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Corresponding author: Matthew L. Niemiller ( cavemander17@gmail.com ) Academic editor: Oana Teodora Moldovan
© 2018 Nicholas S. Gladstone, Evin T. Carter, K. Denise Kendall Niemiller, Lindsey E. Hayter, Matthew L. 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:
Gladstone NS, Carter ET, Niemiller KDK, Hayter LE, Niemiller ML (2018) A new maximum body size record for the Berry Cave Salamander (Gyrinophilus gulolineatus) and genus Gyrinophilus (Caudata, Plethodontidae) with a comment on body size in plethodontid salamanders. Subterranean Biology 28: 29-38. https://doi.org/10.3897/subtbiol.28.30506
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Lungless salamanders in the family Plethodontidae exhibit an impressive array of life history strategies and occur in a diversity of habitats, including caves. However, relationships between life history, habitat, and body size remain largely unresolved. During an ongoing study on the demography and life history of the paedomorphic, cave-obligate Berry Cave Salamander (Gyrinophilus gulolineatus, Brandon 1965), we discovered an exceptionally large individual from the type locality, Berry Cave, Roane County, Tennessee, USA. This salamander measured 145 mm in body length and represents not only the largest G. gulolineatus and Gyrinophilus ever reported, but also the largest plethodontid salamander in the United States. We discuss large body size in G. gulolineatus and compare body size in other large plethodontid salamanders in relation to life history and habitat.
amphibian, habitat, life history, paedomorphosis, subterranean
Body size in amphibians is driven by strong selective pressures, because it interacts with many aspects of life history (
While the reduction of body can be associated with paedomorphic traits (e.g.,
Caves and other subterranean habitats are often viewed as extreme and inhospitable environments characterized by an absence of primary production and limited resources (
The plethodontid genus Gyrinophilus Cope, 1869 includes four semi-aquatic to paedomorphic species endemic to the highlands of eastern North America. Three species are paedomorphic stygobionts found in caves of the Interior Low Plateau and Appalachians karst regions of Alabama, Tennessee, Georgia, and West Virginia in the United States (Niemiller et al. 2009,
Geographic distribution of the Berry Cave Salamander (Gyrinophilus gulolineatus) in relation to karst adapted from
As part of an ongoing study on the demography and life history of Gyrinophilus gulolineatus, we captured a large G. gulolineatus at the type locality, Berry Cave (Tennessee Cave Survey no. TRN3), on 12 August 2018. Berry Cave is located 0.37 km west of the Tennessee River near Wright Bend in Roane County, Tennessee. The main entrance is in a large sink, with the passage from the entrance steeply sloping down to the main stream passage. The passage can be followed downstream to the northeast for ~160m along the stream until large debris and sediment buildup block further exploration. The stream is characterized by a series of riffles and shallow (<0.5 m) pools with primarily chert, cobble, and coarse gravel substrate and significant amounts of coarse woody debris, detritus, and fine mud and sediment in some areas. The salamander was observed and captured in the margin of a shallow (<0.5 m deep) pool located in a small passage upstream from the main entrance chamber. When first encountered, all but the salamander’s head was out of the water, as it appeared to be moving partially over land to continue upstream.
The salamander was captured with a handheld dip net and immediately transferred to a clear plastic bag for processing. We massed to the nearest 0.5 g using a Pesola® spring scale and measured to the nearest 0.5 mm snout-vent length (SVL; tip of the snout to the posterior margin of the vent) and total length (TL; tip of the snout to the end of the tail) using a metric caliper. The salamander was measured four times by MLN, confirmed by NSG and ETC, and then photographed using an Olympus Tough TG-5 Camera. We also noted any physical abnormalities and the overall health of the salamander. Finally, we marked the salamander by injecting a 1.2 × 2.7 mm visible implant (VI) alpha tag (Northwest Marine Technology Inc., Shaw Island, WA) into the dermis of the tail. The salamander was released at its point of capture following processing.
To provide a comparison of body size relations across other large-bodied plethodontids, we later compiled a list of maximum body sizes, modes of development, and habitat for several plethodontid salamanders by conducting a search of the primary literature and relevant field guides (see Table
Mode of development (DD = direct development, m = metamorphic; OP = obligately paedomorphic, FP = facultatively paedomorphic), habitat (AQC = aquatic cave, SAC = semi-aquatic cave, SAT = semiaquatic terrestrial, SUT = surface terrestrial), maximum body size (SVL) and total length (TL) of select plethodontid salamanders based on literature sources and the current study.
Size and life history characteristics of select plethodontid salamanders | |||||
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Species | Mode of development | Habitat | SVL (mm) | TL (mm) | References |
Bolitoglossa dofleini | DD | SUT | 130 | 205 |
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Desmognathus quadramaculatus | M | SAT | 103 | 189 |
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Gyrinophilus gulolineatus | OP | AQC | 145 | 238 | Brandon (1965, 1966), this study |
Gyrinophilus palleucus | OP | AQC | 113 | 186 | Lazell and Brandon (1962), Dent and Kirby-Smith (1963), Niemiller et al. (unpubl. data) |
Gyrinophilus porphyriticus | M | SAT/SAC | 134 | 221 | Brandon (1966), |
Gyrinophilus subterraneus | FP | SAC | 117 | 199 |
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Isthmura bellii | DD | SUT | 146 | 327 |
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Isthmura gigantea | DD | SUT | 161 | 276 | Taylor and Smith (1945) |
Isthmura maxima | DD | SUT | 128 | 244 |
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Phaeognathus hubrichti | DD | SUT | 138 | 268 | Schwaner and Mount (1970), |
The Gyrinophilus gulolineatus observed and captured at Berry Cave on 12 August 2018 measured 145 mm SVL and 238 mm TL, with a mass of 35 g (Figure
A list of maximum body size and total length for several large plethodontid salamanders is reported in Table
Plethodontid salamanders exhibit considerable variation in life history strategies and habitat that has resulted in an extraordinary range of growth rates and age at maturity (
Larger plethodontids are likely to occur in well-oxygenated, moist to fully aquatic habitats, which largely relax allometric constraints on gas exchange. This is particularly relevant to those species that exhibit paedomorphic life history strategies. Paedomorphic individuals may be able to grow unimpeded in their permanently aquatic state owing to indeterminate growth. Obligate paedomorphosis has evolved multiple times within Plethodontidae, with the subfamily Spelerpinae having the greatest richness of paedomorphic species (Chippendale 1995;
Many of the largest plethodontid salamanders are direct-developing (e.g., Phaeognathus hubrichti in the United States; Isthmura bellii in Mexico). Direct-developing species are generally characterized by having larger eggs and longer embryonic development relative to metamorphic or paedomorphic species, and this may related to attaining larger body sizes (
Cave environments are often characterized by low food resources and few natural predators, which likely shaped much of the evolution of many subterranean taxa (
While there has been much focus on life history evolution in salamanders, sampling biases may impact interpretations of the relationship between body size and mode of development. Paedomorphic species may be more difficult to capture, and they are often associated with extreme habitats such as underground springs and caves (
Due to its subterranean existence and cryptic nature, many life history characteristics of G. gulolineatus have yet to be documented. Active survey efforts are continuing to assess the species’ demography in Berry Cave, as well as to better understand the growth of this species. Further biological inventory within the Appalachian Valley and Ridge is underway with the intent to uncover additional localities. Future directions for research include additional life history characterization and study of the species’ ecology.
Funding for this project was provided by the U.S. Fish & Wildlife Service (grant no. F17AC00939). All research was conducted under a TWRA scientific collection permit (nos. 1385 and 1605) and following an approved protocol by the University of Alabama in Huntsville Institutional Animal Care and Use Committee (protocol no. 2017.R005). We especially thank the Healy family for allowing access to Berry Cave.