AMER. ZOOL., 28:1031-1045 (1988)
Ecological and Evolutionary Aspects of Integumentary Respiration:
Body Size, Diffusion, and the Invertebrata1
JEFFREY B. GRAHAM
Physiological Research Laboratory and Marine Biology Research Division,
Scripps Institution of Oceanography, University of California San Diego,
Lajolla,
California 92093
SYNOPSIS. Most animal phyla lack specialized respiratory surfaces and all phyla contain
groups that, for some part of their life history, depend entirely upon integumental diffusion
of respiratory gases. Animals that are diffusion-limited, yet function aerobically are generally small with large surface areas and there has been convergence for this among all
phyla including the coelomate invertebrates. Acoelomates lack specialized respiratory
structures but have highly modified integuments, functional specializations, and features
ranging from symbioses to air gulping that compensate for diffusion limitation. The
diversity of structures functioning for integumentary respiration is much greater among
invertebrates than vertebrates. Among the higher invertebrates with respiratory surfaces,
accessory integumentary O 2 uptake is usually 20 to 50% of total respiration. The high
diffusion constant of O2 in air minimizes boundary effects on gas transfer and permits
larger body size, although this is limited by dry conditions. Terrestrial annelids and
flatworms, both confined to moist habitats, are larger than aquatic forms which often
have accessory gills. Size differences between terrestrial forms in these two phyla reflect
the presence of a circulation in the annelids. Ontogenetic transitions from skin breathing
to other respiratory structures occur among marine invertebrates and vertebrates. Vertebrates apparently exercise greater integratory control over integumental respiration
through adjustment of ventilation and perfusion; however, it is not known if these processes
occur in some invertebrates.
INTRODUCTION
This essay is about ecological and evolutionary factors related to the presence
and persistence of integumental gas
exchange in the animal kingdom. Owing
to the largely vertebrate orientation of this
symposium's contributions and the recent
review of vertebrate integumental respiration (Feder and Burggren, 1985), I have
chosen to broaden the basis for evaluating
the ecology and evolution of integumentary respiration by reviewing its occurrence and scope of function in invertebrates. This is followed by an integrative
discussion of issues common to both groups.
ON BEING THE RIGHT SIZE:
THE WORLD ACCORDING TO
AUGUST KROGH
sole mechanism for O 2 supply. Above a
critical dimension, diffusion distance
becomes too great and the ratio of tissue
surface area to volume too small to permit
delivery of O 2 in the quantity needed to
sustain cellular oxidative phosphorylation.
August Krogh's (1919) pioneering comparative study of tissue O 2 permeabilities
established the quantitative basis for diffusion limitation and led to formulation of
relationships for O 2 consumption (Vo2), O 2
permeability (the Krogh diffusion constant, K), shape, and size. Derivation of this
relationship is presented elsewhere (Krogh,
1941; Alexander, 1971; Atkinson, 1980).
One form it takes shows the maximum body
size possible for diffusion dependence
Treatises on the comparative physiology
of animal respiration usually begin by
establishing the futility of diffusion as the
r <
Vo 2
(1)
where r is the maximum effective dimension an organism can obtain, Po 2 is O2 partial pressure at its surface, Vo 2 and K are
1
From the Symposium on Cutaneous Exchange of
Cases and Ions presented at the Annual Meeting of as defined above, and 6 is a constant for
body shape (6 for a sphere). Assuming an
the American Society of Zoologists, 27-30 December
1986, at Nashville, Tennessee.
atmospheric Po 2 of 0.21 atm, typical tissue
1031
1032
JEFFREY B. GRAHAM
O 2 permeabilities (8 x 10~4 cm 2 atm-'hr~'), and that all O 2 diffusing into the
tissue (of known mass) is consumed at a Vo2
of about 0.08 ml O 2 -g~' -hr~', eq. 1 shows
that r could not exceed about 1 mm if O2
diffusion is to remain adequate for respiration. Equation 1 also indicates that r
changes in relation to the square root of
Po 2 rather than directly. Thus, for similar
diffusion-limited faunas from air-saturated
(150 Torr) and hypoxic (15 Torr) waters,
we would expect r to differ by less than an
order of magnitude. Diffusive limitation
affects metabolic scope as well as size and
complexity. If as stipulated in eq. 1, all O2
entering the cell is consumed, Vo 2 cannot
increase unless dimensions decrease.
There is no escaping these "Kroghian
limits to growth." Although radical changes
in shape (flatworms) and the dispersal of
metabolically active tissue within a watery
mesoglea (Cnidaria and Ctenophora) could
be viewed as ways of circumventing size
limitation, such solutions are without consequence in metazoan evolution. Rather,
the elaboration of a gas exchanging surface
relative to mass opened the door to
increased body size and expanded ecological diversification. Krogh's predictions
regarding the maximum size of skinbreathing animals appear generally true
and much of the work conducted on these
forms has led to graphical depictions of
maximum body radius versus Vo 2 (Alexander, 1971; Atkinson, 1980). Plots of this
nature permit definition of minimum habitat Po 2 for a species and identification of
the critical dimensions at which an organism either enters the realm of obligatory
anaerobiosis (in the case of some nematodes, Atkinson, 1980), or that of respiratory surface elaboration and specialization.
Krogh's (1941) monograph rather naturally directed the focus of comparative
respiratory physiology away from those
animals (particularly the invertebrates) that
rely upon integumentary gas exchange
despite its problems. Attention was rather
directed to the more advanced metazoan
phyla where the first semblances of a specialized respiratory epithelium, the pres-
ence of a primitive circulation, the occurrence of a respiratory pigment, or possibly
all of these, could be demonstrated. One
consequence of this orientation was a tacit
relegation of lower metazoans to the category of "diffusion dependent and relatively lacking in specializations for gas
exchange." A corollary to this—that the
acquisition of respiratory specialization
rendered integumentary (body surface)
respiration largely passe among the higher
metazoan phyla—proved to be another
consequence.
INTEGUMENTARY GAS EXCHANGE IN
INVERTEBRATES
Conceptual problems
Oxygen will diffuse across any epithelial
layer provided the tissue is permeable and
a gradient exists, and this review will document that the invertebrates display a
broader continuum between non-specialized integumentary and specialized respiratory surfaces than is seen among the vertebrates. How then do we establish, in order
not to distort the concept of cutaneous respiration, the operational limit between
integumentary exchange per se and that
occurring across a surface that, although
qualitatively not different from integument, can be defined as a specialized respiratory structure? Two useful indices for
such differentiation are relative surface
area and the thickness of the layer in question. The respiratory surface of many crustaceans is, for example, the thin, cuticlecovered part of a locomotory appendage
that is incidentally ventilated by swimming
or feeding currents. The combined surface
area of these appendages greatly exceeds
that of the carapace; however, in certain
groups, like the more advanced tanaidaceans (which are similar to isopods), hemolymph sinuses within the carapace assume
the respiratory function (Schram, 1986).
Relative cuticle thickness over these areas
is unknown, but presumably reduced.
Another conceptual problem revolves
around the evolutionary disappearance of
specialized respiratory structures, which
has occurred in several phyla. Among the
EVOLUTION AND ECOLOGY OF INTEGUMENTARY RESPIRATION
mollusks, for example, are groups with gills,
groups that have lost gills and respire
through the mantle cavity, and still other
groups in which both gills and mantle cavity have disappeared. Among invertebrates
there is a greater diversity of "moderate"
surface-area increasing morphologies (e.g.,
crenulated body surfaces, a gill-less mantle,
tube feet, papulae, and strategically placed
"thin surfaces" on the carapace and legs
of arthropods) which, because their surface area in relation to body mass is usually
lower than that of a respiratory surface,
can be considered in the context of integumentary breathing. Fuzzy conceptual
boundaries even occur at the farthest
extreme. Does a cuticle that is invaginated
at regular intervals to form spiracles (Uniramian arthropods) or, even more radically, a cuticle that is regularly invaginated
as well as uniformly elaborated in order to
permit an aquatic arthropod to dive with
a layer of air (plastron) over its spiracles,
both constitute forms of integumentary
respiration?
Other differences appear if we attempt
to apply models of diffusive gas transfer
developed for vertebrates (Feder and
Burggren, 1985) to invertebrate integumental respiration. We lack fundamental
morphometric data and constants for
hemolymph flow and O2 saturation (if
indeed hemolymph and respiratory pigments are even present, Table 1). Because
we do have Vo 2 and size data, approximations can be made in some but not all
cases. In water the small size and slow
swimming speed or incident flow around
some creatures may result in low Reynolds
numbers. This means that conditions in the
water-animal boundary layer are dominated by viscous flow, which is to say that
the layer of water next to the animal tends
to adhere to its surface (Vogel, 1981). This
boundary layer will persist and small animals may not even be able to thin or disrupt
it even during movement. The strata of
water encapsulating and tending to flow
along with a small (20-200 jam) planktonic
animal may approach its diameter. Thus,
an additional and more or less permanent
gas diffusion distance becomes an inherent
1033
part of cutaneous respiration (Feder and
Pinder, 1988).
Ecological and evolutionary considerations
The broad occurrence of integumental
respiration among the animal phyla and its
relationship to other respiratory specializations are documented in Table 1. In
many phyla integumental respiration is
deduced from strong negative evidence,
which is the absence of other respiratory
structures. Such structures never evolved
in some phyla; in others they seem to have
become lost in diminutive groups. An
important principle insofar as body size and
cutaneous respiration are concerned is
illustrated by the latter observation: Smallness, even among more advanced invertebrate phyla, replaces the need for an
elaborate respiratory surface.
Two important questions about vertebrate integumentary respiration are how
is it integrated with other gas exchange
surfaces and how much integumentally
derived O 2 is actually distributed to other
tissues (Feder and Burggren, 1985)? We
presently lack quantitative information
about both of these for invertebrate integumentary respiration. However, Table 1
makes it very clear that for the vast preponderance of invertebrate phyla these
questions are simply not relevant.
Table 1 shows that the greatest number
of gill-less animals are exclusively marine.
Among these are highly specialized, ancient
planktonic (Chaetognatha) and filter feeding (Brachiopoda) forms. This diversification is attributable to the origin of most
phyla in the ocean and the subsequent invasion of freshwater and land by relatively
few of them. The evolution of natural
histories within the framework of stable
marine conditions has favored retention of
simple diffusive gas exchangers. Even while
lacking in respiratory structure, some phyla
seize the ventilatory advantages afforded
by induced feeding currents. The proliferation of holoplanktonic phyla and the
nutritional utilization of dissolved organic
matter (DOM, which is 2-5 orders of magnitude more dilute than dissolved O 2 , and
underlines the presence of, among other
TABLE 1. Environment and respiratory specializations of the animal phyla.'
Environment
Phylun
FW
Specialized
respiratory
structure
present
Integumental
respiration
Circulatory
system
present
Open or closed
circulation
Common feed.,
resp. and locomotory surface
Pigment present
(Hb#;Hcy+;
He o; Clc A)h
Protozoa
Porifera
Cnidaria
Ctenophora
Platyhelminthes
Mesozoa
Rhynchocoela (Nemertina)
Gnathostomulida
Rotifera
Gastrotricha
Kinorhyncha
•o
Nematoda
Nematomorpha
Acanthocephala
o
Priapulida
0
Sipunculida
c/o
Mollusca
c
Echiura
c
• OA
Annelida
•
Pogonophora
c
Tardigrada
Onychophora
Arthropoda
•+
Pentastomida
Phoronida
Bryozoa
F.ntoprocta
Brachiopoda
o
Chaetognatha
Echinodermata
Hemichordata
c
Chorda ta
c/o
• Habitat abbreviations are marine (M), freshwater (FW), terrestrial (T), and parasitic (P). Parentheses around the circles indicate only few members of
phylum occur in a habitat.
b
Respiratory pigment abbreviations are hemoglobin (Hb), hemocyanin (Hey), hemerythrin (He), and Chlorocruorin (Clc).
1035
EVOLUTION AND ECOLOGY OF INTEGUMENTARY RESPIRATION
TABLE 2. Comparative assessment ofthefactors affecting the boundary diffusion rates ofO2 and C02 during integumental
gas exchange in sea water (35%o), freshwater, and humid air at 20°C*
Water
Sail
Fresh
5.3
237
155
6.6
295
155
Variable
Access to O2
Co2 (ml/liter)
(/imol/liter)
Po2 (Torr)
/3o2 (jimol/liter/Torr)
Do2 (cmVsec)
Ko2 (nmol/cm/sec/Torr)
II. Removal of CO2
Cco2 (ml/liter)
(jimol/liter)
Pco2 (Torr)
/3co2 (/imol/liter/Torr)
Dco2 (cm2/sec)
Kco2 (nmol/cm/sec/Torr)
III. Water availability
(ml/g)
IV. Heat capacity
(cal/min/°C)
Air
I.
209.5
9,357
155
1.53
0.23 x 10-1
0.35 x 10 <
1.90
0.25 x 10-4
0.48 x 10-"
60.4
0.198
11.96
0.29
13.0
0.34
15.3
0.35
15.7
0.3
0.3
0.3
43.3
0.16 x 10-*
0.69 x 10"'
50.9
0.18 x 10-"
0.92 x 10"'
52.4
0.155
8.12
0.965
1.00
1.73 x 10-5
0.93
1.00
0.0003
* Data are either taken directly or calculated from Dejours (1981).
total O2 content of water (Table 2). While
Po 2 at saturation is not affected by solutes,
O2 solubility or capacitance (/3o2) is reduced
and, from Henry's law, it is the product of
Po 2 and j8 that determines O 2 concentration (Dejours, 1981). In theory a reduced
/?o2 should affect integumental respiration
by reducing the rate (K) that O2 diffuses
into the water-skin boundary layer, but has
not been studied. Because freshwater
invertebrates are hyperosmotic to water
(marine invertebrates are isosmotic) they
must have a stronger diffusion barrier for
water and this is thought to manifest itself
in the absence of DOM uptake in fresh and
brackish water forms (Stephens, 1968) and
should also affect cutaneous gas flux.
The significance to respiration of the
physical differences between water and air
and the properties (diffusion and capacitance) that affect the movement of respiratory gases in air and water are reviewed
Environmental factors
elsewhere (Dejours, 1981; Little, 1983;
How might properties of the ambient Feder and Burggren, 1985). Gases diffuse
environment other than its respiratory gas more rapidly in air than in water because
content influence cutaneous gas flux? How the former is less dense and viscous. Howdo intrinsic properties of a respiratory ever, in accordance with Graham's law, the
medium affect gas exchange potential? Dis- diffusion coefficient (D) of O 2 is greater
solved solutes (e.g., in sea water) reduce the than CO2 in both media (Table 2). Capacfeatures, large absorptive surfaces) by many
larvae and adult forms are both characteristics of the marine but not freshwater
fauna. Marine and freshwater environments impose similar physical constraints
on integumental respiration (Table 2), yet
the former have persisted and changed only
gradually since the Cambrian. In contrast
to freshwater, most marine habitats are
presently typified by more stable temperatures and water levels (on all time scales)
and the presence of well-mixed (aerated)
water. Cloud (1983) speculated that the
explosive transition from the soft-bodied,
marine Ediacara fauna of the Precambrian
to the diversified and hard-bodied forms
of the Cambrian is attributable to the rise
of O 2 in the atmosphere. This has numerous implications insofar as the evolution of
respiratory structure, hard body parts, and
large size are concerned.
1036
JEFFREY B. GRAHAM
itance (/?) differences also underlie the different diffusive properties of O 2 and CO2
in air and water. Because its units are concentration/ Torr, |8 indicates the quantity
of gas that will diffuse into a layer of respiratory medium bordering the skin from
which O 2 is absorbed into the body. Because
air has a large O 2 content and a high partial
pressure, /3o2 is large. By contrast the /3o2
of water is small and this means that both
the thickness and hypoxia gradient of an
unstirred layer of water surrounding an
integumentally-respiring animal would
grow much more quickly compared to the
corresponding layer around a similarlyrespiring animal in air. Even with ventilation or flow-induced mixing at the body
surface, larger boundary layers tend to
form in water.
Body size, K, worms, and rain
Differences in K underlie another principle concerning body size and integumental respiration: Provided an organism has
the internal capacities to absorb and transport the volume of respiratory gases
required by its mass and can otherwise live
successfully, its potential size can be larger
in air than in water. The relative sizes of
aquatic and terrestrial (cryptobiotic) flatworms, earthworms, and leeches confirms
this; the terrestrial forms tend to be larger
than their aquatic counterparts. Moreover,
the smaller water-dwelling leeches and
earthworms have gills. Because annelids
possess an internal circulation, a larger size
differential should be found among them
as opposed to flatworms. The earthworm's
requirement to surface after a rainfall,
which has been attributed to a number of
causes (Laverack, 1963), becomes completely understandable in terms of the profoundly different K's of a humid air-filled
burrow and one that suddenly becomes
flooded with water, even if the Po 2 of the
water is high.
On the other hand a large respiratory
surface exposed to air can become a liability. Other physical properties of air, its
low heat capacity and an extremely small
water content (Table 2), intersect with the
more favorable K to limit maximum size
and habitat for integumental breathers.
The water content of even moist air is
extremely low (Table 2) and cool air holds
less water than warm air. Thus, while air
remains favorable for O2 diffusion, fluctuations in air temperature could adversely
affect water flux. Water molecules diffuse
faster than O 2 or CO2 and the larger integumental breathers are limited to warm
humid environments. Water-dwelling integumental breathers, while not subject to
desiccation, may use added ventilation and
increased surface area to fight the constant
battle of a boundary-layer related O 2 shortage.
RESPIRATORY SPECIALIZATION
AMONG ACOELOMATES
Although lacking respiratory structures,
acoelomates display a range of specializations that aid in the acquisition of O 2 and
seem to mitigate the possible diffusive limits imposed by size or environmental (usually aquatic) hypoxia (Table 3). A few of
the features listed in this table would apply
equally to protozoans but, except for the
foraminifera that attain extremely large
sizes (25 cm), I have not included these
groups. Space does not permit more than
an annotated discussion of Table 3. Parasitic flatworms, nematodes, and acanthocephalans all have larger relative surface
areas than do turbellarians and rotifers,
which are free living. This doubtlessly
relates to factors in addition to respiration
such as nutrient uptake and the potential
for desiccation. Air gulping has been documented in several genera of nematodes
and the Hb (hemoglobin)-O2 dissociation
curves of gut-dwelling species are left
shifted {i.e., higher O2 affinity) compared
to both lung-dwelling and free living species
(Atkinson, 1980). No nematode approaches
Krogh's critical dimension, yet many have
ridged cuticles. Also, nematodes have an
"inside out" design which places metabolically active tissues near the body edge.
Atkinson (1980) calculated that this design
reduced the O 2 diffusion requirement by
20%. This body plan also reduces the Po 2
term in eq. 1 and thus would also lessen
the effect of habitat O2 variation, while
permitting some metabolic scope. The
pseudocoel, which evolved independently
EVOLUTION AND ECOLOGY OF INTEGUMENTARY RESPIRATION
1037
TABLE 3. Adaptive mechanisms present in acoelomate metazoans that likely aid in compensation for diffusion limitations
imposed by body size and environmental O?
Adaptive measure
1. Add photosynthetic symbionts (organelles)
2. Reduce biomass density with a mesogleal matrix
3. Alter body plan
a. Hollow body structure
b. Locate metabolically active tissues peripherally
in stronger O2 diffusion gradient
c. Increase surface area
i. Length and shape
ii. Frenulated cuticle
4. Add respiratory pigment to:
a. Lateral body wall
b. Within pseudocoel
c. Around pharynx
5.
6.
7.
8.
Groups of occurrence
Foraminifera, Cnidaria, Platyhelminthes
Cnidaria, Ctenophora
Cnidaria, Ctenophora
Nematoda, Nemertinea, Platyhelminthes
Nematoda
Acanthocephala, Cestoda, Trematoda, Nematoda
Nematoda, diffusion facilitation
Nematoda, O2 storage
Nematoda, O2 storage following pharyngeal ventilation
d. Alter P50 in accordance with habitat conditions Nematoda
Ventilate body surface
a. Undulation of body
Nematoda, Cnidaria
b. Forced or environmentally caused convection Porifera, Cnidaria, Rotifera, larvae
c. Facultative air gulping
Nematoda
Increase internal circulation
a. Low viscosity pseudocoel mixed by undulation Nematoda, Platyhelminthes
Nemertinea
b. Primitive circulation present
Behavioral orientation to O2 gradient
Nematoda, Turbellaria
Nematoda, Cestoda, Trematoda
Facultative anaerobiosis
in many of these phyla (Barnes, 1980), contributes fundamentally to exteriorization
by displacing body tissues. It also functions"
as a primitive circulatory system, with perfusion occurring by body undulation, and
in some groups contains respiratory pigment. Nemerteans, the only one of these
phyla with a true circulation, move hemolymph by undulation. Hemoglobin in the
body wall (or around the pharynx of some
forms that "inhale" water and air) would
seem to facilitate O 2 diffusion as well as
increase storage (Atkinson, 1980). Some
intestinal ascarids are thought to migrate
regularly between regions of higher
(peripheral) and lower (interior) O 2 concentration for purposes of respiration (i.e.,
replenishing of Hb-O2 stores).
INTEGUMENTAL RESPIRATION AMONG THE
HIGHER INVERTEBRATE PHYLA
Table 4 contains summary information
about integumental respiration in four
major coelomate phyla. For this compilation I have relied again on negative evi-
dence (i.e., no reports of respiratory structures), on experiments in which respiratory
structures were occluded, removed, or otherwise inactivated—with the ensuing effect
on total Vo 2 determined, and on literature
inferences that were based on behavior,
natural history, and anatomy (Pennak,
1978; Barnes, 1980). The subsequent discussion annotates Table 4.
Mollusks
Among the gastropods are several prosobranch families of small intertidal or
amphibious species in which gills and mantle are absent. Other terrestrial families
also lack gills but retain respiratory mantles, and are also suspected of carrying on
cutaneous respiration across other airexposed surfaces. Brown (1984) documented pedal O2 uptake in the whelk
(Bullia digitalis) and concluded this was
especially important during activity when
the foot was more exposed to water above
the substrate and the animal's posture
tended to restrict hemolymph flow between
TABLE 4.
Phylum
hylum
Subphylun
Mollusca
Absence of respiratory structures and occurrence of integumental respiration among four advanced metazoan phyla.
Class
Subclass
Gastropoda
Prosobranchia
Opisthobranchia
Pulmonata
Bivalvia
Anomalodesmata
Scaphopoda
Cephalopoda
Annelida
Order
Family
Archaeogastropoda
Lepetidae
Helicinidae
Mesogastropoda
Omalogyridae
Rissollidae
Pomatasidae
Cyclophoridae
Pterotracheidae
Neogastropoda
Buccinidae
Cephalaspidea
Pyramidellacea
Acochlidiacea
Thecosomata
t
Gymnosomata
Notaspidea
Sacoglossa
Nudibranchia
Systellommatophora
Onchidiidae
Veronicellidae
Basommatophora
Lymnaeidae
Planorbidae
Possible
Respiratory
occurrence of
structure
integumentary
absent
Empirical
respiration
data for
among all
(• all.
o some of integumentary members of
group)
respiration
the group
Notes and comments
terrestrial, no gill
terrestrial, no gill
terrestrial, no gill
one genus Firoloida, lacks gill
large flat pedal disk
pteropods
gills present only in Oxytwe
Dendronotaceans and Eolidaceans lack gills
(superorder)
terrestrial, no lung
(superorder)
siphon predator, formerly subclass Septibranchia
Vampyromorpha
Octopoda
Polychaeta
Oligochaeta
Hirudinea
Piscicolidae
only leech family with gills, aquatic
TABLE 4. (Continued.)
Phylum
Subphylum
Arthropoda
Chelicerata
Class
Subclass
Pycnogonida
Arachnida
Order
Family
Acarina
Trobiculidae
(Hydracarina)
Possible
Respiratory
occurrence of
integumentary
structure
Empirical
respiration
absent
among
data for
g all
((• all,,
o some of integumentary members of
group)
respiration
the group
Notes and comments
o
o
sealed tracheae
(water mites occurring in several suborders)
Crustacea
Cephalocarida
Ostracoda
Copepoda
Branchiura
Branchiopoda
Cirripedia
Malacostraca
Phyllocarida
Eumalacostraca
Uniramia
Symphyla
Pauropoda
Insecta
Pterygota
free living forms lack gills, most lack hearts
parasitic
Thoracica
Acrothoracica
Leptostraca
Thermosbaenacea
Tanaidacea
Mysidacea
Isopoda
Amphipoda
Ephemeroptera
Odonata
Plecoptera
Coleoptera
Trichoptera
Diptera
Echinodermata
Holothuroidea
Apodida
Elasipodida
Crinoidae
o
o
•
o
o
o
o
o
o
lost in some parasites, reduced in interstitial forms
structures present but reduced in some groups
tracheal system limited to anterior part of body
tracheae not present in some, no heart
larvae
larvae
larvae
larvae, adults
larvae
1040
JEFFREY B. GRAHAM
mantle (gill location) and foot. Brown
(1984) also determined that the rate of O 2
diffusion through the foot ofBullia at 15°C
(12.2 /tg/hr) was nearly the same as values
determined for connective tissue by Krogh
(1919). Many small opisthobranchs lack
both gills and a mantle cavity as do nudibranchs. Nudibranchs, however, do have
dorsal cerrata and several early reports (see
Hyman, 1967) suggested the rhythmic
movement of these structures was for the
purpose of integumental ventilation. Sealing the pneumostome of a pulmonate snail
with paraffin still resulted in a 20-50%
residual Vo 2 . The aquatic pulmonates
(Planorbis corneus and Lymnaea
stagnalis)
consume O 2 through their integument
(Little, 1983). For these species Jones
(1961) demonstrated that aquatic O 2 tension, through its direct affect on the integumental contribution to total Vo 2 , in turn
affected "lung" O 2 depletion rate and
hence snail dive time. These snails may
occur at depths beyond the range for routine surface migration (commonly 15 m,
but Lymnaea has been collected at 250 m
in Lake Geneva) and may respire with a
water-filled "lung" as well as integumentally (Pennak, 1978). Among the slugs are
tropical, terrestrial forms (Veronicellidae)
that lack a "lung" and respire cutaneously.
The intertidal dwelling Onchidiidae (On-
imum size (7 cm diameter) by the septum's
ability to provide the force needed to accelerate larger volumes of water. Exclusive
reliance upon integumentary respiration
may also limit size. Among other mollusks,
the class Scaphopoda lack gills but do
actively ventilate a reduced mantle cavity.
Cephalopods have high surface area gills
that are perfused by a closed circulation.
However the number of gills is reduced in
certain forms and Barnes (1980, p. 446)
observed, "In many cephalopods that swim
with webbed arms, the gills are vestigial
and gas exchange takes place through the
general body surface."
Annelida
Integumental gas exchange occurs in
varying amounts in these worms (Weber,
1978). Parapodial gills are present in most
but lacking in planktonic forms and the
narrow, elongate groups that have thin
body walls. Fanworms (Sabellidae, Serpulidae) respire with arborescent branchial
crowns that also function in feeding. These
worms also respire through their general
body surface and the design of both the
crown and burrow determine the extent to
which this occurs. The burrow of Sabella
pavovina, for example, is made of sand and
has a rear opening. The worm's undulations create a ventilatory current. Myxicola
chidium [Onchidella] fioridanum) have small infundibulum resides in a gelatinous burrow
gas-exchanging sacs but respire cuta- that lacks a rear opening and thus cannot
neously while submerged (Arey, 1937; Lit- ventilate its body as fully as Sabella. Myxitle, 1983).
cola is more dependent upon its branchial
crown
for respiration and is less tolerant
Bivalves generate a filter-feeding current through their bodies which also serves of experimental removal of this structure
gill ventilation and respiration. Experi- than is Sabella. In fact, removing the crown
mental blockade of the gills, however, only of Sabella does not affect its O2 consumpreduced total Vo 2 by less than 15%, dem- tion rate. However, if its posterior burrow
onstrating the importance of the integu- opening is then sealed it must emigrate to
mentary surface in respiration (Booth and avoid suffocation (Wells, 1952).
Mangum, 1978). One subclass of bivalves
Burrowing polychaetes rely upon either
(Anomalodesmata) completely lacks gills body undulations or cilia to drive ventilaand must therefore respire exclusively tory currents. Still, gill ligation only reduces
through its integument. The gills of these O2 consumption by about 50%, implying
forms have degenerated into a muscular integumental respiration (Weber, 1978).
septum that moves up and down to force The sea mouse, Aphrodita aculeata, ventiwater through the siphon. In feeding, these lates its burrow by alternately raising and
bivalves use their siphon current to aspi- then lowering the layers of scales (elytra)
rate small prey. Reid and Reid (1974) sug- on its back. Gas exchange takes place in a
gest these animals may be limited in max- narrow channel between the elytra and the
EVOLUTION AND ECOLOGY OF INTEGUMENTARY RESPIRATION
dorsal body wall. Progressive lowering of
elytra drives water down this channel.
Oligochaetes respire through a generalized body integument. Among some small
aquatic species (Tubificidae, Naididae), gills
may be present in the posterior segments.
Many species have integumental folds that
increase body surface area by a factor of
three (Raster and Wolfe, 1982). When the
burrows of the tropical swamp dweller Alma
emini are flooded, it backs to the surface
and inverts its tail around a small air volume to create an integumental lung (Beadle, 1957; Mangum et ai, 1975). Tubifex
rivulorum and to a lesser extent Limnodrilus
hoffmeisteri ventilate their body surfaces by
extending their tails from their burrows
and waving them. Tubifex makes a corkscrew motion and both the length (surface
area) of its body that is extended and the
intensity of its motion correlate with the
extent of hypoxia (Alsterberg, 1922). Soil
dwelling oligochaetes usually have dense
epidermal capillary networks that lie in
close proximity (2 nm) to the body surface
(Laverack, 1963). This proximity increases
O 2 intake and permits expansion of body
size. Alexander (1971) calculated that the
diameter (1.3 cm) of the giant earthworm
Rhinodrilus fafner is close to the critical
maximum possible given its mass (1 kg),
Vo 2 (0.06 ml-g~' -hr~') and skin diffusion
distance (~3 /tm), Lacking ventilation,
earthworms occur in porous moist soil and
depend upon stable rates of O2 diffusion
to their body surface. Factors that dramatically reduce subterranean O2 delivery
such as flooding (or according to Mann
[1962], even drops in barometric pressure), force them to surface to seek air
(Laverack, 1963).
Arthropods
Small arthropods often depend exclusively on integumental respiration. Among
chelicerates, all pycnogonids lack respiratory structures. Some spiders and mites
have reduced spiracles. Trobiculids and
many water mites lack a tracheal system
entirely. Other hydracarina have gas-filled
trachea that are sealed to prevent water
entry. Respiration in both these groups
depends on an integumental gas transfer
1041
phase. Even species with relatively thick
body walls have thin porous areas (Mitchell, 1972; Pennak, 1978). Alternatively
some aquatic mites dive with a plastron
(Barnes, 1980).
Gilled appendages occur on most crustaceans. However, several classes of this
subphylum, cephalocarids, ostracods, freeswimming copepods, and branchiurans lack
gills. Another class, the branchiopods,
named specifically for its respiratory
appendages, is thought to respire integumentally to some extent (Barnes, 1980).
This may be especially the case for animals
in the subclass Conchostraca which are
nearly completely enclosed by their carapace. Daphnia, another genus of branchiopod with a large, enclosing carapace,
increases its Hb concentration when
exposed to hypoxic water (Barnes, 1980).
This increase both facilitates integumental
O2 diffusion and increases storage of this
gas. Barnacles have respiratory structures
and can probably also respire through
extended cirri, which in some cases have
filamentous appendages for this purpose
(Burnett, 1977). Accessory respiratory
structures are absent or less developed in
small barnacles, and stalked barnacles
exchange gases through their stalks during
low tide when their shells are sealed (Petersen et al., 1974). Among the Malacostraca,
mysids, tanaids, thermosbenaceans, and
leptostracans have reduced gills and some
lack them entirely. Hemolymph sinuses
within the carapace of these forms facilitate integumental gas transfer either from
the outside or within the branchial chamber (Schram, 1986).
In no group can the natural history of
cutaneous respiration be better illustrated
than among the isopods. These animals
respire with specialized, high surface area
abdominal appendages (pleopods), which
are in turn modified in accordance with the
vastly different natural histories of the
diverse members of this order and also in
a manner indicative of differential degrees
of dependence upon cutaneous respiration. Interstitial (substrate dwelling) forms
(Microcerberidae), for example, become
quite small and they have fewer and relatively smaller pleopods. The deep sea epi-
1042
JEFFREY B. GRAHAM
benthic forms (Bathynomidae) which
become quite large (carapace length and
width = 42 x 15 cm) have auxiliary respiratory layers or leaflets between each
large pleopod. Parasitic isopods (Bopyridae, Cryptoniscidae, Dajidae) assume a
largely globular shape and have reduced
pleopods or lack them entirely and must
therefore respire across their body surface.
Cutaneous gas exchange is also present in
the terrestrial and intertidal isopods (Oniscoidea) which, to reduce desiccation, have
invaginated gas exchange surfaces (pseudotrachae) on some of their pleopods.
Experimental blockage of pseudotracheae
(Edney and Spencer, 1955) showed that
about 50% of total O 2 consumption occurred through the ventral abdominal
body wall of Ligia oceanica (littoral) and
Oniscus asellus (terrestrial). Porcellio scaber
and Armadillidium vulgare, from dryer hab-
forms diffusion is facilitated by tracheal or
spiracular gills—gas-filled
filaments
extending beyond the body edge. Other
immature aquatic insects have hemolymph-filled gills (Mill, 1972, 1974). Of relevance here, however, is that some larvae
with closed trachea also lack these surface
elaborations. Included here are the dipterans Chironomus riparius (which respires
uniformly across most body surfaces and
has a highly distributed subepidermal tracheal plexus) and Atrichopogon trifasciatus
(in which the subepidermal tracheal plexus
is focused below a zone on the dorsal body
surface where the cuticle is thin). Fraenkel
and Herford (1938) demonstrated cutaneous respiration in blowfly (Calliphora
erythrocephala) and other insect larvae. The
larvae of some caddisflies (Trichoptera) also
lack tracheal gills and, in species with gills,
removal experiments showed no adverse
effect on Vo 2 (Pennak, 1978). Both Dipteran and Trichopteran larvae may dwell
in egg cases which are ventilated by body
undulations. More broadly, Pennak (1978)
has opined that integumental respiration
occurs in the Coleptera, Plecoptera, and
Odanata.
itats, have better developed pseudotracheae on all but two of their pleopods and
correspondingly experienced a greater
reduction (70%) in O 2 consumption following pleopodal blockage, indicating a
smaller, but still significant dependence
upon cutaneous exchange (Edney and
Spencer, 1955).
Amphipods (beach hoppers) are also eco- Echinoderms
logically and morphologically diverse, and
For purposes of this essay the gas
some are adapted to terrestrial life. Gill exchange across echinoderm tube feet and
blockage experiments with hoppers in the papulae will be considered integumentary
family Talitridae show they can also re- respiration. Reciprocal oral and aboral surspire integumentally. Certain shore crabs face blockade experiments with the starfish
(family Ocypodidae) respire aerially (Asterias) demonstrated respiration across
through specialized surfaces on their meral both surfaces and also showed that this anileg segments (Maitland, 1986).
mal can facultatively increase exchange
Integumental respiration among uni- across either surface when the other is
ramians may not be as rare as would be blocked (Cole and Burggren, 1981).
first thought. Symphylans have spiracles on Experimental blockage of the respiratory
their heads but tracheae penetrate only the tree of holothurians resulted in a 60%
anterior three segments, suggesting the reduction in Vo2, suggesting the remainremaining 10 segments may depend on der came via the skin (Newell, 1979). Certain holothurian orders, however, comintegumental transport.
pletely
lack respiratory trees and the class
Two insect orders—Protura and Collembola—lack tracheae (Mill, 1974), and Crinoidea lacks a respiratory system
both groups are predictably small and entirely.
inhabit humid areas. The aquatic larvae
and pupae of some insects, like water mites,
CONCLUSIONS
may have a sealed tracheal system (i.e., the
Invertebrate
integumentary
respiration
trachea or spiracle is sealed and respiration
depends upon gas diffusion from the integThis review establishes the following: 1)
umental surface [Mill, 1974]). In these Integumental respiration remains the prin-
EVOLUTION AND ECOLOGY OF INTEGUMENTARY RESPIRATION
cipal mode of gas exchange in most lower
invertebrate phyla. Many of these animals
possess behavioral, physiological, structural, and biochemical capacities to surmount gas exchange limits imposed by different microhabitats and can at least
partially compensate for diffusion limitation. 2) The integument functions as the
site for gas exchange of nearly all invertebrates during egg and larval development. 3) Integumental respiration augments the total gas exchange in many
invertebrates that possess respiratory
structures. 4) The integument has reevolved a predominant if not an exclusive
gas exchange function in certain groups of
the advanced phyla that have secondarily
lost or reduced their specialized respiratory structures.
Comparative integumentary gas exchange in
vertebrates and invertebrates
While many comparative physiologists
have regarded cutaneous gas exchange as
a vertebrate specialization, this essay clearly
documents the common occurrence of this
gas exchange mechanism in invertebrates.
In what ways should a broader comparative
perspective alter our thinking and approaches to this area of research? A principle that emerges is that integumental respiration is more often the rule than the
exception in the animal kingdom. Many
animals and members of all phyla respire
cutaneously and completely lack specialized respiratory surfaces. Moreover, and as
could be expected on the basis of their
greater diversity, the "integumentary
structures" used by invertebrates for gas
exchange are more diverse, cover a broader
continuum, and exemplify multiple use to
a greater extent than is seen among vertebrates. If we expand our operational definition of integumentary respiratory structure to include the spiracles of insects, then
the case could be made that all animals,
except for a few odd groups that became
exceptionally large, use their body surfaces
in one form or another for respiration. In
any case integumental respiration is a primordial function practiced by nearly all
animals at some time during their ontogeny if not during their adult life. By all
criteria—abundance, diversity, distribu-
1043
tion, antiquity—animals that respire
exclusively via their skin are highly successful.
Another set of principles revolve around
size effects and the evolutionary and ecological factors that have determined body
size during the course of animal evolution.
Many of the exclusively integumentary
breathers remain smaller than Krogh's
critical dimension and thus avoid diffusion
limitation, enjoy a buffer against variable
Po 2 and gain the potential for some metabolic scope. Vertebrates and larger invertebrates of course meet the hypoxia and
scope challenges in an entirely different
fashion and integumentary respiratory
function, which does not occur in all
groups, is often relegated to a secondary
status (Feder and Burggren, 1985). Smallness and the absence of respiratory structure are convergent features in both primitive and advanced invertebrate phyla and
moreover, are particularly strongly linked
in aquatic habitats where low O2 diffusivity
and capacitance limit K and require maximal surface area. To a large extent both
iso- and hyposmiscity in water insulate small
aquatic animals from dehydration and permit the large surface areas needed for gas
exchange.
Concerning the question of environmental adaptation, the invertebrate fauna
again expands our horizons by allowing us
to track integumentary breathing within
phyla where different but closely related
groups (classes, orders) occur in freshwater
and on land. We can, moreover, compare
terrestrial and aquatic integumental respiration in phyla with (annelids) and without (flatworms) circulatory systems. The
diverse habitats of certain invertebrates has
also precipitated dramatic changes in body
size, morphology, and integumentary respiration within certain groups {e.g., terrestrial and parasitic isopods). There has also
been convergence to small size and greater
dependence on integumentary respiration
among the diverse phyla (arthropods, mollusks, worms) comprising the interstitial
fauna.
Nearly all of these phenomena are
unprecedented in vertebrates. Yet marked
parallels do exist between vertebrates and
invertebrates. The early life history of many
1044
JEFFREY B. GRAHAM
marine invertebrates and fishes are much
the same in that both have larval stages
that depend upon cutaneous gas exchange.
Many marine fishes hatch without functional mouths or gills. The small size of
these forms permits sufficient cutaneous
respiration and ion regulation to sustain
development. Some of these small fish
develop thin, encircling layers of myoglobin-rich red muscle which, while powering swimming (Batty, 1984) may also
facilitate transcutaneous O 2 uptake and aid
total respiration. As is likely the case for
cephalopods (Barnes, 1980), most adult
fish do retain some level of cutaneous respiration (Feder and Burggren, 1985). Yet,
it is among the lower vertebrates that,
because of their capacities to modulate
blood flow, the highest expression of integrated function between cutaneous and
other respiratory functions manifests itself.
Included among these is the fine control
of perfusion in amphibian skin (Malvin,
1988), the use of cutaneous exchange by
sea snakes to avoid decompression sickness
and conserve lung gases for buoyancy (Graham et al., 1987a), and the capacity of synbranchid fishes to respire proficiently and
take up ions through their skin because the
gills of these fish are specialized for and
often occupied by air breathing and aquatic
ventilation is energetically costly (Stiffler et
al., 1986; Graham et al, 19876; Stiffler,
1988). On the other hand this may only
reflect the greater scrutiny given vertebrates. There is no a priori reason why
cephalopods, for example, should not have
a similar range of skin and gill perfusion
capabilities.
ACKNOWLEDGMENTS
I thank Drs. Robert Hessler, William
Newman, Fred White, and George Wilson,
and Mr. James Easton for discussions on
the diverse topics covered in this review. I
thank Mr. William Lowell and Ms. Pat
Fisher for technical assistance and Mr. Lai
Chin and Drs. W. Burggren and M. Feder
for critical comments on this paper. This
work was partly supported by NSF DCB
8416852.
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