Copeia 2011, No. 2, 285–295
Comparative Morphometrics in Ranid Frogs (Subgenus Nenirana): Are
Apomorphic Elongation and a Blunt Snout Responses to Small-bore Burrow
Dwelling in Crawfish Frogs (Lithobates areolatus)?
Nathan J. Engbrecht1, Susan J. Lannoo2, John O. Whitaker1, and
Michael J. Lannoo2
The subgenus Nenirana of North American ranid frogs encompasses Pickerel Frogs (Lithobates palustris), Crawfish Frogs
(L. areolatus), Gopher Frogs (L. capito), and Dusky Gopher Frogs (L. sevosus). All four species inhabit caves, crevices, stump
holes, and/or burrows when not in breeding wetlands. Crawfish Frogs obligately inhabit crayfish burrows as their
primary retreat sites, and in this study we examine whether the deep, small-bore crayfish burrows used by Crawfish
Frogs have influenced Crawfish Frog morphology. Specimens of all four species of Nenirana were radiographed and
snout–urostyle length, maximum headwidth, head length, femur length, and tibiofibula length were measured from
films. Our results suggest that if Crawfish Frog morphology is a response to life in burrows, it is due in part to having the
size characteristic of being the largest member of the clade and in part through the shape characteristic of generally
exhibiting an intermediate morphology between Pickerel Frogs and the two Gopher Frog species. Not all shape metrics,
however, are intermediate; among Nenirana, Crawfish Frogs have the longest hindlimbs and the relatively bluntest
snouts. Further, Crawfish Frogs exhibit positive allometry in headwidth, a reversal of the ancestral pattern exhibited by
Pickerel Frogs. None of the morphological features of Crawfish Frogs fit neatly into known or predicted functional/
morphological cause-and-effect relationships associated with burrow occupancy. It may be that the ranid body plan is
generalized enough to permit Crawfish Frogs to inhabit, despite being unable to dig, deep small-bore burrows without
undergoing major morphological changes.
T
HE subgenus Nenirana of ranid frogs (Hillis and
Wilcox, 2005) encompasses four species of North
American frogs: Lithobates palustris (Pickerel Frogs), L.
areolatus (Crawfish Frogs), L. capito (Gopher Frogs), and L.
sevosus (Dusky Gopher Frogs). Pickerel Frogs form the
outgroup to the Gopher Frog/Crawfish Frog clade; Crawfish
Frogs form the outgroup to the Gopher Frog clade (Fig. 1;
Goin and Netting, 1940; Young and Crother, 2001; Richter
et al., 2009). All four species of Nenirana are unique among
North American ranids in that they will preferentially
inhabit caves, crevices, stump holes, and/or burrows when
not in breeding wetlands. This predilection for retreat types
varies across species. Pickerel Frog retreats are generally the
least specific, although these animals have been described as
‘‘the most cave adapted North American anuran’’ (Prather
and Briggler, 2001; Fenolio et al., 2005; Redmer, 2005 ). In
contrast, both species of Gopher Frogs prefer burrows that
include those created by Gopher Tortoises (Gopherus polyphemus; Jensen and Richter, 2005; Richter and Jensen, 2005).
And while Crawfish Frogs can also inhabit a variety of
burrow types and retreat sites while migrating to and from
breeding wetlands (Parris and Redmer, 2005), their ‘‘primary
burrows’’—where they spend the majority of their time
(Thompson, 1915; Heemeyer and Lannoo, 2010; Hoffman et
al., 2010)—are nearly always crayfish burrows. Crayfish
burrows have the advantage of coursing to the water table
(Neil, 1951; Grow, 1981), allowing Crawfish Frogs not only
the security from predators that most burrow types provide
(for an exception see Engbrecht and Heemeyer, 2010), but
also an opportunity to thermoregulate, hydrate, and
overwinter (Brown et al., 1972; Hoffman and Katz, 1989;
Wells, 2008; Hoffman et al., 2010). Crawfish Frogs generally
use a single crayfish burrow for a long period of time, long
enough to wear away, or prevent the growth of, vegetation
and form a bare patch of soil (the ‘‘feeding platform’’) at the
burrow entrance (Hurter, 1911; Hoffman et al., 2010).
Individuals of both Gopher Frog species also form ‘‘feeding
platforms’’ (Richter et al., 2001; Stevenson and Dyer, 2002);
Pickerel Frogs do not. Unlike the retreat sites of other species
of Nenirana (caves and Gopher Tortoise burrows), crayfish
burrows are both deep and small bore, typically not much
wider than the Crawfish Frogs that occupy them.
While each of the species of Nenirana inhabits retreats,
none are truly fossorial in Hildebrand’s (1974) sense of an
animal adapted to dig effectively (Emerson, 1976). According to Emerson (1976), 95% of fossorial anurans dig
backward. Indeed, Crawfish Frog juveniles and Gopher Frog
adults will excavate shallow retreats by digging backward
(Parris, 1998; J. Humphries, pers. comm.; see below). None
of the species of Nenirana, however, have spades, or are
known to have limb specializations (shortening, thickening)
associated with burrowing. Rather than excavate their own
burrows, they generally inhabit natural cavities or burrows
created by other species.
The three Gopher Frog/Crawfish Frog species are of
considerable conservation concern. Dusky Gopher Frogs
are Federally Endangered (USFWS, 2001; Richter and Jensen,
2005), and Gopher Frogs are known from fewer than 20
populations in any state where they occur except Florida
(Jensen and Richter, 2005); collectively, outside of Florida
there may be fewer than 5,000 Gopher Frog adults (SEPARC,
2010). Crawfish Frogs are also thought to be in steep decline
throughout large portions of their range, although due to
their cryptic habits (considered by some to be the most
secretive of North American Rana; Smith, 1950), their status
had been difficult to determine (Parris and Redmer, 2005).
1
Department of Biology, Rm 281 Science Building, Indiana State University, Terre Haute, Indiana 47809; E-mail: (NJE) nengbrecht@
indstate.edu; and (JOW) [email protected].
2
Indiana University School of Medicine, Rm 135 Holmstedt Hall–ISU, Terre Haute, Indiana 47809; E-mail: (SJL) [email protected]; and
(MJL) [email protected]. Send reprint requests to MJL.
Submitted: 11 May 2010. Accepted: 1 February 2011. Associate Editor: S. A. Schaefer.
DOI: 10.1643/CG-10-075
F 2011 by the American Society of Ichthyologists and Herpetologists
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Copeia 2011, No. 2
Fig. 1. Phylogenetic relationships among the four species in the
subgenus Nenirana, with preferred retreat type indicated. Data were
derived from Young and Crother (2001) and Hillis and Wilcox (2005).
Biologists familiar with the many issues surrounding the
conservation of these animals feel they are in a race to
understand their biology before these species are driven to
extinction (SEPARC, 2010).
Here we compare cranial and hindlimb morphology across
all four species of Nenirana. The question that began this
investigation was whether the deep, small-bore crayfish
burrows used by Crawfish Frogs influence Crawfish Frog
morphology. The remaining three species of Nenirana were
examined to provide appropriate outgroup comparisons
(Brooks and McLennan, 1991; Harvey and Pagel, 1991;
Wiens, 2000). Our measurements were similar to those taken
on this species group by Goin and Netting (1940) and on
Crawfish Frogs by Bragg (1953), but while the former authors
were examining characters useful for distinguishing species,
our study examines the morphological correlates of burrow
habitation. We also differ from Goin and Netting (1940) in
two ways: we used Pickerel Frogs for outgroup comparison (to
provide directionality to interspecific differences), and we
examined not only adults but also a range of juveniles to
provide a postmetamorphic ontogenetic series. Additionally,
we analyzed a larger and more geographically widespread
dataset than the one available to Goin and Netting (1940).
MATERIALS AND METHODS
Crawfish Frog, Gopher Frog, Dusky Gopher Frog, and
Pickerel Frog specimens were obtained from museum
collections around the country. One hundred sixty-one
animals were examined. Specimens included in this analysis
were: Crawfish Frogs—48 males, 17 females, and eight
recently metamorphosed (,35 mm SUL) animals; Gopher
Frogs—ten males, nine females, three adults whose sex
could not be definitively determined, six juveniles (between
50 and 70 mm SUL), and three recently metamorphosed
animals; Dusky Gopher Frogs—one male, 13 females, one
juvenile, and two recently metamorphosed animals; and
Pickerel Frogs—27 adults, nine juveniles (between 35 and
40 mm), and four recently metamorphosed animals. The
Crawfish Frog specimens examined in this study were
collected in Indiana. We recognize that juveniles and
postmetamorphic animals are relatively underrepresented
in this sample; they are underrepresented in most collections. Crawfish Frogs are so secretive in terrestrial habitats
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that animals are generally only observed and therefore
collected in and around breeding wetlands. This means
postmetamorphic juveniles and breeding adults are best
represented, while older juveniles and subadults are not.
Specimens were radiographed using an HP Faxitron
Cabinet X-Ray System. Measurements were taken from
radiographs using a Storm-3C301 Electronic Digital Caliper
measured to the nearest 0.01 mm and rounded to the
nearest 0.1 mm. With radiographs, image distortion is
directly proportional to distance of the specimen from the
film (Quinn, 1980). With the Faxitron System, distances of
,1 cm produce a distortion of ,1% (J. T. Eastman, pers.
comm.). Measurements on radiographic images included
snout–urostyle length (SUL), maximum headwidth (HW),
head length measured from a line through the posterior
margins of quadrate bones (HL), femur length (FEM), and
tibiofibula length (TIBFIB). Although we were curious about
forelimb lengths (in the sense of ‘‘the skeleton as a whole’’;
Thompson, 1917), we did not measure forelimb elements
because in most museum specimens, forelimbs are positioned in a dorsal–ventral orientation, which makes measuring bone lengths from radiographs impossible (Fig. 2).
Further, forelimbs are specialized in frog species that burrow
head first (Emerson, 1976), but not (aside from sexual
dimorphism) in species such as those in Nenirana that either
do not burrow or occasionally burrow backward. In order to
compare body proportions (Trueb, 1977), HW, HL, FEM, and
TIBFIB measurements were divided by SUL and arcsine
transformed (see below).
Although preserved specimens are subject to physical
shrinking and expanding when immersed in ethanol (Lee,
1982), our method of using radiographed images to measure
bones (as opposed to collecting external anatomical measurements that include soft tissues) should lessen these
preservation artifacts. Bone decalcification (which could
allow shrinking) was not observed in radiographs.
For this analysis we assume that Pickerel Frogs are basal
within the clade Nenirana (Fig. 1; Goin and Netting, 1940)
and that their morphology approximates the primitive
condition for the clade. We follow Huxley (1972) in
defining allometry as ‘‘different rates of growth of parts of
the body relative to that of the body as a whole.’’
Descriptions of ontogenetic trajectories (for their usefulness
as phylogenetic character states, see Mabee, 2000; Maglia et
al., 2001) were based on regression analyses (metric/SUL vs.
SUL). Ratios were arcsine transformed and tested for
normality using the Shapiro-Wilk normality test. Of the 16
metrics examined (four anatomical measurements for each
of the four species), all but three ratio measurements (head
length/SUL and tibiofibula length/SUL for L. palustris, head
length/SUL for L. capito) were normally distributed after
arcsine transformation. Kruskall-Wallis and Mann-Whitney
U tests (with sequential Bonferroni correction) were used to
test for significance in non-normally distributed metrics.
Non-parametric statistics yielded the same results as parametric statistics, with the exception that relative head
length differed between Pickerel Frogs and Dusky Gopher
Frogs. Average measurements are given as mean 61 SD.
Museum abbreviations follow Leviton et al. (1985) and are
listed at http://www.asih.org/node/204.
RESULTS
Adult body size and shape.—The four species of Nenirana
differ in size and shape (Fig. 2). In our sample, Pickerel Frogs
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Fig. 2. Radiographs of the four species in the subgenus Nenirana. (A) Lithobates palustris (ISU 1522), (B) L. areolatus (UMMZ 103361-1654), (C) L.
capito (FMNH 21741), (D) L. sevosus (CM 18185). Note the relative similarity in body proportions among L. areolatus, L. capito, and L. sevosus, and
the large headwidth of L. capito and L. sevosus.
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Table 1. Mean Morphometric Measurements Made on Specimens (Excluding Recently Metamorphosed Individuals) of the Four Species Comprising
the Nenirana Group. Error bars denote ± one standard deviation from the mean. Abbreviations: SUL = snout–urostyle length, HW = headwidth, HL =
head length, FEM = femur length, TIBFIB = tibiofibula length.
Species
n
L.
L.
L.
L.
36
65
28
15
palustris
areolatus
capito
sevosus
SUL
44.9
87.2
79.3
72.9
6
6
6
6
6.94
9.91
10.65
7.07
HW
15.8
32.4
34.6
31.8
6
6
6
6
HL
2.21
3.49
4.79
2.46
14.0
25.7
26.5
24.6
6
6
6
6
1.55
2.59
3.00
1.46*
FEM
21.5
35.8
32.1
30.9
6
6
6
6
3.37
3.76
3.94
2.18
TIBFIB
24.0
40.9
34.5
33.5
6
6
6
6
3.87
3.99
4.53
2.28
* Because of neck flexing and radiograph image distortion, one head length result was excluded from the analysis.
were smallest (x 5 44.9 mm SUL 6 6.94), Dusky Gopher
Frogs (x 5 72.9 mm SUL 6 7.07) and Gopher Frogs (x 5
79.3 mm SUL 6 10.65) were larger, and Crawfish Frogs (x 5
87.2 mm SUL 6 9.91) were largest (Table 1; Fig. 3). These
values correspond to lengths and relative sizes of these four
species reported in the literature (Goin and Netting, 1940;
Bragg, 1953; summarized by Jensen and Richter, 2005; Parris
and Redmer, 2005; Redmer, 2005; Richter and Jensen, 2005),
although both Goin and Netting (1940) and Bragg (1953)
reported a north–south gradient in size and body proportions in Crawfish Frogs. Within species, females tend to be
larger, but in our samples these differences were not
significant (Crawfish Frogs: males x 5 86.4 mm SUL, females
x 5 89.5 mm SUL, P 5 0.27; Gopher Frogs: males x 5
82.7 mm SUL, females x 5 84.8 mm SUL, P 5 0.52);
therefore, we combined male and female data for adult
analyses. In addition to being the smallest species, Pickerel
Frogs were also the most slender species within the subgenus
Nenirana (Fig. 2).
Comparative measurements of SULs, headwidths (HW),
head lengths (HL), femur lengths (FEM), and tibiofibula
lengths (TIBFIB) are given in Figure 3. Again, Pickerel Frogs
were always smallest. Comparing Crawfish Frogs to the two
Fig. 3. Comparative morphometrics of species in the subgenus
Nenirana (excluding recently metamorphosed specimens). Note the
relatively small size of Lithobates palustris and the clustering of L.
areolatus, L. capito, and L. sevosus, reflecting current hypotheses of
relationships among these species. Note also that while L. areolatus is
larger and has the longest hindlimb elements, HW and HL fall below
values for L. capito. Error bars denote one standard deviation from
the mean.
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Gopher Frog species, Crawfish Frogs have larger bodies and
larger hindlimb elements, Gopher Frogs have larger cranial
metrics (Figs. 2, 3, Table 1; Goin and Netting, 1940).
From the ratios of HW, HL, FEM, and TIBFIB divided by
SUL, three trends were apparent (Table 2). First, Pickerel
Frogs always exhibited different proportions than members
of the Gopher Frog/Crawfish Frog complex—Pickerel Frogs
have narrower heads and significantly longer relative
hindlimb lengths. Second, there were no significant differences in metrics between the two Gopher Frog species.
Third, Crawfish Frog metrics tend to be different from both
Pickerel Frogs and the two Gopher Frog species. Crawfish
Frogs have relatively narrower, shorter heads than both
Gopher Frogs species; in fact, Crawfish Frogs have the
relatively shortest heads of any species of Nenirana (Table 2).
In contrast, Crawfish Frogs have longer tibiofibulas than
Gopher Frogs (Table 2).
Ontogenetic trajectories and allometric growth.—Comparing
body proportions across body size (metric/SUL plotted
against SUL), Pickerel Frogs exhibit significant, strong
negative allometry in cranial measurements (HW/SUL and
HL/SUL; Table 3; Fig. 4A, B, respectively), and weaker, nonsignificant negative allometric shifts in hindlimb elements
(FEM/SUL and TIBFIB/SUL; Table 3; Fig. 4C, D, respectively).
There was substantial variation in hindlimb measurements
(not uncommon for amphibians in general, Shubin et al.,
1995; and this group in particular, Goin and Netting, 1940;
Bragg, 1953) that may have masked ontogenetic trends.
Dusky Gopher Frogs reversed the Pickerel Frog pattern.
Dusky Gopher Frogs exhibited no allometry (isometry) in
HW/SUL (Table 3; Fig. 4A), and weaker, but significant
negative allometry in HL/SUL (Table 3; Fig. 4B). They also
showed significant negative allometry in FEM/SUL (Table 3;
Fig. 4C), and a non-significant negative allometric shift in
TIBFIB/SUL measurements (Table 3; Fig. 4D). Gopher Frogs
resembled Dusky Gopher Frogs in exhibiting isometric HW/
SUL ratios (Table 3; Fig. 4A), and non-significant negative
allometry in TIBFIB/SUL ratios (Table 3; Fig. 4D). But
Gopher Frogs differed from Dusky Gopher Frogs in expressing non-significant negative allometry in FEM/SUL (Table 3;
Fig. 4C).
Ontogenetically, Crawfish Frogs expressed a mosaic of
trajectories of Nenirana and one clearly unique trait.
Crawfish Frogs resembled all species of Nenirana in
exhibiting significant negative allometry in HL/SUL (Table 3; Fig. 4B), but were the only species to exhibit
isometry in TIBFIB/SUL (Table 3; Fig. 4D). They resembled
Dusky Gopher Frogs in expressing significant negative
allometry in FEM/SUL (Table 3; Fig. 4C). The one singular
trait expressed by Crawfish Frogs is the presence of
significant positive allometry in HW/SUL (Table 3; Fig. 4A),
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Table 2. Mean Ratios of Morphometric Measurements Made on Specimens (Excluding Recently Metamorphosed Individuals) of the Four Species
Comprising the Nenirana Group. ANOVA was used to test for differences between means. Data were arcsine transformed before analysis, but true
ratios are shown in the table. Superscript letters indicate significant differences between species at the level of P # 0.01, where different letters
represent significant differences between species. Abbreviations: SUL = snout–urostyle length, HW = headwidth, HL = head length, FEM = femur
length, TIBFIB = tibiofibula length.
Species
L.
L.
L.
L.
HW/SUL
c
palustris
areolatus
capito
sevosus
0.353
0.373b
0.438a
0.438a
6
6
6
6
HL/SUL
b
0.014
0.026
0.028
0.025
0.315
0.296c
0.335a
0.334ab
a reversal of the presumably ancestral pattern exhibited by
Pickerel Frogs. The phenomenon, but not the reason, has
been noted before. Bragg (1953:280) wrote about Crawfish
Frogs: ‘‘the larger the size, the rounder the snout.’’ This
apparent snout rounding is due to a relative increase in
HW relative to HL.
There was large variation in all of the hindlimb metrics.
Both Goin and Netting (1940) and Bragg (1953) also noted
large variability in the proportional hindlimb metrics of
Crawfish and Gopher Frogs. About Crawfish Frog hindlimbs
Goin and Netting (1940:148) wrote: ‘‘The areolata ratios are
so variable that no generalizations . . . can be made until
much larger series can be measured.’’ Some of this variation
is due to geographic differences in size and proportions; it
also seems likely these animals are simply variable.
DISCUSSION
Phylogenetic relationships and morphological trends.—Our
findings for the Gopher Frog/Crawfish Frog complex
generally corroborate the results of Goin and Netting
(1940). While their absolute length values are longer than
ours, they were measuring entire limbs and heads, while we
were measuring limb and skull bones from radiographs;
both Goin and Netting’s (1940) and Bragg’s (1953) calculations of body ratios (HW/SUL, HL/SUL, and TIBFIB/SUL) are
gratifyingly consistent with our results. Further, our morphological analysis corroborates the current thinking about
6
6
6
6
FEM/SUL
b
0.018
0.022
0.019
0.026
0.480
0.412a
0.406a
0.425a
6
6
6
6
TIBFIB/SUL
0.536c
0.471b
0.437a
0.461ab
0.020
0.026
0.027
0.023
6
6
6
6
0.029
0.036
0.036
0.028
the relationships among the four species of Nenirana (Young
and Crother, 2001; Hillis and Wilcox, 2005; Fig. 1): adult
measurements and ontogenetic trends show that not only
are the two Gopher Frog species similar, together they are
more similar to Crawfish Frogs than to Pickerel Frogs. This
tendency for Crawfish Frogs to exhibit an intermediate adult
morphology within the subgenus Nenirana includes cranial
(HW and HL) measurements (Table 1; Figs. 2, 3) as well as
cranial (HW/SUL) and hindlimb (FEM/SUL and TIBFIB/SUL)
relationships (Table 2).
Using Pickerel Frogs as the outgroup to the Crawfish Frog/
Gopher Frog clade (Fig. 1), the ancestral condition includes
a strong negative allometry in cranial metrics (HW/SUL and
HL/SUL) and weak negative allometry (with considerable
variation) in hindlimb morphology (FEM/SUL and TIBFIB/
SUL; Table 3; Fig. 4). Both Dusky Gopher Frogs and Gopher
Frogs relax headwidth allometry (to isometry; Table 3;
Fig. 4A) and tighten hindlimb allometry (to become significantly negative, with Gopher Frog FEM/SUL being the
exception; Table 3; Fig. 4C).
Crawfish Frogs exhibit a curious mix of ancestral (Pickerel
Frog) traits, including significant negative allometry in HL/
SUL (Table 3; Fig. 4B) and isometry in TIBFIB/SUL (Table 3;
Fig. 4D). Crawfish Frogs also exhibit derived traits, including
negative allometry in FEM/SUL (Table 3; Fig. 4C). Crawfish
Frogs reverse the ancestral pattern of negative allometry in
HW/SUL to positive allometry (Table 3; Fig. 4A), an apomorphic trait within Nenirana. The positive allometry in
Table 3. Results of Analyses of Ontogenetic Relationships Examining Metric/SUL against SUL for the Four Species Comprising the Nenirana Group.
Asterisks indicate significance at the level P # 0.01.
Headwidth
Species
L.
L.
L.
L.
palustris
areolatus
capito
sevosus
Equation
y
y
y
y
5
5
5
5
Head length
P-value
0.4120.00(x)
0.34+0.00(x)
0.44+0.00(x)
0.4520.00(x)
P
P
P
P
#
#
5
5
0.01*
0.01*
0.70
0.97
r
2
0.34
0.10
0.01
0.00
Equation
y
y
y
y
5
5
5
5
0.4520.00(x)
0.3320.00(x)
0.4020.00(x)
0.4820.00(x)
Femur
Species
L.
L.
L.
L.
palustris
areolatus
capito
sevosus
Equation
y
y
y
y
5
5
5
5
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P
P
P
P
289
5
#
5
#
P
P
P
P
#
#
#
#
0.01*
0.01*
0.01*
0.01*
r2
0.69
0.10
0.29
0.64
Tibiofibula
P-value
0.5320.00(x)
0.4720.00(x)
0.4720.00(x)
0.5920.00(x)
P-value
0.14
0.01*
0.06
0.01*
r
2
0.06
0.11
0.12
0.71
Cust # CG-10-075R1
Equation
y
y
y
y
5
5
5
5
0.6020.00(x)
0.4920.00(x)
0.4920.00(x)
0.5520.00(x)
P-value
P
P
P
P
5
5
5
5
0.22
0.94
0.22
0.04
r2
0.04
0.00
0.05
0.26
290
Copeia 2011, No. 2
Fig. 4. Ontogenetic relationships of headwidth, head length, femur length, and tibiofibula length in the four members of the subgenus Nenirana.
Ratios given on the y-axis were arcsine transformed before analyses. Asterisks indicate significance at the 0.01 level.
HW/SUL exhibited by Crawfish Frogs supports the observation of Crawford et al. (2009) that post-metamorphic cranial
metrics increase at a faster rate in Crawfish Frogs than in
Southern Leopard Frogs (Lithobates sphenocephalus), which
likely grow in a negative allometric manner similar to
Pickerel Frogs.
To summarize, among Nenirana, Crawfish Frogs have
larger bodies (SUL), longer hindlimb elements (FEM,
TIBFIB), and proportionally blunter (shorter and wider)
snouts (HL, HW; Tables 1, 2). As postmetamorphic Crawfish
Frogs grow, their snouts get proportionately shorter and
wider, their femurs get proportionally shorter, and their
tibiofibulas remain the same relative length. Given that
Crawfish Frogs, alone among Nenirana, obligately occupy
deep burrows that are only slightly larger (bore) than their
bodies, we ask what are the possible influences of burrow
size on Crawfish Frog morphology?
Are elongation and blunt snouts tied to the occupancy of deep,
small-bore burrows?— Crawfish Frogs live most of their lives
in or around—within about 25 cm from the entrance to—
crayfish burrows (Hoffman et al., 2010). Crayfish burrows
are typically small bore and deep, vertically or obliquely
vertically oriented (Thompson, 1915; Heemeyer and Lannoo, 2010). Alone among the species of Nenirana, Crawfish
Frogs obligately occupy burrows that confine and constrain.
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When moving within crayfish burrows, Crawfish Frogs crawl
to ascend and probably back up to descend; there is usually
no available space to jump, although they will turn around.
Crawfish Frogs remain within their burrows throughout the
winter months, except when temperatures are above 4 or
5uC (Heemeyer, unpubl. data); during the summer when
burrows are flooded, frogs emerge to breathe every 30–
40 min (Heemeyer and Lannoo, 2010). Crawfish Frogs jump
into burrows when frightened; when there is less urgency
they crawl forward or back into them. Crawfish Frogs exit
burrows by crawling forward but may jump (lunge) out to
capture prey (Hoffman et al., 2010).
The question that interests us is whether the size and
shape of Crawfish Frogs can be explained by this habitation
of deep, small-bore burrows. Having now examined the
morphology of Crawfish Frogs, the answer is ambiguous. We
do not wish to fall into the trap of unnecessarily breaking
organisms into separate traits and proposing adaptive stories
for each considered separately (Gould and Lewontin, 1979;
Schwenk, 2001). So we begin by noting that the suite of
characteristics presented by Crawfish Frogs (larger bodies,
longer hindlimb elements, proportionally blunter snouts,
and with postmetamorphic growth relatively blunter snouts
and shorter femurs) does not derive simply from Pickerel
Frogs, or from the Pickerel Frog to Gopher Frog trajectory
(Fig. 1). That is, general historical pathways (Emerson, 1988)
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or a simple global shift in developmental trajectories (i.e.,
heterochrony; Gould, 1977; Alberch et al., 1979) cannot
explain the mosaic of morphological changes within the
species of Nenirana presented by Crawfish Frogs. Given this,
it is perhaps most useful to break Crawfish Frogs into unit
parts, and offer not just explanations based on deep, smallbore burrow dwelling (the approach that Gould and
Lewontin [1979] criticized), but give options based on what
we know about the functional morphological relationships
in these structures.
The classic vertebrate response to living in viscous
(including underground) media is elongation (Shine and
Wall, 2008). Among frogs, tadpoles will elongate under
these conditions, for example when living in small-volume
bromeliad tanks filled by the gelatinous remains of their egg
capsules (Lannoo et al., 1987). Tadpoles elongate their tails,
which are supported by cartilaginous vertebrae that resorb
and disappear during metamorphosis. Elongation in adult
frogs is more problematic; unlike salamanders (Duellman
and Trueb, 1986), or tadpoles for that matter, adult frogs are
constrained by the relatively few vertebrae they possess (8–
10 presacral vertebrae; Crawfish Frogs have eight). Crawfish
Frogs achieve elongation, however, by having large bodies
(Table 1; Fig. 3). However, being long and being large are
not the same. In one of the more memorable passages in all
of herpetological literature, Goin and Netting (1940:146)
wrote: ‘‘In general proportions a. areolata and sevosa are
quite similar; both have rounded bodies that are broadest
about midway between the fore and hind limbs, and both
have moderately heavy limbs. In contrast, capito is broadest
in the pectoral region and tapers rapidly to a distinct
‘Gibson Girl’ waist.’’ Our results do not suggest the
generality of this conclusion. Goin and Netting (1940)
examined a small number of Gopher Frogs and undoubtedly
their small sample size was biased in the morphological
direction of a ‘‘Gibson Girl.’’ Indeed, spent females have the
broad pectoral region and narrow waist characteristic of a
‘‘Gibson Girl.’’ Goin and Netting (1940) also suggested that
there was a latitudinal gradient to size in Crawfish
Frogs, with larger frogs being north. This may be more
generally true, and if so it would be interesting to compare
latitudinal gradients in crayfish size, and therefore burrow
diameter.
Most information on frog locomotion centers on jumping
(Barclay, 1946; Gans and Parsons, 1966; Zug, 1972; Calow
and Alexander, 1973). Emerson (1976) summarized this
literature by noting the best jumpers have long, extensible
hindlimbs with muscle mass concentrated proximally to
create lighter distal segments. Longer hindlimbs decrease
forces necessary to provide kinetic energy for the jump. In
addition, frog hindlimbs are positioned more anterior–
posteriorly than in most tetrapods. Gans and Parsons
(1966) note that this shift in orientation along with the
increased folding of the hindlimbs allows the limbs to move
in planes lying more nearly in parallel to the axis of motion
(for a description of the development of the pelvis to
achieve this morphology see Ročková and Roček, 2005). In
frogs, relative hindlimb length is tied to jumping ability
(Emerson, 1976:table 9), and by this criterion members of
the subgenus Nenirana should all be good jumpers, with
Pickerel Frogs being the best, followed by Crawfish Frogs,
followed by the two Gopher frog species (Tables 1, 2).
Indeed, Pickerel Frogs do jump well (often and far), but adult
Crawfish Frogs and the two Gopher Frog species have stout
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bodies (Fig. 2; Goin and Netting, 1940), and as adults none
of these three species are notable jumpers.
Digging in anurans has also been examined. Emerson
(1976), Sanders and Davis (1984), and Burton (2001)
detailed the morphological structure and mechanics of
classic fossorial (sensu Hildebrand, 1974) species. In contrast
to the long hindlimbs of jumpers, hindlimb diggers such as
Glyphoglossus molossus (Emerson, 1976) have foreshortened
hindlimbs, and in particular foreshortened tibiofibulas. We
note that none of the Nenirana have foreshortened tibiofibulas—in all four species tibiofibulas are longer than femurs
and in Crawfish Frogs tibiofibulas grow isometrically
(Tables 1, 2, 3; Fig. 4). Crawfish Frogs, as with all members
of Nenirana, do not have the hindlimb characteristics of
good diggers (but see Parris, 1989). Both adults and juveniles
will however, scrape the soil to dig shallow retreats when
burrows are unavailable (Fig. 5).
Snout morphology is known to be influenced by at least
two functional demands, prey size and head-first burrowing. Amphibians are gape-limited predators. That is,
amphibians swallow their prey whole, and the size of
their gape provides an upper limit to the size of prey they
can ingest (Zaret, 1980). Dundee and Rossman (1989:108)
refer to gape limitation in Crawfish Frogs when they tie
size of prey (anurans and insects) to headwidth. It may be
that blunt snouts play a role in underground habitation,
although, as previously noted, Crawfish Frogs do not dig
forward, nor do they exhibit the forelimb specialization
(Brown et al., 1972) or cervical flexibility of some forward
digging species (Emerson, 1976; Davies, 1984; Nomura et
al., 2009). Stout craniums may serve to clear surface
obstructions from burrows, for example following overwintering, to widen burrows with growth, or in defense
(when faced with threat, Crawfish Frogs dive into their
burrows, turn around to face the entrance [potential
predator], lower their heads, and inflate their bodies [Altig,
1974; Engbrecht and Heemeyer, 2010]). We acknowledge
these possibilities but hesitate to take this adaptationist
approach (sensu Gould and Lewontin, 1979) without
supporting evidence.
Summary and conclusions.—Crawfish Frogs are an ecomorphological paradox. They are large but not classically
elongate as might be expected of a burrow dweller. They
have long hindlimbs but are not great jumpers. Because they
have long hindlimbs, they are not built for backward
digging (although both Crawfish Frogs and Gopher Frogs
will dig shallow retreats in this way). They have blunt snouts
that get blunter with age, but are not headfirst burrowers.
They spend most of their lives in and around burrows, but
are not truly fossorial.
In trying to understand the morphology of Crawfish Frogs
it is important to distinguish between the ability to excavate
habitable primary burrows (true fossorial species; Hildebrand, 1974; Emerson, 1976; Parris, 1998) and the occupation of natural cavities or the co-opting of burrows of other
species, which generally characterizes Nenirana. It may be
that while the requirement of producing burrows exerts
substantial selective pressures on body shape, living in
burrows does not. This, despite the fact that no matter their
size, Crawfish Frogs tend to inhabit crayfish burrows that are
slightly larger (bore) than their bodies—the reason why
Crawfish Frog burrows are characteristically smooth walled
(Thompson, 1915; Heemeyer, unpubl. data). Further, a
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Fig. 5. (A) Top-down view of shallow scrape dug by female Crawfish Frog while migrating to her breeding wetland. Bare area is approximately 10 cm
3 8 cm. Frog is positioned under shallow cover immediately to the left of the scrape (indicated by ‘‘X’’). (B) Oblique view (from upper right to lower
left in photograph A) of Crawfish Frog under cover after digging in, animal is facing the scrape, eye is below and slightly to the right of the ‘‘X.’’ Depth
of scrape is ,4 cm. Photographs by J. Heemeyer.
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slightly larger-than-frog burrow size accommodates the two
in-burrow defensive mechanisms employed by Crawfish
Frogs—body inflation and head lowering (Altig, 1974;
Engbrecht and Heemeyer, 2010).
Our results suggest that if Crawfish Frog morphology is a
response to life in burrows, it is in part through having the
size characteristic of being the largest member of the clade,
and in part through the shape characteristic of generally
exhibiting an intermediate morphology between Pickerel
Frogs and the two Gopher Frog species. Further, Crawfish
Frogs are the only species within the subgenus Nenirana that
exhibit a significant positive allometric shift in headwidth,
reversing the ancestral trend.
The question we asked here was whether the deep, smallbore crayfish burrows used by Crawfish Frogs influence
Crawfish Frog morphology. Our analysis demonstrates
several unique aspects of Crawfish Frog morphology when
compared to other members of the subgenus Nenirana, but
these features do not tie neatly into known or predicted
functional/morphological cause-and-effect relationships associated with burrow occupancy. Perhaps the ranid body
plan is generalized enough to permit animals to inhabit,
despite being unable to dig, deep small-bore burrows
without undergoing major morphological changes. The
same conclusion—that form permits a range of behaviors,
all of them important in understanding the natural history
of a group of organisms—was reached by Cundall (2009) in
considering viper skull form.
MATERIAL EXAMINED
CAS-SU 2174–80; CM 5407, 13371–75, 13378, 18184–97,
69961, 69962; FMNH 121690, 21741, 21743, 26417, 48217–
20, 48222, 48227, 94321, 94323; UF 26, 2375–6, 35370–73,
64262, 66650–53, 87142, 99855–58, 103332–33, 111130,
111132; MCZ 7043, 7044; INSM 24, 25; ISU 2, 395–97, 399,
400, 449–52, 818, 937, 966, 1009, 1492, 1522, 1820, 1865,
2255, 2333, 2473, 2738, 2739-Ra7, 2739-Ra9, 2739-Ra10,
2739-Ra11, 2739-Ra12, 2739-Ra14, 2739-Ra15, 2783, 2822,
3204–07, 3248-Ra1, 3248-Ra2, 3644, 3665; PU 8482, 8483;
TCWC 66467; UMMZ 100304, 101623, 103361-1654,
103361-1655, 105544-1984, 108125-2337, 108125-2336,
110638-2568, 110638-2569, 118078. Seven additional specimens awaiting deposition in the Indiana State University
Vertebrate Collection were also examined.
ACKNOWLEDGMENTS
We dedicate this effort to the memory of Carl Gans. We
thank, and deeply appreciate the cooperation of, the
following scientists for loaning us specimens: R. Drewes, J.
Hanken, T. Hibbitts, K. Krysko, J. Losos, D. Lowe, M.
Nickerson, R. Nussbaum, A. Resetar, S. Rogers, G. Schneider,
R. Stoelting, and R. Williams. We thank J. Eastman for a
consultation on radiographic distortion. J. Heemeyer and V.
Kinney consulted on every aspect of this project; J.
Heemeyer assisted with the statistical analyses and provided
the photographs used in Fig. 5. D. Karns, J. Robb, P.
Williams, and A. Hoffman continually provide valuable
insights into the biology of Crawfish Frogs. We thank J.
Humphries for sharing his observations on Gopher Frog
burrowing, and all the participants in the 2010 SEPARC
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Workshop for sharing their insights into the biology of these
remarkable animals.
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