ArticlePDF Available

Reproductive Ecology of Rhinophrynus dorsalis (Anura: Rhinophrynidae) in México


Abstract and Figures

For this study, we examined a large sample of museum specimens to ascertain the reproductive ecology of Rhinophrynus dorsalis (Mexican Burrowing Toad) in México. Seasonal aboveground activity was highest during May to August, which tracks monthly rainfall patterns across the region. Contrary to previous assertions, mean body sizes were similar between males and females but females attained larger maximum sizes. Male testis size was largest in May, tadpoles appeared in June, and juveniles were present in July, indicating that most breeding begins in May following the first heavy rains of the year. Few specimens possessed food in their stomachs suggesting that aboveground activity may be more devoted to reproduction than to foraging. The timing of reproduction was variable because most gravid females were encountered during May to August, but some were also present in October and January. Clutch size was estimated to range from 630 to 7,700 eggs, which was positively correlated with female body size. Size to sexual maturity in both males and females was reached in 8–9 mo after metamorphosis and at much smaller minimum and average sizes than previously reported. Adult body size was negatively related to latitude, such that the largest specimens were from the most southern latitudes, especially for males. The reproductive ecology of R. dorsalis resembles distantly related burrowing anurans more so than their close aquatic relatives in Pipidae.
Content may be subject to copyright.
Journal of Herpetology, Vol. 55, No. 3, 298–309, 2021
Copyright 2021 Society for the Study of Amphibians and Reptiles
Reproductive Ecology of Rhinophrynus dorsalis (Anura: Rhinophrynidae) in Me´xico
Department of Biology, Coe College, 1220 1st Avenue NE, Cedar Rapids, Iowa, 52402, USA
Illinois Natural History Survey, University of Illinois, Urbana, Illinois, 61801, USA
ABSTRACT.—For this study, we examined a large sample of museum specimens to ascertain the reproductive ecology of Rhinophrynus
dorsalis (Mexican Burrowing Toad) in Me´xico. Seasonal aboveground activity was highest during May to August, which tracks monthly
rainfall patterns across the region. Contrary to previous assertions, mean body sizes were similar between males and females but females
attained larger maximum sizes. Male testis size was largest in May, tadpoles appeared in June, and juveniles were present in July,
indicating that most breeding begins in May following the first heavy rains of the year. Few specimens possessed food in their stomachs
suggesting that aboveground activity may be more devoted to reproduction than to foraging. The timing of reproduction was variable
because most gravid females were encountered during May to August, but some were also present in October and January. Clutch size
was estimated to range from 630 to 7,700 eggs, which was positively correlated with female body size. Size to sexual maturity in both
males and females was reached in 8–9 mo after metamorphosis and at much smaller minimum and average sizes than previously
reported. Adult body size was negatively related to latitude, such that the largest specimens were from the most southern latitudes,
especially for males. The reproductive ecology of R. dorsalis resembles distantly related burrowing anurans more so than their close
aquatic relatives in Pipidae.
General patterns of amphibian ecology and evolution can be
inferred from studies into the life history of individual species.
For example, descriptive studies of courtship have led to
theoretical advances in sexual selection (Ryan et al., 1990) and
social behavior (Wells, 1977). Furthermore, empirical experi-
ments with a single species (Resetarits and Wilbur, 1989) have
extended our understanding of the role that variable behaviors
play in the evolution of life history, such as oviposition site
choice (Resetarits, 1996). Data on life history strategies can be
analyzed in a phylogenetic context to elucidate evolutionary
patterns of reproductive diversity within a clade (Portik and
Blackburn, 2016) or to estimate the ecophysiological conditions
under which reproductive modes evolved globally (Lion et al.,
2019). Data derived from multiple populations on how
reproductive traits vary across geography have important
implications for predicting how species will respond to
environmental change (Blaustein et al., 2001) and for docu-
menting differential selection pressures within species popula-
tions (Miaud et al., 1999). Also, patterns gleaned from life
history investigations are increasingly recognized as indispens-
able to the development of ecologically relevant conservation
strategies (Crump, 2015). Life history has implications ranging
from evolutionary theory to conservation biology, yet we still
lack information on the reproductive ecology of several
widespread North American anurans. The need to fill this gap
in knowledge has been intensified by the rapid rate and severity
of recent amphibian declines (Cohen et al., 2019).
Rhinophrynus dorsalis Dume´ril and Bibron, 1841 (Mexican
Burrowing Toad or Sapo Borracho) is the sole extant member of
Rhinophrynidae, an ancient, monotypic anuran family origi-
nating in the late Jurassic period (Blackburn et al., 2019), that is
sister to the aquatic clawed frogs (Pipidae) from South America
and Africa (Frost, 2020). Rhinophrynus dorsalis is a distinctive
fossorial frog with a red orange middorsal stripe and irregular
yellow dorsolateral marks on a purple-to-black background
skin coloration (Fouquette, 1969, 2005). This species possesses a
particular suite of anatomical traits, including short legs, a
conical head, stout body, small eyes, loose skin, and the absence
of a tympanum, some features of which it superficially shares
with distantly related burrowing frogs in the families Brevici-
pitidae, Hemisotidae, and Myobatrachidae (Ford and Canna-
tella, 1993). Unique among anurans, however, is that R. dorsalis
exhibits a distinctive method of tongue protrusion that has been
posited to be an adaptation for subterranean feeding (Trueb and
Gans, 1983). This species is distributed from extreme southern
Texas (USA) along the coastal plain of the Caribbean versant
through Belize south to Nicaragua, and along the Pacific versant
from Guerrero (Me´xico) to Guatemala and Costa Rica (Camp-
bell, 1998; Savage, 2002; Santos-Barrera et al., 2010). Rhino-
phrynus dorsalis inhabits mesic to arid forests of coastal lowlands
from sea level up to 1,400 m elevation in areas that contain loose
soil (Eisermann, 2017). This burrowing species spends most of
its life underground (Fouquette, 2005) and is irregularly
encountered by collectors, usually after bouts of rainfall when
breeding aggregations form that sometimes last for just a few
days (Stuart, 1961). Sexual maturity is assumed to be reached at
body sizes ranging from 50 to 90 mm snout–vent length (SVL;
Dodd, 2013) with characteristic anuran sexual-size dimorphism
(SSD) where females are much larger than males (Savage, 2002).
Breeding occurs after heavy rains in roadside ditches, small
pools, and other ephemeral waterbodies, with one clutch size
estimate based on Costa Rican populations that ranges from
2,000 to 8,000 eggs (Foster and McDiarmid, 1983).
Rhinophrynus dorsalis possesses one of the most unique
combinations of traits among extant anurans, including a
specialized feeding apparatus (Trueb and Gans, 1983), indepen-
dently derived lack of tympanic middle ear (Pereyra et al.,
2016), prolonged aestivation (up to 2 yr: Fouquette and
Rossman, 1963), distinctive superficial mandibular musculature
(Tyler, 1974), and idiosyncratic cranial anatomy (Trueb and
Cannatella, 1982). Rhinophrynidae is allied to Pipidae (Canna-
tella, 2015); thus, any characteristics that it shares with fossorial
frog families, such as Nasikabatrachidae (Zachariah et al., 2012),
represent convergence. Rhinophrynus dorsalis has not received
much attention despite representing an early branching lineage
of Anura, and its potential contribution to the study of
convergent evolution. Available life history information for R.
Corresponding Author. E-mail:
DOI: 10.1670/20-035
Downloaded from by guest on 02 August 2021
dorsalis is limited to a few historical reports based on largely
isolated breeding events across its extensive distribution (e.g.,
Orton, 1943; Starrett, 1960; Stuart, 1961; James, 1966). Because
the reproductive ecology of R. dorsalis has not been examined in
detail, we set out to use museum specimens to investigate life
history variation in this species across Me´xico. Our densely
sampled data set provides insight into reproduction of the only
living member of an ancient anuran lineage and would not have
been possible without preserved specimens in natural history
We measured 437 cataloged specimens of R. dorsalis from
Me´xico housed in 6 museum collections: The University of
Illinois Museum of Natural History (UIMNH; n=200) and the
Illinois Natural History Survey (INHS; n=5), Champaign,
Illinois; the Museum of Vertebrate Zoology (MVZ; n=39),
Berkeley, California; the California Academy of Sciences (CAS; n
=99), San Francisco, California; the Field Museum of Natural
History (FMNH; n=43), Chicago, Illinois; and the Carnegie
Museum of Natural History (CM; n=51), Pittsburgh,
Pennsylvania (Appendix 1). The specimens were collected
across 59 yr (1919–1978) from 8 states within the species’ range
in Me´xico (Fig. 1). We generated histograms using months as
bins to compare seasonality in the number of specimen records
of this data set with all R. dorsalis specimens from Me´xico on
VertNet ( and all Research Grade observations
of R. dorsalis from Me´xico on iNaturalist (
We measured body size in snout–vent length (SVL) of all
specimens to the nearest 0.01 mm using hand calipers. We
distinguished recently metamorphosed frogs from tadpoles by
the presence of forelimbs (Gosner stage 42), and from juveniles
by the presence of a tail (Gosner stage 45; Gosner, 1960). We
relied on direct examination of the gonads to assess sex because
R. dorsalis does not exhibit the typical secondary sexual
characteristics used to assign sex in adult frogs. For example,
R. dorsalis lacks an external eardrum (tympanum), males lack
enlarged (or cornified) thumb pads, and males lack external
vocal sacs. The presence of enlarged (swollen) testes in
combination with a larger body size was used to determine
sexual maturity in males. We measured length and mid-width
of the left testis from mature male specimens and estimated
male fertility by calculating testis dimensions as a percentage of
male SVL (Meshaka, 2001). To reduce some of the potential
errors derived from preservation artefacts, all reproductive
organs of male specimens were measured from the left side of
the body (Lee, 1982).
We assigned maturity in females based on the following 4
ovarian stages: 1) oviducts were thin and uncoiled, and the
ovaries were somewhat opaque; 2) oviducts were larger and
more coiled, and the ovaries contained some pigmented
oocytes; 3) oviducts were thick and heavily coiled, and the
ovaries were in various stages of clutch development; and 4)
oviducts were thick and heavily coiled, and the ovaries were full
of polarized ova with few nonpolarized ova, which we used as
evidence of a mature clutch and gravid female (Meshaka, 2001).
We estimated sexual size dimorphism (SSD) using the Lovich
and Gibbons (1992) index by dividing the mean adult SVL of the
larger sex (females) by the mean adult SVL of the smaller sex
(males) and then subtracting 1. When the sexes are equal in size,
SSD =0; when males are larger, SSD <0, and SSD >0 when
females are larger. We used this estimate of SSD to examine
geographic variation because this index is statistically optimal
among available dimorphism indices (Smith, 1999).
We examined metabolic tradeoffs temporally between repro-
duction, feeding, and energy storage by calculating the monthly
incidence of developed fat bodies, large liver sizes, and
reproductive status (Lu et al., 2008). We assessed the extent of
lipid deposits associated with gonads (i.e., fat bodies) in the
body cavity of specimens based on 3 scores: 1) trace amounts or
no fat bodies; 2) an intermediate volume of fat bodies; and 3) a
high volume of fat bodies that extend anteriorly within the body
cavity (Meshaka, 2001). We used the highest score as an estimate
of the monthly incidence of extensive fat bodies relative to all
males and females examined in each month. We recorded the
number of individuals of each sex with food in the stomach or
an obvious food item in the upper intestines as a proxy for the
monthly frequency of individuals that had been feeding in each
month. We also examined the extent of liver development into
the visible posterior section of the body cavity based on a
scoring system: 1) the liver had few lobes that occupied up to
30% of the body cavity; 2) the liver had several large lobes that
occupied from 31% to 75% of the body cavity; and 3) the liver
had many large lobes that extended posteriorly into the inguinal
region to occupy 76% to 100% of the body cavity. It has been
shown that liver mass in museum specimens is representative of
livers from freshly collected animals (Withers and Hillman,
2001). We used the highest liver score to estimate the monthly
incidence of well-developed livers relative to all males and
females examined in each month because the liver plays an
important role in energy storage, especially for species that
aestivate for long periods (Mentino et al., 2017).
We used 12 randomly selected gravid females (ovarian stage
4) to examine clutch characteristics. We dissected the clutch out
of the body cavity, gently removed excess moisture with a paper
towel, and weighed the entire clutch to the nearest 0.01 g with
an electronic scale. We weighed a subset of mature ova from
each clutch and then counted the number of individual eggs in
the subset. We extrapolated the mass of the counted subset of
eggs to the weight of the entire brood to provide an estimate of
clutch size (Giesing et al., 2011). We then weighed the female
specimen with the clutch removed to generate estimates of
relative clutch mass as per Shine (1980). We measured the
diameters of 10 randomly chosen ova from each of the clutches
using an ocular micrometer to the nearest 0.01 mm and used the
largest ovum from each clutch to compare with clutch size and
female body size.
The Me´xico state base map was obtained from
and redrawn in Adobe Illustrator (Adobe Systems Inc., San Jose,
California, USA). The photo of R. dorsalis was provided with
permission by M. Pingleton. We used Excel 2016 (Microsoft Inc.,
Redmond, Washington, USA) and Program R version 4.0.3 (R
Core Team, 2020) to organize data, conduct statistical analyses,
and to generate quantitative graphics using the R package
ggplot2 (Wickham, 2016). We present mean measurements
followed by 61 standard deviation (SD). We checked for
normality of data using Shapiro–Wilk tests, compared means
between samples using 2-sample t-tests, compared variances
with analysis of variance (ANOVA) F-tests and Levene’s tests,
and examined relationships between selected variables with
Pearson’s correlation coefficients. We recognized statistical
significance at P<0.05.
We wish to note that several specimens in our sample had
various levels of damage to their anatomy, had been previously
skeletonized, or had entire organ systems removed prior to our
Downloaded from by guest on 02 August 2021
study, so not all measurements were extracted from all
specimens. Likewise, some records were incomplete as a result
of nonsystematic data collection: 4.1% of specimens in our
sample did not have any data on the month of their collection.
Furthermore, a handful of specimens were cataloged under a
single museum tag, such as large lots of tadpoles (e.g., 68
tadpoles cataloged as FMNH 191918). We chose to include data
in relevant analyses and summary statistics from all specimens,
including damaged specimens that still possessed interpretable
characters or those that lacked specific collecting data, such as
fat development when body size was unmeasurable or body
size when collecting month was not recorded or seasonal
activity when the specific locality was unavailable. Consequent-
ly, these inclusions influenced sample sizes across various
categories of our analysis. The data underpinning these analyses
are available from the authors upon request.
Monthly Frequency of Records.—From VertNet collection records
that span 148 yr (1857–2005) representing 724 specimens of R.
dorsalis from Me´xico, we found that specimens were collected in
every month of the year, with distinct peaks in June (n=197) and
July (n=201), and fewer than 10 individuals in 4 separate
months: February (n=3), October (n=4), November (n=3),
and December (n=4; Fig. 2A). The sample of 437 cataloged
specimens we examined generally reflected these same seasonal
patterns (Fig. 2B). In our sample, specimens were collected
during every month except February and December; only one
was collected in October (FMNH 105709), and just two in March
(UIMNH 37223 and UIMNH 47873). The interval with the
greatest incidence of captured individuals in our sample occurred
during May–September, with an apparent peak in late summer
(July–August). Monthly frequency of captures suggests activity
peaks for different classes: males were captured most frequently
in May, females from May to July, tadpoles in July, and juveniles
in August (Fig. 2B). From community science observations on
iNaturalist that span 16 yr (2004–2020) representing 158 Research
Grade observations, we found that observations occurred in
every month, with distinct peaks in June (n=30) and July (n=
35), and fewer than 5 records in 2 separate months: February (n=
3) and December (n=2 Fig. 2C). Taken together, the records from
VertNet and iNaturalist corroborate the paucity of individuals in
our sample that were collected in months outside of late-spring
and summer, especially during September–April (Fig. 2).
Body Sizes.—The variance in body sizes (SVL) between males
(variance =78.61) and females (variance =143.69) was not equal
(Levene’s test, F
=8.15, P=0.005). The mean SVL of adult
males (48.94 68.87 mm, range =30.6–71.47 mm, n=118) was
not significantly different from that of adult females (48.57 6
11.99 mm, range =34.57–77.11 mm, n=40; 2-sample t-test with
unequal variances, t
=-0.19, P=0.85; Fig. 3). The mean SVL of
266 juveniles was 17.65 62.79 mm (range =13–23.25 mm). The
mean total length of 62 tadpoles was 33.23 64.88 mm (range =
17.12–41.84 mm; body size 14.46 64.97 mm [range =7.41–18.66
mm]; tail length: 18.77 62.97 mm [range =9.71–23.55 mm]). The
FIG. 1. Geographic origin of museum specimens in Me´xico of the Mexican Burrowing Toad (Rhinophrynus dorsalis) examined in this study. Sample
sizes are given in parentheses after the Mexican state. Bottom left: Picture of R. dorsalis by M. Pingleton with permission.
Downloaded from by guest on 02 August 2021
mean SVL for 2 specimens that had 4 legs and a tail was 14.34 6
0.19 mm (range =14.20–14.47 mm). The SSD between adult
females and adult males was marginally negative (-0.008),
indicating that the mean body sizes of the specimens were
essentially equal.
Test i c ula r C ycl e .—Mean testis length as a percentage of SVL
was 11.95 62.38% (range =7.12–18.1%, n=107) and testis
width was 5.66 61.01% (range =3.57–8.6%, n=107). A seasonal
change in testis dimensions was evident in our sample (ANOVA:
testis length, F
=16.92, P<0.001; testis width, F
=4.24, P
=0.003). Seasonal testis dimensions exhibited the greatest mean
length and width in May, followed by a rapid drop in June, and
then relatively stable mean values through September, with the
lowest mean length in July and lowest mean width in September
(Fig. 4).
Fat Deposits, Food Presence, Liver Size, and Reproduction.—In
general, males with food and extensive fat did not make up the
majority (>50%) of specimens in any given month except for
those with abundant fat bodies in May and August and food
presence in September (Fig. 5A). The monthly percentage of
males with extensive fat deposits was lowest during June (35%)
and July (16%), and rapidly increased to a peak in August (71%).
The monthly percentage of males containing food was lowest in
August (14%) and highest in September (67%). Females, likewise,
exhibited low percentages (50%) of specimens containing
extensive fat and food in all months except for fat deposits in
May (Fig. 5B). The monthly percentage of females with extensive
fat development was highest in May (55%) and lowest in January,
April, July, and August (all at 0%). The monthly percentage of
females containing food was lowest in August (0%) and highest
in January, July, and September (all at 50%). Large liver sizes were
generally more common among males than females, ranging
from 13% in July to 50% in March. For females, large liver sizes
were present in January (100%), May (13%), and June (17%).
Fewer than 10% of ovarian stage 1 females had extensive fat
deposits and none had well-developed livers (Fig. 5C). Females
in ovarian stages 2 and 3 exhibited the highest frequency of
food, but none of them exhibited extensive fat bodies. Large
livers were detected at similar frequencies among females in
ovarian stages 2, 3, and 4. The relatively higher percentage of
food in the stomachs of stage 2 and 3 females, and a
corresponding lack of extensive coelomic fat, indicates that
feeding is more pronounced during these stages of clutch
FIG. 2. Monthly incidence of Mexican Burrowing Toads
(Rhinophrynus dorsalis) captures from Me´xico based on museum
specimens and community science observations. (A) All specimen
records available on VertNet that possessed month of capture data. (B)
Specimens examined in this study separated by sex and life stage, which
included 495 individual tadpoles (June and July) collected as lots
cataloged under single specimen tags, and a series of 48 juveniles
(November) cataloged in the same manner. Monthly rainfall (mean 6
standard error) displayed on the third axis. Precipitation values were
taken from the Mexican states where 90% of our specimens were
collected (Guerrero, Veracruz, Tabasco, and Chiapas). (C) All Research
Grade observations (i.e., verified by an independent observer) recorded
as on iNaturalist.
FIG. 3. Body size distributions of female and male Mexican
Burrowing Toads (Rhinophrynus dorsalis) from Me´xico. Violin plots
representing body sizes for all males and females in our sample. Sample
sizes are presented above each plot. Dashed line indicates the sample
mean. Filled circles represent gravid females (ovarian stage 4).
Downloaded from by guest on 02 August 2021
development. The amount of ovarian stage 4 females with
extensive fat suggests an increase of lipid stores prior to
oviposition, which is corroborated by the high proportion of
females with fat during the primary egg-laying season (May–
June). The frequency of ovarian stage 1 females containing food
was lowest (22%), followed by stage 4 (23%), stage 3 (33%), and
stage 2 (50%).
Ovarian Cycle.—Gravid females (ovarian stage 4) were detected
from May to August and in October and January (Fig. 6). The
most gravid females, as the proportion of all specimens collected
in a month, were found during May (78%) and June (83%), with
the fewest in April (0%) and September (0%). The months with
the lowest frequency of stage 4 females also exhibited the greatest
frequency of stage 1 females (100% in both April and September).
It is difficult to assess the ovarian cycle from the late autumn
through spring because no specimens in our sample were
collected in November, December, February, or March, but it
appears that reproduction can occur in October and January. The
time period with the most specimens (April to September)
indicates that oviposition starts in May and generally is finished
by August. To that end, all the tadpoles in our sample were
collected from late June to mid-August: 26 June 1957 from
Oaxaca (FMNH 121012); 3 July 1965 from Veracruz (INHS 30749);
7 July 1970 from Oaxaca (MVZ 92710; FMNH 171576, 191917
18); and 14 August 1955 from Veracruz (UIMNH 73482).
Clutch and Egg Size.—The clutch size, body size, and weight of
gravid females were normally distributed (Shapiro–Wilk, W=
0.89–0.97, P=0.12–0.87). From 12 gravid females (mean SVL =
55.64 612.78 mm, range =34.57–77.11 mm; mean weight =
26.01 615.81 g, range =8.2–56.7 g), mean clutch size was
estimated at 3,134.9 62,326 eggs (range =630–7,700 eggs).
Clutch size was positively correlated with SVL (Pearson
correlation, t
=7.23, R=0.92 [0.72–0.98 95% CI], P<0.001)
and specimen weight (Pearson correlation, t
=22.54, R=0.99
[0.97–0.99 95% CI], P<0.001; Fig. 7). Clutch mass increased
FIG. 4. Monthly distribution of testis length and width as a
percentage of male body size in 107 Mexican Burrowing Toads
(Rhinophrynus dorsalis) from Me´xico. Points are jittered for visual
clarity between overlapping values.
FIG. 5. Monthly frequency of food presence in the stomach, extensive
fat in the body cavity, and well-developed livers in the Mexican
Burrowing Toad (Rhinophrynus dorsalis) from Me´xico by male (A),
female (B), and ovarian stage (C). Asterisks (*) next to a month indicate
that no specimens were available for examination.
Downloaded from by guest on 02 August 2021
significantly with increasing SVL (Pearson correlation, t
R=0.94 [0.78–0.98 95% CI], P<0.001). The relative clutch mass
of these 12 female specimens was 32.3 66.57% (range =20.18–
41.67%) and was positively related to both SVL (Pearson
correlation, t
=3.4, R=0.73 [0.27–0.92 95% CI], P=0.007)
and body weight (Pearson correlation, t
=3.26, R=0.72 [0.25–
0.92 95% CI], P=0.009). The mean diameter of 120 measured ova
from the same 12 gravid females was 1.7 60.19 mm (range =
1.07–2.44 mm). Mean and maximum ovum sizes were not
correlated with body size (R=0.31–0.38, P=0.22–0.33), clutch
size (R=0.06–0.15, P=0.64–0.86), or specimen weight (R=0.11–
0.2, P=0.53–0.74).
Growth and Sexual Maturity.—Seasonally, the first tadpoles were
collected on 26 June 1957 from Oaxaca (FMNH 121012) and the
last on 14 August 1955 from Veracruz (UIMNH 73482), with the
most collected in July (n=489; Fig. 2). The earliest seasonal
juvenile record was a single individual (SVL =25.27 mm)
collected on 17 January 1978 in Guerrero (CAS 150150), and the
last was a series of 48 juveniles (SVL range =14.24–19.01 mm)
collected on 2 November 1963 in Tabasco (CM 38925). During the
most densely sampled monthly period (April–September), the
first record of juveniles (SVL range =14.57–18.21 mm) was a
series (n=33) collected on 24 July 1974 (MVZ 112268–11230), and
the last (SVL range =13–17.59 mm) was a large series (n=92)
collected on 14 August 1955 in Veracruz (UIMNH 73390–73481;
Fig. 8).
The smallest adult male (SVL =30.6 mm) collected on 20 July
1963 in Tabasco (UIMNH 62718) appeared to be sexually mature
based on enlarged testes that were 8.82% the length of its body
size. The smallest gravid female (stage 4) was 34.57 mm in SVL
and collected on 1 July 1963 in Tamaulipas (UIMNH 64652), the
smallest ovarian stage 3 female was 36.94 mm in SVL and
collected on 20 July 1963 in Tabasco (UIMNH 62720), the
smallest ovarian stage 2 female was 34.44 mm in SVL and
FIG. 6. Monthly ovarian cycle of female Mexican Burrowing Toads
(Rhinophrynus dorsalis) from Me´xico. See text for details on reproductive
FIG. 7. The relationship between clutch size and body size in 12
female Mexican Burrowing Toads (Rhinophrynus dorsalis) from Me´xico.
Grey shading indicates the 95% confidence interval. The equation for the
line: y =-6,100 +170x. Silhouettes modified from Eisermann (2017)
and drawn to scale relative to each other.
FIG. 8. Monthly distribution of body sizes for 36 females, 107 males,
and 266 juveniles of the Mexican Burrowing Toad (Rhinophrynus dorsalis)
from Me´xico. Points are jittered for visual clarity between overlapping
Downloaded from by guest on 02 August 2021
collected on 20 July 1963 in Tabasco (UIMNH 62717), and the
smallest ovarian stage 1 female was 29.45 mm in SVL and
collected on 15 April 1959 in Tabasco (UIMNH 47874). It is
unclear whether the smallest ovarian stage 1 females were still
maturing with egg laying to occur at larger sizes. Given that the
smallest ovarian stage 4 female was <5 mm larger in SVL than
the smallest ovarian stage 1 female, it is feasible that maturity
and egg laying could have occurred at body sizes between 29
mm and 34 mm.
The mean SVL of ovarian stage 1 females was 39.74 69.19
mm (range =29.45–66.11 mm, n=20), for ovarian stage 2
females it was 50.89 612.03 mm (range =34.44–62.41 mm, n=
4), for ovarian stage 3 females it was 42.42 67.58 mm (range =
36.94–56.57 mm, n=6), and for ovarian stage 4 females it was
55.49 612.03 mm (range =34.57–77.11 mm, n=16). Mean body
size of gravid females (stage 4) was significantly larger than that
of all other ovarian stages (nongravid female stages 1–3 [41.76 6
9.73 mm, range =36.66–66.11 mm, n=30; t
=3.93, P<0.001).
Based on the seasonal distribution of body sizes and
specimen occurrences, tadpole transformation time was ap-
proximately 2 mo (Figs. 2, 7). Males and females could have
reached their minimum body size at sexual maturity (males =
30.6 mm, females =34.57 mm) within 8–9 mo after metamor-
phosis and mean adult body size (males =48.9 mm; females =
48.6 mm) approximately 12 mo postmetamorphic age.
Geographic Variation in Adult Body Size.—From the Mexican
states that had adult specimens of both sexes, we selected those
that had 5 adult females and 5 adult males to compare mean
body sizes across geography, which resulted in 4 state
comparisons. We found that the mean SVL of adult males was
not significantly different from that of adult females in Chiapas
=0.98, P=0.34), Oaxaca (t
=-1.96, P=0.07), Tabasco (t
=-1.08, P=0.30), or Veracruz (t
=1.18, P=0.30; Fig. 9).
Body size as SVL was negatively associated with latitude,
with individuals from higher latitudes exhibiting smaller body
sizes than those from lower latitudes (Pearson correlation, t
-2.7, R=-0.21 [-0.06 to -0.35 95% CI], P=0.008; Fig. 10).
This latitudinal trend persisted when analyzing males separate-
ly (Pearson correlation, t
=-3.04, R=-0.27 [-0.10 to -0.43
95% CI], P=0.003) but disappeared in an analysis of females
only (Pearson correlation, t
=-0.46, R=-0.07 [-0.36–0.23
95% CI], P=0.65). Adult body size showed no linear
relationship to longitude (Pearson correlation, t
=0.42, R=
0.03 [-0.12–0.19 95% CI], P=0.68).
To further examine geographic variation in SSD, we grouped
adult specimens by the degree of latitude or longitude of their
collection (e.g., all male and female specimens from latitude
158N) that had 2 males and 2 females to calculate a mean SVL
for each sex, which resulted in SSD estimates across 7 latitudinal
degrees and 5 longitudinal degrees. We found that SSD was not
significantly related to latitude (Pearson correlation, t
=-2.2, R
=-0.7 [0.11 to -0.95 95% CI], P=0.08) or longitude (Pearson
correlation, t
=0.94, R=0.47 [-0.7–0.96 95% CI], P=0.42).
We used a robust sample of museum specimens from Me´ xico
to provide empirical data on several life history traits for R.
FIG. 9. Violin plots representing body sizes for males and females
Mexican Burrowing Toads (Rhinophrynus dorsalis) across the 4 Mexican
states that had 5 males and 5 females. Sample sizes are presented
above each plot. FIG. 10. The relationship between body size and latitude in the
Mexican Burrowing Toad (Rhinophrynus dorsalis)fromMe´xico (n=163).
Grey shading indicates the 95% confidence interval. The equation for the
line: y =65.2 -0.95x.
Downloaded from by guest on 02 August 2021
dorsalis that complement and, in some cases, extend previous
findings. First, we wish to highlight general biases unique to
studies based on museum collections that should be considered
when interpreting their results (Robertson, 2008; Boakes et al.,
2010; Wehi et al., 2012). Nondeliberate sex biases in vertebrate
collections tend to be skewed toward males because they are
often the more easily captured sex. In some animal groups, such
as frogs, males exhibit a greater frequency of movements, more
conspicuous visual displays, and audible calling to attract mates
(Cooper et al., 2019). Breeding aggregations of R. dorsalis consist
of mostly males, which conspicuously vocalize to attract
females (Savage, 2002; Dodd, 2013), and we note that our
sample contained over twice as many adult males (n=124) as
adult females (n=51). Moreover, collectors’ objectives vary
through time, are dependent upon permits that differ across
political boundaries, and generally follow assessments of
species in need. Rhinophrynus dorsalis has not been in decline
(International Union for Conservation of Nature Least Concern;
Santos-Barrera et al., 2010) and thus was likely not a collecting
priority during the well-documented declines of other Mexican
anurans (e.g., Lips et al., 2004). We note that all the specimens in
our sample were collected before 1980. Geographical biases are
also widespread among museum collections such that the
location and intensity of collecting are influenced by accessibil-
ity and species-specific differences in detectability (Reddy and
Da´valos, 2003). Rhinophrynus dorsalis spends most of its life
underground (Fouquette, 1969), rendering it difficult to target
for collecting relative to surface-dwelling anurans. We attempt-
ed to address biases in museum collections by 1) focusing our
study on a single political entity (Me´xico) to avoid changes in
specimen collecting policies between nations; 2) examining a
sample of specimens collected across decades and from multiple
museums to minimize the impact of individual collector biases;
and 3) including the largest sample of this species to date to
generate a significantly robust biological signal to overcome
these issues and even out potential collecting imbalances.
The literature on the reproductive biology for this species is
based on a handful of primary data sources (Orton, 1943;
Starrett, 1960; Stuart, 1961; Fouquette and Rossman, 1963;
James, 1966; Nelson and Nickerson, 1966; Foster and McDiar-
mid, 1983; Sandoval et al., 2015; Stynoski and Sasa, 2018), which
have been repeated verbatim, or with little added information,
in regional synoptic guides (e.g., Lee, 1996; Campbell, 1998;
Savage, 2002; Fouquette, 2005; Ko¨ hler, 2011; Dodd, 2013; Lemos-
Espinal and Dixon, 2013; Lemos-Espinal et al., 2018). Most
sources report that this species exhibits dramatic sexual size
dimorphism (SSD) with much larger females than males (e.g.,
Fouquette, 1969). The degree of SSD in our sample was
negligible between the mean adult body sizes of males and
females, but there was evidence that females can attain larger
maximum adult body sizes than males. The largest specimen we
examined was a gravid female (SVL =77.1 mm) from Veracruz
(UIMNH 42654) and the largest male specimens (two at SVL =
71.5 mm) were from Chiapas (UIMNH 33585 and INHS 6572).
The largest size record based on a physical specimen was 88 mm
SVL for a female recorded by Nelson and Nickerson (1966) from
Guatemala (MCZ A-2312). From Costa Rica, Savage (2002)
reported an adult SVL range of 50–89 mm, with females
reaching 89 mm and males only 75 mm, but there was not a
clear basis for these measurements. Fouquette (1969) reported
that adults reach sexual maturity at 60–65 mm SVL and that
overall adult range is likely to be 50–88 mm, with females larger
than males, which was echoed by Foster and McDiarmid (1983).
From the Mexican states of San Luis Potosı´ and Nuevo Le ´
Lemos-Espinal et al. (2018; Lemos-Espinal and Dixon, 2013)
reported that the maximum SVL of females is 88 mm and that
adult males averaged 60–65 mm, values that were likely derived
from Fouquette (1969). From the Yucata´ n Peninsula, Lee (1996)
reported an adult SVL range of 60–65 mm SVL, and that females
are substantially larger than males. Campbell (1998) reported
from northern Guatemala, the Yucata´ n, and Belize, that males
reach 65–75 mm in SVL and females 70–80 mm in SVL, but no
reference material was mentioned for these size ranges. Despite
seemingly widely repeated values for body sizes at maturity,
few accounts referred to measurements from specimens or
referenced wild individuals. From a recent account based on a
single breeding night in Costa Rica, Sandoval et al. (2015) found
that the mean body size of females (SVL =81 mm, n=15) was
larger than that of males (SVL =72.1 mm, n=21), and that
larger females were amplexed by larger males. It seems that the
SSD in this species may be less extreme than previous reports
have indicated because most accounts echoed values from Costa
Rica (Savage, 2002) or Guatemala (Nelson and Nickerson, 1966).
Nevertheless, females can exhibit larger maximum body sizes
than males, and the SSD at a specific breeding site (e.g.,
Sandoval et al., 2015) is likely to be more prominent than when
generalizing across its range. We suggest that the SSD in R.
dorsalis may be most evident at tropical latitudes because body
sizes were largest at the lowest latitudes in our sample and in
the literature. However, this geographic pattern in body size
was driven by a sex effect on the slope of the latitudinal cline,
where the slope in males was steeper than that in females, such
that males were smallest at northern latitudes and larger further
south, whereas female body size did not change much across
From Costa Rica, Foster and McDiarmid (1983) reported the
only clutch size estimate for this species (range =2,000–8,000
eggs), which was repeated by Campbell (1998), Savage (2002),
and Ko¨hler (2011). We found that the clutch size range in Me´xico
(630–7,700 eggs) conforms to the upper limit of this previous
report but extends the lower estimate well below 2,000 eggs. In
fact, we found 5 females with body sizes smaller than the mean
of our sample (48.6 mm SVL) that were gravid, and these
specimens had an average clutch size of 1,206 eggs (range 630–
1,617 eggs). The smallest gravid female in our sample (SVL =
34.6 mm) was from Tamaulipas, indicating that either this
species reaches sexual maturity at a much smaller body size in
northern Me´xico than reported elsewhere or that the females
south of Me´xico, from where most of the data in the literature
originated, mature at larger body sizes. To that end, we found
that adult body size in our sample was negatively related to
latitude with larger specimens originating from southern
locations. The largest specimen-backed body size for this
species was recorded from Guatemala (Nelson and Nickerson,
1966), and all reports from south of Me´xico suggest that both
sexes mature at larger body sizes than those we found (e.g.,
Foster and McDiarmid, 1983; Campbell, 1998; Savage, 2002;
Sandoval et al., 2015). It remains unclear whether there is
significant geographic variation in clutch size, and if so,
whether it follows the observed latitudinal variation in body
In our sample, R. dorsalis was most frequently captured in late
spring and summer, with very few records in autumn and
winter. Additional specimen records from VertNet and com-
munity science observations from iNaturalist independently
corroborated that R. dorsalis is active year-round in Me´xico and
Downloaded from by guest on 02 August 2021
that activity is most pronounced from May to August and
lowest from September to April. We detected most gravid
females from May to August, most tadpoles from June to
August, and most juveniles during July and August, indicating
that breeding generally begins in May after the first major
rainfall and likely ceases by September. Males were also most
common in May and their testis size was likewise largest in May
and was much smaller in specimens collected during all other
months. Nevertheless, we also found small juveniles in
November and January, and gravid females in January and
October, indicating that the timing of reproduction can be
variable across its range. In Guerrero, Fouquette and Rossman
(1963) collected a series of specimens during breeding aggrega-
tions that formed shortly after a storm on 19 July 1960. From the
Yucata´ n Peninsula, Lee (1996) found tadpoles (Gosner stage 25;
Gosner, 1960) in early October and suggested that reproduction
may also occur later in the rainy season. In Nuevo Le ´
on, Lemos-
Espinal et al. (2018) suggested that this species will call and
mate at any time during the year because of the unpredictability
of rain and that tadpole development ranges from 1 to 3 mo.
From Texas (USA), Fouquette (2005) also reported that this
species will breed at any time of the year given adequate rainfall
and that tadpoles take 2 mo to develop. From Guatemala,
Stuart (1961) found tadpoles (mean body length =18 mm) on 7
July that were at least 7-wk from the time of egg deposition,
which was presumed to follow a heavy rainfall on 20 May, and
that all tadpoles were metamorphosed by 17 August after
reaching a maximum body size of 25 mm. Campbell (1998)
reported that breeding occurs from June to September in Pete´n,
Guatemala, perhaps based on Stuart (1961). From Costa Rica,
Foster and McDiarmid (1983) reported that the populations
breed once in late May or early June, and that all the tadpoles
will have metamorphosed by the latter part of July and will
disperse synchronously from wetlands.
Fecundity characteristics are poorly characterized among
most fossorial anurans, but for those species with data, most
tend to reach sexual maturity rapidly, invest a significant
amount of their body weight to reproduction, and have short
lifespans (Sullivan and Fernandez, 1999). Our findings on
relative clutch mass (RCM) in R. dorsalis (range =20–42%) are
similar to those reported for other fossorial species (Sze´kely et
al., 2018), but at the higher end of the range for anurans in
general (Kuramoto, 1978). Measurements from fresh R. dorsalis
would likely exhibit higher RCMs because long-term preserva-
tion in ethanol undoubtedly reduced the weight measurements
in our museum specimens (Deichmann et al., 2009). From a
Neotropical frog community consisting of 16 species, RCMs
ranged from 5.5% to 18% with a semifossorial species (Micro-
hylidae: Elachistocleis bicolor) exhibiting the highest RCM values
(Prado and Haddad, 2005). In a separate study on E. bicolor from
Uruguay, Elgue and Maneyro (2017) found that the largest
females produced the largest clutches, but RCM did not increase
with increasing body size. In Dermatonotus muelleri (66.1–81.9
mm SVL), a fossorial microhylid from the Gran Chaco region in
Argentina, RCM averaged 30.2% and was negatively related to
SVL, with larger individuals investing less in reproduction in
terms of clutch mass (St ˘
anescu et al., 2016). Two small
Australian frogs that differ in their habits have some of the
highest reported RCM values: an arboreal species (Pelodryadi-
dae: Litoria dentata) exhibited an RCM range of 34–63% (SVL
range =38–46 mm), and RCM did not increase with increasing
SVL (Greer and Mills, 1998); and a terrestrial species (Myoba-
trachidae: Crinia signifera) exhibited an RCM range of 11–68%
(SVL range =19–27 mm), and RCM was positively related to
SVL (Lemckert and Shine, 1993). We found that reproductive
effort increased with body size in R. dorsalis, such that the
largest female (SVL =77.1 mm) exhibited the highest RCM
(42%), while the smallest female (SVL =34.6 mm) had the
second lowest RCM (22%). Interestingly, Lemckert and Shine
(1993) found that female C. signifera with RCMs >35% were
much less likely to be recaptured again, suggesting that frogs
with greater clutch masses relative to their body masses were
subjected to greater mortality.
The paucity of specimens with recent food items in their
stomach, all of which were collected aboveground, was
somewhat unanticipated given that prior accounts indicated
that this species surfaces at night to feed (e.g., Foster and
McDiarmid, 1983). The morphological study of Trueb and Gans
(1983), however, posited that R. dorsalis has anatomical
adaptations to feed underground. The long and narrow snout
of this species is distinctive among all frogs because it has a
spiny (keratinous) epithelium, calloused nose, and mandibular
tip, which would facilitate forward penetration (Trueb and
Cannatella, 1982; Trueb and Gans, 1983). The fundamentally
distinct lingual mechanism of R. dorsalis appears well-adapted
for subterranean foraging in narrow tunnels (Trueb and Gans,
1983), and its diet, reported to date, consists of only termites and
ants (Savage, 2002; Dodd, 2013). The general lack of food in the
stomachs among the specimens we examined provides corrob-
orative evidence that most foraging in this species is accom-
plished underground and that terrestrial activities may be more
limited than previously appreciated.
Temporal variation in the frequency of large liver sizes and
extensive fat deposits suggests metabolic tradeoffs in relation to
reproduction (Singh and Sinha, 1989). All nonreproductive
females (ovarian stage 1) lacked large livers, and few had
extensive fat, suggesting that their metabolism was geared
toward utilization rather than storage. Gravid females (ovarian
stage 4) tended to possess a combination of large fat bodies and
large livers, indicating that metabolic substrates were maximal
prior to breeding and that body lipids were likely mobilized for
the production of ova (Fitzpatrick, 1976). Metabolic stores from
lipids in coelomic fat bodies and glycogen in livers likely buffers
R. dorsalis against unpredictable rainfall and may also be a
byproduct of a species whose ecological niche is predominately
fossorial. A comparative study on metabolic expenditure (lipid
and nonlipid substrates) and energy allocation in relation to
reproduction among fossorial, semifossorial, and nonfossorial
anurans would be a fruitful avenue of future research (e.g.,
Long, 1986, 1987).
From a large sample of museum specimens, we found that R.
dorsalis in Me´ xico reproduces at much smaller body sizes than
previously reported, and that geographic variation in body size
exhibits a negative relationship with latitude, especially for
males. Reproductive effort was high among gravid R. dorsalis
relative to values reported for other anurans, with clutch masses
comprising up to 42% of body weight, and larger females
possessing larger clutches in terms of both weight and number
of ova. The typical anuran female-biased SSD was nonexistent
in our sample, suggesting that R. dorsalis may differ in this
aspect from species with a similar adult morphology (Zachariah
et al., 2012). This species does not appear to forage much while
aboveground because few adult specimens contained evidence
of recent food items. Comprehensive reproductive information
from the northern (Texas) and southern (Costa Rica) ends of its
Downloaded from by guest on 02 August 2021
range will shed much needed light on the extent to which this
species varies in life history characteristics geographically.
The detailed life history information we gleaned for an
understudied, ancient lineage of anuran would not have been
possible without museum collections. Empirical knowledge of
how organisms live (i.e., natural history) is essential for
understanding how environmental changes affect biodiversity
(Tewksbury et al., 2014) and for conserving species (Greene,
2005). Natural history collections, in fact, house the specimen
resources needed for documenting essential biodiversity vari-
ables (Kissling et al., 2018), yet they are underutilized in this
endeavor (Winker, 2004). The careful examination of museum
specimens can also lead to discoveries that would not have been
possible from other lines of evidence (e.g., Campbell et al., 2018)
because specimens are one of the only sources of biodiversity
data that contain information as varied as diet, reproduction,
and morphology for a single organism (Meineke et al., 2019).
Museum specimens were vital to detailing the reproductive
ecology of the poorly known R. dorsalis and they will continue
to be central to understanding the past, present, and future of
Acknowledgments.—We thank C. A. Phillips (INHS and
UIMNH), L. A. Scheinberg and R. C. Bell (CAS), A. Resetar
and J. Mata (FMNH), C. L. Spencer and J. A. McGuire (MVZ),
and S. Kennedy-Gold and J. A. Sheridan (CM) for hosting our
research at their institutions. We thank C. Y. Feng for her edits
on earlier drafts.
2019. First record of the anuran family Rhinophrynidae from the
Oligocene of eastern North America. Journal of Herpetology 53:316–
J. M. KIESECKER. 2001. Amphibian breeding and climate change.
Conservation Biology 15:1804–1809.
K. O’CONNOR,AND G. M. MACE. 2010. Distorted views of biodiversity:
spatial and temporal bias in species occurrence data. PLoS Biology 8:
CAMPBELL, J. A. 1998. Amphibians and Reptiles of Northern Guatemala,
the Yucat ´
an, and Belize. University of Oklahoma Press, Norman,
CAMPBELL, J. A., E. N. SMITH,AND A. S. HALL. 2018. Caudals and calyces:
the curious case of a consumed Chiapan colubroid. Journal of
Herpetology 52:458–471.
CANNATELLA,D.2015.Xenopus inspaceandtime:fossils,node
calibrations, tip-dating, and paleobiogeography. Cytogenetic and
Genome Research 145:283–301.
ROHR. 2019. An interaction between climate change and infectious
disease drove widespread amphibian declines. Global Change
Biology 25:927–937.
M. HELGEN. 2019. Sex biases in bird and mammal natural history
collections. Proceedings of the Royal Society B: Biological Sciences
CRUMP, M. L. 2015. Anuran reproductive modes: evolving perspectives.
Journal of Herpetology 49:1–16.
DEICHMANN, J. L., J. BOUNDY,AND G. B. WILLIAMSON. 2009. Anuran artifacts
of preservation: 27 years later. Phyllomedusa 8:51–58.
DODD, C. K., JR. 2013. Frogs of the United States and Canada. Volumes 1–
2. Johns Hopkins University Press, Baltimore, Maryland.
´RIL, A. M. C., AND G. BIBRON. 1841. Erp ´
etologie Gen ´
erale ou Histoire
Naturelle Compl `
ete des Reptiles. Volume 8. Librarie Enclyclopedique
de Roret, Paris, France. [In French.]
EISERMANN, K. 2017. A new locality and elevational range extension for
Rhinophrynus dorsalis Dum ´
eril & Bibron, 1841 (Anura: Rhinophryni-
dae), and a noteworthy record for Hypopachus variolosus (Cope, 1866)
(Anura: Microhylidae) in Guatemala. Mesoamerican Herpetology 4:
ELGUE, E., AND R. MANEYRO. 2017. Reproductive biology in a Uruguayan
population of Elachistocleis bicolor (Gu ´
erin-Meneville, 1838) (Anura,
Microhylidae). Cuadernos de Herpetolog´
ıa 31:5–10.
FITZPATRICK, L. C. 1976. Life history patterns of storage and utilization of
lipids for energy in amphibians. American Zoologist 16:725–732.
FORD, L. S., AND D. C. CANNATELLA. 1993. The major clades of frogs.
Herpetological Monographs 7:94–117.
FOSTER, M. S., AND R. W. MCDIARMID. 1983. Rhinophrynus dorsalis. Pp. 419–
421 in G. H. Janzen (ed.), A Costa Rica Natural History. University of
Chicago Press, Chicago, Illinois.
FOUQUETTE, M. J., JR. 1969. Rhinophynidae, Rhinophrynus,R. dorsalis.
Catalogue of American Amphibians and Reptiles 78.1–78.2.
FOUQUETTE, M. J., JR. 2005. Rhinophrynus dorsalis Dum ´
eril and Bibron,
1841: burrowing toad (sapo borracho). Pp. 599–600 in M. J. Lannoo
(ed.), Amphibian Declines: The Conservation Status of United States
Species. University of California Press, Berkeley, California.
FOUQUETTE, M. J., JR., AND D. A. ROSSMAN. 1963. Noteworthy records of
Mexican amphibians and reptiles in the Florida State Museum and
the Texas Natural History Collection. Herpetologica 19:185–201.
FROST, D. R. 2020. Amphibian species of the world: an online reference.
Version 6.1. American Museum of Natural History, New York.
Available from:
sticklebacks transfer information via eggs: effects of maternal
experience with predators on offspring. Proceedings of the Royal
Society B: Biological Sciences 278:1753–1759.
GOSNER, K. 1960. A simplified table for staging anuran embryos and
larvae with notes on identification. Herpetologica 16:183–190.
GREENE, H. W. 2005. Organisms in nature as a central focus for biology.
Trends in Ecology and Evolution 20:23–27.
GREER, A., AND A. MILLS. 1998. Observations on the biology of the
bleating tree frog Litoria dentata (Anura: Hylidae), made on a single
population in Sydney, New South Wales. Australian Zoologist 30:
sexual maturity and short life span in the blue-legged frog and the
rainbow frog from the arid Isalo Massif, southern-central Madagas-
car. Zoology 113:378–384.
JAMES, P. 1966. The Mexican burrowing toad, Rhinophrynus dorsalis,an
addition to the vertebrate fauna of the United States. Texas Journal of
Science 18:272–276.
A. SKIDMORE,AND R. P. GURALNICK. 2018. Towards global data
products of Essential Biodiversity Variables on species traits. Nature
Ecology & Evolution 2:1531–1540.
¨HLER, G. 2011. Amphibians of Central America. Herpeton Verlag,
Offenbach, Germany.
KURAMOTO, M. 1978. Correlations of quantitative parameters of fecundity
in amphibians. Evolution 32:287–296.
LEE, J. C. 1982. Accuracy and precision in anuran morphometrics:
artifacts of preservation. Systematic Biology 31:266–281.
LEE, J. C. 1996. The Amphibians and Reptiles of the Yucatan Peninsula.
Cornell University Press, Ithaca, New York.
LEMCKERT,F.L.,AND R. SHINE. 1993. Costs of reproduction in a population
of the frog Crinia signifera (Anura: Myobatrachidae) from southeast-
ern Australia. Journal of Herpetology 27:420–425.
LEMOS-ESPINAL, J. A., AND J. R. DIXON. 2013. Amphibians and Reptiles of
San Luis Potos ´
ı. Eagle Mountain Publishing LC, Eagle Mountain,
Utah, USA.
LEMOS-ESPINAL, J. A., G. R. SMITH,AND A. CRUZ. 2018. Amphibians &
Reptiles of Nuevo Le ´
on. ECO Publishing, Rodeo, New Mexico, USA.
COSTA,AND C. R. FONSECA. 2019. Global patterns of terrestriality in
amphibian reproduction. Global Ecology and Biogeography 28:744–
AND D. G. MULCAHY. 2004. Amphibian population declines in
Downloaded from by guest on 02 August 2021
montane southern Mexico: resurveys of historical localities. Biolog-
ical Conservation 119:555–564.
LONG, D. R. 1986. Reproductive and lipid patterns of four west Texas
anurans. Ph.D. dissertation. Texas Tech University, Lubbock, Texas.
———. 1987. A comparison of energy substrates and reproductive
patterns of two anurans, Acris crepitans and Bufo woodhousei.
Comparative Biochemistry and Physiology Part A: Physiology 87:
LOVICH, J. E., AND J. W. GIBBONS. 1992. A review of techniques for
quantifying sexual size dimorphism. Growth Development and
Aging 56:269–281.
LU, X., B. LI,Y.LI,X.MA,AND G. M. FELLERS. 2008. Pre-hibernation energy
reserves in a temperate anuran, Rana chensinensis, along a relatively
fine elevational gradient. The Herpetological Journal 18:97–102.
˘LNICEANU. 2018. Coping with aridity: life
history of Chacophrys pierottii, a fossorial anuran of Gran Chaco.
South American Journal of Herpetology 13:230–237.
MEINEKE, E. K., T. J. DAVIES,B.H.DARU,AND C. C. DAVIS. 2019. Biological
collections for understanding biodiversity in the Anthropocene.
Philosophical Transactions of the Royal Society B: Biological Sciences
Seasonal changes in the liver of a non-hibernating population of
water frogs, Pelophylax kl. esculentus (Anura: Ranidae). The European
Zoological Journal 84:525–535.
MESHAKA, W. E., JR. 2001. The Cuban Treefrog in Florida: Life History of a
Successful Colonizing Species. University Press of Florida, Gaines-
ville, Florida.
´TAN T,AND J. ELMBERG. 1999. Variations in life-history
traits in the common frog Rana temporaria (Amphibia: Anura): a
literature review and new data from the French Alps. Journal of
Zoology 249:61–73.
NELSON, C. E., AND M. A. NICKERSON. 1966. Notes on some Mexican and
Central American amphibians and reptiles. The Southwestern
Naturalist 11:128–131.
ORTON, G. 1943. The tadpole of Rhinophrynus dorsalis. Occasional Papers
of the Museum of Zoology 472:1–7.
AND T. GRANT. 2016. The complex evolutionary history of the tympanic
middle ear in frogs and toads (Anura). Scientific Reports 6:34130.
PORTIK, D. M., AND D. C. BLACKBURN. 2016. The evolution of reproductive
diversity in Afrobatrachia: a phylogenetic comparative analysis of an
extensive radiation of African frogs. Evolution 70:2017–2032.
PRADO, C., AND C. F. HADDAD. 2005. Size-fecundity relationships and
reproductive investment in female frogs in the Pantanal, south-
western Brazil. The Herpetological Journal 15:181–189.
ORE TEAM. 2020. R version 4.0.3: a language and environment for
statistical computing. R Foundation for Statistical Computing,
Vienna, Austria. Available from:
´VALOS. 2003. Geographical sampling bias and its
implications for conservation priorities in Africa. Journal of
Biogeography 30:1719–1727.
RESETARITS, W. J., JR. 1996. Oviposition site choice and life history
evolution. American Zoologist 36:205–215.
RESETARITS, W. J., JR., AND H. M. WILBUR. 1989. Choice of oviposition site
by Hyla chrysoscelis: role of predators and competitors. Ecology 70:
ROBERTSON, D. R. 2008. Global biogeographical data bases on marine
fishes: caveat emptor. Diversity and Distributions 14:891–892.
RYAN, M. J., J. H. FOX,W.WILCZYNSKI,AND A. S. RAND. 1990. Sexual
selection for sensory exploitation in the frog Physalaemus pustulosus.
Nature 343:66–67.
´S. 2015.
Sexual size dimorphism and acoustical features of the pre-
advertisement and advertisement calls of Rhinophrynus dorsalis
Dum ´
eril & Bibron, 1841 (Anura: Rhinophrynidae). Mesoamerican
Herpetology 2:154–166.
¨HLER. 2010. Rhinophrynus dorsalis.The
IUCN Red List of Threatened Species 2010:e.T59040A11873951.
SAVAGE, J. M. 2002. The Amphibians and Reptiles of Costa Rica: A
Herpetofauna between Two Continents, between Two Seas. Univer-
sity of Chicago Press, Chicago, Illinois.
SHINE, R. 1980. ‘‘Costs’’ of reproduction in reptiles. Oecologia 46:92–100.
SINGH,R.P.,AND R. C. SINHA. 1989. Seasonal changes in energy reserves
in the common frog, Rana tigrina. Japanese Journal of Physiology 39:
SMITH, R. J. 1999. Statistics of sexual size dimorphism. Journal of Human
Evolution 36:423–458.
˘LNICEANU. 2016. Life
history traits of a Neotropical microhylid (Dermatonotus muelleri,
Boettger 1885) from the Arid Chaco, Argentina. The Herpetological
Journal 26:41–48.
STARRETT, P. 1960. Descriptions of tadpoles of Middle American frogs.
Miscellaneous Publications of the Museum of Zoology University of
Michigan 110:5–37.
STUART, L. C. 1961. Some observations on the natural history of tadpoles
of Rhinophrynus dorsalis Dumeril and Bibron. Herpetologica 17:73–79.
STYNOSKI, J. L., AND M. SASA. 2018. Cannibalism by large tadpoles of
Rhinophrynus dorsalis (Anura: Rhinophrynidae). Herpetology Notes
SULLIVAN, B. K., AND P. J. FERNANDEZ. 1999. Breeding activity, estimated
age-structure, and growth in Sonoran Desert anurans. Herpetologica
Breed fast, die young: demography of a poorly known fossorial frog
from the xeric Neotropics. Salamandra 54:37–44.
STACEY,S.C.TROMBULAK,AND T. A. WHEELER. 2014. Natural history’s
place in science and society. BioScience 64:300–310.
TRUEB, L., AND D. C. CANNATELLA. 1982. The cranial osteology and
hyolaryngeal apparatus of Rhinophrynus dorsalis (Anura: Rhinophry-
nidae) with comparisons to recent pipid frogs. Journal of Morphol-
ogy 171:11–40.
TRUEB, L., AND C. GANS. 1983. Feeding specializations of the Mexican
burrowing toad, Rhinophrynus dorsalis (Anura: Rhinophrynidae).
Journal of Zoology 199:189–208.
TYLER, M. J. 1974. Superficial mandibular musculature and vocal sac
structure of the Mexican burrowing toad, Rhinophrynus dorsalis.
Herpetologica 30:313–316.
WEHI, P. M., H. WHAANGA,AND S. A. TREWICK. 2012. Artefacts, biology
and bias in museum collection research. Molecular Ecology 21:3103–
WELLS, K. D. 1977. The social behaviour of anuran amphibians. Animal
Behaviour 25:666–693.
WICKHAM, H. 2016. ggplot2: Elegant Graphics for Data Analysis.
Springer-Verlag, New York, New York.
WINKER, K. 2004. Natural history museums in a postbiodiversity era.
BioScience 54:455–459.
WITHERS,P.C.,AND S. S. HILLMAN. 2001. Allometric and ecological
relationships of ventricle and liver mass in anuran amphibians.
Functional Ecology 15:60–69.
detailed account of the reproductive strategy and developmental
stages of Nasikabatrachus sahyadrensis (Anura: Nasikabatrachidae),
the only extant member of an archaic frog lineage. Zootaxa 3510:53–
Accepted: 5 April 2021.
Published online: 27 July 2021.
Specimens Examined.—All specimens from Me´xico. CAS: Califor-
nia Academy of Sciences; CM: Carnegie Museum of Natural
History; FMNH: Field Museum of Natural History; INHS: Illinois
Natural History Survey; MVZ: Museum of Vertebrate Zoology;
UIMNH: University of Illinois Museum of Natural History.
Rhinophrynus dorsalis:C
AMPECHE: CAS 145821, FMNH 105709,
MVZ 164755–164758. CHIAPAS: FMNH 117985–117988, FMNH
122285–122290, FMNH 122292–122298, FMNH 122300–122305,
FMNH 173958, INHS 6572, UIMNH 11207–11222, UIMNH 11224–
11235, UIMNH 32507–35212, UIMNH 33585–33587. GUERRERO: CAS
138045–138046, CAS 142492–142583, CAS 150150, MVZ 112268–
112300, MVZ 117606. OAXACA: CM 157128, FMNH 105132–105133,
Downloaded from by guest on 02 August 2021
FMNH 105416–105422, FMNH 121012, FMNH 171576, FMNH
191917–191918, MVZ 51750, UIMNH 32504–32506, UIMNH 37223,
UIMNH 42672–42673. TABASCO: CM 40078, CM 38925a–38925z, CM
38925aa–38925vv, UIMNH 47873–47879, UIMNH 62714–62727.
TAMAULIPAS: CM 90105, UIMNH 32500, UIMNH 64640–64654.
VERACRUZ: CAS 71765–71767, FMNH 1907, FMNH 208013–208014,
INHS 28075–28076, INHS 28176, INHS 30749, UIMNH 26533–
26537, UIMNH 32501–32503, UIMNH 42653–42654, UIMNH
42656–42661, UIMNH 42663–42664, UIMNH 42666, UIMNH
42668–42671, UIMNH 49279–49280, UIMNH 64655, UIMNH
73389–73482. YUCATA
´N: FMNH 551, FMNH 153417.
Downloaded from by guest on 02 August 2021
Full-text available
Despite the common poison and mucous glands, some amphibian groups have differentiated glands associated with reproduction and usually present on the male ventral surface. Known as breeding glands or sexually dimorphic skin glands (SDSGs), they are related to intraspecific chemical communication during mating. Until recently, reproduction associated with skin glands was recognized only in salamanders and caecilians and remained unexplored among anurans. The Brazilian microhylid Dermatonotus muelleri (Muller's termite frog) is known for its very toxic skin secretion. Despite the slippery body, the male adheres to the female back during reproduction, as they have differentiated ventral glands. In this paper, we have gathered data proposing an integrative approach correlated with the species' biology and biochemical properties of their skin secretions. Furthermore, we suggest that the adhesion phenomenon is related to arm shortening and rounded body that make amplexus inefficient, although constituting important adaptive factors to life underground.
Full-text available
The Florida peninsula in the southeastern United States hosts a rich fauna of frogs and toads (Order Anura) with nearly 30 native species representing five families. In addition to the present-day species, fossils of anurans are known from terrestrial deposits in Florida from the Oligocene, Miocene, Pliocene, and Pleistocene (Table 1). These fossils indicate that each of the extant genera, including Acris (Hylidae), Anaxyrus (family Bufonidae), Gastrophryne (Microhylidae), Hyla (or Dryophytes following Duellman et al., 2016; Hylidae), Pseudacris (Hylidae), Rana (Ranidae), and Scaphiopus (Scaphiopodidae) has been present on the Florida peninsula for at least the past 18—and possibly past 30—million years (Pratt, 1989; Morgan, 1993; Table 1). Unlike many other vertebrate groups (Hulbert, 2001), there are no definitive examples of anuran families known from the fossil record of Florida that are not represented among its extant species. Table 1 Summary references on fossils of anuran genera native to the Florida peninsula organized by epoch. Note that all toad fossils in Florida have been reported previously as Bufo, though we treat them here as the genus Anaxyrus that is native to North America. Among North American frogs, the family Rhinophrynidae is among the most morphologically distinctive. This family and the Pipidae together comprise the Pipoidea, which originated in the Jurassic and is among the earliest diverging lineages of extant anurans (Cannatella, 2015; Feng et al., 2017). The single extant species Rhinophrynus dorsalis is today restricted to southernmost Texas, Mexico, and Central America, where it occurs in semiarid and arid areas with loose soils conducive to digging (Dodd, 2013); it has been reported from the Pleistocene of Mexico (Holman, 1969). In addition, extinct taxa that are more closely related to Rhinophrynus than to other pipoid anurans are known from the Mesozoic and Cenozoic of North America, including Rhadinosteus from the Jurassic of Utah (Henrici, 1998), Eorhinophrynus from the Paleocene of Wyoming (Hecht, 1959; Estes, 1975; Krause, 1980), Chelomophrynus from the Eocene of Wyoming (Henrici, 1991; Henrici and Fiorillo, 1993), and the extinct Rhinophrynus canadensis from the Eocene of Saskatchewan (Holman, 1963, 1968, 1969, 1972; Roček and Rage, 2000). To date, there are no Mesozoic or Cenozoic records attributed to the Rhinophrynidae sensu lato from eastern North America (Henrici, 2016). We report fossils referable to Rhinophrynus from two Oligocene sites in Florida. The majority of the fossils come from Brooksville 2, a site comprised of karst fissure fillings in the Suwanee Limestone near Brooksville, Florida that is one of the earliest terrestrial vertebrate sites in Florida (Arikareean, 26–28 mya; Hayes, 2000). In addition, one humerus comes from the I-75 site (Whitneyean; ∼30 mya; Morgan and Czaplewski, 2003) from which several anurans were briefly listed but never described (Patton, 1969; Meylan, 1984; Hulbert, 2001). We provide the first description of any anuran material from the Oligocene of the Florida peninsula and of the Rhinophrynidae from anywhere in eastern North America. In addition to documenting a formerly more widespread distribution of this family, we discuss the first glimpse into possible faunal turnover of anurans on the Florida peninsula during the Cenozoic.
Full-text available
We studied size, age, and growth in Chacophrys pierottii, a fossorial amphibian inhabiting the arid region of Gran Chaco, in northern Argentina. We provide the first detailed demographic data for this cryptic species using skeletochronology. We observed female-biased sexual size dimorphism but no differences in age parameters between the two sexes. Chacophrys pierottii has a short life span of up to 5 a, both males and females reaching sexual maturity after 1 a. Our results suggest that the rapid growth to maturity followed by a relatively short reproductive lifespan is a response to the constraints posed by arid environments. The life history parameters in the studied population of C. pierottii are in line with the observed patterns of other anurans inhabiting xeric habitats. Our study provides conservation managers with basic data required for the accurate assessment of the species status and the adoption of proper conservation strategies.
Full-text available
Climate change might drive species declines by altering species interactions, such as host–parasite interactions. However, few studies have combined experiments, field data, and historical climate records to provide evidence that an interaction between climate change and disease caused any host declines. A recently proposed hypothesis, the thermal mismatch hypothesis, could identify host species that are vulnerable to disease under climate change because it predicts that cool‐ and warm‐adapted hosts should be vulnerable to disease at unusually warm and cool temperatures, respectively. Here, we conduct experiments on Atelopus zeteki, a critically endangered, captively bred frog that prefers relatively cool temperatures, and show that frogs have high pathogen loads and high mortality rates only when exposed to a combination of the pathogenic chytrid fungus (Batrachochytrium dendrobatidis) and high temperatures, as predicted by the thermal mismatch hypothesis. Further, we tested various hypotheses to explain recent declines experienced by species in the amphibian genus Atelopus that are thought to be associated with B. dendrobatidis and reveal that these declines are best explained by the thermal mismatch hypothesis. As in our experiments, only the combination of rapid increases in temperature and infectious disease could account for the patterns of declines, especially in species adapted to relatively cool environments. After combining experiments on declining hosts with spatiotemporal patterns in the field, our findings are consistent with the hypothesis that widespread species declines, including possible extinctions, have been driven by an interaction between increasing temperatures and infectious disease. Moreover, our findings suggest that hosts adapted to relatively cool conditions will be most vulnerable to the combination of increases in mean temperature and emerging infectious diseases.
Full-text available
Global change has become a central focus of modern biology. Yet, our knowledge of how anthropogenic drivers affect biodiversity and natural resources is limited by a lack of biological data spanning the Anthropocene. We propose that the hundreds of millions of plant, fungal and animal specimens deposited in natural history museums have the potential to transform the field of global change biology. We suggest that museum specimens are underused, particularly in ecological studies, given their capacity to reveal patterns that are not observable from other data sources. Increasingly, museum specimens are becoming mobilized online, providing unparalleled access to physiological, ecological and evolutionary data spanning decades and sometimes centuries. Here, we describe the diversity of collections data archived in museums and provide an overview of the diverse uses and applications of these data as discussed in the accompanying collection of papers within this theme issue. As these unparalleled resources are under threat owing to budget cuts and other institutional pressures, we aim to shed light on the unique discoveries that are possible in museums and, thus, the singular value of natural history collections in a period of rapid change. This article is part of the theme issue ‘Biological collections for understanding biodiversity in the Anthropocene’.
Full-text available
Essential Biodiversity Variables (EBVs) allow observation and reporting of global biodiversity change, but a detailed framework for the empirical derivation of specific EBVs has yet to be developed. Here, we re-examine and refine the previous candidate set of species traits EBVs and show how traits related to phenology, morphology, reproduction, physiology and movement can contribute to EBV operationalization. The selected EBVs express intra-specific trait variation and allow monitoring of how organisms respond to global change. We evaluate the societal relevance of species traits EBVs for policy targets and demonstrate how open, interoperable and machine-readable trait data enable the building of EBV data products. We outline collection methods, meta(data) standardization, reproducible workflows, semantic tools and licence requirements for producing species traits EBVs. An operationalization is critical for assessing progress towards biodiversity conservation and sustainable development goals and has wide implications for data-intensive science in ecology, biogeography, conservation and Earth observation.
Natural history specimens are widely used across ecology, evolutionary biology and conservation. Although biological sex may influence all of these areas, it is often overlooked in large-scale studies using museum specimens. If collections are biased towards one sex, studies may not be representative of the species. Here, we investigate sex ratios in over two million bird and mammal specimen records from five large international museums. We found a slight bias towards males in birds (40% females) and mammals (48% females), but this varied among orders. The proportion of female specimens has not significantly changed in 130 years, but has decreased in species with showy male traits like colourful plumage and horns. Body size had little effect. Male bias was strongest in name-bearing types; only 27% of bird and 39% of mammal types were female. These results imply that previous studies may be impacted by undetected male bias, and vigilance is required when using specimen data, collecting new specimens and designating types.
Aim Amphibians exhibit two basic reproductive modes, terrestrial and aquatic, each with different ecophysiological constraints related to evaporative water loss. We hypothesize that these fundamental niche differences will generate strong geographical patterns at the global scale in response to spatial heterogeneity in temperature and water availability. Location Global. Time period Present. Major taxa studied Amphibians. Methods We used global distribution maps of 5,434 amphibian species, classified into terrestrial or aquatic breeders, to estimate the occurrence and proportion of terrestrial breeding species per 1° cell. We used multiple regression models to test the relative importance of seven abiotic variables: annual precipitation, annual mean temperature, annual mean relative air humidity, annual mean actual evapotranspiration, availability of lotic and lentic environments and slope. We used residuals autocovariate (RAC) generalized multiple regression models to control for spatial autocorrelation and a spatial vector based on amphibian phylogeny to account for phylogenetic dependencies among cells. Model generality was evaluated by contrasting results between 11 widely recognized world zoogeographical realms. Results Globally, the occurrence of terrestrial breeding species was better explained by temperature followed by total annual rainfall, relative air humidity and terrain slope. In contrast, the proportion of terrestrial breeders was better explained by terrain slope, followed by total rainfall, temperature and relative air humidity. Actual evapotranspiration and the extension of large lotic and lentic water bodies played a minor role. However, the relative importance and even the sign of the regression coefficients varied among realms, revealing different evolutionary pressures. Main conclusions Niche differences among terrestrial and aquatic breeding amphibian species are reflected in their distinct geographical distribution across the globe. Adequate conditions for terrestrial reproduction to evolve and thrive are reached in distinct ways in different realms. Temperature constraints and slope suggest that reproductive modes will be impacted differently by climate change.
A new genus and species of colubroid snake is described from the isolated highlands of western Chiapas. This enigmatic little snake possesses a unique suite of characters that defies placing it in any known genus and clearly distinguishes it from all known genera. Several of the most unusual features include subcaudals undivided throughout the length of the tail and a simple hemipenis completely adorned with calyces and having a sulcus spermaticus that remains unbifurcated until the apical portion of the organ. Neither of these characteristics is known for any other colubroid of the Western Hemisphere. Consideration of morphology places the new snake in the Dipsadidae and suggests that Adelphicos, Atractus, Geophis, and Chapinophis are among its closest relatives.