Professional Documents
Culture Documents
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
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.
t
..*
V
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.
280
-8
240- i
- !
200
- , i
- Weight in g. per sq.m. bottom in Sallingsund
160
- : (the Limfjord) during 1918-26
- - *
120 -
80 - \
t.
::
60
' i
: t
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.
(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).
( 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.
( 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.
-
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
( 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.
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.
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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