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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

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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.
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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
2Department 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 (matthew.niemiller@uah.edu)
Academic editor: O. Moldovan|Received 12 October 2018|Accepted 23 October 2018|Published 16 November2018
http://zoobank.org/2BCA9CF1-52C7-47B6-BDFB-25DCF9EA487A
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
Abstract
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.
Keywords
amphibian, habitat, life history, paedomorphosis, subterranean
Subterranean Biology 28: 29–38 (2018)
doi: 10.3897/subtbiol.28.30506
http://subtbiol.pensoft.net
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.
SHORT COMMUNICATION
Subterranean
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)
30
Introduction
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 inuence 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,
AmphibiaWeb 2018).
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 caveshes (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).
Methods
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 ries and shallow (<0.5 m) pools with pri-
marily chert, cobble, and coarse gravel substrate and signicant 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, conrmed 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-
ing processing.
Nicholas S. Gladstone et al. / Subterranean Biology 28: 29–38 (2018)
32
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).
Results
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 doeini 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),
Raaelli(2014)
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
L. Niemiller.
Nicholas S. Gladstone et al. / Subterranean Biology 28: 29–38 (2018)
34
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.
Discussion
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 signicantly 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, tradeos
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 ecient 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 signicant allochthonous organic input (i.e., higher inux 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 inux of organic matter from the
surface.ere are a variety of invertebrate taxa that serve as prey for G. gulolineatus
(e.g., isopods, amphipods, craysh, 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 dicult 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 eorts 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 eorts 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.
Acknowledgements
Funding for this project was provided by the U.S. Fish & Wildlife Service (grant no.
F17AC00939). All research was conducted under a TWRA scientic 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)
36
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... On the other hand, Proteus has inherited its aquatic and darkness-loving habits from surface ancestors. Likewise, it has inherited its large body reaching close to 0.1 kilogram, which is about an order of magnitude above the mass of most North American cave salamanders but comparable to the size of the largest known individuals of the Berry Cave salamander (Gyrinophilus gulolineatus; Gladstone et al. 2018). Sustaining a body of this size seems to be in conflict with the energy-poor subterranean ecosystem. ...
... Sustaining a body of this size seems to be in conflict with the energy-poor subterranean ecosystem. A possible explanation lies in the biological richness of some subterranean waters of the Dinaric Karst that are home to Proteus, and in the high organic input from the surface in the Berry Cave (Gladstone et al. 2018). ...
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Book
Caves and other subterranean habitats with their often strange (even bizarre) inhabitants have long been objects of fascination, curiosity, and debate. The question of how such organisms have evolved, and the relative roles of natural selection and genetic drift, has engaged subterranean biologists for decades. Indeed, these studies continue to inform the general theory of adaptation and evolution. Subterranean ecosystems generally exhibit little or no primary productivity and, as extreme ecosystems, provide general insights into ecosystem function. The Biology of Caves and other Subterranean Habitats offers a concise but comprehensive introduction to cave ecology and evolution. Whilst there is an emphasis on biological processes occurring in these unique environments, conservation and management aspects are also considered. The monograph includes a global range of examples from more than 25 countries, and case studies from both caves and non-cave subterranean habitats; it also provides a clear explanation of specialized terms used by speleologists. This accessible text will appeal to researchers new to the field and to the many professional ecologists and conservation practitioners requiring a concise but authoritative overview. Its engaging style will also make it suitable for undergraduate and graduate students taking courses in cave and subterranean biology. Its more than 650 references, 150 of which are new since the first edition, provide many entry points to the research literature.