary fold and framed by 2 longer guard sensilla. Ocelli 2 + 2 (sometimes 1 + 1). Postantennal organ always lacking. Head chaetotaxy with setae a0 and d0; five pairs of dorsal cephalic setae; and two or three subdorsal pairs. Claws without teeth and empodium. Th I with 3 + 3 setae; Th II–III with 4 + 4 setae on row a, 3 + 3 on m row and 4 + 4 on row p. Or a: 3 + 3 and 2 + 2; m: 3 + 3 (m2 and m3 absent) and 1 + 1 lateral; p: 4 + 4 or 5 + 5; two pairs of ss at position m6 and p4. Without lateral microsensillum on Th II. Abd I–III with 2 rows of setae (a and p): 5 + 5 or 6 + 6; one pair of ss at p5; Abd IV with 3 rows of setae (a: 3 + 3 or 4 + 4; m: 2 + 2 (with or without m1 or m4); p: 4 + 4 or 5 + 5; one pair of ss at position p5). Abd V with 2 rows (a and p: 2 + 2 or 3 + 3) one pair of ss at position p3. Each tibiotarsus with 2 or 1 tenent hairs. Ventral tube with 4 + 4 setae. Retinaculum either with 2 or 3 teeth on each ramus or complete absent. Furcula present, reduced or absent. Manubrium, when present, with 2 or 3 pairs of setae, dens if present short or long with maximum 2 setae. Mucro absent except one case. Always with 2 very small anal spines on papillae of the same size.
Acheroxenylla cretensis Ellis, 1976
1 | Furcula and retinaculum absent | 2 |
– | Furcula and retinaculum well developed or reduced, but always present | 3 |
2 | 2 + 2 eyes, occasionally with small pigment spots; p3 on Abd. IV present | A. cretensis Ellis, 1976 (Greece: Creta Island) |
– | 2 + 2 eyes, always with blue pigment spots; p3 on Abd. IV absent | A. canariensis Fjellberg, 1992 (Spain: Canary Islands: El Hierro, Gomera, La Palma, Tenerife, Gran Canaria, Lanzarote) |
3 | Retinaculum with 3 + 3 teeth. Furcula well developed with mucro, long dens with 2 long setae | A. lipsae sp. nov. (Perú: Province Rioja, Cueva de Samuel) |
– | Retinaculum with 2 + 2 teeth. Furcula very reduced without mucro, short dens with 2 tiny setae | A. furcata Fjellberg, 1992 (Spain: Canary Islands: La Gomera, Tenerife, Gran Canaria, Fuerteventura, Lanzarote) |
Holotype female (number FC-UNAM 22501) and one paratype female (numbers FC– UNAM 22502) are kept at Dept. Entomology; Museo de Historia Natural, Universidad Mayor de San Marcos, Perú; two paratypes females one male and one juvenile (numbers FC–UNAM 22500, 22503 to 22325) are kept at Mexican Collembola collection at Facultad de Ciencias, UNAM.
Perú: Region San Martín; Province Rioja, Cueva de Samuel (6°06'92"S, 77°31'58"W) 1,720 m a.s.l. About 5.5 Km North-West of town Naciente de Rio Negro. 16-viii-2017, sample 14470, J. Lips col.
Acheroxenylla lipsae sp. nov. is characterized by the presence of a well-developed furcula with mucro, long dente with two long dental setae each, three manubrial setae and a retinaculum with three teeth. Tibiotarsi are longer than in other species known.
Body length
(average of 7 specimens) = 1.25 mm. Setae not differentiated in macro and microsetae, all smooth and sharp mesosetae about 11 μm with small barbulations. Sensorial setae longer than regular setae, about 30 μm. Sensorial formula as 022/11111. Color, some specimens (Figures
1 Acheroxenylla lipsae sp. nov. 1, group of specimens floating on water close to the guano of oil birds 2 two specimens dorsal view just collected in ethanol 96%; photos 1 and 2 by Josiane Lips 3 dorsal view 4 lateral view, photos 3 and 4 by Maira Montejo and Angela Arango, scale in photos 3 and 4 is 150 μm.
Ant I
with seven dorsal setae, Ant II with 12 setae. Ant III with 17 setae in two whorls, sense organ with two free club-shaped microsensilla, not covered by tegumentary fold; two short guard sensilla (Sgd and Sgv) of same shape and size, and one ventral microsensillum. No eversible sac between Ant III-IV. Ant IV with four cylindrical sensilla, one dorsal and three latero-external; subapical organite, lateral microsensillum and simple subapical bulb (Figure
Head
with typical chaetotaxy for the genus, similar to Xenylla, only 3 subdorsal setae, seta c1 and only 1 setae v (v1), and 3 subequal setae in ocular area (Figure
Leg
chaetotaxy from I to III: precoxae 0,1,2; coxae 3,6–8,5–8; trochanters 5,5,4; femora 12,11,10 one ventral seta very long, as acuminate tenent hair; Tita 19,19,18 (Figures
Dorsal
chaetotaxy of abdomen as in Figure
Ventral chaetotaxy. Thoracic sternites and Abd I without setae. Ventral tube with 4 + 4 setae. Abd II with 9 – 12 setae, one of them (p3) very long; Abd III with 6 setae, p3 slightly longer than others. Abd IV dorsolateral with 5 setae, one of them very long (Figure
Some asymmetries on body chaetotaxy were observed. Several specimens have setae somehow displaced, giving the appearance of asymmetries. One case of supernumerary setae on left side of abdominal segment III was observed on one paratype, where there were 3 setae "p4", giving the appearance of sensorial seta to be on position "p7".
This species is dedicated to Josiane Lips, for her contribution to the knowledge of cave fauna from Perú, Mexico and many other places.
This new species is the largest and most pigmented member of this genus. The main differences of Acheroxenylla lipsae sp. nov. and the other species is the presence of a well-developed furcula with mucro, long dens and two long dental setae, 3 + 3 manubrial setae and retinaculum with 3 + 3 teeth. A. furcata has a reduced furcula, with no manubrial setae, very short dens with one seta each and mucro absent; its retinaculum has only two teeth on each ramus. The type species A. cretensis and A. canariensis lack completely the furcula and retinaculum. All the species have only two eyes per side; nevertheless, in the new species A. lipsae sp. nov., eyes are better developed and closer to each other, and that is why their position seems to be "D" and "E". After the drawings of
About the pigment, A. furcata is white with small spots under each of the 2 + 2 or 1 + 1 eyes and sometimes a scattered bluish gray pigment is present all over the body, while A. lipsae sp. nov. is more pigmented. Tibiotarsi of A. furcata with one apical tenent hair (A1), sometimes weakly clavate, is similar to the new species. The ungues of the Peruvian species is more elongated than in any other species of the genus (ratio tibiotarsus: ungues: 1: 1.0), so this may be a troglomorphic character, and also in the other species tibiotarsus is about twice the length of ungues.
DNA was successfully obtained from three specimens, sequences BCICL008–19 (length 620bp), BCICL009-19 (657bp) and BCICL010 (632bp), which were deposited in the project BCICL of the Barcode of Life Data System (http://www.barcodinglife.org/index.php). Cuticles of two specimens were recovered and mounted in Hoyer’s solution which represent the vouchers and are kept at the author’s institution as type material.
The type locality is Cueva de Samuel. Collecting was done 200 m from the entrance on Guácharo guano, where was the new species found. It is an active cave with water flowing from the cave. The air temperature was 15 °C. Its entrance is about 1,720 m a.s.l. In the first part of the cave there is a gallery with a colony of oil birds (Guácharos, Steatornis caripensis Humboldt, 1817). 500 m deep in the cave there is a big room with many big stalagmites, named Chachapoyas room. There are two small waterfalls, a small at 800 m from entrance and more far another of 10 m. One of the tunnels finishes in a well of more than 40 m.
There were 20 springtails found in the region of Rioja. In two caves only one species was found in each: Cueva del Lobo Perdido (Pseudosinella sp.) and Tragadero de Bellavista (Cyphoderus sp.). Two other caves had three Collembola: Piedra Brillante (Trogolaphysa sp., Pseudosinella sp., Pararrhopalites) and Cueva de los Loros (Pseudosinella sp., Dicranocentrus sp., Trogolaphysa sp.). In Cueva Palestina there were four species: (Pseudosinella sp., Folsomia sp., Folsomiella caeca (Folsom, 1927), Folsomides troglobius (Rapoport & Maño, 1969) while Cueva de Samuel was the most diverse with a new species of Acheroxenylla, and also specimens of Folsomina sp., Pseudosinella sp., Trogolaphysa sp., Cyphoderus sp., Isotomurus sp., Pararrhopalites ecuadorensis Bretfeld et Trinklein, 2000.
Folsomiella caeca (Folsom, 1927) was described from limestone caves in bat dung at Panama. Later it was found at Ecuador in guano from several caves by
In Cueva Samuel, besides the new species, there were other six Collembola found in different samples. Among them, Pararrhopalites ecuadorensis Bretfeld et Trinklein, 2000 was described from one cave from Otonga (Cotopaxi), Ecuador and now is found for the first time from Peru.
The molecular part of this contribution was done thanks to the project "Application of metabarcoding tools to long-term monitoring of soil fauna" (Yves Basset & Héctor Barrios), funded by SENACYT FID16-070. Dr. Diana Silva Dávila, Dept. Entomology; Museo de Historia Natural, Universidad Mayor de San Marcos, Perú kindly lend the cave material collected by Josiane Lips for study. Yony Callohuari (Museo de Entomología Klaus Raven Büller – Universidad Nacional Agraria La Molina) made the slides. Blanca Mejía mounted the cuticles recovered from the sequence’s extraction. Jair Paéz made some drawings under the microscope and prepared the final drawing plates (Fac. Ciencias, UNAM). The Franco-Peruvian Scientific Expedition "Cerro Blanco 2017" lead this study, Dr Jean-Loup Guyot, Dr Xavier Robert, of the Research Institute for Development (IRD), and James Apaéstegui, of the Instituto Geofísico from Perú (IGP). This speleological expedition was organized and supported by Spéléologique Groupe of Bagnols-Marcoule (Gard, France), the Vulcain Caving Club (Lyon, France) and the Espeleo Club Andino (Lima, Peru), the IRD and the IGP. Dr. Frans Janssens reviewed the manuscript and gave important comments to improve it. Larry La Rose (Tres Cruces, N. M. USA) reviewed the final manuscript.