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Fetal Maintenance and Its Evolutionary Significance in the Amphibia:
Gymnophiona
Marvalee H. Wake
Journal of Herpetology, Vol. 11, No. 4. (Oct. 31, 1977), pp. 379-386.
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Sun Sep 9 15:06:33 2007
Volume
11
31
October
1977
Number
4
Fetal Maintenance and its Evolutionary Significance
in the Amphibia: Gymnophiona
Marvalee
H.
Wake
Department of Zoology and Museum of Vertebrate Zoology,
University of California, Berkeley,
CA
94720,
USA
ABSTRACT-The oviducts of several species of caecilians are modified for maintenance of
fetal development through metamorphosis. Nutrition is provided by secretions from epithelial
cells of the duct. Nutritional demands on the parent are great. It is concluded that the
species-specific fetal dentition is functional in obtaining nutrition in the oviduct, in contrast to
previous suggestions. This mode of viviparity is found in members of three of the four families
of caecilians.
Several species of amphibians are known to retain developing young in their oviducts and
to give birth to fully metamorphosed juveniles. The majority of such amphibian species belong
to the order Gymnophiona-the blind, limbless, elongate caecilians of the tropics. Several
aspects of the reproductive biology of caecilians are correlated with the ability to bear living
young. Members of all caecilian species practice internal fertilization and have a number of
morphological and behavioral modifications to facilitate it (Barrio, 1969; Wake, 1968, 1970,
1972); females produce relatively few, but large and yolky eggs (Wake, 1968); oviducts are
capable of great distention and of secretory activity (Wake, 1970). Study of the morphology of
oviducts of pregnant and non-pregnant adult females and the way developing young are
maintained in the oviducts, as well as analysis of the developmental morphology of the fetuses,
has produced some new ideas about the mechanism of viviparity in caecilians. In addition, it
has necessitated review of previous ideas about caecilian fetal growth and nutrition.
Morphology of the Oviduct.-The gross morphology of the oviduct of several species, both
viviparous and oviparous, has been described (Parker, 1956; Wake, 1970).
A
specimen of
Dermophis mexicanus has more extensive epithelial proliferation than seen in other species.
Three 'columns' of epithelium, one ventral, two lateral, fill the lumen of the duct, except for
the space occupied by fetuses. The six 25 mm fetuses have gills, but yolk appears to be
resorbed, or nearly so.
General comments about the microanatomy of the ducts of two viviparous species,
Gymnopis multiplicata and Scolecomorphus kirkii were also presented by Wake
(
1970). Material
is now available representing the non-pregnant Gymnopis multiplicata oviduct, pregnant and
non-pregnant Dermophis, and the pregnant and non-pregnant ducts of Typhlonectes compressi-
cauda. These agree in general with the descriptions by Parker (1956) and Wake (1970). In
non-pregnant females of both species the duct is slender, 1-3 mm in external diameter.
Projections of connective tissue and capillaries covered with epithelium fill the lumen of the
duct. The histology of the oviduct has been examined in more detail in order to consider the
characteristics of the epithelium, especially the secretory cells of pregnant females. The
epithelium is a single cell layer thick, and virtually all cells are ciliated. Nuclei are large; the
1977
JOURNAL
OF
HERPETOLOGY
11(4):379-386
(379)
MARVALEE H. WAKE
surrounding cytoplasm appears stromatous but not granular. With pregnancy, the oviduct dilates
and the luminar projections ramify. The epithelial layer proliferates, and as the connective
tissue-capillary projections ramify, they "enclose" thick beds of epithelium so that glands as
described by Parker (1956) are formed. These are deep multicellular pockets with 'necks' to the
lumen of the oviduct. The cells comprising the glands are not ciliated, nuclei are less deeply
stained, and the cytoplasm is granular.
It is not unusual for oviducal epithelia in mammals to undergo changes from non-
secretory to secretory states in
a
cyclic manner, and the cytological modifications noted above
are characteristic for such states (Bloom and Fawcett, 1968:744-745). Bloom and Fawcett also
state that there are no true glands in the mammalian oviduct and that true glands form by
invagination of epithelia into the basal connective tissue. It appears that the 'glands' of
caecilians are epithelial beds enclosed by connective tissue ramifications. Thus caecilians, and
perhaps other lower vertebrates, lack true glands in the oviducts according to Bloom and
Fawcett's definition of glands.
As noted previously (Wake, 1970), the oviducal epithelium of females carrying small (less
than 50 mm total length) fetuses is intact, and the 'glands,' which I shall refer to as secretory
beds, are extensive. In females carrying larger fetuses, the epithelium is no longer present lining
the lumen in areas around the fetuses, and capillaries and connective tissue comprise the
luminar surface. However, the epithelium is intact well anterior and posterior to the fetuses.
The secretory beds of the oviduct in the vicinity of the fetuses are elongate and deep. In the
most dilated, thinnest-walled oviducts (of female G ymnopis and Typhlonectes carrying several
fetuses of over 100 mm total length), the secretory beds are several millimeters long. They are
disposed parallel to the long axis of the duct, and are often only
a
single secretory cell layer
deep. These secretory beds are of particular significance in viviparous forms, for they secrete
a
nutritive substance that is ingested by the fetuses (Parker, 1936, 1956). The glandular se-
cretion, or 'uterine milk,' was characterized by Parker as
"a
thick white creamy material
consisting mainly of an emulsion of fat droplets, together with disorganized cellular material"
when seen in the stomachs of freshly killed fetuses. Parker also states that many of the fetuses
that he examined had full stomachs, containing (in preservation) "an amorphous non-cellular
mass, but often containing a considerable amount of cellular debris and sometimes some
recognizable erythrocytes." My observations on mouth and stomach contents of fetuses of
several species corroborate his.
I suggest, then, that 1) the epithelium proliferates and becomes secretory at the time
fetuses reach 25-50 mm in length and have nearly resorbed their yolk; 2) that the entire
oviducal epithelium is potentially secretory; 3) that the connective tissue of the inner oviducal
wall ramifies and nearly encloses beds of proliferated secretory epithelium; 4) that
as
oviducal
dilation occurs and epithelium is stripped, the secretory beds remain intact so that sufficient
nutrient substance is secreted to meet fetal nutritional requirements. Histochemical studies are
in progress to determine the nature of the cellular changes, and to determine the components
of the secretion.
Fetal development.-Information on numbers of fetuses in the oviducts of members of the
seven known viviparous genera is scattered. Parker and Dunn (1964) report 2-7 in Schist-
ometopum thomense, Barrio (1 969) reports 6-10 in Chthonerpeton indistinctum; my own
dissections show 1-9 in Typhlonectes compressicauda, 3-4 in Geotrypetes seraphini, 1-12 in
Dermophis mexicanus and 2-8 in Gymnopis multiplicata. Fetuses are usual1 y disposed in nearly
equal numbers in each of the two oviducts. In general, large (6
X
4
X
3 mm) yolky eggs are
taken into the oviducts. Embryos are contained in the egg membrane until much of the yolk is
resorbed, gills are developed, and coordinated movement is possible. The embryos emerge from
the egg membrane at about 10-12 mm in Gymnopis (my data), and 25 mm in Geotrypetes
(Parker, 1956). The fetuses then uncoil and align themselves lengthwise, or with the posterior
one third of the body curved toward the head. My dissections show that small fetuses are
nearly equally spaced in the oviduct and that larger ones do overlap, but their heads are not in
FETAL MAINTENANCE IN GYMNOPHIONA
close association. The embryos and fetuses of Gymnopis, Typhlonectes, and Dermophis have
gills during most of their oviducal existence. The gills of Schistometopum and Geotrypetes are
resorbed shortly after emerging from the egg membrane (Parker and Dunn, 1964). All terrestrial
species have a pair of triramous fimbriated gills; the aquatic typhlonectids have paired sac-like
gills. Both forms of gills are supplied by three aortic vessels. There is some indirect evidence
that gills may be used in gaseous exchange in association with the oviducal epithelium.
Preserved Gymnopis (Wake, 1967, 1969) and Dermophis fetuses frequently are found with one
gill extending above the head and the other along the body and appressed to the oviduct wall.
In Typhlonectes fetuses often have one sac-like gill extended above the head and one down
cloaking the body. The gills are some two-thirds of the length of the fetus, and when the sac
structure of the gill is flattened, it
is
a highly vascularized plate lining much of the
circumference of the oviduct. The oviduct, too,
is
highly vascularized, so gaseous exchange
is
possible. This gill positioning occurred in 24 of 35 fetuses observed in six pregnant female
Typhlonectes. This sugggests that it is a common, perhaps efficient functional arrangement.
Parker and Dunn (1964) suggest that cutaneous exchange may be important, especially for
species whose gills are resorbed early. Gills are resorbed before birth in all forms.
The fetal dentition may be resorbed before birth, or shortly afterward. The edult dentition
is
usually acquired after birth, but may develop in utero (Parker, [I9561 reported
a
145 mm
fetus of Dermophis that has an adult dentition, and in utero acquisition
is
possible in
Chthonerpeton [Parker and Dunn, 19641). According to Parker (1956) newborn Geotrypetes
retain the fetal dentition,
as
do some Gymnopis multiplicata (Taylor, 1955). Parker and Dunn
(1964) note that small (126-161 mm) juveniles of Caecilia tentaculata and C. subnigricans have
a fetal or mixed fetal-adult dentition. This is of significance for it is not known whether
members of the genus are oviparous or live-bearers. Dunn (1942) states that Caecilia probably
lays eggs (for reasons not mentioned other than the 1845 specimen). Gill slits are present in
lchthyophis larvae after hatching and gill resorbtion (Sarasin and Sarasin, 1887-901, but I have
not seen open gill slits in any oviducal embryos. Tschudi (1845) reported a free-swimming
'larva' of C. tentaculata that had open gill slits, but no gills. It is difficult to determine just
what Tschudi was looking at; it
is
possible that he observed the 'collar' annuli which are often
incomplete. It is also possible that the species
is
viviparous, because of the presence of a fetal
dentition. The presence of a fetal dentition in two species and the complete absence of any but
adult-type teeth in all of the known oviparous species allow the inference that the genus
Caecilia may include at least two viviparous species.
There is substantial variation in size of fetus
at
birth. Parker and Dunn (1964) report
birth in Geotrypetes
at
73-77mm fetal total length; Heinroth (1915) records birth at
190-210 mm in Typhlonectes compressicauda. Based on Parker and Dunn's data, birth in
Dermophis mexicanus occurs at approximately 150 mm, and Taylor's (1955) data and my
information indicate that birth takes place
at
110-130 mm in Gymnopis multiplicata. There
appears to be some gross correlation of fetal size with maternal size; adult Geotrypetes are from
235 to 400 mm, the majority of pregnant specimens from 270 to 320 mm; adult Typhlonectes
from 250 to 625 mm, with most (75%) of the pregnant females that I have examined being 330
to 500 mm; mature Gymnopis are 250-500 mm, with pregnant females of Gymnopis of
different sizes show little correlation of size of fetus with size of female within a species. A
maximum fetal size (and state of development) of 110-130 mm was found in females of 283,
341, and 392 mm, so it would appear that fetuses reach that size before birth no matter what
the size of the maternal female.
The demands upon the female for nutrition are very great. Yolk
is
resorbed in
Geotrypetes seraphini at 25-40 mm (Parker, 1956); Geotrypetes angel;, 38 mm; Schistometopum
thomense, 32-36 mm (Parker and Dunn, 1964); Typhlonectes compressicauda, 29-40 mm; and
Gymnopis multiplicata, 24-38 mm (the latter two species from my data). Geotrypetes young of
77 mm may be born of a 235 mm female (each fetus is 32% total length of the maternal
female) (Parker and Dunn, 1964). One hundred twelve mm young of Schistometopum are 57%
the length of the mother, 125 mm young may be born of a 250 mm Gymnopis (50% maternal
382
MARVALEE
H.
WAKE
length), and 200 mm Typhlonectes of 330 mm females (60% maternal length). All measure-
ments are from museum specimens. These percentages may reflect extremes in which
'normal-sized' young are born of small females, and the percentages are reduced for larger
females (for example, a 200 mm young born of
a
500 mm Typhlonectes is 40% of the maternal
total length), but these ratios are still significant. A female Typhlonectes may bear as many as
nine young. The embryos resorb their yolk at approximately 30 mm; they are born at
approximately 200 mm, having increased their lengths 6.6 times during the period of maternal
nutrition. Nine fetuses, each increasing 6.6 times in size, and each 60% of the female's total
length at birth, present great nutritional demands on the maternal female. My data do not
indicate that females carrying large numbers of young have smaller young than females of the
same size with fewer young, nor that females with large numbers of young give birth any earlier
than females with fewer young. However, smaller females may have fewer young. My samples
are small, however, and concrete data consisting of X-rays of females before birth to check fetal
number and growth with records of live births or significant samples of preserved pregnant
females are needed to adequately consider these aspects of reproductive biology.
The mode of fetal nutrition and its evolutionary significance.-Parker (1956) said that
fetuses ingest the 'uterine milk' by mouth, but did not say how. He also stated that the fetal
teeth of Geotrypetes were used after birth to scrape algae from rocks and leaves of the watery
substrate where the animals were found. He suggested that the fetal teeth of Geotrypetes might
function as a rasping organ during early post-partum life (1936, not 1956 as Taylor [I9681
states). He has since (1956, and Parker and Dunn, 1964) steadfastly denied that the fetal
dentition is functional at all. It is interesting that the general conception has been that the fetal
teeth are used to scrape the oviducal wall (Goin and Goin, 1971; Porter, 1972; Salthe and
Mecham, 1974; Taylor, 1968) even though Parker, the only modern worker who has examined
the teeth, has denied their use in that manner. Some (Porter, 1972; Taylor, 1968) have
attributed to Parker the conclusion that teeth were so used.
I propose to substantiate the conclusion that the fetal dentition is functional, and that it
is used to obtain nutrition while fetuses are developing in the oviduct. Parker (1956) stated that
the "special foetal dentition can scarcely be an adaptation for.
.
.
a special foetal mode of
nutrition." He stated that 1) the teeth are apparently unsuitable for the ingestion of milk, 2)
that such an adaptation could not credibly have arisen more than once, and that if it has so
arisen, all the viviparous species would be a close phyletic assemblage, which he pointed out
they are not.
As to the assertion that the teeth are unsuitable for the ingestion of "milk," one must
consider the mechanisms by which it
is
ingested. If milk were simply sucked into the mouth, or
the fetus were passive
as
milk somehow flowed into its open mouth, teeth would not be
necessary. However, I have found epithelial cells and smooth muscle fibers in 'uterine milk' in
the mouth and gut embryos; I have reported the apparent stripping of the epithelium of the
oviduct in the vicinity of the heads of larger fetuses (Wake, 1970). It appears that the teeth are
used to scrape the oviduct lining, stimulating secretion of the 'milk' (as Salthe and Mecham
[I9741 also suggested), and helping to gather the milky secretion. The teeth also bite areas of
the proliferated epithelium, probably effecting more secretion by irritating the secretory cells.
The shapes and arrangements of teeth facilitate these actions (Wake, 1976). In addition, an
out-group comparison with fetuses of Salamandra which use a similar method implies function.
Further, Norris and Prescott (1959) concluded that the flexible jointed teeth in adult Girella
nigricans are adapted for scraping. They postulate that such teeth are able to scrape a greater
surface area of subtidal rocks to obtain algae.
Fetuses are prevented from eating through the dilated oviduct in several ways. The teeth
are flexible and very tiny with
a
rather weak joint at the crown-pedicel junction (Wake, 1976).
This suggests that they are used for holding tissue, not incising through it. The soft proliferated
epithelial tissues could be torn if held by the teeth as the head is turned, but the tissue
association in the oviduct seems to be one that allows epithelium to tear away from the
connective tissue without serious damage. If the mouth were to open sufficiently widely to
383
FETAL MAINTENANCE IN GYMNOPHIONA
place the teeth on the concave surface of the duct, the tension of the wall would cause it to
maintain position so the mouth could not close on it in order to effect a bite. In addition,
fetuses of many species begin resorbtion of teeth before birth, beginning with the outer rows,
thus further lessening the possibility of biting the oviducal wall at the time of greatest duct
dilation. Condition of the duct epithelium suggests that
as
the fetuses stimulate secretion by
scraping, they also ingest areas of proliferated tissue as well
as
their secretions, then move in
the oviduct to an adjacent, un-ingested area. Secretory cell proliferation continues in these
adjacent areas, and in the secretory beds encased in connective tissue, so a supply of nutrient
material
is
assured.
Parker's (1956) and Parker and Dunn's (1964) conclusions about the evolutionary history
of fetal and adult dentitions can also be challenged.
Parker and Parker and Dunn's arguments about evolutionary relationships are based on
the presence of polystichy (multiple rows of teeth) in fishes, in some extinct orders of reptiles
and amphibians, and in certain extant salamander families. They note that polystichy is
frequently restricted to palatal and pharyngeal bones, (ignoring the facts that those specimens
are adults, and the teeth are functional in those specimens). They did point out that the extinct
amphibians and reptiles are not known to change either tooth morphology or number of rows
of teeth, again ignoring the implication of functionality. They cited examples from various
salamander genera whose larvae lose patches of teeth
at
metamorphosis, but
do not replace
them at all
as
adults, and also cite instances in salamanders in which a mixed polystichous-
monostichous (single-rowed) condition exists on particular elements. They note that
a
change
to
a
totally monostichous condition as in adult caecilians is doubtful (their term) among most
salamanders, but state that such a change does occur in
Salamandra atra
and
S.
salamandra.
The
adults of these species do, indeed, have a monostichous dentition following a polystichous one.
Parker and Dunn failed to note that these are two of the exceedingly few species of
salamanders known to be live bearers, and omitted the significance of that fact relative to the
question of the function of the caecilian fetal dentition. In fact, it
is
well known that oviducal
young of
Salamandra
ingest the oviducal wall, maternal red blood cells, and even their siblings
(Amoroso, 1952)-probably using their polystichous dentition. Parker and Dunn point out that
several salamanders shift from
a
monocuspid to
a
bicuspid tooth morphology
at
metamorphosis;
this is indeed
a
shift, though not as radical
a
one
as
that in viviparous caecilians.
They explained the multiple-rowed fetal dentition in terms of Edmund's Zahreihen theory
(19601, apparently accepting travelling stimuli
as
real. Their interpretation according to
replacement theory of the acquisition of multiple rows is sound, for it merely involves retention
of generations of replacement teeth. Further, their analysis of the acquisition of several cusps
on the fetal teeth points out that this may merely involve elaboration of the two cusps of
adults, which,
as
Kerr (1960) stated, are parallel crescent-shaped ridges. They consider that
delay in replacement series to produce the polystichous fetal dentition, with acquisition by
adults of
a
genetic restriction to monostichy, is a reasonable mechanism to explain the change,
but that it does not account for change in tooth form and change in site and arrangement of
teeth. Fetal tooth development and replacement are analyzed by Wake (1976).
Some of Parker's assumptions about caecilian phylogeny are faulty; for example, he stated
that gills in American genera are single and plate-like, while the African forms have triaxial gills.
Triaxial gills occur in all of the American forms except typhlonectids. It is true that viviparity
is
not evidence of close phylogenetic relationship, for
it
occurs in three of the four families of
caecilians.
Parker contended that the fetal dentition is a primitive ancestral character retained
as
a
result of
lack
of function. He concluded that free-living larvae and adults of all species, as
predaceous carnivores, suppressed many-rowed, hinged, multicusped teeth in order to have more
functional single rows of rigid teeth. He postulated an ancestral amphibian with many rows of
hinged teeth on all of its dentigerous elements, and commented that previous workers
considered
a
rasping dentition as 'ichthyic' and suggests that the dentition might be associated
with a vegetarian diet. In that context, he considered caecilians the most primitive order of
384
MARVALEE
H.
WAKE
amphibians. I believe that caecilians are derived amphibians. Among the characters that I
consider derived is the fact that all caecilians apparently practice internal fertilization. This is a
necessary precursor of viviparity, and
a
far greater number of caecilian species than of those of
other amphibian orders are viviparous. Parker and Dunn are concerned that polystichy cannot
have arisen more than once. It is generally conceded that oviparity
is
the primitive condition.
Parker and Dunn do not seem concerned that viviparity must have arisen more than once, since
it
is
only the derived viviparous forms that have the fetal dentition. Though at the time that
Parker made his analysis all caecilians were included in
a
single family, he must have been aware
that viviparity occurs in a mosaic of genera, and that these genera were not the ones considered
primitive on the basis of other characters. Viviparity is now known to occur in three of the
four currently recognized caecilian families (Cae-
ciliidae of both New and Old World, the New World
TABLE
1.
Viviparous species of caecilians.'
Typhlonectidae, and the east African Scoleco-
morphidae). The Caeciliidae comprise both egg-
Family Caeciliidae
Caecilia subnigricans
laying and live-bearing species; several species of
Caecilia ten tacula ta
typhlonectids are known to be viviparous and none
Dermophis mexicanus
to
be
oviparous, and it is likely that all species of
Caecilia oaxacae
these aquatic genera are live-bearing. One species of
Caecilia parviceps
Scolecomorphus
of the monogeneric Scoleco-
Georrypetes angeli
Geotrypetes seraphini
morphidae is known to be viviparous, and nothing is
Gymnopis mulriplicara
known of other species in the genus. Table 1 lists
Schistomeropum homense
the known viviparous species of caecilians. It is
Family Scolecomorphidae
possible that
a
single caeciliid stock gave rise to
Scolecomorphus uluguruensis
viviparous caeciliids in Central and South America
Family Typhlonectidae
and East and West Africa and that the typhlonectids
Ch thonerpeton indistinc tum
and scolecomorphids were subsequently separately
Chthonerperon viviparum
derived from viviparous forms in South America and
Nectocaecilia peters;
east Africa, respectively. There are no dates to
Nectocaecilia ladigesi
Typhlonectes compressicauda
support times of derivation of these stocks, nor any
Typhlonectes natans
information about their reproductive states in evolu-
Typhlonecres obesus
tionary time. However, one need not argue so
conservative an origin, for viviparity
is
thought to
"Oviducal embryos or newborns with fetal
evolve as fertilized eggs are retained in the oviducts
dentitions are known for these species. Addi-
tional species
in
the above and other
for periods of time, and any mechanism for maternal
are suspected to be viviparous.
nutrition is present. No one argues that viviparity in
teleost fishes or in reptiles arose only once, and there
is
substantial evidence for its multiple origin in these
groups.
Another point that Parker clearly appreciated, but ignored in his evaluation of the
evolution and function of the fetal dentition, is that of the distinct differences in morphology
of the fetal dentition among species. Not only are they very different from the adult-type
developing teeth of embryos of egg-laying species, but there are real differences among
viviparous species. These differences are discussed in detail by Wake (1976). Parker does not
account for those differences at all. I suggest that the most plausible explanation for those
differences in external tooth structure among fetal dentitions
is
that selection has produced an
effective dentition in each species. This is not to say that the dentition arose
de novo
in related
species. As an adaptive radiation of caecilian species took (and takes) place, selective factors
influencing the fetal dentition,
as
well
as
other characters, operated according to the discrete
species substrate available, resulting in species-specific modifications of the dental pattern in
fetuses. The tooth morphology of fetuses in each viviparous species is well adapted for use
as
a
scraping device. If the fetal teeth are of adaptive significance,
as
implied by the production of
morphological change through evolution, they likely are functional. Several pieces of evidence,
especially the distinctive morphology and arrangement of the fetal teeth and the presence of
385
FETAL MAINTENANCE IN GYMNOPHIONA
maternal cells in the gut of the fetus, cause me to conclude that the fetal dentition is
functional, and used to stimulate secretory cells of the oviducal epithelium, and to gather and
ingest the 'uterine milk' and components of the oviducal wall. This is a highly derived mode of
viviparity, seen among vertebrates in some elasmobranchs, in live-bearing caecilians, and two
species of salamanders. While placentation is not involved, maternal nutrition of oviducal young
occurs, and gaseous exchange across fetal skin and gills to oviducal capillaries may also take
place. I conclude that viviparity, and with it the fetal dentition, has arisen in caecilians
following the retention of developing eggs by members of several lineages.
ACKNOWLEDGMENTS
I
thank Dr. Jay M. Savage, University of Southern California, for loan of
Gymnopis
multiplicata,
and Dr. John Wright, Los Angeles County Museum of Natural History, for loan of
Typhlonectes compressicauda.
I
am particularly grateful to Theodore Papenfuss, Museum of
Vertebrate Zoology, University of California, Berkeley, for collecting the
Geotrypetes seraphini
used in this work. Histological materials were prepared by Addye Brown, Department of
Anatomy, University of Chicago, and Penny Hermes and Cindy Hillery, Department of Zoology
and Museum of Vertebrate Zoology, University of California, Berkeley. Teriann Asami typed
the manuscript. Parts of this work were supported by National Science Foundation grants GB
6432X and GB 17112 to David B. Wake, Museum of Vertebrate Zoology, University of
California, Berkeley, and by funds to the author from the Committee on Research of the
University of California and from Biomedical Sciences Support Grant RR-7006 from the
General Research Support Branch, Division of Research Resources, Bureau of Health Professions
Education and Manpower Training, National Institutes of Health. Finally,
I
thank David B.
Wake and Ronald Lawson for critical consideration of the manuscript.
LITERATURE CITED
Amoroso, E. C. 1952. Placentation. Pp. 127-31 1
in
Marshall's Physiology of Reproduction. vol. 2. Longmans,
Green Co. London.
Barrio, A. 1969. Observaciones sobre
Chthonerpeton indistincturn
(Gymnophiona, Caecilidae) y su reproduc-
cion. Physis 28:499-503.
Bloom,
W.
and D. Fawcett. 1968. A Textbook of Histology. Ninth Ed.
W.
B. Saunders Co. Philadelphia. 858
PP.
Dunn, R. E. 1942. The American Caecilians. Bull. Mus. Comp. Zool. Harvard. 91:439-540.
Edmund, A. G. 1960. Tooth replacement phenomena in the lower vertebrates. Contr. Life Sci. Div. Roy.
Ontario Mus. 52: 1-190.
Goin, C. J. and
0.
B. Goin. 1971. Introduction to Herpetology. Second Ed. W.
H.
Freeman and Co. San
Francisco. 353 pp.
Heinroth,
0.
1915. Geburt von
Typhlonectes natans
(Blindwuhle) in Aquarium. B. Aquar. Terrienk. 26:34.
Kerr,
T.
1960. Development and structure of some actinopterygian and urodele teeth. Proc. Zool. Soc.
London. 133:401-422.
Norris,
K.
S. and J.
H.
Prescott. 1959. Jaw structure and tooth replacement in the opaleye,
Girella nigricans
(Ayres) with notes on other species. Copeia 1959(4):275-283.
Parker, H. W. 1936. The amphibians of the Mamfe Division, Cameroons. Proc. Zool. Soc. London
1936: 135-163.
.
1956. Viviparous caecilians and amphibian phylogeny. Nature 178:250-252.
and E.
R.
Dunn. 1964. Dentitional metamorphosis in the Amphibia. Copeia 1964:75-86.
Porter,
K.
R. 1972. Herpetology.
W.
B. Saunders Co. Philadelphia. 524 pp.
Salthe, S. N. and J. S. Mecham. 1974. Reproductive and courtship patterns. Ch. 5. Pp. 309-521,
in
Physiology of the Amphibia, Vol. 2, B. Lofts, ed. Academic Press, New York.
Sarasin, P. and F. Sarasin. 1887-1890. Ergebnisse naturwissen Forschungen auf Ceylon in den Jahren
1884-1886. Zur Entwicklungsgeschichte und Anatomie der Ceylonesischen Blindwuhle
lchthyophis
glutinosus.
C. W. Kreidel's Verlag, Wiesbaden. pp. 1-263, 24 plates.
Taylor,
E.
H. 1955. Additions to the fauna of Costa Rica. Univ. Kansas Sci. Bull. 37:499-575.
.
1968. The Caecilians of the World: A Taxonomic Review. University of Kansas Press,
Lawrence, Ka. 848 pp.
Tschudi, J. J. von. 1845. Untersuchungen uber die Fauna Peruana. Herpetologie. 1-80. Druck und Verlag von
Scheitlin und Zollikoffer. St. Gallen.
MARVALEE
H.
WAKE
Wake, M.
H.
1967. Gill structure in the caecilian genus
Gymnopis.
Bull. So. Calif. Acad. Sci. 66:109-116.
.
1968. Evolutionary morphology of the caecilian urogenital system. Part I. The gonads and fat
bodies.
J.
Morph. 126(31:291-332.
.
1969. Gill ontogeny in
Gymnopis.
Copeia 1969:183-184.
.
1970. Evolutionary morphology of the caecilian urogenital system. Part
11.
The kidneys and
urogenital ducts. Acta Anat. 75:321-358.
.
1972. Evolutionary morphology of the caecilian urogenital system. Part IV. The cloaca.
J.
Morph. 136(31:353-366.
1976. The development and replacement of teeth in viviparous caecilians.
J.
Morph.
148(11:33-64.
You have printed the following article:
Fetal Maintenance and Its Evolutionary Significance in the Amphibia: Gymnophiona
Marvalee H. Wake
Journal of Herpetology, Vol. 11, No. 4. (Oct. 31, 1977), pp. 379-386.
Stable URL:
http://links.jstor.org/sici?sici=0022-1511%2819771031%2911%3A4%3C379%3AFMAIES%3E2.0.CO%3B2-W
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Literature Cited
Jaw Structure and Tooth Replacement in the Opaleye, Girella nigricans (Ayres) with Notes on
Other Species
Kenneth S. Norris; John H. Prescott
Copeia, Vol. 1959, No. 4. (Dec. 30, 1959), pp. 275-283.
Stable URL:
http://links.jstor.org/sici?sici=0045-8511%2819591230%293%3A1959%3A4%3C275%3AJSATRI%3E2.0.CO%3B2-V
Dentitional Metamorphosis in the Amphibia
H. W. Parker; E. R. Dunn
Copeia, Vol. 1964, No. 1. (Mar. 26, 1964), pp. 75-86.
Stable URL:
http://links.jstor.org/sici?sici=0045-8511%2819640326%293%3A1964%3A1%3C75%3ADMITA%3E2.0.CO%3B2-V
Gill Ontogeny in Embryos of Gymnopis (Amphibia: Gymnophiona)
Marvalee H. Wake
Copeia, Vol. 1969, No. 1. (Mar. 6, 1969), pp. 183-184.
Stable URL:
http://links.jstor.org/sici?sici=0045-8511%2819690306%293%3A1969%3A1%3C183%3AGOIEOG%3E2.0.CO%3B2-0
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