Research Article |
Corresponding author: Alberto Sendra ( alberto.sendra@uv.es ) Academic editor: Oana Teodora Moldovan
© 2019 Alberto Sendra, Craig Wagnell.
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, Wagnell C (2019) The cave-dwelling dipluran (Diplura, Campodeidae) on the edge of the Last Glacial Maximum in Vancouver Island caves, North America (Canada). Subterranean Biology 29: 59-77. https://doi.org/10.3897/subtbiol.29.31467
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A new cave-dwelling dipluran of the North American endemic genus Haplocampa is described, coming from a couple of caves excavated in a small limestone karstic area near Port Alberni, Vancouver Island (British Columbia, Canada). To Haplocampa belong five soil-dwelling species. L. M. Ferguson cited no less than eight more species living in soil and cave habitats in several US states but without producing any formal descriptions. Haplocampa, in spite of its large lateral crests on the unequal claws, has clear taxonomical features as a Campodeinae and is closely related with the cave-dwelling Pacificampa and Eumesocampa genera, due to sharing similar macrosetae body distribution and absence or reduction of the lateral process. The new proposed species, Haplocampa wagnelli Sendra, sp. n., is rather interesting for its troglomorphic features: antennae with 32 antennomeres; olfactory chemoreceptors, each a multiperforated, folded-spiral structure; and numerous gouge sensilla. In addition, it is one of the northernmost troglomorphic species to have colonised – presumably recently – an area occupied by the Late Wisconsinian North America ice sheet during the Last Glacial Maximum. Furthermore, the close affinities between Haplocampa, Pacificampa (from caves in the extreme east of continental Asia and the southern Japanese Islands), Metriocampa (from the east of Asia and North America) and Eumesocampa (endemic to North America) suggest probable dispersal events over the Bering Land Bridge.
Haplocampa wagnelli , cave fauna, troglomorphic, biogeography, glaciation
Although subterranean diplurans were already known from North America since the 19th century (
Fauna collections were carried out in two sites of Fossli Slot #2 and one site from Kiku Pot (see below the description of caves). Sampling was focused on regions where visible signs of chewed-up organic matter could be seen. Collections were made manually using #00 brushes and kept in small vials with 90% ethanol. Once the specimens were spotted, they were dabbed with a brush moistened with ethanol and immediately placed into vials, labelled and sealed for transport.
The specimens were washed using distilled water and were put between slides and glass coverslips to be examined under a phase-contrast optical microscope (Leica DMLS) using Marc André II solution. The illustrations were made with a drawing tube and the measurements were taken with an ocular micrometre. For measuring the body length, the specimens were mounted ‘in toto’ and were measured from the base of the frontal process distal macrochaetae to the abdomen’s supra-anal valve. Two paratypes were coated with palladium-gold used for scanning electronic microscopic photography (Hitachi S-4100) and measurement of the sensilla.
The morphological descriptions and abbreviations used in this article follow
This species is dedicated to the co-author of this article, a caver who has dedicated many years sampling and exploring in Vancouver Island caves.
Female holotype labeled ♀01 from Kiku Pot Cave, Port Alberni, Vancouver Island, Canada, 5th August 2018, C. Wagnell leg. (SEHU); 1 ♂ labeled ♂01, paratypes from Fossli Slots Caves, Port Alberni, Vancouver Island, Canada and 4 females labeled ♀02–♀05 from Fossli Slots Caves, Vancouver Island Canada, 15th July 2018, C. Wagnell leg. All type material mounted in Marc André solution. Deposited in AS collection.
Four specimens from Fossli Slots Caves, 8th June 2018, C. Wagnell leg as type material mounted in separated aluminum stages and coated with palladium-gold. Deposited AS collection.
Body length 4.4 mm (male) and 3.4–6.0 mm (females). Epicuticle smooth under optical microscope but reticulated in high magnifications in round polygonal structures variable in size (Figs
Moliniform antennae. Every intact antenna in the six type specimens has 32 antennomeres; from 0.5 to 0.7 times longer than body in larger and smaller adults, respectively. First antennomere four times shorter than second antennomere, and apical antennomere 1.3 longer than wide (Fig.
Cupuliform organ occupying 1/3 of the total length of the apical antennomere with about five complex olfactory chemoreceptors, each one a multiperforated–folded spiral structure, all tightly packed in the narrow open space of the cupuliform organ (Figs
Head subtrapezoidal with slightly protuberant lateral posterior angles (Fig.
Thoracic macrosetae distribution (Fig.
Haplocampa wagnelli Sendra, sp. n., length of the body, antennae and metathoracic leg including their segments, the cerci (units in mm), and the number of antennomeres.
Specimen | Body length | Antennomeres | Antennae length | Segment length of a metathoracic leg | Total metathoracic length | |||||
---|---|---|---|---|---|---|---|---|---|---|
Coxa | Trochanter | Femur | Tibia | Tarsus | Pretarsus | |||||
Paratype, ♀04 | 3.40 | 32 | 2.50 | 0.21 | 0.18 | 0.45 | 0.41 | 0.27 | 0.10 | 1.62 |
Paratype, ♀05 | 3.75 | 32 | 2.35 | 0.20 | 0.12 | 0.43 | 0.40 | 0.28 | 0.85 | 1.47 |
Paratype, ♂01 | 4.40 | 32 | 2.52 | 0.21 | 0.12 | 0.48 | 0.46 | 0.28 | 0.10 | 1.65 |
Paratype, ♀02 | 4.90 | 32 | 2.65 | 0.22 | 0.18 | 0.51 | 0.48 | 0.29 | 0.11 | 1.78 |
Paratype, ♀03 | 5.05 | 32 | 3.05 | 0.25 | 0.22 | 0.60 | 0.55 | 0.35 | 0.10 | 2.07 |
Holotype, ♀01 | 6.02 | 32 | 3.20 | 0.21 | 0.17 | 048 | 0.46 | 0.28 | 0.11 | 2.15 |
Distribution of abdominal macrosetae on urotergites (Fig.
Urosternite I with 6+6 macrosetae (Figs
Haplocampa wagnelli Sendra, sp. n., length of cercal articles and total length (units in mm) including number of articles of each cercus.
Specimen, body length | Cerci, Articles length | |||||||
---|---|---|---|---|---|---|---|---|
Base (secondary article) | 1st | 2nd | 3rd | 4th | 5th | 6th | Total length | |
Paratype ♀04, 3.40 mm | 0.78 (7) | 0.22 | 0.25 | 0.28 | 0.36 | 0.38 | - | 2.26 |
Paratype ♀05, 3.75 mm | 0.70 (8) | 0.22 | 0.30 | 0.38 | 0.40 | 0.42 | - | 2.42 |
Paratype ♂01, 4.4 mm | 0.35 (3) | 0.18 | 0.25 | 0.28 | 0.30 | 0.40 | 0.42 | 2.18 |
Paratype ♀02, 4.9 mm | 0.62 (4) | 0.21 | 0.24 | 0.26 | 0.31 | 0.39 | 0.44 | 2.48 |
Paratype ♀03, 5.05 | 0.92 (7) | 0.25 | 0.28 | 0.30 | 0.32 | 0.38 | 0.35 | 2.70 |
Holotype ♀01, 6.02 mm | 0.88 (6) | 0.25 | 0.30 | 0.32 | 0.35 | 0.38 | 0.38 | 2.85 |
Female urosternite I with short subcylindrical appendages, each bearing up to 30 a1-glandular setae in a distal field (Fig.
Male urosternite I with short moderately thick subcylindrical appendages, each bearing about 50 a1-glandular setae in a large field; up to setae covered the with two to three rows the posterior part of the first urosternite (Fig.
29 Map of Fossli Slots caves with spots where Haplocampa wagnelli sp. n. was seen 30 entrance of Fossli Slot #2 cave 31 Kiku Pot cave with spots where Haplocampa wagnelli sp. n. was seen 32 entrance of Kiku Pot cave with Felix Ossigi-Bonanno and Craig Wagnell after the success finding 33 entrance of Kiku Pot cave viewed from inside the cave.
The most visible features are the slightly troglomorphic characteristics of H. wagnelli sp. n., as shown by its antennae with 32 antennomeres, a record within the genus Haplocampa but a moderate antennomere number in a troglomorphic campodeid; and the five complex olfactory chemoreceptors, each one a multiperforated, folded-spiral structure However, any comparison with other Haplocampa species is currently impossible since these sensilla have not been described in any other species of the genus. The closest species to H. wagnelli sp. n. is H. rugglesi from Mount Rainier (Washington, USA), with equal macrosetae distribution on nota and similar on urotergites. Nevertheless, some taxonomic features are unique to H. wagnelli sp. n., such as medial anterior macrosetae on urotergites and three tibial ventral macrosetae. Many taxonomical details remain incomparable what is known described species, due to the lack of high magnifications.
Antennae with moniliform antennomeres and short cerci with a few primary articles. Subtrapezoidal head slightly enlarged in the posterior lateral side. Medial anterior (1+1), lateral anterior (1+1) and lateral posterior (1+1) macrosetae on pronotum; medial anterior (1+1), lateral anterior (1+1) and lateral posterior (2+2) on mesonotum; and medial anterior (1+1) and lateral posterior (1+1-2+2) on metanotum. Dorso-femoral macrosetae one. One to three tibial-ventral macrosetae. Tarsus short and enlarged. Unequal claws with large lateral crests and no lateral process; basal portion of both claws with a visible spiny protrusion; posterior claw with a large backward overhang. Medial anterior or medial posterior urotergal macrosetae present; with or without lateral anterior urotergal macrosetae; and, lateral posterior urotergal macrosetae 0, 1 (lp2) or 2 (lp2,3) on urotergites V to VII. Urosternite I with 6+6 macrosetae; urosternites II to VII with 4+4 macrosetae; urosternite VIII with 1+1. Plain stylus with smooth or a few tiny barbs on stylus setae. Male with glandular a1 and g1-setae. Female with glandular a1-setae.
1 | Lateral posterior macrosetae 2+2 on metanotum; without lateral anterior macrosetae on urotergites; antennae with 24–26 antennomeres | Haplocampa drakei |
– | Lateral posterior macrosetae 1+1 on metanotum; with lateral anterior macrosetae 1+1 on urotergites | 2 |
2 | Without posterior macrosetae on first and second urotergites; antennae with 20 antennomeres | Haplocampa chapmani |
– | Medial anterior or medial posterior macrosetae 1+1 on first and second urotergites | 3 |
3 | Medial posterior macrosetae 1+1 on first and second urotergites; two tibial ventral macrosetae | Haplocampa cf. chapmani |
– | Medial anterior macrosetae 1+1 on first and second urotergite | 4 |
4 | Medial anterior macrosetae 1+1 on third to seventh urotergites; two or three tibial ventral macrosetae; antennae with 32 antennomeres | Haplocampa wagnelli sp. n. |
– | Medial anterior macrosetae only on first urotergites; one tibial ventral macrosetae; antennae up to 21 antennomeres | 5 |
5 | Lateral posterior macrosetae 1+1 on third urotergite; antennae with 19–21 antennomeres | Haplocampa wheeleri |
– | Without lateral posterior macrosetae on third urotergite; antennae with 21 antennomeres | Haplocampa rugglesi |
The caves are all located near the town of Port Alberni, Vancouver Island, British Columbia, Canada (Figs
Fossli #1 (L63.5 D25): swallet entrance with active surface stream. First sightings of H. wagnelli sp. n. on 5th April 2005.
Fossli #2 (L67.5 D26.5): small slot entrance filled with rotten wood. Upper samples collected 15th July 2018, 30 m from the entrance in a moist bed of sandy organic debris. Lower samples collected 6th August 2018, 60 m from the entrance in a moist bed of sandy organic debris 2 m above sump. H. wagnelli sp. n. mud workings visible at both sites.
Kiku Pot cave, (L1489 D92): Breakdown entrance with active stream passage throughout system. H. wagnelli sp. n. first sightings August 2017 while surveying. Collection taken 5th August 2018, at bottom waterfall just below where water disappears approximately 150 m from the entrance on a medium. A medium sized bed of sandy organic material with scattered woody debris. H. wagnelli sp. n. workings were visible over 75%. Area floods during high water. Many mud workings visible on muddy shelves higher in passage. At the time of collection, an adult fungus gnat was noticed hopping around.
Vancouver Island is known to have over 1600 caves, with more mapped and explored caves than the rest of Canada combined. Some caves reach over 10 km, and some host unique geological, palaeontological, archaeological and biological features. Vancouver Island caves are mostly active caves, with streams and rivers running through them most of the year. The caves help the streams to maintain constant water temperatures year round and a proper pH, which increases water quality for fish and wildlife. So far, little has been done to protect the caves from poor logging, mining and recreational practices. All caves west of the Port Alberni area are easily accessed by the public and none so far have protection or proper management. Unfortunately, some already have seen misuse. More needs to be done in the future if we want to protect this special resource.
In Haplocampa species, their unequal claws have large lateral crests, as do many genera of Plusiocampinae. Applying the right criteria,
In all likelihood, Pacificampa Chevrizov, 1978 is the most closely related to Haplocampa, given the strong similarities in the number and distribution of the macrosetae body and the absence of lateral pretarsus processes, with one important difference: the lack of lateral crests in Pacificampa (
Haplocampa and Pacificampa share ecological similarities, and phylogenetic, too. Both are present in subterranean ecosystems. In the case of Pacificampa, all of the five known species have been found in caves and can be considered troglobites. Three of these species can be found in the north of the Korean Peninsula (
H. wagnelli sp. n. is a slight troglomorphic species and several features show this. Among these features are the very slight elongation of antennae, 0.5× to 0.7× the body length, with moniliform antennomeres, and the cerci 0.5× to 0.6× the body length. In troglomorphic campodeids, the length of antennae can double that of the body, with always more than 30 antennomeres, and the cerci can be two or three times the body length; there is also an increase in the number of the cercal articles. Furthermore, troglobitic campodeids have elongated legs, reaching the end of the abdomen and a slim body. All of these features are trademarks of highly adapted subterranean campodeid species (
H. wagnelli sp. n. may represent one of the most northerly cave-dwelling adapted dipluran species being found at 49° latitude north. The most northerly cave-dwelling species is Litocampa hubarti Bareth, 1999, found in Grotte Lyell (Liège, Belgium) at 50° latitude north, and like H. wagnelli sp. n., it shows humble morphological subterranean-adapted features (
Many thanks from Craig to his cave associates: Tawney Lem and Felix Ossigi-Bonanno for the many hours of patiently sitting in the dark with little guarantee of even having a chance of seeing some of the cave animals. We are also indebted to the electron microscopy facility at the Universitat de València, especially to 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 many times Katie Marsen for helping us translate this paper. Finally, but not less important, we are very grateful to both reviewers Loris Galli (Università degli Studi di Genova) and Pedro Oromí (Universidad La Laguna) for their accurate corrections and suggestions the article. And finally, and no less importantly, our acknowledgment to Lynn Ferguson the American biologist who has discovered many of the vast diversity of Haplocampa species and many other dipluran taxa in North America.
A video shot by Felix Ossig-Bonanno (2017) from Fossli Slots Caves
Data type: multimedia