AMER. ZOOL., 39:253-260 (1999)
Two Designs of Marine Egg Masses and their Divergent 1Consequences for
Oxygen Supply and Desiccation in Air
RICHARD R. STRATHMANN2 AND HELEN C. HESS
Friday Harbor Laboratories, 620 University Road, Friday Harbor, Washington 98250
College of the Atlantic, 105 Eden Street, Bar Harbor, Maine 04609
SYNOPSIS. TWO common types of egg masses rely on differing routes of supply of
oxygen in water. When embryos are embedded in a gelatinous matrix, oxygen is
supplied by diffusion through the gel, and thicker masses require more gel per
embryo. When an adherent mass of eggs lacks a gel matrix, oxygen can be provided from water flowing through the open interstices between eggs, and larger
eggs provide larger channels and thus less resistance to flow. Both types occur
intertidally, where they are periodically exposed to air. Exposure to air can have
a greater effect on oxygen supply via interstices than on supply via gel. Oxygen
diffusing in interstices drained of water provides increased rates of supply to masses of adherent eggs. In contrast, diffusion through gel is similar for masses in air
and water. Effects of emersion on desiccation also differ for the two types of egg
masses. Additional gel matrix can reduce salinity change from desiccation while
enhancing oxygen supply, whereas draining of interstices, though necessary for
oxygen supply, may increase risk of desiccation.
INTRODUCTION
Air and water present different hazards
and advantages for embryos. Two of these
hazards are risk of desiccation in air and a
much more limited oxygen supply in water.
Many terrestrial eggs have shells or coats
that limit the loss of water by evaporation
(Hinton, 1981; Booth and Rahn, 1990;
Stewart, 1997). In contrast, coats and capsules of aquatic eggs are commonly quite
permeable to small molecules (Pechenik,
1978, 1983, 1986; Seymour and Bradford,
1995). Oxygen is more easily provided to
eggs in air than in water because of physical differences between the two media. The
diffusion coefficient of oxygen in air is
10,000 times higher than in seawater at
20°C. In addition, air contains 38 times
more oxygen per unit volume than does
seawater (Dejours, 1987; Denny, 1993).
There is more oxygen in air, and it diffuses
faster.
Supply of oxygen to embryos can be especially limited when the embryos are ag1
From the Symposium Aquatic Organisms, Terrestrial Eggs: Early Development at the Water's Edge
presented at the annual meeting of the Society for Integrative and Comparative Biology, 3-7 January 1998,
at Boston, Massachusetts.
2
E-mail: [email protected]
gregated in a mass. Oxygen entering the
surface of a mass is consumed by peripheral
embryos, which leaves little for the inner
ones. As a result, development of inner embryos is commonly retarded by low oxygen
concentrations (Crisp, 1959; Taylor, 1971;
Giorgi and Congleton, 1984; Rankine et al,
1990; Booth, 1995; Seymour et al, 1995;
Strathmann and Strathmann, 1995). Requirements for an adequate supply of oxygen to inner embryos limits the thickness
of aggregated masses of embryos (Seymour
and Bradford, 1995; Cohen and Strathmann, 1995; Lee and Strathmann, 1998).
This is no surprise. Krogh (1941) recognized that organisms larger than 1 mm in
diameter and dependent on diffusion for
their oxygen must have a low metabolism,
and his generalization has appeared in
physiology texts ever since. What is surprising is that aggregations of aquatic embryos can be as thick as they are yet lack a
circulatory system. Special features are required to ensure an adequate supply of oxygen to embryos at the interior of the mass
(Strathmann and Chaffee, 1984; Pinder and
Friet, 1994; Seymour, 1995; Lee and Strathmann, 1998).
Intertidal egg masses experience the additional complication of providing an ade-
253
254
R. R. STRATHMANN AND H. C. HESS
quate supply of oxygen in an environment
that changes with each tidal cycle. Intertidal
egg masses closely resemble masses that
are continuously immersed. How do adaptations for oxygen supply in water affect
oxygen supply and water loss when the egg
masses are exposed to air? Our answers are
speculative, but there are abundant opportunities to test the hypotheses by both experimental and comparative studies.
For simplicity, we shall consider two extreme types of egg masses. In one type, embryos are embedded in a gelatinous matrix.
Many molluscs and polychaetes, some insects and fish, and several other aquatic animals deposit eggs in a matrix of gel (Lee
and Strathmann, 1998). In the second type,
eggs adhere to each other and interstices between embryos are open. Many fish, including intertidal species, deposit this type
of egg mass (Moser, 1984). For each type,
we shall briefly review a simple model of
oxygen supply in water and then predict effects of emersion on oxygen supply and
desiccation.
SUPPLY OF OXYGEN
Gelatinous masses of embryos in water
Under simplifying assumptions, a predicted scaling for supply of oxygen by diffusion to central embryos in a gelatinous
matrix is
= FDC/(NM/V).
(1)
The coefficient F is 6 for a sphere, 4 for a
cylinder, and 2 for an infinite sheet (Lee and
Strathmann, 1998). D is the diffusion coefficient for oxygen in the gelatinous mass,
and C is the concentration of oxygen at the
surface of the mass. NM/V is the oxygen
consumption per volume of mass, with N/
V the number of embryos per volume and
M the rate of oxygen consumption per embryo). /?max is the radius or half thickness at
which oxygen consumption produces a decline of oxygen to zero at the center of the
mass. (The dimensions are length2 X time"1
for D, quantity of oxygen X length 3 for C,
length"3 for N/V, and quantity of oxygen X
time"1 for M.) Equation (1) corrects previous errors (Strathmann and Chaffee, 1984)
in deriving a scaling relationship for a gelatinous mass.
One of the assumptions for equation (1)
is a homogeneous distribution of oxygen
consumption throughout the mass. This
means no dependence of oxygen uptake on
oxygen availability down to the level of anoxia and an even distribution of gel and embryos throughout the mass. A second assumption is no consumption or production
of oxygen by fouling microorganisms. Real
egg masses can violate these and other assumptions of this model (Lee and Strathmann, 1998). The exponent of R estimated
for gel masses of seven gastropod species
was 1.4 and significantly less than the predicted value of 2, though also significantly
greater than 1. Nevertheless, the predictions
of this model approximated the observed
thicknesses and concentrations of embryos
in these masses. The model is suitable for
illustrating physical limits in a simple form.
Gelatinous masses of embryos in air
When a gelatinous mass is exposed to air,
the concentration of oxygen reaches saturation at the surface of the mass, and diffusion still limits supply to central embryos.
Thus the predicted limits on oxygen supply
are similar for gelatinous masses in air and
in air-saturated water, though not identical.
Differences may result from depletion of
oxygen in the boundary layer around the
mass. In water, oxygen depletion in a thick
boundary layer is a possibility. This problem nearly disappears in air because diffusion in air enhances transport of oxygen to
the surface of the mass and also because the
reservoir of oxygen in air is greater than
that in the same volume of water. Thus
emersion at low tide could increase the supply of oxygen to the surface of a mass. A
limit on the effect of the boundary layer is
indicated by its extreme effects on the predicted maximum radius of a spherical mass
(Lee and Strathmann, 1998). With no
boundary layer, the maximum thickness is
as in equation (1), with C the concentration
of oxygen in air-saturated water and F = 6
for a sphere. In still water (giving a maximally thick boundary layer) oxygen is depleted in the water surrounding the mass.
The predicted maximum radius of the
sphere becomes
OXYGEN SUPPLY AND DESICCATION
2
x
= 6DMC/{(NM/V)[1
2(DM/DW)]}
(2)
where DM and D w are the diffusion coefficients of oxygen in water and in the mass
(Lee and Strathmann, 1998). For several
gelatinous masses, DM has been estimated
to be between 75 and 100% of D w (Burggren, 1985; Seymour, 1994; Strathmann and
Strathmann, 1995). Rmax is smaller for a given embryo concentration in still water than
when water at the surface of the mass is airsaturated. The predicted maxium radius allowed by diffusion depends on the factor [1
+ 2(DM/DW)]05 from Eq. 2. A mass with no
boundary layer could be up to 1.7 times the
radius of a mass in still water. This is a
maximum estimate, and the actual consequences of boundary layers on oxygen supply to gelatinous egg masses are probably
less extreme (Seymour, 1994). Water is seldom completely still. With free-stream flow
of 8 cm s"1, the oxygen concentrations
within one mm of the surface of egg masses
of an opisthobranch mollusc were reduced
by only a few percent from concentrations
at >10 mm distance (Cohen and Strathmann 1996). Even in still water, density
gradients produced by exchange of metabolites at the surface of respiring eggs may
cause water to flow (O'Brien et al., 1978).
Because water flow is never so great that
the boundary layer is 0, the effect of the
boundary layer is not so extreme as the estimated maximum. An additional factor is
that gelatinous masses are colonized by a
microflora whose effect on surface oxygen
concentrations exceeds that of the boundary
layer (Cohen and Strathmann, 1996). Also,
photosynthesis and respiration of organisms
in the surrounding water can produce oxygen concentrations that exceed or fall below
saturation from air.
Any advantages of oxygen supply in air
are also decreased or overwhelmed by removal of support by water. In air, a gelatinous mass collapses against the substratum,
which blocks the supply of oxygen through
much of its surface (Seymour et al., 1995).
The effect of this collapse of the gel under
its greater weight in air can be appreciated
by estimating how much thinner the collapsed mass would need to be to maintain
255
the same supply of oxygen to inner embryos. If a sphere collapsed to a sheet, the
shape factor (F) would change from 6 to 2,
and /?max thereby decreased by a factor of
1.73. If oxygen supply through the lower
surface is blocked by collapse against the
substratum, then oxygen is supplied only
through the upper surface and must diffuse
to the lowermost embryos. Then Rmax is further reduced by a factor of 2. Because of
the combined effects of the change in shape
and the block to diffusion through one surface, the spherical mass supported in water
can be 3.46 times as thick as a mass flattened into a sheet against the substratum.
By this estimate, a spherical mass must collapse and spread to less than a third of its
original thickness if the same oxygen supply is to be maintained in air.
Adherent masses of embryos in water
When eggs adhere to one another at only
a few regions of contact on their surfaces
and lack a gelatinous matrix, oxygen can be
supplied by water flowing through interstices between embryos (Strathmann and Chaffee, 1984; Seymour, 1995). A simple model
for supply of oxygen by interstitial flow of
water is based on the pressure difference
required to drive a sufficient flow through
a mass of oxygen-consuming spheres of
uniform diameter (Strathmann and Chaffee,
1984). The equation is
pressure difference
= [1080L2M(x(l - P)3]/(ml5CP3)
(3)
with L the thickness of the mass in the direction of flow through the mass, M the rate
of oxygen consumption per embryo, u. the
dynamic viscosity of the fluid, P the porosity of the mass as proportion of total volume that is interstitial space, d the egg diameter, and C the difference in oxygen concentration between water entering and exiting the mass. This equation is a highly
simplified model of a complex situation, but
it indicates how the properties of a mass
may affect oxygen supply by interstitial
flow. Other things being equal, thicker masses of adherent eggs are expected to be
composed of larger eggs because thicker
256
R. R. STRATHMANN AND H. C. HESS
masses require larger channels for adequate
ventilation of embryos. A positive correlation between egg mass thickness and egg
size is predicted, and this trend has been
found in a sample of fish egg masses (Hess,
1991). Aggregations of small eggs (about
0.1 mm diameter) would resist interstitial
flow and are therefore arranged in thin lamellae (such as those of barnacle broods)
and are presumably supplied with oxygen
by diffusion rather than interstitial flow
(Crisp, 1959). Eggs adhering in thick aggregations are usually >1 mm in diameter,
as for fish, or tethered individually on
threads to form a highly porous and flexible
mass (as in broods of decapod crustaceans).
Adherent masses of embryos in air
Numerous fishes deposit masses of adherent eggs on intertidal surfaces (Marliave,
1981; Taylor, 1990; De Martini, 1991)
where they are alternately exposed to air
and water. Thick, adherent masses of fish
eggs present varied possibilities for costs or
benefits from exposure to air.
When embryos in an adherent mass are
exposed to air, the oxygen supply should be
greatly reduced if the interstitial spaces remain filled with water. There would be no
external moving water to drive flow
through the interstices. Water might circulate slowly within the mass as a result of
the mass's differential heating, evaporative
cooling, or exchange of solutes (O'Brien et
al. 1978; Seymour, 1995). To our knowledge, the circulation of interstitial water
within an exposed mass and its adequacy
for supplying oxygen to embryos have not
been examined.
In contrast, if the interstitial spaces of an
exposed mass are sufficiently drained of
water while the spaces remain open, oxygen
supply to embryos should be greatly increased. Even without interstitial flow, diffusion will be 10,000 times more effective
in an air-filled channel than in a water-filled
channel. Also, there is about 38 times more
oxygen per volume in air than in air-saturated sea water at 20°C, which provides a
larger reservoir of oxygen within the channels between embryos.
The maximum possible length for diffusive oxygen supply in blind-ending tubes
has been estimated for insect tracheae (Denny, 1993), and the estimate can be adapted
to diffusive supply via air-filled interstices
in a mass of adherent embryos. An intertidal egg mass of the stichaeid fish Xiphister
atropurpureus was 2.8 cm thick (Hess,
1991). Porosity was 0.58, and egg diameter
2.2 mm. Oxygen consumption measured at
10°C, was 83 |xl 02 g"1 hr"1 (mass determined by wet weight of blotted egg masses,
units corrected from ml to u.1). The maximum distance for oxygen supply via diffusion in blind channels is estimated from
L2 = 2[ACD(At/A)]/M with L the maximum length and A/A the proportion of
cross-sectional area represented by tracheae
(Denny, 1993). If one assumes that the embryos consume 25% of the oxygen in air at
10°C, then AC, the difference in oxygen
concentration along the channel, is 2.25
mole O2 m~3. This assumption is arbitrary
but sets the lowest concentration of oxygen
far above that at which several types of embryos reduce rates of development and oxygen consumption (Strathmann and Strathmann, 1995). D, the diffusion coefficient
for oxygen in air, is 19.1 X 10 6 m2 sec"1
at 10°C. The oxygen consumption per volume of mass per time, M, is 0.00044 mole
O 2 m~3 sec"1. A generous assumption is that
the channels are entirely free of water and
(A/A) equals the porosity of 0.58. Under
these assumptions, the maximum distance
into the mass for supply by diffusion is
about 33 cm. If the estimate is even approximately correct, then diffusion can supply sufficient oxygen into blind air-filled
channels in the largest egg masses of fish.
It is the high porosity and low oxygen consumption that allows a distance many times
that of an insect tracheal tube.
But the question remains, are fish egg
masses fully drained when exposed to air?
Some have remarkably dry surfaces, but we
know of no report on interstitial water from
field observations of an exposed mass. Intertidal masses of fish eggs are sufficiently
firm to maintain their shape out of water.
This at least provides the possibility of open
air channels. In contrast, the channels between gel-coated amphibian eggs would
collapse if the mass were unsupported by
OXYGEN SUPPLY AND DESICCATION
water, with a consequent reduction in oxygen supply (Seymour et al., 1995).
Complete draining of aggregated fish
eggs may require special conditions, as indicated by preliminary observations on egg
masses of two species of cottid fish. For
both species' masses, blotting with absorbant paper was sufficient to open interstitial
channels, but masses of the two species differed in draining. Ascelichthys rhodorus deposits eggs of 1.7 mm diameter on intertidal
surfaces. The three examined masses were
irregular and ranged from 22 to 30 mm
wide and 4 to 14 mm thick. They had been
detached from the rocks. Each mass absorbed water to a height of 14 to 15 mm in
air when its edge was touched to fluorescein
dyed sea water puddled on a glass plate.
Filled masses, with an edge touching a
glass plate, drained to about the same
height. Partial draining on exposure appears
to be inevitable, but complete draining may
depend on where the eggs are deposited and
perhaps also evaporation.
In contrast, Artedius harringtoni deposits
much smaller eggs (0.95 mm diameter) on
subtidal surfaces. The two masses examined were low mounds 3 to 4 mm at the
thickest and 23 to 25 mm across, both attached to rocks. Masses on vertically oriented rock surfaces filled completely with
water (to a height of greater than 20 mm)
when one edge was immersed or when water was pipetted to the lower edge. There
was no draining of interstitial water without
blotting. If masses like this were exposed
to air, draining would depend on evaporative drying of the mass or adjacent surfaces.
With wettable eggs, such as the ones examined here, water is drawn into the interstices as into a capillary tube. With tubes,
the height that the water rises is inversely
proportional to the radius of the tube. Small
eggs and low porosity may prevent draining
of a mass exposed to air, although the acute
angles between adherent eggs and their distribution in the mass complicate filling and
draining. Also, whether intertidal egg masses are drained or remain filled at low tide
depends on water on adjacent surfaces, as
well as egg size, porosity, and wettability.
Thus parental choice of deposition sites
may affect draining of interstitial channels
257
and hence oxygen supply to embryos during low tide.
DESICCATION
Other things being equal, evaporative
loss of water per mass weight per time is
less for a larger mass, and aggregation of
eggs affords some protection from desiccation. Even with the low rate of loss from
diffusion alone, individual 1 mm spheres
that were completely water-permeable
would initially lose several times their body
mass per hour at 20°C and a relative humidity of 0.5 (Denny, 1993). The proportion of mass of a sphere lost per time decreases with the square of the sphere's diameter. Thus egg masses are expected to
sustain desiccation during several hours at
low tide better than individual eggs. This
prediction is supported by the report that
communal masses of the frog Rana sylvatica suffer lower mortality from desiccation
than single clutches (Forester and Lykens,
1988).
In still air, with only diffusion carrying
water away from the mass, rate of water
loss would be proportional to surface area.
Water loss is more rapid in moving air and
is also dependent on wind speed. With a
flow of air over the evaporating surface,
rate of water loss per area is predicted to be
proportional to (v/L)b, with v the wind velocity, L the distance over which a boundary layer develops, and b a constant dependent on geometry (Leighly, 1987). The value of b for loss of distilled water from regular plane surfaces was about 0.5 and from
a terrestrial snail facing into the wind, 0.64
(Leighly, 1937; Machin, 1964). Thus the
length of the mass in the direction of air
flow is expected to affect rate of water loss.
Water loss per area is less for a mass with
a larger dimension parallel to the wind direction, but total water loss remains greater
for a mass with a larger surface area. For
masses of the same volume, shapes with
smaller exposed surface areas should experience lower rates of water loss as a percent of the total water content of the mass.
Gels and some permeable skins lose water to air as would a free water surface (Machin, 1969; Spotilla and Berman, 1976).
Gelatinous egg masses may do the same,
258
R. R. STRATHMANN AND H. C. HESS
although it is possible that as the gel mass
dries, permeability decreases, as observed
for toads' skins (Machin, 1969) and suggested for gel masses of trichopteran insects, a freshwater snail, and a frog (Berte
and Pritchard, 1983; Forester and Lykens,
1988). Mineral deposits decrease permeability of egg shells or capsules of many
terrestrial vertebrates and gastropods. The
intertidal sea anemone Anthopleura elegantissima attaches gravel to its skin, thereby
reducing the rate of water loss during exposure to air (Hart and Crowe, 1977). Some
marine snails, such as naticids and neritoideans, add mineral grains or deposited
calcium carbonate to capsule walls (Andrews, 1935). Some of these snails, such as
Nerita species, commonly deposit their capsules high in the intertidal zone, but many
others are submerged at all times. Advantages of defense may outweigh costs of reduced gas permeability even for some submerged eggs, but the net benefits of a smaller permeable surface should be greater in
air. Despite these possible means of reducing permeability of egg coats, egg capsules
of the intertidal marine snail Ilyanassa obsoleta lost water at the same rate as the related subtidal species Nassarius trivitattus,
indicating no adaptation of the permeability
of this species' capsule to intertidal life
(Pechenik, 1978). The remainder of this
discussion ignores low permeability of gel
rinds or egg chorions as possible means of
reducing desiccation in air.
We know of no data for desiccation of
intertidal gel masses or masses with open
interstitial channels. Data for adult amphibians indicate expected losses from gelatinous masses. Rates of loss vary with species, relative humidity and wind speed, but
in a sample of salamanders of the size of
many egg masses, the rate of water loss (E)
in mg hr~' was related to the body weight
(W) in g by the equation E = 100W04 in
nearly still air of 60-70% relative humidity
(least squares regressions of log transformed data) (Spight, 1968). Spight's 1 g
salamanders lost about 10% of their starting
weight in 1 hr and his 10 g salamanders lost
about 2.5%. Rates of water loss were greater at lower relative humidity and would
doubtless be greater with greater air speed.
These data suggest that desiccation during
a few hours exposure at low tide could be
a hazard for intertidal egg masses. They are
of a size and shape that, under some circumstances, could result in substantial water loss during a low tide. How do the features adapting them for oxygen supply by
diffusion increase or decrease this vulnerability to desiccation?
Gelatinous masses
Thick gelatinous masses have more gel
per embryo, presumably to provide sufficient oxygen by diffusion (Lee and Strathmann, 1998). Both the globose shape and
high volume of gel per embryo in these
thick gelatinous masses should protect
against desiccation. With a greater volume
of gel per embryo, there is less change in
salinity for a given loss of water per embryo. Thus the gel necessary to enhance
supply of oxygen by diffusion is also a protection against desiccation. In contrast,
masses whose thin shape enhances oxygen
supply should be especially vulnerable to
desiccation by both large surface area and
small amount of gel per embryo. The vulnerability to desiccation could be reduced
for coiled ribbons that provide separated
free surfaces in water but collapse into a
more compact mass when exposed to air;
however, the collapse into a stack that is
many layers thick creates a mass of embryos that is too thick and concentrated for adequate oxygen supply by diffusion.
As the outer portion of a gelatinous mass
dries, water must be redistributed in the
mass. If the hazard from desiccation of the
gel is increased salinity, then a benefit of a
gelatinous matrix is prevention of a sudden
osmotic shock for the embryos. When a
marine egg mass is abruptly exposed to low
salinities, gel or capsule walls similarly protect embryos by providing a slow change
that permits acclimation (Pechenik, 1983;
Woods and DeSilets, 1997). An outer rind
of gel that is free of embryos, as occurs in
egg masses of many annelids and gastropods, may protect outer embryos from desiccation by removing them from the extreme and most abruptly changing end of a
gradient of increasing salinity. These outer
rinds occur on subtidal as well as intertidal
259
OXYGEN SUPPLY AND DESICCATION
egg masses. Thicknesses of outer rinds of
gel in different habitats have not been compared.
Adherent eggs with interstitial channels
For egg masses that are supplied with oxygen via interstitial channels between eggs,
conditions that maintain oxygen supply
may increase desiccation. Water cannot
flow through channels when the mass is exposed to air. Oxygen supply may decrease
if stagnant water remains in the channel or
increase if interstitial water is replaced with
air, but draining the water from the channels
decreases the reservoir of external water
that could protect embryos from desiccation. In contrast to expectations for exposed
gelatinous masses, the features promoting
oxygen supply should increase rather than
decrease the hazard of desiccation.
Two features of masses of adherent eggs
may reduce the hazard of desiccation. One
is that water loss from surfaces within channels should be slow, because air within
channels may be saturated with water. The
surface losing water then becomes the outer
surface of the mass. The other is that channels can be incompletely drained and still
open to air. When egg masses of cottids
were drained by blotting (see above), the
acute angles between adherent spheres retained water. A small reservoir of external
water remains even when channels are open
to air. The remaining interstitial water,
though less than the reservoir in a gelatinous matrix, may provide some protection
against water loss.
Deposition of eggs in habitats that remain humid at low tide may provide the
best of both worlds. The cottid Clinocottus
acuticeps deposits a monolayer of eggs
high in the intertidal zone but under the
alga Fucus, which protects the eggs from
desiccation. Removal of the alga increased
mortality, and embryos were vulnerable to
desiccation in laboratory experiments (Marliave, 1981). Moist sites are a common but
not universal choice for intertidal deposition of eggs, and this choice may serve other functions as well, such as protection
from solar radiation (Biermann et al., 1992;
Rawlings, 1996).
ACKNOWLEDGMENTS
Support was from National Science
Foundation grant OCE-9633193 to R. R.
Strathmann. M. Denny, F. Forster, D. Griinbaum, J. B. Marliave, K. L. M. Martin, and
S. Norton answered questions. R. Hale, C.
Petersen, and S. Norton supplied masses of
adherent fish eggs. R. S. Seymour, P. Verrell, and an anonymous reviewer provided
useful comments and corrections.
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Corresponding Editor: Paul Verrell