Passage to the Terrestrial Life in Amphibians : Events Accompanying This Ecological Transition

17 Pages·1993·6.1 MB·English

by  Jacques Hourdry

ZOOLOGICAL SCIENCE 10: 715-731 (1993) © 1993Zoological SocietyofJapan
REVIEW
Passage to the Terrestrial Life in Amphibians:
Events Accompanying This
Ecological Transition
Jacques Hourdry
Laboratoire de Biologie du Developpement des Vertebres
Inferieurs-CNRS 1134, Batiment 441-91405-Orsay
Cedex, France
CONTENTS
Introduction
I A series of metamorphic changes accompanies the departure from an aquatic environment in
amphibians
A Acquiring another type of locomotion
B Respiratory changes
C Changes in the digestive tract. Effect on the feeding behaviour
D Transition to a new hydromineral equilibrium
E Transition to another type of nitrogen excretion
F Sensory changes
G Departure from water: an energy expenditure for the organism
II A more radical departure from water can eliminate the aquatic larval stage
A
Elimination of the aquatic larval stage in anurans
B Urodeles
C Apodes
D Conclusion
General conclusions
—
ABSTRACT Passing from an aquatic environment to a terrestrial one has been analyzed in
developing amphibians. The emergence occurs at metamorphosis in many species, while appear
dramatic changes of the organizational plan. Metamorphosed animals acquire another type of
locomotion and respiration. Striking transformations take place in the digestive tract and result in
modificationsofthefeedingbehaviour. Waterconservationproblem issolvedbyappearanceofanew
hydromineral equilibrium, which is associated to another type of nitrogen excretion. Nevertheless,
such events do not completely free juveniles and adults from an aquatic environment. Other
amphibians acquire a direct development which puts an end to the aquatic larval stage. This more
radical departure from water exists in several oviparous species and also in various other species in
which the offspring-parental relationship is more or less pronounced.
INTRODUCTION aquaticenvironment toa terrestrialone is always a
major problem. This ecological transition is parti-
Water is the source of life, and passing from an cularly obvious in developing amphibians. The
present article analyzes the departure from an
Received March 29, 1993 aquatic environment during metamorphosis. The
716 J. HOURDRY
associated changes have been studied not only at
the anatomo-morphological level, but also at the 2 Regressionofthetailduringanuranmetamorph-
physiological and biochemical level [4, 21, 23, 33, osis
42, 56, 89, 90, 96]. The degeneration of the tail and its complete
A more radical departure will also be discussed regression characterizes the climax stage (paroxy-
for certain amphibians in which the aquatic larval smal stage) ofmetamorphosis. To the naked eye,
stage disappears. The endocrine determinism the first signs ofdegeneration consist in a thinning
presidingthisecologicaltransitionwillbe analyzed ofthefin andadarkeningoftheendofthetaildue
in another article (in press). to an accumulation of melanophores. All the tail
tissues are altered [29, 88]. The spinal cord,
I A SERIES OF METAMORPHIC CHANGES notochord and epidermis are autolyzed: the cell
ACCOMPANIES THE DEPARTURE FROM constituentsaresegregatedinthelysosomes(auto-
AN AQUATIC ENVIRONMENT phagicvacuoles)wheretheyaredigestedbyhydro-
IN AMPHIBIANS lases (cathepsins). The muscle fibers retract and
become individualized, thus deforming the tail.
A ACQUIRING ANOTHER TYPE OF- The myofibrils break down and the actin and
myosin myofilaments become disorganized (Fig.
LOCOMOTION
1). These processes result in the appearance of
1 The tail, swimming organ in premetamorphic
aquatic larvae
The tail of amphibian larvae is made up of a
fleshy axis with a membranous dorso-ventral fin.
The rythmic undulations of the tail give it an
essentially propulsive function. Swimming can be
very rapid when the tail is well developed with
powerful muscles as in Astylosternus and Lepto-
dactylodon. Caudal undulations are controlled by
the activity of two giant neurons (Mauthner
neurons) in which the axonsfollow the same path
,
as the spinal cord [69]. Such neurons enhance the
immediateflightreflexafteramechanicalorsound
stimulation (impact against the side of the
aquarium). The nerve impulse is then transmitted
to the Mauthner neurons by the stato-acoustic
nerves.
Thedegree ofwater-oxygenation conditions lar-
val endurance. Tadpoles in a well oxygenated
environment receive enough chemical energy fur-
nished by the ATP from respiratory catabolism
and consequently tire very little. The chemical
energyinpoorlyoxygenatedwaterislowersince it
comesfromanaerobiccatabolism (lactinfermenta- Fig. 1. Electron micrographofalongitudinalsectionof
tion), and the animals become incapable of fur- acaudalstriatedmusclefiberfromanAlytesobstetri-
nishing a highly endoenergetic sustained pro- cans tadpole. A, Premetamorphosis. fi, Climax.
pulsion effort [86]. The Z bands (Z) are disrupted during climax
(arrows)andproduceafragmentationofthemyofib-
rills (mf). gl, glycogen. Unpublished micrography
by Pouyet.
Passage to Terrestrial Life in Amphibians 717
bundles of fragmented myofibrils enclosed in calcium thus mobilized contributes to skeletal
round bodies. Enzymes such as actinase and ossification [65].
myosinase could be responsible for these altera- The skeletal ossification of the tadpole is en-
tions [12, 49. 97]. hanced by the thyroid hormones, as observed
The existence of phagocytic processes was de- during induced metamorphosis [47]. Calcium
monstrated in the first studies concerning caudal metabolism is also controlled by the ultimobran-
regression. Thecaudalfibroblastsundergoameta- chial bodies [15, 68]. These bodies favor calcium
bolic reorientation and become capable ofabsorb- storage in the endolymphatic and chalky sacs of
ing and totally digesting the cell fragments thanks the tadpole, a prerequisite for proper ossification
to the lysosomal hydrolases contained in their during metamorphosis.
digestivevacuoles [30,48, 91]. The fibroblastsalso
secrete hyaluronidase, which they use to partially c Effect of nervous system maturation on
liquifytheconnectivetissue,therebycomingcloser locomotion in a terrestrial environment. The new
to the alteration sites. locomotor behaviour acquired by metamorphosed
anuransissupportedbyamaturecerebellum. The
3 Locomotion in metamorphosedanurans development of the dendrites and axons of the
a Adaptations to jumping. This is due to the granular and Purkinje cells in this organ and the
spectacular growth of the hindlimbs. External granular cells migration results in a large number
budsuntilmetamorphosis,thelimbsrapidlylength- of synapses [39, 82]. This conditions the appear-
en at the onset ofthe phenomenon, preliminary to anceofcoordinatedjumpingmovements. Further-
acquiring a jumping type oflocomotion in terrest- more, the cerebellum controls the muscular
rial habitat. Thisadaptationbenefitsfromadistor- tonicitywhichcounterbalancestheeffectofgravity
tion of the pelvic girdle which places the cotyloid in a terrestrial environment.
cavity, articulatedwith the femoral head, in avery Dendrite endings curled around muscle fibers
posteriorposition. A stockybodywith arelatively (neuro-muscular spindles) have been identified in
short spinal column also makes jumping easier. thehindlimbsofRanapipiens duringmetamorpho-
The forelimbs are used when landing on the sis [10]. Suchendingsare sensitivetothedegreeof
ground. They develop in the gill cavities and fiber contraction and make it easier to control the
emerge duringclimax. Whenthe animalsreturnto jump.
apond to reproduce orto escape from apredator,
the springing action of the hindlimbs combined 4 The case ofurodeles
with palmed toes results in a strong swimming The urodeles tail does not undergo spectacular
capacity. morphological modifications during metamorpho-
sis,sinceonlythefinregresses. Thelimbslengthen
b Skelettal ossification. During metamorpho- moderately. The juveniles locomotion on land,
sis, skelettal remodeling is associated with a however, islimited to simple reptation movements
significantossificationwhich impliesamodification by the limbs transversal disposition.
of the calcium metabolism and phosphate and
B RESPIRATORY CHANGES
calcium carbonate deposits in the skeleton.
Skeletal calcium comes from the tadpoles two Amphibian larvae and adults have awide range
endolymphatic sacs and the chalky sacs. Each of respiratory exchangers, which allow a very
endolymphatic sac comes from the endolymphatic progressive transition without acute respiratory
canal which develops at the internal ear level. failure during metamorphosis and the passage to a
Thesesacsslipbetween the skullandthe braininto terrestrial environment [3, 42].
the spinal cord canal during metamorphosis. The
endolymphatic and chalky sacs contain minute 1 Respiratory system in larvae
calcium concretions (aragonite). These deposits Arborescent gills are present during the larval
arelargelyresorbedduringmetamorphosisandthe stage. Each gill consists ofa stem from which rise
718 J. HOURDRY
gill filaments. These filaments are covered with a capillary network, furnishes a second major re-
simple, flat epithelium which is practically next to spiratory exchanger. Moreover, many amphibian
the blood vessels. The skin, with its very dense larvae have lungs, which probably have an early
Fig.2. Metamorphic Discoglossus pictus tadpole: ultrastructural features of the degenerating gills (level of the
stem). Some epitheliocytes (1) undergo a diffuse autolysis and their mitochondria are dilated (m). Other
epitheliocytes (2) contain autophagic vacuoles (AV), residual bodies (RB) and lipid droplets (1). These cells
might be extruded (3) in the connective tissue (CT). Phagocytic cells (4) are also seen. They contain
heterophagicvacuoles(HC)andresidualbodies(RB). Thecapillaries(CA)haveashrunkenlumen. Ontheleft,
a melanophore (ME) can be recognized by its very dark pigment granules (arrows). RB, red blood cell; m,
mitochondrion; n, nuclear remnant. From Hourdry [41].
—
Passage to Terrestrial Life in Amphibians 719
but very accessory function'1' [9]. cavity follows metamorphosis and continues to
When the water is poor in oxygen (hypoxic progress until the adult stage, thus increasing the
conditions), the larvae hyperventilate with their lungs internal surface at least fivefold.
lungs by frequently swallowing air at the surface Oxygen absorption in metamorphosing anurans
[24,94]. Aftereachintake, theflowofwaterinthe takes place essentially through the skin. As soon
gills decreases temporarily. This is due to a as the juvenile stage, however, the septated pul-
stimulation of the mechanoreceptors sensitive to monaryepithelium increasesitscontributionwhile
oxygen pressure in the lung wall and the chemo- the skin thickens and partially loses its oxygen
receptors sensitive to oxygen concentration in the absorbingcapacity. Nevertheless, theskinremains
blood. When hypoxic conditions persist, the re- the primarycarbon dioxide excretingorgan during
spiratory exchanges of the larvae undergo exten- and after metamorphosis.
sive alterations [8]: the blood vessels multiply and Gill degeneration is associated with extensive
become more superficial; the number of gill fila- changes in the circulatory system. The afferent
ments increases. These observationsunderline the and efferent gill arteries regress. Aortic arches
highly plastic morphology of these exchangers. differentiate and irrigate the head (carotide arch),
the trunk and limbs (systemic arch merging and
2 Changes in the respiratory system during meta- forming the dorsal aorta), the lungs and skin
morphosis (pulmo-cutaneous trunk).
The gills regress during metamorphosis (Fig. 2)
[41]. The epitheliumundergoesadiffuse autolysis. 3 Changes in oxygen transfers: appearance ofnew
Its constituents can also be digested inside the hemoglobins andnew redcells
lysosomes (autophagicvacuoles). Thealteredcells The larval hemoglobins (Hb. 1) in most anurans
are usually absorbed by mesenchymal cells with aredifferentfromthosethatreplacetheminadults
phagocytic properties, and are digested inside (Hb. ad). In various frogs (Rana esculenta, Rana
large lysosomes (heterophagic vacuoles). Gill cir- catesbeiana), this substitution accelerates during
culation finally ceaseswhile the gill filamentswith- metamorphosis and continues several weeks after.
er and become pigmented before disappearing. In the tree-frog (Hyla arborea), leopard-frog
In most amphibians, septation ofthe pulmonary (Ranapipiens) and common toad (Bufo bufo), the
W
\»»»»>fi\'»>»»»»i pn t i i , ?-
Xenopus laevis Rana pipiens
— W
BomVIbWIi>n/Ia.W>'»v»a»»r*ieIgalt'ai'T" Hyla arbor1e2a3 4
Rana esculenta
Rana catesbeiana Bufo bufo
Fig. 3. Shift from larval hemoglobins (dotted lines) to adult hemoglobins (continuous lines) in anurans. M,
metamorphosis; w, week; y, year. From Hourdry and Beaumont [42].
(1) They are absent in bufonidae larvae.
720 J. HOURDRY
substitutiontakesplaceaftermetamorphosis. (Fig. sites (liver, bone marrow, etc.), and which replace
3). In urodeles, it can occur slightly before those of the larva [92, 93].
(Pleurodeles waltl, Triturus cristatus) or during
(Ambystoma tigrinum) metamorphosis. C CHANGES IN THE DIGESTIVE TRACT.
EFFECT ON THE FEEDING BEHAVIOUR
The change in hemoglobins has been demon-
strated by various analytical techniques. Elec- During metamorphic climax, the digestive tract
trophoresis, forexample, producesdifferentbands is modified, especially in anurans. Such changes
in anurans [46, 60, 66] as well as in urodeles [27]. are associated with modications in the feeding
The differences found between Hb. 1 and Hb. ad behaviour.
areonlylocatedon oneglobin andneveraffectthe
prosthetic group (tetraheme). The absence of 1 Changes in the digestive tractofanurans
common polypeptide chains has been irrefutably The size ofthe buccal cavity increases consider-
proven by the presence of different amino acid ably following the lengthening of the jaws. The
sequences in the different hemoglobin families. horny tadpoles "teeth" disappear while true teeth
During hemoglobin substitution, the iron from develop.
the Hb. 1 accumulates as ferritin in the Kupffer In larvae, the pharyngeal gill clefts are covered
cells of the liver. The metal will eventually be by a rough epithelium with ridges that form gill
carried by the plasma transferrins and incorpo- filters. Thesefiltersstrainthewaterwhichirrigates
rated into the new hemoglobins at their site of thegillsandretainthefoodparticlesinsuspension.
synthesis (essentiallybone marrow) [7, 63, 80, 83]. During metamorphosis, the pharynx undergoes a
Hb. 1 and Hb. ad have different affinities for substantial reduction. It no longer plays a part in
oxygen [78]. The Hb. 1 in premetamorphic anur- respiration since the gills and gill clefts regress.
anshave ahigh oxygen affinity. Thisiscompatible The gill filters also degenerate.
with an aquaticenvironment where the concentra- During the climax, a dilated stomach is formed.
tion of dissolved oxygen is particularly low. Hb. Its epithelium evaginates into the chorion and
ad have a lower oxygen affinity. Hb. ad produc- becomes tubulargastricglandswhichlengthen and
tion is associated with the presence of new and ramify (Fig. 4). The muscle layer thickens. These
more numerous red cells, developed in different structural modifications are associated with func-
Fig.4. Histological changes in the gastric region during Alytes obstetricans metamorphosis. A and B, Onset of
climax. The epithelium evaginatesintothe chorion (ch) and becomesgastricglands (arrows). Asterisk, lumen;
ms, musclelayer. C, End ofclimax. Thegastricglands arecompletelydifferentiated (arrow): theyeachhave a
neckofmucouscells(mc)intowhichopentubulesmadeupofgranulatedserouscells(ccorchiefcells). Agastric
mucous epithelium (ge) runs along the lumen (asterisk). From unpublished micrographies by Hourdry and
Pouyet.
Passage to Terrestrial Life in Amphibians 721
tional changes such as pepsin and hydrochloric or Bufo vulgaris are herbivorous or detritivorous.
acid production, by chief (or pepsinogen) cells [5, Their keratinized "teeth" tear apart the plant
38, 43, 51, 58] and parietal (or oxyntic) cells [28], organs and scrape the crusts. This results in a
respectively. Twopepsinogenshave beenfoundin suspension of particles which are then swallowed
the gastric mucosa of the adult bullfrog [85, 95]. by the animal. The periodic variations of buccal
These pepsinogens are immunologically indisting- cavity volume, due to the pulsating movements of
uishable fromeach otherand are relatedtohuman its wall, create a water intake and result in the
pepsinogen C. Chitinases are also secreted by the ingestion of food particles.
stomach as soon as it differentiates [64], The particles suspended in the water are usually
The metamorphosing intestine undergoes parti- gathered up by retention on the surface of the
cularlyspectacularchanges. Anoverallshortening various buccopharyngeal structures (Fig. 5) [35].
andrearrangement ofitscoils occurs concomitant- Certain particles are retained by the buccal cavity
ly with the development of the stomach. The papillae and by the dorsal and ventral velums.
histological changes are largely confined to the Such particles adhere to the mucous traps that
epithelium [26,40,42,44]. Degenerationoccursin have differentiatedintheroofofthe buccal cavity.
thelarval (orprimary)epithelium,whiletheexten- In a few cases, traps can be observed on the
sive proliferation of stem cells results in the de- undersideofthe dorsalvelum. The otherparticles
velopment of the new, folded epithelium (secon- areretainedbygillfilters. Afterbeingsweptupby
dary epithelium). watercurrents, they adhere tothe mucousoftraps
located on the underside of the ventral velum
2 Changes in the type offeeding during anuran (branchial food traps) [42, 87]. The gill filters and
development branchial food traps found on the ventral velum
a Premetamorphic larvae. Most tadpoles are make up the tadpole's fltering apparatus. The
microphagous and feed on particles suspended in various mucous secretions are canalized in phar-
thewater(bacteria, protozoa, unicellularalgae...). yngeal grooves where they form cords which are
Benthictadpoles, suchasthose ofRanatemporaria conveyed by the ciliary movements toward the
Fig. 5. Parasagittal section of the buccal (be), pharyngeal (ph) and branchial (br c) cavities in a premetamorphic
anurantadpole. Foodparticlessuspendedinthewater(pa) areretainedbythebuccalcavitypapillae(bp),dorsal
(dv)andventral(vv)velums,andgillfilters(gf). Theythenadheretothemucousoftrapsthathavedifferentiated
inthe roofofthebuccalcavity(A), andonthe undersideofthedorsalvelum (B)andventralvelum(C: branchial
food traps). The water flux is shown by the arrows, g, gill; m, mouth; n. nostril; s, spiraculum; 1-4, gill clefts.
From Gradwell [36].
722 J. HOURDRY
oesophagus. in a terrestrial environment. Simultaneously, new
In short, many anuran species have tadpoles neuronal connections appear between the retina
which are highly specialized suspension users. and the optic tectum [32, 37]. In premetamorphic
Particle retentiononthegillfiltersallowseffortless tadpoles, the tectal electric registrations are solely
feeding which is compatible with accelerated contralateral. On the other hand, these registra-
growth, when trophic conditions are favorable. It tions may be both contralateral and ipsilateral in
is noteworthy that many anuran species lay their metamorphosed animals, due to the development
eggs after heavy rains which leach the soil and ofa system or intertectal connections. Each point
provoke an influx of mineral salts into the ponds, of the binocular visual space corresponds then to
thusstimulating the plankton productiononwhich two tectal points through each eye.
tadpoles feed. The propulsion ofsolid food is enhanced bythe
Cellulose is probably not used by the larvae: the appearance ofstronger peristaltic movements due
thin muscle layer has a weak peristaltism which is to a thicker muscle layer.
not very efficient for breaking down plant cell The secretion of proteinases in the pancreas
walls. Furthermore, the larvae do not have cellu- (trypsin) [73] and the stomach (pepsin) prepares
lase. Amylase from the pharyngeal grooves and the animals for a carnivorous diet. Stomacal
most of all, exocrine portion of the pancreas, has chitinases also prepare the metamorphosed anim-
been observed [55]. This suggests a preferential als for an insectivorous diet. Furthermore, the
digestion ofthe starch found in the food particles. new intestinal mucosa is well equipped for the
Three intestinal brush border glucidases are also absorptionofproteinhydrolysisresidues: anactive
implicated in the hydrolysis of dietary glucides /-glutamyl transferase acts as a membrane-
(glucoamylase, maltase, trehalase). localized transporter of amino acids and possibly
Dietary glucides are the source of lipids and dipeptides [31, 59]. Moreover, this enzyme
hepaticglycogen, whose quantitiesincrease during hydrolyses the 7-glutamic acid-peptide bonds
premetamorphosis and which are the main energy found in physiologically important peptides, such
storage sources for the tadpole. as glutathione and folic acid.
In short, a new feeding behaviour is prepared
b Metamorphic and post-metamorphic anim- during anuran metamorphosis by important
als. Anuran tadpoles usually stop feeding at changes in the digestive tract, while the animals
climax. Indeed, thedigestive tract istooalteredto pass from an aquatic to a terrestrial environment.
function.
Inpost-metamorphicanurans,themouthwidens 3 The case ofurodeles
and stronger jaws with true teeth appear. An The metamorphic changes in the urodelean
eventuallyprehensile tonguedevelops. Thesevar- digestive tract are very restricted [42], although
ious transformations are concurrent with a change many larvae leave the ponds andmigratetoward a
in the diet, since the animals become carnivorous terrestrial environment. The diet is slightly mod-
of insectivorous, and catch preys with their pre- ified, since the animals are still carnivorous pre-
hensile tongue. At the same time, the eyes'1' dators.
migrate toward the plan of symmetry. Such a
D TRANSITION TO A NEW HYDRO-
migrationallowsbinocularandstereoscopicvision,
MINERAL EQUILIBRIUM
keen sight and an efficient perception ofthe preys
Amphibiians are confronted with a majorwater
(1) During metamorphosis, the optical properties of conservation problem in their transition to a ter-
the eye are modified [75, 76]. The tadpole eye isa restrial environment. This problem is solved by a
"fish eye": its spherical lens provides nearly all the series of adaptations which appear during meta-
ocular convergence. The eye of the metamorph-
morphosis.
osed anuran has a lenticular lens, and its converg-
ence is mainly due to the cornea, whose refractive
= =
index (n l, 38) is higher than that of air (n l).
Passage to Terrestrial Life in Amphibians 723
water retention in the plasma, thus avoiding de-
1 Changes in the serumproteins hydration during the animals migration to a ter-
a Qualitative changes. These are extensive in restrial environment.
metamorphosing anurans [11, 67, 81]. The num- Several ecologically-based arguments confirm
ber of molecular species increases at climax and thatthe adaptation ofmetamorphosed amphibians
the band characterizing albumin on an elec- toaterrestrialenvironmentislinkedtoanincrease
trophoregram becomes particularly distinct (Fig. intheconcentrationofserumproteins,particularly
6). These changes are usually more attenuated in serumalbumin:
—
urodeles. In Rana and Salamandra, with terrestrial
adults, the serum protein concentration increases
morerapidlythaninXenopusorPleurodeleswhich
can remain perpetually aquatic.
—
In Bufo arenarum, the serumprotein concen-
tration increases faster if the metamorphosed
animal migrates to a drier environment.
—
In several north-american ambystomatidae, a
relationship has been established between the de-
gree of humidity in which the metamorphosed
animals live and the concentration in serum pro-
teins [61]. In Ambystoma macrodactylum adults,
whichmigratetoadryenvironment,theseproteins
are relatively abundant and suggest an efficient
Fig. 6. Electrophoretic patterns of serum proteins in osmoticwaterretentionin the plasma. InRhyaco-
metamorphosing larvae of Rana temporaria (from
left to right). The albumin band (al) hasadistinctly triton olympicus adults which live in wet areas,
higher anodal mobility and becomes thicker and proteinemia is lower, resulting in poorer water
thicker. From Chen [11]. retention.
2 Evolutionofthehydromineralequilibriumduring
>»1
b Variations in theconcentration ofserumpro- the transition to a terrestrialenvironment
teins. This concentration at least doubles in meta- The appearance of new ionic fluxes results in
morphosing anurans; in Rana catesbeiana for ex- more efficient water conservation when the anim-
ample, it goes from 1.2g/100ml to 3g/100ml. als migrate towards a terrestrial environment.
The increase in serumalbumin is particularly spec-
tacularinthisspecies, from0.08g/100mlto0.8g/ a Hydromineral equilibrium of premetamor-
100ml, a tenfold increase [25, 54]. Urodeles have phic larvae. The aquatic environment of larvae is
weaker variations. very diluted compared to their body fluids where
These increases imply a stimulation of liver sodium (Na+) and chloride (Cl~) ions predomi-
proteosynthesis. In Rana catesbeiana, radioactive nate. The loss of these ions by diffusion and the
precursors have shown that the rate ofserumalbu- invasion of water by osmosis, through the tegu-
min synthesis is multiplied by 6 at climax [54]. ment, are corrected by regulatory mechanisms
During metamorphosis, the higher serum protein which allow Na+ and CI- ions to enter and water
concentrations increase the oncotic pressure (col- to be eliminated (Fig. 7A).
loid-osmotic pressure) of the plasma which is pro- Studies carried out in Rana catesbeiana tadpoles
portional to the number of protein molecules in haveshown that the absorptionofNa+ ionsoccurs
solution. The influence of serumalbumin is note- through the gill epithelium by an "active trans-
worthy since its relatively low molecular weight port" mechanism, which requiresasource ofener-
results in the release of a larger number of mole- gyinorderfortheionstogoagainsttheconcentra-
cules. The increase in oncotic pressure favors tion gradient [20]. Na+ ions create a higher
724 J. HOURDRY
B
Fig. 7. Changes in the hydric (thick arrows) and ionic (sodium: thin arrows; chloride: dotted arrows) fluxesduring
anuran metamorphosis. A, Premetamorphic tadpole. The effects ofthe osmotic gain ofwater and the loss of
sodium andchloride ionsbydiffusion, through the tegument (1), are restrictedbybranchial ionicabsorption (2)
andtheexcretionofanimportantvolumeofdilutedurine(3). B,Adultfrog. Inaterrestrialhabitat,hydricwater
retentionisfavouredbyastorageofsodiumandchlorideionsinthebodyfluids(1,oedemaeffect). Duringastay
in apond, waterabsorption accompaniestheenteranceofsodium andchloride ionsthroughtheskin (2). Water
and ionsfiltrate rapidly through the glomerulusofthenephrons (3), butareweakly reabsorbedthroughthewall
of the nephric tubules (4). On the contrary, a significant reabsorption occurs through the wall of the urinary
bladder (5). Consequently, the urine is slowly excreted (6). The cutaneous loss of water (7) and ions (8) is
relatively important, b, urinary bladder; g, gill; k, kidney (pronephros or mesonephros); m, mesonephros; t,
tegument. From Hourdry and Beaumont [42].
electric potential on the internal side of the gill The amphibianspermanent kidney (mesonephros)
epithelium thanon the externalside, thusallowing alsorecoversNa+ and Cl~ ions. Partoftheseions
Cl~ ions to passively accompany Na+ ions by in solution in the primitive urine crosses the
simple electrostatic attraction. The gill cells, nephron tube wall after being filtered in the
where "active" Na+ ion transport takes place, are glomerulus and returns to the body fluids. The
locatedatthebaseofthegillsandareequivalentto urinary bladder, developed during metamorph-
"chloridecells" infish. In amphibianlarvae, water osis, represents a third Na+ CI- ion recovery
,
invasion is also restricted by the excretion of an organ [53].
importantvolumeofdilutedurineasinfreshwater The mechanisms of ion transfer have been de-
fish. fined in the epidermis [14] and in the urinary
bladder epithelium [53]. The apical membrane of
b The appearance of new ionic fluxes during the epidermal cells becomes permeable to Na+
metamorphosis (Fig. 7B). Metamorphosed am- ions after acquiring sodium "canals". The "active
phibians which have left ponds can return to transport" of these ions towards the body fluids
escape from a predatoror to reproduce. Na+ and occurs specifically through the basolateral mem-
Cl~ ions transport then takes place towards the brane. This "sodium pump" cannot function in
body fluids through the epidermis [1, 6, 14, 79]. lavae because there are no sodium "canals" in