Research Article |
Corresponding author: Alberto Sendra ( alberto.sendra@uv.es ) Academic editor: Oana Teodora Moldovan
© 2018 Alberto Sendra, Kazunori Yoshizawa, Rodrigo Lopes Ferreira.
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:
Sendra A, Yoshizawa K, Ferreira RL (2018) New oversize troglobitic species of Campodeidae in Japan (Diplura). Subterranean Biology 27: 53-73. https://doi.org/10.3897/subtbiol.27.28575
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Two new oversize troglobitic species of diplurans campodeids, Pacificampa daidarabotchi Sendra, sp. n. and Pacificampa nipponica Sendra, sp. n., found in three caves in two southern Japanese islands are described. It is the first record of cave-dwelling Diplurans from Japan and more specifically these are two Campodeinae of Pacificampa Chevrizov, 1978 formally known in continental Asia with three cave-dwelling species described in Russia and China near the north of the Korean peninsula. In P. daidarabotchi sp. n., in addition to its oversized body, the longest ever known in campodeids family, it shows as its main differential taxonomical feature the absence of lp metanotal macrosetae. P. nipponica sp. n. is much closer to continental Pacificampa species but it shows differences in the urotergal macrosetae formula. Both Japanese species have clear troglomorphic features related with their elongated body and appendages and an increase in number and complexity of the sensorial antennal equipment with unique olfactory chemoreceptors. Two biogeographical remarks are inferred: P. nipponica sp. n., has been found in two islands that were connected during the glacial age and P. daidarabotchi sp. n. lives in a single cave near another where P. nipponica sp. n. dwells which allowing to suggest a sympatric distribution; Pacificampa seems to be related with Eumesocampa, a genus from North-America, as a consequence of the Holarctic connection between Asia and America. The interests of P. daidarabotchi sp. n. and P. nipponica sp. n. as endemic species in addition to their biogeographical importance should be taken into consideration to ensure better management of the three touristic caves where they dwell and especially the protection of Mejido-do cave, the only location of the large P. daidarabotchi sp. n. near to an active quarry.
Kyushu Island, Shikoku Island, Pacificampa daidarabotchi , Pacificampa nipponica , cave fauna, troglobite, subterranean, biogeography
To date no data is available about subterranean dipluran fauna in Japanese caves or any subterranean habitats. The knowledge of diplurans in Japan is limited to soil habitats, the first one was a japygid described by
No species of Diplura have described from that moment on, until when an expedition to caves in Japan was carried out from September 5 to 15, 2017. The main objective of this expedition was to sample cave invertebrates in order to understand how communities respond to habitat traits (manuscript in prep.). Eleven carbonate caves were sampled (three on Shikoku Island and eight on Kyushu Island). In Shikoku island, the following caves were sampled: Hiura-do cave (Kumakogen municipality), Inaba-do cave (Tsuno municipality) and Rakan Ana cave (Seiyo municipality). In Kyushu island, the following caves were sampled: Goya Daini Shonyu-do, Goya Daiichi Shonyu-do, Merijo-do and Goya Daysan-do caves (all located in Kitakyushu municipality); Nichiko-do and Nichiko Ni-do caves (both located in Yatsushiro municipality) and Takazawa Shonyu do and Osê-do caves (both located in Kuma municipality) (Figs
The fauna collections were carried out both in transects and throughout several habitats of the caves, prioritizing areas (in the case of general collections) with accumulations of organic matter. The collections were done manually, using brushes and tweezers. The organisms were placed in 70% ethanol immediately after collection. Diplura specimens were found in only three caves (Mejiro-do, Goya Daiichi Shonyu-do and Inaba-do caves) in Kyushu and Shikoku Islands.
The specimens were washed using distilled water and were mounted on slides with Marc André II medium to be examined under a phase-contrast optical microscope (Leica DMLS). The illustrations were made with a drawing tube, and the measurements were taken with a micrometer ocular. To take measurements of body length, the specimens were mounted “in toto” and measured from the base of the frontal process distal macrochaetae to the abdomen’s supra-anal valve. For scanning electron microscopy (Hitachi S-4100), two paratypes were coated with palladium-gold used for scanning electronic microscopic photography and measurement of the sensilla.
The morphological descriptions and abbreviations used in this paper follow
This species is the largest Campodeidae known to date. Daidarabotchi is a giant in Japanese mythology.
Female holotype labeled ME02 from Mejiro-do Cave (33.763N, 130.907E), ISLA 47548, Japan, 10 September 2017, Ferreira, R.L. leg. (SEHU); 1 ♂ labeled ME01 (AS), 1 young female labeled ME03 (SEHU) paratypes from the same type locality, data and leg. mounted in Marc André solution. And 1 ♂, 1 ♀ paratypes from the same type locality, data and leg mounted in separated aluminum stages and coated with palladium-gold (AS). Deposited AS collection and Hokkaido University Insect Collection: SEHU.
Body length 9.5 mm (male) paratype ME01), 10.1 mm (female, holotype) and 6.5 mm (young paratype ME03) (Fig.
One intact antenna in the male paratype ME01 with 37 antennomeres, slightly (1.07) longer than the body (the other antennae of the same specimen is presumably regenerated with 28 antennomeres, 7.4 mm length) and another intact antenna in the young female ME03 with 41 antennomeres, 1.21 times longer than the body (Table
Pacificampa daidarabotchi Sendra, sp. n. 1 Last and penultimate antennomere, paratype ME01 2 olfactory chemoreceptors within the cupuliform organ, paratype 3 detail olfactory chemoreceptor, paratype 4 coniform sensilla on the antennomeres, paratype 5 gouge sensilla on distal whorl on distal antennomere, paratype 6 detail gouge sensillum, paratype.
Pacificampa daidarabotchi Sendra, sp. n., length of the body, antennomeres and metathoracic leg including their segments, and cerci (units in mm); and, number of antennomeres.
Specimen | Body length | antennomeres | Antennae length | Segment length of the metathoracic leg | Total metathoracic length | ||||
---|---|---|---|---|---|---|---|---|---|
Coxa | Trochanter | Femur | Tibia | Tarsus | |||||
paratype ME03 | 6.5 | 41 | 7.9 | 0.30 | 0.35 | 1.05 | 1.10 | 1.00 | 3.8 |
paratype ME01 | 9.5 | 37 | 10.2 | 0.40 | 0.35 | 1.35 | 1.55 | 1.35 | 5.0 |
holotype ME02 | 10.1 | – | – | 0.40 | 0.40 | 1.58 | 1.63 | 1.40 | 5.4 |
Plain frontal process with the three frontal macrosetae smooth. The three macrosetae along each side of the line of insertion of antennomere and x setae smooth and with 31/51/21/30 (a/i/p/x) relatives lengths. Suboval labial palps with latero-external short thick sensillum, with two guard setae, up to 12 setae on anterior border and up to 130 neuroglandular setae.
Thoracic macrosetae distribution (Fig.
Pacificampa daidarabotchi Sendra, sp. n. 7 Pro-, meso- and metanotum, right side, holotype 8 detail epicuticle surface on mesonotum, paratype 9 detail epicuticle surface including external gland in the middle on mesonotum, paratype 10 detail epicuticle surface and the ecdysial suture on metanotum, paratype.
Distribution of abdominal macrosetae on tergites (Fig.
Urosternite I with 7+7 macrosetae (Fig.
Pacificampa daidarabotchi Sendra, sp. n., cercal articles length and total length (units in mm) including number of articles of each cerci.
Specimen | Cerci | Articles length | Total length | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Articles and position | Basal | 1st | 2nd | 3rd | 4th | 5th | 6th | 7th | 8th | 9th | 10th | 11th | 12th | 13th | ||
paratype ME03 | 6 right | 1.7 | 0.7 | 1.1 | 1.4 | 1.6 | 1.6 | 8.1 | ||||||||
Holotype ME02 | 9 right | 1.9 | 0.65 | 0.85 | 0.9 | 1.05 | 1.15 | 1.27 | 1.3 | 1.4 | 10.47 | |||||
14 left | 1.65 | 0.45 | 0.50 | 0.55 | 0.55 | 0,55 | 0.60 | 0.70 | 0.75 | 0.90 | 0.95 | 1.0 | 1.0 | 1.2 | 11.35 |
Female urosternite I with subcylindrical appendages thinner than male appendages (2,7 times longer than wide), each bearing up to 55 a1-glandular setae in a distal field.
Male urosternite I (Fig.
Spermatozoid fascicles present in the paratype male testis but difficult to observe. They are about 100 µm in diameter with a spiral round structure up to 4–7 µm in diameter with 3–5 turns.
Although the former description of Pacificampa Chevrizov, 1978 in Russia near the north of the Korean peninsula had a poorly drawn text, the differential features of the genus were clear: simple subequal claws with no lateral telotarsal process, 3+3 (ma, la, lp) pronotum, 4+4 (ma, la, lp2,3) on mesonotum and 2+2 (ma, lp2) on metanotum with the exception of 1+1 ma in P. daidarabotchi sp. n.; one dorsal femoral macroseta and two ventral tibial macrosetae. Nevertheless, no description of the sexual features was cited in the diagnosis of the genus, nor in any of the proposed species (Pacificampa birsteini Chevrizov, 1978 and Pacificampa caesa Chevrizov, 1978), perhaps this was due to their simplicity. In both sexes the first urosternal appendages are subcylindrical with distal a1 glandular setae slightly more abundant in males than in females. No other glandular setae are present in the first urosternite.
P. daidarabotchi sp. n. differs from other Pacificampa species in several features including its long body with 10.1 millimeters, that is the longest Campodeidae that has ever been recorded. An oversize body could be the rule in the rest of Pacificampa species although there is still not enough data to demonstrate this. Furthermore, it has longer antennae and cerci and more numerous antennomeres and cercal articles than other species of the genus; although the most notable features are the reduction of metanotal macrosetae with 1+1 ma (1+1 ma, 1+1 lp3 in others species of the genus) and the reduction and variability in number of urotergal macrosetae.
Species epithet refers to Japan.
Male holotype labeled SH01 from Goya Daiichi Shonyu-do Cave (33.689N, 130.811E), ISLA 47550, Japan, 9 September 2017, Ferreira, R.L. leg. (SEHU); 1 juvenile paratype labeled from the same type locality (AS), data and leg. mounted in Marc André solution. Deposited AS collection and Hokkaido University Insect Collection: SEHU
Other studied material. 1 ♂, 1 ♀ labeled IN01 and IN02 from Inaba-do Cave (33.439N, 133.086E), ISLA 47549, Japan, 7 September 2017, Ferreira, R.L. leg. (AS).
Body length 5.0 and 6.3 mm (males), 6.0 mm (female) and 4.8 mm (juvenile) (Fig.
Pacificampa nipponica Sendra, sp. n., length of the body, antennomeres and metathoracic leg including their segments, and cerci (units in mm); and, number of antennomeres.
Specimen | Body length | antennomeres | Antennae length | Segment length of metathoraci leg | Total metathoracic length | ||||
---|---|---|---|---|---|---|---|---|---|
Coxa | Trochanter | Femur | Tibia | Tarsus | |||||
paratype SH02 | 4.8 | – | – | 0.20 | 0.17 | 0.60 | 0.70 | 0.65 | 2.32 |
IN01 | 5.0 | – | – | 0.30 | 0.25 | 0.75 | 0.80 | 0.75 | 2.85 |
IN02 | 6.0 | – | – | 0.30 | 0.30 | 0.83 | 0.87 | 0.81 | 3.11 |
Holotype SH01 | 6.3 | 34 | 7.4 | 0.30 | 0.30 | 0.91 | 1.0 | 0.86 | 3.37 |
One intact antenna in the male holotype SH01 with 34 antennomeres, longer (1.17) than the body. Apical antennae 4.6 times longer than wide and central antennomeres 3.5 times longer than wide (Table
Plain frontal process with the three frontal macrosetae smooth. The three macrosetae along each side of the line of insertion of antennomere and x setae smooth and with 25/40/26/20 (a/i/p/x) relative lengths. Suboval labial palps with latero-external short thick sensillum, with two guard setae, up to seven setae on anterior border and up to 110 neuroglandular setae.
Thoracic macrosetae distribution (Fig.
Distribution of abdominal macrosetae on tergites (Fig.
Urosternite I with 6+6 macrosetae (5+5 in juvenile SH02); urosternites II to VII with 4+4 macrosetae; urosternite VIII with 1+1 macrosetae; almost all urosternal macrosetae long, well differentiated and covered by long barbs along the distal half. Smooth apical setae of styli with a short tooth with one tiny thin barb; also, smooth subapical and ventromedial setae, the ventromedial being much longer than the others. Cerci in the holotype with six articles including the basal article, slightly shorter than the body length (0.99); in juvenile paratype young SH02 has two cerci with six and seven articles, 1.30 and 1.41 longer than the body length; their basal articles show several whorls of long thin macrosetae with a few apical barbs, along the medial and distal articles these long macrosetae became smooth and whorls of sorther smooth setae are present among them; all the articles are characterized by an apical whorl of thin smooth setae also present at the end of the last article (Table
Pacificampa nipponica Sendra, sp. n., cercal articles length and total length (units in mm) including number of articles of each cerci.
Specimen | Cerci | Total length | |||||||
---|---|---|---|---|---|---|---|---|---|
Articles and position | Basal | 1st | 2nd | 3rd | 4th | 5th | 6th | ||
Paratype SH02 | 6 left | 1.30 | 0.60 | 0.75 | 1.05 | 1.30 | 1.25 | 6.25 | |
7 right | 2.65 | 0.50 | 0.55 | 0,.0 | 0.70 | 0.80 | 0.95 | 6.75 | |
Holotype SH01 | 6 (?) | 1.40 | 0.60 | 0.80 | 1,00 | 1.20 | 1.25 | 6.25 |
Female urosternite I with subcylindrical appendages slightly thinner than male appendages 2.2 times longer than wide, each bearing 30 a1-glandular setae in a distal field.
Male urosternite I with moderated thick subcylindrical appendages 2 times longer than wide, each bearing up to 50 a1-glandular setae in a field covering the distal fifth of the appendage.
P. nipponica Sendra sp. n. is closer to the continental Pacificampa (P. birsteini, P. caesa by
P. daidarabotchi Sendra sp.n. was found in Mejiro-do Cave (33.763N, 130.907E) which is used for touristic purposes. This limestone cave is located in Kitakyushu City (Fukuoka Prefecture) on Kyushu Island (Fig.
26 Karst landscape in the area where Mejiro-do cave is located 27 Map of Mejiro-do cave, indicating the touristic area (marked in pink), and the locations where specimens of P. daidarabotchi were found (red dots) 28 conduit in the non-touristic area, trespassed by a stream 29 touristic area near the cave entrance 30 speleothems, where some specimens can be observed 31 P. daidarabotchi, living specimen.
Individuals of P. daidarabotchi Sendra sp.n were only found in deeper areas of the cave (at least 250 m far from the entrance), which are relatively well preserved (Fig.
Inaba-do Cave (33.439N, 133.086E) comprises a limestone cave associated to the Chichibu zone, a Jurassic accretionary prism. It is located in Tsuno Town (Kochi Prefecture), in Shikoku Island (Fig.
33 Karst landscape in the area where Inaba-do cave is located 34 Inaba-do cave entrance 35 chamber located at the innermost area of Inaba-do cave 36 P. nipponica, living specimen from Inaba-do cave 37 stone wall built in Goya Daiichi Shonyu-do cave 38 mettalic stairs in Goya Daiichi Shonyu-do cave 39 P. nipponica, living specimen from Goya Daiichi Shonyu-do cave.
Pacificampa nipponica Sendra sp. n. was also found in Goya Daiichi Shonyu-do cave (33.689N, 130.811E), another show cave located in the same municipality of Mejiro-do cave (in Kyushu Island – Fig.
The characteristics of 3+3 (ma, la, lp) pronotal macrosetae and the simple claws without lateral crests put Pacificampa into Campodeinae, a subfamily widespread in all continents except in Antarctica (Conde 1956). The absence of lateral telotarsal process and the extra macrosetae on metanotum, with 2+2 lp2,3, are not common in Campodeinae and this combination characterize Pacificampa genus, distinguishing it from other Campodeinae genera (
Eumesocampa, with three soil-dwelling species cited in several localities in the United States of North-America (
Metriocampa, is more widespread than other genera, with 16 already described species (
All five known Pacificampa species have been found in caves. P. birsteini, P. caesa, including one undescribed Pacificampa species from China (
The presence of P. nipponica Sendra sp. n. in two caves on Shikoku Island and Kyushu Islands is remarkable. These two islands are now separated by a sea, but it is known that they were connected during the last glacial age (20,000–10,000 years ago). Another exemple, among the cave-dwelling fauna, that highlights the biogeographical affinity of these two islands, is that related to a couple of cryptic troglobitic beetle species of the subgenera Paratrechiama and Pilosotrechiama of the genus Rakantrechus (Trechinae) (
P. daidarabotchi sp. n. was collected in Mejiro-do Cave, Kyushu Island, nearby the cave from which P. nipponica sp. n. was collected. A similar distribution, also dwelling in the same cave, has been reported in several subterranean campodeids; Campodea (Campodea) grassii Silvestri, 1912 and Campodea (Campodea) majorica Condé, 1955 from the extreme east of the Iberian peninsula (
Firstly, we would thank Marconi Souza Silva, T. Komatsu and Y. Hara for bringing up the vital sampling effort made. For T. Yamashita, the owner of Mejiro Cave, for allowing us to access the cave. The field trip in Japan was supported by JSPS research grant 15H04409 to KY. Investigation of Mejiro Cave was conducted under the permission from Fukuoka Prefecture (permission ID 29-628). We are also indebted to the electron microscopy facility at the Universitat de València, specially with Enrique Navarro, Pilar Gómez and Rafael Benito for their help and instructions on preparing the material for the scanning electron microscope and obtaining the photographs. We also thank Katie Marsen for helping us translate this paper. We would like also to thanks the revisions works made by Loris Galli and Alessandro Giupponi. R. L. Ferreira is grateful to the National Council of Technological and Scientific Development (CNPq) for a research grant (Process number 304682/2014-4).