Research Article |
Corresponding author: Luis Espinasa ( luis.espinasa@marist.edu ) Academic editor: Oana Teodora Moldovan
© 2014 Luis Espinasa, Monika Espinasa, Dante B. Fenolio, Michael E. Slay, Matthew Niemiller.
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, Espinasa M, Fenolio D, Slay M, Niemiller M (2014) Distribution and conservation status of Speleonycta ozarkensis (Insecta, Zygentoma, Nicoletiidae) from caves of the Ozark Highlands of Arkansas and Oklahoma, USA. Subterranean Biology 14: 51-62. https://doi.org/10.3897/subtbiol.14.8275
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The “thysanuran” (Zygentoma: Nicoletiidae) Speleonycta ozarkensis is the only troglobiotic nicoletiid from the Ozark Highlands. It was originally described with only four specimens from four different cave systems in Arkansas and Oklahoma. The scarcity of available specimens has made it difficult to determine whether morphological variation among populations represents intraspecific or interspecific variation. We examined molecular (16S rRNA) variation among populations and found no evidence that they represent a species complex. Because of its limited distribution and lack of ecological and life history data, S. ozarkensis may be a species of conservation concern. We therefore conducted a conservation status assessment. We bioinventoried 44 caves in Arkansas and Oklahoma to determine the distribution of S. ozarkensis. A new locality in Adair Co., Oklahoma, was discovered and new specimens were collected to better assess morphological variation among populations. Data on ecology and life history was gathered. We determined the conservation status of the species and identified potential threats to existing populations. Despite being known from a few localities, S. ozarkensis has a broad distribution approaching 10,000 km2. Molecular data suggest S. ozarkensis is capable of considerable dispersal and is primarily an epikarstic species, perhaps explaining why it has been infrequently collected from caves. Conservation assessments revealed that S. ozarkensis is at a slight risk of extinction. We identified seven threats impacting populations that vary in scope and severity, but only recreational caving (three caves) and development associated with urbanization (one cave) have the greatest potential to immediately impact populations.
Zygentoma , Thysanura , Cubacubaninae , Speleonycta ozarkensis , Ozarks, troglobite, cave, 16S rRNA
A new genus and species of troglobiotic nicoletiid (“thysanurans”, bristletails or silverfish), Speleonycta ozarkensis
Known localities and specimens of Speleonycta ozarkensis in the Ozark Highlands of Arkansas and Oklahoma.
Locality No. | Cave | County | State | Ownership /Management | No. Specimens |
---|---|---|---|---|---|
1 | Bear Hollow Cave | Benton | AR | The Nature Conservancy | 1 |
2 | Chambers Hollow Cave | Benton | AR | U.S. Forest Service | 1 |
3 | Tweet’s Cave | Newton | AR | Private | 1 |
4 | Wolf Creek Cave | Newton | AR | U.S. Forest Service | 1 |
5 | Wady Cave (AD85) | Adair | OK | Private | 3 |
6 |
Single Barrel Cave | Cherokee | OK | Private | 1 |
7 | Black Hollow Cave | Delaware | OK | State of Oklahoma | 1 |
8 | McGee’s Cave | Delaware | OK | The Nature Conservancy | 1 |
Despite several collecting trips, these caves only yielded a single specimen of S. ozarkensis from each locality (
Because of the species’ limited distribution and lack of information on ecology and life history, S. ozarkensis may be a species of conservation concern. However, the conservation status of this nicoletiid has not yet been assessed under NatureServe and IUCN Red List criteria, because of the recency of its description. In addition, genetic information (16S rRNA gene) is only available for a single specimen collected from Chambers Hollow (=Uno) Cave, Benton Co., Arkansas. The objectives of the present study were to: (1) determine the distribution of S. ozarkensis within the Ozark Highlands of northwestern Arkansas and northeastern Oklahoma; (2) compare newly collected specimens to better assess morphological variation among populations; (3) generate novel DNA sequences for new populations; (4) collect information on ecology and life history, such as microhabitat within caves; and (5) determine the conservation status of S. ozarkensis and identify potential threats to existing and newly discovered populations.
Cave surveys. We surveyed 44 caves in northwestern Arkansas and northeastern Oklahoma within the suspected range of S. ozarkensis between January 2010 and May 2014. Sampling effort varied among caves due to variation in cave length and amount of available habitat. Nonetheless, visual encounter surveys (VESs) were conducted by a minimum of two observers for at least two person-hours in all caves and consisted of visually searching terrestrial habitat (cave floor, cave walls, and underneath rocks and other debris) in human-accessible passages. Specimens encountered were collected by hand and deposited into 95% ethanol for preservation. Any rocks, logs and other debris were returned to their original positions to minimize habitat disturbance.
Morphological analysis. Observations of body parts were made with a Motic K series stereo microscope. Specimens in ethanol were observed directly in petri dishes so as to preserve the integrity of the specimens.
Molecular methods. Genomic DNA from two specimens was extracted using Qiagen’s DNEasy® Tissue Kit by digesting a leg in lysis buffer. PCR amplification and sequencing of a 501 bp portion of the 16S rRNA mitochondrial gene followed standard protocols and primers used previously for nicoletiids (
Conservation assessments. We conducted conservation assessments under both NatureServe and IUCN Red List criteria. NatureServe’s system of assessing conservation status uses ten primary factors grouped into three main categories: rarity, trends, and threats (
Both NatureServe and IUCN Red List assessments use two different measurements of geographic range size: extent of occurrence (EOO; referred to as range extent by NatureServe) and area of occupancy (AOO). We calculated EOO and AOO using the web-based program GeoCAT (
A species may be classified as critically endangered (CR), endangered (EN), or vulnerable (VU) on the IUCN Red List if it meets specific conditions under any one of these five criteria (
Since 2010, we surveyed 14 caves in northwestern Arkansas, including 5 in Benton, 7 in Carroll, one in Newton, and one in Washington counties, and 30 caves in northeastern Oklahoma, including five in Adair, one in Sequoyah, and 24 in Delaware counties. Apart from the seven caves where nicoletiids had previously been reported, at only a new single locality were nicoletiids found. Three nicoletiids were observed at a cave (AD85) in Adair County, Oklahoma, on 18 November 2012 (Fig.
The two specimens collected were adult males measuring 7.3 and 8 mm in body length and were identified as S. ozarkensis. Despite considerably smaller than the two males used to described the species by
The 16S rRNA sequences of both specimens collected from AD85 were identical. Moreover, the sequences were also identical to the 16S rRNA sequence from the S. ozarkensis specimen previously collected from Chambers Hollow (=Uno) Cave, Benton Co., Arkansas (GenBank no. KJ128288).
Conservation assessment.Speleonycta ozarkensis has an EOO of 9,833.69 km2 and an AOO of just 32 km2 in the Ozark Highlands of northeast Oklahoma and northwest Arkansas (Fig.
We identified seven threats documented or suspected to impact populations of S. ozarkensis at the present or in the future, including residential and commercial development, agriculture (livestock farming and ranching), energy production and mining, amateur and scientific collecting, recreational caving, dams and water management, and pollution. These threats vary in scope (negligible to restricted), severity (negligible to serious) and overall impact (negligible to low) among populations. The most significant threats include recreational caving at localities with unrestricted access and the potential for urbanization within the recharge zone of Bear Hollow Cave in Benton Co., Arkansas. Of the eight known occurrences of S. ozarkensis, the main entrances of at least five caves occur on public lands or are managed for their cave and karst resources. Two caves are located on U.S. Forest Service land in Arkansas and are gated or have restricted access due to the presence of endangered bats (Chambers Hollow and Wolf Creek caves). One cave is located on public land owned by the state of Oklahoma (Black Hollow Cave). Additionally, two caves are owned by The Nature Conservancy and are gated (Bear Hollow and McGee’s caves). Scientific and amateur collections are believed to have had a very minimal affect on any single population, as only six specimens have been collected to date. We assigned an overall threat impact of “Medium” based on a NatureServe conservation threat assessment.
We assigned a NatureServe conservation global rank of G3 (Vulnerable) to S. ozarkensis and state ranks of S2 (Imperiled) and S1S2 (Critically Imperiled to Imperiled) for Arkansas and Oklahoma populations, respectively. We classified S. ozarkensis as “Near Threatened” under the IUCN Red List classification. While S. ozarkensis classifies as “Vulnerable” under Criterion 1a (EOO < 20,000 km2 and severely fragmented range or known to exist at no more than 10 locations), there is insufficient evidence at the present time to infer if a continual observed or projected decline (Criterion 1b) and/or extreme fluctuations (Criterion 1c) in EOO, AOO, extent or quality of habitat, number of populations or number of mature individuals exists.
Few nicolettid are known from caves in the US despite the family being common in neotropical caves (
Despite only being collected from eight caves in five counties, S. ozarkensis apparently has a broad distribution approaching 10,000 km2 and includes three ecoregions (Dissected Springfield Plateau, Lower Boston Mountains and Upper Boston Mountains). Ecoregions are defined by general similarity of surface ecosystems, including similarity in both biotic and abiotic characteristics (such as geology, physiography and hydrology that are important constraints in cave development). While previous studies have shown that ecoregions often delimit range boundaries for many subterranean organisms (
More important, molecular data indicate that this species may not be comprised of significant fragmented and isolated populations as distributional data might otherwise suggest. DNA sequences of the 16S rRNA gene were identical between specimens from Chambers Hollow Cave in Benton Co., Arkansas, and AD85 Cave in Adair Co., Oklahoma. These two caves are separated by 48.8 km (straight-line distance). Within the subfamily Cubacubaninae, intrapopulation variation averages 1.7 nucleotide differences (range 0–7; n = 29) while interpopulation variation averages 3.4 nucleotide differences (range 0–13; n = 22) within species at the 16S rRNA locus (
A broad distribution despite few known localities has obvious implications with regards to conservation and management of S. ozarkensis. Our conservation status ranks, G3 (Vulnerable) for NatureServe and “Near Threatened” for IUCN Red List, reflect a broad distribution as well as a medium threat impact. While only known from eight cave systems, five S. ozarkensis populations are afforded some protection. Four caves are gated and one occurs on public land and is managed for its biological and other resources. Restricted access limits potential negative impacts to the populations from recreational caving. The three other localities occur on private lands and may be at a greater risk from recreational caving. The population at Bear Hollow Cave in Benton Co., Arkansas, faces the greatest risk of impacts associated with urbanization. Although the risk is currently low, we recommend that residential and commercial development within the recharge zone and the potential impacts to cave life within this cave system be monitored over the next 10 years. In addition, another recommendation is to resurvey and monitor known localities while also searching for additional cave systems that may harbor S. ozarkensis. The establishment of long-term monitoring programs is needed to provide data on population sizes and threats to individual populations over time. Additional surveys are also warranted to document new localities but also assess whether the distribution of S. ozarkensis is greater than currently known. The species likely also occurs within cave systems and epikarst of the Ozark Highlands of southwestern Missouri.
The two specimens collected from AD85 Cave in Adair Co., Oklahoma, have increased our understanding of the postembryonic development of the S. ozarkensis. A typical adult morphology and presumably sexual maturity has been attained by 7.3 mm, indicating that S. ozarkensis reaches sexual maturity at a length comparable to troglobiotic nicoletiids in the sister genus Texoreddellia (
When Speleonycta ozarkensis was originally described (
An interesting final observation is that the specimens from AD85 in Adair Co., Oklahoma, are host to parasitic mites (Acari; Fig.
Speleonycta ozarkensis is the only described troglobiotic thysanuran from the Ozark Highlands. New biological inventories since 2010 in Arkansas and Oklahoma yielded only one new locality, AD85 in Adair Co., Oklahoma, bringing the total number of occurrences to eight caves in five counties. Despite being known from a few localities, S. ozarkensis has a broad distribution approaching 10,000 km2. In addition, molecular evidence suggests that S. ozarkensis is capable of considerable dispersal and may be primarily an epikarstic species, perhaps explaining why it has been infrequently collected from caves. Our conservation assessments showed that S. ozarkensis is at a slight risk of extinction. We identified seven threats impacting populations that vary in scope and severity, although only recreational caving (three caves) and development associated with urbanization (one cave) have the greatest potential to impact populations in the short term.
We would like to thank Daphne Soares and Gary O. Graening for helping collect the specimens and for providing data. DNA sequencing was performed by students of the BIOL320-112: Genetics Spring 2013 course of at Marist College, with the support of the School of Science. Partial funding for this project was provided by Arkansas Game and Fish Commission, The Nature Conservancy, and United States Fish and Wildlife Service. Ongoing funding in Oklahoma has been provided by the Oklahoma Department of Wildlife Conservation via a state wildlife grant (E-22).