Research Article |
Corresponding author: Luis Espinasa ( luis.espinasa@marist.edu ) Academic editor: Oana Teodora Moldovan
© 2015 Luis Espinasa, Radha Garvey, Jordi Espinasa, Christina A. Fratto, Steven Taylor, Theofilos Toulkeridis, Aaron Addison.
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:
Espinasa L, Garvey R, Espinasa J, Fratto CA, Taylor SJ, Toulkeridis T, Addison A (2015) Cave dwelling Onychophora from a Lava Tube in the Galapagos. Subterranean Biology 15: 1-10. https://doi.org/10.3897/subtbiol.15.8468
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A new population of velvet worms (Onychophora) inhabiting a lava tube cave in the island of Santa Cruz, Galapagos, is reported here. The population size is large, suggesting that they may be troglophilic. Its members are darkly pigmented, with no obvious troglomorphic features. Their 16S rRNA sequence showed no differences when compared to an unidentified species of surface velvet worm from the same island, thus supporting cave and surface populations belong to the same species. Based on the 16S rRNA data, the Galapagos velvet worms derived from an Ecuadorian/Colombian clade, as would be expected of ease of dispersal from the nearest mainland to the Galapagos Islands.
Onychophora , Velvet worms, Galapagos, Santa Cruz, Lava tube, Troglophile, Troglobite, 16S rRNA
The Onychophora, or velvet worms, are considered “living fossils” and among the most interesting groups of animals for evolutionary biologists. Fossils dating back to 540 million years show an overall anatomy which has remained largely unchanged. Extant taxa resemble early Cambrian lobopodians, such as Aysheaia pedunculata (Walcott, 1911) from the Burgess Shale formation in Canada (
Two velvet worm species, the first a Peripatopsid, Peripatopsis capensis (Grube, 1866), and the second a Peripatid, not identified to species but labeled as Oroperipatus sp. (
In the volcanic islands of the Galapagos there are numerous lava tubes. Lava tubes form when a top layer of flowing lava cools while the molten lava beneath the surface continues to flow. As the flow subsides, the lava will empty out forming a lava tube. While a variety of organisms inhabit Galapagos lava tube caves, relatively few are considered to be troglobitic (
The velvet worms are terrestrial and prefer dark environments with high air humidity. They are found particularly in the rainforests of the tropics and temperate zones where they live among moss cushions, leaf litter, under tree trunks and stones, in rotting wood, in termite tunnels or in crevices in the soil into which they can withdraw during the day (
During road work on the main highway near Puerto Ayora, the main town on the Galapagos island of Santa Cruz, the roof of a lava tube collapsed uncovering a large cave. During mapping and exploration of the cave, several velvet worms were discovered. The purpose of this paper is to document this unique population and establish how this cave population is related to other surface Onycophora through 16S rRNA sequencing.
A Location of the Galapagos Islands B Archipelago of the Galapagos. Samples collected were from the island of Santa Cruz C Yellow pins indicate the surface locality and Kübler cave where samples were collected D In blue, overlaid contour of the map of Kübler cave. Notice that the cave is within the city limits of Puerto Ayora.
This study is part of a larger project focused on cave mapping, geological investigations and cataloging biological resources of lava tube caves in the Galapagos (
Collecting and exportation permit #094-2014DPNG for project PC-64-14 to Dr. Theofilos Toulkerdis was provided by Dirección del Parque Nacional Galapagos and Ministerio del Ambiente, Ecuador. Genomic DNA samples were obtained following standard methods for DNA purification using Qiagen’s DNeasy® Tissue Kit, by digesting one lobopod leg of the individual in the lysis buffer. Markers were amplified and sequenced as a single fragment using the 16Sar and 16Sb primer pair for 16S rRNA (
Kübler Cave (El Mirador) has a horizontal length of 914 m and a depth of 70 m. It extends beneath land currently being developed for human habitation at the outer edge of Puerto Ayora (Fig.
When the DNA of the six cave specimens and two surface specimens was sequenced, their 16S rRNA was found to be identical (GenBank # KM102162 and KM102163). The fragment sequence was 455 bp long. When a BLAST analysis was performed, Epiperipatus sp. (KC754524) from Colombia appeared to be the most similar, differing by 62 bp (13.6%), followed by two specimens of an unidentified genus of Peripatidae (KC754526 and KC754520) from mainland Ecuador, from which they differed by 68 bp (14.9%) and 77 bp (16.9%) respectively. Our sequences were also compared against velvet worm species akin to that previously reported for the Galapagos Islands. Two specimens not identified to species but labeled as Oroperipatus sp. (NC015890.1 and JF800076.1) have been sequenced for their 16S rRNA. The Galapagos specimens differed from them by 83 bp (18.2%). Finally, when compared against Peripatopsis capensis (KC754566), they differed by 113 bp (24.8%).
Within the lava tube food web, cave velvet worms appear to be successful predators. This cave specimen was observed apparently feeding on a pill bug (Isopoda: Oniscoidea: Armadillidae). The cave population of the onlychophoran is thought to be large, estimated in at least the hundreds. (Photo by Rickard S. Toomey III).
A population of velvet worms (Onychophora) has been found in a lava tube cave on the island of Santa Cruz, in the Galapagos Archipelago. The American Peripatids are roughly divided into two groups which diverged over 145 million years ago in the Mid-Jurassic; a clade with Ecuadorian and Colombian species and a clade centered mainly in and around the Caribbean (
The cave specimens’ 16S rRNA are identical to that of surface velvet worms collected from the same island, strongly suggesting that both cave and surface populations belong to the same species. Despite cave specimens being darkly pigmented and having no obvious troglomorphic features, the observation of twelve individuals comprising both juveniles and adults, indicated that the population in Kübler Cave (El Mirador) is large. Only a small proportion of the cave could be scanned, especially because in volcanic terrains there are innumerable crevices and rocks where individuals could hide. It is likely that the population is at least in the hundreds, but this is only a rough estimate. Furthermore, specimens appeared to be as healthy and mobile as their surface counterparts. Velvet worms, with their propensity to live in dark habitats, are exaptated to colonize the lava cave habitat and evolutionarily co-opted to become successful troglophiles and troglobites, as reported by
While we have determined that both cave and surface velvet worms collected for this study most likely belong to the same species, some questions still remain: To which species does the Santa Cruz island Onychophora belong? There are two velvet worms reported as occurring on the Galapagos Islands, Oroperipatus sp. and Peripatopsis capensis. The latter species, the Cape velvet worm, is a habitat specialist peripatopsid characterized as having a low dispersal capability and sensitivity to dehydration, restricted to the Cape Peninsula in South Africa (
Our Galapagos specimens also showed significant difference (83 bp; 18.2%) from the specimens available in GenBank of genus Oroperipatus. Instead, they showed the least difference (62 bp; 13.6%) with a member of genus Epiperipatus from Colombia and with specimens of an unidentified genus of Peripatidae from Ecuador (68 bp; 14.9%). This information could be interpreted as our specimens belonging to a different genus from the velvet worms previously reported for the Galapagos. However, cladistic analysis of the Onychophora shows that the American genera are oftentimes paraphyletic (
Another possibility is that
Partial support for the project came from two National Speleological Society grants; the Education and the Conservation grants. The Subterranean Ecology Institute provided additional support for fieldwork. Travel expenses for LE were supported by a VPAA grant from Marist College. Further financial and logistic support was given by ESPE project # 2014-PIT-012. Research and exportation of samples permit was given by the Galapagos National Park (PC-64-14 and 094-2014 DPNG). G. McDaid, R. Toomey, G. Hoese and B. Osburn helped exploring, mapping and/or collecting the specimens. We also thank the two anonymous reviewers for their suggestions.