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OSMOREGULATION IN
AMPHIBIANS AND REPTILES
,1179
Vaughan H. Shoemaker
Departmentof Biology,Universityof California, Riverside, California 92502
Kenneth A. Nagy
Departmentof Biology and Laboratory of Nuclear Medicineand Radiation Biology,
Universityof California, Los Angeles,California 90024
INTRODUCTION
Osmoregulation can have various meanings depending on the organism in question
and the viewpoint of the investigator. Strictly speaking, the term implies maintenanceof the osmotic pressure of the bodyfluids, irrespective of their solute composition or volume.In this review "osmoregulation"signifies the processes by whichthe
amountsof water and specific solutes within the body of an organism are maintained
constant or within tolerable limits. Weexamine the various avenues of in- and
output in the hope of clarifying their relative significance in the water, electrolyte,
and nitrogen budgets of amphibians and reptiles.
The environment is a major factor in determining the nature of the osmoregulatory challenge facing any organism, and amphibiansand reptiles are represented in
a wide variety of habitats. Terrestrial forms range from deserts to rain forests, and
aquatic forms range from fresh water to the seas. Reptiles as a group are more
broadly distributed across this spectrumof habitat types, being generally less dependent on the availability of fresh water and humid environments than amphibians.
Nevertheless, some amphibians can withstand the potentially dehydrating conditions imposed by arid or hypersaline environments, and these provide interesting
examples of physiological adaptation. Both groups are large and phyletically diverse, and relatively few examplesof each have been studied in detail. This makes
generalization both difficult and hazardous. Fortunately, investigators have tended
to select species for study with an eye towardphylogenyand habitat, so that patterns
of adaptation can be broadly sketched.
There are a numberof reviews bearing on this topic: Bentley (4, 5, 8, 9), Bradshaw
(15, 16), Cloudsley-Thompson(24), Dantzler (27, 28), Dantzler & Holmes
Deyrup(33), Dunson(46, 47), Peaker & Linzell (101), Scheer et al (111), Shoemaker
(116), and Templeton(123). Each has its ownparticular emphasis and will provide
449
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450
SHOEMAKER& NAGY
the reader with many details not included here. Wehope that our focus on the
budgetary componentsof the osmoregulatory process will lead to a better understanding of their importance to the welfare of the animal in its natural environment.
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INPUT
Potential avenues of water and salt uptake include drinking, feeding, and uptake
across the skin or mucousmembranes,whereas nitrogen is generally gained only via
food. Water produced in oxidative metabolism is also an avenue of input to the
animal.
Drinking
Amphibians apparently do not rely on drinking to gain water in most natural
situations. For amphibians in fresh water, drinking would compoundthe problem
of water excess imposedby the high rates of osmotic influx of water across the skin
(see below.) Scheer et al (111) reported that Ranapipiens "drinks" in fresh water
(0.5 mMNaC1),but the rate (0.4 ml -~ hr-~) is insignificant compared to osmotic
influx. Bentley (7) found even lower rates of oral water intake in two urodeles (0.1
ml kg-~ hr -~ in Siren and none in Amphiuma).Moresurprising is that terrestrial
amphibians have not been observed to drink even when dehydrated, but changes in
skin permeability may nevertheless allow very rapid water uptake. Frogs placed in
hypersaline media do drink appreciable quantities (13, 73), but they are generally
unable to survive. The few species of adult amphibians that are knownto adapt to
high salinities (e.g. Rana cancrivora, Bufo virdidis, Xenopuslaevis, Batrachoseps
relictus) do so by accumulating sufficient solutes so that the osmotic movementof
water is inward and drinking is unnecessary (59, 60, 75, 106). However,drinking
mayplay a role in the initial stages of saline adaptation in B. viridis. Thereis also
circumstantial evidence that toads (Bufo bufo) drink when maintained in 150 mM
NaC1(54). The euryhaline tadpoles of R. cancrivora remain hypo-osmotic to their
environment at high salinities, implying that they drink to replace cutaneous and
urinary water losses. This has not been directly confirmed (61).
Little is knownabout drinking in most reptiles in the field, and intake rates have
not been measured in those that are knownto drink. Most terrestrial reptiles will
drink in captivity, especially whenwater is sprayed on cage sides or foliage to form
droplets. Seawater drinking is generally absent in captive marine reptiles, such as
sea snakes (48), estuarine turtles (44), and littoral lizards (42, 45), although several
of these animals maydrink whengiven fresh water. An estuarine subspecies of the
snake Natrix sipedon does not drink seawater, but a freshwater subspecies does
drink whenplaced in seawater and dies as a result (102). Reptiles normally living
in freshwater situations, including crocodiles (35) and freshwater turtles (12), generally drink in captivity. Krakauer et al (72) suggested that small burrowing snakes
and amphisbaenians drink water contained in moist soil. In the Australian desert
lizard Molochhorridus, water that contacts the skin is channeled to the mouthvia
capillary grooves, absorbed by hygroscopic mucussecreted near the lips, and swallowed (10). But Phrynosomarn’calli, a lizard occupying a similar niche in American
deserts, does not showthis phenomenon(81). A snake (Bitis peringueyi) living in
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OSMOREGULATION
IN AMPHIBIANS AND REPTILES
451
the NamibDesert may drink water that condenses on its skin during the desert’s
periodic advective fogs (79). Laboratory measurementsof water balance in several
lizards indicate that the desert species can maintain balance without drinking, but
more mesic species cannot (31, 95).
In the field, an Australian lizard (,4mphibolurus ornatus) drinks rainwater in
summerand uses it to excrete dietary electrolytes stored in the body during dry
periods (17). Free-living desert lizards (Dipsosaurus dorsalis and Umascoparia)
labeled with tritiated water, showincreased water turnover during a summerrain,
indicating the animals either drank or exchangedwater across the skin (92, 93).
contrast, tritium-labeled chuckwallas (Sauromalus obesus) showed no evidence of
drinking rainwater that was available in summer(96).
Food
In most amphibiansand in freshwater reptiles, wherewater influx is usually large,
the food mayaccount for only a small fraction of total input. However,for many
terrestrial and nondrinking marine reptiles, preformed water in the diet maybe the
major avenue of water gain. Moreover, nearly all input of salts and nitrogencontaining compoundsoccurs through feeding, although cutaneous uptake of salts
from water can occur in amphibians(see below). Thusthe relative amountsof water,
salts, and nitrogen in various diets are important considerations. Assumingthat
rates of food consumptionare proportional to energy requirements, the available
water, nitrogen, and electrolyte contents per unit assimilable energy are calculated
for several foods and diets (Table 1). Several points emergefrom this analysis:
nitrogen imposesa potentially greater osmoticstress than electrolytes, especially for
carnivores, insectivores, and granivores; 2. herbivores must excrete potassium at
comparativelyhigh rates but vegetation is generally moresucculent than other diets;
and 3. sodium is a relatively unimportant osmolyte in these examples.
Table 1 Nitrogen, electrolyte, and water input from various foods and diets: values are
given relative to digestible energy to permit physiologically meaningful comparison
betweendiets
I:ood
(Animal)
Beefsteak(raw)
a
(Human)
Milletseed
a
(Human)
Cabbage
(raw)
a(Human)
Mixed
desert plants
(Lizard,bSauromalus)
Mealworms
(Tenebrio)
(Lizard,cUta)
d
(Frog, Phyllomedusa)
Nitrogen Sodium Potassium Calcium Chloride
Water
~tmolkca1-1
mlkca1-1
423
7
23
0.5
--
0.12
346
0.3
34
1.5
--
0.04
--
3.85
619
36
249
51
803
14
268
--
127
0.62
877
920
4
8
34
29
---
19
18
0.34
0.27
Calculated from: aWatt&Merrdl(129); bNagy(96) and Nagy&Shoemaker
(99); CNagy
published);dShoemaker
&McClanahan
(118).
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452
SHOEMAKER& NAGY
Adult amphibiansare carnivorous(usually insectivorous), and their diet is thus
especially high in nitrogen and relatively low in electrolytes. Urinaryexcretion of
dietary nitrogen as ammonia
or urea requires amountsof water vastly in excess of
inputs from the diet and oxidative metabolism (118). Thus feeding amphibians
generally dependheavily on other water sources, even if they are able to minimize
evaporative water by either behavioral or physiological means. A few species of
anuranamphibiansexcrete nitrogen primarily as insoluble uric acid or urate salts
and have low rates of evaporative water loss (39, 80, 117, 118). Fluxes of water,
electrolytes, and nitrogen in one of these (Phyllomedusasauvagei) maintainedin the
laboratoryon a diet of insects as the only watersourceare similar to those of desert
reptiles (Tables 2 and 3). Unfortunately,osmoregulatorystudies of amphibiansare
almostalwaysconductedon fasting animals,thus the role of diet is presentlydifficult
to assess.
Input rates of water, electrolytes, and nitrogen via the diet are knownfor only
a few reptiles, all desert dwellers (Tables 2 and 3). In these animals, the food
providesfrom60 to 90%of total water input and all of the salt and nitrogen input.
Metabolic Ve’ater
FromTable2 it is clear that rates of oxidation waterproductionare low in comparison to water losses even in xerophylic reptiles and amphibians.In no case does
Table2 Itemizedwaterbudgetsin various desert reptiles and twospecies of arboreal
frogs; food and metabolismare the only sources of waterprovidedin these examples
Water fluxes (ml kg-1 day-1)
Input
Species
Desert iguana
Dipsosaurus
dorsalis
Mojave Fringetoed Lizard
Urea scoparia
Colorado Fringetoed Lizard
Urea notate
Chuckwalla
Sauromalus obesus
Grooved Tortoise
Testudo sulcata
Desert snake
SpalerosopMs
cliffordi
Argentine tree frog
Phyllomedusa
sauvagei
Mexicantree frog
Pac~ymedusa
dacnicolor
Output
food metabolism total
evaporation feces urine salt
Conditions
gland total
diet (references)
26.9
3.6
30.5
8.6
18.6
0.8
2.5
30.5
field, summer;
desert vegetation (90)
7.1
4.7
11.8
11.0
3.3
0.2
1.5
16.0
9.2
2.1
11.3
8.1
a2.3
--
0.9
11.3
21.1
3.4
24.5
12.3
7.6
1.9
2.7
24.5
23.9
3.7
27.6
7.4
3.7
18.3
--
29.4
15.3
1.4
16.7
12.4
1.2
0.1
--
14.5
field, summer;
desert arihlopofls and
vegetation (93)
estimated field, summer;
insects (Tenebrio larvae)
(31
field, spring;
desert vegetation (96)
outdoors, summer;
green vegetation (23)
laboratory, 30°C;
mice (38)
6.1
2.5
8.6
17.1
0.5
3.8
--
21.4
6.1
2.5
8.6
1
1.6
--
alncludes urinary losses.
250
258
laboratory, 26° C;
insects (Tenebrio larvae)
(117, 118)
laboratory, 26°C;
insects (Tenebrio larvae)
(118)
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OSMOREGULATION
IN AMPHIBIANS AND REPTILES
453
Table 3 Itemized nitrogen and electrolyte budgets for desert lizards (Sauromalusobesus
and Umascoparia) and tree frogs (Phyllomedusasauvagei and a;
Pachymedusa
dacnicolor)
food and metabolismwere the only sources of water in these studies.
Nitrogen and electrolyte fluxes (mmolkg-1 -1)
day
Input
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Species
NITROGEN
Sauromalus
Phyllomedusa
Pachymedusa
POTASSIUM
Sauromalus
Uma
Pl~yllomedusa
Pachymedusa
SODIUM
Sauromalus
Uma
Phyllomedusa
Pachymedusa
CHLORIDE
Sauromalus
Uma
Phyllomedusa
Pachymedusa
food
19.3
23.8
23.8
urine
13.5
17.6
1.1
Output
salt gland
feces
total
----
5.8
1.4
3.5
19.3
19.0
4.6
6.6
1.7
0.72
0.72
2.9
0.9
0.32
0.21
3.0
1.0
---
0.5
0.2
0.03
0.09
6.4
2.1
0.35
0.30
0.51
0.81
0.22
0.22
0.13
0.17
0.33
0.01
0.16
0.97
---
0.2
0.07
0.03
0.09
0.49
1.21
0.36
0.10
3.1
0.6
0.5
0.5
0.04
0.01
0.3
0.004
2.1
0.6
---
0.2
0.1
0.1
0.1
2.3
0.7
0.4
0.1
aConditionsand references as in Table 2.
metabolic water match evaporation, indicating that normally active desert reptiles
cannot remain in water balance without either drinking or eating succulent food.
However, whena reptile uses a humid burrow, evaporation may be reduced to the
point where oxidation water input balances losses. Reptiles living continuously in
very moist soil, such as the small fossorial snakes and amphisbaeniansin tropical
regions, mayexemplify this situation.
Water movesreadily by osmosis across the skin of amphibians, and for steady-state
animals maintained in fresh water this results in a very large net water influx.
Althoughthe magnitudeof this influx varies with body size, species, and temperature, it is typically on the order of 500 ml kg-1 day-1, with the moreterrestrial species
tending to have higher cutaneous permeabilities (5, 94). Aquatic urodeles apparently
have lower rates of osmotic influx (~ 100 ml kg-~ day-~) (7). Dicker & Elliott
(34) placed freshwater-adapted Rana cancrivora into various concentrations of
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SHOEMAKER& NAGY
NaC1, urea, and sucrose. Initial net water fluxes observed were directly proportional to the osmotic gradient, regardless of the nature or concentration of the solute.
Thus an amphibian entering a hyperosmotic environment will initially lose water
across the skin. However,euryhaline species adapted to high salinities maintain
the solute concentration of their body fluids slightly above that of the medium
and thus still obtain water by osmosis, albeit at lower rates than animals in fresh
water.
Amphibians may incur substantial water deficits during periods spent out of
water. In manyspecies of anurans (but apparently not in most urodeles), loss of body
water elicits an increase in the hydraulic conductivity of the skin, whichenables the
animal to rehydrate very rapidly either in water or from a wet surface. However,
there are large interspecific differences such that some species show almost no
change in the permeability of the skin, and others increase rates of water uptake by
about an order of magnitude. The spadefoot toad (Scaphiopus couchi) rehydrates
rapidly only in the first day or two following emergence from its overwintering
burrow(66). At least part of this interspecific difference is caused by differences
the responsivenessof the skin to arginine vasotocin (5, 67). In somecases the ventral
pelvic skin appears to be primarily responsible for this rapid water uptake, and the
animals rehydrate almost as rapidly in a shallow layer of water as when totally
immersed(2, 85). Hypervascularization of the pelvic skin may also enhance water
uptake (21, 107). Also, in species (e.g. Bufo) with extensive "sculpturing" of the
outer skin surface, water movesin capillary channels over most of the body from
the ventral surface that is in contact with water (21, 76).
Soil moisture appears to be a major source of water for someamphibian species.
Passive cutaneous uptake of water from soil is theoretically possible if the free
energy of water in the animal (an inverse function of the concentration of the body
fluids) is less than the free energy of water in the soil (determined by the forces
binding water to soil particles.) In some cases the direction of water movement
follows this simple prediction (84), but other species require wetter soil than would
be predicted on this basis. Fossorial frogs can apparently absorb water from dryer
soil than species that do not normally burrow (128), and the urodeles tested all
require very wet soil for water uptake to occur (119). Intimate contact betweenthe
skin and the soil-capillary channels is required for water transfer, and interspecific
differences maybe due to differences in skin surface structure affecting this contact
(68). As soil dries and its water potential falls, the soil-body gradient mayshift
favor a net efflux of water. Onefactor operating in the animal’s favor in this situation
is that dryer soil has a lower hydraulic conductivity. Also, some species isolate
themselves from the drying soil by forming cocoons from multiple layers of dead
epithelium and possibly other materials (86, 104, 114). In the spadefoot toad
impervious cocoon is not formed, but the burrowed animals accumulate high concentrations of urea in the bodyfluids and thereby maintain a more favorable gradient
with soil water (84, 86).
The skin of adult anurans and urodeles is capable of net transport of sodium and
chloride inward, even when the animals are exposed to environmental concentrations less than those usually found in fresh water (~ 0.2-1 mM).The net rate
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OSMOREGULATION
IN AMPHIBIANS AND REPTILES
455
cutaneous influx of Na in unfed animals in Na balance can be approximated from
the rate of urinary excretion of this ion. For Ranapipiens and Bufo marinus in
"fresh water" this is between0.1 and 1 meqkg-t day-t (57, 111), and values for two
aquatic urodeles calculated from Bentley’s data (7) also fall within this range.
Estimates made using isotopic sodium (63, 64, 94) tend to be somewhathigher
1-3 meq kg-t day-t). Sodiumuptake via the skin probably exceeds dietary gains
(Table 3) in amphibians that spend most of their time in water. Active sodium
uptake shows saturation kinetics and is concentration dependent within the range
of sodium concentrations found in flesh water. Ks typically falls between0.1 and
0.5 mM,with the moreaquatic species having the higher affinities (64, 94). Sodium
depletion of the animal increases the rate of cutaneousuptake, but not Ks. Aldosterone increases sodiumuptake across frog skin in vivo and in vitro, and this is thought
to be the primary meansby which anurans regulate sodium gains by this route (5).
Neurohypophyseal hormones also increase active sodium transport across amphibian skin, but the stimuli for their release (dehydration or solute loading) are
opposite to those for aldosterone and do not coincide with situations in which
increased sodium uptake would be physiologically important.
Amphibiansare exceptional in their ability to conserve sodium while producing
urine at high rates, and the necessity of cutaneous uptake for the maintenance of
sodium balance has recently been called into question. Frogs are not demonstrably
sodium depleted whenkept in running deionized water for up to 60 days (82),
in tap water containing amelioride, which blocks the sodium pump(6). Thus cutaneous sodium uptake is probably essential in aquatic amphibians fasting for long
periods, but available evidence indicates that dietary sodiumintake is usually more
than adequate to balance losses. It is conceivable that amphibians could obtain
sodiumfrom moist soil, but no information is available on this. Interestingly, in vitro
measurementsof short circuit current and transepithelial potentials indicate that
R. cancrivora continues to actively transport sodium inward even in a hypersaline
environment (60, 62). However, urinary sodium concentrations remain very low
(5-20 mM)whenthese flogs are adapted to hypersaline media (60), suggesting
sodiuminfluxes are not particularly large.
In larval amphibiansthe gills rather than the skin provide the site of active sodium
and chloride uptake, and the skin’s acquisition of transport function occurs abruptly
at metamorphosis (36).
Water permeability of reptilian skin in contact with aqueous solutions has been
demonstrated by measuring the movementof tritiated water between the animal and
its bathing medium(56, 105, 125). However,gross influxes and effluxes measured
in this wayare so large (because of exchangediffusion) that net cutaneous water flux
is difficult to determine. Using gravimetric methods, Cloudsley-Thompson(22)
found no cutaneous water gain from damp sand or a water bath in Crocodilus
niloticus, even by dehydrated animals. Similar results were obtained by Diefenbach
(35) in C niloticus and Caimancrocodilus, and by Krakauer et al (72) in several
small snakes and amphisbaenians immersed in moist sand. Evidence that Caiman
sclerops and the freshwater turtles Pseudemysscripta and Trionyx spinifer gain
water across their skin (11, 12), has been questioned on methodological grounds
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SHOEMAKER& NAGY
(35). To date, no reptile has been convincingly shownto take up or lose significant
quantities of water by osmosis across the skin, in markedcontrast to amphibians.
Moreover, Robinson & Dunson (105) have shown that the skin of the euryhaline
turtle MalacIemysterrapin is essentially impermeableto sodium.
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Cloaca and Pharynx
It is not knownwhether water or salts enter amphibians from the aquatic environmentacross epithelia other than the skin. Somearboreal forms are reported to fill
their bladders via the anus for use in wetting egg masses deposited in trees (103).
Freshwater turtles (Trionyx spinifer, Pseudemysscripta, Chelydra serpentina,
Chrysemyspicta) take up sodium from dilute solutions (41, 127). The uptake sites
appear to be the mucousmembranesof the pharynx, cloaca, and cloacal bursae, all
of which display active sodium transport in vitro (41). Somechloride follows the
sodium, but most of the anion influx involves someother substance, possibly bicarbonate. These membranesapparently do not transport potassium. The euryhaline
marine turtle Caretta caretta does not take up sodium or potassium from dilute
solutions (53). Although the cloaca is knownto reabsorb urinary water in many
terrestrial reptiles, cloacal uptake of environmental water has not been demonstrated in aquatic forms. Caimancrocodilus showedno weight gain whenits cloaca
was irrigated with distilled water or physiological saline (35).
OUTPUT
Amphibiansand reptiles lose water, salts, and nitrogen in feces and urine, and
solute-free water by evaporation from skin and respiratory tract. Someterrestrial
and marine reptiles also lose salts and water via salt glands. For animals living in
freshwater, fossorial, or damptropical habitats, water maybe so abundant that the
problem is how to excrete the excess while conserving salts that may be in short
supply. Onthe other hand, marine and terrestrial forms maybe required to excrete
or store excess nitrogen and salts while conserving water.
Evaporation
The integument of most amphibians offers little if any resistance to water
evaporation. Rates of evaporative loss are thus highly dependent on humidity,
temperature, and wind velocity. Tracy (126) estimated that evaporative loss rates
for Ranapipiens in Michigan could vary from 30 to 1600 ml kg-t day-~. Numerous
measurements under a variety of environmental conditions have failed to show
physiologically significant interspecific variations in evaporationrates related to the
appearance or "wetness" of the skin or the animal’s habitat preference. Suchdifferences as have been observed in both anurans and salamanders probably reflect
differences in size and shape as well as postural and other behavioral differences (5,
114, 121). For the vast majority of amphibians,bodysize is the major intrinsic factor
determining the rate of evaporative water loss (114, 121). Large amphibians lose
muchless water per unit of surface than smaller ones, probably because the unstirred boundarylayer increases with body size, and this is the major determinant
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OSMOREGULATION
IN AMPHIBIANS AND REPTILES
457
of water flux whenthe skin itself is highly permeable(100). The secretion of mucus
apparently does not affect the rate of water loss, but mayplay a role in basking
species by preventing skin damagedue to desiccation when evaporation rates are
very high (77).
A few species of frogs do not depend on a humid environment to prevent rapid
dehydration awayfrom water. TwoAfrican tree frogs of the genus Chiromantis (39,
80) and several membersof the South Americangenus Phyllomedusa (118) exhibit
rates of evaporative loss similar to those of desert lizards under comparableconditions and only about 5%of those typical of anurans. The Phyllomedusa possess
specialized glands in the skin which secrete a waxysubstance onto the skin surface
(14). The Chiromantis apparently lack lipid glands, and the mechanismby which
its skin is rendered impermeableremains to be determined. Histologically the skin
of Chiromantispetersi appears indistinguishable from that of other anurans, except
there are multiple layers of iridophores in the dermis of dorsal skin (39). It has been
postulated that the typically low resistance to cutaneous evaporation in amphibians
is a necessary consequence of the use of this organ for water uptake and gas
exchange. Cutaneous respiration has not been measured in either Chiromantis or
Phyllomedusa, but both can take up water rapidly through the skin (39, 118).
The formation of a cocoon, mentioned previously in connection with water exchange with the soil, can also greatly reduce evaporative water losses in air (86).
However, the cocoon renders the frog immobile and forms slowly, and would thus
be of little use to the animal in exposedsituations. Also, species of frogs whichhave
poorly vascularized skin co-ossified with the cranium showreduced rates of water
loss in this region (113), but the benefits of this in the water economyof the frog
have not been evaluated.
Water losses due to pulmonaryventilation have not been measuredin amphibians,
but cutaneous permeability is so high in most cases that respiratory losses are
negligible by comparison.Judging from the situation in reptiles (see below), pulmonary losses probably are a significant componentin Chiromantis and Phyllomedusa.
Bentley (5, 9), Cloudsley-Thompson
(24), and Templeton(123) discussed several
generalizations about evaporation from reptiles. In dry air at 23° C rates of total
evaporation in different species range from 3 to about 2000 ml kg-1 day-l. The
highest rates occur in small (~ 1 g) burrowingsnakes (72), and are like those
in small amphibians. Evaporationrates are strongly correlated with habitat aridity:
diurnal desert lizards have the lowest rates and subtropical fossorial snakes and
amphisbaeniansshowthe highest. This correlation obscures any potential relationships between evaporation and body mass, surface:volume ratio (although this
occurs within a given species), or taxonomicgroup. However,even in desert reptiles,
which have the lowest rates of water loss per unit area of skin, cutaneous evaporation still accounts for about 50%or more of total evaporation at 23° C. Evaporation
from the skin increases with decreasing humidity and increasing temperature. However, pulmonarywater loss increases moreas temperature increases, so that cutaneous evaporation becomes a smaller fraction of the total. Pulmonary evaporation
rates are surprisingly variable in reptiles and do not necessarily reflect metabolic
rate: ratios of pulmonaryevaporation (mg) to oxygen consumption (ml) vary
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0.5 to 4.9, the higher values generally found in aquatic reptiles. Explanationsfor this
mayinvolve difference in 1. oxygenextraction abilities, and 2. extent of any nasal
heat exchanger. Oxygenextraction values vary from about 1 to 4 ml O2 removed
per 100 ml air ventilated. Pulmonary evaporation can be reduced by exhaling
through a cool nasal passage, which cools the air and causes someof its water vapor
to condense mucous membranes.The nose is cooled during inhalation by conduction and evaporation. Onelizard (Dipsosaurus) has been shown to exhale air that
is cooler than its body.
Since the above reviews were written, several studies bearing on evaporation in
reptiles have been published. Licht & Bennett (74) and Bennett & Licht (3)
sured evaporation rates in several mutant snakes (Pituophis and Natrix) having
few or no scales, no superficial dermal layer, and a muchthinner keratin layer than
normal membersof their species. Evaporative water losses in the scaleless snakes
were not higher than in normal snakes, indicating that scales and a thick keratin
layer may not account for low rates of cutaneous evaporation in snakes. Working
with fourteen species of snakes, Cohen(26) reached several conclusions regarding
evaporation: water loss increases with wind velocity and temperature, cutaneous
evaporation increases twofold or more during the shedding cycle, coiled snakes have
less exposed surface area and lose less water as a result, cutaneous water loss
accounts for about 75%of total evaporation in mesic as well as xeric snakes, and
total evaporation correlates well with habitat aridity. The correlation between
evaporation rates and habitat aridity has been questioned by Dmi’el (37), whofound
that two species of colubrid snakes lost water three times faster than two species of
vipers, even though one viper lives in a mediterranean climate, and one colubrid
occurs in a desert. Similarly, Duvdevani& Borut (49) found that evaporation rates
in four species of Acanthodactylus lizards from arid portions of Israel were up to
five times higher than other desert lizards, but a habitat correlation exists within the
genus. In the snakes Dmi’el (37) studied, evaporation increased during activity, but
cutaneous losses remained unchanged, indicating that movementand bending of the
skin during activity does not increase cutaneous water loss. Elick & Sealander (51)
found that cutaneous evaporation rates in juvenile snakes (Diadophis punctatus and
Carphophis vermis) are much higher than in adults of the same species when
expressed in terms of surface area.
Important problems remaining to be investigated include the nature of the barrier
to cutaneous evaporation, the occurrence and function of nasal heat exchangers in
various species, and the mechanismsfor regulating cutaneous and pulmonaryevaporation within a species.
Salt Glands
There is no evidence that any amphibian possesses salt glands. Several excellent
reviews of salt glands in reptiles are available (29, 43, 46, 47, 101) whichcover the
literature through about 1974. The following brief account of salt glands stems from
these reviews. Salt-secreting glands are located in the eye orbit (lachrymal gland)
in marineeuryhaline turtles, near the base of the tongue (posterior sublingual gland)
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OSMOREGULATION
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in sea snakes, and in the nasal region (lateral or external nasal gland) in lizards.
Freshwaterand terrestrial turtles, terrestrial snakes, and manylizard species apparently do not have functional salt glands. The organization of reptile salt glands is
generally similar to that in birds: manyblind-ending branched tubules anastomose
to form the short excretory duct. The tubules contain three types of cells: the
principal (salt-secreting) cells, which touch the basement membranesurrounding
each tubule and join at their apices via junctional complexes to form the narrow
central lumen; mucouscells located primarily in the blind end of the tubule; and
small basal cells of unknownfunction. Principal cell ultrastructure in reptiles is
generally similar to birds, including abundantlateral and basal mitochondria, Golgi
bodies, sparse apical microvilli,, and extensive lateral (but not basal as in birds)
folding and interdigitating of plasma membranes.
The composition and maximum
rates of secretion of salt gland fluid are related
to habitat and diet. Marine turtles and sea snakes produce secretions containing
primarily sodium (400-900 mM)and chloride (600-1000 mM)but little potassium
(20-30 mM).Potassium concentrations in fluid from marine iguanas (Amblyrhynchus cristatus) are higher (235 raM), but NaC1is still the primary solute (up to 1400
mM).In terrestrial lizards, potassium concentrations are muchhigher (200-1400
mM),and potassium is the predominant cation in herbivorous species. Someterrestrial lizards showremarkable plasticity regarding composition of salt gland secretions, with sodium: potassium and chloride: bicarbonate ratios changing greatly in
an appropriate response to different salt loads. However,these adjustments may
require several days. Maximum
secretion rates are highest in the marine iguana and
sea snakes (2.0-2.5 mmolNaCIkg-~ hr-l), but are about one-tenth this in terrestrial
lizards (secreting primarily potassiumchloride). Thesalt glands in desert lizards are
very important in osmoregulation, eliminating about half of the dietary potassium
and most of the sodium (Table 2).
The mechanismof secretion in reptiles is not known[however, see discussion of
mechanismin birds in Peaker & Linzell (101)]. The presence of folds and channels
in principal cell membranessuggests that a "standing osmotic gradient" may be
operating, but this would not account for formation of an hyperosmotic secretion
into the lumen from each cell. Recent evidence indicates that salt gland Na-KATPaseactivities were similar in a lizard (Dipsosaurux dorsalis), a sea snake
(Pelarnis platurus), and an euryhaline turtle (Malaclemys terrapin) [the Na-KATPaseactivity increased in the turtle with an increased plasma Na concentration
(40)]. K-dependent ATPaseis located primarily in the lateral membranefolds
principal cells in D. dorsalis glands (52). In nasal glands from the lizard Lacerta
muralis and the amphisbaenian Trogonophis wiegmanni, the light microscope revealed striations (which correspond to lateral membranefolds), suggesting that
these reptiles mayhave functional salt glands (109) however, salt secretions have
not yet been found in these species.
Aldosterone reduces sodium but not potassium excretion by lizard salt glands
(101). Several other adrenal hormonesmayinfluence salt gland function, but results
to date are inconclusive.
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Digestive Tract
The role of the digestive tract in osmoregulationby amphibiansand reptiles has been
virtually ignored until recently. Althoughthe water and salt content of several foods
have been examined [summarized by Bentley (9)], assimilation of these dietary
substances has received little attention. In Phyllomedusasauvagei feeding on insects
(Tenebrio larvae), fecal water loss amounts to about 10%of dietary intake, not
because the feces are especially dry (~ 60%water), but because the food is highly
digestible (118). Fecal cation losses relative to intake in this species were 4%
potassium and 14% of sodium. Comparable values for Hyla pulchella were 37%
of potassium and 46%of sodium, and the other five species of anurans used in this
study fell within this range. All species examinedlost about 17%of dietary chloride
via the feces. The relative role of absorption and secretion of ions by the gut in
determining fecal output are unknown,but there is indication that the colon plays
a part in regulation of fecal sodiumlosses in toads (Bufo) (25, 54, 55).
In the few reptiles studied, estimated fecal water losses range from 8 to 70%of
food water inputs (Table 2). Reptiles feeding on plant matter have high rates of fecal
water loss, apparently because vegetation is relatively indigestible comparedto other
diets. Generally, less than 20%of the potassium and chloride in the food is lost in
the feces, but herbivorous lizards lose 30-40%of the ingested sodiumvia this route
(Table 3). In an herbivorous lizard (Sauromalus obesus), assimilation percentages
for some substances not shown in Table 2 are organic matter 87%, ash 5%, magnesium 49%,and calcium 68%(98). The rate of calcium assimilation is relatively
high in these lizards (~ 0.5 mmolkg-l day-l), but the meansby whichexcess calcium
is excreted remain unknown.Calcium is excreted by the kidneys in water snakes,
but apparently not in alligators, where fecal excretion occurs instead (29). Templeton et al (124) suggested that the gut or cloaca mayregulate the flux of sodiumand
potassium between feces and body fluids.
Kidneys
Amphibian and reptilian nephrons have proximal and distal segments which are
usually connected by a short intermediate segment. There are no loops of Henle,
and no amphibian or reptile kidney is known to produce hyperosmotic urine. In
amphibians, ciliated nephrostomesopen to the coelomic cavity. Coelomicfluid can
enter the renal tubules by this route in urodeles and may add to the glomerular
filtrate. Nephrostomesof anurans connect to the renal veins, and they may play a
role in water resorption from the bladder (114). Peritubular circulation in both
amphibians and reptiles is derived from the efferent glomerular arterioles and from
renal portal veins.
The amphibiankidney is admirably suited for life in fresh water and, so far as
is known,all amphibians can produce dilute urine at very high rates (~ 10-25 ml
kg-~ hr -t) whenmaintained in fresh water. Glomerular filtration rates (GFR) are
high (~ 20-50 ml kg-I hr l) in this situation, and can be considerably higher in
experimentally water-loaded animals. In anurans, only about half of the filtered
water is resorbed in the tubules, but resorption of sodiumand chloride maybe nearly
complete (",, 99%), see e.g. (57). In larval salamanders, t3FR tends to be lower
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OSMOREGULATION
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(~ 8-16 ml kg-1 hr-l), but only 10-30%of the filtered water and 90-95%of the
filtered sodium are resorbed whenthe animals are in fresh water (71, 122). When
the concentration of the environmental mediumis increased, GFRis drastically
reduced and fractional water resorption increases markedly, Urinary sodium concentrations in adult anurans and urodeles in fresh water are commonlyabout 1 mM
(7, 57, 94).
Amphibiansdeprived of water also quickly reduce urine output, again by reducing GFRand increasing fractional water resorption, and the concentration of the
urine approaches that of the plasma. Althoughthey are unable to produce hyperosmotic urine, renal water conservation is well developed in amphibians because they
can becomecompletely anurie after loss of only a few percent of the body water.
It is usually assumedthat glomerular filtration ceases altogether, but analysis of
kidney function is difficult whenno urine is produced.
Arginine vasotoein (AVT)and, frequently, mammalianneurohypophyseal peptides have strong antidiuretic action in most amphibianstested. In manycases this
results from a combination of glomerular and tubular effects resembling those seen
during water deprivation. Dehydration causes the release of AVTin amphibians,
and it is generally supposed that antidiuresis and the other components of the
"water-balance response" to dehydration (increased water uptake via the skin and
bladder) are controlled by this hormone(8). However,a recent attempt to correlate
circulating AVTlevels with rates of urine production in the bullfrog gave inconsistent results, suggesting that other factors are also involved (110). Corticosteroids,
especially aldosterone, maybe involved in control of renal sodiumexcretion, but in
vivo evidence is scanty (20).
Most amphibians excrete nitrogen primarily as urea and ammonia.Aquatic forms
are generally ammonotelicwhenin fresh water. Someforms, such as Xenopuslaevis,
which is primarily aquatic but sometimesforced to aestivate in soil, switch readily
from ammoniato urea formation. Energetically, ammoniais the most economical
vehicle for nitrogen excretion, but its toxicity precludes its use whenwater turnover
is low. It has been suggested that the main advantages of excretion of ammonia.by
aquatic amphibians are in cation conservation and pHregulation (70), but evidence
is scanty.
In semiterrestrial species, ureotelism appears to be the rule, but these animals
often excrete appreciable amounts of ammoniawhile in water and become completely ureotelic whenwater influx is low. Reduction or cessation of urine production has been shownto lead to the accumulationof urea in a variety of anurans, and
has recently been reported in a salamander (Ambystomatigrinum) (32). Plasma urea
levels of several hundred mMappear to be without deleterious effect, and mayin
fact place the animal in a morefavorable situation for obtaining water from soil or
saline solutions. There is someevidencefor increased rates of urea synthesis in these
situations, but the mechanismsgoverning this are unknown.Accumulatedurea is
rapidly eliminated by the kidneys when the animals return to water. For some
species there is evidence for active tubular secretion of urea, but whenplasmalevels
of urea are appreciable, urinary urea concentrations usually approximate those in
the plasma. This is true even in the crab-eating frog (Rana cancrivora) adapted to
saline conditions where active tubular resorption of urea wouldbe beneficial (112).
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In this situation urine flow rates are greatly reduced (matching osmotic influx)
reducing (~FRto one-fourth "normal" and resorbing more than 90%of the filtrate.
Several representatives of the genus Phyllomedusaexcrete a significant fraction
of their nitrogen wastes as urate, ranging from 80%in P. sauvagei to 20%in P.
hypochondrialis (118). About 5%of the excreted nitrogen is ammonium,with the
balance madeup of urea. In these species the partitioning of nitrogen amongthe
various products is independent of water turnover, and most of the ammonium
excreted is in the form of precipitated urate salts. Whenuricotelic frogs are maintained out of water and fed, precipitated urate accumulatesin the bladder, indicating
continued renal function during water deprivation in these species. In P. sauvagei,
urate excretion prevents the rapid build up of urea in the body fluids and also aids
in electrolyte excretion (45% of the sodium input and 22%of the potassium input
were excreted in precipitated form). Chiromantis xerarnpelina and C. petersi also
excrete large amounts of urate, and these species presumablyreap similar benefits
(39, 80). Uricotelism combinedwith low rates of evaporative water loss place these
arboreal amphibiansin a position similar to that of insectivorous lizards in terms
of their ability to osmoregulate without access to fresh water. The extent to which
kidney function in these species differs from the typical amphibianpattern remains
to be elucidated.
In normally hydrated reptiles, CIFRranges from 0.5 to 16 ml kg-t hr -1 (28).
Although terrestrial
species tend to have lower GFRthan freshwater and marine
species, this is not always true. GFRusually doubles or triples in water-loaded
animals, but somespecies showdecreases and others increases of more than tenfold.
In salt-loaded or dehydrated reptiles, GFRusually decreases, but again there are
exceptions. In several species of turtles, ureteral urine flow stops whenplasma
osmotic pressures increase sut~ciently, apparently because filtration ceases. Urine
flow stops in the desert tortoise (Gopherusagassizii), whenplasma osmolality has
increased 100 mosMabove normal. In the freshwater turtle (Pseudemysscripta),
this occurs with only a 20 mosMincrease (30). Changesin GFRwithin an individual reptile apparently result primarily from differences in the numberof functioning
glomeruli.
Tubular resorption of filtered water in reptiles ranges from about 40 to 90%in
normally hydrated or water-loaded animals to as high as 98% in dehydrated or
salt-loaded animals, which are close to producing no ureteral urine at all (28).
Sodiumresorption ranges from 55 to 98%in normally hydrated animals to as high
as 99.5%in dehydrated turtles (Pseudemysscripta). Changesin sodium resorption
with water and salt loads in various species are inconsistent and generally not large.
For potassium the few results available indicate that tubular reabsorption can
approach 100%, but under different conditions, tubular secretion of potassium
occurs, and net potassium excretion can exceed filtration more than twofold (28).
The osmotic concentration of ureteral urine varies from about 30 to 100%of plasma
osmotic concentration. Althoughthere are hints of somecorrelations between habitat and renal parameters in reptiles, the small numberof species examinedto date
does not warrant generalizations. In the few reptiles examined, AVTdecreases GFR
and increases tubular resorption of water and sodium, and maydecrease secretion
of potassium (28). Aldosterone apparently has little effect on renal function (16).
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OSMOREGULATION
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Nitrogenous excretory products in reptiles are primarily urea and uric acid (or
"urate"), although aquatic reptiles such as freshwater turtles and crocodiles can
excrete up to about 40%of total nitrogen output as ammonia.Urea is important
in most turtles, regardless of habitat, but snakes and lizards eliminate more than
90%of their waste nitrogen as urate. In aquatic reptiles, most urinary ammoniais
apparently synthesized and secreted directly into the filtrate by the kidney tubules.
Urea generally enters kidney tubules by filtration, although there is someevidence
for active secretion and resorption (28). Most of the urate appearing in the urine
of terrestrial reptiles is actively secreted by the tubules. Relatively large volumesof
water accompanyexcretion of ammoniaand urea because both are very soluble, and
high concentrations of ammoniaare toxic. However,urate precipitates easily, thus
removing its contribution to urine osmotic pressure. Moreover,muchof the urinary
cation load maybe boundto the precipitate, thereby reducing urine osmotic concentration even further and facilitating water resorption. Althoughprecipitated urate
has been found in ureteral urine, it is not knownwhetherprecipitation occurs in the
kidney at a site where tubule function maybe affected. Tubular transport of urate
in snakes is dependent on potassium but not sodium. Rates of ammoniaexcretion
via ureteral urine have been measuredin only three reptiles, and range from 0.5 to
about 1.7 mmolkg-1 day-1. Little is knownabout rates of renal output of urea or
urate.
The formation and excretion of urinary precipitates in lizards have been investigated recently. In three desert lizards eating natural diets, about 40%of total
potassium output, and 14%of total sodium output, was in the form of urinary
precipitates (90, 93, 96). The rate of bound potassium excretion in S. obesus increases with increasing potassium intake, and at a given potassium-intake rate,
precipitated potassium output is independentof dietary nitrogen levels (97). Apparently, this is accomplished by recruiting body nitrogen to produce urate when
nitrogen intake is low, as well as by packing more potassium onto each urate
molecule (molar ratios of potassium: urate range from 0.01 to 3.17). Minnich (91)
presented evidence that cations are chemically bound to urate in reptiles, but
McNabbet al (88), McNabb& McNabb(87), and Lonsdale & Sutor (78) suggested
that precipitated cations maybe physically boundor trapped in bird urinary solids.
The relative roles of the kidney and cloaca in precipitate formation are not clearly
defined.
Cloaca and Bladder
The bladder of amphibians is a distensible outpouching of the cloaca and, except
in highly aquatic forms, is usually quite capacious. Semiterrestrial anurans are
commonlyobserved to retain urine equivalent to 20-50% of the bladder empty
weight. Bladder capacity in urodeles in generally muchless than in anurans (1,120).
The anuran bladder resembles the skin in that its permeability to water is generally
variable and under the control of antidiuretic hormone(AVT).The responsiveness
of the bladder to antidiuretic hormones diminishes markedly with water loading,
and this mayalso play a role in regulation of resorption from the bladder (50).
Moreover, the amphibian bladder is capable of actively resorbing sodium from the
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bladder contents. The rate of sodiumtransport by anuran bladders in vitro is usually
increased by neurohypophysealpeptides, aldosterone, insulin, and epinephrine, and
a variety of synergistic effects have been reported. The bladders of most urodeles
studied appear unresponsive to AVTand also perhaps to aldosterone (5, 8).
The potential osmoregulatoryutility of dilute urine stored in the bladder has long
been recognized. Bufonid toads subjected to dehydration in air have been found
to maintain the concentration of the body fluids remarkably~constant until bladder
reserves are exhausted (108, 115). A similar phenomenonhas recently been repo~ted
in a salamander (.4mbystomatigrinum) (1). In dehydrating spadefoot toads (Scaphiopus couchi), bladder water is also resorbed, but the plasma solute concentrations
fluctuate unpredictably before water losses exceed stored reserves (83). It thus
appears likely that a major function of the amphibianbladder is to provide a water
source to compensate losses in amphibians foraging on land. The bladder probably
plays a similar role in fossorial forms, allowing the animal to store water whensoil
moisture is high for use in the event that the soil dries (84).
The bladder could also serve to decrease urinary sodium losses from amphibians
in fresh water; bladder urine from sodium-depletedtoads (Bufo marinus) in distilled
water has a lower sodium concentration (approximately 0.2 mM)than ureteral urine
(1-2 mM)(89). However, bladders tend to be small in aquatic amphibians,
ureteral urine can be as dilute as urine from the bladder, see e.g. (54, 57).
saline-adapted Bufo the sodium and osmotic concentrations of bladder urine tend
to be higher than in ureteral urine (54), but these differences are neither large nor
consistent. Thusthere is little evidence that post-renal modification of the urine by
the amphibian bladder plays an important osmoregulatory role when the animals
are in fresh or saline water, but maybe significant in situations leading to sodium
depletion.
Uricotelic frogs (Phyllomedusa and Chiromantis) accumulate large amounts of
urate in the bladder when they are fed and deprived of additional water. It seems
likely that water resorption and urate precipitation occur in the bladders of these
animals, but this awaits definitive study.
Sections on cloaca and bladder function in reptiles can be found in reviews by
Dantzler & Holmes(29), Bradshaw(16), and Bentley (9). Ureteral urine enters
cloaca, and mayenter the urinary bladder in reptiles that have one (turtles and many
lizards, but not snakes or crocodilians). There is someindication that urine mayalso
enter the colon or large intestine, as occurs in birds. Muchcircumstantial evidence
suggests that these organs can modifyureteral urine before it is voided. Cloacal and
bladder membranesactively resorb sodium from urine, and are permeable to water
in varying degrees. Water resorption mayoccur in conjunction with ion transport,
or simply in response to plasma colloid osmotic pressure (9). There is someevidence
that the cloaca may resorb bicarbonate and secrete potassium. Fromvalues for GFR
and tubular water resorption in normally hydrated reptiles given above, we estimate
that ureteral urine flow ranges from 30 to 220 ml kg-1 day-1. Whencompared to
rates of water loss via voided urine (0.1 to 18 ml kg-1 day-l; see Table 2), it is evident
that post-renal water resorption can be very important in water balance in some
species. In fact, the abilities of reptilian kidneysto vary urine compositionare rather
unimpressive when compared to those of mammaliankidneys. However, urine that
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OSMOREGULATION
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465
is finally voided can be quite different from that produced by the kidneys, again
suggesting that the cloaca, bladder, and intestine play major roles in reptilian
osmoregulation. Recently, Bradshaw(16) has shown that the cloaca of a lizard
(,4mphibolurus ornatus) can resorb up to 450 ml H20 kg-~ day-t, 24 mmolsodium
kg-~ day-1 and 5.5 mmolpotassium kg-~ day-~ whenthese animals are water loaded.
These resorption rates are muchhigher than total input rates estimated for several
lizards (Tables 2 and 3). Braysher(18) reported that cloacal, but not ureteral, urine
of a related species (Amphibolurus maculosus) can be hyperosmotic to plasma. In
the lizard Varanus gouldii, AVTdoubled the rates of water and sodium resorption
by increasing sodium transport and cloacal permeability to water (19). However,
a freshwater turtle (Chrysemys picta) hypophysectomy had no effect on urine
plasmaelectrolyte concentrations (127). Aldosteroneinjections have little effect
the compositionof voided urine in lizards, but turtle bladders respond by conserving
sodium. There is someevidence that corticosterone promotes sodium excretion in
lizards (15).
BALANCE
AND STORAGE
Fully hydrated amphibians typically have a high water content (~ 800 ml kg-~) and
low concentrations of plasma sodium (100-120 mM)and total solutes (200-250
mosM)compared to other vertebrates. This may aid in maintenance of water and
salt balance in fresh water and is probablypart of the basis for the tolerance of many
amphibiansto large losses of water via evaporation. Manysemiterrestrial species of
anurans can withstand the loss of about half of their body water (400 ml kg-~) and
the attendant doubling of body fluid concentrations, and some species have even
greater tolerances. Urodeles are generally moreaquatic and less tolerant of desiccation, but Ambystomatigrinum survives the loss of 450 ml kg-~ (1).
Dehydration tolerance coupled with the ability to store large volumesof water
in the bladder presumably allow amphibians to exploit terrestrial environments
where water etflux by evaporation exceeds influx from feeding. Reductionor cessation of urine production and storage of urea also aid in this, as does the rapid rate
of rehydration through the skin of anurans whenwater is available. Thus most of
the more terrestrial
amphibians appear adapted to let their water balance swing
through wide oscillations, the period of which is dependenton environmentalconditions determining the rate of evaporative water loss. These oscillations are avoided
or greatly dampedin those xerophylic arboreal species that have greatly reduced
evaporative losses and are uricotelic.
Amphibiansadapted to saline media store solutes and remain at least slightly
hyperosmoticto their environment.Studies in whichexposure is relatively brief (a
weekor less) generally showthat storage of electrolytes is the primary factor in
raising the osmotic concentration of the plasma (59, 69, 71), whereas long-term
acclimation usually results in the accumulation of considerable concentrations of
urea (65, 106) or someother non-electrolyte (75), and in increased salinity tolerance.
The exceptional ability of Ranacancrivora to survive in saline media is probably
related to the exceptionally high rates of urea production exhibited in this species.
Experimentation with unfed amphibians may lead to underestimation of salinity
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tolerance, because these fasting animals must deaminate a significant fraction of
their protein to produce and maintain high concentrations of urea (106).
The composition and volumes of body fluids in reptiles as a whole are generally
similar to those for birds and mammals,although reptiles show wider variation.
Fluid volumes, in ml per kg body mass range from 650-760 for total water, 360-580
for intracellular fluid, 150-350for extracellular fluid, and 33-70 for plasmavolume
(9). Similarly, plasma electrolyte concentrations in reptiles are not unusual, with
sodium concentrations ranging from about 112 to 140 mMin normally hydrated
freshwater species, and from 150 to 180 in steady-state terrestrial forms. The marine
iguana has 178 mMsodium, but the plasma of a sea snake (Pelamis platurus)
contains 264 mMsodium. By appropriate utilization of the various avenues of
output, reptiles are apparently able to remainin balance, although the details of this
are knownfor only a few species (Tables 2 and 3). However,in somereptiles under
certain conditions, balance is not achieved, and net storage or depletion of water,
salts, or nitrogen occurs.
There are no documentedcases of reptiles storing water in anticipation of dehydrating conditions, although this mayoccur in the desert tortoise Gopherusagassizii
(30), and the desert lizard Aporosauraanchietae (79). But storage of electrolytes
occurs in at least one lizard: during droughts, Arnphibolurus ornatus continues to
eat sodium-rich ants, thereby maintaining normal fluid volumes but tolerating an
increase in plasma sodium concentration up to 300 mM(17). High-plasma sod~.um
concentrations have been found in other lizards, but these apparently resulted from
water loss rather than salt storage. During winter hibernation in fresh water, plasma-sodiumconcentration in the turtle Trionyx spinifer can drop as low as 81 raM.
The euryhaline turtle Malaclemyscentrata stores urea in body fluids in adjusting
to a seawater environment (58). Amongterrestrial lizards, tolerance to dehydration
appears to be correlated with habitat, with desert species surviving up to 50%body
massloss (95). Reptiles in general are able to tolerate muchwider variations in body
water content and electrolyte concentrations than can birds or mammals.As in
amphibians, this enhancessurvivorship in stressful situations.
CONCLUDING
STATEMENT
Reptiles, because of low skin permeability, uricotelism, and salt glands, are well
adapted to remain in water and solute balance with moderate to low rates of water
turnover. Dietary and metabolic water inputs are frequently sufficient to offset losses
attendant uponexcretion, elimination, and gas exchange, as well as cutaneous losses.
Amphibiansgenerally have very high rates of water turnover unless, like fossorial
forms, they exploit environmental situations where water fluxes across their highly
permeable skins are low. Manyamphibians have remarkable tolerances (shared to
a considerable degree by reptiles) to osmotic imbalances,and are able to rectify these
rapidly whenwater becomesavailable. Striking exceptions to these generalizations
are found in both amphibians and reptiles, and these departures from the usual
pattern provide insights into the physiological adaptability of these diverse and
interesting groups of Vertebrates.
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