AMER. ZOOL., 30:137-146 (1990)
Ecological, Evolutionary, and Physical Factors
Influencing Aquatic Animal Respiration 1
JEFFREY B. GRAHAM
Physiological Research Laboratory and Marine Biology Research Division,
Scripps Institution of Oceanography, University of California, San Diego,
Lajolla, California 92093
SYNOPSIS. Compared to air-breathers, animals that respire aquatically have limited access
to O2 and their habitats are more subject to hypoxia. Because O 2 diffuses more slowly
through water than air, animals in water experience greater diffusion boundary layer
effects on respiratory gas diffusion. While ventilation and specialized exchange surfaces
mitigate O2 diffusion limitations on respiration, most animal phyla, particularly those
confined to aquatic habitats, lack these. Diffusion limitation influences the ontogeny of
aquatic animals and may have also shaped Precambrian metazoans. In spite of a more
limited O2 access, aquatic animals display a much greater spectrum of respiratory adaptation, ranging from the loss of Hb in icefishes to the independent evolution, invention,
and acquisition of Hb in many invertebrates confined to hypoxic habitats. Three features
of aquatic respiratory systems distinguishing them from aerial systems are the widespread
occurrence of integumental respiration, the frequent presence of combined respiratory
and feeding surfaces, and the profound effect of hypoxia on shaping respiratory adaptation, both in shallow water and in the deep sea.
INTRODUCTION
This essay examines ways that the respiration of aquatic animals deviates from
"The Terrestrial Paradigm of Animal Respiration." Its objectives are to describe
unique features of the respiratory mechanisms of aquatic animals. This is done by
contrasting the physical properties of water
and air that affect gas exchange and considering the effects of life in water on the
general nature of animal gas exchangers
and related functions. This review makes
comparisons among similar groups occurring in both terrestrial and aquatic habitats, animals that have secondarily reinvaded water from the land, and species that
have evolved novel degrees or types of respiratory specialization owing to special
circumstances surrounding their long-term
residence in predictable aquatic environments.
AIR AND WATER AS RESPIRATORY
MEDIA
Physical properties
Physical differences between air and
water affecting respiration have been
1
From the Symposium on Concepts of Adaptation in
Aquatic Animals: Deviations from the Terrestrial Paradigm
presented at the Annual Meeting of the American
Society of Zoologists, 27-30 December 1988, at San
Francisco, California.
treated by Denny (1990) in this symposium. There have also been numerous
analyses of how the physiology of animal
respiration differs in air and water (Rahn,
1966; Dejours, 1988). Simply stated, water
is a thousand times more dense than and
fifty times as viscous as air. Depending upon
its temperature and salinity, water contains
20-40 times less O2 by volume, and O 2
diffuses about ten thousand times more
slowly through water than air (Little, 1983).
Figure 1 compares the O 2 availability in
different aerial and aquatic habitats. The
atmosphere contains 21% O2 by volume
which, at a sea level pressure of 1 atm, is
equivalent to an O2 partial pressure (Po2)
of about 155 Torr (=mm Hg, =20.7 kPa).
At atmospheric equilibrium, the Po2 of
water is the same as that in air (0.21 atm),
yet water contains much less O2 than air
(0.5 to 1.0% vs. 21 %, Fig. 1). From Henry's
law we know that the dissolved O2 content
of water is a function of two factors, Po 2
and the O 2 solubility coefficient of water
(Dejours, 1988; Graham, 1988). The solubility coefficient for O 2 in water is not
large and varies inversely with both temperature and salinity.
Diffusion boundary layer
Water has a low O2 content and O 2 also
diffuses through it more slowly. These factors combine to create a limiting condition
137
138
JEFFREY B. GRAHAM
P02
AIR: 2 1 * 0 ,
1 ATU-760mmHg001.3 kPo)
8 0 - 1 6 0 torr
1.SU 4 0 - 1 6 0 torr
ES.BAYS.ESTUARIES 3 0 - 1 9 0 torr
ENCLOSED SEAS
SWAUPS.UUDFLATS.TIDEPOOLS 0 - 4 4 0 torr
OUL PRORLE 0 - 1 8 0 torr
TYPICAL DEPTH PROFILE S 6 - 1 8 0 torr
DEEP SEA * TRENCHES 4 0 - 8 0 * SATURATION
ENVIRONMENTAL ACCESS TO OXYGEN
FIG. 1. Comparison of the O2 availability in air and water habitats. Air contains 21 % O2; the inverted graph
shows Po 2 in relation to altitude, dropping from near 160 Torr at sea level to 35 Torr at 10 km. With the
exception of burrows and soil, terrestrial habitats are usually near Po2 saturation. Water contains less O2 than
air and many shallow habitats experience wide ranges in Po2. Depth-O2 profiles for a mountain lake, the open
ocean, and the open ocean in an area where an O2 minimum layer (OML) is established, show how water O2
content varies with depth as a result of biotic and physical factors.
for aquatic respiration in the form of a
thicker diffusion boundary layer (Feder and
Pinder, 1988, fig. 4; Graham, 1988). This
is most readily visualized as a stagnant or
unmixed "halo of O 2 depletion" around
an aquatic respiratory surface in still water
that, in the absence of stirring (ventilation),
continues to increase in thickness (see also
Krogh, 1941,fig.6). This layer, the natural
consequence of O2 consumption, limits gas
transfer across all respiratory surfaces to a
greater extent in water than in air (Feder
and Pinder, 1988).
Habitat differences
Figure 1 shows that specific habitats
within terrestrial and aquatic environments differ in their relative O2 content.
Exceptions to the general presence of 21%
O 2 in most terrestrial habitats are rare but
do occur in moist soil and in burrows where,
O 2 may fall to 5% (Krogh, 1941; Dejours,
1988). At increasing elevations air still contains 21% O2, but barometric pressure
declines. The Po2 at the top of Mt. Everest
(nearly 9 km, Fig. 1), about 50 Torr, is
barely sufficient to sustain the resting metabolic rate of a maximally hyperventilating
human (Bouverot, 1985).
Relative to air, the O 2 content of water
is more subject to natural variation (Fig.
1). Po2s ranging from 0 to 440 Torr have
been measured in a variety of shallow habitats. In many bays, swamps, and littoral
pools there are large swings in Po 2 , which
rises during daylight hours as a result of
photosynthesis and drops at night due to
biological O2 demand (Dejours, 1988).
Temperate and alpine lakes have seasonally variable O2-depth profiles and some
enclosed seas have permanent anoxic layers at depth. Although surface waters of
the open ocean may also undergo periodic
changes in O2 corresponding to cyclic
AQUATIC ANIMAL RESPIRATION
changes in O 2 production and consumption ratios, they are generally near air saturation (155 Torr). In most areas of the
open ocean, O2 generally declines in the
deeper reaches of the photic zone but
approaches saturation at greater depths.
However, some trenches and in certain
areas, typically in equatorial waters along
the eastern edges of ocean basins, permanent O2 minimum layers (OML) are formed
at depths of from 200 to 1,500 m (Fig. 1).
COMPARATIVE EFFECTS OF AIR AND
WATER ON RESPIRATORY SYSTEMS
139
iccation and also drown if submerged (Little, 1983).
A similar pattern occurs among earthworms (Annelida, Oligochaeta), which
owing to a circulatory system can be larger
than flatworms (Graham, 1988). In families in which both aquatic and terrestrial
species occur, the latter are generally larger
(Barnes, 1980 and refs.). Some terrestrial
genera (Drawida, Glossoscolex, Rhinodrilus)
grow longer than 1 m, yet the mechanical
limitations of burrowing and diffusion-limited integumentary breathing, force them
to remain relatively thin. Alexander (1971)
calculated that the 1.3 cm body diameter
of R. fafner is close to the maximum possible given its mass (1 kg), O2 consumption
rate (Vo2 = 0.06 ml/g/hr), and a 3 ^m
skin diffusion distance (Fig. 2).
Comparisons of air and water as respiratory media usually focus on requisite
changes in respiratory organ structure and
respiration physiology during the evolutionary transition from one medium to the
other. This essay will contrast the effects
Size limitations during ontogeny and in the
of air and water on respiration by com- Precambrian.—Two very different examparing similar groups (i.e., using largely ples, a fish larva and a giant Precambrian
similar respiratory mechanisms) living in fossil marine worm, illustrate the fundaboth media, by considering the respiratory mental role of diffusion-limited respiration
systems of groups that have reinvaded the in the early life of most aquatic animals and
aquatic realm, and by drawing selected suggest its probable importance in the early
examples illustrating the broad adaptive evolution of the metazoans.
expression that aquatic respiration has
Figure 2 shows how limitations of body
undergone.
size and aquatic O 2 diffusion may impinge
on the ontogenetic development of the
Effects of the diffusion limitation of
anchovy, Engraulis mordax. Anchovy larvae
water on body size
are severely limited at hatching. They lack
Terrestrial-aquatic comparisons. —Because a mouth and functional gills, and their
water has a low O 2 content and diffusivity erythrocytes are not fully formed. They
the diffusion boundary layer around an are also small (1.4 mm length) which means
unventilated surface would tend to grow they swim at a low Reynolds number and
faster and larger in water than in air. The thus are likely to be surrounded by a relimplication of this for closely related dif- atively large diffusion boundary layer.
fusion-limited (i.e., integumentary breath- Nevertheless, young larvae must begin
ing) groups living in air and water is that feeding within two days of hatching, and
species adapted to living in air could, all grow and function normally, while
other things being equal, attain a larger depending mostly upon cutaneous respisize than those living in water. Examples ration. The full complement of erythrosupporting this are seen among the terres- cytes does not appear until day 26 and the
trial triclad flatworms (Platyhelminthes, gills do not fully develop until day 34. FigClass Turbellaria, Order Tricladida), which ure 2 shows how the body radius of a larval
are generally larger than their aquatic anchovy changes with growth and closely
counterparts (Little, 1983). Flatworms lack approaches limits calculated by Alexander
a circulation and depend upon their body (1971) for animals with neither respiratory
surface for gas exchange. Because their tis- surfaces nor effective circulation. In
sue-gas permeability is geared for aerial O 2 actuality, the approach is much closer than
uptake to support a larger biomass, ter- shown because Figure 2, by not taking into
restrial triclads run a greater risk of des- account the added limits to respiration
JEFFREY B. GRAHAM
140
10"
\
^CIRCULATION
^
1:
\
^NOCIRCULATION
R. FAFNBR •
DICKINSONIA * - - ' — - 4 5 5 t o r r
\
I
0.1 ;
10to*r
^
6
•
2
•
«
0.01 :
1 •
nm 0.001
ANCHGVr.10°C
I I i
0.01
11—
0.1
FIG. 2. Graph modified from Alexander (1971) showing the inverse relationship between organismic Vo2
and maximum body radius. Functions labeled "no circulation" and "circulation" show, assuming an ambient
Po 2 of 155 Torr, how radius increases in the presence of convective O 2 transport. Data for the giant earthworm
Rhinodrilusfafner (Alexander, 1971) show its radius to be slightly less than the maximum possible at atmospheric
Po 2 . Function below and parallel to the "no circulation" line shows maximum radius at an ambient Po2 of
10 Torr. Values for the Precambrian Dickinsonia (estimated by Runnegar [1982] for two body mass and
thickness relationships) show that its radius exceeded limits imposed by a Precambrian Po2 of 10 Torr. Anchovy
data show estimated radii (from body mass and length relationship) at different body lengths (cm) and ages
(days): 1) 0.2 cm, 2 days post-hatch; 2) 0.6 cm, 11 days, superficial red muscle appears; 3) 1 cm, 21 days; 4)
1.2 cm, 26 days, full erythrocyte count; 5) 1.7 cm, 34 days, gills developed; 6) 2.2 cm, 44 days. Anchovy body
length-mass and Vo2 data provided by Sandor Kaupp.
imposed by the diffusion boundary layer,
overestimates minimum radius.
The growing anchovy needs to maximize the O 2 gradient between water and
skin, which is done by swimming regularly
(Hunter, 1972; Weihs, 1980) and by developing superficial layers of myoglobin-rich
red muscle (11 days). These muscle layers
appear in many larvae and persist until gill
development is completed (Batty, 1984; ElFiky and Wieser, 1988). In addition to
powering swimming these layers may also
function to store O 2 and facilitate its diffusion from water across the integument
(Graham, 1988).
The strong influence of aquatic O2-diffusion limitation on body size can also give
insight into the respiration physiology,
mode of life, and habitat requirements of
fossil animals. This is particularly important for Precambrian animals, known commonly as the Ediacara or Vendian fauna,
whose body form may have been dictated
by their evolution in an hypoxic atmosphere. Dickinsonia costata, for example, was
a soft-bodied, segmented worm-like creature that was elliptical and grew to about
one meter in length. It was thin (perhaps
as thick as 6 mm) and may have had a mass
of up to 3.4 kg (Runnegar, 1982). Dickinsonia was widely distributed in the Precambrian seas and lived epibenthically in shallow water. Its flat, soft body, which is typical
of most animals from this era, likely maximized surface area to favor respiration in
the low O2 content (2% atmospheric O2;
Cloud, 1976) of Precambrian waters.
Although segmented, Dickinsonia did not
AQUATIC ANIMAL RESPIRATION
burrow; it is generally speculated that low
O2 in the Precambrian caused such a severe
interstitial O 2 gradient that all burrowing
was precluded (Runnegar, 1982).
Figure 2 shows Vo2 and body radius
(thickness) estimates for Dickinsonia in relation to radius limits imposed on diffusionlimited animals by the air-saturated water
of Recent (present) times (Po2 =150 Torr)
and that of the Precambrian sea (10 Torr).
These data are from a study by Runnegar
(1982) who derived Vo2 estimates for Dickinsonia from those of extant worms and
estimated body thickness from fossil
imprints and casts. Even though Runnegar
did not consider the added limitations of
the O2 boundary layer and thus overestimated the maximum allowable radius of
Dickinsonia, Figure 2 shows that it probably
could not have survived in Precambrian
seas without a circulatory system and some
surface-ventilating capacity. We obviously
cannot verify this conclusion by determining the metabolic rate of Dickinsonia. Nor
can we be certain that it did not possess an
entirely different mechanism for dealing
with Precambrian O2 limitation {e.g., it
might have been capable of anaerobiosis,
or it might have had symbiotic zooxanthellae that provided O2 by photosynthesis). However, the fossil material indicates
that Dickinsonia could change its body
perimeter thickness and that it may have
had a coelomic cavity (Wade, 1972; Runnegar, 1982). This evidence suggests that
regional body movements by Dickinsonia
could have enhanced integumentary respiration by ventilating its dorsal and ventral surfaces {i.e., periodic refreshment of
the boundary layer) and perhaps mixing
coelomic or gut fluids. This raises the possibility that the early origin of metamerism
and a coelom may have been more closely
linked to the need to ventilate body surfaces in the low O 2 aquatic environments
of the Precambrian than to burrowing.
Comparative respiratory lessons
imparted by the reinvasion of water
The limiting effects of water are further
elucidated by considering selected groups
that have secondarily returned to an aquatic
existence.
141
First, aquatic members of the oligochaete family Glossoscolecidae, and probably several other families, have secondarily evolved from terrestrial species
(Barnes, 1980 and refs.). Predictably, the
more acute diffusion-limited state of integumentary breathers in water forces their
generally smaller size and, to further assist
in respiration, some aquatic oligochaetes
{Branchiura, Dero) have evolved gills. Parallel developments occur among aquatic
leeches (Hirudinea) which were also derived
from terrestrial groups, are generally
smaller, ventilate their body surfaces in
hypoxia, and in the case of one family (Piscicolidae), have gills (Barnes, 1980; Graham, 1988).
Among pulmonate snails, Lymnaea and
Planorbis occur mostly in water. Jones
(1961) demonstrated that, in addition to a
lung, bothL. stagnalis and P. corneus respire
aquatically through their integument. His
experiments, moreover, showed that these
animals can partition their Vo2 between
skin and lung, depending upon aquatic O 2
levels, to regulate submergence time. Also,
when deeply submerged, these animals
ventilate the lung with water, thus using it
as an aquatic respiratory organ (Pennak,
1978). Finally, Planorbis, but not Lymnaea,
utilizes Hb as a respiratory pigment (Weber,
1980).
Modifications in respiratory system
structure and function for life in water are
seen in two arthropod subphyla. Among
arachnids, some water mites entirely lack
a tracheal system while others possess gasfilled tracheae that are sealed by a cuticle
to prevent water entry but allow O2 to enter
from water (Mitchell, 1972; Pennak, 1978;
Barnes, 1980). Aquatic respiration through
an unmodified cuticle occurs in some
aquatic insects (Mill, 1974). Others rely on
sealed tracheal systems that often extend
beyond the body in the form of elaborated
surface projections termed tracheal gills.
While these are typically gas-filled, the
spaces in some larvae contain hemolymph
(Mill, 1974).
Insects typically lack respiratory pigments; however, in several aquatic forms
Hb appears to play a significant function
in respiration, O2 storage, or both. These
include caddis fly (blood worm) larvae {Chi-
142
JEFFREY B. GRAHAM
ronomus, Trichoptera) and the water bugs
(Hemiptera, Notonectidae) Anisops and
Buenoa (Krogh, 1941; Weber, 1980; Mangum, 1985).
Several reptiles exchange respiratory
gases through the integument (Feder and
Burggren, 1985) and this capacity is well
developed among sea snakes (Hydrophiidae), another group that has reinvaded
water. Integumentary gas exchange is
doubtlessly important to these snakes during feeding and diving. This capacity, in
the presence of the reptilian three chambered heart, has led to a highly optimal
system for diving. Studies with Pelamis platurus (Graham et al., 1987) reveal that cutaneous gas exchange, in concert with intracardiac shunting, prevents decompression
sickness, conserves lung O2 stores while
simultaneously assuring cutaneous O2
uptake, and also conserves lung gas for
midwater buoyancy control.
in striking convergence with aquatic insects,
Planorbis, and several other shallow water
phyla (see below), several genera of branchiopod crustaceans (Artemia, Cyzicus,
Daphnia, Moina, and Triops) have evolved
the use of Hb to increase aquatic respiratory effectiveness, act as an O2 store, or
both (Krogh, 1941; Weber, 1980). These
crustaceans are largely dependent upon
integumental gas exchange. Although
hemocyanin is the respiratory pigment of
the malacostracan crustaceans, other subclasses lack all respiratory pigments, and
Hb has apparently independently evolved
in several branchiopods to enhance respiration in habitats where O2 can be low
(Weber, 1980; Mangum, 1985). Correspondingly, the amount of Hb present in
these animals is influenced by ambient O2
concentration (Weber, 1980).
Water influences on the extremes of the
respiratory adaptation-spectrum
Information presented to this point permits focus on the three basic features of
aquatic respiratory systems that distinguish
them from those functioning in air: 1) The
widespread occurrence of integumental
respiration, 2) The frequent presence of
combined respiratory, feeding, and ion and
solute transfer surfaces, and 3) The
remarkable influence that aquatic hypoxia
has had on respiratory adaptation.
Two final examples, the Antarctic icefish
(Chaenichthyidae) and freshwater branchiopod crustaceans, bracket adaptive
extremes to which aquatic respiratory specializations can be driven, depending upon
circumstances such as the phylogeny and
ecology of a particular group and its occurrence in a particular habitat where the O2
supply is (predictably) stable or unstable.
Icefish are unique among all vertebrates
in lacking Hb containing erythrocytes. The
loss of Hb in this family is attributed to
their long-term occurrence in stable habitat conditions of cold (—2°C), high Gycontent waters. Because tissue O2 delivery is
totally dependent upon the volume dissolved in the plasma, icefish have a large
heart and blood volume and a large cardiac
output. Relative to that of most fishes, icefish gill area is reduced and the secondary
lamellae are thick. The gills do function
for O 2 extraction, however, icefish obtain
up to 40% of their Vo 2 through their skin
(Hemmingsen and Douglas, 1970) and have
increased densities of cutaneous vessels for
this (Jakubowski and Byczkowska-Smyk,
1970).
At the opposite extreme to icefish, and
UNIQUE FEATURES OF AQUATIC
RESPIRATORY SYSTEMS
Widespread dependence on integumental
gas exchange
A recent review (Graham, 1988) established that most of the animal phyla living
in aquatic habitats are dependent upon
integumental respiration at some time in
their life histories. In fact, the integument
is the exclusive method of gas exchange in
22 of the 28 marine phyla and 13 of the
16 freshwater phyla. By contrast, only 4 of
the 9 terrestrial phyla depend exclusively
upon integumental gas exchange.
Included among the aquatic forms
dependent upon integumental gas
exchange are most of the marine and freshwater holoplankton, virtually all marine
meroplankton, and a majority of the aquatic
insect larvae and nymphs. Also included
are a number of animals in the four most
AQUATIC ANIMAL RESPIRATION
advanced invertebrate phyla (Mollusca,
Annelida, Arthropoda, and Echinodermata) that are totally lacking in specialized
respiratory surfaces. Moreover, there are
numerous examples of animals in these
phyla (e.g., all the annelids, gastropods,
bivalves, cirripeds, isopods, amphipods,
insects, and holothurians) in which the
integument serves an accessory respiratory
function (Graham, 1988).
The preponderance of gill-less forms
among the marine groups is attributable to
the origin of most phyla in the sea where,
in the presence of historically stable conditions of sufficient water, O2, energy flow,
and nutrient supply, small and nearly
weightless animals could evolve and remain
successful with simple diffusion-dependent
gas exchanging surfaces (Graham, 1988).
This has also been true—but to a lesser
extent historically speaking—for the
world's freshwater environments into
which many marine zooplanktonic groups
have radiated. The single feature most
favoring integumentary gas exchange is
small size and a relatively large surface area
which can be exploited in aquatic habitats
without risk of desiccation. As discussed
elsewhere in this symposium, these attributes also complement a zooplankter's need
to reduce sinking rate (Alexander, 1990)
and acquire dissolved organic matter
(DOM) via integumentary transport (Manahan, 1990).
The low rate of O2 diffusion in water
poses a significant environmental problem
to aquatic animals unable to generate respiratory currents. This includes developing eggs (Giorgi and Congleton, 1984) and
most holo- and meroplankton; Figure 2
summarizes the problems imposed by size
and growth on diffusion-limitation. For
eggs in large masses, intra-egg movements
by developing embryos have been shown
to favor convective O 2 transport (Burggren, 1985; Hunter and Vogel, 1986).
Strathmann's (1990) presentation in this
symposium and previous studies (Chaffee
and Strathmann, 1984) consider the implications of the limited O 2 diffusion through
water on factors such as the spawning
behavior, clutch size, fecundity, and population biology of aquatic species.
143
Presence of combined surfaces for feeding,
ion and solute transfer, and respiration
A fundamental difference between terrestrial and aquatic life is that in addition
to O2, water contains several other life-sustaining products. To access these while also
respiring, aquatic animals depend on a
greater surface contact with water than do
terrestrial animals with air. Marine animals, with the exception of most marine
vertebrates, are isosmotic with sea water,
and apart from the need to regulate specific ions, have evolved capacities to exchange
respiratory gases, dissolved ions, and in
some cases DOM as required and without
risk of desiccation. Fresh water is also a
haven against desiccation, yet the osmotic
gradient between animal tissue and water
requires increased impermeability and the
ionic gradient is less favorable for DOM
uptake (Manahan, 1990). In strong contrast, terrestrial animals depend upon air
for gas exchange (and to an extent, for heat
balance) but little else, and run a high risk
of desiccation in the process.
It is thus not surprising that animals in
12 marine phyla make use of the same surfaces for respiration and suspension feeding. In these forms feeding occurs largely
by either external or internal water filtration in which particulate and dissolved
materials are selectively removed. Filtered
volumes and Vo 2 in these animals are often
closely correlated, and although some filter feeders have separate exchange and filtering surfaces (e.g., bivalves) others (brachiopods, barnacles) do not (Jorgensen,
1966).
Stable conditions in the marine environment have doubtlessly contributed to the
wholesale dependence of the holo- and
meroplankton on integumentary gas
exchange. The dependence of many of
these same animals on DOM uptake is also
special. However, as discussed by Manahan
(1990) in this symposium, the average concentration of utilizable DOM in the ocean
is well below the affinities of most animal
DOM transporters. The resolution of this
apparent paradox lies in the likely occurrence of DOM in patches, microzones of
chemically rich water that persist for rel-
144
JEFFREY B. GRAHAM
atively short times (Alldredge and Cohen,
1987). Such DOM patches have implications for integumentary respiration because
the same factors that form them (i.e., animal excretion, bacterial decomposition)
also cause localized depletion of O 2 (Alldredge and Cohen, 1987). Thus, positive
DOM taxis by zooplankton may necessarily
involve the respiratory trade-off associated
with frequenting zones of hypoxia.
Respiratory adaptations for hypoxia are the
rule rather than the exception in aquatic
habitats: An unprecedented departure
from the terrestrial paradigm
Figure 1 shows that aquatic environments, both freshwater and marine, experience much greater variation in O 2 supply
than do terrestrial habitats. It is not therefore surprising that aquatic animals provide diverse examples of metabolic, physiological, morphological, and behavioral
adaptations to hypoxia and anoxia. These
numerous adaptations document the powerful selective premium imposed on inhabitants of water by O 2 availability. This is
illustrated by the range of adaptative categories—from facultative anaerobiosis to
facultative air breathing, by the diversity
of animals responding to this pressure—
hypoxia adaptations may be found in most
species in a particular habitat, and by the
frequent occurrence of convergent adaptations—Hb has independently evolved as
a respiratory pigment in shallow water
species of no fewer than 8 invertebrate
phyla (Platyhelminthes, Nematoda, Mollusca, Echiurida, Annelida, Arthropoda,
Phoronida, Echinodermata, and Pogonophora; Weber, 1980). In contrast, terrestrial environments never become so O2
depleted and the range of adaptive
responses to altitudinal hypoxia, for example, is less and not as clear cut (Bouverot,
1985).
Adaptations to hypoxia in shallow water
animals differ in an important way from
those of animals living at depth, specifically
in O 2 minimum layers. In shallow waters
O 2 variability is often extreme (Fig. 1) and
many other environmental and biotic factors also vary. Hypoxia can be chronic or
periodic (i.e., diurnal, in phase with the
tides, or seasonal) and may vary in severity
from period to period. Some animals can
avoid hypoxia by moving, but this is not
an option for less mobile forms and sessile
or interstitial inhabitants. In order to survive, these animals must endure hypoxic
or even anoxic conditions, using a variety
of physiologic and metabolic mechanisms.
Shallow waters have also been the primary
route taken by most phyla in the invasion
of land (Little, 1983). This invasion was,
in some cases, very likely facilitated by the
capacity to breathe air, an adaptation initially selected in response to aquatic
hypoxia.
Relative to other oceanic sites at comparable depths, waters of the world's OMLs
have richer nutrient levels, a greater energy
turnover, and a larger biomass. These
regions are chronically hypoxic, but other
physical and biotic variables do not fluctuate greatly. It is not at all surprising that
species frequenting these water masses can
endure hypoxia. Mechanisms enabling this
include maintenance of Vo2 at a low
ambient Po 2 , as seen in OML crustaceans
(Euphausia mucronata: Teal and Carey,
1967; Antezana-Jerez, 1978; and Gnathophausia ingens: Childress, 1971). Another
adaptive mechanism is an increased respiratory surface area. This is known for G.
inge?is (Childress, 1971) and several
euphausids (Antezana-Jerez, 1978). Among
fishes, populations of Scopelogadus mizolepis
(Ebeling and Weed, 1963) and Cyclothone
acclinidens (Kobayashi, 1973) occurring in
O2-poor water have longer gill filaments
(an index of larger gill area) than do populations occurring in more aerated waters.
Also, some species with distributions that
are restricted to O2-depleted waters have
larger gill surfaces (e.g., Chauliodus pammelas: Gibbs and Hurwitz, 1967; Astronesthes lamellosus: Goodyear and Gibbs,
1969; and Cyclothone acclinidens: DeWitt,
1972) than other closely related species. A
most striking example of gill enlargement
among fishes is found in Scopelarchoides
nicholsi which has gill lamellae that are easily twice as long as its branchial chamber
and thus extend into the water from under
the operculum (Johnson, 1974, fig. 43).
In view of its specializations for respi-
AQUATIC ANIMAL RESPIRATION
145
of marine snow, fecal pellets. Science 235:689ration in aquatic hypoxia, it is not surpris691.
ing that the geographic distribution of Sco1978. Distribution of euphausiids
pelarchoides nicholsi corresponds precisely Antezana-Jerez,T.
in the Chile-Peru current with particular referto OML boundaries in the eastern tropical
ence to the endemic Euphausia mucronata and the
Pacific (Johnson, 1982, figs. 59-61). Simoxygen minima layer. Ph.D. Diss., Scripps Institution of Oceanography, University of Califorilarly limited distributions are seen for most
nia, San Diego.
of the species mentioned above. This indiBarnes, R. D. 1980. Invertebrate zoology. Saunders,
cates that selection for hypoxia adaptation
Philadephia.
in the OML has been driven more by the Batty, R. S. 1984. Development of swimming moveadvantages derived from exploiting the
ments and musculature of larval herring (Clupea
harengus).]. Exp. Biol. 110:217-229.
layer's energy resources than by the need,
as in shallow waters, to simply endure Bouverot, P. 1985. Adaptation to altitude-hypoxia in
vertebrates. Springer-Verlag, Berlin.
periods of hypoxia. Accordingly, selective Burggren,
W. 1985. Gas exchange, metabolism, and
processes favoring exploitation of the
"ventilation" in gelatinous frog egg masses. Physiol. Zool. 58:503-514.
energy rich resources in these areas have
often resulted, in addition to the elabora- Chaffee, C. and R. R. Strathmann. 1984. Constraints
of egg masses. I. Retarded development within
tion of respiratory adaptations, in isolating
thick egg masses. J. Exp. Mar. Biol. Ecol. 84:73mechanisms leading to the formation of
83.
endemic OML-adapted species. If it occurs Childress, J. J. 1971. Respiratory adaptations to the
at all, O2-gradient speciation is exceedingly
oxygen minimum layer in the bathypelagic mysid
Gnathophausia ingens. Biol. Bull. 141:109-121.
rare in shallow water and terrestrial enviCloud, P. 1976. Beginnings of biospheric evolution
ronments.
and their biogeochemical consequences. PaleoFinally, in contrast to the occurrence of
biology 2:351-387.
respiratory adaptations for life in the OML, Dejours, P. 1988. Respiration in water and air. Elsevier, New York.
it is noteworthy that both copepods and
chaetognaths, animals apparently lacking Denny, M. W. 1990. Terrestrial versus aquatic biology: The medium and its message. Amer. Zool.
in any or all respiratory specializations, fre30:111-121.
quently occur in large numbers in OML DeWitt, F. A. 1972. Bathymetric distributions of two
waters. We lack all insight into the mechcommon deep-sea fishes, Cydothone acdinidens and
C. signata, off Southern California. Copeia 1972:
anisms used by these integumentary
88-96.
breathers in adapting to life in the OML.
ACKNOWLEDGMENTS
This paper is dedicated to the memory
of Reuben Lasker. I thank Drs. K. Dickson,
G. Jackson, J. Hunter, M. LaBarbera, D.
Manahan, M. McFall-Ngai, and R. Rosenblatt and Mr. S. Kaupp for help with, discussions about, and insight into various
subjects contained in this essay. I also thank
Mr. D. Ward for technical assistance and
Drs. F. Powell and R. Rosenblatt for
reviewing this paper. This work was partially supported by a Guggenheim Fellowship and by NSF DCB87-18449.
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