Short Communication |
Corresponding author: Matthew L. Niemiller ( cavemander17@gmail.com ) Academic editor: Oana Teodora Moldovan
© 2019 Matthew L. Niemiller, Thomas Inebnit, Amata Hinkle, Bradley D. Jones, Mark Jones, Joseph Lamb, Nathaniel Mann, Benjamin Miller, Jennifer Pinkley, Stephen Pitts, Kayla N. Sapkota, Michael E. Slay.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Niemiller ML, Inebnit T, Hinkle A, Jones BD, Jones M, Lamb J, Mann N, Miller B, Pinkley J, Pitts S, Sapkota KN, Slay ME (2019) Discovery of a new population of the federally endangered Alabama Cave Shrimp, Palaemonias alabamae Smalley, 1961, in northern Alabama. Subterranean Biology 32: 43-59. https://doi.org/10.3897/subtbiol.32.38280
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The Alabama Cave Shrimp Palaemonias alabamae Smalley, 1961 is a federally endangered cave shrimp endemic to just four cave systems within and near the greater Huntsville metropolitan area in Madison County, Alabama USA. It is one of two described atyid cave shrimp in the Interior Low Plateau karst region. Here we report the discovery of a new population of P. alabamae from the Fern Cave system in western Jackson County, Alabama. We observed four cave shrimp in August 2018 in an isolated pool in the base-level stream passage of the longest cave system in Alabama. Two cave shrimp were observed during a subsequent survey in July 2019: one in the same isolated pool and a second shrimp in a pool in the main stream passage. Morphological and genetic analyses confirm that this population is closely allied with other populations in Madison County. This new population expands the known distribution of the species into a new county and watershed (Lower Paint Rock River). The potential exists to discover additional populations in Paint Rock River valley and other nearby regions.
Atyidae, conservation, crustacean, Decapoda, distribution, range extension
In the United States, over 1,350 troglobionts and stygobionts (i.e., terrestrial and aquatic cave-obligate species) have been described, and many additional taxa await formal description (
Most cave systems have not been adequately surveyed or studied, and many regions have been grossly underrepresented. For example, less than 7% of caves in Tennessee, the most cave-rich state in United States, have been surveyed for biological resources and even fewer have been repeatedly and comprehensively bioinventoried (
The Alabama Cave Shrimp, Palaemonias alabamae Smalley, 1961, is a stygobitic atyid shrimp endemic to just four cave systems (six caves) in and around the greater Huntsville area in Madison County, Alabama, USA (Figure
Palaemonias alabamae was first discovered at Shelta Cave (Alabama Cave Survey no. AMD4) in northwestern Huntsville, Madison County, Alabama by Thomas Poulson in 1958 and described by
Here, we report on the discovery of a population of P. alabamae from the Fern Cave system (AJK597) located in the Paint Rock River watershed in western Jackson County, Alabama. This discovery represents the first new locality for this federally endangered cave shrimp in 14 years and just the fifth population discovered to date, extending the geographic range of P. alabamae into a new hydrological basin. In addition, this new discovery suggests that this endangered species may be found in other cave systems in the Paint Rock watershed and perhaps further east along the Tennessee River.
The Fern Cave system is located along the eastern edge of the Paint Rock River Valley on Nat Mountain in western Jackson County between the cities of Huntsville and Scottsboro. It is the largest cave system in Alabama with over 25 km of passages developed primarily in the Mississippian-aged Bangor and Monteagle Limestone formations (
As part of a two-year study implemented by the Inventory & Monitoring Branch of the U.S. Fish & Wildlife Service to biologically inventory the Fern Cave system comprehensively, four of us (MLN, BJ, JL, and NM) on 25 August 2018 entered the Davidson Entrance (aka Sump Entrance) located at the base of Nat Mountain at an elevation of ca. 187.5 m (615 ft). The Davidson Entrance directly accesses the “Bottom Cave” section of the Fern Cave system. For much of the year, this section of the cave is inaccessible or only accessible via cave diving due to high water levels. During our visit, water levels were low enough to permit entry through a low airspace swim and crawl for ca. 40 m leading to the main stream passage that can be traversed for several hundred meters to a sump. We searched aquatic habitats using time-constrained visual surveys with headlamps and recorded all fauna observed. A cave shrimp was captured using a handheld dipnet in a shallow, isolated pool in the hands-and-knees crawl between the low-airspace pool near the entrance and the main stream passage. The retained specimen was photographed and then preserved in 100% ethanol for morphological and genetic analyses. We returned the following summer and conducted a second survey on 13 July 2019.
We extracted genomic DNA from three pleopods using the Qiagen DNEasy Blood & Tissue Extraction Kit following the manufacturer’s protocol. A 539-bp fragment of the mitochondrial 16S ribosomal DNA locus was amplified via PCR using primers 16Sar and 16Sbr (
Forward and reverse sequences were trimmed at the ends based on quality and assembled into contigs in ChromasPro v2.1.8 (Technelysium Pty Ltd, South Brisbane, Australia) then aligned using MUSCLE (
We calculated two measures of geographic range size for P. alabamae in the web-based program GeoCAT (
After wading and swimming through the low-airspace pool and passage near the Davidson entrance of the Fern Cave system for ca. 40m on 25 August 2018, we climbed onto a mudbank in a passage that leads to the main cave stream. We searched an isolated pool measuring ca. 5 m long, 2 m at its widest point, and water depth up to 25 cm, with mud/silt substrate and a few larger rocks. We encountered a substantial diversity of life in this pool, including a large cave shrimp (Palaemonias sp.). The shrimp was observed at the edge of the pool in 4 cm of water. This cave shrimp was captured and retained as a voucher by recommendation of USFWS personnel to confirm species identification (Figure
Two cave shrimp were observed during a return trip the following summer on 13 July 2019. One shrimp was observed in the same isolated pool, which was slightly larger in surface area (ca. 6 m long and 2.5 m wide) due to higher water levels. A second shrimp was observed in a quiet pool ca. 0.4 m in depth with silt/sand substrate and scattered cobble in the cave stream. This pool is just downstream of the junction of the passage with the previously referenced isolated pool and the main cave stream.
We identified the specimen from Fern Cave morphologically as Palaemonias alabamae by the presence of degenerate eyes, lack of pigmentation, and a long rostrum with eight dorsal and one ventral spine. In the original description of P. alabamae by
Palaemonias alabamae co-occurs with several other species at Fern Cave, including Southern Cave Crayfish Orconectes australis Rhoades, 1941, Caecidotea bicrenata (Steeves, 1963), Southern Cavefish Typhlichthys subterraneus Girard, 1859, Cavespring Crayfish Cambarus tenebrosus Hay, 1902, and Banded Sculpin Cottus carolinae Gill, 1861. Typhlichthys subterraneus is thought to be a significant predator of P. alabamae (
At the time of federal listing in 1988, P. alabamae was known from two cave systems in Madison County (
Confirmed occurrences of Palaemonias alabamae in Madison and Jackson counties, Alabama.
Cave | ACS no. | County | Geological formation | Watershed | First observed | Last observed |
---|---|---|---|---|---|---|
Shelta Cave | AMD4a | Madison | Tuscumbia Limestone and Fort Payne Chert undifferentiated | Indian Creek | 1958 | 1973 |
Bobcat Cave | AMD1283 | Madison | Tuscumbia Limestone | Indian Creek | 1973 | 2019 |
Hering Cave | AMD6b | Madison | Monteagle Limestone | Lower Flint River | 1991 | 2018 |
Glover Cave | AMD54b | Madison | Monteagle Limestone | Lower Flint River | 1991 | 1998 |
Brazelton Cave | AMD337b | Madison | Monteagle Limestone | Lower Flint River | 1991 | 1998 |
Muddy Cave | AMD1095 | Madison | Tuscumbia Limestone | Tennessee River-Wheeler Lake | 2005 | 2012 |
Fern Cave | AJK597 | Jackson | Monteagle Limestone | Lower Paint Rock | 2018 | 2019 |
Our discovery at Fern Cave extends the distribution of P. alabamae into the Lower Paint Rock River watershed (USGS HUC10 0603000202) and into western Jackson County, 9.7 km to the northeast of the nearest population (Hering-Glover-Brazelton cave system) (Figure
There are a few possible explanations as to why so few populations of P. alabamae have been reported even though the species has been known to science for almost 60 years and is distributed within and adjacent to a major metropolitan area with extremely high recreational and scientific caving activity. First, P. alabamae may in fact be quite rare with an extremely restricted distribution. Many troglobionts and stygobionts are considered short-range endemics (sensu
Another hypothesis to explain the low number of P. alabamae occurrences relates to detectability. Caves and groundwater ecosystems are extremely difficult for humans to access, survey, and study. Caves that are large enough to permit human entry and exploration as well as sinkholes, springs, and wells represent mere windows into a more expansive subterranean realm. And while many caves, springs, and other points of survey of subterranean biology exist within and near the distribution of P. alabamae in northern Alabama, most of these sites have not been adequately sampled. An undescribed species of cave shrimp closely related to P. alabamae is known from three caves to the west along the Tennessee River in Colbert and Lauderdale counties (
Moreover, cave systems that have been repeatedly visited by biologists may harbor P. alabamae populations that are not consistently observed each trip. For example, Muddy Cave had been visited on several occasions previously without reliable cave shrimp observations (
Low detection may be related to population dynamics or temporal variation of groundwater habitat extent, quality, and accessibility for surveys where P. alabamae occurs. Population dynamics of P. alabamae are unknown; however, some caves, such as Muddy Cave where very few shrimp have ever been observed, may represent sinks that are periodically extirpated but recolonized from currently unknown or inaccessible (to humans) source populations. Water levels in all caves where P. alabamae has been reported are highly variable. For example, aquatic habitat at Shelta Cave largely is reduced to shallow pools during summer and autumn but can fill to 6–8 m or more with higher precipitation during late winter and spring months restricting access to upper levels of the cave only (
The dynamic hydrology of these cave systems has made it difficult to effectively assess and characterize P. alabamae habitat. At most sites, cave shrimp are observed in silt or mud-bottomed, isolated pools with little to no flow that persist through dry seasons or remain once the water table has lowered after late winter-spring rainfall (
The discoveries of P. alabamae at Muddy Cave in 2005 and at Fern Cave renew optimism that additional populations may be discovered in the future. The recovery plan for P. alabamae identified two criteria for downlisting the species from endangered to threatened (
We thank the USFWS staff at Wheeler National Wildlife Refuge, particularly Rob Hurt, Emory Hoyle, and Ricky Ingram, as well as David Richardson from the Refuges Inventory and Monitoring (I&M) Branch, for allowing access and providing logistical support. We also thank the Alabama Field Office of the Nature Conservancy for providing local facilities to serve as fieldhouse for the multi-year study of Fern Cave fauna. Funding for this project was provided by the USFWS Refuges I&M Branch, Arkansas Field Office of The Nature Conservancy, Cave Conservancy Foundation (MLN), and The University of Alabama in Huntsville. This work was permitted by the Alabama Department of Conservation and Natural Resources under scientific collection permit no. 2018061776268680 and the Southeastern Cave Conservancy, Inc. under research permit no. 1015.