Ontogenetic Evolution in Frogs

Ontogenetic Evolution in Frogs
Author(s): Bertha Lutz
Source: Evolution, Vol. 2, No. 1 (Mar., 1948), pp. 29-39
Published by: Society for the Study of Evolution
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ONTOGENETIC EVOLUTION IN FROGS
BERTHA LUTZ

Mfutseit
Nacionial, Rio de Jmieiro,Brazil

Received January 5, 1948

The studyof evolution the ontogeny
in GENERAL TREND
of the Frogs (Order Salientiaor Anura) The general trend of modifiedsalien-
has been rather neglected. They have tian ontogenyis towards withdrawalof
probablybeen dismissed as one of the development fromwater. Modifications
minor orders of the vertebrate phylum, of reproductive behavior,habitat prefer-
characterized a well-known cycle,
by life ences and ecotopic adaptations of the
whichcomprisesan aquatic larval period adults are correlatedwith it. The most
and metamorphosis into terrestrial tetra- importantmorphologicalchange is the
pods. The tropicaland subtropical frogs
increase of yolk reserves. Acceleration
show many deviations from this mode
of development also occurs.
of development. At the present time,
Most of the changesobservedare cae-
the lifehistories less than one-third
of of
the describedspecies of frogsare known nogenetic. They affect the embryosand
(Orton, 1946). It seems probable that sometimes larvae and are alreadyin-
the
as the openingup of this fieldproceeds dicated by the size of the unfertilized
otherunusual lifehistories will be added ovum. It seems best to includethemin
to those already describedin the much the generalconceptof clandestine evolI-
scatteredliterature. The very factsthat tion (De Beer, 1930), which must have
the Amphibiaare the most complexver- a very wide field of applicationin em-
tebratesin whichlarvae occur,thatthose bryology. Such changescannotbe regis-
of the Salientia are not always aquatic tered by paleontology and are accessible
and are sometimes replacedby directde- to comparativeanatomy only during a
velopment, oughtto maketheorderinter- transient phase. As long as anuran tax-
esting fromthe point of view of onto- onomycontinuesto be based exclusively
geneticevolution. on adult morphologythey will be left
The present preliminarysurvey is aside in establishing phylogeneticalrela-
based on a numberof peculiarmodes of tionships.
anuran development observed in south- Some of thenovelties monophyletic.
are
eastern Brazil, in the course of many Others recur in different regions under
years, by the late Professor Adolpho similar ecological conditions and, with
Lutz, the author,and theirassistantMr. variationsas to detail,in groups consid-
Joaquim Venancio, and recorded either ered as phylogenetically distinct. Where
forthefirst time(Lutz, 1928, 1929, 1931; instancesof parallelor convergent evolu-
B. Lutz, 1944; Lynn and B. Lutz, 1946, tion appear to be absentthis may be due
1947), or in confirmation earlierwork.
of to the lack of similarecotopes1 or, more
Parallel or convergent cases fromother likely,to their not having been investi-
regions may be mentioned but the data gated. It is, however,only fair to state
available do not permitdetailedcompari- of
that the presentsystematics Salientia
son. (For factualliterature Brandes
see and in need ol revision.
is artificial
and Schoenichen, 1901; Noble, 1925, 1 Ecotope- ecological niche; ecotopic= relat-
1927, 1931; B. Lutz, 1947). ing to an ecotope. Ed.
EVOLUTION 2: 29-39. March, 1948. 29

30 BERTHA LUTZ

TABLE 1. Comparative
tableof development

Name Placementof eggs Stage at hatching Subsequent development
HYLIDAE
Hyla decipiens On open leaves Rudimentary larva Aquatic
Centrolenella On open leaves Fully formed
larva Aquatic
Phyllomedusa Leaves foldedover the Fully formedlarva Aquatic
clutch
CoelonotousHylidae Back of 9 (in singlemass) Submetamorphic Aquatic (in adult habitat)
larva
PIPIDAE
Pipa Back of 9 (in individual Adult form Simple growth
chambers)
BRACHYCEPHALIDAE
Rhinoderma darwinii Vocal sac of e? Adult form Simple growth
BUFONIDAE
(sensu stricto)
Cyclorhamphus fuliginosus Wet ledges of rock Larva Semi-aquatic (glidingon
Cyclorhamphus pinder rocks)
Thoropapetropolitanal Wet outcropsof rock Larva Semi-aquatic (glidingon
Thoropamiliaris rocks)
Zachaenusparvuluts Hollows in banks Terrestrial
larva Terrestrial: hollow
In
LEPTODACTYLIDA E
Eupemphix, Physalaemus Edges of pools Rudimentarylarva Aquatic
Leptodactylusflavopictus I
Leptodactylus pentadactylts Pot-shapedholes Larva Aquatic
(Brazilian form) f
Leptodactylus mystaceuts Earthen nestsopen below Larva Aquatic (semi-permanent
water or damp spots)
nanuts
Leptodactylus Closed earthennests with lairva
Terrestrial Terrestrial(in nest)
aperturein roof
BUFONIDAE
(sensu lato)
Eleutherodactyluts Varied: Hollows, Brome- Adult form Simple growth
liads, etc.

Withdrawalof development from water descentinto water for this purpose; the
is achieved by diverse devices and to reason forit is readilyapparentin Phyl-
varyingdegrees. In some cases special lomedusa, which has no webs between
typesof aquatic or of damp environments the digitsand avoids swimming.
are utilized. In other cases water is Changes of reproductive behaviorand
altogether avoided. The alternative sites habitat preferences merge into ecotopic
for placementof the eggs and ontogeny adaptations selection theusual sense.
by in
are quite varied but may be reducedto a
few main categoriesas shown in table 1. SELECTION PRESSURE

The withdrawalof development from
Organic Selection waterand the correlated ecotopicadapta-
The modifications reproductive
of be- tions of the adults have an interesting
havior and the habitatpreferences the feature common, regardto selection
of in in
adults obviouslyfall withinthe scope of pressure.
organicselection, selectionof the en-
i.e. Adult Salientiaare preyedupon by ar-
vironmentby the organism (Baldwin, boreal snakes,birds,a few mammalsand
1896; C. Lloyd-Morgan,1900, as cited larger membersof their own order and
by J. Huxley, 1942). To take but a few sometimes theirown genus and species.
of
examples: the genus Cyclorhamtphus has They are attackedby leeches,mites,ticks
become closely adapted to a troglodytic and mosquitoes. They have evolvedvar-
way of life, but other neotropicalfrogs, ious devices against predators,such as
like some species of the diurnal,running concealingor aposematiccoloration, pro-
watergenusElosia, seek shelter grottos tectiveresemblance theirbackgrounds
in to
at night,and the,extremely arborealHyla (Cott, 1940), nocturnalhabits and the
albofrenata occasionallyheard calling choice of inaccessiblehabitats (tubular
is
in crevices. Spawningon leaves by Hy- bromeliads and bamboos, burrows and
lidae is merelyan omissionof the usual crevices,etc.).

ONTOGENETIC EVOLUTION IN FROGS 31

Interspecific competition minimized
is abundant there is generally a striking
by ecotopicdivergence bothof adults and dearthof tadpoles,especiallysmall ones.
of tadpoles. Other kinds of enemies,if present,espe-
The enemies of larval salientiansare ciallythe water-fowl,may also take their
notthesame as thoseoftheadults. With toll. Under these circumstances spawn
the possible exception of aquatic birds has to be abundant to insure survival
and snakes, fish and a few freshwater Eggs are verysmall and numerous, rang-
invertebrates, chiefpredatorson tad-
the ing fromhundredsto thousands.
poles are aquatic insects (see table 2). In the mountainstreamsof southeast-
In Brazil, at the timeof spawningnu- ern Brazil, the numberof species of tad-
merous species of frogs congregateat poles is very much reduced and those
most still waters, especially the ponds present resort to special niches. Some
and lagoons of the mote arid sectionsof (Centrolenella eurygnatha) hide under
the country. There, the beginning theof dead leaves and otherdetritus whichac-
rainyseason coincideswith flooding and cumulates in the still reaches. Others
with the onset of the breedingperiod of (Phyllomnedusa guttata) floatin schools,
the anurans. Available habitatsare less breakingthe surfacewith theirenlarged
varied than in the rain and mist forest. dorsal mouth-funnel.A few Hyla tad-
Many tadpoleshave to compete witheach poles cling with their lips and teeth to
otherforfood and are exposed to preda- the rocks. Those of Elosia hide between
tion. Such waters have populationsof stones at the bottom. Delayed hatching,
well-armored insects, carnivorous
the hab- as in the first
two speciesmentioned, pro-
its ofwhichcan be observedin natureand vides additionalprotectionagainstaquatic
in
are described the literature (see Need- insects,which are generallynot so large
ham and Lloyd, 1916 and Costa Lima, as those of the still waters. Fish are
1939-43). Where predatory insectsare mostlyabsent or rare and small if pres-

TABLE 2. Insect enemiesof tadpolesin S.E. Brazil

Taxonomicgroups Habitats Abundance Stages Feeding habits
PLECOPTERA Mountain streams Common Nymphs Carnivorous
DONATA
ODONATA water
fJStill Verycommon Naiads Carnivorous; have been rearedon tad-
Ibromeliads Common poles
TRICHOPTERA Mostly mountain Verycommon Larvae Herbivorous,occasionally carnivo-
streamsin S.E. rous; once seen attackinga small
Brazil tadpole in laboratory
HEMIPTERA
Nepoidea:
(a) Belostomatidae:
Lethocerus (giant Still waters Very abundant Nymphs Attackstadpoles
forms;may ex- and
ceed 100 mm.) imagines
Belostoma Still waters Veryabundant Nymphs Attackstadpoles
and
imagines
(b) Naucoridae:
Cryphocricus Mountain streams Ratherrare Nymphs Predatory
(still reaches) and
imagines
(c) Nepidae:
Ranatra Still waterand Not verycommon Nymphs Predatory
marshes and
imagines
iaie
COLEOPTERA
Diving Beetles:
(a) Hydrophylidae Still water Swarms Larvae - Carnivorous. Larvae verypredatory;
(b) Dytiscidae and an adult seen attackinga Phyllomtze-
imagines dusa tadpole
DIPTERA
(a) Tabanidae Bromeliads Some species Larvae Carnivorous
commonin
certainlocations
(b) Syrphidae: Bromeliads Some species Larvae Carnivorous
commonin
certainlocations
Rhysopsberthae ? Fairly commonin Larvae Parasitic on eggs of Centrolenelta
certainlocations eurygnatha

32 BERTHA LUTZ

ent. Kingfishers sometimes
are seen fly- have concealingcolorationand those of
ing near the banks of streamsand, occa- Thoropa are protectedby their resem-
sionally, water-ouzels are observed on blance to the wet outcrops of rock on
them. whichtheylive. The dimensions theirof
Bromeliadscontairn manyforms ani- habitatsare ample enoughto make inter-
of
mal life, includingsmall snakes, lizards, specific competition unnecessary. T. mili-
crustaceans,mollusks,spiders,occasion- aris is large and has moreroaming habits
ally leeches and scorpionsand many in- than T. petropolitana. Cyclorhatmphus
sects. The possibilitiesof hiding are, fuliginosus and C. pinderiare allopatric
however,much increasedby the division forms (Mayr, 1942).
of the leaf cup into a central tube and The leptodactylids that produce froth
outer compartments, narrowingtowards provide a good example of the gradual
the base of the rosetteof leaves, inserted elimination predatorsand competitors
of
in a verylow spiral. The prolonged car- as specializationin the site of spawning
ryingby the motherof the eggs on her progresses. The smallgeneraEupemphix
back extendsthe protection the adults and Physalaemus lay their eggs at the
of
to their progeny,and the shortening of edge of verysmall puddlesand pools a'nd
the aquatic period to a few days, at sub- are exposed to the usual hazards. The
metamorphosis, decreases the risk from spawn is abundantand the larvae hatch
predationand also from drying,during in a very rudimentary condition;during
prolongedrainlessperiods. A few other the first days theylive underthe froth or
bromeliad-dwelling frogs with ordinary returnto it for shelter. The nests of
tadpoles spawn in the leaf cups but they Leptodactylus mnystaceus,whichare open
are verysmall speciesand lay onlya few below, communicate with semipermanent
eggs. The coelonotous Hylidae need not watersbut entranceinto themcan be re-
competefor food with otherlarvae since tarded. The pot-shapedspawningholes
they hatch with abundantyolk-reserves. of the large species of Leptodactylus, like
There are no competing species in the flavopictus observed-byus, are covered
bamboo in which we foundthe coelono- by a deep blanketof froth thatkeeps out
tous Hyla ohausi. The otherinhabitants competitors and marauders. Almost in-
are coleopteran maggots, presumably veg- violable isolation is achieved in the
etarian,and culicid larvae, in regard to earthenpans of L. nanus whichare dis-
whichthe predator-prey relationship to tant fromwater and can be enteredor
is
the advantage of the frogs. Woodpeck- left only by a small aperture in the
ers and monkeysprobablyhunt for the built-uproof.
beetle grubs but small, dark, submeta- Under these circumnstances, seems
it
morphic of
anurans,unableto leap out, may valid to statethatwithdrawal develop-
finda hiding-place theblack waterand mentfromwater reduces selectionpres-
in
rich mulchwhichaccumulatein the hol- sure duringontogeny. The consequences
lows betweenthe septa of the perforated of this fact,as will be shown later, are
bamboos. in
very important the ontogenetic evolu-
The semiaquatic tadpoles of the tro- tion of the terrestrial vertebrates.
glodytic Cyclorhamphusand the non- Nonaquatic development cannot, of
aquatic larvae of the rock-dwelling Tho- course, preclude the appearance of new
ropa are unmolested aquatic formsof enemies,
by such as the syrphid Rhzysops
fly,
life. Small insects have been seen, by berthae Costa Lima (1946), which is
Mr. Venalncio, hoveringover the spawn 'parasiticon theeggs bothof Centrolenella
of C. pinderi,lying on a ledge of rock eurygnatha, of a rhyacophilid
and caddis-
in a grotto,but theywere being snapped fly which also spawns on open leaves
up by the adult posted in the vicinity. above mountainbrooks. The formation
Both adults and larvae of Cyclorhamphus of mildew on nonaquatic eggs of Eleu-


therodactylus, observed -by Ruthven There is no literature tropicalfrogs
on
(1915) and by B. Lutz (1948), may also comparable thesynopsesof the Wrights
to
come underthisheading. It is, however, on the eggs and on the tadpolesof North
not yet clear whetherfungusinfestation Americananurans,nor are thereenough
occurs in natureas well as in the labora- figures treatment.
available for statistical
tory. The cases in which spawning was ob-
The r6le of intraspecific competition served or in which the eggs were meas-
duringdevelopment, stressedby Haldane ured and counted are used in table 3.
(1932), forintrauterine ontogeny, less The examples are few and somewhat
is
obvious. Increased yolk reserves,cou- heterogeneous theyshow the general
but
pled with intraoval development, make trend.
for independence the embryofromits
of Given the usually very small size of
siblings. Slight differential factorsmay the eggs of frogs and the relative size
ensue fromthe relativepositionof each of the mothers, increasein volumeof
the
egg in the clutch. They can hardly go yolk is significant. Moreover, it is ac-
much beyond the possible advantage of companiedby a drasticreductionin the
a central over a peripheralposition in number eggs to a small fraction the
of of
clutchesdisposed in one layer. In those complements generally laid. The criteria
laid in several layers greaterdifferencqs by which it must be judged are the
may obtainas to gaseous exchangeswith lengthening intraoval life which in-
of
the outside. Comnpetition among terres- creased yolk reservesmake possible and
trial,sedentary larvae nourishedon yolk the degreeof development attainedwith-
is evidently less than it is amnong
far free out other sources of nourishment. In
swimming tadpoles,whichhave to secure many cases the reservesare sufficient to
theirown food. permit reaching adult shape with rem-
nants of yolk in the gut, thus allowing
THE IMPORTANCEOF LARGE-YOLKED for a short period of adaptationto the
EGGS new environment before the risks in-
The passage from (snmall- volved
microlecithal in huntingneed be incurred.
yolked) to macrolecithal(large-yolked) Noble, who did outstanding work on
eggs is the most important aspect of the the biologyqf the Amphibia(1925, 1927,
ontogeneticevolution of the Salientia. 1931), believed that increase of yolk
Incidentally, sheds some light on the mightbe random and occur by sudden
it
evolutionof the next higher classes of change. He mentionsthe fact that in
the vertebratephylum. Gastrotheca eggs may be eitherlarge
the

TABLE 3. Egg size and egg number Brazilian frogs
in

Diameter Cubage Itavl Egg
Species and size of female Diryolk of yolk develop- comple- Site of eggs
(snout to vent) (in mm.) (cub.mm.) (in days) ment

1. Physalaemusfuscomaculatus40 mm. 1.0 0.52 1 1000
Hyla polytaenia 38 mm. 200 standing water
2. Hyla mesophaea 75 mm. 1.5 1.77 1 1000
3. Phyllomedusaguttata 46 mm. 2.0 4.19 14 49 leaves
Centrolenellaeurygnatha 26 mm. 10-30
4. Leptodactylus nanus 24 mm. 2.5 8.18 ? 8-10 closed pans.
5. Coelonotusfissilis 36 mm. 3.0 14.14 14-21 7-13 back of the 9
6. Hyla goeldii 38 mm. 3.5 22.45 14-21 25
7. Eleutherodactylusnasutus 38 mm. 4.0 33.51 28-30 13-14 bromeliads
8. Eleutherodactylusguentheri 40 mm. 4.5 47.71 30-35 22-25 banks of earth

34 BERTHA LUTZ

or small. This point of view may have youngcommon all classes of oviparous
to
been induced by the fact that in frog vertebrates.
ovaries not all the ova reach full size
EXTENT OF MORPHOLOGICAL CHANGE
simultaneously. In developingclutches
of large-yolkedeggs there are often a The extentof morphological change is
few small ones which do not develop. in agreementwith the size of the yolk.
Examinationof theovariesof adultPlyl- The resultantmode of development fol-
lomedusa or Eleutherodactylus females lows two main trends, repetitionand
shows the presence of large-yolked and compensation. One or the other pre-
of small eggs. In the genus Phyllome- dominates,accordingto whetherontog-
dusa the smalleggs,or yolklessegg mem- eny is larval or embryonic.
branes, are found glueing together*the In the formercase, there is a repeti-
edges of the leaves folded over the egg tionof the lifecycleoflarva,metamorpho-
mass by the parentswhile spawning. sis and imago, though hatching is de-
As thoseAmphibiathatwere ancestral layed either to the secondary, perfect
stage, withoutexternal gills or
to theReptilesmayhave had large-yolked tadpole
limbs (Centrolenella, Phyllomedusa), or
eggs, Noble (1931) suggeststhat micro-
to submetamorphosis (coelonotous Hyli-
lecithaleggs may not be necessarily more
dae). When the larvae are adapted to
primitive. The comparative study of
*a free-swimming to a semiaquaticex-
or
moderntropicalanuran development cer-
istence,they show minor morphological
tainlybears out the probability 'that the
changes, fittingthem for life in their
Amphibiaancestralto the Reptilia were respective environments. Those living
macrolecithal, but it also permitsinter- on rocks for instance,like some species
pretingsmall-yolked anuran eggs as re- ofCyclorhamphus Toropa,are stream-
and
lict. The evolutionary value of macro- lined with narrow tails and clinging
lecithal eggs is shown by the fact that mouths. In nonadaptive, sedentary,ter-
large-yolked eggs are the rule in terres- restriallarvae,nonfunctional organs such
trial vertebrates,until the viviparous as the finsand hornyteethare reduced.
mammals are reached. Irrespectiveof The external gills are more variable.
the enzymes thatappear at hatching-time, They may have the usual form (Centro-
it is quite obvious that when the possi- lenella, Phyllomedusa) or be enlarged.
bilities of development, within the egg In the coelonotousHylidae theyare bell-
membranes, at the expense of stored shaped; in both cases they occur in the
or
yolk, are exhaustedthe young organism encapsuled stage and regress as or be-
must rely on outside sources of nourish- fore the larva emerges from the eggs.
ment. The more undeveloped is when Some free,
it terrestrialtadpoles(L. nanus)
this stage is reached,the more defense- show rudimentary fora shortperiod.
gills
less will it be in the struggle survival. The completeabsence of externalbran-
for
In the poikilothermal (ectothermlal) ver- chiae is not uncommon anurans devel-
in
tebrates with increasingly macrolecithal opingfrom nonaquatic eggs (Lynn,1942).
eggs this momentis progressively put In macrolecithal eggs cleavage is re-
off, towards the end of development tarded; the earlyembryo developson top
(anurans withmodified ontogeny),or by of the yolk and formsa precociousnet-
hatchingin adult shape (anurans with work of blood vessels over it. This
direct development, reptiles). The ho- marksa transition theconditions
to found
moiothermal (endothermal)- birds,which in the frogswhichhatch in adult shape.
have helpless chicks, resort to feeding The development theseis embryonic
of
them. The increase of yolk reservesto and there is no metamorphosis. The
the limitattainablefor each kind is the changes of structure correspondingly
are
firststep towardsbetter provision the greater. Some species of Eleutherodac-
for


tylusfromthe Caribbean regiondevelop anurans with directdevelopment, includ-
externalgills for a while but in others, ing the recently described embryo of
includingthose fromsoutheastern Brazil the Ceylonese Rhacophorus? reticulatus
studied by Lynn and B. Lutz (1946, (Kirtisinghe, 1946), whichdevelopsfrom
1947), the pharyngeal pouches never terrestrial eggs.
break through and thereare no open gill
AND ITS CONSEQUENCES
slits. The development functional
of in- ACCELERATION
ternal gills is therefore impossible and A number interesting connected
of facts
thereare no externalones. The opercu- with the rate of developmentcome to
lum and the typicaltadpole mouth,with light as a result of studies on modified
its supporting cartilages, absent. The anuran ontogeny.
are
intestine though convoluted notspirally
is Haldane (1932) points out that there
coiledas in tadpoles. Both pairs of limbs has been a commontendency evolution
in
developoutsideand the limbbuds appear toward the accelerationof development,
quite early,thus obliterating one of the i.e. for certaincharacters appear pro-
to
distinctions betweenAmphibiaand Am- gressivelyearlier in the life cycle and,
niota. conversely, anothertendency towardsre-
The larval tail of Eleutherodactylus, tardation.
however,persists and develops further. Now, in animals with distinctlarval
It passes betweenthe legs of the impris- and adult stages that live in different
oned embryoand becomes ventral,with environments, such as the Salientia with
the partscorresponding the upper
to and aquatic larvae and terrestrial adults,adap-
lower fins in a lateral position. The tive requirements evidently are different
membranous surfaceis greatlyincreased for each of the two stages. Moreover,
and is closely applied to the egg mem- thetransition from one stageand environ-
branes; it is intenselyvascularized and ment to the other requires considerable
active circulation can be observed in it. organic remodelling.
The tail,havinglost its locomotory func- This is a very importantpoint. In
tion, has become the main respiratory the phylogenetic evolutionof the terres-
organ. trialvertebrates therecomes a timewhen
The process by which this occurs is larvae no longer occur and costlymeta-
one of compensation. It is akin,but not morphosis done away with. That there
is
identical, the of in
with "substitution" Klein- has been a breakis evident the Saturop-
enberg(1886) by whichone organserves sida. I interpret nonaquaticanuran on-
as a scaffold and its presenceas a stimu- togeny as equivalent to a preliminary
lus for the formation another,to wit phase of this evolutionary
of process. With
the r6le of the notochord the develop- increasingyolk reserves,there is firsta
in
ment of the backbone. The usual cu- reduction,next a suppression of free-
taneous gas exchangeof the tadpole tail, swimming larval lifeand, finally, abo-
an
no doubt,providesthe initial possibility litionof the larval stage.
for its transformation a respiratory Some forms-
into with terrestrial develop-
organ. However, by becomingone, the ment (for example,Leptodactylus nanus
tail compensatesfor the anuran larval and Zachaenus parvulus), it,may be ob-
gills, which are no longer present,and jected, retain tadpoles; no doubt, but
forthe respiratory function thesaurop- these tadpoles are sedentaryand nour-
of
sid allantois,which has not yet evolved. ished exclusivelyon yolk. They and, a
Compensation thusseen to be a further fortiori,
is the embryosof frogs with di-
diversification an organforthe accom- rectdevelopment
of (Eleutherodactylus and
plishment a function whicha spe-
of for others) come under the heading of shel-
cial organ is lacking. teredembryos(or larvae), in whichform
Respiratorytails are known in other is independent survivalvalue as sug-
of

36 BERTHA LUTZ

gested by Haldane (1933). This has relativelythick. Evaporationis guarded
far reachingconsequences. The need for againstin all the nonaquaticanuran eggs
dual adaptationto two separate environ- mentioned the damp spawning sites,
by
mentsis done away with. Development or by themoreor less saturated condition
becomes self-contained and there is an of the whole environment, especially in
abbreviationof the formativeprocess, the rain and mist forestwhere most of
which follows the shortestroute from these lifehistoriesoccur. Respirationof
fertilized
ovum to adult shape. salientianembryos take place through
can
Acceleration itselfis not an abstract
in the egg membranes. The morphological
concept, nor yeta cause. It is merelyan natureof the respiratory organs (super-
of
effect morpho-physiological changesin ficialnetwork vessels,gills,or respira-
of
secondaryegg structures and during, de- tory tails) is not of paramountimpor-
velopment. Nevertheless, has led to
it tance. The main point is that gaseous
the suppression the larva and of meta-
of exchangebe possibleand that the supply
morphosisin the life cycle of the terres- of oxygenbe sufficient. thisis assured
If
trial vertebrates. Regarded thus, its it seems somewhat immaterialwhether
phylogeneticalvalue and its evolutionary the outside environment aquatic or
be
significancebecomeclear. not. Nonaquatic embryosof Eleuthero-
dactyluscan be keptalive in waterif the
OBSTACLES TO FURTHER EVOLUTION
thickegg membranes are removed. De-
One may ask why modern Salientia veloping eggs of Centtrolenella eurygna-
having evolved thus far were unable to tha,whichdrop intowaterfromthe sup-
continue evolving. This leads to the dis- portingleaf, survive as long as intense
cussion of the obstacles in their way. aerationis assured.
These are generally consideredto be the Mutatis mutandis, this also applies to
of
difficulty emancipating youngfrom
the tadpoles. Phyllomnedusa guttata larvae,
water and the moisturerequirements of which are surfaceswimmers, have been
the adults. Some slightchanges in this kept alive by A. Lutz and me on water
conceptmay lead to a more precise defi- ferns(Hymnenophyllumt) overan hour
for
nition. at a time and then returnedto water.
The examplesused here show thatthe The tadpolesof Leptodactylus mystaceus,
difficulty emancipating youngfrom
of the which spawns in places likely to be
water,as an outside environment, notis flooded, have been seen in damp locations
insuperable. It has beenovercome num-
a by Hensel (1867) and others since.
ber of times and in diverse,manners. The average aquatic tadpoles develop
Development is admittedly not as well lungs early and come up to the surface
isolatedfromcontactwith the outsideas periodically. Only a few species, like
in the cleidoiceggs of reptilesand birds. Hyla claresignata,remain entirelysub-
Nor is this necessary, providedthat the merged, clinging to boulders in swift
physiological requirementsof the em- flowingand torrential waters.
bryos are fulfilled. In some ways they The moisture requirements of the
are easier to provide for than those of adults are due to the persistenceof the
embryosbetterprotectedby hard shells dual respiratory mechanism already seen
against evaporationand other environ- in the tadpoles. Breathingis both cu-
mentalhazards. taneous and pulmonary, with bucco-
Yolk provides the necessary food in pharyngeal respiration in subordinate
both groups. Water metabolism may be r6le.
attended by the intraovalfluidand the
to Some adultfrogsare almostcompletely
gelatinous membranes of anuran eggs aquatic. This is the case withthe rather
whichtakeup moisture veryreadily. The primitive,aglossal African Xenopus,with
membranes thosewhichare buriedare
of the NeotropicalPipa, and also with the


liopelmidAscaphus truei fromthe cold including narrow and shallow ditches.
and swiftmountain streamsof the north- The gelatinousribbonsof eggs extruded
westernUnited States, studiedby Helen fromthe ovaries do not coalesce. The
T. Gaige (1920). The lungsof the latter eggs spaced along themcontainvery in-
were investigated Noble (1927) and
by adequate yolkreserves. Hatchingoccurs
found to be poorly developed. Con- in a very rudimentary condition, expos-
versely, toadsofthegenus
large terrestrial ing the larvae to intenseselectionpres-
Bufo are less dependent moisture
on than sure, whichmust resultin heavy mortal-
most other Salientia. Marcus (1927) ity. The larval stage is shortenedby
citedby Noble (1931) pointsout thatthe early metamorphosis, a very diminu-
at
lungs of the large neotropical species are tive size, quite out of proportion that
to
very well developed and vascularized. reachedby theadults,whichincludesome
The skin is thick and glandular. We of the largestneotropical anurans.
find that formsfrom the semiarid sec- Eleutherodactylus, the other hand,
on
tionsof Brazil, likeBufoparacneniis Lutz, has scrappedthe larval phase by develop-
have extra glands on the legs. These ing directly theegg,and has done away
in
are found again in Bufo alvarius from with the need for dual adaptation and
similar regions of North America and remodelling organogeny. However, the
in Odontophrynuscultripes from the adults of the species observedby us in
scrub sectionof centralBrazil. southeastern Brazil have retaineda very
The correlationseems evident. As thinand moistskin. Their physiological
long as the lungs are poorly developed, requirements so strictthat they fail
are
the skin has to be used as a respiratory to survivewhenremoved from theirusual
organand it can onlyfunction such by
as habitats.
remaining moistand permeable, allowing All around biological improvement,
gases to enterinto solutionso that they openingup further has not
possibilities,
can pass into the blood stream or be of
been achievedby representatives either
expelledfromthe body. genus.
It is not the dependenceof early life
EVOLUTIONARY SIGNIFICANCE
on an aquatic ou,tside environment which
constitutes insuperablebarrierto the
an The modified anuran life historiesal-
further evolutionof the Salientia. The readyknown, whenplaced in theirproper
real obstacleconsistsin the dual respira- sequence,forma numberof linear series
tory mechanism, to be more precise,
or, of ontogeneticevolution, leading from
in the lack of its concentration one,
in specialaquatic to terrestrial
environments
well-developed organ,the lung. and fromabridgedfree swimming larval
life to direct development. Some steps
HIGHEST EVOLUTIONARY LEVEL
are missingbut when the lifehistories of
REACHED
intermediate formsare discoveredsome
Comparisonof some species of the twvo of the gaps may be filled.
neotropicalgenera, which have evolved It is not altogetherimpossible that
furthest to the mode of development
as among the tropicaland subtropicalSali-
or as to therespiratorymechanism,brings entia with unknownlife historiesthere
forthsome very curious evidence. may be formsin which direct develop-
As seen above, the large neotropical ment has been achieved concomitantly
species of Bufo have developedrelatively withimprovement the lungs. But, for
of
well-perfected lungs, concomitantlywith the timebeing,thought along these lines
a thick and glandular skin. The genus must remainspeculative.
has, however, remainedprimitive toas A numberof neoevolutionists make a
life history. Even our largest species distinctionbetweenlarge scaleand limited
will spawn in any kindof standingwater, evolution. They might be inclined to

38 BERTHA LUTZ

considerthe caenogenetic changesin sali- The general trend is towards with-
entian developmentas mere specializa- drawal of development fromwater,with
tions. And yet, the evolutionary trends concomitant changes of reproductive be-
of salientianontogeny, modified towards: havior, ecotopic adaptations,progressive
(1) betterprovisionfor the young; (2) increaseof yolk volunme acceleration
and
withdrawalof development from selec- of developnment.
tion pressure; (3) suppression of the Some of the changesare monophyletic,
dual adaptation to environment, fore- others recur in different familiesunder
shadow the conditions foundin the more similar ecological conditions. Spawning
complex terrestrial classes of the verte- sites vary fromspecial aquatic to mani-
brate phylum. fold nonaquaticlocations.
The way of lifeof frogswiththe usual Withdrawal development
of fromlwater
moisturerequirements due less to ex-
is resultsin the reduction selectionpres-
of
cessive specializationthan to an obliga- sure during ontogeny. This may have
toryrelegation conditions
to whichallow been an important factorin the clandes-
tetrapods withprimitive lungs to survive tine evolution of the terrestrialverte-
in terrestrialenvironments.Idio-adapta- brates.
tionseemsa better termto applyto them Progressive macrolecithism leads to
than specialization. lengthenedintraoval life, with hatching
Evolution,or progress as he calls it, as perfect, as submetamorphic
or larva,
maycometo an end,according Huxley
to or in adult shape. Increase of yolk is a
(1942), whenall thepossibilities inherent firststep towardsimproved provisionfor
to a type of organism have been ex- the young in oviparous vertebrates.
ploited. This is the case of the anurans Morphologicalchanges include differ-
under discussion. In such cases, at any ences in shape, the presenceor absence
rate,one cannotbut ask, whether basic,
a of larval structures, the reduction
and of
qualitativedistinctionbetweenlarge scale nonfunctional organs. In macrolecithal
and limitedevolutionreallyexists. eggs the embryosdevelop on top of the
It seems legitimate sum up by say-
to
yolk. The limbbuds of frogswithdirect
ing thattheancientAmphibia whichwere
development form early, thus annulling
able to evolve-further not surviveas
did
one of the distinctions betweenthe Am-
modernrelicts.
phibia and the Amniota.
Acknowledgments Salientia with aquatic larvae and ter-
restrialadults require a dual adaptation
The authorextendsher best thanksto
Drs. Charles M. Bogert,JamesA. Oliver to two successiveenvironments.Seden-
and Ernst Mayr, for many helpfulsug- tary, terrestrialtadpoles, nourished on
gestions as to the presentationof the yolk, and direct developmentdo away
subjectmatter and formuchtrouble taken to
withthis need. They correspond pre-
and interest shown in this paper; to Dr. liminaryphases in the acceleration of
Julian Huxley, for kindly reading and development that has led to the disap-
discussing earlydraft
an withher,during pearance of the larva and of metamor-
his second visit to Brazil, and to Profes- phosis fromthe life cycle of the higher
sor Costa Lima, for examiningthe table vertebrates.
of insect enemiesof tadpoles. The failure of modern Salientia to
evolve further due to the dual respira-
is
SUMMARY tory mechanism,cutaneous and pulmo-
The ontogenetic evolutionof frogs is nary,and to theirprimitive lungs. Some
discussed on the basis of a number of neotropicalforms have achieved direct
peculiar life historiesobservedin south- development, othershaveimprovedlungs.
easternBrazil. Forms may possibly yet be found in


which both improvements occur simul- 1929. Taxonomy and biology of the
taneously. genusCyclorhamphus. Mem. Inst. Oswaldo
Cruz, Rio de Janeiro,22: 16-25. Pi. I-V.
The arrestedevolution the Salientia
of . 1931. Sur la biologiedes Batraciensdu
foreshadows the evolutionaryachieve- Bresil (Leptodactylts nianus). C. R. Soc.
mentsof the highervertebrates.Though Biol. Paris, 99: 755.
haltedby the exhaustion the biological
of AND B. LUTZ. 1939. I. Notes on the
inherent theirtype of or-
possibilities to genus Phyllomnedutsa
Wagler. Ann. Ac.
Bras. Sc., 11: 219-263. Pls. I-VIII.
ganism, no basic, qualitative distinction LUTZ, B. 1944. Biologia e taxonomia de
between their limited and large scale Zachaenus parvuilus [English summary].
evolutionis apparent. Bol. Mus. Nac., 17: 1-66. Pls. I-XIV.
. 1947. Trends towardsnon-aquatic and
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. 1947. The development Eleu-
of
animals. Methuen and Company, Ltd.,Lon- therodactylusnasuttus
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don. Zool., 79: 1-30. Pls. A, B, I-III.
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et
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