Biological Journal o f t h e Imnean Sociep (1988), 34: 93-104. With 6 figures
The giant tadpole of Pseudis paradoxa
SHARON B. EMERSON
Department of Biology, University of Utah, Salt Lake CiQ, Utah 84112, U.S.A.
Received I September 1987, accepted for publication 13 November 1987
Pseudis paradoxa has an extremely large tadpole with a long, deep tail. These features are also found
in overwintering tadpoles of temperate species where low temperatures delay development and
prolong prolactin exposure. Pseudis paradoxa does not occur in localities with marked seasonal
temperature fluctuations. Low temperature rannot be implicated in the development of the
tadpole. However, the parallels in shape between Pseudis tadpoles and those of temperate
overwintering species suggest that Pseudis tadpoles may have a prolonged exposure to prolactin,
higher levels of prolactin during developmcnt or an increased sensitivity to prolactin.
KEY WORDS:-'ladpole
-
shape - development
~
prolactin.
CONTENTS
. , . .
Introduction .
Material and methods . . .
Results
. . . . . .
Tadpole size and adult size
Pattern of development .
Discussion. . . . . .
Summary, . . . . .
Acknowledgements
. . .
References.
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INTRODUCIION
Anurans undergo a dramatic morphological reorganization at metamorphosis
(DeJongh, 1968; Wassersug & Hoff, 1982; Werner, 1986), and show wide
variation in their temporal pattern of development (Wright & Wright, 1949;
Blommers-Schlosser, 1975; Collins, 1979). As a consequence of these features,
frogs have been the object of recent work focussing on the evolution of complex
life cycles (Wilbur & Collins, 1973; Wassersug & Hoff, 1982; Werner, 1986),
and the effects of changes in the timing of development (or heterochrony) on
larval and adult morphological form (Wassersug & Duellman, 1984; Emerson,
1986; Emerson, Travis & Blouin, 1988). It is in this context that I report
the results of an investigation into the ontogeny and biology of Pseudis paradoxa.
Pseudis paradoxa is a completely aquatic frog found east of the Andes in river
drainage systems from Venezuela to Paraguay and in Trinidad. The family
Pseudidae includes Pseudis (two species) and one other genus, Lysapsus (two
0024-4066/88/060093
+ 12 $03.00/0
93
0 1988 The Linnean Society of London
94
S B EMERSON
species) (Frost, 1985). Pseudis paradoxa is so named because of the discrepancy in
size between its large tadpole and its relatively small adult. In fact, a n early
worker, confusing size with age, had the frog transforming into the tadpole
during ontogeny (Gans, 1956)! There are scattered morphological descriptions
of Pseudis and Lysapsus tadpoles in the literature (Kenny, 1969; Gallardo, 1964;
Cei, 1980; Fernandez & Fernandez, 1921), but little is known of the natural
history of most species. The tadpoles of Lysapsus mantidactylus have been reported
to overwinter (Gallardo, 1964).
The impetus for this work came from finding no comparative studies of
tadpole size and shape to support three assertions about P. paradoxa which have
appeared in the literature: ( 1 ) that Pseudis is remarkable in the size of its tadpole
(Goin, Goin & Zug, 1978), (2) that the tadpole is unusual because it is so much
larger than the adult frog (Savage & DeCarvalho, 1953; Gans, 1956), and (3)
that Pseudis is “almost progenetic with an enormous tadpole and a barely
functional adult” (Cohen & Massey, 1983). As is so often the case in biology
(c.g. Gould, 1974; Hanken, 1985) the present study of the extreme or special
case has provided insights into more general patterns as well. Specifically, data
are presented relating to the correlation of size and shape among larval and
adult frogs, and possible proximal mechanisms producing changes in the
morphology of larval Pseudis.
MATERIAL AND METHODS
I t was difficult to find an appropriate sister-group to the Pseudidae for
tadpole comparisons. The phylogenetic affinities of the family are uncertain
(Savage & DeCarvalho, 1953; Bogart, 1973; Duellman, 1975; Duellman &
Trueb, 1986). 1 therefore compared pseudid tadpoles with those of Rana
calesbeiana, an unrelated but ecologically similar species. I chose this species for
initial cornparisoris because R. catesbeiana, like Pseudis, has large tadpoles; like
Lysapsus, the tadpoles overwinter; and like all species of pseudids, the adult is
very aquatic. Lastly, but not incidentally, there are relatively large numbers of
R. catejbeiana tadpoles in museum collections.
A total of 71 P. paradoxa, 25 L. mantidactylus, and 127 R. calesbeiana tadpoles
were examined. All tadpoles were staged, according to Taylor & Kollros ( 1946),
weighed and measured. Snout- vent ( = body) length, tail length, tail depth,
total length, hindlimb length and body weight ( = total weight) were recorded
for each animal. In addition I used data from the literature on tadpole and
adult size for several species in order to make broader comparisons between the
tadpoles of Pseudis and other frogs.
RESULTS
Tadpole size and adult size
Figure 1 plots the maximum adult snout-vent length of a number of frog
species in relation to the maximum total length of their tadpole. Tadpole length
shows a significant correlation with adult snout-vent length ( r = 0.33,
P < 0.05), but there is considerable variation in that relationship among species.
Frogs that reach a n especially large adult size (SVL > 120 mm) do not show a
PSEUDIS SHAPE AND SIZE
95
Tadpole size (rnrn)
Figure 1. Maximum adult snout-vent length versus maximum total length of tadpole for 60 specks.
The data are derived from Wager (1965) and Inger (1966, 1985). R , and R , are nonoverwintering and overwintering tadpoles of Rana catesbeiana. L , and L, are non-overwintering and
averwintering tadpoles of Lysapsus mantidaclylus. P , and P, are the two size classes of Pseudis tadpoles.
K.m. is Kmina maculatus. The solid line indicates tadpole and adult frog of equal size.
proportional increase in tadpole length. Importantly, for this study, relatively
few species for which there are data have tadpoles that are much larger than the
adult. The significant exceptions in this regard are Kassina maculatus,
overwintering L. mantidactylus and P. paradoxa. Pseudis clearly is unique in the
size of the adult frog compared to the size of the tadpole. As is also clear from
the graph P. paradoxa has the longest tadpole of any species for which there are
data. In museum collections the record size I was able to find was a 220.5-mm
stage XVII individual weighing 78 g. (Other specimens weighed up to 98 g but
were shorter because they were at more advanced stages.)
Figure 1 demonstrates a significant correlation between maximum tadpole
total length and adult snout-vent length across a diversity of species. Werner
( 1986) has published data showing a significant correlation between snout-vent
length at transformation and adult snout-vent length. Not surprisingly, for the
few available data (Wager, 1965), there is a good correlation between
maximum total length of the tadpole and snout-vent length a t transformation
( r = 0.89, P < 0.001). The largest R. catesbeiana tadpole in my sample was
150 mm total length. Using the calculated interspecific regression of maximum
tadpole total length to snout-vent length a t transformation (see Fig. 2) a
150-mm tadpole would transform at about 39 mm. Length at transformation in
that species has been reported to vary from 29 to 60 mm (Collins, 1979). It
therefore seems possible that the largest size class of R. catesbeiana tadpoles was
not included in my sample. T h e maximum length tadpole of P. paradoxa in the
museum collections was 220.5 mm. Using the same regression, the length at
transformation for that Pseudis tadpole would be around 56 mm.
The later developmental stages of R. catesbeiana tadpoles (XX-XXV, Taylor
Kollros) examined in this study had body lengths of 38-46 mm (Fig. 3 ) . The
later stages of Pseudis that were available were similar to R. catesbezana in body
length, with the exception of two specimens (Fig. 3). I assume these two larger
specimens had a maximum total tadpole length of 180-200 mm and would
S. B. EMERSON
96
+
~ ~ 1 . 04 . 2 5 ~ ~
-=0.89
...
. .
10
I 5
Todpole size (mm)
Figure 2. Snout--vent size at transformation versus maximum total length of tadpole for 14 species
of African frogs. The data are derived from Wagcr (1965).
therefore have metamorphosed at around 50-52 mm. T h e other late stage
Pseudis probably had maximum tadpole total lengths f 150-160 mm and would
metamorphose at 39-41 mm. Rana catesbeiana reach sexual maturity at
approximately 95 mm (Oliver, 1955). Sexual maturity in P. Paradoxa is rcached
at 45-65 mm (Gallardo, 1964; Cei, 1980). The available data suggest then that
Pseudis can metamorphose at a length very close to that of sexual maturity. Kana
catesbeiana, on the other hand, does not transform at a length anywhere close to
that of sexual maturity even after overwintering.
Pattern of development
Figures 4 and 5 give total lengths of R. calesbeiana, P. paradoxa, and
L. mantidacplus tadpoles as a function of development stage. As is the case for
other species (Smith-Gill & Berven, 1979), these tadpoles reach maximum
length a t stage XVII. There is wide variation in tadpole weight at a given stage
1
30
X x x x I ~ m ~ x xxFx+
n
Taylor Kollros stage
Figurc 3. Body length versus 'Iaylor Kollros stage of development in Pseudzt paradoxa
ratesbeiana ( 0 ) .
(0)
nnd Rana
PSEUDIS SHAPE AND SIZE
i
*
*:
I40
97
*
.
0
0
.
0
I .
I
t
PI
x
mmxxII
T a y l o r Kollros stage
Figure 4. Total length versus Taylor Kollros stage of development in Rana cateshetana. 0,
Tadpoles
which presumably complete metamorphosis in d single season; 0 , tadpoles which presumahly
overwinter 1 year; *,tadpoles thought to overwinter 2 years.
for all three species (Fig. 6). The variation in tadpole size in the R. catesbeiana
sample is probably related to whether the tadpoles have overwintered and, if so,
for how many winters. Samples from several localities included tadpoles of two
distinct stage classes. For example, a collection made in June 1940 in Reynolds
County, Missouri, contained both stage I and stage XXII individuals. The late
stage tadpoles are presumably those that overwintered. The early stages
represent individuals from that year's spring breeding. Other studies have
shown that overwintering tadpoles metamorphose at larger sizes than tadpoles
that complete their development in one season (Collins, 1979), and that
*
..
..
I
. *. a * .
*.
...
'
::
..
....
8
*
8
n m x mmm
Taylor Kallros stage
Figure 5. Total length versus Taylor Kollros stage of development in P,reudis paradoxa (*and @ )
and Lysapsus mantidactylus (0).
See text for further details.
98
S. B. EMERSON
Taylor Kollros stage
Figure 6. 'lotal weight plotted as a function of stage of development in A e u d i s paradoxa (0)and
Rana catesbeiana (a).
overwintering tadpoles weigh more than tadpoles of the same stage that
complete development in a single season (Viparina & Just, 1975).
Overwintering is correlated with latitude in R. catesbeiana (Collins, 1979), as
differentiation rate is highly temperature sensitive (Smith-Gill & Berven, 1979).
In Fig. 4 the stars represent tadpoles from Michigan populations. The closed
circles are animals from Kansas, California, Arkansas, and Missouri. The
animals represented by the open circles are from South Carolina and have
weights comparable to those recorded by Viparina & Just (1975) for nonoverwintering R. catesbeiuna tadpoles in Kentucky. Given these locality data and
weights, the tadpoles in this sample probably include those that did not
overwinter (the open circles), some that overwintered one year (closed circles)
and a few (the Michigan population) that went through a second winter of
development.
The graph of P. puradoxa (Fig. 5) shows variance at a given stage similar to
that seen in R. catesbeiana. By visual inspection, there appear to be two size
groups in the Pseudis data (stars and closed circles) and a third grouping of
Lysapsus mantidacglus tadpoles (open circles). T h e sizes of the first group of
Pseudis tadpoles appear similar to the size range of the one and two year
overwintering tadpoles of Rana catesbeiana. The second group of Pseudis paradoxa
includes specimens much larger than any Rana catesbeiana I examined.
Tadpole size generally increases exponentially to stage XVII and then
declines as metamorphosis is completed (Smith-Gill & Berven, 1979). Previous
attempts to describe ontogenetic trajectories have included only the exponential
part of the growth curve (e.g. Smith-Gill & Berven, 1979). But the relationship
between maximum tadpole size and transformation size is also of biological
interest and may provide insight into why frogs have different patterns of
growth. A probability function (a 'beta distribution') was found that describes
the cross-sectional, ontogenetic, size distributions. T h e cross-sectional 'growth'
curves from stage I to stage X X V between group 2 R. catesbeiana (closed circles,
PSEUDZS SHAPE AND SIZE
99
TABLE
1. Comparison of total length (y) to Taylor Kollros Stage ( x )
cross-sectional ontogenetic curves between Pseudis and Rana
Spccies
Regression
y
y
Psendis paradoxa
Rana catesbeiana
=
=
2.60xf7.48
1.57 x+6.07
95% C.I.*
slope
95% C.I.
y-intercept
f0.58
f0.45
- 0.92
f0.78
+
*C.I. = Confidence interval.
Fig. 4) and group 1 P. paradoxa (closed circles, Fig. 5) were then compared by
linearizing the beta-distributions and using standard techniques to test for
differences in regression equations (Table 1). The results of that analysis show
no significant differences in the slopes or y-intercepts of the regressions of total
length on stage of development between the two species. That is, the length to
stage relationship is similar for overwintering R. catesbeiana and the smaller size
group of P . paradoxa.
In addition to large size, P . paradoxa is unusual in the shape of its tadpole.
There are three apparent differences between Pseudis and R. catesbeiana: the
depth of the tail, the length of the tail, and the extension of the tail keel onto the
head. Table 2 shows the relationship of tadpole body length to weight, tail
length to weight, and tail depth to weight for Pseudis and Rana from stages I to
XVII. The visual differences are confirmed. The tadpoles of the two species
have very different shapes throughout their ontogeny as indicated by the
differences in the slopes of the regressions. The deeper tail of P. paradoxa is not
just a scaling effect due to the large size of the tadpoles. From the regression
equations Pseudis and Rana of similar size would also have different tail depths.
For example, a 15-g Pseudis would have a tail depth of 37.15 mm while in a 15-g
R. catesbeiana the tail would be 25.1 mm deep. Similarly, when one adjusts for
differences in weight the R . catesbeiana tadpole is significantly shorter total length
than P. paradoxa (Table 3 ) , because Rana has a shorter tail.
DISCUSSION
Two of the principal hormones of amphibian development are prolactin and
thyroxine (White & Nicoll, 1981). Although there is some interspecific
TABLE
2. Regressions for tadpole shape
~~
~~~~
Tail depth : body weight*
Rana catesbeiana
PJeudis paradoxa
logy = 0.8822+0.440 log x
logy = 1.1900+0.325 log x
Tail length : body weight*
Rana calesbeiana
Pseudis paradoxu
Body length: body weight*
Rana catesbeiana
Psendis paradoxu
logy = 1.4019+0.338 log x
logy = 1.5340+0.305 log x
logy = 1.2617+0.278 log x
logy = 1.2037 +0.322 log x
*Covariance analysis indicated significant differences in slope, so
adjusted means could not be tested.
S. B. EMERSON
100
TABLE
3. Covariance analysis: total length versus b o d y weight for Rana
catesbeiana and Pseudu paradoxa
Sourre of variarice
d.f.
Mean square
F value
P
Equality of adjusted means
Zcro slope
Error
Equality of slopes
Error
1
1
83
1
82
0.0793
1.9505
0.0008
0.0001
0.0008
104.43
2568.24
<0.0001
<0.0001
0.11
0.741
variation, prolactin generally influences growth and inhibits metamorphosis
while rising thyroxine levels and sensitivity are thought to promote
metamorphosis. Some of the unique features of the Pseudis tadpole appear
superficially similar to the demonstrated effects of prolactin on developing
tadpoles (White & Nicoll, 1981, and references therein). Increased prolactin
levels result in longer and deeper tails (Derby, 1975; Wright, Majerowski, Lukas
& Pike, 1979), fluid retention (Jaffe & Gesahwind, 1974; Eddy & Allen, 1979),
and growth (Brown & Frye, 1969). Changes in prolactin level can result from
shifts in the hormone itself or, indirectly, from changes in thyroxine. Prolactin
antagonizes thyroxine action at specific target sites (White & Nicoll, 1981).
Rising thyroxine levels during the climax phase of metamorphosis are normally
responsible for reabsorption of the tadpole tail (Derby, 1975); when thyroid
hormone levels are depressed tail reabsorption is delayed (Lynn, 1948). PseudiJ
tadpoles not only have unusually shaped tails, but tail reabsorption is slower
than in other frogs. Pseudis retains the myotomal portion of the tail for two
weeks after metamorphosis (Kenny, 1969). I n other species tail loss is complete
within a few days of transformation (Lynn, 1948).
Unfortunately, the available data on circulating levels of prolactin and
thyroxine in developing amphibians come from only a few systems and are
somewhat contradictory (White & Nicoll, 1981; Alberch, Gale & Larsen, 1986).
It appears premature to draw any general conclusions about the precise
mechanisms through which the two hormones function in the events of
amphibian development (Alberch, et al., 1986). Additionally recent work has
indicated that control of amphibian development is more complicated than a
simple two hormone model (White & Nicoll,1981). Nonetheless, many aspects of
the morphology of Pseudis tadpoles suggest, as a n initial working hypothesis, that
a shift in prolactin levels, sensitivity or exposure time has occurred in this genus.
A similar link between gigantism and shifts in the hormonal system has been
found in a few other anuran species. Giant tadpoles of Rana esculenta and
Scaphiopus holbrooki are the result of a disturbance of the hormonal system
presumably controlled by genetical factors (Wilhoft, 1964; Borkin, Berger &
Gunther, 1981). Oversized Pelobates syriacus were found to lack a thyroid gland
and have an enlarged hypophysis (Boschwitz, 1957). When time of development
was delayed in Bombina orientalis by use of a thyroid inhibitor, the resulting
tadpoles were larger and had deeper tails than untreated tadpoles (Emerson,
unpublished).
The critical next step is to test the ‘prolactin’ hypothesis by comparing
circulating levels of prolactin and thyroxine during development in Pseudis with
those of a closely related taxon lacking giant tadpoles. Such a study would
PSEUDIS SHAPE AND SIZE
I01
provide important baseline information on circulating hormone levels as well as
examine the possible role of prolactin in the production of the giant tadpoles.
Low environmental temperatures and shifts in photoperiod length have also
been implicated in the production of giant tadpoles. I n some temperate species a
reduction in growing season or growth rate (brought about by shifts in
temperature and photoperiod) results in tadpoles that are too small to
metamorphose in a single season (Wilbur & Collins, 1973), and they pass the
winter before continuing development. This phenomenon is commonly referred
to as ‘overwintering’.
While overwintering the tadpoles continue to grow slowly but do not
differentiate. Presumably this growth is related to some level of prolactin
activity. Because overwintering tadpoles have a prolonged exposure to
prolactin, one expects a longer, deeper tail than tadpoles of the same species and
stages that do not overwinter. This change of shape between overwintering and
non-wintering R. catesbeiana is shown in Fig. 4 and Table 4. T h e lengthened
time of exposure to prolactin with overwintering does appear to produce a shape
change similar to that seen in tadpoles at increased prolactin levels in the
laboratory (Derby, 1975; Wright et al., 1979).
Overwintering most commonly occurs in summer breeding, temperate species
such as R. catesbeiana as dropping fall temperatures slow differentiation and
growth rates. In L. mantidactylus, the pseudid species which overwinters,
developmental time also increases with later breeding in the summer (Gallardo,
1964). The distribution of L. mantidactylus includes seasonal environments with
temperatures varying between 7-16°C in July and 21-27°C in January
(Gallardo, 1964). Presumably overwintering and the lengthened time of
development are related to cooler fall temperatures in this species.
The P. paradoxa tadpoles I measured included localities from Paraguay to
Venezuela. T h e largest tadpoles were from Guyana, the smallest from Paraguay
and Bolivia. It appears that there is considerable geographic variation in
tadpole size (Cei, 1980). I t does not seem likely, however, that all the
populational differences in size are due to overwintering (i.e. dropping
temperatures and/or shifts in photoperiod length). For example, in Demerara
Guyana, where some of the largest tadpoles were collected (body
lengths > 200 mm), seasonality is largely a function of rainfall, and there is little
change in day length. The mean annual temperature is greater than 80°F and
shows little seasonal variation. At least some of the Guyanan animals were
collected in roadside trenches. The temperature regime and ephemeral habitat
make it unlikely that tadpoles in this locality ‘overwinter’, in the sense the term
is usually used.
’TABLE
4. Covariance analysis: tail length versus body weight for nonoverwintering a n d overwintering tadpoles of Rana cateJbeiana
Source of variance
Equality of adjusted means
Zero slope
Error
Equality of slopes
Error
d.f.
Mean square
F value
P
1
0.0104
0.0908
0.0021
0.0050
0.0019
5.01
43.66
0.03
<0.0001
2.59
0. I24
1
20
1
19
102
S B.EMERSON
Whatever the actual mechanism producing gigantism, the enlarged tadpoles
of P. paradoxa must result from an increase in developmental time and/or an
increase in growth rate. Unfortunately, more information on the natural history
of the species is necessary before we can distinguish between these two
possibilities. The growth rate of Pseudis tadpoles is unknown except for an
anecdotal observation by Kenny (1 969) that after 4 weeks they were 55-65 mm
in length. From the calculated regression equation of length to weight a 65-mm
Pseudis weighs about 2.4 g. Rana catesbeiana has a similar weight after four weeks
of development (Viparina & Just, 1975). As the eggs of Pseudis were within the
size range recorded for other frogs of the same size (Scott, unpublished) it
appears that the early growth of Pseudis is not unusually fast despite Kenny’s
(1969) suggestions to the contrary. Kenny (1969) indicates a possible
developmental period of around six months for P. paradoxa in Trinidad. This is a
substantially longer time than that recorded for most frog species (Duellman &
Trueb, 1986).
Progenesis is defined as a shift in developmental timing where sexual maturity
is accelerated relative to somatic growth (Gould, 1977), and animals reproduce
with a juvenile or a larval morphology. Presumably Cohen & Massey (1983)
considered Pseudis “almost progenetic” because it metamorphoses at close to its
sexually mature size. They assumed some shift had occurred in the time it took
to reach sexual maturity because of the loss of the postmetamorphic juvenile
growth stage. But, in fact, there are no data to suggest that a shift in the
absolute time to sexual maturity has taken place in Pseudis. All that can be
documented at this point is that most of the body growth has been shifted from
the postmetamorphic to the premetamorphic state of the life history.
SUMMARY
Pseudis paradoxa tadpoles have some characteristics similar to those found in
tadpoles in the laboratory that have been given elevated levels of prolactin or
who have overwintered and had a prolonged exposure to prolactin. However,
more information on natural history and circulating hormone levels is necessary
before it will be possible to positively identify the precise environmental and/or
intrinsic factors responsible for the production of these giant tadpoles.
ACKNOWLEDGEMENTS
I thank the curators at the following institutions for access to museum
collections: American Museum of Natural History; National Museum of
Natural History; British Museum (Natural History); University of Michigan
Museum of Zoology; Museum of Comparative Zoology, Harvard University;
University of Kansas Natural History Museum; Florida State Museum,
University of Florida.
Norman J. Scott provided unpublished data on tadpole proportions and egg
size of Pseudis paradoxa. Dave Stephens introduced me to beta distributions and
F. Hoppensteadt worked out the linearization of a beta distribution. David
Sherman assisted in analysis of the data. H. Greene, N. Scott, J. Collins,
J. Travis, and R . Inger provided helpful comments on an earlier draft of this
manuscript. This research was supported by National Science Foundation
Grant BSR-8305998.
P S E U D I S SHAPE AND SIZE
103
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