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 México

DANIEL F. HUGHES1,3 AND DANIEL B. WYLIE2

1
Department of Biology, Coe College, 1220 1st Avenue NE, Cedar Rapids, Iowa, 52402, USA
2
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 México. Seasonal aboveground activity was highest during May to August, which tracks monthly

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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 conical head, stout body, small eyes, loose skin, and the absence
inferred from studies into the life history of individual species. of a tympanum, some features of which it superficially shares
For example, descriptive studies of courtship have led to with distantly related burrowing frogs in the families Brevici-
theoretical advances in sexual selection (Ryan et al., 1990) and pitidae, Hemisotidae, and Myobatrachidae (Ford and Canna-
social behavior (Wells, 1977). Furthermore, empirical experi- tella, 1993). Unique among anurans, however, is that R. dorsalis
ments with a single species (Resetarits and Wilbur, 1989) have exhibits a distinctive method of tongue protrusion that has been
extended our understanding of the role that variable behaviors posited to be an adaptation for subterranean feeding (Trueb and
play in the evolution of life history, such as oviposition site Gans, 1983). This species is distributed from extreme southern
choice (Resetarits, 1996). Data on life history strategies can be Texas (USA) along the coastal plain of the Caribbean versant
analyzed in a phylogenetic context to elucidate evolutionary through Belize south to Nicaragua, and along the Pacific versant
patterns of reproductive diversity within a clade (Portik and from Guerrero (México) to Guatemala and Costa Rica (Camp-
Blackburn, 2016) or to estimate the ecophysiological conditions bell, 1998; Savage, 2002; Santos-Barrera et al., 2010). Rhino-
under which reproductive modes evolved globally (Lion et al., phrynus dorsalis inhabits mesic to arid forests of coastal lowlands
2019). Data derived from multiple populations on how from sea level up to 1,400 m elevation in areas that contain loose
reproductive traits vary across geography have important soil (Eisermann, 2017). This burrowing species spends most of
implications for predicting how species will respond to its life underground (Fouquette, 2005) and is irregularly
environmental change (Blaustein et al., 2001) and for docu- encountered by collectors, usually after bouts of rainfall when
menting differential selection pressures within species popula- breeding aggregations form that sometimes last for just a few
tions (Miaud et al., 1999). Also, patterns gleaned from life days (Stuart, 1961). Sexual maturity is assumed to be reached at
history investigations are increasingly recognized as indispens- body sizes ranging from 50 to 90 mm snout–vent length (SVL;
able to the development of ecologically relevant conservation Dodd, 2013) with characteristic anuran sexual-size dimorphism
strategies (Crump, 2015). Life history has implications ranging (SSD) where females are much larger than males (Savage, 2002).
from evolutionary theory to conservation biology, yet we still Breeding occurs after heavy rains in roadside ditches, small
lack information on the reproductive ecology of several pools, and other ephemeral waterbodies, with one clutch size
widespread North American anurans. The need to fill this gap estimate based on Costa Rican populations that ranges from
in knowledge has been intensified by the rapid rate and severity 2,000 to 8,000 eggs (Foster and McDiarmid, 1983).
of recent amphibian declines (Cohen et al., 2019). Rhinophrynus dorsalis possesses one of the most unique
Rhinophrynus dorsalis Duméril and Bibron, 1841 (Mexican combinations of traits among extant anurans, including a
Burrowing Toad or Sapo Borracho) is the sole extant member of specialized feeding apparatus (Trueb and Gans, 1983), indepen-
Rhinophrynidae, an ancient, monotypic anuran family origi- dently derived lack of tympanic middle ear (Pereyra et al.,
nating in the late Jurassic period (Blackburn et al., 2019), that is 2016), prolonged aestivation (up to 2 yr: Fouquette and
sister to the aquatic clawed frogs (Pipidae) from South America Rossman, 1963), distinctive superficial mandibular musculature
and Africa (Frost, 2020). Rhinophrynus dorsalis is a distinctive (Tyler, 1974), and idiosyncratic cranial anatomy (Trueb and
fossorial frog with a red orange middorsal stripe and irregular Cannatella, 1982). Rhinophrynidae is allied to Pipidae (Canna-
yellow dorsolateral marks on a purple-to-black background tella, 2015); thus, any characteristics that it shares with fossorial
skin coloration (Fouquette, 1969, 2005). This species possesses a frog families, such as Nasikabatrachidae (Zachariah et al., 2012),
particular suite of anatomical traits, including short legs, a represent convergence. Rhinophrynus dorsalis has not received
much attention despite representing an early branching lineage
3
Corresponding Author. E-mail: dhughes@coe.edu of Anura, and its potential contribution to the study of
DOI: 10.1670/20-035 convergent evolution. Available life history information for R.
 REPRODUCTION IN THE MEXICAN BURROWING TOAD 299

dorsalis is limited to a few historical reports based on largely geographic variation because this index is statistically optimal
isolated breeding events across its extensive distribution (e.g., among available dimorphism indices (Smith, 1999).
Orton, 1943; Starrett, 1960; Stuart, 1961; James, 1966). Because We examined metabolic tradeoffs temporally between repro-
the reproductive ecology of R. dorsalis has not been examined in duction, feeding, and energy storage by calculating the monthly
detail, we set out to use museum specimens to investigate life incidence of developed fat bodies, large liver sizes, and
history variation in this species across México. Our densely reproductive status (Lu et al., 2008). We assessed the extent of
sampled data set provides insight into reproduction of the only lipid deposits associated with gonads (i.e., fat bodies) in the
living member of an ancient anuran lineage and would not have body cavity of specimens based on 3 scores: 1) trace amounts or
been possible without preserved specimens in natural history no fat bodies; 2) an intermediate volume of fat bodies; and 3) a
museums. 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

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MATERIALS AND METHODS
males and females examined in each month. We recorded the
We measured 437 cataloged specimens of R. dorsalis from number of individuals of each sex with food in the stomach or
México housed in 6 museum collections: The University of an obvious food item in the upper intestines as a proxy for the
Illinois Museum of Natural History (UIMNH; n = 200) and the monthly frequency of individuals that had been feeding in each
Illinois Natural History Survey (INHS; n = 5), Champaign, month. We also examined the extent of liver development into
Illinois; the Museum of Vertebrate Zoology (MVZ; n = 39), the visible posterior section of the body cavity based on a
Berkeley, California; the California Academy of Sciences (CAS; n scoring system: 1) the liver had few lobes that occupied up to
= 99), San Francisco, California; the Field Museum of Natural 30% of the body cavity; 2) the liver had several large lobes that
History (FMNH; n = 43), Chicago, Illinois; and the Carnegie occupied from 31% to 75% of the body cavity; and 3) the liver
Museum of Natural History (CM; n = 51), Pittsburgh, had many large lobes that extended posteriorly into the inguinal
Pennsylvania (Appendix 1). The specimens were collected region to occupy 76% to 100% of the body cavity. It has been
across 59 yr (1919–1978) from 8 states within the species’ range shown that liver mass in museum specimens is representative of
in México (Fig. 1). We generated histograms using months as livers from freshly collected animals (Withers and Hillman,
bins to compare seasonality in the number of specimen records 2001). We used the highest liver score to estimate the monthly
of this data set with all R. dorsalis specimens from México on incidence of well-developed livers relative to all males and
VertNet (www.vertnet.org) and all Research Grade observations females examined in each month because the liver plays an
of R. dorsalis from México on iNaturalist (www.inaturalist.org). important role in energy storage, especially for species that
We measured body size in snout–vent length (SVL) of all aestivate for long periods (Mentino et al., 2017).
specimens to the nearest 0.01 mm using hand calipers. We We used 12 randomly selected gravid females (ovarian stage
distinguished recently metamorphosed frogs from tadpoles by 4) to examine clutch characteristics. We dissected the clutch out
the presence of forelimbs (Gosner stage 42), and from juveniles of the body cavity, gently removed excess moisture with a paper
by the presence of a tail (Gosner stage 45; Gosner, 1960). We towel, and weighed the entire clutch to the nearest 0.01 g with
relied on direct examination of the gonads to assess sex because an electronic scale. We weighed a subset of mature ova from
R. dorsalis does not exhibit the typical secondary sexual each clutch and then counted the number of individual eggs in
characteristics used to assign sex in adult frogs. For example, the subset. We extrapolated the mass of the counted subset of
R. dorsalis lacks an external eardrum (tympanum), males lack eggs to the weight of the entire brood to provide an estimate of
enlarged (or cornified) thumb pads, and males lack external clutch size (Giesing et al., 2011). We then weighed the female
vocal sacs. The presence of enlarged (swollen) testes in specimen with the clutch removed to generate estimates of
combination with a larger body size was used to determine relative clutch mass as per Shine (1980). We measured the
sexual maturity in males. We measured length and mid-width diameters of 10 randomly chosen ova from each of the clutches
of the left testis from mature male specimens and estimated using an ocular micrometer to the nearest 0.01 mm and used the
male fertility by calculating testis dimensions as a percentage of largest ovum from each clutch to compare with clutch size and
male SVL (Meshaka, 2001). To reduce some of the potential female body size.
errors derived from preservation artefacts, all reproductive The México state base map was obtained from d-maps.com
organs of male specimens were measured from the left side of and redrawn in Adobe Illustrator (Adobe Systems Inc., San Jose,
the body (Lee, 1982). California, USA). The photo of R. dorsalis was provided with
We assigned maturity in females based on the following 4 permission by M. Pingleton. We used Excel 2016 (Microsoft Inc.,
ovarian stages: 1) oviducts were thin and uncoiled, and the Redmond, Washington, USA) and Program R version 4.0.3 (R
ovaries were somewhat opaque; 2) oviducts were larger and Core Team, 2020) to organize data, conduct statistical analyses,
more coiled, and the ovaries contained some pigmented and to generate quantitative graphics using the R package
oocytes; 3) oviducts were thick and heavily coiled, and the ggplot2 (Wickham, 2016). We present mean measurements
ovaries were in various stages of clutch development; and 4) followed by 6 1 standard deviation (SD). We checked for
oviducts were thick and heavily coiled, and the ovaries were full normality of data using Shapiro–Wilk tests, compared means
of polarized ova with few nonpolarized ova, which we used as between samples using 2-sample t-tests, compared variances
evidence of a mature clutch and gravid female (Meshaka, 2001). with analysis of variance (ANOVA) F-tests and Levene’s tests,
We estimated sexual size dimorphism (SSD) using the Lovich and examined relationships between selected variables with
and Gibbons (1992) index by dividing the mean adult SVL of the Pearson’s correlation coefficients. We recognized statistical
larger sex (females) by the mean adult SVL of the smaller sex significance at P < 0.05.
(males) and then subtracting 1. When the sexes are equal in size, We wish to note that several specimens in our sample had
SSD = 0; when males are larger, SSD < 0, and SSD > 0 when various levels of damage to their anatomy, had been previously
females are larger. We used this estimate of SSD to examine skeletonized, or had entire organ systems removed prior to our
300 D. F. HUGHES AND D. B. WYLIE

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FIG. 1. Geographic origin of museum specimens in México 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.

study, so not all measurements were extracted from all during every month except February and December; only one
specimens. Likewise, some records were incomplete as a result was collected in October (FMNH 105709), and just two in March
of nonsystematic data collection: 4.1% of specimens in our (UIMNH 37223 and UIMNH 47873). The interval with the
sample did not have any data on the month of their collection. greatest incidence of captured individuals in our sample occurred
Furthermore, a handful of specimens were cataloged under a during May–September, with an apparent peak in late summer
single museum tag, such as large lots of tadpoles (e.g., 68 (July–August). Monthly frequency of captures suggests activity
tadpoles cataloged as FMNH 191918). We chose to include data peaks for different classes: males were captured most frequently
in relevant analyses and summary statistics from all specimens, in May, females from May to July, tadpoles in July, and juveniles
including damaged specimens that still possessed interpretable in August (Fig. 2B). From community science observations on
characters or those that lacked specific collecting data, such as iNaturalist that span 16 yr (2004–2020) representing 158 Research
fat development when body size was unmeasurable or body Grade observations, we found that observations occurred in
size when collecting month was not recorded or seasonal every month, with distinct peaks in June (n = 30) and July (n =
activity when the specific locality was unavailable. Consequent- 35), and fewer than 5 records in 2 separate months: February (n =
ly, these inclusions influenced sample sizes across various 3) and December (n = 2 Fig. 2C). Taken together, the records from
categories of our analysis. The data underpinning these analyses VertNet and iNaturalist corroborate the paucity of individuals in
are available from the authors upon request. our sample that were collected in months outside of late-spring
and summer, especially during September–April (Fig. 2).
RESULTS Body Sizes.—The variance in body sizes (SVL) between males
(variance = 78.61) and females (variance = 143.69) was not equal
Monthly Frequency of Records.—From VertNet collection records (Levene’s test, F156 = 8.15, P = 0.005). The mean SVL of adult
that span 148 yr (1857–2005) representing 724 specimens of R. males (48.94 6 8.87 mm, range = 30.6–71.47 mm, n = 118) was
dorsalis from México, we found that specimens were collected in not significantly different from that of adult females (48.57 6
every month of the year, with distinct peaks in June (n = 197) and 11.99 mm, range = 34.57–77.11 mm, n = 40; 2-sample t-test with
July (n = 201), and fewer than 10 individuals in 4 separate unequal variances, t54 = -0.19, P = 0.85; Fig. 3). The mean SVL of
months: February (n = 3), October (n = 4), November (n = 3), 266 juveniles was 17.65 6 2.79 mm (range = 13–23.25 mm). The
and December (n = 4; Fig. 2A). The sample of 437 cataloged mean total length of 62 tadpoles was 33.23 6 4.88 mm (range =
specimens we examined generally reflected these same seasonal 17.12–41.84 mm; body size 14.46 6 4.97 mm [range = 7.41–18.66
patterns (Fig. 2B). In our sample, specimens were collected mm]; tail length: 18.77 6 2.97 mm [range = 9.71–23.55 mm]). The
 REPRODUCTION IN THE MEXICAN BURROWING TOAD 301

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FIG. 3. Body size distributions of female and male Mexican
Burrowing Toads (Rhinophrynus dorsalis) from México. 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).

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
F IG . 2. Monthly incidence of Mexican Burrowing Toads presence in September (Fig. 5A). The monthly percentage of
(Rhinophrynus dorsalis) captures from México based on museum
specimens and community science observations. (A) All specimen males with extensive fat deposits was lowest during June (35%)
records available on VertNet that possessed month of capture data. (B) and July (16%), and rapidly increased to a peak in August (71%).
Specimens examined in this study separated by sex and life stage, which The monthly percentage of males containing food was lowest in
included 495 individual tadpoles (June and July) collected as lots August (14%) and highest in September (67%). Females, likewise,
cataloged under single specimen tags, and a series of 48 juveniles
(November) cataloged in the same manner. Monthly rainfall (mean 6 exhibited low percentages (50%) of specimens containing
standard error) displayed on the third axis. Precipitation values were extensive fat and food in all months except for fat deposits in
taken from the Mexican states where 90% of our specimens were May (Fig. 5B). The monthly percentage of females with extensive
collected (Guerrero, Veracruz, Tabasco, and Chiapas). (C) All Research fat development was highest in May (55%) and lowest in January,
Grade observations (i.e., verified by an independent observer) recorded
as on iNaturalist. 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
mean SVL for 2 specimens that had 4 legs and a tail was 14.34 6
generally more common among males than females, ranging
0.19 mm (range = 14.20–14.47 mm). The SSD between adult
from 13% in July to 50% in March. For females, large liver sizes
females and adult males was marginally negative (-0.008),
were present in January (100%), May (13%), and June (17%).
indicating that the mean body sizes of the specimens were
Fewer than 10% of ovarian stage 1 females had extensive fat
essentially equal. deposits and none had well-developed livers (Fig. 5C). Females
Testicular Cycle.—Mean testis length as a percentage of SVL in ovarian stages 2 and 3 exhibited the highest frequency of
was 11.95 6 2.38% (range = 7.12–18.1%, n = 107) and testis food, but none of them exhibited extensive fat bodies. Large
width was 5.66 6 1.01% (range = 3.57–8.6%, n = 107). A seasonal livers were detected at similar frequencies among females in
change in testis dimensions was evident in our sample (ANOVA: ovarian stages 2, 3, and 4. The relatively higher percentage of
testis length, F4,101 = 16.92, P < 0.001; testis width, F4,101 = 4.24, P food in the stomachs of stage 2 and 3 females, and a
= 0.003). Seasonal testis dimensions exhibited the greatest mean corresponding lack of extensive coelomic fat, indicates that
length and width in May, followed by a rapid drop in June, and feeding is more pronounced during these stages of clutch
302 D. F. HUGHES AND D. B. WYLIE

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FIG. 4. Monthly distribution of testis length and width as a
percentage of male body size in 107 Mexican Burrowing Toads
(Rhinophrynus dorsalis) from México. Points are jittered for visual
clarity between overlapping values.

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
FIG. 5. Monthly frequency of food presence in the stomach, extensive
stage 2 (50%). fat in the body cavity, and well-developed livers in the Mexican
Ovarian Cycle.—Gravid females (ovarian stage 4) were detected Burrowing Toad (Rhinophrynus dorsalis) from México by male (A),
from May to August and in October and January (Fig. 6). The female (B), and ovarian stage (C). Asterisks (*) next to a month indicate
that no specimens were available for examination.
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 7 July 1970 from Oaxaca (MVZ 92710; FMNH 171576, 191917–
the lowest frequency of stage 4 females also exhibited the greatest 18); and 14 August 1955 from Veracruz (UIMNH 73482).
frequency of stage 1 females (100% in both April and September). Clutch and Egg Size.—The clutch size, body size, and weight of
It is difficult to assess the ovarian cycle from the late autumn gravid females were normally distributed (Shapiro–Wilk, W =
through spring because no specimens in our sample were 0.89–0.97, P = 0.12–0.87). From 12 gravid females (mean SVL =
collected in November, December, February, or March, but it 55.64 6 12.78 mm, range = 34.57–77.11 mm; mean weight =
appears that reproduction can occur in October and January. The 26.01 6 15.81 g, range = 8.2–56.7 g), mean clutch size was
time period with the most specimens (April to September) estimated at 3,134.9 6 2,326 eggs (range = 630–7,700 eggs).
indicates that oviposition starts in May and generally is finished Clutch size was positively correlated with SVL (Pearson
by August. To that end, all the tadpoles in our sample were correlation, t10 = 7.23, R = 0.92 [0.72–0.98 95% CI], P < 0.001)
collected from late June to mid-August: 26 June 1957 from and specimen weight (Pearson correlation, t10 = 22.54, R = 0.99
Oaxaca (FMNH 121012); 3 July 1965 from Veracruz (INHS 30749); [0.97–0.99 95% CI], P < 0.001; Fig. 7). Clutch mass increased
 REPRODUCTION IN THE MEXICAN BURROWING TOAD 303

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FIG. 6. Monthly ovarian cycle of female Mexican Burrowing Toads
(Rhinophrynus dorsalis) from México. See text for details on reproductive
stages.

significantly with increasing SVL (Pearson correlation, t10 = 8.43,

R = 0.94 [0.78–0.98 95% CI], P < 0.001). The relative clutch mass
of these 12 female specimens was 32.3 6 6.57% (range = 20.18–
41.67%) and was positively related to both SVL (Pearson
correlation, t10 = 3.4, R = 0.73 [0.27–0.92 95% CI], P = 0.007)
and body weight (Pearson correlation, t10 = 3.26, R = 0.72 [0.25–

FIG. 8. Monthly distribution of body sizes for 36 females, 107 males,

and 266 juveniles of the Mexican Burrowing Toad (Rhinophrynus dorsalis)
from México. Points are jittered for visual clarity between overlapping
values.

0.92 95% CI], P = 0.009). The mean diameter of 120 measured ova
from the same 12 gravid females was 1.7 6 0.19 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
FIG. 7. The relationship between clutch size and body size in 12 and collected on 1 July 1963 in Tamaulipas (UIMNH 64652), the
female Mexican Burrowing Toads (Rhinophrynus dorsalis) from México.
Grey shading indicates the 95% confidence interval. The equation for the
smallest ovarian stage 3 female was 36.94 mm in SVL and
line: y = -6,100 + 170x. Silhouettes modified from Eisermann (2017) collected on 20 July 1963 in Tabasco (UIMNH 62720), the
and drawn to scale relative to each other. smallest ovarian stage 2 female was 34.44 mm in SVL and
304 D. F. HUGHES AND D. B. WYLIE

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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) from México (n = 163).
Grey shading indicates the 95% confidence interval. The equation for the
collected on 20 July 1963 in Tabasco (UIMNH 62717), and the line: y = 65.2 - 0.95x.
smallest ovarian stage 1 female was 29.45 mm in SVL and
collected on 15 April 1959 in Tabasco (UIMNH 47874). It is not significantly different from that of adult females in Chiapas
unclear whether the smallest ovarian stage 1 females were still (t11 = 0.98, P = 0.34), Oaxaca (t14 = -1.96, P = 0.07), Tabasco (t11
maturing with egg laying to occur at larger sizes. Given that the = -1.08, P = 0.30), or Veracruz (t4 = 1.18, P = 0.30; Fig. 9).
smallest ovarian stage 4 female was <5 mm larger in SVL than Body size as SVL was negatively associated with latitude,
the smallest ovarian stage 1 female, it is feasible that maturity with individuals from higher latitudes exhibiting smaller body
and egg laying could have occurred at body sizes between 29 sizes than those from lower latitudes (Pearson correlation, t161 =
mm and 34 mm. -2.7, R = -0.21 [-0.06 to -0.35 95% CI], P = 0.008; Fig. 10).
The mean SVL of ovarian stage 1 females was 39.74 6 9.19 This latitudinal trend persisted when analyzing males separate-
mm (range = 29.45–66.11 mm, n = 20), for ovarian stage 2 ly (Pearson correlation, t116 = -3.04, R = -0.27 [-0.10 to -0.43
females it was 50.89 6 12.03 mm (range = 34.44–62.41 mm, n = 95% CI], P = 0.003) but disappeared in an analysis of females
4), for ovarian stage 3 females it was 42.42 6 7.58 mm (range = only (Pearson correlation, t43 = -0.46, R = -0.07 [-0.36–0.23
36.94–56.57 mm, n = 6), and for ovarian stage 4 females it was 95% CI], P = 0.65). Adult body size showed no linear
55.49 6 12.03 mm (range = 34.57–77.11 mm, n = 16). Mean body relationship to longitude (Pearson correlation, t161 = 0.42, R =
size of gravid females (stage 4) was significantly larger than that 0.03 [-0.12–0.19 95% CI], P = 0.68).
of all other ovarian stages (nongravid female stages 1–3 [41.76 6 To further examine geographic variation in SSD, we grouped
9.73 mm, range = 36.66–66.11 mm, n = 30; t26 = 3.93, P < 0.001). adult specimens by the degree of latitude or longitude of their
Based on the seasonal distribution of body sizes and collection (e.g., all male and female specimens from latitude
specimen occurrences, tadpole transformation time was ap- 158N) that had ‡2 males and 2 females to calculate a mean SVL
proximately 2 mo (Figs. 2, 7). Males and females could have for each sex, which resulted in SSD estimates across 7 latitudinal
reached their minimum body size at sexual maturity (males = degrees and 5 longitudinal degrees. We found that SSD was not
30.6 mm, females = 34.57 mm) within 8–9 mo after metamor- significantly related to latitude (Pearson correlation, t5 = -2.2, R
phosis and mean adult body size (males = 48.9 mm; females = = -0.7 [0.11 to -0.95 95% CI], P = 0.08) or longitude (Pearson
48.6 mm) approximately 12 mo postmetamorphic age. correlation, t3 = 0.94, R = 0.47 [-0.7–0.96 95% CI], P = 0.42).
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 DISCUSSION
body sizes across geography, which resulted in 4 state We used a robust sample of museum specimens from México
comparisons. We found that the mean SVL of adult males was to provide empirical data on several life history traits for R.
 REPRODUCTION IN THE MEXICAN BURROWING TOAD 305

dorsalis that complement and, in some cases, extend previous From the Mexican states of San Luis Potosı́ and Nuevo León,
findings. First, we wish to highlight general biases unique to Lemos-Espinal et al. (2018; Lemos-Espinal and Dixon, 2013)
studies based on museum collections that should be considered reported that the maximum SVL of females is 88 mm and that
when interpreting their results (Robertson, 2008; Boakes et al., adult males averaged 60–65 mm, values that were likely derived
2010; Wehi et al., 2012). Nondeliberate sex biases in vertebrate from Fouquette (1969). From the Yucatán Peninsula, Lee (1996)
collections tend to be skewed toward males because they are reported an adult SVL range of 60–65 mm SVL, and that females
often the more easily captured sex. In some animal groups, such are substantially larger than males. Campbell (1998) reported
as frogs, males exhibit a greater frequency of movements, more from northern Guatemala, the Yucatán, and Belize, that males
conspicuous visual displays, and audible calling to attract mates reach 65–75 mm in SVL and females 70–80 mm in SVL, but no
(Cooper et al., 2019). Breeding aggregations of R. dorsalis consist reference material was mentioned for these size ranges. Despite
of mostly males, which conspicuously vocalize to attract seemingly widely repeated values for body sizes at maturity,
females (Savage, 2002; Dodd, 2013), and we note that our few accounts referred to measurements from specimens or

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sample contained over twice as many adult males (n = 124) as referenced wild individuals. From a recent account based on a
adult females (n = 51). Moreover, collectors’ objectives vary single breeding night in Costa Rica, Sandoval et al. (2015) found
through time, are dependent upon permits that differ across that the mean body size of females (SVL = 81 mm, n = 15) was
political boundaries, and generally follow assessments of larger than that of males (SVL = 72.1 mm, n = 21), and that
species in need. Rhinophrynus dorsalis has not been in decline larger females were amplexed by larger males. It seems that the
(International Union for Conservation of Nature Least Concern; SSD in this species may be less extreme than previous reports
Santos-Barrera et al., 2010) and thus was likely not a collecting have indicated because most accounts echoed values from Costa
priority during the well-documented declines of other Mexican Rica (Savage, 2002) or Guatemala (Nelson and Nickerson, 1966).
anurans (e.g., Lips et al., 2004). We note that all the specimens in Nevertheless, females can exhibit larger maximum body sizes
our sample were collected before 1980. Geographical biases are than males, and the SSD at a specific breeding site (e.g.,
also widespread among museum collections such that the Sandoval et al., 2015) is likely to be more prominent than when
location and intensity of collecting are influenced by accessibil- generalizing across its range. We suggest that the SSD in R.
ity and species-specific differences in detectability (Reddy and dorsalis may be most evident at tropical latitudes because body
Dávalos, 2003). Rhinophrynus dorsalis spends most of its life sizes were largest at the lowest latitudes in our sample and in
underground (Fouquette, 1969), rendering it difficult to target the literature. However, this geographic pattern in body size
for collecting relative to surface-dwelling anurans. We attempt- was driven by a sex effect on the slope of the latitudinal cline,
ed to address biases in museum collections by 1) focusing our where the slope in males was steeper than that in females, such
study on a single political entity (México) to avoid changes in that males were smallest at northern latitudes and larger further
specimen collecting policies between nations; 2) examining a south, whereas female body size did not change much across
sample of specimens collected across decades and from multiple latitude.
museums to minimize the impact of individual collector biases; From Costa Rica, Foster and McDiarmid (1983) reported the
and 3) including the largest sample of this species to date to only clutch size estimate for this species (range = 2,000–8,000
generate a significantly robust biological signal to overcome eggs), which was repeated by Campbell (1998), Savage (2002),
these issues and even out potential collecting imbalances. and Köhler (2011). We found that the clutch size range in México
The literature on the reproductive biology for this species is (630–7,700 eggs) conforms to the upper limit of this previous
based on a handful of primary data sources (Orton, 1943; report but extends the lower estimate well below 2,000 eggs. In
Starrett, 1960; Stuart, 1961; Fouquette and Rossman, 1963; fact, we found 5 females with body sizes smaller than the mean
James, 1966; Nelson and Nickerson, 1966; Foster and McDiar- of our sample (48.6 mm SVL) that were gravid, and these
mid, 1983; Sandoval et al., 2015; Stynoski and Sasa, 2018), which specimens had an average clutch size of 1,206 eggs (range 630–
have been repeated verbatim, or with little added information, 1,617 eggs). The smallest gravid female in our sample (SVL =
in regional synoptic guides (e.g., Lee, 1996; Campbell, 1998; 34.6 mm) was from Tamaulipas, indicating that either this
Savage, 2002; Fouquette, 2005; Köhler, 2011; Dodd, 2013; Lemos- species reaches sexual maturity at a much smaller body size in
Espinal and Dixon, 2013; Lemos-Espinal et al., 2018). Most northern México than reported elsewhere or that the females
sources report that this species exhibits dramatic sexual size south of México, from where most of the data in the literature
dimorphism (SSD) with much larger females than males (e.g., originated, mature at larger body sizes. To that end, we found
Fouquette, 1969). The degree of SSD in our sample was that adult body size in our sample was negatively related to
negligible between the mean adult body sizes of males and latitude with larger specimens originating from southern
females, but there was evidence that females can attain larger locations. The largest specimen-backed body size for this
maximum adult body sizes than males. The largest specimen we species was recorded from Guatemala (Nelson and Nickerson,
examined was a gravid female (SVL = 77.1 mm) from Veracruz 1966), and all reports from south of México suggest that both
(UIMNH 42654) and the largest male specimens (two at SVL = sexes mature at larger body sizes than those we found (e.g.,
71.5 mm) were from Chiapas (UIMNH 33585 and INHS 6572). Foster and McDiarmid, 1983; Campbell, 1998; Savage, 2002;
The largest size record based on a physical specimen was 88 mm Sandoval et al., 2015). It remains unclear whether there is
SVL for a female recorded by Nelson and Nickerson (1966) from significant geographic variation in clutch size, and if so,
Guatemala (MCZ A-2312). From Costa Rica, Savage (2002) whether it follows the observed latitudinal variation in body
reported an adult SVL range of 50–89 mm, with females size.
reaching 89 mm and males only 75 mm, but there was not a In our sample, R. dorsalis was most frequently captured in late
clear basis for these measurements. Fouquette (1969) reported spring and summer, with very few records in autumn and
that adults reach sexual maturity at 60–65 mm SVL and that winter. Additional specimen records from VertNet and com-
overall adult range is likely to be 50–88 mm, with females larger munity science observations from iNaturalist independently
than males, which was echoed by Foster and McDiarmid (1983). corroborated that R. dorsalis is active year-round in México and
306 D. F. HUGHES AND D. B. WYLIE

that activity is most pronounced from May to August and (SVL range = 19–27 mm), and RCM was positively related to
lowest from September to April. We detected most gravid SVL (Lemckert and Shine, 1993). We found that reproductive
females from May to August, most tadpoles from June to effort increased with body size in R. dorsalis, such that the
August, and most juveniles during July and August, indicating largest female (SVL = 77.1 mm) exhibited the highest RCM
that breeding generally begins in May after the first major (42%), while the smallest female (SVL = 34.6 mm) had the
rainfall and likely ceases by September. Males were also most second lowest RCM (22%). Interestingly, Lemckert and Shine
common in May and their testis size was likewise largest in May (1993) found that female C. signifera with RCMs >35% were
and was much smaller in specimens collected during all other much less likely to be recaptured again, suggesting that frogs
months. Nevertheless, we also found small juveniles in with greater clutch masses relative to their body masses were
November and January, and gravid females in January and subjected to greater mortality.
October, indicating that the timing of reproduction can be The paucity of specimens with recent food items in their
variable across its range. In Guerrero, Fouquette and Rossman stomach, all of which were collected aboveground, was

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(1963) collected a series of specimens during breeding aggrega- somewhat unanticipated given that prior accounts indicated
tions that formed shortly after a storm on 19 July 1960. From the that this species surfaces at night to feed (e.g., Foster and
Yucatán Peninsula, Lee (1996) found tadpoles (Gosner stage 25; McDiarmid, 1983). The morphological study of Trueb and Gans
Gosner, 1960) in early October and suggested that reproduction (1983), however, posited that R. dorsalis has anatomical
may also occur later in the rainy season. In Nuevo León, Lemos- adaptations to feed underground. The long and narrow snout
Espinal et al. (2018) suggested that this species will call and of this species is distinctive among all frogs because it has a
mate at any time during the year because of the unpredictability spiny (keratinous) epithelium, calloused nose, and mandibular
of rain and that tadpole development ranges from 1 to 3 mo. tip, which would facilitate forward penetration (Trueb and
From Texas (USA), Fouquette (2005) also reported that this Cannatella, 1982; Trueb and Gans, 1983). The fundamentally
species will breed at any time of the year given adequate rainfall distinct lingual mechanism of R. dorsalis appears well-adapted
and that tadpoles take ‡2 mo to develop. From Guatemala, for subterranean foraging in narrow tunnels (Trueb and Gans,
Stuart (1961) found tadpoles (mean body length = 18 mm) on 7 1983), and its diet, reported to date, consists of only termites and
July that were at least 7-wk from the time of egg deposition, ants (Savage, 2002; Dodd, 2013). The general lack of food in the
which was presumed to follow a heavy rainfall on 20 May, and
stomachs among the specimens we examined provides corrob-
that all tadpoles were metamorphosed by 17 August after
orative evidence that most foraging in this species is accom-
reaching a maximum body size of 25 mm. Campbell (1998)
plished underground and that terrestrial activities may be more
reported that breeding occurs from June to September in Petén,
limited than previously appreciated.
Guatemala, perhaps based on Stuart (1961). From Costa Rica,
Temporal variation in the frequency of large liver sizes and
Foster and McDiarmid (1983) reported that the populations
extensive fat deposits suggests metabolic tradeoffs in relation to
breed once in late May or early June, and that all the tadpoles
reproduction (Singh and Sinha, 1989). All nonreproductive
will have metamorphosed by the latter part of July and will
females (ovarian stage 1) lacked large livers, and few had
disperse synchronously from wetlands.
extensive fat, suggesting that their metabolism was geared
Fecundity characteristics are poorly characterized among
toward utilization rather than storage. Gravid females (ovarian
most fossorial anurans, but for those species with data, most
stage 4) tended to possess a combination of large fat bodies and
tend to reach sexual maturity rapidly, invest a significant
large livers, indicating that metabolic substrates were maximal
amount of their body weight to reproduction, and have short
lifespans (Sullivan and Fernandez, 1999). Our findings on prior to breeding and that body lipids were likely mobilized for
relative clutch mass (RCM) in R. dorsalis (range = 20–42%) are the production of ova (Fitzpatrick, 1976). Metabolic stores from
similar to those reported for other fossorial species (Székely et lipids in coelomic fat bodies and glycogen in livers likely buffers
al., 2018), but at the higher end of the range for anurans in R. dorsalis against unpredictable rainfall and may also be a
general (Kuramoto, 1978). Measurements from fresh R. dorsalis byproduct of a species whose ecological niche is predominately
would likely exhibit higher RCMs because long-term preserva- fossorial. A comparative study on metabolic expenditure (lipid
tion in ethanol undoubtedly reduced the weight measurements and nonlipid substrates) and energy allocation in relation to
in our museum specimens (Deichmann et al., 2009). From a reproduction among fossorial, semifossorial, and nonfossorial
Neotropical frog community consisting of 16 species, RCMs anurans would be a fruitful avenue of future research (e.g.,
ranged from 5.5% to 18% with a semifossorial species (Micro- Long, 1986, 1987).
hylidae: Elachistocleis bicolor) exhibiting the highest RCM values From a large sample of museum specimens, we found that R.
(Prado and Haddad, 2005). In a separate study on E. bicolor from dorsalis in México reproduces at much smaller body sizes than
Uruguay, Elgue and Maneyro (2017) found that the largest previously reported, and that geographic variation in body size
females produced the largest clutches, but RCM did not increase exhibits a negative relationship with latitude, especially for
with increasing body size. In Dermatonotus muelleri (66.1–81.9 males. Reproductive effort was high among gravid R. dorsalis
mm SVL), a fossorial microhylid from the Gran Chaco region in relative to values reported for other anurans, with clutch masses
Argentina, RCM averaged 30.2% and was negatively related to comprising up to 42% of body weight, and larger females
SVL, with larger individuals investing less in reproduction in possessing larger clutches in terms of both weight and number
terms of clutch mass (Stănescu et al., 2016). Two small of ova. The typical anuran female-biased SSD was nonexistent
Australian frogs that differ in their habits have some of the in our sample, suggesting that R. dorsalis may differ in this
highest reported RCM values: an arboreal species (Pelodryadi- aspect from species with a similar adult morphology (Zachariah
dae: Litoria dentata) exhibited an RCM range of 34–63% (SVL et al., 2012). This species does not appear to forage much while
range = 38–46 mm), and RCM did not increase with increasing aboveground because few adult specimens contained evidence
SVL (Greer and Mills, 1998); and a terrestrial species (Myoba- of recent food items. Comprehensive reproductive information
trachidae: Crinia signifera) exhibited an RCM range of 11–68% from the northern (Texas) and southern (Costa Rica) ends of its
 REPRODUCTION IN THE MEXICAN BURROWING TOAD 307

range will shed much needed light on the extent to which this EISERMANN, K. 2017. A new locality and elevational range extension for
species varies in life history characteristics geographically. Rhinophrynus dorsalis Duméril & Bibron, 1841 (Anura: Rhinophryni-
dae), and a noteworthy record for Hypopachus variolosus (Cope, 1866)
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understudied, ancient lineage of anuran would not have been 688–692.
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 REPRODUCTION IN THE MEXICAN BURROWING TOAD 309

FMNH 105416–105422, FMNH 121012, FMNH 171576, FMNH INHS 28075–28076, INHS 28176, INHS 30749, UIMNH 26533–
191917–191918, MVZ 51750, UIMNH 32504–32506, UIMNH 37223, 26537, UIMNH 32501–32503, UIMNH 42653–42654, UIMNH
UIMNH 42672–42673. TABASCO: CM 40078, CM 38925a–38925z, CM
42656–42661, UIMNH 42663–42664, UIMNH 42666, UIMNH
38925aa–38925vv, UIMNH 47873–47879, UIMNH 62714–62727.
TAMAULIPAS: CM 90105, UIMNH 32500, UIMNH 64640–64654. 42668–42671, UIMNH 49279–49280, UIMNH 64655, UIMNH
VERACRUZ: CAS 71765–71767, FMNH 1907, FMNH 208013–208014, 73389–73482. YUCATÁN: FMNH 551, FMNH 153417.

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