A new maximum body size record for the Berry Cave Salamander... 29
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
Nicholas S. Gladstone1, Evin T. Carter2, K. Denise Kendall Niemiller3,
Lindsey E. Hayter4, Matthew L. Niemiller3
1 Department of Earth and Planetary Sciences, University of Tennessee, Knoxville, Tennessee 37916, USA
2Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37916, USA
3 Department of Biological Sciences, e University of Alabama in Huntsville, Huntsville, Alabama 35899,
USA 4 Admiral Veterinary Hospital, 204 North Watt Road, Knoxville, Tennessee 37934, USA
Corresponding author: Matthew L. Niemiller (email@example.com)
Academic editor: O. Moldovan|Received 12 October 2018|Accepted 23 October 2018|Published 16 November2018
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/
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. is salamander measured 145 mm in body length and represents not only the largest G. gulolinea-
tus 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
Subterranean Biology 28: 29–38 (2018)
Copyright Nicholas S. Gladstone et al. 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.
Biology Published by
The International Society
for Subterranean Biology
A peer-reviewed open-access journal
Nicholas S. Gladstone et al. / Subterranean Biology 28: 29–38 (2018)
Body size in amphibians is driven by strong selective pressures, because it interacts with
many aspects of life history (Whitford and Hutchison 1967, Blueweiss et al. 1978,
Hairston and Hairston 1987, Stearns 1992). Although several ecological and evolution-
ary mechanisms can be responsible for body size variation in amphibians, overarching
patterns are elusive (e.g., Bernardo and Reagan-Wallin 2002, Adams and Church 2008,
Slavenko and Meiri 2015). In response to Tilley and Bernardo (1993), Beachy (1995)
argues that a primary inuence on body size in amphibians is a delay in larval and juve-
nile period. In general, K-selected characteristics are correlated with increased longevity
and a shift toward larger propagule size in stable environments. Prolonged developmen-
tal periods may promote neoteny (or prolonged maturation) and can be associated with
reduced energy demand (McNamara and McNamara 1997). is suggests a possible
correlation between increased body size and both paedomorphic and K-selected life his-
tory strategies. However, the relationship between amphibian body size and these life
history strategies is largely unresolved (Yeh 2002, Wiens and Hoverman 2008).
While the reduction of body can be associated with paedomorphic traits (e.g.,
Alberch and Alberch 1981, Yeh 2002), Wiens and Hoverman (2008) concluded that
obligately paedomorphic salamanders (Amphiumidae, Cryptobranchidae, Proteidae,
Sirenidae) exhibit larger body sizes compared to those within clades that undergo met-
amorphosis. is pattern does not seem to translate to paedomorphic species within
clades that possess metamorphic or direct-developing species (Wiens and Hoverman
2008). In fact, paedomorphic Eurycea (Plethodontidae) associated with springs and
caves of the Edward’s Plateau in Texas are characterized by reduced body size relative
to their obligately metamorphic congeners, while both metamorphic and paedomor-
phic Ambystoma (Ambystomatidae) share similar body size (Ryan and Bruce 2000,
Caves and other subterranean habitats are often viewed as extreme and inhospitable
environments characterized by an absence of primary production and limited resources
(Culver and Pipan 2009). Salamanders are one of only two vertebrate groups to have
successfully colonized and obligately live in subterranean habitats. Fourteen species
from two families (Plethodontidae and Proteidae) occur exclusively in caves, and most
have evolved paedomorphosis (Goricki et al. 2012, in press, Niemiller et al. unpubl.
data), which may be a response to limited food resources within terrestrial cave habitats
(Brandon 1971, Wilbur and Collins 1973, Ryan and Bruce 2000). Few studies have ex-
amined the relationship between cave inhabitation and body size, and changes in body
size may not necessarily be associated with shifts from surface to subterranean habitats
(Romero 2009, Pipan and Culver 2017). However, many cave-obligate species (i.e.,
troglobites) exhibit K-selected life history traits such as reduced growth rate, delayed
sexual maturity, and increased longevity (Brandon 1971, Culver and Pipan 2009, Hüp-
pop 2012), and some troglobites and stygobites are larger than their surface congeners,
such as in amblyopsid caveshes (Poulson 1963, 1985, Niemiller and Poulson 2010).
A new maximum body size record for the Berry Cave Salamander... 31
e plethodontid genus Gyrinophilus Cope, 1869 includes four semi-aquatic to
paedomorphic species endemic to the highlands of eastern North America. ree spe-
cies 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, Goricki et al. 2012). Here, we report on a Berry
Cave Salamander, G. gulolineatus Brandon, 1965, from the type locality in Roane Co.,
Tennessee that exceeds the current maximum body size record for the species and rep-
resents the largest Gyrinophilus and plethodontid salamander reported in the United
States. Gyrinophilus gulolineatus is known from just ten localities in the Clinch and
Tennessee River watersheds in the Appalachians karst region of eastern Tennessee (Fig-
ure 1). e largest G. gulolineatus previously reported measured 136 mm snout-vent
length (SVL; tip of the snout to the posterior margin of the vent) from the type locality
(Brandon 1965, 1966).
As part of an ongoing study on the demography and life history of Gyrinophilus gulo-
lineatus, 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. e main entrance
is in a large sink, with the passage from the entrance steeply sloping down to the main
stream passage. e passage can be followed downstream to the northeast for ~160m
along the stream until large debris and sediment buildup block further exploration.
e stream is characterized by a series of ries and shallow (<0.5 m) pools with pri-
marily chert, cobble, and coarse gravel substrate and signicant amounts of coarse
woody debris, detritus, and ne mud and sediment in some areas. e 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 rst encountered, all but
the salamander’s head was out of the water, as it appeared to be moving partially over
land to continue upstream.
e salamander was captured with a handheld dip net and immediately trans-
ferred 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. e salamander was measured four times
by MLN, conrmed 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. e salamander was released at its point of capture follow-
Nicholas S. Gladstone et al. / Subterranean Biology 28: 29–38 (2018)
Figure 1. Geographic distribution of the Berry Cave Salamander (Gyrinophilus gulolineatus) in relation
to karst adapted from Weary and Doctor (2014). Blue circles represent cave localities from which the spe-
cies has been reported, and the red star represents the location of Berry Cave. e top right image shows
the main stream passage near the entrance of Berry Cave that continues throughout the entirety of our
sampling area. e bottom right image shows the large individual captured on 12 August 2018. Photo
credits: Matthew L. Niemiller.
To provide a comparison of body size relations across other large-bodied pletho-
dontids, 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 eld guides (see Table 1 and references therein).
e 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 2). Head width
measured 22 mm. ere was notable damage to the posterior end of the tail, and it is
likely that this individual was >250 mm TL before tail tissue loss. Additionally, the two
distal-most gill rachises on the right side of the head were notably smaller than those
on the left side, while the most proximal right gill rachis was enlarged relative to that
on the left side of the head.
A list of maximum body size and total length for several large plethodontid
salamanders is reported in Table 1. Based on our literature review, G. gulolineatus
is the largest plethodontid based on body size (SVL) in the United States, while
A new maximum body size record for the Berry Cave Salamander... 33
Table 1. Mode of development (DD = direct development, m = metamorphic; OP = obligately paedo-
morphic, 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
Species Mode of
development Habitat SVL (mm) TL (mm) References
Bolitoglossa doeini DD SUT 130 205 Feder et al. (1982)
Desmognathus quadramaculatus MSAT 103 189 Bakkegard and Rhea (2012)
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 MSAT/
SAC 134 221 Brandon (1966), Niemiller et al. (2010),
Niemiller et al. (unpublished data)
Gyrinophilus subterraneus FP SAC 117 199 Niemiller et al. (2010)
Isthmura bellii DD SUT 146 327 Smith (1949), Feder et al. (1982),
Isthmura gigantea DD SUT 161 276 Taylor and Smith (1945)
Isthmura maxima DD SUT 128 244 Parra-Olea et al. (2005)
Phaeognathus hubrichti DD SUT 138 268 Schwaner and Mount (1970), Bakkegard and
Guyer (2004), Graham et al. (2009)
Figure 2. Dorsal view of the Gyrinophilus gulolineatus captured at Berry Cave. Photo credit: Matthew
Nicholas S. Gladstone et al. / Subterranean Biology 28: 29–38 (2018)
only Phaeognathus hubrichti attains a greater total length. Body size in G. gulolin-
eatus rivals that observed in the direct-developing Isthmura bellii species complex
endemic to Mexico.
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
(Tilley and Bernardo 1993, Beachy 1995, Beachy et al. 2017). Representative species
with notable larger body sizes included in Table 1 represent four primary modes of
development in salamanders, with paedomorphic and direct-developing species ex-
hibiting larger body sizes relative to metamorphosing species. Larger species also are
correlated with aquatic habitats, apart from the Isthmura bellii species complex, which
inhabits Neotropical montane forests in southern North America.
Larger plethodontids are likely to occur in well-oxygenated, moist to fully aquat-
ic habitats, which largely relax allometric constraints on gas exchange. is is par-
ticularly 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; Ryan and Bruce
2000; Bonnet et al. 2014). Additionally, neoteny has been predicted to be the pri-
mary causal mechanism of paedomorphosis in salamanders (Duellman and Trueb
1986, Ryan and Bruce 2000). Larger amphibian body sizes are further associated
with longer juvenile periods, which signicantly covary with age at maturation (e.g.,
Desmognathus quadramaculatus and Gyrinophilus porphyriticus, Bruce 1988, Beachy
1995, Beachy et al. 2017).
Many of the largest plethodontid salamanders are direct-developing (e.g., Phae-
ognathus hubrichti in the United States; Isthmura bellii in Mexico). Direct-developing
species are generally characterized by having larger eggs and longer embryonic devel-
opment relative to metamorphic or paedomorphic species, and this may related to
attaining larger body sizes (Wake and Hanken 2004). ere are, however, tradeos
related to larger body size in these terrestrial plethodontids. e habitat must sup-
port gas exchange through adequate temperature and moisture gradients, and these
taxa have evolved physiological mechanisms, such as waxy secretions, to reduce water
loss. Second, terrestrial environments typically have lower food availability, and, ac-
cordingly, terrestrial salamanders often experience more extended periods of inactivity
(Jaeger 1979, 1981, Scott et al. 2007). Phaeognathus, for instance, has rarely (if ever)
been observed outside of burrows in densely forested ravines. Larger body size in such
species is in accordance with the ‘starvation hypothesis’ that predicts that greater mass
is positively correlated to seasonality and periods of low resource availability (Lundberg
1986), because larger individuals can persist through low-resource events by having
A new maximum body size record for the Berry Cave Salamander... 35
greater energy stores and typically more ecient metabolism owing to positive allom-
etry. e starvation hypothesis has received recent support in multiple amphibian taxa,
where body size is positively related to extended inactivity (Valenzuela-Sánchez et al.
2015) and increased precipitation seasonality (Goldberg et al. 2018).
Cave environments are often characterized by low food resources and few natu-
ral predators, which likely shaped much of the evolution of many subterranean taxa
(Gibert and Deharveng 2002). However, this archetype may not be representative of
all subterranean systems, as many caves possess a high surface-environment connec-
tion with signicant allochthonous organic input (i.e., higher inux of organic matter)
driving both terrestrial and aquatic food webs. Cave obligate salamanders often exhibit
reduced growth rates and low metabolic demand (e.g., Hervant et al. 2000), and they
may also exhibit greater longevity owing to the slow pace of life and low predation
pressure associated with subterranean environments (Brandon 1971, Culver and Pipan
2009, Voituron et al. 2011, Hüppop 2012). High resource environments may thus
permit more rapid growth and sustain a larger overall body size. e exceptionally large
Gyrinophilus gulolineatus reported here occurred within 10 m of the cave entrance in
a high ow zone with an abundance of organic matter accumulated in the cave pool.
Berry Cave is a diverse system relative to other caves in the Appalachian Valley and
Ridge (Niemiller et al. 2016), likely due to the large inux of organic matter from the
surface.ere are a variety of invertebrate taxa that serve as prey for G. gulolineatus
(e.g., isopods, amphipods, craysh, atworms, etc.).
While there has been much focus on life history evolution in salamanders, sam-
pling biases may impact interpretations of the relationship between body size and
mode of development. Paedomorphic species may be more dicult to capture, and
they are often associated with extreme habitats such as underground springs and caves
(Ryan and Bruce 2000, Bonnet et al. 2014). More thorough survey eorts and detailed
life history observations within harsher or more isolated environments are necessary to
better understand how paedomorphosis may relate to body size in amphibians.
Due to its subterranean existence and cryptic nature, many life history characteris-
tics of G. gulolineatus have yet to be documented. Active survey eorts 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 scientic collection per-
mit (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.
Nicholas S. Gladstone et al. / Subterranean Biology 28: 29–38 (2018)
Adams DC, Church JO (2008) Amphibians do not follow Bergmann’s rule. Evolution: Inter-
national Journal of Organic Evolution 62(2): 413–420. https://doi.org/10.1111/j.1558-
Alberch P, Alberch J (1981) Heterochronic mechanisms of morphological diversication and
evolutionary change in the neotropical salamander, Bolitoglossa occidentalis (Amphibia:
Plethodontidae). Journal of Morphology 167(2): 249–264. https://doi.org/10.1002/
Bakkegard KA, Rhea RA (2012) Tail length and sexual size dimorphism (SSD) in desmogna-
than salamanders. Journal of Herpetology 46: 304–311. https://doi.org/10.1670/10-307
Bakkegard KA, Guyer C (2004) Sexual size dimorphism in the Red Hills salamander, Phaeog-
nathus hubrichti (Caudata: Plethodontidae: Desmognathinae). Journal of Herpetology 38:
Beachy CK (1995) Age at maturation, body size, and life-history evolution in the salamander
family Plethodontidae. Herpetological Review 26: 179–181.
Beachy CK, Ryan TJ, Bonett RM (2017) How metamorphosis is dierent in plethodontids:
larval life history perspectives on life-cycle evolution. Herpetologica 73(3): 252–258. htt-
Bernardo J, Reagan‐Wallin NL (2002) Plethodontid salamanders do not conform to “general
rules” for ectotherm life histories: insights from allocation models about why simple mod-
els do not make accurate predictions. Oikos 97(3): 398–414. https://doi.org/10.1034/
Blueweiss L, Fox H, Kudzma V, Nakashima D, Peters R, Sams S (1978) Relationships be-
tween body size and some life history parameters. Oecologia 37(2): 257–272. https://doi.
Bonett RM, Steen MA, Lambert SM, Wiens JJ, Chippindale PT (2014) Evolution of pae-
domorphosis in plethodontid salamanders: ecological correlates and re‐evolution of meta-
morphosis. Evolution 68(2): 466–482. https://doi.org/10.1111/evo.12274
Bruce RC (1979) Evolution of paedomorphosis in salamanders of the genus Gyrinophilus. Evo-
lution 33(3): 998–1000. https://doi.org/10.1111/j.1558-5646.1979.tb04753.x
Bruce RC (1980) A model of the larval period of the spring salamander, Gyrinophilus porphy-
riticus, based on size-frequency distributions. Herpetologica: 78–86.
Bruce RC (1988) Life history variation in the salamander Desmognathus quadramaculatus. Her-
Culver DC, Pipan T (2009) e biology of caves and other subterranean habitats. Second edi-
tion. Oxford University Press, Oxford, U.K.
Duellman WE, Trueb L (1986) Biology of amphibians. McGraw‐Hill, New York, USA.
Feder ME, Papenfuss TJ, Wake DB (1982) Body size and elevation in neotropical salamanders.
Copeia 1982: 186–188. https://doi.org/10.2307/1444288
Gibert J, Deharveng L (2002) Subterranean ecosystems: A truncated functional biodiversity:
this article emphasizes the truncated nature of subterranean biodiversity at both the bot-
tom (no primary producers) and the top (very few strict predators) of food webs and dis-
A new maximum body size record for the Berry Cave Salamander... 37
cusses the implications of this truncation both from functional and evolutionary perspec-
tives. AIBS Bulletin 52(6): 473–481.
Graham SP, Hoss SK, Godwin JC (2009):Phaeognathus hubrichti(Red Hills Salamander) re-
cord size. Herpetological Review 40: 196.
Goldberg J, Cardozo D, Brusquetti F, Villafañe DB, Gini AC, Bianchi C (2018). Body size var-
iation and sexual size dimorphism across climatic gradients in the widespread treefrog Sci-
nax fuscovarius (Anura, Hylidae). Austral Ecology 43(1): 35–45. https://doi.org/10.1111/
Goricki S, Niemiller ML, Fenolio DB (2012) Salamanders. In: White WH, Culver DC (Eds)
Encyclopedia of caves. Second edition. Elsevier, London, UK, 665–676. https://doi.
Hairston NA, Hairston NG (1987) Community ecology and salamander guilds. Cambridge
University Press, Cambridge, UK.
Hervant F, Mathieu J, Durand JP (2000) Metabolism and circadian rhythms of the European blind
cave salamander Proteus anguinus and a facultative cave dweller, the Pyrenean newt (Euproctus
asper). Canadian Journal of Zoology 78(8): 1427–1432. https://doi.org/10.1139/z00-084
Hüppop K (2012). Adaptation to low food. In: White WH, Culver DC (Eds) Encyclopedia
of caves. Second edition. Elsevier, London, UK, 1–9. https://doi.org/10.1016/B978-0-12-
Jaeger RG (1979) Fluctuations in prey availability and food limitation for a terrestrial salaman-
der. Oecologia 44(3): 335–341. https://doi.org/10.1007/BF00545237
Jaeger RG (1981) Dear enemy recognition and the costs of aggression between salamanders.
e American Naturalist 117(6): 962–974. https://doi.org/10.1086/283780
Lundberg A (1986) Adaptive advantages of reversed sexual size dimorphism in European owls.
Ornis Scandinavica 17(2): 133–140. https://doi.org/10.2307/3676862
McNamara KJ, McNamara K (1997) Shapes of time: the evolution of growth and develop-
ment. Johns Hopkins University Press, Baltimore, USA.
Niemiller ML, Poulson TL (2010) Subterranean shes of North America: Amblyopsidae. In:
Trajano E, Kapoor BG (Eds) Biology of Subterranean Fishes. Science Publishers, Eneld,
Niemiller ML, Osbourn MS, Fenolio DB, Pauley TK, Miller BT, Holsinger JR (2010) Conser-
vation status and habitat use of the West Virginia spring salamander (Gyrinophilus subter-
raneus) and spring salamander (G. porphyriticus) in General Davis Cave, Greenbrier Co.,
West Virginia. Herpetological Conservation and Biology 5(1): 32–43.
Niemiller ML, Carter ET, Hayter L, Gladstone NS (2018) New surveys and reassessment of the
conservation status of the Berry Cave Salamander (Gyrinophilus Gulolineatus). Technical
Report. U. S. Fish & Wildlife Service, 51 pp.
Niemiller ML, Zigler KS, Stephen CDR, Carter ET, Paterson AT, Taylor SJ, Engel AS (2016)
Vertebrate fauna in caves of eastern Tennessee within the Appalachians karst region, USA.
Journal of Cave and Karst Studies 78: 1–24. https://doi.org/10.4311/2015LSC0109
Parra-Olea G, Garcia-Paris M, Papenfuss TJ, Wake DB (2005) Systematics of the Pseudoeurycea
bellii (Caudata: Plethodontidae) species complex. Herpetologica 61: 145–158. https://doi.
Nicholas S. Gladstone et al. / Subterranean Biology 28: 29–38 (2018)
Pipan T, Culver DC (2017) e unity and diversity of the subterranean realm with re-
spect to invertebrate body size. Journal of Cave and Karst Studies 79: 1–9. https://doi.
Poulson TL (1963) Cave adaptation in amblyopsid shes. American Midland Naturalist: 257–
Romero A (2009) Cave biology: life in darkness. Cambridge University Press, Cambridge, UK.
Ryan TJ, Bruce RC (2000) Life history evolution and adaptive radiation of hemidactyliine sala-
manders. In: Bruce RC, Jaeger RG, Houck LD (Eds) e biology of plethodontid salaman-
ders. Springer, Boston, MA, 303–326. https://doi.org/10.1007/978-1-4615-4255-1_15
Scott DE, Casey ED, Donovan MF, Lynch TK (2007) Amphibian lipid levels at metamorpho-
sis correlate to post-metamorphic terrestrial survival. Oecologia 153(3): 521–532. https://
Sket B (2008) Can we agree on an ecological classication of subterranean animals?. Journal of
Natural History 42(21–22): 1549–1563. https://doi.org/10.1080/00222930801995762
Slavenko A, Meiri S (2015) Mean body sizes of amphibian species are poorly predicted by
climate. Journal of Biogeography 42(7): 1246–1254. https://doi.org/10.1111/jbi.12516
Smith HM (1949) Size maxima in terrestrial salamanders. Copeia 1949: 71. https://doi.
Smith HM, Taylor EH (1948) An annotated checklist and key to the Amphibia of Mexico.
Bulletin of the United States National Museum 194: 1–118. https://doi.org/10.5479/
Stearns SC (1992) e evolution of life histories. Oxford University Press. Oxford, UK.
Tilley SG, Bernardo J (1993) Life history evolution in plethodontid salamanders. Herpeto-
logica 49, no. 2: 154–163.
Valenzuela-Sánchez A, Cunningham AA, Soto-Azat C (2015) Geographic body size variation
in ectotherms: eects of seasonality on an anuran from the southern temperate forest.
Frontiers in Zoology 12, no. 1: 37. https://doi.org/10.1186/s12983-015-0132-y
Voituron Y, de Fraipont M, Issartel J, Guillaume O, Clobert J (2011) Extreme lifespan of
the human sh (Proteus anguinus): a challenge for ageing mechanisms. Biology Letters
Wake DB, Hanken JA (2004) Direct development in the lungless salamanders: what are the
consequences for developmental biology, evolution and phylogenesis? International Jour-
nal of Developmental Biology 40(4): 859–869.
Weary DJ, Doctor DH (2014) Karst in the United States: A digital map compilation and data-
base. USGS Open File Report 2014–1156; Available: http://pubs.usgs.gov/of/2014/1156/
Whitford WG, Hutchison VH (1967) Body size and metabolic rate in salamanders. Physiologi-
cal Zoology 40(2): 127–133. https://doi.org/10.1086/physzool.40.2.30152447
Wiens JJ, Hoverman JT (2008) Digit reduction, body size, and paedomorphosis in salaman-
ders. Evolution and Development 10(4): 449–463. https://doi.org/10.1111/j.1525-
Yeh J (2002). e eect of miniaturized body size on skeletal morphology in frogs. Evolution
56(3): 628–641. https://doi.org/10.1111/j.0014-3820.2002.tb01372.x