AMER. ZOOL.

, 30:189-196 (1990)

Size, Speed and Buoyancy Adaptations in Aquatic Animals1

R. MCNEILL ALEXANDER
Department of Pure and Applied Biology, University of Leeds,
Leeds LS2 9JT, England

SYNOPSIS. Animals are denser than either fresh water or sea water, and therefore tend
to sink, unless they have adaptations that give buoyancy. Very small organisms sink slowly,
reproduce rapidly and can be kept suspended by natural turbulence: individuals lost by
sinking are replaced by reproduction. This is likely to be effective only for organisms of
less than 150 nm diameter. Larger animals will sink unless they swim or evolve buoyancy
organs. Hovering is one of the options available to them, but the "hop and sink" technique
used by some copepods is more economical than steady hovering. Another option is to
use fins as hydrofoils, as sharks, tunnies and many squids do. This implies an energy cost
because work has to be done against drag on the hydrofoils. Many animals are made
buoyant by gas-filled floats, low-density organic compounds or body fluids of unusual ionic
composition. Such buoyancy aids increase the energy cost of swimming at given speed
because they increase the animal's bulk. Buoyancy aids are more economical than hydro-
foils for animals that swim slowly but hydrofoils are more economical for those that swim
fast.

INTRODUCTION fishes (Alexander, 1972), but this new paper

Fresh water has a density of about 1,000
kg/m 3 (varying only slightly with temper-
ature) and sea water about 1,026 kg/m 3 ,
but animals consist largely of denser mate-
rials. Consequently, aquatic animals that
lack buoyancy adaptations are denser than
the water in which they live. Many teleost
fish have gas-filled swimbladders that give
them buoyancy, but most others have den-
sities between 1,060 and 1,090 kg/m s
(Jones and Marshall, 1953). Many squids
are made buoyant by ammonium-rich body
fluids, but others have densities between
1,055 and 1,075 kg/m 3 (Clarke et al., 1979).
Even marine phytoplankton have similar
densities, averaging about 1,080 kg/m 3
(Eppley ^ a/., 1967).
Pelagic organisms will sink to the bottom
unless they have adaptations that give them
buoyancy, or are prevented from sinking
in some other way. In this paper, I review
strategies that are available to them, con-
sidering the advantages of each strategy
for animals of different sizes and for ani-
mals that swim at different speeds. In an
earlier paper on this topic I considered only
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 where v is the sinking speed, r the intrinsic
Francisco, California.
is more general.
I will make various calculations for ani-
mals living in sea water of density 1,026
kg/m 3 . I will assume that typical animals
without buoyancy aids have a density of
1,075 kg/m 3 .
EDDIES
It might be supposed that pelagic pop-
ulations of non-buoyant organisms could
not survive, except by swimming actively.
This is not the case for very small organ-
isms, because natural waters are seldom
still. There are generally eddies, so that
though the average velocity of a dense non-
swimmer is downward, its velocity fluctu-
ates and may sometimes be upward. Also,
reproduction can compensate for individ-
uals that are lost from the population by
sinking. Reproduction could not maintain
a population near the surface if every mem-
ber of the population were always sinking,
but it may be able to do so if eddies some-
times return individual organisms towards
the surface. The reproduction must be
fairly fast, the eddies must be fairly strong
and the mean sinking speed must not be
too great. Riley et al. (1949) showed that a
stable population was possible only if
vz/r < 4K (1)
rate of natural increase (defined by eq. 4,
189
190 R. MCNEILL ALEXANDER

below) and K is the vertical eddy diffusivity of 2 x 10"9 kg, about the same as a large
(a measure of the strength of the turbu- Paramecium. A spherical animal of this mass
lence). For a summary of their argument would have a diameter of 150 nm.
see Hutchinson (1967, p. 283). That argument sets a size limit to reli-
The organisms that depend on eddies in ance on eddies, but even when this strategy
this way are protistans and other small is possible it may not be the best. It wins
members of the plankton. They are small survival at a cost, the loss of the individuals
and sink slowly, so their Reynolds numbers that sink to depths where they cannot sur-
are small and they sink according to Stoke's vive. For a simple (albeit rather unrealistic)
law (see Alexander, 1983 for explanations calculation, imagine an animal that thrives
both of Reynolds number and of Stoke's down to depth D but dies if it sinks further.
law). For a sphere of diameter d, density p (Perhaps it feeds on phytoplankton that live
sinking in water of density pw and viscosity only near the surface.) Assume that its pop-
ulation density is uniform between the sur-
face and this depth. The fraction of the
v = gd\p - Pw )/'18M,,. (2) population lost by sinking, per unit time,
The mass m of the sphere is ird p/6. The is v/D. If the energy content per unit mass
3

gravitational acceleration g is 9.8 m sec"2 of animal is H the rate of loss of energy

and the viscosity of water at 20C is 1.0 x per member of the population, P, is
10~3 Pa sec. We have already agreed to
assume p = 1,075 kg/m 3 , pw = 1,026 kg/ P = Hmv/D. (6)
m3. With these values, eq. 2 gives H can be estimated as the heat of combus-
0 67 tion of the animals, which is likely to be
v = 39 b - (3) about 4 MJ/kg wet mass, and v is given by
(v in m/sec, m in kg). Plankton with long eq. 3. Hence
spines may sink more slowly than this equa-
tion predicts. The sinking rate of the dia- P= 1.6 x 109m'-6V> (7)
tom Thalassiosira was almost doubled when (P in W/kg, m in kg, D in m). This energy
its spines were removed (Walsby and Reyn- cost will be compared, in the Discussion
olds, 1980). section, with the cost of an alternative
If there were no losses by sinking, a pop- strategy.
ulation of density (numbers per unit vol-
ume) N would increase at a rate dN/dt HOVERING
where A second possibility for dense pelagic
animals is that they should swim constantly
dN/dt = rN (4) upwards, just fast enough to avoid sinking;
r is smaller for larger organisms. Fenchel in other words, that they should hover.
(1974) showed that for metazoan poikilo- Most ciliated animals swim at about 1 mm/
therms sec (Sleigh and Blake, 1977), only a little
8 27 faster than the sinking speed of the largest
r 4.0 x 10- ?-- (5) animal that we have calculated could be
(r in sec"', m in kg). kept suspended by eddies. Larger ciliated
The possibility of being kept suspended animals are unlikely to be able to hover.
by eddies depends on v2/r (inequality 1). However, smaller ones might gain an
Eqs. 3 and 5 show that v2/r increases very advantage by hovering instead of relying
rapidly indeed, as size increases. This on eddies, if the metabolic power required
implies that there must be a sharp upper for hovering were less than the rate al
limit to the size of organisms that can be which energy would otherwise be lost, by
kept suspended in this way. The diffusivity animals sinking out of the favourable range
K varies greatly with depth, locality and of depths (eq. 7).
weather but is typically of the order of 0.01 Copepods and other planktonic crusta-
m 2 /sec in the sea (Bowden, 1964). If it has ceans are too large to be kept suspended
this value the limit should occur at a mass by eddies, but they can swim in short bursts
 SIZE, SPEED AND BUOYANCY
at up to 0.3 m/sec (Morris et al., 1985).
They either hover or use the "hop and
sink" strategy, alternately swimming
upwards and sinking down. Haury and
Weihs (1976) argued that hop and sink
could be more economical of energy than
hovering, for animals that use parachute
devices (such as the long antennae of cope-
pods) to slow their sinking. Such devices
can be spread to increase drag while the
animal is sinking passively, and folded to
reduce drag while it is swimming upwards.
The theory of helicopters shows that
hovering is more difficult for large animals
than for similar small ones: the power
required for hovering by geometrically
similar animals of equal density is propor-
tional to (body mass)7/6 (Alexander, 1982).
Synchiropus is a small, dense fish which hov-
ers in sea water by beating its pectoral fins,
but it generally hovers close to the bottom
where energy requirements are reduced by
ground effect (Blake, 1983). Most dense,
hovering aquatic animals are very much
smaller.
HYDROFOILS
A dense animal that swims horizontally
can prevent itself from sinking by using its
fins as hydrofoils: it is then supported by
hydrodynamic lift on its fins in the same
way as an aeroplane is supported by aero-
dynamic lift on its wings. Slow swimming
using hydrofoils may require less power
than hovering (see Blake, 1983, fig. 92).
Many sharks and tunnies are denser than
the water they swim in. Their net weight
is supported mainly by lift on the pectoral
fins (Magnuson, 1970). Squids also use their
fins as hydrofoils (O'Dor, 1988).
An animal of volume V and density p has
weight Vgp in air, but its net weight in water
of density pw is only Vg{p pw). The lift L
that it needs from hydrofoils is equal to
this:
L = Vg(p - Pw ) = mg(p - Pw)/P (8)
where m is the animal's mass. We will cal-
culate the energy cost of producing this
lift.
The drag on a hydrofoil has two com-
ponents, induced drag and profile drag.
The induced drag on a hydrofoil of span s
191
travelling at speed u and giving lift L is
approximately 2L2/irpwii2s* (Alexander and
Goldspink, 1977). If the hydrofoil has the
optimal area for producing this lift at this
speed the two components of drag are
equal, so the total drag is twice the induced
drag. The mechanical power needed to
propel the hydrofoil through the water is
this total drag multiplied by the speed. The
metabolic power Ph is the mechanical power
divided by the efficiency rj
(This equation may underestimate the
power needed if the hydrofoils are small
and move slowly, i.e., if their Reynolds
numbers are low.)
From eqs. 8 and 9
Ph = 4m2g2(p pw)2
+ Vwpwp2us2. (10)
This power could in principle be kept
low by making the span 5 very large. How-
ever, small animals cannot conveniently
carry very long fins. Tunnies (Scombridae)
have pectoral fin spans up to about 0.6 times
body length / (Magnuson, 1973) and we
will take this as an upper limit.
5 = 0.6/. (11)
The lengths and masses of typical tun-
nies are related approximately by the equa-
tion
m = 20/3 (12)
(m in kg, / in m; Magnuson, 1973, fig. 3).
We will use eqs. 11 and 12 to replace s in
eq. 10. As before, we will assume p = 1,075
kg/m 3 and pw = 1,026 kg/m 3 . Webb (1971)
measured the oxygen consumption of fish
swimming with objects attached to their
bodies, to increase drag. The results of his
experiments suggest that the efficiency rj
with which the animal would do work
against the drag on its hydrofoils might be
about 0.10 (see Alexander and Goldspink,
1977). With these values, eq. 10 becomes
P h = 0.051m'-3Vu (13)
(Ph in W, m in kg, u in m/sec). Remember
that this is not the total power required for
swimming at speed u, but the additional
power that is needed because the animal is
192 R. MCNEILL ALEXANDER

denser than the water. It decreases as the if it is ammoniacal fluid of density 1,010
speed u increases. kg/m 3 .
Buoyancy organs make animals bulkier,
BUOYANCY AIDS increasing the energy needed for swim-
Animals use many different materials to ming at given speed. I will estimate the
give buoyancy (Alexander, 1982). Most power that would be needed for swimming
teleost fishes have a gas-filled swimbladder. by a well-streamlined animal such as a fish
Sepia and some other cephalopods have gas- or squid, if there were no need to expend
filled chambers in their shells. Many energy to prevent sinking. I will then esti-
siphonophores have gas-filled floats. mate the energy that would be needed if
A few sharks have densities very close to it acquired a buoyancy organ of appropri-
that of seawater, due to enormous quan- ate volume, which made it larger. I will
tities of the hydrocarbon squalene (density compare the difference (the extra power
860 kg/m 3 ), mainly in their livers (Bone needed because of the buoyancy organ)
and Roberts, 1969). The coelacanth Lati- with the power that I have already calcu-
meria and some lantern fishes (Myctophi- lated for obtaining lift from hydrofoils.
dae) depend for buoyancy on wax esters The mechanical power (drag multiplied
which probably have about the same den- by velocity w) required to propel a rigid
sity. Some mid-water crustaceans have den- body through water is 1/2pw5wsCD, where S
sities little more than that of seawater, due is an area and CD is the corresponding drag
to the large proportions of lipid in their coefficient (Alexander, 1983). The meta-
bodies (Childress and Nygaard, 1974). bolic power P that an animal needs for
Some other animals have low-density swimming can be estimated by dividing this
body fluids that help to match the density power by an efficiency r\'
of the body to that of the water. Many
squids contains large quantities of fluid that P = >/iPwSsCD/ij' (15)
has about the same osmotic concentration This efficiency is not necessarily the same
as sea water or the blood but have the as the one that appeared in eq. 9. It is dif-
sodium ions largely replaced by ammo- ficult to predict on theoretical grounds, at
nium (Denton, 1974). Scyphozoan jelly- least for fish, because the undulatory
fish, ctenophores and some siphonophores movements of fish swimming seem to
have mesogloea that is slightly less dense increase drag above the rigid body value
than sea water, due to exclusion of sulphate (see Alexander, 1982). I will therefore use
ions (Bidigare and Biggs, 1980). metabolic data to establish a relationship
Consider an animal which, without any between power and speed.
buoyancy organs, has volume V and density Most of the animals we have been dis-
p. To match its density to that of the water cussing (fish and cephalopods) are well-
it lives in (pw) it would need a buoyancy streamlined, so most of the drag on them
organ containing volume Vb of material of is presumably friction drag (see Alexander,
density pb. This would increase its total vol- 1983). They swim in the range of Reynolds
ume to (V + Vb) and its mass to (Vp + Vbpb) numbers for which the boundary layer is
expected to be laminar, so we can expect
(Vp + VbPb)/(V + Vb) = pw to find
Vb/V = (p - pj)/(pw - pb).
(14) CD ex (/)- (16)
Notice that Vb/V must be large if (pw pb) where / is body length. We will insert this
is small (i.e., if the buoyant material is only in eq. 15 and assume (controversially, per-
a little less dense than the water). Assume haps) that V is independent of body size
as before that p = 1,075 kg/m s and pw = and speed
1,026 kg/m 3 . The required values of Vb/V
P oc Sw2-5/-0-5. (17)
are 0.05 if the buoyant material is gas of
negligible density, 0.30 if it is squalene or For geometrically similar animals, S oc Vv*
wax esters of density 860 kg/m 3 and 3.06 and / oc Vv'
 SIZE, SPEED AND BUOYANCY 193

P oc y5w25. (18) pounds such as wax esters. An animal that

is growing with relative growth rate G has
I have estimated the constant of this pro- a volume Vb of a low-density compound of
portionality from Webb's (1971) metabolic density pb. To keep a constant proportion
measurements on swimming trout (Salmo of this compound in its body it must accu-
gairdneri). The rates of oxygen consump- mulate it at a rate GVbpb. If the heat of
tion of his control group (without added combustion of the compound is Hb this ties
loads) correlate well with (speed)25 (cor- up energy at a rate
relation coefficient 0.97). I calculate from
the slope of the regression / V = GHbVbPb. (23)
5 25
P = 146V- u (19) This is additional to the power require-
3 ment Pb given by eq. 22.
(P in W, V in m , u in m/sec).
If the animal has a buoyancy organ of DISCUSSION
volume Vb in addition to its basic volume
V it needs additional power Ph I have already argued that animals with-
out buoyancy aids cannot be kept sus-
P + Pb = 146(V + Vb)-5M2-5 pended by turbulence if their masses are
= 146(V-5 + 0.5VbV-5 above about 2 ng. In this section I compare
+ .. >2 5 (20) the merits of different methods of avoiding
sinking, in situations where several are pos-
(using the binomial expansion). If Vb/V is sible.
not too large we can ignore subsequent First, consider small planktonic animals
terms in the expansion and subtract (19) which might be kept suspended by turbu-
from (20) to obtain lence (incurring the loss by sinking given
Pb ~ by eq. 7) or might match their density to
the water by accumulating a low-density
= 73(yb/V)VV-5. (21) organic compound (at the cost given by eq.
3
Since V = m/p and p ~ 1,000 kg/m , 23). Assume (Vb/V) = 0.3 as for squalene
and wax esters. (Triglycerides would be
Pb ~ 23m0bu2b(Vb/V) (22) denser and would be needed in larger
(Pb in W; m in kg; u in m/sec). This is the quantities.) Assume a heat of combustion
extra power needed for swimming at given of 40 MJ/kg, which is probably about right
speed, because of the presence of the buoy- for all these compounds (see data in Weast,
ancy organ. 1987). Equate the growth rate G to the
This power is zero if the animal remains intrinsic rate of natural increase (eq. 5).
stationary (which it can do without effort, With these assumptions, eqs. 7 and 23 tell
if its density is the same as that of the water). us that reliance on turbulence is preferable
However, a buoyancy aid implies other to accumulation of buoyant organic com-
energy costs, whether the animal swims or pounds unless
not: energy is needed to grow the organ,
and to maintain it. I previously attempted D < 4 x 10 9 m 094 . (24)
to estimate the energy cost of secreting gas (D in m, m in kg). Hence organisms of less
into a swim-bladder to replace diffusion than 1 ng mass could not be expected to
losses (Alexander, 1972). My quantitative accumulate low-density organic com-
conclusions were suspect because I had to pounds as buoyancy aids unless (which
guess the efficiency of the process of gas seems improbable) they were restricted to
secretion, but one point is clear: the cost depth ranges of only a few metres.
of maintaining a swimbladder increases I have already argued that dense, ciliated
with depth. It would be equally difficult to animals are unlikely to be able to hover if
estimate the cost of maintaining low-den- they are too large to be kept suspended by
sity ammoniacal fluids. turbulence. Ctenophores are ciliated ani-
It seems much easier to estimate the cost mals with diameters of the order of 10 mm,
of accumulating low-density organic com- but their low densities relieve them of the
194 R. MCNEILL ALEXANDER

10

speed, m/s
1
D

0.1
o

0.01
0.1 10 100 1000 10,000
mass, kg
FIG. 1. A graph on logarithmic coordinates of swimming speed against body mass, with lines calculated from
eq. 27. Above the appropriate line, hydrofoils are more economical of energy than buoyancy aids, as means
of preventing sinking. Below the line, buoyancy aids are more economical. The points show masses and typical
swimming speeds for: O, trout (Sahno Irutta, Holliday et al, 1974); , wahoo (Acanthocybium solandri) and ,
various scombroids (Magnuson, 1973); and A, basking shark (Cetorhinus maximus, Bone and Roberts, 1969).
The scombroids (filled symbols) have densities of 1,080-1,090 kg/m 5 . The other fishes (hollow symbols) are
close in density to the water in which they swim.

need to hover. I have also argued that, On the same graph I show the masses of
even with other means of propulsion, hov- variousfishes,with typical swimming speeds
ering is difficult for large, dense animals,taken from the literature. The trout (Salmo)
because the power required is proportional and the wahoo (Acanthocybium) have swim-
to (body mass)776. bladders, and their densities are very close
For animals of the size range of fishes to that of the water they live in (see Mag-
and squids, hydrofoils and buoyancy aids nuson, 1973, on wahoo). The basking shark
seem the best means of preventing sinking. (Cetorhinus) has enough squalene to bring
What are their relative merits for an ani- its density close to that of seawater (Bone
mal of mass m that swims at speed u? Eqs. and Roberts, 1969). The points for all these
13 and 22 tell us that hydrofoils are more fish lie well below the lines, indicating that
economical if their buoyancy aids are more economical
of energy than hydrofoils would be. The
0.051m 13S /u < 2.3-5M2-5(Vb/V) scombroids have no swimbladder, and their
u > 0.34?/i-24(V/Vb)029. (25) densities are about 1,080-1,090 kg/m s , a
Figure 1 is a graph of speed against body little higher than we assumed in our cal-
mass with lines corresponding to Vb/V = culations. Three of the points lie approx-
0.05 (as expected for a swimbladder, see imately on the "swimbladder" line indi-
above) or 0.30 (squalene or wax esters). In cating that hydrofoils are about as
the part of the graph above the lines, economical as swimbladders would be. Two
hydrofoils are a more economical means other points, however, lie a little below the
of preventing sinking than buoyancy aids. "swimbladder" line, suggesting that these
Below the lines, buoyancy aids are more fish would have needed less energy for
economical than hydrofoils. The change of swimming at their usual speeds, if they had
advantage, from buoyancy aids to hydro- retained the swimbladder. However, the
foils, occurs at a higher swimming speed cost of secreting gas to replace diffusion
for swimbladders than for squalene and wax losses from the swimbladder (Alexander,
esters. 1972) was omitted from the calculation.
 SIZE, SPEED AND BUOYANCY 195

Similarly in cephalopods, the dense Alexander, R. McN. 1983. Animal mechanics, 2nd ed.
squids are the fast swimmers while cuttle- Blackwell, Oxford.
fish (with gas-filled shells) and ammoniacal Alexander, R. McN. and G. Goldspink. 1977.
Mechanics and energetics ofanimal locomotion. Chap-
squid seem to be relatively sluggish. man & Hall, London.
In comparing hydrofoils and buoyancy Bidigare, R. R. and D. C. Biggs. 1980. The role of
aids I have assumed that the fish requires sulfate exclusion in buoyancy maintenance by
to swim at some speed u. Buoyancy aids siphonophores and other gelatinous zooplank-
may save more energy than I have sug- Blake, ton. Comp. Biochem. Physiol. 66A:467-471.
R. E. 1983. Fish locomotion. Cambridge Uni-
gested, by allowing the animal to stop versity Press, Cambridge.
swimming when it has no need to travel. Bone, W. and B. L. Roberts. 1969. The density of
On the other hand, I have ignored the elasmobranchs. J. Mar. Biol. Assoc. U.K. 49:913-
cost of growing and maintaining buoyancy 937.
aids. If low-density organic compounds are Bowden, K. F. 1964. Turbulence. Oceanogr. Mar.
Biol. 2:11-30.
used, this cost is given by eq. 23. A rough Calder, W. A. 1984. Size, function and life history. Har-
calculation using Calder's (1984) equation vard University Press, Cambridge, Massachu-
for the growth rates of fish of different setts.
sizes suggests that the energy cost of syn- Childress,J.J.andM.Nygaard. 1974. Chemicalcom-
position and buoyancy of midwater crustaceans
thesising a low-density organic compound as function of depth of occurrence off Southern
is likely to be low, compared to the extra California. Mar. Biol. 27:225-238.
cost of swimming with it (eq. 22), except Clarke, M. R., E. J. Denton, andj. B. Gilpin-Brown.
for very sluggish animals. 1979. On the use of ammonium for buoyancy in
squids. J. Mar. Biol. Assoc. U.K. 59:259-276.
Eq. 22 shows that it is generally desirable Denton, E. J. 1974. On buoyancy and the lives of
to use material of the lowest possible den- modern and fossil cephalopods. Proc. Roy. Soc.
sity as a buoyancy aid, so that the volume B 85:273-299.
Vb can be kept small. Gas-filled floats should Eppley, R. W., R. W. Holmes, and J. D. H. Strickland.
be preferable to low-density organic com- 1967. Sinking rates of marine phytoplankton
measured with a fluorometer. J. Exp. Mar. Bio.
pounds which in turn should be preferable Ecol. 1:191-208.
to modified body fluids. However, fish Fenchel, T. 1974. Intrinsic rate of natural increase:
swimbladders change volume as the fish The relationship with body size. Oecologia 14:
swims down to greater pressures or up to 317-326.
smaller ones, and the quantity of gas in the Haury, L. and D. Weihs. 1976. Energetically efficient
swimbladder cannot be changed quickly. swimming behavior of negatively buoyant zoo-
plankton. Limnol. Oceanogr. 21:797-803.
This is probably why many of the lantern Holliday, F. G. T., P. Tytler, and A. H. Young. 1974.
fishes (Myctophidae) that make large daily Activity levels of trout (Salmo trutta) in Airthrey
vertical migrations in the sea have lost the Loch, Stirling, and Loch Leven, Kinross. Proc.
swimbladder and obtain buoyancy from Roy. Soc. Edin. (B) 74:315-331.
wax esters (Alexander, 1972). The gas- Hutchinson, G. E. 1967. A treatise on limnology. Vol.
2. Wiley, New York.
filled shells of cuttlefish and some other Jones, F. R. H. and N. B. Marshall. 1953. The struc-
cephalopods collapse under large pres- ture and functions of the teleost swimbladder.
sures (Denton, 1974) which may explain Biol. Rev. 28:16-83.
why so many deep-sea squid rely on ammo- Magnuson, J. J. 1970. Hydrostatic equilibrium of
niacal body fluids for buoyancy. Consid- Euthynnus affinis, a pelagic teleost without a gas
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Magnuson, J. J. 1973. Comparative study of adap-
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migration by fishes. Symp. Soc. Exp. Biol. 26: O'Dor, R. K. 1988. The forces acting on swimming
273-294. squid. J. Exp. Biol. 137:421-442.
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198 RICHARD R. STRATHMANN
TABLE 1. Comparison of approximate values for air (at
I atm) and sea water at 20"C*
Diffusion
Density Viscosity constant for1 O,
gem"' g-cm"'sec"' em'-sec"
Sea water 1.02 1.1 x lO"2 2 x 10"5
Air 1.20 x 10"' 1.8 x 10"4 2 x 10"'
Water/air 850 60 1/10,000
* The values are approximate and are from Sver-
drupetal. (1942), Gray (1957), and Prosserand Brown
(1961).
greater buoyancy for aquatic organisms.
The viscosity of sea water is about 60 times
the viscosity of air (Table 1), a difference
resulting in much slower sinking rates for
organisms. Desiccation is not a problem in
water but often a problem in air. Water
carries an abundance of dissolved and par-
ticulate materials in solution and suspen-
sion, so that abundant nutrients are acces-
sible to small suspended organisms in water.
Small suspended organisms in air do not
have this access to nutrients.
SOME CONSEQUENCES OF DIFFERENCES
IN PHYSICAL PROPERTIES
The differences in physical properties
make water a much more favorable medium
than air for small planktonic organisms,
and this has caused several peculiarities of
aquatic animals that affect life history evo-
lution.
Small stages in the life histories of aquatic
animals are often planktonic. This includes
gametes, embryos, and larvae of otherwise
benthic animals. Sinking and desiccation
are not problems in water and are prob-
lems in air.
Planktonic larval stages have the evolu-
tionary option of feeding on smaller plank-
tonic organisms. This is not an option in
air, where suspended organic material is
less concentrated.
Abundant suspended food in water has
also affected postlarval traits. Large stages
in the life histories of aquatic animals are
often sessile suspension feeders, a rare con-
dition for animals on land. Many suspen-
sion feeders are colonial forms that consist
of many joined repeats of a body plan; this
modular form of construction is unusual
among terrestrial animals though common
for terrestrial plants.
Thus water directly and indirectly favors
both planktonic and sessile habits to a much
greater extent than does air and thereby
produces different conditions for mating
and dispersal.
There is another physical difference
between water and air that may encourage
the scattering of small aquatic offspring.
The diffusion constant of oxygen and many
other molecules in air is about 10,000 times
the diffusion constant in water (Table 1).
Although desiccation of a mass of embryos
can be a problem in air, diffusive supply of
oxygen into a mass of embryos should be
much more rapid in air. Interstitial flow
through a mass of embryos is also retarded
in water because of higher viscosity. The
lower diffusion constant in water and
higher viscosity of water may limit parental
protection of benthic clutches of embryos
and thereby reinforce the evolution of
planktonic embryos and larvae.
These differences in physical properties
of air and water are not the only differ-
ences that might underly different evolu-
tion of life histories, but they are major
ones. The following discussion examines
effects of these differences on mating,
parental protection, dispersal, and their
evolutionary consequences.
MATING
The most striking difference between
aquatic and terrestrial mating is that aquatic
organisms commonly shed female gametes
as well as male gametes. Terrestrial organ-
isms retain female gametes on or in their
bodies. However, the evolutionary conse-
quences of shedding female gametes are
not so striking. When female gametes are
shed, sexual dimorphism is minimal and
male and female gonads are nearly equal
in size, but many terrestrial animals also
show little sexual dimorphism despite cop-
ulation or transfer of spermatophores.
Multiple paternity is another likely conse-
quence of shedding female gametes, but
wind-pollinated plants must be at least as
open to multiple paternity (for example,
Schoen and Stewart, 1986). Although
 EVOLUTION OF LIFE HISTORIES IN THE SEA
shedding of female gametes is distinctively
aquatic, distinctively aquatic evolutionary
consequences are not yet proven.
Dilution of gametes may have conse-
quences that are not yet recognized.
Though water is a benign medium for
gametes, external fertilization is by no
means easy. There is no evidence that dis-
persal of gametes in the sea exceeds dis-
persal of pollen on land. Fertilization by
distant males and females is limited by the
life span of active sperm, predation on
gametes, and dilution of gametes with dilu-
tion probably the greatest obstacle. Pen-
nington (1985) found rapid decreases in
capacity for fertilization downstream from
spawning male sea urchins. In his assay,
percent fertilization decreased to about
20% at 1 m downstream from a single
spawning male even in a slow current. His
simple field experiment suggests that time
and place of free spawning is important in
achieving paternity. Denny (1988) reached
similar conclusions with a diffusion model
and laboratory data. Levitan (1988) argues
that for some free-spawners the high fer-
tilization success in crowded populations
offsets the reduced fecundity from resource
limitation. Under Levitan's hypothesis, it
seems possible that a female that sought
crowded conditions that limited her size
and fecundity could leave more offspring.
Even in less extreme circumstances, a
female would do well to wait until there is
much sperm in the water, and this con-
fronts males with strategic problems that
are not well understood. In many species,
females are induced to spawn by spawning
males; a male that spawns with other males
may therefore be more likely to put his
sperm where the ova are, but he also
encounters greater competition from other
sperm. Though the situation resembles
some group mating displays by terrestrial
males, one would expect there to be less
female choice, more opportunity for mul-
tiple paternity of a clutch, and less pre-
mating competition among males.
Given the difficulties of ensuring contact
between sperm and ovum in suspension, it
is not surprising that a number of devices
for bringing sperm to ova have evolved.
199
Paired mating by copulation, spermato-
phores, or simply paired free-spawning has
evolved many times in marine animals.
Some aquatic sperm transfer resembles
terrestrial sperm transfer, but many aquatic
animals are sedentary or completely sessile,
and for these sperm transfer presents
unusual problems that have been met with
curious solutions, not fully analogous with
either pollen transfer in terrestrial plants
or sperm transfer by terrestrial animals.
One solution to the problem of sperm
transfer is the water born spermatophore.
Water born spermatophores are common
among sessile suspension feeders, presum-
ably because suspension feeding sessile ani-
mals cannot move to mate but are well
equipped to intercept objects from a large
volume of water (Hadfield and Hopper,
1980). Examples of the independent evo-
lution of spermatophores in animals of this
type include some oysters (Coe, 1931),
pogonophorans (Webb, 1963), phoronids
(Zimmer, 1967), vermetid gastropods
(Hadfield and Hopper, 1980), and spionid
polychaetes (Rice, 1980).
Terrestrial organisms have spermato-
phores, but methods of transfer are differ-
ent even in the closest analogues to water
dispersed spermatophores. Some plants,
such as milkweeds (Bookman, 1981), pack-
age many pollen grains into pollinia, but
these are transferred by insects. To my
knowledge, windborn pollen grains are not
combined in large packets. Some arachnids
(Thomas and Zeh, 1984) and amphibians
(Halliday and Verrell, 1984) deposit sper-
matophores on the ground, but transfer
depends on motility of females, and this
mode of transfer depends on moist habi-
tats.
Water born spermatophores of solitary
benthic animals potentially could combine
passive dispersal of spermatophores with
single paternity for a clutch of eggs. Single
paternity of clutches fertilized by water
born spermatophores is not inevitable,
however. In the vermetid gastropod Ser-
pulorbis squamigerus, the males produce
sperm over a longer period than the females
produce eggs; the females store sperm; and
the frnales might therefore store sperm
200 RICHARD R. STRATHMANN

TABLE 2. cially severe in water, but visibility is poor

Some distinctively aquatic types of mating.

Type of mating Aquatic Terrestrial

in many waters and may limit the effec-
tiveness of offering advertised rewards to
Female gametes shed common absent pollinators.
Passively dispersed sper-
matophores with poten- In summary, release of female gametes
tial for single paternity common absent? before fertilization, passive dispersal of
Sessile copulators common rare spermatophores capable of fertilizing all
By pollinators absent common ova of a female, and copulation between
sessile organisms are common traits for
aquatic animals but rare among terrestrial
from several spermatophores (Hadfield, animals and plants (Table 2). Transfer of
1967). Nevertheless, single paternity male gametes by an animal that receives a
appears to be likely in some other benthic reward is common among terrestrial plants
marine animals with spermatophores, and but absent among marine organisms.
the combination of single paternity for an
entire clutch and passive dispersal of male PARENTAL INVESTMENT PER OFFSPRING
gametes by the ambient fluid may be com- To my knowledge, minimal parental
mon in water for animals though rare or investment per offspring is generally lower
absent on land for both animals and plants. for free-living aquatic animals than for free-
Most thoracican barnacles are outcross- living terrestrial animals or terrestrial
ing hermaphrodites whose penises can plants with seeds. Propagule sizes between
reach farther than their body length. Opti- 50 and 100 fim occur among bivalves, opis-
mal male allocation involves not only den- thobranchs, polychaetes, ectoprocts, pho-
sity of neighbors (Charnov, 1987) but ronids, and echinoids that begin feeding as
potentially such factors as risk of losing a larvae (Silen, 1954; Strathmann and Ved-
penis to a predator. What is unusual in bar- der, 1977; Emlet et al., 1987; McEdward
nacles is the combination of a plant-like and Strathmann, 1987). The energy con-
sessile habit with the active copulation of tent of eggs less than 100 (im in diameter
animals. has been estimated to be about 0.003 joules
Given the sessile habit of many marine of energy or less for some of these animals.
animals and plants and the difficulties in The data tabulated by Anderson (1972)
mating with distant neighbors, it is sur- suggest that free-living terrestrial insects
prising that there are no known marine have eggs larger than 100 /im in smallest
analogues of pollinators. There are two dimension, and this seems to be the rule
obvious hypotheses for the absence of for most externally deposited eggs of free-
marine pollinators but neither has been living terrestrial animals whose adults are
investigated. (1) For a given added invest- several millimeters or more in length.
ment in energy or materials, passive dis- (Minute metazoans tend to have small eggs
persal of more gametes may provide more wherever they live.) When minimum
fertilizations than a reward for pollinators parental investment per offspring is lower,
that carry male gametes. Water is a more maximum fecundity per reproductive allo-7
favorable medium than air for passive cation is higher. Fecundities exceeding 10
transport of male gametes. Also if pro- are common among free-living aquatic ani-
spective pollinators have access to better mals but uncommon for terrestrial ani-
alternative sources of food in aquatic hab- mals.
itats than in terrestrial habitats, higher When we include plants, however, the
rewards to pollinators might be required aquatic-terrestrial contrast is not so great.
in aquatic habitats (as suggested by L. Plant spores, whether terrestrial or aquatic,
Hickey, personal communication). (2) Costs can be much smaller than propagules of
to pollinators might be greater in water so free-living animals. Fungi release propa-
that the necessary rewards might be greater gules to the air that are on the order of 10
in water than in air. Costs of locomotion Mm diameter (Ingold, 1971) and thus orders
or risks during a search may not be espe- of magnitude smaller in volume or weight
 EVOLUTION OF LIFE HISTORIES IN THE SEA
TABLE 3. Differences between marine and terrestrial dispersal.
Characteristics of dispersal
Obligate with reproduction
Fortuitous consequence of feeding larvae or shed ova
Must pass good sites without settling
Characteristics of dispersal
Propagule adapted for dispersal
Growth during dispersal
Actively leaves bad substrata
than any propagules released into the water
by aquatic animals. Seeds of vascular plants
tend to be larger than freely spawned eggs
of aquatic animals, though the smallest
seeds of orchids and some other vascular
plants with saprophytic germlings are
reduced to a little more than 100 /*m in
size (Salisbury, 1942; Ingold, 1971; Har-
per, 1977).
Several factors could contribute to the
generally larger sizes of propagules for free-
living animals in air. The abundance of
small food in water permits initiation of
feeding at minute sizes and desiccation is
not a problem. However, the problem of
desiccation is avoided by many aerial prop-
agules that remain in a dry and inactive
phase until they encounter a moist site. The
advantages of minimizing parental invest-
ment per offspring are obvious; more off-
spring can be produced. The limits on low
parental investment per offspring are less
obvious because they are affected by
numerous factors: risks from predators,
competitors, and the physical environment
on the one hand and methods of nutrient
uptake and rates of growth of offspring on
the other.
ADULT SIZE AND BROODING
For many taxa of aquatic animals, species
with small adults are commonly brooders
with embryos held on or in the adult body,
but in species with larger adults, there is
no care for offspring or offspring are
released at an earlier stage (Table 4). The
trend can be found within a class or even
within a genus. Not all taxa of aquatic ani-
mals show this trend. It is unreported and
unapparent in crustaceans. I know of only
one report of the opposite trend: among
201
Marine larvae Terrestrial animals
common rare
common absent or rare
common rare?
Marine larvae Terrestrial seeds
no? common
common no
common no
gastropods of the genus Margarites in the
North Pacific a species with the largest
adults is an umbilical brooder (Lindberg
and Doberteen, 1981). Thus brooding is
size dependent in many taxa of aquatic ani-
mals, and the smaller adults provide pro-
tection to more advanced stages. A result
of size-dependent brooding is that dis-
persal of embryos and larvae of closely
related aquatic animals can range from
none to tens of kilometers. I have found
no reference to decreased parental care by
larger adults in terrestrial organisms and
provisionally conclude that this pattern is
rare or absent in air. I also know of no
analogy to this trend in either terrestrial
or aquatic plants.
There are several possible reasons for
the association of large adult size with less
brooding in aquatic animals (Strathmann
and Strathmann, 1982). Only one of these
hypotheses directly involves the physical
properties of water. In comparisons both
within and between species, larger individ-
uals usually have larger clutches. The low
diffusion constant and high viscosity of
water (Table 1) may limit gas exchange for
embryos near the center of large clutches
(Strathmann and Chaffee, 1984). How-
ever, all the hypotheses for less brooding
by larger adults indirectly involve the phys-
ical properties of water; it is because water
is a benign medium for small planktonic
animals that large aquatic adults can release
embryos or larvae into the surrounding
fluid. The common inverse correlation
between adult size and brooding in many
aquatic animals appears to result from an
alternative to brooding in aquatic habitats.
This alternative is more costly or absent in
air.
202 RICHARD R. STRATHMANN

TABLE 4. The association of small adult size with brood- but releases potentially long-lived larvae
ing in marine animals.* (Richmond, 1987). Thus for aquatic ani-
Taxon Source mals, modular construction is associated
Polychaeta, Sabellida Knight-Jones and Bowden
with increased brooding after fertilization
(1984) and decreased dispersal of planktonic
Bivalvia Sastry (1979) propagules.
Veneridae Sellmer (1967) The example of ascidians is instructive
Ostraeidae Sellmer(1967) because the module size is smaller in the
Gastropoda, Crepidula Gallardo (1977), Hoagland
(1977)
colonial than in the solitary forms, but the
Polyplacophora Pearse (1979), Creese and amount of tissue of one genotype and its
O'Neill (1987) longevity can be at least as great in colonial
Lepidochitona D. J. Eernisse(1988) forms as in solitary forms. Thus the cor-
Cephalopoda, Octopus Green (1973) relation between adult size and genet size
Brachiopoda, Articu- Reed (1987), C. Thayer that occurs among solitary forms of ben-
lata (personal communica-
tion) thic animals breaks down in comparisons
Ophiuroidea Hendler and Littman that include both solitary and colonial as-
(1986) cidians. Several causes for the association
Asteroidea Chia(1968) of modular construction and brooding have
Asteriidae Menge(1975)
Asterinidae Dartnall (1968, 1971)
been suggested (Strathmann and Strath-
Emson and Crump (1979) mann, 1982; Jackson, 1986; Grosberg,
Holothuroidea 1987). A general hypothesis for the rela-
Cucumariidae Menge(1975) tion between module size and brooding is
Synaptidae unpublished review of lit- that smaller modules provide more surface
erature for brooded clutches of embryos. Some
Fishes of coral reefs Barlow (1981) hypotheses are peculiar to coloniality: col-
;
Crustaceans are notable by their absence. onies might commonly allocate more to
growth and less to dispersing propagules
than do solitary forms, and thus have more
MODULAR CONSTRUCTION AND space for brooding; or colonies might ben-
BROODING efit more from settling and growing in
Brooding is common among colonial proximity to kin. Whatever the causes, this
animals that are composed of many small is another association of life history traits
modules (Strathmann and Strathmann, that appears to be peculiar to aquatic ani-
1982; Jackson, 1986). Animals with mod- mals in contrast to terrestrial animals or
ular construction include bryozoans, terrestrial plants. Also, the degree to which
pterobranch hemichordates, compound terrestrial plants are modular does not
ascidians, and several kinds of hard corals appear to be correlated with the distances
and soft corals. The ascidians provide the over which seeds are dispersed, whether
strongest correlation between brooding modular construction is defined in terms
and modular construction because almost of branches or ramets.
all colonial ascidians brood and most soli-
tary ascidians spawn gametes into the sur- LARVAL DISPERSAL
rounding water. The scleractinian corals Dispersal of terrestrial animals and plants
provide the most vexing exception to this contrasts with dispersal of benthic marine
correlation because many do not brood, animals with planktonic feeding larvae. It
and there is no apparent relation between makes sense for mobile organisms to dis-
polyp size and brooding (for example, perse when cues indicate that conditions
Szmant, 1986). Larval offspring of brood- are likely to be better elsewhere and stop
ing colonies typically disperse for very short moving when they reach a place where
distances (van Duyl et ah, 1981; Olson, conditions are likely to be better than they
1985; Jackson, 1986; Grosberg, 1987), are elsewhere. This pattern of dispersal is
though there can be exceptions as in the very common for mobile animals on land
coral Pocillopora damicornis, which broods or in the sea but is not the pattern for a
 EVOLUTION OF LIFE HISTORIES IN THE SEA
great many sedentary benthic marine ani-
mals (Table 3). (1) Dispersal of marine lar-
vae is obligate with sexual reproduction.
For many marine animals this is the only
form of reproduction and not a response
to poor conditions. (2) Passive transport of
planktonic feeding larvae can carry off-
spring far beyond any advantageous dis-
persal distances or favorable habitats. Such
extensive transport is common because with
most feeding larvae there is an obligate
period of growth before the larvae become
competent to settle. Though marine dis-
persal can be over enormous distances, with
some feeding larvae crossing oceans
(Scheltema, 1977), models of spreading risk
by dispersal indicate diminishing returns
or increasing costs from dispersal in envi-
ronments with plausible patterns of vari-
ation (Palmer and Strathmann, 1981). Even
without a feeding larva there can be an
obligate dispersal period; when ova are shed
into the plankton, there is typically more
than a day of planktonic development
before competence for settlement. (3) Dis-
persal of marine larvae may be a byproduct
of putting propagules in the plankton for
feeding or safety. Most feeding larval stages
of benthic marine animals develop in the
plankton rather than on the bottom, pos-
sibly because a small unprotected animal is
safer in the plankton than on the bottom
(Strathmann, 1982). In marine species in
which embryos are protected in benthic
broods or egg masses, larvae are not
released into the plankton until they are
capable of feeding or nearly competent to
settle. In the latter case, planktonic periods
are short and dispersal usually quite lim-
ited. Thus the obligate dispersal occurring
during the precompetent larval period may
be an accidental byproduct of a migration
of offspring into the plankton for safety or
acquisition of food (Strathmann, 1982,
1985).
It is tempting to compare dispersal of
seeds of terrestrial plants and dispersal of
larvae of sessile marine animals because
both are sessile as adults and both have
passively dispersed propagules, but the
analogy between seed dispersal and larval
dispersal fails in at least three ways (Table
3). (1) Among benthic marine species in
203
similar conditions, duration of the larval
phase is correlated with the amount of lar-
val growth so that in general the larvae that
grow the most also disperse the most. Seeds
in air do not grow during dispersal. To my
knowledge, the seeds that germinate and
grow during dispersal are aquatic seeds, as
in mangroves. (2) In contrast to many
widely dispersed seeds of terrestrial plants,
the marine larvae that disperse the most
(feeding forms) have no structures that are
specifically for dispersal. The larval struc-
tures consist mostly of devices for feeding,
defense, and (in competent stages) habitat
selection. Other than initial upward swim-
ming, special adaptations for larval dis-
persal are not apparent, and many marine
species with planktonic adults have larvae
similar to the dispersing larvae in species
with sedentary benthic adults (Strath-
mann, 1985). In contrast, terrestrial fruits
or seeds commonly have special devices
whose only known function is to enhance
dispersal (Harper, 1977). (3) Marine larvae
possess some capacity to move from a poor
habitat. Seeds can abstain from germina-
tion but movement to a new position is
beyond their control.
DISPERSAL OF AQUATIC ANIMALS
THAT ARE N O T MARINE
Feeding planktonic larvae have been
eliminated from the life histories of most
marine animals that have invaded fresh-
water. Non-marine aquatic animals com-
monly have a dispersal or resting phase in
their life history that is adapted to dry con-
ditions; such a desiccation resistant phase
is rare among marine animals. Desiccation
resistant phases include many types of cysts,
unhatched embryos, and other inactive
stages (Hutchinson, 1967; Pennak, 1978)
as well as the flying adults of many insects
with aquatic larvae (Usinger, 1956; Cheng,
1976).
Possession of a stage that can withstand
a period in air suggests that an aerial dis-
persal route is advantageous for many non-
marine aquatic organisms. Lakes and ponds
are isolated and ephemeral (Hutchinson,
1957), whereas marine habitats are per-
manently connected by large expanses of
water (Schopf, 1980; Tchernia, 1980). In
204 RICHARD R. STRATHMANN
TABLE 5. Potential consequences of decreased planktonic
larval period for benthic animals.
More regular recruitment, less irregular year
classes
Decreased dispersal
Less genetic variation within populations
More genetic variation between populations
Adaptation to more local conditions
More inbreeding
More simultaneous hermaphrodites
More interaction among kin
More speciation
More extinctions
Shorter geographic ranges
persistent systems of streams passive dis-
persal is overwhelmingly downstream,
whereas marine habitats are better con-
nected by multi-directional water routes.
It appears that marine organisms can be
more fully aquatic than many other aquatic
organisms and that this affects the way they
disperse.
EVOLUTIONARY CONSEQUENCES AND
CORRELATIONS OF MODE OF
DEVELOPMENT
Do aquatic life history traits have inter-
esting and peculiarly aquatic evolutionary
consequences? Evolutionary correlates of
larval dispersal suggest that the answer is
yes. We should expect some peculiarly
marine evolutionary patterns that arise
from peculiarly marine patterns of life his-
tory traits.
For species with sedentary adults, larval
dispersal is reported to have numerous and
partly related evolutionary consequences
(Table 5). Duration of the planktonic larval
period potentially affects regularity of
recruitment to the adult population (Thor-
son, 1946; Ebert, 1983), genetic variation
within and among sites (Berger, 1973; Bur-
ton, 1983; Eernisse, 1984; Buroker, 1985;
Waples and Rosenblatt, 1987), adaptation
to local conditions (Crisp, 1978; Strath-
mann, 1982; Vermeij, 1982; Ayre, 1985),
inbreeding and interaction with kin (Jack-
son, 1986; Grosberg and Quinn, 1986;
Grosberg, 1987), inbreeding or outbreed-
ing depression (Grosberg, 1987); the evo-
lution of hermaphrodites (Heath, 1977;
Strathmann et ai, 1984), geographic range,
speciation, and extinction (Powell, 1942;
Shuto, 1974; Scheltema, 1977; Hansen,
1980; Perron and Kohn, 1985; Jablonski,
At this stage of marine evolutionary
studies some qualifications must be added.
Good comparative data are few. Larval dis-
persal is not the only mode of dispersal.
Some animals are frequently rafted to other
sites (Jokiel, 1984; Highsmith, 1985; Jack-
son, 1986), and dispersal of sperm may
contribute to gene flow (R. Grosberg, per-
sonal communication). Dispersal is not the
only determinant of gene flow, and gene
flow is not the only determinant of cohe-
sion or divergence of populations (Berger,
1977; Burton, 1983; Hedgecock, 1986).
Obligate dispersal is not favorable to col-
onization because descendants cannot be
retained at favorable sites once they have
been reached (Strathmann, 1974). Geo-
graphic range is not correlated with extent
of larval dispersal in all faunas (D. Lind-
berg and M. Russell, personal communi-
cation), and species durations are con-
founded with species geographic ranges
(Russell and Lindberg, 1988). Neverthe-
less, duration of the planktonic larval stage
is the primary determinant of dispersal for
many sedentary marine animals. Extensive
larval dispersal is common among marine
animals and unusual elsewhere, and even
more peculiar to marine animals is the
extreme variation in scale of dispersal of
closely related animals with its varied evo-
lutionary consequences. Winged and wing-
less insects could be considered a terres-
trial analogue, but wings do not appear to
have such a large effect on dispersal and
gene flow in carabids (Liebherr, 1988), and
I do not know what patterns have been
found for other families that include
winged and wingless species. Modes of
development of benthic marine animals and
their evolutionary consequences appear to
differ from those common among terres-
trial or freshwater organisms.
A peculiarly marine evolutionary pat-
tern may arise from the correlation
between adult size and brooding. Brooding
and a shorter planktonic larval period are
associated with small adult size (Table 4)
within a number of taxa of marine animals.
 EVOLUTION OF LIFE HISTORIES IN THE SEA
This association may connect otherwise
unrelated traits. Among closely related
species, larger adult size is commonly cor-
related with greater age at maturation,
greater longevity, more bouts of repro-
duction, and greater fecundity (Strath-
mann and Strathmann, 1982). Adult size
also affects interspecies interactions
(Menge, 1975). All the consequences listed
in Table 5 have not followed every time
that small adult size has evolved, but small
adult size and its correlates are connected
to evolutionary trends in a manner that
appears to be peculiar to marine animals.
A very short planktonic period is also
common among colonial benthic animals
with modular construction and here also
there are consequences for gene flow,
inbreeding, and interactions among kin.
Coloniality can also result in indefinite
growth and longevity and in reduced allo-
cation to reproduction (Jackson el al., 1985;
Harvell and Grosberg, 1988). Here again,
a peculiarly marine correlation between
adult and larval traits may connect traits
that would otherwise be unassociated or
related in quite different ways.
Available evidence suggests that there
are peculiarly marine evolutionary pat-
terns that arise from peculiarly marine life
history traits, and that these life history
traits have resulted in large part from the
different physical properties of air and
water.
ACKNOWLEDGMENTS
NSF grant OCE8606850 supported this Dartnall, A. J. 1971. Australian sea stars of the genus
study at the Friday Harbor Laboratories
and at the library of the Marine Biological
Association. J. F. Ammirati, J. Bergdahl, Denny,
W. T. Edmondson, J. S. Edwards, R. K.
Grosberg, L. Hickey, R. Kaufman, R. H. Ebert, T. S. 1983. Recruitment in echinoderms.
Laushman, G. M. Odell, C. Petersen, J.
Truman, and others answered some of my Eernisse, D.J. 1984. Lepidochilona Gray, 1821 (Mol-
questions about life on land.
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