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REPRODUCTIVE AND LARVAL ECOLOGY OF MARINE

BOTTOM INVERTEBRATES
BY GUNNAR THORSON
Zoological Museum, University of Copenhagen
(Received 15 Febwmy 1949)

CONTENTS
PAGE
I. Introduction . . . . . . . . . . . . . . I
11. Waste of eggs and larvae during development . . . . . . . . 3
111. Spawningand fertilization . . . . . . . . . . . 6
IV. Types of larval development . . . . . . . . . . . 8
V. .
Sources of waste during pelagic life . . . . . . . . . I2
( I ) Food conditions . . . . . . . . . . . . I3
(2) Temperature conditions . . . . . . . . . . . I5
(3) Metamorphosis . . . . . . . . . . . . 16
(4) Transport by currents from shelf to deep sea . . . . . . . 18
( 5 ) Enemies . . . . . . . . . . . . . . 19
.
VI. Geographical distribution and mode of development . . . . . . zx
( I ) Asexual reproduction . . . . . . . . . . . 21
(2) Sexual reproduction . . . . . . . . . . . 22

VII. Species able to vary their mode of reproduction . . . . . . . zg


VIII. The shell apex theory . . . . . . . . . . . . 33
IX. Summary. . . . . . . . . . . . . . . 35
X. References . . . . . . . . . . . . . . 38

I. INTRODUCTION
The method most commonly used in studies of the ecological relations of a marine
animal is to indicate the quantitative or the geographical occurrence of the animal on
a map, and then, from own observations, hydrographical tables, etc., to construct
a picture of the amplitudes, respectively average values, of temperature, salinity,
substratum, etc., within the area in which the animal occurs. Such studies are helpful
if we want to gain some knowledge of the conditions prevailing within the area where
the particular animal lives, and will be a valuable help to such people as scientists
working on applied biology, and fishermen who wish to know in what kind of
localities they are to look for the animals desired. If, however, we want to get a
fundamental knowledge of the factors which enable the animals to maintain their
population within a certain sea-area, the method outlined above is far from satisfactory.
It has often been pointed out that for our purpose average values of ecological
factors, such as temperature, salinity, substratum or amount of food, are of little
interest; we do not want to know the average temperature, but the limiting tempera-
ture, which will most probably prove to be found among the highest, or the lowest
B R XXV I
2 G. THORSON
temperatures within the area. While most modem marine ecologists are aware of
this fact, it is often overlooked that similar aspects have to be considered concerning
the animals examined. Ecological studies on an average population will not give US
the fundamental information we want, because such a population may comprise
quite young animals, older but immature, and old mature animals, and because the
environmental requirements of these various stages may be, and for several species
are known to be, quite different-for the mature animals even different within and
outside the breeding season.
But if, on analysing the ecological factors, we consider the limiting values, not the
average values, on analysing an animal population we have to focus our attention
upon the most sensitive stages within the life cycle of the animal. These stages-the
weakest link of the chain--will normally be found during the breeding period and
larval development, when the requirements of the organisms from the environment
are often much more definite than during the other periods of their life cycle.
Examples :
( I ) Temperature. Marine invertebrates require very definite and normally much
higher temperatures to ripen and spawn their sexual products than are necessary for
them outside this season (Orton, 1920); young cleavage stages need more precise
and limited temperature intervals than older larvae and bottom stages (Pelseneer,
1901; S. Runnstrom, 1 9 2 7 ~ ) .Off den Helder, Holland, it was found that the
decapods Cancerpagurus, Crangon crangon (both down to depths of 30 m.), Portunus
holsatus and Carcinus mamas were able to survive the heavy ice of the winter of 1947,
while the eggs attached to their pleopods were killed (unpublished information from
Dr Venvey and Dr Kristensen).
( 2 ) Salinity. For Crangon crangon 'the salinity range available for the normal
development of the eggs only covers the upper part of the salinity range in which
full-grown animals are able to live' (Broekema, 1941,p. 45). Spermatozoa of echino-
derms require a rather high salinity and a fairly high pH to be active, much higher
values than are required by the adult animals (Mortensen, 1921, 1937, 1938;
Horstadius, 1925).
(3) Amount of food. The food requirements of invertebrate larvae seem on the
average to be 5-10 times higher than those of their parents at the bottom (Zeuthen,
I 947). On certain occasions a dense accumulation of phytoplankton seems necessary
to start the spawning of a whole stock of invertebrates (Miyazaki, 1938; Thorson,
'936, '946)-
Corresponding to these various claims on the environment, many marine inverte-
brates undertake migrations during their breeding season. This is the case with
invertebrates which totally change their habitat at the time of breeding, e.g. Eriocheir
sinennsis (Panning, 1937); or such species as only breed within a smaller part of the
geographical area in which they regularly occur, e.g. Loligo vuulgaris (Tinbergen &
Verwey, 1945). It also applies to animals which, during their breeding season,
migrate within their area of occurrence, from deeper water to the tidal zone, e.g.
Echinus esculentus (Stott, 193I), Coscinasterias tenuispina (Crozier, 1920), the proso-
Reproductive and larval ecology of invertebrates 3
branchs Lacuna pallidula (Pelseneer, 1902), Lamellaria l a t m (Peach, I 858), and
Ilyanussa obsoleta (Batchelder, I ~ I S ) the
, nudibranch Trevelyana clocea (Eliot, 1904),
several Aeolidae and Doridae (Sauvage, 1873, p. 27), and the crabs Tachypleusgigas
(Mohr, 1941), Maia squinado, and Corystes cassivelaunus (Duncan, 1946, p. 139), or
from the tidal zone to deeper water, e.g. Leptasterias aequalis, the prosobranch
Nucella ( =Acanthina) lapilloides (Hewatt, 1937), and Cancer pagurus (Williamson,
I 900).
Thus, the conditions of breeding and larval development constitute a very essential
point for all studies of the reproduction and fundamental ecology of marine bottom
invertebrates. Within this critical period the waste takes place which determines
whether or not an animal stock will be able to maintain itself.

11. WASTE OF EGGS A N D LARVAE DURING DEVELOPMENT


The next point to be discussed here is the extent of the waste of eggs and larvae,
and its causes. The quantity of eggs and larvae produced by the bottom invertebrates
within a given area of the sea varies considerably from species to species. In spite of
these differences in the number of eggs all the species that constantly occur in an
area during a long period of years recruit their stock on a sufficiently large scale to
maintain the population. The only claim that can be made to the number of eggs
and larvae produced per pair of adult animals per lifetime to maintain the population
is that, on an average, one pair of larvae will reach the stage of fertility and spawning.
Thus it may be concluded that species with a large number of eggs have a larger
wastage of eggs and larvae than those with only a few eggs. A study of the egg
numbers of different species may accordingly give us good hints as to the toll levied
under different conditions and in different types of development.
If we compare the egg numbers of free-living, non-parasitic invertebrates from
land and sea, it is obvious that the average numbers of eggs produced are very small
in the terrestrial as compared with the marine species. While most species of ter-
restrial invertebrates produce from a few hundred to a few thousand eggs, at the
most, most marine species will produce from several thousands to some millions of
eggs per female per lifetime. Even in those species which are viviparous, ovovivi-
parous or oviparous with large yolky eggs, the number of eggs produced by the
marine species seems to surpass by far that of the terrestrial ones. Also the species
living in fresh water generally produce much smaller numbers of eggs than the
marine ones. Thus the waste of eggs and embryos of invertebrates in the sea is much
larger than on the land and in fresh water. But also the quantities of eggs in marine
animals vary considerably from species to species.
The diagram in Fig. I , giving the average number of eggs spawned by marine
bottom invertebrates (echinoderms, nemerteans, polychaetes, prosobranchs, tecti-
branchs and decapods) with different types of development, clearly shows that all
species which produce a really large number of eggs have a long planktotrophic
pelagic larval life, during which, accordingly, a huge waste takes place. Fig. I ,
however, shows also that within species with planktotrophic larvae the egg number
1-2
4 G. THORSON
varies astonishingly from one kind of animal to another (from 1100to ~oo,ooo,ooo
eggs), and observations in Danish seas enable us to state that the waste also varies
very much from year to year within the individual species. Fig. 2 shows the rather
constant populations at the bottom from year to year of those animals which have

t
..*
V

Species with vlvi-


-
Specks with large Species with small
parity or a high eggs or a primi- eggs and a long
degree of brood- tivetypeofbrood- pelagic plankto-
protectlon. Non- protection. Non- trophic larval life
pelagic develop. pelagic develop.
ment ment

Fig. I . The number of eggs produced per female per breeding season of marine bottom invertebrates
(echinoderms, nemerteans, polychaetes, prosobranchs,tectibranchs, and decapods) with different
types of development.

a very short pelagic life (Nucula nitida) or a non-pelagic development (Macoma


catarea), as compared with the fluctuating populations of animals (Cultellus,
Abra, Corbula) in which the larvae have a long planktotrophic pelagic life. The
biologist who attempts to estimate the number of fish-food animals present within
a certain bottom area has therefore to focus his attention on the mode of development
of these animals. The species reproducing without a long pelagic planktotrophic
Reproductive and larval ecology of invertebrates 5

280
-8
240- i
- !
200
- , i
- Weight in g. per sq.m. bottom in Sallingsund
160
- : (the Limfjord) during 1918-26
- - *

120 -

80 - \

Weight in g. per sqm. bottom off the north


coast of Fyn during 1918-24
80

t.
::
60
' i
: t

Weight in g. per sqm. bottom In Nissum


400 - Bredning (the Limfjord) during 1910-24
360 - +
320
280
-- it
i -*.
: + ,
I
,<
,

240 - pi \&
200 -
160 - *.; !
120 -
, I

::
: \ * *3

80 -
,A Corbulo gibbo (long pelagic larval Ilfe)

f
i
:
40 -,-A-.--
.-.--- --&.tm -%*-.-,-.-Nuculo
p+*A-+-+..+4r
+=.+.+.
;
. nitido (very short pelaglc life)
t

Fig. 2. Variations from year to year in a stock of bottom invertebrates in Danish waters recruited
partially by larvae with a long planktotrophic pelagic life, partially by larvae with a very short
pelagic life or a non-pelagic development (from Thorson, 1946).
6 G . THORSON
larval life will occur in nearly the same number from year to year, and form a solid
basis for a calculation of minimum conditions for fish production, while the species
reproducing with pelagic planktotrophic larvae may vary so much in number from
year to year that no calculations can be based upon them (Thorson, 1946). As,
further, the extremely varying number of adults at the bottom is responsible for the
production of eggs and larvae the next year (Korringa, 1947),calculations will be
even more uncertain.
The fluctuations of marine invertebrates with a long planktotrophic larval life are
of such a character that they are, no doubt, due to a combination of several ecological
factors, and since species reproducing in this way constitute at least 70% of all
marine invertebrates in Recent seas, it seems worth while to study in detail the waste
of pelagic larvae and the conditions causing them.
111. SPAWNING AND FERTILIZATION
Copulation, found in the polychaete Capitella, all the higher prosobranchs, all
opisthobranchs, cephalopods, and most crustaceans, is the most certain method of
fertilization. In the genital duct of the female the activity of the spermatozoa may
be stimulated and they will have a good chance of finding an egg of their own species,
and so of accomplishing a roo% fertilization. Further, the eggs inseminated inside
the maternal animal may, by viviparity, internal brood protection, or covered by a
capsule or a gelatinous mass, be protected against infections by infusoria and bacteria,
or attacks by enemies during their development; while eggs fertilized when drifting
freely in the water must be spawned in a state which allows the spermatozoa and
accordingly infusoria and bacteria to attack them.
Several marine invertebrates without copulatory organs have a ‘pseudo-copula-
tion’, which gives nearly all the advantages known in the real copulation. In the
nemerteans Amphiporus and Lineus the male and female secrete a common mass of
slime, and embedded in this, spawn their eggs and sperm. No sperm is lost, and the
eggs are laid in the slime, protected from enemies. Such ‘pseudo-copulation’ is also
known in the nemerteans Carcinonemertes (Coe, 1902,1943,p. 265), and Micrura
alaskensis (up to fifty specimens spawning together in a common slime coil, Coe,
I~OI),and in the polychaetes, Nereis diwersicolor (several females coiled around one
male, Dehorne, I ~ Z S ) Scolecolepis
, fu&inosa (several spawning in a common mass of
slime, Claparkde & Metschnikoff, 1869), and Nicolea zostericola (male spawning
between the tentacles of the spawning female, Herpin, 1925).
Species shedding their eggs freely in the water seem also to economize their
spermatozoa. Several cases are known in which a male and a female with this mode
of spawning will not shed their sexual products unless they are quite close to one
other, e.g. the actinian Sagartia troglodytes (Nyholm, 1943),the prosobranchs
Patella coerulea and P . lusitanica (v. Medem, 1942), Helcion pellucidurn (Ankel,
1936), Gibbula tumida (Gersch, 1936), and Ckznculus bmthelothi (unpublished),
and the echinoid Toxopneustes oariegatus (Tennent, 1910).
However, large numbers of marine invertebrates, including most Actinozoa,
Reproductive and larval ecology of invertebrates 7
several Polychaeta, nearly all Echinodermata, Placophora, and Lamellibranchiata
and the most primitive genera of the Prosobranchiata, spawn their eggs and sperm
freely in the water, where the fertilization takes place without the males and females
approaching each other. Thus, large quantities of sperm widely dispersed in the
water masses may be assumed to perish before meeting any eggs of their species,
and eggs dispersed by the movements of the water, seem to have a poor chance of
meeting spermatozoa of their own species within the relatively short period in which
they can be fertilized (e.g. 2k12 hr. in Echinus esculentus (Carter, 1931),2 days in
Arbaciapunctuluta (Loeb & Lewis, I ~ O I 3) ,days in Urechis caupo (Whitaker, 1937),
and less than 4 hr. for several other eggs). This, in addition to the fact that a low
salinity and a low pH often occur in shallow coastal areas where fresh water flows
out, and may make the spermatozoa inactive (Mortensen, 19204 1937, 1938;
Horstadius, 1926), is the basis for the supposition of Mortensen (1938, p. I I ) that
the main reason for the large number of eggs compared with the small number of
young that settle in various echinoderms, is failure of a very high percentage of the
eggs to be fertilized. Belding (1930, p. 10)suggests failure in fertilization to be the
main source of waste during the development of the bivalve M y a arenaria. This,
however, is contradicted by the fact that waste of eggs and larvae of a similar order
of magnitude is known within such groups of marine invertebrates in which failure
in fertilization seems to be excluded, since copulation takes place before spawning
(Thorson, 1946, p. 445). An example of this is that a single specimen (hermaphrodite)
of the tectibranch Apbsiu californicu, in less than 5 months after copulation, spawns
480,000,000 eggs, all developing into planktotrophic pelagic larvae (McGinitie, 1934,
1935, and own observations).
Remarks in the prefaces of such papers in the widespread literature dealing with
the embryology of marine invertebrates seem, however, when compiled, to give
a solid basis for a biological rule of the greatest interest, namely, that among marine
invertebrates shedding their eggs and sperm freely in the water the males are the
first to spawn, thus stimulating the females to shed their eggs, which, shed directly
into a suspension of sperm of their own species, have especially good chances of
being fertilized.
In order to show the superior value of this rule, I quote the species in which it has
been observed-actinians and ceriantharians : Sugartiu troglodytes, Cm*unthuslloydii
and Pachycerianthus multiplicatus (all Nyholm, 1943); echinoderms : Antedon bifida
(Seeliger, 1892), Asterias rubens (Gemmill, 1914),Amphiura jiliformis (Mortensen,
192oa), Ophiopholis aculeuta (Olsen, 1942), Strongylocentrotus Zividus (Fox, 1924),
Holothuria tubulosu (Selenka, 1876) and H . marmorata (Mortensen, 1937), Cucumaria
frondosa (J. & S. Runnstrom, 1919), Thyone briureus (Ohshima, 1925), and Lepto-
synuptu inhaerens (S. Runnstrom, 1927 b); gephyreans: Phmcolosoma vulgare
(Gerould, 1906), Priupulus cuudatus (Lang, 1939); polychaetes : Nereis cultriferu
(Herpin, 1925), N . dumerili (Just, 1929), N . limbata (Lillie & Just, 1913), and
N . vexillosa (Johnson, I 943), Pionosyllis lamelligera (Herpin, I 923), Eusyllis blom-
strandi (Herpin, 1925), Eunice harassi (Herpin, 1924), and Hydroides dianthus
8 G. THORSON
(Hargitt, 1910); nemerteans : Cerebratulus sp. (Coe, I 943); brachiopods : Lingula sp.
(Yatsu, 1902); chitonids: Chiton cinereus (Hoffmann, 1931),C. marmoratus and
C . squamosus (Metcalf, 1893),Ischnochiton magdalenensik and Mopalia lignosa (Heath,
I 905), and Chaetopleura apiculata (Grave, 1922, 1932); prosobranchs : Hahotis
tubercuhta (Stephenson, 1924),and H . gigantea (Murayama, 1935),Gibbula magus,
and G . cinerarius (Robert, I 902); lamellibranchs: Crassostrea virginica (Galtsoff,
1932,1938a,b) and C.gigas (Elsey, 1936;see Galtsoff, 1938~).
Observations on several other species are available which show that spawning
suddenly sets in for a whole stock at the bottom. Such an ‘epidemic spawning’ of
a whole population is known from the polychaetes Podarke sp., Diopatra sp. (Hargitt,
I ~IO),and Branchiomma vesiculosa (Hornell, I 894), the nemertean Cerebratulus
Zacteus (B. C. Wilson, I~OO),and the lamellibranchs Mytilus edulis and Macoma
baltica (Battle, 1932),Pecten irradians (Gutsell, 1930),Modioh modiolus (Wiborg,
1946),and Tivehstultorum (Coe, 1947).Fox (1923)showed how Red Sea sea-urchins
(Dindema setosum) spawn together around full moon, and summarizes what was
known on such lumar periodicity in the reproduction of marine animals. Korringa
(1947)concludes that in several marine invertebrates the sequence of neaps and
springs, or-in areas with little or no tidal amplitude-of dark and moonlit nights,
is closely associated with sexual maturation. Ripening of the sexual products is
started simultaneously in a whole population, resulting in an ‘epidemic spawning’
when the eggs and sperms are mature. This gives another example of the paramount
importance of the rule given above.
Whether the males induce spawning in the females, or either sex is able to induce
spawning in the other sex, the ecological result will be the same: eggs and enormous
masses of sperm will be present simultaneously within a rather small water area,
thus improving the chances of the fertilization of all the eggs spawned.
In several cases it has turned out that a ripe female will not spawn unless surrounded
by active sperm of its own species. This means that sperm rendered inactive by a low
salinity or a low pH, as found by Mortensen (1938,p. I I) for echinoderms, will not
result in unfertilized eggs, since the eggs will not be shed at all. A few female
echinoderms, which will only spawn when chances of fertilization are good, shed
millions of eggs of which only a few will reach metamorphosis in spite of the high
percentage of fertilization.
This, in connexion with the biological rule given above, seems to show that inactive
sperm, although occurring in nature, or the failure of insemination, cannot explain
the enormous waste found in most marine invertebrates during development. The
heavy waste takes place after fertilization, during the free-swimming pelagic life.
IV. TYPES OF LARVAL DEVELOPMENT
Eggs. and embryos may be more or less protected during their development. The
best protection is given by species with viviparity or with a highly organized brood
protection. From these types of development all transitional stages are found, from
primitive cases of brood protection, eggs laid in capsules or gelatinous masses
Reproductive and larval ecology of invertebrates 9
attached to a substratum, and single eggs adhering separately to a substratum, to
eggs shed singly and developing suspended in the water or floating along the bottom.
I have given examples of these modes of development (Thorson, 1946, pp. 419-21).
No connexion seems, however, to exist between the mode of oviposition and the
mode of development in marine invertebrates. Viviparity seems usually to be asso-
ciated with a non-pelagic development, but may also result in pelagic larvae (e.g. in
the prosobranchs Planaxis sulcatus (Risbec, 1935) and Littorina angulifera (Lebour,
1945)), and nearly all eggs shed singly and suspended in the water develop into
pelagic larvae with a long planktonic life (exceptions are the polychaetes Arenicola
marina, Thelepus cincinnatus and Ampharete grubei, cf. Thorson, 1946). All other
types of oviposition may result in non-pelagic young or planktotrophic larvae varying
from species to species. Here no rules can be given.
The embryos with a non-pelagic development originate in most cases from large
yolky eggs, sufficiently rich in food to support the whole development to the young
bottom stage (known for echinoderms, polychaetes, prosobranchs and lamellibranchs)
or exceptionally from yolky eggs surrounded by a substance like egg-white (proso-
branchs of the genera Natica and Amauropsis). In species with the above-mentioned
types of development, the food available is contained in an egg of a constant size for
each species, therefore all the hatching young of the same species will be at the same
stage of development. This is not the case when the embryos feed on nurse eggs;
here eggs of a size normally found to develop into pelagic larvae are laid several
together within a common egg space. Only a few of the eggs develop into embryos,
which will not hatch until they have devoured all the rest of the eggs, the nurse eggs,
within the egg space. Such nurse eggs are known from antarctic crinoids (Mortensen,
192ob),ophiuroids (Mortensen, 1921,1936),polychaetes (Wilson, 1928; Soderstrom,
1920; Mesnil & Caullery, 1g17), nemerteans (Schmidt, 1932, 1934), and several
prosobranchs (cf. Thorson, 1946), and the number of nurse eggs devoured per
embryo varies from a few in Natica catena, an average of 20-30 per embryo in
Polydora hoplura and Nucella lapillus, IOO in Buccinum undatum, 2500 in Neptunea
antipa, 7000 in Sipho (Colus)islandicus, to ~o,ooo-~oo,ooo nurse eggs as food for
a single embryo in the North Atlantic deep-sea prosobranch Volutopsis norvegica
(Thorson, 1935, 194oa, 1946).
Often there is a great variability in the number of embryos per egg space in
individual species, and, accordingly, in the number of nurse eggs at the disposal of
a single embryo. In the prosobranch Sipho (Colus) islandicus the number of nurse
eggs within a single egg capsule will always be rather constant while the number of
embryos per capsule may vary from I to 16. These embryos leave the capsule when
they have reached the stage of development which the nurse eggs at their disposal
are able to support, and hence it is evident that each of the sixteen embryos contained
in a single capsule will hatch at a much younger stage than a single embryo contained
in a capsule with plenty of food at its disposal (Thorson, 1935). In the prosobranch
Natica catena the number of nurse eggs at the disposal of the individual embryo
varies from 5 to I 10 in the Northern Kattegat and from 2 to 27 on Heligoland and
I0 G. THORSON
farther southwards. This means that the embryos hatch as non-pelagic young in the
Kattegat, but may hatch as pelagic larvae in the southern North Sea and the English
Channel (Thorson, 1946). The prosobranchs Thais haemastoma (= T . jloridana),
Plunaxis sulcutus, and Columbella rustica may develop with pelagic larvae in one
locality and with non-pelagic, nurse egg-feeding young in another locality (Bacci,
1947;Burkenroad, 1931;Franc, 1943;Lamy, 1928;Thorson, 1940b,and un-
published). Finally, occasional formation of twin embryos in large yolky eggs may
give rise to development of pelagic larvae in species normally hatching as non-pelagic
young (example : Lunatia pallida, Thorson, 1946).

G I -0.1 mm.

- D
1 mm. F H

Fig. 3. Planktotrophic larval types (above) and lecithotrophic larval types (be1ow)of each of the groups
Echinoidea, Holothurioidea, Asteroidea, Nemertini, and Polychaeta, viz. A, EucidariS metulmia;
B, Heliocidaris erythrogzamma; C, Holothuria arenicola; D, Psolus phantapus; E, Asterope
carinifma; F, Hemicia sanguinolenta; G, Pilidium magnum; H, Oerstedia dorsalis; I, Nereis
dumm'li (small larval type); and K, Nereis d u m ' l i (large larval type). The scale below left refers
to A-G, the scale above right to I-K. The magnification of H is unknown (compiled from Coe
(1943),Hempehnann (I~KI), Mortensen (1921,1937)~and Thorson (1946)).

As shown in the diagram (Fig. I), the embryos developing into non-pelagic young
are free from the huge waste found among larvae with a pelagic stage. However,
within the pelagic larvae the toll levied during their life in the plankton also varies
from species to species. Two main types of pelagic larvae may be distinguished:
larvae which, though swimming in the plankton, feed on their own yolk content
(lecithotrophic larvae), and larvae which feed on phytoplankton (planktotrophic
1arvae).
The lecithotrophic pelagic larvae, mainly developing from fairly large yolky eggs,
are of a clumsy shape, rather unfit for locomotion (Fig. 3), and are often carried
about almost passively by the currents. They take no food from the plankton, but
feed exclusively on yolk within the egg cell from which they originate. Most of these
larvae will stay for a long time in the plankton, others (e.g. Nucula and sponges) for
Reproductive and larval ecology of invertebrates I1
a short time only. Ecologically, they have the following advantages: they may use
the water masses for spreading over wide areas, but they are totally independent of
the plankton as a source of food, their chances of reaching the stage of metamorphosis
thus being better than those of planktotrophic larvae. The disadvantages are: the
large size of the eggs, which means a rather small number of eggs per mother animal,
and in consequence the inability of the relatively small stock of larvae to take advantage
of years with good food conditions to increase the numbers of its species.
This larval type, hitherto neglected, is unknown in all marine Gastropoda, but
seems to occur in most Porifera, in Anthozoa (species of the genera Bolocera, Tealia,
Pachycerianthus and Edwardsia), in Echinodermata (species belonging to the genera
Antedon, Echinaster, Solaster, Fromia, Henricia, Tropiometra, Ophiura, Ophioderma,
Heliocidaris, Cucumaria and Psolus); the type within the echinoderm larvae is
mentioned by Fell (1945, 1948) as ‘vitellaria’, in Polychaeta (species within the
genera Nereis, Mysta, Syllis, Odontosyllis, Eunice, Amphitrite, Capitella, Notomastus,
Branchiomma, and Artacama), in Nemertea (species of the genera Cephalothrzx,
Oerstedia and Malacobdella), in Brachiopoda ( Terebratella inconspima, Percival,
19++),in Lamellibranchiata (within the genera Yoldia and Nucula), and in Amphi-
neura (Chaetopleura). A compilation of the literature for each species is given in
Thorson (1946, pp. 436-7).
Larvae of this type seem to be totally absent from high arctic seas, but constitute
about 10% of the species with pelagic larvae in temperate as well as tropical sea
areas.
The planktotrophic larvae with a long pelagic life, known in the literature as
veliger, tornaria, pilidium, trochophore, etc. (cf. Fig. 3), mainly originate from very
small eggs poor in yolk, and swim briskly about in the water masses from which
they take their food. Most of these larvae spend 2-4 weeks (in summer) and 1-3
months (in winter) in the plankton. While the larvae of this type, belonging to
polychaetes, prosobranchs, tectibranchs, and lamellibranchs, resemble the adults
apart from those organs which enable the larvae to swim or float (e.g. cilia, pro-
visional bristles, velum), the larvae of nemerteans (pilidium) and echinoderms
(Fig. 3A, C, E, and G) do not show the slightest similarity to their parents. Ecolo-
gically the planktotrophic larvae with a long pelagic life have the followingadvantages:
they originate from small eggs poor in yolk, are cheap to produce, and the mother
animals when only I year old may often produce such eggs on a large scale. Their
long life in the plankton enables them to spread far with the water masses, to settle
in new areas, and found new populations. Of all the different types of larvae, these
are best fitted to be invaders. Their disadvantages are: their high requirements of
food, their total dependence on the food conditions in the plankton, and their
exposure to voracious enemies. The waste during their pelagic life varies enormously
from year to year according to the conditions in the plankton, and their stock at the
bottom undergoes pronounced fluctuations (Fig. 2).
This is the larval type met with in the development of more than 70% of all
marine invertebrates in Recent seas. It is hardly represented in extreme arctic seas
I2 G. THORSON
and in the deep sea, but is common in up to 55-65% of the species in boreal seas,
and 80-85 yo of the huge number of species living in the tropical seas.
The planktotrophic larvae with a short pelagic life are characterized by the fact
that their size and organization are the same, or very nearly the same, at the moment
of hatching and at the moment of settling. Their pelagic life seems to last from a few
hours (for most of the species) to a few days. The larvae seem to be able to feed in
the plankton, and several of them are known to do so, but it is likely that under
certain conditions they may settle without having taken in food during their short
pelagic life. Thus, feeding on the plankton is of secondary importance to them,
while the spreading of the larval stock and the chance of finding a suitable sub-
stratum seem to be the main requirements. The eggs are usually small or medium
sized, but large eggs may also develop in this way, e.g. Bela (= Lora) trmelyana
(Thorson, 1946).
This larval type, unknown in the echinoderms, is known among polychaetes
(species of the genera Autolytus, Arenicola, Terebellides,Hydroides, Serpula, Poma-
toceros, Miroserpla, Filograna and Spirorbis); prosobranchs (species of the genera
Annaea, Gibbula,Hydrobia, Turritella and Bela);opisthobranchs (viz. the tectibranch
Akera bullata, and probably several species of nudibranch larvae). A compilation of
the literature is given in Thorson (1946).
Larvae of this type will probably occur in about 5 yoof the invertebrate species in
all Recent seas from the Arctic to the Tropics. As, however, their stay in the plankton
is very short, their significance as planktonic larvae is much smaller than indicated
by this percentage.
V. SOURCES OF WASTE DURING PELAGIC LIFE
The waste of larvae within these three larval types seems to be controlled mainly by
two factors: the time they spend in the plankton, exposed to voracious enemies, and
their dependence on the plankton as a source of food. Concerning the lecithotrophic
larvae, we know too little of the number of eggs produced per mother animal to give
a reliable figure for the waste. For one of them, however, Solaster endecu, we know
that at Bergen an animal spawns several times a week during March-April, about
3000 eggs being shed during the main spawning, which lasts for 2 hr. (Nordgaard,
1912).Thus it seems reasonable to estimate the total number of eggs permfemale per
season as at least ~o,ooo-zo,ooo.This relatively large number of eggs in a species in
which the larvae are totally independent of the plankton as a source of food, seems
to show that the toll levied by enemies is an important factor in waste of pelagic
larvae. Accordingly, waste among larvae which spend only a few hours in the plankton
seems to be extremely small. The polychaete Spim~bisborealis, which has larvae of
this type, will only produce a few hundred eggs per female per year (Thorson,
'946).
The enormous waste is therefore found only among larvae of the third type, those
with a long planktotrophic pelagic life. As larvae of this type are to be found in the
majority of all Recent marine invertebrates, it seems reasonable to focus our interest
Reproductive and larval ecology of invertebrates '3
especially upon them. It was shown that failure of fertilization could not explain the
enormous waste found for this larval type; that is to say the waste takes place during
the free-swimming pelagic life. Thus we must study those conditions within this
period which may be supposed to cause the waste: the food conditions, the temperature
conditions, the toll levied by animal predators, and the problems of metamorphosis.

(I) Food conditions


There are three ways in which we may obtain information about the size and type
of food used by the different pelagic larvae: (i) the diameter of the oesophagus and
the first part of the intestine of the larvae (as no peristaltic movements take place,
half the diameter of the lumen, at most, can be filled with food if the cilia are to move
freely); (ii) the size and type of food actually found in the intestines and stomachs of
the larvae in nature; and (iii) the size and type of food, which in culture experiments
have supported a successful development of the larvae. Using these methods, the
following results have been obtained (Thorson 1946,pp. 446-50).
The decapod larvae and older larvae of the polychaete Magelona live mostly or
exclusively on animal food, and so do occasionally the larvae of Nephthys, Polydora
and Chaetopterus. A few polychaete larvae (Polydora, Nephthys, Lanice, Glycera,
and Chaetosphaera)are able to feed on large diatoms, viz. Chaetocerasand Coscinodiscus
up to 200 p long. The rest-by far the majority of the bottom-animal larvae-feed
on small phytoplankton organisms, and furthermore the larvae which usually feed
on animal food and large diatoms may do the same occasionally. T h e maximum size
of phytoplankton organisms which the larvae are able to swallow is for lamellibranchs
8 p, for echinoderms, prosobranchs, opisthobranchs, and most polychaetes 50 p,
but culture experiments and observations in nature have shown that the size of
phytoplankton normally devoured by bottom animal larvae is smaller, namely from
2 to 30 p.
Thus the main part of the food of pelagic bottom-animal larvae is composed of
nannoplankton (average maximum diameter about 5 p), and at least the larvae of
lamellibranchs and prosobranchs are able to feed exclusively on ultraplankton
(Girder & Sparck, 1932).The different species of ultraplankton are, however, of
quite different value as food for the same species of larvae (Bruce, Knight & Parke,
1940;compilation by Korringa, I 940),and different species of ultraplankton feeders
seem to have quite different requirements as regards the quality of their diet. The
larvae of Venus mercenaria, for instance, are easily nourished by a quantity of
different ultraplankton organisms, most of which are disregarded by the much more
particular larvae of Crassostrea virginica (verbal information from Prof. V. L. Loos-
anoff, Milford).
The food requirements of the planktotrophic pelagic larvae are much greater than
those of the adult animals at the bottom. If the oxygen consumption, as normally
supposed, gives an approximate measure of the calorie production of the animals,
i.e. of the quantity of food absorbed, a 10y marine invertebrate would utilize five
times as much food per weight and time unit as a I g. animal (Zeuthen, 1947,p. 134).
’4 G. THORSON
However, some of the food ingested is probably not absorbed in the intestine, but
will-though partially killed and useless for other larvae-leave the intestine with
the faeces. Further, a probability which cannot be excluded is that utilization of the
food is poorer the shorter the intestine of the animal in question, that is, the smaller
the animal is. Filtration studies on Ostrea and Mytilus seem to support this con-
jecture. The ratio of food filtered off to food digested seems to be considerably
higher in larvae than in adult lamellibranchs (Jergensen, 1943; Zeuthen, 1947,
p. 1 3 5 ) ~although the ratio given in these papers seems to have been estimated
somewhat too high (verbal information from Barker Jergensen). Thus it can be
taken for granted that the quantity of food which must be swallowed by a plankto-
trophic pelagic larva to support the combustion necessary for its considerable calorie
production is of a high order of magnitude. Sparck (verbal information) has
estimated that a larva of Ostrea edulis has to consume I million micro-organisms
(ultraplankton) during its 1-2 weeks’ larval life in order to complete its
development.
Hence it might be expected that most pelagic larvae living under natural conditions
would starve and perish after only a few hours’ lack of food, some species being
more particular and accordingly more difficult to rear than others. Unfortunately,
the relation between the production of phytoplankton and the occurrence of plankto-
t r s p h c larvae in nature is still very little known. T h e modern investigations on
phytoplankton production, calculated by the rate of photosynthesis, deal with phyto-
plankton as a whole. Assimilation of the large diatoms may dominate the figures
arrived at, while we are only interested in the figures for the nannoplankton and
ultraplankton, but these are not available. And even in the quantitative counts of
phytoplankton throughout the year we have little help, as the nude flagellates,
probably one of the most essential food sources of our larvae (Cole, 1939), are
completely destroyed by preservation (Steemann Nielsen, 1937, p. 16),and are there-
fore neglected in the counts. Thus, the relation between phytoplankton production
and larval occurrence is one of the most urgent problems in marine larval ecology,
and at present it seems impossible to estimate the significance of starvation for the
total waste of pelagic larvae.
Several observations seem, however, to show that the adaptability of the larvae to
poor food conditions is much greater than hitherto assumed. In the Sound (Denmark)
there are seasons with pronounced maxima and minima of phytoplankton production
(Steemann Nielsen, 1937), but in spite of these extremely varying food conditions,
the planktotrophic larvae of Limapontia capitata and Zirphaea crispata, for instance,
apparently thrive and grow in the plankton in all the months of the year, and larvae
of the genera Aporrhais, Bittium, Nassa, Akera and Philine, may occur in the plankton
during 8-9 months of the year. After 5 days of starvation, large larvae of Nassa
reticulata kept in culture dishes were in good health and swimming briskly about.
Larvae and young of Mytilus edulis, exposed to different conditions in culture dishes
and in nature for a period of 6 weeks, showed a variation in the volume of the
individual specimen from I (poorest conditions, just metamorphosed) to 4000 (best
Reproductive and larval ecology of invertebrates '5
conditions), but even the smallest specimens found after the experiments were in
good health. It is, however, necessary to distinguish between such quantities of
food as ( I ) starve and kill the larvae, (2) allow the larvae to vegetate for some time
though without growth and development, and (3) actually support the growth and
development of the larvae.
A heavy waste is, however, caused not only by food conditions which kill the
larvae, but also by the food conditions which postpone their growth and development,
a longer stay in the plankton exposing them to animal predators. I n these two ways
the poor food conditions are, no doubt, responsible for an essential part of the wastage
of planktonic larvae. How large a part of the waste is the result of food conditions
is at present unknown. A comparison of the number of eggs shed per female per
season in species with lecithotrophic and with planktotrophic larvae, which stay for
an equal period in the plankton, will help in solving the questions, but such egg
numbers are not at hand for the lecithotrophic species. The figures for the lecitho-
trophic asteroid Solaster endeca (3000eggs shed by one female during 2 hr., Nord-
gaard, 1912)and the planktotrophic asteroid Asterias rubens (2,500,000eggs shed by
one female during 2 hr., Gemmill, 1914)seem to show the significance of the food
conditions as a direct or indirect cause of waste.

(2) Temperature conditions


It has been calculated on the basis of figures for polychaetes, echinoderms,
prosobranchs, lamellibranchs, and decapod crustaceans that the pelagic life of
planktotrophic larvae in northern seas (Massachusetts, Plymouth, Scotland, West
Norway, Denmark) lasts about 3 (2-4)weeks in summer and early autumn and from
I monthup to 2 or even 3 months in winter (Thorson, 1946,pp. 451-7). A compilation
mainly based on the data of echinoderm development (Mortensen, 1921,1937,1938;
Onoda, 1936)shows that the larvae living in seas with higher temperatures seem to
require just as long a time for their pelagic development as those living in northern
seas (Thorson, 1946,pp. 455-6). This is also clear within the individual genera. The
tropical species of Ophiothrix and Ophiocoma have just as long a pelagic life as their
northern relatives. This agrees with the observations that, at a given temperature,
the eggs of southern species of Paracentrotus and Psammechinus cleave more slowly
than those of a northern species of the same genus (Fox, 1939a),that the heart beats
more slowly in the tropical Ostrea dentata than in the more northern circumpicta
(Takatsuki, 1929,pp. 102-12),and that the oxygen consumption in adult lamelli-
branchs is of about the same order of magnitude, e.g. at ' 0 C. in arctic, at 8" C. in
boreal, at 1 2 O C. in Mediterranean, and at about 25-30" C. in tropical species
(Orton, 1923; Sparck, 1926,1936;Thorson, 1936, and unpublished observations
from the Persian Gulf).
Within a restricted area the temperature, however, is of the greatest influence
upon the duration of the pelagic life. Crassostrea erirginica has, at ~ 4 - 2 7C.,
~ a free
swimming life of I week (J. Nelson, 1908), at 23-24" C.of 13 days, at 20" C. of 17
days, and (in Canada) at still lower temperatures up to at least 21 days (T. C.Nelson,
16 G. THORSON
1928b). Similar figures for other oysters are given by Korringa (1940), and Mort-
ensen (1931, 1937) gives, without figures, examples of the relation between the
temperature and the length of the larval life in echinoderms. Thus, a low temperature
may lengthen the pelagic life, and a high temperature may shorten it (provided that
the food conditions are good enough to support the increased metabolic rate at these
high temperatures).
Sudden changes in temperature may be lethal to the larvae (Allen & Nelson, 191I,
Hagmeier, 1930), but will normally not occur in nature. Sven Runnstrom gives, for
some northern echinoderms, lamellibranchs, and opisthobranchs, the temperature
limits within which the eggs are able to develop. The minimum amplitude for these
species seems to be 11' C.; in Echinocyamuspusillus it is as great as 2 5 O C. In the
Sound (Denmark) it would seem that the temperatures during the actual breeding
seasons never surpass the limits which Runnstrom found to be lethal to larvae of the
same species in his area (Thorson, 1946).
The area of distribution of a species may comprise an area in which the adult
animals may vegetate, a somewhat smaller area in which they may vegetate as well
as ripen their sperm and eggs and spawn them (spawning seems to require a still
higher temperature or other stimuli than the process of ripening), and an even
smaller area in which a successful development of the embryos and larvae may take
place. However, the temperatures required for spawning are so high and definitely
limited that they will normally allow the eggs and larvae to develop regularly (pro-
vided that other conditions are favourable). That is to say, the situation found in the
Sound will probably also hold true for other sea areas. If so, the temperatures
during the breeding seasons do not seem to be lethal to the larvae originating during
these seasons. However, the pelagic larvae may be carried by the currents to areas
with colder water, but during this rather slow transport they will continue their
development and old larvae are much more resistant to low temperatures than
young eggs.
Thus it can be taken for granted that the sea temperatures which control the
process of ripening and spawning and thus play a significant part as limiting factors
for the distribution of adult invertebrates, will normally be high enough to support
the development of eggs and larvae of those species which can spawn in a given area.
Thus under natural conditions the significance of the temperature for the pelagic
larvae as a cause of waste seems mainly to be limited to a retardation of the develop-
ment, low temperatures retarding the life in the plankton where the larvae are
exposed to voracious enemies.

(3) Metamorphosis
When a pelagic larva feeding on a pure algal diet changes during metamorphosis
to a carnivorous mode of feeding, as, for example, the larvae of Asterius and Nassa,
it seems reasonable to suppose that this would cause a physiological revolution in the
larvae, corresponding to what is known to happen during the pupal stages of insects,
when, for instance, a butterfly changes from a herbivorous larval stags to a honey-
Reproductive and larval ecology of invertebrates I7
sucking imago. Similar phenomena, however, do not seem to take place in marine
larvae. The experiments of Zeuthen (1947, Fig. 21, pp. 83,90) show clearly that the
metamorphoses of Asterias and Nassa are not connected with any essential change of
respiration intensity. According to Zeuthen’s curves, the physiological changes
during metamorphosis seem, on the contrary, to take place so gradually that they
may hardly cause any significant waste of the larvae.
A synopsis of the data scattered in the literature, supplemented with my own
observations, gives a solid basis for the statement that young pelagic larvae of marine
invertebrates (echinoderms, polychaetes, brachiopods, nemerteans, prosobranchs
and crustaceans) are positively phototactic, while old larvae approaching the stage
of metamorphosis are negatively phototactic. Young larvae crowd at the surface
while old larvae gather near the bottom. (Exceptions are found in larvae of those
species in which the adult stages live in the tidal zone or near the surface (Asterias
rubens, Pygospio elegans, Pomatoceros triqueter, Spirorbis borealis, Mytilus edulis and
Balanus balanoides), and which accordingly are photopositive even in their oldest
larval stages). Ecologically these rules mean that young larvae spend their pelagic
life in the free water masses near the phytoplankton-producing surface and with
good chances of spreading, while old larvae owing to their photonegativity are
forced towards the bottom to the substratum where they are going to settle (cf.
Thorson, 1946, pp. 460-3).
T. C. Nelson (1928b, p. 189) held that those invertebrate larvae which, at the
time of settling, happen by chance to ‘fall upon good ground’ are much less numerous
than the vast hordes which by chance ‘fall by the wayside’ and are lost. In the light
of our findings this does not seem to be generally true, but it may be true of species
highly selective with regard to the substratum. For the echinoderms (Mortensen,
1921,pp. 105-6, 1938) and polychaetes (Wilson, 1932b, 1937, 1948;Day & Wilson,
1934)it has been shown that the choice of a substratum is not entirely due to chance,
for larvae ready to metamorphose are able to postpone metamorphosis until they find
a substratum suitable for adult life, meanwhile continuing to swim and grow for
a period of several days to several weeks. Observations on ‘swimming-crawling
stages’ of prosobranch larvae (Lebour, 1931, 1937) and on the attachment zones of
larval echinoderms, polychaetes, phoronids, prosobranchs, tectibranchs, lamelli-
branchs, and crustaceans in ‘bottle collectors’ (Thorson, 1946) seem further to show
that the ability of postponing metamorphosis and actively seeking a substratum is
widely distributed among marine larval invertebrates. In a water area with a bottom
current of only half a knot the larvae forced towards the bottom by their photo-
negativity and testing the substratum at intervals may be carried over a distance of
24 km. in 24 hr., i.e. 170 km. per week, and their chance of finding a suitable sub-
stratum for settling and metamorphosis seems to be great. As regards some species
(Protodrilus),it would seem that if the larvae are to metamorphose, the mechanical
character of the substratum must be combined with certain inorganic unknown
substances (Jagersten, 1940), while for others (Ophelia) only the physical condition
of the substratum plays a part, chemical stimuli being of no significance for the
B R XXV 2
I8 G. THORSON
metamorphosis (Wilson, 1948). Also the colour of the substratum in relation to the
phototaxis of the larvae seems to be significant for the settling of several forms
(Gregg, 1945; Weiss, 1947;Walton Smith, 1948).

(4) Transport by currents from continental shelf to deep sea


However, in spite of all these circumstances,larvae able to postpone metamorphosis
for weeks may miss a suitable substratum. Along the ocean coasts where the shelf is
rather narrow and the deep sea is not far off, heavy and strong currents may carry
the larvae away from their shallow water habitat. These conditions may, no doubt,
cause a large waste of larvae, since their own locomotion will not help to resist the
nearly passive transport with the currents (Korringa, 1941). Johnson’s investigations
(1939) on the sand crab, Emerita analoga, which only inhabits sandy beaches near
the shore in southern California, show that the fourth zoeal stage of this species
occurred regularly in plankton hauls at a distance of I 25-1 30 miles from the mainland
shores. The first zoeal stage, which may last up to 4 weeks or more under laboratory
conditions, but is probably of somewhat shorter duration in nature, was, however,
only met with in plankton less than 20 miles from the shore. Thus, for a form such
as Emerita with a pelagic life of about 4 months, the transport by currents to the
deep sea will, no doubt, be a heavy cause of waste. In most marine invertebrates
(polychaetes, echinoderms, gastropods, lamellibranchs), from temperate as well as
from tropical seas, the total pelagic larval life will, however, last only about 3 weeks
(Thorson, 1946, pp. 451-6); this is the same time as the first zoeal stage of Emerita
took to develop, which was never found in high sea plankton. Thus Johnson’s
observations, proving that a heavy waste actually takes place among Emerita larvae
during transport to the deep sea, just as clearly show that for most other larval
invertebrates-those with a 3 weeks’ pelagic life-such a transport will only be of
little significance along the southern Californian coast. This slow seaward transport
may probably be explained by the fact that ‘the main movement’ (of the currents)
‘ are mostly parallel or oblique to the coast line, a fact which may result in considerable
lapse of time in carrying larvae to the outer stations’ (Johnson, 1939, p. 243). Along
the northern Californian coast, north of Point Conception, where the shelf is much
more narrow and the deep sea accordingly much closer to the shore (cf. Shepard &
Emery, 1941), conditions may be otherwise. This seems to be supported by the
fairly large number of brood-protecting species (actinians, asterids, holothurians)
found along this coastal stretch. However, no exact calculations are available.
Along the European coasts of the Atlantic this waste seems also to be of less
significance than once supposed. Here the predominant wind comes from the west,
especially during the summer half of the year when most European invertebrates
have their breeding season, and the currents influenced by these winds will normally
follow the coast lines and thus transport the larvae to other areas, but only rarely
beyond the shelf. The tidal currents will normally be of a rather stationary character,
that is to say most of the larvae removed during ebb tide from the areas where they
were spawned will be carried to other areas of the coast within the shelf.
Reproductive and larval ecology of invertebrates I9
Now and then larvae, during their long pelagic life, will be nearly stationary over
the bottom where their parents live. This is the case, for instance, even in open and
rough sea areas, when a bank rising from a deeper bottom causes upwelling and
circulating currents, that is eddies or swirls (cf. Orton, 1937). Thus, on the Dogger
Bank in the North Sea-a sandy region surrounded by vast areas of deep muddy
bottom with a totally differing fauna-Davis (1923, pp. 18-19) found two large
populations of newly metamorphosed Spisula subtruncata which had settled 153 and
243 miles, respectively from the only possible parent-population. Also Wilson’s
(1948) observations on the settling of pelagic larvae of Ophelia bicornis on the Bull-
hill Bank near Plymouth seem to suggest a rather stationary life during the pelagic
phase.
Along the African Atlantic coast (Gulf of Guinea), where the north-east trade
wind blows, there is a rather constant surface current from the shelf towards the
open ocean, which no doubt causes a catastrophic waste of pelagic larvae. Observa-
tions on the development of prosobranchs by Knudsen (1949) show that about 68%
of the species along this coast have a direct development without any pelagic life,
i.e. a much higher percentage of non-pelagic larvae (corresponding to that known
between Iceland and the Faroes) than was to be expected from the temperature and
southerly position of the area.
If, however, larvae able to postpone their metamorphosis are carried to areas
where no suitable substrata occur, their situation seems to be rather bad, although
their chances of succeeding are by no means totally lost. Thus, after an abnormally
prolonged larval period they may actually metamorphose and grow in mid-water.
Day (1937, p. 36) showed this for the polychaete Scolecolepis fuliginosa, and T. C.
) Mytilus edulis. In the tectibranch Diaphana minuta the embryonic
Nelson ( 1 9 2 8 ~for
whorls on the adult shells found round Iceland are much larger in specimens from
depths exceeding 1000m. than from shallow water. In both localities the larval
shells were of the pelagic type, the difference being that the last larval whorl in the
deep-sea specimens increases more than usual and continues its growth for a longer
time than usual, no doubt as a result of a retarded larval life followed by a mid-water
metamorphosis (Lemche, 1948; Thorson, 1946, p. 466). From the Sound we know
several examples of such mid-water metamorphosis in echinoderms, polychaetes,
prosobranchs and opisthobranchs, and the puzzling ‘ Benham-stage ’ in Arenicola
marina, common in the North Sea but totally absent from the Sound, may probably
be explained in a similar way (Thorson, 1946, p. 467; but see Newell, 1948).

( 5 ) Enemies
Several of the factors previously supposed to be very critical for the developing
larvae (failing fertilization, unstable temperatures, choice of unsuitable substratum,
etc.) have thus proved to be much less critical than hitherto assumed. Since, never-
theless, a large waste actually takes place among the pelagic planktotrophic
larvae, the main causes for this must be sought for among factors hitherto regarded
as less essential. The most essential factor neglected by students of marine larvae up
2-2
20 G. THORSON
to the present time is the toll levied by enemies. T h e tiny, fragile larvae, which are
rapidly dissolved after death, have, no doubt, often been overlooked in the stomachs
and intestines of larger animals such as fishes, embedded as they are in a common
mass of larger and more conspicuous food animals. A thorough study of the literature,
however, shows the enormous waste which may be ascribed to such predators. In
the plankton we find enemies ranging from the small Noctiluca, through a number
of different Hydromedusae, Medusae and Ctenophora to Copepoda and pelagic
fishes (herring, pilchard, sprat, mackerel, garfish). Also the bottom animal larvae
in the plankton may feed on other pelagic bottom animal larvae. Such carnivorous
forms are the larvae of Mugelona and decapod Crustacea, partially of Nephthys,
Polydora, Chaetopterus, Polynoidae, Poecilocheatus, Phoronis and of Actinia. Of the
bottom animals the following are known to feed on pelagic larvae: coelenterates of the
genera Aurelia (Scyphistoma),Alcyonium, Virguluria,Sagartia, Edwardsia, Cerianthus,
Puchycerianthus, the echinoderm Echinocyamus, molluscs of the genera Nussa,
Mytilus, Pecten and Ostrea, and barnacles, which, combing the water mass with
their arms, will, no doubt, take a heavy tribute of the pelagic larvae. Also larger
crustaceans, as Cumacea and Amphipoda, may feed on pelagic bottom animal larvae,
and so may ascidians and fishes of the genera Gadus and Centronotus (see the synopsis
in Thorson, 1946, p. 471).
It has been calculated that a medium-sized Mytilus edulis, filtering 1.4 litres of
water per hour, may in this way retain and kill about IOO,OOO pelagic lamellibranch
larvae in 24 hr., during the maximum breeding season in a Danish fjord (Thorson,
1946, p. 470). Cerruti (1942),studying the oyster larvae near Taranto, regards the
animal depredators as the most essential cause of waste, and figures a series of
different animals, planktonic as well as benthonic, with oyster larvae in their
stomachs and intestines. Korringa (1941),studying oyster larvae in Holland, found
‘that the toll levied by animal depredators is the most important cause of the
diminution of the larval herds in the Oosterschelde ’.
Summarizing the discussion given above, I am of opinion that the conclusions
drawn by Cerruti and Korringa as regards oyster larvae may also be drawn for
pelagic bottom animal larvae in general. Depredation by other animals is probably
the most important cause of wastage of planktonic larvae. Starvation may also
directly cause a heavy waste, which, however, seems to have been estimated too
high. T h e most common effect of poor food conditions, low temperatures, or lack of
a suitable substratum on the waste of larvae will be an indirect one, namely a retarda-
tion of the metamorphosis of the larvae, that is, a longer stay in the plankton exposed
to large crowds of voracious enemies.
But, in addition, the question of getting a good start on the bottom after meta-
morphosis and settling is more urgent for species with a pelagic than with a non-
pelagic development, and to the former group it is a handicap which may increase
waste considerably. Thus it is well known that species with a non-pelagic develop-
ment normally have a very long spawning season, often the whole year, i.e. eggs and
young are produced some few at a time over a long period, and the young are often
Reproductive and larval ecology of invertebrates 21
able to feed on their own content of yolk during the first difficult time after hatching.
Species with pelagic, planktotrophic larvae will spawn their eggs much more
rhythmically or even ‘epidemically’ in correspondence with the temperature, lunar
phases, or maxima of phytoplankton, and the metamorphosis and settling of larvae
originating from these spawnings will also take place ‘acutely’, vast hordes of larvae
settling, contemporaneously, often within a few days, on the same area of bottom,
thus making their mutual competition especially keen.

VI. GEOGRAPHICAL DISTRIBUTION AND MODE OF DEVELOPMENT”


(I) Asexual reproduction
Besides the sexual mode of reproduction mentioned above, asexual reproduction
takes place in several groups of marine invertebrates. This vegetative mode of
reproduction is common in the coelenterates, sponges, polychaetes, and nemerteans,
is met with in several asteroids, ophiuroids, and holothurians, but is unknown in the
crinoids, echinoids, gephyreans, molluscs, and crustaceans.
We know several examples of marine invertebrates which, recruited from eggs
and larvae from other localities, may vegetate and grow for a long time in a sea-area
in which they are unable to ripen and to spawn their sexual products. This would
seem to mean that species able to reproduce in a vegetative way (by fission, laceration,
budding, etc.) would have a good chance of competition in such areas where conditions
for a sexual reproduction are unfavourable. However, experience seems to show
that species with asexual reproduction alone are of little importance and form a rather
small percentage of the animal populations of all seas, arctic, temperate and tropical,
hitherto investigated, and have a comparatively small area of distribution.
The disadvantages of this mode of reproduction thus seem to outweigh the
advantages to such an extent that the animals play only a small part in competition.
The disadvantages of asexual reproduction are, among others, the sw11intmsity of
reproduction and the small possibilities for the species of spreading to other areas.
T h e intensity of asexual reproduction must necessarily be small because the animql
which starts to reproduce has to support the new individual with enough organic
substances of its own for it to develop into an adult. For example, the high arctic
asteroid Stephanasterias albula, which in East Greenland reproduces exclusively in
an asexual way by fission of the disc (Thorson, 1936,pp. 22-3), seems to produce
only one new individual a year, and seems to disappear along the south-eastern
Greenland coast, being replaced by Leptasterias groenlandica, an animal of the same
size and feeding habits living in the same biotope and at the same depths, but repro-
* I regret that I have had to disregard the original paper of Wimpenny (1941),which also touches
on some of the problems mentioned here. Wimpenny’s paper, so far as concerns the bottom invertebrates
of the coastal zones, is based upon a series of concepts, for instance, the hypothesis of slow metabolic
rates in arctic and quick in tropical marine animals, the theory of quick life cycles in tropical marine
animals, the idea that no marine animals have an optimum temperature as low as that in which polar
invertebrates must live, the quicker metabolisni in male individuals, etc., which have been generally
abandoned by workers in this field. Thus, the basis for my conclusions is so far from that of Wimpenny
that it would carry us too far to go more deeply into these matters here.
22 G. THORSON
ducing by eggs and sperm. Other species, however, are able to produce much more
young per year asexually, although the number is always small compared with
species reproducing by eggs and sperm. Thus the actinian Sagartia Zacerata may
undertake more than seventy lacerations in the course of a year (Stephenson, 1935,
p. 353). But even in such species the chances in competition over wide areas are
small because of their poor ability to spread. If they got a chance of spreading they
would probably be able to thrive and compete in several different coastal areas.
A remarkable example supporting this hypothesis is provided by the actinian
Diadumene luciae, which, though only reproducing by longitudinal fission, has in
recent times spread from Connecticut (1892)to the Plymouth Docks (1896),Naples
(I~II), den Helder in Holland (1913),and the Suez Canal (1924,cf. Stephenson,
1935,pp. 205-6), no doubt transported to these localities on ships' bottoms.
Most species able to reproduce in a vegetative way are, however, also able to
reproduce by eggs and sperm, and have thus a much better chance in competition.

(2) Sexual reproduction


The lecithotrophic pelagic larvae (apart from high arctic seas) and the plankto-
trophic larvae with a short pelagic life seem to be equally frequent in all sea areas.
As first suggested by Murray (1895,1898)and Chun (1897),there seems, however,
to be a strictly regulated equilibrium between the percentage of species with a non-
pelagic development as compared with species with planktotrophic larvae with a long
pelagic life, a balance which varies regularly and gradually from the Arctic to the
tropics.

( a ) The Arctic
In the high arctic seas (East Greenland) about 95yoof all marine species of bottom
invertebrates seem to develop without a pelagic phase, by large yolky eggs (Fig. 4)
or by nurse eggs, and, rarely, by brood protection or viviparity (Thorson, 1936,
p. 75). As the ecological conditions are rather simple here, it seems possible to give
an explanation of the causes of the non-pelagic development. Owing to a stabilization
of the water masses at the surface (due in part to melting ice) during the same short
season in which light conditions are optimal for assimilation, the normal period of
phytoplankton maximum in East Greenland does not exceed 1-14 months (outer
coast and fjords respectively, Thorson, 1936,p. 85). During this season the tempera-
ture in the surface layer from 4 to 10 m. ranges from 2.5 to 4'5" C. (at depths less
than 4 m. the temperature is 5-8" C., but the water is so brackish that all the larvae
will be killed (cf. Thorson, 1936,pp. 80-3)). Thus, in order to survive in these areas,
a planktotrophic pelagic larva has to complete its pelagic development from hatching
to metamorphosis within 1-14 months at a temperature below 4-5"C. or-for most
larvae-below 2.5" C. The figures given for the duration of the pelagic larval life in
Ostrea (pp. 15, 16)at different temperatures show that a fall of temperature of a few
degrees only (from 24-27 to 20' C.)will more than double the duration of the pelagic
life. The average length of a planktotrophic pelagic larval life in temperate as well as
Reproductive and larval ecology of invertebrates 23
tropical seas is estimated at about 3 weeks. T h e ability of completing larval life in
less than 1-14 months at temperatures below 4.5’ C., with its requirement of rapid
growth and a high metabolism, is not common, and only a few species possess it.
When, however, a larva is able to thrive under these severe conditions, the plankto-
trophic pelagic larval development seems to afford good opportunity in competition
even in the Arctic. Thus it is highly interesting that in an area in which 95 yo of the
species have a non-pelagic development, the 5 yo reproducing with pelagic plankto-
trophic larvae seem to comprise several of the species which quantatively are the
commonest within the area (viz. Saxicava arctica, Mya truncata, Ophiocten sericeum,
Strongylocentrotus droebachiensis, etc., Thorson, 1936, pp. 77-8). This ability to
thrive under poor conditions seems also to hold good for the same species in boreal

- 0.5 rnm.
8
1
I
I
I
1 1
1 I
14
5 rnrn.
I
0
,

Fig. 4. Egg size of arctic lamellibranchs (above, left) and crustaceans (above, right) compared with
boreal or more southerly species of the same genera (below). Mucous membranes, if any,
I

surrounding the eggs disregarded, only the nutritive contents of the eggs being compared.
I, Modiolaria laevigata; 2,M . marmorata; 3, Vemtsfluctuosa; 4, V . gallina; 5 , Macoma calcarea;
6 , M. baltica; 7, Arcaglacialis; 8, A. noae; 9, Cardium ciliatum; 10,C. exiguum; I I, Spirontocaris
groenlandica; 12,S . manchi; 13, Sclerouangon boreas; 14, Crangon crangon.

seas. Thus, the larva of M y a truncata is the only lamellibranch which has its season
of occurrence in the Sound in DecemberIJanuary, that is, in the very heart of the
winter with its poor food conditions and low temperatures (Jergensen, 1946).
Nevertheless, high temperatures are utilized as much as possible by pelagic plankto-
trophic larvae even in high arctic seas. Thus, they occur in the plankton in summer,
and all adult species reproducing by pelagic larvae in East Greenland are associated
with the surface layer, ‘the fjord-water layer’, which in summer has positive
temperatures, while all bottom invertebrates associated with the constantly negative
‘polar current layer’ (from 15 to 25 m. downwards) have a non-pelagic development.
Curiously enough, species with pelagic lecithotrophic larvae seem to be absent, or
nearly absent, from high arctic sea areas, where their independence of the plankton
as a source of food and their ability of spreading theoretically would seem to make
them well fitted for competition. T h e conditions in high arctic seas seem, however, to
be so severe that there are no chances for compromise methods. Here the mode of
larval development must be ‘all or none’: either the safety first method with a non-
24 G. THORSON
pelagic development, when the parent animals support their young with such a large
amount of nourishment that their development to a bottom stage is insured, or the
cheap method, with small eggs and pelagic planktotrophic larvae, which, if able to
compete during their pelagic life, have a chance of settling in huge numbers and of
conquering new areas.

(b) The Antarctic


In the antarctic seas the percentage of bottom invertebrates with a non-pelagic
development seems to be still greater than in the Arctic (Murray, 1898;Mann, 1948).
Especially as regards the echinoderms this is supported by recent figures. Thus, of
the antarctic crinoids, ten of the nineteen species known, i.e. 53 yo,are viviparous,
while only five viviparous species are known among the 600 crinoid species from
other seas (John, 1938). Of the ninety-four species of ophiuroids from antarctic and
sub-antarctic seas, the mode of reproduction is known for fifty-six species, thirty-one
of which, i.e. 56%, are viviparous (Mortensen, 1936,p. 204). Of the 114species of
asteroids from antarctic seas, sixteen, i.e. 14%, are directly known to protect their
brood (Fisher, 1940,Ludwig, 1go4), but of the genera Leptychaster, Mirastrella,
Rhopiella, Henricia, Pteraster, Hymenaster, Anteliaster, Lysasterias, Diplasterias and
Neosndaster, in which all the species hitherto examined have proved to protect their
brood, there are species in the Antarctic which may be supposed to reproduce in the
same way (Fisher, 1940). If these species, a total of thirty-four, are added to the
sixteen certain cases of brood protection, we arrive at fifty brood protecting species,
i.e. 44% of the total number of species. Of the thirty species of echinoids known
from antarctic and sub-antarctic seas, eleven, i.e. 37%, are known to protect their
brood (Mortensen, 1910,1936). T h e percentage of brood protecting antarctic holo-
thurians seems also to be very high (Ludwig, 1904;Vaney, 1925;Ekman, 19z5),
though no modern figures are available. I n contrast to these figures we only know
with certainty two larval ophiuroids, two larval asteroids, one larval echinoid and
one larval holothurian from the antarctic plankton (McBride, 1920;McBride &
Simpson, 1908;McIntosh, 1934;Mortensen, 1913).
A similar tendency to protect their brood is known too for other groups of antarctic
bottom invertebrates, although they have been less thoroughly studied. T h e few
antarctic lamellibranch species in which the mode of reproduction has been in-
vestigated, protect their brood, viz. the genera Modiolarca, Kidderia, Phaseolicama,
Limopsis, Lasaea, Cyamium and Pseudokellya (cf. Bernard, 1898; Pelseneer, 1903;
Mortensen, 1910; Mann 1948,p. '90). The egg capsules of sixteen species of
antarctic prosobranchs frorn the Discovery expedition, kindly placed at my disposal,
seem all to have a non-pelagic development, and no pelagic molluscan larvae are
known from the antarctic plankton (Simroth, 191I). Several antarctic and sub-
antarctic actinians are known to protect their brood (Anemonia, Actinia, Cricophorus,
Epiactis, Urticina and Marsupifer, cf. Clubb, 1902;Kirk & Stuckey, 1909;Carlgren,
1901,19z4),and so are a rather large number of antarctic polychaetes (Polynoe,
Cirratulus, Eteone, Flabellizera, Polydora and Potamilla, cf. Gravier, 1923).
Reproductive and larval ecology of invertebrates 25
Thus, the tendency towards a non-pelagic development seems to be still more
pronounced in the antarctic than in the arctic waters, a fact which at first glance
seems curious, since the antarctic seas are so well known for their rich plankton
production which serves as food for the large stocks of whales living there. However,
this enormous production takes place at the very surface of the open ocean, while the
bottom invertebrates dealt with here inhabit partly the shallow water shelves of the
antarctic coasts, where the food conditions are known to be extremely poor, and
partly the deep sea far from the producing surface layer. Hardy (1928), in his maps
on the production of phytoplankton round South Georgia and South Shetland,
shows that production is extremely poor in the very coast zone of these groups of
islands. Hart (1934, pp. 215-16), who, in the coastal waters of South Georgia,
examined the phytoplankton production during the whole summer from November
to March, found maxima from November to January comprising two continuous
periods of production of 3 and 2 weeks respectively, separated by a pronounced
minimum. Thus, the connexion of a very low temperature (4 to I' C., Elcman, 1935,
p. 303) and a very short period of phytoplankton production seems to be the main
obstacle for a pelagic larval life here as in the Arctic. Hart explains the very scanty
production at South Georgia as a result of strong winds causing rapid movements
of the surface layers (i.e. the individual phytoplankton organism is exposed to the
light at the surface during too short a period to assimilate and reproduce), and of the
opacity of the water due to inorganic material in suspension. As similar conditions,
strong winds and water opacity, seem to prevail also along the other antarctic shores,
it seems reasonable to generalize the results found in South Georgia and South
Shetland for all the antarctic coastal waters.
The bottom invertebrates in arctic as well as antarctic seas thus show the same
tendencies towards a non-pelagic development, and in both areas this tendency may
be explained through the same ecological conditions, namely, very limited periods
of continuous phytoplankton production in connexion with very low water tempera-
tures, Hence it is surprising to find that most arctic species are able to support their
non-pelagic development by means of much smaller eggs than the antarctic species,
and without the viviparity and brood protection so dominant in the latter group.
It seems probable that historical aspects should be taken into consideration here,
namely, that the antarctic fauna has had a longer time to develop its tendency to
abandon the pelagic life than the arctic fauna. And the poor food conditions in
antarctic and arctic regions seem to support this tendency even to such extremes as
are found in the antarctic species. The greater the individual is when spawned, the
smaller is its relative consumption of oxygen (Zeuthen, 1947, p. 134),that is, the
smaller its food requirements and the better its chance of competing under poor
food conditions. Thus it might be expected a priori that evolution in these poor
regions would advance not only from a pelagic to a non-pelagic life, but also towards
a brood protection from which the young start their free life at the bottom as late as
possible.
26 G. THORSON

( c ) The deep seas


The dominance of non-pelagic development in the arctic and antarctic seas seems also
to hold good for the deep seas, the third large region of the seas with low temperatures
and poor food conditions. Figures showing the mode of development of deep sea
species are, however, rather scanty, and new exact figures for a sufficient number of
species are highly desired. In this area, as in the Antarctic, the echinoderms have been
best studied and discussed. Mortensen (1921,p. 249), though having directly proved
the pelagic larval type of the deep sea echinoid Laganum diplopora, and admitting
that many other deep sea forms, judging from the characters of their eggs, may have
pelagic larvae, states that ‘we have not yet definitely ascertained a single phase of
a larva of a deep sea form found at the surface’. Several echinoderm larvae actually
found at the surface in mid-ocean originate from coastal forms with a long larval life.
Others may originate from the deep sea, where (I again quote Mortensen) ‘a great
percentage of them (i.e. the echinoderms) have large eggs, and therefore certainly
must have an abbreviated development ’. Finally, Sven Runnstrom (Leptosynapta
inhaerens, 1924) has shown that even species with small eggs may have a non-pelagic
development.
Other examples showing the general tendency to a non-pelagic development are
found among the deep sea shrimps (Crytocheles, Bythocaris, Spirontocaris and
Parapasiphae, cf. Sars, 1912,p. 3 ; Balss, 1927, p. 951) and in the genus Scalpellurn
(Hesse, 1924, p. 169). T h e deep sea species always have a small number of very large
eggs, deviating on this point from the shallow water forms. T h e few prosobranchs
which inhabit the deep sea, of which the development is known, also have a non-
pelagic development, viz. Sipho, Acrybia, Volutopsis norvegica. T h e latter has giant
embryos (Thorson, 1940n and unpublished observations).
As the phytoplankton can only assimilate, and so multiply, in the uppermost water
layers, only these layers seem sufficiently rich in food to support a pelagic larval
development. If, thus, a deep sea species reproduces with planktotrophic larvae
having a long pelagic life, the larvae will have to rise by the aid of their own loco-
motory organs through a water column often 2000-4000 m. high, or even more,
from the bottom to the food producing surface layer, and to cover the same distance
when descending to settle after having completed their pelagic life. This seems to be
a nearly hopeless task. Mortensen (1921,p. 250) calls attention to the help possibly
given by vertical currents in carrying the larvae to the surface, as is known, for
instance, for the fish Reinhardtius hippoglossoides. I cannot agree with Mortensen
on the importance of this point. For fish which migrate to a restricted area to spawn
it seems likely that an area will be chosen where local vertical movements of the
water may carry the larvae towards the surface (cf. also the life cycle of the crustacean
Euphausia superba in the Antarctic), but conditions are quite different for species
distributed evenly over large areas of the deep sea bottom and spawning here without
migrating. Here no vertical currents can influence the mode of larval development.
I n some parts of the area in which the animals live there may be vertical currents
Reproductive and larval ecology of invertebrates 27
moving towards the surface, in others towards the bottom, and in others, again, no
vertical currents at all. It seems most reasonable to conclude that widely and evenly
distributed species depend only on the directly surrounding environment, which has,
as in the arctic and antarctic seas, poor food conditions and low temperatures, and
that a non-pelagic development will be totally dominant. This assumption seems to
be supported by the few observations available.

Percentual dirtrlbutlon of protobranchr w l t h


pelaglc (0)and non-pelaglc (m) development
from East Greenland t o the Canary Islands

-
East
c

Green-
h
E
-----
.. . -
W.md
5. Ice-
.
Faroes.
Shet.
%Nor-
my.W.land,
S. Eng- Canary
Islands
land land land land, Sweden, Channel
Orkneyr Denmark Islands

Fig. 5. The relations between a pelagic/non-pelagic larval development in


prosobranchs throughout the North Atlantic.
These ecological conditions, which show so many common features for the deep
sea, the arctic and the antarctic seas, and which enable the same animals to live and
to reproduce there, contribute to explain the 'equatorial submergence' of many
arctic and antarctic coastal forms (Hesse, 1924;Thorson, 1936).
Leaving now the faunas with a non-pelagic larval development, we may summarize
our recent knowledge in the following way: pelagic development is nearly or totally
28 G. T H O R S O N
suspended in the deep sea, and is restricted to the shelf faunas. I n the arctic and
antarctic seas pelagic development is nearly or totally suppressed, even in the shelf
faunas, but starting from here the percentage of forms with pelagic larvae gradually
increases as we pass into warmer water, reaching its summit on the tropic shelves
(Thorson, 19406,p. 235).
l’he graph (Fig. 5) gives a good illustration of this, and as the prosobranchs seem
to be especially sensitive to ecological changes (in high arctic seas we know pelagic
larvae of polychaetes, echinoderms and lamellibranchs, but not a single prosobranch),
they also seem to be especially well fitted to serve as a ‘barometer’ of the ecological
conditions. The graph ranges from 0% of pelagic planktotrophic larvae in East
Greenland to about 70% at the Canary Islands. In the Persian Gulf, with its
extremely high water temperatures but rather poor food conditions, 75”/0of the
species have pelagic larvae (Thorson, 194ob),and in the tropical area round the
Bermudas about 85 yoof all the prosobranchs examined have pelagic larvae (calculated
from Lebour, 1945).This is the maximum percentage of pelagic larvae hitherto
known from a marine area, and higher figures may hardly be found in other areas,
as all tidal zones-even in the richest tropical areas-have a number of species which
reproduce in a non-pelagic way, thus preventing their young from being carried
away from the area by a heavy swell. Graphs of the same type, though somewhat
less pronounced, may be constructed for other groups of marine invertebrates (e.g.
the echinoderms, cf. Thorson, 1936,Fig. 3).

( d ) The tropics
The rule that the highest percentages of species with a long pelagic planktotrophic
life is found along the tropical coasts may at the first moment seem curious because
of the general assumption of a richer production of plankton in temperate than in
tropical seas. This assumption, however, is based upon studies of the surfaces over
the deep sea-not upon observations from the shelves, where the production of
phytoplankton may be just as rich or even richer in the tropics than in temperate
seas (information from Prof. E. Steemann Nielsen, cf. also Hentschel, 1936,pp. 141-
65). But what especially makes the tropical coastal waters well fitted to support a
large stock of pelagic larvae is probably the fact that the light conditions enable the
phytoplankton to assimilate all the year round. T h e production of phytoplankton
in a tropical coastal area will on an average take place throughout the year or at least
during a much longer period and much more continuously than in temperate and
arctic seas.
The question now arises whether the tropical marine invertebrates breed during
the whole year, too, thus being able to make a practical use of this long period of
phytoplankton production. Semper’s statement from the Philippines (1885, pp. 135-
6), that the marine invertebrate species there breed continuously throughout the
whole year, has been severely attacked by Mortensen (1921, pp. 245-6, 1937,1938),
who found that most species of echinoderms had distinct breeding seasons even in
the tropics. However, investigations carried out on the Great Barrier Reef especially
Reproductive and larval ecology of invertebrates 29
in order to learn ‘whether in a tropical marine area of this nature, the breeding of
common animals goes on fairly steadily all the year round, or whether there is a con-
certed breeding season for the majority of them at some particular time of year’
(Marshall & T. A. Stephenson, 1933, p. 219), showed that ‘breeding of animals was
by no means confined to any one part of the year, it occurred in every month, and
therefore in winter as well as in summer’, but ‘if a census of all species could be
made a majority of them would be found spawning either exclusively or most actively
in the warmer months’ (Anne Stephenson, 1934, p. 270).
In plankton off the Madras coast, larvae of polychaetes occurred throughout the
whole year, though with a maximum during the season (November to March) with
the richest production of phytoplankton (Aiyar, 1933). These facts seem to support
those from the Barrier Reef, although the Madras larvae had their maximum in the
winter months. Panikkar & Aiyar (1939), discussing these problems on the basis of
their investigations of breeding among brackish water animals from Madras, conclude
that reproduction takes place in that area throughout the year, some species repro-
ducing equally in all months, others reproducing in all months but more intensively
during a certain season of the year, others, again, reproducing during one restricted
season of the year only, and finally some reproducing during two or more restricted
seasons of the year, mainly in relation to the rainfall.
These observations from the tropics show that, although several of the species
have a restricted breeding season, this season is on an average much longer than the
breeding seasons of species living in temperate seas, and while in temperate seas
most species will breed within the same few months which will result in a crowding
and a keen competition of the larvae in the plankton, the tropical species breed
within such different seasons that their larval stock taken as a whole is more or less
equally distributed in the plankton all the year round. Thus, although maxima and
minima occur even in the tropical coastal areas, it is easily understood that the
conditions for a pelagic planktotrophic larval development are especially favourable
there. A long season of phytoplankton production is associated with a long season
of larval occurrence in the plankton. The competition among the larvae is much less
keen than in temperate-not to speak of arbtic-seas, where all pelagic larvae have
to crowd and to feed from the plankton during a few restricted maxima of phyto-
plankton production.

VII. SPECIES ABLE T O VARY THEIR MODE OF REPRODUCTION


T h e survey given above seems to show that a mode of reproduction and development
well fitted for an arctic area will normally be unfit in a temperate or a tropical region
of the sea, and it seems reasonable to seek one of the main reasons for the restricted
distribution of species in this fact. T h e question then arises whether the mode of
reproduction and development is fixed for the individual species throughout its area
of distribution or whether the species is able to change its mode of reproduction and
development in accordance with the environment. This latter ability-poecilogony-
was first mentioned by Giard (1904), who gives a number of examples of its occurrence
30 G. THORSON
in the sea, which, as far as the echinoderms are concerned, have proved to be wrong
(Mortensen, 1921, p. 241). That the ability exists is, however, a fact, although it is
nearly or totally absent in some animal groups, but plays a great part in others.
Recently acquired knowledge is sufficient to merit examination of some of the larger
groups of marine invertebrates to determine the proportion of species with more
than one type of reproduction at their disposal.
Among the Actinozoa most forms in temperate seas reproducing by eggs and
pelagic larvae have one more mode of reproduction at their disposal, that is, either
brood protection or asexual reproduction (fission, laceration), but rarely both modes
(Stephenson, 1929, p. 159). In the Porifera asexual reproduction (gemmulae and
gemmula-larvae) may occur in species which reproduce by eggs and larvae also
(H. J. Wilson, 1894). I n the Echinodermata, a few species reproduce both asexually
(by division) and by eggs, but the great majority have only sexual reproduction of
a very constant type throughout their area of distribution. In the Prosobranchia a few
species (three cases known) may change from nurse-egg feeding with a non-pelagic
development to a type where all eggs develop into pelagic larvae; a few species
(Lacuna pallidula and Brachystomia rissoides) may vary in egg size but not in larval
type, but the overwhelming majority of forms have only one mode of reproduction
and development at their disposal throughout their area of occurrence (Thorson,
1946). In the Opisthobranchia only one type of reproduction and development is
known for each single species, and the same is the case in the Lamellibranchiata,
where, however, the size of prodissoconch I and the metamorphosing veligers
indicate a certain lability of the length of the pelagic life, without changes in the
principal mode of larval development. Even in the Crustacea the mode of reproduc-
tion and development seems to be very constant in a single species throughout its
area of distribution. T h e few exceptions, namely, Balanus balanoides whose larvae,
normally hatched as nauplii, may instead hatch in the cypris stage; the amphipod
Mellitapellucida with varying egg sizes in different localities, and, among the shrimps,
Palaemonetes varians with larger eggs in fresh than in brackish water, and Crangon
crangon, small summer eggs and larger winter eggs (for references see Thorson,
1946),by no means disturb the general picture. Thus, apart from the actinians and
the sponges, whose conditions of reproduction and distribution deserve closer study
in the coming years, all the groups mentioned above seem to be very constant in
their mode of reproduction and development throughout their area of occurrence.
In the Polychaeta conditions are quite different. Here individual species often
show an astonishing lability in their mode of reproduction and development: from
asexual to sexual, from viviparity and brood protection to pelagic larvae. Examples
are Nereis dumerilii (four modes of sexual reproduction, including viviparity, pelagic
and non-pelagic development, Hempelmann, I 91 I ) , N . xonata (East Greenland :
non-pelagic development in the inner fjords, pelagic larvae at outer coast, un-
published), N . pelagica (non-pelagic development at Cherbourg, I 8 days’ pelagic
life at Plymouth, Herpin, 1925; Wilson, 1932a), Syllis vivipara, which seems to be
only a young viviparous form of the oviparous S. prolifera, and Ehlersia nepiotoca,
Reproductive and larval ecology of invertebrates 31
a young viviparous form of the oviparous Ehlersia sexoculata (Mesnil & Caullery,
1916), Harmothoe imbricata (brood protection in arctic seas, free eggs and swimming
larvae in Danish seas, Izuka, 1912;Thorson, 1936, 1946), Spio jilicornis (pelagic
larvae in spring, non-pelagic embryos feeding on nurse eggs in late summer, Mesnil
& Caullery, 1917), Pygospio elegans (able to reproduce with larvae of nearly all types
from entirely non-pelagic ones feeding on nurse eggs to those with a long pelagic
life varying within the areas in which they live and the seasons of the year, Thorson,
1946), Cirratulus cirratus (brood protection in the Falklands and gelatinous spawn
with non-pelagic development in northern seas, Fauvel, 1916; Cunningham &
Ramage, I 888), Arenicola claparkdei (pelagiclarvae in Japan, non-pelagic development
at Puget Sound, Okuda, 1938, Guberlet, 1934), Dodecacmu concharum (three types
of sexual reproduction, two modes of asexual reproduction, Mesnil & Caullery,
1898a, b ; Dehorne, 1927; Martin, 1933), and Pomatoceros triqueter (normally
oviparous with a very short pelagic life, occasionally viviparous with non-pelagic
young, v. Drasche, 1884; Gravier, 1923, p. 218). To these may be added the varying
egg sizes of Terebellides stroemi, Nicolea xostericola and Ampharete grubei (Thorson,
1946). As the modes of reproduction in the polychaetes are still very little known,
future observations will, no doubt, add a number of examples to those mentioned
here, which extend nevertheless over the whole polychaete group from the most
primitive to the most specialized forms.
It should be pointed out here that in the polychaetes the varying egg sizes play
a much greater part in competition than, for instance, in the echinoderms and
nemerteans. In these latter groups the planktotrophic, pelagic larvae (plutei,
auricularia, bipinnaria, and pilidium) belong to quite another larval type than the
barrel-shaped or ovoid lecithotrophic larvae (cf. Fig. 3). In these groups a change
from a planktotrophic to a lecithotrophic larval type caused only by a small increase
of the egg volume seems to be totally excluded. In the polychaetes, however, the
planktotrophic and the lecithotrophic larvae are principally of the same shape as well
as type of organization. The only difference is that the lecithotrophic larvae contain
more yolk, that is, they are fatter than the planktotrophic ones, and have no or
reduced swimming cilia, shorter swimming bristles, and the intestine not yet con-
nected with the mouth (cf. Fig. 3 I, K). Here it seems most likely that a small
increase in egg volume may cause the polychaete larvae to change from a plankto-
trophic to a lecithotrophic form, which, of course, makes the larvae much more
capable of competing in ecologically different areas.
When studying, in 1937,the fauna of the Persian Gulf, I found to my astonishment
that this sea-area-which is among the warmest in the world-harboured several
species of polychaetes already familiar to me from earlier studies in high arctic, East
Greenland, waters, while all the Persian Gulf species of echinoderms, molluscs, and
crustaceans were new to me and unknown in the Northern Atlantic. Although
historical reasons may be involved here, it seems reasonable to relate this cosmopolitan
distribution of a number of polychaetes to their ability to change their mode of
reproduction in accordance with ecological conditions. I n order to replace these
32 G. THORSON
accidental observations by exact figures, I listed all the species of polychaetes,
echinoderms, prosobranchs and lamellibranchs known from the coastal zone (from
depths less than 300 m.) within the area: Ireland, Southern England, the Channel,
Portugal, and the Azores, i.e. the Lusitanian area of the European coast, to see how
many of these species had also been found in the Indian Ocean area (from, but
exclusive of, Australia to Madagascar) including the Red Sea and the Persian Gulf.
Fortunately, the main parts of the polychaete fauna of the two areas have been
worked up by the same zoologist, one of our greatest recent authorities on polychaete
systematics, Pierre Fauvel, so we may be reasonably sure that species from European
and Indian seas mentioned under the same name are really identical."
The results arrived at are as follows:

Polychaetes I44 (28'4%)


Echinoderms 2 (2.2%)
Prosobranchs (0.7 %)
Lamellibranchs 216 4 (1.9%)

While 28.4% of the Lusitanian polychaetes (278 Polychaeta errantia, 230 Poly-
chaeta sedentaria) are also found in the Indian Ocean area, the average numbers of
species of Lusitanian echinoderms, prosob ranchs, and lamellibranchs found in
Indian seas is less than 2 "/, and while the number of polychaete species common to
the two areas seems to be steadily increasing after each new collection is worked up,
a thorough revision of the common species of the other groups seems, on the contrary,
to reduce their number. 'Thus, previously, the lamellibranch Saxicava rugosa has
been enumerated among the cosmopolitan species, but Lamy (1923)has shown that
the tropical forms belong to distinctly different species, and also the world-wide
distribution of Mytilus edulis has been severely questioned. The four species of
Lusitanian lamellibranchs actually found in the Indian Ocean area are here only
known from the Red Sea, and may thus have migrated through the Suez Canal. The
only Lusitanian prosobranch actually found in Indian seas is Lamellaria perspicua,
and the two echinoderms common to the two areas are Amphipholis squamata and
Echinocardium cordatum.
Dr Olga Hartman, the American authority on polychaete systematics, who uses
the word 'species' in a more narrow sense than Fauvel, has kindly placed her un-
published list on Californian polychaetes at my disposal. Using this list, Mrs E.
Wesenberg-Lund and I found that 18--20% of the polychaete species living along
the European West coast were also found in California, while the number of West
* The literature used in working out the list for the polychaetes was: Aziz (1938),Fauvel (1911,
1923, 1927,1932,1939),Mesnil & Fauvel (1939),Monro (1937),and E. Wesenberg-Lund (1949);
for the echinoderms: Koehler (1904,1905,1910,1921, 1924), Koehler & Vaney (I~IO),Meijere (1904).
Mortensen (1927, 1940),Nobre (1930-31),and Sluiter (1901); for the two molluscan groups: Daut-
zenberg & Bavay (1912),Dautzenberg & Fischer (1925),Jeffreys (1863-9),Lamy (1923),Lynge (1909),
Melvill& Standen (1901-6),Nobre (193z),Prashad (1932),Scheprnan (1908-13), and Watson (1897),
and for all groups: the Plymouth Marine Fauna (1931).
Reproductive and larval ecology of invertebrates 33
European species of echinoderms, prosobranchs and lamellibranchs living in
Californian waters amounts to less than 2%.
Here again the difference between the polychaetes and the other groups is so
striking, and the ability of the former group to compete under totally different
conditions so astonishing, that the explanation must be sought in the resistance of
this group during the most sensitive stages of its life cycle, i.e. during its reproduction
and larval development.

VIII. THE SHELL APEX THEORY


While in high arctic seas we know a few polychaetes, lamellibranchs and echinoderms
which reproduce by pelagic larvae in spite of the poor conditions prevailing there,
all high arctic prosobranchs hitherto examined proved to have a non-pelagic develop-
ment (Fig. 5)) and not a single larval prosobranch is known from arctic or antarctic
plankton. As, in contrast to this, in the tropical marine area round the Bermudas up
to 85 yoof the prosobranchs reproduce by pelagic larvae, and as the individual proso-
branch species has aconstant mode of reproduction throughout its area of distribution,
this group of animals seems to be a very fine ‘barometer’ of ecological conditions.
The American conchologist, Dall (1924)) points out that the shape of the top
whorls-the apex-of shells of adult prosobranchs is often different, even in closely
related species, probably as a result of different modes of development, but he did
not draw the logical conclusion from this observation, namely, that the shape of the
apex may inform us whether the species in question has a pelagic or a non-pelagic
mode of development. To-day we know the mode of development of about 200
species of prosobranchs, the larval type of which was unknown when Dall published
his paper. Thus we have the opportunity to test the above hypothesis. As a general
rule, a clumsy, large apex points to a non-pelagic development, while a narrowly
twisted apex, often with delicate sculptures, points to a pelagic development. As,
however, the notion ‘a clumsy or a narrowly twisted apex’ is different in large and
in tiny adult shells and may even be different in temperate and tropical genera (in
tropical genera the pelagic larvae may attain a much larger size of shell before leaving
the plankton than in temperate genera, cf. Dawydoff 1940, Lebour, 1945), a general
rule valid for all apices cannot be given. Only when we know the type of apex
derived from a pelagic or a non-pelagic development within the individual genus,
can reliable results be obtained. Fig. 6 shows the conditions in the genus Natica
( = Polynices) in which the species N . montagui and N . nitida having a pelagic, and
N . pallida and N . clausa a non-pelagic mode of development. It is my hope during
the coming years to be able to study more closely these interesting problems which,
thoroughly elaborated, may give also valuable information about the larval develop-
ment in fossil species, and, at least in broad features, about the conditions of phyto-
plankton production. D r H. Lemche, with whom I have collaborated in the apex
studies mentioned above, in a recent paper (1948), has given good evidence that
such studies may give reliable results concerning larval development even in tecti-
branch gastropods.
B R XXV 3
34 G. THORSON
The paleo-ecological significance of these apex studies is further supported when
combined with modem studies on oxygen isotopes in calcareous shells of marine
invertebrates. Urey (1948) has shown that the ratio of oxygen isotopes ( 0 l 8 to 0 l 6 )
in such calcium carbonate secretions varies with the temperature prevailing in the
sea when the secretion took place. ‘It is evident that, if an animal deposits calcium
carbonate in equilibrium with water in which it lives, and the shell sinks to the
bottom of the sea and is buried securely in the earth and remains unchanged from
that time to this, it is only necessary to determine the ratio of the isotopes of oxygen

Fig. 6. Top-whorls of four species of the prosobranch genus Nuticu showing two species with a
pelagic (above) and two species with a non-pelagic larval development (below).

in the shell to-day in order to know the temperature at which the animal lived’
(Urey, 1948, pp. 491-2). When combining Urey’s inspiring theories, supported by
his subtle technique, with our recent knowledge of marine ecology, it seems possible
not only to find out the average temperature at which the shell-secreting animals
lived, but-using the rings of growth distinctly marked, for instance in several large
lamellibranchs-it seems possible by special analysis of summer rings and winter
rings to find out the temperature amplitudes of these ancient seas.
Urey states that careful work during many years is required if his temperature
scale is to be fully reliable, and several years will also elapse before the apex theory
outlined above will be fully worked up. The perspectives are, however, very
promising, and give a good example of the significance of collaboration between
widely different branches of modem science.
Reproductive and larval ecology of invertebrates 35
IX. SUMMARY
I . In analysing the ecological conditions of an animal population we have above
all to focus our attention upon the most sensitive stages within the life cycle of the
animal, that is, the period of breeding and larval development.
2. Most animal populations on the sea bottom maintain the qualitatively composi-
tion of the species composing them, over long periods of time, though the individual
species use quite different modes of reproduction and development. This shows
that species producing a large number of eggs have a larger wastage of eggs and
larvae than those with only a few eggs. The wastage of eggs in the sea is much larger
than on the land and in fresh water.
3. In the invertebrate populations on the level sea bottom, large fluctuations in
numbers from year to year indicate species with a long pelagic larval life, while
a more or less constant occurrence indicates species with a very short pelagic life or
a non-pelagic development.
4. In most marine invertebrates which shed their eggs and sperm freely in the
water, either ( a ) the males are the first to spawn, thus stimulating the females to
shed their eggs, or ( b ) an ‘epidemic spawning’ of a whole population takes place
within a few hours. Both methods greatly favour the possibility of fertilization of
the eggs spawned and show that the heavy wastage of eggs and larvae takes place
after fertilization, during the free swimming pelagic life.
5 . Embryos with a non-pelagic development may originate ( u ) from large yolky
eggs, in which case all the hatching young of the same species will be at the same
stage of development, or ( b ) from small eggs which during their development feed
on nurse eggs, when the individual embryos of the same species may vary enormously
in size at the stage of hatching.
6 . Three types of pelagic larvae are known: (a)Lecithotrophic larvae, originating
from large yolky eggs spawned in small numbers by the individual mother animals;
they are independent of the plankton as a source of food although growing during
pelagic life, are absent from high arctic seas but constitute about 10% of the species
with pelagic larvae in all other seas. ( b ) The planktotrophic larvae with a long
pelagic life, originating from small eggs spawned in huge numbers by the individual
mother animal; they feed from, and grow in, the plankton, constituting less than
5 yo of high arctic bottom invertebrates, 55-65 yoof the species in boreal seas, and
80-85 % of the tropical species. (c) The planktotrophic larvae with a short pelagic
life having the same size and organization at the moment of hatching and at the
moment of settling; these constitute about 5% of the species in all Recent seas.
7. To find out the factors which cause the enormous waste of eggs and larvae, we
thus have to study those forms (constituting 70% of all species of bottom inverte-
brates in Recent seas) which have a long planktotrophic pelagic life, as only species
reproducing in this way have really large numbers of eggs.
8. The food requirements of the planktotrophic pelagic larvae are much greater
than those of the adult animals at the bottom. The adaptability of the larvae to poor
3-2
36 G. THORSON
food conditions seems, nevertheless, to be greater than hitherto believed. T h e
significance of starvation seems mainly to be an indirect one: poor food conditions
cause slow growth, prolong larval life, and give the enemies a longer interval of time
to attack and eat the larvae.
9. At the temperatures to which they are normally exposed, northern as well as
tropical larvae seem on an average to spend a similar time (about 3 weeks) in the
plankton. The length of the pelagic life of the individual species may, however, vary
significantly in nature. In the Sound (Denmark) the larvae are never exposed to
temperatures outside the range which they are able to endure. The wastage caused
by temperature, like that due to starvation, seems mainly to be an indirect one : low
temperatures postpone growth and metamorphosis, and give the enemies a longer
time to feed on the larvae.
10. When a larva feeding on a pure algal diet metamorphoses into a carnivorous
bottom stage, a ‘physiological revolution’ occurs and a huge waste of larvae might
be expected. Experiments have, however, shown that this is not the case.
1 1 . Young pelagic larvae are photopositive and crowd near the surface; larvae
about to metamorphose are photonegative. Larval polychaetes, echinoderms, and
presumably also prosobranchs, may prolong their pelagic life for days or weeks until
they find a suitable substratum. Forced towards the bottom by their photonegativity
and transported by currents over wide bottom areas, testing the substratum at
intervals, their chance of finding a suitable place for settling is much better than
hitherto believed.
12. Continuous currents from the continental shelf towards the open ocean may
transport larvae from the coast to the deep sea where they will perish. Such condi-
tions may (for instance in the Gulf of Guinea) deeply influence the composition of
the fauna, while in other areas (European western coast, southern California) they
seem to be only of small significance.
13. The toll levied by enemies appears to be the most essential source of waste
among the larvae. A list of such enemies, comprising other pelagic larvae, holoplank-
tonic animals and bottom animals, is given on p. 20. A medium-sized Mytilus
edulis, filtering 1-4 1. of water per hour, may retain and kill about IOO,OOO pelagic
lamellibranch larvae in 24 hr. during the maximum breeding season in a Danish
fjord.
14. Species reproducing in a vegetative way, by fission, laceration, budding, etc.,
might be expected to have good chances of competition in such areas where condi-
tions for sexual reproduction are unfavourable. Nevertheless, they only supply
a rather small percentage of the animal populations of all Recent seas, probably
because their intensity of reproduction is low and because they are unable to spread
to new areas. Most forms reproducing in a vegetative way have sexual reproduction
as well.
15. Pelagic development is nearly or totally suspended in the deep sea, and is
restricted to the shelf faunas. I n the arctic and antarctic seas pelagic development
is nearly or totally suppressed, even in the shelf faunas, but starting from here the
Reproductive and larval ecology of invertebrates 37
percentage of forms with pelagic larvae gradually increases as we pass into warmer
water, reaching its summit on the tropic shelves.
16. In order to survive in high arctic areas a planktotrophic, pelagic larva has to
complete its development from hatching to metamorphosis within 1-1 3 months
(i.e. the period during which phytoplankton production takes place) at a temperature
below 2-4O C. Most larvae, that is in 95% of the species, are unable to do SO and
have a non-pelagic development, but if a pelagic larva is able to develop under these
severe conditions the planktotrophic pelagic life seems to afford good opportunities
even in the Arctic. Thus the 5 % of arctic invertebrates reproducing in this way
comprise several of the species which quantitatively are most common within the
area.
17. The antarctic shore fauna has poor conditions similar to those ofthe Arctic. The
longest continuous periods of phytoplankton production are 2 and 3 weeks respec-
tively, and pelagic larvae have, in order to survive, to complete their development
within this short space of time at a temperature between I and 4’ C. Accordingly,
non-pelagic development is the rule, but most arctic species are able to support their
non-pelagic development by means of much smaller eggs than the antarctic species,
where brood protection and viviparity is dominant. The antarctic fauna has apparently
had a longer time to develop its tendency to abandon a pelagic life. The greater the
size of the individual born, the smaller its relative food requirements and the better
its chance of competing under poor food conditions.
18. The relatively few data on reproduction in deep sea invertebrates point to
a non-pelagic development. The larvae of such forms, in order to develop through
a planktotrophic pelagic stage, would have to rise by the aid of their own locomotory
organs through a water column 2000-4000 m. high or more (often with counteracting
currents) to the food producing surface layer, and to cover the same distance when
descending to metamorphose and settle.
19. The ecological features common to the deep sea, the arctic and the antarctic
seas, which enable the same animals to live and to reproduce there, contribute to
explain the ‘equatorial submergence’ of many arctic and antarctic coastal forms.
20. In the tropical coastal zones where the percentage of species with pelagic
larvae reaches its maximum, the production of food for the larvae takes place much
more continuously than in temperate and arctic seas, because light conditions enable
the phytoplankton to assimilate all the year round. The tropical species of marine
invertebrates breed (in contrast to temperate and arctic species) within such different
seasons that their larval stock, taken as a whole, is more or less equally distributed in
the plankton all the year round. This makes the competition in the plankton less
keen.
21. The fact that a mode of reproduction and development, well fit for an arctic
area, is unfit in a temperate or tropical area of the sea is probably one of the main
reasons for the restricted distribution of species.
22. In most groups of marine invertebrates the individual species have only one
mode of reproduction and development, which accordingly restricts their area of
38 G. THORSON
distribution. In the polychaetes, however, the individual species often show an
astonishing lability in their mode of reproduction and development which enables
them to compete in wide areas of the sea, Thus, out of the Western European species
of polychaetes, 28.4% have been found also in the Indian Ocean, and IS%, at least,
along the Californian coast, while the corresponding number of Western European
echinoderms, prosobranchs and lamellibranchs found also in the Indian Ocean and
California amounts to less than 2%.
23. The pelagic or non-pelagic development of marine prosobranchs has proved
to be a very fine ‘barometer’ for ecological conditions. Recent observations, still
not elaborated, seem to indicate that the shape of the top whorls, the apex, of the
adult shells of prosobranchs may show whether the species in question has a pelagic
or a non-pelagic development. This discovery may also give us valuable information
about the larval development in fossil species, and help us to form an idea about
ecological conditions in sea areas from earlier geological periods.
1 am much indebted to Dr Gordon Gunter, Institute of Marine Science, University of Texas,
Port Aransas, Texas, for correcting the manuscript.

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