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DISCOVERY REPORTS

VOLUME XXXI

DISCOVERY REPORTS

Issued by the National Institute of Oceanography

VOLUME XXXI

CAMBRIDGE

AT THE UNIVERSITY PRESS

1962

PUBLISHED BY
THE SYNDICS OF THE CAMBRIDGE UNIVERSITY PRESS

Bentley House, 200 Euston Road, London, N.W.i

American Branch: 32 East 57th Street, New York 22, N.Y.

West African Office: P.O. Box 33, Ibadan, Nigeria

Printed in Great Britain at the University Press, Cambridge
{Brooke Crutchley, University Printer)

CONTENTS

SWIMBLADDER STRUCTURE OF DEEP-SEA FISHES IN RELATION TO THEIR
SYSTEMATICS AND BIOLOGY (published 7th November i960)

By N. B. Marshall

Introduction PaSe 3

Material and Methods 5

Survey of Structure 6

Structure and Systematics 5°

The Swimbladder as a Hydrostatic Organ 68

Bathypelagic Fishes without a Swimbladder 81

Vertical Distribution and the Swimbladder 82

The Physics and Biology of Vertical Migrations 85

Pelagic and Benthic Fishes, the Swimbladder, and Aspects of the Economy of Deep-Sea

Life 95

Summary IJ3

References IJ6

Plates I-III following page 122

THE BENGUELA CURRENT (published 30th November i960)
By T. John Hart and Ronald I. Currie

Introduction Page I27

Previous Work I3°

Methods used in the 'William Scoresby' 135

Itineraries H1

Coastal Geography and Bottom Topography 144

Meteorology H7

Surface-Currents J53

Observed Distribution of Temperature and Salinity 156

The Water Masses J75

Upwelling J^4

Non-Conservative Properties l92

Bottom Deposits ; 204

Microplankton 20°

zooplankton 2°8

Economic Resources of the Benguela Current 274

Review of the Main Features of the Benguela Current 277

Comparison of the Benguela Current with other upwelling regions .... 280

Organic Production in the Benguela Current 284

Summary 2°°

References 2°9

80442

vi CONTENTS

THE APPENDAGES OF THE HALOCYPRIDIDAE (published 13th March 1961)
By E. J. lies

Introduction page 301

The Appendages, Their Interrelation and Function 302

Feeding-Mechanism 3X^

The Appendages in other Halocyprididae 321

Comparison of Halocyprididae and Cypridinidae 322

Summary 324

References 325

REPRODUCTION, GROWTH AND AGE OF SOUTHERN FIN WHALES (published
1st November 1961)

By R. M. Laws

General Considerations page 331

The Ovaries 341

Graafian Follicles 345

The Corpus Luteum 352

Corpora Albicantia, Corpora Aberrantia and Corpora Atretica 363

Accumulation of Corpora up to the Attainment of Physical Maturity .... 385

The Reproduction Cycle 394

Newly Mature Females 409

Multiparous Females 425

Age-Determination of Means of the Ovarian Corpora 459

Summary 477

References 482

Plates IV-VII following page 486

DISCOVERY &r l

REPORTS

Vol. XXXI, pp. 1-122

Issued by the National Institute of Oceanography

SWIMBLADDER STRUCTURE OF DEEP-SEA

FISHES IN RELATION TO THEIR

SYSTEMATICS AND BIOLOGY

N. B. Marshall

CAMBRIDGE

AT THE UNIVERSITY PRESS

1960
Price Fifty-five shillings net

PUBLISHED BY

THE SYNDICS OF THE CAMBRIDGE UNIVERSITY PRESS

Bentley House, 200 Euston Road, London, N.W. 1

American Branch : 32 East 57th Street, New York 22, N.Y.

Printed in Great Britain at the University Press, Cambridge
{Brooke Crutchley, University Printer)

[Discovery Reports. Vol. XXXI, pp. 1-122, Plates I-III, November i960.]

SWIMBLADDER STRUCTURE OF DEEP-SEA

FISHES IN RELATION TO THEIR

SYSTEMATICS AND BIOLOGY

N. B. MARSHALL
British Museum (Natural History)

^ H- 0
Wood*

CONTENTS

Introduction page 3

Material and Methods 5

Survey of Structure 6

Classification of the species considered 6

Order Isospondyli 7

Suborder Stomiatoidea 7

Suborder Salmonoidea ......... 27

Suborder Clupeoidea 3°

Order Iniomi 3°

Suborder Myctophoidea 3°

Suborder Alepisauroidea 43

Order Miripinnati 43

Order Cetunculi 43

Order Giganturoidea .......... 44

Order Lyomeri ........... 44

Order Allotriognathi 44

Order Berycomorphi 45

Order Percomorphi 48

Order Pediculati 5°

Suborder Ceratioidea 5°

Structure and Systematics 5°

The larval swimbladder 59

The swimbladder wall 60

Mechanical properties of the swimbladder wall 63

Fat-invested swimbladders 65

The Swimbladder as a Hydrostatic Organ 68

The gas-producing complex 69

The retia mirabilia 69

The gas-gland 73

The resorbent part of the swimbladder 78

Bathypelagic Fishes without a Swimbladder 81

Vertical Distribution and the Swimbladder 82

Compressibility of gases 84

Energy requirements of the swimbladder 84

Gas requirements of the swimbladder 84

The Physics and Biology of Vertical Migrations .... 85

The evidence of vertical migrations 85

The physical and biological environment 86

Physical problems 89

Thermocline crossers 89

Gas secretion 89

Gas resorption 92

Partial migrators 94

Gas secretion 94

Gas resorption 95

Pelagic and Benthic Fishes, the Swimbladder, and Aspects of the

Economy of Deep-sea Life 95

Summary IJ3

References IJ6

Plates I-III follotoing p. 122

SWIMBLADDER STRUCTURE OF DEEP-SEA

FISHES IN RELATION TO THEIR

SYSTEMATICS AND BIOLOGY

By N. B. Marshall

British Museum (Natural History)

(Plates I— III, Text-figures 1-47)

" When one picks up a fish, one may be said, allegorically, to hold one of the knots in an endless web of
netting, of which the countless other knots represent other facts, whether of marine chemistry, physics
or geology, or other animals and plants. And just as one cannot make a fish-net until one has tied all the
knots in their proper positions, so one cannot hope to comprehend this web until one can see its inter-
nodes in their true relationship." bigelow (icno)

INTRODUCTION

IN both structure and function the teleost swimbladder is one of the most plastic of vertebrate
organs. While it is primarily a hydrostatic organ, making a fish weightless in water, it may also be
modified for respiratory, sensory and sound-producing activities (Jones and Marshall, 1953). Apart
from the respiratory aspect, this statement is equally true of many deep-sea fishes. And the exception
is understandable, for the use of the swimbladder as a lung is obviously limited to physostomatous
teleosts, those with a pneumatic duct joining the sac to the foregut. Virtually all deep-sea fishes
have a completely closed (physoclistous)1 swimbladder.

Cuvier and Valenciennes (1848) appear to have been the first to discover a swimbladder in a deep-
sea fish. Concerning the salmonoid genus Argentina, Valenciennes wrote as follows: 'La vessie
natatoire de l'Argentine a un autre caractere anatomique et physiologique fort interessant pour nos
etudes; elle ne communique pas avec le canal digestif; je n'ai pu du moins trouver de conduit pneu-
matique dans les trois individus d'especes differentes que j'ai disseques et dont les visceres etaient
cependant parfaitement conserves.' (In the following volume (1850) they record the presence of a
swimbladder in the hatchet fish, Argyropelecus hemigymnus.) Nearly forty years later, Giinther (1887)
made a similar observation in his ' Challenger ' Report : ' In none of the abyssal forms examined by me
have I found an open communication between the air bladder and the oesophagus, not even in those
which are referred to the Physostomatous division.'

In defining the family Sternoptychidae, in which he included the deep-sea fishes, Sternoptyx,
Ichthyococcus, Maurolicus, Gonostoma and Chauliodus, Giinther (1864) stated that the swimbladder
was simple when present. But under the family Scopelidae (containing fishes now placed in the
order Iniomi) he remarked that the swimbladder was absent, a statement that is true with the notable
exception of the lantern fishes (Myctophidae).

There are other observations on the structure of the swimbladder in Giinther's 'Challenger'
Report (1887) on deep-sea fishes. Further reference will be made to these later, but we may notice
here that the rete mirabile of Gonostoma denudatum was described as a 'conical muscular body'
attached to the posterior ventral part of the swimbladder. This confusion is hardly surprising, for the
gas-secreting complex (retia mirabilia and gas-glands) of deep-sea fishes is highly developed. The
large rete of G. denudatum contains thousands of closely associated arterial and venous capillaries

1 See page 50.

4 DISCOVERY REPORTS

running forward in parallel to supply the gas-gland, and superficially these small blood-vessels look

very like the fibres in a muscle.

However, a year before the publication of Giinther's Report, Coggi (1886) had described certain
structures in the swimbladders of G. denudatum and Scopelus benoiti ( = Hygophum benoiti). He re-
marked that the ' red bodies ' (retia mirabilia) of these two species were very like those of physoclistous
teleosts and that the cells in the epithelial body (gas-gland) of Gonostoma were very large. In the
other species Coggi figured three retia mirabilia, each supplying a corresponding lobe of the gas-
gland. We shall see later that this is a constant feature of the myctophid swimbladder. But his finding
of an opening into the ' pneumatic duct ' is an error. Presumably he found the opening into the gas-
resorbing part of the swimbladder, which in myctophids is an ' oval ', and is placed at the front of the
sac (see pp. 30-42).

Apart from this early account, the only other detailed work on the structure of the swimbladder of
bathypelagic fishes has been that of Rauther (1922) on the lantern fish, Diaphus rafinesqnei and
Nusbaum-Hilarowicz (1920) on the hatchet fishes Sternoptyx and Argyropelecus, and a species of
Cyclothone. Ray (1950) was the first to find and figure a fat-invested swimbladder, this being in the
lantern fish, Lampanyctus leucopsarus. In his report on deep-scattering layers in the Monterey Bay
area, Barham (1957) referred to work by Jollie (1954, Ph.D. Thesis) on the anatomy of this organ.

There are numerous records of the presence or absence of the swimbladder in both pelagic and
benthic deep-sea fishes in Alcock's (1899) Investigator Report. Concerning benthic fishes only, Holt
and Calderwood (1895) described the swimbladder of the deep-sea gadoid, Mora and those of certain
macrourids. Presence or absence observations may also be found in Garman (1891) and in a few
other papers which will be referred to in the descriptive part of this report. Lastly, Beebe and
Vander Pyl (1944) gave the dimensions of the swimbladder in two lantern fishes, Myctophum affirie
and Lampanyctus macropterus, while Kanwisher and Ebeling (1957) measured the volume and gas-
content of this organ in a number of bathypelagic fishes.

Considering only the observations made during the latter half of the nineteenth century, there is
evidence that the swimbladder is found in numerous deep-sea fishes. But despite this early work,
various authorities imposed a pattern on nature without further investigation. They decided that a
swimbladder could not function in the deep-sea environment owing to the high hydrostatic pressures,
and that it was therefore absent in deep-sea fishes. This organ is certainly absent in pelagic fishes
whose living-space is centred below the 1000-m. level, but it is present in many fishes that swim
above this depth and in numerous species living below, near the deep-sea floor.

The survey in this report has involved the examination of about ninety species of deep-sea fishes,
certain aspects of which have already been published (Marshall, 1950, 1951, 1954, 1955; Jones and
Marshall, 1953; Denton and Marshall, 1958). The first part is concerned with the description of the
swimbladders of bathypelagic fishes. It will be found that this organ is commonly present in a
number of major groups (e.g. the Gonostomatidae, Sternoptychidae, Myctophidae and Melam-
phaidae). In these and other fishes the gas-producing structures are highly developed.

In teleosts, the structural features of the swimbladder are not often of use in classification, but a
gratifying feature of this survey has been the discovery that this organ has a distinctive design in the
Stomiatoidea, deep-sea Salmonoidea, Myctophidae and Anoplogastridae. This aspect is considered
in the second part of the report and leads to discussion of the evolution of bathypelagic fishes.

Then follow sections concerned with the larval organ, the fine structure of the swimbladder wall,
and fat-invested swimbladders. In a number of species the swimbladder contains gas during the
larval phase which is passed in the surface-waters, but the organ regresses and is invested with fat
after metamorphosis to the adult form.

INTRODUCTION 5

The remaining sections are devoted to functional-morphological and biological aspects. Now,
development of the first aspect obviously depends on adequate knowledge of both form and function.
Having undertaken a survey to the point where generalizations on morphology could safely be made,
it was a pleasure to turn to the work of Dr P. F. Scholander and his colleagues on functional aspects
of the swimbladder in deep-sea fishes. Full reference is made to this work at a later stage. In parti-
cular, Scholander's (1958) concept of counter-current exchange in the retia mirabilia and his review
of this principle in biology has been very helpful.1 I am also indebted to Dr Ragnar Fange's (1953)
fine work on structure and functions of the euphysoclist swimbladder. In the section on the swim-
bladder as a hydrostatic organ, findings on the structure of the retia mirabilia and gas-glands are
considered in the light of this physiological work, a task that was made easier by my former colla-
boration with Dr F. R. Harden Jones (Jones and Marshall, 1953).

In the final biological section, the structural development (and absence) of the swimbladder in
bathypelagic fishes is considered in relation to vertical distribution and vertical migrations. This has
involved some consideration of the physical and biological environment and leads to the final part,
which begins with a survey of the swimbladder in benthic deep-sea fishes. Considering only the
fishes taken below a depth of 2000 m., at least half the number of species have capacious swimbladders.
In the pelagic environment, as already mentioned, this organ is absent in fishes concentrated below
the 1000-m. level. This surprising difference led me to consider, to use a concept more familiar to
botanists, the ' life forms ' of fishes from the upper and lower reaches of the bathypelagic environment.
Again, I was helped by former collaboration, this time with Dr E. J. Denton (Denton and Marshall,
1958). The buoyancy balance-sheet of a fish with a capacious, gas-filled swimbladder is such that it
can carry a firm skeleton and well-knit muscles. But these two tissue-systems and others are much
reduced in pelagic fishes living below a depth of 1000 m., although this is not surprising in view of the
poor food-supply around them. These fishes may well have lost the swimbladder simply because
there is not sufficient potential energy in their environment to maintain the ' extra ' tissues that can
be carried by this hydrostatic organ. In pursuing this, and other ideas, I have tried to follow the
thought behind the quotation that heads this report.

MATERIAL AND METHODS

Most of the fishes used in this report have been taken during the Discovery investigations. The
positions at which they were caught are listed under the name of each species in the descriptive
section (pp. 6-50) and unless otherwise indicated the station numbers refer to the Discovery col-
lections.

In nearly all instances, the swimbladder was found by dissecting the fish under a binocular micro-
scope. After noting the position of the organ, and where possible, tracing the blood supply, the swim-
bladder was removed and cut open so as to display the retial system and gas-glands. As these are
well-developed in deep-sea fishes, their structure was readily appreciated. Where sufficient material
was available more than one dissection was made.

In certain species (Cyclothone braueri, C. Hvida, Argyropelecus olfersii, A. aculeatus, Polyipnus
laternatus, Opisthoproctas soleatus, Vinciguerria attenuata, V. nimbaria, Myctophum punctatum and
Diaphus dofleini) the fine structure was studied by means of serial transverse sections. An account of
this work appears in the sections dealing with the swimbladder wall (pp. 60-65), fat-invested swim-
bladders (p. 65-68) and the swimbladder as a hydrostatic organ (p. 68-81).

1 To Scholander's list of organs in which this physiological principle is operative (the retia mirabilia of the teleost swim-
bladder, the gills of fishes, the placenta, the vertebrate kidney and the retial vascular structures of mammals) may be added
the choroidal gland of the eyes of bony fishes (see Barnett, 1951).

6 DISCOVERY REPORTS

In the descriptive section, measurements are given of the standard length of the fish dissected, the
major and minor axes of the swimbladder (which approaches an ellipsoid in form) and the length of
the retia mirabilia. Clearly, the dimensions of the sac in a preserved fish will be smaller than those
occurring in the living state. However, in most specimens the swimbladder was well expanded.
Where conditions were otherwise, this has been noted.

SURVEY OF STRUCTURE

Classification of fishes considered in this report1

Order ISOSPONDYLI

Suborder STOMIATOIDEA (p. 7)

Family Gonostomatidae : Vinciguerria attenuata Cocco (p. 7); V. nimbaria Jordan & Williams
(p. 9); PolHchthys mauli (Poll) (p. 9); Bonapartia pedaliota, Goode & Bean (p. 11); Maiirolicas
muelleri (Gmelin) (p. 11); Gonostoma denudatum Rafinesque (p. 13); G. elongatum Giinther (p. 13);
G. bathyphilum, Vaillant (p. 13); Photicthys argenteus Hutton (p. 13) Ichthyococcus ovatus (Cocco)
(p. 14); Cyclothone signata Garman (p. 15); C. braueri Jespersen & Taning (p. 16); C. Uvida Brauer
(p. 18); C. microdon (Giinther) (p. 19); C. acclinidens Garman (p. 19).

Family Sternoptychidae : Argyropelecus aculeatus Cuvier & Valenciennes (p. 19); A. olfersii
Cuvier (p. 20); A. sladeni Regan (p. 21); A. hemigymnus Cocco (p. 21); Sternoptyx diaphana Hermann
(p. 21); Polyipnus laternatus Garman (p. 22).

Family Astronesthidae : Astronesthes niger Richardson (p. 23); A. lucifer Gilbert (p. 23); A.
gemmifer Goode & Bean (p. 23); A. similis Parr (p. 25); Borostomias antarcticus (Lonnberg) (p. 26);
Diplolychnus mononema Regan & Trewavas (p. 26).

Family Stomiatidae : Stomias affinis Giinther (p. 26); S. colubrinus Garman (p. 27); S. ferox
Reinhardt (p. 27).

Family Melanostomiatidae: Bathophilns metallicns Welsh (p. 27); B. pawned Parr (p. 27);
Eustomias obscurus Vaillant (p. 27); Echiostoma tanneri (Gill) (p. 27).

Family Chauliodontidae: Chauliodus sloanei Schneider and C. barbatus Garman (p. 27).

Family Idiacanthidae: Idiacanthus fasciola Peters (p. 27).

Family Malacosteidae : Malacosteus niger Ayres and Photostomias guerni Collett (p. 27).

Suborder SALMONOIDEA (p. 27)

Family Opisthoproctidae : Opisthoproctus soleatus Vaillant (p. 27); O. grimaldii Zugmayer (p. 28);
Winteria telescopa Brauer (p. 28); Macropinna microstoma Chapman* (p. 28).

Family Microstomidae: Xenophthalmichthys danae Regan* (p. 28).

Family Bathylagidae : Bathylagus benedicti Goode & Bean* (p. 29) ; B. glacialis Lonnberg* (p. 29) ;
B. antarcticus Giinther (p. 29); B. argyrogaster Norman (p. 29).

Suborder CLUPEOIDEA (p. 30)
Family Alepocephalidae : Bathytroctes rostratus Giinther* (p. 30); Xenodermichthys copei (Gill)

(p. 30); Searsia koefoedi Parr (p. 30).

Order INIOMI

Suborder MYCTOPHOIDEA (p. 30)
Family Myctophidae: Myctophum punctatum Rafinesque (p. 30); Diaphus rafinesquei (Cocco)
(p. 30); Electrona tenisoni (Norman) (p. 32); E. rissoi (Cocco) (p. 32); E. antarctica (Giinther) (p. 32);

1 Species or groups marked with an asterisk were not examined by the author.

SURVEY OF STRUCTURE 7

Hygophum benoiti (Cocco) (p. 34); Benthosema glaciate (Reinhardt) (p. 34); B. suborbitale (Gilbert)
(p. 35); Diogenichthys atlanticus (Taning) (p. 36); Myctophum humboldti (Risso) (p. 36); M. affine
(Lutken)(p. 36); Diaphus dofleini Zugmayer (p. 37); D. garmani Gilbert (p. 37); D. luetkeni (Brauer)
(p. 37); D. agassizii Gilbert (p. 38); Notolychnusvaldiviae (Brauer)(p. ifi);La7npadenachavesi{Co\\zt\.)
(p. 38); Lampanyctus giintheri Goode & Bean (p. 38); L. alatus Goode & Bean (p. 38); L. pusillus
(Johnson) (p. 40); Gymnoscopelus nicholsi (Gilbert) (p. 41); G. townsendi (Eigenmann & Eigenmann)
(p. 41); Gonichthys coccoi (Cocco); Ctenobranchus nigro-ocellatus (Gunther); Diaphns coeruteus
Klunzinger and Gymnoscopelus braueri (Lonnberg) (p. 42).

Family Neoscopelidae : Neoscopelus macrolepidotus Johnson (p. 42); Scopetengys tristis Alcock

(P- 43)-

Family Scopelosauridae (p. 43).

Suborder ALEPISAUROIDEA (p. 43)
Order MIRIPINNATI (p. 43)
Order CETUNCULI
Family Cetomimidae: Ditropichthys storeri (Goode & Bean) (p. 43); Cetostoma regani (Zugmayer)

(P- 43)-

Family Rondeletiidae: Rondeletia bicolor Goode & Bean* (p. 44).

Order GIGANTUROIDEA : Gigantura vorax Regan (p. 44)
Order LYOMERI
Family Eurypharyngidae: Eurypharynx pelecanoides Vaillant (p. 44).
Family Saccopharyngidae : Saccopharynx ampullaceus Harwood* (p. 44).

Order ALLOTRIOGNATHI (p. 44)
Family Stylophoridae : Stylophorus chordatus Shaw (p. 44).

Order BERYCOMORPHI (p. 45)
Suborder ANOPLOGASTROIDEA

Family Stephanoberycidae : Stephanoberyx monae Gill (p. 45).

Family Melamphaidae: Melamphaes megalops Liitken (p. 46); M. unicornis Gilbert (p. 47);
M. mizolepis (Gunther) (p. 47); M. cristiceps Gilbert (p. 47).
Family Anoplogastridae : Anoplogaster longidens (Gill) (p. 47).

Order PERCOMORPHI (p. 48)

Family Chiasmodontidae: Chiasmodon niger Johnson (p. 48). Pseudoscopelus scriptus and Dysalotus

alcocki (p. 49)

Order PEDICULATI (p. 50)

Suborder CERATIOIDEA* (p. 50)

Order ISOSPONDYLI

Suborder STOMIATOIDEA Family Gonostomatidae

Vinciguerria attenuata Cocco (Text-fig. 1)

St. 254, 350 04' 00" S., 20 59' 30" E., 21. vi. 27, TYF, 20o(-o) m. B.M. Reg. no. 1930.1.12. 265-72. Standard

lengths of two fishes examined 43-5 and 39-5 mm.

The swimbladder of this gonostomatid lies above the stomach and ends over the origin of the pelvic

8 DISCOVERY REPORTS

fins (Text-fig. id). The sac is thin-walled and ellipsoidal in form, the measurements of the major
and minor axes in the 43-5-1111™. fish being 8-5 and 275 mm.

Text-fig. 1. Swimbladder of Vinciguerria attenuata, viewed: (a) dorsally; (b) ventrally; (c) laterally, and (d) in position in
body-cavity offish. Veins shown black, arteries white, av, artery-vein pair to gas-gland ; bpr, by-pass branch of retial artery;
en, resorbent capillary network;^, gas-gland ; ra, retial artery; rv, retial vein; rm, rete mirabile. (a, b and c, x 10; d, x 175.)
Note on orientation of swimbladder, in this and subsequent figures. Where the swimbladder is drawn with the major axis
vertical, the anterior end is uppermost. If this axis is horizontal, the anterior end is to the left.

In the larger fish, the rete mirabile, which is found at the rear end of the sac, is a massive cylindrical
structure with a length and diameter of o-8 mm. The gas-gland is a fairly broad transverse band of

SURVEY OF STRUCTURE 9

tissue investing the floor and lateral walls of the sac (Text-fig. ia-c). The forward, mid-ventral edge
of the gland lies about half-way along the length of the swimbladder. The median part runs across
the sac, while the lateral sections extend backwards and upwards to end just below the pigmented
roof.

The rete mirabile is bipolar1 in structure. It is formed from an artery and vein which break up into
several thousand closely intercalated capillaries, these running parallel courses along the length of
the organ. At the forward end they recombine into arteries and veins which supply the gas-gland.
Two lateral artery-vein pairs enter the gland behind and just below its two upper edges, while there
is a mid-ventral association of a vein with two flanking arteries. The vein runs forward to a point
about half-way between the rete and gas-gland and then forks before entering the gland. The two
arteries closely follow this venous path (see pp. 78-79 for stomiatoid blood circulation).

Behind the gas-gland there is an extensive capillary network running over the whole of the sac
(and just below its inner epithelium). The arterial supply comes from a branch of the retial artery,
which forks just before entering the rete. This branch runs forwards along the left side of the rete
to a point just in front of it and then gives off a number of sub-branches. In ventral aspect, the
vascular pattern may be appreciated by reference to Text-fig. ib. It will be seen that the artery
divides into three main sub-branches. Text-fig. ic also shows that one main sub-branch travels to
the roof of the sac and there subdivides into arterioles and capillaries.

The capillary circulation is completed by the three veins to the gas-gland, which give off lateral
venules. Those from the mid-ventral vessel and those from the lower sides of the two lateral vessels
are associated with the arterioles of the three ventral sub-branches referred to in the last paragraph.
The venules from the upper sides of the two lateral vessels divide to form capillaries that join those
of the single dorsal arterial sub-branch.

This capillary circulation forms the resorptive part of the swimbladder, the region where gases
diffuse into the blood when deflation of the sac becomes necessary.

The swimbladder of the smaller (39*5 mm.) fish has a very different appearance although its
structure is basically the same. But the comparison of these two swimbladders, coming from fishes
taken in the same haul, will best be left to a later section (p. 64-65).

Vinciguerria nimbaria Jordan & Williams
St. 1768, 330 49-8' S., 120 50-8' E., 19. v. 36, N 100 B, 290-i5o(-o) m. Standard length of fish 34 mm.

The structure of the swimbladder of this species is much like that of V. attenuata. The major and
minor axes of the ellipsoidal sac measured 5-5 and 2-0 mm.

Pollichthys mauli (Poll) (Text-fig. 2A-c)

St. 273, 90 38' 00" S., 120 42' 30" E., 31. vii. 27, N 100 B, n8(-o) m. B.M. Reg. no. 1930.1.12. 254-9. Standard
length 43 mm.

This species has a capacious, thin-walled swimbladder occupying much of the upper part of the
body cavity. The sac is ellipsoidal, the measurements of the major and minor axes in the above fish
being 5-0 and 2-2 mm. The posterior part of the organ fits snugly into a recess in the fore part of the
enlarged, rear section of the kidneys, while the anterior end lies above the stomach.

At the posterior extremity of the sac is a single, bulbous rete mirabile (length 1-2 mm.), which
supplies a horseshoe shaped gas-gland investing much of the floor and lateral walls of the swimbladder.
The gland fits round the rete and encircles an oval-shaped capillary area, which is set in the middle
part of the floor.

1 See also page 69.

DISCOVERY REPORTS

en gg

rm bpr

Text-fig. 2. Swimbladders of PoUichthys mauli, viewed (a) ventrally, (b) laterally, and (c) in position in body-cavity of
fish, and Bonapartia pedaliota, viewed (d) ventrally, (e) laterally, and (f) in position in body-cavity of fish. Veins shown black,
arteries white, a, artery to gas-gland; bpr, by-pass branch of retial artery; en, resorbent capillary network; gg, gas-gland;
ra, retial artery; rv, retial vein; rm, rete mirabile, vc, vein to capillary network, (a, X20; b, x 12-5; C, x 1-5 ; D, x 10; E, x 6;
f, xo-9.)

SURVEY OF STRUCTURE n

The rete, like that of Vinciguerria, is bipolar. At the forward end is a large median vein which soon
forks to send branches round the inner edges of the gas-gland. Each of these two branches is accom-
panied by an arterial vessel, an association supplying the anterior parts of the gland. The posterior
parts on either side of the rete also receive two artery-vein pairs (see Text-fig. 2).

The capillary network, through which gas may leave the swimbladder, is fed with arterial blood
through a vessel coming from the retial artery. This by-passes the rete and runs forward along the
mid-ventral line to give off arterioles that break up into capillaries. The venous part of the circulation
comes from the large median vein of the rete.

Bonapartia pedaliota Goode & Bean (Text-fig. 2D-f)
St. 1582, 05° 39-1' S., 460 22-3' E., 29. iv. 35, N 450 H, i900-i8so(-o) m. Standard length 67-0 mm.

The swimbladder of Bonapartia is a thin-walled, capacious ellipsoidal sac lying immediately in
front of the enlarged posterior part of the kidneys. When fully expanded it is likely to occupy more
of the body cavity than that shown in Text-fig. 2F. The major and minor axes of the sac measured
about io-o and 5-0 mm.

A large club-shaped rete mirabile (length 3-6 mm.) runs under the posterior part of the swim-
bladder floor. Again it is bipolar in structure, supplying the gas-gland through vessels that are formed
by the capillaries when they reach the anterior end of the organ. The gland, which is a single structure,
fits closely round the rete. Its form may best be appreciated by reference to Text-fig. 2D.

Immediately in front of the gland, and on the floor of the sac, is an oval-shaped capillary region.
As in Pollichthys and Vinciguerria, the arterial part of the circulation is provided by a branch of the
retial vessel. The venous part could not be traced in its entirety but seems to arise from two vessels
running forward through the gland. (These veins may also provide part of the glandular supply.)

Maurolicus muelleri (Gmelin) (Text-fig. 3)
St. 2072, 460 31-6' N., 070 42-9' W., 22. v. 37, TYFH, i7o(-o) m. Standard length 22 mm.

As in other gonostomatids, the swimbladder of Maurolicus lies forward of the posterior part of the
kidneys. The major and minor axes of the ellipsoidal sac spanned 4-5 and 2-0 mm. The walls were
quite thin, having a thickness of between 10 and 20//.

A single rete mirabile (length 075 mm.) is found at the posterior end of the sac and is formed by
an artery from the dorsal aorta and a vein from the cardinal vessel (between the kidneys).

The gas-gland is four-lobed. Two smaller, rounded lobes lie above and to the side of the front part
of the rete. The two larger lobes are oval in shape and extend over the floor and side walls of the
middle section of the swimbladder. The long axes of these two lobes are parallel to that of the sac
and measure 1-4 and 1-5 mm., the left being the larger. Each lobe receives a closely associated
artery-vein pair emerging from the front of the rete, which is thus bipolar in structure.

There is a fine-meshed network of capillaries (the resorbent surface) lying just below the inner
epithelium of the sac and between the lobes of the gas-gland. The median ventral area between the
two larger lobes extends forward beyond their anterior ends, while the two lateral areas between the
small and larger lobes extend upwards over the side walls of the sac. The arterial supply to the
capillary network comes from a branch of the retial artery, which runs forward under and beyond the
rete to a point close in front of its distal end, where it divides into three sub-branches. Two of these
run outwards, each between the corresponding small and large lobe of the gas-gland. The third sub-
branch proceeds forward along the mid-ventral line between the two large glandular lobes. These
three vessels give off lateral arterioles, which break up into capillaries. The four veins to the gas-
gland lobes complete the capillary circulation, each vein sending off branches that partly encircle the

I2 DISCOVERY REPORTS

lobe supplied. The forward and lateral edges of the two smaller lobes have a vein running round
them, while the whole of the inner edges and about half of the outer edges of the larger lobes are
similarly supplied with a venous system. The periglandular veins give off venules that divide again
and again to form a dense capillary system, which is eventually linked with that formed by the branch
of the retial artery. (The arteries to the lobes play no part in this capillary formation and do not
branch until they have entered the gland.) The pattern of arterioles and venules can best be appre-
ciated by reference to Text-fig. 3 a.

This extensive capillary complex forms the resorptive region whereby gases diffuse out of the
swimbladder and into the blood stream.

Text-fig. 3. Swimbladder of Maurolicus muelleri: (a) viewed ventrally, and (b) shown in position in the fish. Veins shown
black, arteries white. Note the two small and two large lobes of the gas-gland, av, artery-vein pair to gas-gland ; bpr, by-
pass branch of retial artery ; en, resorbent capillary network ; gg, gas-gland ; ra, retial artery ; rv, retial vein ; rm, rete mirabile,
(Swimbladder, x 30; fish, x 2.)

SURVEY OF STRUCTURE 13

Before continuing this survey, certain generalizations may be introduced at this stage. By doing
so the descriptions can be more readily followed and needless repetition avoided.

We have seen that the swimbladders of the foregoing species of gonostomatid fishes have certain
common features. These are: (1) a single, bipolar rete mirabile, which is formed at the posterior end
of the sac, and (2) a resorbent capillary system that obtains its arterial supply through a by-pass
branch of the retial artery. These characters are also shared by other stomiatoid fishes with a well-
formed swimbladder in the adult phase. Furthermore, the first feature, at least, can be traced in
adults with a regressed swimbladder. In the following descriptions, unless otherwise stated, the
lengths of the major and minor axes of the sac are given in parenthesis after the standard length of
the fish.

Gonostoma denudatum Rafinesque (Text-fig. 4 a)

B.M. Reg. no. 85.6.22. 73-6. Messina. Standard length 81 mm. (16-0 x 2-0 mm.)

The swimbladder is elongated and fits close beneath the kidneys, extending down some two-thirds
of the length of the body cavity. It originates above the bases of the pectoral fins and ends over the
pelvics. Reference to Text-fig. 4 a will show the close reciprocal relations between the shapes of the
swimbladder and kidneys.

The bipolar rete mirabile, which is club-shaped and about 2-5 mm. in length, runs straight into the
posterior end of the swimbladder floor. It is formed from two vessels running down through the
kidneys from the dorsal aorta and the cardinal vein. The gas-gland invests most of the swimbladder
floor and also extends over the lateral walls of the wider, posterior part of the sac.

Just before its point of entry, the retial artery gives off the by-pass branch to the capillary system.
Although not traced, this system must be formed immediately in front of the more extensive, posterior
part of the gas-gland.

Gonostoma elongatum Giinther (Text-fig. 4B, c)

St. 285, 20 43' 30" S., oo° 56' 30" W., 16. viii. 27, i25-i75(-o) m. B.M. Reg. no. 1930.1.12. 74-7. Standard
length 149 mm.

At first sight the swimbladder appears to be completely absent in this species. In place of the long
gas-filled sac found in G. denudatum is a long rod-like mass formed of golden-yellow fat globules
suspended in a reticulum of connective tissue cells. At the posterior end of this rod the fatty tissue
extends over a small cream-coloured body that receives an artery and vein running down through the
posterior enlarged part of the kidneys (see Text-fig. 4c). These vessels are clearly homologous with
those forming the rete mirabile in G. denudatum. In fact, the creamy-coloured tissues to which they
lead are the remnants of the gas-gland and rete mirabile.

Gonostoma bathyphilum Vaillant
No trace of a swimbladder could be found in this species, not even in a fairly young fish (standard
length 77-5 mm.) from St. 3094, 440 20' N., 160 49' W., 21. v. 54, TYFH, isoo(-o) m.

Photichthys argenteus Hutton (Text-fig. 5)

St. 101, 33° 50' to 340 13' S., 160 04' to 15° 49' E., 15. x. 26, N 450 H, 3SO-40o(-o) m. Standard length 141 mm.
(4-5 x 2-0 mm.).

The swimbladder of Photichthys is unusual in form. The sac is a long tube originating over the
stomach and extending down about three-quarters of the length of the body-cavity.

At the posterior end is an ellipsoidal bipolar rete mirabile, which is rather more than 3 mm in length
and about 1-5 mm. in middle depth. The capillaries of the rete are formed by two vessels coming
from the dorsal aorta and cardinal vein (between the kidneys).

14 DISCOVERY REPORTS

The gas-gland invests the walls of the sac over a length of about 10 mm. in front of the rete. As
the swimbladder was quite relaxed the walls appear to be rather thick.

Giinther (1887) dissected a Photichthys taken by the 'Challenger' Expedition and described the
swimbladder as a ' long simple sac with thick walls '. As already mentioned in the introduction, the
' conical muscular mass ' at the posterior end is clearly the rete mirabile.

Text-fig. 4. Swimbladder of (a) Gonostoma denudatum (lateral view), and (b, c) G. elongatum (lateral views). In (c) the
regressed swimbladder is shown enlarged with part of its investment of fatty tissue, av, artery-vein pair to regressed swim-
bladder ; bpr, by-pass branch of retial artery ; //, fatty tissue ; gg, gas-gland ; int, intestine ; k, kidney ; pi and pv, positions of
pectoral and pelvic fins ; ra, retial artery ; rv, retial vein ; rm, rete mirabile ; rsb, regressed swimbladder ; st, stomach, (a, x 7-5 ;
B, x5-4; c, X15.)

Ichthyococcus ovatus (Cocco) (Text-fig. 6)
St. 1590, 240 10-4' N., 170 18' W., 13. x. 35, TYFB, 400-320 m. Standard length 34 mm. (7-0 x 2-5 mm.).

While much of the structure could be seen, the swimbladder of this fish was much distorted.

A single rete (length 2-0 mm.) enters the posterior end of the sac to supply a gas-gland (with one
median lobe and two lateral lobes) lying on the floor of the sac. Immediately in front of the gland

SURVEY OF STRUCTURE 15

is part of the resorbent system, which receives two arteries from the by-pass branch of the retial
artery. The curious lateral projection of the swimbladder shown in Text-fig. 6 is undoubtedly due to
distortion. This is probably the roof of the posterior part of the sac, the part that fits closely within
the recess formed by the kidneys.

This projection contained the other part of the resorbent capillary system, for it is supplied from
a third branch of the by-pass artery and receives branches from periglandular veins. However, the
full appreciation of the circulatory system must be left until a better preserved specimen is available.

rv ra

Text-fig. 5. Swimbladder of Photichthys argenteus (lateral views). Above, general view; below, posterior part of swim-
bladder, also showing the appearance of the gas-gland in transverse sections, gg, gas-gland; hit, intestine; pv, origin of
pelvic fins; ra, retial artery; rv, retial vein; rm, rete mirabile; st, stomach. (Top figure, X2'4; bottom figure, x 12.)

Cyclothone Goode & Bean

In Cyclothone the swimbladder regresses after metamorphosis into the adult form and becomes
invested with fat, which is deposited between the tunica externa and peritoneum of the larval organ.
As the peritoneum may be regarded as forming the outermost layer of the swimbladder wall (see
Fange, 1953), and as, in Cyclothone, it completely surrounds the fat and the regressed tissues, this
entire structure will be called a swimbladder in the description that follows.

Cyclothone signata Garman (Text-fig. 7C-E)
Dana St. 7735, 29. vi. 51, 580 20' N., io° 00' W., 1500-m. wire. Standard length 31 mm.

The swimbladder of this fish lies just in front of the posterior part of the kidney, the backward
end reaching a little beyond the points of insertion of the pelvic fins. In side view the organ is
elliptical in shape, having a length of about 3 mm. and a median depth of rather less than 1 mm.
Except for the postero-ventral part, it is covered with black peritoneum, which also covers a tubular
backward extension running under the bulbous terminal segment1 of the kidney.

This backward extension contains an artery and vein, which enter the rear part of the swimbladder
and then divide into a number of smaller vessels. These are bound together in a long rete mirabile

1 This is largely formed by the Stannius body (Owen, 1938).

16 DISCOVERY REPORTS

having a length of at least 5 mm. After taking a twisting course through loose connective tissues, the
rete enters a heart-shaped gas-gland set in the anterior floor of the bladder. This gas-gland is re-
latively large, with a length of 1-4 mm. and a width of 1-3 mm. and with the glandular tissue arranged
in numerous lacunae. The swimbladder has thick walls consisting mainly of loosely woven connective
tissues formed within a viscid matrix. There was no investment of fat and this is unlikely to have
disappeared through leaching action, for the fish was preserved in formalin. However, Dr Aughtry,
who has studied the ecology of Cyclothone signata in the Monterey area, California, has written to me
of his finding a fat-charged swimbladder in fishes from 27-0 to 35-0 mm. in standard length.

Text-fig. 6. Swimbladder of Ichthyococcus ovatus, viewed from above. The three lobes of the gas-gland are on the floor of
the sac. bpr, by-pass branch of retial artery ; en, resorbent capillary network ; gg, gas-gland ; ra, retial artery ; rv, retial vein ;
rm, rete mirabile. ( x 16.)

Cyclothone braueri Jespersen & Taning (Text-fig. 8)

St. 287, 2° 49' 30" S., 90 25' 30" W., 19. viii. 27, TYF, 85o(-o) m. Standard lengths of two individuals examined,
33 and 31 mm.

St. 3094, 440 20' N., 160 49' W., 21. v. 54, TYFH, isoo(-o) m. Standard length 26-5 mm.

The swimbladder lies well back in the body cavity, the posterior end being above the base of the
pelvic fins and immediately in front of the bulbous part of the kidneys. In the 31 -mm. fish the organ

SURVEY OF STRUCTURE 17

is 3 mm. in length and is invested with reticular connective tissue charged with fat droplets. Two
blood-vessels, which are closely bound together, enter the posterior under-surface and run forward
to a spherical whitish body set in the middle of the fatty tissue. This body has a diameter of 0-6 mm.
and within it are the regressed gas-gland and capillaries of the rete mirabile, these being enveloped
by a fibrous coat and bound together with more diffuse connective tissues.

rsb

Text-fig. 7. Fat-invested swimbladders of Cyclothone microdon (a and b) and C. signata (c, D and e). (a and c, lateral views ;
D and E, ventral views.) bk, bulbous, posterior part of kidney; gg, gas-gland ; ft, fatty investment of regressed swimbladder ;
mt, intestine; oy, ovary; pv, origin of pelvic fins; rm, rete mirabile; rsb, regressed swimbladder; st, stomach, (a, x 13-5;

B. x 37-5; c. xi8"9; d, xi8-9; e, x 30.)

3 DM

18 DISCOVERY REPORTS

In the 33-mm. fish the lumen of the sac was not entirely obliterated and the investment of fat was
relatively less voluminous, there being a padding of this tissue at the front and rear parts of the sac.
On the floor of the sac was a regressed gas-gland. The artery to this structure was traced backwards
to the dorsal aorta, while the vein runs to the bulbous part of the kidney, where it may join the renal
venous system.

The 26'5-mm. fish has no fatty investment (and it is preserved in formalin) the thick-walled sac
measuring about 3 mm. in length. There is a heart-shaped gas-gland on the floor of the anterior half
and this receives a long rete mirabile (about 3-5 mm. in length) which enters the posterior end of the
organ. The microscopic structure of this swimbladder will be described in a later section (p. 66).

Text-fig. 8. Fat-invested swimbladder of Cyclothone braueri. bk, bulbous, posterior part of kidney ; ft, fatty investment of
regressed swimbladder; oy, ovary; pv, pelvic fin; rsb, regressed swimbladder. ( x 18-9.)

As the larvae of Cyclothone braueri have a gas-filled swimbladder, it is clear, as previously men-
tioned, that the organ gradually regresses and receives a thick coating of fat during the adult phase.

Nusbaum-Hilarowicz (1920) studied the histology of the swimbladder of a species of Cyclothone,
under the name C. signata, but in view of Jespersen's and Taning's (1926) critical work, the species
is most likely to be C. braueri. The figures and description show that the swimbladder of this fish was
in much the same developmental phase as the 26-5 mm. individual described above.

Cyclothone livida Brauer

St. 3094, 440 20' N., i6°49'W., 21. v. 54, TYFH, i50o(-o)m. Standard length of two fishes examined 55 and
37 mm.

In both these individuals the swimbladder has much the same position in the body-cavity as that
of C. braueri. It is sausage-shaped, having a length of about 5 mm. in the larger fish and about
4 mm. in the smaller one. The middle diameter in both is about 1-5 mm.

Under the layer of black peritoneum that invests the swimbladder come the silvery or faintly
golden globules of the fatty tissue. This entirely fills the swimbladder and, as in C. braueri, the fat
droplets are held in a rather wide meshed reticular connective tissue. In the middle of the swim-
bladder is a cream-coloured body receiving blood-vessels entering the posterior end of the organ.

The swimbladder of the larger fish was taken for transverse sectioning and the following extra
details of structure seen. At its posterior entry and for most of its course to the regressed gas-gland,
the blood system consists of six small vessels bound closely together. Three arterioles each have an

SURVEY OF STRUCTURE 19

associated venule. Close to the gas-gland there are twelve vessels formed no doubt by the forking of
each of the six vessels. The twelve vessels continue into the pear-shaped mass of the gas-gland.

Besides these two fishes, dissection of several other smaller individuals has revealed transition
stages between the gas-producing swimbladder of the larvae and the fat-invested structure of the
adult (see p. 66).

The microscopic structure of the swimbladder of the 55-mm. fish will be described in a later
section (pp. 66-67).

Cyclothone microdon (GiAnther) (Text-fig. 7 A, b)
St. 239, 460 56' 00" S., 460 03' 00" W., 2. vi. 27, N 450, i35o-io5o(-o) m. Standard length of fish 52 mm.

As in other adult Cyclothone, the fat-invested swimbladder of C. microdon is slung in the rear part
of the body-cavity, the backward end lying just before the enlarged posterior part of the kidneys.

In the middle of the blimp-shaped mass of fatty tissue is a small pear-shaped, cream-coloured
body, receiving blood-vessels that enter the posterior under-surface of the organ. A vein, which may
be an extension of the renal venous complex, runs forward from the bulbous posterior part of the
kidney. The origin of the artery that runs side by side with it could not be traced with certainty.
After entering the swimbladder these two vessels continue forward within the fatty tissue and spiral
round each other just before entering the pear-shaped structure. This consists of regressed glandular
cells and associated capillaries, which are invested and bound together with connective tissues. In
the above fish this structure measured 075 mm. in length and 0-3 mm. in greatest width, while in
another individual of the same size the length was 0-4 mm.

Cyclothone acclinidens Garman

John Murray Expedition, St. 95 Arabian Sea, 2-m. tow-net, 1400-m. wire. B.M. Reg. no. 1939.5.24. 115-250.
Standard length of fish 30 mm.
The swimbladder of this species has a very similar structure to that in the four species just described,

Family Sternoptychidae

Argyropelecus aculeatus Cuvier & Valenciennes (Text-fig. 9)

St. 257, 350 01' 00" S., io° 18' 00" E., 24. vi. 27, N100H, mm. B.M. Reg. no. 1930.1.12. 367-8. Standard
length 23 mm. (3-5 x 2-5 mm.).

The swimbladder of this hatchet fish is ellipsoidal in form and is slung in the upper part of the
body-cavity. At the posterior end of the sac is a massive rete mirabile. It originates at the level of
the long axis and extends under the sac over a length of 1-2 mm. Seen from below, the rete is acorn-
shaped, the bulbous head consisting of the first division of the artery and vein into finer vessels.
These then divide again into the thousands of closely intercalated capillaries that form the rest of this
structure.

The gas-gland encircles a heart-shaped capillary bed which extends over the middle region of the
swimbladder floor. There are two glandular lobes, each consisting of a band of tissue with expanded
posterior and anterior regions (see Text-fig. o,b).

Arteries and veins leave the front of the rete and run into the gas-gland. There are lateral vessels to
the posterior expanded parts of the gland and three central vessels running forwards along the mid-
ventral line. The middle vessel is a vein which forks to send a branch to each of the anterior expanded
parts. On either side of the vein is an artery, each of which follows the bifurcations to the gas-gland.

The arterial supply to the capillary network comes from the artery to the rete mirabile, which
sends off a branch just before its point of entry. This branch runs forwards along the right side of

3-2

2o DISCOVERY REPORTS

the rete and then forks into two sub-branches (see Text-fig. 9B) serving the left and right halves of
the capillary area. Each sub-branch gives off arterioles dividing to form capillaries. The venous part
of the capillary circulation comes from the glandular veins from branches running along the inner
edges of the two lobes. These branches break up into venules and capillaries that join the arterial
complex. The capillary arterial stream is thus by-passed round the rete mirabile, but the return
venous flow eventually runs through this structure by way of the glandular veins.

Text-fig. 9. Swimbladder of Argyropelecus aculeatus, viewed (a) in position in fish, (b) ventrally, and (c) laterally. Veins
shown black, arteries white, av, artery-vein association supplying gas-gland ; bpr, by-pass branch of retial artery ; en, resor-
bent capillary network; gg, gas-gland; ra, retial artery; rv, retial vein; rm, rete mirabile. (a, xi;b, x 22-5; C, x 17.)

Argyropelecus olfersii (Cuvier)
Taken by M.V. 'Sarsia' off Concarneau. Standard length 38 mm. (4-5 x 3-0 mm.).

The swimbladder is suspended in the upper half of the body cavity. The sac is oval in outline, and
as it is quite relaxed the walls are fairly thick.

A long, club-shaped rete mirabile, with a length of 275 mm., enters the posterior end of the sac
to supply the gas-gland. An artery from the dorsal aorta and a vein from the cardinal system (between
the kidneys) run into the posterior end of the rete.

The gas-gland extends over the roof, side walls and floor of the rear half of the sac, the part over
the first two regions appearing to be subdivided into five or six lobes. There is a single lobe on the
floor. Each lobe receives an artery and vein from the rete mirabile, while an interglandular capillary
network extending over the inner surface of the roof also obtains blood from anterior retial vessels.
Longitudinal sections also revealed that there is a capillary network in the floor of the sac (in front of
and around the gas-gland). A branch of the retial artery, which subdivides just before entering the
rete, runs under the latter and then forwards to break up into capillaries, which run over the inner

SURVEY OF STRUCTURE 21

surface between the ventral and lateral sections of the gas-gland. The entire capillary circulation,
which seems to be much like that of A. aculeatus, must form an effective inner surface for the diffusion
of gases into the blood.

Argyropelecus sladeni Regan

St. 285, 20 43' 30" S., oo° 56' 30" W., 16. viii. 27, N450H, i75-i25(-o) m. B.M. Reg. no. 1930.1.12. 401-6.
Standard length 20 mm. (175 x 1-5 mm.).

The swimbladder of this species is almost spherical and lies above the stomach in the upper half
of the body cavity.

The single rete mirabile receives an artery from the dorsal aorta and a vein that originates between
the kidneys. The retial complex formed from these two vessels is cylindrical and enters the floor of
the sac from behind to supply the gas-gland. This covers part of the floor and extends backwards
and upwards over the side and rear walls of the sac. Viewed from above through a hole cut in the roof
of the sac, vessels leaving the rete can be seen running forwards over the floor to the ventral part of
the gland.

The two non-glandular areas on either side of these vessels are invested with a capillary net-
work, which has been described more fully under A. aculeatus.

Argyropelecus hemigymnus Cocco

Nusbaum-Hilarowicz (1920) found the swimbladder of this hatchet fish to be dilated anteriorly and
narrowed posteriorly. Two ligaments of connective tissue attached to the front part of the sac extend
upwards to a fastening on the roof of the body-cavity. The walls are constructed of an outer layer of
long fibres (mainly running around the sac), a middle and thick layer of loose connective tissue and
an inner epithelial layer which forms the gas-gland. This covers the floor and lateral walls of the
forward part of the swimbladder, there being a small, median, ventral lobe and two larger lateral
lobes. A single long rete mirabile enters the rear part of the swimbladder and runs forwards under the
floor to the gas-gland.

Sternoptyx diaphana Hermann (Text-fig. 10 c, d)

St. 281, oo° 46' 00" S., 50 49' 15" E., 12. viii. 27, TYF, 950-850^0) m. B.M. Reg. no. 1930.1.12. 416-25. Stan-
dard length 14 mm. (2-7 x 2-5 mm.).

St. 269, 150 55' 00" S., io° 35' 00" E., 26. vii. 27, TYF, 700-6oo(-o) m. B.M. Reg. no. 1930.1.12. 413-15. Stan-
dard length 39 mm. (9-0 x 5-0 mm.).

The swimbladder is a heart-shaped organ lying in the upper half of the body-cavity. The long axis
of the sac, which is thin-walled, is directed downwards and slightly backwards, so making an acute
angle with the vertical axis of the fish.

There is a pair of suspensory ligaments running from the roof of the body-cavity to an attachment
on the posterior part of the roof of the swimbladder. The other suspensory structures, which are more
in the nature of mesenteries, are attached to the anterior middle region and the bottom of the sac.
Both taper to points of attachment on the peritoneum of the body-cavity, the former to a point
opposite the top of the stomach, and the latter to a point behind the basal part of the intestine.

The single, club-shaped rete mirabile, which has a length of 2 mm. in the larger fish, enters the
roof of the swimbladder. It receives a branch from the posterior cardinal vein and an artery (running
between the kidneys) from the dorsal aorta. The gas-gland invests the roof and is composed of three
lobes, each receiving blood-vessels from the rete mirabile.

The fine structure of the swimbladder of this species has been described by Nusbaum-Hilarowicz
(1920). Besides noting the bipolar structure of the rete mirabile, he saw that certain of the outgoing

22 DISCOVERY REPORTS

retial vessels formed a capillary network over the inner surface of the sac between the lobes of the

gas-gland.

Polyipnus laternatus Garman (Text-fig. ioa, b)

Position, 130 25' N., 18° 22' W., 28. x. 25, N 450 V, 90o(-o) m. B.M. Reg. no. 1930.1.12. 458-67. Standard
lengths 32-5 and 26-5 mm.

St. 1582, 05° 39-1' S., 460 22-3' E., 29. v. 35, N 450 H, I900-i85o(-o) m. Standard length 36-0 mm.

The swimbladder of this species is suspended in the upper half of the body-cavity, just above the
stomach. The sac is more or less oval in side view, with its long axis parallel to that of the fish. In
the three individuals examined (in the order given above) the sac had a length and middle depth of
7-0 and 4 mm., 175 and i-o mm. and 6-o and 3-5 mm.

Text-fig. 10. Swimbladders of Polyipnus laternatus (a and b) and Sternoptyx diaphana (c and d). a and C, lateral views,
showing position of swimbladder in body-cavity ; c and D, rete mirabile and gas-gland, ft, fatty investment of swimbladder ;
gg, gas-gland ; k, kidney ; oy, ovary ; rm, rete mirabile ; st, stomach, (a, x3-5;b, xii-5;c, x5;d, x7-5-)

A long club-shaped rete mirabile enters the posterior end of the swimbladder, the measurements
of its length in the two largest fishes being about 3-5 mm. The gas-gland lies immediately in front of
the rete and is partly or entirely divided into two left and right halves.

A layer of fatty tissue invests the swimbladder walls of the 26-5 and 32-5 mm. fishes. The de-
position of the fat takes place between the peritoneal layer surrounding the sac and the tunica externa,
transverse sections through the swimbladder of the 36 mm. fish revealing that the space between
these two layers is filled with loose reticular connective tissue (see also p. 67). The resorbent capillary
circulation has not been closely investigated. However, there is an artery running forward by the

SURVEY OF STRUCTURE 23

side of the rete mirabile, which is undoubtedly homologous with the artery forming part of the
capillary network in other stomiatoids. Sections also reveal that there is a capillary network on the
floor of the sac between the lobes of the gas-gland and there also appears to be another network
in the roof.

Family Astronesthidae
Astronesthes niger Richardson (Text-fig. 11)
Dana St. 1378111, 200-m. wire. B.M. Reg. no. 1929. 1.4. 93. Standard length 41 mm. (5-5 X2>5 mm.).

The swimbladder of this fish, which is elliptical in profile and has thin walls, is slung above the
stomach, the extremities lying over the origins of the pectoral and pelvic fins.

A rod-like rete mirabile (1-5 mm. in length) enters the posterior part of the sac. Its blood supply
comes from an artery that runs backwards and then upwards between the kidneys to the dorsal aorta
and from a vein joining the cardinal vessel at the front end of the enlarged, rear part of the kidneys.

The gas-gland has two lobes, the left being the larger. This is an elongated band of tissue with an
enlarged and rounded posterior part, which lies immediately in front of the rete mirabile and invests
the lateral walls of the sac. The right lobe is a triangular patch of tissue lying opposite the tip of the
left lobe. The length of this lobe is 1-3 mm. as compared with the 3-2 mm. span of the other one.

Each lobe receives blood-vessels leaving the forward end of the rete. The artery and vein to the
right lobe run along the lateral walls of the sac.

The resorbent capillary network, which lies just under the inner epithelium, covers most of the
swimbladder roof. The by-pass vessel from the retial artery runs forwards along the right side of
the rete and then describes an undulating course about the long axis of the sac. This artery gives off
arterioles on either side, which break up into capillaries. The circulation is completed by venules and
capillaries that come from vessels running along the upper edges of the gas-gland lobes.

Astronesthes lucifer Gilbert (Text-fig. 12 A, b)
B.M. Reg. no. 1922.6.7. 14-23. Misaki, Japan. Standard length 73 mm. (16-5 X3>5 mm.).

The swimbladder of this astronesthid is an elongated ellipsoid sac tapering to a point anteriorly.
Above the base of the pelvic fins and at the posterior end of the organ is a single, bulbous rete mirabile,
2-5 mm. in length and 1-3 mm. in width. This is fed with arterial blood by a vessel that extends
backwards and then turns upwards through the kidneys to join the dorsal aorta. The vein enters the
kidneys at the point where they begin to enlarge behind the swimbladder.

The two lobes of the gas-gland, which extend over the floor and sides of the swimbladder, come
immediately in front of the rete mirabile. Along the upper and lower parts of each lobe are vessels,
which lead to the rete.

Astronesthes gemmifer Goode & Bean (Text-fig. 12D)
Westmann Isles, Iceland. B.M. Reg. no. 1950.6.30. 2. Standard length 168 mm. (20x3 mm.).

The swimbladder of this species was found over the posterior half of the stomach. It is an elongated
organ with very thick walls. At the posterior end of the bladder is a conical rete mirabile measuring
about 3-5 mm. in length and 1-5 mm. in greatest width.

The gas-gland appears to be a solid rod-like structure, but actually consists of two closely con-
tiguous lobes which together fill most of the lumen of the sac. All the tissues appear to be very con-
tracted, or it may be that the organ regresses during adult life.

DISCOVERY REPORTS

Text-fig. ii. Swimbladder of Astronesthes niger, seen (a) in fish; (b) laterally, and (c) ventrally. Veins shown black, arteries
white, av, artery-vein pair to gas-gland; bpr, by-pass branch of retial artery; gg, gas-gland; k, kidney; ra, retial artery;
rv, retial vein; rm, rete mirabile. (a, x 2; b, x 8; c, x 12.5.)

SURVEY OF STRUCTURE
gg

Text-fig. 12. Swimbladders of Astronesthes lucifer (a and b) ; Borostomias antarcticus (c) and Astronesthes gemmifer (d). Lateral
views. In (c) two transverse sections of the swimbladder show the inner disposition of the gas-gland, ft, fatty investment
of swimbladder; gg, gas-gland; k, kidney; oy, ovary; psb, posterior end of swimbladder; ra, retial artery; rv, retial vein;
rm, rete mirabile ; sb, swimbladder. (a, x7"5; b, x i ; c, x 2; d, X4-8.)

Astronesthes similis Parr

Dana St. 939, 500-m. wire. B.M. Reg. no. 1929. 1.4. 81. Standard length 105 mm. (20x5 mm.).

The swimbladder bauplan of this species is similar to that of other Astronesthes spp. The pointed
forward end of the sac, which is thin-walled, lies opposite the posterior edges of the gill covers.
There is a bilobed gas-gland immediately in front of the bulbous rete mirabile, which enters the

26 DISCOVERY REPORTS

posterior floor of the swimbladder. The left lobe of the gland is the larger, measuring about 6 mm. in

length against the 4 mm. span of the right lobe.

Borostomias antarcticus (Lonnberg) (Text-fig. 12 c)

St. 114, 520 25' 00" S., 90 50' 00" E., 12. xi. 26, N 450, 650-70001. B.M. Reg. no. 1930.1.12. 474. Standard
length 167 mm.

The swimbladder of this individual proved to be a tubular structure lying above the anterior part
of the stomach. It is club-shaped, measures about 13 mm. in length and contains a regressed gas-
gland and rete. An artery and vein run into the posterior part of the organ and can be traced back to
the backward section of the kidneys. Both the remains of the swimbladder and these blood-vessels
are surrounded by a layer of fatty tissue.

Diplolychnus mononema Regan & Trewavas
Standard length 137 mm.

No trace of a swimbladder could be found in this individual.

Text-fig. 13. Fat-invested swimbladders of Stomias affinis (a and a') and S. colubrimis (b). Lateral views, ft, fatty invest-
ment of swimbladder;^, gas-gland; oy, ovary; rm, rete mirabile ; rsb, regressed swimbladder. (a, X4"5; a', x 11-5; b, x 17-5.)

Family Stomiatidae

Stomias affinis Gunther (Text-fig. 13 a)

St. 276, 50 54' 00" S., 11° 19' 00" E., 5. viii. 27, TYF, i5o(-o) m. B.M. Reg. no. 1930.1.12. 542-3. Standard
length 106 mm.

In this individual there is a regressed swimbladder lying above the ovaries. Fatty tissue invests
the organ and is continued forwards and backwards into rod-like prolongations. The anterior one
extends to the front of the ovary, while the backward one, which is more slender and tapering, ends
rather more than half-way down the body-cavity.

The length of the swimbladder is about 4-5 mm. Entering the posterior end is an artery and vein
supplying a club-shaped rete mirabila which is about 1-5 mm. in length. In the middle of the bladder
is a small gas-gland, o-8 mm. in length, which all but obliterates the lumen. Forward of the gland
there is no lumen, but merely a ' solid ' mass of connective tissue.

SURVEY OF STRUCTURE 27

Stomias colubrinus Garman (Text-fig. 13B)
Position, 130 25' 00" N., 180 22' 00" W., 28. x. 25, N 450 V, o,oo(-o) m. Standard length 103 mm.

Beginning above the base of the pectoral fins and running just below the kidneys is a well-defined
strand of fatty tissue, with a length about four-fifths that of the body-cavity. Within this tissue, about
three-fifths of the way along its length, was found the regressed tissues of the swimbladder. Running
forward to a posterior rete mirabile is an artery and vein. The rete leads to solid club-shaped structure
which consists of a mass of regressed gland cells invested with connective tissues. The rete and gland
were about 2-5 mm. in length.

Stomias ferox Reinhardt

Position, 410 37' N., 120 30' W., 10. x. 25, N 200 H, 90o(-o) m. B.M. Reg. no. 1930.1.12. 541. Standard length of
fish 85 mm.

As in S. affinis and S. colubrinus, there is a well formed strand of fatty tissue, lying just below the
kidneys and originating above the base of the pectorals. In the above individual this fat body ex-
tended for about 25 mm. down the body-cavity to end in a tapering section attaching to the intestinal
mesentery.

No remains of retia mirabilia or gas-gland could be found in this tissue.

Family Melanostomiatidae
No swimbladder could be found in adult individuals (judged by the development of the gonads) in
each of the following species: Bathophilus metallicus Welsh, B. pawned Parr, Eustomias obscurus
Vaillant, Ecliiostoma tanneri (Gill).

Beebe and Crane (1939) gave an account of the internal organs of a number of species but made no
mention of a swimbladder.

Family Chauliodontidae
Chauliodus sloanei Schneider and C. barbatus Garman
No swimbladder was found in two adult fishes examined.

Family Idiacanthidae
Idiacanthus fasciola Peters

No swimbladder was found in adult specimens.

Family Malacosteidae

No trace of a swimbladder could be found in adult Malacosteus niger Ayres and Photostomias guernei
Collett.

Suborder SALMONOIDEA

Family Opisthoproctidae
Opisthoproctus soleatus Vaillant (Text-fig. 14D)
St. 3484, 390 55' N., 200 01' W., 1. x. 56, IKMT, 750(^0) m. Standard length 35 mm. (6-5 x 2-5 mm.).

The swimbladder of Opisthroproctus, which is ellipsoidal in form, lies above the stomach. When
fully expanded it is evidently no less capacious an internal float than the swimbladder of a myctophid
(of the same size).

4-2

28 DISCOVERY REPORTS

Two blood-vessels enter the anterior end of the sac and then subdivide to form about twelve
branches, which take more or less parallel courses within the swimbladder wall until they reach the
gas-gland. Each of these vascular branches consists of from six to twelve closely associated capil-
laries, which are arranged in the form of a ribbon. In cross-section the ribbon consists of alternating
arterial and venous capillaries (or arterioles and venules), the arterial elements having a diameter of
about i2(i while the venous ones measure about 20 fi. Clearly these are retial structures (see Text-
fig. 14D), but they are quite unlike the massive retia of most teleosts with a closed swimbladder. Such
elements might well be called micro-retia mirabilia.

These retia enter the gas-gland without subdividing and form capillary loops within the secretory
tissue. The gland occupies a median region and entirely surrounds the sac. Beyond the gas-gland the
walls consist of an inner epithelium and outer connective tissues. Perhaps it is here that resorption
of gases takes place.

Opisthoproctus grimaldii Zugmayer (Text-fig. 14 e)

St. 1746, from 320 02-1' S., 870 02-5' E. to 310 56-6' S., 86° 55-1' E., 22. iv. 36, D.R.R. 2513 m. Standard length
65 mm. (15-0 x 6-o mm.).

Opisthoproctus grimaldii has a capacious swimbladder which is rounded anteriorly and tapers to a
point at the other extremity. As in O. soleatus, blood-vessels enter the forward tip of the sac. There is
a large vein that originates between the kidneys (presumably coming from the cardinal vein), while
there are two arteries, one being a branch of the mesenteric system, the other running forward from
the vessel to the ovaries.

Again, these vessels subdivide to form micro-retia, each composed of a ribbon of closely associated
capillaries (from twelve to sixteen). The venous elements have a diameter of from 12 to ibfi, while
their arterial counterparts measure from 8 to io//. At the forepart of the swimbladder there appeared
to be about 30 micro-retia, these running backward to supply glandular patches, which seemed to be
less concentrated than those of O. soleatus. However, they were most numerous over the middle part
of the sac. These patches are formed of cells varying in size from about 30 to 150^.

Winteria telescopa Brauer (Text-fig. 14 A, b)
St. 2066, 040 56-4' N., 140 467' W., 5. v. 37, N 450 B, 1550-0 m. Standard length 100 mm. (5-0 x 2-0 mm.).

The swimbladder of Winteria is suspended in the body-cavity just behind the stomach. In the
above individual the sac is very relaxed, the walls being thick and having a nacreous appearance.
From the posterior end of the swimbladder a long band of connective tissue runs backwards to an
attachment on the right ovary.

An artery and vein enter the anterior end of the sac and subdivide into a number of smaller vessels,
which run towards the gas-gland. This is found in the posterior half of the sac and seems to be a
flattened oval structure lying on the floor of the swimbladder. However, the tissues are so shrunken
that this may not be its true form. Running to the glandular area are at least twelve micro-retia
composed of from eight to fourteen capillaries.

Macropinna microstoma Chapman
Chapman (19426) was unable to find a swimbladder in this species.

Family Microstomidae
Xenophthalmichthys danae Regan
Bertelsen (1958) records that the swimbladder is absent.

SURVEY OF STRUCTURE

A well-developed swimbladder is found in the genera Argentina, Glossanodon, Microstoma and
Nansenia (Cohen, 1958; Fange, 1958, and personal observation). Fange's description of the swim-
bladder of Argentina silus shows that micro-retia are also present in another deep-sea salmonoid and
that the system is highly developed. I have also found an extensive development of micro-retia in
Microstoma and Nansenia. However, as these four genera appear to consist of benthic fishes they are
not considered here. Further discussion may be found in the section on pages 53-54.

The swimbladders of the two species of Opisthoproctus and Winteria telescopa were not sufficiently
well preserved to trace the resorbent capillary network. However, it is likely to be found at the
posterior end of the sac. This is certainly true of Argentina and Microstoma, in which this part is thin
walled and carries a capillary bed (see also pp. 79-80).

Text-fig. 14. Swimbladders of Winteria telescopa (a and b) and Opisthoproctus soleatus (d), seen from below. In (c) part
of a micro-rete of Winteria is seen and in (e) two micro-retia of Opisthoproctus grimaldii, which supply patches of gas-gland.
gg, gas-gland ;int, intestine; Iv, liver; mrm, micro-rete mirabile ; oy, ovary; ra, retial artery; rv, retial vein; sb, swimbladder;
st, stomach, (a, X3"5; b, xi2"5; c. x°o; D, xio; E, x 60.)

Family Bathylagidae
In his synopsis of this family, Chapman (1943) recorded that the swimbladder is completely absent.
Beebe (1933), who examined the internal organs of Bathylagns benedicti and B. glacialis, made no
mention of this organ, while I could find no trace of it in B. antarcticus and B. argyrogaster.

30 DISCOVERY REPORTS

Suborder CLUPEOIDEA

Family Alepocephalidae

Alcock (1899) stated that the Alepocephalidae have no swimbladder. Beebe (1933) examined the
internal organs of Bathytroctes rostratus and Xenodermichthys copei, but made no mention of a swim-
bladder. I was unable to find any trace of this organ in an adult of the latter species, nor in Searsia
koefoedi.

Order INIOMI
Suborder MYCTOPHOIDEA
Family Myctophidae
Myctophum punctatum Rafinesque (Text-fig. 15A-C)
St. 3233, 460 02' N., 090 19' W., NH, o m. Standard lengths of fishes 74-5, 71-0, 69-0 and 59-0 mm.

In this lantern fish a capacious swimbladder is found above the stomach. The anterior end is
opposite the margins of the gill-covers, while the posterior extremity lies under the origin of the
dorsal fin. The sac is thin-walled and ellipsoidal in form, the major and minor axis measuring n-o
and 4-5 mm. in the 69-o-mm. fish.

Three retia mirabilia are found on the underside of the forward, rounded end of the sac. The retial
blood supply comes from an artery running backwards and downwards from the dorsal aorta and
returns through a vein that joins the hepatic portal system.

In the 74-5-mm. fish, each of the three retia mirabilia (which have a length of about 2 mm.) runs
to a corresponding lobe of the gas-gland. The middle lobe is shaped rather like a rose petal and lies
over the floor, while the left and right lobes, which are fan-like, extend over the lateral walls. As in
all lantern fishes, the surface of the gland has a convoluted appearance, due to the meanderings of the
capillary loops with their associated investments of gland cells. This kind of rete in which the arterial
and venous capillaries run straight to the gas-gland without forming larger vessels is termed unipolar.

Above the retia mirabilia is a resorbent ' oval ' which is partly expanded. It measured 2-5 mm. along
the longitudinal axis and 2-2 mm. in width. The oval bears a fine-meshed network of capillaries fed
by two branches of the retial artery. The venous return is through a large vessel running upwards
and forwards to a point between the kidneys, presumably to the posterior cardinal vein.

In the 69-mm. fish the oval is partly expanded and the opening into the swimbladder has a diameter
of 2-5 mm. The capillary-bearing tissue is an egg-shaped blister measuring 3-5 along the longitudinal
axis and 3-0 mm. in greatest width. The oval of the 59-mm. fish is shut, the inner surfaces of the
walls being thrown into folds. The fine structure of the oval in the closed phase will be dealt with
in more detail in a later section (p. 80).

Diaphus rafinesquei (Cocco) (Text-fig. 1 5 D, e)
St. 3484, 390 55' N., 200 01' W., 1. x. 56, IKMT, 75o(-o) m. Standard length 70 mm.

A detailed description of the swimbladder of this myctophid has been given by Rauther (1922).
According to his reconstruction of transverse sections (shown in his fig. 13), the swimbladder of his
fish measured about 7 mm. in total length. The middle depth was rather less than 1 mm. In the
Discovery fish the length of the sac is about 20 mm. and the middle depth about 7 mm. Rauther
showed the walls of the swimbladder to be relatively thick, but the sac was clearly not in an expanded
condition. There was an outer fibrous layer which did not cover the roof, and then came two layers
of loose and closely packed connective tissue fibres.

SURVEY OF STRUCTURE 31

Continuing Rauther's description, the inner epithelial layer forms an extensive gas-gland covering
most of the floor and side walls of the swimbladder, and also the roof of the anterior part. There are
three retia mirabilia supplied by an artery that joins the dorsal aorta close to the coeliac artery, while
the venous return is through a vessel opening into the portal system. The left rete extends upwards
to the roofing part of the gas-gland, while the middle and right retia supply the remaining glandular
area. Measured from Rauther's fig. 13 the lengths of the retia, in the order just mentioned, are about
2-5-3-0 mm.

Text-fig. 15. Swimbladder of Myctophum punctatum, seen (a) in position in body-cavity of fish, (b) laterally, (c) ventrally
(anterior part of organ). The oval of Diaphus rafinesquei is shown in Text-figs. 15 D and E. cm, circular muscle of oval;
ram, radial muscle of oval; gg, gas-gland; op, opening from oval into swimbladder chamber; ov, oval; ra, retial artery;
rv, retial vein ; rm, rete mirabile ; vov, vein to oval. Veins shown black, arteries white, (a, x 1 ; b, x 5 ; c, x 1 2 ; D, x 7 ;

E, XI5.)

There is an anterior chamber, called by Rauther the praevesica, opening into the right side of
the main sac just behind its forward tip. The chamber has an outer fibrous layer and an inner much-
folded layer of loose connective tissue containing a capillary network. Rauther remarked that this
hlood-system was like that he found in the respiratory part of the swimbladder of the mud-minnow,

32 DISCOVERY REPORTS

Umbra. The arterial supply for the network comes from the retial artery, while there is a vein running
forward and upwards from the chamber to the cardinal (?) vein.

Examination of the Discovery fish revealed that Rauther's 'praevesica' is no more than a very
distorted oval. In this fish the oval lies immediately to the right of the retia mirabilia and the capillary
bearing surface is blown out in the form of a blister, due no doubt to the release of pressure as the
fish was hauled to the surface. Had sections been cut of this structure, it would also have looked like
an anterior chamber. At the base of the oval is a circular aperture with a diameter of about 0-75 mm.
which opens into the main cavity. From the rim of this opening radial muscles extend outwards and
are crossed by a complex of circular muscle fibres. Clearly the whole structure conforms to that of the
oval found in some fishes with a closed swimbladder, much like that described in the perch (Perca
fluviatilis) by Saupe (1939).

Like Myctopham punctatum and Diaphus rafinesqnei, each of the other lantern fishes dissected has
an ellipsoidal swimbladder provided with three unipolar retia mirabilia. The gas-gland is three-
lobed, each lobe receiving a corresponding rete. An oval is also present.1 In view of this, the de-
scriptions which follow will be confined to the more significant features. Immediately after the length
of the fish, measurements of the major and minor axes of the swimbladder appear in parenthesis.

Electrona tenisoni (Norman) (Text-fig. i6d-f)

St. 2023, 500 177' S., 00° 23-1' E., 28. iii. 37, N 100 B, 750-4oo(-o) m. B.M. Reg. no. 1948. 5. 14.16. Standard
length 47-0 mm. (4-5 x 1-5 mm.).

The swimbladder of this fish is well developed, although this is hardly revealed by the dimensions
of the sac, which is much contracted. Three retia, almost 2-5 mm. in length, enter the anterior floor
to supply a heart-shaped gas-gland. The bunched-up appearance of the gland, which covers much
of the floor, also reveals the collapsed state of the organ.

Towards the base of the retia, but more to the right side of the sac, is the oval, with wrinkled

outer walls. The inner tissues lining the wall are folded and ridged, and bear a network of blood

capillaries. The structure is almost closed, there being but a small opening (about 0-5 mm. in diameter)

communicating with the main lumen of the swimbladder. The blood-supply consists of two branches

from the retial artery and a large vein, which runs forward and upward to the cardinal vein between

the kidneys.

Electrona rissoi (Cocco)

St. 101, 330 50' to 34°i3'S., i6°04' to i5°49'E., N 450, 40o-35o(-o) m. B.M. Reg. no. 1930.1.12. 597-8.
Standard length 61 mm. (12x4 mm.).

This species has a capacious swimbladder occupying about three-quarters the length of the body-
cavity. On the right of the sac and just behind the anterior tip is the oval, which receives a large
vein and a number of small branches coming from the retial artery. The organ is almost closed, the
walls having a much folded appearance. Around the opening into the main cavity of the swimbladder
are circular and radial muscles.

Electrona antarctica (Giinther) (Text-fig. i6a-c)

St. 114, 520 25' 00" S., 90 50' 00" E., 12. xi. 26, N 450, 650-70o(-o) m. B.M. Reg. no. 1930.1.30. 622-7. Standard

lengths of two fishes examined, 26-0 and 59-0 mm.

St. 2535, 520 40-8' S., 02° 45-4' E., 16. i. 39, N 100 B, 1050-0 m. Standard length 36 mm.

In all three fishes the swimbladder is oval in outline and is suspended in the body-cavity over the
forward half of the stomach. The sac of the smallest specimen measured a little more than 3 mm. in

1 The part of the swimbladder serving for gas-resorption.

SURVEY OF STRUCTURE

length and 3 mm. in greatest width. The retia mirabilia are contained in a conical projection at the
anterior end, and they are wound spirally round one another. When opened out, three long retia
were revealed, each about 5 mm. in length, these running to a gas-gland covering about three-
quarters of the swimbladder floor.

st Iv sb

rm gg st

Text-fig. 16. Swimbladders of Electrona antarctica (a, b and c) and E. tenisoni (d, e and f). b, c, e and F are ventral views.
gg' gas-gland; hit, intestine; k, kidney; h, liver; ov, oval; oy, ovary; ra, retial artery; rv, retial vein; rm, rete mirabile;
sb, swimbladder ; st, stomach ; vov, vein to oval, (a, x 3-5 ; b, x 15 ; c, x 17-5 ; d, x 6 ; E, x 18 ; F, x 14.)

The fish from St. 2535 has a rather larger swimbladder measuring nearly 4 mm. in length. In this,
the arterial supply for the retia mirabilia came from the coeliaco-mesenteric vessel. The walls of the
bladder were quite thin.

Finally, the swimbladder of the 59-mm. fish measured no more than 2-0 and V2 mm. across the
major and minor axes. It is clear that the organ regresses during the adult phase.

DISCOVERY REPORTS

Hygophum benoiti (Cocco) (Text-fig. 17)
B.M. Reg. no. 85.6.22. 120-9. Straits of Messina. Standard length 4-1 mm. (7-0 x 2-0 mm.).

The swimbladder of this lantern fish is both thin-walled and capacious. At the anterior end three
retia mirabilia run into the gas-gland, which covers most of the floor and side walls of the forward
half of the organ. Each rete has a length of nearly 3-0 mm.

Over the point of entry of the retia mirabilia into the gas-gland and rather to the right of the swim-
bladder is a forward conical extension (the distorted oval) receiving a rich supply of blood-vessels.
Within the oval the walls are thrown into a series of longitudinal ridges.

Text-fig. 17. Swimbladder of Hygophum benoiti, seen (a) laterally, and (b) ventrally. gg, gas-gland; ov, oval;

rm, rete mirabile. (a, x 13-5 ; b, x 19.)

Benthosema glaciale (Reinhardt) (Text-fig. i8d-f)

Position, 13° 25' N., 180 22' W., 28. x. 25, N 450 V, 90o(-o) m. B.M. Reg. no. 1930. 1. 12. 641-7. Standard length
of fish 45-5 mm. B.M. Reg. no. 1911.2.8. 3-12. Between Faroes and S.W. Ireland. Standard length of fish
58-5 mm.

The swimbladder of this myctophid is thin walled and lies above the stomach. In the 45-5 mm.
fish it measured 5-5 mm. in length and about 2 mm. in depth and width at the middle region. A
bulbous projection at the fore-end of the bladder contains the three retia mirabilia, which run back-
wards to a gas-gland investing much of the floor and side walls. Each rete has a mean length of
about 3 mm., the two outer systems being rather longer than the middle.

Just behind the base of the bulbous forward projection and on the left-hand side of the swimbladder
is a small rounded chamber (the oval) receiving many blood-vessels. The oval has a sphincter-con-
trolled opening into the main cavity, while the walls are thrown into radially disposed folds. In the

SURVEY OF STRUCTURE 35

Discovery fish the chamber was about 0-5 mm. in diameter and the inner opening, which was oval,
measured 0-5 x 0-3 mm. The corresponding figures for the other fish are o-6 and 0-2 x 0-2 mm.

In both fishes the anterior part of the swimbladder was entirely invested by fatty tissue, which
extended under the organ (and beyond it in the larger individual).

Text-fig. 18. Swimbladders of Benthosema suborbitale (a, b, c), and B. glaciate (d-f). a, c, d, e, lateral views; b, dorsal view.
The almost closed oval of B. glaciale is seen in diagrammatic transverse section and from below in (f). bl, urinary bladder;
gg, gas-gland; int, intestine; k, kidney; ov, oval; oy, ovary; ra, retial artery; rv, retial vein; rm, rete mirabile; st, stomach;
vov, vein to oval, (a, x 11-5; b, x 15; c, x 15; d, x 11 ; e, x 10; f, x 20.)

Benthosema suborbitale (Gilbert) (Text-fig. i8a-c)

St. 2067, 24°i2'N., 210 12-2' W., 12. v. 37, N450H, 68(-o) m. B.M. Reg. no. 1948.5. 14. 185-91. Standard
length of fish 24 mm. (4-3 x 1-3 mm.).

A thin-walled swimbladder originates over the forepart of the stomach and extends over some
two-thirds of the length of the body-cavity.

The gas-gland invests the floor of the foremost third of the organ. As in all myctophids, the gland
receives three retia mirabilia, which enter the anterior and lower part of the swimbladder.

5-2

36 DISCOVERY REPORTS

Not far behind the forward tip and on the right-hand side of the bladder, the oval, which is almost
closed, appears as a small circular blister, about 0-3 mm. in diameter. This has a small opening into
the main cavity and the much folded walls have a rich supply of blood capillaries.

Diogenichthys atlanticus (Taning)

St. 288, oo° 56' 00" S., 140 08' 30" W., 21. viii. 27, TYF, 25o(-o) m. B.M. Reg. no. 1930.1.12. 846-7. Standard
length 25-5 mm. (3-0 x o-6 mm.).

The swimbladder of this specimen was in a relaxed state, the walls appearing thicker than they
would be when the sac is inflated. The three retia mirabilia are bound together in a bulbous forward
extension and are closely followed by the gas-gland, which covers about three quarters of the swim-
bladder floor.

Myctophum humboldti (Risso)
St 1566, 400 42' S, 360 05-5' E., 9. iv. 35, N 70 H, 0-5 m. Standard length 50 mm. (8-0x4-0 mm.).

This species has a capacious thin-walled swimbladder. The three retia mirabilia run underneath
the forward, rounded end of the swimbladder to the gas-gland, which is three lobed and extends over
the floor and lateral walls. Each rete is about 3 mm. in length, while the gas-gland has a length of
about 2-5 mm. and a width (when flattened out) of about 4-5 mm.

Myctophum affine (Liitken) (Text-fig. 19)

St. 694, 040 05!' N.,-30° 00' W., 10. v. 31, NH, o m. B.M. Reg. no. 1948.5. 14. 234-6. Standard length 51 mm.
(9-0 x 4-0 mm.).

Text-fig. 19. Swimbladder of Myctophum affine, seen (a) in body-cavity, (b) ventrally (anterior end), and (c) laterally (anterior
end), gg, gas-gland; int, intestine; ov, oval; ra, retial artery; rm, rete mirabile; st, stomach; vov, vein to oval, (a, x^-^;
b, X25; c, X25.)

The swimbladder is thin walled and extends down some three-quarters of the length of the body-
cavity. The retia mirabilia extend back from the foremost tip of the sac and run to an oval-shaped
gas-gland lying on the floor of the anterior half. The gland measured 1-5 mm. in length and 1-25 mm.
in width, while the retia spanned about 1-5 mm.

To the left of the forward end of the swimbladder is the oval, which is closed, and appears as a
wrinkled projection with thick, expanded walls.

SURVEY OF STRUCTURE

Diaphus dofleini Zugmayer (Text-fig. 20 A, b)

St. 250, 360 09' 00" S., 5° 33' 00" W., 17. vi. 27, TYF, 3<x>(-o) m. B.M. Reg. no. 1930. 1. 12. 831-2. Standard
length 32 mm. (6-5 x 1-5 mm.).

This lantern fish has a thin-walled swimbladder, which originates over the forepart of the stomach
and spans nearly two-thirds the length of the body-cavity. The retia mirabilia arise to the right of the
lower surface of the sac, about 1 mm. behind its forward end. Each rete is nearly 1-5 mm. in length.
The three lobes of the gas-gland, which invest the middle part of the swimbladder floor, are roughly
oval in outline and measure 2-5 and 1 mm. in length and breadth.

Text-fig. 20. Swimbladders of Diaphus dofleini (a and b) and D. garmani (c). A and c are lateral views; B is a ventral view.
gg, gas-gland ; int, intestine ; k, kidney ; ov, oval ; oy, ovary ; pc, pyloric caecum ; rm, rete mirabile ; st, stomach, (a, x 8 ; B, x 10 ;
c,x8-5.)

Just above the point of origin of the retia and on the right side of the sac, the oval appears as a
circular cap (about 0-75 mm. in diameter). It is partly open, the capillary-bearing part being sur-
rounded by a ring of connective tissue containing circular and radial muscle fibres.

Diaphus garmani Gilbert (Text-fig. 20 c)
B.M. Reg. no. 1934.5.4. I_2- Montserrat. Standard length 34-5 mm. (6-o x 2-0 mm.).

A thin-walled swimbladder was found just above the stomach. The three retia mirabilia are bound
together in a club-shaped forward extension of the swimbladder. They are about 1 mm. in length
and supply a rather small gas-gland. This extends over the floor and lateral walls of the foremost
quarter of the organ.

Diaphus luetkeni (Brauer)

St. 288, oo° 56' 00" S., 140 08' 30" W., 21. viii. 27, TYF, 25o(-o) m. B.M. Reg. no. 1930.1.12. 846-7. Standard
length 34 mm. (3-5 x 1-2 mm.).

As the swimbladder of this fish was relaxed, the walls appear thick, while the gas-gland occupies
most of the floor. When the sac is expanded, the dimensions must be considerably more than those
given above.

38 DISCOVERY REPORTS

Standard length 54 mm. Diaphus agassizii Gilbert

This individual contained a well-developed swimbladder measuring about 7 mm. in length.

Notolychnus valdiviae (Brauer) (Text-fig. 2 id)

St. 1586, 020 39-4' N., 500 46-4' E., 2. v. 35, TYFB i6so-95o(-o) m. B.M. Reg. no. 1948.5. 14. 310-25. Standard
length 19 mm. (1-5 x 075 mm.).

As in other myctophids, the swimbladder originates over the stomach, but is so small that it does
not extend beyond this organ. Except for the roof, the gas-gland covers the entire inner surface of
the sac. The three retia mirabilia, which have a length of about 1-75 mm., run backwards and up-
wards along the right lateral wall of the stomach and enter the anterior part of the swimbladder floor.

In another fish (standard length 19-5 mm.) from St. 1586 the swimbladder had a length of nearly
2-5 mm. Though the sac of both fishes was somewhat relaxed, it would seem that the swimbladder of
this species is reduced in size.

Lampadena chavesi Collett (Text-fig. 21A-C)
Position, 5i°23'N., n°47'W. B.M. Reg. no. 1911.2.8. 1. Standard length 75 mm. (9-5 x 3-5 mm.).

The swimbladder of this lantern fish arises above the forepart of the stomach and extends down
the remainder of the body-cavity. The three retia mirabilia enter the right anterior part of the sac
and run backwards to supply a gas-gland covering the forward half of the swimbladder floor.

Each rete has an individual length. The innermost one, with a span of about 2-5 mm. supplies the
foremost lobe of the gas-gland, while the next lobe is fed by the middle complex, which is 4-5 mm. in
extent. The outermost rete is the largest (about 5-75 mm.) and runs to the posterior lobe of the gland.

Alongside the retia, forming an anterior extension of the swimbladder, is a conical projection
(presumably the oval) that is well supplied with blood-vessels.

Lampanyctus giintheri Goode & Bean (Text-fig. 22 a)

St. 710, 210 45' S., 39° 50' W., 26. x. 31, TYFB, 294^0) m. B.M. Reg. no. 1948.5. 14. 534-56. Standard length
53 mm. (9-5 x 2-5 mm.).

In this species the swimbladder is a thin-walled sac occupying about four-fifths the span of the body-
cavity. The rounded forward extremity lies just behind a vertical line drawn through the base of the
pectoral fins.

The three retia mirabilia lie under the forepart of the swimbladder and extend backward to the
medially situated gas-gland. Each rete is almost 3 mm. in length, while the gas-gland, which invests
the floor and side walls, has a length of 2-3 mm. The artery and vein supplying the retia mirabilia
come from the dorsal aorta and hepatic portal system respectively.

Centred above the middle point of the retia and on the left side of the swimbladder, the oval
appears as a thin-walled blister, 1 -8 mm. in width. This opens into the main cavity through an oval
aperture situated in the side wall just above the retia. The walls of the oval are richly supplied with
capillaries and larger vessels.

Lampanyctus alatus Goode & Bean (Text-fig. 22 b)

St. 2057, 120 09' S., 040 28-2' W., 29. iv. 37, N 450 B, i450-70o(-o) m. B.M. Reg. no. 1948.5. 14. Standard
length 57-0 mm. (9-0 x 2-5 mm.).

This species has a capacious swimbladder extending down about two-thirds the length of the
body-cavity. The walls are rather thin but well strengthened, with collagen fibres.

In side view the swimbladder has a gradually tapering forward section, the floor of which is

SURVEY OF STRUCTURE

st int sb

Text-fig. 21. Swimbladders of Lampadena chavesi (a) in body-cavity; (b) ventral view; (c) dorsal view (anterior end), and
(D) Notolychnus valdiviae, lateral view, gg, gas-gland; int, intestine; k, kidney; ov, oval; rm, rete mirabile; sb, swimbladder;
st, stomach, (a, x 6-9; b, x 99; c, x 18-9; D, x 30.)

4°

DISCOVERY REPORTS

covered by the gas-gland. This has three lobes, each receiving a rete mirabile. The retia originate in
front of the sac, and are bound together to form a cylindrical structure, before diverging over the
under surface of the gas-gland. The left, middle and right retia have lengths of about 2-5, 3-0 and
4-0 mm. respectively, differences parallel to those found in Lampadena chavesi.

Text-fig. 22. Swimbladders of Lampanyctus gnentheri (a) lateral view of anterior half, and L. alatus (b), ventral view of
anterior half, gg, gas-gland ; op, opening of oval into main cavity of swimbladder ; ov, oval ; ra, retial artery ; rv, retial vein ;
rm, rete mirabile. (a, x 27; B, x 22-5.)

Lampanyctus pusillus (Johnson)

St. 1602, 17° 59-9' S., 04° 27-1' E., 27. x. 35, TYFB, i7s(-o)m. B.M. Reg. no. 1948.5.14. 389-91. Standard
length 22 mm. (3-0 x 0-5 mm.).

St. 100 C, 330 20-330 46' S., 15° 18' -15° 08' E. 4. x. 26, TYF, 25oo-20oo(-o) m. B.M. Reg. no. 1930.1.12.
762-3. Standard length 33 mm. (6-5 x 1-5 mm.).

The swimbladder of this species lies over the posterior half of the stomach and extends beyond it
as far as the level of insertion of the pelvic fins. In both specimens the sac is considerably relaxed.

The retia mirabilia originate to the left of the anterior tip of the swimbladder and extend back-
wards to the gas-gland, which covers the forward part of the floor. Close examination of the 3 3 -mm.
fish revealed that each rete has a different length. The inner one supplies an anterior lobe of the gas-
gland, the middle one a middle lobe and the outer one a posterior lobe. Their lengths in the order
given are 3-0, 2-3 and i-8 mm.

An oval is present on the roof of the sac above the forward part of the retia.

SURVEY OF STRUCTURE

Gymnoscopelus nicholsi (Gilbert) (Text-fig. 23)

St. WS 213, 49°22'S., 6o°io'W., 30 v. 28, N 4-T, 249-259 m. B.M. Reg. no. 1948.5. 14. 621-6. Standard
length 50 mm.

The swimbladder, which is found over the middle region of the stomach, measured no more than
2-5 mm. in length. As in all myctophids, three retia mirabilia, which are closely bound together,
enter the anterior end of the swimbladder. The gas-gland is oval in outline and invests the floor of the
swimbladder over its anterior half. The walls of the bladder are so thick that little remains of the inner
cavity. Clearly, the organ has undergone considerable regression.

Text-fig. 23. Swimbladder of Gymnoscopelus nicholsi (a) seen in position in body-cavity, and (b) ventral view.
gg, gas-gland; int, intestine; k, kidney; rm, rete mirabile; sb, swimbladder; st, stomach, (a, x 12; B, x 22-5).

Ceratoscopelus townsendi (Eigenmann & Eigenmann)

St. 703, io° 59-3' N., 27°03-8'W., 17. x. 31, TYFB, 358-0 m. B.M. Reg. no. 1948.5. 14. 584-5. Standard
length 55-0 mm. (5-5 x 1-5 mm.).

Being in a rather relaxed condition, the swimbladder of this fish did not extend beyond the pyloric
end of the stomach. The three retia mirabilia enter the floor of the sac at its forward end to supply a
gas-gland that extends from one extremity to the other. However, when the sac is expanded con-
ditions may well be different.

Opposite the point of entry of the retia is the oval, which has the appearance of a collapsed blister.
The capillary network is fed through a vessel from the retial artery, while the return circulation is by
way of a large vein running upwards to the roof of the body-cavity.

42 DISCOVERY REPORTS

No trace of a swimbladder was found in adults of the following species: Gonichthys coccoi (Cocco),
Ctenobranchus nigro-ocellatus (Giinther), Diaphus coeruleiis Klunzinger, and Gymnoscopelus braueri
(Lonnberg).

Family Neoscopelidae

Neoscopelus macrolepidotus Johnson (Text-fig. 24)

John Murray Expedition St. 145, Maldive Area, 494 m. B.M. Reg. no. 1939.5.24. 475-84. Standard length
118 mm. (30-0 x io-o mm.).

A capacious swimbladder with rounded anterior and tapering posterior extremities runs down the
greater part of the upper body-cavity. The lower half of the sac, which is rather thick walled, is
invested with pigmented peritoneum.

Text-fig. 24. Swimbladder of Neoscopelus macrolepidotus, seen (a) from below. In (b) is shown a single rete and lobe
of the gas-gland, gg, gas-gland; rm, rete mirabile. (a, x 3-9; b, x 9-3.)

The gas-gland covers some two-thirds of the floor of the sac and is fed by five massive retia mira-
bilia. These originate from a blood-vessel junction, which is found on the right-hand side of the
anterior under-surface of the swimbladder. The junction receives a large vein from the hepatic portal
system and an artery from the system of vessels on the roof of the stomach. There is also a blood-
vessel (probably an artery) running backwards to the junction from the forward end of the swim-
bladder. But the fish is so poorly preserved that it is impossible to trace the blood-system with any
certainty.

SURVEY OF STRUCTURE 43

A careful search was made for the resorptive part of the swimbladder. No trace of an oval could be
seen or indeed of any such special capillary bearing region.

Scopelengys tristis Alcock
I have confirmed Alcock's (1899) finding that this species has no swimbladder.

Family Scopelosauridae

In this family, which consists of several species belonging to a single genus, the swimbladder is
absent in adolescent and adult individuals. The larvae have not been examined.

Suborder ALEPISAUROIDEA
Elsewhere I have stated that these iniomous fishes have no swimbladder (Marshall, 1955).

Order MIRIPINNATI

The swimbladders of these oceanic fishes have already been described (Bertelsen and Marshall, 1956).
During the larval phase the swimbladder is functional, but it regresses during the adolescent phase
and in Mirapinna, at least, is a rudimentary structure in the adult.

. There are two retia mirabilia receiving blood-vessels that extend forwards from the posterior end
of the swimbladder. In a larval Parataeniophorus gulosus of standard length 27-5 mm. the front part
of the sac is thick-walled and the walls are invested with a well-developed gas-gland on either side.
The posterior part of the sac is thin-walled and is presumably concerned in the resorption of gases.
In an adolescent P. festivus of standard length 42-0 mm. the thin-walled part of the swimbladder
is much reduced and the retia mirabilia and gas-gland have begun to regress. In the rudimentary
organ of Mirapinna, these structures are barely recognizable.

Order CETUNCULI
Family Cetomimidae
Ditropichthys stored (Goode & Bean)
St. 2059, 090 11-4' S., 05° 17-4' W., 30. iv. 37, N 450 B, 1900-1400 m. Standard length 30 mm.

In this fish a small swimbladder was found with a strong attachment to the roof of the stomach.
The sac measured about 2-5 mm. in length. Entering the posterior end of the sac was an artery
coming from a vessel running along the stomach wall. Another vessel originating in the roof of the
body-cavity ran to the ' anterior ' end.

Transverse sections through this organ revealed it to be much regressed, the small lumen having
a curiously complicated form. Much of the bulk of the swimbladder is formed by a voluminous
submucosa. The sections suggest that during the regression of the organ, the sac becomes doubled
back, the anterior and posterior ends coming together at the back. Within the lumen there were
remnants of the cells composing the gas-gland.

The interpretation of this curiously regressed organ must be left until earlier stages in the life-
history become available. Evidently the larvae of this species have a well-formed gas-filled swim-
bladder.

Cetostoma regani (Zugmayer)
No trace of a swimbladder was found in this species.

woods

HOLE,
MASS

6-2

DISCOVERY REPORTS

Family Rondeletiidae
Rondeletia bicolor Goode & Bean
Parr (1929) records the absence of the swimbladder in this species.

Order GIGANTUROIDEA

Regan (1925) included the absence of a swimbladder in his diagnosis of this order. I was unable to
find any trace of this organ in a Gigantura vorax of standard length 74 mm.

Order LYOMERI

Bertin (1934) has given an account of the internal organs of Eurypharynx pelecanoides and Sacco-
pharynx ampullaceus, but no mention is made of a swimbladder. I was unable to find this organ in
an individual of the first species.

Text-fig. 25. Swimbladder of Stylophorus chordatus, seen (a) from below, and (b) in the body-cavity of the fish, en, capillary
network; gg, gas-gland; k, kidney; lu, lumen of swimbladder; rm, rete mirabile; sb, swimbladder; st, stomach, (a, x 15;
b, x 1-8.)

Order ALLOTRIOGNATHI

Family Stylophoridae
Stylophorus chordatus Shaw (Text-fig. 25)
St. 296, 8° 12' N., 180 49' W., 26. viii. 27, TYF, 45o-5oo(-o) m. Standard length 177 mm.

This individual contained a small elongated swimbladder, lying just below the black-speckled
kidneys and originating a little before the pyloric end of the stomach. The sac measured about
12-5 mm. in length and i-o mm. in diameter and is attached by a mesentery to the dorsal wall of the
stomach.

Within the mesentery is an artery and vein running close together to the anterior end of the sac.
The two vessels continue together for about 3 mm. along the left-hand lateral walls and then sub-
divide to form a single rete mirabile having a length of about 2 mm. The rete enters the lumen of the
sac about half-way along its length (of about 4 mm.).

Examination of serial transverse sections revealed the disposition of the resorbent and glandular
parts of the swimbladder. The capillaries of the former lie just below the inner epitheleum and occur
over much of the lumen anterior to the point of entry of the rete. The glandular tissue lies behind this
point in the posterior half of the lumen. In supplying the gland, the retial capillaries do not unite
to form larger vessels. The rete is thus unipolar.

SURVEY OF STRUCTURE

Reference to Text-fig. 25 will show the small volume of the lumen compared with the total volume
of the sac. Between the inner epithelium and the tunica externa is a voluminous layer of lamellar
fibres belonging to the submucosa, which thus makes up most of the total volume. Clearly this is
a regressed swimbladder, which is doubtless relatively better developed during the early life-history.

In having a swimbladder with clearly separate glandular and resorbent parts, Stylophorus is
evidently an euphysoclist. But it is unusual in having these two parts reversed in position, for in most
euphysoclists (without an oval) the fore part is secretory, while the rear part is resorbent.

Text-fig. 26. Swimbladder of Stephanoberyx monae, seen (a) from above. In (b) is shown the blood supply to the right lobe
of the gas-gland, cl, capillary hop; gg, gas-gland; ov, oval; rm, rete mirabile. (a, x 5-5; b, x 17.)

Order BERYCOMORPHI

Family Stephanoberycidae

Stephanoberyx monae Gill (Text-fig. 26)

Oregon St. 1426 (290 07' N., 870 54' W.), 24. ix. 57, 600 fathoms, trawl. Standard length 83-5 mm. (16-0 x 8-o mm.).

The swimbladder of this species is ellipsoidal in form and extends down most of the length of the

upper part of the body-cavity.

The blood supply for the retia enters the floor of the sac close to its posterior end. The artery and
vein form two long retia mirabilia (about 8 mm. in length). In the fish dissected the retia were dis-
placed in position, but presumably extend forward along the swimbladder floor. Each rete runs to
a corresponding lobe of the gas-gland, where the capillaries form loops running through the secretory
tissue. The retia are thus unipolar in structure.

Immediately above this point of entry of the retial blood supply there is an oval on the roof of the
sac. This measured about 5 mm. in diameter and was partly closed. The capillary network of this
resorbent structure was plainly visible under the high power of a binocular microscope.

DISCOVERY REPORTS

Family Melamphaidae

Melamphaes megalops Liitken (Text-fig. 27)

St. 13° 25' N., 18° 22' W., 28. x. 25, 44-m. net, horizontal 90o(-o) m. Standard length 56 mm. (8-5 x 5-0 mm.).

In this species there is a capacious swimbladder which, when fully inflated, must occupy about
three-quarters of the length of the upper part of the body-cavity.

Text-fig. 27. Swimbladder of Melamphaes megalops, seen (a) in fish ; (b) ventrally, and (c) dorsally (posterior end). The
oval is shown in (d). cm, circular muscles of oval ; gg, gas-gland ; op, opening of oval into cavity of swimbladder ; ov, oval ;
ram, radial muscles of oval; rm, rete mirabile. (a, x 1 ; b, x 10; c, x 5 ; d, x 25.)

At the posterior end of the sac, an artery and vein run forward to supply a single rete mirabile,
which measures about 1 2 mm. in length. After its formation the rete runs backwards but soon bends
sharply to run along the right-hand side of the gas-gland. Having reached a point ahead of the
forward edge of the gas-gland, it turns back to enter the gland. Here it separates into capillary loops
that meander among the secretory cells. As in Stephanoberyx, the rete is unipolar. An extensive
gas-gland covers the median part of the swimbladder floor, the length and breadth being about 3 mm.

Just in front of the posterior tip and on the roof of the sac is an oval (about 2 mm. in diameter),
which was almost closed, the entry into the sac measuring about 0-5 mm. in width.

The circular sphincter muscles that close the oval could be seen around the rim of the opening,
where they are crossed by the long relaxed fibres of the radial complex. When these contract, the oval
is expanded, the capillary network then being fully exposed to the gases in the swimbladder. During
this phase gases are free to diffuse into the blood.

SURVEY OF STRUCTURE 47

Melamphaes unicornis Gilbert (Text-fig. 28 E, f)
St. 3484. 39° 55' N-. 2°° 01' W., 1. x. 56, IKMT, 75o(-o) m. (estimated). Standard length 51 mm. (6-5 x 2-5 mm.).

The swimbladder of this melamphaid, which was quite relaxed, lies above the posterior half of
the stomach.

Blood-vessels running down from the roof of the body-cavity enter the swimbladder roof at the
posterior end, where they supply the oval, which was completely closed.

The single rete mirabile is about 3 mm. in total length. Since the sac is much contracted the rete
may well have been displaced forward from its natural position. In this swimbladder it originates
in a median lateral position and runs forward and across the floor of the sac, then turning backward
to the gas-gland, which is indented along its posterior edge.

Melamphaes mizolepis (Giinther) (Text-fig. 28b-d)

St. 288, oo°56'S., i4°o8-5'W., 21. viii. 27, YFT, 25o(-o) m. B.M. Reg. no. 1930.1.12. 1031-40. Standard
lengths of two individuals examined 15 and 37 mm.

In the smaller of the two fishes dissected a small spherical swimbladder was discovered over the
anterior part of the stomach. It measured 0-4 mm. in diameter. The rete mirabile runs forward to
enter the posterior part of the swimbladder roof and then turns sharply downward to follow the
outline of the organ as far as the front part, where it joins the gas-gland. This is a compact spherical
structure almost filling the lumen.

The posterior tip of the rete appeared to be closely bound to the stomach. Actually two branches
from the blood-vessels running over the stomach enter the rete.

The structure of the swimbladder in the larger fish was very similar. The diameter was o-8 mm.
In both individuals it is obvious that the swimbladder is little more than a regressed organ.

Melamphaes cristiceps Gilbert

St- i°i. 33° 5°' to 34° 13' S., i6°04' to i5°4o/E., 15. x. 26, N 450 H, 1310-1410111. B.M. Reg. no. 1930.1.12.
1006-8. Standard length offish 80 mm.

A small swimbladder was found behind the stomach and just in front of the ovaries. It measured
3-5 mm. in length. As in M. mizolepis, the rete mirabile runs round much of the swimbladder before
entering the gas-gland. It is evident that the swimbladder of this species is also regressed.

A fully developed swimbladder is also found in Melamphaes macrocephalus, M. nigrofulvus,
M. opisthopterus ? M. nycterinas and M. cristiceps ? (Kanwisher and Ebeling, 1957).

Family Anoplogastridae

Anoplogaster longidens (Gill) (Text-fig. 28 a)

St. 239, 46°56'S., 46°03'W., 2. vi. 27, N 450, i05o-i35o(-o) m. B.M. Reg. no. 1930.1.12. 974-6. Standard
length of fish 98 mm.

In the medium-sized individual examined the swimbladder was found to be a small, almost
spherical sac overlying the foremost part of the stomach. Excluding the retia mirabilia, it measured
rather more than 3 mm. in length and about 2 mm. in greatest depth. The walls are thick and tough.

Two retia mirabilia about 1 mm. in length enter the posterior end of the swimbladder, each running
to a lobe of the gas-gland. Together the two glandular lobes invest the floor and lateral walls of the sac.

The swimbladder is surrounded by fatty tissue which is continued backwards for about 20 mm.
to taper off above the end of the stomach. The blood supply for the retia mirabilia came from vessels
within the fat body.

DISCOVERY REPORTS

Text-fig. 28. Swimbladders of Anoplogaster longidens (a) seen from below; Melamphaes misolepis, (b) lateral view, (c) dorsal
view, (d) lateral view; M. unicornis, (e) dorsal view; (f) lateral view, ft, fat investment; gg, gas-gland; ov, oval; rm, rete
mirabile. (a, x 8-5 ; B, C, d, x 25 ; e, x 10 ; F, x 6.)

From this dissection it would appear that in adult Anoplogaster the swimbladder can have very
little hydrostatic function.

Order PERCOMORPHI

Family Chiasmodontidae

Chiasmodon niger Johnson (Text-fig. 29)

St. 239, 46°56'S., 46°03'W., 2. vi. 27, N 450 H, io50-i35o(-o) m. B.M. Reg. no. 1930.1.12. 1058. Standard
length 50 mm. (8-o x 1-5 mm.).

Position, 6° 55' N., 150 54' W., 2-m. tow-net, horizontal, 8oo(-o) m. B.M. Reg. no. 1930. 1. 12. 1057. Standard length
49 mm. (8-o x 1-5 mm.). B.M. Reg. no. 1922.5.26. 1-2. Madeira. Standard length 104 mm. (21-0 x 3-0 mm.).

In each of the three fishes examined, the swimbladder is an elongated ellipsoidal sac, which in the
104 mm. specimen occupied the greater part of the upper half of the body-cavity.

The retia are formed from an artery and vein that enter the forward tip of the sac. In the 49-mm.
fish there were eight, each running backward to supply a corresponding lobe of the gas-gland and
having a length of 3-25 mm. A closely similar retial measurement was also obtained from the
largest individual.

SURVEY OF STRUCTURE

In the 50-mm. fish a transverse diaphragm was found in the posterior half of the swimbladder.
There is an aperture in the central part of the diaphragm, through which the anterior chamber con-
taining the retia and gas-gland, communicates with the posterior chamber. It is clear that the
structure of the swimbladder of Chiasmodon is essentially similar to that found in other physoclist
teleosts, in which a diaphragm separates an anterior gas-producing chamber from a posterior resorbent

Text-fig. 29. Swimbladder of Chiasmodon niger (ventral view), seen in three different states of activity ; (a) with the resorbent
posterior chamber well expanded, (b) with the gas-secreting and resorbent chambers about equal in volume, and (c) with
the gas-secreting chamber well expanded, dm, diaphragm; gg, gas-gland; rm, rete mirabile. (a, x 6-9; B, x 19-5; c, x 18.)

chamber. It is also evident that the relative volumes of these two chambers vary in the three specimens.
In the largest fish the diaphragm is close behind the gas-gland in the anterior third of the swim-
bladder, while it occupies a median position in the 49-mm. individual. These variations will be con-
sidered at greater length in the section concerned with gas resorption (p. 81).

The swimbladder is absent in two other members of the Chiasmodontidae, Pseudoscopelus scriptus
and Dysalotus alcocki.

5o DISCOVERY REPORTS

Order PEDICULATI

Suborder CERATIOIDEA

The combined researches of Garman (1899), Waterman (1948), R. Clarke (1950) and Bertelsen (1951)
show that the deep-sea angler fishes have no swimbladder. Bertelsen's work reveals that this organ
is also absent in the larvae.

STRUCTURE AND SYSTEMATICS

The foregoing survey has revealed that the species of major groups of bathypelagic fishes (Stomia-
toidea, Salmonoidea, Myctophidae and Anoplogastroidea) have swimbladders conforming to an
individual structural pattern or bauplan. Within each group there are, so to say, variations on an
original structural theme. The bearing of these findings on classification will now be considered.

Order Isospondyli

Deep-sea isospondylous fishes with a swimbladder are all physoclists : they lack a pneumatic duct,
which in physostomatous Isospondyli connects the swimbladder to the foregut. The acquisition of
a closed swimbladder in these stomiatoids and deep-sea salmonoids must have been imposed on them
by their living-space in oceanic mid-waters. The physostomatous isospondyls live in the relatively
shallow seas over the continental shelves, or in freshwater. While at least some of these forms can
secrete gas, this is a slow process, but they are readily able to inflate their swimbladders by gulping
in air at the surface and forcing it down the pneumatic duct. On the other hand, a visit to the surface
by a hypothetical physostome living several hundred metres below the surface is clearly ' out of the
question '. Such a fish would not only be faced with a long climb to the surface, but having replenished
the swimbladder gases, would then have to resolve the problem of the gradient in hydrostatic pressure
as it returned to its level in the ocean. After diving to a depth of say, 500 m., the volume of the
swimbladder would be compressed to about one-fiftieth of its capacity at the surface. If the fish is to
use its swimbladder as a hydrostatic organ, it must then secrete gas, and to make up the volume (to
5 per cent of the body volume, see p. 68) at a pressure of 50 atmospheres would obviously require
highly developed retia mirabilia and gas-glands. The retention of a pneumatic duct and air-gulping
habits by a mid-water, deep-sea fish is therefore a biological reductio ad absurdum.

Suborder Stomiatoidea

The stomiatoid swimbladder has a character complex which may be defined as follows : It is para-
physoclistous1 with a single, bipolar rete mirabile at the posterior end. As might be expected, the
blood supply to the rete comes from vessels originating behind the swimbladder. The capillary
network of the resorbent surface arises from a side branch of the retial artery and part of the venous
circulation to the gas-gland. The venous blood thus eventually passes through the rete. The gas-
producing complex is highly developed, the gland consisting of one to four lobes. A schematic
diagram is shown in Text-fig. 30 A.

Comparison of this definition with that of any of the following groups (pp. 53-56) will fully reveal
the very characteristic design of the stomiatoid swimbladder. It will also provide further support
for the classification of the stomiatoids as a distinct suborder of the Isospondyli.

Regan (1923) was the first to appreciate the essential unity of the stomiatoids. His definition of the

1 This term was introduced by Rauther (1922) and refers to simple closed swimbladders in which the glandular and
resorbent parts are not sharply localized. It is contrasted with the euphysoclistous type, the resorbent part of which is clearly
separate from the glandular part, being either in the form of an oval, or an anterior or posterior section of the sac. In the
latter forms, the two parts are often divided by a diaphragm. Fange (1953) has also pointed out that in euphysoclists the
resorbent part is thin-walled, while the glandular part is thick-walled. In paraphysoclists there is no such distinction.

STRUCTURE AND SYSTEM ATICS

A stomiatoid

D Neoscopelus

Melamphaes

B salmonoid

E Miripinnati

H Stephanoberyx

C myctophid

Stylcphorus

Chiasmodon

Text-fig. 30. Schematic diagrams showing the essential structural features of the swimbladders of (a) stomiatoids, (b) deep-
sea salmonoids, (c) Myctophidae, (d) Neoscopelus, (e) Miripinnati, (f) Stylophorus, (g) Melamphaes, (h) Stephanoberyx,
(J) Chiasmodon. Arteries shown black, veins white, bpr, by-pass branch of retial artery; en, resorbent capillary network;
dm, diaphragm ; g£, gas-gland; mrm, micro-rete mirabile; ov, oval, rm, rete mirabile.

7-2

52 DISCOVERY REPORTS

group was later somewhat amplified (Regan and Trewavas, 1929). The stomiatoids were regarded as
being most closely related to the clupeoids, but differing from them in possessing photophores.
Certain alepocephalids and searsids, which are clupeoids, also have light organs, but the individual
feature of the stomiatoid photophore pattern is the presence of one or two series of lights along each
side of the mid-ventral line and one or more photophores associated with each eye (Brauer, 1908;
Marshall, 1954).

It is evident that much of Regan's appreciation of the stomiatoids could not be put into words.1
At all events his definition of them has proved to be inadequate. But when the swimbladder characters
are considered together with those Regan used, the stomiatoids are revealed as a ' natural ' mono-
phyletic group. The implications of this will best be discussed at later stages in this systematic section.

Turning now to the arrangement of the stomiatoids into families, study of the swimbladder
provides no new insight. It will be remembered that the Chauliodontidae, Melanostomiatidae,
Malacosteidae and Idiacanthidae have no swimbladder, while such features as can be seen in the
rudiments of this organ in certain of the Stomiatidae are merely typical of the suborder. Even in the
Gonostomatidae, Sternoptychidae and Astronesthidae, which have swimbladders, the knowledge
gained has little bearing on their relationships. This may best be shown by the following illustration :

Considering the first two families, Hubbs (1953) has cogently urged that they should again be
referred to a single family, Sternoptychidae, with subfamilies Gonostomatinae, Maurolicinae and
Sternoptychinae. Hubbs sees these subfamilies (in the order given) as forming a series ranging from
forms with generalized to those with specialized body-shapes. Comparison of the swimbladder structure
in the three groups also shows that there are no clear-cut differences between them, but if swim-
bladder characters alone were considered, the Astronesthidae could also be put with them (and into
the same family). However, the other characters of the Astronesthidae indicate that they are best
regarded as a separate family and that they are closer to the Chauliodontidae and Melanostomiatidae
than to the gonostomatids and sternoptychids (Regan and Trewavas, 1929).

At the generic level, however, swimbladder characters can be of use in definitions, but not always.
This may best be shown by short descriptions under the genera that were studied :

Family Gonostomatidae

Gonostoma. The differences between the swimbladders of G. denudatum and G. elongatum are so great that no
common features can be found to typify the genus.

Cyclothone. The larval swimbladder (in which the gas-gland is found anteriorly), regresses and becomes
invested with fat in the adult.

Pollichthys. An oval-shaped resorbent area on the floor of the swimbladder is surrounded by a horseshoe-shaped,
single-lobed gas-gland. The bladder is ellipsoidal in form.

Vinciguerria. The resorbent area lies between the rete mirabile and a boomerang-shaped single-lobed gas-gland,
which extends over the floor and side walls of the median part of the swimbladder.

Photichthys. The swimbladder of this gonostomatid is readily distinguished from those of other genera by its
elongated tubular form.

Maurolicus. The gas-gland consists of two pairs of lobes, a smaller pair near the rete mirabile and a larger pair
on the floor of the mid-region of the bladder. The resorbent area lies between these lobes.

Bonapartia. There is a single lobe to the gas-gland, immediately in front of which comes the resorbent area,
which invests the floor of the swimbladder.

Ichthyococcus. The gas-gland has three lobes.

Family Sternoptychidae
Sternoptyx. The gas-gland is three-lobed, while the resorbent area lies between and beyond these lobes.

1 Pantin (1954) aptly calls such recognition 'aesthetic', as opposed to the analytical deductive methods that the systematist
must eventually use.

STRUCTURE AND SYSTEMATICS 53

Argyropelecus. The gas-gland surrounds the resorbent area which is on the floor of the swimbladder. The form
of the swimbladder is ellipsoidal but approaches that of a sphere.

Polyipnus. The gas-gland is bilobed and the resorbent area lies between the lobes. In the adult the swimbladder
is invested with fat.

It will be seen that certain swimbladder features, particularly the form of the gas-gland and its
position relative to the resorbent area, can be used as diagnostic features in certain of the genera.
Perhaps the associated circulatory system could also have been used; for instance, in the genera
Vinciguerria, Maurolicus and Polltchthys. But the circulatory system can vary considerably within a
genus and its species (see Godsil and Byer's (1944) study of the tunnies). Until more data are avail-
able it would seem best not to use the arrangement of blood-vessels as taxonomic characters.

Lastly, this survey has not been wide enough for much to be said on the distinguishing of species
of deep-sea fishes by means of individual swimbladder structures. In one genus, Gonostoma, the
three species are very unlike in this respect; I have already written (Marshall, 1950, 1954, 1955;
Jones and Marshall, 1953) that G. denudatum has a normal type of swimbladder, that in G. elongation
the swimbladder regresses and becomes invested with fat, and that G. bathyphilun has no swimbladder.
Differences of this order would seem, at first sight, to call for separate generic status for these three
species. But reference to the papers just mentioned will show that there is a correlation between the
degree of development of the swimbladder and the vertical distribution of each species. There seem
tp be parallel correlations in eye-structure, coloration (Marshall, 1954) and in other features (pp. 99-
100). As closer study of such correlations is in progress, review of the status of the genus Gonostoma
will be left until this work is completed. At present, however, there seems little justification for
changing the present classification.

Suborder Salmonoidea

The design of the swimbladder in the deep-sea salmonoids is very unlike that of the stomiatoids. The
individual features are as follows: The swimbladder is euphysoclistous1 (see footnote on p. 50) and
the blood-vessels forming the retial system break up into numerous micro-retia, each consisting of
a relatively small number (less than 50) of arterial and venous capillaries (or arterioles and venules).
The gas-gland is diffuse rather than compact (Text-fig. 30 b).

The deep-sea salmonoids undoubtedly form a compact, natural group within the suborder Sal-
monoidea. Gunther (1866) placed Argentina and Microstoma in the Salmonidae and Brauer (1906)
regarded Winter ia and Opisthoproctus as other members of this family. Trewavas's (1933) anatomical
study of Opisthoproctus properly revealed its salmonoid affinities, while the later work of Chapman
19420, b, 1943, 1948) clearly established the relationships between the above genera and Rhyncho-
hyalus, Bathylagus, Leuroglossus, Dolichopteryx and Macropinna. More recently, Bertelsen (1958) has
shown that Xenophthalmichthys is also an argentinoid fish, being closely related to Microstoma
and Nansenia.

After Berg (1940) had introduced a new suborder (Opisthoproctoidei) for Opisthoproctus, Chapman
(19426) subscribed to this opinion, but proposed that all the other genera should also be included in
the new suborder (Berg puts them in the Salmonoidea).

The swimbladder characters support Chapman's contention that Opisthoproctus should not be
placed apart from the other deep-sea salmonoids. To Chapman's (1942 a) list of characters for his
' opisthoproctoid ' fishes may be added those given above concerning the swimbladder. Furthermore,
the similarities in the design of the swimbladder are so striking that some support is given to Hubbs's

1 In Argentina, Glossanodon, Microstoma and perhaps in Nansenia the posterior part of the swimbladder is thin-walled
and functions as the resorptive part of the sac. In Opisthoproctus and Winteria this part of the sac may also have this function,
but the material available was not sufficient to confirm this suspicion.

S4 DISCOVERY REPORTS

(1953) idea of putting the deep-sea salmonoids into a single family, Argentinidae. (At present they
are grouped into the families Argentinidae, Bathylagidae, Microstomidae, Xenophthalmichthyidae,
Dolichopterygidae, Winteriidae, Macropinnidae and Opisthoproctidae.) While Hubbs may be want-
ing to make too great a leap in the other direction, there would seem to be good reason for regrouping
of these fishes to give better expression of their relationships. Perhaps the suborder Salmonoidea
might be split into the divisions Salmoniformes and Argentiniformes, the latter containing the deep-
sea forms. The last four families, in parentheses above, could be united into one, Opisthoproctidae,
following Hubbs's first suggestion in his paper, while Xenophthalmichthys, in view of Bertelsen's
(1958) work, could be included in the Microstomidae.

Order Iniomi

When defining this order, Berg (1940) wrote that the swimbladder, if present, has a pneumatic duct.
The only iniomous fishes with a swimbladder are the Myctophidae and Neoscopelus (see also Marshall,
1955) and these have a closed swimbladder. There is nothing resembling a pneumatic duct in the
adult, although the ' oval ' in the myctophids may perhaps arise from the posterior part of the larval
connection between the gut and the swimbladder. Like the stomiatoids, the iniomous fishes were
most probably derived from an early type of teleost fish with an open swimbladder, and as Tracy
(191 1) suggested, the oval may have been evolved by a progressive reduction of the pneumatic duct.
At all events, it would be interesting to study the development of the 'oval' in a myctophid.

The swimbladder of iniomous fishes is very unlike that of the stomiatoids and salmonoids. It is
physoclistous1 with three to five retia mirabilia which originate at the anterior end of the bladder.
As might be expected, the retia draw their blood from vessels that arise in front of the swimbladder.
Each rete usually supplies a corresponding lobe of the gas-gland.

Suborder Myctophoidea

The myctophid swimbladder is definitely euphysoclistous, having at the anterior end of the sac
an ' oval ' type of resorbent surface. There are always three unipolar retia mirabilia supplying the
gas-gland (see Text-fig. 30 c). These individual features provide more evidence for regarding the
myctophids as a compact monophyletic group, but the ancestor of the myctophids can hardly have
been 'derived from Isospondylous stock very like the Gonostomatidae ' as Fraser-Brunner (1949)
supposed. The differences between the stomiatoid and myctophid swimbladders are very consider-
able as Table 1 shows.

Table 1 . Stomiatoid and myctophid swimbladders

Myctophidae

Stomiatoidea

Swimbladder type

Euphysoclist (with oval)

Paraphysoclist

Number of retia

Three

One

Type of rete

Unipolar

Bipolar

Position of rete

Posterior

In view of this, it is unlikely that the specialized swimbladder of a stomiatoid could have been
transformed into that of a myctophid. As already suggested, the Myctophidae were probably derived
from an early generalized form of isospondylous fish. The common origin of the myctophid and
stomiatoid lines of evolution would thus be further back in the early history of the teleosts.

1 I was unable to determine whether Neoscopelus was a euphysoclist or paraphysoclist.

STRUCTURE AND SYSTEMATICS 55

Neoscopelus

Apart from the uncertainty of its type of swimbladder, this genus is readily distinguished from all
myctophids in the number of retia mirabilia, there being more than three retia (five in two individuals
that were examined (Text-fig. 30 d). Neoscopelus has been classified within the Myctophidae, either
as one of the genera, or as the type, of the subfamily Neoscopelinae (Fraser-Brunner, 1949). In many
ways it is quite unlike the myctophids (sensu stricto), particularly in the arrangement and structure of
the light organs (Brauer, 1908). Such differences, together with those found in the swimbladder,
certainly indicate that the genus should be placed apart from the myctophids. As already suggested
(Marshall, 1955), it might be better to put it into a separate family (Neoscopelidae) together with the
genera Scopelengys and Solivomer.

Order Miripinnati

The basic features of the swimbladder of these fishes have already been described (Bertelsen and
Marshall, 1956). In the sharp separation of an anterior thick-walled secreting part from a posterior
thin-walled resorbent part, the organ is euphysoclistous, but there appears to be no diaphragm. The
gas-gland receives its blood supply through two unipolar retia mirabilia that originate in the middle
region of the sac and are formed from a posterior artery and vein (Text-fig. 30 e).

The only known oceanic fishes with two such retia mirabilia are Anoplogaster and Stephanoberyx,
but in the latter genus, and in the Melamphaidae, the resorbent part of the swimbladder is formed by
an oval.

Order AUotriognathi , Family Stylophoridae

The swimbladder of Stylophorus is readily distinguished from those of other pelagic, deep-sea fishes.
It is euphysoclistous with a single unipolar rete mirabile receiving blood from an artery-vein pair
that originates in front of the forward end of the sac. Unlike most euphysoclists, the front half of the
swimbladder is provided with a resorbent capillary system, while the rear half contains the gas-
producing glandular tissue (Text-fig. 30F). The organ regresses during adult life.

Order Berycomorphi

The bathypelagic members of this group are mainly to be found in Regan's ( 1 9 1 1 ) order Xenoberyces.
The families are Stephanoberycidae,1 Anoplogastridae and Melamphaidae. Parr (1929) also placed
the Rondeletiidae in Regan's order, but Harry (1952) has provided ample evidence for regarding this
family, together with the Barbourisiidae and Cetomimidae, as forming a 'natural group widely
distinct from all other families of fishes. . .'. The three genera considered in this report, Stephano-
beryx, Anoplogaster and Melamphaes, all have a closed swimbladder2 with one or two unipolar retia
mirabilia that originate at the posterior end of the sac.3 In Stephanoberyx and Melamphaes, the swim-
bladder is definitely euphysoclistous, for an 'oval' is present (Text-fig. 30 G, h).

Regan (191 1) decided that the Stephanoberycidae and Melamphaidae were sufficiently different
from ' typical Berycomorphi ' to be placed in a separate order, Xenoberces. They are also distinct in
swimbladder characters. As we have seen, in Stephanoberyx, Anoplogaster and Melamphaes, there are
one or two retia that originate at the posterior end of the swimbladder. In the Berycomorphi, as
restricted by Regan, all available evidence shows that the retia originate at the anterior end of the sac
(Rauther, 1922; Nelson, 1955).

1 Stephanoberyx may be demersal rather than pelagic in habit.
Stephanoberyx is said to have a pneumatic duct (Regan, 191 1 ; Berg, 1940), but I was unable to find one.
Dr A. Ebeling, who is revising the Melamphaidae, has been good enough to tell me that in certain melamphaids
(Melamphaes s.s.) the retia are at the front of the swimbladder.

56 DISCOVERY REPORTS

But such differences, together with those found by Regan, would hardly seem to require separate
ordinal status. Regan himself felt that the Xenoberyces were ' probably derived from the same stock
as the Berycomorphous fishes '. It would thus be preferable to regard the ' Xenoberyces ' as a sub-
order of the Berycomorphi. The other fishes of this order (Regan's Berycomorphi) would form the
other suborder.

The order Berycomorphi (sensu lato) may be defined as physoclistous teleosts with the anterior
rays of the vertical fins spinous and with nineteen principal rays (seventeen of which are branched) in
the caudal fin (eighteen principal rays with sixteen branched in the Polymixiidae). Pelvic fins sub-
abdominal or thoracic, with or without a spine, and with three to thirteen soft rays. Mouth bordered
above by protractile premaxillae ; one or two supramaxillae. Orbitosphenoid present or absent.

Suborder Berycoidea: Families Polymixiidae, Berycidae, Diretmidae, Trachichthyidae, Mono-

CENTRIDAE, ANOMALOPIDAE, HOLOCENTRIDAE

Orbitosphenoid present ; a subocular shelf usually developed, palate usually toothed one or two supra-
maxillae (Regan, 191 1). Swimbladder with retia mirabilia originating at the anterior end of the sac.

Suborder Anoplogastroidea : Families Stephanoberycidae, Melamphaidae, Anoplogastridae1

No orbitosphenoid; no subocular shelf; palate toothless; a single supramaxilla, triangular in shape
(Regan, 191 1). Swimbladder with one or two retia mirabilia, usually posterior in position: an oval
at the posterior end of the sac.

Order Percomorphi, Family Chiasmodontidae

Like many other percomorph fishes, Chiasmodon niger has a euphysoclistous swimbladder with a
diaphragm separating an anterior gas-producing chamber from a posterior resorptive chamber
(Text-fig. 30J). Jones and Marshall (1953) and Fange (1953) have drawn attention to percormorphs
with this type of swimbladder.

To conclude, there is the problem of what the structural pattern of the swimbladder may add to
present conceptions of the relationships between the major groups of deep-sea teleosts.

The Isospondyli undoubtedly contain the most generalized forms of teleosts. Although the fishes
of each isospondylous suborder are specialized in varying degrees, they still retain certain characters
of the early primitive teleosts. While the stomiatoids have special features, such as light organs, that
are correlated with a bathypelagic mode of life, Regan (1923) looked on them as being quite similar
to the clupeoids. He found the skull of Photichthys to be very like Elops, which is perhaps the most
primitive of all living teleost genera. The extreme development of the gas-producing tissues of the
swimbladder (or the complete loss of this organ) is also an adaptation to a deep-sea existence, but the
structural pattern is quite unlike that in any other group, whether deep-sea or otherwise.

It is unlikely, as already stated, that the Myctophidae, with a very different form of swimbladder,
were derived from a stomiatoid stock. In acquiring an oval, the myctophids have a remarkably
advanced type of swimbladder relative to their position in the evolutionary scale of teleosts. Above the
Iniomi, an oval is not encountered until the Anacanthini (cod-like fishes) are reached. However, an
oval would seem to be no more efficient a resorbent surface than the capillary system in stomiatoids.
Astronesthes is no more limited in its vertical migrations than the myctophids on which it feeds (see
p. 88). From the functional as well as the structural aspect, the conclusion repeated in the first
sentence of this paragraph seems to be justified.

1 Grey (1955) has confirmed that Anoplogaster cornuta (Val) is the young of Caulolepis longidens Gill and also synonymizes
the latter under the former (in accordance with the principle of priority in the International Rules of Zoological Nomen-
clature).

STRUCTURE AND SYSTEMATICS 57

The Miripinnati and most Anoplogastroidea resemble the stomiatoids in having retia that are formed
at the posterior end of the swimbladder, although both groups consist of euphysoclists, while all
stomiatoids are paraphysoclists. The transformation of a stomiatoid type of swimbladder, with its
unique vascular arrangements for the resorption of gases, to either the miripinnatous or anoplo-
gastrid form would seem most unlikely. It is thus evident that the stomiatoids are a well-defined
phyletic line of isospondylous fishes which, as the result of evolution in other directions, have left no
living descendants.

Earlier discussion suggests this is also true of the deep-sea salmonoids. They are a compact,
specialized group, forming a morphological (perhaps also an evolutionary) series towards forms like
Opisthoproctns. However, the 'bauplan' of their swimbladder could very well have been derived
from the more generalized condition seen in the salmonids.1

i >>'.' ft... #

' •-- 2j''«

. mrm

Text-fig. 3 1 . Semidiagrammatic representations of transverse sections through the swimbladder wall of (a) Salmo ; (b) Opis-
thoproctus. cp, capillaries ; ie, inner epithelium ; gg, gas-gland ; mrm, micro-rete mirabile ; sm, submucosa ; sml, layer of smooth
muscle ; te, tunica externa.

In Salmo the swimbladder is supplied with arterial blood through branches of the coeliaco-mesen-
teric and intercostal vessels. Venous blood leaves through a vessel running forward to the portal
system and through others leading to the intercostal and gonadial veins. The capillary stem may here
and there form associations, but there is no regular development of retia mirabilia. The inner epithe-
lium over the forward part of the sac, consists of columnar cells, elsewhere of flattened or cubical
cells (Rauther, 1922). All that is required to turn such a swimbladder into the deep-sea salmonoid
type is the regular association of capillaries to form micro-retia mirabilia, the differentiation of the
inner epithelium to form gas-glands and, of course, the loss of the pneumatic duct. This may be
better followed in Text-fig. 31, which shows semi-diagrammatic, transverse sections through the
swimbladder walls of Salmo fario and Opisthoproctus soleatus.

The lineages represented by the orders Iniomi, Cetunculi, Chondrobrachii and Miripinnati may
well have evolved from a common ancestor. Presumably this ancestral fish had advanced beyond the
level of organization of the primitive Isospondyli (in that its premaxillae excluded the maxillae from
the biting edge of the upper jaw and the mesocoracoid arch was lost from the shoulder girdle). The
orders Giganturoidea and Lyomeri may also belong to this evolutionary complex (Bertelsen and
Marshall, 1956).

The only fishes in these orders with swimbladders are the Myctophidae, Neoscopelidae (Iniomi),
and the Miripinnati. The Myctophidae and Neoscopelns are considered to be rather closely related,
1 Fahlen (1959) has shown that there are (micro)-retia mirabilia in the swimbladder of Coregonus lavaretus.

58 DISCOVERY REPORTS

and this, as we have seen, is supported by the similarities between their swimbladders. But there is
little resemblance, other than that implied by the general label ' euphysoclist ', between the miri-
pinnatous and myctophoid type of swimbladder. Again, it would seem that the two groups are not
closely related and that each is the result of a distinct evolutionary trend within the iniomous complex.
But morphological knowledge of the various groups is by no means comprehensive. In time it may
be possible to regard the Chondrobrachii, Cetunculi, Miripinnati and perhaps the Giganturoidea and
Lyomeri as suborders of the Iniomi. At present their differences are more apparent than their
similarities.

Whereas the Isospondyli are the basal group of soft-rayed fishes, the Berycomorphi occupy a
similar position within the spiny-finned groups. These fishes have ' advanced ' beyond the iniomous
level of organization in the development of spinous rays in the vertical and pelvic fins. But like many
of the soft-rayed fishes with a fully developed caudal fin, nearly all Berycomorphi have nineteen
principal rays in this fin.

After their origin, the berycomorphs seem to have split up into two series of lineages, now repre-
sented by the suborders Berycoidea and Anoplogastroidea. The former group mainly consists of
shallow and deep water fish, whereas in the latter the fishes are predominantly bathypelagic in habit.
It is curious that like the stomiatoids among the Isospondyli, the purely deep-water group of beryco-
morphs acquired a swimbladder with a reversed polarity, the gas-secreting complex coming to a focus,
as it were, at the posterior end of the sac. The differences between the stomiatoid and anoplogastroid
swimbladder, to which some reference has already been made, are summarized in Table 2 :

Table 2. Szvimbladder structure: Berycomorphi mid Isospondyli

Isospondyli Berycomorphi

Swimbladder Stomiatoidea Anoplogastroidea

Type Paraphysoclist Euphysoclist (with oval)

Type of rete Bipolar Unipolar

Position of rete Posterior Posterior

Number of retia One One or two

As in the earlier comparison between the stomiatoids and myctophids, there is little reason to
suppose that the second group might have been derived from the first. However, the berycomorphs
may well have come from a primitive type of iniomous fish (in that its premaxillae alone formed the
biting part of the upper jaw). The present-day representatives are all marine fishes and their evolu-
tionary radiations, with the notable exception of the Holocentridae, have been mostly directed to-
wards the deep ocean. Considering only marine teleosts, it looks as though some of the groups, that
evolved during the early 'explosive' radiations of the soft-rayed and spiny-rayed teleosts, were
' edged out ' from the more productive shelf-waters into the deeper, less favourable waters of the ocean.

As the common ancestor of both assemblages is likely to have had an open swimbladder, and as
a closed one seems to be essential for an oceanic fish, it may well be that the physoclistous condition
was independently evolved in the deep-sea Isospondyli and Berycomorphi. Furthermore, the same
is probably true within the Isospondyli themselves, for it seems clear that the deep-sea salmonoids
were derived from physostomatous stock (p. 55) and it is also evident that the stomiatoids were not
part of this evolutionary line (p. 50). Again, the type of closed swimbladder possessed by the Mycto-
phidae could well have been independently acquired. While the common ancestor of the soft-rayed
and spiny-rayed groups must be sought at an early stage in teleost evolutionary history, the common
factor in these developments of a closed swimbladder seems to be no more than residence in a living
space in the deeper reaches of the ocean.

structure and systematics s9

The larval swimbladder
The teleost swimbladder arises early in development as an outgrowth of the dorsal or lateral walls of
the foregut. While the embryonic formation of the swimbladder in a deep-sea fish has yet to be
described, the sequence of events is likely to be very similar to that in shallow water fishes. When
considering the general features of myctophid larvae, Holt and Byrne (191 1) mentioned that from a
very early stage the roof of the swimbladder appeared to be darkly pigmented. It is also clear from
Jespersen and Taning's (1926) figures that the early post-larvae of gonostomatid fishes have a well-
formed swimbladder. In post-larval Vinciguerria and Maurolicus I found the swimbladder to be
full of gas.

The presence of gas in the larval swimbladder raises an interesting question concerning the early
functioning of the organ in the deep-sea environment. In many shallow water fishes the sac is first
inflated by the larvae gulping in air at the surface and passing it down the larval pneumatic duct
(which disappears during later development in physoclists). While the larval life of most bathypelagic
fishes is passed in the surface-layers, it seems likely that the eggs are shed at deeper levels. Hatching
may thus take place as the eggs float upwards from the depths. If so, many larvae could be far from
the surface-film when the larval swimbladder is ready to be filled with gas.

However, McEwan (1940) found that, in Hemichromis, the connection between the larval swim-
bladder and the gut never developed a lumen and, to make sure of the implications of this discovery,
the early larvae were denied experimentally all access to the surface. In spite of this the larval swim-
bladder became filled with gas. McEwen found that at one stage the lumen was obliterated by the
swelling of highly vacuolated cells forming the inner epithelium. Having expanded to the limit, these
cells suddenly collapsed to form a flat epithelium, after which gas appeared in the cavity. If such
a mechanism is found in deep-sea fishes, it is obvious that the larvae need not seek the surface-
film in order to initiate the use of the swimbladder as a hydrostatic organ.

At least five species of Cyclothone (braueri, signata, microdon, pygmaea, and acclinidens) must have
a gas-filled swimbladder during their larval life, but after metamorphosis the organ regresses and
becomes invested with fatty tissue. Presumably this is also true for other deep-water fishes with
a fat-invested swimbladder in the adult phase. All such species will best be considered in a
separate section (pp. 65-68). In the Miripinnati (Bertelsen and Marshall, 1956) and Stylophorus,
the larval swimbladder also undergoes regression, but does not serve as an attachment for fat in
the adult.

Lastly, all available evidence shows that bathypelagic fishes, without any trace of a swimbladder
when adult, are also without a definite larval organ. (I have examined larval paralepidids, scopel-
archids, and melanostomiatids without finding a swimbladder.) Furthermore, Bertelsen (1951)
remarked that larval ceratioids, like the adults, have no swimbladder, but he suggested that 'gela-
tinous tissue under the skin, which is present in all Ceratioid larvae in more or less well-developed
condition, could be regarded as a floating organ '. More recently, Shelbourne (1956) has seen a corre-
lation between the pelagic habit in fish eggs and larvae and the development of large subdermal
spaces in the young stages. As these spaces seem to be filled with low density fluids derived from the
yolk, they act as buoyancy chambers. It is clear from Shelbourne's figures that voluminous subdermal
spaces are developed regardless of the presence or absence of a swimbladder in the larval phase.
This is also true of bathypelagic fishes. Larval myctophids belonging to species with a well-formed
adult swimbladder (e.g. Benthosema glaciale, Hygophum benoiti, Myctophum punctatum) have large
subdermal spaces, particularly in the head region (see Taning's (191 8) figures). Regarding fishes
without a swimbladder, we have already referred to Bertelsen's findings in the ceratioids. It would

8-2

WOODS

HOLE,

MASS.

60 DISCOVERY REPORTS

seem that the larval swimbladder is not sufficient to bring the specific gravity of the larva to that of the

environment. 'Buoyancy tanks' are required as well.1

The swimbladder wall
Excluding the peritoneal investment, there are four main layers of tissue in the swimbladder wall :
an outer, closely-knit fibrous layer; a middle, loosely- woven, fibrous tissue layer; a layer of smooth
muscle fibres, and an inner epithelial layer. The outer layer is usually known as the tunica externa,
while Fange (1953) called the middle layer the submucosa, for in structure and position it is very like
the layer of the vertebrate gut that already has this name. As Fange (1953) has said, '. . .from an
embryological and comparative anatomical point of view the teleostean swimbladder is nothing else
than an isolated part of the digestive tube, although adapted to special functions '. The inner layer
consists of pavement epithelium, which is locallyjiifferentiated to form the gas-gland.

The swimbladder lies outside the coelom, between the gut and the kidneys. It is retroperitoneal in
position, but it becomes invested in varying degrees with peritoneal tissue. While the dorsal edge
of the peritoneum usually runs along the lateral walls of the swimbladder, in some teleosts this limit
lies above the organ (Freunde, 1938). Between the peritoneum and tunica externa, there may be
a padding of loose, reticular, connective-tissue cells. Strands of connective tissue also run between
the roof of the sac and the outer coat of the kidneys, which lies close to the swimbladder wall.

The peritoneal coat and the tunica externa are mainly formed of closely packed collagen fibres.
The submucosa is by far the most voluminous coating of the swimbladder wall and it usually consists
of a reticulum of loosely packed, collagen fibres within a gelatinous ground-substance (Saupe, 1939;
Fange, 1953). This layer is particularly thick under the gas-producing structures of the swimbladder.
Between the submucosa and the inner epithelium there is a layer of smooth muscle cells which I have
been able to identify in a number of the fishes considered in this report.

From this general outline we may turn to closer consideration of the swimbladder wall in certain
deep-sea teleosts.

Family Sternoptychidae, Sternoptyx diaphana

The fine structure of the swimbladder wall of this hatchet fish has been described by Nusbaum-
Hilarowicz (1920), who divided the layers of tissue into three sections: outer, middle and inner. The
outer section consists of two layers of long connective tissue fibres, the fibrillar axes of the topcoat
being at right angles to those of the undercoat. From his plate VIII, fig. 9 it is evident that the
fibres of the undercoat describe circular paths about the long axis of the sac. The middle section is
a loosely-woven reticulum of fibres, which are delicately fashioned and form most of the wall-
thickness. The cavities between the fibres hold a homogeneous and transparent substance, which is
not stained by such dyes as haematoxylin or eosin. Nusbaum-Hilarowicz suggested that in the living
animal this substance is probably a serous fluid. Undoubtedly this layer corresponds to what Fange
(1953) called the submucosa, and he remarked that, '. . .the submucosa often has a jelly-like, half-
fluid consistency '. As is usual, the inner layer consists of flattened epithelial cells which are locally
differentiated to form the gas-gland.

Argyropelecus

The histology of the swimbladder wall of Argyropelecus hemigymnus was also described by Nusbaum-
Hilarowicz. There is an outer layer, presumably the tunica externa, consisting of long fibres with
elongated nuclei, which for the most part are set across the long axis of the sac. Underlying this

1 It would be interesting to know whether pelagic fish larvae with a swimbladder have relatively smaller subdermal spaces
than those without this organ.

STRUCTURE AND SYSTEMATICS 61

circular layer is a thick layer (the submucosa) of fibres forming a loosely-woven reticulum. As in
Stemoptyx, this fibre complex would appear to be developed within a gelatinous matrix. Last comes
the inner, filmy coat of pavement epithelium.

Longitudinal sections were prepared of the specimen of Argyropelecus olfersii described on p. 20.
The tissue composition of the walls is much like that of A. hemigymnus. Above the gas-gland, the
roof has a thickness of 50-100//, most of this consisting of the submucosa. The floor of the sac under
the gas-gland is about three times as thick as the roof, but this swimbladder was in a very relaxed
state. When the swimbladder is taut and in the steady state, the walls must be a good deal thinner,
even remembering that the above measurements have been taken from tissues shrunken by pre-
servation and subsequent preparation.

Family Gonostomatidae, Vinciguerria attenuata

The swimbladder taken for sectioning came from a fish of standard length 32-5 mm. The sac was well
expanded, the major and minor axes measuring 7-5 and 2-5 mm. The gas-gland was flattened and
well displayed, appearing much like that of the fish described on pp. 7-9.

Over the roof of the rear part of the swimbladder the walls measured about 20// in thickness.
There is a thin tunica externa formed of fibres running round the sac; then comes the reticulate
submucosa which takes up most of the wall thickness. Near the rete mirabile the walls are padded
• with a voluminous submucosa measuring about 250// in thickness. The swimbladder is lined with
a filmy pavement epithelium.

Vinciguerri nimbaria

The swimbladder described on p. 9 was used in the preparation of serial transverse sections. It is of
particular interest in that the sac was much contracted, but not collapsed, while the gas-gland formed
a thick bunched-up mass.

The swimbladder is completely invested by a layer of peritoneum bearing many melanophores
and formed of close-set fibres. The thin tunica externa is made up of circular fibres, while the very
thick submucosa varies from 50 to ioo/< in width. Owing to the relaxation of the sac, the fibres of the
submucosa have been thrown into a series of undulations (see also p. 65).

Cyclothone

During the larval phase, the species of Cyclothone have a gas-filled swimbladder, which regresses and
becomes invested with fat after metamorphosis to the adult. The development of the latter condition is
dealt with in another section (pp. 65-68). Here we deal with the wall structure of the larval swimbladder.

The species of Cyclothone studied by Nusbaum-Hilarowicz (1920) was probably braueri and not
signata (see p. 18). It is evident from his plate VIII that the swimbladder was in the larval condition,
although fig. 3 shows a trace of the regular reticulate tissue (which holds the fat) at one end of the sac.

He found a thin but tough outer layer (tunica externa), consisting of long fibres that encircle the
sac followed by another thin layer of rounded and branching cells. The next and median layer (sub-
mucosa) was very voluminous at the front and rear sections, but quite thin in the middle region. This
was formed of fibrillar and loosely compacted tissue. The inner epithelial layer formed the gas-gland
at the front of the sac.

Transverse sections through the swimbladder of a Cyclothone braueri of standard length 26-5 mm.
revealed much the same tissue structure. The swimbladder has a length of about 3 mm. and around
the gas-gland the walls have a thickness of from 100 to 200//.

A 10-mm. larval stage of C. pygmaea from Thor station 144 was also sectioned. There is little that
need be added, except to mention that the sac is completely invested with a densely pigmented

62 DISCOVERY REPORTS

peritoneal coat. This is formed of strong close-set fibres that tend to run along the major axis of

the swimbladder.

Astronesthes niger

The swimbladder described on p. 23 was examined under a high-power binocular, the tissue layers
of the walls being teased apart. The sac is completely enveloped by the peritoneal coat, which is
constructed of close-set fibres that are set along the major axis. The underlying tunica externa is
formed of circularly disposed fibres. Next follows the thick submucosa with its loose network of
fibres that run in all directions.

Family Myctophidae, Myctophum punctatum

A swimbladder measuring about 12 mm. in length and 5 mm. in depth was sectioned.

The peritoneum extends round the floor and lateral walls of the sac. It is formed of lamellar
collagen fibres (about 5-10// in width) which run along the major axis of the sac. This layer carries
melanophores. The underlying tunica externa is barely detectable, but is comprised of fibres that run
round the swimbladder. As is usual, the submucosa forms most of the wall thickness, this being
about 300/* under the gas-gland and about 50// in the roof of the sac. Remains of the ground substance
could be seen adhering to the loose fibrillar network. Here and there the cells of the ground substance
could be detected. Finally, there is a filmy coat of pavement epithelium lining the inner surface
of the sac.

Diaphus rafinesquei

Certain details of the structure of the swimbladder wall have been described by Rauther (1922). As
in Myctophum punctatum, the fibrous peritoneum (' fibrose hiille ') does not completely invest the sac
but extends rather more than half way up the lateral walls. Between the peritoneum and what
Rauther drew as a thick circular layer of fibres is a padding of loose, reticular connective tissue. The
circular layer must represent the tunica externa and the submucosa. Microscopic examination of the
swimbladder of the fish from Discovery station 3484 (see pp. 30-32) revealed other structural details.

At least at the forepart of the organ, the peritoneal coat extends over the roof of the sac. It is
formed of fine and close-set collagen fibres together with a number of elastic fibres. The tunica
externa consists of relatively strong fibres running round the sac, while the more delicate fibres of the
submucosa form a loose network. As far as could be judged the lateral walls are about 50^ in thick-
ness, the submucosa accounting for about nine-tenths of this dimension.

To summarize, the wall of the swimbladder usually has this structure : a voluminous loosely- woven
reticulum of collagen fibres in a gelatinous ground-substance separates the thin, but tough outer
fibrous layer from the inner, filmy epithelium lining the sac walls. Clearly this tissue-complex must
have adequate mechanical, as well as gas-proofing qualities.

In the steady state any loss of gas by diffusion out of the sac can be countered by the activity of the
gas-gland. Presumably the walls will be under tension without undue strain. It would also seem
likely that the fibres of the submucosa will lie close together within the gelatinous matrix, so forming
a densely matted tissue, not the loose reticulum seen in prepared sections.

Concerning the gas-proofing qualities, a fish living at a depth of 500 m. will most probably have
80 per cent of oxygen in its swimbladder gases, so the swimbladder wall must contain a pressure of
40 atmospheres of oxygen against the tensions of this gas in the body fluids. (About 0-2 atmosphere
for arterial blood.) Evidently, the swimbladder wall must be remarkably impermeable to oxygen.

structure and systematics 63

Mechanical properties of the swimbladder wall
Apart from Alexander's (1959a, b, c) studies of the swimbladder wall of cyprinid and other fishes,
little is known of the physical properties of this tissue-complex. In cyprinids the posterior chamber
of the swimbladder is remarkably inextensible, a property that is related to the high collagen content
of the walls: the anterior chamber is more extensible (Alexander, 19596). The swimbladders of pike
and trout are much more extensible and much weaker than cyprinoid swimbladders (Alexander,
1959^). Judged by their fine structure, this is also true of the swimbladders of bathypelagic fishes in
comparison with those of cyprinids.

Some preliminary notion of the physical properties of the swimbladder wall can be deduced from
the observations of Scholander, Claff, Teng and Walters (1951) and Jones (1952). These workers
considered how far a closed swimbladder might restrict rapid vertical movement in a fish above a
certain level — the level at which it was in hydrostatic equilibrium. Scholander and his colleagues
suggested that a fish would not move upwards beyond a level involving more than a 25 per cent
change in the volume of its swimbladder, which is in good agreement with Jones's figure of 22 per cent.

An increase of 25 per cent in the volume of a swimbladder will not lead to more than a moderate
extension of the walls. As this figure may well apply to deep-water pelagic fishes, we may briefly
consider what would happen to the ellipsoidal swimbladder of a myctophid. (A fish with a standard
length of 70 mm. will have a swimbladder with a volume of about 0-25 ml.) An increase of 25 per
cent in the volume will be accompanied by rather less than 10 per cent increase in the lengths of the
major and minor axes, assuming the walls are uniformly elastic and the sac is free to expand.

There is a further consideration : when fully expanded, the oval is by far the thinnest part of the
swimbladder of a myctophid, and during the hauling of a fish to the surface, the oval may be blown
out in the form of a blister. (This condition was found in several specimens of Myctophum pimctatum
and Diaphus rafinesquei (see Text-fig. 15^/). Taking an oval with the walls distorted in the form of a
hemisphere, the surface area will be increased by a factor of two. If this amount of expansion can
be sustained by the flimsiest part of the swimbladder, it is unlikely that the limitation of rapid upward
movements is set by the range of extensibility of the walls. (In Argyropelecus also it is clear that the
swimbladder can sustain more than a 10 per cent increase in the lengths of the major and minor axes.)
The restriction is more likely to be related to the fishes' incapacity to cope with more than a certain
decrease in its density, there being a limit to what can be done by compensatory movements of the
fins and body.

Whatever may be the limits of extensibility, it is rare to find a bathypelagic fish with a burst swim-
bladder or ruptured body-wall. While it may be easy to miss a small hole in the swimbladder of
a preserved fish, distension of the organ (so that the viscera are forced out of the mouth or anus) is
also unusual, except perhaps in hatchet fishes (see also p. 95).

In a letter Dr F. R. Harden Jones has told me that perch (Perca fluviatilis) with burst swimbladders
do not appear to have ruptured body-walls, although in some instances the pressure may be sufficient
to evert the rectum. Out of a sample of 106 cod taken by trawl at 20 fathoms, he found 45 per cent
with broken swimbladders. At greater depths (30 fathoms and above), all were broken. But there is
no evidence that the swimbladder walls of vertically migrating deep-sea fishes are any tougher in
relation to the size of the sac than those of perch or cod. Saupe (1939) gives 250-300// as the thickness
of the walls in the perch, but makes no mention of the size of the fish. This may be compared with
the measurements (20-300//) given earlier in this section, for various species of stomiatoids and
myctophids. Furthermore, there is no indication that the collagenous elements in the swimbladder
wall of bathypelagic fishes are more closely packed than those of shallow water species.

64 DISCOVERY REPORTS

Perhaps these differences between perch, cod and bathypelagic teleosts have a functional rather
than a mechanical basis. A cod being hauled to the surface in a trawl is subjected to pressure changes
beyond those it normally experiences. This would not apply to those bathypelagic fishes which
migrate upward each day to the surface-waters. However, discussion of this will best be left to the
section dealing with gas resorption (pp. 78-81).

Text-fig. 32. Semidiagrammatic reconstructions of the swimbladder of Vinciguerria in (a) an expanded, and (b) a com-
pressed state. Note the changes in shape of the gas-gland cells (shown black) and the retia mirabilia (rm). The undulating
patterns in the submucosa of the compressed swimbladder may be better seen in the microphotograph in PI. I, fig. 1. Below
are shown cross-sections of the capillaries of the retia (vc, venous capillaries, others arterial). In those belonging to (a) both
sets of capillaries are expanded, as during gas secretion: in (b) the arterial capillaries are occluded, as during gas resorption.

During the migration of a fish towards the surface, the physical properties of the swimbladder wall
must be adequate to withstand any stresses that might arise. But the walls will presumably be under
tension without undue strain. It would also seem likely, as we have said, that the fibres of the sub-
mucosa will lie close together within their gelatinous matrix. When the fish dives to its daytime level,
certain evidence suggests that the swimbladder cannot be kept at the required volume in the face of
pressure gradient (p. 91). As the swimbladder is compressed the volume of the fish will decrease and
it would seem desirable that the tissues of the walls should be freely adjustable as the sac decreases
in size. If, for instance, the connective tissues were ' rigid ', with little play, kinks would appear in the
wall which might eventually lead to one part of the delicate gas-gland being forced against another
(see Text-fig. 32). However, the presence of a voluminous, semi-fluid submucosa will allow the
tissues to relax in a uniform manner and so the swimbladder may keep its shape. In a large Diaphus
rafinesquei, the swimbladder submucosa is about 150// in thickness, and in a sac with major and
minor axes of 12-0 and 7-0 mm., the volume of this tissue will be rather more than one-tenth of that
of the gas.

STRUCTURE AND SYSTEMATICS 65

If the sac is compressed to half its buoyant capacity, the volumes of the gaseous and gelatinous
phases will differ by no more than a factor of five. This assumes that the volume of the submucosa
is unchanged. But according to Le Chatelier's theorem, colloidal gels may be expected to take up
more water if subjected to an increase in pressure (Johnson, Eyring and Polissar, 1954). At all events,
a study of this aspect would be of interest.

Some indication of the flow-patterns in the submucosa of a compressed swimbladder was found in Vin-
ciguerria. Sections were cut through two swimbladders, one of which was well expanded, the other com-
pletely relaxed. These are shown in Text-fig. 32 and PI. I, fig. 1 . The lines of flow are indicated by the
undulations of the fibres in the submucosa. The great change in the shape of the gas-gland cells can
also be seen. While looking at these sections I was reminded of the experiments described by Le Gros
Clark (1945). An inflated rubber balloon, the surface of which was lightly oiled, was coated with a
plastic material, such as gelatin or collodion. As the balloon was deflated, small elevations appeared on
the surface of the plastic, each of which sent out a triradiate pattern of anticlines as the contraction pro-
ceeded. Such elevations were found in the submucosa of the relaxed swimbladder (see PI. I, fig. 1) and
under each were arches of fibres, looking not unlike the strata forming an anticline in the earth's crust.

Turning finally to the gas-proofing properties of the swimbladder wall, Fange (1953) has clearly
shown that it is the ' secretory mucosa ' which is impermeable to gases. The secretory mucosa is the
inner epithelium of the secretory part of the sac. During gas-production this tissue is in a relaxed
state and covers the inner surface of the bladder (the resorbent part being contracted). It is hardly
surprising that this should be so, for the other parts of the swimbladder carry many blood-vessels
through which gases would be lost.

Evidently the inner epithelium is the 'inner tube', the connective-tissues being merely the 'tyre'.

Fat-invested swimbladders
The presence of a fat-invested swimbladder in a deep-sea fish was first discovered by Ray (1950). In
her study of the peripheral nervous system of the myctophid Lampanyctus leucopsaras, she figures
(pi. 12, fig. 30) a transverse section through the trunk at the level of the swimbladder. Like a normal
gas-filled organ, it lies immediately below the kidneys and is surrounded by peritoneum, which is
darkly pigmented, as is usual in deep-sea fishes. The organ is filled with reticular connective tissue
having all the appearance of a system of fat-storing cells. Barham (1957) has given these further
details: 'In the adult state the bladder is largely filled by fatty connective tissue. A well developed
gas-gland is present and almost fills the reduced lumen, but in some specimens a gas bubble may
be present.' He also records that another myctophid, Diaphus theta, has a similar type of swimbladder.
As already stated in the descriptive section, fat-invested swimbladders are found in a number of
bathypelagic fishes. These are:

Suborder Stomiatoidea: Family Gonostomatidae, Cyclothone spp., Gonostoma elongation; Family
Sternoptychidae, Polyipnus laternatus; Family Astronesthidae, Borostomias antarcticus; Family
Stomiatidae, Stomias colubrinus, S. affinis. Order Berycomorphi: Family Anoplogastridae, Anoplo-
gaster longidens.

Kotthaus (1952) has also found a well-formed fat-bearing swimbladder in another deep-sea beryco-
.morph, Hoplostethus islandicus (family Hoplostethidae).

It will thus be seen that fat-invested swimbladders are found in deep-water fishes belonging to
seven different families and three orders.

As already mentioned, the post-larval stages of Cyclothone have a small gas-filled swimbladder. It
is after metamorphosis that the swimbladder regresses and becomes invested with adipose tissue. In

66 DISCOVERY REPORTS

Cyclothone braueri metamorphosis occurs at a length of from n to 14 mm. (Jespersen and Taning,
1926), but two individuals of lengths 17 and 26-5 mm. (St. 3094, i50o(-o) m., 21. v. 54) still had no
deposit of fat around the swimbladder. However, in another fish of length 26 mm. there was a small
cushion of adipose tissue at the anterior end of the sac. In a 31 -mm. fish the larval swimbladder had
lost its ellipsoidal shape and appeared as a glistening white sphere (with a diameter of 0-6 mm.) in
the middle of a blimp-shaped mass of fat, having a length of about 3 mm.

rsb ft

C D

Text-fig. 33. Diagrammatic reconstructions of four stages (a-d) in the fatty investment of a regressing larval swimbladder
in Cyclothone livida. The gas-gland is shown black, ft, fatty investment of swimbladder; lu, lumen of swimbladder;/)/), pig-
mented peritoneum ; rsb, regressed swimbladder ; sbw, swimbladder wall.

Above and below the vertical diameter of the sphere, there was only a thin covering of fat. Finally,
in a 56-mm. individual the remnants of the larval swimbladder measured no more than 0-15 mm. in
diameter and needed to be carefully looked for in its fatty investment. It would thus appear that the
swimbladder is fully adipose in adults of about 35 mm. and upwards.

In Cyclothone livida (also from St. 3094) the sequence of changes is much the same and is sum-
marized in Text-fig. 33. As in C. braueri, the larval swimbladder was completely regressed and
surrounded by a sausage-shaped mass of fat when the fish had reached a length of about 37 mm.

This most advanced stage in the development was examined microscopically. In Text-fig. 34 is
a drawing of a transverse section at the level of the regressed swimbladder (see also PI. I, fig. 2). The
left-hand figure shows the reticular system of fat-storing cells surrounding the central regressed part
of the larval swimbladder. This part is shown enlarged on the right. An outer fibrous layer encloses
a mass of regressed gas-gland cells, mostly without nuclei, and the remnants of the retial capillaries.
The remaining space is filled up with fine loosely-woven reticular tissue, which is undoubtedly the
remains of the submucosa. The tunica externa must be represented by the outer fibrous layer, which
has much the appearance of the outer circular layer fibres described by Nusbaum-Hilarowicz (1920).
The mass of fat-charged cells is almost entirely bounded by the darkly pigmented peritoneum with
its fine mosaic of melanophores. Thus the fat is deposited between the peritoneum and the tunica
externa and in this way comes to invest the larval swimbladder as it regresses.

STRUCTURE AND SYSTEMATICS 67

Varying degrees of adipose tissue investment have been found around the swimbladders of adults
of the hatchet fish, Polyipnus laternatus. This is shown in Text-fig. 35.

The top drawing represents a swimbladder from a 32-5-mm. fish and the sac has a relatively thin
layer of fat around it. The middle and lower swimbladders came from 26-5 and 33-5-mm. fishes. In
these the swimbladder is buried in a mass of fat, the outline of which has some congruence to that of
the sac. As in Cyclothone, the fat was surrounded by darkly pigmented peritoneum.

Text-fig. 34. Cross-sections through the fat-invested swimbladder of Cyclothone livida. On the left is shown the reticular
fat-charged tissue surrounding the regressed swimbladder, which is shown enlarged on the right and has a diameter of about
300//. crm, remains of capillaries of rete mirabile ; pp, pigmented peritoneum; rft, reticular fatty-tissue; rsb, regressed swim-
bladder ; rgg, regressed gas-gland cells ; sm, submucosa ; te, tunica externa.

Text-fig. 35. Different degrees of fat-investment of the swimbladder of Polyipnus laternatus. The top swimbladder ( x 7-5),
showing the least degree of investment, is from a fish of standard length 32-5 mm. The middle one ( x 8) comes from a
26-5-mm. fish, while the bottom one ( x 6) is from a 33-5-1™™. specimen, ft, fatty investment of swimbladder ; gg, gas-gland;
pp, pigmented peritoneum; rm, rete mirabile; sbw, swimbladder wall.

9-2

68 DISCOVERY REPORTS

Compared with the swimbladder of the 32-5-mm. fish, those of the other two fishes are consider-
ably regressed, although the main features can be clearly distinguished. It is probably significant that
the dimensions of the fat body surrounding the swimbladder of the 33-5-0101. fish are much the
same as those of the swimbladder of the 32-5-011x1. individual. It would seem that as the swimbladder
regresses, the space left between the peritoneum and tunica externa is filled with fat. But the marked
difference between the swimbladders of these two equal-sized fishes suggests there must be wide
variability in the stage at which this regression begins to occur.

A hydrostatic organ consisting entirely of fat is superior to one containing gas in that fats are
relatively incompressible. However, fats are not much lighter than sea water, having a density of
about 0-9. In a marine fish the volume of gas-filled swimbladder need only be 5 per cent of the body
volume to make the fish weightless in water (Jones and Marshall, 1953). But a marine fish without
such an internal float requires about 30 per cent of fat by weight for neutral buoyancy. Clearly the
replacement of gas by fat is an inadequate substitution, so far as buoyancy is concerned. In Gono-
stoma elongatum, Denton and Marshall (1958) found relatively little fat, the more significant fact being
that this species almost achieves neutral buoyancy by having reduced muscular and skeletal systems.
But in Cyclothone, as will be shown later (p. 103), there is, in addition to the fat investing the swim-
bladder and deposited in the mesenteries, a well-developed system of fat sinuses under the skin. In
a well-fed Cyclothone these stores of fat may occupy up to 15 per cent of the body volume (about
13 per cent of the body-weight assuming the fish to be neutrally buoyant). Again, the more significant
feature, particularly in a poorly nourished fish, is the reduction of the heavy muscular and skeletal
tissues.

The following conclusion seems apt: In a number of bathypelagic fishes the swimbladder regresses
after metamorphosis and becomes a convenient site for the deposition of fat, but this plays a relatively
small part on the ' credit ' side of the ' buoyancy balance sheet '.

THE SWIMBLADDER AS A HYDROSTATIC ORGAN
The teleost swimbladder acts as a hydrostatic organ by making the fish weightless in water. Whatever
movements the fish may make, whether up or down, the nervous control of the swimbladder is such
that it continues to function towards this 'desirable' end. In terms of cybernetics, the 'feed-back'
is arranged to steer this system towards this ' goal ', the weightless condition. In other terms, here is
what the fishes told the diver in one of Isak Dinesen's (1958) 'simple' stories: 'We fish rest quietly,
to all sides supported, within an element which all the time accurately and unfailingly evens itself out.
An element which may be said to have taken over our personal existence, in as much as, regardless of
individual shape and of whether we be flatfish or roundfish, our weight and body is calculated
according to that quantity of our surroundings which we displace.'

Knowing the density of the tissues (about 1-076), it can be shown that the volume of the swim-
bladder in a marine teleost must be about 5 per cent of the body- volume if the fish is to be in hydro-
static equilibrium with the sea (Taylor, 1921). Measurements of this percentage volume in shallow
water species closely agree with this theoretical figure (Jones and Marshall, 1953). Furthermore,
Kanwisher and Ebeling (1957) have found a similar agreement in bathypelagic teleosts, their measure-
ments of the swimbladder volume in various stomiatoids, myctophids and melamphaids ranging from
3-2 to 6-5 per cent of the body-volume. If deprived of their swimbladders, these deep-water fishes
would need to sustain a downward force equivalent to 3-2-6-5 per cent of their weight in air in order
to maintain themselves at a constant depth. Calculations made by Denton and Shaw show that the
energy 'saved' can be quite appreciable (Denton and Marshall, 1958). Yet some energy is required
to keep the swimbladder inflated at the appropriate volume and the amount is directly related to the

THE SWIMBLADDER AS A HYDROSTATIC ORGAN 69

depth (Parr, 1937; Kanwisher and Ebeling, 1957), but in absolute terms this amount may be quite
small (see p. 84). However, many of the bathypelagic fishes with swimbladders undertake daily
vertical migrations. These will be considered in a later section (pp. 85-95). Here the main concern is
with the structures involved in maintaining the swimbladder as a hydrostatic organ. These are the
gas-secreting complex (rete mirabile and gas-gland) and those allowing of the loss of gases from the
swimbladder (the resorbent capillary complex).

The gas-producing complex
The swimbladder produces gas by means of a capillary system supplying a glandular area. The gland is
formed by localized modification of the epithelial cells that line the sac.

In physoclists and some physostomes (e.g. cyprinids, pike and eels) the capillaries form retia
mirabilia. These consist of regular and intimate intercalations of arterial and venous capillaries, which
follow parallel courses and carry blood to and from the gas-gland.1

The retia mirabilia
Some account of the form and size of the retial system has already been given in the descriptive part
of this report (pp. 7-50). In this section the emphasis will be on the fine structure.

Woodland (19110, b) was the first to appreciate the essential features of retia mirabilia. He
divided them into two types, unipolar and bipolar. In both kinds, an artery and vein subdivide to
form the close and regular association of capillaries, (which may number many thousands), that supply
the gas-gland. Before entering the gland, the retial capillaries of the bipolar type recombine to
form arteries and veins, these then breaking up within the gland to form the capillary circulation.
In the unipolar type the retial capillaries merely continue into the gland.

Both kinds of retia are found in the swimbladders of deep-sea fishes. All stomiatoids have a single,
bipolar rete mirabile : the myctophids have three unipolar retia. Now some species of both groups
live under similar hydrostatic pressures and undertake daily vertical migrations, and on this account,
there would appear to be ' nothing to choose ' between the efficiency of both types of system.

Apart from this consideration, it is interesting that the two most diverse groups of pelagic, deep-sea
fishes, the stomiatoids and myctophids, differ in this particular way. However, it will be as well to
remember Pantin's (1951) observation: that given certain standard parts, the number of structural
solutions to a physiological requirement is limited by the nature and number of these parts. In this
instance, given an artery and a vein that form a retial system, there would appear to be only two ways
this system could feed a gas gland. The retial capillaries can either continue into the gas-gland (uni-
polar retia) or combine to form larger vessels (bipolar retia) before doing so.

The nature of the swimbladder as a whole must also be considered. Woodland (191 1 a) and Fange
(1953) have shown that the retia mirabilia of teleosts with a euphysoclistous swimbladder are unipolar
in type. This survey has provided further evidence for this generalization. Besides the Myctophidae,
the other bathypelagic euphysoclists are the Miripinnati, Anoplogastroidea, Stvlophorus and Chias-
modon. All these fishes have unipolar retia. At least some of the deep-sea salmonoids are euphyso-
clists and their micro-retia run straight to the gas-gland. This is hardly surprising.

Apart from the stomiatoids, the only other fishes known to have bipolar retia are the eels (Apodes).
The development of a bipolar retia system in the first group would appear to be linked to the venous
part of the resorbent area, which drains into vessels that also supply the gas-gland. Such a circulation
would hardly be feasible with the unipolar type of rete (see also p. 78). However, in both euphyso-
clists and eels, the secretory and resorbent parts have their own circulatory systems (Fange, 1953).

1 In view of this association in parallel, the noun rete is quite inappropriate, but the adjective is justified, for these capillary
systems are wonderful instances of biological engineering in miniature. A better name would be fastis mirabilis.

7o DISCOVERY REPORTS

This being so, euphysoclists simply require unipolar retia, but the eels are an exception to this
' rule '. It should also be stressed that a bipolar retial system is not a characteristic of all paraphyso-
clists. Unlike the stomiatoids, other teleosts with this type of swimbladder (Synentognathi and
Microcyprini) have unipolar retia.

Turning now to the composition of the retia, Krogh (1922) was the first to appreciate the extra-
ordinary extent of the capillary elements. In a cross-section of the two retia of the freshwater eel he
estimated that there were 88,000 venous and 116,000 arterial capillaries. As the two retia were
4 mm. in length this gave aggregate lengths of 352 and 464 m. for the two sets of capillaries. Krogh
also pointed out that the capillary elements are remarkably long compared to those in muscles, which
are otherwise among the longest in the vertebrate body (e.g. 4 mm. in eel retia against 0-5 mm.
in muscle).

Similar data are given in Table 3 for various species of bathypelagic fishes (see PI. I, figs. 3 and 4 for
the appearance of a rete in cross-section). The significance of the rjv ratio will become apparent in the
text which follows.

Table 3. Retial length : swimbladder volume ratios

Total

Number

Retial

length of

rjv = retial

of retial

length

capillaries

length : volume

Species

capillaries

{mm.)

(»>■)

(ml.) of sac

Eel (Anguilla anguilla)

204,000

4-0

816-0

3°

Argyropelecus aculeatus

5,000

2-0

io-o

5°

Polyipnus laternatus

7,000

3-0

21-0

100

Vinciguerria mnibana

5,000

i-o

5-o

150

Myctophum punctatum

2,000

2-5

5-o

Melamphaes megalops

500

12-0

6-o

3°

At first sight the figures for the total lengths of the retial capillaries seem iow compared with
Krogh 's 816 m. for the freshwater eel. But as the retia are an essential part of the gas-producing
mechanism, their numerical constitution will be best regarded in relation to the volume of the swim-
bladder. (The volume of the eel swimbladder was estimated from Fange's (1953) fig. 17, assuming
the secretory sac to be a perfect ellipsoid.) In view of this, an rjv ratio was calculated (r being the
total length of the retial capillaries, and v the volume of the swimbladder (ml.)).

While these figures can only be rough approximations, it will be seen that, except for Polyipnus and
Vinciguerria, the rjv ratio of the eel is much the same as those of the bathypelagic species. And in
comparing these data, it should be remembered that during its reproductive migration the freshwater
eel becomes a deep-sea fish. The agreement between the ratios is thus not altogether surprising. But
before considering this problem further, reference must be made to Scholander's (1954, 1958)
theoretical study of the rete mirabile of deep-sea fishes.

Following earlier suggestions, Scholander convincingly argued that the retia must form a counter-
current system allowing of gaseous exchange between the arterial and venous capillaries. Without
intimate contact between the two sets of vessels, the blood leaving the gas-gland would be continually
removing oxygen from the swimbladder. He wrote as follows in his 1958 paper (page 7):

The atmospheric oxygen which is dissolved in the sea water has a gas pressure of no more than one-fifth
of an atmosphere at any depth, and the arterial pressure in the fish is slightly below this. So across the
thin swimbladder wall of a fish living at a depth of 2000 m. there is a drop in oxygen pressure of nearly
200 atmospheres. The swimbladder is a living organ and is circulated with blood. At a pressure of 200
atmospheres the blood becomes charged with ten times its own volume of oxygen by simple physical
solution, and if such amounts were to leave the swimbladder there would soon be no oxygen left. In more

THE SWIMBLADDER AS A HYDROSTATIC ORGAN 71

general terms, one may state the problem thus: How can a steep concentration gradient be maintained
across a barrier in spite of the fact that liquid is continuously streaming through it? The answer lies in the
arrangement of the vascular channels.

Clearly, the retia will be most efficient in gaseous exchange if the capillary elements fit together so
as to obtain the greatest possible surface of contact. Scholander (1954, 1958) had some interesting
observations on this aspect. Transverse sections through the retia of a deep-sea eel (Synaphobranchus),
a rose-fish (Sebastes) and a rat-tail (Coryphaenoides) showed that the arterial and venous capillaries
fit together to form either a chequer-board1 or a hexagonal star pattern. The eel has the first arrange-
ment, one giving the maximum gaseous diffusion between the afferent and efferent capillaries, and
Scholander (1954) went on to say '. . .it is remarkable that we find it in our deepest fish. The only
other solution to the topological problem of making four polygons (black or white) meet at one point
in such a way that black always borders white is realized in the hexagonal star pattern found in the
rete of the rosefish ' (and in that of the rat-tail).

While looking through serial transverse sections of the swimbladder of various stomiatoids,
Argyropelecus aculeatus, Vinciguerria nimbaria and Polyipnus, I found both types of pattern in the
same rete. In Polyipnus, for instance, there is a transition from the hexagonal to the mosaic arrange-
ment in passing from the proximal to the distal end of the rete (see PL I, fig. 4). At the beginning
of the rete the arterial capillaries are occluded and form an hexagonal pattern round the larger
(6-8//) venous capillaries. About half-way down the rete, the arrangement is much the same, except
that the arterial capillaries are partly open. Lastly, over the distal third of the rete, the two sets of
capillaries form a mosaic pattern and are equal in size (6-7/1). In the specimen of Argyropelecus
aculeatus, except for a middle area at the proximal end, the rete showed a hexagonal star pattern
throughout.

In a specimen of Vinciguerria attenuata, however, the rete of which was well expanded, the
capillaries formed a mosaic pattern at all levels (see Text-fig. 32a). The seemingly curious mixture
found in other stomiatoid retia is likely to be no more than a reflection of the unique arrangement
whereby venous blood from the resorbent capillary bed returns through the rete (p. 79). During the
secretory phase the rete will be fully expanded and both sets of capillaries will then form a mosaic
pattern. When gases are being lost from the swimbladder the arterial capillaries must be closed, while
the venous elements will be fully expanded. In this way a hexagonal pattern would be formed. The
mixture of patterns found in some retia would thus be due to the physiological state of the fish when
it died in the net. Preservation and fixation might also play some part, but evidently not in the rete of
Vinciguerria attenuata mentioned above.

In the Myctophidae, the vascular system of the oval does not involve the retia, other than that the
arterial blood may come from a branch of the retial artery. In two species, Myctophum punctatum
and Diaphus dofleini, transverse sections through the retia showed the capillaries to be rounded rather
than polygonal, the appearance being more like a system of condenser tubes than a mosaic. In the
living fish, their shape may be otherwise.

Apart from the intimacy of their association, the total surface of contact between the capillaries
will obviously be directly proportional to their length. And an increase in length will not only lead to
increased exchange of gases, but also slow down the rate of blood-flow and so further enhance the
efficiency of the exchange. But before considering this aspect in bathypelagic fishes, some mention
must be made of Scholander's (1954, 1958) concept of the rete as a device for the building up of
high pressures.

Assuming that gases are liberated from the blood, Scholander derived an equation, showing that

1 'Mosaic' would be a more apt descriptive term.

72 DISCOVERY REPORTS

the equilibrium pressure is directly proportional to the diffusion across the retial capillaries and the
amount of oxygen dissociated from a unit volume of blood. The inverse terms in the equation are the
blood solubility coefficient for oxygen and the rate of blood-flow in the retial capillaries. Again, the
longer the retial capillaries the greater the diffusion and the less the blood-flow, both of which will
enhance the build-up of equilibrium pressures. Theoretically, a small difference in gas-tension in the
arterial and venous capillaries at the beginning of the rete could lead to pressures of several thousand
atmospheres at the end near the gas-gland. However, active secretion of oxygen by the gas-gland
accords better with present knowledge than a liberation of this gas from the blood (Scholander, 1954;
Sundnes, Enns and Scholander, 1958). On the other hand, the gas-gland cells might not accept
oxygen from the blood unless the tension was higher than that in the swimbladder. This aspect must
be left for future experiments : here we may simply remark on the significance of long capillaries for
the efficient exchange of gases in the retia, particularly in those of deep-sea fishes. Regardless of the
attainment of high pressures, a deep-sea fish must have well-developed retia in order to prevent the
loss of gases from the swimbladder. Using his equations and reasonable values for the various con-
stants, Scholander (1958, p. 9) calculated ' . . . that the exchange through the rete in a deep-sea eel is so
great that if the blood in swimbladder has an oxygen tension of two hundred atmospheres it will leave
the bladder with an oxygen tension only a few millimetres higher than in the arterial blood '.

In proportion to the size of the swimbladder, bathypelagic teleosts have large retia mirabilia, the
relative development of these systems being greater than those of shallow water species (Marshall,
19150, 1954; Jones and Marshall, 1953). This difference may be given rough quantitative expression
by obtaining values of the ratio / x bjr for species from the two types of environment (/ and b being the
lengths of the major and minor axes of the sac (which approaches an ellipsoid in form) and r the
length of the retial capillaries).

Values of this ratio are given in Table 4 (p. 74) for various species of deep- and shallow-water
fishes. Drawings of the swimbladders of some of the latter species may be found in Text-fig. 36.

The first six species in the shallow-sea group are epipelagic fishes. It will be seen that the ratios
in these species are far higher than the figures obtained for the deep-sea species. But as regards a
counter-current exchange-system it is the absolute rather than the relative length of the retial
capillaries that is significant. However, apart from Pollichthys, Vinciguerria, Argyropelecus and Astro-
nesthes among the deep-sea group and Hyporhamphns from the epipelagic species, the retia of the
bathypelagic species are longer (some much longer) than those in the surface-swimming species. And
there is another factor to be considered, the diameter of the capillaries, for the smaller this is the
greater the efficiency of gaseous exchange. Two of the exceptions among the deep-sea group have
relatively small capillaries, which measured 7-8 ft in diameter in Argyropelecus and Vinciguerria. (There
are no data for the other two.) In the epipelagic species the capillaries are 10// or more in diameter.

Table 4 also reveals that the ratios and retial dimensions of Gadus minutus and Capros aper are close
to those of the bathypelagic species : this is not surprising in view of the depth-range of these two fishes.

Considering only the deep-sea fishes, it would be reasonable to expect that the deeper the living
space the longer would be the retia. In Table 4 it will be seen that the retia of Stephanoberyx monae
and Melamphaes megalops are much longer than those of the other deep-sea fishes. Now the first
species may well be demersal rather than pelagic in habit and it has a depth-range extending down to
2295 m. (Grey, 1956). Norman's (1929, 1930) data for Melamphaes megalops suggests that this fish
tends to be concentrated well below the 500-m. level. The populations of the other species tend to be
centred above this depth. Even more striking instances of this correlation between the retial span
and depth can be found if abyssal fishes are also considered. But this will best be left until the final
section of this report.

THE SWIMBLADDER AS A HYDROSTATIC ORGAN

The gas-gland
In parallel with their retia, the gas-glands of bathypelagic teleosts are relatively large compared with
those of shallow- water species. Some attention has already been drawn to this (Marshall, 1950,
1954; Jones and Marshall, 1953). Here a closer comparison will be made between various epipelagic

Text-fig. 36. Swimbladders of some epipelagic and bathypelagic fishes, showing the relative developments of the retia
mirabilia and gas-glands. Epipelagic species: (a, a') Cypsilitrus cyanopterus; (b, b', b") Danichthys rondektii; (c, c') Exocoetus
volitans; (d, d') Petatichthys capensis; (e, e') Hyporhamphus sp. Bathypelagic species: (f) Vinciguerria attenuata; (g) Argyro-
pelecus aculeatus; (h) Myctophum punctatum; (j) Chiasmodon niger; (k) Melamphaes megalops. Gas-gland dotted; retia, with
striations along the major axes. In a', b', b", c', d' and e' part or the whole of the gas-secreting complex is shown enlarged.
(A, xo-38; a', x 10; B, xo-6; b', x 5; b", 2-5; C, x 1 ; c', x 5; D, x i; d', x 5; e, x i ; e', X4; F, x 10; G, x 10; H, x 38; J, x6;
K, x 5.)

74 DISCOVERY REPORTS

Table 4. Szvimbladder dimensions and retial lengths of some bathypelagic and shallozv-

water teleosts

Length of

major axis I

minor axis b

retia r

Species

(mm.)

(ca)

Deep-sea

Gonostoma denudatum

16-0

2-0

2-5

Pollichthys mauli

5-°

2-0

1-2

Bonapartia pedaliota

IO'O

5-o

3-6

Vinciguerria attenuata

8-5

27s

o-8

Argyropelecus aculeatiis

8-5

4-5

i-5

Polyipnus latematus

6-o

3-5

3-0

Astronesthes niger

5-5

2-5

i-5

Myctophum punctatum

12-0

4-5

2-2

Diaphus rafinesquei

20-0

6-o

2-5

Lampanyctus giintheri

9-5

2-0

2-8

Melamphaes megalops

8-5

5'°

12-0

Stephanoberyx monae

16-0

8-o

Chiasmodon niger

16-0

3-0

3'5

Shallow sea

Cypsilurus cyanopterus

140-0

20-0

i-5

1870

Danichthys rondeletii

90-0

io-o

1-25

720

Exocoetus volitans

58-0

6-o

175

200

Petalichthys capensis

107-0

6-o

i-o

640

Hyporhamphus sp.

6o-o

5"°

2-5

120

Scombresox saurus

105-0

6-o

1 -25

500

Gadus mimitus

38-0

6-o

3-0

Capros aper

23-0

6-o

2'5

and bathypelagic species. The extent of the gas-glands of some of these fishes can be seen in Text-
fig- 36-

While these drawings give a ready impression of the relatively large expanse of the glands in deep-
sea species, a more meaningful comparison may be made by estimating the ratio of the surface-area
of the gas-gland to the volume of the swimbladder. Measurements were made only on fishes showing
good expansion of the gland and swimbladder, the results being given in Table 5. Before considering
these figures it should be remembered that the comparison of gas-glands in terms of surface-area is
not entirely appropriate, since some are more than one cell in thickness. But as the glands of the
three flying fish appear to be no more than one cell thick, this will not bias the figures in favour of the
deep-sea species. Of these, Vinciguerria attenuata and probably the two Astronesthes, have single
layer gas-glands, while those of Argyropelecus and the three lantern fishes are multi-layered.

The proportionately greater glandular surface in the bathypelagic species will be immediately
obvious. The contrast is as great as that between the two environments. The flying fishes spend most
of their life not far below the surface, while the populations of the deep-sea species are centred at
various levels between 200 and 1000 m.

The significance of these differences may be appreciated by comparing the flying-fish, Cypsilurus
cyanopterus, with the lantern fish, Myctophum punctatum. A 600-g. Cypsilurus will have a swim-
bladder volume of about 30 ml., while the corresponding figure for a 5-g. Myctophum will be 0-25 ml.
Assume that the flying fish and lantern fish live at mean pressures of 1-5 and 30 atmospheres re-
spectively. Considering the swimbladders only during the steady state, when the gas lost by diffusion
is being made up by secretion, we may further assume that the flying-fish loses 5 per cent of the
contained gases during the course of a day. The same percentage may be taken for the lantern fish

THE SWIMBLADDER AS A HYDROSTATIC ORGAN 75

for the time it spends at its daytime level (say, 12 hr.). To make good this loss, the flying-fish must
secrete 1-5 ml. gas at a pressure of 1-5 atmospheres. The lantern fish must produce 0-0125 m^ at
30 atmospheres or 0-25 ml. at 1-5 atmospheres. Thus, while the volume of the flying-fish swimbladder
is 120 times that of the lantern fish, the relative amounts of gas required to restore a gradual loss of
buoyancy differ by no more than a factor of 6.

Table 5. Relative development of the gas-gland in some epipelagic and

bathy pelagic fishes

Standard

Surface-area of gas-

length

gland (mm.'1) .-volume

Species

(mm.)

of swimbladder (mm.3)

pipelagic

Cypsilunis cyanopterus

290-0

1/120

Danichthys rondeletii

214-0

1/120

Exocoetus volitans

159-0

1/160

Hyporhamphus sp.

II2-0

1/25

athypelagic
Astronesthes niger

41-0

i/4

A. similis

104-0

1/6

Vinciguerria attenuata

43"5

i/7

Argyropelecus acaleatus

23-0

i/7

Benthosema suborbitale

24-0

1/2

Lampanyctus giintheri

53-°

i/3

Myctophum punctatum

71-0

i/5

Melamphaes megalops

56-0

1/16

Chiasmodoti niger

104-0

i/4

However, in estimating the figures in Table 5, it was found that a Cypsilunis of the above weight
has a gas-gland with a surface-area of 25 mm.2, while the figure for the lantern fish is about 20 mm.2
Furthermore, the lantern fish has a gas-gland consisting of many layers of cells, whereas that of the
flying fish is probably single-layered. This would suggest that the lantern fish is readily able to make
up the loss of gas. But, unlike the flying-fish, the lantern fish undertakes extensive vertical migra-
tions. Towards sunset it will climb several hundred metres towards the surface-layers, and after
spending the hours of darkness near the surface, will then dive to its daytime depth. In considering
the relative development of the gas-gland, it is clear that vertical migrations must also be taken into
account. This will best be dealt with at a later stage (p. 89). Here we may turn to the fine structure
of the gas-glands.

In shallow-water fishes there is considerable variability in the fine structure of the gas-glands
(Woodland, 191 1 a; Fiinge, 1953) and this is also true of deep-sea fishes. However, three main groups
may be recognized (see Text-fig. 37).

(1) Gas-glands consisting mostly of giant cells. Capillaries partly intracellular. Vinciguerria and
Sternoptyx. In the first genus the cells of the expanded gas-gland measure from 100 to 150// in length.
Nusbaum-Hilarowicz (1920) gives the dimensions of the cells of Sternoptyx as 50-95//. In Vinci-
guerria the extent of the intracellular capillaries is considerably greater than that of the intercellular
elements, but the reverse seems to be true of Sternoptyx.

(2) Gas-glands consisting mostly of medium-sized cells. Capillaries intercellular. Cyclothone,
20-50//; Maurolicus, 20-40//; Argyropelecus, 25-50//; Polyipnus, 25-50//.

(3) Gas-glands with small cells. Capillaries intercellular. Myctophum punctatum, 15-20//;
Diaphus dofleini, 10-15//; Opisthoproctus soleatus, 15-25//.

Giant cells are also found in the gas-glands of shallow-water fishes, such as Carapus, Perca and

76 DISCOVERY REPORTS

Zeus. In reviewing the available information, Fange (1953) suggests that such cells may be quite
common among euphysoclists. But the two genera in the first group of deep-sea fishes appear to be
unique in having glands that are largely composed of giant cells. In Vinciguerria these cells may be
as much as 100// in depth, a striking contrast to the 10-15^ cells of the gas-gland of Diaphus dofleini,
which are disposed in several layers to a depth of about 200^. The gas-gland of Vinciguerria is also
remarkable in two other ways, the first being that the greater part of the contact between the giant

Text-fig. 37. Three types of gas-glands in bathypelagic fishes; (a) consisting mostly of giant cells {Vinciguerria), with intra-
cellular capillaries; (b) with medium-sized cells (Polyipnus), and (c) with small cells (Myctophidae). The base of the cell of
Vinciguerria is 170/1 in length, while the cell of Polyipnus fitting into the U-bend of a capillary is about 50//. wide. The
cells of Myctophum are from 10 to 17/* in length along their longer axes, ic, intracellular capillary ; pec, pericapillary cytoplasm.

cells and the capillaries supplying them is within the cytoplasm. Secondly, these intracellular
capillaries connect with one another through fine canals in the cytoplasm, the lumen of the canals
being little more than ifi across, too fine to admit the elliptical red blood corpuscles, which are about
6-8 n long and 2-3^ wide.

A number of workers (see Fange, 1953) have observed that the cytoplasm around the capillaries
stains differently from the remaining cell contents. I have also seen this in the gas-glands of Argyro-
peleats, Polyipnus, Vinciguerria, Maurolicus, Cyclothone and Opisthoproctus . After staining with

THE SWIMBLADDER AS A HYDROSTATIC ORGAN 77

haemalum and eosin, the pericapillary cytoplasm has a hyaline, homogeneous appearance, which
contrasts with the lilac or salmon-pink colour of the other cell contents. The hyaline border varies
from 2 to 6/1 in thickness.

In his plates of the gas-gland of Sternoptyx, Nusbaum-Hilarowicz (1920) shows the pericapillary
borders to have a striated appearance, and this has also been reported in other fishes by Vincent and
Barnes (1896) and by Bykowski and Nusbaum (1904). Like Fange (1953), I was unable to detect
this, but the sections of the giant cells of Vinciguerria did reveal that the interface between the blood-
system and the cytoplasm can be the site of intense activity. The borders look as though they are
breaking down to form small vacuoles (PI. II, fig. 3) and this process seemed also to be taking place
along the intercapillary canals in the cytoplasm. In sections of the gas-gland of Polyipnus laternatus
the pericapillary border almost had a striated appearance, but closer examination showed the striation
to be a series of elongated ' vacuoles ' aligned normally to the bore of the capillaries.

These cytoplasmic inclusions cannot be gas-bubbles as they have a different optical appearance,
and in Vinciguerria, the hyaline blobs that appear along the capillaries look very like the vacuoles that
are lying free in the cytoplasm. It may also be significant that the vacuoles are generally larger near
the interface between the gland cells and the swimbladder cavity.

In a series of papers, Scholander and his colleagues (Scholander and van Dam, 1954; Scholander,
1954, 1956; Sundnes, Enns and Scholander, 1958) have argued that the Root effect (the release of
oxygen from oxy-haemoglobin by a lowering of the pH of the blood) plays little part in the secretion
of this gas against the high oxygen pressures that exist in the swimbladders of deep-sea fishes. (By
using marked oxygen (O18) Scholander, van Dam and Enns (1956) showed that the gas must come
from the water surrounding the fish (cod) and be transported as oxy-haemoglobin from the gills to
the swimbladder).

In particular, if the lower limit of the blood pH is taken as 6-5, the Root effect is almost non-
existent in deep-sea fishes, such as the long-nosed eel {Synaphobranchus-pinnatus), the blue hake
(Antimora violacea) and the round-nosed ratfish (Coryphaenoides rupestris), but is well marked in
shallower-water species like the tautog (Tautoga onitis). (Scholander and van Dam (1954) determined
the oxygen dissociation of the blood at oxygen-tensions from 0-2 to 140 atmospheres and at acidities
down to pH 5-6.) Thus in deep-sea fishes the oxygen seems not to be liberated directly from the
blood, but to be actively secreted by the gas-gland cells. Furthermore, even in the shallow water
toadfish (Opsatius tau), Wittenburg (1958) has shown (in a very neat way) that the gas-gland cells are
able to transport oxygen from the blood plasma into the swimbladder. After supplying the fish with
carbon monoxide in (presumably) sufficient quantities to immobilize the haemoglobin, oxygen was
still secreted into the swimbladder. Wittenburg suggested that this active transport of gas is by way
of an iron-haem protein.

Perhaps the foregoing observations of the gas-gland cells of Vinciguerria also support this idea.
Perhaps there are three main phases in the formation of the gas bubbles that are eventually released
into the swimbladder. The first consists of an intense interaction between the blood and the peri-
capillary cytoplasm, when vacuoles are formed. Fange (1953) has shown this part of the cytoplasm
to be devoid of glycogen, while acid-phosphatase activity seems to be concentrated around the peri-
pheral zones of the gland cells. The second phase would be the growth of those vacuoles and their
transport to the interface between the cell and the lumen of the swimbladder. Some of the energy
for this process would be provided by the breakdown of glycogen. The vacuoles may discharge their
contents into the mucous fluid covering the gas-gland, after which gas bubbles are formed (third
phase) eventually bursting to release their contents (mainly oxygen) into the swimbladder cavity.
(Gas-bubbles have never been observed within the gland cells.) The function of the vacuoles would

78 DISCOVERY REPORTS

be to supply 'high tension' gas-nuclei around which the bubbles could form. However, due to
surface-tension, the gas-pressure within a bubble is inversely related to the diameter of the bubble,
which means that considerable pressures will be required for its growth. But in the foam found in
lung-alveoli, Pattle (1958) discovered that the surface-tension of the bubbles was much reduced by
a surrounding layer of insoluble protein. Perhaps the foam covering the gas-gland has somewhat
similar properties.

In conclusion, it must be acknowledged that little is known of gas-secretion by the swimbladder,
particularly in deep-sea fishes. As Scholander (1956, p. 523) has written: ' In spite of all the information
available regarding the function of the gas-gland in fishes, one may safely say that none of the three
cardinal feats of the gland can as yet be explained: namely, the production of 100-200 atmospheres
of oxygen, of 10-20 atmospheres of nitrogen and of 0-1-0-2 atmospheres of argon.' In the endeavour
to solve these problems the giant cell gas-gland of Vinciguerria should provide excellent experimental
material, particularly for histochemical studies.

The resorbent part of the swimbladder

We have already seen that the swimbladder volume of a marine teleost must be kept near or equal to
some 5 per cent of the body volume. There is evidence that teleost fishes have a certain latitude of
movement above a level of neutral buoyancy (Scholander, Claff, Teng and Walters, 1951 ; Jones,
1952), but beyond this range the fish will tend to be 'ballooned' out of control as the volume of its
swimbladder (and hence its own volume) increases. Apart from the dangers of injury, an upward
migration involving a threefold increase in the volume of the swimbladder means that the fish must
exert (by compensatory movements) an upward force equal to about 10 per cent of its weight in air
in order to make 'downwards headway' (Denton and Marshall, 1958).

During a migration towards the surface, a teleost with a closed swimbladder must reduce the
volume of the sac to a manageable, just buoyant, level by loss of the contained gases to the blood. This
diffusion takes place through special resorbent surfaces with a rich supply of capillaries, some account
of which has been given in the earlier descriptive section (pp. 7-50). These findings can now be
summarized and discussed. Other aspects will also be considered in a later section on vertical
migrations.

Order Isospondyli, Suborder Stomiatoidea

In this group there is a close association between the resorbent system and the gas-gland, for the
venous return from the capillaries is generally by way of veins running from the gland to the rete
mirabile. These veins may return from the gland {Astronesthes niger, Vinciguerria and Maurolicus), or
run along the inner edge of the gland {Pollichthys). Argyropelecus also has periglandular veins but these
may also pass through the gland. (With the material available it was not possible to make a close
study of these venous channels.)

The arterial capillaries of the resorbent surface are formed from a branch of the retial artery which
leaves this vessel just before it flows into the rete, to run forward alongside the latter. On reaching
the resorbent area, it breaks up into arterioles and capillaries, which together with the venous elements,
form the resorbent complex.

Since the venous blood from this complex eventually flows through the rete mirabile, a bipolar
retial system would appear to be essential. To supply the venous part of a resorbent area a unipolar
rete would have to give off hundreds of separate venous capillaries, which might then have to run for
considerable distances before meeting their arterial counterparts (see, for instance, Vinciguerria,
Maurolicus and Astronesthes niger). Such an arrangement might well be functionally unbalanced

THE SWIMBLADDER AS A HYDROSTATIC ORGAN 79

with the arterial system, particularly in fishes that make upward vertical migrations. To keep the
swimbladder from over-inflation the rate of gas-removal should be high : hence the need to remove
venous blood from the capillary system as quickly as possible (see also pp. 92-94).

The resorbent circulation of the stomiatoid swimbladder would appear to be unique among deep-
sea fishes (perhaps also among teleosts in general). It presumably functions as follows: During gas-
resorption, contraction of the arterioles forming the retial capillaries will close down the flow of
arterial blood through the rete (Fange (1953) has shown how such contraction can lead to capillary
closure). As the retial artery is still open blood can only flow down the arterial branch supplying the
resorbent area. Blood returning from the system will be free to flow through the rete, since the
venous capillaries will be fully open (presumably they have extra room for expansion owing to the
virtual closing of their arterial counterparts). During gas-secretion both sets of retial capillaries will
be open and the gas-gland fully expanded. Arterial blood will now flow from the retial artery into
the dilated arterioles (and so through the rete) rather than down the by-pass vessel into the resorbent
system. Furthermore, when the gas-gland is expanded, the resorbent system is contracted (Fange,
1953) and this may well lead to a stoppage of the resorbent circulation.

Just how this antagonistic action of the secretory and resorbent mucosa is brought about in the
stomiatoids has yet to be determined. In euphysoclist teleosts, the action is perfectly clear (see
p. 81 of this section). However, the smooth muscles of the swimbladder wall are likely to be
involved. (In Argyropelecus and Polyipnus the muscle layer is close to the inner epithelium.) The
disposition of the fibres may be such that those controlling the expansion of the capillary network are
contracted during resorption, while those around the gas-gland are relaxed. The opposite would occur
during gas-secretion. An extreme instance of this antagonism may be seen in Text-fig. 32 of the
swimbladder of Vincignerria.

Dissections made of two specimens of Argyropelecus aculeahis show the swimbladder as it probably
appears during the resorptive and secretory phases. Considering only the former condition, the
relatively large expanse of the capillary layer and the bunching up of the gas-gland is particularly
striking (Text-fig. 38).

As already indicated, the capillary circulation of stomiatoids is unique in that the venous return-
flow is through the rete mirabile. In the groups now to be considered the secretory part of the swim-
bladder is perfectly distinct from the resorbent part, this having a separate venous system (which
usually runs into the hepatic or cardinal veins). Teleosts with such a swimbladder are called euphyso-
clists and are to be distinguished from paraphysoclists, those in which the two parts are not so sharply
delimited (Rauther, 1922).

Salmonoidea (deep-sea). In a recent revision of the argentinine fishes (genera Argentina and
Glossanodon), Cohen (1958) has shown that the swimbladder has two distinct parts, comprising an
anterior, thick-walled, cylindrical chamber and a posterior, thin-walled diverticulum. From Fange's
(1958) observations and my own, it is clear that the anterior chamber contains the gas-gland and the
micro-retia. Cohen described the posterior diverticulum as having a vessel from the distal end that
seemed to drain into the renal portal system (or is this the dorsal aorta?), while a vein from the front
of the down-turned part leads to the hepatic portal vein. In a specimen of Argentina sphyraena
(standard length 170 mm.), I found a well-marked posterior diverticulum in which the down-turned
part, that runs forward beneath the thick-walled chamber, measured 13 mm. in length. The inner
epithelium of this part was thrown into folds and contained a capillary network. There is thus good
indication that the diverticulum is the resorbent part of the swimbladder. I also found a thin-walled
posterior chamber in Microstoma microstoma, but this had no down-turned antrorse section. Nansenia
may also have such a structure (the individual I examined was not well-preserved).

8o DISCOVERY REPORTS

In Winteria and Opisthoproctus the swimbladder does not appear to be differentiated into two
sharply demarcated sections. The micro-retia and gas-gland are certainly found in the anterior part
of the sac, but behind this the walls seem just as thick. Perhaps the capillary system is found in the
rear part of the sac, but I was unable to ascertain this in the material at my disposal.

Text-fig. 38. Swimbladder of Argyropelecus aculeatus, (a) with the resorbent capillary network expanded and the gas-glands
contracted, (b) with the capillary network relaxed and the gas-glands expanded, en, capillary network; gg, gas-gland.

Order Iniomi, Suborder Myctophoidea

Myctophidae. The resorbent surface of the lantern fish swimbladder is an ' oval ' like that found in
various gadoid, macrourid and spiny-finned fishes. It is a thin-walled circular part of the swimbladder
and is surrounded by radial and circular smooth muscle fibres, having an antagonistic action. When
the radial fibres contract (the circular ones being relaxed), the oval with its rich supply of capillaries
is stretched and exposed to the gases in the swimbladder. The circular muscles act as a sphincter.
As they contract the thick-walled parts of the swimbladder wall surrounding the oval are drawn
towards its centre, eventually coming together. As the oval shuts, its walls are thrown into ridges and
folds, and at the end of the process it looks like a wrinkled projection on the face of the sac.

In most of the myctophids I dissected, the oval had this appearance. It was fairly well expanded
in two specimens of Myctophum punctatum and one of Diaphus dofleini, and half-open in a specimen
of D. rafinesquei and of Lampanyctus guentheri. It has already been suggested that the structure
Rauther (1922) described in Diaphus rafinesquei as the praevesica is actually an oval, and the same is
presumably true of the conical projection found at the front end of the swimbladder of Lampadena
chavesi (see pp. 38-39).

A longitudinal section of a closed oval in Myctophum punctatum is shown in PI. III. At high
magnifications the circular and radial muscles could be seen, the former having a ' bunched-up '
appearance. The inner epithelium, close to which lies the capillary network, is thrown into folds,
while the tissues in the walls have relaxed during the closure. No doubt this accommodation is made
possible by the semi-gelatinous nature of the submucosa, although in the oval of the perch (Perca
fluviatilis) Saupe (1939) found the gelatinous and fibrous components to be much reduced.

The myctophid oval lies at the anterior end of the swimbladder close to the retia mirabilia (see

THE SWIMBLADDER AS A HYDROSTATIC ORGAN 81

Text-figs. 15-23). Its arterial supply usually comes from a branch or branches of the retial artery,
while the venous return is through a vessel draining into the cardinal vein.

Order Miripinnati

In these teleosts the swimbladder is only functional during the larval phase (Bertelsen and Marshall,
1956). As in certain percomorph fishes, the anterior, thick-walled secretory part is sharply distinct
from the posterior thin-walled section, but there is no intervening diaphragm. Although it has not
been closely examined, there can be little doubt that the thin-walled part is concerned with gas-
resorption.

Order Berycomorphi, Suborder Anoplogastroidea

Both the Melamphaidae and Stephanoberyx have a typical ' oval ' which is set on the roof of the swim-
bladder near its posterior end. A drawing of the almost closed oval of a Melamphaes megalops is
shown in Text-fig. 27. In the specimen of M. unicornis (Text-fig. 28) examined, the oval, from which
a large vessel drains into the cardinal vein, was completely closed. The oval of the Stephanoberyx
monae was in much the same condition as that of Melamphaes megalops.

Order Percomorphi

Chiasmodontidae. Chiasmodon niger. In this species a diaphragm divides the anterior gas-secreting
chamber from the posterior resorbent chamber. Such a partition is found in the Solenichthyes,
Thoracostei, certain Percomorphi and Scleroparei (Fange, 1953 and personal observation) and is
probably quite common in zeomorph fishes (a diaphragm is found in Zeus faber). As Fange (1945,
1953) has shown, the movements of this diaphragm are controlled by the antagonistic action of the
secretory and resorbent parts. During gas-production the muscle fibres of the secretory part relax,
while those of the resorbent mucosa are contracted. The antagonism reverses during gas-resorption.
Considering first the latter, the contraction of the muscles in the secretory chamber pulls the dia-
phragm to the forward end of the swimbladder, while the relaxation of the resorbent layer ensures that
the capillary layer is expanded and fully exposed to the gases. During secretion the diaphragm moves
to the posterior end of the sac and now the gland is fully expanded.

The swimbladders of the three Chiasmodon examined each show different phases of this process
(Text-fig. 29). In the 104-mm. fish the gland is bunched up and its chamber occupies no more than
one-fifth of the total length of the swimbladder. This fraction is rather more than a half in the 49-mm.
fish, while in the third fish it is a quarter. Having regard to the previous paragraph, it is evident the
swimbladder of the first and third fishes show the disposition of the tissues during resorption and
secretion respectively.

BATHYPELAGIC FISHES WITHOUT A SWIMBLADDER

Summarizing the earlier descriptive section, the following groups either lack a swimbladder, or it is
regressed in the adult phase:

Order Isospondyli. Suborder Stomiatoidea : Gonostomatidae, Cyclothone spp., Gonostoma elongatnm,
G. bathyphilum; Astronesthidae, (in Diplolychnus mononema, Borostomias antarcticus, Astronesthes
gemmifer, the swimbladder seems to regress during adult life) ; Stomiatidae ; Melanostomiatidae ;
Chauliodontidae ; Idiacanthidae ; Malacosteidae.
Suborder Salmonoidea: Bathylagidae.

Suborder Clupeoidea: Alepocephalidae (many of these fishes appear to be benthic in habit);
Searsidae.

82 DISCOVERY REPORTS

Order Iniomi. Suborder Alepisauroidea. Suborder Myctophoidea : Scopelosauridae ; Mycto-
phidae : while most species have a swimbladder, the following species lack this organ : Lampanyctus
braneri, Ctenobranchus nigro-ocellatus, Gonichthys coccoi, Diaphns coeraleus. In Electrona antarctica,
the swim bladder regresses during the adult phase and as already mentioned (p. 65), the swim-
bladders of Lampanyctus leucopsarus and Diaphus theta are reduced and invested with fat.

Order Cetunculi, Order Miripinnati, Order Giganturoidea, Order Lyomeri. Order Allotriognathi:
Stylophorus chordatus. Order Berycomorphi, Suborder Anoplogastroidea : Anoplogaster longidens,
Melamphaes mizolepis. Order Percomorphi, Chiasmodontidae: Pseudoscopelus scriptus, Dysalotus
alcocki. Order Pediculati, Suborder Ceratioidea.

VERTICAL DISTRIBUTION AND THE SWIMBLADDER

In his ' Challenger' Report, Giinther (1887, p. xxxiii) has written: ' I formerly assumed that the fishes
of the open sea were living either near to the surface or at the bottom, but I think now that Mr Murray
is right in supposing that certain fishes live habitually in intermediate strata, without ever coming to
the surface or descending to the bottom.' The biologists of the ' Valdivia' Expedition (1898-9) were
the first, however, to give close consideration to the fact that deep-sea fishes live at different levels in
the ocean. After distinguishing between benthic and bathypelagic species, Brauer (1906) proceeded
to discuss this problem and the difficulties involved with the use of open-nets. But the expedition
did fish some closing-nets and Brauer gave examples of species taken with this gear (e.g. St. 120,
Cyclothone microdot!, 1500-900 m. ; St. 227, Sternoptyx diaphana, 800-600 m.; St. 229, Lampanyctus
nigrescens, 1000-800 m.). The Deutsche Sudpolar Expedition (1901-3) used open vertical and hori-
zontal nets, and some details are given of the apparent vertical distributions of the deep-sea fishes that
were taken (Pappenheim, 1914).

Since these earlier expeditions, our knowledge of the depth distribution of bathypelagic fishes has
been largely due to the 'Michael Sars' Expedition in 1910 (Murray and Hjort, 19 12); the Danish
Oceanographic Expeditions in the Mediterranean and adjacent Atlantic waters during 1908-10
Uespersen, 1915; Taning, 1918 and Jespersen and Taning, 1926); the Discovery Investigations
(Norman, 1929, 1930); the Dana Expeditions (Regan and Trewavas, 1929, 1930; Bertin, 1934, 1937;
Ege, x934> :948> 1953; Bruun, 1937, Bertelsen, 1951 and Bertelsen and Marshall, 1956) and the
Bermuda Oceanographic Expeditions (Beebe, 1937). From these and other publications, Grey (1956)
has compiled a valuable and detailed survey of the bathypelagic and benthic fishes found below
a depth of 2000 m. A more general appreciation of vertical distribution may be found in Marshall ( 1 954).

Besides tangible evidence from the nets, underwater observations are now beginning to play their
part. Since Beebe's (1934) dives in a bathysphere, a number of observers have been down in bathy-
scaphes. To take but one account (Peres, 1958), it is clear that an experienced observer can both
enlarge and corroborate present knowledge. During three dives off Cap Side, Peres found that the
schools of lantern fishes not only occurred in a mid-water layer (mainly from 400 to 700 m.), but were
also clustered close to the bottom (about 10 m. above 1500 m.). He also saw that Argyropelecus
hemigymnus is found between 250 and 600 m. (with a maximum at 350-400 m.), which is a striking
confirmation of Jespersen's (191 5) estimates from open-nets.

These findings, so far as they concern the fishes dealt with in this report, may now be summarized:
A. Fishes with centres of concentration between depths of about 200 and 1000 m.

Reference to the papers cited earlier will show that any species may have a considerable vertical
range about its centre of concentration. And, apart from diurnal migrations, the main depths of

VERTICAL DISTRIBUTION AND THE SWIMBLADDER 83

occurrence may vary in space and time. Species living in very transparent waters live further down
than their relatives in less clear waters (comparison of Beebe's (1937) and Grey's (1955) data with
those obtained in other parts of the Atlantic (Murray and Hjort, 1912) reveals this). Furthermore, the
higher the latitude the less the depth of maximum concentration (Murray and Hjort, 1912). There
may also be seasonal changes, species tending to live nearer the surface during the winter months
(Jespersen and Taning (1926), Taning (1918)).

Order Isospondyli. Suborder Stomiatoidea. Apart from those listed in section B, most stomiatoids
seem to belong here. Suborder Salmonoidea : Opisthoproctus, Winteria, Bathylagidae. Apart from
Bathylagus argyrogaster, which was taken mainly above 500 m., the commoner species taken during
Discovery Investigations appear to be concentrated between 500 and 1000 m. (Norman, 1930).

Order Itiiomi. Most alepisauroids (Marshall, 1955) and Myctophidae.

Order Giganturoidea, Regan, 1925.

Order Allotriognathi, Stylophorus chordatus (Bruun et al. 1956).

Order Berycomorphi: Melamphaidae. The commoner species taken in Discovery nets (Norman, 1929,
1930) appear to come from depths between 500 and 1000 m.

B. Fishes with centres of concentration between depths of about 1000 and 4000 m.

Order Isospondyli. Suborder Stomiatoidea: Gonostomatidae, Cyclothone microdon, C. livida, C.
acclinidens, C. obscura, Gonostoma bathyphilum.

Order Lyomeri. The centre of distribution of Eurypharynx pelecanoides seems to lie between 1400
and 2800 m. (Grey, 1956).

Order Apodes. Certain of the deep-sea eels such as Cyema atrum, Serrivomer parabeani and Avocettina
infans appear to be commoner at these deeper levels (Grey, 1956).

Order Berycomorphi: Melamphaes nigrescens (Grey, 1956) and possibly M. cristiceps (Norman, 1929,
1930) occur below 1000 m.

Order Pedicidati: Suborder Ceratioidea. Metamorphosing, adolescent and adult deep-sea angler
fishes are mainly to be found at or below a depth of 1500 m. (Bertelsen, 1951).

By referring to the descriptive part of this report, it will be clear that the populations of bathy-
pelagic fishes with fully developed gas-filled swimbladders are centred in the upper reaches (200-
1000 m.) of the deep-sea. The main groups are the Gonostomatidae (most species), Sternoptychidae
(hatchet fishes), Astronesthes spp. Myctophidae, and Melamphaidae (most species). While numerous
species from these levels lack a swimbladder [the Melanostomiatidae, Stomiatidae, Chauliodontidae,
Idiacanthidae, Malacosteidae, Bathylagidae, Alepisauroidea and Giganturoidea are the main groups
(but see also the summary on p. 81-82)], this condition is universal in the fishes centred between depths
of 1000 and 4000 m.

Hydrostatic pressure increases by one atmosphere for each 10 m. of depth and the average depth
of the ocean is about 4000 m. It might thus be supposed that the limitation imposed on the develop-
ment of a gas-filled hydrostatic organ is simply related to the pressure factor. Clearly, the aspects to
be considered concern the compressibility of gases and the amounts of energy and gas required to
keep the swimbladder inflated at the appropriate volume against high hydrostatic pressures.

84 discovery reports

Compressibility of gases
The swimbladder gases of deep-sea fishes consist largely of oxygen (Scholander and Van Dam, 1953 ;
Kanwisher and Ebeling, 1957) and this gas alone will be considered.1 At normal temperature and
pressure the density of oxygen is 1*429 g./l., which value is about one seven-hundredth of the density
of sea-water. In other words, at a depth of 7200 m., the density of oxygen is equal to that of seawater,
and the gas would thus have lost its positively buoyant properties.

A fish having 95 g. of fat-free tissue, with a density of 1-076 (taking Taylor's (1921) estimate) and
a 5-ml. swimbladder will have a density of about 1-07, which is well above the value for seawater
(1-028) at this depth. Clearly a gas-filled swimbladder would be virtually useless. However, we shall
see later that abyssobenthic fishes with well-developed swimbladders may range as deeply as 5000 m.
At such a level the density of oxygen is about 0-7. Thus to achieve neutral buoyancy, either the
volume of the swimbladder must be considerably increased or the density of the tissues be reduced.
There is no evidence of the first desideratum being met, but there is good indication of a general
lightening of the tissues (see p. 96).

Energy requirements of the swimbladder

The combined partial pressures of the gases dissolved in seawater at any depth total no more than one
atmosphere. The oxygen tension is thus about one-fifth of an atmosphere, yet the partial pressure of
this gas in the swimbladder may be 200 atmospheres or more (Scholander, 1954). Thus, between the
uptake of oxygen by the blood circulating through the gills and its entry, under the appropriate
pressure, into the swimbladder, it is clear that considerable energy will be required to concentrate the
gas. By using the energy of compression equation, Parr (1937) calculated that, to fill its swimbladder
to the requisite buoyant volume, a fish living at a depth of 1000 m. would use 300 times as much
energy as the amount it would need at 10 m. While appreciating this, Bruun (1943) pointed out that
the absolute amount of energy needed is quite small. He expressed it thus: 'If we take an adult
Spirilla of a weight of 10 g. and with a shell containing about 0-5 ml. gas, it would cost about 13 g.
calories to fill it at 2000-m. depth, corresponding to only a few mgs of food.' Looking at the problem
from much the same aspect, Scholander (1954) has calculated that for each part of oxygen secreted
into the swimbladder a minimum of 3 per cent must be diverted to the work of compression. Like the
compressibility factor, it would thus seem that the energy problem is not so serious as it might
first appear.

Gas requirements of the swimbladder

While the proportion of oxygen needed for the energy of compression seems not to be excessive, gas
must be available in sufficient quantity, if the swimbladder is to be kept inflated at the volume for
weightlessness in water. The greater the depth the more the gas needed for a given unit of buoyancy
(see pp. 89-90). But it should be remembered that most species of bathypelagic fishes have swimbladders
with a capacity of 0-5 ml. or less. On the other hand, many of these fishes move up and down in the
sea each day. As these migrations take place within the upper 1000 m. of the ocean, the effects of
pressure on gas-density need not be considered. (At 500 m. the density of oxygen is about 0-07.) But
as it swims downwards to regain its daytime station, the main physical stress facing a fish is the pro-
vision of enough oxygen to fill the swimbladder. From this general introduction we may turn to the
physical and biological aspects of vertical migration.

1 The swimbladder also contains nitrogen (from about 2 to 15 per cent), argon and carbon-dioxide. If the partial pressure
of C02 ever reached 50 atmospheres, which from the papers cited, seems unlikely, it would exist as a liquid at temperatures
of 1 30 C. and below.

THE PHYSICS AND BIOLOGY OF VERTICAL MIGRATIONS 85

THE PHYSICS AND BIOLOGY OF VERTICAL MIGRATIONS
After reviewing the evidence for the daily changes in the vertical disposition of bathypelagic fishes,
some appreciation of their physical and biological environments will be given. In moving up and
down, these fishes are following inner urges, and in so doing are exposing themselves to changing
physical and biological conditions. Discussion of these aspects forms the third part of this section
and leads to the final one, which centres around the vertical distribution of pelagic and benthic
deep-sea fishes with a swimbladder.

The evidence for vertical migrations
Study of the deep-sea fishes taken by the ' Challenger' (1872-6) led Giinther (1887) to regard species
with well-developed luminous organs and eyes as nocturnal surface-swimmers, which during the
daytime, withdraw to the darkness of the deeper waters. The 'Valdivia' (1898-9) and 'Gauss'
(1901-3) took numerous luminous fishes in surface-nets at night, and both Brauer (1906) and Pappen-
heim (19 14) concluded that many deep-sea fishes regularly seek the surface-waters during the hours
of darkness. The fishes they listed include several species of myctophids, Astronesthes niger, Idia-
canthus fasciola, Stomias affirm and certain melanostomiatids.

Murray and Hjort (19 12) also found that Astronesthes niger and Idiacanthus could be taken at the
surface during the night. Moreover, the hauls of the ' Michael Sars ' enabled Hjort to be more precise
concerning the vertical migrations of Gonostoma elongatum and Photostomias guerni. During the day
both species were only to be found in nets fished at 500 m. and below, but at night were taken between
150 and 500 m. Jespersen (191 5) was also able to analyse the diurnal changes in distribution of
Argyropelecus hemigymnus in the Mediterranean. Daytime hauls revealed that the populations were
centred below 500 m., whereas at night the main concentrations were between about 150 and 500 m.

The Dana Expeditions fished many nocturnal nets, and scrutiny of the papers concerning the fishes
(Regan and Trewavas, 1929, 1930; Ege, 1934, 1948) shows that numerous stomiatoids were taken in
the upper 50 m. during the night. However, many species were not caught in these near surface-nets.
Considering only the former and the commoner records, the following are evidently nocturnal surface
fishes: Astronesthidae ; Astronesthes niger, A. indicus, A. filifer, Melanostomiatidae: Eustomias
obscurus, E. brevibarbatus, E. macrurus, Bathophihis metallicus, B. pawneei and Melanostomias
spilorhynchus; Stomiatidae, all species, except Stomias nebulosus and S. colubrinits ; Idiacanthidae,
Idiacanthus fasciola; Chauliodontidae, Chauliodus danae, Malacosteidae, Photostomias guerni and
Aristostomias polydactylus.

However, by far the commonest fishes in the surface-waters at night are the Myctophidae. Many,
but seemingly not all, species can be netted at the surface after sunset. In the eastern tropical Pacific,
Beebe and Vander Pyl (1944) studied the migration of various species, particularly Gonichthys coccoi.
By day, the schools were centred about 400 m., but just after dark the fishes appeared at the surface,
where they swarmed between 7.0 and 10.0 p.m. Thereafter, they appeared to disperse or withdraw
from the surface, but were still caught there until 6.30 a.m., when they withdrew to their daytime
levels.

The other species that massed near the surface after dark included Lampanyctus macropterus,
L. omostigma, Myctophum affine, M. aureolatematum, M. evermanni, M. laternatum, M. reinhardti,
Notolychnus valdiviae. But the catches of certain species, notably Lampanyctus mexicanus, came from
deeper-lying waters at all times of day. Other evidence for diurnal movements in Myctophidae may
be found in the papers by Taning (1918), Tucker, 1951, Grey (1956) and Barham (1957).

WOODS
HOLP

Mass'

86 DISCOVERY REPORTS

Besides the evidence to be got from nets, studies of fishes in relation to deep-scattering layers
(Marshall, 1951; Tucker, 1951; Hersey and Backus, 1954; Kanwisher and Ebeling (1957); Backus
and Barnes (1957); Johnson, Backus, Hersey and Owen (1956) and Barham (1957)) indicate that
bathypelagic species, particularly those with swimbladders, are a conspicuous constituent of these
layers. Furthermore, it seems likely that the most prominent of the fish sound-scatterers will prove
to be myctophids. Clearly, when surer identification becomes possible, echo-sounders will provide
the biologist with a valuable record of these changing events.

In conclusion, a beginning has been made on observing vertical migrations from bathyscaphes.
After dives off Villefranche, Tregouboff (1958) wrote as follows: 'La plongee de nuit a permis
egalement d'observer la migration nocturne vers la surface de divers autres animaux, tels que les
Crevettes Euphausiaces, lesquelles, ayant quitte leur zone habituelle de 500 m. de profondeur environ,
ont apparu en nombre a partir de 100 m. de profondeur. A leur cote chassaient activement, egale-
ment a ce niveau, des petits Argyropelecus, qui se sont maintenus aussi nombreux jusqu'a 250 m.,
tandis qu'au jour on ne les capture au filet fermant qu'a partir d'au moins de 500 m. Enfin, des petits
Myctophidae et quelques Cyclothone ont effectue egalement un deplacement notable vers la surface
et se sont montres, surtout les premiers, en grande quantite deja entre 200 et 300 m. de profondeur.'

The evidence to be got from nets, sound exploration and bathyscaphes also suggests that the
vertical migrations of deep-water fishes differ in extent. However, these findings will best be left
until the third part of this section, when the physical problems facing fishes as they move up and
down will be considered.

The physical and biological environment

The headquarters of bathypelagic fishes are in the tropical and temperate parts of the ocean. They live
below the mixed surface zone, which contains all or the greater part of the actively assimilating
phytoplankton, and has an average depth of about 75 m. The lower limit of this zone is marked by
a distinct thermocline, which tends to be permanent in subtropical and tropical regions, but is seasonal
in temperate waters. Temperatures range from about io° to 300 C. and salinities from about 32 %0
to4i%0.

Below this thermocline comes a transition zone separating the surface mixed layer from the cold,
deep water. Iselin (1936) calls this the thermocline layer, for in the warmer parts of the ocean, the
temperature drops quite rapidly from about 200 C, its value just below the near-surface thermocline,
to about 50 C. at about 1000 m. Taking the level of the lower thermocline to be the depth at which
the rate of change of temperature is greatest, in the North Atlantic it is in this lower transition zone
that the values of dissolved oxygen begin to fall towards the minimum value. But over much of the
eastern tropical Pacific north of the equator, the fall in quantity of dissolved oxygen begins below the
upper thermocline, and a thick oxygen minimum layer (containing less than 0-25 ml./l.) is found
between depths of 100 and 1000 m. (Wooster and Cromwell, 1958). Conditions appear to be similar
over the central area of the equatorial Indian Ocean, where there is an equally thick oxygen minimum
layer (with values i-o ml./l. or less) between much the same depth-intervals (Sverdrup, Johnson and
Fleming, 1942). In the Atlantic, the lowest values (1-5 ml./l. or less) are centred at a depth of about
400 m., below the North and South Equatorial currents (Riley, 1951).

Turning to submarine light, the thermocline layer contains the twilight zone of the ocean. Using
a sensitive photomultiplier tube, Clarke and Wertheim (1956) were able to measure the penetration
of sunlight down to depths of about 600 m. in clear water off the Western North Atlantic coast.
However, the threshold of light for the eyes of many bathypelagic fishes is likely to be well below this
level (Denton and Warren, 1957).

THE PHYSICS AND BIOLOGY OF VERTICAL MIGRATIONS 87

While sunlight cannot penetrate far (if at all) below this depth, there is still light from the luminous
organs of deep-sea animals (Clarke, 1958). At depths between 1000 and 4000 m., temperatures range
from about 6° to i° C. in temperate and tropical regions, while the quantities of dissolved oxygen
are generally above 2 ml./l.

Considering now the biological structure of temperate and tropical oceanic waters, the well
illuminated surface waters (down to about 100 m.) form the living-space of the primary producers,
the phytoplankton. And, except in the tropical eastern Pacific, these upper layers (from the surface
down to about 200 m.) contain far greater quantities of zooplankton than the waters below (Jespersen,
1935 ; Vinogradov, 1955; Foxton, 1956; Zenkevitch and Birstein, 1956; Bogorov, 1958). Riley (1951)
has estimated that the total oxygen consumption and phosphate regeneration below the density
surface sigma t 26-5 (average depth 200 m.) is equivalent to a utilization of about one-tenth of the
surface production of organic matter by the plants. Thus, about nine-tenths of this organic production
will be consumed in the upper 200 m., and, compared to the average depth of the ocean, this layer is
little more than a ' surface film '-1

While the waters below 200 m. support sparse populations of zooplankton, there is good evidence
of a secondary maximum in the intermediate thermocline layer. In the western North Atlantic
Leavitt (1938) found a mid-depth maximum centred at a depth of 800 m. (there was also a lower
lying, but lesser concentration at 1600 m.). Jespersen (1935) also found a mid-water maximum of
zooplankton (at about 1000 m.) in the tropical Pacific Ocean, whereas in the north-western part it is
centred higher in the water at about 500 m. (Bogorov and Vinogradov, 1955). It would seem that
the rapid increase of density and viscosity in the thermocline layer slows down the fall of detrital
material, so that it tends to accumulate at mid-depths. Such concentrations of suspended material
will support detritus-feeding animals and their predators. As Miyake and Saruhashi (1956) have
pointed out, oxygen-minimum layers in the Atlantic and Pacific Oceans occur most frequently along
the same sigma-? surface (27-2-27-3) and are most marked in the more productive regions. However,
in the equatorial Pacific (Albatross stations III— 133, between o° and 150 N.), Jerlov (1953) found a
mid-depth maximum of suspended particles between 700 and 800 m., a level 150 m. below the centre
of the oxygen-minimum layer.

Below these rather slight mid-water concentrations, the biomass of zooplankton is small until the
bottom waters are reached. The concentration of plankton near the bottom has been repeatedly
observed from bathyscaphes (Bernard, 1955; Peres, Picard and Ruivo, 1957; Peres, 1958 and Tregou-
boff, 1958). Apart from ' microplankton ' (some of which is detritus), aggregations of larger forms,
such as euphausiids, sergestids and chaetognaths have been seen. (The observations were made in the
Atlantic (off Portugal) and in the Mediterranean at depths ranging from 600 to 2200 m. and the layer
seems to be about 100 m. in depth.) Such near-bottom concentrations of plankton are likely to be
widespread and may at least partly explain Riley's (1951) finding that the rates of oxygen consumption
near the deep-sea floor appeared to be larger than those in the main body of Atlantic deep water. At
all events, these bathyscaphe observations are a valuable contribution to deep-sea biology.

The time and effort given each day to vertical migrations by countless oceanic animals is one of the
most striking features of their biology. But the plants can only actively assimilate carbon in the
surface-waters, and the resulting marine pastures support not only the animals that occupy the same
living-space, but also those in the underlying waters. Considering the fishes, there can be little doubt
that their daily climb towards the surface is a feeding migration. In the western North Atlantic, to

1 'The autotrophic zone has a depth of 200 metres at most and includes less than 5 per cent of the volume of the ocean.
Below this zone, life depends on organic matter carried down by organisms sinking from above or by the vertical migrations
of animals back and forth between the depths'. Redfield (1958).

88 DISCOVERY REPORTS

take but one instance, it is surely significant that most deep-scattering layers are detected between
depths of 300 and 600 m., the levels between which Leavitt (1938) found minimum quantities of
zooplankton. It seems most likely that the fishes take what food they can get during the day, but have
a proper meal at night. Like the vertically migrating plankton animals, the up-and-down movements
of bathypelagic fishes must be governed by the daily rhythm of submarine illumination, a rhythm that
can readily be followed by their highly sensitive eyes. As Denton and Warren (1957) have shown,
their pure-rod retinae contain visual gold, a pigment with enhanced sensitivity for the deeper pene-
trating, blue rays from the sun.

But not every species of bathypelagic fish is able to take direct advantage of the near-surface con-
centration of food. Adults of the deeper-living pelagic fishes (Lyomeri, ceratioid angler fishes,
Cyclothone spp. etc.) are not found near the surface at night. This is also true of many species living
in the upper 1000 m. Fishes with tubular eyes (hatchet fishes, Opisthoproctus, Winteria, Scopelarchus,
Evermannella, Gigantura, etc.), are rarely, if ever, taken in nets fished close to the surface. It is thus
evident that there are different degrees of vertical migration. These may now be summarized.

A. Bathypelagic fishes migrating upward to the surface mixed layer.

These are able to cross the thermocline and have already been mentioned in the first part of this
ection (p. 85-86). Certain species of the stomiatoid families, Astronesthidae, Chauliodontidae, Melano-
stomiatidae, Stomiatidae, Idiacanthidae and Malacosteidae. Numerous species of Myctophidae.

Of the Astronesthidae, it appears that only species belonging to the genus Astronesthes cross the
upper thermocline. It is also likely that some of the myctophids (e.g. Lampadena spp.) do not reach
the surface-layer. The position regarding the smaller gonostomatids (e.g. Vinciguerria spp., Mauro-
licus spp., Ichthyococcus) is less certain. While they live for the most part in the upper 500 m. and
evidently undertake vertical migrations (Grey, 1955), the larger individuals are not often taken near
the surface at night. Perhaps they migrate to levels close below the thermocline.

B. Partial migrators of the upper 1000 m.

Cyclothone braueri (and probably C. signata), Sternoptychidae, various Myctophidae, Melamphaes
spp. Evidence for the migrations of hatchet fishes has already been given (p. 85), while Grey
(1955) has noted that Cyclothone braueri and Melamphaes spp. are taken at higher levels by night
than by day.

C. Deeper partial migrators

In the western North Atlantic diurnally migrating deep-scattering layers can be detected down to
1000 m. (Moore, 1958). This may well be near the threshold of light for the highly sensitive eyes of
deep-water fishes (see above). In discussing this problem, Clarke (1958) wrote as follows: 'A depth of
about 900 to 1000 m. would appear to be the shallowest level in clear water at which day and night
changes in illumination would be below the threshold of perception and at which daylight would
never be sufficiently strong for the inhabitants to be seen by their predators or by their prey.' Diurnal
migrations geared to submarine sunlight would thus seem to be confined to the upper 1000 m.
of the subtropical and tropical ocean. In temperate waters the threshold must be nearer
the surface.

But certain of the deeper-living fishes seem to undertake vertical migrations. Off Bermuda, Grey
(1955) found that the daytime catches of Cyclothone microdon came from nets fished between 800 and
2000 m., while at night the upper level rose to 250 m. The populations of Cyclothone pallida, Melam-
phaes microps, M. opisthopterus and M. robustus also occupied higher levels at night. It may be that

THE PHYSICS AND BIOLOGY OF VERTICAL MIGRATIONS 89

vertical migrations were confined to these individuals that were living by day above the threshold of
light. However, there is a distinct possibility that the deeper living fishes may be migrating upwards
to the mid-water concentration of plankton, which is centred at levels between 500 and 1000 m. (see
p. 87). Considering the plankton maximum at 800 m. in the western North Atlantic, this could
mean that the diurnal movements of the fishes living below this level were taking place without the
cues provided by submarine sunlight. However, it was in this area and at a depth of 900 m. that
Clarke (1958) found a maximum in the frequency of luminescent flashes from deep-sea animals.
Furthermore, Kampa and Boden (1957) have found a diurnal rhythm in the mean frequency of
flashes from animals in a sound scattering layer in the San Diego trough. The frequency was least at
midday, greatest during the twilight migration of the layer and maintained at an intermediate level
during the night. If this thythm proves to be common to all diurnally migrating, deep-scattering
layers (and these occur down to at least 800 m.), it might well be the cue for the upward migrations of
the deeper living fishes. Zenkevitch and Birstein (1956) visualize a ladder of migration extending to
very deep levels down which organic matter produced at the surface is conveyed to the greatest depths.
Perhaps luminescent light will prove to be as important as sunlight in maintaining the daily move-
ments up and down the ladder. Recently, Nichol (1958) has estimated the maximal distance at which
the light of various marine animals can be seen in seawater by eyes that can just perceive light of
i-6 x io-10^ w/cm2. In very clear water the distances vary from 6 to 170 m., and luminescent flashes
have been detected down to a depth of 3750 m. (Clarke, 1958).

PHYSICAL PROBLEMS

Against this background of their physical and biological environment, we may now turn to the
physical stresses that face a fish moving up and down in the water column. Clearly, these will depend
on the extent of its vertical displacement. In considering the migrations of fishes with swimbladders,
they may be divided as before into thermocline crossers, those that pass through the upper thermo-
cline into the surface mixed layer, and partial migrators, those that remain below the thermocline.

Thermocline-crossers
Gas secretion
While fishes are diving to their daytime levels, the pressure exerted on the swimbladder gases will
increase by 1 atmosphere for every 10 m. of the descent. An adult of one of the larger myctophids,
e.g. {Myctophum punctatum) weighs about 5 g. and the capacity of its swimbladder will be about
0-25 ml. If it moves from 10 to 300 m. and produces no gas during the descent, the volume of the
swimbladder will be compressed to 0-017 mL To inflate the sac to the requisite capacity it must
produce about 0-23 ml. gas at a pressure of 30 atmospheres or 6-9 ml. at one atmosphere, the pressure
of dissolved gases in seawater. Supposing the fish to have an oxygen consumption of 1 ml./hr., the
physical problem of secretion seems insuperable.

Using the energy of compression equation as a basis for their calculations, Kanwisher and Ebling
(1957) have considered the physiological effort needed. They take a 10-g. fish with a 0-4 ml. swim-
bladder and an oxygen consumption of 0-4 ml./hr. Assuming that one-third of the blood circulation
is available for the swimbladder and the efficiency of the secretion process is 25 per cent, they com-
pute that 33 hr. secretion would be needed to restore buoyancy after a migration from the surface
to a depth of 400 m. But judging from the movements of deep-scattering layers, the time taken for
the downward migrations would be not much more than 1 hr. and (presumably) the fish will ascend
again in about 12 hr.

9o DISCOVERY REPORTS

Perhaps the figure for the oxygen consumption is too low. Job (1955) found that a 5-g. Salvelinns
fontinalis will take up 1 ml./hr., and from his graphs the figure for a 10-g. fish would be about 1-2 ml.
But the oxygen requirements of an alpine char are not necessarily those of a lantern fish. However,
it is clear that lantern fishes are very active. Summing up his bathyscaphe observations, Peres (1958)
wrote the following concerning these fishes: 'Les individus sont presque sans cesse en mouvement,
mais dans les directions les plus variees.' Furthermore, they have a relatively large expanse of gill
surface. Using Gray's (1954) procedure, I have measured the gill-surface of two Myctophum puncta-
tum, both with a weight of about 5 g. The number of gill-lamellae per millimetre of gill-filament is
about 50 and the gill area per gram of body weight is 600-700 mm.2 Comparing this figure with those
got by Gray and those listed by Fry (1957), this lantern fish can be put among the active species with
a relatively large gill surface.1

There is a further aspect. The catches of the 'Michael Sars' led Hjort (1935) to conclude that the
twilight depths of the warm Atlantic were inhabited by a Lilliputian fauna of bathypelagic fishes.2
This is particularly true of the species with a swimbladder. The adults of most gonostomatids,
sternoptychids, Astronesthes spp., myctophids and melamphaids range between 20 and 150 mm. in
standard length and weigh from about 0-5 to io-o g.

Now the oxygen consumption of fishes does not follow the surface rule, nor is it proportionate to
weight. When the logarithm of the rate of respiration is plotted against the logarithm of weight, the
slope of the curve is less than unity (usually from o-66 to 0-9). The rate of uptake of oxygen falls
between surface-area and weight dependence (Fry, 1957).

Thus, the smaller the species, the greater its oxygen consumption per unit of body weight. This
may not mean that extra oxygen would be available for gas secretion, but coupled with the consider-
able expanse of gill surface in such fishes as the myctophids and Astronesthes spp., the idea is not to be
dismissed. At all events it is striking that the only predatory fishes with swimbladders which cross
the upper thermocline are the species of Astronesthes? and there is a marked tendency for the adults
of this genus to be smaller than those of other predatory stomiatoids (Chauliodontidae, Stomiatidae,
Melanostomiatidae, Idiacanthidae and Malacosteidae), which as we have seen, have no swimbladder.

Lastly, hydrostatic pressure has an effect on the rate of metabolism. Fontaine (1930) experimented
on Pleuronectes platessa, Ammodytes lanceolatns, Gobius minutus, and Anguilla anguilla, finding that an
increase in pressure from the atmospheric level to 100 kg. /cm.2 (1 kg./cm.2 = 0-968 atm.) enhanced
the rate of oxygen consumption by 35-88 per cent. The smaller the fish, the greater was this per-
centage increase. Using the first species, Fontaine showed that the rate of oxygen consumption
steadily rose as the pressure was increased to 125 kg./cm.2, but thereafter fell rapidly, the fish being
killed at a pressure of 150 kg./cm.2.

A myctophid or astronesthid diving to its daytime level might pass from a pressure of a few
atmospheres to one of about forty or fifty. There is thus a possibility that their rate of oxygen uptake
would tend to increase with depth. However, it is not certain that deep-water fishes would be in-
fluenced in the same way as shallow-water species, although Anguilla anguilla spends part of its life
as a deep-sea fish. The question can only be decided by comparable experiments on deep-water
species.

But even supposing that the oxygen consumption of a 10-g. deep-sea fish (say, a large myctophid)

1 Astronesthes niger, which is also a thermocline-crosser also has about 50 gill-lamellae per millimetre of gill-filament.
Argyropelecus aadeatus, presumably a partial migrator, has about 40.

2 While nets give a limited impression of the size range of a species, bathyscaphe observations do not controvert Hjort's
view.

3 Astronesthes spp. seem to have a decided liking for myctophids (Murray and Hjort, 1912; Beebe and Vander Pyl, 1944).

THE PHYSICS AND BIOLOGY OF VERTICAL MIGRATIONS 91

is three times the value taken by Kanwisher and Ebling (1957), the gas secretion time for a downward
migration of 100 m. would still be 11 hr. At this rate the fish could just restore its buoyancy to the
neutral level between the daily descent and ascent.1 Moreover, it seems unlikely that the gland could
produce oxygen fast enough to keep pace with the increasing pressure during the descent. A striking
proof of this may well have been given by Hersey and Backus (1954). While following a descending
deep-scattering layer they found that the resonant frequency of the reflected sound increased, as
though elements in the nature of gas-bubbles were being compressed. As they remark, the bubbles
were probably the swimbladders of fishes.

But if the cells of the gas-gland are able to store oxygen in a combined form, the task of restoring
buoyancy would be quickened. As we have seen (pp. 73-75), the gland is highly developed in comparison
with the volume of the swimbladder. If, by this means, buoyancy can be regained a few hours after
the descent, the remaining hours before the ascent could be given to storing oxygen in the gland. If
the cells have not reached saturation level by the time the fish is ready to ascend, it may be that some
oxygen could be transported to them during the early part of the climb. Deep-scattering layers are
known to rise quite slowly for several hours before sunset (see Clarke and Backus, 1956). During this
time the (relative) reduction in pressure could be tolerated without the resorptive part of the swim-
bladder being brought into play (see pp. 96-97). Thus, while the gland would not be secreting it could be
storing oxygen. These considerations are at least in keeping with present conceptions of gas-pro-
duction. Scholander (1954) is inclined to think that oxygen in compound form may be stored in the
gland-cells for intermittent use.

The oxygen secreted into the swimbladder comes from the water passing over the gills. How does
a fish obtain enough oxygen if it lives in an oxygen minimum layer during the daytime ? To take an
extreme instance, and one already cited (p. 86), the oxygen level is below 0-25 ml./l. between depths
of 100 and 1000 m. in the eastern tropical Pacific, north of the Equator. It is here that Beebe and
Vander Pyl (1944) investigated the diurnal migrations of myctophids.

Thus, apart from the upper 100 m., the waters in this part of the ocean would seem to contain
insufficient oxygen for active metabolism. (At 200 C. the oxygen consumption of the goldfish, a
tolerant species, starts to fall below an oxygen content of 2-5 mg./l. (= 1-75 ml./l.) (Fry and Hart,
1948).) Apart from the other bodily processes, the maintenance of an oxygen pressure of 40 atmo-
spheres in the swimbladder would be against a diffusion gradient of about 10,000 to 1 (Kanwisher
and Ebeling, 1957). This seems a gigantic task.

Active life for fishes in this oxygen minimum layer would seem to pose a physiological dilemma.
They would have to work very hard to get enough oxygen and the more active they were, the more
oxygen would be required. To consume 0-5 ml. 02 per hour, a lantern fish or Astronesthes would have
to pass at least 3 1. of seawater over its gills (assuming that two-thirds of the dissolved oxygen would
be taken up by the blood). A fish with a volume of, say 5 ml. would not be capable of pumping 1 ml.
of seawater over its gills in a second, or even half this volume. In trout (volume about 900 ml.) Van
Dam (1938) found the maximum ventilation-volume to be about 5 ml. /sec.

Perhaps the activity of these fishes is largely suspended during the day. It was in the Eastern
Tropical Pacific that a single haul of a mid-water trawl yielded over 5000 fishes, most of which were
the small lantern fish, Diogenichthys scofieldi (Marshall, 1954). This is a phenomenal catch and one is
led to wonder whether it might be due to reduced activity. Lantern fishes are not known to concen-
trate in great numbers in dense schools nor are they easy to catch. Daytime observations from a
bathyscaphe might well be revealing.

1 There is, of course, no certain evidence that the vertical migrations of any particular individual are carried out day after
day. In an adult fish the extent of these displacements may also vary in time and space.

92 DISCOVERY REPORTS

If the activities of these fishes are largely confined to night time, when they are swimming in the
well-oxygenated surface waters, it is difficult to see how enough oxygen can be obtained to fill their
swimbladders. Use of the gas-gland as an oxygen store would seem to be essential for such fishes.
The problem (a most intriguing one), remains.

Gas resorption

During its daily climb towards the surface, a deep-sea fish must lose gas from its swimbladder as the
hydrostatic pressure is reduced. While the physical problem is simply the converse of that faced
during descent, it is a more critical one. Being overweight is presumably no handicap to a diving
fish, but during the rise the swimbladder must be kept from exceeding the volume necessary for
neutral buoyancy. If this is not done, the fish will lose control and start to ' balloon ' upwards to the
surface at an ever-increasing rate. Even predatory fishes without a swimbladder are not entirely free
from this problem. Gunther (1887) relates how Johnson found a gulper-eel (Saccopharynx ampul-
laceus) floating at the surface. The fish had swallowed a nine-inch, deep-sea gadoid (Halargyreus)
' . . . the stomach of which was forced up into the mouth by the distended air bladder, showing how
rapidly both fishes must have ascended to the surface '.

As we have seen, most of the migrating fishes with swimbladders weigh between 0-5 and 10 g.
Considering once more a 5-g. fish with a swimbladder volume of 0-25 ml., a migration from a depth
of 400-50 m. will cause the sac to expand to about 2-0 ml. if no gas is lost. So during the ascent, about
1-75 ml. gas, the greater part of which will be oxygen, must disappear into the blood.

Such problems have been considered by Jones (1951, 1952) and are based on experiments with
perch (Perca fluviatilis), which, like the deep-sea fishes with swimbladders is a physoclist. Jones (1952)
has calculated that a migration from 500 to 100 m. by a physoclist should extend over 34 hr. if the
swimbladder is to be kept at the volume of neutral buoyancy. He suggests the difficulty could be
overcome if the fish had a small swimbladder (the extra space being filled with fat), or thick, pressure-
resisting walls bounding the sac, or if the rate of resorption is 20-30 times that supposed in the perch.

Considering these suggestions, the deep-sea fishes have a reduced swimbladder (compared to the
perch) in that they live in a denser medium and so need less buoyant support. In freshwater fishes,
the volume of the swimbladder is 8 per cent of the body volume (see Jones and Marshall, 1953).
Moreover, the walls of their swimbladders are quite thin (see pp. 60-65). The rate of removal of gas
from the sac must thus be high.

The quantity of gas diffusing into a capillary bed will directly depend on: (1) the area of the bed;
(2) the rate of flow of blood; (3) the concentration gradient (the difference in tension between the
swimbladder gases and those in the blood; (4) temperature. The rate of diffusion will also be inversely
related to a ' frictional ' component, the thickness and nature of the tissue through which the gases
move, and on the size of the gas molecules.1

The Lilliputian fauna of bathypelagic fishes have decidedly large expanses of capillaries relative to
the volumes of their swimbladders (see the descriptive section, pp. 7-50). In Table 6 this is expressed
as a ratio of surface of resorbent area : volume of swimbladder. The swimbladder volume is taken to
be 5 per cent of the body volume. The surface-area of an ' oval ' is readily calculated (but is a minimal
value owing to some collapse of the swimbladder) since it is circular. In the stomiatoid fishes the
area of the capillary bed was got by dividing it into convenient sub-areas. This will also be a minimal
value.

1 Fick's law for diffusion processes is expressed thus: y- = — ^> a -=- , where dn is the amount of substance diffusing

across an area a, in time dt, dcjdx is the concentration gradient, R is the gas constant, T the absolute temperature, / the
'frictional resistance' and N the Avogadro number.

THE PHYSICS AND BIOLOGY OF VERTICAL MIGRATIONS

Table 6. Resorbent surface-area : swimbladder volume ratios in various

bathy pelagic fishes

Area of

Resorbent

resorbent

Volume of

area. -volume

surface

swimbladder

ratio of

Species (standard length mm.)

(mm.2)

(ml.)

swimbladder

Stomiatoidea

Vinciguerria attenuata (43 -5)

ca. 0-08

250

Maurolicus muelleri (22-0)

1-2

o-oi

120

Argyropelecus aculeatus (48-0)

9-0

0-06

150

Astronesthes niger (41 0)

15-0

0-05

300

Myctophidae

An oval

Diaphns rafinesquei (70-0)

3°

0-30

100

Myctophum punctatum (7 1 -o)

0-25

100

Melamphaidae

An oval

Melamphaes mizolepis (56-0)

0-07

115

These ratios are higher than that found in the perch (using Saupe's (1939) figure for the area of the
oval). The two myctophids, the melamphaid and Maurolicus have ratios that are at least twice as
large as that of the perch. In Vinciguerria and Astronesthes this factor is 4 and 5 respectively.
' Clearly, the concentration gradient in these fishes will be much higher than that ever existing in the
perch. At a depth of 500 m. the partial pressure of oxygen in the swimbladder will be some 40
atmospheres, a tension several hundred times greater than that in the blood flowing through the
capillary bed. This would indicate that the rate of oxygen removal would be limited by the rate at
which blood could flow through the resorbent area.

Now, in myctophids the vein or veins leading from the oval to the cardinal vein are extremely
large. Furthermore, the by-pass vessel (or vessels) from the retial artery to the oval can take all the
blood that would flow through the retia during gas-secretion. Text-fig. 39 shows two large veins
from the oval of Myctophum punctatum, and they unite to form a single vessel running to the cardinal
vein. In the stomiatoids the resorbent surface is also fed with blood through a by-pass of the retial
artery while the venous return is through the venous capillaries of the rete (see pp. 78-79).
However, the retial flow will not be a limiting factor, which may be seen by using Poiseuilles'
law. For a series of n parallel tubes the resistance to the flow of blood will be proportional to :

(Length of a tube)

(Number of tubes) > (Diameter of tube)4

Using the figures for the diameter and length of the venous capillaries, and for the by-pass artery
and other vessels involved in the capillary bed, it can be shown that the retial capillaries have less
resistance than that developed in the larger vessels. It would thus seem that the resorbent vascular
system in both stomiatoids and myctophids will carry relatively large amounts of blood over a
given time.

Temperature will also play a part, though a small one, in accelerating the diffusion of gas into the
capillary bed. In the subtropical and tropical ocean, a fish migrating from a depth of 500 m. to the
surface will pass from temperatures of about 8-1 8° C. to those ranging from 20 to 300 C. Thus over
wide areas of the warm ocean the rise in temperature is io° C. or more. However, in terms of absolute
temperature the percentage increase in diffusion rate in passing from io° to 250 C. is less than
10 per cent.1

1 Taking the rate at 20° C. as unity, the value of the diffusion constant rises 1 per cent per degree (Prosser et al. 1950).

94 DISCOVERY REPORTS

Finally the ' frictional resistance ' must be very small in the resorbent areas of these fishes. The
capillary bed is very close to the gases of the swimbladder (Text-fig. 40), the intervening connective
tissue being no more than 1/1 in thickness (judging from transverse sections).

Considering only the fishes that are known to cross the near-surface thermocline, the preceding
discussion could well indicate that their rate of gas resorption is 20-30 times that of the perch. They
have a factor of 2-5 in their favour in resorbent surface volume of swimbladder ratio, and a factor
many times this related to the concentration gradient of gas. The unknown factor is the amount of
blood the resorbent surface can handle in a given time. However, judging by the ascent of deep-
scattering layers (Clarke and Backus, 1956), the time taken to reach the surface (including the slow
rise before sunset) is at least 2 hr.

Text-fig. 39. Venous part of the circulation to the oval in Myctophum punctatum ( x 15). Note the size of the oval veins
relative to the retial vein, ov, oval ; ra, retial artery ; rv, retial vein ; rm, rete mirabile ; vov, veins to oval.

lumen of swimbladder

Text-fig. 40. Part of the resorbent capillary network of the swimbladder of Argyropelecus aculeatus. Note the very
thin layer of tissue separating the capillaries from the lumen of the swimbladder.

Partial migrators

Gas secretion

During their vertical migrations, fishes that do not penetrate beyond the upper thermocline will be
subjected to lesser physical stress than those that go on to the surface mixed layer. A hatchet fish
migrating from a depth of 150 to 400 m. is not faced with providing as much oxygen for the swim-
bladder as a lantern fish moving from 20 to 400 m. However, as we have seen (pp. 74-75) the rete
and gas-gland of a hatchet fish swimbladder are highly developed, seemingly as well as those of a
lantern fish. In view of the earlier discussion concerning gas-production in thermocline-crossers,
this aspect need not be pursued at greater length.

THE PHYSICS AND BIOLOGY OF VERTICAL MIGRATIONS 95

Gas resorption

During its upward migration, the pressure on the same hatchet fish will be reduced by about 60 per
cent ; the figure for the lantern fish is about 90 per cent. It seems odd that the resorbent surface : swim-
bladder volume ratio of the hatchet fish Argyropelecus aculeatiis is greater than the values for the two
lantern fishes (see Table 6). But as already suggested, the figures for the two lantern fish in Table 6
are likely to be low. If the radius of their 'ovals' was actually 4 mm. instead of 3 mm., which may
well be under natural conditions, the ratios would be about 170 instead of 100. For it is a striking
fact that lantern fishes brought up in nets hardly ever have the viscera pushed into the mouth by
extra expansion of the swimbladder, whereas this is not uncommon in hatchet fishes. It is also
interesting that Astronesthes niger, which appears near the surface by night, has a much higher ratio
than Argyropelecus aculeatus, a partial migrator.

PELAGIC AND BENTHIC FISHES, THE SWIMBLADDER, AND
ASPECTS OF THE ECONOMY OF DEEP-SEA LIFE

There is a far-reaching correlation between the focal depths of the living-space and the presence or
absence of a swimbladder in fishes from the mid-waters of the ocean (pp. 82-83). While a highly
developed, gas-filled swimbladder is found in about half the species that swim in the upper reaches
(200-1000 m.) of this environment, this organ is absent or regressed in all fishes with populations
centred below the 1000-m. level. Is such a relationship with depth also found in fishes living on or
near the deep-sea floor ? The surprising fact, as already indicated, is that much of the answer is in
the negative.

The main families to be considered are the Alepocephalidae, Bathypteroidae, Harpadontidae,
Ipnopidae, Synaphobranchidae*, Halosauridae,* Notacanthidae*, Moridae*, Macrouridae*, Zoar-
cidae, Brotulidae*, and Liparidae. In the families marked with an asterisk, a swimbladder is com-
monly present, but is absent in the others. Using Grey's (1956) list of species that are found below
a depth of 2000 m., at least half of a total of some 240 species should have swimbladders.

Before giving special consideration to those species that range into the deeper, abyssal parts of the
ocean, appreciation is due to observers in bathyscaphes and to underwater photography. Until these
records were available, there was always the possibility that some of the supposedly benthic fishes
might not live near the bottom. Hjort (Murray and Hjort, 1912), believed that the Bathypteroidae
were mid-water fishes, but they have now been seen actually resting on the bottom, supported by the
two long pectoral rays and the single, elongated caudal ray (Houot and Willm, 1955). Representatives
of the Halosauridae, Moridae, Macrouridae and Brotulidae have also been observed near the bottom
(Fages et al. 1958; Peres, Picard and Ruivo, 1957). I have seen halosaurid, notacanthid and morid
fishes in photographs of the deep-sea floor taken by Dr A. S. Laughton of the National Institute
of Oceanography.

Nybelin (1957) has listed the species that have been fished below a depth of 3000 m. There are
sixty-eight. (Alepocephalidae (7), Harpadontidae (2), Bathypteroidae (3), Ipnopidae (3), Synapho-
branchidae (3), Halosauridae (2), Notacanthidae (1), Macrouridae (16), Zoarcidae (1), Lycodidae (2),
Brotulidae (25), Liparidae (3).) Thus forty-seven species may at least be suspected of having swim-
bladders.

However, there is the possibility that the deeper living species might have lost this organ. Yet
Giinther (1887) found a swimbladder in Typhlonus nasus, taken by the 'Challenger' at depths of
3934 and 4465 m., and in Acanthonus spinifer, trawled at 3242 m. Besides these two brotulids, a

96 DISCOVERY REPORTS

swimbladder is found in the deep-sea eel Synaphobranchus kaupi (= S. pinnatus) (Scholander and
Van Dam, 1954) (depth range: 200-3599 m-) and in tne macrourid, Nematonurus armatas (Hagman,
1921) (281 to 4600 m.). 'At least forty-six of the more than seventy-six specimens recorded were
caught between about 2600 and 3660 m.' (Grey, 1956).

In view of these findings I have examined the following species, the depth range1 of which appears
after the scientific name: Moridae, Antimora rostrata (403-2904 m.); Macrouridae, Lionurus filicauda
(2515-4846 m.); Brotulidae, Aphyonus gelatinosus (2550-4360 m.); Typhlonus nasus (3932-5090 m.);
Mixonus laticeps (3200-4575 m.); Bassozetus taenia (4575-5610 m.) and Bassozetus compressus
(1920-2744 m.). Except in Aphyonus gelatinosus and Typhlonus nasus, each of these species has a
capacious swimbladder extending down the greater part of the body cavity. Drawings of some of
them appear in Text-fig. 41.

Thus a well-developed swimbladder is present in fishes that may range down to depths of about
5000 m. This is remarkable in view of the previous discussion concerning the compressibility of
gases (p. 84). At a depth of 5000 m. the density of oxygen is about seven-tenths that of
seawater.

A fish with a fully developed swimbladder containing oxygen would require tissues with a density
of about 1 -04 to be neutrally buoyant at this depth. But this requirement may well be met. These
deeper-living fishes have rather lightly ossified skeletons and the muscles sheathing their flanks are
fairly thin. In PI. 3 a radiograph of Lionurus filicauda is shown against one of the poor cod, Trisopterus
minutus, a shallow-water fish. It will be seen that the skeleton of the cod is more sharply revealed
than that of the macrourid:2 there is also a striking difference in the size of the otoliths. Denton and
Marshall (1958) have shown that the density of fish muscle is relatively high, which is not surprising
in view of the heavy protein molecules that are required for contraction. In bathypelagic fishes
without a gas-filled swimbladder, reduction of muscle and bone can bring the animals close to neutral
buoyancy.

The swimbladders of these fishes are also remarkable in having extremely long retia mirabilia
(see Text-fig. 41). In Lionurus filicauda there are six retia, each having a length of at least 20 mm. The
two retia of Bassozetus taenia are about 25 mm. long, while the single one of B. compressus has a
length of 17-5 mm. In the deep-sea eel, Synaphobranchus kaupi, the span of the rete is about 10 mm.
(Scholander, 1954).

These findings are surely significant in view of the previous discussion on retial length and the
efficiency of gaseous exchange between the arterial and venous capillaries (pp. 70-72). As we saw, the
deeper the living-space the longer should be the length of the capillaries. This is strikingly revealed
in Table 7. (The data for Antimora viola, blue hake; Sebastes marinus, rose fish; Nezmnia bairdii,
common rat-fish; and Synaphobranchus kaupi are taken from Scholander and van Dam (1954) and
Scholander (1954).)

Apart from the general trend, which is quite evident, it is interesting that the deeper living of the
two Bassozetus species has the longer retia, and two in place of one. Here, then, is indication that the
swimbladders of abyssal fishes may well be functional at great depths.

But the gas-glands do not appear to be highly developed, which might suggest that their function
is simply to keep the swimbladder ' topped up ' with gas. Abyssal fishes are unlikely to move very far
from the deep-sea floor, except perhaps during the breeding season, although they could have a
relatively wide freedom of movement in the vertical plane. If the upper limit of this zone is marked
by a pressure reduction of 20 per cent (Jones, 1952), an abyssal fish with a closed swimbladder and in

1 Depth-range data have been taken from Grey (1956), Nybelin (1957) and Bruun et al. (1956).

2 The 'Challenger' fishes were preserved in alcohol so there is no danger of the degree of ossification being reduced.

PELAGIC AND BENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP-SEA LIFE 97

hydrostatic equilibrium at a depth of 4000 m., could swim upwards for 800 m. without the need to
lose gas. When it descended there would be no extra gas to find.

These abyssal fishes have not retained their swimbladders simply to solve problems in the second
law of thermodynamics. A fish with a swimbladder is able to remain poised off the bottom without
undue effort and it can thus devote a greater part of its energy to seeking its food. If a near-bottom

Text-fig. 41 . Swimbladders of (a) Bassozetus taenia ; (b) B. compressus ; (c) Antimora rostratus ; (d) Lionurus filicauda ; (e) Argy-
ropelecus aculeatus. In the two species of Bassozetus and Lionurus filicauda, note the extremely long retia mirabilia, which may
be compared with the rete of Argyropelecus. Note also the capillary loops in the gas gland of Bassozetus compressus. gg, gas-
gland ; rm, rete mirabile. (a, x 3-6 ; B, x 3 ; c, x 0-7 ; D, x 3 ; E, x 3.)

13 DM

98 DISCOVERY REPORTS

Table 7. Length of retia and the depth range of some deep-sea fishes

Fishes

Depth range (m.)

Length of retia (mm.)

Number of retia

Bathypelagic species

Stomiatoidea

200-1000

075- 4-0

Myctophidea

(centres of concentration)

1-5 - 4-0

Benthic species

Sebastes marinus

30-1680

7-0 -io-o

Antimora viola

560-1830

7-0 -IO'O

Stephanoberyx monae

-2295

8-o

Nezumia bairdii

140-2300

7-0 -13-0

Bassozetus compressus

-2744

17-5

Synaphobranchus kaupi

200-3599

1 o-o

1 ?

Lionurtis filicauda

25 J 5-4846

20-0*

Bassozetus taenia

4575-5610

25-0

concentration of plankton is also found over the abyssal plain, such a fish could take full advantage
of this food as well as that on and in the sediments. Macrourids plough up the oozes, no doubt in
search of food, and they also take planktonic forms such as euphausiids, sergestids and copepods
(Marshall, 1954). Bathypteroid fishes, which have no swimbladder and come to rest on the oozes
after swimming, may be more limited in their choice. A radiograph of one of these fishes showed the
skeleton to be well ossified and, as the myotomes are compact and well-developed, they are un-
doubtedly heavier than their environment, which as Jones and Marshall (1953) point out, is no
handicap to a fish living on the bottom. But the more striking fact is that about two-thirds of the
fishes that range below 3000 m. have swimbladders.

Besides its buoyant effect, the swimbladder can also be used to produce sounds. Certain species of
macrourids have special drumming muscles attached to the swimbladder, but sounds can be made
without such aid (Marshall, 1954). The gas-filled sac may act as a resonator to enhance the noises
produced by neighbouring structures, such as the grinding of the pharyngeal teeth. In the abyssal
darkness, sounds might be vitally important for communication between the sexes during the breeding
season. After studying certain sounds recorded in deep water, which were like those made by fishes,
Griffin (1955) suggested that the 'fish' might use the sounds for echolocation of the bottom. His
concluding remarks are interesting : ' Finally it must be pointed out that even though this recording
does reveal a fish-call plus its echo from the bottom, we have no direct evidence that the unknown fish
could hear such an echo, and still less that it would pay any attention if it did. Yet the "echo-fish"
could easily have heard these bottom echoes if it had an auditory sensitivity equal to that of any fish
adequately studied to date, and in the unlighted depths of the ocean echolocation could be as advan-
tageous to a fish as it is to a bat flying in darkness through the air.'

By becoming closely associated with the inner ears the swimbladder can also act as a hydrophone.
Such association is known in one group of benthic deep-sea fishes, the Moridae, (Svetovidov, 1948)
a family containing about seventy species. In other fishes a connection between the ears and swim-
bladder is correlated with a wide frequency range and low auditory threshold (Jones and Marshall,
1953). At present we can only add that the deep ocean is by no means a silent world.

It must now be evident that there is a striking difference between the development of the swim-
bladder in the pelagic and benthic fishes of the deep ocean. Taking a vertical section over the deep-sea
floor between depths of 2000 and 5000 m., at least half of the pelagic fishes with centres of concen-
tration in the upper reaches (between 200 and 1000 m.) have capacious swimbladders and the same
is true of the bottom-dwelling species. But this organ is regressed or absent in the pelagic fishes living
in the intervening waters below the 1000-m. level.

PELAGIC AND BENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP-SEA LIFE 99

The evidence suggests that the swimbladder is perfectly functional in benthic species ranging
beyond a depth of 2000 m. Why has this organ been lost in the deeper-dwelling pelagic fishes?

There are many differences between fishes living in the upper and lower reaches of the pelagic
environment. Clearly, the most relevant contrasts may be made within genera consisting of species
that inhabit both regions. Gonostoma is one such genus, and here G. denudatum will be contrasted
with G. bathyphilum.

The populations of the first species are centred above 1000 m., while those of the second are con-
centrated well below this level. Certain differences between these species have already been con-
sidered (Marshall, 1954, 1955; Denton and Marshall, 1958).

Gonostoma denudatum has a capacious, gas-filled swimbladder, but there is no trace of this organ
in bathyphilum (p. 13). Radiographs of the two fishes show the skeleton of the first species to be
more heavily ossified than that of the second. Furthermore, the flanks of denudatum are sheathed
with well-formed scales, while the skin of bathyphilum is naked. Correlated with the firmer skeleton,
the myotomes of denudatum are more compact and extensive than those of bathyphilum. This is
particularly evident along the post-anal part of the body, which is slimmer and less robust in bathy-
philum (see Text-fig. 42).

By comparison with bathyphilum, the eyes and light organs of denudatum are highly developed. In
fishes of the same size, the diameter of the eye in the former is rather less than half that of the latter,
and there is a striking difference in the relative development of the dioptric parts (Marshall, 1954).
Reference to Text-fig. 42 will show the extraordinary contrast in the size of the photophores.

Having proportionately larger eyes, it is not surprising that denudatum has larger optic lobes. But
this difference in emphasis extends to all parts of the brain (see Text-fig. 42). Particular attention may
be drawn to the corpus cerebellum, the volume of which in denudatum is about double that of bathy-
philum (Text-fig. 42). Now there seems to be a direct correlation between the degree of development
of this nervous centre and locomotor activity (see Healey, 1957; Kurepina and Pavolovsky, 1946),
which would suggest that G. denudatum is the more active species. As we have seen, the myotomes
of this species are better developed.

Parallel differences are also found in the gill-system. In G. denudatum the four gill-arches bear
filaments along their entire length. In the specimen drawn in Text-fig. 42 the average length of the
filaments on the second arch is about 2 mm., and there are some six filaments to each millimetre of
the arch. The filaments bear about 60 lamellae per millimetre.

Conditions are very different in G. bathyphilum. On the first gill-arch the filaments are confined to
the forward part of the lower arm, while on the other arches they occur along the entire extent of the
lower arms. The filaments are short and feathery (about 1 mm. long and three or four per millimetre
along the second arch). The number of lamellae on a i-mm. filament is about 20-25. While there is
the possibility that the skin of G. bathyphilum, being scaleless, might assist in respiration, there is
striking indication that the tissues are much regressed by comparison with those of G. denudatum.

Finally, this economy of living substance in bathyphilum is also revealed in the size of the kidneys,
which in Gonostoma consist of paired anterior parts joined by thin bridges of tissue to an unpaired
posterior part. Comparison of a G. bathyphilum (standard length 77-5 mm.) with a G. denudatum
(standard length 81-5 mm.) showed that the kidneys of the latter have a more compact appearance
and are much larger than those of the latter. (The anterior parts in both species have much the same
length (7-0 mm.) but those of denudatum are more voluminous. The posterior parts of the kidneys of
denudatum are larger by a factor of about three.)

Now in teleosts the simpler products of catabolism (ammonia and urea) tend to be excreted by the
gills, while the more complex products (creatine, creatinine and uric acid) are dealt with by the

13-2

IOO

DISCOVERY REPORTS

kidneys. But as both gills and kidneys in bathyphilum are greatly reduced, there can be little doubt
that denudatum is the more highly organized and active species.

The species of Cyclothone also live at different levels in the ocean. C. braueri, a light-coloured
species, occurs mainly between 500 and 1000 m., while the populations of the black species (livida,

• • • B

Text-fig. 42. Comparison of the external appearance, gill development and brain of Gonostoma denudatum atlantkum (a a', a")
and G. bathyphilum (b, b\ b""). The gill filaments shown in (a') and (b') are from the second gill arch, fb, forebrain; mb, m.d-
brain; cb, cerebellum, (a and B, X075; a' and b', x 12-5; a" and b", x 5.)

PELAGIC AND BENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP-SEA LIFE 101

microdon, acclinidens and obscura) are centred at levels of iooo m. and below. Of the forty-four
recorded specimens of obscura, only three came from nets fished above a depth of 2000 m. (Grey,
1956), while C. microdon is common between levels of 1000 and 2000 m. (Murray and Hjort, 1912).
We may thus compare the three species braueri, microdon and obscura, as they seem to occur at
increasingly deeper levels.

During the larval phase, which is passed in the surface waters, a gas-filled swimbladder is present
in the species braueri and microdon, but the organ regresses and becomes invested with fat after
metamorphosis (pp. 65-66). Knowledge of the life-history of obscura matches its trivial name.

C. braueri and C. microdon grow to about the same size (70 mm.), but there is some evidence that
the regression of the swimbladder occurs at a later stage in the former. At a length of from 30 to
35 mm., the swimbladder of braueri is beginning to regress but a cavity is still present, while in
C. microdon of this size regression is almost or quite complete.

Besides this difference, which requires closer study, the degree of development of the eyes and
light-organs forms a graded series in the three species. This was first appreciated by Brauer (1908) and
also considered by Hjort (Murray and Hjort, 1912).1 It will be seen that the eyes are largest in
braueri, as compared with microdon, which has medium-sized eyes, while those of obscura are extremely
small. The same is true of the photophores. It should be added that Brauer regarded the light organs
of C. obscura to be rudimentary and found some of them to be absent.

Having no specimens of C. obscura, I have only been able to compare the brains of braueri and
microdon, which came from individuals of about the same size (25 mm.). Drawings of these appear in
Text-fig. 43. Measured from the tip of the forebrain to the end of the cerebellum, both brains have
much the same length (2-0 mm.). But the optic lobes and, evidently, the cerebellum of braueri, are
considerably larger, the width of the former being i-i mm. in braueri and 07 mm. in microdon.

Comparison of the gill-system of these two specimens is also revealing. In both species, filaments
are borne on the lower arms of the first, second and fourth arches, but on only the forward half of
this part of the third arch. In C. braueri the filaments are both larger and more numerous, there being
12 per mm. on the first arch, compared to nine in microdon. Reference to Text-fig. 43 will show the
difference in filament size.

To summarize, in these three species of Cyclothone, the deeper the living-space, the less the develop-
ment of the eyes, photophores, brain and gills. Since the greater part of the populations of C. braueri
live above the threshold of light, while both microdon and obscura are most common below this level,
the relatively large eyes and photophores of braueri might seem to be related to an existence in the
twilight zone. But this factor cannot be invoked to account for the marked difference in eye and
photophore development of microdon and obscura. Some factor (or factors) related to the deeper
living-space of obscura would seem to be involved.

To conclude these studies of related fishes, two species of the family Gonostomatidae will be con-
sidered, Maurolicus muelleri and Cyclothone microdon. Maurolicus is most abundant above a level of
500 m. (Koefoed, 1958) while C. microdon, as already indicated, is mostly to be found below 1000 m.
The first species has a well-developed gas-filled swimbladder, while in Cyclothone this organ is
obliterated in the adult phase.

Drawings of these two fishes may be found in Text-fig. 44. The much greater development of the
eyes and light-organs of Maurolicus will be immediately obvious. The myotomes of this fish are also
much more compact and extensive. In a well-nourished Cyclothone microdon, the myotomes appear
at first sight to be more voluminous than they actually are. Much of the space between the skin and

The species that Brauer took to be Cyclothone signata Garman proved to be a separate species, which was called
C. braueri, by Jespersen and Taning (1926).

DISCOVERY REPORTS

Text-fig. 43. The development of the body muscles, gill filaments and brain of (a, a', a") Maurolicus muelleri; (Bb, Bbb)
Cyclothone braueri, and (b, Bm, Bbm) C. microdon. In A and B, which are transverse sections through the body just in front
of the caudal peduncle, the muscle fibres are shown in black and are drawn to scale. The drawings of the gill filaments
are from the lower part of the first gill arch, fb, forebrain; mb, midbrain; cb, cerebellum, (a, b, x 15; a', Bm, Bb, X20;
a", Bbb, Bbm, x 9.)

PELAGIC AND BENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP-SEA LIFE 103
myotomes is taken up by extensive fat sinuses, which are especially capacious along the back between
the head and the dorsal fin. Subcutaneous fat sinuses also occur between the pelvic and anal fins,
between the muscles moving the dorsal and anal rays, and above and below the caudal peduncle.
The drawing of the fish in Text-fig. 44 B is actually of the closely related species, C. pallida, in which
the lack of pigment in the skin makes the sinuses easier to trace.

nnrvY

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Text-fig. 44. External appearance of (a) Maurolicus muelleri; (b) Cyclothone pallida. Both, x 3.

Reference to Text-fig. 43 will show that the brain of Maurolicus is large compared to that of
Cyclothone microdon. (The standard lengths of the two fishes measured 35-0 and 36-5 mm. in the
order just given.) This is even more true of the gill surface. On the lower part of the first gill arch of
Maurolicus, the filaments have an average length of 1-5 mm. and there are 5 per mm. The number of
lamellae per millimetre of filament is about 50. The first two corresponding figures for Cyclothone
microdon are 0-2 mm. and 7 per mm. Once more there is ample evidence that the species from the
upper mid-waters is the more highly organized and active fish.

Apart from the greater development of the myotomes in Maurolicus, there is a striking difference in
the nature and composition of the muscle, which may be seen in Text-fig. 43. The drawings are of
cross-sections taken just in front of the caudal peduncle. Here the myotomes of Cyclothone microdon
are formed of one type of large muscle fibre, each with a diameter of about o-i mm. Maurolicus has
two types of muscle fibre. The inner parts of the myotomes consist of fibres with about half the
diameter of those of Cyclothone, while those forming the outer parts are about half as small again.
These latter are presumably red fibres.1 As the cross-sectional area of the inner parts alone is about
equal to the corresponding area of myotomes in C. microdon, it will be seen how much finer in texture
are the muscles of Maurolicus. Study of the density of the fibrils in the muscle fibres of these two
species would be of interest.

1 Red muscle also forms a considerable part of the myotomes of the tunny-like fishes (Kishinouye, 1923), which are the
most active of all teleosts.

io4

DISCOVERY REPORTS

It will now be clear that the body-tissues of Cyclothone are much reduced by comparison with those
of Maurolicus. A striking indication of the reduced economy of life in Cyclothone is (again) found in
the form of the kidneys, which have been studied by Owen (1938). One of his drawings is reproduced
in Text-fig. 45. The entire system consists of two tubules only,
which run side by side down the body-cavity and unite at the
bladder. This must surely be one of the simplest kidneys in
any adult fish of this size. In Maurolicus the kidneys are much
more voluminous and have a compact appearance like those of
shallow-water teleosts.

These detailed studies of related species may now be used
as a guide (see Table 8) to a more general survey of the
pelagic fishes living in the upper and lower reaches of the
deep-sea. Here the fishes with swimbladders, species belonging
to the families Gonostomatidae, Sternoptychidae, Astronesth-
idae and Myctophidae and having centres of concentration
between depths of about 200 and 1000 m. will be compared
with those of the groups Lyomeri and Ceratioidea, which have
no swimbladder and are most common well below the 1000-m.
level.

When these two assemblages are contrasted, the differences
between them prove to be very like those between the closely
related species that have just been considered. The facts may
best be summarized in Table 8. The observations under the
Lyomeri and Ceratioidea are based on the work of Nusbaum-
Hilarowicz (1923), Bertin (1934) and Tchernavin (19470,6),
Waterman (1948), and Bertelsen (1951) and also on personal
observation.

A few observations may be added concerning the ceratioid
angler fishes. I have looked at females of Melanocetus murrayi,
Neoceratias spinifer and Danaphyrne. In all three, the first gill-
arch is devoid of gill-filaments. Drawings of filaments from
the second arch are shown in Text-fig. 46. In Neoceratias
and Danaphryne there are no more than 50-60 gill-filaments
in each gill chamber.

In the deeper living fishes, every possible economy of tissue has been developed. Compared with
the species that live above them and within swimming distance of the productive surface-waters, they
seem degenerate. It might be argued that the most trenchant economy has been effected by the
evolution of dwarf-males in the Ceratioidea. During the free-living existence it must take much less
food to maintain a male than its partner. However, there are other factors to be considered (Bertel-
sen, 1951).

The ceratioid angler fishes, Cyclothone spp., and probably the Lyomeri (Eurypharynx has a lepto-
cephalus larva), spend their larval life in the plankton-rich surface-waters. Evidently there is not
sufficient food of a suitable nature to sustain the larvae at the depths occupied by the adults. How-
ever, a good start in life must counterbalance the hazards of this type of life-history.

It is now well-known that the waters below 1000 m. support sparse populations of planktonic
animals in comparison with the waters near the surface. The relevant papers and additional evidence

V-B

Text-fig. 45. Diagrammatic reconstruction
of one of the two tubules forming the kidney
of Cyclothone (after Owen, 1938). ( x 7-5.)
B, bladder; G, glomerulus; Pi, Pz, first
and second parts of proximal convolute;
T, terminal segment.

PELAGIC AND BENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP-SEA LIFE 105

Table 8. The relative developments of tissue in two assemblages of bathypelagic fishes

Lyomeri and Ceratoidea1

Gonostomatidae (most species),
Sternoptychidae, Astronesthes
spp. Myctophidae (most species)

Vertical range

Swimbladder

Skeleton

200-1000 m.

Present

Well formed and mod

Musculature
Eyes

Well developed
Large

Light organs

Highly developed

Brain
Gill-system

Large, well developed
Well developed

1000-4000 m.

Absent

Reduced, particularly in Lyomeri and poorly

ossified
Reduced, particularly in Lyomeri
Relatively small (except in certain male cera-

tioids)
Present only on female ceratioids and on tail of

Lyomeri
Small
Much reduced

Text-fig. 46. Filaments from the second gill arch of (a) Neocer alias spinifer; (b) Melanocetns murrayi; (c) Danaphryne sp.

(a, X40; B, X20; c, X40.)

may be found in Foxton's (1956) paper. Reference to his table 7 will show that in tropical and sub-
tropical waters the mean volume of zooplankton between the surface and 150 m. is more than twenty-
times that between 1000 and 1500 m. In the Kurile-Kamchatka area, the biomass (mg./m.3) of
plankton between the surface and 100 m. is about forty times the value measured between 1000 and
2000 m., (and about ninety times greater than that between 2000 and 4000 m.) (Zenkevitch and
Birstein, 1956).

Extra data on the biomass of zooplankton in the North-western Pacific are given by Bogorov
(1958). In the surface-zone (0-200 m.) the biomass is 1000 mg./m.3 or more, while in the 'transition
zone ' (200-500 m.), which is generally richer in species than the surface-zone, the biomass falls to
about 350 mg./m.3 Below this comes a 'deep-sea zone' (500-6000 m.) in which the biomass varies
from 2-64 to 78 mg./m.3 Between 6000 m. and the deep-sea floor the zooplankton-content is less than
1 mg./m.3 Finally some indication of the paucity of life in deeper waters is also given by measure-
ments of the oxygen consumption and phosphate regeneration (Riley, 195 1). Over the Atlantic
(between 450 N. and 540 S.) the curves of oxygen consumption (ml./l./year) fall sharply below depths
ranging from about 250 to 800 m. (see Riley's fig. 25) and Text-fig. 47 of this Report.

1 The Giganturoidea could also be placed in this assemblage. Nearly all the sizeable specimens in the Dana collections
have been taken by nets fishing below a depth of 1000 m., and, apart from their large tubular eyes, they have a low level
of tissue development, much like that described under the Lyomeri and Ceratioidea. The giganturoids also have very small
kidneys.

io6

DISCOVERY REPORTS

PELAGIC AND BENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP-SEA LIFE 107

Since diurnal migrations are an integral part of the lives of so many fishes existing in the upper
oceanic reaches, it is clear that they could not survive and reproduce their kind without drawing on
the rich food-supply in the surface-waters. But this feeding-level is beyond the direct reach of the
species living below 1000 m. Evidently the most potent environmental stress, against which they
have evolved, is the sparse supply of food. But one favourable factor must have been the coolness of
their surroundings : the lower the temperature the less the food required for maintaining life (Brown,
1957)- On the other hand, at high hydrostatic pressures the pace of life, measured by the rate of
oxygen consumption, seems to be increased (p. 90). And, while they do not have to contend with
turbulent waters like the fishes that migrate to the surface-mixed layer, the laminar viscosity of the
cool seas (50 C. or less) through which they must move is nearly double that at the surface in the
warm ocean.

The conclusion is inescapable that the paring-down of the tissues, particularly the reduction of
muscle and bone substances, is the most striking of these fishes' adaptations to their living-space. As
we have seen, there is every indication that the black Cyclothones, ceratioid angler fishes and gulper-
eels (Lyomeri) are much less active than the fishes living above them in the upper 1000 m. of the
ocean. With the reduction of these tissues they have not only acquired an economy of life to match
their food-supply, but have also reduced, more probably eliminated, the effort required to maintain
their level in the ocean.1 If Gonostoma elongatum, which also lacks a gas-filled swimbladder, comes
'close to neutral buoyancy (Denton and Marshall, 1958), this must surely be true of these fishes. In
a well-fed Cyclothone microdon, the fat stored around the regressed swimbladder, attached to the
mesenteries, and deposited in the subcutaneous sinuses must take up more than 10 per cent of the
volume of the fish. This light tissue (with a density of about 0-9), together with the reduced muscular
tissues and flimsy skeleton, may well make these fishes neutrally buoyant. In a letter to me, dated
8 November 1958, Dr Peres has recorded his daytime bathyscaphe observations of Cyclothone,
Gonostoma and Chaidiodas. He writes: 'Ces animaux sont toujours immobiles, paraissant Hotter; ils
semblent attendre la proie sans la poursuivre, et il m'a ete impossible de voirs quelles sont les nageoires
dont le mouvement aide a leur equilibre. En revanche les petits Myctophum sont presque toujours
en mouvement.'

Cyclothone feeds on copepods and chaetognaths (Giinther and Deckert, 1953), while Nusbaum-
Hilarowicz (1920) found fish-scales and eye-lenses in the gut of C. braueri. In three individuals of
C. microdon taken at St. 395 (480 26f S., 220 10' W. to 480 z6\ S., 220 06J' W. 13. v. 1930; N 450 H;
1 500-1400 m.), I found the remains of copepods, chaetognaths, euphausiids, together with detrital
material and faecal pellets. Female ceratioid angler fishes feed on organisms ranging from copepods
to squids and fishes, while in the dwarf, free-living males, copepods, chaetognaths and Phronima
have been found (Bertelsen, 1951). Saccopharynx takes fishes (including benthic species);
Eurypharynx, crustaceans, worms and fishes (Bertin, 1934). The angler fishes lure their prey
and certain species can master fishes several times their own length. Perhaps Saccopharynx,
which is also a giant swallower, attracts prey by means of the spongy luminous tissue on its wisp of
a tail.

Thus all these fishes, including Cyclothone, are predatory, and they possess jaws that are adapted
for taking a very wide size-range of food organisms. If we again make the same comparisons of species
from the upper and lower mid-waters, this adaptation is strikingly revealed.

1 Certain of the deeper-living cephalopods (e.g. Vampyroteuthis, Cirroteuthidae, Amphitretus and other octopods) ' . . .have
lost most of their firmness and muscular power. They develop a thick coat of jelly-like subcutaneous tissue and the muscles
themselves are sometimes degenerate and invaded by this jelly' (Morton, 1958). This parallel in the most active group of
nektonic invertebrates is most striking.

14-2

108 DISCOVERY REPORTS

Reference to Text-fig. 43 will show that C. microdon has much longer jaws than Manrolicus , the
suspensoria of which are more or less vertical in position. It is clear that the diet of Mauroliciis must
be restricted, probably to organisms the size of large copepods. However, it lives nearer to good
supplies of such food.

Again, Gonostoma bathyphilum possesses longer jaws hinged to more backwardly carried sus-
pensoria than its relative G. denudation (see Text-fig. 42). This tendency is carried to an extreme in the
Lyomeri in which the suspensoria and jaws are many times longer than the neurocranium. More-
over, the premaxillae and maxillae have been lost, the teeth in the upper part of the mouth being
carried on the palatopterygoid elements (Tchernavin, 1947a). The skeleton is also reduced in many
other ways. But the most fantastic regression of bone and other tissues occurs in the Monognathidae,
fishes that may well live in the same oceanic layers as the Lyomeri (Bertin, 1938).

The jaws, and especially the buccal cavity, of most female ceratioid angler fishes are also large.
' The length of the premaxillary and maxillary is usually more than 50 per cent of the distance from
snout to end of cranium and reaches 100-150 per cent in Caulophryne and many Linophrynids '
(Bertelsen, 1951).

The degree of adaptation of the jaw-mechanisms of these fishes is perfectly evident, a structural
emphasis fitting them to an environment with poor supplies of food. In such surroundings it is an
advantage to be able to take the largest possible meal that comes along, and at the same time, not to
turn aside from a copepod. As Thorson, quoted by Moore (1958) has pointed out, the swallowing
capacity of a predator must not only be proportional to the sparseness of the prey, but also be inversely
related to its own speed of movement. (Moreover the copepod (or euphausiid) may at least be partly
a carnivore and thus be well down the food-chain that begins with the plants of the surface-waters.
Bogorov (1958) mentions that deep-sea copepods, such as Pareuchaeta, and Bathycalanus feed
on radiolarians and other small animals. Some deep-sea decapods and amphipods are also
carnivores.)

Despite their reduced economy of life, or rather because of it, these fishes are not to be regarded as
' misfits '. Cyclothone microdon is perhaps the most ubiquitous fish in the ocean, its range extending
from subarctic to antarctic regions, although, the catches of mid-water nets are likely to give a ' false '
impression of its abundance owing to its reduced activity. Off Bermuda, Beebe (1937) took eight
times as many Cyclothone as lantern fishes, but the ocean must support greater numbers, certainly
a greater weight, of the latter. (Cyclothone spp. are less easily recognized from a bathyscaphe than
lantern fishes ; thus experienced observers usually see more of the latter.)

Besides the regression of the muscular and skeletal systems, we have seen that the eyes and light-
organs of these deeper living fishes are small in comparison with those of the species living above
them. I have also implied that this economy of tissue must be linked to reduced development of the
nervous and excretory tissues, a correlation which will also apply to the circulatory system. (A study
of the alimentary system would also be of interest, for Nusbaum-Hilarowicz (1920) found the in-
testine of Cyclothone to be particularly simple in structure.)

Considering for the moment the eyes, if submarine sunlight is the only controlling factor in their
development, the benthic fishes of the abyssal plain would be expected to have markedly regressed
visual organs, but this expectation is by no means realized. As Hjort (Murray and Hjort, 191 2) wrote:
' But if it be the case that the size of the eyes in pelagic fishes decreases vertically with the decreasing
intensity of light, how can we explain the fact that the bottom fishes, like Macrurus ( = Nematonurus)
armatus, living in abyssal depths possess large and apparently well-developed eyes.' Perhaps this
should be called Hjort's Paradox. However, the eyes of the abyssal macrourids and brotulids do tend
to be relatively smaller than those of their relatives living over the continental slopes (Marshall,

PELAGIC AND BENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP-SEA LIFE 109
1954),1 and in a few species such as Aphyonus gelatinosus, the eyes are much reduced. These apparent
exceptions will be discussed at a later point (pp. 111-112).

If we compare a black Cyclothone, an angler fish or a gulper eel with an abyssal bathypteroid,
macrourid or a brotulid, the difference in the relative development of the eyes is not the only con-
trasting feature. Actually the bathypteroids have small eyes, but their myotomes and skeleton are
far better developed, being almost as firm and well-knit as those of their shallow-water relatives, the
lizard fishes (Synodontidae). A 3 - f t . Nematonurus armatus is far better equipped with all manner of
tissues than a 3-ft. gulper-eel (and it has kept its swimbladder). The small brotulid Mixonus caudalis
is similarly 'better off' than a black Cyclothone or an angler fish. Many other such contrasts could
be made, but here we need only add that the gill-surface of the benthic fishes is far better developed
than that in the bathypelagic species.

But the deep-sea floor supports a larger standing crop of animal-life than do the deeper mid-waters
of the ocean. In the Kurile-Kamchatka Trench region, which lies under a productive stretch of
surface-water, the biomass of bottom-dwelling animals in a square metre was measured at 6-94 g.,
between depths of 950 and 4070 m. Between 5070 and 7230 m. the quantity fell to 1-22 g./m.3
(Zenkevitch and Birstein, 1956). Bottom samples taken by a Petersen grab from the 'Galathea'
indicate that the deep-sea floor supports an average of ten animals per square metre with a total
weight of about 1 g., and this must be a minimum value. Having given these figures, Sparck (1956)
concludes thus: 'This surprising density right down to between 5000 and 8000 m. suggests that food
conditions in the abyss are not so poor as we have been inclined to think, and this in turn leads us
to suppose that abyssal water currents must be stronger than formerly believed.'

The key-organisms in the sediments, perhaps those at the base of the food pyramid, are the bacteria
(Zobell, 1954; Zobell and Morita, 1956). They can exist on the dissolved organic matter in seawater
and convert intractable substances such as cellulose and chitin into their own substance. The authors
just mentioned suggest that the bacteria may be used directly as food, or may aid digestion by living
as symbionts in the gut of bottom-dwelling animals. Whatever may be the actual conditions, it is
clear that large standing-crops of mud-eating holothurians can exist at depths exceeding 6000 m.
(Hansen, 1956). While these animals may be largely free from the attacks of predators, holothurians
may still form 30-50 per cent of the biomass of benthic organisms in depths from 3000 to 7000 m.,
in regions where predatory groups such as the asteroids are particularly abundant (see Zenkevitch,
1954, fig. 2). Finally, at depths down to at least 2500 m., conditions of life at the bottom are favour-
able enough to attract detachments of active pelagic organisms, such as euphausiids, sergestids and
lantern fishes (pp. 87-88).

It would thus seem that there is sufficient food on or near the bottom to satisfy the day-to-day
requirements of the relatively highly organized bodies of bathypteroid, macrourid and brotulid fishes.
As we have seen, species belonging to the second and third groups have retained a gas-filled swim-
bladder. There is structural and biological evidence that this organ is functional, even at great depths,
but because of its decreased buoyant properties at high pressures some reduction of tissue density is
necessary if the animals are to be in hydrostatic equilibrium with their environment. Furthermore,
there is evidence that the muscular and skeletal tissues have been somewhat reduced. Even so, the
level of development of these and other tissues is much superior to that possessed by the bathypelagic
fishes poised above them in the deep, nutrient-poor waters of the ocean. In the endless struggle

1 Moreover, Nematonurus armatus has a wide depth range (2S0-4600 m.) extending from regions receiving sunlight to
unlit depths. In Lionurus filicauda, which seems to be restricted to the abyssal plain (2515-4846 m.), the eyes are propor-
tionately smaller. A 500 mm. Nematonurus armatus has orbits measuring 18 mm. in diameter (Nybelin, 1957) while in a
400-mm. Lionurus filicauda the eyes are about 10 mm. in diameter.

no DISCOVERY REPORTS

for a living-space, interaction between fish and environment has been such that tissues have evolved

not only to match the biological environment, but to conform to the physical stresses besides.

We are now in a better position to consider the deeper dwelling bathypelagic fishes. Presumably
the species of Cyclothone once had a gas-filled swimbladder in the adult phase, but this is now only
functional during larval life. Gonostoma bathyphilum has lost all trace of this organ, but it is well
developed in a related species, G. denudation. The ancestors of the ceratioid angler fishes and the
gulper eels may also have had a swimbladder.

Now it is clear that the loss of this organ is not related to the pressure factor, or indeed, to any
physical effect. The foregoing discussion simply suggests that the cause largely resides in the trophic
conditions obtaining in the deeper mid-waters of the ocean. To begin with, a pelagic fish with a swim-
bladder is able to carry more muscle, attached to a firmer skeleton, than a fish (of comparable dimen-
sions) without such buoyant uplift (Denton and Marshall, 1958). In turn, the proper maintenance
and functioning of these tissues require well-developed circulatory, respiratory, alimentary, excretory
and nervous systems. But with the loss of the swimbladder, the degree of tissue organization could
become ' geared-down ' to the low level of potential energy in the biological environment.1 At the
same time neutral buoyancy could be approached or, more likely, achieved.

Moving into the upper thousand metres of the ocean, it is surely significant that most of the plankton
feeders, the small gonostomatids, hatchet fishes and lantern fishes possess a swimbladder (Marshall,
1 951). Having this internal float, they are able to carry the muscle necessary to propel them upwards
during their daily migrations to the food-rich surface-waters. It is also striking that most of the
predatory fishes (Stomiatidae, Melanostomiatidae, Chauliodontidae, Idiacanthidae, Malacosteidae and
Alepisauroidea) lack a swimbladder. (The exceptions are Astronesthes spp. and Chiasmodon niger.)
We have seen that (pp. 85-86) some of these fishes also undertake vertical migrations. It is probable
that they, like Gonostoma elongatum, come close to neutral buoyancy through a reduction of skeletal
and muscular tissue (Marshall, 1954, 1955; Denton and Marshall, 1958), but the regression of these
tissues is by no means so marked as that in the pelagic fishes living in the deep, underlying
waters.

Chauliodus sloanei is one of these predators living in the upper mid-waters. The younger individuals
live fairly close to the surface and are thus well placed for food (Ege, 1948; Haffner, 1952). The
deeper dwelling, older fishes grow to lengths of more than 250 mm.

During the daytime Dr Peres has watched Chauliodus from a bathyscaphe and in a letter dated
17 November 1958 has written of his observations. These fishes hover in the water with the long axis
of the body at an acute angle to the horizontal plane, the head being above the tail. At the same time
the long second dorsal ray, which is tipped with luminescent tissue (Brauer, 1908), is curved forward
over the head so that the extremity of the ray lies in front of the mouth. Clearly, the fish is behaving
very much like a female ceratioid and is angling for prey. It is also looking obliquely upward, poised
in a good position for detecting prey silhouetted against the down-going and scattered rays of sun-
light, but towards sunset, it moves upwards to richer feeding grounds. While the density of its bone
and muscle is less than that of a myctophid, it is much the larger fish, and what it lacks in unit
muscle-power it gains in size and power of movement, which is also true of most of the other pre-
datory fishes without a swimbladder. Moreover, it is interesting that the only predatory stomiatoids
containing this organ are the species of Astronesthes, which are smaller than their predatory relatives
without it (p. 90). Like its myctophid prey, Astronesthes niger, which crosses the upper thermocline
during its migrations, has a firm skeleton and compact well-formed myotomes.

1 If a teleost had both 'light weight' tissues and a capacious hydrostatic organ it would be overbuoyant.

PELAGIC AND BENTHIC FISHES, SWI MBL ADDER, ECONOMY OF DEEP-SEA LIFE m

But Hjort's Paradox is still unresolved. I have mentioned that certain of the brotulids are ex-
ceptional in having very regressed eyes. Aphyonus gelatinosas is such a species and it lacks a swim-
bladder. The tissues of its body are also much reduced by comparison with another brotulid of about
the same size, Mixonns laticeps, a species with a swimbladder. This brotulid has an elongated tapering
body, sheathed with scales and equipped with well-knit myotomes. The skeleton is quite firm. The
eyes are small, but well-formed, with a wide pupil and a large lens. In the type specimen, which
measures 125 mm. in standard length, the horizontal width of the eye-ball is about 4-0 mm.

As indicated by its specific name, Aphyonus has a gelatinous appearance. It is semi-transparent
and colourless, except for deep-set points of pigment that represent the remains of the eyes. The skin
is loose and scaleless, while the skeleton and myotomes are much reduced, the notochord being
persistent.

While the type-specimen of Aphyonus gelatinosus is bulkier and somewhat longer (standard length
130 mm.) than that of Mixonus laticeps, it has a much simpler gill-system. On the first arch there are
about fifty filaments with an average length of about 1-5 mm., the second arch bears about forty
filaments, while there are only two to three on the fourth arch. Mixonus laticeps has somewhat shorter
filaments but there are at least a hundred on the first arch and about eighty on the second. Moreover
the filaments carry about twenty-five lamellae per millimetre, about twice as many as those developed
in Aphyonus.

These contrasts are very like those already shown to exist between pelagic fishes from the upper
and lower oceanic reaches. Perhaps Aphyonus is one of the deeper-living pelagic fishes. This genus,
together with Barathronus, Sciadonus and Leucochlamys are placed by Nybelin (1957) in a new sub-
family Aphyoninae, ' ... as they show many mutual similarities and in many respects differ from other
Brotulids. As common characteristics may be mentioned a comparatively small body size, a thin
loose scaleless skin without or with only very feeble pigmentation, strongly reduced eyes and bone
tissues, and a more or less persistent notochord; an opercular spine, characteristic of the typical
Brotulids, is lacking.' Moreover, they have very reduced gills and from Nybelin's figures of Bara-
thronus erikssoni and Sciadonus kullenbergi, it is clear that a swimbladder is absent. As the cleft of the
mouth runs obliquely upward in Barathronus, Nybelin has suggested that this genus is pelagic in
habit. The only direct evidence is the rather young specimen of Barathronus parfaiti that was found
by Legendre (1934) in the stomach of a long-finned tunny (Thunnus alalunga).

I suggest that the entire subfamily consists of deep-dwelling, bathypelagic fishes. If this proves to
be so, the common characters might not be indicative of genetic affinity, but rather of convergent
adaptation to their food-poor environment. {Barathronus and Sciadomus are viviparous, while the
ovaries of the type of Aphyonus gelatinosus contain many eggs, suggesting oviparity.) The deeper
mid-waters could even be regarded as a refuge for species that have been edged-out of the two main
feeding grounds of the ocean, the waters under the interface between sea and atmosphere and those
near the interface between sea and sediments.

If the Aphyoninae are not benthic fishes, the abyssal fauna consists almost entirely of species with
small to moderately large eyes.1 Now Denton and Warren (1957) suggest there are two main factors
related to the size and development of the eyes in deep-water fishes. A fish living in the twilight zone
is exposed to a large field of light, and here the size of the eye matters less than the relative proportion
of the dioptric parts, a wide pupil being necessary. To perceive spots of luminescence efficiently a
large collecting pupil is required; the bigger the eye the better. These conditions are met in fishes

1 Typhlonus nasus is a blind brotulid and might be an exception, but it has a small, thin-walled swimbladder. The bones
are soft and flimsy and the myotomes excessively thin. The eyes of Ipnops are not regressed but curiously modified. Leucicorus
htsewsus, which looks more like a bottom-dwelling brotulid, seems to be an exception (see also Marshall, 1954).

ii2 DISCOVERY REPORTS

from the upper iooo m., but what of the abyssal species? Their small to moderately large eyes are
equipped with wide pupils and large lenses, and they have presumably retained their visual powers
because there is luminescent light to be seen (some deep-sea bacteria are luminescent). Furthermore,
at least some of them start life in the upper, lighted layers of the sea. (The same is true of the deep-
dwelling pelagic species.) A flash of light may mean a euphausiid meal for a Cyclothone, or signify
a predator. While the eyes of some of these fishes do not properly fulfil the second requirement, they
have gone some way to meet it. However, the loss of the eyes in some pelagic fishes, that exist below
the iooo-m. level, is compensated for by a marked development of the lateral-line organs on the head.
Aphyonus has large canals and so has Ditropichthys storeri, which may well belong to this fauna (see
also Marshall, 1954).

These considerations may seem far removed from swimbladder problems. But they have been set
down because I once thought that the regression of the eyes and swimbladder might be linked to the
disappearance of the pseudobranch. Myctophids, which have well-developed eyes and swimbladders
also have large pseudobranchs. In Gonostoma bathyphihim and Aphyonus gelatinosus, with small or
regressed eyes and no swimbladders, the pseudobranchiae are absent. Now Copeland (1952) found
that removal of these organs in Fundiilus inhibited the inflation of the swimbladder. Furthermore, the
blood to the choroidal gland of the eye passes through the pseudobranch in teleosts, although the
functional relationship is not clear (Barnett, 1951). However, despite a thorough search under the
skin of the gill-chambers of Astronesthes niger and Gonostoma denudation, fishes with swimbladders
and large eyes, I was unable to find any trace of pseudobranchiae.

We have seen that the loss of the swimbladder in pelagic fishes of the deeper, mid-oceanic waters
is not related to the pressure factor, but rather to their harsh biological environment, one that seems
to be lacking in the potential energy required to maintain the extra tissues associated with an internal
float. Is the regression of the eyes in such fishes as the Aphyoninae, the Monognathidae and Cyclo-
thone obscura also to be explained on this basis? Is this a further economy of living tissue?

In dealing with blind cave fishes, Walls (1942) points out that the elimination of the eyes is but
a small economy, most of the energy released from food going into motor and secretory activity.
However, there is an associated saving of tissue in the central nervous system in the form of a much
reduced optic tectum (see Marshall and Thines, 1958). On the other hand, Heuts (1951) maintains
that the slow growth-rates, low metabolism and regressed tissues (including the eyes) in Caecobarbus
are adaptations to the limited food resources of the environment. He goes on to suggest that this is
true of all cave fishes. But this is too sweeping a generalization, as Breder (1953) and Cahn (1958) have
shown. Some cave fishes, such as Anoptichthys jordani, may have good supplies of food and they are
most active animals. An Anoptichthys, which has a well-developed swimbladder, carries much more
muscle than a Cyclothone microdon of the same size. Apart from these considerations, caves differ
from the deep mid-waters of the ocean in being totally dark.

To return to blind deep-sea fishes, Heuts's concept of the regression of the visual tissues seems
more applicable to their case than to the condition found in some cave fishes. While economy in the
form of reduced visual and nervous tissue is a small item in the energy balance sheet of an Anopt-
ichthys, it might well be critical for an Aphyonus. As if to compensate for its loss of vision, Aphyonus
has a well-developed ' Ferntastsinn ' sense in the form of neuromast organs on the head. Do these
require less energy to maintain than eyes? At all events, they require smaller centres in the brain.
Here the problem may be left with the thought that the food-factor may well be critical, but it may
not be the only factor involved.

We are left with certain concepts, which are partly summarized in Text-fig. 47. Living in the
ocean at depths above 1000 m. are several hundred species of pelagic plankton-feeding fishes with

PELAGIC ANDPENTHIC FISHES, SWIMBLADDER, ECONOMY OF DEEP SEA-LIFE 113
well-formed, gas-filled swimbladders. They are muscular, active little fishes with large eyes and
brains and highly developed light-organs. Because of the extra propulsive power that a swimbladder
allows, they are able to make daily visists to the food-rich, surface-waters, which they must do to
maintain their highly organized bodies. Living with them are almost as many predatory fishes,
nearly all of which have lost an internal float. In spite of this, these fishes come close to neutral
buoyancy by reducing their muscular and skeletal tissues. All have well-formed eyes and brain, and
many have complex batteries of light organs. Some of these fishes also migrate to the surface-layers,
compensating for their reduced myotomes by increased size of body.

Living below them in the deep mid-waters, are more than a hundred species of pelagic fishes with
no swimbladders and very reduced tissues. They are nearly all predatory fishes, many of which lure
their prey instead of pursuing it. As they are likely to be neutrally buoyant they can hover in the water
without undue effort. The energy balance sheet of these species seems closely fitted to the limited
supplies of potential energy around them.

On the abyssal plain, about 250 species of benthic fishes have been taken below a depth of 2000 m.
Well over half have well-formed swimbladders and a number of species may range as deeply as
5000 m. Compared with the deeper bathypelagic fishes they are highly organized, but show some
reduction of bone and muscle to compensate for the reduced positive buoyancy of a swimbladder at
great depths. Most of the species without a swimbladder have an equally good organization, but the
food supply seems sufficient to satisfy their day to day requirements.

These differences in form and organization of the tissues are reminiscent of Raunkiaer's (1934)
concept of life form in plants.1 ' All over the world environments varying from place to place deter-
mine the existence of different life forms, because the demands of the plants, which are, at any rate,
partially expressed by their structure, must of necessity be in harmony with the environment if life
is to continue.' Raunkiaer saw that certain structural features were correlated with certain types of
environment and that these features were shared by diverse species of plants. Reference to this
section, particularly to the table on p. 105, will show that this is also true of the assemblages of fishes
that live at the upper and lower levels of the bathypelagic environment. As I hope to continue with
this problem, to look more closely at some of the knots in Bigelow's (1930) 'endless web of netting',
these few remarks will suffice to conclude this Report.

SUMMARY

Structural development of the swimbladder (pp. 6-50)
Dissection of about ninety species of bathypelagic teleosts has shown that a well-developed, gas-filled
swimbladder is present in numerous stomiatoid fishes (most Gonostomatidae, Sternoptychidae,
Astronesthes spp.); salmonoid fishes (Opisthoproctus, Winterid) Myctophidae (most species), Melam-
phaidae (most species) and Chiasmodon niger (Chiasmodontidae). The swimbladder regresses during
adult life in the Miripinnati, certain of the Stomiatidae and a few Myctophidae and Melamphaidae.
It is completely absent in numerous stomiatoids (Melanostomiatidae, Chauliodontidae, Idiacanthidae
and Malacosteidae), Alepocephalidae, certain Myctophidae, Scopelosauridae, Alepisauroidea, Gigan-
turoidea, Lyomeri and Ceratioidea.

1 Certain continental zoologists have also developed the idea of 'Lebensformtypen' in animals (see Macfadyen, 1957), but
the concept is more familiar to botanists.

ii4 DISCOVERY REPORTS

SWIMBLADDER STRUCTURE AND CLASSIFICATION (pp. 50-58)

The structural plan of the swimbladder has thrown new light on the classification of these groups.
The stomiatoids are revealed as a compact (paraphysoclistous)1 group with a single, bipolar rete
mirabile at the posterior end of the swimbladder which has a resorbent capillary bed, obtaining its
arterial blood through a by-pass branch of the retial artery. Differences in swimbladder structure
may also be useful in distinguishing genera.

The deep-sea salmonoid fishes have a very different (euphysoclistous)1 form of swimbladder with
micro-retia mirabilia supplying the gas-gland. The myctophid swimbladder is also euphysoclistous
(with an oval) and three unipolar retia mirabilia enter the anterior end of the sac to carry blood to the
three-lobed gas-gland. The families Anoplogastridae, Melamphaidae and Stephanoberycidae (sub-
order Anoplogastroidea, Berycomorphi) yet again have a euphysoclistous swimbladder (with an oval)
and one or two unipolar retia mirabilia, which run forward from the posterior end of the sac. These
and other findings are used to discuss the development of a closed swimbladder in the deep sea,
particularly in the predominantly physostomatous1 Isospondyli, and to consider evolutionary re-
lationships.

The swimbladder wall (pp. 59-65)

The fine structure of the swimbladder wall in bathypelagic teleosts is much like that of other physo-
clistous groups. Excluding the peritoneal investment, an outer, thin but tough layer of collagen fibres
(tunica externa) is separated from the inner epithelial layer by a more voluminous reticulum of fibres
developed within a semi-fluid, gelatinous matrix. There is also a layer of smooth muscle fibres near
the inner epithelium. Following descriptions of the fine structure of the swimbladder wall in certain
species, there is some discussion of its mechanical and gas-proofing qualities. In particular, attention
is drawn to the role of the submucosa in a swimbladder undergoing compression during a migration
into deeper waters. The semi-fluid submucosa would seem to allow the tissues to relax in a uniform
manner and the sac to maintain its ellipsoidal shape.

Fat-invested swimbladders (pp. 65-68)

In certain bathypelagic fishes (the stomiatoids, Cyclothone spp., Gonostoma elongatum, Polyipnus
later natus, Borostomias antarcticus, Stomias colubrinus, S. affinis, the myctophids, Latnpanyctus
leucopsarus, Diaphiis theta and the anoplogastroid, Anoplogaster longidens), the swimbladder regresses
after metamorphosis and becomes invested with fat, which is deposited between the peritoneum and
the tunica externa. It is pointed out that this replacement of gas by fat can have but little effect on
the ' credit side ' of the ' buoyancy balance sheet '.

The swimbladder as a hydrostatic organ and the structure of
the gas-producing and resorbent parts (pp. 68-81)

Like species living nearer the surface or over the continental slope, the volume of the swimbladder in
bathypelagic fishes is about 5 per cent of the body volume. It thus functions as a hydrostatic organ,
making its possessor weightless in water. But compared to shallow-water species the gas-producing
complex (rete mirabile and gas-gland) is highly developed :

1. The product of the number and length of the capillaries forming the retia is high compared to
the dimensions of the swimbladder. These two features, together with the form of arrangement of the
capillaries, are also considered in relation to the design of the retia as counter-current systems allowing

1 See p. 50.

SUMMARY u5

of gaseous exchange between the arterial and venous capillaries. There is evidence that the deeper
living species tend to have longer retia.

2. The development of the gas-gland, as expressed by its surface area, is much more pronounced
in bathypelagic than in epipelagic species. There appear to be three main types of gas-glands; (a) with
many giant cells, (b) with medium sized cells, and (c) with small cells. Intracellular capillaries are
found in the first type. Certain cytological features of the gas-gland cells of Vinciguerria seem in
keeping with the accumulating evidence that the cells actively transport gases from the blood plasma
to the lumen of the swimbladder.

The structural features of the resorbent part of the swimbladder, the part by means of which the
gas-content can be reduced, are reviewed. Certain aspects of form and function are considered.

The swimbladder and vertical distribution (pp. 82-85)

A well-developed gas-filled swimbladder is only to be found in bathypelagic fishes with centres of
concentration above the 1000-m. level. While numerous other species in the same environment lack
such a swimbladder, this condition is universal in bathypelagic species that occur belozv a depth of
1000 m. The loss of the swimbladder in the deeper living species might seem to be related to the
pressure factor, to the compressibility of gases and the amounts of energy and gas required to keep
the swimbladder inflated at the appropriate buoyant volume against high hydrostatic pressures.

The swimbladder and vertical migrations (pp. 85-95)

Many of the bathypelagic fishes living in the upper oceanic reaches (200 to 1000 m.) undertake
diurnal vertical migrations. After reviewing the evidence for these movements, the physical and
biological background of these migrations is considered. While a number of species cross the near-
surface thermocline during their upward migrations, other species are rarely if ever taken in the
surface-layers and may be called partial migrators. The physical problems of gas secretion and
resorption are considered for both types of migrator. While these fishes are small, active species with
a relatively large gill-surface, the provision of enough gas to fill the swimbladder during and after
a downward migration seems an immense physiological task unless the gas-gland can store oxygen
in a combined form. Concerning the loss of gas during an upward migration, the high ratio between
the resorbent surface and the volume of the swimbladder and the very steep concentration gradient
between the tensions of the swimbladder gases and those in the blood, may well mean that the rate
of gas resorption is high enough to keep pace with the reduction in hydrostatic pressure.

the swimbladder and the economy of life in the deep sea (pp. 95-113)

At least half of the benthic species that range below a depth of 2000 m. have well-developed, gas-filled
swimbladders, with very long retia mirabilia. Considering also the bathypelagic species, there is
a direct correlation between the length of the retia and the depth of the living space, a further striking
indication of the function of the retia as systems for the counter-current exchange of gases. Apart
from implying that the swimbladders of these fishes are functional at great depths (down to 5000 m.)
these facts suggest that the loss of the swimbladder in bathypelagic fishes with centres of concen-
tration below the 1000-m. level is not due to the pressure factor. The most potent influence is seen to
be the food-poor environment of these fishes, one without the necessary nutriment to support the
' extra ' tissues that can be carried at neutral buoyancy by a hydrostatic organ. Compared with the
fishes with swimbladders living in the upper reaches (200-1000 m.) of the bathypelagic environment
(and with benthic species), the tissues of these deeper living species are much regressed. The life-
forms of diverse fishes from these different levels are no less striking than those found in plants.

15-2

n6 DISCOVERY REPORTS

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15-3

n8 DISCOVERY REPORTS

Gunther, K. and Deckert, K., 1953. Morphologisch-anatomische und vergleichend bkologische U titer suchungen iiber die

Leistungen des Viszeralapparates bei Tiefseefischen der Gattimg Cyclothone (Teleostii, Isospondyli). Z. Morph. Okol.

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London: Allen and Unwin, pp. 202-10.

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PLATE I

Microphotographs of transverse sections through
the swimbladder.

Fig. i. Vinciguerria nimbaria; section cut towards the posterior end
of the swimbladder between the rete and gas-gland ( x 150). Note
the artery-vein pairs (each an association of a large and small
vessel) running to the gas-gland and the undulating appearance
of the fibres in the submucosa.

Fig. 2. Section through the regressed swimbladder of Cy clot hone livida
( x 300). Note the capillaries of the regressed rete mirabile and
the regressed cells of the gas-gland (mainly to be seen in the upper
right half of the section. See also text fig. 34).

Fig. 3. Section through the rete of Polyipnus laternatus ( x 130). Note
the section cut through the by-pass branch of the retial artery at
the top of the photograph.

Fig. 4. Enlarged part of Fig. 3 ( x 580). The ' triangle ' of nuclei (at
about 7 o'clock) in Fig. 3 will be again seen in this figure. The
larger capillaries in this section belong to the venous part of the
retial circulation.

DISCOVERY REPORTS, VOL. XXXI

PLATE I

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PLATE II

Microphotographs of parts of the swimbladder, taken from sections
(figs. 1-3, transverse section; fig. 4 longitudinal section).

Fig. 1. Giant cell of gas-gland of Vinciguerria attenuata ( x 675). Note
the intracellular capillaries, surrounded by lighter staining peri-
capillary cytoplasm and the fine canals joining the capillaries. The
vacuolated nature of the pericapillary cytoplasm can also be seen.
b = base of cell.

Fig. 2. Much enlarged part (X1500) of a giant gas-gland cell of
Vinciguerria attenuata to show the vacuolated nature of the cyto-
plasm surrounding the capillaries.

Fig. 3. Appearance of part of the gas-gland in a compressed swim-
bladder of Vinciguerria nimbaria ( x 225). Note the very different
shape of the cells from the one shown in fig. 1 , which came from a
fully expanded swimbladder. The intracellular capillaries and peri-
capillary cytoplasm (here without vacuoles) may also be seen.

Fig. 4. Entry of a rete into lobe of gas-gland of Myctophum punctatum
( x 67-5). Note the parallel system of capillaries forming the rete
and the capillaries running among the gas-gland cells.

DISCOVERY REPORTS, VOL. XXXI

PLATE II

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.ism-tol sdj lo sanod

PLATE III

Fig. i . Microphotograph of longitudinal section of a much contracted
oval in the swimbladder of Myctophum punctatum ( x 120). Note
the many blood vessels running through the relaxed tissues of the
oval, mostly consisting of the submucosa. The radial muscles of
the oval (rm) may be clearly seen. An arrow in the main cavity
of the swimbladder points to the almost completely closed opening
of the oval.

Fig. 2. Radiographs of Trisopterus minutus (above) and Lionurus
filicauda (xi), Note the very much sharper appearance of the
bones of the former.

DISCOVERY REPORTS, VOL. XXXI

PLATE III

•

- -.

WITH THE AUTHOR'S COMPLIMENTS

DISCOVERY
REPORTS

Vol XXXI, pp. 123—298

Issued by the National Institute of Oceanography

THE BENGUELA CURRENT

by
T. John Hart and Ronald I. Currie

Woods Hole Oceanographic institution
ATLAS GAZETTEER COLLECTION

CAMBRIDGE

AT THE UNIVERSITY PRESS

1960

Price seventy'five shillings net

<^>A~^^

PUBLISHED BY
THE SYNDICS OF THE CAMBRIDGE UNIVERSITY PRESS

Bentley House, 200 Euston Road, London, N.W. 1
American Branch: 32 East 57th Street, New York 22, N.Y.

Printed in Great Britain at the University Press, Cambridge
(Brooke Crutchley, University Printer)

[Discovery Reports. Vol. XXXI, pp. 123-298, November i960.]

THE BENGUELA CURRENT

By
T. JOHN HART AND RONALD I. CURRIE

4>_

CONTENTS

Introduction page 127

Previous work

Early voyages ....

Previous scientific observations

The work of the 'Meteor' Expedition

Methods used in the 'William Scoresby'
Observations and collections .
Estimation of salinity and phosphates
Estimation of dissolved oxygen
Treatment of the plankton samples

Itineraries ....
Survey I (March) .
Survey II (September-October)

Coastal geography and bottom topography

Meteorology

Wind systems .....

The trade wind .....

The coastal winds ....
Weather preceding and during the surveys

Surface-currents

Previous data ......

Currents during the surveys .

Observed distribution of temperature and salinity

First survey (autumn)

Horizontal distribution of temperature and salinity
Vertical distribution of temperature and salinity
Second survey (spring) ......

Horizontal distribution of temperature and salinity
Vertical distribution of temperature and salinity .
Stability of the water masses

The water masses

Water-masses of the South Atlantic
Temperature-salinity relationships of the South-west
Water masses of the upper layers (0-200 m.)

Oceanic and coastal surface-water

Dynamic height anomalies .

Surface topography

Topography of the 200 db. surface
Water masses at 200-600 m. .
The Antarctic Intermediate Water .

Upwelling

Previous work on the mechanism of upwelling

The effect of winds on the South-west African coast

Observed winds and hydrographical conditions

The mechanism of upwelling .

Depths affected by upwelling .

Centres of upwelling ....

Influence of the direction of the coastline

Seasonal variation of upwelling

African

waters

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'34

•35
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137
137
139

141
141
142

144

147
147
149
150

J53
153
'55

156
158
158
161
166
166
169
175

i75
!75
177
179
179
179
181
183
183
184

184
184
185
186
188
190
191
191
191

iz6 CONTENTS

Non-conservative properties p^ge 192

The distribution of dissolved oxygen l92

Normal and abnormal conditions within the current .... 198

The distribution of dissolved inorganic phosphate-phosphorus . . 201

Bottom deposits 204

MlCROPLANKTON 20D

Terminology and presentation of data 206

Taxonomic notes 2IS

Diversity of the microplankton 219

Distribution of the main groups of microplankton 225

First survey 225

Second survey 229

Distribution of the main diatom groups 234

First survey 234

Second survey ........••• 24°

Special distributional features 245

Observations on discoloured water . . . . . . . .252

The distinction between offshore and inshore diatom floras . . . 256
The cosmopolitan distribution of marine plankton diatoms and the
' ecological characterization ' of the more important species from the

Benguela current .......••• 263

ZOOPLANKTON 268

Polychaeta 268

Chaetognatha 268

Entomostraca 268

Ostracoda 269

Mysidacea 209

Cumacea ............ 27°

Amphipoda 27°

Euphausiacea . . . . . . . . • • • .271

Decapoda and Stomatopoda . . . . . . . . .271

Mollusca 271

Larvacea ............ 272

Eggs and young stages of fish ........ 272

Distribution of the zooplankton 273

Economic resources of the Benguela current 274

Fish and fisheries 274

Seals 274

Whales 275

Guano Islands 27S

Review of the main features of the Benguela current .... 277

Normal conditions ........... 277

Abnormal conditions .......... 278

Comparison of the Benguela current with other upwelling regions . 280

Organic production in the Benguela current 284

Summary 286

References 289

THE BENGUELA CURRENT

By T. John Hart and Ronald I. Currie
(Text-figs. 1-96)

INTRODUCTION

When the National Institute of Oceanography took over the ships of the 'Discovery Investiga-
tions' in 1949 one of the first objects was to round off some of the work done in the southern
hemisphere by the older organization. That research had included a survey of the Peru coastal
current, carried out by the R.R.S. 'William Scoresby' in 1931. The late E. R. Gunther, who was in
charge of the scientific work at sea, published a valuable report on the results of that survey, which
clearly demonstrated the need for further research in such areas. Other duties prevented further
work on the data collected from the Peru current prior to the war, and since then much work has
been done there by scientists from other countries. The smaller analogous region off South-west
Africa on the other hand has received less attention. The 'William Scoresby', however, was recom-
missioned in 1950 for a voyage to South Africa and the Indian Ocean, and accordingly our new
programme, planned in outline by Dr N. A. Mackintosh, allowed for a hydrological and plankton
survey of the Benguela current, at first in February-March, and (after subsequent alterations to the
ship's programme) again in September-October. There were thus two surveys, the first in the autumn
and the second in the spring. They were carried out on similar lines, but within the limits imposed by
other items in the programme, of which whale-marking was the most important.

In this report, which aims at providing a general interpretation of the observations made during
these two surveys, we apply the name ' Benguela current ' to the region of cool upwelled coastal water
along the South-west coast of Africa. This water, characterized by a pronounced negative surface
temperature anomaly is found mainly between 150 S. and 340 S., and within 100 sea-miles of the
coast. Thus it forms only the eastern periphery of the anticyclonic gyral of the South Atlantic, and
the adjacent circulation of warmer subtropical water to the westward is excluded. The latter we prefer
to speak of as the South-east Trade Wind Drift.1 This choice of nomenclature, avoiding the applica-
tion of the name Benguela current to the whole northward flowing limb of the gyral, has arisen from
evidence brought together both by Defant (1936) and in the present report, indicating that two
distinct current systems are involved, very much as Gunther (19360) found in the Peru current.
Moreover, the name ' Benguela current ' is very generally associated with the cold water, so that we
hope our restriction of the use of this name to the coastal element will not be misleading, and that it
may eventually become generally accepted.

The Benguela current, then, is one of those regions off the western coasts of the continents, where,
through the action of the prevailing winds, the effect of the earth's rotation, etc., the cool, nutrient-
rich subsurface waters well up to the surface. An intense production of phytoplankton throughout
most of the year is promoted thereby, resulting in an abundance of marine life of all kinds.

The rich life of the sea in this region is in striking contrast to the desert or semi-desert conditions
that prevail in the adjacent land areas. The cool water along the coast condenses the moisture from
the sea-breezes blowing towards the land, in much the same way as if a mountain range intervened,
and the coast lying to leeward, in the rain-shadow, as it were, becomes arid and desolate.

1 Hydrographic Department, 1939.

iz8 DISCOVERY REPORTS

The abundant marine life of the region contains much which is of value to mankind. Whales,
fur-seals, guano islands and potentially rich fisheries are all to be found there. Linked up with these
features are areas in the open sea along the coast, with extraordinarily low concentrations of oxygen
in the subsurface layers ; the bottom deposit of diatomaceous mud is devoid of all but a few highly
specialized forms of life capable of existing under almost anaerobic conditions, for sulphuretted
hydrogen is evolved through the action of sulphate-reducing bacteria, and locally, under conditions
not yet fully understood, this process sometimes increases to such an extent that even the surface
waters are affected (Copenhagen, 1934, 1953). This may prove to be one of the factors leading to the
recurrent mass mortalities of fish, another peculiar feature usually encountered near the northern
limits of the region. Later we shall refer to the lethal effect of oxygen deficiency but it can also
reasonably be argued that these mortalities are due more directly to the action of noxious water-bloom,
probably of dinoflagellates, since visible discolorations of the sea by super-abundance of living
organisms are yet another phenomenon frequently met with, often coincidentally with the mortalities
(Brongersma-Sanders, 1948). These mass mortalities and water-bloom formations, which usually
take place between midsummer and autumn, seem to link up with seasonal fluctuations in the physical
conditions; but the mortalities only assume catastrophic proportions at long intervals, and these show
no regular periodicity. Possibly they may follow accentuated deviations from the normal variations
in physical factors of the environment, for it will be realized that here again there is close analogy
with conditions sometimes encountered off Northern Chile and Peru: the aguaje phenomena, the
' Callao painter ' or ' el Pintor ', and the dreaded ' el Nino ' current.1 Further data bearing on these
problems were among our secondary objectives; primarily the surveys were planned to improve our
knowledge of the current system as a whole — the norm against which more pronounced local and
temporary deviations can be assessed.

Most of the earlier observations from the Benguela current formed but a small part of more extensive
programmes as the ships concerned passed down the coast on their way to the Indian Ocean; and
more recently, although four of the 'Meteor's' transatlantic profiles traversed the area, they were
necessarily carried out at widely separated intervals of time, so that the extent to which they are
comparable is limited. Dr Brongersma-Sanders, whose recent work provides an invaluable guide to
the literature, has also emphasized the need for more data (1947), and pioneer South African workers
in several different fields of research have done the same.

We endeavour to do full justice to previous workers in the next section of this report, but the point
has been raised here to show that even such limited observations as could be carried out on a small
ship over short periods could still be expected to further the knowledge of the region considerably.

The plan of the surveys consisted of three main lines of full ' stations ' (off 'Walvis Bay, Sylvia Hill,
and the Orange river) worked east and west, that is, nearly normal to the coast and to the main trend
of the isotherms ; and four lines of intermediate or subsidiary stations, the first in the northern part
of the area east and west, the second south-westward out to the offshore end of the first line of full
stations, and from the inshore end of each line of full stations to the offshore end of the next. The
east and west lines were disposed almost on the same latitudes as the eastern portions of previous
' Meteor ' profiles, and thus afforded some direct comparison with previous work. Positions of all the
stations and the 200 m. depth contour are shown in Figs. 1, 2 and 4 (pp. 143 and 146).

During the first survey (Fig. 1), we endeavoured to work the outermost station on each east- west
line in oceanic depths beyond the continental slope, and the spacing of subsequent stations was
therefore determined partly by the width of the shelf in the longitudes chosen and partly by practical

1 Hitherto known by this name in oceanographical literature, Schweigger (1949) has recently challenged the correctness
of this usage.

INTRODUCTION 129

considerations. In general they were from 10-25 sea-miles apart. At full stations complete series of
water-samples with temperature determinations at standard depths throughout the water-column
were obtained ; simultaneously standard series of vertical-closing plankton nets were fished down to
1000 m., or as deep as soundings permitted, and a vertical haul with the fine-meshed phytoplankton
net was made. Towed plankton nets were not fished during the first survey owing to lack of time.
Full details are given in the Station list (see references).

At the intermediate stations the ship was hove-to for a vertical haul with the phytoplankton net,
which enabled us to make temperature observations with the bathythermograph loaned by the
U.S. Navy, down to the limit of the depth range of the instrument (138 m.). Three hauls with a
commercial otter-trawl (WS 974, 990, 999) were made on the continental shelf, providing some
indication of the nature of the demersal fish-fauna and material for speciation studies in the genus
Merluccius (hake) by Mr N. B. Marshall of the British Museum (Natural History).

Seventeen full stations and twenty-two intermediate stations were worked, over the area of some
60,000 square miles, in nine days. We could not spend more time in order to make the coverage more
complete, since this could only have been done at the expense of the rest of the ship's programme.
Details of the itinerary are given below (pp. 141-144).

The second survey (Fig. 2) was essentially a repetition of the first, at the opposite season of the year,
but with more time available it became possible to increase the collections at the reoccupied stations,
and to make some additional observations. Oblique and horizontal towed plankton-nets were fished
at all full stations in addition to the vertical series, and horizontal towed nets at intermediate stations.
Bottom samples were collected at nearly all the stations on the shelf, and a few additional stations
were occupied for this purpose alone, to gain further knowledge of the distribution of thediatomaceous
'azoic' mud. The ship also worked in collaboration with Commander W. J. Copenhagen for a brief
period while in the Walvis Bay area, assisting in researches he has described in another report
(Copenhagen, 1953). Additional intermediate stations were worked both north and south of the area
previously covered, and alternate stations on the most northerly, east-west line were made into full
stations. Thus the number of full stations was increased to twenty and of intermediate stations to
forty-four (thirteen being bottom-sampling stations only).

Full details of meteorological, physical and chemical data collected, and biological collecting gear
used at each station on both surveys, are given in the Station List, already published in the Discovery
Reports (1953). Methods are described and discussed in a later section of this report.

The ship was commanded by Lieut. -Cmdr A. F. Macfie, O.B.E., R.D., R.N.R., whose experience
and ready assistance with the work at sea, and advice to the scientists when practical considerations
rendered modifications of programme unavoidable, were prime factors in the successful completion
of both surveys. Mr R. Baty, the chief Engineer, and his department gave unstinted help in servicing
scientific gear, despite unlooked for difficulties with other auxiliary machinery. Mr K. Maclean, the
chief officer, who organized the assistance needed from the watch on deck during station work, also
obtained valuable recorder runs with the echo-sounding machine, and with the bo'sun, Mr Yorke,
devoted much care to its maintenance. Mr M. R. B. Hawkins, the navigator, also recorded meteoro-
logical data, and Mr W. Slater, third officer and trawling expert, also helped in many ways outside
his routine duties. Such projects must always depend upon the able co-operation of the whole ship's
company, so that the data recorded and the biological collections made are a reflection of the way all
hands turned to at an arduous, unfamiliar assignment.

The scientific personnel were Dr T. J. Hart, Dr (then Mr) Robert Clarke and Mr R. 1. Currie.
Dr Hart was in charge of the work at sea during the first survey, handing over to Dr Clarke at the Cape

130 DISCOVERY REPORTS

as previously arranged. Dr Clarke's judgement in making additional observations during the second
survey, when more time unexpectedly became available, greatly increased its value. Owing to his
preoccupation with whaling research he has not participated directly in the writing of this report.
In preparing the account of the second survey we have frequently made use of his journal. That the
field work owed much to his efforts throughout should be obvious. All chemical estimations made at
sea were carried out by Mr Currie.

We are particularly indebted to the Director of the Marine Biological Association's Plymouth
Laboratory and his staff for unrivalled working facilities before the new premises of the National
Institute were available, for much fruitful discussion and for practical help. By arrangement with
Dr G. A. Steven, Skipper W. H. Crease with his crew of the R.V. ' Sula ', and the M.B. ' Gammarus ',
gave much help while the ship was in Plymouth on her outward voyage, and again on her return.

All our colleagues on the staff of the National Institute have assisted the work in some measure,
but special thanks are due to Dr G. E. R. Deacon and Dr N. A. Mackintosh for their valuable advice
and encouragement during the preparation of this report, to Dr H. F. P. Herdman for the care and
attention he devoted to the scientific equipment of the ship before sailing, and to Miss D. M. E.
Wilson for assistance in computing of values and checking data for the station list.

The assistance of the naval authorities who ' mothered ' the ship when she called at Devonport,
Gibraltar, Freetown and Simonstown, extended down to the provision of odd spares for what must
have seemed to them some very odd gear, and was, of course, absolutely essential to the successful
completion of this part of the programme.

We also wish to record our thanks to the Director of the Naval Weather Bureau for providing
relevant meteorological data; to Cmdr C. E. N. Frankcom, O.B.E., R.N.R., of the Marine Division,
Meteorological Office, and to Mr E. W. Barlow of his staff for data on surface drift and much helpful
discussion.

Dr J. H. Oliver assisted greatly in devising a suitably robust instrument for carrying out our
phosphate determinations and by providing laboratory facilities in London before the ship sailed.
Dr K. R. Butlin, of D.S.I.R., assisted by confirming the presence of sulphate-reducing bacteria in
the bottom-sample from St. WS 1074.

Many people in the Union of South Africa befriended the ship, both officially and personally.
Among those who helped more particularly with our Benguela current problems were: Dr C. von
Bonde, then Director of the Fisheries Survey Division, Department of Commerce and Industries,
and his staff, who gave us laboratory facilities and opportunities for discussion on many topics of
common interest. The Head of the South African Weather Bureau provided most valuable data.
Commander W. J. Copenhagen, with whom we have discussed plankton production and the 'Walvis
Bay problem ' over many years, introduced us to Dr Liebrandt, Director of Chemical Services, Depart-
ment of Agriculture, who provided chemical laboratory facilities on this occasion. Dr S. P. Jackson
of the Geography Department, University of Witwatersrand, gave most valuable advice on the
meteorological factors involved, as did Professor J. H. Day of Cape Town University on zoological
matters. Dr J. H. Maconnell of Walvis Bay, supplied some first-hand local information on the fish
mortalities.

PREVIOUS WORK

Early voyages
West African exploration received its greatest initial impetus in the latter half of the fifteenth century.
Continuing their pursuit of the Moors, the Portuguese initiated a series of somewhat warlike
exploratory voyages down the West African coast. Attempts to sail southward were for a long time

PREVIOUS WORK 131

defeated by a great reef off Cape Bojador, but this was eventually passed in 1433 or 1434, and further
voyages became more and more directed towards trading and colonization. King John commissioned
an esquire of his country, Diego Cao, to continue further exploration into the Gulf of Guinea, and on
his second voyage in 1484-6 Diego Cao penetrated southward beyond the mouth of the river Congo
(Ravenstein, 1900).

It was the custom of the Portuguese at this time to set up marble pillars surmounted by a cross,
with which to mark their achievements. These pillars, or 'padraos', had been introduced to replace
wooden crosses which were used before but found to rot away too quickly. Diego Cao carried several
of those padraos with him, constructed and suitably inscribed, before leaving Portugal. He set up
one at the most southerly point which he reached, naming it ' Cabos do Padraos '. It is now known
as Cape Cross. It seems that Cao sailed rather further south than this, to about 220 09' S., before he
returned to the north.

Interesting to note is a remark by Ravenstein (1900) on Martellus's chart, which documented the
discoveries of this period. He says, ' To the south of it [Cape Cross] on Martellus' chart, we notice
a Praia dos Sardinhas (sardine shore), now known as Sierra Bay. . .'. The position of this shore
coincides with the region where we now know that extensive mortalities of fish occur. It is possible,
therefore, that Diego Cao had observed such a mortality of sardines.

Diego Cao appears to have died on the return voyage, and the exploratory work was taken over by
Bartholomeu Diaz. Diaz left Portugal in 1487 and was the first to succeed in rounding the Cape of
Good Hope. He set up a padrao at Luderitz Bay (Diaz Point) and another at the Cape. The final
linking up of the trade route to the east was accomplished by Vasco da Gama (1497-9) (Ravenstein,
1898). One might conjecture that da Gama had benefited from the experience of his predecessors
for on his way to the Cape he stood well out to sea and first touched the South African coast at
St Helena Bay. In so doing he would have avoided the greater part of the contrary currents and winds
of this coast, and would have been able to tack into the trade wind, but there is, of course, no proof
that it was these considerations that led him to adopt such a route.

Although the early Portuguese place-names are very descriptive and tell us a lot about their observa-
tions, no detailed records of these voyages have been found. Several expeditions visited this coast in
the following centuries, principally in search of guano and further inland exploration, but not until
the nineteenth century have we been able to find any records of meteorological and hydrographical
observations.

Previous scientific observations
In 1820 Major James Rennell summed up the existing knowledge of the ocean currents' and this work
was published posthumously in 1832. With regard to the currents of the South-west African coast
he remarks (pp. 119 et seq.):

But we have no detailed accounts of the circumstances of the currents along-shore, between the parallels of 280
and 1 ii° south, although the existence of such is well known ; so that the continuity of the thread of current is never
broken between that in the Indian Sea and the Equatorial current. The first notice, from authority, of a current
hereabout, is its issuing from the deep recess of the coast of Benguela, between 9F and n° S., in a W.N.W. and
N.W. by W. direction, (as if the water had been forced in there) and with a rate of 14 to 25 and 30 miles per day.
From the just mentioned Bay of Benguela the current ranges along the coast to the N.W. receiving the waters
of the Zahir or Congo River, the outfall of whose waters runs nearly in the same direction with the sea current,
that is N.W., and only marks its character by the increased velocity of the stream, and the lowering of its temperature.

While commenting thus on the coastal currents, Rennell was well aware of the more definite drift
produced by the trade wind farther from the coast. This he called the South Atlantic current.

i32 DISCOVERY REPORTS

The generally accepted theory that the cold current along the coast was a direct flow from high
southern latitudes was held until the middle of the nineteenth century, although Rennell recognized
a continuity in the surface drift from the Indian Ocean to the Atlantic, around the Cape of Good
Hope. Sir James Clark Ross (1847) on his passage to the Antarctic carried out a series of temperature
measurements around the Cape, which show conclusively that the cold water on the west coast was
an isolated phenomenon, and was not continuous to the south. Whilst approaching the African Coast
in the vicinity of Paternoster Point on the 8 March 1840, he remarks:

By 1 p.m. the next day the temperature of the sea had fallen from 700 to 56-5° F., that of the air being 65 ° and
the mist unpleasantly cold to our feelings. We were at this time in 32° 21' S., 17° 06' E., therefore about 45 miles
from Paternoster Point, when we struck soundings in 127 fathoms on a bed of fine dark sand. We had expected
to have found an elevation in the temperature both of the air and sea on our approach to the African coast, by
reason of the heat radiation from its shores ; but the cause of the depression became evident on the morning of
the 9th, when having sighted Cape Paternoster at daylight, we found we had to contend against a current increasing
in strength and coldness of temperature as we neared the land.

Ross had to spend several days beating up to the Cape, and while doing so he took the opportunity
of making observations of temperature at different depths and distances from the land. These he has
tabulated, and from them he concludes :

All these circumstances combine to show that a northerly current of very limited extent, but of considerable force
exists from the Cape of Good Hope, along the western coast of Africa; which in general terms, may be represented
by a volume of water sixty miles wide and two hundred fathoms deep, averaging a velocity of one mile per hour,
and of the mean temperature of the ocean, running between the shores of Africa and the waters of the adjacent sea.
The cloud of mist which hangs over this stream of cold water is occasioned, of course, by the condensation of the
vapour of the superincumbent atmosphere, whose temperature is generally so many degrees higher than that of
the sea. It is sufficiently well defined to afford useful notice to seamen of their near approach to the land.

After leaving Simon's Town, Ross continued his temperature measurements, and
found the temperature of the surface of the sea to increase rapidly after leaving Cape Point, . . .showing that we had
got to the southward of the cold water current that runs along the west and perhaps the south coast of Africa.

It is evident therefore that this current does not come down directly from the south, as it only extends to seven
or eight miles from the Cape and beyond that distance we have to descend to over six hundred fathoms to find
water of so low a temperature.

These observations do not appear to have received very wide attention, for even up to 19 10
(Engeler), some authors upheld the continuity between the West Wind Drift and the cold current on
the west coast of South Africa. Findlay (1874), Bourke (1878) and Gallon (1883) all speak of a south
polar current on this coast, although Bourke appears to have been mystified by the patchy distribution
of the cold water. 'But the most remarkable feature of this N.W. current from the Cape of Good
Hope is the sudden manner in which its cold waters simultaneously appear along the land to the
northward of Cape Frio.'

The origin of the cool water by upwelling was inferred both theoretically and by comparison with
other regions by Witte (1880), Buchan (1895) and Schott (1902). It was finally confirmed by the
serial oceanographical observations of S. M. S. 'Mowe' (Schott, Schulz and Perlewitz, 1914).

Many early writers on the region make general references to its great wealth of marine life.
Pechuel-Loesche (1882, p. 283) writes of 'a species of herring Pellona africana that presses shorewards
from the South Atlantic current in immense shoals, from November to February '. Though most of
his observations were made far to the north, where the upwelling is a much more seasonal phenomenon
than in the region off South-west Africa, the analogy with the behaviour of other clupeoids farther
south is most striking. Pechuel-Loesche also appears to be responsible for the present name of the
current.

PREVIOUS WORK 133

As we have said, Rennell (1832) applied the name 'South Atlantic current' to the more definite
drift of the trade wind offshore. Later, Findlay (1867) called the current the ' South African current',
a name also used by Dankleman (1878). This name referred to the whole water movement off the west
coast of South Africa, and this again was termed the ' Sud-atlantische Stromung ' by Pechuel-Loesche
(1882). In a later paper, however, cited by Schott (1931), Pechuel-Loesche uses the name 'Benguela-
stromung'. The Africa Pilot, Part II, 1939, distinguishes two current systems, the South-east Trade
Wind Drift, and the Benguela current inshore, and as stated previously we have chosen to follow this
nomenclature throughout this paper.

Of the more recent expeditions to the South-west African region, that of the Valdivia has con-
tributed most to our knowledge of the biology of the region. The majority of their stations lay further
from the coast than we could have wished, but nevertheless their observations have helped to lay a
basis for later work. In collating these observations Schott (1902) was able to summarize the existing
data on the physical phenomena of the region, but of all the ' Valdivia's ' work that part which has been
of most service to our present investigations is the great advance in the taxonomy of many of the
southern subtropical organisms which resulted from her collections in adjacent waters. Karsten's
report on the phytoplankton (1906), which quotes from Schimper's field notes, has been a constant
help in working up the microplankton.

The voyage of S.M.S. 'Mowe' in 191 1 was more strictly concerned with surveying the coastal
regions, and some valuable physical and chemical data were collected. Evidently no biological ob-
servations were made. The physical data have been dealt with by Schott, Schultz and Perlewitz (1914)
and later by Franz (1920, 1921) who considered at length the seasonal fluctuations of the current.

Our knowledge hitherto of the oceanographical phenomena of the region is, however, based
principally on the extensive work of the Deutsche Atlantische Expedition 'Meteor'. The data
collected by the 'Meteor' enabled Defant (1936) to investigate the mechanism of the current system,
while numerous papers, among which Hentschel's work is outstanding, have provided an under-
standing of the general biology of the region. The 'Meteor's' work will be referred to later (p. 134).

Systematic collecting by the vessels of the Discovery Committee, which in these waters was mostly
during the winter months and off the southern part of the South-west African coast, has aided the
identification of our material, and has also been a guide to the extent to which species found in
abundance in the Benguela current are peculiar to that region, or are merely local concentrations of
wide-ranging oceanic forms. In this way both Hendey's report (1937) on the Plankton Diatoms of the
Southern Seas, and John's report (1936) on the southern species of the genus Euphausia, help in the
interpretation of the 'William Scoresby's' collections.

Much pioneer work has been carried out by the South African Division of Fisheries and Marine
Biological Survey under the direction of Dr J. C. F. Gilchrist and latterly by Dr C. von Bonde
and his successors. Dr K. H. Barnard of the South African Museum has been particularly active
among the many specialists working upon this material, and although the collections rarely extended
north of the Orange river, they form the basis of our knowledge of many species extending farther
north. Boden's account (1950) of the coastal plankton diatoms from Cape Peninsula to Lambert's
Bay has been a constant help.

Work on analogous conditions elsewhere has, of course, advanced our knowledge of the basic
physical and biological factors important in upwelling regions. Schott's work (1902, 1931, 1942,
1 951) on the Peru current and upwelling regions generally, has done much to show how closely
analogous the different upwelling regions are. Gunther's account (1936) of the work of the 'William
Scoresby ' in the Peru current, gives details of the current pattern, mortality phenomena and dis-
coloration of the sea, all of which are closely mirrored in the Benguela data.

i34 DISCOVERY REPORTS

Perhaps the best known of all upwelling regions, owing to its ready accessibility, is the Californian
current. Abundant recent researches into its oceanography carried out by various leading workers
show essentially similar relationships to those which we have found in the Benguela current. The
numerous references in later sections should show how valuable this work has been in interpreting
the present data.

One feature of the Benguela current region which has attracted widespread interest is the occurrence
of fish mortalities, particularly in the vicinity of Walvis Bay, and their possible causes, biological or
otherwise. The whole subject has been comprehensively discussed by Dr Brongersma-Sanders (1948)
who treats all the relevant literature thoroughly. This and further recent work, in particular some of
the results of the Danish ' Galathea ' Expedition (1950-2), will be discussed in the appropriate sections.

The work of the 'Meteor' expedition
The extensive data collected by the ' Meteor ' in 1925-7 have revealed the general pattern of the circula-
tion in the South Atlantic (Wiist, 1950) and the disposition of the observations was such that some of
them fell within the South-west African region. This enabled Defant (1936) to present the most
complete account of the region so far.

The ' Meteor ' observations consisted of several more or less latitudinal lines of stations across the
Atlantic Ocean. The eastern ends of five of those great sections fell within the Benguela current, and
it is those stations which Defant used. Defant supplemented his study of the ' Meteor ' observations
by a new analysis of the Dutch surface current observations. These he meaned in one degree areas
(one degree of latitude by one degree of longitude) for each quarter of the year, and his results
(Fig. 6) present us with an interesting new interpretation of the surface water-movements. The out-
standing feature of these current charts is that they reveal a one-sided line of divergence. It lies- in
a N.N.W. direction along the coast, from about 200 to 300 S. In the south it is about 160 sea-miles
from the coast, and in the north 300-350 sea-miles. To the west of this line the current sets to the
west, but to the east of it the current runs more or less parallel to the divergence but is somewhat
irregular on its coastal boundary.

Comparing this system with the iso-anomaly lines of surface temperature (the lines of equal
difference from the latitudinal mean) Defant further finds that the region of strongest negative
anomaly, the coldest water, is confined to the coastal current, and is most marked in the region between
230 and 310 S. where the divergence is also most pronounced.

The vertical thermo-haline distribution on the five ' Meteor ' ' Profits ' shows a correspondingly good
agreement with the surface picture. 'Profil' IV in 340 S. shows but little evidence of upwelling close
against the land, while on 'Profils' II (28A0 S.) and VII (220 S.) the characteristic uplift of the iso-
therms and isohalines against the coast indicates the upwelling of the subsurface-waters from a depth
of about 300 m. The more northerly 'profils' suggest a sinking rather than an uplift of water against
the coast. In 'Profil' VI (15-160 S.) the isotherms and isohalines, at a depth of 30-40 m., descend
toward the coast, and in 'Profil' VIII (90 S.) this is even more pronounced. Thus the region of most
intense upwelling, as adduced from the vertical pictures, corresponds with the position of the most
marked negative surface temperature anomaly and the most well-defined divergence in the surface
currents.

Defant then considers theoretically the problem of the circulation by examining the effect of winds
on two bodies of water of different density lying in a canal. This will be discussed in more detail later,
but for the present it will suffice to say that by applying his derived theory to the South-west African
waters, he concludes that outside the divergence there must be a vertical eddy in the upper layers.
Below the axis of this eddy the water will move towards the east, ascending to the surface inside the

METHODS USED IN THE 'WILLIAM SCORESBV 135

divergence line and producing in the coastal waters a distribution of density such that a current will
form parallel to the coast. Seawards of the divergence line, and in the upper part of the vertical eddy,
the water will be transported offshore.

Studying the general biology of the region, Hentschel (1936) found it necessary to adopt some
arbitrary spatial definitions of the several sea areas he discussed. The 'ten degree field' extending
westwards as far as St Helena which he took as his Benguela current region has unfortunately masked
the great richness of the coastal current inshore. Consequently most of the generalizations he felt able
to make apply rather to the subtropical oceanic surface water. Of the existence of the rich coastal belt
he was, of course, very well aware. This was the only part of the region where large quantities of
diatoms were to be found among the microplankton. He did not, however, regard the coastal current
as distinct from the oceanic circulation, whereas our present results indicate that the natural boundary
between the two types of surface-water is more significant than any of the boundaries of his arbitrarily
chosen areas. No doubt he was unable to demonstrate the effect of this natural boundary on account
of the wide spacing of the ' Meteor ' stations, and the fact that the physical data were only partly
digested by the time his work was published. His reference to the characterization of the region by
the steep east-west gradient in microplankton quantities rather than by an abrupt transition such as
our results indicate, his inclusion of many warm-water forms among the characteristic dominants of
the region, and his insistence on the dominance of Dinophyceae over Diatoms among the protophyta,
all arise from the same causes. Provided this is all borne in mind it can be seen that his generalizations
are in very good agreement with our own findings — that is, apart from his insistence on the importance
of the ' South-west Africa Tongue ' which will be discussed later.

While extremely valuable for interpreting the large-scale picture, the 'Meteor's' observations
unavoidably had the disadvantage of being widely spaced both in time and geographically, and the
'William Scoresby' surveys can be considered as the next logical step in making a more localized and
intensive study of the Benguela region in particular.

METHODS USED IN THE 'WILLIAM SCORESBY'

Observations and collections
Throughout the two surveys the watch-keeping officers maintained regular meteorological observa-
tions. In addition to those kept at four-hourly intervals, further records were taken while the ship
was occupied on ' station '. The observations included personal estimates of the force and direction of
wind, sea and swell, and instrumental records of barometric height, and dry- and wet-bulb temperature.

Continuous echo-soundings were made whenever possible, but these were restricted to the conti-
nental shelf and slope, as the depth range of the machine (720 fathoms, 1317 m.) did not permit any
deep-water sounding. The latter were eventually obtained by a Lucas wire-sounding machine, but
unfortunately this was not functional during the first survey. On the second survey, however, the
Lucas machine made it possible not only to obtain deep soundings but also to delimit the extent of
a region of reducing mud on the sea floor. For this the sampling technique depended upon the nature
of the sediment, and both Baillie rods and snapper leads were found effective. The samples were
preserved in alcohol after a preliminary examination.

The 'William Scoresby' was fitted with a distant-reading thermograph which provided a con-
tinuous record of the sea temperature. Since the bulb of this instrument was installed in the engine
condenser intake, the record represents the temperature at a depth of about 4 m., but this of course
varied considerably with the degree of loading of the ship. Checks on the accuracy of the instrument

136 DISCOVERY REPORTS

were made frequently by comparison with insulating water-bottle measurements, and showed no
significant deviation from the original calibration.

It was decided while planning the surveys that intermediate observations of temperature between
the lines of full stations would be invaluable in constructing a detailed picture of the upper layer
circulation. For this a bathythermograph was used. The instrument, the standard U.S. Navy pattern
manufactured by Wallace and Tiernan Prod. Inc., New Jersey, conformed to the specifications of
accuracy prescribed by the makers. (Temperature ±o-i° F. and pressure ±4^ ft. with a depth limit
of 450 ft.) Frequent calibrations of both temperature and pressure elements indicated a remarkable
constancy, and no correction of the results has been necessary.

All water-samples were taken by standard methods, at the depths recommended by the Association
Internationale d'Oceanographie Physique. The Nansen-Pettersson insulating water-bottle was used
for sampling the shallower depths, as a rule not over 400 m., but on certain occasions it was operated
to a depth of 600 m. when an additional reversing hoist could be omitted thereby. At greater depths
Munro-Ekman reversing water-bottles were employed. Three of the latter were used in each hoist,
and while all carried two protected reversing thermometers, the upper and lower bottles were equipped
with unprotected reversing thermometers as well.

Biological collecting during the surveys was mainly confined to standard series of plankton net
hauls. The nets used and method of fishing were similar to those employed during the pre-war work
of the Discovery Investigations (Kemp, Hardy and Mackintosh, 1929). The vertical series at full
stations in oceanic waters included hauls with the Nansen pattern closing net, 70 cm. diameter at the
mouth (N 70 V), at depth intervals of 50-0 m., 100-50, 250-100, 500-250, 750-500 and 1000-750 m.
At shallow water stations the series was modified so as to work as close to the bottom as possible.
A 100-0 m. vertical haul with the N 50 V phytoplankton net was also made. During the second
survey oblique hauls were made with the i-m. stramin net (N 100 B) and 70 cm. silk tow-net (N 70 B)
on 200 m. of warp, maximum depth being recorded by Kelvin tube, and a i-m. net (N 100 H) was
also towed horizontally at the same time. These were in addition to the vertical series. Towed nets
were not used during the first survey. In addition to the hauls at full stations, the N 50 V was worked
at all the intermediate bathythermograph stations on both surveys.

A full-sized commercial otter-trawl (OTC) and conical dredge (DC) were used at a few stations on
the shelf during the first survey, and during the second, numerous bottom-samples were collected
with snapper-lead and Baillie rod. Full details of dates, times, etc., at which these types of gear were
used are given in the Station List (1953) which also includes full definitions of the standard abbrevia-
tions employed.

The centrifuging of water-samples was not employed as a routine method for phytoplankton
sampling, but was used for provisional identifications of dominant organisms in areas of discoloured
water, whence surface-samples were preserved for subsequent analysis.

It was important above all to extend the basic physical and chemical observations over the widest
possible area, and it was mainly for this reason that we did not attempt more comprehensive work on
the phytoplankton, and more particularly on the smaller organisms known to escape nets. The Harvey
method of pigment extraction from the catch of a fine-meshed vertical net fitted with a flow-meter
(Harvey, 1934), which had proved most useful in the antarctic zone (Hart, 1942) was not used because
it was already known from the 'Meteor' results (Hentschel, 1936) first, that dinoflagellates were of
vastly greater relative importance in this area than in the antarctic, and their mixed pigments tend
to vitiate direct visual colour match ; secondly, that the nanno-plankton forms would similarly be of
greater relative importance here. In the event, we found diatoms so numerous in the rich coastal belt
that the earlier form of Harvey's method would most certainly have yielded valuable results. More

METHODS USED IN THE "WILLIAM SCORESBY' 137

recent refinements of the pigment extraction method successively developed by Riley (1938), Krey
(1939) and Richards and Thompson (1952), should certainly prove a most valuable line of investiga-
tion in the Benguela current area.

Estimation of salinity and phosphorus
The confined laboratory accommodation on board the 'William Scoresby' made it necessary to
restrict as much as possible the amount of analysis carried out in the ship. Estimations of at least
salinity, phosphate and oxygen were desirable for the work. Of these properties the salinity is by far
the most stable, and unaffected by normal storage, and it was decided to keep the salinity samples for
later analysis on shore. This has been the practice in the past on board the 'William Scoresby'. The
estimations were eventually made by the Government Laboratory, London, to whom we owe our

thanks.

The Atkins-Deniges colorimetric method was used for the determination of the dissolved inorganic
phosphate-phosphorus. Recently, many new photometric systems have been described, which
facilitate the colour comparison and attain a high standard of accuracy, but after experimentation both
before the cruise and later on board the ship, it was decided that in the conditions in which we worked
a visual comparison would yield the most satisfactory results of the required degree of accuracy.
This method was adopted and we are greatly indebted to Dr J. H. Oliver for perfecting a suitable
instrument for the purpose.

A Lovibond type of colorimeter was used. This had a series of thirty-three specially made glass
slides, with colours flashed on to them representing a range in phosphate concentration from 0-03 to
3-00 mg. atoms P/m.3 The slides were calibrated by the same operator in a shore laboratory, against
standard phosphate solutions (KH2P04) made up in phosphate-free sea-water. (This latter, of salinity
35-oo%„, was collected for the purpose in the Gulf of Guinea.) This procedure obviated any salt-error
in the estimation. The sensitivity of the method varies slightly with the intensity of colour, and is at
its lowest, ±0-05 mg. atoms P/m.3, at concentrations of 3-00 mg. atoms P/m.3 All the phosphate
samples were analysed within a maximum of 10 hr. after collection.

Estimation of dissolved oxygen
Winkler's method was used for the determination of dissolved oxygen. The samples were stored under
a water-seal in the precipitated form (Mn(OH)3) and all were analysed within 20 hr. of collection.
Standardization of the sodium thiosulphate was effected by titration with an approximately equal
strength (0-22 n) solution of potassium iodate. This standard, kept in a slightly alkaline solution,
proved very stable even in the most adverse climatic conditions.

For normal sea-waters the Winkler method works very well, but in the presence of certain con-
taminants the analysis can lead to erroneous results. It was to be expected, therefore, that in the
vicinity of the South-west African coast, where organic production is very high, such contamination
might be encountered. The principal sources of interference were considered to fall into three groups:

1. Large quantities of micro-organisms in the samples.

2. Relatively high concentrations of nitrites.

3. The presence of hydrogen sulphide.

Organic matter can affect the Winkler estimation in two ways. First, direct oxidation of organic
matter is very rapid around pH 12-0, and this might occur during the initial alkaline stage of the
analysis. Secondly, the iodine when liberated is liable to be absorbed by the micro-organisms. As
it was not possible to analyse all the samples immediately after collection, and as they would have to
be stored in one or other of these two stages, it was necessary to decide which course would cause the

138 DISCOVERY REPORTS

least interference. Experiments on the determination of oxygen in dilute dinoflagellate cultures were
made at the Marine Biological Association's Laboratory at Plymouth before the cruise. Those demon-
strated that the principal interference took place through absorption of iodine by the dinoflagellates.
Samples titrated immediately after acidification and liberation of the iodine showed a higher oxygen
content than those titrated 2 hr. after acidification. In this period the mean absorption of iodine
was equivalent to 0-4 ml. of oxygen per litre at 150 C. in 3 hr. No difference was observed in samples
stored in alkaline-precipitated condition for periods up to 10 hr. It was decided, therefore, to store
samples in the latter condition.

Allee and Oesting (1934) found that quantities of nitrite of 071 mg. atoms N/m.3 and over were
sufficient to affect the Winkler method. The interference occurs through the nitrite's liberating iodine
from the potassium iodide and giving a greater quantity of iodine than would normally be released
through the acidification of the manganic hydroxide precipitate in the presence of potassium iodide.
The error is, of course, to overestimate the amount of oxygen present. 071 mg. atoms N/m.3 is quite
a high figure for the sea, but as no nitrite estimations were made the extent of any error likely to arise
was unknown. The modified Winkler method used to deal with hydrogen sulphide, however, also
removes any interference due to nitrite.

Some of the sediments on the sea-bed in the region of Walvis Bay are populated by sulphate-
reducing bacteria, whose activity results in the production of hydrogen sulphide. This gas, liberated
into the overlying water, appears to coexist, in a dynamic state, with the dissolved oxygen (Durov and
Turzhova, 1947). To obtain a true estimation of the oxygen content at a particular time and position
it was necessary, therefore, to put an end to the oxidation-reduction reaction as soon as possible after
sampling. Although Alsterberg's method (1926) would have been preferable we tried to accomplish
this by using the Rideal-Stewart modification of Winkler's method, which could conveniently be
carried out with the chemicals available on board. The method consists of a preliminary oxidation,
carried out by treating the acidified water sample with potassium permanganate. When the reduction
is complete any remaining permanganate is destroyed by the addition of potassium oxalate, after which
the normal Winkler method is continued.

Parallel determinations on samples from Walvis Bay with both the Rideal-Stewart and unmodified
Winkler methods gave the results shown in Table 1.

Table 1. Dissolved oxygen content of water-samples from Walvis Bay

Sample no.

1
2

3
4
5
6

7
8

Oxygen determinations on water-samples taken in Walvis Bay using both the Rideal-Stewart and unmodified Winkler
methods. The samples have been arranged in order of concentration, and they were all analysed at the same intervals after
collection.

A further test was carried out on four similar samples with the unmodified Winkler method. Two
of the samples were analysed immediately after collection, while two were kept for 4 hr. before
analysis. The first two showed respectively 041 and 0-39 cc. 02/l. more than the second two. If this

Dissolved 02 content
(cc. 02//)

Unmodified Winkler

Rideal-Stewart W

o-oo

0-03

o-oo

0-09

o-oo

o-i 1

°'°5
0-30
0-46
0-64
o-68

0-13
0-38
0-51
o-8o
o-88

METHODS USED IN THE 'WILLIAM SCORESBY' 139

reduction in the oxygen content of the second two samples was solely due to reduction by hydrogen
sulphide, the result would indicate that a concentration of about o-8 cc. H2S/1. had been oxidized in
the 4 hr. which elapsed. Unfortunately we had no opportunity of making more experiments of this
nature, and it is not possible to say precisely how efficiently the Rideal-Stewart method accomplished
the task which it was set.

TREATMENT OF THE PLANKTON SAMPLES

The microplankton catches (N 50 V samples) were worked up by a counting technique essentially
similar to Hensen's method, as described by Steuer (191 1). From the whole sample, thoroughly
mixed by agitation in a spherical Stempel flask, subsamples were drawn off with an 0-5 ml. Stempel
pipette and placed in a cell on a large slide, ruled with squares of approximately i-8 mm. These can
almost be contained within one field of the low-power objective (-§ in.) of an ordinary compound
microscope. The cell was originally intended for counting centrifuged samples at sea, where a cover-
glass must be used. It measured approximately 10 x 24 of the squares and 0-4 mm. in depth so that
almost exactly 0-3 ml. of fluid could be contained in it, trapped under a large rectangular cover-glass.
For this work cover-glasses were not used during the early stages of the counts, but the cell was found
very convenient to contain the larger volume of fluid while spreading it over the face of the slide with
a mounted needle. When difficult rich subsamples prolonged the counting, or higher powered
objectives than the £ in. were needed for identification, it was found that evaporation at room tempera-
ture allowed one to apply a cover-glass after some 45 min. Most of the counts took more than 2 hr.
and continuous observation for a longer period increased personal error due to eye-strain, though
a brief pause sufficed to counteract this. Thus the use of a cover-slip during the later stages, to prevent
the preparation drying up, became an essential part of the technique.

The rulings on the face of the slide enabled one to resort to higher magnifications, or to recapitulate
when necessary, without ' getting lost ', and it was thus quite practicable to work through the whole
subsample, using a large mechanical stage. A very abundant inshore pennate diatom, Fragilaria
karsteni, has the habit of growing in very long ribbon-shaped colonies, and it was found that the
numbers of frustules could be estimated rapidly, and with a high degree of accuracy, by measuring the
ribbons under low power with a micrometer eyepiece, then measuring the width of a few individual
frustules under high power and dividing appropriately.

For the method as a whole to be successful the subsample must not be so thick that individual cells
or colonies obscure each other unduly. With large samples this was avoided by preliminary fractioniza-
tion and adjustment of volume, using a large (5-ml.) Stempel pipette and measuring cylinders for
added water. Errors were obviously increased by such a crude method, but could be reduced by
making separate counts at different dilutions for the more difficult stations, and pooling the results ;
and by such expedients as counting large or conspicuous species at normal dilutions where the density
of smaller dominant species necessitated further subsampling before they could be counted. When
the general nature of the flora had become familiar it was nearly always found possible to judge the
extent of fractionization and dilution needed from the settlement volume and macroscopic appearance
of the sample. At worst two trials enabled the necessary adjustment to be made.

The main object of this line of work was to study the spatial distribution of the larger phytoplankton
organisms in relation to the hydrological features of the area. Obviously such estimations can bear
little direct relation to the total amount of phytoplankton present — it has long been known that there
are many autotrophic organisms among the minute forms that escape the finest nets — but it is claimed
that, so far as the diatoms and larger dinoflagellates are concerned, they show up the grosser quanti-
tative differences quite fairly in areas such as this, where the gradient of population density is very

i4o DISCOVERY REPORTS

steep. The quantitative differences are so marked, as between the coastal current and the oceanic
surface-water to the west, that even such crude measures as settlement volumes can be shown to be
statistically significant.

The numerically estimated totals of Protophyta, and of dominant groups or species, when plotted
logarithmically, showed distributional patterns in good agreement with hydrological features inde-
pendently assessed. Moreover a 50% alteration, in either direction, of the values assigned to the
contour lines made little difference to their position on the chart. Crude as the method undoubtedly
is, errors of this magnitude are very unlikely and the counts are therefore believed quite fairly to
represent the broad outlines of the distribution of such organisms as were retained by the finest grade
of bolting-silk. All the counting was carried out ashore, while working at the Plymouth Laboratory.

The great variety of the Benguela current plankton is shown by the fact that although only diatoms
and Ceratia were identified down to species, the raw counts include some 200 categories of organisms.
This unfortunately makes it impracticable to publish them in full, but the tables of derived values,
dealing with group totals and relative abundance of more important categories, show the number of
categories observed during each estimation, in addition to volumes and fractions of samples examined.
This should give some idea of the qualitative richness of the microplankton of the area in addition to
its great quantity.

For the study of relative importance of the various categories these counts should be quite satis-
factory since several hundred individuals were involved in most of them. More than 300 individuals
were counted at 79 % of the stations, and at more than half of these (42 % of the total) over 600 indivi-
duals. Only at the very poor stations, where concentration (as opposed to dilution) might greatly
have increased the manipulative errors, did the numbers fall below 300 per station. These poor
samples constituted 21 % of the total and the numbers of individuals counted in them ranged from
90 to 288 with an average of 209.

Changes in relative abundance are important when it can be shown that species or groups have
'indicator value'; that their distributions are mainly restricted to water-masses that can be dis-
tinguished by their physical attributes. When this can be established, plankton distributions may
provide evidence of water-movement and of areas of mixing, of real value to the physical oceano-
grapher and to fishery research.

It has proved impossible to complete group-sorting of the zooplankton collections in time to con-
sider them fully in this report. The vertical net series for the first survey have been almost completely
sorted, and individual zoologists able to work up some of the groups have come forward. In this
general description of the plankton conditions, we have mentioned only such important (and often
elementary) features as became apparent at the sorting stage, adding specific identifications confirmed
or established by specialists whenever it has been possible to do so. Some reports on single groups
have already appeared and acknowledgements to those who are aiding the work in this way will be
found in the zooplankton section. Examination of second survey material has only been completed
for pilchard eggs, larvae and post-larvae, the importance of which became apparent at an early stage.
A preliminary account of their distribution has already appeared (Hart and Marshall, 1951).

Complete sorting of all groups, except Protozoa, Coelenterata, Copepoda and small nauplii (mainly
of Copepoda), has been attempted. For the latter subsampling proved the only practicable procedure,
and at a few very rich stations subsampling had to be adopted for some of the other groups also.
Nearly all the work has to be carried out under a binocular dissecting microscope, since many of the
animals were much smaller than their relatives in cold seas. We are very grateful to Dr M. V. Lebour,
and others working at Plymouth who have occasionally corrected or confirmed provisional identifica-
tions for us.

DISCOVERY REPORTS 141

ITINERARIES

Survey i (march)
On the afternoon of the 1 March 1950, the 'William Scoresby' proceeded southward from Lobito
Bay towards the outer end of the first line of stations (WS 964, see Fig. 1). This course involved some
two days steaming, and it was not until early on the morning of 3 March that the first indications of
the Benguela current were met with. In 160 13' S., n° 31' E. the distance thermograph revealed a
sudden decrease of sea temperature from 270 C. at 02.45 hr. to 20-5° C. at 03.45 hr- At the same time
the echo-soundings showed a sudden increase in depth from 1 10 m. to 439 m. followed by a return to
the shallower 1 10-m. level. During the day the temperature rose again, but not to its initial (tropical)
level. Evidently the ship had crossed one of the most northerly patches of the cold upwelled water so
characteristic of the Benguela system. This may possibly have been associated with the indentation
of the continental shelf indicated by the soundings.

The projected position of the first station was reached just after noon on the 4th, and during the
rest of that day six stations were completed, at intervals of some 18 sea-miles, as we worked eastwards
in towards the land. The weather was moderately favourable at the first station ( WS 964) and improved
as land was approached. Station WS 970, marking the inshore end of the 'Mowe Point' line was
completed at 01.27 hr. on the 5th, and the course was continued south-westwards working the five
stations of the northern intermediate line (WS 971-5) throughout that day. The wind and sea
increased as we proceeded offshore, but fortunately moderated again on the morning of the 6th when
we reached the first full station position, WS 976 in 220 50' S. 1 1° 38' E., the outermost station of the
'Walvis Bay Line'. This and the following day were spent in completing stations WS 976-9, and on
the morning of the 8th, after stations WS 980 and 981, the ship went into Walvis Bay. Here some
arrears of chemical analyses were dealt with and some useful information on local fishery matters was
gleaned from some of the residents.

Leaving Walvis Bay on 9 March, the ship passed through large areas of discoloured water, mainly
of an olivaceous colour, with small patches of a deeper brown or reddish colour. Surface samples
were examined, showing immense numbers of diatoms with but few Gymnodinium spp. The more
densely coloured patches contained a small dinoflagellate, which subsequent work on preserved
material has shown to be Peridinium triquetrum. Seals (apparently fur-seals) were seen playing lazily
in the discoloured water. Our course lay south-westwards, and the middle line of bathythermograph
stations was completed by 04.38 hr. on the 10th. At 08.05 hr- the first full station of the ' Sylvia Hill '
line was begun in fine weather, and the clear, almost metallic blue colour of the water here formed
a sharp contrast to the turbidity of that inshore. The Nansen-Pettersson water-bottle was visible at
a depth of 20 m. By the end of the station, however, the water was obviously more opaque, and
steaming eastward we again passed through more discoloured patches within the hour, and con-
tinued to do so until 17.05 hr. At station WS 986 there was much macroplankton about the ship;
many Ctenophores, mainly in a necrotic condition, and colonies of Salps, were taken out with the
hand net. Small shoals of fish were seen, but could not be sampled.

The 'Sylvia Hill' line was completed before dawn on the nth, and proceeding south-westwards
again, on the southernmost line of bathythermograph stations, an otter trawl was used at WS 990.
The catch contained several large hake, a fair selection of the other common ground-fish of the region,
and some good specimens of Stomatopoda. The outer station of the ' Orange river ' line, WS 996, was
reached at 15.55 nr- on the J lth anci tne remaining stations of this line were continued in fine weather,
being completed by 03.45 hr. on the morning of 14 March.

Further observations would, of course, have been desirable, but the commitments of the rest of the

3-2

i42 DISCOVERY REPORTS

programme, and the rather urgent need for repairs to some of the auxiliaries, was such that we had
been fortunate in carrying out most of the coverage planned before proceeding to Simon's Town,
where we arrived on 16 March.

Survey II (September-October)
The second survey of the current had not originally been contemplated, but preliminary examination
of the results of the first survey indicated that a repetition would be very desirable, and subsequently
a necessary alteration in the programme of the ship made it possible. It was decided that certain
extensions to the programme would greatly enhance the value of the repeated stations. Details of this
expanded programme were decided upon by Mr Clarke, and its value can readily be appreciated from
the results obtained.

Leaving Simon's Town on 19 September 1950, we worked a series of bathythermograph stations
(see Fig. 2) round the Cape of Good Hope, and up to the Orange river mouth where the ship arrived
on 21 September. Numerous fur seals were encountered on this journey, and several fairly extensive
patches of olivaceous coloured water were crossed. Full stations were worked in approximately the
same positions as on the first survey, while the ship steamed out along the Orange river line, and this
was completed on the 23rd. Our course now lay north-eastwards, repeating bathythermograph
observations, and the inner end of the ' Sylvia Hill ' line was reached on the 25th. The full stations
WS 1064 and 1065 were completed by about midday on the 26th, and then a slight diversion was
made to take some bottom samples to the north of the line. This included a circumnavigation of
Hollam's Bird Island, a guano island concerning which the following extract is quoted from Dr Clarke's
journal:

By 1700 hrs. we had approached to within half a mile of Hollam's Bird Island. As we steamed over the shelf which
surrounds the island, the echo-sounder showed several fish shoals, densely packed, in ten fathoms of water.

The island is small and low, not rising more than forty or fifty feet in its highest part. . . . An elaborate sheerlegs
is a conspicuous feature of the island, and its skeleton framework overhung the rock strandflat and adjacent breaking
water, like some part of the wrecked architecture of an amusement park — even to the strings of electric lamps
counterfeited by rows of cormorants sitting equally spaced along the struts of the sheers. Near this structure stood
a small roughly built shed — the island is visited at times by the government guano collectors.

The higher ground lay back from the landing place, and from these higher parts the cliffs fell away steeply, the
yellowish rock face being boldly streaked with white spillings of guano. And everywhere, crowded thickly upon
the slopes, and as far as the highest point, were the fur seals. As we came within half a mile we could hear their
barking above the drumming of the surf. From a distance it was a dog-like noise, like many packs of hounds, only
deeper in tone. The din must have been tremendous for anyone landing there and walking among the crowded
seals. There were many hundreds of seals on this scrap of rock: I made no estimate, but Mr Currie put the popu-
lation around 1300, probably more. The island with its multitudinous seals looked like a currant cake, of the kind
children call 'flies' funeral'. The shiny coats caught the sun, and reflected so many black points, some in slow
movement and some quite still, on the wet slopes and crags. Most movement was on the lower rocks, near the land-
ing-place, where the heavy surf was lively with heads and flippers and the strandflat populous with seals coming
and going from the water.

Although I could only, from the distance at which we sailed, identify among the birds the cormorants on the
sheers, there were obviously great numbers of birds grouped among the seals. At 1700 I counted flocks of about
fifty cape gannets, fifteen cape cormorants and five southern black-backed gulls ; and also five cape pigeons, although
these were farther off.

The visit to Hollam's Bird Island was worthwhile if only to have seen so much life on this tiny island off
the barren 'Skeleton Coast' — life so teeming that only a scene in Antarctic seas is comparable. It brought home
more vividly than anything else how real and astonishing are the effects of the productivity of the Benguela
Current.

ITINERARIES

'43

Fig. i. Station chart, survey I, March 1950. Positions of
' bathythermograph and phytoplankton ' stations are shown
by open circles, those of ' full ' stations by closed circles.

Fig. 2. Station chart, survey II, September-October 1950.
Symbols as in Fig. 1. Solid inverted triangles indicate
positions of bottom sampling-stations.

After visiting Hollam's Bird Island we completed the full stations of the central line, and the ship
steamed towards Walvis Bay making bathythermograph observations at WS 107 1-4. On the 29th the
'Walvis Bay' line was started and worked out to WS 1079, after which further station work was
delayed by a strong southerly gale which set in. The ship was hove-to for two days while the gale
increased to force nine (Beaufort), and not until the afternoon of 2 October did it abate sufficiently
to permit us to continue observations, whereupon stations WS 1080 and 1081 were completed, and
the ship sailed to Walvis Bay.

i44 DISCOVERY REPORTS

After we left Walvis on 6 October, a series of bottom-samples were taken up past Cape Cross
(WS 1082-7), and then the bathythermograph observations were resumed, and continued up to
Mowe Point, with two detours (WS 1092 and 1094) inshore for bottom sampling, en route.

In this area, and also on the 'Mowe Point' line station, numerous large shoals of fish were
encountered. Here again, we quote from Dr Clarke's Journal:

9th October, 1950. In the early hours of today (0100 to 0430) the officer of the watch reported that the ship steamed
through large shoals of small fish, like herring or pilchards. This was in position 200 35' S., 120 55' E. to 200 10' S.
i2°3o'E.

Again from 2015 to 2145 (around 190 43' S., 120 36' E.) we found ourselves passing multitudinous shoals of
fish. It was a dark night, and I stood and watched the shoals scatter from our approaching forefoot, one after
another, betrayed by a burst of greenish blue luminescence, so that the shape of each fish showed up in ghostly
outline. Below the forefoot, and fanning out to port and starboard, the shoals were like the showery explosion of
roman candles under water.

I counted a hundred shoals (each estimated at > 100 < 1000 fish) appearing in 4 minutes 23 seconds, or 0-4 shoal
( > 40 < 400 fish) per second ; the ship was then steaming at about eight knots.

The ship was stopped in an attempt to catch some of these fish with both baited hooks and jiggers,
so that the species might be determined, but all efforts were unsuccessful.

Further station work was continued with two short interruptions to mark some whales, and the
second survey completed on 12 October.

Two bottom-samples were taken to the north, at WS 1 106 and 1 107, to ascertain if the 'azoic ' mud
extended so far north. Approaching station WS 1107, between 14.15 and 15.21 hr. on 14 October,
patches of blood-red water were observed, some 20-30 yards across, a bucketful was collected, and
microscopic examination of preserved subsamples showed that the organisms causing the dis-
coloration were almost certainly ciliate protozoa such as have previously been seen to cause red
water elsewhere (see p. 255).

COASTAL GEOGRAPHY AND BOTTOM TOPOGRAPHY

The west coast of South Africa stretches in a more or less N.N.W. direction from the Cape to about
1 8° S., then continues north and N.N.E. into the Bay of Benguela. Practically the whole length of
this coast is characterized by a narrow coastal belt of low-lying land gradually ascending to the high
interior plateaux at a distance of about 80-100 miles inland. The coastal belt is fertile in the south,
but gradually passes into scrub, and north of 300 S. is a truly arid desert. This desert, which con-
tinues to about 140 S., is known in South-west Africa as the Namib. It is almost completely waterless,
although heavy dews occur, and the small annual rainfall (Fig. 3) generally occurs in a very short
space of time, draining into the Atlantic almost as quickly. The dew is sufficient to support a very
scanty xerophytic flora, but cultivation is only possible up country in the more fertile valleys. The
presence of the desert is principally due to the cold water lying along the coast, which causes condensa-
tion from the lower layers of the air above it (Scherhag, 1937), and acts like a mountain range, leaving
the land to leeward in its rain shadow. North of the desert, in Angola, the sand gradually gives way
to wooded country within the range of the seasonal tropical rains.

Although in itself arid, the South-west African coast has a very large drainage area, extending
across the interior to the western slopes of the Drakensberg mountains on the other side of the
continent. Practically all of this drainage, however, is collected in the Orange river, and other rivers
along the coast are only periodic torrents, during the summer rains in the south-west.

The topography of the sea-bed is shown in Fig. 4. It appears to be affected in a large degree by the

COASTAL GEOGRAPHY AND BOTTOM TOPOGRAPHY 145

Orange river, for the great underwater promontory sweeping seawards from the river mouth suggests
a considerable alluvial deposition from the great drainage system.

Although more data are still needed, the representation of such major features of the sea-bed seems
adequate for our present purpose. The chart (Fig. 4) has been constructed from :

1 . The most recent Admiralty Charts of the region.

2. Carte Bathymetrique Internationale. A IV (International Hydrographic Bureau, Monaco, 1938).

3. 'Meteor' expedition bathymetric charts (Stocks, 1941).

4. Soundings made by the 'William Scoresby'.

JFMAMJ J ASOND

JFMAMJJASOND

PORT NOILOTH

J FMAMJ J A S O N D

DASSEN

ISLAND

LUDERITZ BAY

Fig. 3. Mean annual rainfall in inches, at five points on the South-west African coast: Mossamedes (150 12' S.), Walvis
Bay (220 56' S.), Luderitz Bay (260 39' S.), Port Nolloth (290 14' S.), and Dassen Island (33° 26' S.). (From data in Royal
Naval Meteorological Service and South African Air Force, 1944.)

Over the greater part of the area covered by our surveys, the continental shelf, defined approxi-
mately by the 200 m. contour, is about 40 miles broad, widening to about 90 miles off the Orange
river mouth, and to 70 miles off Walvis Bay. Off Concepcion Bay, in 240 S., there is a sharp indenta-
tion on the shelf edge, and as at Luderitz Bay the shelf is less than 20 miles broad.

North of 200 S. the shelf narrows, and between 160 and 130 S. is almost non-existent, the slope
falling straightway from the coast into the depths of the Angola Basin. The shelf edge off Bahia dos
Tigres is much dissected into deep valleys which extend to depths of 1000 m.

The bottom slopes away fairly steeply from the coast to the 100-m. contour along most of the coast-
line, and then more gradually to the shelf-edge, forming virtually a submarine plain, a feature most
pronounced off the Orange river. From the shelf-edge there is a fairly gradual and constant slope to
3000 m., interrupted only off the Cape Peninsula where deep canyons are numerous between 500 and
3000 m., and in 200 S. where the continental slope is very gradual and at 1000 m. grows into a buttress
forming the northern end of the Walvis Ridge.

The Walvis Ridge leaves this buttress in a westerly direction at 3000 m., and runs southwards and
then to the west again to link up with the central Atlantic Ridge. In 250 S., 6° E. there is a prominent

146

DISCOVERY REPORTS

Fig. 4. Topography of the sea-floor of the South-west African region. Depths in metres. The hatched area shows
the extent of the continental shelf. For origin of data see text.

peak on the ridge rising to less than 1000 m. from the surface. Soundings over this deeper part of the
ridge are scarce and there may be a gap in about 22° S., but even so it can be little more than a break
in the 3000-m. contour, and the results of the ' Meteor ' expedition have already demonstrated the
significance of this ridge in the circulation of the deeper waters. The Walvis Ridge forms a very
effective barrier to northward movement of the Antarctic bottom water, the potential temperature of
the bottom water in the Cape Basin being less than i-o° C, while in the Angola Basin it averages more
than 2-0° C. (Wust, 1935).

METEOROLOGY 147

In 310 20' S., n° 20' E., there is what appears to be a sea-mount rising from 4000 m. to within
1000 m. of the surface, but this is evidently an isolated feature.

Soundings taken on the 'William Scoresby's' line of stations are plotted in the respective vertical
sections (Figs. 12-18, 22, 23, 25-30). In these diagrams the vertical scale is, of course, very exaggerated
(about 320 times). The absence of much shelf, with development of a fairly gradual slope, is clear on the
most northerly section, while on the Walvis line there are two shelves about 25 miles broad, the upper
just over 100 m. deep, and the lower at 300 m. At Sylvia Hill the coast slopes away steeply to a narrow
shelf at 200 m., while on the Orange river line the shelf is much broader, about 50 miles, at 175 m.
This latter represents the northerly part of the promontory referred to off the Orange river.

METEOROLOGY
Wind systems
The movements of the sea are so closely linked with those of the overlying atmosphere that any account
of the oceanographical phenomena of a region must necessarily take into consideration the prevailing
meteorological conditions. Fortunately, off South-west Africa these seem to fluctuate so regularly
(apart from minor variations) that a normal or ' average ' pattern can be formulated, which serves as
a background against which the data relating to the periods of these two surveys can be considered.
The general account which follows is based upon data collected by the Meteorological Services of the
Royal Navy and the South African Air Force (1944), supplemented by the work of Dr S. P. Jackson
(1951) who has long been interested in the weather of South-west Africa.

The wind system over the South-west African waters depends mainly upon the subtropical high-
pressure region which overlies the South Atlantic. The latitudinal axis of this anticyclonic centre is
situated between 260 and 300 S. From the centre the pressure gradient decreases gradually to the
north, but to the south, where it borders on the zone of the 'westerlies', the gradient is much steeper.
Round this high-pressure region the winds blow anti-cyclonically, so that off South-west Africa, which
lies in the eastern side of the pressure system, the winds are predominantly south or south easterly.
The coastal region, however, lies in the transition belt between the oceanic and continental pressure
systems, and so in the proximity of the coast the winds become modified by the fluctuations between
the two systems. It is necessary, therefore, to distinguish two separate wind regions — that offshore
where the South Atlantic anti-cyclone acts alone, and the other inshore, where both the oceanic and
continental pressure systems play a part.

The trade wind
In the summer, when the anti-cyclone lies in about 300 S., strong constant winds are produced, which
affect the whole oceanic region northwards from the Cape. About 80-85 % or" these winds are south-
easterly, and they blow with an average velocity of 11-21 knots. At the Cape peninsula these 'south-
easters' are a prominent feature of the summer climate, but the strongest winds are farther north,
between 250 and 300 S. North of 250 S. both the velocity and constancy of the trade winds diminish.
In winter time the anticyclone moves northwards and intensifies slightly — generally about 2 milli-
bars higher than in summer — so that the centre of highest pressure comes to lie in approximately the
latitude of Luderitz Bay (260 S.). Owing to the steep southward pressure gradient the trade winds in
300 S. then become intermittent. This northward displacement of the pressure system brings the
Cape region under the influence of the depressions of the westerlies, which, travelling eastwards from
the south-west Atlantic, bring rain to South Africa, accompanied by the attendant cyclonic variation
of the winds. The effect of these depressions extends as far north as Port Nolloth, where they produce

1 48

DISCOVERY REPORTS

JUNE TO AUGUST DECEMBER TO FEBRUARY

MORNING AFTERNOON MORNINC AFTERNOON

WALVIS 50
BAY

Jjjbrfa

50-

C NNE E SE SSWWNW C N NE E SE SSWWNW C N NE E SE SSWWNW C N NE E S£ S SWWNW

LUDERITZ

BAY

i—

□c

PORT

LL.

NOLLOTH

C N NE E SE S SWWNW C N NE E SE S SWWNW C N NEE SE S SW WNW C N NE E SE S SWWNW

C NNE ESE SSWWNW C N NE E SE S SWWNW C N NE E SE S SWWNW C N NE E SE S SWWNW

CAPE
TOWN

50-

hJd

■J lnt^te?H-J

C N NE E SE S SWWNW C N NE E SE S SWWNW C N NEE SE S SWWNW C NNE E SE S SWWNW

WIND FORCE
| 1 3-I3KTS HHJ I4-27KTS| | 28 - 40KTs[2 ^ OVER 41 KTS

Fig. 5. Percentage frequency of coastal winds in winter and summer. (From data in Royal Naval

Meteorological Service, etc., 1944.)

METEOROLOGY 149

a light, but quite pronounced winter rainfall (Fig. 3) which does not occur in the more northerly parts
of South-west Africa. The region of strongest winds also shifts north in winter, and lies in about the
latitude of Walvis Bay, where 30% of the trade winds have a velocity of over 16 knots.

The coastal winds (Fig. 5)
Although the inshore region remains under the influence of the South Atlantic anti-cyclone, the winds
are also affected by the variations in pressure over the continent, and as this fluctuates diurnally with
the heating and cooling of the land, so the coastal winds develop a marked diurnal variation (Fig. 5).
During the day, when the land is warmed up, the overlying air mass becomes light, and this causes
the cooler, more dense air over the sea to flow inland. This continues until equilibrium is regained,
and stable conditions are once more set up. On the whole these coastal winds, while they last, are
stronger than those at sea, but when the trade is blowing strongly over the open ocean one generally
finds the coastal winds are also stronger.

In summer (December -February), when the anti-cyclone is in its southern position, south winds are
prevalent on the coast as far north as Luderitz Bay (Fig. 5), generally having an easterly component
in the morning. This seems to be the effect of the anti-cyclone exerting its influence on the relatively
stable air mass over the coastal waters and land during the night and early morning. As the land warms
during the day, however, the wind veers round to the south and south-west and intensifies, reaching
at Luderitz an average velocity of 22-27 knots. This may occur fairly early in the day, and the sea-
breeze then continues until after nightfall when the pressure systems become balanced, and the anti-
cyclone once again becomes the dominating influence. It will be remembered, however, that in summer
the anti-cyclone has its greatest effect in the Luderitz Bay region, and that north of this its influence
steadily decreases, so that at Walvis Bay the stable air mass during the dark hours appears to be little
affected by the anti-cyclone, and the conditions experienced there during the night are either complete
calms or light northerly winds. As the day progresses, and the temperature effect comes into play,
the wind backs to the west and then S.S.W. from which the sea-breeze develops just after noon, and
blows with a mean force of 11-16 knots.

In winter, as might be expected with the northward shift of the pressure systems, the seasonal
variation is much more pronounced south of Orange river than on the more northerly part of the coast.
With the westerly depressions, the Cape receives winds more or less evenly distributed between north
and south from the westerly sector. A marked feature of the winters is the north-westerly gales, which
along with south-westerly weather are associated with the passage of the depressions. These features
are less prominent at Port Nolloth where the trade and the diurnal variations begin to take effect.

Occasionally, when the anti-cyclone is not strongly developed near the coast, small depressions form
close to the shore, and move northwards. On these occasions the sky remains cloudy, and a light
north-west wind sets in with a force of about 7-10 knots. These conditions have a remarkable effect
upon the sea temperature, which increases suddenly and has been known to reach as much as 23-9° C.
at Walvis Bay.

At both Luderitz Bay and Walvis Bay there is a marked increase in easterly winds during the
mornings in winter time (Fig. 5), but in both cases they are replaced with the much stronger south-
westerly breeze in the afternoons. Pressure is high on the continental plateau in winter and, coupled
with the lower pressure over the coast, leads to an outward push of air from the plateau. This usually
becomes obliterated later in the day, partly by a diurnal variation of the east wind itself further inland.
Amidst these easterly winds, when conditions are favourable, the noteworthy ' Berg winds ' occur,
which, blowing with considerable force towards the coast, make conditions extremely unpleasant on
account of their high temperature compared with the generally cool coastal climate.

4-2

150 DISCOVERY REPORTS

The Berg winds are extremely hot, dry winds which blow seawards across the desert, carrying much
sand and dust. They may last from a few hours to several days. A temperature of 1 1 50 F. was recorded
at Port Nolloth one day during a Berg wind. The highest recorded at Walvis is 1040 F. but the average
lies about 900 F. These winds are most frequent in winter, but can occur whenever the pressure
gradient and heating of the surface air inland is suitable. When the ' William Scoresby ' visited Walvis
Bay on 5 October 1950, a typical Berg wind was encountered. It blew for 4 or 5 hr. at 17-21 knots
and produced a fine deposit of sand all over the ship. The air temperature reached 990 F. and the
wind was uncomfortably dry. The Berg wind does not have much effect over the sea, for coming up
against the cool dense air over the water the light hot air diverges upward, away from the sea surface.

In the coastal region, then, the principal wind of force is the sea-breeze, or 'soo-oop-wa' (as the
natives call it), S.S.W. in the north and more southerly in the south. Jackson (personal communication)
reckons that the sea-breeze probably has a fetch of some 80-100 miles over the sea, that is from its
divergence from the south-east trade.

Weather preceding and during the surveys
There are not very many settlements along the desert coast of South-west Africa, and consequently
the number of stations which make regular climatological observations is very small. Fortunately,
however, records are maintained at Walvis Bay, Luderitz Bay, and Alexander Bay and these are used
by the South African Weather Bureau in the construction of synoptic charts of the South Atlantic
and South African region. Although we have not had access to the original data we have seen the
synoptic charts published at Pretoria and have extracted the data for these three coastal stations as
accurately as possible.

While shore observations are useful up to a point, observations at sea would have been much more
desirable, but the sparsity of observing ships in the region during the survey makes it impossible to
construct a complete enough picture. Most of the observations at sea are made on the main shipping
route from Capetown to Sierra Leone, well outside the area of our survey. Such observations as there
are, however, have been listed in Table 2, and do serve to show the constancy of the offshore winds,
nearly all the observations, at least during survey II, lying in the south to east quadrant.

The only estimate, therefore, of the weather conditions preceding the surveys must be based on the
observations made at the three coastal stations ; and although the importance of the diurnal variations
of the inshore winds has already been explained, all the synoptic charts are based on observations
made once daily, at 08.00 s.a.s.t. These shortcomings of the records at our disposal have to be accepted,
but must be borne in mind in interpreting the data.

The observations from the three shore stations for the periods preceding and during the surveys
are given in Table 3. It can be seen that before survey I the weather at Walvis Bay had been calm
or northerly, while at Luderitz Bay, right up to the time the ship visited the locality, the winds had
mainly been southerly. At Orange river there had been very little wind for the whole month pre-
ceding and during the Survey.

Prior to Survey II, however, conditions were very different. Both Walvis Bay and Luderitz Bay
had experienced much stronger winds, mainly from between south and west. As on the first survey,
Orange river experienced comparatively calm weather.

So much for conditions on the coast. The constancy of the trade wind has already been shown from
the observations at sea (Table 2). From the synoptic charts we can get some further information upon
the state of these winds. It has not been considered advisable to calculate the vectors and velocities
of the oceanic winds from the isobars, as they are based on so few recording stations. Regular observa-
tions come from the South African coastal stations, Tristan da Cunha and St Helena, and the observa-

METEOROLOGY 151

tions of any ships in the neighbourhood are also included. But considering the vastness of the area
affected, these few points must only allow a very approximate picture to be drawn.

The anti-cyclone rarely appears as a single entity, but is usually composed of several distinct high
pressure centres slowly travelling across the Atlantic in an easterly direction towards South Africa.
When one of these has passed, conditions become more diffuse until the next high pressure centre
takes control. The cycle appears to average about four days, but it should be noted that the wind is
dependent on the pressure gradient between the anti-cyclone and the lower pressure regions to north
and east, and consequently does not vary directly with the position of the anti-cyclone.

Table 2. Ships' observations (positions approx.) of the wind at sea during the

' William Scoresby ' surveys*

Wind

Date 1950

Latitude

Longitude

(vel. in knots)

5 March

240 20' S.

8° 20' E.

S.S.E. 18

8 Sept.

290 40' s.

ii° E.

S.E. 12

13 Sept.

i5°oo'S.

8°E.

S.E. 18

13 Sept.

190 20' S.

5°E.

S.E. 24

13 Sept.

250 40' S.

9°E.

E.S.E. 24

14 Sept.

260 30' s.

7° 40' E.

S.S.E. 18

15 Sept.

200 20' S.

io° 30' E.

S.E. 12

15 Sept.

22° 20' S.

8° 40' E.

S.S.E. 18

16 Sept.

27° 00' S.

I2°I0'E.

S.S.W. 6

17 Sept.

270 00' S.

1 40 00' E.

S.E. 12

17 Sept.

22° 20' S.

8° 10' E.

E.S.E. 24

17 Sept.

29° 30' s.

n°oo'E.

S. by W. 6

17 Sept.

25° 3°' S.

50 00' E.

S.E. 18

19 Sept.

25° 5°' S.

io° 30' E.

S. by E. 24

20 Sept.

270 40' S.

12° 00' E.

S.S.E. 18

20 Sept.

22° OO' S.

9° 00' E.

S.S.E. 24

24 Sept.

21° 40' S.

8° 20' E.

S.E. 6

25 Sept.

19° 40' s.

6° 00' E.

S.S.E. 12

25 Sept.

270 40' s.

90 00' E.

N.W. 6

26 Sept.

29° 20' s.

i2°4o'E.

W. 12

27 Sept.

20° OO' S.

io° 40' E.

S.S.E. 12

28 Sept.

290 20' s.

1 30 40' E.

W. 18

28 Sept.

i5°4o'S.

8° 30' E.

S.E. 12

28 Sept.

230 10' S.

70 00' E.

S. 12

30 Sept.

29° 3°' s-

140 20' E.

S.S.W. 18

30 Sept.

260 00' S.

n°3o'E.

S.S.E. 12

30 Sept.

1 6° 50' S.

5° 10' E.

E.S.E. 30

1 Oct.

21° I0' S.

7° 3°' E.

S.E. 30

8 Oct.

1 8° 30' S.

ii° 20' E.

N.N.W. 6

8 Oct.

190 20' s.

5° 30' E.

S.S.W. 6

10 Oct.

15° 20' S.

70 10' E.

Calm

* Compiled from information collected by voluntary observing ships for the Meteorological Office.

In February and March 1950, the pressure gradient was not so pronounced as in September-
October, and the centres of high pressure lay rather farther south in February and March, in about
300 S. Moreover the anti-cyclone in the September-October period was more intense, and frequently
associated with quite marked low-pressure areas over the coastal region. The trade winds were, there-
fore, stronger and more constant before and during survey II.

Regular observations of wind were of course maintained aboard the 'William Scoresby' throughout
both surveys, and these have been rather useful in illustrating some of the short-term effects on the
water movement.

During survey I, after the ship left Lobito, the wind was fairly light from the south-westerly sector,

'52

DISCOVERY REPORTS

but steadily increased in force and backed to S.S.E. as the outer end of the Mowe Point line was
reached. The wind here was blowing with a force of 4-5 Beaufort, but became lighter and veered to
the south as land was approached. As we proceeded offshore to the seaward end of the Walvis Bay
line it once more became S.S.E. but rather more variable in force, and when Walvis Bay was reached

Day

1
2
3
4
5
6

7
8

9
10

11
12

H
15
16

17
18

19
20

23
24

27
28

3°

1
2

3
4
5
6

7
8

9
10
11
12
13
14

able 3 . Coastal winds

Walvis

Luderitz

Alexander

Walvis

Luderitz

Alexander

Bay

Bay
February

Bay

Bay
September

Bay

Calm

S.S.W. 30

S.W. 6

N.W. 6

S. 6

Calm

S. 30

Calm

S.W. 6

Calm

—

Calm

S. 30

—

S.S.W. 12

—

N. 6

S. 12

Calm

S.W. 18

—

W. 6

Calm

—

S.S.W. 18

—

S. 6

N.W. 6

S. 18

—

S.W. 18

Calm

N. 6

S.E. 12

S.W. 18

S.W. 24

Calm

N. 6

Calm

S.W. 6

S.W. 18

S. 6

S.S.W. 6

S.S.W. 12

—

W.N.W. 6

Calm

—

N. 6

S.W. 18

S.S.E. 6

S.S.W. 6

N.W. 12

—

Calm

S. 18

—

S.W. 12

Calm

S. 12

S.E. 6

S.S.W. 12

Calm

S.S.E. 12

Calm

W.S.W. 12

S. 36

S.E. 6

Calm

S. 6

Calm

N.N.W. 12

S.S.W. 24

S. 6

N. 6

S. 18

Calm

N. 6

N. 12

Calm

S. 6

Calm

S.W. 18

Calm

—

Calm

—

Calm

S. 6

Calm

S.S.W. 18

—

S. 12

—

S. 6

—

S. 6

W.S.W. 30

S.W. 30

—

N. 6

S.E. 6

Calm

S.W. 6

S.W. 30

—

N.W. 6

—

Calm

W. 6

S.W. 24

S. 6

W.N.W. 6

—

Calm

S.W. 6

W. 6

—

Calm

—

Calm

N.N.W. 6

S. 6

—

Calm

—

Calm

W.S.W. 6

S. 6

Calm

—

S.S.W. 24

S.W. 18

Calm

S.S.W. 6

Calm

S. 18

S.S.W. 30

Calm

S. 6

Calm

S.S.W. 12

W.S.W. 18

Calm

—

S.W. 6

N.N.E. 6

Calm

March

S.W. 30

S.S.W. 24
October

S.W. 6

S.S.W. 12

Calm

S.S.W. 12

S.S.W. 30

N. 6

S.S.W. 30

S.S.E. 6

W.S.W. 6

S.W. 12

Calm

N.W. 6

—

S.S.E. 6

Calm

S. 6

—

S.S.E. 12

S.W. 6

Calm

S.W. 6

S. 6

—

E.N.E. 6

S.W. 12

Calm

S. 18

Calm

W.S.W. 6

Calm

S. 6

Calm

W.S.W. 6

Calm

—

Calm

S.W. 12

Calm

—

S.W. 30

—

N.W. 6

—

Calm

S.S.W. 6

N. 6

S. 6

Calm

—

W. 6

—

S.W. 12

Calm

—

S.W. 18

Calm

S.S.W. 6

—

S.S.W. 6

S.W. 12

Calm

—

Calm

S.S.W. 12

S.W. 24

—

Wind direction and velocity in knots, extracted for the three stations Walvis Bay, Luderitz Bay and Alexander Bay, from
the synoptic charts of the Daily Weather Bulletin, 08.00 S.A.s.T. issued for the above months of 1950 by the Weather Bureau,
Pretoria.

SURFACE-CURRENTS 153

it died away completely. These calm conditions persisted until the inner end of the Luderitz line,
but towards the Orange river line the wind built up again. It did not, however, become very strong —
force 3-4 from the east of south. Off the Orange river mouth the wind dropped.

On Survey II the wind was light after we left Simon's Town, but increased after Saldanha Bay to
force 4-5 and remained so until the seaward end of the Orange river line, except for a short calm spell
off the Orange river mouth. The passage north to Hollam's Bird Island was very calm, but as we
steamed seawards the wind increased from west of south, remaining between S.S.W. and S.S.E., force
4-5, up to Walvis Bay. The course seawards from Walvis Bay was attended by an increasing southerly
wind which reached gale force at the outer end of the line, and the ship was hove to against this for
nearly two days. The wind then fell quickly and the ship returned to Walvis Bay in light northerly airs.
At Walvis Bay the Berg wind already mentioned was encountered, and conditions remained variable
with a fair proportion of north-westerly wind up to Cape Frio, north of which the passage became
increasingly calm.

SURFACE- CURRENTS

Previous data
Since the ship was working to a strict time-schedule it was impracticable to make any direct observa-
tions on the amount of set and drift to which she was subjected. A few occasions, however, presented
themselves when trustworthy fixes (stellar or shore) could be correlated with an uninterrupted
passage of the ship, thereby giving an estimate of the amount of drift due to wind and currents. With
accurate wind observations it was then possible to get a fairly good idea of how much of the drift was
caused by the currents alone. These data, although useful in relation to the other oceanographical
observations, are insufficient to give any comprehensive picture of the circulation, and for this it has
been necessary to draw on other sources of information.

In the South Atlantic Ocean the surface-currents take the form of a large anti-cyclonic gyral of water
movement, a circulation impelled principally by the south-east trade winds. These drive the surface
water in a westerly direction away from the African coast, and reaching South America it is returned
southwards in the Brazil current, and eventually back to Africa in a current flowing more or less in the
same direction as the Southern Ocean current but separated from the latter by the subtropical
convergence.

Off the South-west African coast there is, therefore, a wind-driven transport of water, principally to
the west but rather more northerly in the south of the region (Table 4). It has already been noted
that the south-east trade, although very constant in force and direction offshore, becomes much more
variable nearer the coast in the proximity of the continental shelf, and consequently, considering
purely a wind-driven circulation, one would expect the currents also to behave with much greater
irregularity in this region. Unfortunately very few current observations have been made in the coastal
region since it lies off the track of the main shipping lanes, but sufficient exist to confirm the irregular

Table 4. Mean set and drift of the south-east trade wind drift

Latitude 12°-i8° S. Latitude i8°-24° S. Latitude 24°-30° S.

Mean set

No. of

Mean set

No. of

Mean set

No. of

and drift

obs.

and drift

obs.

and drift

obs.

Nov.-Jan.

244 ° 2 miles

141

273° 4 miles

146

3 1 6° 5 miles

175

Feb. -April

248° 3 miles

iS3

2800 4 miles

157

3040 4 miles

165

May-July

2850 3 miles

164

3 1 2° 3 miles

170

3330 3 miles

180

Aug.-Oct.

2800 4 miles

160

2970 4 miles

181

3 1 40 4 miles

189

After Hydrographic Department,

!939-

i54 DISCOVERY REPORTS

nature of the sets (Miihry, 1864; Koch, 1888; Hessner, 1892; Walther, 1893; Reincke, 1896; Bachem,
1896; Gilchrist, 1903; E.K., S.M.S. 'Sperber', 1907; Pohlenz, 1908; Muffling, 191 1; Clowes, 1954),
and the British Admiralty Pilot (Hydrographic Dept., 1939), p. 48, remarks with regard to the coastal
waters: 'The general set of the current southward of the Congo river is parallel with the coast in
a northerly direction at the rate of from 10 to 25 miles a day; but it is very irregular, both in direction

Fig. 6. Charts of surface currents for the four quarters of the year. After Defant, 1936.

and velocity, for sometimes, between October and June, but principally in March, April, and May,
the direction of the current is completely reversed, and is found setting southward, and sometimes
south-eastward.'

Defant (1936) has analysed the Dutch current observations, and meaned them for four quarters into
one degree areas (i° longitude by i° latitude), and concludes from his analysis (Fig. 6):

Ein Blick auf diese Stromfelder lehrt, dass das Charakteristische in ihnen die in alien Monaten wieder mit nicht zu
iiberbietender Deutlichkeit auftretende einseitige Diver genzlinie ist; sie lauft nordnordwestwarts langs der Kiiste
Siidwestafrikas von etwa 300 bis iiber 200 siidl. Br.; im Siiden ist ihr Abstand von der Kiiste rund 160 sm, im
Norden 300-350 sm. Das Gebiet ostwarts dieser Divergenzlinie, das ist gleichzeitig das Gebiet des Kontinental-
abfalles und des Schelfes, hat eine Stromung nordnordwestwarts, also parallel der Diskontinuitatslinie und mehr
oder minder auch parallel dem allgemeinen Kustenverlauf. Das Gebiet westwarts der Divergenzlinie hat im
wesentlichen einen Strom nach Westen.

This interpretation of Defant's appears to correspond fairly well with the data in the possession of
the Meteorological Office, the position of Defant's N.N.W. current being similar to that pictured by

SURFACE-CURRENTS 155

the Meteorological Office current charts and more or less on the main shipping lane from Capetown
to Sierra Leone.

The current-system of the region affected by the south-east trade wind seems clearly explicable on
these lines, but although such an average picture may suffice for navigational purposes even in the
more variable inshore region, it cannot assist in the interpretation of the hydrological conditions
observed there. The irregularities already referred to show how much the inshore currents must
depend upon local wind and local conditions generally. For a significant interpretation of the water
movements here a synoptic rather than an 'average' picture would be needed. Existing data do not
suffice for this, but a practicable working compromise has been attempted by correlation of the
'William Scoresby's ' meteorological observations with the oceanographic data, and with the meteoro-
logical records of such other ships as were in the vicinity at the same time.

Currents during the surveys
In March 1950, on the passage southwards from Lobito Bay, the first appreciable effect of current
was felt south of Bahia dos Tigres, where a moderate set to the north-east was noted. On the most
northerly line of stations (WS 964-70) an allowance of i° was made on the shoreward course for
northerly set, and this maintained a latitudinal line of stations, but it is impossible to say just how
much of this was the effect of current as distinct from the wind. At the stations on the outer end of the
Walvis Bay line, however, a northerly set of about 1 knot was encountered with a light wind ; the
observed position of station WS 978 lying 16 miles north-north-east of its intended position. This
northerly set was found at the offshore end of the three lines of full stations, and on the Walvis Bay
and Sylvia Hill lines gradually became more easterly as land was approached, until at the inshore
end of these lines the set was E.N.E. with negligible wind effect.

At the inshore end of the most southerly line, just off the mouth of the Orange river, the set
appeared to be S.S.W., against a light wind from the same quadrant.

On the second survey, in spite of the stronger winds, little genuine current effect was recorded.
Inshore at Orange river mouth, the ship, while lying-to for the night, showed negligible movement in
completely calm conditions. Seawards, however, between WS 1052 and 1053 there was a northwards
drift of 14 miles in 14 hr., but this may have been due to the wind. Between WS 1057 and 1061, the
first pure current-effect was noted, the ship being set 065 ° at \ knot with no wind, and at WS 1063
a slight north to north-east drift was probably due to the light south-west wind, and current must
have been almost absent. These conditions continued between WS 1064 and 1067 and on the circum-
navigation of Hollam's Bird Island there was no current at all. From 240 02' S., i3°5i'E. to
22° 46' S., 140 20' E. the current set 0350 10 miles in \z\ hr., and later a similar set was observed off
Swakopmund where the vessel was stopped and drifted 0350 for 3-5 miles in 5 hr. (0-7 knot). Again
when stopped off Pelican Point lighthouse at WS 1076 the set was 035 ° 07 knot with no wind. The
tide was on the flood then at Walvis Bay, and this may have accounted for the set.

From WS 1081 to Walvis Bay no drift was experienced, and a perfect course was made. As the
winds were very light it is probable that there was negligible water-movement. After departing from
Walvis Bay no drift of any consequence was encountered, and currents were disregarded in setting
courses.

Summing up, the set on both surveys appears to have been very little, but when it was observed
it was generally in a northerly direction in the offshore region, becoming more easterly nearer the
land. The S.S.W. set off the Orange river is inexplicable at the moment, and it is impossible to say
how much tidal streams were responsible for the E.N.E. sets experienced inshore.

156

DISCOVERY REPORTS

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY

This section will be devoted to a description of the horizontal and vertical distribution of the physical
and chemical properties of the waters which were surveyed. In the following sections an attempt will
be made to relate these observed distributions to the prevailing meteorological conditions and the
geography of the area with a view to elucidating the mechanism underlying the process of the up-
welling and its fluctuations as we found them.

(«) (*)

Fig. 7 (a). Distribution of sea surface-temperature (° C), survey I, March 1950. (b) Distribution of sea surface-temperature
(° C), survey II, September-October 1950. Both compiled from station observations and distant-reading thermograph records.

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY 157

As the water masses under consideration exhibit a general northward trend, it will be more con-
venient to treat the results of both surveys from south to north, and not, therefore, in the chrono-
logical order of the stations worked during survey I.

The charts showing the distribution of surface-temperature (Fig. 7) and surface-salinity (Fig. 8)
show that on both surveys the isotherms and isohalines ran more or less parallel to the coast. Within

.CAPE FRIO

20-i
S.

[MO WE POINT

3530

25H

SURVEY: I

CAPE CROSS

tVALVIS BAY

CONCEPCION
BAY

SYLVIA HILL

, CAPE FRJO

ORANGE
R.

30'

10° E.

"I r

15°

MO WE POINT

CAPE CROSS

SURVEY: II

75 BAY

CONCEPCION
BAY

ORANGE
R.

10 E 15"

(«) (*)

Fig. 8 (a). Distribution of surface-salinity (%0), survey I, March 1950. (b) Distribution of surface-
salinity (%0), survey II, September-October 1950.

this system the cooler and less saline waters lay adjacent to the land, and the warmer, more saline
waters farther offshore. Superimposed upon this distribution, however, there was a pronounced series
of tongue-like formations within which the cooler coastal waters alternated with intrusions of the
warmer oceanic waters lying to the west. Thus the cool waters were not in the form of a continuous
belt along the coast, but rather were present as a series of isolated patches extending out from the
coast and entering into eddies with the warmer oceanic waters. It will be shown, further, that within
these eddies the cooler coastal waters were sharply separated from the warm oceanic surface-waters.

5-2

■58 discovery reports

First survey (autumn)

Horizontal distribution of temperature and salinity
On the first survey the lowest surface-temperatures were found in the south of the region, off Pater-
noster Point (320 40' S.) where the lowest recorded was 12-5° C. This cold water, although we have
no direct evidence, was probably confined to a fairly narrow coastal strip. In the vicinity of Cape of
Good Hope the thermograph readings reached a value of 170 C. only 3 miles offshore, and so there
is little likelihood that the cool water extended east of this point.

25-

sL- * ** 2 i:

*5 £h ^ ?k S SJ 12-5*

'« #5 ** 5-o

^ |f §5 £* 5|io-o5

7-5

**-

5-0,

\f>

>/!

2-5^

0*00

11*

-2

Fig. 9. Photograph of the annotated distant-reading thermograph chart for
Saturday, 11 March 1950. Vertical scale, temperature in ° C.

Northwards, towards the Orange river mouth, the extent of cool water became more restricted, and
in 290 S. the warmer oceanic water penetrated more closely to the coast. The outflow of fresh water
from the Orange river can be detected over a wide area. The surface-salinities at stations in the neigh-
bourhood were vastly reduced (32-39 %0 at WS 1001) but the reduction affected only a thin surface-
layer, and 50 miles offshore at WS 1000 the surface-salinity was that of the normal sea-water of the
region. To the west of station WS 998 the boundary with the warm oceanic water was sharply

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY 159

defined by a sudden increase in both temperature and salinity (from 18-36° C, 35-01 %0 to 20-18° C,
35-20 %0).

The bathythermograph observations north of WS 996 show that the Orange river line of stations
lay along the southern boundary of an extensive wedge of cool water, WS 955 marking its most westerly
limit. To the north of this, typical oceanic temperatures were present at WS 994 and 993 but cooler
water was again encountered at WS 992. The contouring of the isotherms shows these high surface-
temperatures (WS 994, 993) as a tongue of oceanic water converging with the coast, and the strong
temperature gradients on either side of it suggest that it was sharply discontinuous with the sur-

CAPE FRIO

20°H

140

MO WE POINT

25-

CAPE CROSS

'WALVIS BAY

\ ' \ UCONCEPCION

130, „ * Vbl - BAY

' , 12-5 . '2^|
I I I

, \ v • /'l V % SYLVIA HILL

v \U-v ' i2-c5V"'

14-0

, CAPE FRIO

MO WE POINT

35-20

CAPE CROSS

WALVIS BAY

CONCEPCION

■■ BAY

ORANGE
R.

30"

SYLl'IA HILL

ORAXGE
R.

\ 1 1 1 1 1 1

IO°E. 15° I0°E.

(«) W

Fig. 10. Distribution of (a) temperature, and (b) salinity at a depth of 100 m., survey I, March 1950.

rounding cooler water; this is specially noticeable on its northern side, where the temperature fell
3-5° C. in about 15 miles at a distance of 60 miles west of Luderitz Bay (27° S.) (see Fig. 9).

On the next line of stations in 25° S. another such eddy can be defined, but here the oceanic water
appeared to extend right in to the coast, causing the cooler water from the south to be displaced
seawards. The increase to oceanic temperatures was not evident until WS 986, the westernmost
station on the line. It may be that local heating of the surface-waters in the vicinity of station WS 988
had complicated the picture here, but the salinity at WS 988 was higher by 0-06 %0 than at the next
station seaward, not only at the surface but throughout the water column. A difference in salinity of
this order of magnitude may not be significant in itself, but in conjunction with the temperature data

160 DISCOVERY REPORTS

it strongly supports the hypothesis of an offshore influence at this point. Moreover the data to the
north of this line also point to the presence of oceanic water converging southwards to this position.
Off Walvis Bay, and to the north of this warm wedge, the water was cooler again, but both the
salinities and temperatures are higher than usual for the coastal water, the inshore values of 35-15 %0
and 1 70 C. being more suggestive of some admixture between the two types of surface-water. At the
western end of this line of stations, in 230 S., there was again a sudden increase of temperature and
salinity into the northern boundary of the warm wedge, with temperatures of over 190 C. and salinities
over 35-2o%0.

20-
S

25-

30-

.CAPE FRIO

[MOWE POINT

I0°E

ORANGE
R.

Fig. 11. Distribution of temperature at a depth of 200 m., survey I, March 1950.

To the north of 230 S. the oceanic waters extend in a thin surface-layer apparently pressing towards
the coast between 220 and 200 S.

Along the coast the cooler water becomes more and more confined, and eventually to the north of
1 90 S it appears to converge strongly with the very warm offshore waters (> 220 C.) in a series of
eddies about 25 miles from the coast. Finally all trace of it disappears in 160 S., where at 15 miles
offshore a temperature of 260 C. was recorded. This whole region between 160 and 190 S. is typical
of a convergence region, with very sharp and considerable variations of temperature. Probably the
observations demonstrate a compression of the normal convergence between subtropical and tropical
surface water, resulting from the presence along the coast of water so abnormally cool for such
latitudes. This marked the northern limit of the upwelling region in March 1950.

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY 161

At a depth of 20 m. the same general characteristics of the surface distribution are to be found, but
by 50 m. a change is evident. The disposition of the isotherms and isohalines at these depths repre-
sents a transition in varying stages between the surface distribution and that at greater depths. The
isotherms and isohalines at 100 m. (Fig. 10) exhibit some more considerable changes which are
worthy of note. It will be seen that little change is evident in the Luderitz Bay-Orange river region,
(270 to 300 S.) but the cooler coastal water can now be traced more continuously along the coast, and
extends to the north in a tongue leaving the coast in the vicinity of Walvis Bay. On the landward
flank of this extension warmer water is present, apparently intruding southwards along the coast as far
as Concepcion Bay (240 S.). The eddy in 250 S. at stations WS 986 and 987 is still present, and from
the north of it another area of low temperatures extends offshore through WS 977, with a markedly
lower salinity (35-o6%0) than the surrounding water at WS 976 and 978 (35-23 %0 and 3 5 • 1 6 %0
respectively).

The smaller number of observations made below this depth make it impossible to construct any
detailed picture. It is evident, however, that at a depth of 200 m. (Fig. 11) there was an extensive
area of cooler water extending N.N.W. from the area between Orange river and Luderitz Bay, the
axis of this belt running through WS 986 and 977. Between this tongue and the coast the water was
warmer and more saline and suggests a flow from the north along the edge of the continental shelf as
far south as Luderitz Bay.

Vertical distribution of temperature and salinity

At most stations there is a layer of almost homogeneous water at the surface, within which the
density remains almost constant with depth. This is generally referred to as the convection layer.
Throughout the region it is present to a greater or lesser extent, and as a rule it is underlain by a

Table 5. Depth of the convection layer

Survey I

Survey II

Survey I

Survey II

Depth

Deptt

Station

(m.)

Station

(m.)

—

1 105

—

1 104

—

1 103

WS964

1 102

WS965

IIOI

WS966

3°

1 100

WS967

1099

WS968

1098

WS969

1097

3°

WS970

1096

WS971

3°

1093

WS972

1091

WS973

1090

WS974

1089

WS97S

1088

WS976

5°

1080

WS977

1081

WS978

1079

5°

WS 979

1078

WS980

1077

3°

WS981

1075

3°

Where the depth figure '0

occurs, it

indicates that the

Station

WS982
WS983
WS984
WS985

WS986
WS987
WS988
WS989

WS990
WS991
WS 992
WS 993
WS994
WS995

WS966
WS997
WS998
WS 999
WS 1000
WS 1001
WS 1002

Depth
(m.)

4
o
o

o
o
o
o

3°

10
10
20
10
20
o
o

Station

WS 1074
WS 1073
WS 1072
WS 1071

WS 1070
WS 1069
WS 1064
WS 1063

WS 1062
WS 1061
WS 1060
WS 1059

WS 1058
WS 1057

WS 1056
WS 1055
WS 1054
WS 1053
WS 1052
WS 1051
WS 1050

Depth

(M.)

10
30

3°

3°
o
o
o

o
10

100

5°
3°
10
20
10
o

i less than 10 m. in thickness.

162 DISCOVERY REPORTS

strong temperature discontinuity layer, through which the salinity remains almost constant. This

discontinuity is therefore a layer of great stability.

The distribution and depth of the convection layer is set out in Table 5, zero indicating where none
existed or where it was too thin to be recorded by our observations (< 10m).1

Comparing this table with the distribution of surface temperature and salinity (Figs. 7 and 8) it is
clear that the convection layer is well developed in the oceanic surface-water, but is notably absent
or ill defined in the cooler coastal waters, in which the temperature decreases more steadily from the
surface to the sea-bed.

The Orange river line (280 30' S.). The vertical sections of temperature and salinity (Figs. 12 and 13)
show that both the isotherms and isohalines trend upward to the coast. Although this pattern may
suggest an active vertical uplift of water against the coast, such a movement does not appear likely in
view of the well-developed discontinuity and the impoverished nature of the surface-waters (fig. 50).
The great reduction in salinity of the surface-waters at the inshore stations has already been referred
to, and the resulting decrease in density of the surface layers has led to very great stability at these
stations.

It is suggested that this section shows an advanced stage of the upwelling process : a relic of previous
upwelling rather than a stage of active uplift.

The Sylvia Hill line (25° S.) (Figs. 14 and 15). The whole water column at the inshore stations,
WS 988 and 989, was very stable. Clearly there is no indication of inshore upwelling on this line, but
then it will be remembered (p. 160) that the inshore stations were apparently influenced by a convergent
tongue of oceanic water from the north, and that the cooler water had been displaced offshore. In this
cooler water the lower stability and patterns of the isohalines in particular are strongly indicative of
vertical motion at stations WS 986 and 987.

The Walvis Bay line (23 ° S.) (Figs. 16 and 17). The salinity section shows a prominent tongue of
highly saline water near the surface. Within this the temperatures are high, and it is characterized
by a pronounced thermal discontinuity. This is the northern edge of the intrusion of oceanic water
which curves to the south and influences the inshore station on the preceding line. On this Walvis
section the discontinuity remains well marked at the inshore stations, and the relatively high tempera-
ture and salinity of the latter show that no active upwelling was in evidence. The nature of the inshore
water masses here is somewhat problematical, for they appear to exhibit characteristics of a mixture
of the oceanic and coastal waters. The most plausible interpretation is that previously upwelled water
has subsequently become mixed with oceanic water and the resultant mixture occupies the area in the
proximity of the coast at Walvis Bay.

The Mowe Point line (190 44' S.). Extending throughout the area to the north of Walvis Bay the
oceanic surface-waters form a thin layer about 50 m. deep, overlying a very strong temperature
discontinuity. A section through this layer is shown in Fig. 18, which shows the most northern line
of stations (the Mowe Point line). It will be seen that on the inshore boundary of this layer the dis-
continuity weakens and slightly cooler water lies against the coast. Although no salinities were taken
in this region it is highly probable that the coastal water is again an admixture of the oceanic and
coastal water types. There is a slight indication that the upward trend of the isotherms towards the
coast may represent a very early stage of upwelling.

1 Xo salinity observations have been available for the 'bathythermograph stations', and so certain assumptions have been
necessary. At all full stations the character of the upper layer density distribution, and consequently the convection layer,
was primarily dependent upon variations of temperature, and the slight variations of salinity have affected the density curves
only slightly. It has therefore been considered justifiable to define the convection layer from the temperature curves at the
bathythermograph stations, as the layer within which the temperature remained almost constant.

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY

163

Fig. 12. Distribution of temperature (° C). Section off the mouth of the Orange river, 12-14 March 1950, survey I.

Positions of stations are shown in Fig. 1.

STATIONS WS996

WS997

WSW)
I

WSIOOO

WS IOOI

WS 1002
I

50O

Fig. 13. Distribution of salinity (%0). Section off the mouth of the Orange river, 12-14 March 1950, survey I. Positions of

stations are shown in Fig. 1.

164 DISCOVERY REPORTS

At all of the stations below the discontinuity layer the temperature and salinity decrease with depth
towards the core of the antarctic intermediate water.

This outline of the conditions on the first survey leads us to the conclusion that, in the region
surveyed, two principal types. of surface-water can be identified.

(a) The coastal or upwelled water, with a low salinity of 35-00 %0 or less, and low temperature
<i8-o° C, and as a rule without any marked convection layer.

WS989
I

300

Fig. 14. Distribution of temperature (° C). Section off Sylvia Hill, 10-11 March 1950, survey I.

Positions of the stations are shown in Fig. 1.

STATIONS WS986

SEA MILES ,„

OFFSHORE

ws«e wswj
I

100

200-

300

Fig. 15. Distribution of salinity (%0). Section off Sylvia Hill, 10-11 March 1950, survey I. Positions

of the stations are shown in Fig. 1 .

(b) The offshore or oceanic water with a high temperature, usually > 180 C, high salinity
> 35-20 %0 and a well-developed convection layer.

It is evident that mixtures of these waters occur, as was found in the vicinity of Walvis Bay, but
generally they are found sharply distinguished from one another with a pronounced boundary.

There is also evidence of considerable surface heating having affected the coastal waters on survey I,
and along with the lack of evidence of active upwelling, this suggests that the conditions throughout
the area represent a quiescent state subsequent to previous upwelling.

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY

1 6S

STATIONS

SEA MILES.
OFFSHORE l75

WS97S,

IOO—

200-

° 300-

400-

500

Fig. 16. Distribution of temperature (° C). Section off Walvis Bay, 6-8 March 1950, survey I.

Positions of stations are shown in Fig. 1.

STATIONS
SEA MILES
OFFSHORE 175
O-

WS97(.

WS977

WS97B
I

WS979

IOO-

200-

300-

ISO 125

t 1

>35 27 V.^

___ 3525

100

WS980 WS98I
I I

500

Fig. 17. Distribution of salinity (%,,). Section off Walvis Bay, 6-8 March 1950, survey I.
Positions of stations are shown in Fig. 1.

6-2

1 66

DISCOVERY REPORTS

STATIONS WS%4
SEA MILES 125 '
OFFSHORE 0

100-

200

Fig. 18. Distribution of temperature (° C). Section ofF Mowe Point, 4-5 March 1950, survey I. Constructed from
bathythermograph observations, the positions of which are shown on Fig. 1.

Second survey (spring)

Horizontal distribution of temperature and salinity
On survey II the trend of the surface isotherms and isohalines was similar to that on survey I, but
throughout the whole region the temperatures were markedly lower. This can to a large extent be
attributed to the seasonal change, survey II having taken place about the coolest time of the year; but
also, as will be shown in what follows, the more active upwelling before and during this survey has also
contributed to the overall effect.

4" EAST

Fig. 19. Distribution of surface-temperature (° C.) between Cape Cross and Mowe Point, survey II, constructed from station
observations and distant-reading thermograph records. The track of the ship between stations is shown by the thin line.

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY 167

The lowest surface-temperature recorded (Fig. yb) was io° C, off the mouth of the Orange river,
but all along the coast as far south as the Cape of Good Hope the temperatures remained below 130 C.
In 3 1° to 3 2° S. oceanic water with a temperature of 150 C. approached more closely to the coast, but
to the north of this the coastal water extended far seawards, forming a broad tongue with its axis
extending westwards in 29 ° S.

In contrast to survey I the Orange river line of stations, which occupied the same positions on both
surveys, lay on the northward side of this tongue of colder water. To the north of these stations
oceanic water again intruded towards the coast in 280 S. The low salinities in the vicinity of the

20-
S

25°H

\PE FRIO

WiMOWE POIXT

CAPE CROSS

U'ALl'IS BAY

COXCEPCION
BAY

io-4-

SYLVIA HILL

CAPE FRIO

MOWE POIXT

A CAPE CROSS

LVIS BAY

XCEPCIOX
BAY

ORANGE
R.

17.4 HILL

ORANGE
R.

1 I I I I I 1 1 1 1 1 1

10° E 15° IO°E 15°

(«) (*)

Fig. 20. The distribution of (a) temperature (° C), and (b) salinity (%0) at a depth of 100 m. on

survey II, September-October 1950.

Orange river mouth were again evident. A sudden increase in salinity between stations WS 1054
and 1055 marked the boundary of coastal and oceanic waters.

Another sharp boundary was traversed between stations WS 1059 and 1060 on the northern side
of the oceanic water.

To the north of 270 S. the cooler waters became very extensive, and up to Walvis Bay in 230 S. there
was a complex series of small eddies formed by the cooler water, apparently driving offshore in a
north-westerly direction. Throughout this area sharp fluctuations of sea temperature were continually
encountered, but the temperature remained consistently low.

168 DISCOVERY REPORTS

The stations at the inshore end of the Walvis Bay line all show the typical features of the cool
coastal waters, with temperatures of less than 130 C. and salinities of less than 35-00 %0. The stations
at the offshore end of the line, on the other hand, lying in warmer and more saline water, are charac-
teristic of oceanic conditions. (It should be noted here that the contouring of the isotherms at
WS 1079-81 may be open to question for the observations at WS 1079 were taken before, and those
at WS 1080 and 1081 after, a considerable gale. As will be shown later (p. 188) this gale produced
a considerable alteration in the position of the surface isotherms, and yet no allowance could well be
made for this in the general picture).

20-
S

, CAPE FRIO

25-

30v

POINT

IO E IS

Fig. 21. The distribution of temperature (° C.) at a depth of 300 m. on survey II, September-October 1950.

Between the Walvis Bay line and the Mowe Point line the distribution of surface-temperature is
exceedingly complex. From the bathythermograph observations and the records from the distant
reading thermograph a more detailed construction of the surface isotherms has been set out in Fig. 19.
It will be seen that while the cool coastal water (less than 140 C.) continues along the coast as far as
Mowe Point, the temperature rises fairly rapidly offshore to an area of relatively high temperature
some 60 miles from the coast. Here the temperature is typically oceanic, reaching a recorded maximum
of 16-5° C. This area of high temperature, a patch about 60 miles in diameter, is apparently an isolated
feature, for on its western boundary the temperature is again lower (15-5° C.) Several interpretations
could be made of this distribution, and unfortunately little guidance can be obtained from the sub-
surface data, which are only available at the stations. It may be that this phenomenon is solely due

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY 169

to local surface-heating, but on the other hand the bathythermograph observations definitely suggest,
although not conclusively, that this feature is part of an extensive detached eddy between ' oceanic '
and 'coastal ' types of water. If this interpretation is correct the cooler water outside this warm area
would combine to give the eddy an overall diameter of some 120 miles, and extending in depth to 50 m.

At Cape Frio, in 180 30' S., a temperature of 15-1° C. was recorded about 7 miles offshore, but
north of this yet another patch of cooler water was present, extending up to the Cunene river mouth.
From there northwards, however, the temperature of the surface-waters increased steadily, until in
140 S. the tropical boundary was encountered and the temperature increased rapidly to values over
22° C.

The distribution of temperature and salinity at a depth of 100 m. (Fig. 20) has the same general
characteristics as that at the surface, the cooler and less saline waters lying uniformly along the coast,
with the warmer more saline waters offshore. Although the smaller number of observations at this
depth are probably responsible for the smoothing out of the isotherms and isohalines, they still show
up quite clearly the pronounced eddy in the vicinity of the Orange river. The regions of lowest
temperature and salinity as shown by the io-o° C. and 34-80 %0 isolines are present to the south of the
Orange river and off Luderitz Bay.

At 150 m. an entirely different pattern appears. This is not illustrated but along with the distribu-
tion at 200 m. it represents a transition to the distribution at 300 m. (Fig. 21). At 300 m., in spite of
the paucity of observations, it is possible to recognize that the distribution is roughly similar to that at
a depth of 200 m. on survey I. Here we find an apparently anomalous situation with the warmer and
more saline water nearest to the coast while the cooler water lies further offshore. There can be no
doubt that further to the west warmer water must have been present, and so it seems that on this
survey the cooler water at this depth must have been still more extensive and further displaced from
the shore than on survey I. This was concurrent with an increase in the current of warmer water
which runs south along the coast.

Vertical distribution of temperature and salinity
An outstanding feature of the second survey in comparison with the first is the absence of the very
strong thermoclines which were found so frequently in March. At most stations, particularly those in
the offshore waters, there is a convection layer on the surface, and below this the temperature and
salinity decrease gradually into the deeper water. In several places where a well-defined convection
layer had apparently been present, surface heating has reduced the density and produced a thin stable
surface layer. The depth distribution of the convection layer on survey II is shown in Table 5.

The Orange river line (280 30' S.). The low surface salinities inshore are a result of the fresh-water
inflow of the river, and they have produced a very stable surface layer at station WS 1050. Further
offshore, however, at WS 1051 a thin convection layer is present, and this deepens and becomes more
pronounced farther to the west. The vertical sections of temperature and salinity (Figs. 22 and 23)
contrast vividly with the conditions in March. The marked upward slope of the isotherms and iso-
halines towards the coast, combined with the active offshore transport of surface-water as suggested
by the salinity section, shows most clearly the characteristics of active upwelling. It will also be seen
that the isotherms and isohalines, while approaching the surface inshore, also rise towards the surface
in the proximity of the edge of the continental shelf. There seems to be clear indication, therefore, of
an additional divergent movement in this position. As will be shown later, this is probably associated
with the mechanism of the process of the upwelling.

North of the Orange river line the tongue of warm offshore water at WS 1057 and 1058 has an
almost constant temperature in the upper 100 m. A relatively sharp boundary was present on the

170

DISCOVERY REPORTS

STATIONS WSI056

SEA MILES
OFFSHORE 175

WS IOS0

Fig. 22. Distribution of temperature (° C). Section off the mouth of the Orange river, 21-24 September
1950, survey II. Positions of the stations are shown in Fig. 2.

STATIONS WSIOSt

SEA MILES
OFFSHORE l75

100

200-

400

Fig. 23. Distribution of salinity (%0). Section off the mouth of the Orange river, 21-24 September
1950, survey II. Positions of the stations are shown in Fig. 2.

TEMPERATURE

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY 171

northern side of this wedge, where it abutted on the cooler coastal water. At stations WS 1061 and
1062 a slight temperature inversion was revealed by the bathythermograph observations, at depths
of 105 and 75 m. respectively (Fig. 24).

The Sylvia Hill line (250 S.). Stations WS 1063-70 did not
lie sufficiently far to the west to reach the boundary with oceanic
water, and consequently they all lie within the coastal water.
The vertical sections (Figs. 25 and 26) show that active up-
welling must have been taking place on this line.

The Walvis Bay line (230 S.). Here again there are indications
of active upwelling (Figs. 27 and 28). The inshore waters show
an interesting point: the salinity of the inshore surface-water is
very low (34-84 %0) and remained low out to WS 1078 (34-96 %0).
Below this, however, the salinity increased to 34-97 %0 on the
sea bed of the continental shelf.

The salinity section suggests that there is a pronounced up-
lift of deeper water taking place on the edge of the continental

10 II
1 1

12 13

.-/'

SO-^

WSIOG2 ',

/ WSI06I

100-

/ r
/

Fig. 24. Graph ot temperature (° C.) against
depth (metres) at stations WS 1061 and 1062,
showing inversions present at these stations.

STATIONS WSI070

SEA MILES
OFF SHORE l0°
O-

WS IOt.9

WS 1068
I

WSK%4

Fig. 25. Distributions of temperature (° C). Section off Sylvia Hill, 25-27 September 1950, survey II.

Positions of the stations are shown in Fig. 2.

STATIONS WSI070
SEA MILES
OFFSHORE 100

WSIOM
I

WSIOM

•100

30O

200- „--

Fig. 26. Distribution of salinity (%0). Section off Sylvia Hill, 25-27 September 1950, survey II.
Positions of the stations are shown in Fig. 2.

DISCOVERY REPORTS

500

Fig. 27. Distribution of temperature (° C). Section off Walvis Bay, 29 September-3 October 1950,
survey II. Positions of the stations are shown in Fig. 2.

STATIONS WSIOSO

SEA MILES

OFFSHORE

O-

100-

200-

X 300-

400-

500

150

WS 1081 WSI079

I I

125 IOO

J L

WSI078
I

WSI077 WSI075
I I

Fig. 28. Distribution of salinity (%0). Section off Walvis Bay, 29 September-3 October 1950, survey II.

Positions of the stations are shown in Fig. 2.

OBSERVED DISTRIBUTION OF TEMPERATURE AND SALINITY 173

shelf, and that the low salinity of the surface-layers inshore must be connected with this movement,
but it is difficult to interpret the significance of such a movement.

The lack of any salinity observation in the region of the large eddy between the Walvis Bay line
and the Mowe Point line prevents us from drawing any conclusion about the structure and movement
of these waters.

The Mowe Point line (190 44' S.) (Figs. 29 and 30). Throughout the greater part of this line the

STATIONS WSII02
SEA MILES I

OFFSHORE l25
O

WSIIOI

WSI097 WSIO%

I I

-200

Fig. 29. Distribution of temperature (° C). Section off Mowe Point, 9-1 1 October 1950, survey II.

Positions of the stations are shown in Fig. 2.

STATIONS WSII02
SEA MILES I

OFFSHORE l25
O

200

3O0-

Fig. 30. Distribution of salinity (%,). Section off Mowe Point, 9-1 1 October 1950, survey II.
Positions of the stations are shown in Fig. 2.

7-2

174 DISCOVERY REPORTS

highly saline water at the surface, bounded both inshore and offshore by water of lower salinity, shows
that the stations have sectioned the northern edge of oceanic surface-water which was involved in the
large eddy lying south of this line. The isotherms and isohalines both slope upwards towards the
coast at the inshore stations, but this does not necessarily mean that active upwelling was taking place.
The same effect could be created by the presence of the oceanic water so close to the coast, compressing
the coastal type of water into a narrow strip adjacent to the land. The salinity and temperature
distribution in such a strip of water would then necessarily, on account of the laws governing the
density distribution, resemble the pattern created by upwelling.

The isolation of this inshore water from the deeper water, apparent in the salinity section (Fig. 30),
suggests that active upwelling was not taking place.

To the north of this section another centre of upwelling may have been present at Cape Frio (see
Fig. 7 b) in 180 30' S., but there are insufficient data to decide this question.

To sum up, it is evident that the same essential features were present on both of these surveys.
On the second survey we can distinguish the same two types of surface water.

(a) The coastal or upwelled water, which on survey II is characterized by temperatures below
14-0° C. and salinities of less than 35-00%,,. The convection layer in this water is better developed
than on survey I, but the underlying discontinuities are not so pronounced. These differences must
be caused by the stronger winds and upwelling on survey II.

(b) The offshore water, characterized by temperature over 14-0° C. and salinities of over 35-10 %0.
This is in general cooler, but very similar in other respects to the same type of water on survey I.

In survey II, active upwelling was found on the two southern sections, and possibly also on the
Walvis Bay line, while only on the northernmost section (the Mowe Point line) were quiescent condi-
tions encountered.

Table 6. Stability of the 0-50 m. and 0-100 m. layers

Survey I Survey II

■

iob datjdz

Station

10s datjdz

Station

1
0-50 m.

0-100 m.

0-50 m.

0-100 it

WS976

-63

845

WS 1 102

975

743

WS 977

2000

H53

WS 1 100

675

550

WS978

2113

1535

WS 1098

500

495

WS 979

1825

1297

WS 1096

1213

855

WS980

2050

1387

WS981

I77S

—

WS 1080

268

WS 1081

388

478

WS986

1088

992

WS 1079

258

WS987

475

577

WS 1078

175

230

WS988

1825

I237

WS 1077

638

538

WS989

1 100

—

WS 1075

150

—

WS996

875

1257

WS 1070

163

262

WS997

1850

1413

WS 1069

375

37°

WS998

1900

1540

WS 1064

438

3°5

WS 999

2138

1778

WS 1063

500

—

WS 1000

2375

817

WS 1001

7688

5H5

WS 1056

162

WS 1002

4°7S

—

WS 1055

138

WS 1054

275

5°3

WS 1053

250

387

WS 1052

200

447

WS 105 1

650

617

WS 1050

2450

—

the water masses j7s

Stability of the water masses
To obtain some further comparison of the characteristics of the upper water layers on the two surveys
the vertical stability of the water columns has been determined. This has been calculated approxi-
mately as io5 datjdz for the layers 0-50 m. and 0-100 m., and is set out in Table 6.

In spite of the instability of the water at WS 976 the great stability of the upper 50 m. at all the
other stations on survey I contrasts most vividly with the generally lower stability on survey II. This
pronounced difference, the whole region being some ten times more stable in the upper 50 m. on the
first than on the second survey, reflects clearly the difference in the meteorological conditions on the
two surveys.

THE WATER MASSES
Water masses of the South Atlantic
Wiist (1935) plotted T-S curves for three more or less meridional lines of 'Meteor' stations in the
Atlantic Ocean. The remarkable similarity of these curves within the South Atlantic is at once apparent
from his diagram (his p. 216). Excepting the upper layers where external factors come into play,
the curves all fall within a regular pattern. A typical T-S curve for the South-east Atlantic is shown
in Fig. 31.

The ' Bottom ' water is a cold dense mass of water lying in the deeper basins. It originates in the
Antarctic, where cooling processes in the proximity of the continent cause the water there to sink
down the continental slope, and being very dense it spreads out across the ocean floor. The main
centre of this sinking appears to be the Weddell Sea, but it probably also occurs at other points along
the Antarctic coast. The water thus formed can be traced by its low temperature and salinity, and it
describes a northward flow into the South Atlantic. Partly under the influence of the earth's rotation,
but probably mainly owing to the bottom topography, the principal flow takes place up the western
side of the South Atlantic. A certain amount of the water flows up into the Cape Basin, but this does
not go far north since its passage is interrupted by the Walvis Ridge, a connecting ridge between the
African continent and the Central Atlantic Ridge. Wiist (1935) demonstrated that the potential
temperature of the bottom water south of the Walvis Ridge was about 1 ° C. lower than that to the
north of the ridge where it was over 20 C. He suggests that the flow up the western side of the ocean
infiltrates in a cyclonic movement through a gap in the Central Atlantic Ridge (the Romanche gap)
and enters the Angola Basin from the north.

Lying above the bottom water, and extending up to nearly 1000 m. from the surface, there lies
a great mass of water called the ' North Atlantic deep water '. Owing to its great homogeneity it
occupies relatively little space on the T-S diagram (Fig. 31), the observations within it being clustered
around an intermediate maximum of salinity. Taking other factors into account, however, Wust has
shown that the deep water is, in actual fact, composed of three separate layers. As far as we are con-
cerned the three deep water layers can all be taken together, and considered as having a general
southward flow. The water leaving the North Atlantic does so principally on the western side, so that
the best-defined flow in the South Atlantic is found down the South American coast, the movement
in the eastern part of the ocean being much less well defined. On reaching higher latitudes the whole
mass of deep water becomes directed to the east.

Above the deep water, there is a layer of minimum salinity. This characterizes the main axis of
northward flow of the ' Antarctic intermediate water '. Formed by the sinking of antarctic surface-
water, from the antarctic convergence in about 500 S., this layer moves northward at a depth of
between 600 and 800 m. Again the strongest movement is on the western side of the ocean, and indeed

176 DISCOVERY REPORTS

in the eastern South Atlantic there seems to be a tendency to an eastward movement, particularly
in the Gulf of Guinea, where it apparently diverges cyclonically from the main northerly trend. Thus
in the South-west African region the flow is again ill defined.

In the subtropical region between the surface-waters, and the salinity minimum of the antarctic
intermediate water the T-S curves follow a nearly straight line relationship to within about 200 m.
of the surface, above which the circulation becomes more complex within the tropical and sub-
tropical surface and subsurface layers. This water mass, represented by the nearly straight line
part of the curve, has been termed the 'South Atlantic central water' (Sverdrup, Johnson and
Fleming, 1946). The process of its formation is still rather obscure. Sverdrup et al. (1946)
suggest that it is probably formed by a simple process of sinking along surfaces of equal density in
the region of the subtropical convergence, as the vertical T-S relationship of the South Atlantic

15-

10'

67, /'4O0 1 ^
(ISO)/0 ^

1000-

•\ N A DEEP

3250

ANTARCTIC BOTTOM WATER

M 50

SALINITY

3500

35 50

Fig. 31. A typical temperature-salinity curve for the south-east Atlantic, drawn from observations at ' Discovery' station 673.
The water masses represented on the curve are named. The additional points in open circles are the T-S relationships at
the stations (675, 671 and 668) at the depths (in brackets) shown. These stations lie in a north-south line across the subtropical
convergence, so the points show the horizontal T-S relationships at subsurface depths across this region, indicating the close
similarity to the vertical T-S curve for the South Atlantic central water. Depths are in metres.

central water corresponds closely with the horizontal T-S relationship in the subtropical convergence
region (see Fig. 31). Clowes (1950), however, has taken exception to this view on the grounds that
an examination of the surface T-S relationships in the region o° to 200 E. and 300 to 400 S. fails to
show any similarity to the vertical T-S curve of the South Atlantic central water. He considers that
a more likely explanation is a direct mixing between the antarctic intermediate water and the sub-
tropical surface- and subsurface waters, which would probably take place in the region of the sub-
tropical convergence.

North of the antarctic convergence in about 500 S., where the antarctic surface-water sinks to form
the intermediate water, there lies a belt of warmer water, the subantarctic water, whose characteristics
suggest that it is a mixture of antarctic water and warmer water from the north. Extending north-

THE WATER MASSES 177

wards to the subtropical convergence, a distance of about 600 miles, this is a relatively shallow layer.
Under a well-mixed surface-layer, which is rather poorly saline, there is a pronounced subsurface
salinity maximum, and below this again the water becomes less saline.

It seems fairly certain (Deacon, 1936) that this subsurface salinity maximum represents the core
of a southward flow within the subantarctic zone. The properties of this water suggest that it is
replenished from two sources, from a subsurface highly saline current within the subtropical zone
itself, and (to a lesser extent) from subantarctic water sinking at the subtropical convergence and
returning to the south. The vertical T-S curve below the subtropical convergence suggests that the
central water there is a mixture between water of higher salinity than the surface-water and the
antarctic intermediate water (see Fig. 31), showing that it is probably the subsurface current which is
involved in the mixture in this region. The subsurface salinity maximum is not generally distributed
over the ocean, however, and no doubt elsewhere it is the surface-water which mixes with the inter-
mediate water as occurs in the subtropical region itself.

Above the salinity maximum where present, and generally over the subtropical zone, the surface
water is a fairly homogeneous layer, and its movements, governed principally by the trade winds,
follow an anti-cyclonic pattern. From the Brazil current flowing southwards down the western side of
the South Atlantic, the water is carried to the east with a decreasing southerly component. It appears
to be the balanced effect of this movement with the northward drift of the subantarctic surface-water
which is responsible for the maintenance of a sharp subtropical convergence. Deacon has already
pointed out that there is not much likelihood of this water sinking at the subtropical convergence, and
it is probably mostly carried east in a direction more or less parallel to the convergence. As it reaches
the eastern side of the ocean, it turns more to the north, and, with perhaps a contribution from the
Agulhas current (Dietrich, 1935 a, b), it returns up the eastern side of the Atlantic as the South-east
trade wind drift. Across the Atlantic, and forming a line approximately from Angola to Rio, about
the 230 C. surface isotherm, there is a convergence of the surface-water, and to the north of this line
there is a warm highly saline layer which is very poor in nutrients and sharply divided from the under-
lying water by a strong discontinuity layer. This is the tropical surface-water, which owes its existence
to the immense amount of heating and evaporation in this region. From the African side the south
equatorial current carries this water across the Atlantic to Brazil, somewhat in the form of a left-hand
screw. Within itself the layer is homogeneous and well mixed.

Temperature-salinity relationships of the South-west African waters
The typical T-S curve for the offshore stations of the 'William Scoresby ' is very similar to the general
pattern described for the South Atlantic.

None of the 'William Scoresby' stations was in deep enough waters to encounter the Antarctic
bottom water which the ' Meteor ' observations showed to fill the depths of the Cape Basin, but at all
stations of sufficient depth off the continental slope the North Atlantic deep water was encountered.
At WS 976 only, a maximum salinity of 34-91 %0 at 2420 m. was recorded. This represented the nearest
observation to the core of the upper deep water, but at all other stations salinity values around
34-80 %0, and still increasing at the lowest depths of observation, indicated that the central core of the
upper deep water had not been reached.

Sometimes between the southward flow of the North Atlantic deep water and the northward flow
of antarctic intermediate water, a slight temperature inversion is produced, such as was recorded at
station WS 996 where the water at 1470 m. with a temperature of 3-05° C. was 0-04° C. warmer than
the water at 11 70 m. Deacon has recognized this layer of minimum temperature, but considers that

178 DISCOVERY REPORTS

the flow of the intermediate current is principally in the layer of minimum salinity, and that its flow
in the layer of minimum temperature is probably much affected by turbulent mixing with the under-
lying deep water.

A well-marked layer of minimum salinity was encountered at all stations off the continental shelf
on both of the surveys. Table 7 shows the depths and observed salinities in the layer of minimum
salinity. Wiist developed a method for studying the mixing path of a water type from its T-S relation-
ships. Initially the water type is plotted as a point on a T-S diagram. As it mixes with adjacent layers

SALINITY '/o»

34 00

-J I L

3500

35 50

Fig. 32. Temperature -salinity relationships of the water layers between 100 m. and the salinity minimum of the Antarctic
intermediate water. The heavy line shows the relationship in the core of the Antarctic intermediate water from its source
(left) to its northern limit (right), after Wiist, 1935. The thin line is the line characteristic of South Atlantic central water
(Sverdrup, 1946).

the point moves along a line, until eventually its characteristic, say a salinity minimum, disappears
(Fig. 32). Thus one can follow the water type from its beginning until it is completely obliterated by
mixing with other waters. This method is known as the ' Kernschichte methode ' — the core method.
Applying it to the intermediate water one finds that in the core of the antarctic intermediate layer the
effect of vertical mixing has altered the T-S relationship from the original water type (T = 2-2° C,
S = 33-80 %o) to a value of T = 4-7° C, S = 34-4 %0 off South-west Africa (Fig. 32). As the salinity

Table 7. Salinity minima in the antarctic intermediate layer

Station

WS976
WS 977
WS978
WS986
WS996
WS 997
WS 1056
WS 1070
WS 1080
WS 1081

WS 1 102

Salinity minimum

(%o)

34-5°
34-34
34-45
34-38
34-34
34-31
34-33
34-42
34-38
34-29
34-31

Depth
(m.)

700

820

600'

800

600

570

600

600, 820

780

990

630

The figures show the minimum values of salinity recorded at 'William Scoresby' stations,

and the depths of the observations.

THE WATER MASSES 179

minimum finally disappears at T = 6-6° C, S = 34-95 %0 in about 150 N., so we can consider that the
antarctic intermediate layer off South-west Africa contains only about 50 % of the original water type.

Above the antarctic intermediate water core, and to within 100 m. of the surface, all the 'William
Scoresby' observations fall fairly close to a nearly straight line joining the points T = 14-0° C,
S = 35-20 %0 and T = 4-7° C, S = 34-40 %0. It will be seen that this line lies somewhat to the left
of Sverdrup's curve for the South Atlantic central water (Fig. 32) (Sverdrup et al. 1946), but it
should be remembered that Sverdrup has taken a mean curve for the whole South Atlantic.

Above 100 m. external influences come into play and the water becomes subjected to heating,
cooling, evaporation, etc., and these account for the more widely spaced distribution of the T-S points.
But the effect of these external influences is fairly well defined and with caution it is possible to derive
at least some information concerning the surface water-layers from their T-S relationships.

Water masses of the upper layers (0-200 m.)
Oceanic and coastal surface-waters
The different types of surface-water which were recognized from the general distribution of tempera-
ture and salinity (p. 174), form, of course, a natural grouping for the T-S curves of the upper water
masses. As the upwelled water has been brought to the surface from some subsurface depth offshore,
its T-S characteristics are similar to those of the water at the depth from which it was upwelled,
except that it has undergone a certain amount of modification in the process of uplift.

If we compare an inshore and offshore station on the first survey — stations WS 1000 and 996
(Fig. 33 a) — it is clear that at the inshore station the upper 50 m. is composed of a mass of water
corresponding to that at 200 m. at the offshore station, but warmed up, reaching a temperature of
180 C. at the surface. The low salinity (34-9 %0) of this water on the surface contrasts strongly with
the high salinity (35-18 %0) of the oceanic surface-water. Similarly on survey II (in Fig. 336) there
is again a contrast, although rather less pronounced.

The T-S diagrams also demonstrate clearly the mixed nature of the water inshore at Walvis Bay
on survey I. Comparing Fig. 33 c with Fig. 33a, we can see that the surface-water at stations WS 979
and 980 lie somewhere between the true oceanic and true coastal characteristics.

Finally, for the 250 S. line on the first survey the T-S diagrams (Fig. 33d) show the 'oceanic'
characteristics of the inshore 'station'.

We see, therefore, that the upwelled water originates from the South Atlantic central water, at
depths of 200-300 m. Apparently the upwelled water is not subjected to any significant mixing with
the warmer and more saline 'offshore' surface-waters in its process of uplift. Indeed, everything
suggests that it remains quite discrete from the latter. On the sea surface, as we have already seen,
there is in most cases a sharp boundary between the two types of water except in areas where mixing
has obviously taken place.

It is evident that these two water masses form, on both surveys, a series of eddies along the coast,
tongues of upwelled water diverging offshore and inter-locking with wedges of offshore water con-
verging towards the coast. It is difficult to generalize about the depth to which the eddies extend, as
some of them appear to retain their identity to the depth of upwelling while others are very much
shallower.

Dynamic height anomalies
Owing to the lack of direct observations of surface-currents it has been necessary to resort to some
indirect method of estimating the actual water movements which were taking place during the surveys.
The most widely used of such methods is that based upon the theorem developed by Bjerknes

180 DISCOVERY REPORTS

(Sandstrom, 1919). Other methods, such as the isentropic analysis used by Montgomery (1938), have
in certain cases an advantage, but after experimentation with both methods, and bearing in mind that
the observations do not properly satisfy the requirements of either, a straightforward presentation of
the dynamic height anomalies has been made. A few words may be said about the theoretical implica-
tions of this method in so far as the present work is concerned.

SALI

NITY '/v,

WS996

20-

345
_l ■ ' ' 1_

350

35 5

-J 1 I

WSI05&

345

350

i/-\°

1 1

p ■

■ 1 1

20 -

s—°

WS980

WS976

ws <??<}•'

15*-

SJS

100

•

y 300

•

10-

•

"300

15-

10"

345 350

J I I I I 1 1 I

355

_j 1

WS986 o

,00/ (

'JOO

W5 968

C D

Fig- 33- Temperature-salinity relationships at 'William Scoresby' stations, (a) WS 996 and WS 1000 (broken line) off
Orange river mouth, survey I. (b) WS 1052 (broken line) and WS 1056 off Orange river mouth, survey II. (c) WS 976
(broken line), WS 979 (dotted line) and WS 980 off Walvis Bay, survey I. (d) WS 986 and WS 988 (broken line) off Sylvia
Hill, survey I. Positions of stations are shown in Figs. 1 and 2.

First it should be noted that Bjerknes's theorem applies to currents in which a state of 'stationary
motion ' is maintained. In other words, it assumes that while the current flows the distribution of
mass in the water remains unaltered. This implies that no mixing, or change in properties of the
water particles along their path, may take place, and that no vertical translatory movement should
occur. On these assumptions the horizontal movement of the water can be related to the distribution

THE WATER MASSES 181

of mass within that water. Parr (19386) has already emphasized the importance of these points in
interpreting charts of dynamic height anomalies.

In the waters off South-west Africa, it is quite obvious that the requirements of Bjerknes theorem
are not satisfied. Clearly the wind in this region has a considerable effect on the sea-surface, and there
are undoubtedly considerable vertical movements of the water masses. It is therefore considered
unwise to place too much reliance on the charts as depicting actual currents, but rather to look upon
them as plans of the distribution of mass within the water above an arbitrary level surface.

In the construction of the charts it is desirable to choose a surface of no motion, above which the
mass of water can be calculated. In the present observations it is impossible to be certain that such a
surface does exist. Normally such a surface is chosen at a considerable depth, where the movements, if
any, will be so small relative to those at the surface that they can be ignored. The 'William Scoresby's'
observations lie, however, for the greater part in shallow waters, and there is little likelihood that any
level will present a surface of no motion in these observations1. As the best compromise, however, the
600 decibar surface has been chosen, and the topographies of the sea-surface, and the 200 db. surface,
are shown relative to this in the charts in Fig. 34. Many of the present observations have been made
in the relatively shallow waters of the continental shelf where they cannot extend to the depth of the
reference surface chosen in the deeper water offshore. Helland-Hansen (1918) proposed a method to
overcome this difficulty. He suggested that the land mass in the vertical section representing the
continental shelf and slope, should be replaced by a fictitious body of water which is considered to be
at rest, and in which the isosteric surfaces would, therefore, be horizontal. In the adjacent water
mass the isosteric surfaces would tend to become horizontal as they approach the continental slope,
for, owing to friction, the velocity along the sea-bed must approach to zero. For this reason Helland-
Hansen suggested that the isosteres as they approach the sea-bed should be drawn horizontal and
produced horizontally through the land mass, thus furnishing arbitrary levels for the calculation of
the heights of the isobaric surfaces over the land mass. In face of the difficulties this seems a fairly
reasonable assumption to make, but it has no physical basis whatsoever, and it is indeed difficult to
imagine the existence of such an arrangement. Groen (1948) has discussed another method which
was suggested by Sverdrup, and proposed yet another, that of continuing the isosteric slopes into
the land mass, but it is doubtful whether these produce a picture any more realistic than that given by
Helland-Hansen's method which has been used in the following.

Although a precise picture of the currents at different levels cannot be attained, it is intended that
the charts should at least serve as a check on the water-movements deduced from the distribution of
temperature, salinity and other properties of the water masses. The movements shown will probably
be more correct during survey I when there was less vertical movement, than during survey II.

Surface topography (Fig. 34)
On survey I the most pronounced feature of the chart shows the tendency to a movement towards
the coast in the latitude of Walvis Bay (230 S.). This flow appears to bend southwards along the coast
and is no doubt responsible for the mixed nature of the water inshore at Walvis Bay, and the pro-
nounced oceanic influence at the inshore stations on the 250 S. line. In its southerly movement, it
displaces away from the coast the north-westerly flow of coastal waters from the south, so that in

25 ° S. there is a southerly movement of mixed oceanic water inshore, and a northerly movement of
coastal water offshore.

1 Attempts to define a level of no motion using techniques such as that of Sverdrup and Flemming (1941) have given
little guidance with the present observations beyond suggesting that the 600 decibar surface may be one of relatively little
motion.

8-2

182

DISCOVERY REPORTS

_L I I L

Fig- 34- Dynamic height anomalies of the sea-surface and 200 db. surfaces relative to the 600 db.

surface, for survey I and survey II.

THE WATER MASSES 183

The eddy which lies to the north of the Orange river line is probably a fair representation of the
westerly flow of coastal water adduced from the temperature and salinity observations.

On survey II the movements are considerably more intense. Undoubtedly the sparsity of data
shows a simpler picture than is shown in the surface-temperature chart (Fig. jb) which is constructed
from a much greater number of observations, but within the three great eddies shown, the cooler
coastal waters show a pronounced offshore, or longshore movement to the north and west. In
conjunction with this the oceanic waters move in an easterly direction towards the coast.

There were very few occasions on which the set of the ship could confidently be ascribed to water-
movement as distinct from wind leeway. At the station on the outer end of the Walvis Bay line on
survey I a northerly set of about 1 knot was encountered with a light wind. This agrees with the
computed currents (Fig. 34). The only other occasion upon which we can be reasonably certain the
effect was solely due to currents was between stations WS 1057 and 1061 on survey II. When the ship
was steaming north from the Orange river line stations to the inshore end of the 25 ° S. line, she was
set 065 ° at h knot with no wind. Once more this is in agreement with the computed currents.

Topography of the 200 db. surface
The lesser number of observations at this depth give the appearance of a very simplified pattern.
On survey I there is clearly a southerly movement along the coast from the north, penetrating south-
ward and tapering in towards the coast, and finally disappearing in about 280 S. Seawards of this the
water appears to move to the N.N.W.

On survey II offshore the principal movement is once more to the north, but there is some indica-
tion of a south-easterly flow on the landward side of a trough line running north-west through
WS 1070. This tendency to a southerly or onshore movement at this depth in the water adjacent to the
continental shelf will later (p 1 90.) be seen to be connected with the process of upwelling. It is postulated
that this is a compensatory movement replacing the water which has been drawn up to the surface
inshore and we have, therefore, called it the compensation current.1 This southerly current is warmer
and more saline than the waters seaward of it in the trough which separates it from the northerly
current farther offshore.

The water masses at 200-600 m.
Generally speaking, on both surveys, the waters in this layer correspond very closely with the mean
temperature-salinity relationship already outlined for the South Atlantic central water. Table 8 gives
the salinity values corresponding to the given temperatures at each station. On the first survey the
mean range of salinity at the given temperature is only o-n %0, and on the second survey o-io%0.

Table 8. Temperature-salinity relationships of the water masses between 200 and 600 m.

Survey I Survey II

perature

fC.)

976

977

978

986

996

997

1102

1100

1098

1080

1081

1079

10 JO

1056

'055

12-0

35-03

35-io

I 1-0

34-91

—

34-83

34-82

34-91

34-97

35-oo

34-87

34-9o

—

io-o

34-76

34-84

34-73

34-79

34-73

34-72

34-80

34-84

—

34-74

34-Si

34-82

34-8o

3476

34-78

Q-o

34-65

34-75

34-67

34-7°

34-67

34-63

34-72

—

34-66

34-71

34-75

3469

3467

34-68

8-o

34-56

34-65

34-6i

34-6o

34-64

34-62

34-6o

34-63

—

34-59

34-63

34-67

34-65

34-59

7-0

3452

34-58

34-55

34-52

34-55

34-57

34-44

34-56

—

34-51

34-54

—

34-57

34-52

34-50

34-52

34-48

34-45

34-44

34-31

34-51

—

34-43

34-66

—

34-47

34-45

34-43

5-0

34-5I

—

34-34

3431

—

34-36

34-39

The salinity values, corresponding to the given temperatures at each station are shown in parts per thousand. Mean: Survey I = o-ii%„;
II = 0-10%,.

1 Yoshida and Mao (1957), and later workers have shown that divergence and consequent upwelling at the surface is
likely to be accompanied by a poleward movement in the subsurface layer.

184 DISCOVERY REPORTS

It may be said, therefore, that on the basis of the temperature-salinity relationship, it is not
practicable to distinguish any significantly distinct water masses in the layer 200-600 m., and also
that it is all characteristic of the South Atlantic central water. As will be shown later, however, when
dealing with the non-conservative properties oxygen and phosphate, a very marked distinction is
present in this layer.

The antarctic intermediate water
The depth distribution of the observed salinity minimum in this layer has already been given in
Table 7. It is noteworthy that at its core off South-west Africa only 50% of the original water type
is present. Later it will be shown that the upwelling takes place from considerably lesser depths than
this, and it is in fact South Atlantic central water which is upwelled and not, as has often been supposed,
the Antarctic intermediate water. It is true that the former may contain a little of the latter but the
proportion of antarctic intermediate water must be extremely low.

UPWELLING

Previous work on the mechanism of upwelling
Several explanations have been put forward to account for the presence of the cold water along the
south-west African coast. The earliest idea held was that the Benguela current was a continuation of
the west wind drift, bringing down cold water from the higher latitudes of the antarctic. Ross (1847)
(see p. 132), however, demonstrated that this could not be true because warmer water was present to
the south of the Benguela current, cutting off any continuous flow from the antarctic. Yet this view
was maintained by some authorities even as late as 1910 (Engeler). Ross did not offer any satisfactory
alternative explanation to the South Polar current theory, but later workers gradually developed the
idea that the cold water must come up from subsurface layers. Several suggestions were made as
to how this uplift, or upwelling, came about. Witte (1880) deduced on theoretical considerations that
the upwelling must be brought about either by the effect of the earth's rotation on such a meridional
current as this, or possibly by offshore winds driving surface-water away from the coast. Murray
(1888, 1 891) showed the latter to occur in the lochs on the west coast of Scotland, where, in summer-
time, offshore winds produced a depression of the surface temperature along the shore. Buchanan
(1880) and Buchan (1895) held that the same process was of general application to the major upwelling
regions off the west coasts of the continents. Schott (1902), however, while considering that the
upwelling along the north-west African coast could be explained on these grounds (as the winds blow
either parallel to the coast or offshore), pointed out that this could not hold good for the south-west
African coast. Here the winds were principally onshore in the coastal region.

Schott offered an alternative explanation. Since the main impulsive force of the Benguela current
was the south-east trade wind, the current would be deflected, under the influence of the earth's
rotation, away from the coast. The water thus removed must be replaced, and owing to the direction
of the coastline this would have to be a vertical compensation. This theory Schott supported with the
fact that where the African coast recedes to the north-east (in about 170 S.) the upwelling fades out
and becomes an irregular phenomenon, the compensation flow then being able to take place hori-
zontally on the sea surface from the north-east.

Thorade (1909) states, with regard to the California current, that 'Auch dieser Grund kann fur uns
nicht in Betracht kommen, denn einmal ist unser Auftriebgebiet bedeutend weiter von Aquatorial-
strom entfernt, und dann entwickelt sich dieser [the trades] am Kraftigsten gerade wahrend der
Wintermonate, in denen die Auftrieberscheinung im Riickgange begriffen ist'. Thorade proceeded

UPWELLING 185

to explain the Californian upwelling by Eckman's theory of currents. He showed that the upwelling
is a direct effect of the coastal winds which on the assumptions of Eckman's theory need not blow
offshore to produce an offshore transport of surface water. A wind blowing parallel to the coast would
be sufficient to induce such a transport with consequent upwelling.

Sverdrup (1938), from a detailed examination of the Californian current, supports this view, and
concludes that the upwelling is a direct effect of the local winds transporting surface-water away from
the coast. Gunther (1936) found that on the Peru Coast the 'William Scoresby's' observations indi-
cated that the upwelling was brought about ' as a result of wind acting in conjunction with forces due
to the earth's rotation'.

The present work indicates that while the trade wind in the open ocean must maintain the denser
water nearer the surface inshore, the periodic and local intense upwelling is probably mainly dependent
upon the local coastal winds producing a northwards, longshore or offshore displacement of the
surface water, thus initiating a vertical compensation flow from the subsurface layers.

Ekman's theory (1905) provided the basis of our present-day understanding of the effect of wind
stress on the sea-surface. It shows us qualitatively that, owing to the effect of the earth's rotation and
frictional forces, the drift produced by a wind blowing over the ocean deviates at an angle of 45 ° to the
left of the wind direction in the southern hemisphere. Owing to the viscosity of the water, the velocity
in this drift current will decrease regularly with depth. There will also be an increased deflection with
depth, until a point is reached where the current is directed against the surface drift. At this point
the velocity of the current is about i/23rd of that at the surface, and Ekman has termed this depth (D)
the ' depth of frictional influence '. While the current vectors at different levels in the wind current
vary, the total transport remains directed normal to the wind direction (that is 900 to the left in the
southern hemisphere).

These results apply to an ocean of which the bottom is very deep, and where the influence of coast-
line and varying density of the water is not considered. In this latter respect, the quantitative applica-
tion of the theory is hindered, as the magnitude of the reaction between the different density layers
in the sea is not known. Eddy viscosity is, however, a measure of this reaction, and more recently
Rosby and Montgomery (1935) have introduced the conception of a 'mixing length' which varies
with depth and upon which the eddy viscosity is dependent. On this basis they find that the deviation
of the drift is not constant as Ekman postulated, but varies with the strength of wind and with the
latitude. Even these improved assumptions, however, still appear to fall short of giving a realistic
picture.

Ekman further studied the problem of wind drift in the presence of coastlines and where the sea
bottom was shallow. Where the bottom is greater than twice the depth of frictional influence it does
not have much influence, but in shallower water there is a restriction of the deflection and slowing of
the turning with depth, until in very shallow water the whole movement follows the direction of the
wind (the effect of the earth's rotation in this case being negligible). Thus in coastal regions three
main factors affect the wind drift.

1. The position of the coastline in relation to the water in question.

2. The relation between the depth D and the sea bottom.

3. The direction of the wind stress, in relation to the direction of the coastline.

The effect of winds on the South-west African coast
We can find the approximate magnitude of D in metres from the relationship :

D = 7-6 W/Jsin 6,
where the wind stress Wis expressed in m./sec, and 6 is the latitude. (For wind stresses <6 m./sec.

186 DISCOVERY REPORTS

the formula is replaced by D = 3-67 *Jw3l<Js'm 6 (Sverdrup et al. 1946).) Even with force 8 winds the
depth D is of the order of 200-250 m., and therefore it is evident that only in the coastal region will
D have an effect upon the wind current. The region where the south-east trade prevails, outside the
continental shelf, will be void of any bottom-effects.

Thus in the open ocean the south-east trade wind will produce a surface drift in a westerly direction
and a total transport of water to the south-west. The lighter surface-water will therefore be trans-
ported away from the African coastal region. The presence of the coastline, however, prevents any
surface replacement of this water in the coastal region, and therefore a vertical replacement or
upwelling must follow. This vertical movement in the coastal region will create a distribution of
density such that the heavier water lies against the coast, and a relative current will be produced
running northward along the coast.

The intensity of this relative current will depend upon both the direction of wind and the direction
of the coastline. Now, in South-west Africa, the coast runs N.N. W. to S.S.E. and the trade wind is
south-easterly becoming more southerly in higher latitudes. The angle between the wind and the
coast increases, therefore, from south to north, and one might expect from this an intensification of
the relative current to the north.

The total transport of the wind current is, however, directly proportional to the wind stress and
inversely proportional to the sine of the latitude, so the decreasing strength of the trade wind to the
north of the region will tend to reduce the intensity of the relative current. The ultimate development
of the latter will depend on the magnitude of these various effects.

The winds in the coastal region must have an additional modifying influence on the relative current
set up by the trade wind. Furthermore, as we pass into the coastal region the sea bottom, rising to the
continental shelf, will have an increasing effect on the deflection of the wind current from the wind
stress. It is not practical, however, to calculate the deflection as the coast is approached, since the
wind also veers the nearer the coast one gets.

Observed winds and hydrographical conditions
The synoptic charts of the South-west African Weather Bureau show that in September-October the
trade winds were consistently stronger than in February-March. Theoretically this would have given
rise to a greater relative current along the coast in the former months.

To estimate the effect of the coastal winds upon this relative current the wind vectors for three
coastal stations have been plotted (Fig. 35) on the assumption that they would produce a surface drift
at 450 to the left of the wind direction. All such vectors producing a drift between a line parallel to
the coast to the north and a line normal to this offshore, have been considered positive, while all other
winds have been taken as negative. From this figure it can be seen that during the first survey the
coastal winds would only be expected to intensify the relative current off Luderitz Bay, little effect
being exercised by the light winds and calms at Walvis Bay and Orange river. On the second survey
in September-October there was a greater amount of coastal wind, particularly at Walvis Bay and
Luderitz Bay At Luderitz, it was predominantly positive and so would have intensified the relative
current, whiie at Walvis Bay the greater variation of direction might have been contributory to a more
rapid breakdown of the relative current into eddies.

The relatively calm spells at Walvis Bay and Orange river in March are reflected in the absence of
convection layers in these sections while the greater wind stress in spring is associated with better
mixed inshore waters in that season (Table 5).

A comparison of these features of the wind activity with the distribution of surface temperature
and salinity on the two surveys suggests that the localized intensification of upwelling and indeed the

UPWELLING 187

breakdown of the relative current into eddies may be largely dependent on the localized coastal winds.
Clearly, however, a correlation between such observations as wind observed at coastal stations, within
some modifying influence of the land, and hydrographical observations at sea must at best be rather
rough, and a more satisfactory correlation might be expected if it were possible to compare the winds
at sea with the coincident hydrographical changes. The only opportunity which we have of making

30 -1

o
z

f EBBUAftr MARCH

14 21 IS I 7

zjsry

30-

O--

30 J

^ n

Fig. 35. Predominant coastal wind vectors before and during the two 'William Scoresby' surveys at three points on the
coast — Walvis Bay, Luderitz Bay and Orange river mouth. Winds which would produce a longshore northwards, or off-
shore drag on the sea-surface are taken as positive and other winds as negative. Wind speeds are in knots. Heavy black lines
indicate the beginning of the survey in each position.

such an estimate of the short-term effect of the wind on the sea-surface was the occasion of a S.S.E.
gale off Walvis Bay. While steaming west along the Walvis Bay line on the second survey the ship
was forced to heave-to for nearly 48 hr. When the gale subsided the ship returned eastwards, and a
comparison of the sea-surface temperatures before and after the gale reveals some interesting features.
In Fig. 36 the sea-surface isotherms have been drawn from the station observations and the
distant- reading thermograph records; they are in black for the westward passage preceding the
gale, and in red for the eastward passage following the gale.

188 DISCOVERY REPORTS

During the period of this gale the wind records at Walvis Bay do not show any particularly stormy
trend, and so it appears, as indeed one might expect, that the gale was solely due to increased velocity
of the trade wind.

In interpreting the results certain assumptions must be made. First, surface heating must be
assumed to have been regular within the region in question. Secondly, the turbulent mixing of the
upper water layers must be assumed not to have had any great effect in the lowering of temperature
in the surface waters. This latter seems justifiable since the depth of the mixed layer at WS 1079
before the gale was 50 m., and within this the temperature was nearly uniform.

Fig. 36. Effect of wind and surface-temperature. The ship's track, stations and isotherms are shown in black for the west-
ward passage along the line of stations off Walvis Bay. While at the seaward end of this line, a S.S.E. gale was encountered
which blew for about 24 hr. at Beaufort force 8-9. Subsequently the ship returned eastward to Walvis Bay, completing
WS 1081 en route, and the track and isotherms on the return journey are shown in red. Probable surface water-movements
during the interval are indicated by the arrows.

If these assumptions are correct we can imagine that the clockwise rotation of the isotherms offshore
was indeed the result of a clockwise water-movement. The change inshore suggests that an offshore
movement south of the line had been accompanied by a landward compensation flow in two wedges,
one moving south through the position of WS 1081, and the second right inshore at Walvis Bay.

The mechanism of upwelling
With the accumulation of further theoretical knowledge of the movements of ocean currents it was
soon to be realized that upwelling was probably a far more complex process than a simple uniform
uplift of the subsurface layers. Without any factual data at his disposal, Bobzin (1922), in the third
part of his work, viewed the movements of the Benguela current from a theoretical angle. His
deductions, based on a consideration of the general principles of the movements of ocean currents,
suggested that the Benguela current existed in the form of a left-handed screw, proceeding towards
the equator. This conclusion, in view of later work, seems to have been almost a premonition.

Gunther (1936) found from the 'William Scoresby' observations in the Peru current that the up-
welling was a localized phenomenon, and took place within a series of well-defined horizontal eddies,
while Defant (1936) working on the 'Meteor' data from the South-west African region developed

UPWELLING x89

a schematic system for the upwelling there, although his data were too widely scattered to obtain as
detailed a horizontal picture as Gunther did.

Defant started by considering theoretically what events would occur in a long straight canal over
which a wind was blowing. If two bodies of water of different density are superimposed in the canal,
and if the canal runs north and south in the southern hemisphere and has a wind blowing over it from

STATIONS
SEA MILES
OFFSHORE '
0-

WSIO50
I

100-

300-

5O0-

Fig. 37. Distribution of the anomaly of specific volume. Section off the mouth of Orange river on survey II. The probable
direction of water-movement in a vertical plane, deduced from the shape of the isosteres, is also indicated. Positions of
stations are shown in Fig. 2.

south to north, then the upper water layer would be set in motion. Under the provisions of Ekman's
theory of wind drift, and when the thickness of the upper water layer is greater than the depth of
frictional resistance, the lower water layer should remain at rest, while the boundary between the two
would take up a slope across the canal. This slope would rise to the right (east, if one faces in the
direction of flow of the surface-current) and thus the underlying heavier water would accumulate on
the right-hand side of the current. At the same time a transverse circulation would form in the upper
layer, which would depend on the velocity and direction of the wind. The upper layer circulation will
form a left-handed screw motion. This would be strongest if the wind blew from the east, and sup-
pressed if it blew from the west.

Applying these deductions to the South-west African coast we can regard the coast as the canal
bank on the east. The west bank is missing, but this does not matter since the wind which is being
applied (the south-east trade) is of limited lateral extent. Defant thus deduced a circulation pattern
as in his fig. 7. The circulation is complicated by the fact that in the sea there are not two separate
well-defined density layers but a general increase of density with depth. The trade wind induces a
transverse circulation similar to that in the canal, a horizontal axis being present above which the water

9-2

WOODS
HOLE

MAS.q'

i9o DISCOVERY REPORTS

moves to the west, while below the water rises to the east. The trade wind, however, does not extend
right into the coast, and so inside its coastal boundary the surface-water is not drifted to the west, but
moves north purely by virtue of the distribution of density. This agrees with the conception of a one-
sided divergence which Defant derived from the surface-current pattern and showed in his fig. 7.

Sverdrup (1938) was more fortunate than Defant in having at his disposal detailed repeated
observations off the coast of California. From these he was able to calculate directly a vertical
velocity-profile across the upwelling region, and to relate it to the prevailing wind vectors as recorded
at coastal stations during the surveys. From this, Sverdrup argues that as upwelling occurs along the
coast, the dense upwelled water is in time transported offshore as was the surface-water which it arose
to replace. Eventually conditions will be set up whereby a convection cell develops between the
denser water lying on the surface and the lighter offshore water, this cell becoming sharply enough
defined to be regarded as a boundary.

That such a mechanism operates on the South-west African coast we cannot be certain, but the
available evidence strongly suggests that it does. The pattern of the isosteres on the Orange river line
(survey II, Fig. 37), which is probably the most complete section through an area of active upwelling,
is the best guide to an interpretation of such movements. Assuming the surface-waters to be under
the stress of a wind effective in their offshore transport, the distribution of mass on this section can be
interpreted on the basis of the water-movements suggested by the arrows. The convection cell between
stations WS 1053 and 1054 marks the boundary between the coastal and oceanic water types, to which
reference has already been made, and seems to act like a roller bearing between the two systems of
water-movement. Movement of this boundary to the west (left) would be accompanied by an
upwelling from about 300 m. depth.

Depths affected by upwelling
The most straightforward method of determining the depth of upwelling is to utilize the T-S diagrams.
From these it is possible to determine from what depth in the offshore water the coastal waters
originate. On p. 179 it was shown that in the process of uplift from subsurface depths, the coastal
waters remained discrete and that a rise in their temperature was the only important change that took
place. If then we take the origin of the T-S curve for the coastal waters at the point where it arises
from the T-S curve of the offshore water, the depth on the offshore T-S curve will give us a measure
of the depth of origin of the coastal water. These depths are set out in Table 9. The first figure shows
the depth from which water is elevated to the surface. Where a range of depths are shown the second
figure represents the maximum depth affected, but it is not necessarily implied that water is brought
from this depth right to the surface. It is normally elevated from this depth to a somewhat lesser
depth on the continental shelf.

Table 9. Depth of upwelling

Survey I

Survey II

Latitude

(m.)

(«.)

i9°44'S.

—

220

23° S.

—

200-230

25° S.

ca. 200

275-300

280 30' S.

200-350

180-320

upwelling 191

Centres of upwelling
The recurrence of upwelling in particular localities has been demonstrated by Schott (1931) and
Gunther (1936) in the Peru current. In the Benguela current this question has not received so much
attention, but Copenhagen (1953) has suggested that seven such localities exist off the South-west
African coast. He goes on to correlate these centres with the bottom topography. The position of the
centres of upwelling is deduced from a comparison of the coastal temperature with the temperature
of an arbitrary latitudinal standard, taken by Copenhagen as the temperature 200 miles from the coast.

Although the 'William Scoresby's' observations are insufficient to apply this method, it is note-
worthy that the areas of low surface-temperature (Fig. ya, b) were found in more or less the same
regions as those outlined by Copenhagen, that is to say: (1) Saldanha Bay to Orange river mouth;
(2) north and south of Luderitz Bay and extending to Walvis Bay on survey II; (3) Cape Frio to
Cunene river mouth.

A closer examination of the charts, however, shows that the colder water in the vicinity of Orange
river mouth lay in 280 S. in survey I, while in survey II it was centred on 290 S. some 60 miles farther
south. It is noteworthy also that the 200 m. contour representing the edge of the continental shelf is
50 miles offshore in 280 S., but 90 miles offshore in 290 S. This area of cold water appeared to show no
particular correlation with the topography of the sea-bed.

Probably the most that can be said from the present results is that the conditions on survey II,
which represent a characteristically active period of upwelling, show that upwelling was most pro-
nounced in the regions: (1) from 290 to 300 or 310 S. ; (2) from 280 S. to Luderitz Bay and northwards
to Walvis Bay; (3) possibly an additional area from Cape Frio to Cunene river mouth. To the south
of 300 S. we have insufficient data to allow any conclusions to be drawn.

Influence of the direction of the coastline
The absence of any pronounced upwelling from Cape Frio southwards to 22° S. while it is present
both to the north and south of this area appears to be rather significant when the shape or direction
of the coastline is considered. North of Cape Frio, the coastline runs approximately north-south.
From Cape Frio to Walvis Bay its direction changes to about 3300 to 1500 and south of Walvis Bay
to about 3520 to 1740. With a S.S.W. (202^°) wind, assuming that the drift is 450 to the left of the
wind direction, the resultant water-movement in the region between Cape Frio and Walvis Bay would
be in the direction 1600 to 3400 about io° onshore towards the coast. Clearly, therefore, along this
stretch of coastline the effect of the sea-breeze which is S.S.W. in this area would be to pile water
against the coast, rather than remove it and create upwelling.

North of Cunene river mouth (170 S.) the coastline bends away gradually in an easterly direction.
This marks the northern boundary of the upwelling and it is possible that Schott's suggestion that the
replacement flow for water carried offshore by the wind can occur on the surface, without necessi-
tating the vertical circulation of upwelling along this stretch of coast.

The southern boundary of the current which lies at the Cape of Good Hope may also be considered
to be an effect of the direction of coastline relative to the wind direction.

Seasonal variation of upwelling
The observations made by the ' William Scoresby ' cannot alone be regarded as illustrative of seasonal
variation of the current. The overall lower temperatures and greater wind and upwelling during
survey II, while probably characteristic enough of winter conditions, could no doubt be found at
least to some extent at almost any time of the year in suitable meteorological conditions. It is, therefore,

i92 DISCOVERY REPORTS

more desirable to look upon the difference between the two surveys as an example of the current in two
phases — at survey I a quiescent phase subsequent to upwelling, and at survey II a phase of active
upwelling.

It is very difficult to determine how much the upwelling varies throughout the year. Clearly it is
a phenomenon which can occur at all seasons. Schott (1902), Franz (1920) and Bobzin (1922) have
all endeavoured to make estimates of the intensity of upwelling at different seasons.

Schott based his estimate on the extent of the upwelling zone and a comparison of the temperature
of the inshore waters with that of the offshore waters at a distance of about 300 km. from the coast,
and he agrees with Franz in placing the maximum period of upwelling in August and the minimum
in summer. Schott, however, put the minimum in November and Franz in February. Bobzin, on the
other hand, derived his estimate from a comparison of the mean monthly and mean yearly temperatures
and their mean variation, and this led him to conclude that upwelling reached its maximum in summer
(October-December) and its minimum in June.

Bobzin ascribed the discrepancy between his results and those of Schott and Franz to the effect of
solar heating of the upwelled water, which would be at its greatest in summer and at its minimum in
winter, thereby masking the true changes of temperature due to upwelling. The criteria used by
Bobzin to estimate the upwelling are based on somewhat abstract considerations. Moreover, his
conclusions are based on a large number of temperature observations taken at Swakopmund and
Luderitz Bay — only two points on a coastline some 1000 miles in length. It seems doubtful, therefore,
whether Bobzin's ' Relatives Mass des Auftreibbewegung ' produces any more accurate a picture than
derived by Schott and Franz.

On the assumption that wind is the primary cause of upwelling, then we may consider the winds
to be as good a measure as anything else of the frequency of upwelling. In winter the trade winds are
slightly stronger than in summer, and one might expect a consequent intensification of the relative
current in winter. On the other hand, it is evident from Fig. 5 that the coastal winds reach their
greatest upwelling effect in that season. Clearly the crucial point is the relative effect of the trade wind
and the coastal wind, but without more detailed observations we can go no further.

NON-CONSERVATIVE PROPERTIES

The distribution of dissolved oxygen
Since dissolved oxygen is related to the biological process in the sea, its distribution is governed not
only by water-movements and interchange with the atmosphere, but also by the varying biological
activity in the water masses.

The oxygen content (Figs. 38-44) usually reaches its maximum concentration in the surface-layers
of the sea as a result of atmospheric exchange and the photosynthesis of the phytoplankton in these
layers. Beneath the surface-layers the oxygen content decreases towards the sea-bed. Normally in
sea-waters the oxygen content remains fairly high in the deeper layers, but off South-west Africa there
is a very rapid decrease with depth in the inshore waters, so that even in normal conditions in this
region a content of less than 1 ml. 02/l. is found in the vicinity of the sea-bed on the continental shelf.
The sections from survey II (Figs. 41-4) show that the layer of low oxygen slopes upwards towards
the surface as the coast is approached. Furthermore, it extends beyond the edge of the continental
shelf, producing a layer of minimal oxygen content adjacent to the continental slope, at depths of
about 400 m. on survey II.

On survey I this layer of minimal oxygen is much more pronounced, not only offshore, but also
inshore where it extends to the sea-surface at the coastal station WS 981 off Walvis Bay (Fig. 40).

NON-CONSERVATIVE PROPERTIES

193

STATIONS WS990

SEA MILES I

OFFSHORE 175

WS997

100-

300-

150

;

4-50
/

Fig. 38. Distribution of dissolved oxygen. Section off the mouth of Orange river, 12-14 March 1950,
survey I. Positions of stations are shown in Fig. 1.

STATIONS
SEA MILES
OFFSHORE 100
O

WS986

WS989
I

£ 200-

300-

400

Fig. 39. Distribution of dissolved oxygen. Section off Sylvia Hill, 10-11 March 1950, survey I.

Positions of stations are shown in Fig. 1.

Here, even with a recorded phytoplankton population of more than io7 cells (Table 14) the surface-
water was only 5-8% saturated with oxygen (cf. Steeman-Nielsen, 1957, p. 75).

A comparison of the oxygen sections with those of temperature and salinity shows that the low
oxygen content exhibits features of distribution similar to those of the upwelling water. Therefore

194

STATIONS WS97G

SEA MILES I

OFFSHORE I'S

O-

100-

200-

300-

400-

WS977
I

DISCOVERY REPORTS

WS978

Fig. 40. Distribution of dissolved oxygen. Section off Walvis Bay, 6-8 March 1950, survey I.

Positions of stations are shown in Fig. 1.

STATIONS
SEA MILES
OFFSHORE I7S
O-

WSIOSfa

WSI055

WSIOS3
I

100

300-

400 -L

WSIOSI

WSI050
I

Fig. 41. Distribution of dissolved oxygen. Section off the mouth of Orange river, 21-24 September 1950,

survey II. Positions of stations are shown in Fig. 2.

to trace its origins let us first examine the waters at subsurface depths adjacent to the continental
shelf, from which the upwelling occurs.

If we plot the dissolved oxygen content against temperature for survey I in the 200-600-m. layers
(Fig. 45), we see that the stations closer to the continental shelf and to the north of the region have
the lowest oxygen content, while those farther offshore and in the south have a higher oxygen content.

NON-CONSERVATIVE PROPERTIES

195

STATIONS WS 1070
SEA MILES I

OFFSHORE IOO

WSIOM

IOO-

E 200

300-

400

Fig. 42. Distribution of dissolved oxygen. Section off Sylvia Hill, 25-27 September 1950, survey II.

Positions of stations are shown in Fig. 2.

STATIONS

SEA MILES
OFFSHORE I"

WSI080
I

WSI078

VWI077 WSI075
! I

Fig. 43. Distribution of dissolved oxygen. Section off Walvis Bay, 29 September-3 October 1950, survey II.

Positions of stations are shown in Fig. 2.

It was suggested on p. 183 that the water against the edge of the continental shelf at these depths
exhibited a southerly movement, and therefore it is interesting to amplify our own results from some
stations of the 'Meteor' (Wattenberg, 1933) to the north and south of the region. These are plotted
in Fig. 46 and show a still wider contrast between the stations in the north and in the south. The
positions of the 'Meteor' stations are shown in Table 10. The two curves from the 'Meteor' stations

196

DISCOVERY REPORTS

STATIONS WS1I02
SEA MILES I

OFFSHORE l25
O '

WSIIOO

W5IO%

300

Fig. 44. Distribution of dissolved oxygen. Section off Mowe Point, 9-1 1 October 1950, survey II.

Positions of stations are shown in Fig. 2.

10"

NORTHERN

SOUTHERN

• WS976. O WS996

A VVS977 OWS98G A WS997
» WS978

"i 1 r

2 3 4

OXYGEN CC AlTRE

F'g- 45- Temperature and oxygen in the 200-600 m. layer at the 'William Scoresby' stations, survey I. Positions of the
stations are shown in Fig. 1. The two heavy lines are taken from Fig. 46, and show the temperature/oxygen relationships in
this layer to the north and south of the area surveyed, compiled from selected 'Meteor' stations.

are reproduced in Fig. 45 and show that the 'William ScoresbyV observations lie in between these
two curves, the stations in the north and closer to the continental shelf lying near to the curve for the
' Meteor's ' northern stations.

The decrease in oxygen content at the northerly ' Meteor ' stations between 8° and 120 C. represents
the layer of minimal oxygen content which extends across the tropical South Atlantic ocean (Fig. 47).
This layer Riley (1951) has shown to result probably from the balance between the rates of decomposi-

NON-CONSERVATIVE PROPERTIES '97

tion of detrital organic matter falling from the shallower layers, and the rate of renewal of oxygen by

turbulent processes.

If, therefore, the indication of southerly movement along the edge of the continental shelf at these
depths is real, such a movement would carry this oxygen-depleted layer into the region of theBenguela
current in this depth horizon. The water bounding such a current to the west as shown by the offshore
stations has a higher oxygen content which can be ascribed to water of the type shown by the ' Meteor '
southern stations.

20-

Z ID-

"^—

-i 1 r

2 3 4

DISSOLVED OXYGEN

XI88: 9 S 9 E

• 189: 9°S 6°E

OI45: 15° S 7°E

4 144: Ib'S 9°E

a 19 ■■ 37° S. l(>°E.

CC /LITRE

Fig. 46. Temperature and oxygen in the layer of minimum oxygen at selected stations of the 'Meteor' expedition, to the
north and south of the area surveyed by the 'William Scoresby'. The positions and dates of these stations are given in
Table 10.

With subsequent upwelling it might be expected that the water uplifted to the surface would be
heavily depleted in dissolved oxygen and this the more so the farther north in the region. The presence
of this water on the continental shelf would accentuate the effects of local decomposition of organic
matter on the sea-bed, and consequently the depletion of oxygen would become more accentuated
towards the coast on the continental shelf. This proceeds to such an extent that anaerobic conditions
are created on the sea-bed (p. 204).

Tabh 10. Positions of the Deutsche Atlantische Expedition 'Meteor' stations used in

the construction of Fig. 46

Date

11. vii. 1925

12. xi. 1925
4-5. v. 1926

6. v. 1926

5. ix. 1926

6. ix. 1926

Station no.

Position

36° 40' S., 16° 22-5' E.

34°02'S., I5°48'E.

144

160 03-5' S., 090 29' E.

145

i5°i6-5'S., o6°32-6'E

188

080 58' S., 080 577' E.

189

090 00' S., 060 00' E.

i(j8

DISCOVERY REPORTS

60u SO" 40" 30" 20" IO'

90" 80" 70" 60" SO" 40" 30" 20" IO

IO" 20"

Fig. 47. The distribution of the layer of minimum oxygen in the South Atlantic Ocean. From Wiss. Ergebn. dtsch. Atlant.
Exped. 'Meteor', Bd. ix, Beil. xxxvu. This figure shows the oxygen content at a depth of 300 m.

Normal and abnormal conditions within the current
A comparison of the dissolved oxygen sections for survey I and survey II (Figs. 38-40 and 41-4)
shows that the oxygen depletion on the continental shelf was much more pronounced during survey I,
and in particular in the Walvis Bay region where even at the sea-surface inshore (WS 981) the oxygen
content was only 0-33 c.c. 02/l. The consequences of such an immense depletion of dissolved oxygen
are discussed later (p. 199) in the consideration of its effects upon fish mortality, but for the present
we must consider what conditions lead up to such a catastrophic event.

The maintenance of aerobic conditions on the continental shelf must be dependent to a great extent
upon the renewal of oxygen by turbulent processes. In this case one would expect, as indeed is shown
by the results of survey II, that in the conditions which set up a strong northerly current the introduc-
tion of more highly oxygenated water would be at its maximum, and the oxygen on the continental
shelf would probably be continually renewed.

But if the currents were slowed down, stopped or even reversed, then the converse might be expected
to occur. The turbulent renewal of oxygen would be at its minimum, the effects of decomposition on

NON-CONSERVATIVE PROPERTIES 199

the anaerobic sea-bed would become magnified, and the production of hydrogen sulphide by the
sulphate-reducing bacteria in the bottom sediments (p. 204) would assist in the depletion of oxygen.

The conditions found at Walvis Bay on survey I exemplify this. The previously upwelled waters,
warmed and mixed with the influx of oceanic water, may be considered to have produced almost
stagnant conditions in this region, and some few days before our arrival in Walvis Bay a small mortality
of fish was observed by the local inhabitants.

The meteorological records (Fig. 35 and Table 3) show that, prior to our arrival in Walvis Bay,
there had been a predominance of calm and northerly winds for at least four or five weeks. It is
highly probable that adverse weather conditions such as these must be responsible for the occurrence
of such conditions of stagnation as are eventually associated with fish mortality.

These abnormal conditions always occur in the summer (Copenhagen, 1953) during which time
northerly winds predominate at Walvis Bay. This fact is not shown to advantage in Fig. 5, probably

«: imj

Fig. 48. Predominant wind vectors at Walvis Bay during the fish mortality of the summer of 1942/3. The wind vectors are
plotted in the same manner as in Fig. 35. From the records of the climatological station at Walvis Bay.

because these winds represent rather exceptional circumstances, and they do not necessarily occur in
every year. Other opportunities do occur, however, of comparing these abnormal conditions with
meteorological records.

In January of 1943 a considerable mortality of fish was reported by Dr McConnel at Walvis Bay
(Brongersma-Sanders, 1948). It extended from Walvis Bay to Concepcion Bay, a distance of some
60 miles along the coast.

At this time hourly meteorological observations were taken at Walvis Bay. The winds recorded
there are plotted (Fig. 48) in the same manner as in Fig. 35, any winds between south-west through
south to east-south-east being counted as positive and all other winds as negative. The negative winds,
mainly north to north-west, are those which would have been conducive to the abnormal conditions,
and Fig. 48 shows that they persisted throughout January 1943.

A mortality of much greater extent occurred in the summer of 1924-5 (Reuning, 1925) and the wind
records from Walvis Bay (Fig. 49) again show that after the end of December conditions would have
been favourable for the production of abnormal conditions.

One further example is a smaller mortality observed at Walvis Bay in December 1925, and through-
out this month the winds were either northerly or calms.

There appears, therefore, to be a well-defined correlation, at least between the occurrence of fish
mortalities and the spells of calm weather or northerly winds, which create abnormal conditions in the
vicinity of Walvis Bay.

200

DISCOVERY REPORTS

Fig. 49. Wind vectors at Walvis Bay preceding and during the fish mortality in the summer of 1924/5. The wind vectors
are plotted in the same manner as in Figs. 35 and 48. From the records of the climatological station at Walvis Bay.

STATIONS
SEA MILES

WS996

WS997
I

WS998 WS999

I I

WSI000

WSIOOI

WSI002
I

HORE I"

ISO 125 100

75 50 25 0

1 1 1

- ■ — — — — — ._ . s , ( — f . ■ — ■ — / , . _|

__•_ _ O 50

■---. — .. — — - '■. / — *- _ -- / _H

S - - - _ — _■

■ — - 100 / ■ -y^ ' -_■

/ s — "

IOO-

' / — 200 -^ /_^

y ,- - 2 so - _fl

/ '

__»_■_ _^D

y s s

£ 200-

' ^^A^ / _^

t—

_^- •* ._H

IOO ' /_■

150' / _i

— / _■

3O0-

/ _fl

( _i

400-

200 fl

Fig. 50. Distributions of phosphate (mg. ats. P/m.3). Section off the mouth of Orange river, 12-14 March 1950,

survey I. Positions of stations are shown in Fig. 1.

NON-CONSERVATIVE PROPERTIES

The distribution of dissolved inorganic phosphate-phosphorus
The sections showing the distribution of inorganic phosphate (Figs. 50-6) indicate that on both surveys
the pattern of distribution is essentially similar.

The lowest phosphate concentrations are found in the oceanic surface-waters, where from a com-

STATIONS WSI07O
SEA MILES '

OFFSHORE l0°
O-

WSIOW

IOO

Fig. 51. Distribution of phosphate (mg. ats. P/m.3). Section off Sylvia Hill, 10-11 March 1950, survey I.

Positions of stations are shown in Fig. 1.

STATIONS WS97(j

SEA MILES I

OFFSHORE 175
O

4O0

Fig. 52. Distribution of phosphate (mg. ats. P/m.3). Section off Walvis Bay, 6-8 March 1950, survey I.

Positions of stations are shown in Fig. 1.

plete absence of phosphate values of up to 0-5 mg. ats. P/m.3 were found. The upwelled coastal waters
present a sharp contrast. In them the phosphate content is very high, on occasion reaching more than
2-0 mg. ats. P/m.3.

Below the surface-waters the phosphate concentration increases down to the sea-bed inshore and

202

DISCOVERY REPORTS

to greater depths offshore. In places there is a layer of maximal phosphate off the edge of the conti-
nental shelf. This coincides approximately in depth with the layer of minimal oxygen, but like the
maximal phosphate layer in the equatorial parts of the ocean, it is much less well defined than the

STATIONS WSIO50

SEA MILES I

OFFSHORE 175
O-

IOO-

200-

WSI05S
I

WSI05I
I

WSIO50

400

Fig. 53. Distribution of phosphate (mg. ats. P/m.3). Section off the mouth of Orange river, 21-24 September 1950,

survey II. Positions of stations are shown in Fig. 2.

STATIONS WS98G

SEA MILES I

OFFSHORE 100

WS987

Q 200

Fig. 54. Distribution of phosphate (mg. ats. P/m.3). Section off Sylvia Hill, 25-27 September 1950, survey II.

Positions of stations are shown in Fig. 2.

oxygen minimum layer, and the phosphate concentration more often increases almost regularly to
greater depths. The maximum concentration is reached in the antarctic intermediate water.

In the layer of minimal oxygen, however, the inorganic phosphate concentration reaches values of
about 2-0 mg. ats. P/m.3 With upwelling, this extremely phosphate-rich water is brought up on to the
continental shelf, where it provides the necessary nutriment and permits the growth of the heavy
crops of phytoplankton in the coastal waters. In several of the sections it will be apparent that the

NON-CONSERVATIVE PROPERTIES

203

STATIONS WSIO8O

SEA MILES I

OFFSHORE

O-

I50

WSI08I WSI079

I I

125 100

WSI078
I

WSI077 WSI075
I I

'200

400

Fig- 55- Distribution of phosphate (mg. ats. P/m.3). Section off Walvis Bay, 29 September-3 October 1950, survey II.

;Positions of stations are shown in Fig. 2.

STATIONS WSII02

SEA MILES ,,_
OFFSHORE '"
0

WSM00

WS 1096

200-

300-

Fig. 56. Distribution of phosphate (mg. ats. P/m.3). Section off Mowe Point, 9-1 1 October 1950, survey II.

Positions of stations are shown in Fig. 2.

phosphate concentration on the continental shelf is higher than that in the water which is being
upwelled, and one must attribute this to further enrichment by local decomposition of organic matter
on the shelf.

On the Orange river line of survey II (Fig. 53) there is a divergence of phosphate-rich water
towards the surface at the edge of the continental shelf. This corresponds with the diverging current
which was postulated from the isosteres on this line of stations (Fig. 37).

204 DISCOVERY REPORTS

BOTTOM DEPOSITS

One of the most interesting features of the South-west African region is the presence, on the sea-floor
of the continental shelf, of an extensive area of diatomaceous mud. In contrast to the great deposits
of diatom ooze which occur in the deep ocean, this zone is confined to shallow waters, and by its
very proximity to the sea-surface has made its periodically catastrophic effects all the more evident.

The extent of the diatom mud was outlined by Marchand (1928). He described it as extending
principally from 21 ° 30' S. to 240 30' S. (a distance of about 200 miles) and running seawards for
some 25-30 miles from the coast. The bottom samples from this area in his words 'have a green
colour and are of a muddy or clayey consistency. The stench emanating from them is unbearable and
somewhat similar to hydrogen sulphide or the odour characteristic of putrefaction.'

Close to the coast, however, this mud was not found, and Marchand says that it gives place to a belt
of grey sand on which the marine fauna and flora were abundant. It appears, therefore, that the evil
smelling mud was confined to an area of the sea-bed between depths of about 50 and 1 50 m., extending
along the coast for some 200 miles.

The absence of marine life in this diatom mud, and the uselessness of the ground for trawling, led
to the name by which it is now known, the ' azoic zone ' (strictly speaking the name ' anaerobic zone '
would be more precise, for the mud does in fact support bacteria and is, therefore, not ' azoic ').

Copenhagen (1934) examined the deposits in the azoic zone closely and concluded that the evil smell
was in fact hydrogen sulphide, and that it originated from the activities of sulphate-reducing bacteria
(Butlin, 1949) which were shown to be present in the sediment. Analyses of the sediment revealed a
high content of organic matter and, on drying, a whitish-yellow deposit, evidently of sulphur, became
apparent on the surface of the mud.

Microscopical examination of the sediment has shown it to be composed mainly of diatom frustules,
although towards the seaward limit of the zone foraminiferal remains become increasingly abundant
(Marchand, 1928).

The importance of the azoic zone in the circulation of the waters of the Benguela current became
evident when the results of survey I were examined. It was decided, therefore, on survey II to include
a series of bottom sampling stations in an attempt to delineate more clearly the total extent of the
zone. Samples were taken to the south and to the north of the limits noted by Marchand (1928), and
these have shown that the azoic mud extends, at least patchily, for some 400 miles along the coast,
from Cunene river mouth (170 30' S.) in the north, to about 250 S. Seawards of the deposit is a fairly
rapid change to the stone-grey globigerina ooze which characterizes the sediments of the continental
slope and floor of the deep ocean to the west.

It is particularly interesting, however, that the azoic mud was not found on the Orange river line,
nor in the trawl at station WS 990 on survey I, and this suggests that the southern limit must indeed
be somewhere in the region of 25 ° S. The sediments on the shelf south of the azoic zone do not
differ markedly in appearance from the azoic mud, but they have none of the offensive smell of the
latter.

Reference to Figs. 38 and 41 shows that over this area the oxygen content of the water overlying the
sea-bed, exemplified by the Orange river line, was by no means so depleted as that found, for example,
off Walvis Bay over the azoic zone (cf. Figs. 40 and 43). This, in turn, relates to the higher content of
dissolved oxygen in the water which was being upwelled on the Orange river line (as shown by the
oxygen content at 200-300 m. off the edge of the continental shelf) as compared with that upwelling
further to the north.

The evidence, therefore, points strongly to the probability that this diatomaceous sediment to the

BOTTOM DEPOSITS 205

south of the azoic zone is maintained in an aerobic state by the circulation over it of upwelled water
which is not heavily depleted of oxygen.

Another factor, however, which must be considered is that the northerly winds and calms experienced
at Walvis Bay (p. 199) do not appear to prevail on the stretch of coast south of 250 S., and their absence
may ensure a free circulation of the current over the sediment ; but it is felt that these meteorological
conditions may concern more implicitly the intensity of the development of the anaerobic region
rather than determine the presence or absence of such a zone.

The presence of anaerobic conditions is essential for the growth of sulphate-reducing bacteria, and
if the sediment is kept oxygenated they cannot survive.

We have already seen (p. 198) how particular conditions within the current may magnify the effects
of hydrogen sulphide production, and indeed at times it is even evolved actively from the sea-surface.
There are many observations of bubbles of the gas rising to the sea-surface, but perhaps the following
newspaper account gives the most graphic description! (News Chronicle, 1938):

SEA GAS ATTACKS TOWN

Swakopmund, the small coastal town in strewn on beach, sharks come into surf gasp-
South-west Africa, is undergoing a gas attack ing on evening tide.

set up by continuous submarine disturbances. Cause. A geologist, discounting volcanic
Heavy sulphurous fumes, especially towards action, says sulphuretted hydrogen, pro-
evening, are penetrating as far as 40 miles duced by bacteria on the sea floor from cal-
inland. cium sulphate or gypsum, accumulates until

Effect. Atmosphere like a London fog, it raises islands of mud, which eventually

metalwork turned black, public clocks burst,
blotted out by deposit, thousands of fish

In 1 95 1 a particularly active disturbance took place, and on 16 February the Bulawayo Chronicle
(Anon., 1951a) reported:

SEA ERUPTIONS OFF SOUTH-WEST AFRICA

Swakop. S.W.A. Thurs. species, such as sea snakes and eels, which

The stench of sulphurous sea eruptions are found only occasionally when the sea

pervades the air day and night. Buildings bottom of their habit undergoes violent

which were white yesterday, are discoloured disturbance.

and black today. The sea appears to be boiling with bubbles

Dead fish are being washed up along the rising to the surface, but the temperature of

beaches for over 100 miles to the north from the water is only 6o°-70° F.

Swakopmund. They include many strange

These eruptions continued through March and three mud islands were thrust up in Walvis Bay
(Anon., 195 1 b). The largest, about 100 yards long, disappeared overnight.

The islands were similar to one which was thrust up in 1900. Waldron (1910) reported on the latter,
from which samples were taken by an officer of a regiment at Walvis Bay, who swam out to the island.
The samples were typical of the mud lying on the sea-bed in the bay, and the temperature of the
water remained low in spite of the fact that 'steam' was observed to issue from the northern side of
the island. The appearance of the island was accompanied by a very strong smell of hydrogen sulphide.
As yet no satisfactory explanation of the formation of these islands has been reached.

The importance of the sediment of the azoic zone in yet another way has been emphasized by
Brongersma-Sanders (1948) who has shown the significance of this anaerobic deposition of organic
matter to oil geology. It is noteworthy how closely the conditions of deposition within this upwelling
current parallel those found associated with fossil deposits.

Study of this diatomaceous mud— first distinguished by Neaverson (1934) from the nearly colour-
less diatomaceous ooze of some deep-sea deposits — may also yield interesting evidence on the silicate

206 DISCOVERY REPORTS

cycle in the sea, by comparison and contrast between the diatom populations found living in the area
(the biocoenosis) and the assemblage of forms found in the deposit (the thanatocoenosis). The problems
that this type of work may help to solve may even include evidence as to the speed of subsurface
currents, as may be seen from the brilliant exposition by Kolbe (1957) working on more specialized
samples from very deep waters (cores taken during the Albatross Expedition).

Preliminary examination of our samples from the Walvis Bay line already suggests striking differences
between the bottom deposits and the plankton. Of the forms remaining recognizable in the deposits
a vastly greater proportion belong to the Discoidae than have yet been recorded in any of the numerous
plankton samples from the area of which analyses are now available. That this may be due to much
more rapid re-solution of the less strongly silicified forms has been suggested previously on the basis
of work in other diatom-rich waters (Hart, 1934, 1942).

MICROPLANKTON

Terminology and presentation of data
The term ' microplankton ' is used here to describe the approximate size-limits of the organisms, plant
and animal, captured in routine vertical hauls of the N 50 V. These nets were constructed as near to
the specification of the J-m. nets previously used by the 'Discovery Investigations' as post-war
materials permitted. The finest bolting-silk obtainable was found to give an approximate mesh size of
40 x 50 fi in use. Some few large organisms are present in the catches, and have been tabulated with
the others in the summarized results of numerical estimations, but general sampling of the micro-
plankton, more especially of the phytoplankton, was the primary purpose of these hauls.

This definition of the term microplankton agrees with the usages of Sverdrup, Johnson and
Fleming (1946, p. 275), based largely on that of Ekmann (1935). They relate the general terms
expressive of size limits to methods of capture, thus :

Microplankton : captured by coarse or medium tow-nets.

Microplankton: captured by the finest grade silk nets.

Afawwoplankton : liable to escape the finest silk, hence also 'centrifuge plankton'. Also studied by
using fine filters, sedimentation methods, etc.

The nannoplankton (Lohmann) may be said to include or overlap various groupings of minute
forms proposed by more recent specialist workers, such as '//-flagellates', 'ultra-plankton' and
' hekisto-plankton ' (Cole, 1952).

Though the usage has varied we find that the outstanding plankton workers of the past agree upon
the necessity of treating these generally descriptive terms in an elastic manner (cp. Steuer, 191 1;
Johnstone, Scott and Chadwick, 1924). At first the prefixes macro- and micro- seem to have referred
broadly to large plankton organisms visible to the naked eye, and to the host of smaller forms that can
be seen with the aid of the microscope. But Johnstone, Scott and Chadwick referred all net-caught
plankton to the macroplankton, so that for them microplankton became synonymous with Lohmann's
nannoplankton.

Meunier (19 13) intended his use of the term microplankton to be construed in the earlier sense, but
with restricted application : to unicellular organisms only. This would very nearly meet our needs in
discussing the Benguela current material, were it not that the multicellular alga Trichodesmiiim is of
some importance among the phytoplankton in that region. Moreover, the relative abundance of the
smaller metazoa is obviously an important factor if the ' conditions of life ' of the phytoplankton are
to be considered.

More recently Ekmann (1953, p. 312), while adhering to his own early definitions (as given by

MICROPLANKTON 207

Sverdrup et al.) has added approximate size-limits — 60-1100/^ — for the microplankton. Now since
Ekmann is dealing with zooplankton this may suit his purpose well enough ; but many phytoplankton
organisms, especially colonial diatoms, are well sampled by nets, although the individual cells are well
below 60 n in greatest dimensions. The colonial habit permits their retention by the silk, while their
highly developed powers of flotation lead to differential settling-rates or actual failure to settle,
defeating the centrifuge or reversing-microscope methods of estimating relative abundance, that
would otherwise be far more satisfactory than the old net method. The postulation of actual size-
limits also brings us up against the fact that in Nature individual species can always be found whose
normal range of size-variation bestrides any proposed limit. Many individual species of diatoms and
of dinoflagellates normally vary in size from about 35 /i to over 100//, and a single important example
of a species completely overlapping the proposed upper limit is provided by the well-known Noctiluca
tniliaris. Most samples of this cosmopolitan organism that we have examined, from many parts of
the world, have had the majority of individuals ranging between 300 and 600// in greatest dimensions,
but some frequently attain to 1200 or 1500// and have been known to reach 2000// (Lebour, 1925,
p. 69). Clearly we must admit with Gran (in Murray and Hjort, 1912) and with Johnstone, Scott and
Chadwick (1924, p. 75) that ' ... it is impossible to establish clear and absolutely logical distinctions . . . '
in the application of these broadly classificatory terms.

This becomes even more obvious when other technical terms, broadly descriptive of aetiological
attributes of various categories of plankton organisms, such as those introduced by Haeckel and the
Kiel school of planktologists, and by other workers in this field from many countries, come under
review (cf. Hart, 1942, p. 268). They are but a part of the jargon without which generalizations cannot
be succinctly expressed, and attempts to define them with undue regard to a rigid specialized connota-
tion lead to frustration, because Nature herself seems able to find ' exceptions to every rule '. This
obtrusive antithesis should not mean that naturalists must foreswear the ecological point of view.
Major types of woodlands, whether defined by foresters or (in somewhat different terms) by terrestrial
plant ecologists, are none the less real entities because some kinds of trees are to be found in more than
one of them.

This problem of terminology may be partially solved by the growing practice of holding international
conferences of recognized leading workers in a given subject, to seek agreement on definitions accept-
able to the majority. The alternative is for the individual worker to redefine his own usage when
necessary.

The first solution is hampered by language difficulties and the rank growth of 'the literature',
such that the richest of languages proves insufficient to provide suitable terms that can be used in
specialized connotation, without trespass upon the jargon of some other ' branch of knowledge '. The
second, to some extent inescapable, can easily lead one into tedious and unprofitable etymological
discussion !

Here we attempt a working compromise by following the usage of Sverdrup, Johnson and Fleming
(1946) for most ecological terms. This usage is mainly derived from that of the earlier works
mentioned above. When less widely known terms have been employed we have tried to make their
meaning plain from the context where they first appear. The meaning of some phrases coined merely
for description of the present data will, we hope, prove sufficiently clear if the words are read in their
generally accepted, non-specialized sense.

Terms relating more particularly to the phytoplankton are used in the sense that Gran and Braarud
(1935) have ascribed to them, as nearly as the differing conditions in this part of the southern hemi-
sphere permit. They have been evolved from the earlier system of ' plankton elements ' devised by
Gran (1902, 1932) for ecological characterization of the species, during the period when plankton

208 DISCOVERY REPORTS

workers were gradually building up concepts capable of wider application than the older ' plankton
types ' of Cleve.1

Gran's system itself involves the use of some of Haeckel's terminology. ' Holoplanktonic ', ' mero-
planktonic' and 'tychopelagic', defining the degree to which organisms are dependent on the sea
bottom at some period of their history, are widely accepted. ' Oceanic ' and ' neritic ', however, can
soon lead to anachronisms in dealing with the phytoplankton, if applied in a rigidly restricted sense
(cf. Hart, 1942, p. 283). Many undoubtedly holoplanktonic 'oceanic' diatoms, to be found in the
open sea at all seasons, may attain considerable abundance in coastal ('neritic') sea-areas. Con-
versely many ' meroplanktonic ' (and therefore truly ' neritic ') species seem able to go on reproducing
vegetatively for so long that they may often form a considerable proportion of the phytoplankton in
some ' oceanic ' areas far beyond the edge of the shelf.

To avoid the confusion that could arise through the necessity of listing some species as both oceanic
and neritic, we suggest the use of the word ' panthalassic ' to describe these ubiquitous forms. The
word was used by Johnstone, Scott and Chadwick (1924) and is given in Henderson' 's Dictionary of
Scientific Terms (1953) as: 'living both in coastal and offshore waters; neritic and oceanic', but we
have not yet discovered who first used it in this sense.

To distinguish species of very wide distribution, whether neritic, oceanic or panthalassic, we have
here used the adjective ' cosmopolitan ' in its general sense, when their known distribution shows a
higher degree of tolerance towards temperature and salinity differences than is necessarily shown by all
the panthalassic species. There are many regions where occupation of both inshore and offshore
waters does not involve very wide tolerance of these two best-known parameters of the surface-waters.

Use of the expressions 'dominant' or 'predominant', practically unavoidable in discussing dif-
ferences between phytoplankton populations, provides another example of the difficulties involved
when words so useful in their generally accepted sense acquire an arbitrary, specialized connotation,
through the attempt to define them objectively. Numerical preponderance at some arbitrarily chosen
level can be misleading (from the point of view of potential productivity) of orgmisms varying so
widely in size and shape, and invites the further criticism that all known counting methods involve
errors. Yet, if we are to attempt anything less subjective than the addition of such descriptions as
' abundant ', ' common ', or ' rare ' to the organisms identified, some form of counting — and acceptence
of arbitrary levels in drawing deductions from the counts — is unavoidable. Conversely, it should not
be forgotten that admittedly subjective observations by the earlier naturalists lead to the first recogni-
tion of any recurring pattern of plankton distribution.

The whole subject is one to raise echoes of the resounding controversies, as to methods of quanti-
tative plankton investigations, that followed publication of Haeckel's famous Plankton Studien, and
the replies of Hensen and others, of which the best brief account that we have come across is given by
Johnstone (1908).

Throughout the subsequent development of plankton study the early methods have been periodically
subjected to destructive criticism, too often by those who have never learnt to count plankton, and
constructive reviews like that of Gran (1932) have been few. Considerations which should help to
place the matter more fairly in perspective are:

First, the truism that the ideal comprehensive quantitative method may indeed be approached, but

1 Cleve's ' Plankton Types ' constitute the first clear epitome of the close relation between plankton population and con-
ditions of the milieu, that may be evident whenever neighbouring water masses are exceptionally well defined. When further
work made it clear that water-movements and seasonal changes frequently produced more complicated inter-relationships,
it was against the background of Cleve's concept that the new evidence was marshalled. Cleve's 'types' are still distinguish-
able in essence wherever abrupt differences in environment recur with the consistency usual around southern Scandinavia,
but few sea-areas provide such clear-cut examples.

MICROPLANKTON 209

never achieved. Hensen himself had discovered that methods had to be varied to suit the study of
different organisms.

Secondly, the necessity for wide, rapid coverage in collection, especially in the less known areas.
This often renders crude estimates of relative frequency of greater immediate value than limited series
of more accurate data, and was the main reason for our choice of an 'antiquated' method here.
The principle is epitomized in Gran's phrase 'a single "absolute" estimation of phytoplankton
would be about as valuable as a single temperature determination carried to the third decimal
place '.

We have used Hensen's methods for subsampling and counting from routine vertical hauls of the
fine silk -J— m. net (N 50 V), but do not follow the early workers in regarding the hauls as repre-
senting a constant fraction of the entire contents of the theoretical volume of water filtered. The
estimations from counts we regard as roughly comparable indications of relative abundance, within
the limits of the very large differences involved in plotting (say) the estimated totals on a logarithmic
scale. They are, however, much more accurate as regards the relative importance of species within
single samples; and more accurate for small samples than for large ones that have to be diluted to
render subsamples small enough to count.

We have found it easier to appreciate the relative frequencies involved by tabulating the actual
estimated numbers in primary tables, but in any form of graphic representation it becomes necessary
to use logarithmic or other functional ordinates. For the logarithmic reductions we have the classic
precedent of Professor Hentschel's work on the 'Meteor' centrifuge-plankton (Hentschel (1936)), and
the wide applications of logarithmic scales in dealing with many types of biological data have more
recently been well reviewed by Williams (1947). Other scale reductions are indicated on individual
diagrams, and it is hoped that sufficient tabular data are included to forestall queries arising from the
distortions unavoidable in graphic presentations of this kind.

Recognizing the limitations of these numerical estimates, derived from roughly comparable hauls,
the necessity to adopt some arbitrary definition of dominance must still be faced; though we have
ventured to retain such useful expressions as 'frequent' and 'important' in their loose, generally
accepted sense. Now, the surveys were planned to include observations within two distinct types of
surface-water and the boundary region between them. Hence our criterion of dominance must be
applicable to individual samples. We cannot, for instance, employ some method like that of Sargent
and Walker (1948), who determined most satisfactory levels of significance (on a percentage basis) by
pooling results from a whole series of observations. Their method, one of the best we have yet seen,
demands, first, that the observations be restricted to a single water mass (though ' succession ' with
increase in 'age' of the surface-water may be apparent), and, secondly, adequate seasonal coverage;
so that ' succession ' should not be confused with ' sequence ' (i.e. changes in population due to invasion
of the area by a different water mass).

Our definition derives direct from the raw data — the estimates of numbers of each category
recognized (some 12-50 categories) at each of the eighty-odd stations, arrayed in numerical order from
the original counts. We regard the first seven on each list as 'dominant'. By this means the local
importance of the more exclusively offshore species is not obliterated by the vast preponderance of
the inshore forms, as it would be if the results from the whole of this survey area were pooled. Further,
the local importance of some panthalassic species, present in the proportion of (say) 20,000/100,000 at
some impoverished offshore station, is not obscured by its presence in greater quantity — perhaps
200,000 — at a rich inshore station where the estimated total might be some 200 million, and the first
eight or ten categories all exceed two million.

Considering only the thirty-nine stations from each survey that were repeated at approximately the

zio DISCOVERY REPORTS

same positions,1 this arbitrary choice of a level of 'dominance' was found to show the following
results :

(a) The lowest (7th) 'dominant' ranged between 07 and 7-1% of the estimated total, mean 3-5%
with aM 1-3. At only two of the seventy-eight stations was its value below 1%, and although the
5 % level was exceeded at 8/78 stations, the eighth number of the list (highest category excluded on this
scheme) exceeded 5 % of the total once only.

(b) The sum of the 'dominants', i.e. ^th of the numbers on each list, ranged between 59-8 and
99-6% of the estimated totals, mean 81 -6% with aM 10. The level fell below 60% at one station only,
below 65 % at 5/78 stations, and it exceeded 95 % at 6/78 stations.

For the four samples of visibly discoloured surface-water, three examined by the drop method and
one with the aid of the centrifuge, the 5% level was chosen as the lower limit of 'dominance'.

In the primary tables for the first (autumn) survey the stations numbers are given in chronological
order as they were worked, from north to south. During the second survey interpolation of extra
stations (mostly for bottom-sampling) and the fact that it was worked from south to north destroys
the sequence of the serial numbers. The data have, therefore, been listed so that microplankton data
from repeat positions are given in the order in which the corresponding stations had been occupied
during the first survey. Although this results in the last becoming first, it should not be confusing
because, if the serial numbers are disregarded, it also has the result that observations made in equi-
valent positions are treated in the same sequence in the Tables for each survey (cf. Figs. 1 and 2,
and Tables 14 and 15).

Stations where full series of hydrological and plankton observations were made have been dis-
tinguished by printing their serial numbers in ordinary type, while those where only the micro-
plankton net and bathythermograph were used are given in italics.

As an aid to verbal description, the four main lines of observations worked east and west have been
named from the most prominent topographical features near their coastal terminations, in order from
north to south : the Mowe Point line, Walvis Bay line, Sylvia Hill line and Orange river line. The three
lines of subsidiary observations connecting them have been termed the northern, mid- and southern
intermediate lines. Approximate mean latitudes for stations worked on each of the four main lines are :
Mowe Point line, 190 40' S.; Walvis Bay line, 220 40' S.; Sylvia Hill line, 250 20' S.; and the Orange
river line 280 40' S.

The order in which groups of organisms, and lesser taxonomic units within the groups, have been
arrayed in tables and diagrams, has been governed by the main object of this part of our work:
description of the rich microplankton flora as a whole. Strict adherence to the sequence of some
recognized scheme of classification would render them very cumbersome and even perhaps misleading,
owing to the impracticability of publishing the raw data in full, or of identifying members of all
groups down to the same taxonomic level. These difficulties, added to the admittedly unequal sampling
of certain groups by the net method, have prompted the following explanation of the relation between
our arbitrary arrays and systematic classification, since we have no wish to do violence to system-
atists' views, whenever they seem well established.

First we give the sequence of main groupings represented in the Benguela current samples, all of
which, excepting the silicoflagellata,2 are usually regarded as classes of algae, according to the classifica-
tion of Fritsch (1935, 1945) — perhaps the most widely accepted at the present time.

1 That is omitting the extra stations worked south and north of the main survey area during the second survey.

2 Fritsch treats the silicoflagellata, whose affinities are still in doubt, as a minor group of uncertain status, at the end of his
discussion of the chrysophyceae. We are indebted to Dr M. W. Parke of the M.B.A. Laboratory, Plymouth, for advice on
this point.

MICROPLANKTON 211

The five classes out of the eleven considered by Professor Fritsch that were not represented in our
material have been omitted. They include the large thallose, attached marine forms, and others with
few, if any marine representatives. The sequence of his scheme is indicated by the roman numerals.
To each group a summary of the disposition of individual categories (whether species, genera or
larger units) that we recorded, has been added :

I Chlorophyceae. With two species of Trochischia, rarely and in small numbers only.

II Xanthophyceae. Halosphaera only, extremely local.

III Chrysophyceae. With the Coccosphaeriales lumped here because they cannot be adequately
sampled by nets (numerically they are a most important group in warmer seas, as nannoplankton
methods have shown). Phaeocystis, here mercifully less abundant than in colder seas.

Silicoflagellata. With two species, never very abundant but widely distributed.

IV Bacillariophyceae. With ninety-five species or generic categories.

VI Dinophyceae. With forty-two categories, although only the Ceratia and a few most obviously
important of the other thecate forms were identified down to species.

XI Cyanophyceae. Only one important species here: Trichodesmium thiebautii.

From the 'Meteor' results (Hentschel, 1936) we know that the Coccosphaeriales, smaller Dino-
phyceae and even some of the Chlorophyceae, would figure much more prominently in relation to
members of the other groups, if we were considering 'ideal' samples in which nanno- and micro-
plankton forms were represented with equal fairness. On the other hand, Halosphaera and the silico-
flagellates belong to groups wherein few marine species are known, whatever method of collection is
adopted. These limitations, especially those implicit in the choice of the net method, our reasons for
which have already been mentioned, led to the decision to treat the phytoplankton under three main
headings: Diatoms (Bacillariophyceae), Dinophyceae and 'other Protophyta' or 'other plants'; that
is, in descending order of their abundance in these samples, in our main list and primary tables and
diagrams.

Within these groups the order of genera adheres to recent systematic practice, though the more
detailed description of the diatom flora has involved some arbitrary arrays to be described later.

In the main list the genera of diatoms follow the classification proposed by Hendey (1937), but the
species within each genus are arranged alphabetically, because the subgeneric arrangements proposed
for some large and important genera are still highly debatable. The Dinophyceae follow the sequence
used by Schiller (1933), and the heterogeneous assemblage of 'other plants' the order in which their
main groups occur in Fritsch's general classification of the algae.

Chief among the many works consulted for identifications were the Nordisches Plankton series and,
for the diatoms, Lebour (1930), Hustedt (1927-37), Hendey (1937) and Boden (1950). For the Dino-
phyceae, Lebour (1925) and Schiller (1933) were of the greatest assistance.

The Protozoa and Metazoa have been treated less thoroughly than the phytoplankton in these
samples because the larger ones were better sampled by coarser nets. The genera of Tintinnoinea were
determined with the aid of Kofoid and Campbell's Monograph (1929), but to have done the same for
the Radiolaria (equally important at a few stations) was beyond my capacity (T.J.H). Similarly,
among the Metazoa, while some individual species of local importance were recorded separately, the
Nauplii and other larval categories are quite unequal in systematic status. These diverse groups of
animals are listed as nearly to the generally accepted taxonomic order as their nature permits.

The diatoms being by far the most abundant organisms in these samples, are discussed in greater
detail than the other main groups, and hence we endeavour to make plain the inter-relations between
systematic classification, and arbitrary arrays used merely as an aid to presentation of data, at the
outset.

2i2 DISCOVERY REPORTS

Hendey's classification of the class Bacillariophyceae (diatoms) aims at providing a system wherein
the great structural differences between the most abundant plankton forms are more clearly empha-
sized than they were in earlier systems; among which that of Schiitt (1896) with minor modifications
by subsequent workers, is still the most widely accepted arrangement.

Schiitt's scheme divided the whole group into two suborders Centricae and Pennatae, based upon
cell-symmetry around a supposedly central point in the one group, and a more or less iso-bilateral
symmetry in the other. Most marine plankton forms belong to the Centricae; and the majority of
the attached marine forms, freshwater and soil diatoms to the Pennatae. To this extent the scheme
shows a reflection of the earlier ideal, ultimately found impracticable, of classifying diatoms principally
upon the mode of life, as Smith (1853-6) had tried to do. The main morphological basis of Schiitt's
scheme soon shows up the incompatibility : although most of his Pennatae are not to be found as normal
constituents of the marine phytoplankton, some lesser subdivisions of the group are well represented
therein; so that the agreement between systematic classification based on morphology and primary
habitat differences, although better than it is in many other classes of organisms, is by no means
complete.

Hendey (1937, 1951) has pointed out that the major subdivisions of the Centricae (variously ranked
as sections, families or tribes in later modifications of Schiitt's scheme) show structural differences so
marked that their inclusion within a single suborder seems questionable. Some of them (Biddul-
phineae, Soleniineae) even show a type of symmetry that it is very difficult to relate to a supposedly
central point. Moreover, even the Pennatae include groups of very diverse structure, although they
do not show such extreme divergence from the main characters of the suborder as do some of the
Centricae.

Hendey, therefore, proposed that the class Bacillariophyceae, regarded as including only the one
order Bacillariales, should be divided into ten suborders of equal systematic status. The first five of
these include the forms assigned to various minor rankings in the more recent modifications of Schiitt's
Centricae (e.g. Hustedt, 1927-37) while the last five were included in Schiitt's Pennatae. Hendey
(1937) has himself pointed out that with regard to rankings below the level of suborders, his arrange-
ment is not materially different from the earlier ones, and he has been at pains to make due acknow-
ledgement to Schiitt and other workers in this field. The formal terminations of the family and sub-
family names that he has adopted merely serve to render his classification of the Bacillariophyceae
consistent with generally accepted usage among other classes of algae.

Table 1 1 shows Hendey's classification, excluding the genera not represented in the material that
he was working on when he first formulated it. That material consisted of a large selection of plankton
samples from most of the areas traversed by ships of the Discovery Investigations in the Southern
Hemisphere, prior to 1935.

In Table 1 1 the genera and corresponding supra-generic rankings observed in our Benguela current
material have been printed in ordinary type, leaving the groups that have as yet been recorded only
from other parts of southern seas distinguished by italics.

Supra-generic rankings, either at the level of suborder or family, were found to lend themselves to
the definition of four of the five arbitrary groupings used later in this report, for descriptive purposes
only. They are preceded by numbers in brackets, and printed in bold type in Table 1 1 .

The fifth group is a lumping of such members of the last five of Hendey's suborders as occurred in
the Benguela current samples. In this report they have been termed ' Pennatae ' for the sake of brevity
not from any desire to revert to the older classification.

Whether one thinks of them as the Pennatae of Schiitt, or the last five suborders of Hendey's
system, those familiar with marine phytoplankton will know that nearly all the planktonic members

Table II. Classification of plankton diatoms proposed by Hendey
(i937) with the genera and higher groups seen in the Benguela
current material in ordinary type, others in italics. Note: this is not
a complete classification, many non-marine or non-planktonic genera
having been omitted. Inclusion of all diatom genera would slightly
alter the sequence of some of the units of less than sub-ordinal rank.

Sub- Sub-

orders Families families Genera

DISCINEAE

Coscinodiscaceae

Melosiroideae

Melosira
Hyalodiscus

Skeletonemoideae

Skeletonema

Stephanopyxis

Detonula

Thalassiosiroideae

Thalassiosira

Coscinosira

Lauderia

Schroderella

Bacterosira

Coscinodiscoideae

Coscinodiscus
Charcotia
Planktoniella
Gossleriella
Schimperiella
Actinocyclus
Hemidiscaceae

Hemidiscoideae

Hemidiscus
Actinodiscaceae

Stictodiscoideae

Stictodiscus
Arachnoidiscus

Actinoptychoideae

Actinoptychus

Asterolamproideae

Asterolampra
Asteromphalus
AULACODISCINEAE
Eupodiscaceae

Pyrgodiscoideae

Pyrgodiscus

Aulacodiscoideae

Aulacodiscus

Eupodiscoideae

Eupodiscus
AULISCINEAE

Auliscaceae

Auliscoideae

Auliscus
BIDDULPHIINEAE

Biddulphiaceae

Biddulphioideae

Biddulphia
Bellerochea
Cerataulus
Cerataulina

Triceratioideae

Triceratium

Trigonium

Pseudotriceratium

Lithodesmium

Ditylum

Hemiauloideae

Hemiaulus

Eucamphioideae

Eucampia
Streptotheca
Climacodium
Anaulaceae

Anauloideae

Anaulus
Chaetoceraceae

Chaetoceroideae

Chaetoceros

The first four of the five arbitrary groupings used for descriptive
summaries in this report coincide with suborders or families in the
system, and are shoivn beloio in heavy type. The fifth group, a
heterogeneous lumping from the last five suborders, has been termed
' pennatae' for the sake of brevity, but is not intended to imply
reversion to earlier classification (see text)

Sub- Sub-

orders Families families Genera

SOLENIINEAE

Bacteriastraceae

Bacteriastroideae

Bacteriastrum
Rhizosoleniaceae

Rhizosolenioideae

Rhizosolenia
Guinardia
Leptocylindraceae

Leptocylindroideae

Dactyliosolen
Leptocylindrus
Corethronaceae

Corethronoideae

Corethron
Araphidineae

Fragilariaceae

Fragilarioideae

Fragilaria
Fragilariopsis
Asterionella
Synedra
Thalassionema
Thalassiothrix
Meridionoidcae

Meridian
Tabellarioideae

Licmophora
Grammatophora
Striatella
Rhabdonema
Entopyla
RAPHIDIOIDINEAE
Eunotiaceae

Eunotia
MONORAPHIDINEAE

Achnanthaceae

Achnanthoideae

Achnanthes
Cocconeioideae

Cocconeis

BlRAPHIDINEAE

Naviculaceae

Naviculoideae

Navicula
Trachyneis
Scoresbya
Pleurosigma
Amphiproroideae

Amphiprora
Tropidoneis
Gomphonemaceae

Gomphonemoideae

Gomphonema
Cymbellaceae

Cymbelloideae

Cymbella
Amphora
Epithemiaceae

Epithemioideae

Epithemia
Bacillariaceae

Nitzschioideae

Nitzschia
Chumella
Bacillarioideae

Bacillaria
SURIRELLINEAE

Surirellaceae

Surirelloideae

Surirella
Campylodiscoideae

Campylodiscus

214 DISCOVERY REPORTS

of this group belong to the two families Fragilariaceae and Naviculaceae, with a few species of the
genus Nitzschia. These forms, which fall into the suborders Araphidineae and Biraphidineae of
Hendey's system, exhibit features that fit them for a free-floating existence (if the teleological expres-
sion may be forgiven). Such features are the development of catenary, branching or ribbon-forming
colonies ; attenuated form of the individual cells ; or the possession of cell-walls much slighter than
those of their bottom-dwelling relatives. Indeed, in an aetiological sense, they have collectively been
well described as 'reversionary plankton forms', by Lloyd (1926). However, in this material, as in
that from other coastal areas, we find that a small proportion of bottom-dwelling forms (e.g. Achnanthes
which falls within Hendey's Monoraphidineae) occur tychopelagically in the plankton. In need of a
summary group-heading that would include these also, it was felt that the old term ' Pennatae ', though
of doubtful value in its taxonomic sense, would be more convenient than some cumbersome phrase
such as 'last five suborders'. The expression 'small pennate diatoms' that Marshall (1933) found
convenient for ecological description of material from the Great Barrier Reef, is only a partial equiva-
lent, since large species like Thalassiothrix longissima and Pleurosigma capense are included in the
Benguela grouping.

For the rest, Hendey's suborder Discineae suited our purpose well as it stands, but coming to the
suborder Biddulphineae it seemed best to divide the outstandingly abundant Chaetocerids from the
others at family level, for the latter derive from several subfamilies, whereas the Chaetoceraceae
include but the one subfamily, and indeed, in this material, only the one genus. The Soleniineae,
consisting almost exclusively of holoplanktonic forms, provided a convenient grouping at the level of
the suborder.

Thus four of our five arbitrary groupings can be defined in terms of widely accepted system-
atic assemblages, though these are not of equal status. The fifth group remains heterogeneous.
Abstracting them from the classification table, and summarizing their main ecological characteristics,
we have:

I Suborder Discineae. Most of the species neritic and probably meroplanktonic, with heavily
silicified frustules. Exceptions (holoplanktonic, relatively more abundant in the sparser phyto-
plankton at greater distances from land) were some of the Thalassiosira spp. and the definitely oceanic
Planktoniella. The colonial habit and gelatinous or spiny projections of the former, and thin, hyaline,
ribbed extensions of the valve margins of the latter, may conceivably assist flotation.

II Family Biddulphiaceae. Mainly neritic, few solitary, but the others showing very varied
development of the colonial habit. A few are oceanic, holoplanktonic (very rare in these samples,
e.g. Hemiaulus Hauckii). Majority meroplanktonic (Eucampia, Biddalphia) or even bottom-dwelling
species (Triceratium) whose occasional presence alive in the plankton may justify their inclusion as
tychopelagic species.

III Family Chaetoceraceae. Mainly holoplanktonic in the vegetative phases, but a majority form
specialized resting spores and are, therefore, probably meroplanktonic. Many neritic, few oceanic
species. In comparison with II, with which they form the suborder Biddulphiineae, the Chaeto-
ceraceae show an increased development of structural features that must tend to aid flotation : thin, less
strongly silicified frustules, and horns produced into long setae. Mainly colonial.

IV Suborder Soleniineae. Nearly all holoplanktonic, many oceanic or panthalassic, few neritic.
Structurally they include large and medium-sized tubular species, solitary or in colonies of few cells
and long chains of small cylindrical species.

V ' Pennatae '. A heterogeneous arbitrary grouping, as explained in detail above. It consists
of the few normally planktonic members of Hendey's Araphidineae and Biraphidineae (the ' reversionary
plankton forms ' of Lloyd) with such few bottom-dwelling forms from the last five of Hendey's sub-

MICROPLANKTON 215

orders (Pennatae proper, if one prefers Schutt's system) as were found to occur tychopelagically in
these samples. Mainly meroplanktonic, neritic.

Taxonomic notes
Changes in nomenclature of phytoplankton species have been adopted where recent taxonomic
research seems to justify them. Most of these are better known to plankton workers under earlier
names current in general handbooks such as Engler and Prantl's Pflanzenfamilien, the Nordisches
Plankton series and M. V. Lebour's Planktonic Diatoms of Northern Seas. It is hoped that these notes
may prevent further confusion. They give first the name used in this report in bold type, the best
known previous synonym, and then the authority for the change. Full synonymy is not attempted
here. Some brief comment has been offered concerning changes that still seem to the writer to be
of doubtful value, but detailed taxonomic study would require a separate report. (Where the first
person has been used in this section the opinions expressed are those held by one of us (T. J. H.)
personally.)

Hemidiscus cuneiformis Wallich (i860), formerly Euodia cuneiformis (Wallich) or E. cuneiformis
Schiitt.

Hustedt (1927-37, p. 903) and Hendey (1937, p. 264) have explained how the foundation of several
species that they believe to be but varieties or phases of the type, coupled with Castracane's error in
supposing that Euodia Bailey, 1861, predated Wallich's foundation of the genus Hemidiscus, has led to
prolonged uncertainty as to the correct naming of this species. It is interesting to note that in all the
welter of confusion Cleve (1901, p. 330) had worked back to the combination now considered correct,
although he later supported Gran's use of Euodia cuneiformis (Wallich) as synonymous with E. gibba
Bailey (Gran, 1905, p. 45).

Actinoptychus senarius Ehrenberg, previously widely known as A. undulatus (Bailey). Hendey
(1937, pp. 271-2) shows that Ehrenberg's specific name should be adopted upon grounds of priority.
Confusion arose because Ehrenberg first described it as a species of Actinocyclus (Ehrenberg, 1838).
Later he himself recognized the structural differences that seemed to warrant the splitting of this
genus into Actinocyclus as most subsequent workers have known it, and Actinoptychus which he
established as a distinct genus, with A. senarius as the type-species (Ehrenberg, 1841, 1843). The
figures of this form given as an unnamed species of Actinocyclus by Bailey (1842) first received the
specific epithet undulatus from Kutzing (1844), and the combination Actinoptychus undulatus (Bailey)
was made by Ralfs in the fourth edition of Pritchard's History of the Infusoria, 1861 ! Ehrenberg him-
self seems to have had no doubt that the unnamed figure of Actinocyclus sp. given by Bailey, and later
called Actinocyclus undulatus by Kutzing, was specifically indentical with his own ' Actinocyclus ' (later
Actinoptychus) senarius (Ehrenberg, 1843, p. 328).

Cerataulina pelagica (Cleve) Hendey comb, nov., more widely known as C. BergoniiH. Peragallo
or Cerataulus (Cerataulina) Bergonii (H. Peragallo).

Hendey (1937, p. 279) states that though Peragallo first suggested the need for a new genus
(Cerataulina) when he described the species Cerataulus (Cerataulina) Bergonii H. Peragallo (1892),
he did not define that genus. Later it appears that Cleve (1894, p. 1 1) accepted Peragallo's tentatively
proposed name, while pointing out that the form which he had himself described earlier as Zygoceros
pelagicum (Cleve, 1889, p. 54) was a complete synonym. Yet the genus Cerataulina does not seem to
have been properly established anywhere until Schutt's publication of 1896 (in Engler and Prantl,
p. 95). Hendey's proposed combination seems the only means of bringing the species within the
bounds of accepted rules of nomenclature, though plankton workers have been familiar with
' C. Bergonii ' for so long that they cannot but regret the change.

216 DISCOVERY REPORTS

Chaetoceros atlanticum var. (or phase) neapolitana (Schroder) Hustedt, previously often re-
garded as a distinct species, C. neapolitana Schroder. Here lumped with the type.

Gran and Yendo (191 4) noted that this form, which they regarded as a distinct species, was most
often to be found in the warmer waters around Japan, while the highly variable and cosmopolitan
C. atlanticum Cleve was mainly confined to the colder water masses in that region. Earlier work round
Japan suggests that the neapolitana form might be found in the colder waters also. Though Okamura
(1907) identified his specimens as C. atlanticum, Gran and Yendo seem satisfied that they were the
neapolitana form, and doubted the localities whence they were recorded in consequence !

Hustedt (1927-37), Hendey (1937) and Boden (1950), the latter working on South African material,
have regarded neapolitana as a variety of C. atlanticum. It was Hustedt who regularized this change,
and both he and Hendey also dealt with the very confused synonymy of the type.

Our material seems clearly to support the view that neapolitana can hardly be a separate species.
Both the type (C atlanticum) and the variety occurred together at some stations near the shelf-edge,
with seemingly intermediate forms, and neapolitana more frequently than type or intermediates in the
warmer oceanic water still farther offshore.

The regular banded appearance of the setae, due to chloroplasts penetrating into them and disposed
at regular intervals, was very characteristic of the neapolitana phase, and is shown in figures of material
from other localities by Schroder himself (1900) and Cupp (1943) among others. However, our
material also showed individual colonies of both type and intermediates with a similar disposition of
chloroplasts. We have to remember that the movements of chloroplasts within the shell are probably
governed by light intensity. Hence this appearance in preserved samples may depend more upon the
depth at which they were captured and time interval prior to fixation than upon any greater tendency
towards this pattern in the neapolitanum phase, rather than in type or ' intermediate ' strains.

Certainly we would agree with Gran and Yendo that neapolitana is a warm-water phase of the
species, and this is also the view of Cupp (1943) and Takano (1954) who gives excellent figures of
what he terms var. neapolitana and var. skeleton.

It seems significant to me that when material from the north-eastern Atlantic only has been studied,
there are many examples of diatoms that show a polymorphism, seemingly so definitely related to
temperatures (and therefore having a distinctive space/time distribution) that systematists have
failed to agree upon the specific or subspecific status of the different forms. Yet, when material from
regions with steeper temperature gradients has been examined, these same cosmopolitan diatoms have
seemed to fall much more convincingly into categories of less than specific rank (often obviously linked
by intermediate forms) of single types. Thus these chaetocerids, and the solenoids mentioned below,
seem justifiably 'lumped' on the basis of our Benguela current material, derived from a typical
upwelling region where the temperature gradients are frequently very steep. Such abrupt variations
in temperature are also to be found near the northern limits of the Kuroshiwo current, whence some
of Gran and Yendo's material and most of Takano's was derived.

Chaetoceros costatum Pavillard, previously widely referred to as C. adhaerens Mangin.

This change was advocated by Hustedt (1927-37, pp. 699-700). Its propriety is not very obvious
from the figures he reproduced from Pavillard and from Mangin. Cupp (1943, p. 127) follows
Hustedt and gives better figures, that agree well with the varied South-west African samples we
studied.

In our material the species was very restricted in distribution, but abundant at four autumn stations
inshore. Here the range of variation in dimensions coupled with the presence of mucous (or ' pecti-
naceous ') cushions between corners of adjoining cells, a character of Mangin's definition, in chains
that also displayed the intercalary bands shown by Pavillard's figure, led me to conclude that Hustedt

MICROPLANKTON 217

is correct in accepting Pavillard's specific name on grounds of priority (Pavillard, 191 1, p. 24,
fig. ib, c; Mangin, 1912, p. 39, fig. 25, pi. II, fig. 10).

The intercalary bands arranged in imbricating fashion were hard to see in some of the colonies, and
many of the frustules resemble the two lower ones in Pavillard's figure, where the bands are visible
only where they approach the cell margin as seen in broad girdle view. Such banding on the con-
nective zone is a rare feature among Chaetocerids, viewed under ordinary conditions, but characteristic
of the related genus Attheya.1

Some of our material even suggested that Chaetoceros imbricatus Mangin (191 2, fig. 37) should also
perhaps be considered as a synonym of C. costatum Pavillard, the cells in the chains were so closely
adpressed, but I could not feel sure of distinguishing between these forms and phases of C. didymum
like the var. agregata also figured by Mangin (191 2, fig. 37) from the type locality of his C. imbricatus
off Brest, under the working conditions imposed by normal plankton analysis. C. didymum was
exceedingly abundant, in a welter of varieties or phases, at most inshore stations during our Benguela
current survey. The question must be left open, with the admission that further detailed work may
serve to show the presence of C. imbricatus Mangin here, and that it may have been wrongly included
with C. costatum Pavillard, or with some phase of C. didymum in my counts. As the numbers involved
were exceedingly small in comparison with those of clearly indentifiable species, the point is of small
.moment in considering the diatom flora as a whole.

Chaetoceros subsecundum (Grunow) Hustedt formerly known as Chaetoceros diadema (Ehrb.) Gran.

Hustedt ( 1 927-37, p. 645) details the argument by which, under the International Rules for Botanical
Nomenclature, the widely known specific name diadema, finely descriptive of the resting spores, and
based on Syndendrium diadema Ehrenberg 1854, should be supplanted by the above combination,
based on C. distans (Cleve) var. subsecunda Grunow (ex Van Heurck, 1881 (1880-5).

It appears that Grunow was right to reject diadema on realizing that the forms in question were
related to Chaetoceros, Syndendrium diadema becoming a nomen cofifusem, since it was based upon the
resting spores only. Unfortunately, Grunow was mistaken in relating it to C. distans Cleve (1873),
itself a misidentification of C. dichaeta Ehrenberg. It thus became necessary to elevate the varietal
name to specific rank as Hustedt has done, though there is still much doubt and confusion about the
full synonymy.

I am greatly indebted to Mr N. I. Hendey for a personal communication helping to clear up this
obscurity.

Rhizosolenia imbricata Brightwell var. (or phase) Shrubsolei Cleve, often previously considered
as a distinct species, R. shrubsolei Cleve.

Our Benguela material of this usually small and narrow form of comparatively cold waters seems
to me to provide ample support for the view that it is not specifically distinguishable from the stouter
form of warmer seas described as R. imbricata by Brightwell.

Hustedt (1927-37, p. 584) gives formal expression to this view, and points to the synonymy with
R. striata Greville and the apparent lack of justification for the establishment of Peragallo's R. atlantica
and R. pacifica, both seemingly also synonyms of R. imbricata Brightwell.

A footnote of Gran's (1905, p. 52) anticipates Hustedt's decision, pointing out that if the specific
identity of the two forms could be demonstrated, Brightwell's name should be the one used on
priority grounds, and it would seem that Cleve himself had drawn attention to the matter.

At several Benguela current stations both forms were present, mainly very much as figured by
Lebour (1930, p. 97) under the name R. shrubsolei Cleve, but many individuals intermediate both with

1 Intercalary bands have also been described in Chaetoceros teres, visible only after special treatment and mounting (Mangin,
1908) and in Chaetoceros eibenii by Pavillard (1921).

%$■ ,
^OODs

zi8 DISCOVERY REPORTS

regard to their size and degree of flattening of the valves were also present. Also' I gained a distinct
impression of a relative increase in numbers of the stouter form in the warmer waters before re-reading
the debatable taxonomic literature.

Boden (1950) who worked on material from the Atlantic side of Cape Peninsula has also accepted
Hustedt's view, but a full study of the earlier synonymy and detailed re-examination of our material
in further support thereof would require a separate publication.

Fragilaria Karsteni Boden nom. nov. instead of F. capensis Karsten.

Boden (1950, p. 406) has explained that Karsten's term was preoccupied by F. capensis Grunow,
1863, which differs structurally and in size from the species under discussion, hence the need for
the new name that Boden has established.

Thalassionema nitzschioides (Grunow) Hustedt, previously very widely known as Thalassiothrix
nitzschioides Grun., Van Heurck.

Hendey (1937, p. 336) points out that although Grunow wrote of the possibility of a need to establish
a new genus Thalassionema he did not define this proposed genus at all, and that Hustedt (1927-37,
p. 244) was the first to do so. Hendey holds, therefore, that the authority should be ascribed to
Hustedt.

Noctiluca miliaris Suriray, instead of N. scintillans (Macartney) to which this widely known
organism is often referred.

On this vexed question we have accepted Schillers (1933-7) verdict in favour of the later
N. miliaris Suriray (1816), 1836, against the earlier synonyms Medusa marina Slabber (1771) 1778,
and Medusa scintillans Macartney, 18 10. Kofoid (1919) who first produced good evidence of the
dinoflagellate affinities of this enigmatic, heterotrophic form, preferred Macartney's specific name for
it. Before that most marine biologists had used Noctiluca miliaris Suriray.

We have not been able to consult all the early references quoted by Schiller, but if the genus
Noctiluca of Suriray is accepted, as it has been by almost all naturalists ever since Ehrenberg used it in
1834, ■* seems only consistent to use his specific name for the type-species also; since the earlier
synonyms placed the organism in a ' false genus '. Under admittedly much more recent interpretations
of the ' rules of nomenclature ', they should therefore lapse ; unless Suriray had himself decided to
use one or the other in making a 'new Combination'. Most probably he did not know of the earlier
descriptions.

Dinophysis tripos Gourret, previously widely known as Dinophysis homunculus var. tripos (Gourret).

It is now generally held that Stein's D. homunculus is a synonym, in part, of at least three of the
species in the Caudata group of Dinophysis: D. caudata Kent, which should replace homunculus as
a specific and as group-name on grounds of priority, D. diegensis Kofoid and D. tripos Gourret.
Lebour (1925) has pointed out that in D. tripos the hypotheca always shows a second smaller more
dorsal point, in addition to the well-defined ' Tail ' ; whereas in D. caudata varieties the tendency to
form a definite projection in the corresponding position is much less pronounced. A single figure of
an extreme variety of D. caudata from the Persian Gulf by Dr V. Pietschmann, reproduced by Schiller
(1933, p. 157, f. 145, u.) shows a definite secondary 'point', but it is appreciably smaller and less
acute than that of D. tripos, even when comparing it with the figures of the latter (several are given by
Schiller) in which the feature is least developed. 'Discovery' material both from the east and west
coasts of Africa seemed to me (T. J. H.) to be clearly ascribable to D. tripos Gourret, although
D. caudata Kent may also be found at some of the localities.

In the Benguela current, D. tripos was limited to the extreme north of the area covered by our
survey, and to the extra stations south of the area that preceded the second survey. It was not observed
in the central portion of the coastal current where the heaviest diatom catches were taken and where

MICROPLANKTON 219

the negative temperature anomaly was greatest. This can scarcely be due to the effect of temperature,
however, for the species is often abundant in water as cold as this (in the absolute sense, not in terms
of iso-anomaly) far to the south on the Atlantic side of Cape Peninsula. Further, it may be equally
abundant in warm waters of the Agulhas current on the east coast, as far north as Durban and probably
beyond. This implies temperature tolerance throughout the range io° to 23 ° C. at the least. The dis-
continuity in distribution off the south-west coast could, however, be due to a markedly stenohaline
reaction on the part of D. tripos. The area from which we found it almost absent coincides with the
low salinities observed northwards from the Orange river mouth throughout the area of maximum
upwelling activity to Luderitz Bay and beyond.1

The point has been mentioned here because Schiller (1933) who has done so much to clear up the
taxonomy of the Caudata group, added the trenchant note 'Ob immer stenohaline?' concerning the
distribution of D. tripos, which suggests that this trait had already been noticed in other regions.

Diversity of the microplankton
The rich variety of the microplankton in the region surveyed may be judged from the list of all
208 categories recorded in the routine counts (Table 12). This table also shows their frequency of
occurrence, and the frequency with which they occurred as dominants in each of the two separate
•series of thirty-nine stations, repeated at approximately the same positions, and in the smaller sub-
sidiary series as shown by the column headings.

Table 12. List of all microplankton categories recorded among routine counts, with data on their
frequency of occurrence, and dominance, as shozvn by column headings

Species or category

DlATOMACEA

Melosira sphaerica Karsten

Skeletonema costatitm (Grev.) Cleve

Stephanopyxis palmeriana (Grev.) Griinow

S. turris (Grev. & Arnott) Ralfs

Thalassiosira condensata Cleve

T. excentrica Karsten

T. hyalinum (Griin.) Gran

T. rotula Meunier

T. subtilis (Ostenfeld) Gran

Thalassiosira spp. non det.

Bacterosira fragilis Gran

Coscinodiscus gigas Ehrenberg

C. janischii A. Schmidt

C. parvulus Karsten

C. radiatus Ehrenberg

Coscinodiscus spp. non det.

Actinocyclus spp. non det.

Planktoniella sol Wallich

Hemidiscus cuneiformis Wallich

Actinnptychus senarius Ehrenberg

Asterolampra spp. non det.

Asteromphalus heptactis (Brebisson) Ralfs

Biddulphia longicruris Greville

B. mobiliensis Bailey

B. regia (Schultze) Ostenfeld

Cerataulina pelagica (Cleve) Hendey

Triceratium favus Ehrenberg

Triceratium spp. non det.

Station

Six extra

Three extra

Four dis-

WSio76

Second

survey

stations to

coloured

(extra, no

First

survey

J9 stations

south of

north of

water-

counterpart on

39 stations

(repeated)

mam

area

main area

samples

first survey)

Domi-

°resent

nant

Present

nant

Present

nant

Present nant

Present >5%

Present nant

2
1

1
3

1 1

1 0

3 0

— —

—

1 1

— —

0
0

3 1

3 0

1 0

—

— —

2 0

1 0

2 0

— —

—

2 0

— —

—

2 0

— —

1 0

—

0
0

1 0
1 0

— —

1 Here Dietrich (1950) has shown iso-lines of negative anomaly of 0-5-1-5 %0 salinity, with normal values north and south,
and but a little distance seaward.

220

DISCOVERY REPORTS

Table 12 {cont.)

First survey
39 stations

Species or category
DlATOMACEA
Ditylum brightu-elli (West) Griinow
Hemialus hauckii Griinow
Eucampia cornula (Cleve) Griinow

E. zoodiacus Ehrenberg
Chaetoceros affine Lauder
C. atlanticum Cleve

C. compressum Lauder

C. constrictum Gran

C. convolutum Castracane

C. costatum Pavilliard

C. curvatum Castracane

C. curvisetum Cleve

C. debile Cleve

C. decipiens Cleve

C densum Cleve

C. difficile Cleve

C. didymum Ehrenberg (vegetative phases)

C. didymum Ehrenberg (resting spores)

C. holsaticum Schiitt

C. imbricatuin Mangin

C. laciniosum Sthutt

C. lorenzianum Griinow

C. parallelis Boden

C. periwianum Brightwell

C. pseudocrinitum Ostenfeld

C. sociale Lauder

C. strictum Karsten

C. subsecundum (Griin.) Hustedt

C. subsecundum (Griin.) Hustedt (resting spores)

C. teres Cleve

C. tetras Karsten

C. van heurcku Gran

Chaetoceros spp. non det.

Bacteriastrum delicatulum Cleve

B. hyalinum Lauder

B. varians Lauder

Rliizosolenia alata Brightwell

R. cylindrus Cleve

R. fragilissima Bergon

R. hebetata (Bailey) Gran

R. imbricata Brightwell

R. robusta Norman ex Pritchard

R. setigera Brightwell

R. simplex Karsten

R. stolterfothii H. Peragallo

R. tyliformis Brightwell

Guinardia blavyana H. Peragallo

Guinardia sp. non det.

Leptocylindris danicus Cleve

Dactyliosolen mediterraneus H. Peragallo

Corethron criophilum Castracane

Fragilaria granulata Karsten

F. karsteni (Karsten) Boden

AsteHonella japonica Cleve & Moller ex Gran

Thalassiothrix frauenfeldii (Griin.) Cleve & Griin.

T. longissima Cleve ex Griinow

Thalassionema nitzschioides (Griin.) Hustedt

Striatella sp. non det.

Achnanthes longipes Agardh

Navicula membranacea Cleve

Navicula spp. non det.

Pleurosigma capense Karsten

Pleurosigma sp. non det.

Nitzschia closterium (Ehrb.) Wm. Smith

N. delicatissima Cleve

N. longissima (Breb.) Ralfs

Ar. seriata Cleve

Present

17
22

4
2
15
4
5

[2
'3

I
I

1 1

2
7

5
7
5
1

5
17

Domi-
nant

4
1

13
12

22
1

5
6
6

o
o
o

o
I
o
7
3
o

7
1

5
2

o
o
6

2
O

o
o

2
I

Second survey
3g stations
(repeated)

Six extra

stations to

south of

main area

Three extra

stations to

north of

main area

Four dis-
coloured
water-
samples

Station

WS 1076

(extra, no

counterpart on

first survey)

Present

Domi-
nant

Present

Do?ni-
nant

Present

Domi-
nant

Present >5% Present

Domi-
nant

4
IS
22
26
22

4
10

3
3

5
10

2
22

2
10
17
14

9
14

6
21

6
28

5
14
19

5
o

o
II

I
o
o
o
o
o

o
9

— 2

MICROPLANKTON

Table 12 (cont.)

221

Species or category
DlNOPHYCEAE
Prorocentrum micans Ehrenberg
Prorocentrum sp. non det.
Palaeophalacroma verrucosum Schiller
Phalacroma Rudgei Murray & Whitting
P. argus Stein
P. minutum Cleve
Phalacroma spp. non det.
Dinophysis ovum Schutt
D. sphaerica Stein

D. acuminata Claparede & Lachmann
D. schrbderi Pavillard
D. srhiietii Murray & Whitting
D. tripos Gourret
Gynmodinium spp. non det.
Noctiluca miliaris Suriray
Warnowia sp. non det.
Blastodinium mangini Chatton
Blastodiniacea non det.
Ellopsidaceae non det.
Sphaerodinium sp. non det.
Peridinium triquetrum (Ehrb.) Lebour
P. crassipes Kofoid
P. depressum Bailey
P. elegans Cleve
P. oceanicum Vanhoffen
Peridinium spp. non det.
Goniaulax spinifera Clap. & Lachmann
Goniaulax sp. non det.
Pyrodinium sp. non det.
Amphidoma nucula Stein
Ceratium candelabrum (Ehrb.) Stein
C.furca (Ehrb.) Clap. & Lach.
C. pentagonum Gourret
C. lineatum (Ehrb.) Cleve
C.fusus (Ehrb.) Dujardin
C. tripos (O. F. Miiller) Nitzsch
C. arietinum Cleve
C. limulus Gourret
C. platycorne von Daday
C. ranipes Cleve
C. vultur Cleve
C. buceros Zacharias
C. massiliense (Gourret) Jorgensen
C. macroceros (Ehrb.) Cleve
C. trichoceros (Ehrb.) Kofoid
Goniodoma polyedricum (Pouchet) Jorg.
Goniodoma sp. non det.
Small Dinophyceae non det.

Other Protophyta
Trichodesmium thiebautii Gomont [filaments]
Phaeocystis sp. non det. [colonies]
Trochischia brachiolata (Mob.) Lemm.
T. multispinosa (Mob.) Lemm.
Halosphaera viridis Schmitz
Umbilicosphaera sp. non det.
Coccosphaeriales (other) non det.
Dictyocha fibula Ehrenberg
Distephanus speculum (Ehrb.) Haeckel

Protozoa
Challengeridae
Acanthometridae
Radiolaria (other)
Foraminifera
Sticholonche sp. non det.
? Cyclotrichium meunieri Powers

Station

Six extra

Three extra

Four dis-

WS 1076

Second survey

stations to

coloured

(extra, no

First survey

J9 stations

south of

north of

water-

counterpart on

39 stations

(repeated)

main area

samples

first survey)

. * .

Domi-

Present nant Present nant Present nant Present nant Present >5% Present nant

— — — — — — — — 3 1 —

— - — 1 o — — — — — — — —

I o — •

I o ■ ■

I o

1 O I o

I o

2 O — — — —

I o

I o ■

60 — _______

I o

4 o 6 o 6 4 — — — — — —

3 o 1 o — — — — 1 o — —
1 o 2 o s 1 — — — — — —

— — 1 0 — — — — —

1 o — — — — — — ■ — ■ — —

20 — 10 —

— — 1 o — — — — — — — —

— — — — — — — — 3 3 — —

3 1 — _________

1 o — — — — — — — — — —

2 o —

8 £,__________

36 8 39 16 6 1 2 1 30 1 o

14 6 2 o — ■ — ■ — — — ■ — — —

— — 1 o — — — — — — — —

1 o — — — — — — ■ — — — —

1 o — — — — — — — — — —

13 1 40 30 — — —

11 010 o 6 o — — — — — —

— 4° — — — — — —

II I 4 O 2 O

24 2 19 O 5 O 2 O

9 i 6 o 6 3 — — — — —

19 I 12 OI020 — ■ — —

— — 70 ___ _

40— — — —

— — — — 40 — — ___

— — I o — — _ — — — — —

— — 6 o 5 o 1 o — — — —
10 o 2 o • — — — — — — — —

1030 — — — — —

2 O - — I o — ■

— — 2 0 —

4 i 8 3________

j 0

I 0 __

2 O 5 O — — — —

2 o — —

! 0 — — . — . — —

4 Oil O 2 O — —

I o 2 O

7 016 o 4 o — — — — 1 o

4450 — — — — — —

22 I 21 O 4 O

24 3 33 74020

3 o 9 o 4 o 2 o — — — —

— — — — — — — — 1 1 — — .

J-l-2

222

DISCOVERY REPORTS
Table 12 (co?it.)

Station

Six extra

Three extra

Four dis-

WS 1076

Second survey

stations to

coloured

(extra, no

First survey

39 stations

south of

north of

water-

counterpart on

39 stations

(repeated)

main area

samples

first survey)

1 \
Domi-

Domi-

Donii-

Domi-

Species or category

Present nant

Presenl nant

Present nant

Present > 5

Present nant

Protoza

Ciliata (other, Tintinnids excepted)

Tintinnopsis spp.

Codonella spp.

Codonellopsis spp.

Favella spp.

Parafavella spp.

Epiplocylis spp.

PJiabdonella hrandti Kofoid & Campbell

Rhabdonella spp.

Rhabdonellopsis spp.

Parundella spp.

Xystonella spp.

Xystonellopsis spp.

Undella spp.

Undellopsis tticoltaria (Laackmann) K. & C.

Proplectella spp.

Dictyocysta spp.

Bursaopsis spp.

Amphorella spp.

Steenstrupiella spp.

Amphorellopsis spp.

Dadayiella spp.

Tintinnus lusus-undae Entz, Snr.

Salpingella spp.

Tintinnoinea (non det.)

Metazoa
Diphyids (Siphonophora)
Chaetognatha

Polychaeta mainly larvae and post-larval
Ova: ? molluscan
Pteropoda : Limacina juv.
Pteropoda : ? Gymnosomata juv.
Post-larval lamellibranchs
Molluscan larvae, other
Ova: mainly Copepodan
Egg packets: mainly Harpacticid
Ova: Euphausian
Nauplii

Evadne nordmanni Lov£n
Ostracoda
Copepoda
Cumacea

Euphausiidae: early larvae
Euphausiidae: late larvae -> adult
Ophioplutei
Appendicularia
Doliolidae
Fish eggs
Fish larvae and post-larvae

Seston
Cast skins, etc.
Faecal pellets

— —40 —

4 O 2 O I o — — — — — —

I 017 I- — — 2 O

1 o 2 O

j 0

I O I O

10 on o — — — — — — — —

9210 — — — — — — —

10 1 4 o — — — — — — — —

2 o 1 o — — — — — — — —

— 30 —

2 o — — — — — — — —

2070 10 10

6 o 7 o — — — — — — — —

1 o — — — — — — — — —

— — 5 o —
202130 — — 20 — —

2 o — — — — — — — — — —

2020 — — — — — — —

- — — — — — 2 o — —

x O

— — 60 — — 10 — — —
407030

2010 — — — — —

10 o 1 o 3 o 20

30 — — 20 — — — —

1 O I o 2 o — — — — — — ■

2 I

4360 — —

3020 — — — — — — —

— — 1 o 3 o — — — — — —

I o — — — — — — — — —

21 10 28 3 3 o 1 o 1 o —

22 3 16 13020 —

2I?0

37 16 37 14 6 2 2 1 —

1 o — — — — — — — — —

38 15 35 14 6 2 2 1 — —
4010 — — — — — — —

105030 — — — — —

— — 3 o — — —

1 o — — — — — — — — — —

17 1 5 o 2 o — — — — — —

2 o • — — 2 o — — — — — —

608020 — — — — —

608020 —

From the full list, shorter series limited to the categories occurring as dominants (a) during both
surveys, (b) during the first survey only, and (c) during the second survey only, have been abstracted
in Table 13. Here the frequency data have been summarized in the form of double fractions. Thus
the entry ' Stephanopyxis turris 10/3 and 11/1 ' signifies that this species was present at ten out of the
thirty-nine stations of the first survey and dominant at three of those ten; present at eleven of the
second survey stations, but dominant at only one of them.

223

MICROPLANKTON

This table provides most of the basis for selection of the relatively more important forms, without
which detailed consideration of the vast mass of data on distribution and relative abundance could
not usefully be attempted. It seemed best to insert it here, following immediately upon the full list
from which it has been derived, although the further consideration of individual species — distribu-
tions, etc. in which it has been utilized is deferred until after the description of main group distribution.

Tables 12 and 13 suffice to bring out one important difference between the rich diatom-flora of this
typical subtropical upwelling region, and that of other sea areas where diatoms predominate, such as
the antarctic zone of the southern ocean. The colder water flora and that of the Benguela current have
alike been described as ' monotonous ' (in a restricted sense) since the one class of algae predominates
in both of them. The colder water flora, however, tends to be characterized by a more extreme
monotony, in that one or two species are frequently found to predominate over all the others to a very
marked degree, over wide areas and for long periods of time (Hart, 1934; Marumo, 1953). The
Benguela current samples are very much more varied, as shown by the large number of species
recorded as dominants on the criterion chosen here. Even if we apply the criterion used by the
Japanese — least number of species needed to attain 50% of the total cell count — the diversity of the
Benguela samples would be more than twice as great as that of many antarctic ones, at least five or
six species being needed to attain this proportion in most of the catches. Indeed, when we consider
the occasional predominance of dinoflagellates, and of Trichodesmium at some of the poorer stations,
and the fact that such nannoplankton forms as Coccosphaeriales and small dinoflagellates would
certainly bulk far more largely had it been practicable to use other sampling methods, it seems very
doubtful whether this plankton should be regarded as ' monotonous ', even in the restricted sense.

Table 13. Abridged frequency data: Categories occurring as dominants at one or more of

the thirty-nine repeated stations

(a)

(b)

During both sun

eys

During the first survey only

During the second survey on ly

Stephanopyxis turris

10/3 and 1 1/1

Eucampia zoodiacus

1 1/4 and 0/0

Skeletonema costatum

1/0 and 3/1

Thalassiosira excentrica

14/3 and 3/1

Chaetoceros costatum

4/4 and 1/0

Thalassiosira spp. non det.

2/0 and 14/5

T. subtilis

12/2 and 14/3

C. didymum (resting spores)

13/6 and 3/0

Coscinodiscus spp. non det.

8/0 and 28/1

Planktoniella sol

19/6 and 24/9

C. pseudocrinitum

2/1 and 0/0

Asteromphalus heptactis

5/0 and 6/1

Chaetoceros affine

2/1 and 4/1

C. subsecundum

1 1/3 and 3/0

Chaetoceros atlanticum

0/0 and 15/5

C. compressum

17/13 and 24/9

C. teres

15/7 and 2/0

C. lorenzianum

2/0 and 14/9

C. constrictum

22/12 and 26/19

C. van heurckii

9/5 and 1/0

C. peruvianum

8/0 and 10/ 1

C. convolutum

17/7 and 22/5

Chaetoceros spp. non det.

3/2 and 0/0

C. sociale

1/0 and 5/3

C. curvisetum

1 5/1 1 and 18/12

Rhizosolenia simplex

8/2 and 8/0

Rliizosolenia se tiger a

0/0 and 10/3

C. debile

4/3 and 4/2

Leptocylindrus danicus

5/2 and 2/0

R. styliformis

7/0 and 17/11

C. decipiens

5/1 and 14/8

Pleurosigma capense

3/1 and 1/0

Thalassionema nitzschioides

1/0 and 7/1

C. difficile

8/5 and 14/2

Nitzschia closterium

10/2 and 6/0

Nitzschia longissima

2/0 and 6/1

C. didymum (vegetative

phases)

12/6 and 10/2

Peridinium crassipes

3/1 and 0/0

Codonella spp.

1 '0 and 1 7/ 1

C. strictum

1 1/7 and 10/6

Goniaulax spinifera

14/6 and 2/0

C. tetras

4/1 and 2/2

Ceratium candelabrum

13/1 and 4/0

Rhizosolenia alata

23/6 and 22/5

C. lineatum

1 1/1 and 4/0

R. hebetata

26/12 and 18/7

C. fusus

24/2 and 19/0

It. imbricata

7/1 and 13/2

C. tripos

9/1 and 6/0

Dactyliosolen mediterraneus

7/1 and 10/6

C. arietinum

19/1 and 12/0

Fragilaria granulata

1/1 and 14/5

Acanthometridae

4/4 and 5/0

F. karsteni

5/3 and 9/7

Radiolaria (other)

22/1 and 21/0

Asterionella japonica

17/9 and 14/7

Rhabdonella brandtii

9/2 and 1/0

Nitzschia delicatissima

19/14 and 21/9

Rhabdonella spp.

10/ 1 and 4/0

N. seriata

22/9 and 28/18

Dictyocysta spp.

20/2 and 13/0

Peridinium spp. non det

36/8 and 39/16

Ova, ? molluscan

2/1 and 0/0

Trichodesmium thiebautu

4/1 and 8/3

Pteropoda : Limacina juv.

4/3 and 6/0

Foraminifera

24/3 and 33/7

Ova: Euphausian

2/1 and 0/0

Ova, mainly Copepodan

21/10 and 28/3

Appendicularia

1 7/ 1 and 5/0

Egg packets, mainly Harpacticid

22/3 and 16/1

Nauplii

37/16 and 37/14

Copepoda

38/15 and 35/14

Cast skins, etc.

9/4 and 32/10

Faecal pellets

15/7 and 27/4

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MICROPLANKTON

225

Distribution of the main groups of microplankton

First survey
The estimated numbers of the main groups of microplankton present in the hauls from each station
are given in Table 14, with the approximate distances of the stations from the nearest point on the
coast. The fractions examined, number of species or other categories recognized in each count, and
the settlement volumes of the catches are also given, together with percentages of the main groups
relative to the totals, as shown by the column headings. These data, excepting the percentages, are
also shown graphically in Figs. 58-64, designed to aid general description of the results on each
separate line of stations.

2o°-

25 -

WE POINT

I04-

■°bl 1

105-

io*| J

10*

..o'JM

io;-

-lO<T .-■■1

WALVIS BAY

s
o
u

T
H

30.

SYLVIA HILL

ORAVCE
R.

SURVEY I

1 1 1 1 1 1 r

0° 15° EAST

Fig. 57. Distribution of the microplankton, estimated totals per net haul, survey I, March 1950.

(Station numbers are shown in Fig. 1.)

Fig. 57 shows the estimated microplankton totals in the first survey contoured logarithmically.
From this the concentration of the heaviest catches in the coastal waters, more particularly in the
centre of the region, is quite clear. The zone of rich coastal microplankton was narrow in the south,
off the mouth of the Orange river, and reached its greatest extent seawards off Walvis Bay. The increase
in width of the zone with decreasing latitude up to this point was interrupted by one deep constriction
at the seaward end of the Sylvia Hill line. North of Walvis Bay the coastal microplankton was much
less abundant, though still richer, especially in phytoplankton, than that of the offshore waters. The

226 DISCOVERY REPORTS

coastal zone also narrowed again to the north, and off Mowe Point the general tendency of diminishing
quantity of microplankton with increasing distance from land was somewhat obscured by the presence
of relatively poor isolated catches within the coastal region. The hydrological data and qualitative
plankton observations combine to show that these were due to actual tongue-like intrusions or isolated
patches of more oceanic surface-water (see pp. 157, 246), with inherently poorer plankton content,
and not merely to local impoverishment of the coastal water population. It would seem that the Mowe
Point line was near the northern limit of the main region of upwelling at the time of this survey,
and that some inter-digitation of the distinctive types of surface-water (and even some overlapping of
these in the vertical plane) was the result. Such effects, well known to occur on a large scale near the

WS970 WS969 WS9b8 WS967 WS9M> WS9bS «VS9M

'S970 WS969

III I III

(*#•-'

METAZOA

""protozoa"

NO SESTON RECORDED

SEA MILES FROM LAND

■a

MICROPLANKTON
PHYTOPLANKIOnT""*^^ _

-rf

VOLUME

IOO-,

I 1 1

10-

-ri

DIATOMS

rrr^"

DINOPHYCEAE** ~ , —

■a

NO OTHER PLANTS
RECORDED

•d

METAZOA

PROTOZOA

•d

NO SESTON RECORDED

0 '

SEA MILES FROM LAND

Fig. 58. Distribution of main groups of microplankton,
estimated totals per net haul. Mowe Point line, survey I,
4-5 March 1950. The histogram shows the settled volumes
of the catch in millimetres.

Fig. 59. Distribution of main groups of microplankton,
estimated totals per net haul, survey I, Northern Inter-
mediate line, 5 March 1950.

northern limits of the analogous Peru coastal current, must necessarily affect any simplified presenta-
tion of data collected with an arbitrarily chosen spatial limit, and plotted on the horizontal plane only,
as here.

Inshore on the Sylvia Hill line the two innermost stations show, as did the stations inshore on the
Walvis Bay and mid-intermediate lines, the heaviest concentrations of phytoplankton. According to
the hydrological evidence (p. 162) these occur in old and rather mixed upwelled water. The two
outermost stations on the Sylvia Hill line present a strong contrast. The phytoplankton, in quantity
more characteristic of oceanic water, consisted of a rather neutral mixture of coastal and oceanic
species. The hydrological evidence we have seen tends to link these two stations with more purely
coastal water farther to the south, but the relatively high salinities and the salinity section (Fig. 15) in
particular, suggest that they may lie in rather mixed oceanic water, into which some very recent
upwelling was introducing a pattern of vertical layering.

One other distributional feature well shown in Fig. 57 — the extreme poverty of the microplankton
offshore in the south of the area, even at moderate distances from land — is much more difficult to
understand. The point is reconsidered later when the results from the Orange river line are described
in detail.

227

MICROPLANKTON

From Fig. 58 it can be seen that, on the Mowe Point line, the quantities of all main groups excepting
Protozoa were highest inshore, with a pronounced falling off at the third station seawards, some slight
secondary increase farther out and then a general decrease, most marked among the diatoms, to the
low oceanic values at the seaward end of the line. ' Other plants ' were observed in very small numbers
some distance offshore, but not at the two outermost stations. The proportion of Dinophyceae to
diatoms was above the average for the whole survey area, and Seston was not noted at the dilutions
necessary to obtain counts. The relative abundance of Protozoa here was due mainly to large Radio-
laria and especially tintinnids. The total estimated numbers of microplankton were relatively small

throughout.

It should be noted that the stations have been plotted so that the distance scale from the land sea-
wards reads from the left of the page, regardless of chronological sequence. This has been done so
as to secure uniformity of treatment throughout the series of diagrams (Figs. 58-64, 66-72).

o
d

HC?

WS963 WS984 W5985

"'On

70"M^;

VOLUME

IIOO

OINOPHYCEAf'

NO OTHER PLANTS
RECORDED

OO
SEA MILES FROM LAND

SO 60

SEA MILES FROM LAND

Fig. 60. Distribution of the main groups of microplankton,
estimated totals per net haul, survey I, Walvis Bay line,
6-8 March 1950.

Fig. 61. Distribution of the main groups of micro-
plankton, estimated totals per net haul, survey I,
Middle-Intermediate line, 9-10 March 1950.

On the northern intermediate line the quantities of microplankton were still small and rather
uniform, greatest at a moderate distance out towards the shelf-edge and least, owing mainly to the
usual drop in diatom numbers, at the station farthest offshore. The proportion of Dinophyceae to
diatoms was unusually high, and it will be shown later that local abundance of Gonianlax spinifera
was mainly responsible for this. Neither ' other plants ' nor Seston were observed on this line.

Conditions more typical of the Benguela current proper were first encountered on the Walvis Bay
line (Fig. 60). Here the vastly greater quantities of diatoms in the inshore waters and their abrupt
decrease seawards are even reflected in the settlement volumes. (The latter are rarely a reliable guide
to plankton quantities, being frequently distorted by differential packing among organisms of diverse
shapes, the presence of small numbers of extra large organisms, and the necessity of settling out large
samples in relatively wide cylinders, so that the volumes cannot be read with the same accuracy as the
small ones.) They are included only for their value as a basis for crude comparison with earlier
collections in other areas, from some of which numerical estimates are not yet available.

228

DISCOVERY REPORTS

wsqso ws9<)i ws<m wsws wsw ws<ns

SEA MILES FROM LAND

Fig. 62. Distribution of the main groups of microplankton,
estimated totals per net haul, survey I, Sylvia Hill line,
io-ii March 1950.

-0
■6

\\ MICROPLANKTON

Lii

VOLUME
PHYTOPUNKTON |OQ

IO.

J l_L

-.PINQPMICEAE.

NO DINOPHrCEAE OTHER PLANTS-.

RECORDED
-NO OTHER PLANTS INSHORE

SEA MILES FROM LAND

Fig. 63. Distribution of the main groups of microplankton,
estimated totals per net haul, survey I, Southern Inter-
mediate line, 11-12 March 1950.

WSI002 WSIOOI WSIOOO WSW WSS9B wsw

J I I III

So ■ 100

SEA MILES FROM LAND

Fig. 64. Distribution of the main groups of microplankton, estimated totals per net haul, survey I,

Orange river line, 12-14 March 1950.

On the Walvis Bay line Protozoa and Metazoa were present only in very moderate numbers, their
relative importance greatly increasing beyond the point where the rich diatom plankton declined. Yet
again this transition zone was the only point where 'other plants' were noted.

Rich inshore conditions persisted right out to the seaward end of the short mid-intermediate line,
with large volumes, very large numbers of diatoms, and relatively few Dinophyceae (Fig. 61).

MICROPLANKTON 229

Seston was recorded at the two outer stations, the first time it had been observed (in the very small
fractions used to obtain microplankton counts) during this first survey.

The Sylvia Hill line (Fig. 62) showed extreme contrast between the two diatom-rich inshore
stations, and the impoverished offshore stations, where Dinophyceae were almost as numerous as the
diatoms.

Again, the southern intermediate line (Fig. 63) showed very similar conditions; a heavy diatom-rich'
microplankton inshore; while offshore, though all the other groups showed some slight falling off in
numbers from the third station seaward (where diatoms still predominated) the relative importance
of those other groups was much greater in the smaller catches.

Finally, on the Orange river line (Fig. 64) the rich diatom plankton of the two inshore stations
contrasted strongly with extremely small quantities of phytoplankton offshore, though moderate
numbers of Protozoa, Metazoa and considerable quantities of Seston were recorded there. The capture
of large numbers of herbivorous zooplankton especially the Pteropod Limacina bulimoides at these
offshore stations, and the large quantity of Seston present, suggested that recent intensive grazing may
have reduced a richer phytoplankton offshore not long before the stations were worked ; because the
greater width of the continental shelf at this point would lead one to expect greater seaward extension
of the rich inshore conditions here at most times. The zooplankton data derive from the sorting of
-material from nets of coarser mesh, so that this point cannot be indicated in the uniform series of
diagrams.

Second survey
Primary data concerning groups totals, relative percentages, etc., for the microplankton samples
obtained during the second survey are given in Table 15. This has been constructed so that the
sequence of stations, and of the lines of stations, follows that of the corresponding observations made
during the first survey, regardless of their chronological order (cf. Table 14).

The total microplankton estimates for the second survey, contoured logarithmically in Fig. 65
(corresponding to Fig. 57 for the first survey) show an underlying similarity of distribution, consistent
with the idea that upwelling activity proceeds (doubtless with minor fluctuations in intensity) through-
out most of the year, over the major part of the area. Except in the extreme south, where the observa-
tions on the Orange river line are anomalous, rich catches inshore with rapid decrease in quantity as
one proceeded seawards was the general rule. The heaviest catches of all were again obtained off
Sylvia Hill and Luderitz Bay, and yet again an incursion of offshore water with contrastingly poor
plankton was evident immediately seawards of the richest area, suggesting recurrence of the swirl
centred (perhaps) to the south of the one encountered here during the first survey. A tongue-like
intrusion of sparsely populated oceanic water in the north, on the Mowe Point line, was even more
clearly defined than during the first survey, owing to the working of three extra stations to the north
of the repeated series.

With all these points of resemblance to the distribution observed during the first survey there are
still some differences, showing that even within a current-system apparently so persistent throughout
most of the year, some seasonal changes affect the plankton population. Thus during the second
survey the region of rich coastal plankton was smaller and did not extend so far seaward, especially
off Walvis Bay. Conversely, the offshore microplankton, though still much more scanty than that to
be found inshore, was generally somewhat richer than it had been during the first survey, especially
to the north. Indeed, on the Mowe Point line (Fig. 66) only the station farthest inshore was appreci-
ably richer in diatoms than those near the seaward end of the line. ' Other plants ' were recorded only
near the apparent transition point between the rapidly dwindling coastal plankton and the seasonally

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MICROPLANKTON 231

enriched offshore community in the poorest sample. A tendency towards restriction of this group to
the transition zone had also been apparent on several of the lines worked during the first survey.

Other main groups were very evenly distributed on the Mowe Point line during the second survey.
The quantities of Metazoa were moderately high, and considerable quantities of Seston were recorded,
suggesting that feeding and growth of the smaller plankton animals might be proceeding more uni-
formly and somewhat faster at this period than in the autumn.

20°

25°H

S "

o
u

T
H

io4-io5[
io5-io6r

MOWE POINT

IO-IO "

IO-IO

IVALVIS BAY

SURVEY: I
1 r

EAST

— T 1 1

10° 15°

Fig. 65. Distribution of the microplankton, estimated totals per net haul, survey II,
September-October 1950. (Station numbers are shown in Fig. 2.)

On the northern intermediate line (Fig. 67) similar conditions prevailed, indicating that the relative
richness of offshore phytoplankton and general abundance of small zooplankton feeding voraciously
were features distinguishing the samples collected during the second survey from the ones from
corresponding first survey positions.

The figures for the Walvis Bay line (Fig. 68) show a rich diatom plankton right inshore and a
secondary peak at station WS 1079. The work on this line was interrupted by a gale, so that some
considerable time elapsed between the working of this and the preceding inshore stations. There is
hydrological evidence (p. 1 88) supporting the view that surface-drift of inshore water during the interval
led to this apparent anomaly. In other respects the features of the microplankton distribution offshore
on this line during the second survey were similar to those found farther north: moderately high

232

DISCOVERY REPORTS

WSIO06 WSCW7 WSI098 WSK399WSIIOO WSIIOI WSIIO?

MICROPLANKTON
PHYTOPLANKTON*. ./

VOLUME
MLS
IOO

I I I 1 1 I I

DIATOMS

_— . DJNOPHYCEAE

» OTHER
PLANTS
ONLY RECORDED
AT WS IOS9

NO '
SESTON

"at wsio<x>"

'■%

rQv

SEA MUS FROM LAND

Fig. 66. Distribution of the main groups of microplankton,
estimated totals per net haul, survey II, Mowe Point line,
9-1 1 October 1950. The histogram shows the settled volume
of the catch in millimetres.

10*

HO*

I. '

-id

-id
-id

>I093

ws 1090 ws io89 ws ioss

. MICRQfLANKJON

^ PHYTOPLANIOON^ .

J L 1JJ

VOLUME
OOi

MLS
O

. OTHER PLANTS
RECORDED AT WS "
1090 I WSIO88ONLY

META20A
"" PROTOJoV"

SESTON

SEA MILES FROM LAND

Fig. 67. Distribution of the main groups of microplankton,
estimated totals per net haul, survey II, Northern Inter-
mediate line, 8-9 October 1950.

WSI07S WSI077 WSI078 WSD79 WSI08I WS I060

,WS I074 WSI073' WSD72 WS 1071

rIO

■d

d
d

„ ^^1^ VOLUME

■d

MIS
IOO-,

■d

1 1

ill!

-id
■d
■d

0jX ...P^OPHYCfAE.

■d

"'"••-•■:.: •"

...OTHER PLANTS

..■■■"" ''-.NO OTHER

NO OTHER PLANTS PLANTS

WS 1078 AT WSOFO

■d
-d

-.-.."■

METAZOA

SESTON

50 IOO

SEA MILES FROM LAND

Fig. 68. Distribution of the main groups of microplankton,
estimated totals per net haul, survey II, Walvis Bay line,
29 September-2 October 1950.

SEA MILES FROM LAND

-cf

-D4

VOLUME
MLS
IOO-|

■id

1 1 1°

-d

V Di£*S&—

■d
-d

OTHER PLANTS

-d

-id

■■^L

META.2QA..

PR0T07n<

"" SESTON

■id

Fig. 69. Distribution of the main groups of microplankton,
estimated totals per net haul, survey II, Middle Inter-
mediate line, 28 September 1950.

MICROPLANKTON 233

values for Metazoa and Seston throughout, 'other plants' mainly in the transition zone and rather
more diatoms, relatively, than had been found at the corresponding positions in autumn.

The group data for the mid-intermediate line show more profound differences from the conditions
found there during the first survey. Then the diatom-rich coastal plankton had extended right out to
the seaward end of the line (Figs. 61 and 65). During the second survey (Fig. 69) the rich coastal
plankton with diatoms dominant was confined to the inshore station, the other groups were relatively
more important throughout than they had been in autumn, and the secondary increase in diatoms
towards the seaward end of the line was mainly due to offshore species. Conditions here and on the

WSIOM
d '

d
-d
d

WSI062 WSDfcl WSIObO WSI059WSIOS8 WS IOS7

MICROPLANKTON

MLS
IOOO

IOO-

J L

^TWwWED A1

... 1fIVO„

PROTOZOA
NOT RECORDED
""'AT WSIOM 2

a
o'
d
d
d
hd

OTHER PLANTS RECORDED
AT-WS K36I

NO
SESTON RECORDED
AT WS IQbl

SEA MILES FROM LAND

Fig. 70. Distribution of the main groups of microplankton,
estimated totals per net haul, survey II, Sylvia Hill line,
21-24 September 1950.

Fig. 71. Distribution of the main groups of microplankton,
estimated totals per net haul, survey II, Southern Inter-
mediate line, 24-25 September 1950.

adjacent lines both north and south displayed the general narrowing of the zone of rich coastal plankton
that seemed characteristic of the second survey in its most extreme form.

The extremely rich diatom plankton found at the inshore station on the Sylvia Hill line (Fig. 70)
showed clearly that, quite locally, the coastal population attained a density as great as that observed
during the autumn, but proceeding seawards we again encountered the conditions met with farther
north: a more rapid transition to relatively scanty offshore plankton, and greater relative abundance
of Metazoa and Seston than had been observed there during the first survey.

A very similar distribution of the main groups was also evident on the southern intermediate line
(Fig. 71) where the diatom population inshore was one of the richest sampled during either survey.
' Other plants ', chiefly represented by isolated filaments and a few rafts of Trichodesmium thiebautii,
attained their maximum numbers and greatest relative importance in the comparatively scanty
offshore plankton on this line, but it should be emphasized that the species was not observed in any-
thing approaching bloom-forming quantities.1 Such blooms as we observed during the surveys were

It is one of the commonest and most widely distributed bloom-forming organisms throughout the warm and temperate
regions of the South Atlantic.

234 DISCOVERY REPORTS

due to diatoms, dinoflagellates and ciliate Protozoa, but it is quite probable that Trichodesmium may
also form blooms within the area sometimes.

The conditions observed on the Orange river line during the second survey did not conform to the
generalizations found to hold good for the rest of the area (Fig. 72). Here a diatom-rich plankton
with both oceanic and neritic elements was found at the two offshore stations, and inshore there was
an exceptionally poor phytoplankton with a high proportion of Metazoa and Seston. The hydrological
data and qualitative plankton observations give some basis for the ' explanation ', necessarily somewhat
speculative, of this reversal of the usual pattern of quantitative distribution that has been attempted
later (p. 245).

.VSIOiO WSIOSI WSOS2 WSOS3 WS054

50 IOO

SEA MILES FROM LAND

Fig. 72. Distribution of the main groups of microplankton, estimated totals per net haul, survey II,

Orange river line, 21-24 September 1950.

Distribution of the main diatom groups

First survey
The distribution of the main groups of diatoms, distinguished as described on p. 214, is summarized
in Table 16. This shows the estimated total diatom numbers, estimated group totals, and relative
percentages for each individual station. The stations are arrayed in order of the seven lines of observa-
tions as they were worked, from north to south (cf. Table 14).

As a further aid to description, the estimated group totals have been plotted on a logarithmic scale,
in relation to the distance of each station from the coast (Figs. 73-76). In these figures the distance-
scale reads seawards from the left of the page for each line, departing from the chronological sequence
in order to secure uniformity of treatment in this respect.

In commenting on the group distribution, reference has been made to qualitative data not given
here, because the group totals alone can be misleading where they unavoidably include species of
widely differing ecological attributes. This involves some repetition later, the whole difficulty resulting
from the impracticability of publishing the raw data in full.

On the Mowe Point line, the estimated diatom totals were small in comparison with those for the
survey as a whole. They were highest inshore and showed a secondary peak at the shelf-edge,

MICROPLANKTON

235

Table 16. First survey {autumn).

Station

WS964
WS965
WS966
WS967
WS968
WS969
WS970

WS971
WS972
WS973
WS974
WS97S

WS976
WS 977
WS978
WS 979
WS980
WS981

'WS 982
WS983
WS984
WS985

WS986
WS987
WS988
WS989

WS990
WS 991
WS 992

WS993

WS 994
WS99S

WS996
WS 997
WS998
WS 999
WS 1000
WS 1001
WS 1002

Estimated

total

diatoms

73. '24
143,400

363.750

i.°34>25°

22,500

4,118,400

1,382,500

386,000
972,000
1,010,000
314,000
202,000

282,000

212,000

816,000

98,328,000

45.344.°°°
9,987,300

74,070,000
40,180,800
69,432,000
27,477,000

97,300

1 1 ,400

270,450,000

158,508,000

74,006,400

258,300,000

50,692,800

19,800

16,800

12,300

16,000

13,800

3,000

1,200

42,300

7,758,000

43,710,000

Discineae

Estimated total diatoms and numbers in the main
Biddulphiineae Chaetoceraceae Soleniineae

diatom groups
' Pennatae '

Numbers

47,060

123,000

26,250

61,750

i,500

833.184

108,500

18,000
147,000
276,000
156,000

24,000

20,000

21,600

2,000,000

1,936,000

2,185,200

1,302,000

2,305,200

168,000

396,000

4.300

3,600

9,720,000

8,649,000

4,147,200

nil

100,800

4,200

1,800

3,000
4.500
75°
nil

300
nil
nil

/o
64-4
85-8

7-2

3-8
67

20-2

7-8

47
15-1

27-3
497
n-9

7-1

9-4
2-6

2-0

4'3
21'9

i-8

0-2

4'4

3i-5
3-6

5-5

5-6

0-2
21-2
I0"7
14-6

18-8

32-6

25-0
07

Numbers

nil
nil
nil
30,000
nil

243>936
112,000

nil
nil
nil
nil
nil

nil
nil
nil

80,000

3,328,000

194,400

384,000
648,000

nil

2,500

nil
7,470,000
4,329,000

105,600
nil

96,000
nil
nil
nil

nil
nil
nil
nil
nil
nil
nil

5-9
8-2

Numbers

nil
nil

206,250

1,030,000

2,250

'23-552
172,000

8,000
33,000
nil
ml
34,000

6,000

64,000

552,000

93,888,000

22,080,000

2,57°.4°°

59,580,000

36,792,000

67,968,000

25,992,000

34,000

6,900

2-7 208,170,000

2-7 118,872,000

0-2 56,448,000

— 243,450,000
0-2 45,024,000

9.3°°
5.!°°
8,400

2,000

300

500

200

41,400

— 7.434.000

— 38,006,000

o-i
69

2-0

0'5
i-6

2-6

°/
/o

567
63-0
io-o

3-o

12-4
2-1

3-4
16-8

2-1
30-2
67-6

95-5
49-1

257
80-4
916
97-9
94-6

34"9
60-5
77-0

75-o

76'3
94-3

88-8
47-0

30-4
68-3

!2"5
2-2
16-7
167
97-9

95-8

87-0

0/
A>

Numbers

'9.548
8,400

35.00°

32,500

12,000
484,704 11-38
810,000 58-6

334.o°°
231,000
418,000

46,000

18,000

58,000
62,000
74,400
32,000
264,000
69,300

1,488,000

72,000

336 000

45,000

10,000

900

4,005,000

1,512,000

614,400
nil
nil

4,500

2,400
nil

4,000

2,400

nil
400
600

nil

26-7

5-8
8-6

2-0

53-2

58-6
23-8
41-4
14-6
8-9

20-6

29-3

<o-i

o-6

°7

2-0
0-2

o-5

0-2

10-3

8-o

i'5
0-9

o-8

22-7
H-3

25-0
17-4

33-3
'•4

Numbers

6,516

12,000

96,250

480,000

6,750

2,433,024

180,000

26,000
516,000
316,000
112,000
126,000

198,000

66,000

68,000

2,328,000

17,736,000

4,968,000

11,316,000
363,600

960,000
1,044,000

46,500

nil
41,085,000
25,146,000

12,691,200

14,850,000

5,472,000

1,800

7,500

2,100

7,000
6,600

x>75°
600
nil

324,000
5,704,000

0/
/o

8-9

8-4

26-5

29-4
30-0

59-i

13-0

577

357
62-4

70-2
31-1

20-6

2-4

391

497

'5'3
0-9

i-4

3-8

47-8

15-2
x5'9

17-1

57
io-8

91
44-6
17-1

437
47-8
58-3

5°'3

4-2
13-0

diminishing to characteristically small oceanic values offshore. There was a marked minimum between
the two peaks, believed to be due to intrusion of offshore water.

Considering the groups severally, it can be seen that the Discineae reached their greatest numbers
in the richer inshore water. Here the neritic Stephanopyxis was dominant. The greatest relative
importance of the group was attained at the poorer offshore stations, however, where the essentially
oceanic Planktoniella sol accounted for most of the group-total.

Biddulphiineae were observed only at the two inshore stations, and at the secondary peak station
near the shelf-edge. The neritic species Eucampia zoodiacus was the only one seen in the fractions
counted, and the group was of little relative importance.

Chaetoceros species were unusually scanty close inshore, but predominated at the shelf-edge peak
station. The group was not seen at all at the two offshore stations though these were re-examined
carefully.

236 DISCOVERY REPORTS

Soleniineae were abundant close inshore, present elsewhere in very moderate numbers, becoming
of some relative importance only in the very small minimal haul, and again at the outer end of the
line. Leptocylindrus danicus, one of the few neritic species in this essentially holoplanktonic group,
was mainly responsible for the inshore maximum. Various Rhizosolenia species, among the most
cosmopolitan of all plankton diatoms, were present at the minimal station ; while right offshore the
oceanic species Rhizosolenia simplex was the dominant form.

'Pennatae' formed an unusually high proportion of the total diatom count at the inshore peak
station and were second only to Chaetoceros among the group totals at the shelf-edge peak. The small
'reversionary plankton forms' Nitzschia spp. and Asterionella japonica were chiefly responsible, with
a considerable proportion of the larger Thalassiothrix longissima at the shelf-edge. The latter usually
showed a more oceanic distribution than other members of the group in these surveys.

WS970 WS969 WS968

W5966 WS965 WS9M
I I I

WS975

« TOTAL DIATOMS
-» CHAETOCERACEAE
-' "PENNATAE"
■> BIDDULPHIINEAE
o DISCINEAE
- SOLENIINEAE

so ido

SEA MILES FROM LAND

Fig. 73. Estimated total diatoms, and diatom group totals, survey I. A. Mowe Point line, 4-5 March 1950.

B. Northern Intermediate line, 5 March 1950.

On the northern intermediate line, the estimated diatom totals were very moderate throughout,
with a slight maximum at the second and third stations seaward, diminishing to the outer end of the
line.

From the group figures it appears that Discineae were relatively somewhat more important in the
small catches here than over the survey area generally. The panthalassic species Thalassiosira excentrica
and Planktoniella sol (oceanic) were both among the dominants at the three slightly richer stations at
the middle of the line. This may have been due to the mixing conditions thought to have obtained
within the ' Goniatdax-patch ' (see p. 251).

Biddulphiineae were not observed in the routine analyses on this line and species of Chaetoceros
were present in small number at the two inshore stations only. A majority of this group proved to be
mainly neritic throughout the survey, but on the other lines they were nearly always dominant inshore ;
not the most poorly represented group, as here. Soleniineae were dominant inshore and at the peak
station, represented mainly by panthalassic cosmopolitan species such as Rhizosolenia hebetata and
R. alata ; the falling off in relative importance of this group towards the seaward end of the line was an
unusual feature thought to be bound up with the mixing conditions referred to above.

On this northern intermediate line the ' Pennatae ' were the most important single group numerically,
with the minute Nitzschia delicatissima the most important individual species, joined by the large

MICROPLANKTON 237

Thalassiothrix longissima at the seaward end of the line (one of the few details in which this series
approached a norm for the area as a whole!).

On the Walvis Bay line (Fig. 74) the estimated diatom totals reached high values at the three inshore
stations, with a sharp decline beyond the shelf-edge, levelling out to moderate amounts at the two
oceanic offshore stations. The high inshore values proved typical of the main upwelling region on
most of the lines worked throughout both surveys, as can be seen from the subsequent diagrams.

Discineae were present in fair numbers inshore, represented mainly by Stephanopyxis turns and
Thalassiosira subtilis, the one definitely a neritic species, the other panthalassic. Offshore the numbers
declined, at first in parallel with the estimated diatom totals, levelling at the two outer stations to give
a slight secondary increase in relative importance. This was due mainly to the species Thalassiosira

WS98I

TOTAL DIATOMS
CHAETOCERACEAE
- -' 'PENNATAE"
.„„„„... BIDDULPHIINEAE
o DISCINEAE
-■ SOLENIINEAE

n ' ' ' lio ' ' ' ""

SEA MILES FROM LAND

Fig. 74. Estimated total diatoms, and diatom group totals, survey I. A. Walvis Bay line, 6-8 March 1950.

B. Middle Intermediate line, 9-10 March 1950.

excentrica, with lesser numbers of Planktoniella sol. Biddulphiineae were present inshore and of con-
siderable importance at station WS 980, but were not observed seawards of the peak station WS 979.
The group was represented here entirely by Eucampia soodiacus, as on the Mowe Point line.

Chaetoceros was by far the most important group over the Walvis Bay line as a whole. It was
strongly dominant at the two richest inshore stations, where a profusion of neritic species were present,
and at the first of the poorer stations, seawards. There, however, the single ' relatively oceanic ' species
Chaetoceros convolatum alone accounted for most of the group total. Still further offshore the group
dwindled rapidly, both in estimated numbers and in relative importance.

Soleniineae were present at all stations on the line in consistently small numbers, becoming
relatively important in the poorest offshore plankton. Cosmopolitan Rhizosolenia spp. predominated
throughout, accompanied at one inshore station, where the group total was highest, by the mainly
neritic Dactyliosolen mediterraneus.

' Pennatae ' were an important group on this line, especially at the innermost and outermost stations

15-2

238 DISCOVERY REPORTS

where they predominated. Even at the intervening stations they ranked second only to the chaeto-
cerids. The unavoidably heterogeneous nature of the group, however, was very evident. Whereas
inshore the strongly neritic species Fragilaria karsteni predominated, along with Asterionella japonica,
it was the oceanic Thalassiothrix longissima and panthalassic Nitzschia delicatissima that accounted for
nearly all of the group totals farther out.

The mid-intermediate line proved too short to extend beyond the rich coastal diatom zone. The
estimated diatom totals were high throughout and very closely paralleled by the group-totals for the

WS986

-D

D4
d

"W5990 WS|Wl WS992 WSW WS994 WS995

• • TOTAL DIATOMS

-♦ CHAETOCERACEAE
■ -' "PENNATAE'
». BIDDULPHIINEAE
o DISCINEAE
— SOLENIINEAE
\ '"
\
\

IOO

SEA MILES FROM LAND

F'g- 75- Estimated total diatoms, and diatom group totals, survey I. A. Sylvia Hill line, io-ii March 1950.

B. Southern Intermediate line, 11-12 March 1950.

predominating chaetocerids. The other groups clearly fulfilled a minor role, much on the same level,
with 'Pennatae' of some consequence inshore. Apart from the profusion of neritic Chaetoceros
species, at least ten in number, the species of most importance were :

Among the Discineae, inshore, Stephanopyxis turris diminishing rapidly as one proceeded seawards;
and Thalassiosira sabtilis, which reached its highest numbers and relative importance at station
WS 983.

Among the Biddulphiineae, Eucampia zoodiacus at the two inshore stations only.

Among the Soleniineae, Dactyliosolen mediterraneus and much lesser numbers of the more cosmo-
politan Rhizosolenia spp. farther offshore.

Among the ' Pennatae ', Fragilaria Karsteni and Asterionella japonica inshore with Thalassiothrix
longissima at station WS 984.

On the Sylvia Hill and southern intermediate lines, diatom distribution followed an essentially
similar pattern. Very high estimated totals were recorded inshore, with an abrupt decrease near the
shelf-edge some 60 sea-miles from the land, and a levelling out to very low values towards the sea-

MICROPLANKTON 239

ward ends of each series of observations. Chaetocerids were by far the most important group, as can
be seen from the way in which their group-totals follow closely in parallel with the figures for total
diatoms. Inshore they were represented by the usual rich variety of species, mainly neritic but some
with panthalassic tendencies. Offshore there was some apparent overspill of the most abundant
inshore forms, but the more definitely oceanic members of the genus, such as Chaetoceros convolution
and C. peruvianum, were relatively much more important in the very poor phy toplankton met with there.

The estimated totals for other groups was also greatest inshore, but the relative importance of those
with offshore representatives was much greater near the shelf-edge and beyond.

The Discineae were represented mainly by Thalassiosira spp. Of these T. hyalinum, T. rotula and
the panthalassic T. subtilis were commonest inshore ; T. excentrica and T. subtilis (again !) offshore. The
oceanic Planktoniella sol was of some relative importance in one extremely small sample from near the
outer end of the southern intermediate line.

W5I002 WSIOOI WSIOOO WS999 WS998 WS997

WS996

-iO

TOTAL DIATOMS
CHAETOCERACEAE
"PENNATAE"
BIDDULPHIINEAE

-IO

SO IOO

SEA MILES FROM LAND

Fig. 76. Estimated total diatoms, and diatom group totals, survey I, Orange river line, 12-14 March 1950.

The Biddulphiineae were almost entirely confined to the inshore stations on both series, though
Eucampia zoodiacns was recorded in very small numbers from station WS 986, at the seaward end of
the Sylvia Hill line. This same species accounted for most of the inshore totals for the group, as we
had found farther north at this season, but here there was a small proportion of Cerataulina pelagica
in addition.

Soleniineae formed only a small proportion of these samples. The higher numbers at three inshore
stations were due to the mainly neritic species Dactyliosolen mediterraneus and Leptocylindrus danicus.
The very small totals for this group at offshore stations show that it was of some slight relative
importance there, but only because of the prevailing poverty of the offshore phytoplankton. The
offshore species included Bacteriastrum hyalinum, the more cosmopolitan Rhizosolenia spp. and
R. simplex.

The 'Pennatae' were more heavily outnumbered by the dominant chaetocerids at the inshore
stations of these two lines than they had been farther north, but still ranked second among the diatom
groups. The dominant inshore species — Fragilaria karsteni, Asterionella japonica and Nitzschia seriata
— were the same as those recorded on the two previous lines. Offshore small numbers of Nitzschia
dehcatissima, N. seriata and Thalassiothrix longissima accounted for most of the group totals, together
with Fragilaria granulata at station WS 994. This species was recorded only at this one station during
the first survey, but much more frequently and abundantly during the second, when it showed a con-
sistently offshore distribution. The very small totals of ' Pennatae ' recorded at stations WS 986 and 994
just suffice to indicate greater relative importance than that of the chaetocerids, so clearly dominant
at all the other stations of the Sylvia Hill and southern intermediate lines.

24o DISCOVERY REPORTS

Although the very great difference in quantity between the rich diatoms inshore and the impoverished
phytoplankton population farther out is well shown by these two series of observations, the qualitative
distinctions are less clear than they seemed to be on other lines worked during the first survey. This
is believed to be due to the wide tolerance of the more panthalassic species of Chaetoceros, Nitzschia
and Thalassiosira. Prolongation of the lines seaward would almost certainly have demonstrated their
replacement as dominants by more exclusively oceanic species, but this desideratum could not be
foreseen in planning the surveys. ' Ideal ' coverage can never be wholly attainable in such work, and
had we extended these two series, practical considerations of steaming time, fuel consumption and
water supply must have enforced a corresponding curtailment of the rest of the ship's programme.

The inshore zone of rich diatom phytoplankton was narrower on the Orange river line (Fig. 76)
although the shelf is wider there, and diatoms were exceptionally scanty for a considerable distance
seaward. Even at the two stations right out beyond the shelf-edge the catches were still very small.
Peculiar local conditions must have obtained here, for the rich zooplankton and abundance of Seston
indicate heavy grazing of what must have been a very much richer standing crop of plants not long
before. Further deviation from the conditions prevailing farther north were indicated by the presence
of essentially neritic species along with the oceanic ones at the stations farthest from land.

Even so, apart from the narrowing of the rich coastal belt and extreme poverty of the outer stations
on the shelf, the group distribution of diatoms on this line still shows some of the main features
observed farther north. Thus most of the chaetocerids so completely dominant inshore were neritic
ones, although the panthalassic species Chaetoceros convohitum was present in greater proportion than
was usual inshore elsewhere. The decline in relative importance of this group at the impoverished
offshore stations, with correspondingly increased proportions of Discineae, Soleniineae and ' Pennatae '
there, is well shown in Fig. 76.

Specific data for the groups other than Chaetoceros show that the panthalassic Thalassiosira subtilis
and oceanic Planktoniella sol among the Discineae and Thalassiothrix longissima among the ' Pennatae '
were relatively more important offshore as in the other more normal series.

Second survey
Similar treatment of the data from the Mowe Point line on the second survey shows that at that season,
although the inshore station was still the richest by far, the diatom totals diminished rapidly as the
ship proceeded offshore. A minimum was reached at station WS 1099 near the edge of the shelf and
there was then a considerable secondary rise in estimated totals at the three offshore stations (Table 17
and Fig. 77).

Totals for each of the four main diatom groups present1 varied roughly in parallel with those for
total diatoms, but whereas the numbers and the proportion of Chaetoceros and 'Pennatae' were
greatest inshore, there were many more Soleniineae present at the outer stations. These outer stations
were somewhat less well defined qualitatively than those on some of the more southerly series at group
level, since they still contained a moderately high proportion of Discineae and Chaetoceros, both groups
containing a majority of inshore species. The more detailed data seem to show up their distinction
fairly clearly, though there was evidently more tendency towards offshore transport in the turbulent
conditions prevailing than had been observed during the autumn survey.

Among the Discineae the inshore maximum was due mainly to Stephanopyxis turris and Thalassio-
sira spp. Though the secondary rise in numbers of the group at the offshore stations included some
of these two categories, Stephanopyxis there formed a much smaller proportion of the totals, Thalas-

1 Biddulphiineae were not observed on this line.

MICROPLANKTON

241

Table 17. Secotid survey (spring). Estimated total diatoms and numbers in the main diatom groups

Estimated

Discineae

Biddulphiineae

Chaetoceraceae

Soleniint

' Pennatae '

total
diatoms

Stat

ion

1
Numbers

Numbers

t
Numbers

0
0

Numbers

0
0

[102

1,734,000

42,000

2-4

nil

—

606,000

349

729,000

42-1

357,000

20-6

[101

5,208,000

162,000

nil

—

1,632,000

3I-3

2,640,000

5°7

774,000

149

[100

4,968,000

189,000

3-8

nil

—

792,000

!5'9

3,609,000

727

378,000

7-6

[099

185,400

9,000

nil

—

28,800

I5-5

49.500

26-7

98,100

529

[098

2,082,000

90,000

nil

—

930,000

447

300,000

14-4

762,000

36-6

[097

1,398,000

132,000

9'4

nil

—

531,000

38-0

105,000

7'5

630,000

45-i

[096

19,320,000

3,072,000

159

nil

—

1 1,064,000

57'3

936,000

4'8

4,248,000

220

1093

3,618,400

489,600

135

nil

—

2,091,600

57-8

126,000

3'5

911,200

25-2

[091

969,300

S1^00

5'3

nil

—

221,400

22-8

518,400

53-5

178,200

18-4

[090

1,317,000

81,000

6-2

nil

—

492,000

37"4

609,000

46-2

135,000

10-2

[089

117,000

16,200

13-8

nil

—

9,900

8-5

85.500

73'1

5.400

1088

1,159,500

i,500

nil

—

48,000

4'i

1,101,000

95-0

9,000

o-8

ioSo

483>300

18,900

3'9

nil

—

8,100

405,000

83-8

5!.30o

io-6

[081

405,000

10,800

nil

—

24,300

6-o

256,500

633

113,400

28-0

1079

1,962,000

58,50°

3-o

nil

—

198,000

io-i

1,206,000

61-4

499.5oo

25-5

[078

25. 500

7,500

294

nil

—

nil

—

nil

—

18,000

70-6

[077

402,600

133.800

33-2

8,400

87,600

21-8

nil

—

172,800

429

■075

22,923,000

576,000

2'5

nil

—

11,061,000

48-3

45,000

0-2

11,241,000

49-0

1074

11,835,000

315,000

6,000

<o-i

1,326,000

112

6,000

<o-i

10,182,000

86-o

•°73

87,000

19,500

22-4

nil

—

52.5oo

60-3

3,000

3'5

12,000

13-8

1072

820,800

79,200

9-6

nil

—

168,000

20-5

393,600

48-0

180,000

21-9

1 07 1

2,694,000

39,000

nil

—

195,000

7-2

1,698,000

631

762,000

28-3

1070

1,941,600

52,800

nil

—

734,400

37-8

508,800

262

645,600

33 '3

1069

840,600

882,00

10-5

nil

—

654,000

77-8

22,800

75,600

9-0

1064

67,950,000

630,000

0-9

270,000

0-4

64,800,000

95-4

180,000

o-3

2,070,000

3-o

1063

312,300,000

1,200,000

0-4

30,000

<o-oi

296,100,000

948

210,000

<o-i

14,760,000

1062

258,680,000

1,000,000

0-4

480,000

0-2

236,800,000

91-6

nil

—

20,400,000

7-8

1 061

27,264,000

2,136,000

7-8

24,000

o-i

19,440,000

7i-3

nil

—

5,664,000

20-8

1060

10,740,000

252,000

2-3

nil

—

6,816,000

63-5

nil

—

3,672,000

34-2

1059

199,800

36,000

18-0

nil

—

19,800

19,200

124,800

62-3

1058

416,400

44,400

107

3,600

84,000

20-2

36,000

8-6

248,400

59-°

i°57

161,200

72.540

45-0

nil

—

14,260

8-8

1 1 , 1 60

7-o

63,240

392

1056

6,375.6o°

171,600

2-7

39,600

o-6

4,422,000

694

198,000

3'1

1,544,400

24-2

1055

28,584,000

1,281,600

4-5

nil

—

25,488,000

892

72,000

0-2

1,742,400

6-i

io54

3.9°°

2,100

53-8

nil

—

nil

—

nil

i,Soo

46-2

i°53

1,500

1,050

70-0

nil

—

!5°

io-o

nil

3°o

20-0

1052

4,800

3,000

62-5

nil

—

nil

—

nil

1,800

37-5

1051

67,800

24,000

354

nil

—

38,400

566

600

0-9

4,800

7-1

1050

103,500

39,600

38-3

nil

—

55,200

53-3

nil

—

8,700

8-4

siosira showed specific differences, and there was a very marked increase in the typically oceanic
Planktoniella sol (absent inshore) from station WS 1099 seawards.

Some of the dominant coastal chaetocerids persisted (in reduced numbers) to the outer end of the
line, but again more typically offshore forms such as C. convolutum and C. lorenzianum showed marked
increase in relative importance from station WS 1099 seawards. Similar specific differences were
shown within the two other groups also: Inshore Rhizosolenia setigera and Leptocylindrus danicus were
the most important solenoids, while offshore Rhizosolenia styliformis and Dactyliosolen mediterraneus
were the most abundant of all the diatoms at this time. Fragilaria karsteni and Asterionella japonica
were among the dominant ' Pennatae ' inshore. The former was not seen more than 30 sea-miles from
land, and though Asterionella was found farther out it was present only in relatively small numbers
there. The cosmopolitan Nitzschia seriata was observed in both localities, but offshore it appeared
that N. delicatissima was the most numerous species of the group at this season.

242 DISCOVERY REPORTS

The results from the northern intermediate line showed essentially the same features as those
observed off Mowe Point, most of them even more definitely (Fig. 77). It is true that Fragilaria
karsteni was not present among the ' Pennatae ' at the inshore station, but this was 30 miles from the
land, and from all our other observations the species seemed to be the most strongly neritic in habit
of all the important plankton forms in this area. The solenoid community, with some few of the more
oceanic Chaetoceros spp. was even more completely dominant offshore, where the line extended into
a region where almost all the microplankton was essentially oceanic in character. At station WS 1088,
no less than 94% of the diatoms was made up of the cosmopolitan Rhizosolenia spp. R. styliformis,
R. hebetata and R. imbricata.

WSD96 WSI097 WSI098 WSI099 WSIIOO WSHOI WSII02

re?
rf

rf
rf
rf

rrf
rf
rf
rf
rf

WS 1093

WS I09I

WS O90 WS 1089 WS O88

-• TOTAL DIATOMS

- CHAETOCERACEAE
-' 'PENNATAE"

>■■ BIDDULPHIINEAE
o DISCINEAE

— SOLENIINEAE

160

SEA MILES FROM LAND

Fig. 77. Estimated total diatoms and diatom group totals, survey II. A. Mowe Point line, 9-1 1 October 1950.

B. Northern Intermediate line, 8-9 October 1950.

The dominance of this solenoid community at offshore stations persisted in very marked degree
at the outer end of the Walvis Bay line, where, however, there was a larger proportion of Thalassiothrix
longissima, perhaps the most oceanic of the ' Pennatae ', among the small fraction of the total not
accounted for by the solenoids. Indeed it would appear that with minor modifications the solenoids
predominated in the offshore plankton from about the middle of the area to the northern limit of our
serial observations at the time of this second survey (cf. Table 17, Figs. 76-8).

The inshore stations on both the Walvis Bay and mid-intermediate lines also displayed common
features that differed markedly from those observed in autumn. In spring the rich coastal flora of
Chaetoceros spp., with Asterionella and Fragilaria karsteni among the 'Pennatae', etc., was confined
to the innermost stations, with an abrupt diminution seawards before the shelf-edge was reached. There
was thus a pronounced narrowing of the rich coastal belt here in spring, where it had been wide, and
fanned out seaward to the shelf-edge on the Walvis Bay line, during the first (autumnal) survey
(cf. Fig. 57 and Fig. 65). The spring results resembled more the extreme contrast within a relatively
short distance out from the coast, that had been shown on the Sylvia Hill line, immediately to the
southward, in autumn. The distributional pattern is consistent with the active upwelling which was
demonstrated by the hydrological results from this region. Within the upwelling water, the larger

MICROPLANKTON 243

concentrations of phytoplankton were found at the stations nearest to the coast, and there was a rapid
decrease seawards before even the shelf-edge was reached. On the occasions where the stations
extended far enough from the coast, a secondary increase in the phytoplankton is evident — the
abundance beyond the shelf-edge was greater than on the first survey. The population in this secondary
increase included some oceanic forms among its dominants and it seems probable that it was associated
with the divergence of oceanic water beyond the shelf-edge, which was postulated in the interpretation
of the mechanism of upwelling (p. 188, Fig. 37).

Turning to conditions observed on the Sylvia Hill line itself during the second survey (Fig. 79) it
can be seen that although the falling-off seawards was pronounced, diatom members were still very

, WS075 WSI077

W^I078

WS079

WSO8I

WS 1080

~W|i074 WSI073 WSI07 2 WSKD7I

■ • TOTAL DIATOMS

. « CHAETOCERACEAE

, , PENNATAE"

..„„„,.„ BIEXXJLPHIINEAE
o- o DISCINEAE
SOLENIINEAE

SO IOO

SEA MILES FROM LAND

Fig. 78. Estimated total diatoms and diatom group totals, survey II. A. Walvis Bay line, 29 September-2 October

1950. B. Middle Intermediate line, 28 September 1950.

high at the second station seawards, with coastal chaetocerids and ' Pennatae ' still strongly dominant.
While the neritic Biddulphiineae were observed at the inshore station only, as was to be expected,
members of the other two groups persisted right to the outer end of this comparatively short line, and
it was only at the outermost station that the oceanic solenoids became equally important. This
distribution resembled that seen on the mid-intermediate line (that next to the N. in the series) during
the first survey.

On the southern intermediate line, the falling-off in quantity from the exceptionally rich inshore
station was steep, but the succeeding stations seawards were still quite rich and showed a typical
coastal flora extending fully 50 sea-miles from the coast. It seems probable that here again the inshore
stations were characteristic of the active upwelling shown on the Sylvia Hill line. The sharp fall in
abundance from station WS 1060 to station WS 1059, and the persistence at the latter station and
those towards the seaward end of the line of a scanty oceanic type of plankton, was correlated with the
pronounced intrusion of oceanic water to the north of the Orange river line, illustrated by the surface-
temperature pattern (Fig. 76).

The detailed figures for the southern intermediate line in spring show some minor anomalies at
group level that require comment. At the outer oceanic station Discineae and 'Pennatae', both

244 DISCOVERY REPORTS

groups containing a majority of inshore species, were relatively important. The individual counts
show, however, that the oceanic species Planktoniella sol accounted for most of these Discoidae, and
the typically offshore species Thalassiothrix longissima and Fragilaria granulata were prominent among
the ' Pennatae ', though in that group panthalassic Nitzschia spp. were also numerous. It was here that

WSIOb3 WSIOM WSIObq

W5I070
1

-io8 ^^>.

-o7 '"•■- ^s^

,x "■'--■--. '.-^

-d*

-D3

WSI062WSIObl W5D60 WSIOS9 WSIOS6 WSDS7

D
D7

-o6
d

- TOTAL DIATOMS
♦ CHAETOCERACEAE
-' "PENNATAE"

- BIDDULPHIINEAE
o DISCINEAE

SOLENIINEAE

SEA MILES FROM LAND

Fig. 79. Estimated total diatoms and diatom group totals, survey II. A. Sylvia Hill line, 25-27 September 1950.

B. Southern Intermediate line, 24-25 September 1950.

WSD50WSI05I WSIOS2 WSI053 WSI054
III II

-• TOTAL DIATOMS
- CHAETOCERACEAE
-' "PENNATAE"
BIDDULPHIINEAE

WSIOSS
I

~ 1 1 1 1 1 1

fO KX)

SEA MILES FROM LAND

WSIOS6

Fig. 80. Estimated total diatoms and diatom group totals, survey II, Orange river line, 21-24 September 1950.

relatively large numbers of Trichodesmium thiebautii, the filamentous, sometimes colonial blue-green
alga most important among the few ' other plants ' in these samples, were met with.

Finally, the Orange river line showed an extraordinary reversal of the conditions observed during
the first survey, the two diatom-rich stations now being found far beyond the projecting shelf-edge
at the outer end of the line. Further, they showed a most extraordinary admixture of species. Though
oceanic forms such as Chaetoceros atlanticum, C. peruvianum and Planktoniella sol were among the
dominants, the essentially coastal Chaetoceros compressum was abundant at station WS 1055. In the

MICROPLANKTON

245

absence of further serial observations to the southward, we can but speculate as to the reasons for this
reversal of a feature that remained clear throughout the eleven other series of both surveys. We have
seen from the hydrological sections that active upwelling was very pronounced on this line of stations.
The stations on the continental shelf lay within the very recently upwelled water, perhaps too recent
for extensive plankton production to have got under weigh. The two rich stations were beyond the
edge, and may be comparable with those showing secondary offshore increase in phytoplankton on
the more northerly series of observations.

20-

25°H

S 1

o
u

T _
H

3d-

N \

<I0

MO HE POINT c a
IO-IO

o6-,o7

io7-to8

>I0°
H'ALIIS BAY

SYLVIA HILL

ORANGE
R.

SURVEY I

— 1 1 r

10° 15° EAST

Fig. 81. Distribution of Chaetoceros, survey I, March 1950
(Station numbers are shown in Fig. 1.)

20°-J

25°.

O
U

T
H

30:

MO WE POINT

oosn
ios-io6r~i

io^io7p

io^o8l

IVALVIS BAY

IO°

OMNGE

SURVEY: II

EAST

Fig. 82. Distribution of Chaetoceros, survey II, September-
October 1950. (Station numbers are shown in Fig. 2.)

Special distributional features
It is hoped that the following figures are fairly illustrative of the main distributional trends, sum-
marizing the features described in discussing group distributions, and giving examples of the most
marked divergences from typical group pattern shown by certain individual species. Most of them
are based upon estimated numbers per net haul, contoured logarithmically. Percentage of total
diatoms has been used as the criterion for certain categories whose great relative importance in the
scanty offshore plankton could not be shown by consideration of their numbers alone. This need
arises from their cosmopolitan tendencies permitting them to attain equal or even greater abundance

16-2

246 DISCOVERY REPORTS

farther inshore, without, however, forming any significant proportion of the vastly richer vegetation

present there (cf. Figs. 93-5).

Figs. 81 and 82 show the outstanding importance of the group Chaetoceraceae in the rich coastal
waters during both the seasons studied, and the relative narrowing of that zone in spring as compared
with autumn (1st survey). Comparison with Figs. 57 and 65 shows how large a proportion of the total
microplankton observed inshore was composed of the members of this one group of diatoms.

20°-

yiMOWE POINT

25°-

S "

T
H -I

3C*

NIL I I
<|0«Q

I0-I05{g5

WALVIS BAY

ID'

■SYLVIA HILL

ORANGE
A.

SURVEY : I

EAST

Fig. 83. Distribution of Planktoniella, survey I, March 1950.
(Station numbers are shown in Fig. 1.)

EAST

Fig. 84. Distribution of Planktoniella, survey II, September-
October 1950. (Station numbers are shown in Fig. 2.)

The distribution of the one discoid species found to be most numerous in the scanty offshore
phytoplankton — Planktoniella sol — is shown in Figs. 83 and 84. The finger-like extensions towards
the coast shown near the northern limits of the rich coastal upwelling area seem fairly indicative of
actual intrusions of oceanic waters, conforming with hydrological data assessed quite independently
(cf. Rayner in Gunther, 1935; Hart, 1953 and Fig. 95 below).

In contrast to Planktionella most of the Discineae observed on these two surveys were distributed
mainly inshore or over the continental shelf. The distribution of Stephanopyxis turris, one of the most
numerous of these, is shown in Figs. 85 and 86. It can be seen that though it was clearly an essential
coastal form, both in autumn and spring, Stephanopyxis was absent from the middle of the Chaetoceros
zone at both seasons. Further, it was distributed rather more to the northward in spring (Fig. 86)

MICROPLANKTON 247

than in autumn (Fig. 85). This feature cannot be explained by the seasonal shift in temperature alone,
for the species is common in coastal waters round Cape Province, to the south of the area surveyed,
at most seasons, and indeed all round the coasts of South Africa. A stenohaline tendency, such as that
which seems to account for a similar distribution of the dinoflagellate Dinophysis tripos, might be
partly responsible, since the region from which these species seem to be absent corresponds with the

20°

25° .

O
U
T
H 1

30<?

SURVEY:!

IO°

25-

S
O

T _|

30"

'o-io3^

MOWE POINT 3 4E»™a

io-io S

io4-io5i

WALVIS BAY

EAST

10"

SYLVIA HILL

ORANGE
R.

SURVEY -II
1

EAST

Fig. 85. Distribution of Stephanopyxis turris, survey I, March
1950. (Station numbers are shown in Fig. 1.)

Fig. 86. Distribution of Stephanopyxis turris, survey II,
September-October 1950. (Station numbers are shown
in Fig. 2.)

area of maximum negative salinity anomaly. The reduction in salinity is but slight, however, and
Stephanopyxis shows so much adaptability elsewhere that an excluding effect of the superabundant
chaetocerids, operating physically by crowding and/or chemically by noxious external metabolites
(cf. Lucas, 1947) seems a more reasonable hypothesis.

Fig. 87 shows the distribution of Eucampia zoodiacus during the first (autumn) survey, when it
seemed to be strictly confined to the rich coastal waters from Luderitz Bay northwards. The only
Biddulphioid diatom observed in large quantities in any of these samples, the species was not seen at
all in spring; when the group — almost exclusively a coastal one — was represented by forms such as
Eucampia cornuta, Biddulphia longicruris, B. regia and Cerataulina pelagica, irregularly distributed and
all in very small numbers. Eucampia zoodiacus seems to be a coastal form tending to flourish late in

248 DISCOVERY REPORTS

the succession so far as this region is concerned, its autumn distribution being rather similar to that
shown by Stephanopyxis turris, but without the apparent inhibition in the richest part of the Chaeto-
ceros zone.

Aster ionella japonica was the most abundant of the 'Pennatae' in the rich coastal waters, sometimes
extending seawards, but in comparatively small numbers, as can be seen from Figs. 88 and 89. It was
quite uninhibited by the huge quantities of chaetocerids, among which it flourished during the autumn

20°

25°.

S
O
U

T
H

302-

SURVEY : I

•am MO WE POINT

■olio5 □

io5-io6

> 10

WALVIS BAY

SYLVIA HILL

ORANGE
R.

IO 15 EAST

Fig. 87. Distribution of Eucampia zoodiacus, survey I,
March 1950. (Station numbers are shown in Fig. 1.)

20-

25°H

S
O

T
H

30°-

NIL Q

MOWE POINT

<io5

io5-ioc

io6-io7

sfgp

>I07

VALVJS BAY

SURVEY- I

SYLVIA HILL

ORANGE
R.

10° 15° EAST

Fig. 88. Distribution of Asterionella japonica, survey I,
March 1950. (Station numbers are shown in Fig. 1.)

survey. Less numerous, but almost equally widespread in spring. The narrowing of the coastal
zone and apparently increased tendency towards fanning-out of the coastal waters in the extreme
north of the area at that season were features shown in some degree by other important inshore
species.

The distribution of both the species of Fragilaria met with is shown in Figs. 90 and 91. Fragilaria
karsteni proved to be the most strictly coastal of the diatoms encountered in the plankton here during
both surveys ; one might almost describe it as neritic. Though somewhat less widespread in autumn
than it was during the spring survey, the heaviest individual hauls of the species were obtained in
autumn near Walvis Bay.

Fragilaria granulata was a species of the outer shelf stations and offshore waters found mainly in

MICROPLANKTON 249

spring. It can be seen that its distribution never overlapped that of F. karsteni during these two
surveys, and this emphasizes the extent to which the latter can be regarded as an ' indicator ' of inshore
conditions.

Two abundant 'Pennatae' have not been dealt with in this series: Nitzschia delicatissima and
N. seriata. They tended to be irregularly distributed, perhaps reaching their greatest relative

20"

25°H

T
H

30-

SURVEY- 1 1

NIL

<-o5n

MO WE POINT « 6

iotio
>io6

WALVIS BAY

SYLVIA HILL

ORANGE
R.

10° 15" EAST

Fig. 89. Distribution of Asterionella japonica, survey II,
September-October 1950. (Station numbers are shown
in Fig. 2.)

20e

25<

T J
H

30=

fRAGILAKIA > | q*

KARSTENI

SURVEY:!

ORANGE
R.

IO° 15° EAST

Fig. 90. Distribution of Fragilaria karsteni and F. granula'a,
survey I, March 1950. (Station numbers are shown in
Fig. 1.)

importance in outer shelf- waters. Since they are among the most completely cosmopolitan of all
marine plankton diatoms and, moreover, very difficult to separate with certainty when working at the
speed necessary to obtain counts, it is scarcely surprising that they did not show such well-defined
distributional trends as most other members of the group.

Figs. 92 and 93 show the relative importance (percentage of total diatoms) of Thalassiothrix longissima,
the most essentially oceanic of the ' Pennatae ' in this area, to be considerable at the offshore stations,
where the total phytoplankton was poor. It was equally abundant at some rich shelf stations where,
however, its proportion of the whole flora was insignificant.

This same method of treatment was also found necessary to show the high relative importance of
the solenoid group offshore during the second survey only. Here they were definitely dominant, and the

250

DISCOVERY REPORTS

offshore flora proved richer at that season than it had been during autumn. Though essentially holo-
planktonic, the highly cosmopolitan species concerned easily attain greater numbers nearer land at
other times and in other areas, although rarely achieving dominance there. Fig. 94 shows the solenoids
as a percentage of total diatoms during the second (spring) survey only. The individual species mainly
concerned showed a fairly definite sequence as the survey proceeded from south to north. To the
south, far out off Luderitz Bay, Rhizosolenia alata was dominant. Proceeding northwards this was

2C5-

25°

S
O

T -|

3Cf-

F. KARSTENI I 1

NIL I I

IO-IO j }

^ORANGE
R.

SURVEY 1

IO° 15° EAST

Fig. 91. Distribution of Fragilaria karsteni and F. granulata,
survey II, September-October 1950. (Station numbers are
shown in Fig. 2.)

NIL □

Fig. 92. Distribution of Thalassiothrix longissima, survey I,
March 1950. Expressed as a percentage of the total diatoms.
(Station numbers are shown in Fig. 1.)

succeeded by R. styliformis, more or less co-dominant with varying proportions of R. alata, these last
being superseded in the extreme north of the area studied by Dactyliosolen mediterraneus.

In Fig. 95 an attempt has been made to demonstrate another aspect of distributional study, the
development of a localized flora where the distinctive offshore and inshore populations most nearly
approached each other, near the northern limits of the rich upwelling zone in autumn. The distribu-
tions shown are estimated numbers of Planktoniella sol, regarded as the characteristic offshore form ;
Goniaulax spinifera, the dinoflagellate predominating in the intervening ' patch ' j1 and the estimated

1 The word ' patch ' is here used in its generally accepted sense to describe the area where Goniaulax predominated. It is
not intended to denote exceptional population density as in descriptions of visibly discoloured areas resulting from water-

MICROPLANKTON 251

group totals for the chaetocerids, with their pronounced maximum of development inshore. A degree
of overlapping in the horizontal plane seems reasonably accounted for by vertical layering, for which
there is some hydrological evidence. The point cannot be established from plankton data alone.

The presence of the Goniaidax patch just where the intrusive tongues of oceanic water extend farthest
inshore seems strongly suggestive of mixing between the two types of surface-water. Some time-lag-
general slowing of dispersive agencies— must also be postulated, to permit development of the third

20°

25°

S
O

U
T
H

30*

NIL □

SURVEY
1

I0«

15'

EAST

Fig. 93. Distribution of Thalassiothrix longissima, survey II,
September-October 1950. Expressed as a percentage of total
diatoms. (Station numbers are shown in Fig. 2.)

20°

25°

S
O
U

T
H

30°

EAST

Fig. 94. Distribution of the Soleniineae expressed as a per-
centage of the total diatoms, survey II, September-October
1950. (Station numbers are shown in Fig. 2.)

distinctive localized type of flora. Much of our evidence points to the prevalence of the conditions
required for this immediately prior to the autumn survey. The relatively high stability of the surface-
layers, temperature and salinity distribution, and several features of the plant population combine to
show that upwelling activity was then much reduced, and the plant succession at or just beyond its
peak. Relatively ' old ' surface-water from inshore, such as these conditions imply, should mix more
readily with the offshore water than would that cooled by recent upwelling.

bloom formation. Goniaulax spp. have been known to cause water-bloom elsewhere, but such discoloured water as we were
able to sample during these surveys was caused by other organisms. This does not preclude the probability that it may
sometimes form blooms in this area — perhaps at other seasons.

252

DISCOVERY REPORTS

IO EA5T

IO EAST

Fig. 95. Distribution of (A) Planktoniella, (B) Goniaulax, and (C) Chaetoceros between Mowe Point and Sylvia Hill, survey I,
March 1950. Where there is no shading none was recorded. The lightest shading represents estimates of < io4 per net
haul, the next io4~5, and so on.

Observations on discoloured water

Large areas of the sea near Walvis Bay were discoloured ' blackish ' by diatoms during our first survey,
the general appearance being dark green to black, and opaque, very similar to that described in arctic
regions by Brown (1868) and found by him to be due to diatoms also. In the Benguela current we
found the inshore chaetocerids, especially Chaetoceros didymum and Aster ionella japonica, to be the
species chiefly responsible. Within this same region, however, were many more localized brownish or
khaki-coloured discolorations, forming irregular bands and streaks roughly parallel with the coast,
sometimes associated with foam streaks and lanes of dead and dying macroplankton — mainly
ctenophores and salps — at the surface. A minor fish mortality had occurred near Walvis Bay just
before we got there.

Three samples from some of these more strikingly discoloured waters were obtained off Sandwich
Harbour (about 220 30' S. and 10 sea-miles offshore). Subsequent detailed microscopic examination
of these yielded the results shown in Tables 18, 19 and 20.

MICROPLANKTON

253

Table 18. Sample A of discoloured water near Sandwich Harbour. Collected at 13.45 nr- on 9 March
lg^o. Mixed, fractionized and diluted so that contents of 2-5 ml. could be counted direct, several counts
being summed. Factor to reduce numbers to cells/ml. x 0-4

Estimated

x 0-4^ esti-

area in

mated

optical

Estimated

No.

no. of

section

volume

% by

%by

% by

Species or category

counted

cells /ml.

y?jml.

jx3jml.

number

area

volume

Peridinium triquetrum

387

ISS

44.795

217,000

40-38

20-53

13-9

Asterionella japonica

324

130

15,600

286,000

3379

7-15

18-3

Prorocentrum micans

137

33.88o

374,000

I4-33

15*53

23-9

Thalassiosira spp.

28,000

292,000

5'44

12-83

187

Stephanopyxis turn's

17,280

210,000

i-67

7-92

J3-4

Peridinium spp.

74,400

150,000

1-67

34-09

Chaetoceros didymum

1,200

9,000

0-63

o-55

o-6

Eucampia zoodiacus

1,500

8,000

0-63

0-69

°-5

Nitzschia delicatissima

200

0-42

0-03

o-o 1

Chaetoceros curvisetum

300

2,200

0-31

0-14

o-i

Small 'Pennatae'

—

700

0-21

—

0-04

Staphylocystis sp.

1,200

0-21

o-55

o-i

Copepod egg

—

12,000

o-io

—

o-8

Small Dinophyceae non det.

—

500

0-21

—

0-03

Total Dinophyceae

544

218

1 53.475

742,700

56-80

70-42

47-53

Total diatoms

411

164

64,252

808,100

43-10

29-44

5I-65

Other organisms

300

12,000

o-io

0-14

0-80

Total microplankton

95°

383

218,227

1,562,800

—

The area in optical section of the total organisms in 1 ml. of this sample, when spread over a Sedgwick-Rafter counting-
chamber, would thus be about 500 Whipple's International Standard Units, or o-2 parts per thousand, and their volume
some 1-5 parts per million of water. (The Sedgwick-Rafter cell, 5x2 cm. in area and with sides 1 mm. deep, holds 1 ml. of
fluid spread over an area of 10 cm. (= io9/x2). One W.I.S.U. is a square 20 /x on one side (= 400 /r2). One ml. = (io12/x3).)

Table 19. Sample B of discoloured zvater near Sandwich Harbour. First of two collected at 14.10 hr. on
9 March 1950. Noted as ' Khaki coloured water, reddish at a distance '. 1J8 of 10 ml. of the well-mixed
sample, i.e. of 0-55 ml., examined direct by drop method and counts summed. Factor to express results as

u-L/ur ViX. fiuo. uciu /ru.

/\ J. O

Estimated

xi -8 ^esti-

area in

mated

optical

Estimated

No.

no. of

section

volume

%by

Species or category

counted

cells/ml.

fjfi/ml.

\x?\ml.

number

areas

volume

Peridinium triquetrum

1.530

2,754

795,906

3,855,6oo

86-55

80-29

55-34

Asterionella japonica

122

220

26,400

484,000

6-91

2-66

6-95

Eucampia zoodiacus

33,750

180,000

1-41

3-4°

2-58

Small 'Pennatae'

4,100

32,800

1-29

0-41

0-47

Thalassiosira spp.

56,000

568,000

1-26

5-65

8-15

Peridinium spp., small

18,000

813,600

113

1-82

n-68

Prorocentrum micans

11,088

115,200

o-57

112

1-65

Stephanophyxis turris

37,44o

455,00°

0-41

3-78

6-53

Chaetoceros constrictum

4,375

22,400

0-22

0-44

0-32

Tintinnidae

3,600

400,000

0-13

0-36

5-74

Nitzschia delicatissima

200

0-06

o-oi

Cast skins of nauplii

600

40,000

0-06

o-57

Total Dinophyceae

1,560

2,808

824,994

4,784,400

88-25

83-23

68-67

Total diatoms

204

368

162,137

1,742,400

11-56

16-35

25-01

Other organisms

4,200

440,000

0-19

0-42

6-31

Total microplankton

1,767

3.182

99!.33!

6,966,800

—

Area in optical section

of organisms

in 1 ml. in

Sedgwick-Rafter

counting-chamber

: about

2478 W.I.S.U.

or nearly

1 part per thousand. Volume nearly 7 parts per million.

17-2

254

DISCOVERY REPORTS

Table 20. Sample C of discoloured water near Sandwich Harbour. Collected immediately after Sample B
{Table lg), but in a streak of noticeably more turbid water 'Khaki-coffee coloured'. 0-25 ml. of well-
mixed sample examined by drop method and counts summed. Factor to express results as approx. nos.

cells /ml. x 4

Estimated

x 4 === esti-

area in

mated

optical

Estimated

No.

no. of

section

volume

%by

% by

Species or category

counted

cells/ml.

\j?\ml.

fi3lml.

number

area

volume

Peridinium triquetrum

1.363

5.452

1,575,628

7,632,800

88-36

76-13

61-12

Asterionella japonica

306

36,720

673,200

4-96

1-77

5-39

Small 'Pennatae'

192

19,200

153.600

311

0-93

1-23

Peridinium spp.

258,000

904,000

065

12-47

7-24

Thalassiosira spp.

50,400

511,200

0-58

2-43

4-09

Chaetoceros constrictum

17,500

89,600

o-45

0-85

0-72

Stephanopyxis turris

69,120

840,000

0-39

3-34

6-73

Nitzschia delicatissima

864

2,400

0-39

0-04

0-02

Chaetoceros compression

8,800

40,000

0-32

0-42

0-32

Prorocentrum micans

9.856

102,400

0-26

0-48

0-82

Chaetoceros dichaeta

4,800

108,000

0-19

0-23

o-86

Eucampia zoodiacus

6,000

32,000

0-13

0-29

026

Tintinnidae

7,200

800,000

0-13

o-35

6-40

Rhizosolenia setigera

5,600

600,000

0-06

0-27

4-80

Total Dinophyceae

i»377

5.508

1,843,484

8,639,200

89-27

89-08

69-18

Total diatoms

161

654

219,004

3,050,000

10-58

10-57

24-42

Other organisms

7,200

800,000

0-13

o-35

6-41

Total microplankton

i»54°

6,170

2,069,688

12,489,200

—

Area in optical section of the organisms in 1 ml. in Sedgwick- Rafter counting-chamber: about 5160 W.I.S.U., or 2 +
parts per thousand. Volume about 12-5 parts per million.

These tables allow comparisons, not only of the constituents, but also of the relative density of the
microplankton in each sample in terms of numbers, area in optical section, and volumes, per millilitre.
It is seen that sample C (Table 20) was by any standard nearly twice as dense as B. Sample A was
much thinner, but the ratio varied little in terms of numbers, area or volume.

As to the constitution of the samples it appears that the small dinoflagellates Peridinium triquetrum
and Prorocentrum micans were the main constituents of the thinnest of these samples (Table 18).
with quite a high proportion of Asterionella and other inshore diatoms. The two richer samples
(Tables 19 and 20) show a definite 'bloom' of Peridinium triquetrum, the other constituents providing
less than 12% of the total number of organisms estimated.

Peridinium triquetrum, a neritic species of very wide distribution, has been recorded 'blooming' in
association with a fish mortality on at least one previous occasion, at Rostock in the Baltic on
10 October 1917 (Lindemann, 1924, who called it by its old name Heterocapsa triquetra). Linde-
mann's plankton observations were only made after a considerable search for other possible causes
of the catastrophe had proved fruitless. The Peridinium triquetrum was co-dominant with Krypto-
peridinium foliaceum and other microplanktonic organisms were present only in quite insignificant
proportions.

Our Benguela current findings, added to Lindemann's observations, might seem to suggest
Peridinium triquetrum as a probable ' cause ' of the Walvis Bay mortalities, but it has to be remembered
that in both instances the mortality had begun before the observations on the bloom were made. The
bloom may or may not have been present when the fish were killed. Braarud (1945) has shown that
very high production of P. triquetrum (and sometimes of Prorocentrum also) may occur in heavily

MICROPLANKTON 255

polluted waters, inimical to most other marine plankton organisms, in the inner Oslo Fjord. Thus it
even seems possible that these blooms might be the result, rather than the cause, of the mortalities.

The seemingly conflicting statements on the nature of the discolorations so often seen near Walvis
Bay do seem to be partially resolved by our observations. Gilchrist's (1914) early insistence upon
the vast proliferations of diatoms in the area are amply confirmed. Then to the dinoflagellate blooms
described above we can add one of ciliate Protozoa (considerably to the northward but still within
the Benguela current area) which was sampled at the end of the second survey. Further we have little
doubt that Marchand's contention that blooms due to Noctiluca miliaris also occur there will eventually
be vindicated.1

In the past each commentator has tended to assume that the most recently identified bloom-forming
organism was responsible for all the other macroscopically similar visual effects reported from the
area. This was natural enough when direct observations were few and often obscurely recorded. The
point which we can claim from our results is that blooms — visible discolorations — due to widely
differing types of organisms may occur (mostly at different times no doubt) within the same relatively
small sea area.

The estimates of area and volume of the bloom-forming organisms in Tables 18-20 have been
made from the means of numerous measurements and approximation to the nearest geometrical
figure. They do not pretend to be precise, but are unlikely to show positive error. They are given here
in the hope that the relative quantities of plant substance represented by counts of the various species
may be better appreciated with their aid. The areas in particular may interest those familiar with
Whipple's ([1889], 1908) concept of the International Standard Unit, a square 20 /i on the side
viewing the organisms in optical section, which was found very useful in practical limnological work.
These findings suggest that it could be very useful in marine work also, but it has to be borne in
mind that it is only in the study of these blooms (or in cultures) that the marine plankton worker ever
encounters populations approaching the densities shown in Tables 18-20. Usually he has to deal
with populations sparser by at least one order of magnitude than these. It is in fresh waters that such
concentrations are frequently met with.

From the volumes the relative size relations of the more important plants found in these samples
can be computed, with the results shown in Table 21. This shows, for example, that here one cell of
the diatom Stephanopyxis turris was roughly eleven times as big as one cell of Chaetoceros constrictum,
and twenty-five times as big as one of the dominant dinoflagellates, Peridinium triquetrum. Obviously
it is important to establish dominance by methods going further than the counts alone when possible.
Lohmann (1908) made an attempt in this direction by analogous methods in Kiel Bay, but generally
speaking the range of size variation, even within single species of phytoplankton organisms, is so great
that application of the method to large series would demand recalculation of volume factors every
few samples, and the increase in time and labour involved would make it quite impracticable.

An intense red discoloration observed close inshore (WS 1107) in 130 05' S. at the conclusion of
the second survey proved to be due to swarming of a ciliate protozoan Cyclotrichium meunieri Powers
(probably synonymous with Halteria rubra Lohmann = Mesodinium rubrum Lohmann (Apstein).)
Large-scale discolorations caused by this organism had previously been seen in the waters round
Cape Peninsula (Hart, 1934).2 When swarming this animal distorts itself or bursts spontaneously in

1 Trichodesmium thiebautii, the Cyanophycean that so often forms blooms in many parts of the tropical and subtropical
Atlantic, probably does so in the Benguela current area on occasions. It was dominant in some of our poorer plankton hauls,
but we have not yet seen it there in bloom-forming quantities.

2 An unfortunately premature communication, missing Lohmann (1908), Apstein (1908), Paulsen (1909) and even Darwin
(1839). I tried to rectify these mistakes in a second letter published in 1943, but cannot blame myself for having missed
Powers (1932). Our ship left Europe in 1933 when his work had barely had time to reach European libraries, and being

256 DISCOVERY REPORTS

any quantity of water small enough to permit one to examine it microscopically, the process being
accentuated in greater or less degree by addition of all the narcotics or fixatives tried hitherto. Bary
and Stuckey (1953) found very dilute hydrogen peroxide the best narcotic, leaving a larger minority
of relatively little distorted specimens available for subsequent fixation. When the ciliates burst many
of the coloured 'platelets' (Lohmann)1 are extruded. The enormous numbers of these in the sample
from WS 1 107 were observed in the field by Clarke and Currie, and their likeness to Hematococcidae
noted. The preserved sample, however, showed the characteristically shrunken remains of many of
the ciliates that had not burst (cf. Lohmann, 1908, fig. 7, no. 53, p. 201), so many indeed, that the
discoloured water must have contained not less than 13,370 per ml. It seemed pointless to attempt
counting of the freed 'platelets' since the vast majority had unquestionably been aggregated (in
varying numbers) within ciliates before the sample was taken. A small Gymnodinium sp., one other
small dinoflagellate and a Coscinodiscus sp. were present in very small numbers (up to 7 per ml.).

Table 21. Size inter-relations of organisms from the samples taken off Sandzvich Harbour, 9 March 1950.
Selected to cover the dominants and species covering the extremes of variation in volume; others omitted

Chaeto-

Peri-

Rhizo-

Thalas-

Chaeto-

Proro-

ceros

dinium

Approx. volume

solenia

Stephano-

siosira

ceros

centrum

con-

trique-

(estimated) in /x3

setigera

pyxis turris

spp.

dichaeta

micans

strictum

trum

(1 fj? = io-liml.)

Rhizosolenia setigera
Stephanopyxis turris
Thalassiosira spp.
Chaetoceros dichaeta

10J
i6i

loi

i6i
4

23
6

2
1*

47
11

4*
3

107

150,000

35.00°

14,200

9,000

Prorocentrum micans
Chaetoceros constrictum

23
47

2
1

6,400
3,200

Peridinium triquetrum

107

1,400

Dense swarms of this ciliate have thus been seen near the two ends of the region where the Benguela
current is best defined. It seems unlikely from what is known of its proclivities elsewhere, that the
conditions of negative anomaly of temperature and salinity in between would prove exclusive to it.
Probably, therefore, before long some more fortunate observer will be able to add it to the list of
diverse forms now known to give rise to visual discolorations there at various times.

The distinction between offshore and inshore diatom floras

Yet another array of the data, based upon arbitrarily selected distance limits, serves to show up the
distinctive features of the flora of the inshore and offshore waters during the two surveys, providing
a basis for ecological characterization of the species within each of the main diatom groups. Some
repetition of points made in discussing distribution at group level is involved here, but seems to the
writer (T.J.H.) to be unavoidable if the apparent anomalies due to the cosmopolitan and panthalassic
species are to be made clear.

The arbitrary limits first chosen were: stations within 40 miles from the coast regarded as within
an inshore region, and stations more than 100 miles from the coast, regarded as definitely oceanic or

without fore-knowledge that we were to encounter his ciliate more than a year later, we could hardly be expected to have
included it in the small working library carried at sea! I have hoped to clear up some of the misunderstandings following
my 1934 letter in a separate publication, but the topic seems dangerous! (T.J.H.).

1 These were described as 'most probably symbiotic algae', and given the name Erythromonas haltericola by Lohmann
(1908). Concerning them also Apstein (1908) wrote 'this is perhaps the alga living symbiotically in Mesodinium rubrum' .
I mentioned them as 'Coloured granules some 4/i in diameter, possibly symbiotic zoochlorellae' in ignorance of the earlier
work, though this may now seem to be incredible (T.J.H.).

MICROPLANKTON 257

offshore. It then became clear that the results from the wide intermediate or 'outer shelf zone
(40-100 miles from the land), besides yielding the obvious intermediate averages, also showed up the
extent to which surface-waters of the two more distinctive types were overstepping the arbitrary
limits chosen on each of the two surveys. The full value of this feature could only be realized by
considering individual species on each line of stations as we have already treated the main groups.
Though this is impracticable here it still seemed worthwhile to include average values for the arbitrary
'outer shelf zone, despite the masking effect of the 'averaging' process in the following tables, for the
reason given above.

For this special purpose the anomalous results from the Orange river line were not considered,
and this leaves thirty-two stations at repeat positions on each of the two surveys for comparison.

Table 22 shows the average estimated diatom totals per net haul, and the average totals and per-
centages for each main group as previously defined, when the data are arrayed in this fashion. It also
provides in effect a crude summary of the line-upon-line treatment of main group-distribution already
given. It is essential that the relative quantities indicated should be kept in mind if the percentages
for species within each group, given in Tables 13-17, are to be properly understood.

Table 22. Average estimated diatom totals, with average numbers and percentages of the main diatom

groups, when the data are grouped according to distance from the coast as shown. (Results from the Orange

river line excluded)

Average

estimate

of total Average Average Average Average Average

diatoms Discineae Biddulphiineae Chaetoceraceae Soleniineae ' Pennatae'

per net , * , , * , , * , , * * , — * * ,

haul Numbers % Numbers % Numbers % Numbers % Numbers %

Inshore stations <40 sea miles from the coast

First survey 85,157,491 2,836,753 3-33 1,528,631 i-8o 68,024,177 79-88 877,582 1-03 11,890,348 13-96

(autumn)
Second survey 65,979,818 884,173 1-34 72,400 o-n 58,486,700 88-64 146,455 0-22 6,390,090 9-68

(spring)

'Outer shelf stations 40-100 sea miles from the coast

First survey 15,712,563 217,934 1-39 14,672 0-09 14,673,800 93-39 80,419 051 725-738 4'02

(autumn)
Second survey 2,158,972 82,025 3'8° 225 o-oi 811,229 37'57 727»°9I 33"6S 538,402 24-94

(spring)

Offshore stations > 100 sea miles from the coast

First survey 156,287 20,972 13-42 None 22,480 14-38 31,510 20-16 81,323 52-03

(autumn) seen

Second survey 779,740 17,880 2-29 None 139,260 17-86 515,400 6610 107,200 13-75

(spring) seen

From Table 22 it appears that:

(1) the Discineae were of minor importance offshore during the first (autumn) survey. Elsewhere
they formed but a small proportion of the total diatoms, their greater numbers inshore notwith-
standing during both surveys.

(2) The Biddulphiaceae were of very minor importance inshore, mainly in autumn. Very small
quantities of this group were observed on the 'outer shelf, and none at the offshore stations.

(3) The Chaetoceraceae were strongly dominant inshore at both seasons, rather more so in spring
than in autumn. They were also strongly dominant on the 'outer shelf in autumn, but much less so
during spring. Offshore they were outnumbered by other groups at both seasons.

(4) The Soleniineae were the dominant group offshore during spring. They ranked second to

258 DISCOVERY REPORTS

the chaetocerids on the 'outer shelf in spring, and to the 'Pennatae' offshore in autumn. Inshore
they were relatively unimportant at both seasons.

(5) The 'Pennatae', though generally much less abundant than the chaetocerids, ranked second
to that group at the inshore stations during both surveys. They were rather more important in autumn
than in spring right inshore, but this trend was reversed on the 'outer shelf. Offshore the group was
relatively much more important in autumn than during spring, although slightly more abundant in
the richer spring catches.

Table 23. Relative importance of the group Discineae, and percentage of the several species, within the
group. Results arrayed according to distance from the land as shown, omitting those from the Orange
river line

Inshore

< 40 sea-miles

from land

' Outer shelf

40-100 sea-miles

from land

Offshore

>ioo sea-miles

from land

(a) Average total diatoms

(b) Average total Discineae
b\a as percentage

First survey
(autumn)

85,!57,49i

2,836,753

3-33

Second survey
(spring)

65,979,8i8
884,173
i-34

First
survey

I5,7I2,563
217,934
i-38

Second
survey

2,158,972
82,025
3-80

First
survey

156,287
20,972
13-44

Second
survey

779-74°
17,880
2-29

Average total for each category as per-
centage of the average total for the
group (M category/6 as %)

Skeletonema costatum

Stephanopyxis turris

Thalassiosira condensata

T. excentrica

T. hyalinum

T. rotula

T. subtilis

Thalassiosira spp. non det.

Bacterosira fragilis

Coscinodiscus gigas

C. janischii

Coscinodiscus spp. non det

Actinocyclus spp. non det.

Planktoniella sol

Hemidiscus cuneiformis

Actinoptychus senarius

Asterolampra spp. non det.

Asteromphalus heptactis

—

i-56

I-I5

—

16-0

6-46

2-52

12-12

2-8

—

0-92

19-5

—

11-41

—

0-16

13-8

—

27-2

50-43

70-63

11-82

I3-3

3473

275

23-20

0-03

—

<o-oi

—

o-34

5-61

0-20

I4-85

o-oi

—

0-02

o-u

9-84

32-I5

0-03

o-oi

0-46

<o-oi

0-15

o-oi

0-64

—

0-41

—

0-08

o-49

0-40

4-76

45'0

0-3

54-7

6-o
30-2

47-3

6-7

Table 23, which shows the relative importance of the various Discineae when the data are grouped
in this fashion, provides strong evidence of the neritic or inshore habit of most of the species. Though
several extended to the outer shelf, eleven out of the eighteen categories were not seen farther offshore.
Planktoniella sol was clearly the most essentially oceanic species. Although sufficiently adaptable to
occur inshore its numbers increased very markedly with increasing distance from land during both
surveys. The remainder of the scanty offshore representation of the group consisted chiefly of more
panthalassic, but equally cosmopolitan, species like Thalassiosira excentrica and T. subtilis.

The most important Discineae inshore were Stephanopyxis turris and various species of Thalassio-
sira. They were most prominent in autumn (or late in the succession) while the less numerous forms
provided greater relative proportions of the group totals in the smaller spring catches (e.g. Asterom-
phalus heptactis).

MICROPLANKTON 259

The Biddulphiaceae (Table 24) were very sparsely represented in the area surveyed. Inshore, in
autumn, Eucampia zoodiaais was of some slight importance, and just extended on to the outer shelf
area. There, however, Cerataulina pelagica formed a slightly higher proportion of the very small group
average. Eucampia zoodiaais was not observed during the spring survey, when Biddulphia longicruris
provided the bulk group totals. Biddulphiaceae were not observed more than 100 miles offshore during
either survey, though one of the species recorded, Hemiaidus hauckii, has been seen far out in the
South Atlantic on other occasions, and should probably be regarded as an oceanic form.

Table 24. Relative importance of the group Biddulphiaceae, and percentage of the several species within
the group. Results arrayed according to distance from the land as shown, omitting those from the Orange
river line

Inshore

' Outer

she Ij '

Offshore

<40 sea-miles

40-100 :

sea-miles

>ioo sea

-miles

from

land

from land

1 '
First survey

Second survey

First

Second

First

Second

(autumn)

(spring)

survey

85,157,491

65,979,818

15.712,563

2,158,972

156,287

779.74°

1,528,631

72,400

14,672

225

—

i-8o

o-i 1

0-09

o-oi

9905

—

i-66

0-95

53-04

—

0-02

—

i-3§

—

100

—

98-32

—

45-58

—

(a) Average total diatoms

(b) Average total Biddulphiaceae
bja as percentage

Average for each category as % of (b)
Biddulphia longicruris
Cerataulina pelagica
Triceratium favus
Hemiaidus hauckii
Eucampia cornuta
E. zoodiacus

The tremendous local importance of the Chaetoceraceae is clear from Table 25, which also illu-
strates the very cosmopolitan nature of the species of this family. All of those which we were able to
identify are widely known from other regions, ranging from ' boreal ' to ' warm temperate ', with some
which extend into truly tropical surface-waters as well.

Within this area most of them were essentially neritic — inshore and outer shelf species — and of
these a majority were more abundant in autumn, or late in the succession, than in spring. Most
important of all, however, were three panthalassic species which must be among the most widespread
and abundant of all marine plankton diatoms : Chaetoceros compression, C. constrictum and C. curvi-
setum. The first two of these were almost equally abundant at both seasons, while C. curvisetum, the
most numerous of all the diatoms according to these estimates, showed a distinct maximum in spring,
though vast numbers had been found in the autumn samples also.

Of the more strictly neritic species C. didymum was the most abundant, especially in autumn, when
vast numbers of the very characteristic resting spores were present. C. subsecundum and most of the
other neritic species of lesser but still considerable local importance, for example, C. affine, C. costatum,
C. debile, C. teres, C. tetras, showed a similar time distribution. C. strictum, however, showed a strong
inshore maximum during the spring survey.

The most abundant and widespread of the oceanic species, C. convolutum, showed a spring maxi-
mum here. So also did two oceanic forms of lesser importance in these samples : C. atlanticum and
C. peruvianum.

The ' ecological characterization ' of the species of this most important and difficult genus of marine
plankton diatoms arrived at by the late Professor Gran, through continued efforts towards improving
his system of ' plankton elements ' as applied in the northern hemisphere (Gran in Murray and Hjort,
1912; Gran and Braarud, 1935), can thus far be extended to this southern area without serious

18 DHJC

26o DISCOVERY REPORTS

discrepancy. Two well-known cosmopolitan species, however, were found to be distributed here rather
differently from what might have been expected from their previously known dispositions elsewhere.
C. lorenzianum, usually regarded as a neritic form, here reached its greatest relative importance in the
offshore samples, with a strong spring maximum. Conversely C. decipiens, one of the most widespread
of all oceanic species, was more plentiful here inshore in spring than it had been offshore during the
autumn survey.

Table 25. Relative importance of the group Chaetoceraceae, and percentage of the several species ivithin
the group. Results arrayed according to distance from the land as shown, omitting those from the Orange
river line

Inshore

'Outer

shelf

Offshore

< 40 sea-miles

40-100 sea-miles

> 100 sea-miles

from

land

from

land

from

land

First survey

Second survey

First

Second

First

Second

{autumn)

(spring)

survey

(a) Average total diatoms

85,157,491

65,979,818

15,712,563

2,158,972

156,287

779.74°

(b) Average total Chaetoceracea

68,024,177

58,486,700

14,673,800

811,229

22,480

139,260

bja as percentage

79-87

88-64

93HI

37-58

14-40

17-86

Average for each category as percentage

of the average total for the group (M

category/6 as %)

Chaetoceros affine

0-12

1-67

1-32

i-oo

—

C. atlanticum

—

<o-oi

3-09

—

3-66

C. compression

14-18

18-70

42-92

3791

26-69

17-23

C. constrictum

21-76

11-65

I3"59

22-o6

—

23-48

C. convolution

o-oi

<o-oi

°-33

3-93

io-68

11-25

C. costatum

0-79

—

i-io

0-19

—

C. curvatum

—

o-oi

—

C. curvisetum

22-12

45-67

3-57

692

56'94

2197

C. debile

460

0-41

0-45

—

C. decipiens

0-36

5-05

0-08

5-2i

4-89

—

C. didymum

5-93

1-89

1-96

0-98

—

1-29

C. didymum (resting

spores)

»3-57

0-02

6-99

—

C. difficile

1 -63

i*3S

5-48

1-48

—

1-48

C. holsaticum

—

o-34

—

C. imbricatum

—

0-25

—

C. laciniosum

<o-oi

0-02

—

C. lorenzianum

0-31

0-85

—

5-17

—

17-92

C. peruvianum

0-05

0-29

—

o-6o

C. pseudocrinitum

0-13

6-05

—

C. sociale

—

0-39

0-37

—

2-58

C. strictum

1-84

10-93

3-98

2-09

—

C. subsecundum

6-28

0-30

1-20

968

—

C. subsecundum (resting spores)

0-22

—

C. teres

1-04

<o-oi

3-98

—

C. tetras

o-ii

o-66

2-37

—

C. van heurckii

4'9S

o-io

I-39

—

o-So

—

Chaetoceros spp. non

det.

—

2-57

—

This evidence of a more panthalassic trend than was hitherto suspected for these two species, in a
region of exceptionally steep temperature gradients and rapid changes in conditions of the milieu, is
not surprising. Indeed, the general conformity of the majority of the genus to the distributional
pattern that might have been predicted from their known proclivities elsewhere, seems even more
remarkable to me under these conditions, which seem quite sufficient to account for the occurence of
both warm-water and cold-water forms together within a limited area. When the need for a reasonable

MICROPLANKTON 261

amount of elasticity in the application of the ecological terms is borne in mind, the value of the earlier
work seems to me most amply justified (T.J.H.).

Within the group Soleniineae, consisting almost wholly of holoplanktonic cosmopolitan forms, the
difficulty involved in any attempt at further ecological characterization is augmented by the almost
completely panthalassic nature of some of the most important species. This results in some species
showing maximum importance offshore under oceanic conditions in spring, but inshore under neritic
conditions in autumn or vice versa. The compromise implicit in the word panthalassic seems as far as
one can go in any attempt at brief summary of their distributional tendencies !

Table 26. Relative importance of
group. Results arrayed according
river line

the group Soleniineae, and percentage of the several species zvithin the
to distance from the land as shown, omitting those from the Orange

Inshore

' Outer

shelf

Offshore

<40 sea-miles

40-100 sea-miles

> 100 sea-miles

from land

from

land

from

land

First survey

Second survey

First

Second

1
First

Second

(autumn)

(spring)

survey

(a) Average total diatoms

8S.iS7.491

65,979,818

15.712.563

2,158,972

156,287

11W\°

(b) Average total Soleniineae

877.582

H6.45S

80,419

727,091

2>l>5l°

515,400

bja as percentage

1-03

0-22

0-51

33-68

20- 1 6

66-io

Average for each category as percentage

of the average total for the group

category jb as %)

Bacteriastrum hyalinum

0-21

—

1-17

—

B. varians

0-16

—

0-02

—

Rhizosolenia alata

1-83

0-41

36-78

21-11

36-92

8-67

R. cylindrus

—

0-02

—

R. fragillissima

—

0-58

—

R. hebetata

9-34

0-76

49-94

5-4°

49-62

4-85

R. imbricata

1-08

0-19

163

2-II

3-8i

2-25

R. robusta

0-05

—

006

R. setigera

—

66-29

—

3-09

—

0-12

R. simplex

—

5-80

0-67

9-65

—

R. stolterfothii

074

—

R. styliformis

0-13

o-6o

o-45

30-25

—

74-69

Guinardia sp. non det.

—

0-09

—

Leptocylindrus danicus

15-88

4-66

2-72

—

Dactyliosolen mediterraneus

70-53

2-23

—

36-90

—

919

Corethron criophilum

0-05

24-86

0-77

°-43

—

0-23

A few species, notably Leptocylindrus danicus with its maximum late in the succession, were definitely
limited to the neritic samples in both series. Rhizosolenia setigera, seen only during the spring survey,
was important inshore at that season.

The most completely cosmopolitan species, that helped to render this group dominant offshore in
spring and of considerable importance there in autumn also, should probably be regarded as essentially
oceanic, but so adaptable that they may attain higher numbers among the vastly heavier catches of
other forms in enriched coastal waters on some occasions. A similar difficulty is found when one
attempts ecological classification of some of the dominant phytoplankton species of antarctic surface
waters (Hart, 1942).

In the Benguela current area the important panthalassic solenoids were: Rhizosolenia alata and
R. hebetata, especially late in the succession inshore, but also augmenting the group's spring maximum
offshore; R. styliformis, here showing a more distinct oceanic trend and spring maximum; and

18-2

262 DISCOVERY REPORTS

Dactyliosolen mediterraneus. This last provides the greatest enigma, being found in great numbers
inshore during the first (autumn) survey, but also among the dominants on the outer shelf and offshore
(especially in the northern part of our area) in spring. It is possible that more restricted temperature
requirements may account for this anomaly if the spring temperatures inshore are suboptimal for this
species. Conversely, Corethron criophilum, undoubtedly an oceanic form in most of its phases, here
showed a very definite maximum inshore in spring, which might be explained by 'preference' for
lower temperatures.

The ecological relationships of the ' Pennatae ' (Table 27) at group level are not very clear, chiefly
because it is an arbitrary ' unnatural ' assemblage of the diverse ' reversionary plankton forms ' with
sundry tychopelagic species, introduced solely to assist in concentrating the data to within manageable
proportions. At the specific level, however, most of them can be seen to conform to definite distribu-
tional trends much more clearly than most of the solenoids.

Fragilaria karsteni, Asterioriella japonica and the rarer tychopelagic species all had a definitely inshore,
neritic distribution. Fragilaria karsteni was most abundant in spring and Asterionella japonica in
autumn. Thalassiothrix longissima was an offshore form with a spring maximum, and so in the main
was Fragilaria granulata, which never overlapped its congener.

The only important ' Pennatae ' not clearly assignable to one of the distributional trends that we now
feel to be recognizable (somewhat dimly, perhaps) are Nitzschia delicatissima and N. seriata. These
are among the most ubiquitous, cosmopolitan, panthalassic diatoms known, as all marine plankton
workers must agree. Here they were prominent at all distances from land especially in spring.
N. seriata was the more important inshore, while N. delicatissima showed maximum relative importance
in the scanty offshore catches in autumn, though not nearly so numerous there as it was on the 'outer
shelf during both surveys.

Table 27. Relative importance of the group Pennatae, and percentage of the several species within the
group. Results arrayed according to distance from the land as shozvn, omitting those from the Orange
river line

{a) Average total diatoms
{b) Average total 'Pennatae'
bja as percentage

Average for each category as percentage
of the average total for the group {M
category jb as %)

Fragilaria granulata

F. karsteni

Asterionella japonica

Thalassiothrix longissima

Thalassionema nitzsch hides

Striatella sp. non det.

Navicula membranacea

Navicula spp. non det.

Pleurosigma capense

Pleurosigma sp. non det.

Nitzschia closterium

N. delicatissima

N. lojigissima

N. seriata

Inshore

<40 sea-miles

from land

'Outer shelf

40-100 sea-miles

from land

Offshore

> 100 sea-miles

from land

First survey
{autumn)

85,157,491

11,890,348

13-96

Second survey
{spring)

65,979,818

6,390,090

9-68

First
survey

I5.7I2,563
725.738
4-62

Second
survey

2,158,972
538,402
24-94

First
survey

156,287

81,323
52-03

1
Second

survey

779,74°
107,200

!375

12-77

64- 1 5
0-06

0-04
o-oi

0-02

o-8i

0-31

0-06

2177

o-iS

48-95

5-42
i-54
4-35

0-03
0-17
o-oi

8-24

0-06

995

—

0-21

62-78

6-oi

6-12

18-60

o-oi

i-95

—

0-08

3!-24

604

3-36

29-04
i-68

118

0-06

31"

2-37
7-96

0-23
1696

0-52

11-80
55-04

0-78
19-36

9-4°

45-43

1-92

3973

microplankton 263

The cosmopolitan distribution of marine plankton diatoms and the
'ecological' characterization' of the more important species from

the benguela current

A further selection of the most important or typical diatom species observed within the area permits
concise illustration of the extremely cosmopolitan distribution of these in other regions, so that it is
the relative importance of the various forms rather than their mere presence and absence that must
be studied before relationships between the floras and their 'conditions of existence' begin to be
perceptible. This further selection has been used to give examples of the brief 'ecological charac-
terizations ' of species, on Gran's lines, that are so helpful in the attempt to perceive some order in the
ever-changing phytoplankton communities.

Table 28 shows reported occurrences of these typical Benguela current species in various other
regions, ranging from the North Atlantic to the antarctic zone of the southern ocean. Some of these
have received much less complete coverage than others, and yet other regions might be added,
especially around Japan (cf. Aikawa, 1936), but the table is surely adequate to show the very cosmo-
politan distribution of most of the species. This fact was generally recognized by most of the earlier
phytoplankton workers (cf. Gran and Braarud, 1935, and Aikawa 1936, among others), but it probably
became so obvious to them that they rarely sought to stress it. The species listed in Table 28 are
selected on the ground that we have observed them to be dominant, typical or otherwise important in
the Benguela current, and without reference to their occurrence elsewhere. But there is no reason to
suppose that the less important or typical species — except perhaps the neritic ones (see below) — are
any more restricted in their distribution. At least it can be said that of all the eighty-two species
identified from the Benguela area so far, none are ' new to science '.

The supreme importance of the inshore chaetocerids (of the group Hyalochaete) in the upwelling
regions, can only be fully appreciated when quantitative data are considered, but is still apparent here
in the relatively large number of species recorded. It can also be seen that the holoplanktonic, mainly
oceanic solenoids are perhaps the most completely cosmopolitan of all plankton diatoms, though
panthalassic 'reversionary plankton forms' such as Nitzschia seriata are almost equally widely
distributed.

The few important species that seem to be limited to the Benguela current area and adjacent South
African coasts are all inshore ones: Chaetoceros strictum and C. tetras, Fragilaria granulata and
F. karsteni. Certain other coastal species are recorded from comparatively few of the other regions
mentioned, but since these include major upwelling regions their very widespread distribution is in
no doubt. Further sampling will almost certainly reveal their presence in the less favourable inter-
vening areas eventually, though probably in such small numbers as to form but an insignificant pro-
portion of the sparse populations to be found there. These forms include C. costatum, recorded else-
where from the coast of southern Europe and North Africa, California and Japan ; C. psendocrinitum,
S. temperate coasts of Europe and California, and C. van heurckii, recorded only from California and
the Madras coast of India among the other localities considered. Nitzschia longissima also has a com-
paratively restricted occurrence, so far as it is yet known, being recorded only from the other African
localities, California and Japan.

Proceeding to brief ' ecological characterizations ' of the several species on the basis of our observa-
tions in the Benguela current area, it is necessary to make the proviso that maximal occurrence during
spring or autumn may indicate either a normal seasonal effect or merely that these species tend to
flourish earlier or later in a succession that quite probably repeats itself several times in the course of
a year, as the more or less persistent upwelling system waxes and wanes.

264

DISCOVERY REPORTS

Table 28. Distribution in other regions, defined below (with sources), x positive records

South African

Worth and

Tropical

Indian

West

East

Southern

Selected abundant or

waters

Atlantic

Ocean

Pacific

Ocean

typical Benguela

*•

—^ >

current species

■J

1 1

DlSCINEAE

Stephanopyxis turris

—

Thalassiosira subtilis

—

Planktoniella sol

—

BlDDULPHIACEAE

Biddulphia longicruris

—

Eucampia zoodiacus

—

Chaetoceraceae

Chaetoceros affine

—

C. atlanticum + var.

X X

—

X X

X —

neapolitanum

C. compressum

—

C. constrictum

—

. —

—

. —

C. convolutum

—

C. costatum

—

C. curvisetum

—

C. debile

—

C. decipiens

—

C. didymum

—

C. difficile

—

C. laciniosum

—

C. lorenzianum

—

C. peruvianum

—

— ■

C. pseudocrinitum

—

C. sociale

—

C. strictum

C. subsecundum

—

— ■

—

C. teres

—

C. tetras

C. van heurckii

—

SOLENIINEAE

Rhizolenia alata

R. hebetata

—

R. imbricata

—

R. setigera

—

R. styliformis

Leptocylindrus danicus

—

Dactyliosolen mediterraneus

—

Corethron criophilum

Pennatae

Fragilaria granulata

—

F. karsteni

Asterionella japonica

—

Thalassionema nitzschioides

—

Thalassiothrix longissima

—

Nitzschia closterium

—

N. delicatissima

—

N. longissima

—

N. seriata

1 Atlantic coast of Cape Province (Boden, 1950).

2 Between Cape Town and Port Elizabeth (Karsten, 1906).

3 Agulhas current (Hendey, 1937).

4 'Northern Seas' (Lebour, 1930).

5 Bay of Fundy, Gran and Braarud, 1935.

6 Temperate and subtropical North Atlantic, including
Canary current (K. R. Gaarder, 195 1).

7 Tropical Atlantic (Karsten, 1906, and others).

8 Madras coast of India (Subrahmanyan, 1946).

9 Chu San I. China, ca. 300 N. lat. (Sproston, 1949).

10 Pacific coast of Japan (Aikawa, 1936; Marumo, 1954;
Takano, 1954).

11 Pacific coast of North America, including California
current (Cupp, 1943; Sleggs, 1927; Allen, 1938).

12 Peru current (Hendey, 1937)-

13 Subantarctic, mainly Atlantic sector (Hart, 1934;
Hendey, 1937).

14 Antarctic (Hart, 1934, 1942; Hendey, 1937).

MICROPLANKTON 265

Stephanophyxis turris was here an inshore ('coastal' or 'neritic') species found mainly in the northern (warmer)

part of the area surveyed. Much more abundant in autumn than during spring.

Thalassiosira subtilis had a panthalassic distribution. Maximal abundance inshore in autumn; greatest relative

importance offshore during the spring survey.

Planktoniella sol. An oceanic species relatively important at sparsely populated offshore stations only, during

both surveys.

Biddulphia longicruris. An inshore species frequent and 'typical' though never abundant, in spring samples; not
yet observed at all in autumn ones at the dilutions necessary to obtain counts.

Eucampia zoodiacus. An inshore species with precisely the converse of the seasonal distribution of Biddulphia
longicruris. Eucampia zoodiacus was not seen at all during analysis of the spring samples. In autumn it was abundant,
sometimes one of the dominant species close inshore.

Chaetoceros atlanticum (type) mainly offshore with pronounced spring maximum.

Chaetoceros atlanticum var. neapolitanum even more definitely restricted to offshore waters than the type (with
relatively high temperature) but also in some of the same samples.

Chaetoceros affine (syn. C. Ralfsii) here a strongly neritic species much more abundant in autumn than during spring.

Chaetoceros compressum was one of the most abundant species at both seasons inshore, but sufficiently panthalassic
for the 'overspill' to dominate at a few of the sparser offshore catches as well.

Chaetoceros constrictum. Very important during both surveys. Distributed much like C. compressum.

Chaetoceros convolutum was mainly an offshore species most abundant during spring.

Chaetoceros costatum, an inshore species most numerous in autumn (or late in the succession).
' Chaetoceros curvisetum, mainly inshore and with a spring maximum, but very important at both seasons. The
most abundant species in these samples. Showed sufficient panthalassic tendency to dominate some offshore
samples as well, like C. compressum and C. constrictum, which often occurred with it.

Chaetoceros debile. Inshore, most in autumn, very local here.

Chaetoceros decipiens. Panthalassic, though mainly offshore here, more in spring than in autumn.

Chaetoceros didymum. An inshore species with pronounced autumnal maximum, when the resting spores were
even more abundant than the vegetative phase.

Chaetoceros difficile. Mainly inshore with autumn maximum.

Chaetoceros laciniosum. An inshore species, local here, with strong spring maximum.

Chaetoceros lorenzianum. Panthalassic here with spring maximum far offshore at the outer end of the Orange
river line.

Chaetoceros peruvianum. Offshore form more abundant during spring than in autumn.

Chaetoceros pseudocrinitum. An inshore or shelf species here, most in autumn.

Chaetoceros sociale. A panthalassic species on its showing here, abundant at some very localized inshore stations,
but relatively more important offshore in spring.

Chaetoceros strictum. An inshore species observed most abundantly during the spring survey.

Chaetoceros subsecundum. An inshore species with autumn maximum, when many of the characteristic resting
spores were present.

Chaetoceros teres. An inshore species most abundant in autumn here.

Chaetoceros tetras. A very local species abundant at a few inshore stations, most in spring.

Chaetoceros van heurckii. An inshore species most abundant in autumn.

Rhizosolenia alata. Panthalassic rather than exclusively oceanic here, most important offshore in spring, but
numerous during both surveys.

Rhizosolenia hebetata. Present here almost exclusively in the form (or phase) semispina. Was most numerous
inshore in spring, but of much greater relative importance offshore, especially in autumn. Panthalassic seems a
fairer description than oceanic for this extremely cosmopolitan form.

Rhizosolenia imbricata. Here var. Shrubsolei was more frequent than the type, but both were present in the same
samples at times. Panthalassic, reaching its greatest relative importance offshore at both seasons.

Rhizosolenia setigera. An inshore form with spring maximum.

Rhizosolenia styliformis. Panthalassic, but mainly offshore with a pronounced spring maximum.

Leptocylindrus danicus. An inshore species most abundant in autumn.

Dactyliosolen mediterraneus. Panthalassic, maximum inshore in autumn, but offshore during the spring survey!?
Stenothermal.

266 DISCOVERY REPORTS

Corethron criophilum. Panthalassic here, where most were seen inshore or on the outer shelf in spring. Of its
generally oceanic character in most phases there can be no doubt.

Fragilaria granulata. Panthalassic? Recorded here only from the outer shelf or even offshore, never overlapping
with the next species. Not recorded elsewhere except off South Africa.

Fragilaria Karsteni. Very definitely neritic and with a spring maximum, but also quite abundant during the
autumn survey. Recorded elsewhere only off Cape Province (Karsten (syn. F. capensis) Boden).

Asterionella japonica. An important inshore and outer-shelf species, especially in autumn when it was one of the
few other species to rival the dominant chaetocerids in abundance, and partly responsible for visible discoloration
of the water at some stations close inshore.

Thalassiotlmx longissima, though never very abundant, was relatively important offshore at both seasons, rather
more so in spring than during the autumn survey.

Thalassionema nitzschioides. An inshore species, very local in this area, chiefly in spring (or early in the succession).

Nitzschia closterinm. Tychopelagic, a littoral species fairly frequent in plankton close inshore, but never abundant
here.

Nitzschia delicatissima. Panthalassic, mainly offshore with an autumn maximum here.

Nitzschia longissima. Never abundant, but very characteristic of the inshore plankton here, especially on the
spring survey. Possibly littoral, tychopelagic.

Nitzschia seriata. Panthalassic, abundant and important at both seasons studied. Most important offshore in
spring, but more abundant inshore.

Comparing these ecological notes with those of other workers, principally Gran, Lebour, Braarud
and Gran, Cupp and K. R. Gaarder, as referred to in the sources of Table 28, it appears that a large
majority of the species considered important or typical in the Benguela area were disposed therein
just as one would expect from their recorded distributions elsewhere. Minor modifications of previous
ecological characterizations based on these results, and on earlier work in the southern ocean (Hart
1934, 1942), are suggested as follows:

Thalassiosira subtilis should probably be regarded as panthalassic rather than oceanic. Though
cosmopolitan in the open oceans, it frequently attains greater abundance near land. Gaarder's (1951)
note that though widespread in the Michael Sars material from the North Atlantic, the species was
observed most abundantly close in to the Azores, accords with this view.

Conversely several of the dominant chaetocerids of the rich inshore waters, though undoubtedly
neritic in the main as recorded elsewhere, showed a more or less pronounced panthalassic trend ; since
lesser numbers of them flourished sufficiently far offshore to dominate the sparser communities
encountered there. This trend was most marked in Chaetoceros Lorenzianum, but was also shown by
the three most abundant of all the diatoms met with: C. compressum, C. constrictum and C. airvisetam.

The inshore or neritic species C. sub secundum exhibited a striking seasonal difference from its known
disposition in the northern hemisphere, where most observers have recorded a strong maximum in
spring or early summer. On our two surveys it was relatively much more abundant in autumn.
Possibly we missed an earlier maximum through lack of full seasonal coverage, which would show up
any repetition of the succession at a shorter interval of time. Equally we may here have a real dif-
ference due to the ' conditions of existence ', biological as well as physical. In the northern hemisphere
the species has been regarded as arctic-boreal or boreal, but both Gaarder's results and our own show
that it can flourish in much warmer temperate waters than the earlier records suggest, where it must
find itself among a very different and much more varied phytoplankton community.

The holoplanktonic cosmopolitan solenoids: Rhizosolenia alata and R. hebetata.f. semispina would
seem definitely better described as panthalassic rather than oceanic. Their dominance at certain
sparsely populated oceanic stations is unquestioned, but at the same time they were often found in
greater numbers among the rich Chaetoceros plankton close inshore. The same applies in a less marked
degree to R. imbricata (mainly the variety Shrubsolei; the larger type phase was rarer and 'more

MICROPLANKTON 267

oceanic' here, though they occasionally occurred in the same samples). Temperature is probably the
factor involved, having regard to the distributional records of the two forms elsewhere (cf. p. 217).
Similarly Corethron criophilum and even the well-known Rhizosolenia styliformis both tended to
display a more panthalassic trend than their usual designation as oceanic forms would lead one to
expect. In support we may cite the abundant occurrence of Corethron (in some of its phases) close in
to the land as well as offshore in the antarctic zone of the southern ocean, and the occurrence of almost
pure communities of Rhizosolenia styliformis in the shallow waters of the North Sea (Hardy, 1923;
Wimpenny, 1936).

Concerning Dactyliosolen mediterraneas previous opinions were 'neritic' (Lebour) and 'neritic,
sporadically oceanic'. K. R. Gaarder (1951) found moderate numbers of it in samples from all over
the area covered by the 'Michael Sars' to the west and south of the British Isles. In the Benguela
material the species was locally abundant offshore in spring and inshore in autumn, suggesting that it
thrives only within narrow limits of temperature (stenothermal, with optimum range about 150 to
1 90 C). Certainly 'panthalassic' would seem to be the best brief description of its general distribu-
tional trend.

Finally, two of the most abundant 'pennatae', Nitzschia delicatissima and N. seriata, previous
ecological descriptions of which range from 'perhaps oceanic, but often abundant inshore', to
definitely 'neritic', would in the opinion of the writer (TJ.H.) be better described as panthalassic—
expressing the duality of the best of the earlier descriptions in one word. They were numerous in both
inshore and offshore samples in the area studied here, and also in antarctic seas (Hart, 1934, 1942).
These minor differences from previous brief ecological descriptions of the species are so few that
it is the general concordance with the opinions of those with the greatest experience of working
through large collections of material that is striking, encouraging the belief that in this direction at
least plankton workers grope towards 'the truth' to some purpose. Although Gran's 'system of
plankton elements' must necessarily be modified as data from the less-known sea-areas becomes
available, the ideas implicit therein remain one of our greatest aids in the attempt to understand the
relations between phytoplankton communities and their 'conditions of existence'.

This comparison of the diatom-flora of the Benguela current with those of other regions brings out
one important point, implicit in much that has been published already, but little emphasized by the
earlier authors: that there is a fundamental difference between the diatoms and, for example, the
species of oceanic zooplankton, in the nature of their distribution.

Although there are some cosmopolitan species of zooplankton, the range of the majority is subject
to some limit beyond which they are unknown. Where there is a region offering an environment
similar to that occupied by such a species, but isolated from it, we normally find there a similar species,
but a distinct one. Most of the plankton diatom species, however, excepting certain neritic, polar, or
markedly stenothermal warm-water forms, are not limited in their dispersal by ' barriers ' to anything
like the same extent as the zooplankton. Many of the more cosmopolitan diatoms may turn up almost
anywhere in the oceans of the world, and become locally important or even dominant, wherever the
'conditions of existence' best suit them.

It is for this reason that the plankton floras of adjacent water masses must be studied with more
regard to the differing proportions of the various species within them, than to the presence or absence
of particular forms.

268 DISCOVERY REPORTS

ZOOPLANKTON

On both of the ' William Scoresby's ' surveys net hauls were made to sample the zooplankton. Full
particulars are given in the Station List (1953). On survey I these consisted of a series of vertical hauls
with the ' Discovery ' N 70 V net, and were taken only on the three main latitudinal lines of stations.
On survey II the hauls were extended to include a surface haul with a metre stramin net (N 100 H) at
all stations and in addition an oblique haul with a metre stramin and 70 cm. net (N 100 B, N 70 B)
was made at all ' full stations ' — that is, again on the latitudinal lines of stations.

One of us (T.J.H.) has sorted the zooplankton hauls from survey I, and the material has so far as
possible been distributed to specialists in the various groups. Reports on some groups have already
been published, and we present a synopsis of the findings of these. Where it has not yet been possible
to find specialists to work up the groups, they have been provisionally identified and the results are
used in the following general account, sometimes merely to give a picture of the distribution of the
group as a whole. Some important groups, notably the Copepoda, have not yet been dealt with.

The zooplankton samples from survey II have not yet been sorted, apart from some groups — fish
eggs and larvae, Cumacea and Chaetognatha — whose distribution had proved unusually interesting
during the first survey. These results are included in the following account.

POLYCHAETA

Most of the polychaets in the collection were larval or juvenile forms. These have not yet been
examined in detail and it is hoped that they will be dealt with separately at a later date. It is interesting
to note, however, that some seemed to show a tendency towards a prolonged post-larval sojourn in the
plankton over the regions where the bottom waters were exceptionally deficient in oxygen.

Chaetognatha
The chaetognaths in the collection from survey I have been examined and identified by Mr P. M.
David, and will be dealt with in a separate report by him. The following notes have been made from
the figures kindly supplied by Mr David.

The distribution of the species seems to follow a rather similar pattern on all three lines of stations.
Close to the coast in the surface-layers Sagitta friderici Ritter-Zahony was dominant. Immediately
seawards of this, S. serratodentata Krohn became the dominant species, still, however, in the shallower
waters of the continental shelf, although this latter species was also found in smaller numbers at the
oceanic stations WS 977 and 996. S. decipiens (Fowler) occupied a position just off the edge of the
continental shelf and generally somewhat deeper in the water column, the main centre of abundance
varying from line to line in depths of about 100-400 m.

Eakrohnia hamata (Mobius) was concentrated mainly farther seawards than the Sagitta decipiens,
in the deeper layers, while above the Enkrohnia hamata population, varying numbers of Sagitta
minima (Conant) and S. lyra (Krohn) were taken. Some numbers of S. lyra were also taken at station
WS 978.

Entomostraca
Dr J. P. Harding has very kindly confirmed the identification of the specimens of Cladocera which
were picked out from the samples. Both Evadne nordmani Loven and Podon polyphemoides Leuck.
were present in the collections, and Evadne nordmani was the relatively more abundant species.

The Cladocera were present only at the stations lying close to the coast. Off Walvis Bay at WS 981,
they reached their greatest concentration, more than 600 Podon polyphemoides and nearly 2200 Evadne

ZOOPLANKTON 269

nordmani being present in the 50-0 m. haul. At the next station seawards, WS 980, they were only
present in the 50-0 m. haul (one Podon polyphemoides and twenty Evadne nordmani), the 100-50 m.
haul and all other hauls on this line of stations being devoid of Cladocera.

On the Sylvia Hill line only two E. nordmani were taken at the station closest to the coast (WS 989),
and although no specimens were taken on the Orange river line, one specimen of E. nordmani was
recorded farther south at WS 1043 on the second survey.

It was very noticeable during sorting how completely the Ostracoda gave way to Cladocera close in
to the land on each line of stations. Here it seems that the marine ostracods constitute an essentially
oceanic mid-water group, while the Cladocera were confined to the most neritic part of the coastal
current. The two groups showed an almost complete absence of overlap in the first survey samples.

Ostracoda
Mr E. J. lies (1953) has published a report on the ostracods in the collection. Nearly all of these
occurred at the offshore stations. As with the mysids, variety rather than numerical abundance
characterized the group. Three genera were present, and of one of these, Conchoecia, twenty-three
species occurred in the samples.

Four or five species of Conchoecia predominated, but by far the greatest number were contributed
by the species Conchoecia elegans Sars.

C. elegans mainly inhabited the 500-250 m. layer off the edge of the continental shelf on the three
main lines of stations, but there are also indications that it shows a vertical migration, similar to that
described by Fowler (1909) in the Bay of Biscay, and more than eighty adults were found in the
50-0 m. layer at the night station WS 977.

C. nasotuberculata Miiller, and C. curta Lubbock, both appeared to occupy a depth distribution
similar to that of C. elegans, or perhaps at rather shallower levels. C. alata Miiller was found at
greater depths, 500 m. or more, while C. symmetrica Miiller was amongst the deepest species of all,
possibly even exceeding 1000 m., the greatest depth of the net hauls.

C. teretivalvata lies occurred in quite large numbers in the shallower layers, i.e. in samples from
250-100 m., except at one station, WS 976, where an anomalous haul of twenty-four specimens
occurred in the 750-500 m. layer.

As previously noted the ostracods did not overlap the Cladocera, and indeed at the inshore stations
their niche appears to be filled by the latter group.

Mysidacea
Dr Tattersall (1955) has examined and reported on the collections of mysids,1 and the following
remarks are abstracted from her report.

Only at one station, WS 1002, were large numbers of individuals taken. Here, in the 50-0 m. haul,
there were over 450 specimens of the gregarious mysid, Gastrosaccns sanctus (van Beneden). One
small juvenile specimen of the same species was taken rather farther seaward at station WS 1000.
Both these stations are somewhat farther south than is normally recorded for this species.

In spite of the paucity of numbers in the net hauls at the other stations, there was a richness of
species in which ten genera and sixteen species were recorded. Many of these occur within the known
geographical range of the species. Boreomysis rostrata Illig occurred in the deeper 750-500 m. hauls
at the offshore stations. Two species, however, show an interesting deviation from their normal range.
Dactylamblyops hodgsoni Holt and Tattersall has previously been recorded only from deep waters in

1 Her report is on a much larger collection which includes those from the Benguela current.

19-2

27o DISCOVERY REPORTS

the Southern Ocean, and at station WS 976 one juvenile specimen was taken in the 1000-750 m. haul.
The other species, Eachaetomera zurstrasseni (Illig), although originally recorded from the Indian
Ocean west of the Chagos Islands, has only been recorded once in the waters to the west of Cape
Town, and is usually only taken in the far south of the Atlantic Ocean. One specimen occurred at
station WS 976.

CUMACEA

The Cumacea were identified by Dr N. S. Jones and the following account has been abstracted from
his report on the group (1955).

Four genera and five species were present in the samples, but only the genus Iphinoe attained con-
siderable numerical importance. This is not altogether surprising, for the Cumacea are normally
bottom-living forms, but the appearance of one species (Iphinoe fagei, Jones) in considerable numbers
in the plankton— exceeding 7000 in one haul at station WS 989 — is of great interest.

The collections of Cumacea are confined to the stations relatively close to the coast, in shallow water.
Evidently there is a succession of species from north to south. Bodotria glabra Jones occurred only in
small numbers and only on the most northerly line of stations (190 44' S). On both the Walvis Bay
line and Sylvia Hill line the two species of Iphinoe, I. africana Zimmer and /. fagei, were dominant
in abundance. Upselaspis caparti (Fage) was present only off Walvis Bay and Diastylis rufescens Jones
occurred only on the Orange river line.

The large catches of Cumacea occurred in the night hauls at stations WS 988 and 989, and I. fagei
was the most abundant species. Jones notes that 'although the species present in these hauls may be
able to live normally in the plankton, they show no special adaptations to this mode of life and their
nearest relatives are coastal bottom-living forms'. Further, he says that when Cumacea have been
caught in tow-nets at night, adult males have usually predominated, especially when attracted by
artificial light, although in some recent records newly moulted adult or ovigerous females have out-
numbered the males. In the hauls containing the largest numbers of specimens described here, both
males and females of all stages were represented. These could possibly have been a nuptial swarm,
but the following is a rather attractive alternative explanation.

It is interesting to compare these catches with a sample of the bottom fauna taken near Walvis Bay
by Professor Spark (1953). Here, in the belt of sand inside the anaerobic zone (p. 204), Spark took
1910 Cumacea in a Petterson grab sample. Both stations WS 988 and 989 lay over the anaerobic zone,
and if Spark's specimens were the same species, Iphinoe fagei, then it seems reasonable to suppose that
the great development of the anaerobic zone in March may have forced the Cumaceans up from their
usual habitat on the sea-bed, to adopt a planktonic existence in the waters nearer the surface where
oxygen would have been available.

The numbers of Iphinoe sp. corresponded closely with the distribution of the pilchard eggs and
larvae (see p. 272).

Amphipoda
Although the amphipods have been separated from the samples, they have not been identified further,
and it is only possible to remark on the total abundance of the group. They were present in relatively
small numbers at all of the stations except WS 981. Their greatest abundance was at the offshore
stations, where at WS 986, over 270, which appear to be mainly juvenile Vibilia sp., occurred in the
50-0 m. haul, but they were also present in moderate numbers at the inshore stations on the Orange
river line. These Vibilia sp. appeared in numbers at stations where salps were also abundant, as was
to be expected from the known commensalism between these animals.

ZOOPLANKTON 271

EUPHAUSIACEA

Boden (1955) notes that fourteen species of euphausiids were represented in the collection from survey I.
The numbers of adult euphausiids were quite small, but larvae of some species were numerous in some
of the catches.

Nyctiphanes capensis Hansen was only taken at the stations on the continental shelf — excepting one
larva which occurred in the 1000-750 m. haul at WS 997. It was present on all three latitudinal lines
of stations. On the Orange river line the larvae extended farther seawards than the adults, but on the
Walvis Bay line the greatest abundance of larvae— totalling 5000 specimens — occurred at WS 979,
and this coincided with the greatest number of adults (twenty-seven) on this line.

The adults of Euphausia lucens Hansen, an oceanic species, occurred in very small numbers at the
offshore stations, but a large haul of 237 adult females was taken in the 50-0 m. layer at WS 1000 on
the continental shelf, and the adults were also present off the Orange river mouth (WS 1001 and
WS 1002). The larvae were mainly abundant at the offshore station on the Orange river line (WS 996),
but Barry (1956) in comparing Boden's material with some from New Zealand, questions the identifica-
tion of these larvae as E. lucens and considers they may belong to some other species.

E. tenera Hansen, a tropical to subtropical form, occurred only at WS 996, at the offshore end of the
Orange river line. Most larvae of this species were in the 250-100 m. haul. Boden is of the opinion
that many of the unidentified pre-furcilia larvae encountered at other stations may in fact be E. tenera.

E. recurva Hansen, which occurred offshore on the Walvis Bay and Orange river lines, shows some
suggestion of diurnal migration. E. hanseni Zimmer was represented by four adults in the 250-100 m.
layer at stations WS 978 and 987 just off the continental shelf.

Of Nematoscelis megalops G. O. Sars mostly larvae were taken at the oceanic stations, and these,
concentrated at about 250 m. during the day, show a diurnal vertical migration.

A species usually common in this area, Thysanoessa gregaria G. O. Sars, was present in very small
numbers, well offshore.

Four species of Stylocheiron were also recorded.

Decapoda and Stomatopoda
The collections of survey I have been examined and described by Dr M. V. Lebour (1954). Nearly-
all of the material consists of larval stages, but a few species are represented in adult form. A large
number of genera and species were represented, but few were present in any abundance and the small
number of individuals does not warrant a detailed account of their distribution.

Calliatiassa larvae were present at the inshore stations at Walvis Bay and on the continental shelf
on the Orange river line. The phyllosoma larvae of jfasus lalandii (Lamark), the common crawfish of
South Africa, were represented only by two specimens taken at stations WS 992 and 1000.

Among the Brachyuran larvae, a species of Ebalia occurred at both the offshore and shelf stations
on the Orange river line.

Five adult specimens of the stomatopod, Squilla armata Milne-Edwards, were taken in a trawl in
128 m. of water at WS 990. Larvae of the same species occurred in ones or twos at the three inshore
stations off Orange river mouth.

MOLLUSCA

The collections of planktonic molluscs have been reported on by Dr J. E. Morton (1954).

Specimens of the surface-living gastropod, Ianthina ianthina (Linnaeus) and /. globosa Swainson
were taken by hand nets at two offshore stations (WS 1057 and 1058) on survey II. The heteropod,

TT^

WOODS
HOLE.
MASS.

272 DISCOVERY REPORTS

Atlanta peroni Lesueur, a species common in subtropical Atlantic waters, occurred in small numbers

at the offshore station on the Orange river line on survey I.

The pteropod Limacina was, however, numerically the most abundant mollusc in the collections.
Two species occurred, the first L. inflata (d'Orbigny) only in small numbers at the offshore station
WS 986. The other species L. bulimoides (d'Orbigny) also occurred at the same position, but was
principally found at the offshore stations on the Orange river line. Here it reached great concentrations
at the two stations WS 996 and 997. More than 3000 individuals were taken in the 250-100 m. haul
at station WS 997.

We have seen (p. 229) that there was evidence of heavy grazing of the phytoplankton at these two
stations and this may well be attributed to these enormous numbers of pteropods. Also present at
these two stations were some specimens of the gymnosomatous pteropod, Pnenmodermopsis pancidens
Boas and its close association with the Limacina bulimoides and its probable feeding habits suggest that
it may have been preying upon the L. bulimoides.

Two species of lamellibranch larvae occurred in the collections. Five hundred and forty individuals
of larva 'A' were taken in the 50-0 m. haul at station WS 981 off Walvis Bay. The other species,
larva ' B ' was present off Sylvia Hill at stations WS 988 and 989 and more numerously off the Orange
river mouth where 600 were taken at station WS 1002.

Larvacea
The appendicularia from the samples, which include the genera Oikopleura and Fritillaria, have not
yet been identified, but some remarks may be made on the distribution of the group as a whole.

Very large numbers occurred at the three inshore stations on the Walvis Bay line (WS 979, 980 and
981) reaching a maximum of about 5400 in the 50-0 m. haul at WS 980. The numbers fell off sharply,
however, and only five individuals were present between 500 m. and 100 m. at station WS 978.
At the stations seaward of this, modest numbers occurred in the surface-layers.

On the Sylvia Hill line of stations, a reversal of these conditions was observed. At the outermost
station, WS 986, fairly large numbers occurred in all of the hauls. At WS 987 none of the hauls
contained appendicularia. At station WS 988, large numbers (> 200) were again encountered in
both the 50-0 m. and 100-50 m. hauls and at the station nearest the coast numbers decreased once
more.

This distribution was nearly paralleled on the Orange river line, where virtually all of the appendi-
cularia occurred at the two offshore stations. None was present inshore at stations WS 1000, 1001 and
1002. At the offshore stations numbers were highest in the surface -layers, and decreased with depth.

The explanation of this distribution is not easy without a more specific identification of the indivi-
duals. It may conceivably be the result of the presence of two separate populations of appendicularia
— the first, in abundance inshore at Walvis Bay and extending southwards to WS 988 and 989 at the
inshore end of the Sylvia Hill line, and the second, offshore on the Orange river line and Sylvia Hill
line (WS 986) and extending northwards in decreasing numbers to the offshore end of the Walvis Bay
line. Confirmation of this suggestion, will, however, have to await a more detailed examination of the
species.

Eggs and young stages of fish
Hart and Marshall (1951) have already commented on the fish-eggs and larvae which occurred in the
plankton hauls. Of particular interest were the large numbers of eggs and larvae of Sardinops sagax
ocellata, which occurred at the inshore end of all of the lines of stations, but particularly at the inshore
stations on the Walvis Bay and Sylvia Hill lines. The greatest catch of 1000 eggs was taken in the

ZOOPLANKTON 273

50-0 m. haul at station WS 989. Evidently spawning took place within 25 miles of the coast, in
depths of about 50-150 m. A few post-larvae were taken in the deeper net hauls, but all were con-
fined to the waters on the continental shelf. The heaviest catches occurred where the mean temperature
of the upper 50 m. of the water column lay between 130 and 14-5° C. The importance of locating a
spawning ground of this, the South African pilchard, is referred to on p. 270.

The eggs and young stages of other fish were also taken, notably those of the stockfish (Merluccius
capensis), and of anchovies {Engraulis sp).

Distribution of the zooplankton
From the foregoing notes it is evident that there are many characteristic features in the zooplankton
distribution, several of which might be expected from the known behaviour of the organisms. The
ostracods, for example, are in this region an essentially mid-water group, lying off the edge of the
continental shelf and showing a fairly well-defined distribution of species with depth, Conchoecia
elegans being the dominant species and occupying the 500 250 m. layer. In the shallower waters,
the role of the ostracods appears to be taken over by the Cladocera, which locally reached great
abundance inshore on the Walvis Bay line.

The mysids were, on the whole, very poorly represented numerically, and only the one species,
Gastrosaccas sanctus, which is normally particularly gregarious, attained any considerable numbers.
This concentration occurred in the rather diluted water off the Orange river mouth. On the more
northerly lines very few specimens were taken, and it is interesting to compare this with the abundance
of cumacea at these more northerly stations.

The dominant cumacean, Iphinoe fagei, is closely related to other bottom living forms, and shows
no particular adaptations to a planktonic existence. The large numbers occurring planktonically
inshore on the Sylvia Hill line may be explained as being a nuptial swarm. But when one considers
other phenomena — such as the presence of larval tubicolous polychaets with their tubes partly
developed, the larval lamellibranchs with shells developed, and the post-larval Ophiuroids, all in the
plankton — then one is more inclined to accept the alternative explanation, that the sea-bed of the
anaerobic zone did not present a desirable environment and forced into the plankton many organisms
which would otherwise have been present on the sea-bed at these stations.

The presence of the euphausiid Nyctiphanes capensis on the continental shelf is quite characteristic
of its habit, and the other euphausiid, Euphansia Incens, only reached large numbers in the vicinity of
the Orange river mouth, again in the shallow coastal waters. The close similarity in succession of
species between the euphausiid fauna of this region, and that found off California, described by Boden,
seems significant in view of the hydrological similarities between the two regions.

At the offshore end of the Orange river line the large numbers of the pteropod Limacina bulimoides,
evidently grazing heavily on the phytoplankton (p. 229) and probably being preyed upon in turn by
the gymnosomatous pteropod Pneumodermopsis pancidens, is the only major occurrence of the pelagic
molluscs in the collection.

The distribution of the Larvaceae is strongly indicative of the presence of two separate populations,
one in the coastal waters to the north, and the other in the oceanic waters to the south.

The association between the young amphipods (Vibilia sp.) and the salps, both of which occurred
in numbers at the offshore end of the Sylvia Hill line, is no doubt an example of the well-known
commensalism between these animals.

The correlation between the numbers of cumacea and the numbers of eggs and young stages of the
pilchard is probably purely coincidental, but may be of some value since the cumaceans are fairly
large and easily seen, and could perhaps be used as an 'indicator' for the pilchard eggs.

274 DISCOVERY REPORTS

Taking the zooplankton as a whole, one gets the impression of a rather patchy and spasmodic
distribution, quite large numbers of individuals of particular species occurring rather locally. This
impression must, of course, be contributed to very largely by the fact that a relatively small number
of stations cover a rather large area, but nevertheless there are few occurrences which suggest the
population of specific water masses by particular organisms. The picture formed, in contrast to that
created by the phytoplankton, rather suggests an independence from the more particular water masses,
and an occupation by the animals of ecological niches more suited to their own habit than conforming
to the circulation of the water masses. This applies in particular to the chaetognaths, whose distribu-
tion follows a similar pattern on all three lines of stations — Sagitta friderici occupying the water near
the coast, with S. serratodentata a little farther offshore, and S. decipiens in the deeper water at the
very edge of the continental shelf.

ECONOMIC RESOURCES OF THE BENGUELA CURRENT

Fish and fisheries
In a region so organically rich as the Benguela current it is only to be expected that animals higher in
the food chains and of more direct interest to man should also be found in abundance. In fact the
pelagic fishes are already being increasingly exploited and among them the South African pilchard
takes first place as the basis of extensive fisheries at various points along the coast. Following closely
in importance are fisheries for the 'maasbanker ' {Trachurus trachurus), stockfish (Merluccius capensis)
and snoek (Thyrsites atun), and many sharks are taken principally for their liver oil.

It is clearly impossible, in a brief oceanographical survey, to obtain more than a glimpse of the fish
populations and any account of these is more in the ambit of the Fisheries Division of the Department
of Commerce and Industries in the Union of South Africa, which is conducting extensive research
on this problem.

However, the inclusion of regional plankton sampling as part of the survey did reveal one point of
major significance to the economic development of the region, and that is the discovery of an extensive
spawning ground of the South African pilchard. As stated on p. 272 evidence was found of great
concentrations of eggs and larvae near the coast in the vicinity of Walvis Bay and Sylvia Hill. It is
not necessary, however, to enlarge on this here, for the details have been given in an earlier publica-
tion (Hart and Marshall, 1951).

Shellfish also have their place in the economic resources of the current, and there is a thriving fishery
for the rock lobster (Jasiis lalandii) on the coast in the southern part of the Benguela region. Although
not yet developed, it is possible that squid may some day contribute to a fishery. Frequently large
numbers of these animals were seen preying voraciously on saury pikes and lantern fish attracted by
the lights of the ship when she was lying at the offshore stations.

Seals
There are several herds of the Cape Fur Seal (Arctocephalus pusillus) on the west coast of South Africa.
Their breeding-grounds extend from Cape Cross (21 ° 40' S.) to Algoa Bay on the south-east coast,
and established hauling-out places on the west coast are at Cape Cross, Hollam's Bird Island, several
islands near and south of Luderitz Bay, at Kleinsee, Elephant Rock, and some more rocky islets near
and south of Saldanha Bay (Rand, 1956). The places where the seals haul out are probably determined
largely by the availability of suitable islets, and the topography of the coastline.

These seals are exploited commercially, and during the winter attention is focused on the yearlings
of both sexes. During the summer, takings are limited to the bulls in certain rookeries.

economic resources of the benguela current 275

Whales
At the beginning of this century some experimental whaling was started in South African waters, and
so encouraging were the initial reports that by 191 2 some twenty-five companies joined in the quest
from the Congo right round to the east coast (Olsen, 1915). Land stations were built, and on the
west coast these have operated from time to time at Cape Lopez, Lobito Bay, Elephant Bay, Mos-
samedes, Port Alexandria, Tiger Bay, Walvis Bay, Luderitz Bay and Saldanha Bay.

Initially this whaling was based on the humpback whale. It appears, however, from the successes
of various stations and the failure of others that the original theories concerning the migrations of the
humpback up the west coast were open to question. An increasing amount of evidence suggests that
the humpbacks, on their northward route from the antarctic, do not arrive at the Cape and progress
steadily up the Benguela, but rather that they avoid the cold waters of the current and keep well out
to sea, only striking the coast as far north as Portuguese West Africa. Blue whales, fin whales and
sei whales are taken at Saldanha Bay, but rarely at the stations north of the Benguela current. Catches
of sperm whales at Saldanha Bay have increased in recent years, but it appears that they are mostly
found at some distance from the coast.

The small scale of the whaling in the Benguela waters suggests that the current does not form a
particularly attractive environment for whales. This of course may be because the whalebone whales
in these more northerly latitudes are seeking warmer waters for breeding rather than feeding. It is
rather surprising, however, that there appear to be so few sperm whales in the Benguela current. The
catches shown in the statistics are poor, and Townsend's charts (1935) also show that very few sperm
whales were taken in the Benguela waters. Indeed, these charts showing sperm whales taken to the
north of the Benguela, to the west in the south-east trade wind drift and to the south, create the
impression that the sperm whale also must specifically avoid the cold coastal waters. These records of
the varying intensity of whaling in different areas do not necessarily represent the density of the whale
population, and they are coloured by the preference of the whalers for specific types of whale, but
nevertheless they are strongly suggestive.

It is more difficult to interpret this avoidance of the Benguela current by the sperm whales than by
the whalebone whales. The latter, we know, feed in the Antarctic, but for the former one might expect
the rich waters of the Benguela to be an attractive feeding-ground. One can only presume that if the
picture created by these records is correct, then there must be some other factor, such as the absence
of suitable food organisms, etc., which makes the current unfavourable for the sperm whale.

Guano Islands
The fertile waters of the Benguela current, with their abundant stocks of fish, support enormous
populations of sea birds. Practically every rocky promontory and island along the coast is densely
inhabited by birds during the nesting-season. The relatively favourable climate with a markedly low
rainfall has, in places where the topography has been suitable, led to considerable accretions of guano.
Perhaps the most renowned deposits are found on the island of Ichabo (260 17' S.) about which an
anonymous writer (obscurely described as ex-member of committee, 1845) quotes the following

humorous poem:

There's an island that lies on West Africa's shore,

Where penguins have lived since the flood or before,

And raised up a hill there, a mile high or more.

This hill is all guano, and lately 'tis shown

That finer potatoes and turnips are grown

By means of this compost, than ever were known ;

276 DISCOVERY REPORTS

And the peach and the nectarine, the apple, the pear,

Attain such a size that the gardeners stare,

And cry, 'Well! I never saw fruit like that 'ere!'

One cabbage thus reared, as a paper maintains

Weighed twenty-one stone, thirteen pounds and six grains,

So no wonder Guano celebrity gains.

Attention was first drawn to the value of the deposits on Ichabo by Morrell (1852)1, an American
sealer. His earlier reports had been rapidly followed up, and by 1845 most of the guano had been re-
moved from Ichabo and ships disappointed in their search there turned to the other islands and coastal
deposits. Now, the utilization of the recent deposits is controlled, and for this purpose the islands
are divided administratively and geographically into two groups : the ' northern group ' comprising the
islands to the north of Orange river mouth, and the ' colonial group ' extending from 3 1 ° S. to the Cape.

Hutchinson (1950), in his monograph on vertebrate excretion, has dealt at some length with the
South African deposits, and his work presents us with a very useful summary of what is known of them.

In both groups of islands there are three species of birds which make the major contribution to the
deposits. These are as follows:

The Cape Gannet [Morns capensis Lichtenstein), (2) the Cape Penguin (Spheniscus demersus
Linnaeus), and (3) the Trek Duiker (Phalacrocorax capensis Sparrman).

In addition to these three species it is probable that the other cormorants make minor contributions.
These birds fulfil the principal biological attributes necessary for deposition of guano, in that they are
colonial in nesting, and excrete at their nesting-sites. The best guano is formed where there is a
minimum of extraneous matter such as sand and feather, etc. introduced into the deposit.

The guano, once deposited, is subjected to weathering, and it is through this process that the
characteristic types of guano are developed. Rain and spray both wash the guano, and this results
in the leaching of nitrogenous compounds from the deposit, producing the rather inferior phosphatic
guano, with a low nitrogen content.

There is some evidence that the guano of the ' northern islands ', which resembles the modern
Peruvian guano, is relatively rich in nitrogen compared with the guano of the ' colonial islands '. The
difference may be related to the higher rainfall in the 'colonial group' islands (e.g. Dassen island,
see Fig. 3).

It appears that relatively flat islands, which are sufficiently high to allow deposition of guano well
clear of the splash zone, form the most favourable substrate for successful accretion. The island of
Ichabo in the ' northern group ' is the richest producer, and some 2000 tons of guano are deposited there
annually. From all of the west South African deposits about 1 0,000 metric tons are harvested annually,
which can be taken as roughly equivalent to the annual deposition. Assuming an average content of
phosphate (P205) of 10%, thiswould indicate an annual removal of about 440 metric tons of phosphorus
from the sea in this region — an amount which would be equivalent to the complete removal of
phosphorus from about 5^ km.3 of upwelled water. As the total volume of water in the Benguela
current is probably of the order of io4 km.3, the phosphate removed and deposited as guano must
represent a very small part of the available phosphate in the upwelled water.

There is a certain amount of fluctuation in the total annual yield of guano and to some extent this
may be related to the availability of food for the birds. In years of catastrophic mortalities of fish
(see p. 199) there is some evidence of a fall in guano production, but such variations are by no means so
pronounced as on the Peruvian coast. Perhaps this may to some extent be explained by the fact that
the region most affected by these catastrophic phenomena is situated to the north of the islands, in

1 The publication date of his narrative; his voyages took place much earlier.

REVIEW OF THE MAIN FEATURES OF THE BENGUELA CURRENT 277

the vicinity of Walvis Bay, and may only affect the northernmost guano islands. Other adverse
phenomena such as abnormal meteorological conditions may have a more general effect over the
whole region of the Benguela current.

REVIEW OF THE MAIN FEATURES OF THE BENGUELA CURRENT

The detailed description of the ' William Scoresby's ' observations has presented a large number of
facts and clearly, before advancing further, we must endeavour to bring these together to create a
picture of the current as a whole.

Probably the most obvious feature of this, as of any other upwelling region, is the presence of water
at the sea-surface many degrees cooler and incomparably richer in life than that normally found in the
open ocean in the same latitude. On account of the temperature anomaly we find, as has been clearly
demonstrated by the two 'William Scoresby' surveys, that the surface isotherms are disposed more
or less meridionally in contrast to their latitudinal disposition over the greater width of the ocean.
This is paralleled in the salinity distribution, and combines with the distribution of many of the other
properties investigated in defining the entity of the Benguela current.

Within this general scheme a more detailed picture emerges, and one of the first things to notice
is that nearly all of the physical, chemical and biological properties of the current exhibit discontinuity
or irregularity both in time and in space. The Benguela current consists of a series of anticyclonic
eddies, of interlocking tongues of cool and warmer water, of areas of rich and relatively poor phyto-
plankton, all of which merge into a complex pattern which is in a constant state of change or flux.
This quality of irregularity and instability is in fact one of the features which emphasize the discrete
character of this upwelling region.

In the 'William Scoresby's' two surveys there was a great contrast in conditions, and we have
presented evidence to show that while in survey II, in spring (September-October), a state of active
upwelling was encountered, on survey I, in autumn (March), the current was, at least in part, in a
quiescent phase. One cannot be dogmatic about the criterion of normal conditions in such a region,
but as the Benguela current is usually looked upon as a region of upwelling, we feel that there is a
precedent for accepting conditions of active upwelling as being normal within the current and periods
of quiescence as abnormal. It is in this light that we shall proceed to summarize the facts already
presented and go on to consider the significance of upwelling in relation to the economy of the ocean
as a whole.

Normal conditions

We have remarked on the greater activity of upwelling on the September-October (second) survey
of the R.R.S. 'William Scoresby' and perhaps the first and most striking feature can be seen in the
chart of surface isotherms (Fig. yb). Here the low surface-temperatures inshore compared with those
in the oceanic water to the west, and the configuration of the isotherms, gives one the impression of
the cold water masses inshore driving actively out from the coast and thrusting out into the warmer
oceanic waters.

This cool, low salinity water (Fig. 8 b) moving offshore, clearly does not originate uniformly along
the coast, but is produced in localized regions. In some cases these may be related to specific features
on the sea-bed (Fig. 4), but in general it seems more probable that the dominating effect is that of the
local winds in the particular areas. Our results have led us to deduce that while the trade wind far
out at sea maintains a tension on the coastal water masses, the local diurnal winds are probably mainly
responsible for producing an effective northwards along-shore or offshore drag on the sea-surface
and supplying the energy necessary to create these localized centres of upwelling.

278 DISCOVERY REPORTS

In the initial stages of upwelling the lighter surface-water must first be affected and removed away
from the coast. To replace it, cooler and denser water must be raised from subsurface depths. This
in turn will, however, be transported offshore, and where it meets the lighter surface-waters a relatively
strong convection is set up. For example, on the Orange river line of stations the offshore waters are
sharply separated from the cooler and denser upwelled waters by a pronounced convection cell

(Fig- 37)-

Evidently this sharp demarcation is present to a greater or lesser extent along the westward edge
of the upwelling waters. The rapid alterations in temperature as this boundary was crossed (Fig. 9)
throughout the region bear ample testimony to this, and so it appears that although no geographical
boundary is present, the upwelled waters are in fact separated sharply from the warmer oceanic
surface-waters lying to the west.

The upwelled waters have a lower temperature and salinity than the offshore surface-waters, and
if one compares their T-S relationships with those at the offshore stations, it can be seen that they
correspond to those at subsurface depths offshore (Fig. 330) and while they undergo little or no
mixing in the process of uplift, they are subjected to some degree of heating when they reach the
surface. From this comparison we can determine the depth from which the upwelled water originates
and this is seen to be in the layer between 200 and 300 m.

At this depth there is evidence of a subsurface current flowing southwards along the edge of the
continental shelf, which we have termed the 'compensation current', and which appears to be the
replacement source for water which is upwelled. In this respect it is interesting to note that the
compensation current decreases in width in its southward journey (Fig. 34) as would be expected in
a replacement flow.

In the waters of the compensation current the content of dissolved oxygen is extremely low and this
can be attributed primarily to the source of the water in the oxygen minimum layer which extends
over the tropical South Atlantic. Within the compensation current there is a gradual increase in
oxygen content from north to south, probably on account of lateral mixing with the adjacent well-
oxygenated oceanic waters. The significance of this low oxygen content will be the more evident in
the next section of this paper (p. 279).

The waters of the compensation current, and those which are upwelled, have a relatively high
content of dissolved inorganic phosphate phosphorus, and the entry of large supplies of this (and
probably other) nutrient into the euphotic zone is of major importance to the biology of the region.

We have shown that in the coastal waters a large standing crop of phytoplankton was present. The
main concentrations were found along the coast in the vicinity of the inshore end of the Sylvia Hill line
(250 S.), where the numbers were made up by large quantities of Chaetoceros sp. and Fragillaria
karsteni (at the station closest to the coast). In the warmer more saline oceanic waters, several species
of solenoids, Thallasiothrix longissima, Fragillaria karsteni and Planktoniella sol were prominent in the
phytoplankton, while in the vicinity of the boundary region the sparse flora contained elements of
both the coastal and oceanic floras.

The results of survey II present us, therefore, with a picture of an actively upwelling region,
extending in a belt some 80 miles wide along 1000 miles of the western coast of South Africa, an area
within which the abundance of flora far exceeds that of the ocean to the west.

Abnormal conditions
On survey I in the autumn (March) we see similar general features, that is, cooler and less saline water
along the coast, the eddy-like formation of the surface isotherms (Fig. ja), etc., but in the more
detailed features there is a marked contrast with survey II. This is most clearly seen in the vicinity

REVIEW OF THE MAIN FEATURES OF THE BENGUELA CURRENT 279

of Walvis Bay. Here the surface isotherms show a tongue of warm oceanic water pressing towards
the coast, and influencing the region as far south as the Sylvia Hill line of stations (250 S.). The water
masses on the landward side of this tongue are a mixture (Fig. 33 c, d), evidently derived from oceanic
and coastal water types. The penetration of this influence to 250 S. creates in that latitude a reversal
of the normal conditions, and there we find the apparent anomaly of warmer and more saline water
lying along the coast, with the cooler and less saline water at the offshore stations ( WS 986 and 987).

To the north of this wedge an extensive layer of oceanic water extended over the current, typically
populated with a flora in which Planktoniella sol was a conspicuous member. In the southern part of
the wedge, however, the flora was typically that of upwelled water, and inshore on the Sylvia Hill line
(250 S.) and Walvis Bay line (230 S.) the largest quantities of chaetocerids encountered on the surveys
were found.

It can be seen from Figs. 57 and 65 (pp. 225 and 231) that the highest concentrations of phyto-
plankton extended over a considerably larger area in survey I than in survey II. This was probably
associated with the greater age of the upwelled water, but it may be that the greater stability of the
upper water layers also enhanced its growth. In the offshore, unmixed oceanic water, the converse
was true, and the phytoplankton there on the average was in fact four or five times less plentiful than
on survey II. This may be associated with the more pronounced divergence of subsurface water which
Occurred seawards of the boundary on the second survey.

This great standing crop of phytoplankton, supporting a correspondingly large crop of zooplankton,
must eventually sink down and die, and the nature of the bottom deposits is sufficient evidence that
a very large part of the sinking and death takes place in the coastal region. The conditions prevailing
at the time of the first survey would certainly have been conducive to this. The meteorological records
show that there was little wind, particularly in the vicinity of Walvis Bay, and the currents appear to
have been equally sluggish. Indeed, while the ship steamed across these waters, masses of moribund
organisms, both phytoplankton and zooplankton, were encountered.

All this organic material sinking to the sea-floor decomposes fairly rapidly, and in so doing will both
liberate nutrients and consume oxygen. That nutrients are released in some quantity is strongly
suggested by the phosphate sections (Figs. 50-56) which show concentrations of phosphate in the
waters of the continental shelf which exceed those in the water upwelling from greater depths. This
local nutrient regeneration must play an important part in supplying the dense growth of plants with
sufficient nourishment.

The removal of oxygen by decomposition has, however, less beneficial effects. So complete is this
process that the water overlying the sea-bed of the continental shelf becomes completely anaerobic,
and permits the growth of sulphate-reducing bacteria in the sediment. These bacteria, liberating
hydrogen sulphide, enhance the effects of decomposition, and the hydrogen sulphide further reacts
with the dissolved oxygen in the overlying waters.

We have already noted that the upwelling water originates from a layer of low dissolved oxygen
concentration, and with the further removal of oxygen on the continental shelf it becomes still further
depleted. In the normal conditions of flow of the current it does not become seriously reduced, as we
can see from the oxygen sections of survey II (Figs. 41-44).

Presumably there is at these times a sufficient flow of water over the region to prevent stagnation.
In abnormal conditions, however, the cessation of upwelling, and influx of warmer water on the
surface, stopping or even reversing the current, has disastrous effects. These are demonstrated at
Walvis Bay, on survey I, where the computed currents (Fig. 34) show a southerly flow in the wedge
of oceanic water penetrating into the region, and where the section of dissolved oxygen (Fig. 40) shows
that the oxygen depletion actually extended to the sea-surface inshore.

28o DISCOVERY REPORTS

We believe that these events contributed, at least in part, to a small mortality of fish which occurred
at Walvis Bay in March 1950. At times such mortalities assume catastrophic proportions
(Brongersma-Sanders, 1948) and may seriously affect the fish stocks in this area.

Brongersma-Sanders (1948) has preferred to consider that the mortalities are due to poison
originating from the discoloured water which is so frequently coincidental with mortalities. Some of
the organisms causing such discolorations are known to be toxic to higher animals. The toxicity, of
course, depends on the organism causing the bloom, and in the Walvis Bay region Dr Brongersma-
Sanders suggests that a species of Gymnodinum may be the origin of such poisons. One of us (T.J.H.)
has examined several discolorations or blooms in South African waters, and none of these were
caused by that particular genus. Peridinium triquetrum, known to have predominated in some of them,
has once been recorded in quantity coincidentally with a fish mortality in the Baltic (Lindemann,
1924), but it is a common dominant of polluted inshore waters so that its occurrence near Walvis Bay
after a minor mortality might be the result rather than the cause of that phenomenon. This does not,
of course, rule out the possibility that Brongersma-Sanders' hypothesis may be proved correct by
further work, but from the existing evidence it seems to us more probable that the mortalities are
caused by the coincidence of several unfavourable factors, one of which may be toxicity of bloom-
forming phytoplankton organisms.

Not much more need be said about the animal populations. The collections of zooplankton have as
yet only been analysed from survey I. They show a certain individuality in the general fauna of the
current, but, as might be expected, the planktonic animals do not appear to show such a close cor-
relation with the water masses as do the phytoplankton. Apart from this the ' William Scoresby '
collections have provided some interesting material in connexion with the wider questions of the
distribution of planktonic animals, a subject which lies outside the scope of this paper.

The abundance of the higher animals — the large populations of pelagic fish, seals and birds — and
the presence of rich guano islands, are all characteristic features of upwelling regions and bear
testimony to their productivity. The apparent scarcity of whales is seemingly anomalous but is
perhaps an understandable exception (p. 275).

The discovery of a rich breeding-ground of the pilchard (p. 272) is yet another facet of this
interesting region and it emphasizes the fact that many important features may yet be revealed by a
more detailed examination of the region.

COMPARISON OF THE BENGUELA CURRENT WITH OTHER

UPWELLING REGIONS

The features which we have described in the Benguela current have their parallel in other upwelling
regions in the world, and in comparing these one is struck by the surprising similarity of the process
and its attendant phenomena, in widely separate geographical localities.

Upwelling is characterized by a divergence of subsurface water masses towards the surface, and as
such it is a widespread phenomenon throughout the oceans. By virtue of the effect of the earth's
rotation on a current in the ocean the more dense water is found on its left-hand side (looking in the
direction of flow) in the northern hemisphere, and on its right-hand side in the southern hemisphere.
If the velocity of the current is sufficiently great, more dense (and consequently deeper) water will be
lifted to the surface. This may occur along the edge of any suitable current, and may consequently
occur either at a solid geographical boundary or at an oceanic boundary with another current. In the
latter case we have examples in the divergences in the equatorial regions of the ocean, and in the
former the divergences on coastal boundaries of fast-moving currents, for example the Agulhas

COMPARISON OF THE BENGUELA CURRENT WITH OTHER UPWELLING REGIONS 281

current. Such upwelling may vary with the velocity of the current independently of the winds, and
we may distinguish it by referring to it as geostrophic upwelling.

On the other hand upwelling may be brought about by the direct influence of winds on the surface-
waters, and it is into this category that the major upwelling regions of the world fit. This type of
upwelling depends on the lie of the coastline and direction of the winds in relation thereto. It may occur
at almost any time throughout the year (e.g. Peru, Benguela, etc.), but in certain regions of seasonal
winds it may be a more restricted seasonal phenomenon (e.g. off south-east Arabia or the Indian
coasts, Somali coast, Red Sea, etc.). The greater importance of this coastal upwelling derives from
the greater depths which it affects. In geostrophic upwelling an upward tilt of isopycnals does occur,
and the water brought to lie on the surface depends on the degree of tilt. In coastal upwelling, how-
ever, the isopycnals may be thrown up very steeply in response to the action of wind on the sea-
surface and deep-lying density layers may be transported right up to the surface. In these conditions
waters with a higher nutrient content are brought up to the surface, and the subsequent growth of
life makes their presence all the more evident.

There are, as we have said, four extensive areas of coastal upwelling, all on the western coasts of the
continents of North and South America and Africa, and it is in these that we may look for analogies
and differences in the phenomenon.

These currents have certain visible features in common — a negative surface-temperature anomaly,
characteristic coastal winds, frequent fogs over the cold water, and arid or desert conditions over the
adjacent land. These phenomena, however, may be modified by the topography of the land. Thus, in
South and West Africa, there is relatively low-lying land for some 80-100 miles from the sea; here the
Namib desert occupies quite a broad strip along the coast, and the sea-breeze can develop a consider-
able reach over the land. But in Peru the high Cordillera of the Andes is nearer to the coast ; it confines
the desert to a much narrower strip, and causes the coastal winds to blow more or less parallel to the
coast and axis of the Cordillera.

There are also striking differences in the submarine topography of the various regions, which might
be expected to influence the process of upwelling. Off South-west Africa the continental shelf is
relatively broad compared with that off South America, where the steep slopes of the Andes are
projected below the sea-surface to abyssal depths, with only a relatively narrow continental shelf.
McEwen (19 12) suggested that the upwelling off California showed a striking correlation between the
areas of cold water and submerged valleys or other regions where the depth of the sea-bed increased
rapidly with distance from the coast. Gunther (1936) could find no evidence of such a correlation
off Chile and Peru, and the present work has indicated little or none off South-west Africa. Recently,
Yoshida and Mao (1957) have constructed a realistic mathematical model of upwelling off California
with little consideration for bottom-effects. There is, therefore, an accumulating amount of evidence
which suggests that the actual process of upwelling may not be greatly influenced by the width of the
continental shelf in these regions, although there may be effects on the attendant phenomena of the
upwelling.

Essentially, the process of upwelling takes the same form in all of these regions. The discrete, eddy-
like structure of the surface isotherms is common to all (Peru, Gunther, 1936; California, Sverdrup
and Fleming, 1941; Morocco, Currie, unpublished), and the disposition of isopycnals suggests that
the basic mechanism is similar in all cases, conforming to the pattern outlined by Sverdrup (1938).
We have shown that the same basic mechanism probably occurs in the Benguela current (Fig. 37) and
Gunther's density figures for the San Juan line off Peru suggest that a similar vertical circulation is
present there also. It is a mechanism, however, which involves rather complex water movements in
three dimensions. Fig. 96 may perhaps help to clarify them. It is based on our inferences as to the

282 DISCOVERY REPORTS

water movements in the Benguela current, and is a diagrammatic and somewhat idealized version of
them, but we feel that it is a fair representation of the circulation which is probably common to the
major upwelling regions (but the mirror image of those in the northern hemisphere).

A striking feature of the Peru current is the very large apparent size of the anti-cyclonic eddies,
which far exceed the dimensions of those found in the Benguela and California currents. There is
some indication that these large eddies off Peru may conceivably have within them smaller eddies, but
in themselves they appear to be peculiar to the Peruvian coast, and one can only assume that it must
be constancy in the driving forces which enables them to persist and achieve such large dimensions.

Fig. 96. A perspective diagram showing an idealized picture of the principal horizontal and vertical water-movements in the
process of upwelling. The isosteres are represented by the thin lines on the 'cut' faces of the water masses. The shaded
sinuous line on the sea-surface represents the continuation of the boundary convection between the upwelled and oceanic
surface-waters. The name of the deep compensation current has been abbreviated.

The Peru current itself, of course, is very much more extensive than any of the other upwelling
regions, for it runs along the South American coast for nearly 2000 miles. Furthermore it is unique
in having within its range the subtropical convergence, and consequently involves subantarctic
waters in addition to subtropical waters. By comparison the subtropical convergence in the South
Atlantic lies well to the south of South Africa (Deacon, 1933). In spite of its great size, however, the
Peru current has a slightly smaller negative temperature anomaly ( — 8° C.) than the Benguela
( — 9°C), and both exceed by far that off California ( — 3° C.) and Morocco ( — 3° C), (Dietrich, 1950).

Upwelling affects similar depths in all of these regions. Gunther (1936) quotes figures of 40-360 m.
with a mean at 133 m. in the Peru current. Sverdrup (1941) states that in the California current
upwelling was evidently confined to the upper 200 m., and in the Benguela current we have placed it
at depths between 200 and 300 m. This removal of water from the 200-300-m. level appears to be
accompanied in most cases by a subsurface compensation current. We have described this compensation

COMPARISON OF THE BENGUELA CURRENT WITH OTHER UPWELLING REGIONS 283
current below the Benguela current, flowing southwards and converging with the edge of the
continental shelf and bringing water of low oxygen content southwards from the equatorial region.
A similar current, better defined, is found off California (Sverdrup and Fleming, 1941) and also
below the Peru current, although in the latter case the circulation is more complex. We have mentioned
the inclusion of the subtropical convergence in the Peru current. At this convergence, subantarctic
water sinks and flows northwards along the coast below the warmer subtropical waters. Off the Peru
coast one can identify the southward flowing compensation current, but in 200 S. it meets the north-
ward flowing subantarctic water and is forced under the latter but continues to flow south. A salinity
maximum and the low oxygen content are also identifiable to at least 350 S.

The outstanding feature of these compensation currents is their low oxygen content, which in the
Benguela current is traceable to the origin of the water in the minimal oxygen layers of the equatorial
parts of the oceans. Sverdrup and Fleming (1941) have shown that a further reduction of oxygen
takes place with the local decomposition of organic matter. Off the California coast the level of the
oxygen minimum lies at a greater depth than off Peru and South-west Africa. Water with an oxygen
content of less than i-o ml./l. was rarely found at depths of less than 250 m., even at the inshore
stations off California, whereas both in the Peru current and Benguela current upwelling brings the
low oxygen water up on to the shallower reaches of the continental shelf.

It is clear that there are very close similarities between the abnormal conditions found off South-
west Africa, and the 'Callao Painter' and 'Aguaje' off Peru. At the north end of the Peru current
periodic incursions of warmer water invade the region where cool upwelled water is usually present.
These are referred to as the 'El Nino' current, and Gunther (1936) states that 'one finds in place of
the cool Peru Current diverging from the shore, hot poorly saline water of the Equatorial Counter
Current flows southwards and converges with it. The rise in temperature kills fish and plankton
which then decompose and emit sulphuretted hydrogen on an enormous scale. This is the Callao
Painter. . .'. While the 'Callao Painter' or 'Aguaje'1 occurs in conjunction with the 'El Nino', it can
also be associated with the convergence of warm oceanic water with the coast, and in this respect
we find a close parallel with the conditions off Walvis Bay on survey I.

We have expressed the opinion (p. 199) that the low oxygen content of the upwelled water,
accentuated under conditions of stagnation or reversed flow of the current, must be a very important
factor in the catastrophes off South-west Africa. The coincidence of low oxygen and the manifesta-
tions of the Callao Painter is strongly suggestive of a similar sequence of events off the coast of Peru
(Burtt, 1852; Currie, 1953 b).

Perhaps it is significant in this respect that records of pronounced abnormal conditions and fish
mortalities are rare on the California coast, where the low oxygen water does not normally appear to
be elevated to the proximity of the sea-surface on the continental shelf.

The frequency of records of green diatomaceous mud from the Peru coast (Neaverson, 1934) lend
further support to the theory that conditions on the sea-bed of the continental shelf must be virtually
anaerobic. Otherwise the chlorophylls and associated pigments would be oxidized to give the sedi-
ments a brownish or grey appearance.

Deposition of diatomaceous mud occurs at a much greater depth off Peru than off South-west
Africa. Off South-west Africa the diatom mud occurs principally between depths of 50 and 150 m.,
though it extends to greater depths at the landward end of the Walvis Ridge. The sediments in the
deep water beyond the continental shelf are mainly globigerina ooze. Off Peru, however, Neaverson

1 Evidently some confusion attends the use of the name 'Aguaje'. In the New Velasquez Dictionary it is denned as 'A
current in the sea, persistent or periodical ; e.g. the Gulf Stream ' ! Dr Wooster points out to us his impression that ' Aguaje '
used in Peru refers to discoloured water of biological origin, only occasionally associated with the 'Callao Painter'.

284 DISCOVERY REPORTS

(op. cit.) records diatom mud in abyssal depths; it is usually brown, but sometimes retains a greenish
appearance (WS 694, 1216 m.). Tentatively one may ascribe this deposition in deep water to the lesser
width of the continental shelf off Peru. The persistence of a green colour of organic origin in these very
deep water sediments in the Peru Basin is more difficult to understand, for the sediment must be
deposited through water which is fairly well oxygenated.

ORGANIC PRODUCTION IN THE BENGUELA CURRENT

The 'William Scoresby's' surveys were aimed at obtaining a more detailed picture of water-movements
and plankton distribution in the Benguela current than had hitherto been available. What we have
obtained, therefore, is a more or less instantaneous picture of what was taking place on the two
surveys. Such limited observations, particularly in a region of such great variability, can tell us little
about such a complex process as organic production. We can, however, say something of the biological
activity which was taking place in the particular water masses and from this obtain some idea of how
the biological processes within the current compare with those in the adjacent oceanic waters.

On the second survey the greatest quantities of phytoplankton were taken close to the coast between
240 and 260 S., in an area where active upwelling was taking place. Further offshore the quantities
decreased, and this suggests that the most favourable conditions for the proliferation of the phyto-
plankton were present in the very (nutrient) rich, cold water entering the euphotic zone. The upwelling
water enriched by the local regneration must have had a very high concentration of dissolved inorganic
phosphate-phosphorus, and even this profuse growth of phytoplankton had only reduced it to levels
still above 1 mg. at P/m.3. Further seawards, phytoplankton and phosphate both decreased.

In the oceanic surface-water offshore there was a secondary increase in the quantity of phyto-
plankton, but the amount of phosphate continued to decrease. Qualitatively, however, this offshore
phytoplankton was different from that inshore, being dominated by panthalassic or more definitely
oceanic species — some of the solenoids in particular for which no doubt the oceanic environment,
enriched by lateral mixing from the coastal waters and perhaps also by some divergence seawards of
the boundary (see Fig. 96), presented most favourable conditions.

It seems, therefore, that on survey II we have a situation analogous to that described by Sargent and
Walker (1948) in the California current. There they found the richest population, dominantly
chaetocerids, in the recently upwelled water. From this there was a succession, in the eddies of
upwelling water, to a rather sparse warmer water flora in the upwelled water which had been in the
surface for the longest time. On survey II in the Benguela current, the eddies were not so far developed,
and what we have reported may be a compression of the succession indicated by Sargent and Walker,
between the coast and the boundary region, with a separate and distinct oceanic flora to the west of
the boundary.

On the first survey, in autumn, the quantity of phytoplankton in the oceanic water was considerably
less, by four to five times, than in spring, but there is some evidence that at least in places it may have
been richer shortly before the survey was made. At stations WS 996 and 997 the very marked phos-
phate depletion in the surface-layers, with the presence of a large number of pteropods and numerous
faecal pellets, suggests that the low crop of phytoplankton may recently have been much greater and
had since been reduced by heavy grazing by the pteropods.

In the coastal waters, however, in the relatively abnormal conditions of the autumn survey (I) the
average numbers of phytoplankton were greater than in spring, and the area of high concentration
extended farther from the coast. Chaetocerids again dominated in the richest region but not all of
the dominant species were the same. Many more Asterionella japonica, Eucampia zoodiacus and

ORGANIC PRODUCTION IN THE BENGUELA CURRENT 285

Stephanopyxis turns were present than in spring. One noteworthy feature is that the richest stations
on survey I were found in the coastal waters between 230 and 260 S. where the effects of heating and
mixing with more saline water were clearly recognizable. Even amidst this dense flora, relatively
great quantities of phosphate were recorded. In this area, as we have noted, many moribund plankton
organisms and lines of foam, probably accumulations of dying phytoplankton, were observed on the
sea-surface, and the conditions would, therefore, have been conducive to a rapid regeneration of
nutrients from the decomposing plankton (Seiwell and Seiwell, 1938). Many resting spores of
Chaetoceros didymum and C. subsecundum occurred in the plankton samples, but we have insufficient
data to decide whether these were associated with such conditions or merely exhibit the seasonal
change in autumn.

The development of the peak population under such conditions is not altogether surprising, for
even with uninhibited exponential growth it must take some time for diatoms to reach such dense
concentrations in a newly upwelled water mass, and on this occasion the greater age of the upwelled
water and higher temperatures would have favoured such a development.

On both surveys the contrast between the densities of the coastal and oceanic populations of phyto-
plankton was an outstanding biological feature of the region. It should be specially noted that on
survey I the coastal populations reached a figure some four orders of magnitude greater than those in
the oceanic waters, and on survey II the range was three orders of magnitude. The actual figures
are given in Tables 14 and 15 (pp. 224 and 230), and their distribution in Figs. 57 and 65 (pp. 225
and 231).

Even the crude settlement volumes of the net hauls (Tables 14 and 15) suffice to show that the rich
inshore phytoplankton of the Benguela current is roughly comparable in quantity to that found in the
Peru current (Gunther, 1936) and in the more oceanic waters of the antarctic zone during the main
increase (Hart, 1934, 1942). They are significantly poorer than those found in northern antarctic
coastal waters (South Georgia) in late spring, but much richer than the values recorded there during
the post-maximal decrease and in winter. In the Benguela coastal waters there seems to be but little
seasonal falling off in quantity so long as the surface-layers are replenished by upwelling, so that it is
quite probable that the total annual production there equals or even exceeds that of the South Georgia
area, though the latter (at the height of the spring increase) can amount to 7-10 times the Benguela
or Peru averages. These figures from South Georgia in fact furnish by far the greatest standing crop
values yet known to us from any part of the world.

The open ocean, we know, presents a relatively stable and uniform environment and this in turn
appears to be accompanied by stability in the biological processes occurring in these waters. On the
other hand, the dominant physical feature of upwelling regions is their irregularity even under normal
conditions and this is paralleled with a constantly changing biological picture.

Unfortunately our knowledge of the upwelling process is still far from being quantitative and until
we can measure the processes of advection, eddy diffusion and mixing in the upwelling water we can
go no further than to describe a very generalized picture of the environment and conjecture about the
processes occurring therein.

Nor do the biological phenomena lend themselves to ease of measurement, continually undergoing
rapid and extensive fluctuations. Steeman-Nielsen and Jensen (1957) have shown how the high-
standing crop of phytoplankton is accompanied by a high rate of primary production. The transfer
of organic matter through the organic cycle is initially dependent on the grazing of the herbivorous
animals, and the success of the transfer depends on the efficiency of the grazing process. The high-
standing stock of higher animals in the area shows that the extent of the grazing must be very great.
Nevertheless plants which are not eaten eventually sink, die and decompose, and in the bottom deposits

286 DISCOVERY REPORTS

of the South-west African region there is evidence that sinking and death of the phytoplankton occurs
on a large scale. This, together with the ephemeral nature of the upwelling, leads one to question the
efficiency of the grazing and to suppose that it may not reach its potential level, and that much
organic matter may be lost at this early stage in the organic cycle.

It is tempting to speculate on the possible interactions of primary production, sinking and grazing
in a region such as this, but our data do not permit us to put any time-scale on the processes involved
and so at best such a discussion would be truly speculative. Clearly this would be one of the prime
considerations in any more extensive a study which might be contemplated in the future. It is quite
outside the scope of an exploratory survey such as was made by the 'William Scoresby'.

SUMMARY

The R.R.S. 'William Scoresby' made two surveys of the waters off the South-west African coast as
part of a more extensive programme of oceanography and whale-marking in the Atlantic and Indian
Oceans.

These surveys, the first in autumn (March) and the second in spring (September-October) 1950,
were planned to obtain a more detailed picture of the water movements and biological features of this
region than had hitherto been attempted. Furthermore, the comparison of this region with the Peru
coastal current which had at an earlier date been surveyed by the same ship and with other upwelling
regions was one integral part of the wider field of work, the study of organic production in the oceans.

The report commences with a brief account of the early voyages and previous scientific work in this
region, notably referring to the work of the 'Meteor' expedition, 1925-7, some of whose observations
were made in South-west African waters.

The oceanographical methods used on these surveys are described together with the various
laboratory techniques and methods of analysis which were later used in interpreting the observations.
This section on the work of the R.R.S. ' William Scoresby ' is concluded with a detailed account of the
itinerary of each survey.

A description of the topography of the coastal region of South-west Africa and the adjacent sea-floor
follows. An outstanding feature of the coast is an extensive arid desert, the Namib desert, whose
existence is intimately connected with the presence of cool surface-waters along the coast. On the
sea-floor, the continental shelf has a width of some 40-80 miles and from the edge the bottom slopes
away steeply into the abyssal depths of the Cape and Angola basins. These basins are separated by
the Walvis Ridge, a prominent feature which connects the continent of Africa to the Central Atlantic
ridge.

The wind system over the south-west African region is shown to be divided into two well-defined
components, the south-east trade wind which predominates over the oceanic waters and the diurnally
variable coastal winds which prevail in a belt extending seawards some 80 miles from the coast. The
trade wind can be considered as the eastern limb of the anti-cyclonic circulation of air over the South
Atlantic and the coastal winds as a divergence of the coastal boundary of the trade winds, resulting
from the extensive diurnal pressure changes over the continent. The coastal wind of importance is
S.S.W., which brings warm, moist air from the ocean over the cool coastal waters, and leads to the
formation of fogs and the aridity of the land to leeward.

During the surveys, the trade wind was weaker in March (survey I) and better developed in
September-October (survey II). The coastal winds were on the whole weak in March and stronger in
September-October.

The sea-surface currents are, like the winds, divisible into two clearly defined circulations. In the

SUMMARY 2S7

region of influence of the trade wind, a N.N.W. flow is induced and this forms the eastern limb of the
anti-cyclonic circulation of the South Atlantic. Nearer the coast and sharply demarcated from this
drift, the currents are variable, and as the oceanographical observations show, are characterized by
pronounced vertical movements. We have restricted the use of the name Benguela current to this
coastal circulation in which the upwelling movements occur and have referred to the oceanic circulation
as the 'south-east trade wind drift'.

The distribution of temperature and salinity of both surveys has shown that these two currents are
characterized by two different types of water — the coastal or upwelled water, and the oceanic water
which is warmer and more saline. Varying mixtures of these two types occurred in some areas.

A comparison of the two surveys showed that while in September-October (survey II) active
upwelling was taking place over most of the region surveyed, in March (survey I) the waters were
more quiescent and a large part of the coastal region was occupied by an influx of mixed oceanic water.

The relationship of the water masses in the south-west African region to those in the South
Atlantic as a whole is discussed at some length, and it is evident that the cool, less saline coastal waters
are derived from the South Atlantic central water at subsurface depths (200-300 m.) offshore.

A computation of the dynamic height anomalies of the sea-surface relative to the 600 db. surface
agrees essentially with the deduced water-movements and emphasizes the eddy-like nature of the
coastal circulation. The topography of the 200 db. surface (relative to 600 db.) depends on rather few
observations at this depth, but indicates a southerly flow along the edge of and converging with, the
continental shelf. It is suggested that this is a replacement flow for the water which is upwelled, and
it has been termed the 'compensation current'.

The mechanism of the upwelling has been examined, and it was found to be essentially similar to
the process off California described previously by Sverdrup (1938). Where the upwelled waters of the
Benguela current meet the warm oceanic waters a convection cell develops, which forms a sharp
boundary, and the position of this, although variable, lies some 40-80 miles offshore, in the vicinity of
the edge of the continental shelf and the position of divergence in the surface wind system.

The distribution of dissolved oxygen in the subsurface ' compensation current ' suggests that the
latter is continuous with the oxygen minimum layer in the equatorial parts of the ocean, and may
indeed arise from the latter. The impoverishment of oxygen in this water which is evidently the source
of the upwelling water, is further accentuated by the decomposition of organic matter on the sea-bed
of the continental shelf, and in certain areas anaerobic conditions are created where sulphate-reducing
bacteria thrive and liberate hydrogen sulphide into the overlying waters. In March (survey I) the
depletion of oxygen extended to the sea-surface inshore at Walvis Bay and we believe this may have
contributed to a small mortality of fish which occurred at Walvis Bay during the survey. The associa-
tion of this phenomenon with the incursion of mixed oceanic water and calm conditions at Walvis Bay
suggested a correlation between the fish mortalities and such conditions, and examination of earlier
records of winds, strengthens the correlation between mortalities and calms or northerly winds in this
area.

The considerable amount of decomposition of organic matter taking place on the sea-bed of the
continental shelf led to a further enrichment of the already phosphate-rich upwelled water.

On survey II an attempt was made to determine the total extent of the anaerobic or 'azoic' zone
on the sea-floor of the continental shelf. This was found to extend, at least in patches, for a distance
of 400 miles along the coast.

The terminology used in the account of the microplankton and the taxonomy of the main groups
met with during the two surveys are discussed at length. Part arbitrary groupings, devised solely to
aid presentation of these data, are also described in detail. Drastic changes in the accepted practice in

288 DISCOVERY REPORTS

the literature of the subject over the last few years seem to make this essential. For the same reason
full notes are given on recent changes in taxonomy of certain individual species better known under
earlier names.

The diversity of the microplankton is demonstrated by the full list of all microplankton categories
recognized during the routine analyses, and tabulation of the records of frequency of occurrence and
of dominance.

The next two subsections deal with the distribution of the main groups of the microplankton, and
in particular the distribution of the dominant group, the diatoms; arrayed according to the grouping
devised for this purpose. The two surveys are treated separately with the aid of diagrams and tables.
This shows that the general pattern of distribution of the more important microplankton species
conformed fairly closely to the disposition of the water masses.

In the rich upwelled coastal waters chaetocerids were dominant, with certain markedly neritic
species from the other groups (e.g. Stephanopyxis turris, Encampia zoodiacus, Fragilaria karsteni and
Asterionella japonica). The extent and average intensity of the rich inshore phytoplankton were
greatest during the first (autumn) survey, though the heaviest individual hauls were obtained in spring.
Forms such as Planktoniella sol and Thallassiothrix longissima were typically dominant in the much
sparser phytoplankton of the offshore waters, together with certain solenoids during the second survey.
The transition zone, which seems nearly to coincide with the hydrologically determined divergence
region, usually contained a scanty microplankton consisting mainly of more panthalassic types from
either of the main habitats.

The more extensive coastal production in autumn (survey I) with numerous resting spores of the
dominant chaetocerids is thought to represent a late stage in the succession of waters earlier enriched
by upwelling, since that process was proceeding but weakly at the time. Probably this is not a purely
seasonal effect, for upwelling probably persists, intermittently, throughout most of the year. Hence
the succession may be repeated several times annually. During the spring survey (II) the rich coastal
area was narrower, and the proportions of the dominant species rather different, with few resting
spores. Upwelling activity was great, as shown by marked instability of the surface-layers among other
hydrological features. Here an early stage in the probable succession is postulated, some of the
enriched water having risen to the euphotic zone too recently for the phytoplankton crop to have taken
full advantage of it. Attention is drawn to the analogy with conditions observed in the California
current by workers benefiting from more complete seasonal coverage (Sargent and Walker 1948).

Conversely, the scanty offshore phytoplankton was much richer during the spring survey than it
had been during the autumn. Here it seemed that the increased turbulence occasioned by greater
wind stress was proving definitely beneficial to plant production.

In the section on special distributional features, species have been selected whose distribution in the
routine hauls seemed best to illustrate either the general distributional trends or divergence from the
pattern typical of the group to which they belong. Their distribution is described and charted in detail.

Observations on visibly discoloured sea-water within the area surveyed confirmed that the dark
green to opaque black appearance of large areas near Walvis Bay was due to the dense population of
inshore diatoms, as Gilchrist (1914) had previously recorded. Chaetoceros didymum and Asterionella
japonica were two of the species mainly responsible. Within this same area more localized brownish
discolorations were also seen, and three samples from these showed the development of a definite
' bloom ' of Peridinium triquetrum, with lesser numbers of Prorocentrum micans and diatoms, some-
times associated with lanes of salps and ctenophores dying at the surface. A minor fish-mortality had
occurred near Walvis Bay just before. Detailed analyses of these samples are given, and their possible
significance in relation to mortality phenomena discussed.

REFERENCES z89

On the second survey one intense red discoloration was seen close inshore in the extreme north
of the area, which was found to be due to the ciliate Cyclotrichiam meumeri Powers ( = Mesodinium
rubrum Lohmann) and its associated symbiotic alga. This is discussed in relation to previous observa-
tions of it round Cape Province, and recent revisions of the taxonomy.

A rearrangement of the data concerning the main diatom groups, based on arbitrarily selected
distance limits, illustrates the distinction between offshore and inshore diatom floras, and provides
some basis for ecological characterization of the species within each of the groups, somewhat on

Gran's lines.

This concept is carried a stage further in an attempt at ' ecological characterization ' of the more
important plankton diatom species of the area. Comparison with their recorded distribution elsewhere
shows that they are even more cosmopolitan than was generally recognized hitherto. This lends point
to the argument that it is the relative importance of the various forms, rather than their mere presence
and absence, that must be studied before the relations between marine plankton floras and their
'conditions of existence' begin to be perceptible. In this there seems to be a basic contrast between
the planktonic floras and faunas, for 'presence or absence' is often of real significance in the latter.

The zooplankton has been completely sorted only from survey I. Some groups have been reported
on and the findings of these are summarized. The outstanding feature of the zooplankton distribution
appeared to be its greater independence of specific water masses than the phytoplankton and a con-
spicuous patchiness in the distribution of some species.

A brief account is given of other life in the current— notably the fish, seals and whales, and also the
guano islands, all of which are outstanding economic features of the region.

Reference is made to a spawning ground of the South African pilchard, located between Walvis
Bay and Sylvia Hill. This is a point of some importance but has been dealt with in a separate
publication.

Many features of the Benguela current are similar or analogous to those of other upwelling regions
and a concluding section is devoted to comparing the main features of the four major upwelling
regions of the world. The extraordinary richness of upwelling regions in comparison with the adjacent
oceanic waters presents interesting material for speculation on the process of organic production in
these environments. At present, however, our knowledge of the magnitude of the processes does not
permit any quantitative treatment of this problem.

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and 240.

[Discovery Reports. Vol. XXXI, pp. 299-326, February 1961)

THE APPENDAGES OF THE HALOCYPRIDIDAE

E. J. ILES

(Department of Zoology, The University of Manchester)

CONTENTS

Introduction page 301

The Appendages, their Interrelation and Function .... 302

Antennules ............ 302

Antennae ............ 303

Labrum 305

Mandibles 306

Paragnaths 311

Maxillulae 311

Maxillae 313

First trunk-limbs 316

Second trunk-limbs . . . . . . . . . • 3J7

Furca ............. 317

Penis 318

Feeding-Mechanism 318

Type of food 318

Feeding on fine material . . . . . . . . .318

Feeding on large material 320

The Appendages in other Halocyprididae 321

Comparison of Halocyprididae and Cypridinidae .... 322

Summary 324

References 325

THE APPENDAGES OF THE HALOCYPRIDIDAE

By E. J. lies

(Department of Zoology, The University of Manchester)
(Text-figures 1-14)

INTRODUCTION

A prolonged systematic study of ostracods has impressed me with the remarkably constant
pattern of the structure, even to the fine details of setation, of the appendages of the Halo-
cyprididae. In earlier literature (Muller, Claus, Sars, Vavra), brief descriptions of the anatomy of
these animals are to be found, but they usually refer only to isolated limbs or to the carapace. More
recently Skogsberg (1920, 1946) has given minute details of the structure and setation of appendages in
a number of species, but nowhere is there a description of the anatomical and spatial relationship of
the various limbs to each other. This is essential to the proper understanding of the functional
morphology, the way in which the limbs are used, which, in its turn, is essential as a background to
further advances in the study of the taxonomy and thus the evolution of the group. The following
paper is an attempt to supply this deficiency.

The family Halocyprididae is included in the Myodocopa, which is characterized as follows : shell
generally with an antennal notch ; seven pairs of appendages ; frontal organ usually present ; antenna
biramous with well-developed propod, exopod multiarticulate and bearing natatory setae, endopod
normally small and often prehensile in the male; mandibular palp pediform; caudal furca with
lamellar rami bearing marginal spines. All the members of the Halocyprididae are planktonic and
have appendages adapted to this mode of life.

Although numerous species have been studied during the course of my work, one was selected for
intensive study, namely Conchoecia borealis G. O. Sars var. antipoda G. W. Muller, not because it is
more typical of the group than any other species, but because material fixed in alcoholic bouin was
available in the Discovery collections. This had been very kindly handed to me by Professor H.
Graham Cannon. The material was suitable for cutting wax sections which could be used to check
certain features of anatomy. Formalin-fixed material also available from the Discovery collections was
unsuitable for embedding in wax. It was used, however, for the preparation of thick celloidin sections
for study by methods similar to those described by Professor H. Graham Cannon (1933). The greater
part of my work on the group, however, has been carried out by the use of fine or microdissection
methods. After removing the carapace, antennules and frontal organ, the remaining appendages of
the left side of the animal were separated by cutting the arthrodial membranes by which they articulate
with the body. By this means, not only could an independent study of the isolated appendages be
carried out, but the body of the same animal could be mounted left side uppermost. With sufficient
care in dissection, the relationship of the inner faces of the undisturbed appendages of the right side
could then be studied. In preserved material the appendages occupy a range of positions which must
represent those which they could take up during life. Study of a number of such specimens and the
articulation and musculature of their appendages has been of value in interpreting the observations
of live animals made by Muller (1894).

Muller (1906), whose figures were quoted by Skogsberg (1920), gave a very wide distribution for

3°2 DISCOVERY REPORTS

Conchoecia borealis antipoda, between i° S. and 650 S. in the Atlantic Ocean at depths of 470-1600 m.
The Discovery specimens used for study were taken at stations 138, 529, 661, 662 and 671 which
ranged from 430 08' S. to 57° 36' S. From the data provided by the samples taken with closing
nets the specimens would appear to have been captured at depths greater than 250 m. to below
1000 m. The species would appear to be a deep-water form.

Miiller (1906) regarded Conchoecia borealis and C. antipoda as separate species, but Skogsberg (1920)
stated that the differences between them were too small to merit greater rank than that of a variety.
Both authors found the females to be larger than the males ; the Discovery specimens bear out this
difference in size. Skogsberg (p. 718) also found 'that the shoulder-vault had a sharp edge contrary
to what is stated by G. W. Miiller 1906', both males and females being alike in this character. In
the few males examined from the Discovery collections the shoulder-vault was sharp-edged but not
quite so far expanded as in the females. Skogsberg described the setation of the appendages in great
detail, but some repetition and further discussion has been found necessary in this report.

The intensive study of C. borealis antipoda leads on to a comparison with other halocyprids, e.g.
Archiconchoecia, Euconchoecia and Halocypris and to a comparison of this group with the Cypridinidae.

ACKNOWLEDGEMENTS

I wish to thank the National Institute of Oceanography, and in particular Dr Mackintosh and
Dr Bargmann, for making their valuable collections available to me for study. My thanks are especially
due to Professor H. Graham Cannon for his continued encouragement and interest in my work.

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION

Antennules (Figs. 1 and 2)
The antennules are uniramous and exhibit sexual dimorphism. Their shafts articulate antero-dorsally
with the body of the animal, close beneath the hinge of the carapace. They are normally directed
straight forward.

In the male (Fig. 1 B) each is rigidly bound to the long slender shaft of the frontal organ by a single
pair of inner dorsal hooked seta. The three terminal setae are of great length. Of these latter, the
principal and one of the secondary setae bear an armature of spines and setules, which lock them
together for part of their length. Only the apices diverge. This armature differs in other species and
is a specific character of differential value. The setae are directed forward and slightly downward
through the anterior gape of the carapace. By flexure of the apical articles of the antennule, they can
be folded back and beneath the animal, between the bases of the appendages. Besides the principal
and secondary seta there are two so-called ' tube-setae ' near the apex of the antennule. These are
much shorter than the principal setae, stout, bluntly ending and very thin walled.

In the female (Fig. 1 A) the shafts of the antennules are not locked to the frontal organ. The inner
dorsal setae extend forward to just beneath the rostrum. A single apical seta, corresponding to the
principal seta of the male antennule, is extended forward and downward, but its length is such that it
extends only slightly beyond the margin of the carapace (Fig. 2, a1s). The secondary setae of the
female are similar to the sensory tube-setae of the appendage of both sexes. In both sexes these
terminal tube-setae are carried hanging downward within the anterior gape of the carapace.

It would seem that in the halocyprids the function of these appendages is largely sensory, though
there is no experimental evidence of this. The thin- walled tube-setae are of a type similar to other
' chemo-sensory ' setae found in the Crustacea. They lie directly in the path of the water-current
flowing through the carapace, because they hang vertically in its anterior gape. The principal setae,

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION

303

as already mentioned, show sexual dimorphism and specific variation in their armature, and may have
some special secondary sexual function. The fact that in some species, even in the male, their free
tips have a structure similar to the sensory tube-setae may mean that they also are sensory.

1° ks sh

Fig. 1. Conchoecia borealis antipoda. Right antennule from inside. A, female; B, male with frontal organ, f.o. frontal organ;
h.s. hooked seta; sh, shaft; a and c, tube setae; b and d, secondary setae (tube setae in female); e, principal seta.

Fig. 2. C. borealis antipoda. Female with left valve of carapace removed, antennal exopod omitted. alt antennule; ats, prin-
cipal seta of antennule; a2, antennal shaft; a2en, antennal endopod; c.f. caudal furca;/.o. frontal organ; ist, isthmus linking
body to carapace; lb, labrum; tnn.b. mandibular basis; mn.c. mandibular coxa; tnn.p. mandibular palp; mxlt maxillule;
mx2, maxilla; trv first trunk limb; tr„, second trunk limb.

Antennae (Fig. 2, a2, Fig. 3)

The antennae are biramous with the exopod composed of eight or nine articles and the endopod small
with not more than three articles. The endopod shows sexual dimorphism. As in most Myodocopa,
each relatively enormous, broadly expanded shaft contains a powerful musculature. Each articulates

3o4 DISCOVERY REPORTS

antero-laterally with the body just behind the antennules and extends straight forward. The multi-
articulate antennal exopod with its long natatory setae is similar in both sexes. It articulates somewhat
to the outside of the apex of the shaft, the articulation corresponding exactly in position with the base
of the antennal notch of the carapace (Fig. 2). It can be extended through this notch or withdrawn
into the carapace and then lies beneath the body of the animal, with its natatory setae embraced by
the palps of the mouth-parts and the bases of the first trunk-limbs.

The broad, flattened basal article of the endopod (Fig. 3) articulates with the shaft on its inner
surface near the apex. It bears two short setae which differ in structure in different species. The
second article bears two setae of moderate, but unequal length, of which at least the apices are thin-
walled. Besides these, in the male there are three very short setae, but not more than one of them is
present in the female; in the female of Conchoeia borealis antipoda they are all absent. The end-article
bears three 'tube-setae' similar to those of the antennule. In the male there is a clasping organ

Fig. 3. C. borealis antipoda. Right antenna from inside. A, female; B, endopod of male.
c.o, clasping organ; en, endopod; ex, exopod; n.s, natatory setae; sh, shaft.

(Fig. 3 B, c.o) which Skogsberg (1920) considered to be a modification of the end-article itself. This
is a hook-like structure which differs somewhat in form on the two sides of the animal, and also
differs in different species. Normally the longer setae of the ramus extend vertically downwards, just
within the anterior gape of the carapace ; the ramus can, however, be moved antero-posteriorly.

The main adaptation of the antenna is for swimming. The exopod of the appendage can be extended
through the antennal notch and moved freely, even when the valves of the carapace are tightly closed.
The form of this notch and hollowing of the carapace below and behind it allow free backward move-
ment of the exopod. The exact match in position of the articulation between the antennal exopod and
shaft with the notch leads to the notch serving as a rowlock for the backward stroke of the oar-like
exopod and its natatory setae. The articulation is bicondylar, with the one condyle ventral and the
other dorsal but slightly displaced outward and forward. The main part of the musculature enclosed
in the antennal shaft is the flexor musculature of the exopod. Skogsberg (1920) described the swimming
action of the antennae and pointed out that it resulted in a forward propulsive stroke. In fact, the
bicondylar articulation leads to the exopod swinging back in an arc with a slight downward movement.
This downward movement gives a slight uplift to the front of the body exactly like that produced by
our arm action in the breast stroke. Uplift in the water will also be produced by the boat-shape of

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION 3°5

the carapace. In Conchoecia borealis, as in many other species, development of the shoulders of the
carapace into sharp flanges provides hydroplanes which also contribute to uplift of the animal when
it is swimming. The main component of the swimming-stroke can thus be concerned with forward
propulsion.

As has been pointed out, the antennal endopod shows sexual dimorphism. The tube-setae are
probably sensory, and in the male the hooked clasping-organ probably had a copulatory function.

Fig. 4. C. borealis antipoda. A, transverse section through labrum and mandibular basis showing distal articular process of
coxa in labral socket; B, right mandibular coxa and part of basis from inside, ax, dorsal articular condyle of coxa; a.p, distal
articular process of condyle; a.p.m, anteroposterior labral muscle; b, basis; b.c, articular surface of basis and coxa; b.in, in-
cisor edge of basis; c, coxa; c.in, incisor edge of coxa; fl, anterior dorsal flange of coxa; Ib.g, posterior labral gland; Ib.s, wall
of labral socket.

Labrum (Figs. 2, 4, 7, 8, 10)
The labrum is well developed and filled with gland-cells. It is usually described as being helmet-
shaped. In section, its ventral surface is flattened and its dorsal surface rounded (Fig. 4 A). It arises

3o6 DISCOVERY REPORTS

ventrally in front of the mouth and projects forward below and between the shafts of the antennae.
The vertical posterior surface forms an anterior boundary to the oral atrium (Fig. 8). The atrium is
bounded laterally by the mandibles, paragnaths and maxillules, and leads antero-dorsally into the
oesophagus, which is directed slightly forward and upward. The posterior wall of the labrum usually
bulges back to some extent, between the mandibular coxae. It is, however, provided with antero-
posterior muscles (Fig. 4 A, a.p.m.), which can draw it forward and so increase the volume of the
atrium. It bears a median patch of short, fine, dorsally directed bristles (Fig. 8). Ventrally to the oral
atrium, a thin flat surface, with thickened cuticle, extends back horizontally from the labrum like
a shelf. This may be termed the labral lamina (Fig. 8, lb. I). Laterally, the posterior edge of this
lamina takes the form of comb-like structures. The whole posterior surface of the labrum and the
labral lamina is supported by sclerites continuous with the ventral sclerite system of the animal.

The labrum contains two systems of glands. The anterior of these consists of a number of large
unicellular glands, closely packed and running dorso-ventrally. Their openings are evenly spaced over
the ventral and lateral walls of the labrum. The openings can only be seen clearly in heavily stained
material (e.g. with chlorazol black), when they appear as small crater-like depressions. The second
system is a paired compound gland, the two components of which lie partly within the posterior part
of the labrum (Fig. 4 A, Ib.g), but extend into the body on either side of the oesophagus. These latter
glands open through the posterior wall of the labrum into the oral atrium.

Fig. 5. C. borealis antipoda. Right mandible from inside, b, basis; b.in, incisor edge of basis; c, coxa;
c.tn, incisor edge of coxa; en, endopod; ex, exopod; m, molar surface of coxa.

Mandibles (Figs. 4, 5, 6)

Possibly the most interesting feature of the appendages of the Halocyprididae is the structure and
articulation of the mandible. Each mandible is biramous, the endopod being large and pediform, the
exopod minute. There have been frequent references in the literature to the presence of a gnathobase
on its basis as well as on its coxa. This feature is in fact used as a character diagnosis of the whole
group.

The coxa is elongate (Fig. 4 B, c, Fig. 5) and articulates with the side of the body immediately
behind the base of the antenna (Fig. 2). The dorsal part is narrow and extends between the base of
the antenna and the isthmus which links the carapace with the sides of the body of the animal. The
anterior surface of this extension is laterally concave to accommodate the backward swelling of the
antennal base. At the apex of the extension there is a cuticular thickening which forms the articular
condyle (Fig. 4 B, a.c). Just beneath this condyle a rigid triangular flange (Fig. 4 B, ft) extends
forward. Curving downward and inward below the articulation with the body, the gnathobase

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION

3°7

(Fig. 4, c.in) extends into the oral atrium. As mentioned above, it forms a lateral boundary to the
atrium (Figs. 7 and 8). Anteriorly at this lower end the coxa is produced into a distally directed
process (Fig. 4 B, a.p), which Skogsberg (1920, p. 570) describes as more or less triangular and 'against
which the endite on the following joint rests with an antero-inner edge'. Skogsberg also refers to the
term 'Zahnhocker' adopted by Claus (1891) for this process. In fact the structure is much more
rounded than is suggested by these descriptions and is directed (it should be noted) much more nearly
parallel to the longitudinal axis of the coxa than is shown in the figures given by Claus (1 891, pi. xxn,
figs. 6 and 15). The statement that the endite of the following joint rests on it is quite erroneous.
No doubt Skogsberg based it upon observations of isolated mandibles. Examination of the appendage
in situ and in section, shows that the process fits exactly into a thickened socket, which is part of the

Fig. 6. C. borealis antipoda. Diagrammatic anterior view of a thick transverse section through mandibular region. (Antennal
shafts omitted to show mandibular coxae.) a^f.o, base of antennules and frontal organ; a2, antennal socket; a.c, dorsal
articular condyle of mandibular coxa; a.p, distal articular process of mandibular coxa; fl, anterior dorsal flange of mandi-
bular coxa; ist, isthmus linking body with carapace; lb, labrum; mn.b, mandibular basis; mn.c, mandibular coxa.

sclerite framework supporting the oral surface of the labrum (Fig. 4 A, a.p and Ib.s, Fig. 8). The
projection of this peg into the socket in the labrum is sufficiently deep to make it difficult to remove
the appendage during dissection. The mandibular coxa is thus restricted in its movement to rotation
about the axis formed by this articular process and the dorsal condyle. This axis, in fact, coincides
fairly accurately with the anterior margin of the area of articulation of the coxa with the body
(Fig. 4 B). In relation to the body of the animal, the axis of rotation of the coxa extends upwards,
sloping slightly outwards and backwards (Figs. 2 and 6).

The mandibular musculature has been figured by Muller (1894, pi. 55). The extrinsic musculature
of the coxa is in fact very much more complex than is shown in his figures. Full details of this
musculature will not be given here, but it is significant that the arrangement of the muscular elements
is such that they will rotate the coxae about the axes which result from their bicondylar suspensions.
The anterior dorsal muscles originate near the hinge-line of the carapace and are inserted on the
flanges anterior to the dorsal condyles. Since the axes of rotation of the coxae slope markedly out-

3°8 DISCOVERY REPORTS

wards dorsally, these muscles extend at wide angles to them. Contraction of the muscles will result
in outward rotation of the coxae so that their gnathobases separate. The posterior dorsal muscles
originate near the anterior dorsals and are inserted on the posterior margins of the coxae. On con-
traction they will rotate the coxae inwards, bringing the gnathobases together. It is the transverse
musculature which is so complex. Elements of it originate on various parts of the anterior hypostomal
apodeme, or intermandibular tendons fused to it and on the antenno-labral apodeme. These are
inserted on various parts of the coxae. The majority will rotate the coxae inwards, giving a powerful
biting action by the gnathobases.

The coxal gnathobase is, as has frequently been pointed out, complex in structure. For the purpose
of description it may be considered in four parts. Curving into the oral atrium distally, immediately
above the posterior labral shelf, are three parallel incisor edges (Figs. 4, 5, Fig. 8, c.iri). Although, as
Claus (1891) pointed out, the structural pattern is more or less specifically constant, there is in
Conchoecia antipoda, as in other species, some individual variation. Broadly speaking, the distal ridge,
which extends the full width of the gnathobase, is, at least posteriorly, clearly divided into teeth. The
middle and proximal ridges are much less regularly toothed, but always bear a long tusk-like posterior
tooth. Dorsally to these ridges, the surface is shallowly concave. At the base of this depression there
is a ridged pad, the masticatory pad (Fig. 5, Fig. 8, m). Skogsberg (1920) describes this as being covered
with fine papillae placed close together. Muller (1894) more correctly refers to it as bearing isolated
conical spines. These short sharp spines are so closely packed that the surface formed by their tips
does in fact give the impression of being papillose. It is only by focusing through their depth in a
whole mount, or seeing them in section that a true picture of the structure is obtained. The third
region is the posterior margin of the gnathobase. Here there are four stout spines arranged in a dorso-
ventral row (Fig. 8, m.c). These curve into the oral atrium and radiate slightly along the length of the
row. Posterior to these teeth there is a dense group of radiating ' needle spines ', each of about the
same length as one of the teeth (Fig. 8, tn.f). The fourth structure is a dorsal group of fine spines,
almost continuous in distribution with the posterior group, but directed towards the mouth and
projecting slightly into it.

The basis articulates with the coxa so that it extends forward almost at right angles to the latter
(Fig. 4 A, Fig. 5). It is clear that its main movement is through a dorso-ventral arc, but rotation of the
coxa about its axis will of course move the distal end of the basis laterally inward or outward. On the
inner face of the basis, near its distal end, is a fine seta of moderate length, which extends inward across
the labrum. At the anterior edge of the gnathobase are two setae, one long and one short, which
extend ventrally. On the ventral surface of the gnathobase itself, are two further closely adjacent
setae, which also extend ventrally and somewhat posteriorly. Near its distal end the basis bears
dorsally a small mamilliform appendix (Fig. 5 ex, Fig. 7, tnn.e), with a long anteriorly directed seta.
Muller (1890, 1894) and Skogsberg (1920) have referred to this structure as representing the exopod
of the appendage.

Proximally and ventrally a flange of the basis extends inward to form the gnathobase (Figs. 4, 5, b.in;
Fig. 8). This gnathobase lies ventral and parallel to the incisor edges of the coxal gnathobase. It is
separated from the latter by the backwardly projecting labral lamina (Fig. 8). The basal gnathobase
consists of a single sharp biting edge formed by a row of six shouldered teeth. It is followed posteriorly
by first an isolated spine, then a short, stout, spine-like seta. Ventral to the incisor edge is a single
serrated tooth (Fig. 8, v.i). On the posterior ventral surface of the gnathobase are a series of short, stout,
bristles. The basis and coxa articulate with each other by a fulcrum, which occurs about midway
between the distal articular process of the coxa and the upper surface of the joint (Fig. 4 B, b.c). It is
clear that rotation of the basis about this fulcrum will produce a backward and forward movement of

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION 309

the gnathobase and this, if the coxa gnathobase remains rigid, will produce a shearing action. Rotation
of the coxa will lead to a biting action of the gnathobases of the bases as well as of those of the coxae.
The two apical articles of the three-jointed palp are somewhat flattened transversely. The tip of
the palp bears two stout claw-like setae (Fig. 5). These are pectinate on their posterior margins and
curve posteriorly towards their tips. One of these claws is equal in length to the palp itself, the other
is about two-thirds of this length. Besides these, there is, near by, a more slender seta of about the
same length as the shorter claw and also a series of four fine setae of about half this length. A series
of setae are present on the anterior margin of the palp. When the palp is folded inwards these extend
towards the margin of the carapace. Distally on the middle article is a long stout pectinate seta, which
is, however, more flexible than the terminal claws. Its length is such that it extends almost to the
apex of the shorter terminal claw. Adjacent to it are two much shorter fine setae. A further short

0'5 mm

Fig. 7. C. borealis antipoda. Mouth and first trunk appendages viewed from mid-line; caudal furca in front of tips of trunk
appendages shown in outline; armature of setae omitted, mn.b, mandibular basis (gnathobase); mn.e, mandibular exopod
(mammiliform appendage) ; tnn.p, mandibular palp (endopod) ; mxl p, palp of maxillule ; mx2en, maxillary endopod ; mx2ex,
maxillary exopod ; trxex, exopod of first trunk limb.

seta arises near the apex of the proximal article. The posterior margin bears a further series of setae.
There are two long pectinate setae of the same form as the long anterior one. The first of these arises
near the distal end of the middle article and the other from a similar position on the proximal article.
Both reach to near the apex of the shorter terminal claw. The middle article bears a shorter fine seta
on its posterior distal margin and the proximal article three similar short fine setae distributed along
the distal half of the posterior margin. All the finer setae bear fine secondary setules. The articulation
of the proximal article of the palp with the basis is provided with lateral cuticular facets which limit
its movement to a dorso-ventral direction. The limits of movement allowed by the articulation would
seem to be from a position where the proximal article is directed nearly vertically upward from the
basis to one with it directed vertically downward. The second and third articles can be extended
straight in line with the proximal article or flexed toward the body. The articulation of the articles in
series is such that the palp can be extended upwards and outwards, with the terminal claws near
the antennal notch of the carapace, or folded downwards and inwards. Due to a slight diagonal
setting of the articulation between the basale and the proximal article of the palp, the downward and
inward movement is accompanied by a rotation of the palp about its axis, in such a fashion that the

3io DISCOVERY REPORTS

short anterior marginal setae extend across the labrum towards the middle line (Fig. 10) and the short
posterior marginal setae interlace with the ventral setae of the basale (Fig. 7). The length of the palp
and that of the basis are such that during the downward arc of movement of the former, first the
long posterior marginal setae, secondly the apical claws and lastly the long anterior marginal seta
are drawn down the anterior margin of the carapace. At the posterior extreme of this movement,
the terminal claws lie between the palps of the maxillulae and the endopodites of the maxillae. The
posterior marginal setae lie with their tips pressed against the surface of the labrum. Finally the long
anterior marginal seta lies just inside the ventral margin of the carapace, with its apex within range
of the claws of the palp of the maxillule.

The outstanding structural features of the mandible are the presence of a gnathobase on the basis
as well as on the coxa and the bicondylar articulation of the coxa. Skogsberg (1920, pp. 556-7) has
pointed out that the mandible is used for holding food fast and for mastication. With reference to the
incisor edge of the basis, he stated that as G. O. Sars (1887) pointed out, 'it seems to have the same
function as the cutting part on the mandible of many other Crustacea, while the pars incisiva of the
coxa serves as a sort of tuber culum molar e, to break up the food more finely'. He stated that the latter
process also serves partly as a ' cutting organ '. The bicondylar suspension of the coxa, which seems to
be surprisingly uncommon in the Crustacea, is important in that it will enable an extremely powerful
crushing action to be carried out by the gnathobases, while the firm proximal support provided to the
palp will facilitate its independent movement. The disadvantage is that the arrangement will strictly
limit the size of food-material which can be passed between the coxal gnathobases. Borradaile (1922)
has described how in the shore crab (which also has a bicondylar suspension of the mandible) the food
is first broken up by other appendages, before passing between the mandibles. In Conchoecia, it is
difficult to see how, with the possible exception of the maxillules, appendages other than the mandibles
could function in this manner. Quite clearly the shearing action of the gnathobases of the mandibular
bases must have the function of cutting food into pieces which will pass between the gnathobases of
the coxae into the oral atrium. This, as will be shown, is confirmed by the type of food material found
in the stomachs of the animals.

The structure of the coxal gnathobase is complex and so also must be its function. It is interesting
to note its division into incisor and molar processes in a manner similar to that of the mandibular
gnathobase of the Malacostraca. There can be no doubt that the function of the incisor edges of these
structures in Conchoecia will play an important role in breaking up food material passed between
them. It is more difficult to visualize the function of the molar surfaces, with their closely packed
spines. These probably would serve to grip and crush food-material, particularly if this were small, soft
particles. The row of four teeth on the posterior margin of the molar surface must serve to retain
food-material in the oral atrium, which same function in the case of smaller particles would be
served by the fringe of fine spines. The fine orally directed spines will clearly aid transport of food-
material into the mouth.

In his earlier work, Muller considered that the halocyprids might to a limited extent be bottom-
living and use their mandibular palps for walking, as do the cypridinids. It is now clear, however,
that they are planktonic during the whole of their life-cycle. This leaves the mandible free for its
important role in feeding. The palp with its well-developed apical claws, extending beneath the oral
atrium in the flexed position, and its wide arc of antero-posterior movement, is well adapted to grasping
food and bringing it within the range of action of the mouth-parts. In dissected appendages it is
difficult to see what function the marginal setae of the palp could possess in the whole animal, but
when the palps are flexed it is evident that they could aid retention of food beneath the labrum and
oral atrium.

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION

3ii

Paragnaths (Fig. 8)
In the halocyprids the paragnaths are well developed. They extend ventrally immediately behind
and closely investing the hinder margins of the mandibular coxae (Fig. 8, p.g). Each paragnath is
triangular in shape and almost completely occupies the space between the mandibular coxa and the
protopod of the maxillula. The anterior margin, where it borders on the mandibular coxa, is edged
with a series of short fine bristles, which extend forward and inward towards the bristles on the margin
of the molar surface of the mandible.

Functionally the paragnaths are important because they complete the lateral walls of the oral atrium.
The anteriorly directed spinules of their anterior borders aid retention of food material within the
atrium.

Fig. 8. C. borealis antipoda. View enlarged from Fig. 7 of oral atrium, b.in, incisor edge of mandibular basis; c.in, incisor
edge of mandibular coxa; lb. I, labral lamina; Ib.s, labral socket; m, molar pads of mandibular coxa; m.c, molar claws; m.f,
bristle fringe of molar surface; m.t, molar tooth; mxxenx, pre-coxal endite of maxillule; mxlen2, coxal endites of maxillule;
oes, oesophagus; p.g, paragnath; v.t, ventral tooth of basal gnathobase.

Maxillulae (Figs. 8, 9 & 10)
The maxillulae are uniramous, the endopod forming the palp and the protopod bearing well-developed
endites. They arise ventro-laterally, immediately behind the paragnaths and project vertically
downwards.

The proximal article of the protopod, generally considered to be the pre-coxa, is very short. The
coxa is somewhat longer. There appear to be two endites (Fig. 8, mx1en1,mx1en2, Fig. 9), the proximal
being pre-coxal, the distal arising from the coxa. The latter is, however, deeply bifid. It would seem
useful to adopt the view of Muller (1894 et seq.) and Skogsberg (1920), who considered this endite to
consist of two fused endites, comparable to the two distal endites of the cypridinids. The pre-coxal
endite bears a series of stout setae, of which the two nearest the body are brush-setae, the more distal

3i2 DISCOVERY REPORTS

anterior are pectinate and the remainder spine-setae. The proximal endite arises in the angle between
the limb and the body. The ventral body-wall, in preserved material, usually bulges downwards
between the proximal endites of the two sides, but is provided with muscles radiating to it from the
anterior hypostomal apodeme. It would appear probable that this muscular system is used in conjunc-
tion with the labral muscle to enlarge the oral atrium. Depression of the body-wall must be by haemo-
coelic pressure, and flexure of the body. The middle and distal endites bear a series of powerful,
inwardly directed spine-setae. The anterior spine-setae are pectinate with their secondary teeth
apically directed. Skogsberg referred to the movable articulation between the articles of the protopod
and their well-developed independent musculature. He also pointed out that the endites are not
movable in relation to the articles from which they arise. Independent movement of the proximal

0-1 mm

Fig. 9. C. borealis antipoda. Right maxillula from inside, b, basis; c, coxa; e«1, first article of endopod;

en2, second article of endopod; p.c, pre-coxa.

articles is great, but may be analyzed into two main components. One movement of each is rotation
with respect to the length of the limb, thus swinging its endite through a horizontal arc. The other is
a rocking movement which swings the endite through a small vertical arc. Skogsberg pointed out the
marked divergence of the direction of the endites with the limb at rest. He did not, however, point
out their range of movement or their relation to the other appendages. The proximal (pre-coxal)
endites may be more or less directed towards one another across the body when its floor is raised. More
usually they are directed forward between the paragnaths toward the incisor edges of the mandibular
coxae; then the floor of the body is usually depressed. By an anterior rocking of the limb, their setae
are thrust forward and upward between the molar spines of the mandibular coxae, their proximal
brush-setae extending almost to the mouth. The coxa can move relative to the pre-coxa but the
positions of its endites will also depend upon movements of the latter. The total range of movement
of the coxal endites would seem to be from a position where they point straight across the body to one
in which they point somewhat forwards and inwards between the mandibular gnathobases. They may
be depressed to a position pointing slightly ventrally to the gnathobase of the mandibular basis or
elevated so that they point towards the incisor surfaces of the coxa of this limb.

The palp of the maxillula (Fig. 2, Fig. 7 mx-^p, Fig. 9) is generally accepted to be the endopod, but
the basipod, which is very short and bears no endite is, as Hansen (1925) pointed out, partly fused with
the first article of the endopod. The second article of the palp (first endopod article) is the longest of

THE APPENDAGES, THEIR RELATIONSHIP AND FUNCTION 313

the whole appendage. It is broad, being flattened laterally in relation to the animal. On its anterior
border it bears a series of four long setae, which extend forward to the region of the outer setae of the
basis of the mandible. On the posterior margin there are three long setae which extend ventrally and
backwards outside the maxillary endites. The anterior edge and inner face bear three further setae,
which extend medially beneath the endites, together with a single seta arising from the inner face of
the basis. The terminal article is cylindrical, tapering only slightly towards its apex. In Conchoecia
antipoda its length is only slightly greater than the width of the previous article and it is normally
directed backwards at right angles to the axis of the palp. At its apex it bears a group of five setae.
Two of these are stout claws, of which one is about two-thirds the length of the other. Two other
setae are more slender, but claw-like, and of about the same length as the shorter main claw. The fifth
seta is very slender and about the same length as the longest claw. All of these curve forwards.
Muller (1894) stated that the endopod is so bent inwards that it lies nearly parallel to the endites of
the stem. It is true that the palp may take up this position, but it may also slope outwards to some
extent. Besides this, some antero-posterior movement can take place. The end-article seems only
capable of movement through a dorso-ventral arc, relative to the preceding article. The extent of this
movement is from a position in line with the rest of the limb to one pointing posteriorly almost at
right angles to it. Rotation of the protopod about its axis results in movement of the apical article
of the palp through a horizontal arc, so that its total field of action is fairly large. It can be extended
backwards with its claws interlacing with those of the maxilla, or extended forwards with them lying
over or between the gnathobases of the mandibular basis. It does not, however, seem that the claws
can be extended into the oral atrium, or folded inwards sufficiently to reach the endites of the protopod

of the limb.

It has been pointed out above, that the maxillulary palps have anteriorly curved apical claws and
their movement must be mainly through a horizontal arc. In fact it seems probable that their main
function must be to pass food material forward on to the gnathobases of the mandibular bases. The
maxillulary endites are well developed, but their armature is very much less powerful than that found
in the cypridinids where they are used for mastication of the food (Graham Cannon, 1933). It would
seem that in halocyprids they have little masticatory function. The direction in which their few spines
and setae point and their range of movement would indicate that the distal endites probably serve to
grip food in the mid-line and to transfer it from the gnathobases of the mandibular bases to the region
of the incisor edges of the mandibular coxae in the oral atrium. Similarly it seems likely that the
proximal endites push food forward on to the molar surfaces of the mandibular coxae and aid transport
of food into the mouth.

Maxillae (Figs. 7, 10 & 11)
The maxillae are biramous with one ramus jointed and pediform, the other unjointed. The protopod
bears a well-developed epipod.

There has in the past been some variance of opinion regarding which pair of appendages the fifth
pair of limbs of many ostracods represent. Graham Cannon (1925, 1926) has shown quite clearly that,
on the basis of the segmental excretory organs, in Cypridopsis vidua ( = Pionocypris vidua), they are
the maxillae. There is no reason to doubt that they represent the same pair of appendages in the
Halocyprididae. Besides this, however, there are almost as many opinions regarding the homologies
of the parts of the limb as there have been workers on the group. This is too extensive a topic to
consider here in detail. On the basis of the musculature and segmentation of the appendage, it would
appear that Skogsberg's view (1920) is reasonable. This view is: that the shaft extending ventrally
from the body of the animal (Figs. 7, 11) is the protopod; the inwardly directed distal 'endite' with

DISCOVERY REPORTS

mn.g 'fa

Fig. 10. C. borealis antipoda. Ventral view of body (only part of antennae included). a2, antennal shaft; ist, isthmus linking
body to carapace; lb, labrum; mn.b, mandibular basis; mn.c, mandibular coxa; mn.g, mandibular basal gnathobase; mn.p, man-
dibular palp; mxx, maxillula; mx1p, palp of maxillula; mx2, maxilla; mx2v, vibratory plate of maxilla; trv first trunk limb;
trxv, vibratory plate of first trunk limb; tr2, second trunk limb.

independent musculature (Fig. 7 mx2en, Fig. 11, en) is the endopod; and the long posteriorly directed
pediform portion of the limb (Fig. 7 mx2ex, Fig. 11, ex) is the exopod. The vibratory plate would
then be an epipod. In general impression the limb is pediform. The protopod normally extends directly
ventrally beneath the body from a ventro-lateral attachment, immediately in front of the isthmus,

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION 315

which links the body of the animal with its carapace (Fig. 2, tnx2). In this position the vertical
flattened epipod, in the form of a vibratory plate, extends outwards towards the carapace. Plumose
setae, arranged in three groups, extend from the margin of this epipod. At the apex of the protopod
is the large anteriorly directed endite-like structure, which, as already mentioned, is probably the endo-
pod of the appendage. This bears at its apex a group of three pectinate claw-setae, which curve
inwards and slightly backwards (Fig. 10). Dorsally and externally to them are three moderately long,
anteriorly directed brush-setae. The setae of the endopod may be directed towards the apical claws
of the maxillularly palp, but forward movement of the shaft of the maxilla brings them into the region
of the distal endites of the maxillule. A degree of ventral extension of the endopod is also possible.
Proximal to the endopod, there are on the shaft of the maxilla two groups of setae, borne on slight
prominences, which probably represent endites. There are three setae in thedistal group, a long outer
brush-seta, a median brush-seta of about half its length and an extremely short inner seta. The more

02 mm

Fig. 11. C. borealis antipoda. Right maxilla from inside, en, endopod; ep, epipod; ex, exopod; p, protopod.

proximal group consists of a brush-seta of about the same length as the longest in the distal group
and a much shorter seta. The setae in these two groups are directed towards the distal endites of the
maxillule, though their position varies with movement of the shaft and they can be directed more
dorsally towards the proximal maxillulary endites.

The exopod (Figs. 7, 10 and n) is divided into three articles. The first two of these are long, the
terminal very short. The articulation of this ramus is slightly to the outside of the distal extremity of
the protopod and at rest extends back parallel to the body of the animal. At the apex of the exopod
there are two long claw-setae which curve downwards, and a much more slender one. From the lower
edge arise a series of setae extending downwards. These setae are in series with a long brush-seta
extending downwards from the ventral surface of the endopod. Of them, there are four in a group
arising from a prominence at about a third of the length of the proximal article from its base. A further
pair arise near its apex. The second article bears a similar single seta about the middle of its length.
A second series of setae arise from the median face of the exopod and extend inwards across the
mid-line. There are on the first article two of these near to the proximal group of ventral setae and
a third near the distal pair. The second article bears a single medially directed seta near its ventrally
directed seta. Somewhat dorsally from the outer face arise a third series of setae, which extend back-
wards, upwards and slightly outwards. Two of these are near the apex of the proximal article and
a third arises at about two-thirds of the length of the second article.

316 DISCOVERY REPORTS

Besides the antero-posterior movement of the shaft of the maxilla, the exopod is capable of similar
movement. In preserved material it usually lies parallel to the margin of the shell, with its terminal
claws directed straight back. It may, however, be flexed ventrally to produce a curvature of the limb,
while the terminal article may be flexed so far that the claws are directed vertically downwards at right
angles to the remainder of the limb. Professor A. C. Hardy has pointed out to me, in a personal
communication, that the live animal quite normally extends the whole limb vertically downwards.
Such a movement will draw the ventral setae and terminal claws forward along the ventral posterior
margin of the carapace and bring the whole maxilla within reach of the inward arc of movement of
the mandibular claws.

Fig. 1 2. C. borealis antipoda. A, female right first trunk limb from inside ; B, apex of the same appendage in male.

ep, epipod; ex, exopod; p, protopod.

With its wide range of antero-posterior movement and ventrally curved terminal claws, the
elongate exopod of the maxillae may play some part in collection of food. The short endopods, with
posteriorly curving claws, probably play a main role in food transport in conjunction with the
maxillulary palps. The endites, as described above, are very poorly developed. Their long slender
brush-setae may assist in forward transport of fine food-material, but can be of little use for manipula-
tion of larger material. Marginal setae of the exopod may aid retention of food-material.

The epipod of this appendage, in conjunction with that of the first trunk-limb, undoubtedly creates a
respiratory water-current through the carapace in a manner similar to that in Cypridopsis ( = Piotiocypris
vidua) and in Cypridina described by Graham Cannon (1926, 1931). Miiller (1894) had in fact
observed this current in Conchoecia experimentally with the aid of carmine particles. He also described
how the epipods beat continuously and independently of other movements of the limbs.

First trunk-limbs

The first trunk-limbs are uniramous, jointed and pediform. The protopod bears a well-developed
epipod. They show sexual dimorphism. Though very similar in general appearance to the maxillae,
as pointed out by Skogsberg (1920), their endopods are even less well developed. The protopod of
each arises immediately behind that of the maxilla so that it extends ventrally below the posterior
extreme of the isthmus linking the body of the animal with the carapace. It bears an epipod similar
to that of the maxilla. As might be expected from its position in relation to the protopod of the

THE APPENDAGES, THEIR INTERRELATION AND FUNCTION 3>7

maxilla, it bears no endites and no setae. The part of the limb which Skogsberg considered as the
endopod bears a single long brush-seta extending forward towards the mid-line of the animal
(Figs. 7 and 12). The exopod of the appendage (Figs. 7, 10 and 12) has four articles, the proximal
being the longest, the distal, as in the case of the maxilla, being the shortest. In the female, there are
two distal claws and a seta, similar to those of the maxilla, but in the male there are three extremely
long natatory setae, which can curve upwards as far as the hinge-line of the carapace. Further setae
on the exopod may be described as similar to those of the maxilla. Projecting ventrally there is a
single apical seta on the inner face of the protopod in series with two further setae on the first article
and one on the third article. Projecting towards the mid-line from the inner face are three setae on
the first article, one on the second and one on the third. There is only one seta extending outwards
from the limb, on the first article of the exopod. In addition, however, there are further setae (not
represented) on the maxilla— a dorsal distal seta on the first article of the exopod and a dorsal medial
seta on the third article.

Movement of the limb would seem to resolve into an antero-posterior movement of the protopod
and a dorso-ventral extension and flexure of the exopod. The ventral flexure of the limb may not be
as great as that of the maxilla but the dorsal extension is greater.

The epipods of these appendages beat in conjunction with those of the maxillae. It is possible that
the limbs themselves could take part in collection of food, but the enormously elongate apical setae
in the male are strongly suggestive of some function of locomotion in this sex.

side of the
only setae

Second trunk-limbs (Figs. 2 & 13)
The second trunk-limb (Fig. 2, tr2, Fig. 13) is very short with three articles. It arises at the
body just behind the first trunk-limb. At rest it is directed dorsally and posteriorly. The
arising from this appendage are two apical setae, one of which is very long,
extending to the posterior dorsal margin of the carapace and the second of
which is only half the length. Muller (1894) described the movement of this
appendage in some detail. Apparently, as its structure suggests, it is extremely
mobile; it can be flexed or rotated freely.

The immediate function which comes to mind in the case of these limbs,
with their position high on the side of the body of the animal and extreme
mobility, is that of cleaning. Muller, however, pointed out that these limbs
cannot reach the epipods of the maxillules and maxillae, the most obvious
structures to require cleaning. Furthermore he described how these structures
are self-cleaning. Muller was, in fact, not able to observe the second trunk-limb
performing any definite function. Some doubt must thus remain about this.

Furca (Figs. 2 & 7)
The furca of the Myodocopa is so well known as to need little more than brief
mention. Each furcal plate bears eight claws, an anterior group of four large Fig. 13. C. borealis anti-
ones and a posterior of four smaller ones. All eight claws radiate outwards g£ ^ £££?""*
from the furca, the most anterior one, which arises from the anterior border

of the furcal plate, pointing markedly anteriorly. The more posterior claws point slightly back-
wards. All the claws are bipectinate on their posterior margins. Antero-posterior flexure of the
trunk of the animal and hence antero-posterior movement of the caudal furca, can be considerable.
Thus the trunk may be stretched out straight posteriorly to extend the caudal furca through the

3-2

3i8 DISCOVERY REPORTS

posterior gape of the carapace, or it may be flexed forward to bring the furcal claws between the bases
of the appendages. In this latter position, the anterior claws extend between the endites of the maxil-
lules, with their apices almost in the oral atrium. There can be no doubt that these claws have a
cleaning function as is commonly the case in ostracods.

Penis

The structure of the penis of the halocyprids has been described by Skogsberg, but though his and
earlier descriptions make it difficult to understand the three-dimensional structure of the organ, this
is not in itself relevant to the present topic. It is, however, worthy of note that this extremely large
organ is unilateral and set well to the side of the animal. In this position, though it extends downwards
to the ventral margin of the carapace, or even beyond, it does not impede the movement of the limbs
and leaves a clear path for the flexure of the trunk and anterior extension of the caudal furca.

FEEDING-MECHANISM

Type of food

Muller (1894, 1927) stated that the stomachs of halocyprids contained the remains of copepods. He
further stated that these have been trapped on the sticky shell, drawn in by the mandibular palps and
conveyed with the sticky secretion of the shell-glands into the mouth and stomach. Elofson (1941)
also found copepod remains in the stomachs of certain species of Conchoecia and I too have found such
copepod remains in the stomachs of numerous species. I have even seen a specimen of C. bispinosa,
which had a large part of the crushed but only slightly dismembered exoskeleton of a small copepod
in its stomach ; usually, however, the only identifiable remains are limbs, but it has not been previously
noted that these are usually derived from animals of a size equal to or greater than that of the ostracod.
It is difficult to understand how large prey could be trapped in a sticky secretion of the carapace,
unless this secretion was much more copious than would be indicated by the size and number of the
glands. In fact, the stout spines and claws present on the mandibles and maxillules, together with the
powerful gnathobases of the former, give the impression of a voracious predator.

I have noticed that, whether or not there are any copepod remains in the stomach of a halocyprid,
there is usually a mass of fine material. This confirms Muller's observations (1894); but in addition
the material sometimes contains diatom remains, a fact not stated by Muller. The type of food con-
tained in the stomach bears little relation to the size of the animal. Thus, some stomachs of the large
C. valdiviae have been found to contain nothing but fine detritus while, on the other hand, those of
the comparatively small C. echinata have had limbs and other remains of copepods obviously from
animals larger than the ostracod. Diatoms and other fine detritus could have been derived from
the copepods which had been eaten; frequently, however, as has been stated, such material may be
present without any copepod-remains. Furthermore, the appendages, particularly the proximal endite
of the maxillule, have, in addition to spines, an armature of slender setae and brush-setae, which
is reminiscent of a particulate feeder (cf. Cypridina antarctica according to Graham Cannon, 1933).

Feeding on fine material

Whether diatoms or detritus are deliberately collected by Conchoecia as food or are swallowed acci-
dentally is difficult to decide. There is no trace of any filter-feeding-structure in these animals, but there
are two ways in which such material could be collected. Muller's description of the observations upon
which he based his conclusions regarding the feeding of halocyprids provides evidence regarding one
of these.

Muller described (1894, p. 109) how carmine particles, suspended in water in which Conchoecia

FEEDING-MECHANISM 3i9

was swimming, became trapped in the sticky secretion of the marginal glands of the carapace. He
observed this to be drawn in by the mandibular palps and formed into a mass by the mouth-parts.
He pointed out that this process took place whether anything was trapped in the secretion or not.
Elsewhere (p. 127) he stated that he was not able to observe directly that it was swallowed, but found
that the stomach contents were similar in nature to this material. It is perfectly clear, from the structure
of the mandibular palps, that they could draw in the secretion of the marginal glands from the front
half of the carapace, as observed by Muller. The apical claws are suited to such function (Fig. 2),
while the posterior marginal setae and possibly also the anterior marginal setae could contribute to the
process. Muller (1894) held the view, repeated by Caiman (1909), that the greater development of the
anterior marginal glands of the carapace may be associated with this process. It is not, however,
universally true that these glands are better developed than the others. In fact, if anything, Conchoecia
antipoda has them less well developed. It would be possible, however, for the secretion from the more
posterior parts of the ventral margin to be drawn forwards by the anterior curving claws of the
maxillary exopod ( Fig. 2) . The possibility of the limb moving in this fashion has already been considered
(page 316). The secretion could thus be brought within range of the movement of the claws of the
mandibular palps and added to any food collected directly by them. The only appendages which can
reach the posterior margin of the carapace, which is also provided with numerous glands, are the
second trunk-limbs. Their fine setae are poorly adapted to movement of such material, while their
range of movement could hardly bring it within reach of other appendages. Thus although food-
material may be trapped by secretion from the glands of the carapace, these cannot be entirely sub-
servient to this function.

The structure of the appendages shows that Midler's statement, that food-laden secretion dragged
in by the mandibular palps is passed into the oral atrium by the palps of the maxillule, probably does
not cover the whole process. It is improbable that the movement of these structures would be sufficient
to pass material directly into the oral atrium. When the mandibles are folded under the body, their
claws extend into the field of movement of the maxillary endopods (Fig. 7) which with their back-
wardly curved claws could easily withdraw material from the mandibular claws. The maxillulary
palps, with their forwardly curved claws could then draw food-material forward from the maxillary
endopods to bring it below the labrum in the region of the mandibular gnathobases.

The other possible method of collection of fine material is quite different. I have frequently noted
that preserved material may have a mass of detritus held beneath the labrum by the open cage of setae
formed by the infolded mandibular palps. This could of course have been passed forward by the
maxillulary palps, and could also be contained in the secretion from the marginal glands of the cara-
pace, which has been swept in by the posterior marginal setae of the mandibular palps. There is,
however, another possible explanation for the presence of detritus in this region. The beat of the
epipods of the maxillules and maxillae creates a water-current through the carapace, and will carry
detritus with it. Muller (1894) has, indeed, described how detritus is carried in this manner in the live
animal. A large part of the water-current must flow between the mandibular palps and over the
surface of the labrum in just that region where the numerous openings of the anterior labral glands
are situated. This resembles the food-collection mechanism described by Graham Cannon (1933) in
Cypridina. There is no information available regarding the nature of the secretion of the labral glands
in Conchoecia but, if it is comparable with that of other Crustacea, it will be a sticky secretion which
will entangle any detritus swept in with the water-current, as in the case of Cypridina. The secretion
together with the detritus would then be held in place by the marginal setae of the mandibular palps
and be available as a source of food-material. Whether detritus is collected in this manner beneath
the labrum of Conchoecia as food-material can only be determined experimentally.

3-3

320 DISCOVERY REPORTS

But by whatever means fine material is collected, it seems that it will be massed beneath the labrum,
and that transport to the oral atrium must follow. It has been pointed out already that the downward
arc of movement of the mandibular basis brings the incisor edge backwards and upwards into line
with the distal endites of the maxillule. By this means the posterior spines and setae of the basal
gnathobases, together with the gripping action of the incisor edges, could transport food-material into
the path of forward-movement of these endites. By their shearing action, the basal gnathobases may at
the same time cut up any larger material trapped in the secretion. During the upward arc of movement
of the mandibular bases, the lateral combs of the labral lamina would retain material in the oral atrium.

Though the transversely directed spines of the distal maxillulary endites could play some part in
trituration of food, it seems likely that this would mainly be with large material. It is possible that the
peculiar structure of the molar pads on the mandibular coxae is an adaptation for trituration of fine
material. Certainly such material, trapped in sticky secretion, would be retained between them by the
fringing spinules on the posterior margin of the coxal gnathobase and on the anterior borders of the
paragnaths. Forward thrusting of the proximal endites of the maxillules, with their brush-setae and
pectinate spines (Fig. 7) together with that of the few long brush-setae of the maxillary endites, would
all the time tend to move material forward and upward towards the mouth. Here the orally directed
spinules of the coxal gnathobases of the mandibles, together with the spinules on the oral wall of the
labrum, would finally bring food into the mouth. Peristaltic action of the oesophagus would then
take over.

During the whole feeding-process, the marginal setae of the appendages must aid retention of material
in positions where it can be manipulated by the appropriate appendages.

Feeding on large material
Despite his observations of live specimens, Midler quite clearly did not observe a Conchoecia feeding
on a copepod. He found the copepod remains in the stomachs of specimens and related this to
his observation of the way in which the animal collected the secretion of the marginal carapace
glands with carmine particles trapped in it. He did not take into account the size of the prey.
There is, then, no direct evidence that the secretion of the glands of the carapace is involved in
capture of copepods. A powerful swimmer such as Conchoecia should easily capture a copepod,
with the aid of its clawed mandibular palps. Whether the sticky secretion of the carapace glands,
or perhaps the labrum, aid such capture by immobilizing the prey can be determined only by
observation.

Copepod remains which are found in the stomachs of halocyprids are of such size that they would
pass betweeen the bases of the trunk-limbs and mouth-parts. They usually show some evidence of
crushing. From a specimen with an almost intact copepod in its stomach, it seems likely that
captured prey swallowed without being broken up into smaller portions is crushed by the mouth-parts
just sufficiently to enable digestion to take place. The initial grasping of such prey by the mandibular
palps may possibly be aided by the maxillary exopods, the claws of which are apposed to those of the
mandibular palp. It has been pointed out already (page 309) that, during inward flexure, the man-
dibular palps point slightly inward and rotate appreciably about their axes. Such movement would
draw any prey inward and upward and press it firmly against the ventral surface of the labrum. The
maxillulary palps could then help to grip the prey. A ventral movement of the apices of the mandibular
bases will bring the shearing action of their gnathobases into play, but small prey would be moved
back to pass between the bases of the appendages. In this position, manipulation of the food could
be aided by the maxillulary palps and the maxillary endopods. Once the anterior end of the prey has

THE APPENDAGES IN OTHER HALOCYPRIDIDAE 321

been moved back clear of the labrum, the maxillulary endites could, with their strong spines, grip
it and probably to some extent crush it. A forward and upward thrusting of the endites would
progressively move the prey through the oral atrium into the mouth. The angle at which the oeso-
phagus leaves the oral atrium is of importance, in that there is no hindrance to direct passage of food
into it. During transport of prey into the oral atrium, it would be subjected to further crushing by
the coxal gnathobases of the mandibles, while the four posterior molar spines would aid transport by
gripping the prey during the recovery movement of the maxillules.

It has been noted that the portions of larger copepods contained in the stomachs of Conchoecia are
of such a size that they would just pass between the bases of the limbs and into the oral atrium, but
the large specimens from which they are derived will not be able to pass. Each must be held below
the level of the labrum mainly by the mandibular palps. The incisor edges of the mandibular bases
could then shear portions, particularly limbs, from the prey. The slight rotation of the coxa, necessary
to carry out this process, and the slight downward movement of the apices of the bases, would not
prevent the palps from continuing to hold the prey in position. The secretion of the anterior labral
glands could then entangle portions broken free and simplify their retention by the appendages.
Further transport of these fragments probably resembles that of small whole prey.

THE APPENDAGES IN OTHER HALOCYPRIDIDAE

In order to add to the overall picture of the Halocyprididae it is of interest to compare the appendages
of Conchoecia with those of other genera. A detailed comparison must, however, be postponed until
more species of these other genera have been studied. Some characteristic features, however, may be
considered. In Euconchoecia and Archiconchoecia, particularly, the setation of the antennule and
the secondary sexual characters of the antennal endopod of the male differ from those of Conchoecia
but, apart from differences of the mandibular gnathobases and the enormously elongated terminal
setae of the male first trunk-limb of Euconchoecia, the remaining appendages are closely similar in
structure and interrelation in all genera. Of particular note is the fact that the mandibular coxa has
an articulation with the labrum similar to that described on page 307 in Conchoecia. Not only does this
show a functional similarity in the mandible, but it also provides a new taxonomic character common
to the genera.

Among the halocyprid genera, differences may be seen in the structure of the molar surface of the
mandibular coxa. Skogsberg (1920, p. 740) questioned the homologies of the masticatory pad and
the oval cavity on the coxa of Euconchoecia. In Conchoecia, the molar pad is in fact situated in a slight
depression, though this is less marked than the depression in the coxa of Euconchoecia. The main
differences between this latter genus and Conchoecia would appear to be as follows. In Euchonchoecia
the small sharp conical bristles of the central and proximal parts of the molar pad are absent. On the
posterior and oral surface of the molar surface of the coxa, there are up to twelve or thirteen molar
claws instead of only four as in Conchoecia. The marginal bristles are much less dense and the orally
directed group seems to be absent. These latter are functionally replaced by the more proximal
marginal claws. Skogsberg further pointed out that the claws can be folded inwards into the oval
depression. The functional significance of this is unknown, but may be some adaptation to the trans-
port of food in the oral atrium. The structure of the molar surface differs less in Archiconchoecia. The
molar spine (Miiller's spine 'D') is absent, and the molar claws and bristles are less well developed.
The structure of the molar surface in the genus Halocypris has been discussed by Skogsberg (1920).
In H. globosa it is very similar to that of Conchoecia. Halocypris brevirostris differs particularly in the
absence of marginal molar claws. The condition in other species of the genus has not been described.

322 DISCOVERY REPORTS

Skogsberg (1920, p. 584) considered, like Miiller, that Claus was not justified in placing H. globosa in
the separate genus Halocypria, since the differences were of 'so slight a nature'. He had not then
studied H. globosa and when later (1946) he redescribed this species he revised his views somewhat.
He then considered that in many ways the species was intermediate between H. brevirostris and
Conchoecia. A definite decision on this question must be deferred until other species of the genus
have been redescribed, but in view of the small variation in the structure of the coxal gnathobase in
Conchoecia and the differences in other genera, it seems likely that Claus was justified in his opinion.
The two species should probably be placed in at least separate sub-genera, if not separate genera.

Miiller (1906) described the interesting species Thaamatocypris echinata. In many ways this
resembles the halocyprid genera; in particular the mandible possesses a gnathobase on the basis as
well as on the coxa. The maxilla and first trunk-limb are similar to those of the halocyprids and bear
similar vibratory plates. Though its distal article differs from, the maxillule somewhat resembles, that of
Conchoecia ; there are, however, many differences, the most remarkable of which would appear to be
the absence of an antennal notch. This would seem to be related to the fact that though the antennal
shaft and exopod are similar to those of the halocyprids, the endopod also is well developed and has
a natatory function. In addition the antennule is distinctly segmented and is possibly natatory
(Skogsberg, 1920, p. 119). In relation to these differences Skogsberg discussed the stabilizing effect
of the spines on the carapace. It is also noteworthy that the caudal furca differs from that of the
halocyprids. It would be interesting to know if the mandible has a similar articulation to that of the
other halocyprids. Midler's figures (1906, pi. vi) indicate that there are many differences in the incisor
edges of the mandible, while the molar surface must be of quite different structure. In addition the
terminal setae of the mandibular palp are elongate and not claw-like. The figures and description give
no reference to any process on the coxa, which could represent the articular process of other halo-
cyprids. If such an articulation is absent, it would add further weight to the differences between the
Thaumatocypris and the other halocyprids. The impression is that Miiller was justified in placing his
species in a sub-family separate from that including the other Halocyprididae.

COMPARISON OF HALOCYPRIDIDAE AND CYPRIDINIDAE

Skogsberg (1920) compared the morphological details of the appendages of the Halocyprididae with
those of the Cypridinidae, but did not compare the whole animals from a functional viewpoint.
Graham Cannon (1931, 1933) has made such a comparison between the Cypridinidae and the Podo-
copa. A similar comparison with the Halocyprididae is of interest.

An immediately obvious difference between Conchoecia and a cypridinid is the form of the carapace
and the antennal notch (Fig. 14). In the former group, the carapace is usually elongate with a straight
hinge-line and is very light and delicate ; in the latter it is generally rounded with a curved hinge-line
and is heavily calcified. The antennal notch of Conchoecia extends back very nearly parallel to the
hinge-line with a well-developed rostrum above. Behind the notch, the surface of the carapace is
hollowed to allow free backward swing of the antennal exopod. In the Cypridinidae the antennal
notch is narrower and usually slopes upward towards the hinge-line ; there is no prominent rostrum.
Associated with differences in the carapace there is a difference in posture of the animal. In a
typical cypridinid the main axis of the body slopes anteriorly upward much more markedly
than it does in Conchoecia. The ventral apodemes, which are similar in the two groups, indicate an
upward curvature of this axis much further forward in Conchoecia than in Cypridina. The nervous
system, also, extends further to the posterior in Conchoecia (cf. Claus, 1891, pi. 1, fig. 11 and Graham
Cannon, 1931, fig. 10B). The antennal shaft adds to the appearance of anterior uptilting in Cypridina.

COMPARISON OF HALOCYPRIDIDAE AND CYPRIDINIDAE 323

In many members of this genus it is as broad as it is long and its longitudinal axis slopes upward.
In Conchoecia it is elongate and extends forward. The orientation of the body of Conchoecia is similar
to that of the Podocopa and it is possible that this is more primitive. It is, however, suggested that
the orientation of the body and arrangement of the antenna and antennal notch is partly adapted to
differences in the mode of swimming in the two groups. As has been mentioned when considering

Fig. 14. Diagrams comparing A, C. borealis antipoda, and B, Cypridina (Macrocypridind) castanea. av antennule; a2, ant-
tenna; f.o, frontal organ; lb, labrum; mn, mandible; mxv maxillule; mx2, maxilla; mx2v, vibratory plate of maxilla; trv first
trunk limb; trxv, vibratory plate of first trunk limb; tr2, second trunk limb.

the function of the antenna, the swimming action in Conchoecia is a forward propulsive stroke with
only a small downward component, associated with the light, boat-shaped carapace. In the Cypri-
dinidae, though there is a forward propulsive stroke (as mentioned by Skogsberg (1920)) the greater
downward component is associated with the heavy, often rounded carapace. Even in those Cypri-
dinidae such as Cyclindroleberis which have an elongate carapace, the body and antennal shaft have
a marked upward slope anteriorly. It is interesting that in the genus Halocypris where the carapace
is heavy and rounded rather like that of a typical cypridinid, the orientation of the body and antennal
shaft also is more like that of a cypridinid ; and the antennal notch is also more shallow.

The other interesting comparison is the adaptation of the appendages for feeding. Graham Cannon

324 DISCOVERY REPORTS

1931, 1933) has pointed out that in the Cypridinidae there has been a backward shift in adaptation
of the limbs for this purpose. Here, instead of the mandibles, the maxillules and maxillae are the
main biting-mouth-parts. This is accompanied by a more posterior position of the mouth relative to
the appendages. Thus the mouth lies posteriorly to the mandibular coxae, the oral atrium being
bounded laterally by the maxillulae ; the paragnaths are not developed. In Conchoecia, however, like
the Podocopa, the mandibles are the main biting-mouth-parts, with the maxillulae playing only a
small part in the process and the maxillae not adapted at all for biting the food. In this genus the
mouth lies between the mandibular coxae, which also laterally bound the oral atrium, and the
paragnaths are well developed. The difference in adaptation of the appendages for feeding is correlated
with adaptation for walking. Thus in bottom-living cypridinids the mandibular palp is used for
walking and the mandible is no longer used for biting the food. The gnathobase is reduced and adapted
merely to assist transport of food into the mouth. The same pattern is retained in planktonic members
of the group, such as Gigantocypris (see Graham Cannon, 1940), or Cypridina (Macrocypridina) castanea
(see Graham Cannon, 1933) which is illustrated for comparison with Conchoecia in my Fig. 14. In
the Podocopa, on the other hand, it is the antennal endopod which is used for walking and this leaves
the mandible free for biting the food. Conchoecia does not walk at all and the mandible is free for
biting the food. The palp, though well developed, differs in structure from that of the Cypridinidae
and is used for capture of food.

SUMMARY

The functional interrelation of the appendages and their setae in Conchoecia borealis antipoda is
described. Apart from differences in secondary sexual characters, there is little difference in other
members of the genus Conchoecia.

A new feature of the articulation of the mandible with the body has been found in the Halo-
cyprididae. A distally directed condyle on the distal apex of the coxa articulates in a skeletal socket
on the oral surface of the labrum. This with the usual dorsal condyle restricts movement of the coxa
to rocking about a vertical axis.

The anterior dorsal extrinsic muscle of the mandibular coxa is inserted on a flange which extends
forward from the region of the dorsal condyle. This muscle thus serves to rotate the coxae outward
and separate the mandibular gnathobases.

It has been confirmed that members of the genus Conchoecia are mainly predators on copepods.
The method of capture and mastication of such food is discussed. The gnathobase of the basis of the
mandible is probably concerned with reducing such food to a size that can be swallowed.

It seems probable that Conchoecia species can also feed on fine material. This may be collected by
the secretion of the marginal glands of the carapace or by labral gland secretion.

The appendages of Archiconchoecia, Euconchoecia and Halocypris are in general similar in structure
and arrangement to those of Conchoecia. Their mandibles have the same type of articulation. There
are, however, differences in the gnathobases of the mandibular coxae, which must result in functional
differences needing investigation.

The differences in the gnathobases of the mandibular coxae of Halocypris globosa and H. brevirostris
are probably of sufficient significance to warrant inclusion of these species in separate genera, as
suggested by Claus.

A redescription of Thaumatocypris echinata Miiller is necessary, in order to clarify its systematic
position.

Conchoecia is compared with Cypridina. The functional pattern of the mandibles and more posterior
limbs of the former, as well as the position of the mouth, do not show the backward shift present in
Cypridinidae.

REFERENCES 325

REFERENCES

Borradaile, L. A., 1922. On the month-parts of the shore crab. J. Linn. Soc. Lond. vol. XXXV, pp. 115-42. P^ i°> "■

CALMAN, W. T., 1909. Crustacea. In Lankester: A treatise on Zoology. Part VII, 3rd fasc, pp. 56-70, London.

Cannon, H. Graham, 1925. On the segmental excretory organs of certain fresh-water ostracods. Phil. Trans, vol. ccxiv,

pp. 1-27, pis. 1 and 2.
io26. On the feeding-mechanism of a fresh-water ostracod 'Pionocypris vidua' (O. F. Miiller). J. Linn. Soc. Lond.

vol. xxxvi, pp. 325-75, 2 pis.

1927. On the feeding-mechanism o/Nebalia bipes. Trans. Roy. Soc. Edinb. vol. lv, pp. 355-69.

I93I. On the anatomy of a marine ostracod Cypridina (Doloria) levis, Skogsberg. Discovery Rep. vol. 11, pp. 435-82,

pis. vi- vi 1.
!Q33. On the feeding-mechanism of certain marine ostracods. Trans. Roy. Soc. Edinb. vol. lvii, pp. 739-64.

1940. On the anatomy of Gigantocypris mulleri. Discovery Rep. vol. xix, pp. 185-244, pis. 39-42.

Claus, G., 1890. Die Gattungen und Arten der mediterranen und atlantischen Halocypriden nebst Bemerkungen iiber die Organisa-
tion derselben. Arbeiten aus dem Zool. Inst. Wien, vol. IX, pp. 1-34.

^i. Die Halocypriden des atlantischen Oceans und des Mittelmeeres. Pp. 1-81, pis. 1-26. Wien.

Elofson, O., 1941. Zur Kenntnis der marinen Ostracoden Schwedens besonders mit Berucksichtigung des Skageraks. Zool. Bidr.
Uppsala, vol. xix, pp. 215-534.

Hansen, H. J., 1925. On the comparative morphology of the appendages in the Arthropoda. A. Crustacea. Studies in Arthro-
poda II, pp. 1-176, pis. 1-8, Copenhagen.

Muller, G. W., 1890. Ueber Halocypriden. Zool. Jb. vol. v, pp. 253-80, pis. 28-9.
' ^94. Die Ostracoden des Golfes von Neapel und der angrensenden Meeres-Abschnitte. Fauna und Flora des Golfes von
Neapel, vol. xxi, pp. 1-404, pis. 1-40.

i9o6. Ostracoda. Wiss. Ergebnisse der deutschen Tiefsee-Expedition auf dem Dampfer ' Valdivia', vol. vin, pp. 29-154,

pis. 5-35-

1927. Ostracoden. In Kukenthal-Krumbach, Handbuch der Zoologie, vol. in, 4, pp. 399-434, Berlin.

Sars, G. O., 1887. Nye Bidrag til Kundskaben om Middelhavets Invertebratfauna. 4. Ostracoda mediterranea. Arch. Math-

Naturv. vol. xn, pp. 173-324, pis. 1-20.
Skogsberg, T., 1920. Studies on Marine Ostracods. Part 1. Zool. Bidr. Uppsala. Suppl. Bd. 1.

I946. Ostracoda. Rep. Scient. Res. 'Michael Sars'. North Atlantic Deep-sea Exped. 1910, vol. v, pp. 1-26.

Vavra, W., 1906. Die Ostracoden der Plankton-Expedition. Ergebnisse der Plankton-Expedition der Humbolt-Stiftung, vol. 11,

pp. 1-76, pis. 1-8, Kiel und Leipzig.

[Discovery Reports, Vol. XXXI, pp. 327-486, Plates IV-VII, November 1961.]

REPRODUCTION, GROWTH AND AGE OF
SOUTHERN FIN WHALES

By
R. M. LAWS

CONTENTS

General considerations page 331

Introduction 33 1

Acknowledgements 332

Material 333

Previous work ........... 334

Migrations 339

The ovaries 341

Size 34i

Giant ovaries 343

Morphology 343

Relations 344

Graafian follicles 345

Foetal ovaries 345

Immature ovaries 345

Adult ovaries 347

Primary follicles 347

'Recently ovulated' females 347

Pregnant females 348

Lactating females 349

'Resting' females 35°

Ovarian cysts 35 1

Conclusions 35 l

The corpus luteum 352

Formation of the corpus luteum 353

Bilateral activity of the ovaries 355

The corpus luteum of ovulation 35*>

The corpus luteum of pregnancy 35°

Size 356

Morphology 358

Vesicular corpora lutea 359

Accessory corpora lutea ......... 3"1

Conclusions 3"2

Corpora albicantia, corpora aberrantia and corpora atretica . . 363

The corpus albicans 3^3

Morphological types 3^4

Age groups of normal corpora albicantia 366

Persistence of corpora albicantia 3^9

Accumulation of corpora albicantia 37^

Corpora aberrantia ........•• 3°°

Corpora atretica 3°2

Conclusions 3°3

Accumulation of corpora up to the attainment of physical maturity 385

The frequency of corpora in early baleen groups 385

The number of corpora at the attainment of physical maturity . .386

Material and methods 387

Results 388

Comparisons between the number of corpora in young age groups and at

physical maturity 392

33o CONTENTS

The reproductive cycle page 394

Introduction 394

The sex ratio 395

The breeding season 395

The male reproductive cycle 395

The follicular cycle in females . . . . . . . .401

Pregnancy and foetal growth 401

The pairing season and the season of parturition .... 403

Sexual maturity 406

The mean length at sexual maturity 406

The age at sexual maturity 407

Newly mature females 409

The mammary gland 409

The first pregnancy .......... 410

Growth in length just after puberty 413

The first ovulations .......... 416

Puberty and its relation to the migratory cycle . . . . .421

MULTIPAROUS FEMALES 425

The pairing season and the calving season . . . . . .425

Post-partum heat ........... 429

Females simultaneously pregnant and lactating 429

Evidence from the sizes of corpora albicantia ..... 430

Anomalous corpora albicantia of lactating females .... 434

Ovulation after abortion, stillbirth, or loss of calf .... 436

Post-lactation heat 436

The lactation period ^/\/\

The sexual cycle and its relation to the migratory cycle .... 450

Variation of fertility with age 454

Multiple ovulations 454

Proportion of females in oestrus or pregnancy 455

Variations in fertility with time 456

Age-determination by means of the ovarian corpora .... 459

The rate of accumulation of corpora albicantia ..... 459

Types of corpora albicantia 460

The sexual cycle 460

Recovered whale marks 463

Age-determination .......... 465

Comparison with other methods 466

Applications ........... 470

Survival curves .......... 470

Growth curves 475

Summary 477

References 482

Plates IV-VII following p. 486

REPRODUCTION, GROWTH AND AGE
OF SOUTHERN FIN WHALES

By R. M. Laws

(Plates IV-VII and Text-figs. 1-60)

GENERAL CONSIDERATIONS
Introduction

In his paper on the southern stocks of whalebone whales, Mackintosh (1942) summarized the work
which had then been published and discussed some additional unpublished data. He remarked
that ' In recent years a good deal of new material relating to the breeding, growth, and age of whales
has been collected by members of the Discovery Committee's staff and other biologists who have
sailed in factory ships to the Antarctic. Work on this material, which includes records of large numbers
of ovaries, has been interrupted by the war, but it is hoped that it will be resumed in the future and
much progress should be revealed when the results are available' (p. 216); and later (p. 226), 'The
most important problem is to ascertain how many corpora lutea on the average are added each year
in a sexually mature female '. Annual collections of ovaries were initiated, and have been continued,
as a means of comparing the relative condition of the stocks of whales from year to year. A great deal
of extra material has, therefore, accumulated since 1942 and continues to increase yearly. In a series
of papers (Mackintosh and Wheeler, 1929; Wheeler, 1930; Wheeler, 1934; Peters, 1939; Mackintosh,
1942) attention was drawn to the use of counts of the corpora lutea and corpora albicantia in fin-whale
ovaries as a measure of age. Ovarian scars have also been used for determining age in other groups
of animals, for instance seals (Bertram, 1940; McLaren, 1958; Mansfield, 1958), the cow (Dawson,
1958), birds (Maynard, 1888; Wynne-Edwards, 1939), and even insects (Bertram and Samarawic-
krema, 1958). Several estimates of the annual rate of accumulation of corpora albicantia in fin whales
have been published ranging from 0-9 (Peters, 1939) to 2-5 (Wheeler, 1934), but they do not stand
up to detailed criticism. When the present investigation began the main objects were to establish to
what extent corpora albicantia persist in the fin-whale ovaries, and to determine the average annual
increment of corpora and the range of variation, so that they might be used to estimate the age of
whales. There are also many reasons why a better knowledge is needed of the whole breeding cycle
of fin whales and other species. It is of intrinsic biological interest and it has an important bearing
on population dynamics and on practical problems arising from the regulation of whaling.

Two main approaches to the solution of these problems have been made. One is by way of a
detailed study of the gross and microscopic anatomy of the ovaries. The other is by investigation of
the annual reproductive cycle of the species. These are dealt with in the two main parts of this paper.
My own interest in this work began when I spent the antarctic whaling season 1953/54 on board
the floating factory ' Balaena ', and the time has come to present the results of this recent work
although new material continues to arrive. One considerable disadvantage is that it has still not been
possible to study the breeding biology of fin whales directly, in the breeding areas. In fact we still
do not know with certainty the location of these areas, though we may confidently assume that they
lie in the tropical and subtropical zones of the oceans. Even if the breeding herds were located it is

332 DISCOVERY REPORTS

hard to see how the anatomical and physiological work which is really needed could be done in such
regions except at prohibitive cost. Such work is only made possible in the Antarctic by taking advantage
of the facilities provided by the existing whaling operations.

With the exception of a few observations made at South African whaling stations (Saldanha
Bay 330 i' S., i8° o' E., and Durban 290 52' S., 310 1' E.) some 30 years ago all the material on which
this work is based has been collected during a few months of the year in the Antarctic, where the
animals migrate to feed on krill. Since the 1950/51 season the pelagic whaling operations for fin
whales in the Antarctic have been confined to January, February, and the first part of March. As the
main part of the pairing season is from May to July, elucidation of events at this, the most important
stage in the annual cycle, could hardly be more difficult. Even the observations from South African
land stations are not truly representative of the breeding population, because they are situated near
migration routes at positions probably well south of the breeding grounds.

It is therefore necessary to make inferences from the condition of animals killed in the Antarctic
as to the events in the breeding season some six months previously; a procedure which is only
justified by necessity. One species of baleen whale, the humpback whale, Megaptera novaeangliae
(Borowski) has recently been studied on or near the breeding grounds (which in this species are in
inshore waters) and is described in a series of important papers by Chittleborough (1955a, 19556,
1958). We may, with certain reservations, draw on this work for comparison.

Part of the original work described in the present paper has already been presented in two short
preliminary papers (Laws, 19580, 19596).

Acknowledgements

This paper could not have been written had it not been for the strenuous efforts of the biologists who
collected or examined material over a long series of years, first for the ' Discovery ' Committee and,
from 1949, for the National Institute of Oceanography. In particular I wish to thank Dr H. E.
Bargmann, Dr M. Begg, Dr M. R. Clarke, Dr R. H. Clarke, Mr P. R. Crimp, Mr J. D. Currey,
Mr A. E. Fisher, Dr F. C. Fraser, Dr J. E. Hamilton, Dr K. A. Kermack, Dr N. A. Mackintosh,
C.B.E., Dr L. H. Matthews, F.R.S., Dr F. D. Ommanney, Dr D. A. Parry, Mr D. F. S. Raitt,
Dr G. W. Rayner, Mr A. Saunders, Mr J. H. Smoughton, Mr H. W. Symons, Mr R. D. Weston,
Dr J. F. G. Wheeler, and Mr G. R. Williamson.

My own introduction to whale biology on board F/F ' Balaena ' in 1953/54 owes much to the facilities
provided by Hector Whaling Ltd. through Capt. C. P. Virik, and to the co-operation of Cdr H. E.
Buckle, A.M., C.B.E., Senior Whaling Inspector, Mr C. E. Ash and Mr H. W. Symons, Chemists,
Mr Harry Weeks and many others. I would also like to thank Gunner Ragnar Hem for hospitality
enjoyed during a short voyage on board the whale catcher, ' Setter IX'.

A number of British and Norwegian Whaling Companies have generously co-operated in these
studies by providing facilities for biological work on factory ships, or by collecting whale ovaries for
subsequent examination in the U.K. (The latter scheme was initiated by Mr A. H. Laurie in 1934.)
These are Hector Whaling Ltd., Chr. Salvesen and Co., Johan Rassmussen and Co., A/S Melsom
and Melsom, A/S Svend Foyn Bruun, and A/S Thor Dahl. It gives me pleasure to acknowledge the
help of the whaling inspectors in the factory ships ' Balaena ', ' Southern Harvester ' and ' Southern
Venturer'. The Ministry of Agriculture, Fisheries and Food has been most co-operative. To all these
individuals and organisations I am indebted.

As regards the examination of the material I am particularly grateful to Mr A. E. Fisher who has
made most of the histological preparations and, with Mr J. H. Smoughton (to whom I am also
indebted) has undertaken nearly all the routine examinations of ovaries since 1955. Dr R. H. Clarke

GENERAL CONSIDERATIONS 333

kindly made his preliminary analysis of the accumulated data on the ossification of the vertebral
epiphyses available to me. I am also indebted to Professor J. T. Ruud and Mr Age Jonsgard for
interpreting some baleen-plate material.

Mr A. Style has drawn most of the figures in this paper and Mr A. Madgwick is responsible for
some of the photographs.

In the preparation of this paper I have greatly benefited from discussions with Mr S. G. Brown,
Dr R. G. Chittleborough and Mr A. Jonsgard. I should also like to thank Dr Mackintosh and
Dr Bargmann for their help at all stages of the work.

Material
Investigations of the breeding biology of whales have to be based on systematic examination of the
reproductive organs, and the following routine observations and collections are made when possible
by biologists working in floating factories.

Both sexes

i . Date, noon position of factory.

2. Length of whale measured in straight line from tip of upper jaw to notch of tail.

3. Physical maturity; condition of vertebral epiphyses (Wheeler, 1930).
• 4. Baleen plate for examination (Ruud, 1945).

5. Measurement of blubber thickness.

6. Observations on diatom film (Hart, 1935), parasites, scars, etc. (Mackintosh and Wheeler, 1929).

7. Since 1955/56 ear-plugs have also been collected (Purves, 1955; Laws and Purves, 1956).

Females

8. Sexual maturity.

9. Foetus present or absent (uterus searched, or not ascertained). If present sex and length and if possible weight
are recorded.

10. Condition of mammary gland; greatest depth and whether virgin, resting, intermediate, or lactating (Mackin-
tosh and Wheeler, 1929).

11. Collection of ovaries, mainly from mature females (fixed and stored in 10% formalin).

Males

12. Measurement of testes and collection of specimen.

By far the most useful information comes from the ear-plugs and ovaries. In the antarctic pelagic
whaling season 1953/54, in addition to the usual routine observations, I made a detailed study of a
series of 168 pairs of fin-whale ovaries collected at relatively short post-mortem times (1-14 hr.). The
main purpose of this study was an investigation of the variations in the morphology and histology of
the corpus luteum and corpora albicantia. Specimens were fixed in formalin, Bouin, Heidenhain's
Susa, Zenker-formol and Zenker-formol with post-osmication. One important practical conclusion
was that for standard routine examination of whale ovaries some uniform method of slicing was
essential and in 1954 a commercial bacon-slicing machine was acquired. With this machine slices of
uniform thickness down to 1 mm. can be produced if the material has previously been hardened
either by freezing or by storing in formalin. In routine examination 5 mm. slices are cut and all ovary
material obtained since 1954 has been treated in this way.

Between 1934 and 1939 and again from 1945 to 1955 through the kind co-operation of a number of
whaling companies annual collections of blue whale (Balaenoptera musculus) ovaries were received
and examined. With the decline in the catch of blue whales these collections were decreasing in
importance and in the season 1955/56 the whaling companies were asked to collect fin-whale ovaries.
The companies' collections for this season totalled 334 pairs of fin-whale ovaries. Date, and position,

334 DISCOVERY REPORTS

length, and size of foetus if present were recorded. In 1954/55 and 1955/56 a further 159 pairs of
ovaries were collected by whaling inspectors and biologists in the three British floating factories and
numerous other observations were made. The methods of examining this material have been
standardized and it has provided much of the data for this paper.

In addition to this recent material I have had access to the records kept by the ' Discovery '
Investigations from 1925 onwards (since 1949 incorporated in the National Institute of Oceanography).
The data which are of relevance here consist mainly of observations of length, physical and sexual
condition, state of fusion of the vertebral epiphyses, counts of the number of corpora lutea and
albicantia, some measurements of the dimensions of these bodies, and measurements of the genitalia
and foetuses. There are in addition limited collections of ovarian and testis material. The most
important part of this varied material is in the form of counts of the ovarian corpora made by no less
than fifteen different observers. One consequence of this is that there is a considerable variation in
the quality of the work, since the different workers have applied different methods and criteria. It is
difficult to make allowance for these variations and although all the records have been freely used in the
course of the work it is preferable, where possible, to rely mainly on the more recent material to
illustrate the present paper. For this reason there are discrepancies in amount of material between
the various tables in this paper, but it is scarcely practicable or necessary to explain these discrepancies
in every case.

Previous work

The first comprehensive studies of southern hemisphere fin whales were undertaken by the ' Discovery '
Investigations in 1925, although Barrett-Hamilton (Hinton, 1925) had examined some 300 whales at
South Georgia in 191 3/14. This early work and later research by various workers up to 1940 is reviewed
by Mackintosh (1942). The anatomy of the urino-genital system of fin whales has been described by
Ommanney (1932) who dissected four foetuses.

Mackintosh and Wheeler (1929) worked at South Georgia and Saldanha Bay and their paper based
on 1577 fin and blue whales established the general outline of the biology of these species and remains
the most important single source of information on the biology of the fin whale. Consideration of the
time of follicular ripening ; the occurrence of corpora lutea of ovulation, and minute foetuses ; the
onset of increased testis activity in males, all suggested the earlier part of the southern winter as the
beginning of the breeding season. These workers plotted foetal lengths, drew a mean growth curve,
and by assuming all foetuses grow at the same speed they calculated the proportions conceived in
different months. The majority of pairings appeared to take place in June and July and the gestation
period was estimated to be just under a year. From the sizes of the largest foetuses and smallest
calves they concluded that the average neonatal length of fin whales is 6-5 m. The length of the calf
at weaning was estimated in a similar fashion to be about 12 m. and the lactation period to last about
6 months on average, from mid-June to early December. From these conclusions and because
approximately half of the adult females they examined were pregnant they decided that each breeding
cycle usually lasted 2 years. However, Wheeler (1930) was aware that in the fin whale a post-partum
ovulation can result in one pregnancy being followed immediately by a second. From an examination
of length frequencies they concluded that it was likely that both blue and fin whales attained sexual
maturity at an average age of 2 years, and they gave figures for the average body length at sexual
maturity for both sexes.

They showed that in general the number of corpora lutea and corpora albicantia in the ovaries
increased with increasing body length, which suggested that corpora albicantia persist and accumulate
in the ovaries during life. Ovulation was shown to be spontaneous, and they advanced arguments for

GENERAL CONSIDERATIONS 335

believing the females to have a polyoestrous cycle. The abundance of ripening graafian follicles is
suggestive ; the protracted breeding season allows time for several dioestrous cycles ; and the fact that
some whales, with more than 30 corpora albicantia, must be more than 30 years old if monoestrous
was thought to be important.

If the female is polyoestrous and individual females become pregnant at 2-yearly intervals, then
up to, say, six ovulations may be possible in one season. Because female whales are gregarious it could
be expected that their experience would be similar and each year a certain number of ovulations
would tend to occur more commonly than others. When they plotted the frequencies of corpora in
their material they found peaks occurring at 4-5, 12, and 19 corpora and suggested that these repre-
sented the increase in numbers of corpora at intervals of 2 years. Wheeler (1930) developed and
modified this hypothesis. He examined the state of fusion to the centra of the vertebral epiphyses
and by this criterion classed individuals as physically mature or immature. With less than 15 corpora
females were almost invariably physically immature, and with more than this number, physically
mature. The frequency distribution of corpora in his larger material shows maxima at 1,7, 11, 18 and
21 corpora. Three of these peaks precede physical maturity. He pointed out that in the first group
the greatest number of corpora is at the beginning, which meant that the first ovulation was usually
followed by pregnancy, whereas in subsequent seasons unsuccessful ovulations were thought to
precede pregnancy. The importance of this work lies in the fact that it established a close relation
between the attainment of physical maturity and the rate of accumulation of corpora. The fact that
there is so little variation in the number of corpora accumulated at physical maturity implies that the
rate of accumulation is very regular and/or very small. Wheeler's work suggested that there were on
average three breeding seasons before the attainment of physical maturity so that about five ovulations
occur each breeding cycle, or on average 2-5 per year.

In a later paper Wheeler (1934) applied this method of age-determination to 472 mature females
for which records were available and calculated average mortality rates. We know now that the peaks
in the frequency distribution of corpora in his material are not significant, but his figures demonstrate
that the decline in numbers of fin whales of increasing ages (as shown by corpora numbers) in his
sample, is exponential. Brinkmann (1948) published the results of investigations in 1939/40 based
on records of 918 female fin whales. His work confirmed the earlier estimates of size at sexual and
physical maturity, but he concluded that in the fin whale 13 corpora have been accumulated on the
attainment of physical maturity. This discrepancy between Brinkmann's material and that of Wheeler
(1930) and Peters (1939) who respectively found 15 and 14-15 corpora at physical maturity is readily
explained by differing criteria of physical maturity, for this is rather a subjective observation. More
recently, Japanese workers have obtained an even lower figure of 11-5 (Nishiwaki, 1950a, 1952).
Brinkmann discussed ' corpus luteum accumulation as a clue to age determination '. He found similari-
ties between the frequency distribution of corpora in his material and Wheeler's (1930), but did not
come to any definite conclusions.

Laurie (1937) found a similar correlation in blue whales between the accumulation of 1 1-12 corpora
and the attainment of physical maturity. He found no regular occurrence of maxima in his frequency
distributions, but believed that comparison of certain features in the frequency curves for two suc-
cessive years indicated an increment of slightly more than one corpus each year. By consideration of
the fresh appearance of certain corpora he concluded that on average 1-13 were formed each breeding
season, but then states that this is the annual increment. If ovulatory periods recur at 2-yearly intervals,
then by this argument the annual increment should only be 0-57 corpora.

Ruud (1940, 1945) developed a new method of estimating the age of whalebone whales, based on
the ridges present on the baleen. For 14 northern hemisphere fin whales he compared the number of

336 DISCOVERY REPORTS

corpora in the ovaries with the results of baleen readings and found them to be in agreement with the
findings of Mackintosh and Wheeler. He suggested that in the breeding season up to 6-7 ovulations
are possible before pregnancy supervenes. In the light of these estimates of age he suggested that the
age at sexual maturity was more likely to be 3 years than 2.

Mackintosh (1942) gave a valuable summary of all aspects of the biology of whalebone whales. He
had little to add to the earlier work on reproduction and age, though in the light of accumulated data
he made some slight amendments to the average lengths at sexual maturity. He was also able to give
particulars of a very important whale mark recovered in 1941 which had been carried by a female fin
whale for 6 years. The ovaries were recovered and had eight corpora. As there is no reason to suppose
this whale was conspicuously immature when marked, he concluded that in this individual ' the rate
of accumulation cannot have been much more than one a year (or two every 2 years), and, since there
was no clue to the whale's age at the time of marking the rate of accumulation may have been even
slower' (p. 227). On the other hand, if this female was immature when marked then the incremental
rate could have been higher. This is hardly compatible with Wheeler's estimate, but it is in agreement
with Peters's (1939) calculations.

Peters claimed that, as there was a very great difference in the development and activity of the
corpus luteum of pregnancy and of ovulation, he had been able to establish morphological and histo-
logical criteria for distinguishing the corpora albicantia representing pregnancies and ovulations. By
counting the former and assuming a 2-year reproductive cycle he provisionally estimated that in
the fin whale there is an average of i-8 ovulations in 2 years, and in the blue whale 1-9 ovulations.
Consideration of his criteria, the colour and texture of the gland and the arrangement of the connective
tissue trabeculae, suggest that he was confusing the various stages of regression (see below, p. 384).
Nor is there such a marked difference between the corpora lutea of pregnancy and ovulation as he
states. No other workers have been able to make such a distinction between the types of corpora
albicantia in whales although this is well known in the cow (Hammond, 1927; Benesch and Wright,
1950), and is claimed for deer (Cheatum, 1949; Robinette, Gashweiler, Jones and Crane, 1955),
but disputed by Golley (1957). In any case his estimates were based ultimately on only seven pairs of
fin-whale ovaries and four pairs of blue-whale ovaries.

Robins (1954) has recently claimed that in the humpback whale (Megaptera novaeangliae) it is
possible by morphological criteria to distinguish corpora lutea and corpora albicantia representing
ovulations from those representing pregnancies. Dempsey and Wislocki (1941) believed that in this
species restriction of the blood supply to the centre of the corpus luteum results in the formation of
a central cavity. Robins suggested that this applied only to the corpus luteum of pregnancy, which is
larger than the corpus luteum of ovulation (average 100-130 mm. and 80 mm. respectively), and claimed
that the presence of a central cavity or, in corpora albicantia, a central core was diagnostic of a corpus
of pregnancy. This hypothesis was based on a small number of ovaries and has not been confirmed.
A basic assumption, that the formation of a cavity is a result of the large size of the corpus luteum of
pregnancy, does not agree with observations on the incidence of cavities in fin- and blue-whale corpora
lutea (see below, p. 359). Van Lennep (1950) studied the histology of blue- and fin-whale corpora and
concluded that the corpora albicantia were persistent and that regression was completed in 3-4 years.
He was able to find no constant differences between corpora associated with ovulation or with
pregnancy, but made some suggestions about possible distinctions. Harrison (1949) and Sergeant
(Anon., 1955) made histological observations on Globicephala, but were unable to distinguish the two
types of corpora. Harrison stated that in this species only serial histological sections could be expected
to give a precise indication of the number of corpora albicantia, which regress to become invisible
macroscopically. Comrie and Adam (1938) made some observations on the ovaries of Pseudorca.

GENERAL CONSIDERATIONS 337

Japanese workers presented a vast amount of data in a series of papers on the results of their
investigations (Nishiwaki and Hayashi, 1950; Nishiwaki and Oye, 1951; Mizue and Murata, 1951;
Ohno and Fujino, 1952; Kakuwa, Kawakami and Iguchi, 1953). These followed the methods
employed by Mackintosh and Wheeler (1929) and are in general agreement, though it is clear that no
consistent pattern is present in the occurrence of maxima in the frequencies of corpora. They give
average lengths at sexual and physical maturity, but there are variations and inconsistencies in their
findings. As criteria of physical maturity they accept fusion of the epiphyses in mid-lumbar or
thoracic regions and since fusion is in fact usually completed in the anterior thoracic vertebrae their
estimates are necessarily low.

Ruud had shown that the ridges on the baleen plates could be used to estimate the ages of whales,
though after the first few years wear at the tips was greater than replacement in the gum so that the
method then gave minimum ages only (Ruud, 1940, 1945 ; Ruud and Jonsgard, 1950). The technique
is to record and amplify the variations in thickness of the baleen plate by means of a suitable apparatus.
In these recordings they claim to be able to distinguish annual steps or ridges associated with changes
in the nutritive state of the individual. As long as the pattern diagnostic of the baleen laid down in
lactation is present they feel they can be quite confident about the age. In his second paper, Ruud
showed that the age of the fin whale at sexual maturity was more likely 3 years than 2. In the third
paper it was shown that the blue whale also attained sexual maturity at later ages, averaging 5 years.
In the first season of maturity slightly less than two ovulations occur and corpora subsequently
accumulate at a rate of a little more than one a year; the maximum number of ovulations in any one
period of heat appeared to be four. Hylen, Jonsgard, Pike and Ruud (1955) published the results of
the examination of baleen plates from over seven thousand fin whales taken in the antarctic between
1945/46 and 1952/53. They state that they believe age groups O, I, II and III can be determined with
great exactitude, because traces of suckling baleen can be recognized. In older groups there is some
confusion, but they believe that the mistakes are few in group IV. Elsewhere (Hylen et al. unpublished
report) they stated that sexual maturity in the female is attained in groups II-IV, averaging 4 years of
age. A full account of the method is to be given in a later publication.

Tomilin (1940, 1945) also drew attention to the use of the ridges on the baleen plates for ageing
whales and Nishiwaki in a series of papers (Nishiwaki and Hayashi, 1950; Nishiwaki, 1950a; 19506;
195 1 ; 1952) took up the problem. In the first two of these papers he drew attention to changes in the
coloration of the crystalline lens of the eye. He measured the absorption of light by the lens (expressed
as a percentage) using a photocell, and claimed that it increased regularly with age, as measured
relatively by length, ovarian corpora, testis weight and physical maturity. This is not a very con-
vincing piece of work, because large corrections are necessary to allow for the changes dependent on
variations in the time post-mortem. Nevertheless, Nishiwaki (1950 a) believed that it was more
accurate and reliable than any other method of age-determination although it does not give a measure
of absolute age. In the next two papers he takes up the question of ageing by means of the ridges in
the baleen plates by Ruud's method and using his recording apparatus. He suggests that the average
age at sexual maturity, which Ruud had placed at three years, should be four years, as Hylen et al.
(unpublished report) later confirmed. He also suggests that four corpora accumulate each baleen
period. Later (195 1) he examined the rate of growth in length of the baleen by comparing the distance
from gum to the first main ridge, with the length of baleen formed in the next period. This ratio he calls
the growth index, which is expressed as a percentage of the latter period, and he calculates the weekly
growth-rate during the whaling season. Assuming the growth-rate to be constant throughout the year
he found that the annual increment was equivalent to one full growth-period. In a later paper
Nishiwaki (1952) re-examined his data and combined the results of the work on the crystalline lens

338 DISCOVERY REPORTS

with the baleen readings. He confirmed that the female fin whale attains sexual maturity at 4 years of
age and the male at t,\ years and used two large blue-whale foetuses to obtain an estimate of the degree
of coloration of the lens at birth. He then calculated the annual increment in coloration of the lens
from birth to sexual maturity (taking 4 years as the age at maturity) and applied this to the increase
in coloration from sexual maturity to physical maturity to obtain an estimate of the length of this
period, which he found to be approximately 6 years. He then assumes that two ovulations occur at
sexual maturity and in the fin whale a further 9-5 up to physical maturity. Then the annual increment
of corpora after the first year should be 1-5. The discrepancy between Nishiwaki's estimate of the
number of corpora accumulated at physical maturity (11-5) and those of earlier workers (13-15)
results from the use of different criteria as mentioned below, but this would not affect the result
since it applies to both number of corpora and coloration of the lens. In the same way he obtains
for the blue whale an average increment of corpora of 1-64 per year, and gives a table showing growth
in length from sexual maturity up to 12 years. Although the figure of two to three ovulations per
breeding cycle obtained by Nishiwaki agrees quite well with the conclusions put forward in the present
paper, there are serious objections to his methods. The most important is the controversial nature of
the evidence from the crystalline lens. Corrections are necessary to allow for the post-mortem changes,
and the estimate of the degree of coloration at birth seems to be little more than a guess. Recent
work both on baleen plates and on ear-plugs suggests that sexual maturity in the female fin whale is not
attained until on average 5 years of age.

Since Mackintosh and Wheeler (1929) and Ommanney (1932) gave a general account of the repro-
ductive tract, this aspect of the reproductive biology has received little attention, apart from an
important paper by Matthews (1948). He demonstrated a well-marked cycle of change in the uterine
mucosa from sexual immaturity, pregnancy, lactation, and anoestrus correlated with the state of the
ovaries, mammary gland, etc. Post-partum involution is rapid and appears to occur without loss of the
mucosa. Slijper (1949, 1956) also gives some information on the reproductive organs during pregnancy.

Relevant work on other species will be discussed later in this paper, but mention must be made here
of a valuable series of papers on the humpback whale (Megaptera novaeangliae) by Chittleborough
(1954, 1955a, 19556, 1958) who was able to work on this species in the southern winter near its
breeding grounds off West Australia.

When the present work began in 1954 the general outline of the biology of the fin whale had been
established relatively unchanged since 1930. The female was assumed to be polyoestrous and various
estimates of the rate of ovulation had been made, none of which could be accepted without reservations.
No conclusive evidence of the complete persistence of corpora albicantia had been put forward and
they could not be used as measures of age except in a very general way. The estimates of age based on
baleen plates still required a final proof and could only be applied to young animals. The nature of the
evidence from the crystalline lens was controversial.

Since then a new method of age-determination has been discovered by Purves (1955) and its value
confirmed by Laws and Purves (1956), Nishiwaki (1957), Nishiwaki, Ichihara and Osumi (1958) and
Purves and Mountford (1959). This depends on the presence of well-defined laminations in the
ear-plug of whalebone whales which, once laid down, constitute a permanent record. Work on large
collections of ear-plugs from antarctic fin whales is proceeding. This appears to confirm the figure for
the annual increment of corpora albicantia given in this paper, but suggests that the ages at sexual
maturity of both sexes are higher than previous workers have claimed.

The major part of the present paper concerns the female reproductive biology, and the work was
carried out before the value of the ear-plug was known. Probably the most important confirmation of
the value of the ear-plug for age-determination lies in the correlation which has been found between

GENERAL CONSIDERATIONS 339

the ages estimated from the ovaries and from the ear-plugs of a series of female fin whales. The value
of this evidence depends on the completely independent nature of the two lines of work and for this
reason and because they were not available when the work was carried out the ear-plug data will not be
used in the first part of this paper.

Migrations
The growth-rates and mature sizes of northern and southern hemisphere fin whales are very different
and the average annual cycle is 6 months out of phase, so we can take it that there is no important
degree of interchange between them (Omura, 1950; Jonsgard, 1952; Pike, 1953), but the animals in
both hemispheres do undertake long seasonal migrations. Kellogg (1929) summarized what was then
known about the migrations of baleen whales. Most of this evidence relates to whales seen on passage
in the northern hemisphere and reveals a movement from low to higher latitudes in spring and a
return movement in the autumn. Mackintosh (1942) has also discussed the evidence for these migra-
tions and concludes that it ' can leave no doubt that there is a general tendency for Blue and Fin whales
to undertake long annual migrations between the Antarctic and temperate or tropical waters, though
this is not to say that the Antarctic is completely deserted in winter or the warmer waters in summer '
(p. 250). The humpback whale is a coastal species and migratory herds may regularly be seen from
the coasts (Chittleborough, 1953 ; Dawbin, 19566). In the longitude of New Zealand the main herds
are said to leave antarctic waters in early May, to reach 460 S. by mid-June, and to arrive at the
breeding area at latitude 150 S. by mid-August.1 On the return migration they reach 460 S. by early
November and arrive at the feeding area about 66° S. by mid- to late December. The vanguard and
rearguard reach the respective latitudes approximately 6-7 weeks earlier or later than the main group
(Dawbin, 1956, p. 193). The fin whale is not a coastal species so direct observations of migrating
animals are few and most of the evidence is circumstantial, but we may also reasonably draw analogies
with the humpback whale. Some direct evidence comes from whale marking ; 22 humpback whales
marked in the antarctic were recovered off north-west Australia (Rayner, 1940), and a further nine
in recent years, but so far there are only two marked fin whales to demonstrate the migration.2 One
marked in the antarctic in 640 52' S., 220 30' E. in February was recovered off Cape Province, South
Africa, 330 04' S., 170 50' E. at the end of June 2 years later (Rayner, 1940); another was marked in
October off the coast of Brazil in 280 03' S., 460 17' W. and recovered after 11 years near South
Georgia in 520 55' S., 380 42' W. (Brown, 1954)2. Rayner and Brown established, as a result of marking
returns, that these whales tend to return to the same antarctic locality and are partially segregated in
certain broad areas though there is some lateral dispersal.

The indirect evidence comes from a number of sources. There is an important reference by Morch
(191 1) to the occurrence of great numbers of fin whales along the Brazil coast, between 120 and 180 S.
latitude every year from May to November, but this has not been confirmed. It is significant that
whaling operations in the Antarctic have been largely confined to the period October-April with the
largest catches obtained from December to March. In low latitudes off South Africa catches are
made in the period May-October. This indicates that the bulk of the population spend the winter
months in lower latitudes, and the summer in the Antarctic, but at one time catching was carried on
throughout the winter at South Georgia, so not all migrate north in the autumn. Recently Brown
(1957, p. 163) has found that 'not all rorquals go south for the southern summer and it may be that
more than was thought either miss the southern migration altogether, or get out of step with the main
migration movements'.

1 Chittleborough's work suggests mid-July off West Australia.

2 Later mark recoveries have confirmed the humpback movements and Brown (1959, i960) gives details of five addi-
tional fin whale recoveries.

Mackintosh and Brown (1956) examined the records of whales observed through an organized
look-out system in the R.R.S. ' Discovery II ', covering nearly 47,000 miles steaming in the Antarctic,
and drew up a curve showing the variation in the size of the antarctic population of the larger baleen
whales, month by month. This curve shows a maximum in February/March and a minimum in
July /August and indicates that most of the population leaves the antarctic zone in winter. This curve
represents the total numbers of blue, fin, and humpback whales, although a few sei whales may be
included and some immature age groups are probably missing. From inspection of the antarctic
catches and the variations in numbers calculated by Mackintosh and Brown it appears that fin whales
spend an average period of about 4 months south of the antarctic convergence and that the main part
of the population is south of the convergence from mid-December to mid-April.

The incidence of diatom infection on the skin of whales is indirect evidence of migrations (Hart,
1935) and suggests that while some individuals may spend the winter in antarctic waters almost all
migrate to low latitudes in winter. Similar evidence is provided by the parasites which attack blue
and fin whales in low latitudes and the partly explained presence of healed oval scars (Mackintosh and
Wheeler, 1929; Mackintosh, 1942; Pike, 1951).

The chief contributing factors to the migrations of fin whales are undoubtedly food and temperature.
Marr (1956) states that the main diet of the southern baleen whales consists of the crustacean Euphausia
superba, known as krill, over 20 mm. long, and it appears that this size is very much more abundant
in January, February and March than at other times of the year. The main concentrations of krill are
confined to the East Wind drift in latitudes south of 6o°-65° S. except in the Atlantic Sector where the
Weddell drift brings a rich population into lower latitudes as far north as South Georgia (540 S.). The
whales feed heavily on these populations of krill in summer and must feed but little in the warmer
waters in winter. As a result, the animals in the winter catch at low-latitude shore stations show
progressively decreasing blubber thicknesses and they are in poor condition when they move south
in the spring. Once they are in antarctic waters the blubber thickness and oil production increase
as the season advances (Ash, 1955, 1956).

Whales are mammals and maintain a body temperature of about 370 C. This implies that in cold
waters more energy is expended to maintain this temperature than in warm waters. On average at the
latitude of 620 S. the sea surface temperature is above — 1° C. from December to June, but at 640 S.
this temperature is exceeded only from January to April (Mackintosh, 1946), which is also the period
when large krill appear to be abundant. When krill ceases to be abundant it is presumably dis-
advantageous for the baleen whales to be in cold waters and by moving to warmer regions they are
able to reduce their energy expenditure while drawing on their reserves of fat.

The pattern of migration which has now been described applies to the population as a whole, but
the movements of the different classes of fin whale differ in time and there are regular seasonal changes
in the composition of the antarctic population from month to month. The sex-ratio tends to remain
fairly constant, but Mackintosh (1942) suggests that the vanguard of the main herds of fin whales
arriving on the whaling grounds in January is composed mainly of males and towards the end of the
season females tend to be in excess of males. The percentage of immature whales in the catch increases
towards the end of the season and the average length of the catch decreases. Wheeler (1934) showed
that at South Georgia the average age declines through the season ; the majority of physically mature
females are taken in December, of sexually mature but not yet physically mature females in January,
and the peak influx of immatures is in February. This is also true of the pelagic catch though the
corresponding maxima occur rather later. The antarctic population of adult females also shows con-
spicuous seasonal variations in quality. Mackintosh (1942) showed that at South Georgia the per-
centage of adult females in the catch which were pregnant fell from 85 % in October to 27 % in

GENERAL CONSIDERATIONS 34*

April, these figures being averaged over a number of years. A similar though less marked decline
from December to March has been shown in the pelagic catch also by a number of workers (Mackin-
tosh, 1942; Nishiwaki and Hayashi, 1950; Nishiwaki and Oye, 195 1 ; Ohno and Fujino, 1952; Kakuwa,
Kawakami and Iguchi, 1953). This is partly a result of the entry into the catch of resting females
which were recently lactating and therefore protected and under-represented in the catch, but Ohno
and Fujino (1952), Kakuwa, Kawakami and Iguchi (1953) and Laws (19590) also suggest that preg-
nant females migrate northwards earlier than the others.

Ash (1955) showed how the rate of increase in blubber thickness was constant through the season
and could be represented by a straight line ; the curves describing the increase in oil content for two
consecutive seasons (1953/54 and 1954/55) are nearly parallel, indicating that the rate at which whales
lay down fat is independent of the store already there. He suggested that the variations about the
regression lines representing blubber thickness and oil production might indicate waves of migration
coming south, and points out that such waves of migration were observed by Mackintosh and Wheeler
(1929) at South Georgia. In a later paper (Ash, 1956) he broke down the data on blubber thickness
into separate figures for males, and for pregnant, non-pregnant and lactating females. He shows that
males and non-pregnant females are represented by two curves which are almost identical, while the
curve for pregnant females is well above, but nearly parallel to them, closely following the alterations
in slope. He suggests that whales arrive in the Antarctic in groups which are made up of males, females
which are pregnant and those which are not, and that these groups maintain their identity throughout
the season. Ohno and Fujino (1952) have similar data.

We may conclude then, that fin whales undertake long seasonal migrations between the Antarctic
and waters to the north. In the summer, largely from December to April, they are feeding on
Euphausia mperba in high latitudes and then move northwards to become dispersed over an immense
area of ocean in winter, some to tropical waters and many in sub-tropical and temperate regions. It
would appear that both the north and south migrations of older animals and of pregnant females are
in advance of those of other groups and that the sexually immature animals are later.

THE OVARIES

For ovaries examined since 1954, drawings and records of the size and appearance of the ovaries, and
the number, size, and appearance of the corpora lutea, corpora albicantia and follicles were made.

Size
No late foetal ovaries have been examined, but the average dimensions of four pairs of fixed ovaries from
foetuses between 2 and 3 m. in length were: length 46 mm., breadth 17 mm., depth 12 mm.; the
mean weight of single ovaries was 6-6 g.

Measurements of the dimensions of fixed post-natal ovaries are inaccurate because of distortion,
but measurements were made on 131 pairs of fresh unfixed ovaries in the 1953/54 season.

Eight immature ovaries were of mean length 27 cm., breadth 8-2 cm., depth 3 cm. ; 52 ovaries from
non-pregnant mature females were of mean length 31-1 cm., breadth 11-4 cm., and depth 4 cm. Of
105 pairs of ovaries from pregnant females the ovary which contained the corpus luteum was of mean
length 33-2 cm., breadth 12-1 cm., depth 4-2 cm. (excluding the corpus luteum) and for the other
ovary the length was 32-3 cm., breadth 11-9 cm., depth 3-9 cm.

Weight is a better index of the size of the ovary and there are records of the combined weight of
both ovaries for 1567 female fin whales from eight seasons between 1939/40 and 1955/56. The
frequency distribution of combined ovary weights (in 0-5 kg. groupings) for these three classes of

342 DISCOVERY REPORTS

animals are presented in Text-fig. i . The records for immature females are not of course representative
of the whole class of immatures, for, owing to the operation of the minimum length regulations, they
include only those animals which are nearing sexual maturity. The intersection of the curves for
immature and non-pregnant mature ovaries is at 0-6 kg. and for immature and pregnant ovaries at
0-95 kg., but owing to the wide variation in ovary weight near puberty there is a considerable overlap.
Between immature and non-pregnant mature, the overlap is from 0-25 to 175 kg., and between
immature and pregnant from 075 to 175 kg. It is not, therefore, possible to distinguish between all
immature and mature females on the basis of ovary weight. The mean ovary weights for the different
classes are shown in Table 1 . The difference between the mean ovary weight of pregnant and non-
pregnant mature females is both absolutely and proportionately much greater than Chittleborough
(1954) noted for the humpback whale, and is statistically significant.

COMBINED OVARY WEIGHT
* * IMMATURE

NON- PREGNANT

PREGNANT

SINGLE OVARY WEIGHT

3 c NON PREGNANT

« • PREGNANT WITH C.L.

►•-— • PREGNANT WITHOUT C L

5 6 7
KILOGRAMS

2 3

KILOGRAMS

Text-fig. 1. Frequency distributions of ovary weights.

Table 1 . Summary of ovary weight records

Combined weight (kg.) Single weight (kg.)

Class

Immature

Non-pregnant

Pregnant with corpus luteum ^

Pregnant lacking corpus luteum J

Total

No. of pairs

Mean

No. of ovaries

Mean

132
569

o-97
1-97

352

1-04

866

3-i4

403
391

2-13
1-24

1567

1 146

The increased weight of the ovaries of pregnant females is only partly explained by the presence of
the large corpus luteum. The mean weight of 372 corpora lutea was o-88 kg. (see p. 357), and the
ovaries of pregnant females weigh on average 1-17 kg. more than those of non-pregnant females. The
discrepancy is probably to be accounted for by increased vascularization and increase in follicle size
and numbers (see p. 348) which affects both ovaries of pregnant females.

In two recent seasons (1953/54 and 1955/56) 1146 mature ovaries were weighed separately. The
frequency distribution is shown in Text-fig. 1 and the mean weights are set out in Table 1. These
figures show that there is a mean difference of about 0-2 kg. between non-pregnant and pregnant
ovaries without the corpus luteum, and a difference of about 0-89 kg. between the two ovaries of a
pregnant female which is accounted for by the corpus luteum (mean weight o-88 kg.).

the ovaries 343

Giant ovaries
Although the combined weight of a pair of fin-whale ovaries is usually less than 10 kg. and of blue-
whale ovaries under 16 kg., there are two records of ovarian hypertrophy. One is of an 83-ft. pregnant
blue whale with ovaries weighing in all 59-4 kg. (Laws, 1954). The other, previously unpublished, is
a lactating female fin whale with ovaries together weighing 52 kg. (26 kg. each), which were examined
at South Georgia in 1929. Both ovaries of this whale had a number of large bodies which appeared
like hypertrophied corpora lutea; they showed a corona-like structure and several of them had a
central cavity (see p. 359), but they were composed of white fatty tissues. There were four of these
bodies in one ovary, of mean diameter 30, 25, 18 and 13 cm., and six in the other ovary measuring
23, 22, 21, 17, 11 and 8 cm. In the first ovary there were four corpora albicantia but no macroscopically
visible follicles, and in the second ovary was a large protruding cyst 12 cm. in diameter.

In both examples of giant ovaries there was excessive fat deposition, but the blue-whale ovaries
were otherwise normal. The fin-whale ovaries now described must be classed as pathological in view

of the ten abnormal fatty bodies.

Morphology

The external appearance of the ovaries has been described and figured by Mackintosh and Wheeler
(1929) and Ommanney (1932). In the foetus they are small, compact, tending to taper posteriorly
with an irregularly grooved surface divided into a number of flattened lobes by branching sulci. In
sexually immature females the ovaries elongate, and the smaller grooves gradually disappear so that
the surface is smooth. Towards sexual maturity the development of Graafian follicles leads to the
formation of rounded protuberances. In the adult the ovaries usually have a flattened elongated
egg-shape, tapering posteriory, with many rounded follicles and corpora albicantia protruding, the
latter often attached by only a small area at the base. The corpora lutea usually project almost entirely
from the body of the ovary and are sometimes connected only by a narrow neck. The colour of the
ovary is a pink-grey-white, varying somewhat with the circumstances of death.

The ovary is reduced in thickness at the hilum, where it is attached to the mesovarium. Blood
vessels and lymphatics enter and leave the ovary along this narrow connexion and the ovarian artery
divides into a number of branches before entering the ovary. In a 68 ft. non-pregnant mature female
there were respectively 1 5 and 1 6 arteries visible at the hilum of each ovary.

The medulla is a dense mass of white fibrous tissue supporting the many tortuous arteries, veins
and large lymphatic sinuses. The larger arteries have a spiral configuration (Reynolds, 1950). A few
branches pass into the cortical layer which invests the medulla up to the hilum. This cortex is 1-6 cm.
in thickness and contains the developing and atretic follicles, the corpora lutea and corpora albicantia.

At the periphery of the cortex of sexually immature females under 60 ft. long a thin layer of cubical
germinal epithelium rests upon a fibrous tunica albuginea which is already 150-250// thick. In
sexually mature females no germinal epithelium has been found and the tunica albuginea is usually
more than 1 mm. thick. The large follicles rest on the medulla and as they expand protrude from the
surface of the ovary, filling the full thickness of the cortex. It is probable that the protrusion of the
follicles and corpora as they mature is a consequence of the relatively rigid fibrous supporting nature
of the cortex and medulla of baleen whales. In the odontocetes Globicephala melaena (Harrison, 1949),
Pseudorca crassidens (Comrie and Adam, 1938), and Physeter catodon (Matthews, 1938a), the ovary
accommodates the growing follicle or corpus luteum so that the latter remains for the most part
invested by cortical tissue and the ovarian surface is smooth. In some fin-whale ovaries there are a
few small stalked mushroom-shaped bodies of fibrous tissue projecting from the hilus or from the
ovarian surface.

344 DISCOVERY REPORTS

Laws (1957) examined the distribution of corpora albicantia and corpora lutea in 394 fin-whale
ovaries and found the probability that the corpora are not randomly distributed to be highly signifi-
cant. For 30 ovaries for which the orientation was known 74-1 % of the total corpora were in the
anterior half. In 32-7% of ovaries with two or more corpora they are entirely confined to the anterior
half of the ovary. The position of the corpora in relation to the long axis of the ovary was measured
in 96 fin-whale ovaries. This shows a progressive decline in the frequency of corpora at increasing
distances from the anterior pole, and they are completely absent from the posterior third of the largest

ovaries.

Relations

Ommanney (1932) has described the position of the ovaries in relation to the reproductive tract in the
foetus. An adult female and an immature female have been examined closely in connexion with the
present study and will be briefly described.

In the foetus the ovary lies free on the broad ligament and the triangular fibrous sheet extending
from the ovarian funnel does not cover the ovary (Ommanney, 1932, figs. 12 and 13).

One ovary of a 75-ft. pregnant female weighed i-6kg. and measured 27 x 12 x4 cm. It bore a
corpus luteum, weight 0-7 kg., diameter 10-3 cm., and three large corpora albicantia. The other ovary
weighed 0-65 kg. and measured 25 x 12x3 cm., but had no corpora. The transparent fibrous sheet
extending from the ovarian funnel was rhomboid in shape and measured 60 x 50 cm., the longest axis
stretching from the anterior pole of the ovary to the uterine horn. The ostium abdominale was situated
just anterior to the intersection of the two main axes. The edges of this sheet were free except where
it was attached by a short ligament in the vicinity of the anterior pole of the ovary, and by a longer
and more slender ligament medially to the uterine horn ; in contrast to the foetus it was not attached to
the posterior pole of the adult ovary. This sheet is normally folded lengthwise so that it invests the
anterior part of the ovary and is attached to the broad ligament along the line of this fold. It cor-
responds to the funnel-shaped pouch described by Harrison (1949) in Globicephala melaena, and as in
that species the inner aspect is lined by numerous membranous ridges running inwards to the ostium,
which is lined by ciliated fimbria. The short ligament attaching the anterior end of this pouch was not
observed to continue to the ostium abdominale in this specimen as described by Daudt (1898) and
Ommanney (1932). An immature female 61 ft. in length had ovaries 24x5-2x2 cm. in size; the
relations of the ovary were similar, but the pouch differs somewhat from that of the pregnant female.
It over-arched the anterior two-thirds of the ovary and resembled the bursa ovarii of the dolphin
Stenella figured by Burne (Fraser, 1952, fig. 33) or the 'delicate arched covering or pavilion' of
Globicephala (Murie, 1873). In this immature female a conspicuous fimbriated groove extended from
the anterior pole of the ovary to the foremost edge of the ostium abdominale. This was described by
Ommanney (1932), but was not observed in the pregnant female described above.

The Fallopian tube lies on the broad ligament partly covered by the ovarian sac. In the pregnant
female it was 61 cm. in length when straightened out. At the ostium abdominale the diameter of the
lumen was 4-0 cm.; at a distance of 20 cm. from the ostium it was 1-5 cm. in collapsed diameter and
lined by numerous longitudinal folds, and a further 20 cm. from the ostium it had narrowed to 4 mm.
and had four longitudinal folds. For the first two-thirds of its length it was sinuous, and then almost
straight; where it entered the uterine horn there was no papilla or constriction. The Fallopian tube
of the immature female measured 49 cm., the first 22 cm. next to the ostium being much folded and
the remainder more direct. The lumen was 1-75 cm. in diameter at the ostium, 1-25 cm. at a distance
of 10 cm. from the ostium, 1-05 cm. at 20 cm. distance and 0-3 cm. at 30 cm. distance. For the first
half the epithelium was much folded, but regular longitudinal folds appeared in the second part.

From the anterior pole of the ovary a large fold, the plica diaphragmatica, runs lateral to the

THE OVARIES 345

kidneys and forwards to the diaphragm; a large pink-coloured lobe of fatty tissue arises from this
fold near to the anterior pole of the ovary. In the pregnant female it measured 42 x 25 x 10 cm. and
in the immature female about 33 x 21 x 7 cm. This reddish-pink fatty lobe is very conspicuous against
the grey-white peritoneum and serves as a useful landmark when searching for the ovaries on the
flensing deck. Rounded fatty lobes have also been noticed in the broad ligament.

From the posterior pole of the ovary two conspicuous ovarian ligaments extend, one to the uterine
horn and the other along the broad ligament. In addition a broad fold representing the mesovarium
runs over the broad ligament carrying most of the blood vessels, lymphatics and nerves to the ovary.

The differences between this account and the description given by Ommanney (1932) are the result
of comparing the foetal anatomy with the adult. The most important respect in which they differ is
the development of the ovarian sac in the sexually immature and adult female, whereas in the foetus
the ovary 'lies free on the ligamentum latum and is not enclosed in any sort of sac or pavilion'
(Ommanney, 1932, p. 444).

GRAAFIAN FOLLICLES

Foetal ovaries

Chittleborough (1954, pi. 1) found abundant primary follicles up to 0-13 mm. in diameter in ovaries

from near-term humpback-whale foetuses 4-54-4-66 m. long. The average neo-natal length in this

species is 4-56 m. (Chittleborough, 1958).

The neo-natal length of fin whales averages 6-4 m. (Laws, 19596) and of 956 foetuses of known
length in the present material none was above 6-o m. Only 0-9% are above 4-0 m. and only 0-4%
above 4-5 m. This is a result of sampling being restricted to a period when most females are in mid-
pregnancy, whereas Chittleborough's sample are in early or (the majority) in late pregnancy. Con-
sequently no near-term fin-whale foetal ovaries are available for examination. All foetal ovaries
examined including the largest, from foetuses measuring 3-8 and 4-16 m., show as yet no development
of primary follicles. The genesis of follicles must, therefore, begin in the last 2 or 3 months of gestation
as in man.

Immature ovaries
Owing to the minimum size regulations for the antarctic pelagic catch in recent years only the larger
immature females are sampled.

The cortex of two pairs of immature ovaries from females of length 54 and 56 ft. which have been
sectioned for histological examination contained very numerous primary follicles, most of which were
from 45 to 70 fi in diameter. These are already separated from the germinal epithelium by a tunica
albuginea which is about 150-250 fi in thickness (PI. IV, fig. 6).

The size frequency distribution of the largest follicle in 80 pairs of immature ovaries in the material
is shown in Text-fig. 2. The majority, 66%, are less than 1 cm. in diameter; only 17-5 and 8-8% are
over 2-0 and 3-0 cm. respectively, the largest being about 5 cm. With few exceptions these follicles
appeared to be atretic with thick elastic walls, and when a sample was examined histologically it was
confirmed that they were in varying degrees of atresia.

One immature female examined in 1954 (on 10 February, length 68 ft.) had ovaries of unusual
appearance. The body of each ovary was very thin and strap-like, measuring 22 x 6-5 x 1-5 cm. and
26-5 x 5-5 x i-o cm., the corresponding weights being 0-4 and 0-3 kg. Each ovary had several large
follicles projecting from the surface and often connected only by a small neck. The largest were
3-5 and 2-7 cm. in diameter. These follicles had very thin transparent walls in which the blood vessels
were very conspicuous. In view of their relatively small size and lack of turgidity it seems unlikely

3-2

346

DISCOVERY REPORTS

Table 2. Immature fin whale females approaching puberty : mean maximum

follicle diameters

Mean max. follicle size (mm.)

Size of ,

Month

sample Monthly

Grouped

S.E.

January

20 io-8

—

2-25

February

14 io-6

—

171

March

12 5-0

—

April

3 6-ol

May

2 6-oj

o-o

269

June
July

2 29-5 1
1 3o-oJ

29-66

2-12

August*

4 32-5

—

2-I7

October

1 25-0 1
3 33-oJ

November

31-25

S-69

* 61-63 ft-

length.

f The March

sample values are all recorded as about 5

mm.

a 40

O 30

y 20

IMMATURE

NON-PREGNANT

PREGNANT

4 S 6

DIAMETER IN CMS.

Text-fig. 2. Frequency distributions of maximum follicle diameters.

that these were maturing follicles, but they may have reached a stage of development at which regres-
sion was about to begin.

Mackintosh and Wheeler (1929) showed that the size of the largest follicle in female fin whales
approaching puberty increased from a minimum in January-April, to about 3 cm. in June and July.
There are in the present material 62 pairs of ovaries from immature females which were approaching
puberty (defined as females over 63 ft. in length, except for four immature females taken at Durban
which were 61-63 ft. in length). In Text-fig. 3 the means and variation of seven samples from January,
February, March, April and May combined, June and July combined, August, October and November
combined, are presented. The June/July sample is from Saldanha Bay, South Africa, and the August
sample is from Durban, South Africa. Although the size of the critical samples is small, this evidence
suggests that there is a follicular cycle showing one or more peaks from June to November or December,
when the maximum follicle size is about 3 cm. or more, and minimum values between December (or
January) and May, when the maximum follicle size is about 1 cm. or less. The absolute maximum
size, from an immature female taken in November, was about 5 cm.

This agrees with conclusions about immature humpback whales based on material collected in the
breeding season of this species. Chittleborough (1954) states that immature females with follicles at

GRAAFIAN FOLLICLES 347

or above 3 cm. in diameter are maturing and approaching the first ovulation. The fin- whale material
shows that in most mature females and in some immature females, follicles above 3 cm. may be in
cystic atresia. The present evidence suggests that immature fin whale females may be approaching
the first ovulation in June, July, August, October, November and possibly September and December.

§ 40

2
<

20 14

SIZE OF SAMPLE
3 4

20 14

2 20-

< 10

■Hvi

- / -• — •-

J J A

MONTHS

Text-fig. 3. Monthly mean size of largest follicle in 62 pairs of ovaries from immature females which
were approaching puberty (mean ±2 S.E. ; black, South Africa; white, Antarctic).

Adult ovaries

Primary follicles

Laws (1957) stated that in adult fin-whale ovaries the tunica albuginea is from 0-95 to i-6 mm. in
thickness and that no primary follicles had been seen in histological preparations. Since then very
small numbers of primary follicles have been observed in the ovaries of two mature fin whales, one
of length 73 ft. in anoestrus, and one of 70 ft. pregnant with a foetus 279 m. long. These primary
follicles are very few and scattered in distribution and their absence in other mature females examined
is probably more apparent than real. For instance, the average surface area of one ovary of a non-
pregnant mature female is about 800 sq. cm. and it would be a major task to sample even one pair
adequately. Usually only one or two samples representing 0-1-0-3 % of the surface area are embedded
and in a large series it is impracticable to examine more than about one-tenth of this material histo-
logically, so that less than 0-05 % of the cortex is searched. The large size of the organ is a very real
handicap in any studies of the finer details. It is probable, however, that the numbers of primary
follicles decrease greatly with age. In the rabbit, for instance, Desaive (1941) found that these
decreased from 120,000 at 3 months to 6000 at 18 months.

' Recently ovulated ' females
There are records of the diameter of the largest follicle in 23 recently ovulated fin whales taken in the
Antarctic, most frequently in November-December. These may be characterized as females which had
a large and apparently normally active corpus luteum in the ovaries, but in which an intensive search
of the uterus failed to reveal a foetus. Four pregnant females with a foetus less than 4 cm. long are
also included in this group. The correctness of the diagnoses of recent ovulations is confirmed by the
data set out in Text-fig. 4. Thus, in pregnant females considered as a whole, the mean maximum

348 DISCOVERY REPORTS

follicle size is 278 ±0-15 cm. and the recently ovulated class of females has a mean maximum follicle
size of 3 -8 ±0-53 cm. This statistically significant difference disposes of the possibility that the
' recently ovulated ' females were pregnant females in which a foetus had been missed in the search,
or even pregnant females which had aborted their foetus when harpooned. It is, however, possible
that very small embryos could have been overlooked in some of them. The occurrence of recently
ovulated females in summer in the Antarctic is a fact which is of great importance in establishing the
nature of the annual reproductive cycle in the female fin whale (p. 436).

Chittleborough (1954) does not give figures for the size of the largest unruptured follicle in the
ovaries of humpback females after ovulation. He gives (in his fig. 3) maximum follicle sizes for females
approaching ovulation, which by his definition are females in which the largest follicle is over 3 cm.
in diameter. For 38 females with follicles over this critical diameter the mean maximum follicle size
is 4-4 cm., and the largest follicle, at 10-5 cm., was close to the time of rupture. One pair of ovaries
had maturing follicles measuring 53, 37, 35, 34 and 30 mm.

Pregnant females

It has been pointed out that most of the females in this class which have been examined are in mid-
pregnancy (with foetuses 0-5-3-0 m. in length). The frequency distribution of the diameter of the
largest follicle in 341 pairs of pregnant ovaries is shown in Text-fig. 2, the mode being 2-5 cm. and
the mean 2-78 ±0-15 cm. This is in contrast to the condition in humpback whales in late pregnancy
in which the mean diameter of the largest follicle in 45 pairs of ovaries is 6-4 ±0-9 mm. (Chittle-
borough, 1954). There are very few records from fin whales in the last quarter of pregnancy and the
diameter of the largest follicle in lactating whales (1-93 ±0-34 cm.) although smaller than in pregnant
females is not as low as in late-pregnancy humpbacks. However, in the Antarctic the majority of
lactating fin whales taken are in late lactation (p. 446).

The records from pregnant females can be subdivided according to the foetal lengths so as to give
an indication of the variation in follicle size during pregnancy. This has been done for 341 females and
the result is given in Text-fig. 4, which shows the range, mean and twice the standard error of the
mean for each foetal length group. In the 0-0-5 m- grouP f°ur records from foetuses of length 4 cm.
or less have been removed to the ' recently ovulated ' class. Out of 23 records for the 4-6 m. length
group, two are of maximum follicle diameters of 7 and 8 cm. These are clearly separate from the
remaining records and if used they introduce a heavy weighting; they are thought to be abnormally
persistent large cystic follicles and in calculating the mean size they have been rejected. Only two
records of follicle size from females with foetuses over 5 m. are available; the largest follicles were
respectively 8 cm. (mentioned above) and 2 cm. in diameter.

The mean maximum diameter decreases from 3 -8 ±0-53 cm. in recently ovulated females to
2-53 ±0-3 cm. in the first few months of pregnancy, then appears to increase to 3-12 ±0-28 cm. at
mid-pregnancy followed by a decrease to 2-07 ±0-42 cm. about 1 month before parturition. With the
exception of recently ovulated females the values for the mean ± 2 s.E. overlap, owing to the variability
in follicle size, but the maximum values and the percentage of records over 3 cm. (Text-fig. 4) also
follow this pattern, so it probably represents a real cycle in follicle activity, with a period of about
5-6 months. Such follicular cycles are known during pregnancy in other mammals and are usually
of the same period as the dioestrous cycle (see p. 352). Usually the follicles enlarge but enter cystic
atresia before maturing, but in some species ovulation takes place with the production of accessory
corpora lutea. It is unfortunate that there is no material from late pregnancy for the fin whale, but it
is impossible to ignore the evidence concerning follicle size in late-pregnancy humpback whales,
because in other respects the two species have so many features in common. The values for late-

GRAAFIAN FOLLICLES 349

pregnancy humpback whales have, therefore, been inserted in Text-fig. 4 at a foetal length cor-
responding to late pregnancy in the fin whale.

Another factor which must be mentioned is that in mature blue and fin whales the diameter of the
largest follicle is proportional to the body length (Nishiwaki and Oye, 195 1 ; Nishiwaki and Hayashi,
1950). It is shown later (p. 411) that older mature females are in advance of younger mature females
in their sexual cycle and, therefore, have the larger foetuses at any one time. In the material under
consideration, which is limited in time to a few months, the average maternal age and the average
maternal body length increase with increasing foetal length. In accordance with the findings of the
Japanese workers there would, therefore, be a bias towards larger follicle diameters in the second half

100

§ so

9
8

i-
uj 5

-1 3
U

6 01 ' o^ 10 20 x> 10 to °

PREGNANT (FOETAL LENGTH)] LACTATION [ RESTING j PREGNANT

' J 'j/a's'o'n'd'j 'f'm' a'm'j 'Jv'a's'o'n'd' J ' f'ma'm' JJy A S

Text-fig. 4. Follicular activity at different stages of 2-year cycle. Above, percentage of follicles over 3 cm. in diameter;
below, size of largest follicle (mean ± 2 S.E., and range; near-term values from humpback whale).

of pregnancy. If allowance is made for this there is an even greater decline in follicle size during the
second half of pregnancy in individual females, which gives a closer agreement with the findings for
late-pregnancy humpback whales.

Lactating females

Owing to the regulations prohibiting the taking of lactating whales and the small numbers entering
antarctic waters, follicle records from only 56 lactating fin whales are available. The majority of these
females would be in late lactation (see p. 446). They show a mean maximum follicle diameter of
1 -93 ±0-34 cm. and a range from 0-5 to 5-0 cm. Chittleborough (1954) gives the range of maximum
follicle diameter for 60 humpback whales in late lactation as 1-0-5-0 cm., which is in very close
agreement, especially since some of the fin-whale records may be from females in mid- or early
lactation. (It is not possible to estimate the stage of lactation of individuals.) For three humpback
whales in mid-lactation the largest follicles are i-i, 1-5 and i-8 cm. and for three in early lactation the
maximum follicle sizes were o-6, o-8 and 2-6 cm. respectively. These were probably in very early

35o DISCOVERY REPORTS

lactation because the corpus luteum was still large (97 mm.) and in gross appearance similar to the
corpus luteum of pregnancy. Of the humpback females in late lactation 18% had maturing follicles
(diameters 35-50 mm.) or had recently ovulated. Of the lactating fin whales 19-6% had maximum
follicle diameters of 35-50 mm. and five had recently ovulated (see Table 19, p. 430). Such close
agreement might be taken to suggest that the larger follicles in late-lactating female fin whales may be
approaching ovulation, but it is also possible that some follicles are regressing after a former period
of activity, as appears to be the case in the second half of pregnancy. Gross and histological examina-
tion suggests that the majority of graafian follicles in fin whales taken in the Antarctic are in atresia,
but that some are apparently healthy.

An examination of follicle sizes in earlier and later phases of the sexual cycle throws some light
on this point. We have seen that in the second half of pregnancy follicle size was declining (expressed
as absolute maximum size, mean maximum size and percentage above 3 cm.), and from late pregnancy
to late lactation there is an increase in follicle size. The six records from early and mid-lactation
humpback whales are not sufficient to permit any firm conclusions, but in view of the probable
follicle size in late pregnancy the 2-6 cm. follicle in early lactation is suggestive of post-partum
follicular activity. In the fin whale, considering follicle size alone, either there is a period of follicular
activity at some time between parturition and late lactation, or the follicles in late lactation are maturing,
or both possibilities obtain.

As regards the first alternative 15 lactating fin whale females were simultaneously pregnant (p. 430).
The mean foetal length is 1-69 m., which corresponds to a foetal age of about 7 months and means that
the current pregnancy began very soon after the termination of the previous pregnancy. It appears
likely that nearly all lactating females have a post-partum ovulation but that, owing to the physio-
logical demands of lactation, the majority fail to conceive an embryo. Evidence confirming this view
is presented in a later section of this paper (p. 430).

The second alternative is discussed in the following section. The evidence of five late-lactation females
which had recently ovulated is highly suggestive.

' Resting ' females
' Resting ' females are here defined as mature females which are not pregnant, not lactating and not
recently ovulated (that is, with corpus luteum), but some of them appear to be approaching ovulation,
or to have ovulated fairly recently. The mean maximum follicle diameter of this group is 1 -93 ± 0-29 cm.,
which is virtually identical with the figure for lactating females. The mean maximum follicle diameter
for 'resting' humpback whales is 2-0 cm. (Chittleborough, 1954) although by definition this is not
a directly comparable group.

Four considerations suggest that this class of fin whales undoubtedly includes some females in
pro-oestrus or recent post-oestrus. First, the 'resting' condition is usually the state preceding
pregnancy (except for post-partum conceptions). Secondly, it embraces the ' recently ovulated ' class,
because ovulation succeeds dioestrus (or anoestrus) and pro-oestrus, and is in turn succeeded by
pregnancy, dioestrus or anoestrus. Thirdly, if we accept as the criterion of current or recent follicular
activity the possession of follicles over 3 cm. in diameter, then 16% are or have recently been active.
Fourthly, the largest follicle in this group was 8 cm. in diameter, as compared with 5 cm. in late
lactation.

Evidence will be presented later in this paper (p. 436) showing that there is in fact an ovulatory
period at the transition from lactation to 'resting' anoestrus. This explains the range of follicle
diameters which is found and also the existence of a class of ' recently ovulated ' females in antarctic
waters during the summer months.

GRAAFIAN FOLLICLES 35i

Ovarian cysts
Cystic follicles are of common occurrence in the ovaries of fin whales taken in the Antarctic and may
be up to 9 cm. in diameter.

Other cyst-like structures also occur, very infrequently, and may be termed ' ovarian cysts ' ; they
are aberrant cystic follicles and it is difficult to find an exclusive definition for them. Usually, they
may be distinguished from true cystic follicles because their walls are either unusually thin or un-
usually thick, and the contents may be either fluid, gelatinous, or paste-like. Out of over 2000 ovaries,
ovarian cysts occurred in three immature females, 11 pregnant, eight 'resting' and one lactating

female.

The largest, from an immature female, was fluid-filled, 35-5 cm. in mean diameter, and weighed
4-3 kg. It was thick-walled and abundantly supplied with blood vessels. Another, from a 'resting'
female was 16 cm. in diameter and weighed 0-9 kg. Other large cysts were from a lactating female
(20 cm.) and three pregnant females (14, 20 and 21 cm.). The smallest, from a pregnant female, was
2 cm., fluid-filled, with a fibrous wall 8 mm. thick. Four cysts from 7 to 20 cm. in diameter had
either fluid or gelatinous contents and a peripheral layer of luteal tissue 7-10 mm. thick. Two of these
were from ' resting ' females and two from pregnant females. The abnormal fin-whale ovaries con-
taining 10 bodies superficially like corpora lutea, but composed of white fatty tissues and measuring
from 8 to 30 cm. in diameter, have already been mentioned (p. 343). On one of these ovaries there
was a 12-cm. fluid-filled cyst. One 5-4-011. cyst from a 'resting' female was similar in external
appearance to a corpus luteum, but contained a thick brown paste. Follicles with a cellular internal
structure, like an agglomeration of bubbles, are occasionally seen.

Conclusions
There are insufficient data from the examination of the follicles of fin whale females taken in the
Antarctic to establish the variation of follicular activity during the lactation and ' resting ' phases of
the annual cycle, but what little there is suggests that there is a period of follicular development in
early lactation and another immediately after lactation. In the humpback whale, in which lactation is
prolonged over io| months, this post-lactation ovulation usually coincides with the male sexual
season and initiates the next pregnancy.

An observation by Chittleborough (1958) is of especial interest in connexion with a possible post-
partum ovulation period. In one pregnant humpback female in late pregnancy (foetus 3-92 m.) the
follicles had developed considerably and one follicle, 48 mm. in diameter, was maturing. The corpus
luteum of pregnancy was in the early stages of resorption, similar in size and structure to the condition
normally found during early lactation. This condition is rare ; in over 70 other females during advanced
pregnancy there was no such marked resorption of the corpus luteum and no follicular development.
This exception strongly suggests that when the suppressing effect of the corpus luteum and placenta
is removed after parturition, there may be a post-partum follicular cycle. Marshall and Moir
(1952) review work in this field and show that the oestrogen content of blood and urine in the
human female increases during the second part of pregnancy to a maximum just before parturition.
The concentration rapidly falls at parturition so that after 3-4 days it has reached the level for non-
pregnant females. This oestrogen is mainly secreted by the placenta. It is well known that oestrogen
suppresses follicular growth.

The data from pregnant females lends itself more readily to treatment because it is possible to
subdivide the sample and compare the variation in follicle sizes over a period of 1 1 months. It is then
apparent that there is a single cycle of follicular development during pregnancy. It is now generally

352 DISCOVERY REPORTS

accepted that in mammals follicular activity is limited but not necessarily suspended during pregnancy,
because the secretion of progesterone by the corpus luteum prevents pre-ovulationary differentiation
and causes cystic atresia (Gillman, 1941 ; Van der Horst and Gillman, 1945, 1946).

It is well known that in the rat there are oestrous cycles during pregnancy (Long and Evans, 1922;
Nelson, 1929; Swezy and Evans, 1930; Swezy, 1933). The follicular development proceeds only up to
a certain point, when cystic atresia begins, and corpus luteum cysts sometimes form, the granulosa
degenerating and the theca interna luteinizing. Similar luteinized cysts are occasionally found in
whale ovaries (p. 351). In the guinea-pig (Bujard, 1953) the percentages of growing follicles at different
stages of pregnancy are indicative of four oestrous cycles. In Elephantulus (Van der Horst and Gill-
man, 1945) there are three phases of follicular growth during pregnancy; in early pregnancy small
cystic follicles form, which are replaced by large cystic follicles and they in turn by small cystic
follicles. In some pinnipeds Harrison, Matthews and Roberts (1952) found two periods of follicular
stimulation after implantation of the blastocyst. In the elephant seal, Mirounga leonina, Laws (1956 c)
found one period of follicular growth during the free blastocyst stage and another follicle cycle just
after implantation.

Williams, Carrigus, Norton and Nalbandov (1956) observed mating by ewes in early and late
pregnancy. Heats during pregnancy were not accompanied by ovulation in the animals which were
killed to check on this point. They found a significant increase in follicle number and follicle size
from early pregnancy up to the 25th day of pregnancy ; during the remainder of pregnancy the follicle
number remained constant, but follicle size decreased significantly.

The follicular activity in the fin whale during pregnancy is at a maximum at mid-pregnancy which
is, for the average female, in November/December. Elsewhere (p. 450) it is shown that the fin whale
is probably seasonally monoestrous with peak ovulatory periods in June-July and November-
December. It seems probable that the follicular cycle during mid-pregnancy in the female fin whale
represents a suppressed oestrous cycle as for example in the rat, guinea-pig and sheep.

In some mammals ovulation is of regular occurrence during pregnancy. In the mare, for instance,
the corpus luteum of pregnancy regresses after about 30 days and is replaced by a set of accessory
corpora lutea by the luteinization of all follicles with antra, the larger of which ovulate (Asdell, 1946;
Amoroso, Hancock and Rowlands, 1948). Similarly in the elephant, Loxodonta africana, further
corpora lutea are formed during pregnancy (Perry, 1953); in the rodent, Lagidium peruanum (Pearson,
1949) and in the porcupine, Erithizon (Mossman and Judas, 1949) accessory corpora lutea form during
pregnancy. Hansson (1947) showed that in mink (Mustela vison) oestrus, mating and ovula-
tion can occur during the free blastocyst period, and recently Harrison and Neal (1956) and Neal and
Harrison (1958) have shown that the badger (M. meles) may have up to 9 months delay in implantation
during which as many as three ovulations may take place.

Although the fin whale has a follicular cycle during pregnancy there is no evidence that ovulation
ever occurs during pregnancy. There are a number of primiparous females in the present material
which have only ovulated once and many of these are in late pregnancy, in lactation, or post-lactation.
In these animals it is certain that no ovulations can have occurred during pregnancy.

THE CORPUS LUTEUM

Corpora lutea are normally formed from all ruptured follicles, but usually they soon degenerate if
fertilization of the ovum and implantation do not occur, and are then referred to as corpora lutea of
the cycle or corpora lutea of ovulation. The life-span of the corpus luteum of ovulation in different
species is remarkably uniform and independent of body size. ' The range of variability encountered is
about 10-20 days (the upper limit being represented by the cow), but in the great majority of animals

THE CORPUS LUTEUM 353

it is probably of the order of only 10-15 days ' (Eckstein, 1949, p. 400). In some mammals the corpora
lutea of ovulation are short-lived and probably non-functional, but they can be activated by a copula-
tion which does not result in pregnancy, or by mechanical stimulation of the cervix. They may then
persist longer and are called corpora lutea of pseudopregnancy. With the exception of some carnivores
and marsupials pseudopregnancy appears to be largely confined to the rodents.

There is no evidence of pseudopregnancy in any of the cetaceans which have been studied and it is
unlikely that this condition occurs in whales, as it could hardly have passed undetected. It is here
assumed that the corpus luteum of ovulation in the whale conforms to the generalization made by
Eckstein (1949) and that it persists in a recognizable form for less than a month, probably for about
15-20 days.

If fertilization and implantation occur the corpus luteum persists for a long period as a corpus
luteum of pregnancy. In the whale this period covers the duration of pregnancy, but in some mammals
the corpus luteum degenerates before the end of pregnancy, or may be replaced by a set of accessory
corpora lutea as in the mare and elephant (Amoroso, Hancock and Rowlands, 1948; Perry, 1953).

Accessory corpora lutea are usually defined as corpora formed as the result of luteinization of an
unruptured follicle at the same time as the normal corpus forms, whether it be a corpus luteum of
ovulation, or of conception. In the mare during pregnancy a set of corpora are formed by the luteiniza-
tion of all or nearly all the follicles with antra; the larger follicles ovulate, the smaller luteinize
(Amoroso, Hancock and Rowlands, 1948). In the elephant the accessory corpora also form from
either ovulated or unovulated follicles (Perry, 1953). Accessory corpora lutea in the Norway rat form
by luteinization of unruptured follicles (Hall, 1952). In histology and function they appear to be
identical, whatever the mode of formation. Brambell (1956) uses the term accessory corpora lutea
as synonymous with corpora lutea atretica, for certain animals, but there is an important difference
which he points out earlier. The corpora lutea atretica form from medium and large unruptured
follicles by ' hypertrophy and hyperplasia of the cells of the theca interna after the degeneration of
the membrana granulosa'. The luteal tissue in true corpora lutea is derived from the membrana
granulosa.

In the present account the term ' accessory corpus luteum ' is used to describe corpora formed at the
same time as a corpus luteum of pregnancy or a corpus luteum of ovulation, whether derived from
ovulated follicles or from unruptured follicles. In the case of a multiple ovulation when there are
only one or two foetuses and more than one or two of the corpora have rupture points, the largest
are assumed to be corpora lutea of conception and the others are classed as accessory corpora lutea
of pregnancy. Similarly when there is a multiple ovulation without conception, the largest ruptured
follicle is assumed to be the corpus luteum of ovulation and the others, whether ovulated or not, are
termed accessory corpora lutea of ovulation. In the fin whale there is no evidence for the formation of
accessory corpora lutea during pregnancy, as in the mare, elephant, viscacha, and porcupine (Amoroso,
Hancock and Rowlands, 1948; Perry, 1953; Pearson, 1949; Mossman and Judas, 1949), and this is
not a regular feature of pregnancy in the whale. In any case accessory corpora lutea only comprise
3-4% of all corpora lutea.

Formation of the corpus luteum

The humpback whale is the only species of baleen whale which has been extensively studied in the
breeding season and it is convenient to complete the fin-whale picture by reference to the findings of
Chittleborough (1954). First, it is necessary to show that the size of the fully formed corpus luteum
is similar in the two species ; it has already been established that the sizes of follicles at different stages
of the sexual cycle are similar.

4-2

354 DISCOVERY REPORTS

Chittleborough gives a mean diameter for the corpus luteum of 29 females in late pregnancy, when
the corpus is at its maximum size, of 12-3 cm. If nine records of early and mid-pregnancy humpback
females (Matthews, 1937) are combined with his data the mean diameter is n-89± 1-58 cm. which is
virtually the same as the size of the fin-whale corpus luteum, mainly from early and mid-pregnancy
(1 i-44±o-54 cm.). We may, therefore, assume that the details of ovulation in the fin whale, for which
we have no direct evidence, are very similar to the condition in the humpback whale.

Text-fig. 5. Morphological variation in corpora lutea. See text for explanation.

In the humpback material there were 35 females which were found to have just ovulated, the blood-
stained hole (from 4 to 13 mm. in diameter) being immediately obvious on the surface of the ovary.
Immediately after ovulation the follicle was collapsed and the wall wrinkled. The size range at this
stage was 2-2-6-0 cm. (median 3-7 cm.) and the smallest recently formed corpora lutea are about 4 cm.
in diameter (Chittleborough, 1954, fig. 4), suggesting that the size of the original mature follicle at
ovulation was of the order of 6-8 cm. (see Harrison, 1948, p. 247). This is in agreement with the
maximum size of unruptured mature follicles given by Chittleborough ; of five above 6 cm. the mean
diameter was 7-1 cm., but four of these lay between 6 and 7 cm. and one was 10-5 cm. in diameter.

In 25 recently ovulated fin whales the largest follicle (which was presumably the second largest at
ovulation) had a mean diameter of 3 -8 ±0-53 cm. and the absolute maximum size was 9 cm. Chittle-
borough (1954, p. 58) gave one example of a female humpback whale approaching ovulation; the two

THE CORPUS LUTEUM 355

largest follicles measured 5-3 and 3-7 cm. The fin-whale follicle size at ovulation is probably appreci-
ably greater than 6 cm.

These observations suggest that in the fin whale the follicle ruptures when it enlarges to about
7 cm., possibly at a greater size than this, so that the mature corpus luteum of pregnancy is about one
and a half times the size of the follicle at ovulation. Immediately after ovulation the ruptured follicle
loses fluid and shrinks to about 4 cm. As the folding of the follicle wall becomes more obvious luteal
tissue forms from the granulosa (Text-fig. 5 a) and the centre of the ruptured follicle is often filled
with a translucent gel, the tertiary liquor folliculi. This central part soon fills with luteal tissue though
a central cavity may remain. At the same time the newly formed corpus increases in size.

Harrison (1949, pp. 245-7) has described the histological appearance of a corpus luteum at this
stage of development in the pilot whale, Globicephala melaena, and concludes that the general appear-
ance is of an open ' lace-like ' arrangement of luteinizing granulosa cells. Considerable trabeculation is
present (see Text-fig. 56); projections of theca externa containing thecal vessels form the central core
of the trabeculae, and large groups of theca interna cells are present at the bases of the trabeculae and
at the periphery of the developing gland. The slit-like central cavity is lined by fibroblasts.

In fin and humpback whales a fresh, unfixed, recently formed corpus luteum can usually be dis-
tinguished macroscopically from later stages. The outer membrane is very thin, with numerous blood
vessels visible immediately beneath it, and the luteal tissue is soft, pale in colour and expanded in
contrast with the firmer, more yellow tissue in later stages and especially during pregnancy. The initial
size of the corpus luteum is dependent on the size of the follicle at ovulation. In the recently ovulated
class it averages 8-28 ±0-82 cm. (range 1 "5— 13*5 cm.). Once formed it continues to increase in size
for some months if pregnancy supervenes. The distribution of lipoids at different stages of pregnancy
is illustrated in plate IV.

Bilateral activity of the ovaries

Slijper (1949) gives records of 17 fin whales for which it was known whether the corpus luteum of
pregnancy came from the left or right ovary, and there are 37 similar observations made at South
Georgia by the ' Discovery ' Investigations. In this sample of 54 fin whales the corpus luteum was in
the right ovary in 32 cases (59-2%). Similarly for blue whales, Slijper gives 22 records and there are
an additional 21 records from South Georgia. In 24 of these (55-8 %) the corpus luteum of pregnancy
was in the right ovary. Slijper's original sample indicated that in 59 % of blue whales and 65 % of fin
whales the corpus luteum was in the right ovary.

As regards the distribution of corpora albicantia, there are in all records of 671 corpora albicantia
from 69 fin whales and 41 1 corpora albicantia from 54 blue whales which are relevant. Of these
51-8 and 52-3% were in the right ovary of fin whales and blue whales respectively. Combining both
the corpora lutea and corpora albicantia, of 724 fin-whale corpora 5 2-4 ±3 "72% were in the right ovary
and of 454 blue-whale corpora 52-4 + 4-68% were in the right ovary. Even when the blue and fin
whale data are combined the distribution is not significantly in favour of the right ovary (52-4012-92),
but nevertheless it seems possible that there is a slight prevalence of the right side in both these species.

Slijper (1949) presents evidence which appears to show that in the Odontocete whales ovulation
occurs almost invariably from the left ovary, and he also gives a number of observations which suggest
that the left ovary is larger than the right. Both Slijper, and Brambell (1956) refer to the prevalence
of the right side in bats, and the left side in monotremes. Slijper suggests that the prevalence of a
particular ovary is connected with uniparity and discusses further examples. He presents one case
of transference of the ovum from the right ovary to the left uterine cornu in a fin whale.

356

DISCOVERY REPORTS

l cm

Text-fig. 6.

Vesicles found in uteri of two
pubertal females.

The corpus luteum of ovulation

There are records of the diameter of the corpus luteum of ovulation of 59 female fin whales. These
are in the recently ovulated class of females, taken in the antarctic, the majority outside the usual
conception period for the species (see p. 450). They may be characterized as females which had an
apparently normally active corpus luteum in the ovaries, but in which an intensive search of the
uterus failed to reveal a foetus. Examination of the mean size of the largest follicle in this group
(p. 347) confirms this diagnosis.

The size range of these corpora lutea of ovulation is 1 "5— 13*5 cm. and the mean diameter, 8-28±
0-82 cm., is well below the mean size of the corpora lutea of pregnancy (Text-fig. 7). This corresponds
to a mean weight of 0-375 kg. and a weight range of 3-4 g.
to 1-5 kg. (Text-fig. 8). Some of these corpora lutea of
ovulation are of very recent formation (Text-fig. 5 b) and
show the characteristic unexpanded cross-section of an
early stage of formation.

Two of them, which represented first ovulations of
females at puberty, were associated with the occurrence
of unusual cysts (Text-fig. 6) in the uterine cornu on the
same side as the corpus luteum. These cysts were at first
thought to be small embryos. They were sectioned by
Dr R. Willis (Department of Pathology, The School of
Medicine, Leeds), who reported that they do not show any
features suggestive of embryonic products or gestational
changes. The bulk of the tissue in the walls of the

vesicles is structureless and degenerate, and where surviving tissue is present it seems clear that it
must have arisen from the endometrium itself.

In its morphology the corpus luteum of ovulation is similar to the corpus luteum of pregnancy and
no constant differences have been observed (see below, p. 362).

The corpus luteum of pregnancy

Size

There are insufficient data from the early stages of pregnancy to justify a precise statement about the
duration of the initial phase of growth of the corpus luteum of pregnancy. What there is suggests
that the corpus luteum continues to grow until the foetus is about 10-20 cm. in length, at an age of
one or two months. It then remains of constant size until late pregnancy. The extensive data now
available provide no evidence that the corpus luteum decreases in size towards the end of pregnancy,
as Mackintosh and Wheeler (1929) suggested. There is actually some slight indication of an increase
in corpus luteum size in late pregnancy, because six corpora associated with foetuses averaging 5-74 m.
in length were 5 mm. larger in mean diameter than the mean size in earlier stages of pregnancy.
Because of the small size of the sample and the variability in corpus luteum size this difference is
not significant.

Chittleborough (1954, p. 46) gives a probable growth curve for the early development of the hump-
back-whale corpus luteum by linking the largest corpus luteum found in each month. This suggests
that the corpus steadily increases in size for the first two months, when it approaches the range found
in late-pregnancy corpora lutea.

The mean diameter of 523 fin-whale corpora lutea of pregnancy was 11 -44 ±0-154 cm- an^ the

THE CORPUS LUTEUM 357

range of variation 6-2-17-5 cm. The lower limit is the smaller of two corpora lutea associated with
twin foetuses and the smallest corpus luteum from a uniparous pregnancy is 7-5 cm. The frequency
distribution of corpus luteum diameter is shown in Text-fig. 7.

There are 372 records of the weight of fin-whale corpora lutea. The mean weight is o-88i ±0-04 kg.
and the range 0-2-2-4 ^g- The frequency distribution is shown in Text-fig. 7. Chittleborough (1954)
suggests that there is a relation between the weight of the corpus luteum and the age of the female

10 is

WEIGHT IN KILOGRAMS

523 C.L PREGNANCY

59 CL OVULATION

26 CL ACCESSORY

IO
DIAMETER

15
IN CMS.

Text-fig. 7. Frequency distributions of weights and diameters of corpora lutea.
The means ± 2 S.E. are shown.

using the total number of corpora in the ovaries as an index of relative age. He found an increase
in corpus luteum size with increasing age. In fin whales no such increase in size could be demonstrated.
In Text-fig. 8 average corpora lutea weights at different diameters have been plotted on a double
logarithmic scale for 372 fin whales. Five blue-whale records and three sperm-whale records have
been added at the upper and lower limits of the size range. This gives a linear relationship, as is to be
expected, and suggests a probable maximum weight for the extreme fin-whale corpus luteum diameter
(17-5 cm.) of 3-2 kg. Thus the extreme weight range in this larger sample is from 0-14 to 3-2 kg., a
sixteen-fold increase from smallest to largest, as compared with a less than three-fold increase in
diameter (6-2-17-5 cm-)-

FIN CL.
FIN CA
BLUE CL.
SPEFIM CL.

12 IOO

358 DISCOVERY REPORTS

In further discussions of the size of the corpora lutea and corpora albicantia the mean diameter will
be used as a measure of size instead of weight both because of its smaller variability and because there
are many more records of diameter than of weight. This applies especially to the corpora albicantia
which, being usually embedded in the ovary, are difficult to weigh accurately.

Morphology

The various morphological types of corpora lutea are illustrated in Text-fig. 5 and PI. IV, fig. 1 . The corpus

almost invariably protrudes from the surface of the ovary and is sometimes connected only by a narrow

neck of tissue (as in Text-fig. 5 k, I). This is probably related to the relatively rigid fibrous structure of the

stroma, for in the smaller sperm-whale and pilot-whale

ovaries, which are less fibrous, the corpora lutea do not

usually protrude so much. The overall shape of the

corpus is spheroidal and some are flattened, with an oval

cross-section. The point of rupture of the original

follicle is usually visible as a small stigma, surrounded

by a corona of everted pinkish-yellow tissue, which is

usually about 2-4 cm. in diameter. In sections the

luteal tissue is seen to be tortuously folded and tightly

packed, as if Text-fig. 5 b had been tightly compressed.

This meandrine appearance is due to the initial folding

of the follicle wall and the growth of fibrous trabeculae,

which carry the blood vessels supplying the gland. The

central cavity is compressed at an early stage to a thin

slit. The fibrin in this slit is replaced by connective tissue

so that septa ramify throughout the gland in a pattern

complementary to the trabeculae formed by ingrowth

of the theca externa. These internal connective tissue

septa have no blood vessels PI. IV, fig. 2.

The most commonly formed corpora lutea are types c, d and e in Text-fig. 5. Together they con-
stitute 70% of a sample of 88 fin-whale corpora in which the morphology was noted. Types d and e
are the most common, comprising 48% and type c, in which there is a stigma but no corona, com-
prises 22%. The next most abundant type are corpora lutea in which the central cavity has not been
completely obliterated after ovulation (types h-k). In this small sample 17% were of this type. In
a larger sample of 107 vesicular corpora lutea the cavity varies in size from 3 mm. to 13-3 cm. in
diameter. The larger corpora lutea have the larger vesicles, the mean cavity diameter increasing from
i-8 cm. at a corpus diameter of 7-8 cm. to 4-1 cm. at a corpus diameter of 14-15 cm. (Text-fig. 9).
The cavity is filled with gel, fluid, or fibrin strands and bounded by a thick layer of avascular hyaline
connective tissue.

Another type is the everted corpus luteum. In these corpora the corona maybe equal to (Text-fig. 5/)
or greater than (Text-fig. 5^) the mean diameter of the corpus luteum. The largest corona measured was
12-3 cm. in diameter (from a corpus luteum 13-3 cm. in diameter) and the second largest was 10-5 cm.
across. The first, partially everted, type accounts for 8 % of this sample and the fully everted type for
3 %. The least common type is very similar to the cavitate bodies, but the stigma is widely open, there
is no gel or fluid and the hyaline inner wall is usually very thick (Text-fig. 5/). Only 2% (two cases)
of the corpora in this sample were of this type, and the true percentage in a larger sample would be
very small because if observed in the course of routine slicing this shape has invariably been noted.

3 4 S 6 7 0 9 IO

DIAMETER IN CMS.

Text-fig. 8. Relation of weight to diameter for whale
corpora lutea and corpora albicantia (fin whale mean
values; other species, single records).

THE CORPUS LUTEUM 359

Vesicular corpora lutea

In Text-fig. 5, these morphological types have been arranged in the order of their development. They
fall into two main groups ; the non-vesicular types (c-g) which are obviously related, and the corpora
with cavities (types h-l). In a large sample of 701 corpora lutea which were grouped according to the
presence or absence of a cavity 17-1% had a cavity. Often the vesicular type lack a corona and the
stigma is inconspicuous. In the single specimen of type k, the thinner part of the wall gave the impres-
sion that it had been under pressure from the liquor folliculi. The connective tissue septa are radially
arranged in a regular pattern. This radial arrangement of trabeculae and internal septa is observed in
all the corpora with large vesicles, but not in type /.

The mode of formation of the cavity calls for some comment since Dempsey and Wislocki (1941)
and Robins (1954) have suggested that cavity formation in the humpback whale is related to the large
size of the corpus luteum. Robins suggested that the absence of a cavity is diagnostic of a corpus
luteum of ovulation and this, if true, would be of great value in studies on the reproductive cycle and
of age-determination.

Dempsey and Wislocki base their conclusions on the examination of 16 pairs of ovaries, not all of
which were from pregnant females. The corpora lutea they examined were 3-6 cm. in diameter so,
even allowing for excessive shrinkage as a result of fixation (which is not borne out by the histological
appearance), they are well below the normal size range for corpora lutea of pregnancy in both fin and
humpback whales. In fact it appears likely that they were corpora lutea of ovulation. These authors
' conclude that the large size of the whale's corpus luteum imposes certain anatomical peculiarities
and physiological limitations on its vascular supply. The luteal arterioles and capillaries are apparently
unusually long. The functional restrictions in consequence of the lengthening of these vessels make
it impossible for the luteal tissue ever to fill the entire cavity of the luteal body. These limitations
result also in nearly complete avascularity of the centre of the corpus luteum, associated with excessive
fibrosis and hyalinization ' (p. 250).

Robins (1954) found that in all the functional corpora lutea (37 in number) which he examined
from both early and late pregnancy there was a central cavity, 'variable in size but always quite
noticeable'. He also found that a variable proportion of corpora lutea [corpora albicantia?] did not
possess this characteristic cavity or core. Robins suggested that, owing to the small size of the corpus
luteum of ovulation (up to 88 mm.) there appears to be no anatomical limitation on the blood supply
and luteal cells continue to fill the cavity so that no distinctive centre remains. This is supported by
several whales which had ovulated twice without successful fertilization and showed the regressing
corpora lutea to lack the characteristic centre of the corpus luteum of pregnancy. According to
Robins, if pregnancy intervenes the gland continues to expand and, in accordance with the ideas of
Dempsey and Wislocki, anatomical limitations prevent blood vessels from supplying the centre of
the gland so that a thick avascular hyaline zone forms, limiting the thickness of the luteal tissue and
causing the central cavity to be retained.

There are several important objections to this hypothesis. It has been pointed out that the corpora
examined by Dempsey and Wislocki were only 3-6 cm. in diameter, but nevertheless contained central
cavities. The corpus luteum of ovulation is of this order of size. Personal examination of humpback-
whale ovaries from the Antarctic (unpublished) shows that the non-vesicular corpora lutea of pregnancy
are more common than the type with cavities. Chittleborough (1954) illustrates a 12-cm. functional
corpus luteum of late pregnancy which clearly has no central cavity.

It has been established that in the fin whale only 17-1 % of the corpora lutea have a cavity. Corpora
lutea are found up to 16 cm. in diameter which are without cavities and a blue-whale corpus luteum

360 DISCOVERY REPORTS

of pregnancy which was 19 cm. in diameter lacked a cavity. Conversely, cavities are found in the
much smaller corpora lutea of other animals; in man, for instance, corpora lutea of pregnancy or
ovulation less than 1 cm. in diameter commonly have cavities (Dubreuil and Riviere, 1947) and vesi-
cular corpora lutea are relatively common in the cow (Hammond, 1927). These observations mean
that the hypothesis of vascular limitation is untenable.

Secretion of fluid by the follicle wall continues for an appreciable time after ovulation and vesicular
corpora lutea in other mammals are usually attributed to the continued secretion of liquor folliculi by
the ruptured follicle after the aperture has become closed (Brambell, 1956, p. 474). According to
Robinson (1918) the persistence of the central cavity in the ferret depends on the degree of separation
of the internal limiting membrane at ovulation. The point of rupture of the follicle is closed by a
tenacious coagulum, the tertiary liquor folliculi, which also redistends the collapsed follicle often to
the size it originally was before ovulation (Harrison, 1948).

/^^__

1 1 1 1 1 1 1 1

9 10 11 u 13

CL. DIAMETER IN CMS.

9 10 II \2

CL DIAMETER IN CMS

Text-fig. 9. a, Relation between cavity diameter and corpus luteum diameter, b, Relation between corpus

luteum size and the incidence of cavities.

The appearance of fin-whale corpora lutea of the vesicular type suggests that they are usually formed
in this way. In most corpora with large cavities (Text-fig. 5 h-k) the stigma is inconspicuous and there
is no eversion of luteal tissue to form a corona. This suggests that the aperture became closed again
after ovulation and remained closed. The corpus illustrated in Text-fig. $k has a small stigma, but
the corpus has a distended appearance and the luteal tissue has obviously been subjected to pressure
from inside, presumably by continued secretion of fluid. The most uncommon type of corpus (Text-
fig. 5 /) has an opening and a conspicuous corona. It immediately suggests that the aperture closed
after ovulation, but that the internal fluid pressure later forced it open when the corpus luteum had
almost attained its definitive size and form.

There is a relation between the size of the corpus and the size of its cavity (Text-fig. ga). For
107 fin-whale corpora for which the cavity size is known the mean size of the cavity increases from
i-8 cm. at a corpus size of 7-8 cm., to 4-1 cm. at a corpus size of 14-15 cm.

There is also a relationship between the size of the corpus luteum and the prevalence of the vesicular
type. For 701 corpora lutea, 120 of which have cavities, the percentage of vesicular corpora in suc-
cessive size groups increases from about 10% at a corpus size of 6-7 cm. to about 20% in corpora
above 13 cm. in diameter (Text-fig. gb). In other words the larger corpora show a greater tendency
to have cavities. Extrapolation suggests that corpora below 3-4 cm., forming from ruptured follicles,
would not be vesicular. The limited material available supports this. In Text-fig. 10 a number of small
accessory corpora lutea are illustrated and all which have central cavities are formed from unruptured
follicles. These accessory corpora lutea are produced in such limited numbers that they do not affect
the figure for the percentage of corpora with cavities. Corpora lutea of ovulation with a mean diameter

THE CORPUS LUTEUM 361

of 8-28 ±0-82 cm. might be expected to include a slightly lower proportion with cavities than pregnancy-
corpora. Of fifteen corpora lutea of ovulation examined in 1953/54 and 1955/56, only one (67%)
possessed a central cavity, but this is too small a sample to give a significant result.

Accessory corpora lutea
Of 760 corpora lutea examined, 28 or 37% were accessory corpora ranging from 0-4 to 8-5 cm. in
diameter, the mean diameter being 3-88±o-8 cm. and the weight about 45 g. It is likely that many
more small accessory corpora lutea form, but corpora less than 7 mm. in diameter are usually missed
in the routine examinations; one accessory corpus 1 mm. in diameter has, however, been seen in
histological preparations. The material is rather too sparse to allow firm conclusions to be drawn, but
accessory corpora lutea of ovulation appear to occur as frequently as accessory corpora lutea of
pregnancy.

Text-fig. 10. Morphological variation in accessory corpora lutea. See text.

They fall into two main groups; the larger, having developed from ruptured follicles, show a
stigma and small corona, but the smaller are formed from unruptured follicles.

A female fin whale 73 ft. in length taken on 8 February 1954 had recently ovulated, but no products
of conception were seen in the uterus. There were three small corpora lutea in one ovary, one of which,
23-5 mm. in diameter, had ovulated, and two measuring 13 and 15 mm. (Text-fig. log, h) had developed
from unruptured follicles. The appearance of the luteal cells is similar in all three. They are derived
from the membrana granulosa because theca interna cells can be seen at the periphery of the gland

5-2

362 DISCOVERY REPORTS

and at the base of the trabeculae. Only part of the follicle wall has contributed to the luteal tissue and
for the most part the follicle has undergone avascular hyaline degeneration to form a hard knob of
collagenous tissue.

Other accessory corpora illustrated in Text-fig. 10, have formed in this way either from the whole
{c, i) or part (d, g, h,j, k, I) of the mural epithelium. Quite large accessory corpora can form without
ovulation; one measuring 37 mm. in diameter is illustrated in Text-fig. ioa4.This was the smallest of
four active corpora in the ovaries of a 76-ft. female taken on 27 February 1954, which was pregnant
with a 4-2 m. male foetus. There were 11 corpora albicantia. The three largest corpora lutea have
formed from ovulated follicles and one is conspicuously everted, with a corona measuring 7-5 x 8-o cm.
Another accessory corpus luteum (Text-fig. 10b) which measures 4-5 cm. has a stigma on the surface
of the ovary and one lobe of luteal tissue is undergoing hyaline regression. Text-fig. 10/ is an example
of an accessory corpus luteum, 1 -9 cm. in diameter, formed from an unruptured follicle, in which
the central cavity has been obliterated by an ingrowth of luteal tissue.

These small accessory corpora formed from unruptured follicles are similar to the ' corpora lutea
atretica' of Brambell (1956, p. 501), but the membrana granulosa appears not to degenerate and theca
interna cells are distinguishable at the periphery.

Conclusions

In fin whales there is perhaps a slight tendency for the right ovary to ovulate more frequently than
the left ovary. It appears that the size of the mature graafian follicle of fin whales at ovulation is about
7 cm. but there is clearly a great individual variation in size at this stage.

The corpus luteum of ovulation averages 8-28 cm. in diameter, weighs about 375 g. and probably
persists for 15-20 days. There is no evidence that pseudopregnancy ever occurs. If pregnancy super-
venes, the newly formed corpus luteum continues to grow for about 2 months, when it reaches an
average size of 11-44 cm- and weighs about 881 g. There is no evidence of a decrease in size in late
pregnancy. No correlation between the size of the corpus luteum and the age of the female has been
found. Accessory corpora lutea of ovulation or pregnancy are uncommon, those above about 7 mm.
in diameter amounting to only 3-7% of all corpora lutea. They form either from ovulated follicles or
by luteinization of smaller unruptured follicles, and have a mean diameter of 3-88 cm. and an average
weight of about 45 g. Additional corpora lutea are not formed during pregnancy.

No constant morphological or histological differences have been found between corpora lutea of
ovulation and corpora lutea of pregnancy. The incidence of vesicular corpora has been studied and gives
no support to Robins's (1954) suggestion that the presence or absence of a cavity is diagnostic of a corpus
luteum of pregnancy or a corpus luteum of ovulation respectively. In fact only 17-1 % of corpora lutea
of pregnancy have a fluid- or gel-filled cavity. Nor does the material support the contention of Dempsey
and Wislocki (1941) that the factor responsible for the formation of a cavity is a restricted blood supply
to the centre of the large corpus luteum of the whale. A corpus luteum 1 9 cm. in diameter possessed no
central cavity. There is, however, some evidence that the larger corpora lutea show more of a tendency
to be vesicular than the smaller corpora, but the difference is only 10% over the size range 6-13 cm.
It appears that at corpus sizes below about 3-4 cm. a cavity is present only in some of those accessory
corpora which have developed from unruptured follicles.

The presence or absence of a cavity or, in corpora albicantia, of a central core of connective tissue,
cannot, therefore, be used to distinguish the corpora formed as a result of ovulation only, from those
representing pregnancy (see also p. 365).

Van Lennep (1950) suggests that at the same stage of regression corpora lutea of ovulation can be
expected to be smaller than corpora lutea of pregnancy and this might afford a means of distinguishing

THE CORPUS LUTEUM 363

between corpora albicantia of ovulation and pregnancy. The total size range of corpora lutea of
ovulation and pregnancy is 16-0 cm. and the overlap is 7-3 cm., so size alone cannot be diagnostic.
It is suggested below that size correlated with a quantitative measurement of histological regression
could perhaps be used to distinguish these two types of corpora in individual females.

Van Lennep also suggests that two types of corpora albicantia can be distinguished, those with
straight connective tissue trabeculae and those with branched trabeculae. He suggested that ' Most,
if not all, corpora albicantia of the first type are probably derived from corpora lutea of ovulation as
only young corpora lutea of pregnancy have been found to possess the same structure and may there-
fore be supposed to become corpora albicantia of the second (branched) type' (p. 597). It is shown
later that these types of corpora albicantia correspond to vesicular and non-vesicular corpora lutea
respectively. In fact van Lennep's distinction is the reverse of that suggested by Robins. Finally,
mention must be made of the comprehensive paper of Dubreuil and Riviere (1947), who conclude
that there is still no certain means of distinguishing the human corpora lutea of pregnancy and ovula-
tion. Much attention has been given to this subject because of the legal implications. The work of
Peters bearing on this problem will be discussed in the next section (p. 384).

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND

CORPORA ATRETICA

The corpus albicans
The corpus luteum of ovulation after 2-3 weeks and the corpus luteum of pregnancy after about
1 1 months undergo degenerative changes and rapidly shrink in size. The luteal cells disappear, the
colour of the former lobes of luteal tissue changes to a tawny brown and the white connective tissue
septa become increasingly more conspicuous (PI. V, fig. 1).

There is some confusion about the nomenclature of the body so formed. The regressed corpus
luteum of the whale is not properly a corpus albicans, a term which is correctly applied to the
unpigmented old corpora of certain other animals. Usually some pigment remains even in the very
old corpus of the fin whale and the more recent regressing bodies are well pigmented like the corpus
rubrum of the cow, although they are a yellow-brown in colour. The term corpus fibrosum might be
applied to the old corpus which has lost most of its pigment.

Mackintosh and Wheeler (1929) refer to the active corpora lutea and the regressed corpora lutea
as corpora lutea a and b respectively. The latter is technically a more correct terminology than corpus
albicans, but it leads to confusion. The term corpus albicans is now generally used to describe old
corpora lutea whether pigmented or not, and to avoid introducing yet another terminology it is
proposed to refer to all old corpora lutea as corpora albicantia.

The corpus albicans material is much more extensive than that available for study of the corpus
luteum, because one pair of ovaries may contain over fifty corpora albicantia, but usually only one corpus
luteum. In 1953/54 a detailed study of 1381 fresh unfixed corpora albicantia was undertaken by the
author in F/F ' Balaena ', and various morphological types were distinguished. These ovaries were
sliced by hand. Unfortunately no large collection of fin-whale ovaries was undertaken in 1954/55,
and it was not until after the 1955/56 season that a collection of ovaries became available for routine
examination. Using a slicing machine cutting at 5 mm., all the corpora above about 7 mm. were
examined and some of those smaller than this. In all 4065 corpora albicantia were systematically
examined, classified and measured. It is necessary to make clear one important point about the
measurements. In calculating the mean diameter of the corpus luteum, measurements were made
on three axes. Since most corpora albicantia are embedded in the ovary and do not project like the

364 DISCOVERY REPORTS

corpus luteum, routine measurements of only two diameters have been practicable during slicing. It
is assumed that since the corpora appear to be randomly oriented, this does not introduce any important
degree of error into the results. The corpora were placed in three morphological classes (independent
of size) to be described below. These are termed ' young ', ' medium ' and ' old ' corpora albicantia,
and are believed to represent three definite stages in the regression of the corpus luteum. The evidence
for this view is presented below.

The mean diameter of 3181 corpora albicantia from pregnant females is 2'56±o-o3 cm., and for
884 from non-pregnant females it is 2-52±o-o7cm. From this season there are only 89 corpora
albicantia from females known to be lactating, and the mean size is 2-5 ±0-9 cm. These differences
are not significant, and this mean diameter corresponds to a weight of about 10 g. (see Text-fig. 8).
In Text-fig. 1 1 the percentage size frequency distribution of these corpora albicantia from pregnant

S 10

DIAMETER IN CMS

Text-fig. 11. Frequency distributions of corpora albicantia sizes.

-• pregnant; O O non-pregnant.

and non-pregnant females is presented. They range in size from 7 to 80 mm. corresponding to a
variation in weight from less than 0-4 g. to about 300 g. It will be noticed that a proportion of non-
pregnant females ('resting females') have a large corpus albicans about 4-75 cm. in diameter, whereas
the curve for pregnant females lacks this subsidiary peak. The modal diameter for both groups is
2-25 cm. Only 34 corpora albicantia have been weighed, mostly in the size range 4-7 cm., because it
is difficult to isolate corpora albicantia for weighing, embedded as they are in the ovarian stroma. The
results have been incorporated in Text-fig. 8 where the mean weights for corpora albicantia 2-3 cm.,
3-4 cm., 4-5 cm., etc. in diameter are plotted on a double logarithmic graph. These points fall along
the regression line for corpora lutea, so there has been no observable alteration in density cor-
responding to the change from corpus luteum to corpus albicans. Corpora albicantia sizes will be
discussed more fully when the different morphological classes have been described.

Morphological types

In Text-fig. 12 and PI. V, fig. 1 the various morphological types of corpora albicantia are illustrated and
if they are compared with the corpora lutea illustrated in Text-figs. 5 and 10 the similarity in their archi-
tecture is readily apparent. In general the white connective tissue septa of the corpus albicans are much
thicker than those in the corpus luteum and the lobes of brown hyaline collagen, representing the

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 365

transformed luteal tissue, occupy relatively less space. All stages in regression are seen, from bodies
similar to the corpus luteum, to bodies in which the connective tissue septa have enlarged at the
expense of the pigmented tissue so as to fill almost the whole volume of the corpus (PI. VI, fig. 1). One
macroscopically visible feature which enables even the most recent corpora albicantia to be distinguished
from the corpus luteum is the relatively sudden change in the appearance of the luteal tissue from
an opaque yellow, to a hyaline brownish yellow. Occasionally a corpus luteum is found in which some
lobes are hyaline, others still characteristically luteal and others intermediate in condition.

Total

No.

Percentage

2 S.E.

701

1381

2082

120
246

366

17-1
i7-8
17-6

2-88
2-015
i-66

484

897
231

158

18-2
17-4
20-4

3"4°
2-54
5-01

Text-fig. 12. Morphological variation in 'young' and 'medium' corpora albicantia.

Table 3. Incidence of vesicular or radiate corpora in different groups

With cavity

(

Tntnl Nn

All corpora lutea pregnancy

All corpora albicantia

All corpora lutea + all corpo

albicantia
' Young' + ' medium' corpora albicantia
'Old' corpora albicantia
All corpora albicantia associated with

a vesicular corpus luteum

The most distinctive bodies are the corpora albicantia with a central cavity or core of connective tissue,
and a stellate structure with septa arranged radially (Text-fig. 12k and PI. VI, fig. 3). These clearly
represent the products of regression of vesicular corpora lutea and a consideration of their frequency is
confirmatory. If the corpora lutea and corpora albicantia samples are combined there is a sample of 2082
corpora and the incidence of the vesicular type is iy58± i-66%. The percentages of this type among
' young ' and ' medium ' and ' old ' corpora albicantia (as defined below) are given in Table 3 , which shows
that the differences are not significant. It appeared likely that in ovaries where the corpus luteum was of
the vesicular type there was a higher proportion of radiate ' corpora albicantia (20-35 %) suggesting that
some females had more tendency than others to accumulate this type of corpora, but this difference
in the percentages is found to be not significant.

We may conclude that the incidence of the vesicular type of corpora does not vary significantly
among different groups of corpora albicantia and corpora lutea. This also confirms that the incidence
of cavities is not appreciably different in corpora lutea of ovulation compared with corpora lutea of
pregnancy. Since the production of corpora of ovulation presumably equ?ls or outnumbers the

366 DISCOVERY REPORTS

production of pregnancy corpora lutea in the life of the whale, if there were any important difference
such as Robins (1954) or Van Lennep (1950) suggest, this would affect the proportion of 'radiate'
corpora albicantia and it might be expected to be significantly higher (Van Lennep) or lower
(Robins) than the incidence of vesicular corpora lutea of pregnancy.

Age groups of normal corpora albicantia
Three groups of corpora albicantia have been identified in fin-whale ovaries on the basis of gross
anatomical and histological changes. Since they have an important bearing on age determination in
whales they must now be described in some detail. The corpora have been examined macroscopically,

lcm.

i — 1 — 1 — 1 — 1
5 mm.

Text-fig. 13. A, typical 'young' corpus albicans; B, typical 'medium' corpus albicans; C, 'old' corpus albicans which
still has a conspicuous pigmented layer. (Large-scale drawings are from thick sections cleared in xylol and methyl salicylate.)

when fresh or after fixation in formalin ; by examination of 5 mm. thick slices cleared in xylol and
methyl salicylate; and by histological examination of material fixed by various techniques. The
material for histological examination has been fixed in formalin, Bouin's fluid, and Zenker-formol
(Helly) and part of the latter material was post-osmicated with 2% osmium tetroxide to demonstrate
the distribution of lipoids. This material has been embedded and sectioned by the standard paraffin
wax technique and stained with Heidenhain's Iron Haematoxylin and Eosin, Delafield's Haematoxylin
and Eosin, Mallory's trichrome, Masson's trichrome, and Van Gieson.

The routine macroscopic examinations and counts are made by eye on formalin-fixed material.

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 367

' Young corpora '

This group includes those corpora which have undergone least regression; some are very recent
bodies, parts of which still appear macroscopically like the corpora lutea from which they have
developed.

The size range of 628 corpora of this type is 1-5-7-5 cm-» mean diameter 4-01 ±0-07 cm., cor-
responding to a weight of about 41 g. The great range means that size cannot be used as a distinguishing
character. Usually, but not invariably, corpora of this type project from the surface of the ovary after
the fashion of corpora lutea.

The macroscopic appearance of a typical 'young' corpus albicans is shown in Text-fig. 13 A and
PI. V, fig. 1. There is a conspicuous central core of white connective tissue, but the lobes of brown
collagenous tissue are extensive and the connective tissue septa are rather inconspicuous. It appears
that when the corpus luteum regresses the blood supply to the luteal tissue is cut off and hyaline
degeneration of this tissue then occurs. As the luteal cells are replaced the corpus luteum shrinks in
size and the network of connective tissue strands condenses and becomes more conspicuous.

In the 'young' corpus albicans, vascular reinvasion of the pigmented collagenous tissue has begun,
and a number of spiral arteries can be seen, but it has not progressed very far (Text-fig. 13 A and
PI. V, fig. 2). The white connective tissue core and septa, representing the original cavity of the
newly ruptured follicle, are avascular and remain so throughout subsequent regression.

Examination of cleared thick sections shows the yellow pigment granules to be distributed evenly
throughout the hyaline collagen. Sometimes, in very recent corpora, they are very densely arranged
so as to give the corpus a shining golden-yellow appearance. Thin sections stained for lipoids (Zenker-
formol fixed, and post-osmicated) show the distribution of pigment very clearly (PI. V, figs. 2, 3, 5, 6).

Rossman (1942) has shown that the pigments of the corpus luteum and the corpus albicans have
little in common. He states that it is generally held that the colour of the corpus luteum is due to a
carotenoid dissolved in lipin droplets (see PI. VI, figs. 3-5) so that the colour largely disappears on
treatment with fat solvents. The pigment of whale corpora albicantia does not dissolve in fat
solvents (xylol, methyl salicylate), which suggests that it is similar to the 'luteolipin' described by
Rossman in the corpora of the rhesus monkey, Macaca rhesus.

' Medium ' corpora

These represent a later stage of regression and have usually sunk into the general stroma of the
ovarian cortex so that they do not project very far. They retain a characteristic stigma and corona at
the surface. They are smaller than the more recent corpora with a mean diameter, for a sample of
1098 of 2-94±o-045 cm., corresponding to a weight of about 15 g. The size ranges from 0-7 to 5-5 cm.
and this character is not used for identification.

The macroscopic appearance of a typical ' medium ' corpus albicans is shown in Text-fig. 13 B. The
central white connective tissue core does not show further enlargement from the ' young ' condition,
but as the corpus shrinks in volume the septa become rather more conspicuous. The most charac-
teristic macroscopic change is a reduction in the amount of brown hyaline tissue. In thick cleared
sections vascularization can be seen to have progressed much further, and there are large thick-
walled vessels at the periphery of the corpus. This tangle of sclerotic blood vessels gives to the corpus
a thick white connective tissue capsule. Material stained for lipoids shows that there is a clear
unpigmented zone of collagen in the vicinity of the blood vessels (PI. V, fig. 2), and demonstrates that
phagocytic activity proceeds inwards from the vascularized outer trabeculae towards the inner avascular
connective tissue septa. As the phagocytes take up the pigment and move inwards they concentrate the

368 DISCOVERY REPORTS

pigment so that the colour of the lobes darkens with age. This progressive invasion by blood vessels
and phagocytes is shown in Text-figs. 13 A, B, and C, Text-fig. 14 and in Pis. V-VII.

In the 'medium' corpora the smaller spiral vessels are more numerous in comparison with the
' young ' corpus, and often impart a reddish hue to the pigmented layer so that bodies of this group
are usually a darker reddish brown in colour as opposed to the tawny brown, or even yellow colour of
the most recent corpora albicantia.

'Old' corpora

Evidence shortly to be presented establishes that this
group represents the final stages of regression of whale cor-
pora lutea, and within this group there is no further
reduction in size. The mean diameter of 2339 ' old ' corpora
albicantia is 2-013 ±0-025 cm-> corresponding to a weight
of about 5 g., and the size range is from 0-7 to 5-0 cm.

They are characterized by increased centripetal penetra-
tion of thick -walled blood vessels and closing of the lumen
of vessels near the periphery so that the external white
connective tissue trabeculae become even more conspicuous.
The layer of pigmented tissue is further reduced and
concentrated so that it forms a thin hyaline pigmented zone
separating the inner, avascular, connective tissue from the
outer trabeculae which are now much thicker and composed
largely of contorted non-functional thick-walled blood
vessels (PI. VII, fig. 1). Text-fig. 13 C shows the macroscopic
appearance of one of the least regressed corpora in this
group, which still has a conspicuous amount of pigmented
hyaline tissue. Text-fig. 13 C, Text-fig. 14 and Pis. V-VII
show how the pigmented tissue is replaced by blood vessels
growing centripetally.

There is no further reduction in the volume of the corpus albicans which is now composed largely
of unpigmented collagen, and further regression takes the form of progressive vascular and phagocytic
invasion and continuing reduction of the area of the pigmented zone. As this becomes thinner it
becomes increasingly more densely pigmented and the final stages of regression which have been
observed show in section an almost white, avascular, connective tissue body with a very thin darkly
pigmented zone outlining the internal septa. In places this pigmented zone may be completely
resorbed, as in PI. VI, figs. 4-7. The reduction and concentration of the pigmented area and its
replacement by sclerotic arteries is illustrated in Pis. V and VI.

The rate of thickening of the walls of the blood vessels during regression of the corpus albicans is
shown in Text-fig. 15. For each of 10 'old', 12 'young' and 'medium' corpora albicantia and one
corpus luteum measurements of the external and internal diameters of the arterioles were made with
a projection microscope. Only data from stained sections of corpora in which it was possible to
measure 10-20 independent arterioles have been used, which explains the small size of the sample.
The mean percentage thicknesses of the vessel walls for the three groups of corpora are plotted against
the mean corpus diameter in centimetres, and it appears that the rate of the regression in size of the
corpora albicantia is correlated with the rate of change in the thickness of the vessel walls. Once the
corpora enter the ' old ' group their volume does not decrease further, but it is likely that the vessels

I mm.

Text-fig. 14. Thick cleared section of a typical
'old' corpus albicans. Note avascular core and
internal septa below.

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 369

finally lose their lumen and become solid cords of connective tissue. There is some evidence
that the external diameter of the arterioles may also increase with age. The average diameter of
10 arterioles in the single corpus luteum examined is 95-3 //, for 147 arterioles from 'young' and
' medium ' albicantia it is 109 ft, and for 1 1 1 arterioles from ' old ' corpora it is 130 fi. This difference is
not, however, statistically significant.

The relative thickness of the vessel wall seems to be a better quantitative index of the age of the
corpus than the diameter of the corpus and in general there appears to be less overlap between the two
groups of corpora albicantia in respect of this character. It would be interesting, though laborious,
to determine the relative thickness of the arteriole
walls for a complete series of say thirty corpora albicantia
from one pair of ovaries so as to gain some idea of the
variation in corpus size within a single animal. Since
for corpora albicantia of similar age, those formed from
corpora lutea of ovulation will be smaller than corpora
albicantia of pregnancy, it might perhaps be possible
to identify corpora of these two origins and to place
them in a chronological series. It might also be possible
in this way to establish the relative frequency of corpora
lutea of pregnancy and ovulation. This is the only
possible means of distinguishing corpora albicantia of
pregnancy from corpora of ovulation which is suggested
by the present study. It depends on the assumption
that although there is a large variation in corpus luteum
size in the whole population, for a single female it
might be expected that the size variation in corpora
lutea of these two origins would be slight.

5
u

\-
uj

<
a

a
O
U

20 30 40 50 60 70 SO 90

ARTERIOLE WALL AS°/0OF TOTAL DIAMETER

ICO

Text-fig. 15. Relation between size of corpus and
thickness of arteriole walls (corpus luteum — triangle ;
'young' and 'medium' corpora albicantia — open
circles, 'old' corpora albicantia — black circles).

Persistence of corpora albicantia
In the routine examination of the 1955/56 ovary
collection 4065 corpora albicantia were classified into
these three stages of regression — 'young', 'medium'
and ' old ' — on the basis of their macroscopic appearance in the 5 mm. slices. The main criteria used
are the relative amounts of white connective tissue and brown ' luteal ' tissue. These types represent
stages in a continuous process so there is no definite line of demarcation between corpora in each of
the groups and it is sometimes difficult to decide in which of two groups a corpus should be placed.
This applies more to distinguishing ' young ' from ' medium ' corpora than ' medium ' from ' old '. In a
large sample these marginal corpora may be expected to cancel each other out. In addition to the
author, two colleagues (Mr A. E. Fisher and Mr J. H. Smoughton) have independently undertaken
the examination of parts of the material, and the fact that the results are consistent although obtained
by three separate workers supports the validity of the classification.

In Text-fig. 16 the frequency distribution of mean diameters of these three types is presented. There
is an extensive overlap between all three groups; the size range for 'young' corpora is 1-5-7-5 cm.,
for 'medium' corpora 0-7-5-5 cm., and for 'old' corpora 0-7-5-0 cm. The mean values and two
standard errors are 4-01 ±0-07, 2-94 ±0-05 and 2-01 ±0-03 cm., respectively. The frequency distribu-
tion for each group is as symmetrical as for the corpus luteum size frequency (Text-fig. 7).
The youngest corpora albicantia are most variable, both because the sample is smaller and because

6-2

37° DISCOVERY REPORTS

they include some which are of very recent origin and are presumably still in the initial phase of very
rapid regression. These probably account for the shoulder in the 'young' frequency curve at 475 cm.
The most striking of these frequency distributions is that for ' old ' corpora albicantia, which is very
symmetrical and suggests that no more than 30 out of 2339 corpora (1-3%) have either been wrongly
allotted to this group instead of to the ' medium ' group, or have disappeared completely. This is the
extent of the alteration required to make the curve quite symmetrical, and it may well be the result
of chance. The fact that the curve for this group is symmetrical and non-skewed confirms that these
corpora represent the final stage of regression in size and that very few are less than 1 cm. in diameter.
If 'old' corpora continued to regress in size, but some of those under 1 cm. in diameter were being
missed, then the frequency curve should be skewed, with a steeper slope where the lower sizes are

700

1 1 \ °'d

600

soo

400

1 medium

300

200

| young

100

J^TT* • 1 — 0 -1_

3 4

DIAMETER IN CMS.

Text-fig. 16. Size frequency distribution of 'young', 'medium', and 'old' corpora
albicantia. Means + 2 S.E. are indicated.

cut off. In fact it is symmetrical, like the frequency curve of corpora lutea. This material is con-
vincing direct evidence of the persistence of corpora albicantia throughout life in the female fin whale.
This conclusion can be checked by two methods which involve only the size of the corpora and not
their morphological type. In the first method the size frequency distributions in whales with 1, 2,
3, ... to over 30 corpora albicantia have been plotted separately. The modal diameter decreases as
the proportion of old corpora albicantia in the samples increases. In Text-fig. 17 the modal diameters
have been plotted against the number of corpora albicantia for those groups in which the sample size
was over 40. The modal diameter decreases in the first groups from about 4 cm. in the single corpus
group to 2 cm. in the groups with over 1 1-12 corpora; the mode then remains more or less the same
for the remainder of the groups. If corpora continued to regress in size until they finally disappeared
then the modal size should continue to decline instead of stabilizing at 2 cm. This is both the mean and
modal size of the ' old ' group of corpora albicantia.

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 371

A second method is to take all the corpora albicantia up to 3 cm. in diameter, and to calculate the
proportions in the size groups o-i, 1-2 and 2-3 cm. for each of the groups of females with 1, 2, 3, ...,
to over 30 corpora albicantia. The percentage composition of the 0-3 cm. groups is plotted in this way
in Text-fig. 18. If there is complete regression in size of the corpora albicantia one would expect, as
more corpora accumulate, a progressive and continued increase in the percentage of corpora in the

": 3 -

10 20

NUMBER OF C ALBICANTIA

30 >30

Text-fig. 17. Variation in modal diameter of corpora albicantia with increasing corpora numbers.

10 20

NUMBER OF C. ALBICANTIA

Text-fig. 18. Variations in percentages of corpora albicantia in different size groups,
with increasing corpora numbers.

0-1 and 1-2 cm. groups, and a decrease in the proportion of 2-3 cm. corpora, until at the higher
corpora numbers the great majority are in the 0-1 or 1-2 cm. group. Text-fig. 18 shows that there is
initially a rapid decrease in the proportion of 2-3 cm. corpora and a complementary increase in the
proportion of 0-2 cm. corpora, but when about fifteen corpora albicantia have accumulated this change
in the proportions of corpora albicantia ceases, and the numbers of 0-2 and 2-3 cm. corpora are nearly
equal. The numbers of 0-1 cm. corpora remain small and do not show any significant increase. This
means, as before, that the corpora albicantia regress in size to a modal diameter of 2 cm. and then no

372 DISCOVERY REPORTS

further. Those corpora included in the 'old' group are, therefore, assumed to be fully regressed
corpora, at least as regards size.

Clearly there is in general no complete regression of corpora in respect of size. Nor is there any
evidence that the corpora shrink to a mean diameter of 2 cm. and a weight of about 5 g. and then
become indistinguishable from the ovarian stroma by further loss of pigment. Corpora albicantia of
this size can easily be identified even if they appear to have lost all their pigmentation, because their
white avascular connective tissue stands out against the darker colour of the ovarian cortex. Nor is
there any histological evidence for eventual disintegration and resorption by phagocytes, because no
intermediate conditions have been observed. A consideration of the rate of formation of ' old ' corpora
albicantia lends further support to this conclusion (Text-fig. 22). Once they begin to form the increase
in their number is linear showing that they accumulate at a constant rate which shows no sign of
decreasing, at least up to a total corpora number of 30 or 40. If their life-span was less than the period
covered by the material then their numbers might be expected to approach or to reach an upper limit
at which loss was balanced by replacement.

It has already been established that the mean diameter of the fin-whale corpus luteum of pregnancy
is 11-44 cm- (P- 356), the mean diameter of the corpus luteum of ovulation is 8-28 cm. (p. 356) and
the mean diameter of the accessory corpora lutea is 3-88 cm. (p. 361). The latter group comprise only
37% of all corpora lutea examined, and their effect on the ensuing discussion is negligible. The corpora
albicantia, which represent former corpora lutea of all three types, have been shown to regress to a
mean size of 2-01 cm.

Table 4. Mean diameter of corpus luteum and mean or modal diameter of fully
regressed corpus albicans for five species

Mean or modal size (cm.)

-* ,

Percentage

Species

Corpus luteum

Corpus albicans

regression

B. physalns

11-44

2-0

82-6

B. musculus

1375

2-4

82-6

M. novaeangliae

11-98

c. 1-9

84-1

P. catodon

7-25

1-25

82-8

G. melaena

c. 5-0

c. 0-85

83-0

The frequency distribution of the diameters of corpora lutea of pregnancy is a symmetrical curve
with the mean approximating to the mode and it is likely that the curve for corpora lutea of ovulation
would be similarly symmetrical if there were more records, although the size range is greater.
Unfortunately, we have few records of corpora lutea of ovulation, because they persist for such a short
period and are mostly produced during the months before the present antarctic whaling season begins
(see p. 437). If the numbers of corpora lutea of pregnancy produced are equal to the numbers of
corpora lutea of ovulation, then a size frequency curve for all corpora lutea would have a mean which
would be the resultant of the mean diameters of the corpora lutea of ovulation and pregnancy, in this
hypothetical case 9-86 cm., which means that corpora lutea as a whole regress to 2 cm., that is by
79-7% of their initial diameter. On the other hand, if on average only one out of three ovulations is
followed by pregnancy the resultant mean size of all corpora lutea will be 9-33 cm. and the percentage
regression will be 78-6% of the initial diameter. It should be noted that the difference between the
amount of regression in these two cases is only 1 % and even with a ratio of four unsuccessful ovula-
tions to one pregnancy the variation is only increased to 1-7%. Conversely, if all ovulations were
successful and followed by pregnancy the percentage regression would be 82-6%. The range, from
a ratio of four unsuccessful ovulations to one pregnancy, to no unsuccessful ovulations, is only 4-6%.

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 373

There are reasons for believing that in the fin whale there are about two unsuccessful ovulations
to one pregnancy (see pp. 459-63) and this appears also to be the case in Globicephala melaena
(Fisheries Research Board of Canada. Annual Report, 1953).

This regression in diameter, in the second and most likely case, corresponds to a decrease in weight
from 500 to 5 g. (from Text-fig. 8), that is a percentage decrease of 99%. Because the density does
not change during regression this will equal the percentage decrease in volume.

Unfortunately we do not have material directly representative of the contribution of the corpora
lutea of ovulation to the accumulating corpora albicantia, but as has been shown, the maximum
variation from the true percentage regression is unlikely to be more than 4-6%. In order to compare
material from different species we can only compare the size of the corpus luteum of pregnancy and
the size of the fully regressed corpora albicantia, derived from both corpora lutea of pregnancy and
corpora lutea of ovulation. The results might be expected to vary slightly according to the ratio of

l/S

2
<

Hb0

10-

/ ?y/

5 -

p//

0 ■

LARGEST
C.LJ?

MEAN C.LP

MEAN C.L. \%
MEANC.LQ z

■SMALLEST
C.L0.

I 2 3

DIAM. OF REGRESSED C.A. (CMS.)

Text-fig. 19. Mean diameters of corpus luteum of pregnancy and mean or modal diameters of fully regressed corpus albicans
(blue, fin, humpback, sperm and pilot whale). For the fin whale the estimated mean size of corpora lutea of pregnancy and
ovulation is shown (Fj), and method of estimating regressed size from initial diameter is indicated by dotted lines.

ovulation and pregnancy corpora lutea although with small samples the experimental error will be
greater than this variation. In Table 4 and Text-fig. 19 the mean sizes of the corpus luteum of
pregnancy and the mean sizes of fully regressed corpora albicantia are given for five species of whales.
The data for the blue whale, humpback whale and sperm whale were obtained in the same way as the
fin whale data, though the material for the last two species is less abundant. The figures given for
Globicephala melaena are very approximate and are derived from the very few measurements given
by Harrison (1949). Nevertheless, the values for the percentage regression in diameter fall within the
range 82-6-84- l % • Mansfield (1958) gives measurements of 30 corpora lutea (mean diameter 24-4 mm.)
and 155 corpora albicantia (mode 6 mm.) of the Atlantic walrus, Odobenus r. rosmarus. These suggest
that the walrus corpus luteum regresses by about 75-5% in diameter, but the method of measurement
may be slightly different. For the two whale species for which the most observations are available
the percentage regression is identical.

This table shows that on average corpora lutea from 5 to 13-75 cm. in average diameter, of very
different cetacean species, regress by a similar amount to a final size which is proportional to the
initial size. From this it follows that corpora lutea of varying sizes in a single species should regress

374 DISCOVERY REPORTS

on average to a similar fixed percentage of their original size. Presumably this is determined by the
initial size of the graafian follicle and the connective tissue framework, and it is conceivable that the
corpora of ovulation might regress to a different percentage of the initial size, owing to a possible
initial difference in the amount of connective tissue in the gland.

We have material which enables us to check this hypothesis. It has been shown that the 'old'
corpora albicantia represent the final products of regression of corpora lutea both of ovulation and
pregnancy, and we have records of the size frequency of 2339 'old' corpora albicantia which enables
a very accurate frequency curve to be drawn. One assumption must be made — that corpora lutea
of ovulation and pregnancy are formed in the approximate ratio 2:1, but we can also test the hypo-
thesis using other ratios. There are good reasons, given later in this paper (see pp. 459-63), for
believing that this assumed ratio is in fact correct. This means that the mean diameter of all corpora
lutea will be 9-33 cm. and the upper regression line in Text-fig. 19 must be amended to the lower
for the fin whale (Fx) at least.

In addition to the size frequency distribution of ' old ' corpora albicantia there are records of the
size frequency of 523 corpora lutea of pregnancy (Text-fig. 7). By using the graph (Text-fig. 19) these
size frequencies have been converted into the corresponding size frequencies for the resulting corpora
albicantia (Text-fig. 20, curve B). If both types of corpora regress to the same extent then the
frequency curve for all ' old ' corpora albicantia represents the sum of the frequency curves of ' old '
corpora albicantia derived from corpora lutea both of ovulation and of pregnancy.

For direct comparison these frequencies are converted into percentages. The intervals for the
calculated corpora albicantia of pregnancy are different from the intervals for total 'old' corpora
albicantia because the peak value of this curve is almost exactly 2-5 cm. If it were drawn to the same
intervals as the total 'old' corpora albicantia the result would be to convert a symmetrical curve to
a skewed curve, so the points are displaced by 0-25 cm. with reference to the total ' old ' corpora
albicantia. The true frequency curve for corpora lutea of pregnancy (Text-fig. 7) has a shoulder at a
size corresponding to the interval 2-0-2-5 cm. in corpora albicantia and this has been drawn in to make
the curve more symmetrical (Text-fig. 20, curve B).

If the old corpora albicantia curve is the sum of fully regressed corpora lutea of ovulation and
pregnancy in the ratio 2:1, it may be considered to be composed of three units, and the corpora
albicantia of ovulation and pregnancy as two and one units respectively. In Text-fig. 20 the corpora
albicantia of pregnancy (B) total 100% and total 'old' corpora albicantia (A) are converted to equal
300%. If our assumption is correct a symmetrical curve totalling 200% (C) should be obtained by
subtracting the corpora albicantia of pregnancy frequencies (B) from the total ' old ' corpora albicantia
frequencies (A). This curve (C) should have a mean, mode and size range approximating to these
values for the sample of corpora lutea of ovulation sizes converted to corpora albicantia of ovulation
sizes. In Text-fig. 20 the size range, mean value and two standard errors (D) for the calculated
corpora albicantia of ovulation are shown for comparison because the sample is too small to give a
smooth curve. In fact, curve C is symmetrical, and its mean and mode approximate very closely to
the mean corpus luteum of ovulation diameter converted to corpus albicans of ovulation size.

The hypothesis can be tested with other ratios of corpora lutea of ovulation and pregnancy, but
none gives such a good fit. For instance, on the assumption that the numbers of corpora lutea of
ovulation and corpora lutea of pregnancy are equal, curve A is drawn so as to total 200 %, and curve B
as 100%, so that curve C should equal 100%. Curve C is again symmetrical with apeak at i-8 cm.,
but the size range is much less than expected (from D) and part of curve B falls outside curve A,
which is improbable.

It is, therefore, probable that the ' old ' corpora albicantia represent fully regressed corpora lutea of

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 375

which about two-thirds are contributed by corpora lutea of ovulation and one-third by corpora lutea
of pregnancy. The regression is to a constant proportion of the former size, and corpora lutea of
ovulation and pregnancy do not appear to differ in this respect. A negligible proportion are missed in
the routine examination.

It has been stated that the smallest corpus albicans which is expected to be observed in the routine
examination is about 7 mm. in diameter. Below this size it is probable that some will be missed
because the thickness of the slices is 5 mm. On the basis of the regression factor established above
a corpus albicans of 7 mm. corresponds to a corpus luteum of 3-2 cm. in diameter and it is therefore
likely that the majority of, but not all, corpora albicantia representing former corpora lutea under
3 cm. in diameter, are missed in the routine examination.

2 3

DIAMETER IN CMS.

Text-fig. 20. A, size frequency distribution of all 'old' corpora albicantia; B, size frequency distribution of 'old' corpora
albicantia of pregnancy (calculated from Text-fig. 19); C, resulting size frequency distribution of 'old' corpora albicantia of
ovulation; D, calculated mean diameter +2S.E., and size range of 'old' corpora albicantia of ovulation (see text for
explanation).

There was no corpus luteum of pregnancy smaller than 3 cm., but four out of 59 corpora lutea of
ovulation were under this size, that is, 6-8%. In terms of total 'old' corpora albicantia this will
represent 4-5% (because there are about two corpora lutea of ovulation to one corpus luteum of
pregnancy). The accessory corpora lutea, some of which do not represent ovulations, range from
0-5 to 8-5 cm. in diameter with a mean of 3-88 cm. so a larger proportion of them will be unrepresented
by observable corpora albicantia. In fact 11 out of 26 were under 3 cm. in diameter, that is 42-3%,
and since accessory corpora lutea comprise about 37% of all corpora lutea this amounts to about
i-6% of all' old' corpora albicantia. The accessory corpora lutea which are expected to be observed
when fully regressed, that is to say those which are initially 3 cm. in diameter or larger, amount to
2-1% of all corpora lutea.

376 DISCOVERY REPORTS

Thus, there is no permanent record in the form of fully regressed corpora, of 4-5 % of corpora lutea
of ovulation and pregnancy in the ovaries. On the other hand, 2-1% of the 'old' corpora albicantia
are expected to represent accessory corpora lutea, so there is a net loss of 2-4%. So far we have been
considering fully regressed corpora, but 42-5 % of all corpora albicantia in this sample of 4065 were
either 'young' (15-5%) or 'medium' (27-0%) and had not fully regressed. The corpus luteum which
would eventually be represented by a fully regressed corpus albicans of 7 mm., can be shown in these
two groups to have regressed to 1-4 or i-o cm. respectively, which means that the effective number of
lost corpora albicantia considered as a percentage of all corpora albicantia (' young ', ' medium ' and
'old') is considerably less than 2% and probably nearer 1%.

This is such a small fraction of the total that it is probably within the observational error and it will
be assumed for the purposes of applying the corpora counts to age-determination that all ovulations,
whether successful or not, are recorded permanently in the ovaries by corpora albicantia.

Accumulation of corpora albicantia
It has now been established that corpora albicantia of the three groups, ' young ', ' medium ' and ' old '
represent stages of regression. It might be possible to obtain an estimate of the absolute rate of
regression by examining the proportions in which they occur and the relative rates at which they
accumulate.

For 393 pairs of ovaries with three or more corpora albicantia collected in the season 1955/56 the
mean numbers of 'young' corpora albicantia for pregnant and non-pregnant females are 1-522 ±0-125
and 1 -586 ±0-185 respectively. There is no significant difference between these values and the com-
bined mean value is i-544±o-i04. Individual females had up to five 'young' corpora in the ovaries;
only 15 out of 393 had more than three. Unfortunately, there are only nine records of lactating
females, and they give a mean number of 1 -778 ± 0-688 ' young' corpora albicantia. This is not signifi-
cantly different from other samples, but the large standard error means that there could be a difference
of up to one 'young' corpus albicans between lactating and non-lactating females.

At the time of writing the 1956/57 sample has not yet been fully examined, but for 251 pairs of
ovaries which have been sliced (and have three or more corpora albicantia) the mean numbers of
'young' corpora albicantia for pregnant and non-pregnant females are 1-473 ±0-126 an^ J '545 ±0-3 18
respectively. There is thus no significant difference between the mean numbers of ' young ' corpora
albicantia present in each of these two seasons.

Using the 1955/56 data it is also possible to compare the mean number of ' young ' corpora albicantia
of females in part of the former sanctuary (area I),1 with the mean number of ' young ' corpora in the
older whaling areas (material mainly from area II). In area I the mean is 1-674 ±0-200 and in the
other areas it is i-507±o-i2i. Again the difference is not significant. The area I stock has been only
slightly fished and the annual mortality rate appears to have been about 10% prior to 1956, whereas
it has been found that in the older whaling areas the mortality rate is possibly over twice as high
(International Commission on Whaling, Eighth Annual Report, p. 24).

It would appear then, that there is little change in the average number of ' young ' corpora albicantia
produced from year to year, and that even great changes in the condition of the stock have had no
significant effect on the mean number of ' young ' corpora in the ovaries. This is a point of con-
siderable importance which will be referred to later (p. 384) in connexion with the constancy of the
average annual increment of corpora albicantia.

Considering now those ovaries in the 1955/56 collection containing five or more corpora albicantia
(sample size 323) we can determine the mean number of 'medium' corpora present. This is 3*220±

1 There are six antarctic whaling 'areas'. Area I is in the South-east Pacific Ocean (60-120° W.).

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 377

0-206, and the ratio between the mean numbers of 'young' and 'medium' corpora albicantia is
therefore 1 : 2-085. We will assume that it is 1:2.

'Young', 'medium' and 'old' corpora albicantia represent consecutive stages of regression and, if
the sampling is representative, the average duration of these stages should be proportional to the
frequency of each group, since they do not disappear. The 'medium' corpora albicantia are twice
as common in the samples as the ' young ' corpora.

The antarctic pelagic whaling season for fin whales lasted 58 days or 0-16 years in 1956, and 69 days
or 0-19 years in 1957, 1958 and 1959. It is, therefore, reasonable to suppose, for present purposes, that
sampling is instantaneous and at yearly intervals. The majority of corpora albicantia are formed
several months before the sampling period and very few actually during the sampling period (see
below, pp. 450-53). If the average duration of the 'young' stage extends over x sampling periods,
then the 'medium' stage, because it is twice as frequent, persists over 2X sampling periods. If
sampling were not restricted to a short annual period then the actual ratio of ' young ' to ' medium '
corpora in the samples might be very different from 1 : 2, and the actual duration of ' young ' corpora
(in terms of months, rather than sampling intervals) may be much less than half the duration of the
' medium ' stage.

An example will make this point clearer. Suppose the average month of formation of corpora
albicantia is August. Then the average sampling date (in February) is some 6 months later and for
'young' corpora albicantia to be fully represented in the samples they must, on average, persist in
this stage for over 6 months. In the simplest case, in order to fit the data a corpus albicans formed
in August must be present as a ' young ' corpus albicans only in the first sampling period, and as a
' medium ' corpus albicans in the two succeeding annual sampling periods. Whereas, on average, the
'young' stage need last at a minimum for just over 6 months (less than 18 months at a maximum) in
order to be represented in only one sampling period, ' medium ' corpora can last as long as 35 months
(but not less than just over 12 months) in order to be represented in two sampling periods.

It is, however, known that 'young' corpora albicantia do not disappear during pregnancy and
because ovulations do not occur during pregnancy the average duration of this stage of regression must
be at least 10 or 11 months, though the rate of regression may be more rapid during lactation
(see p. 434).

In estimating the average annual increment of corpora it is not, therefore, the absolute duration of
each stage, but the relative duration in terms of the number of sampling periods that occur during
each stage which is important.

Because the relation between the average numbers of ' young ' and ' medium ' corpora approximates
to a simple ratio, in the equation below t must approximate to a whole number.

Let n= observed average number of 'young' corpora albicantia;
t = duration of this regression stage in sampling intervals ;
a = annual increment (to be ascertained).

Then a = njt, and the shorter the duration the larger must be the annual increment (or vice versa)
to provide the observed value of n.

The parameter n is known ; t must be sought by trial and testing with other evidence but is assumed
to be a whole number (not a fractional value), for the reasons given above.

If t = 1 then a = 1-544 ±0-104;
t = 2 then a = 0-772 ±0-052;
t = 3 then a = o-5i5±o-035;
t = 4 then a = o-386±o-026.

Values of t higher than 2 are excluded by virtue of the sexual cycle of the mature female and the

378 DISCOVERY REPORTS

high percentage of these females which are found to be pregnant (p. 455); this requires appreciably
more than one ovulation in 2 years.

The second case (t = 2) is a possibility, but for a 2-year breeding cycle it gives a ratio of ovulation cor-
pora to pregnancy corpora of approximately 1 : 2. This does not fit the conclusions about the percentage
regression factor and the data on the size frequency of fully regressed corpora albicantia (p. 374)
which indicate a ratio of 2 : 1 ; nor is it in agreement with the evidence from the sexual cycle (p. 460 ).

The first and simplest case (t = 1) appears much the most probable. For a 2-year breeding cycle
it gives a ratio of ovulations to pregnancies of approximately 2:1, which is in agreement with the
conclusions drawn from the size frequency of fully regressed corpora (p. 374). It is also in agreement
with estimates of the average annual rate of ovulation obtained by other quite independent methods
(p. 460) It also means that on average the regression to 'old' corpora albicantia takes about 3 years,
which was the opinion of Van Lennep (1950, p. 596), based on histological grounds. This evidence
strongly suggests that the average annual increment of corpora is about 1-5, although on the present
evidence a possible increment of 075 cannot be completely excluded. Further support for t = 1,
comes from the growth estimates (on pp. 413-415, and Text-figs. 38 and 39).

In Text-figs. 21 and 22 the mean numbers of 'old' and recent (that is 'young' and 'medium')
corpora albicantia for different total corpora numbers have been plotted and curves fitted to them. It is
then apparent that the average number of recent corpora continues to increase with age. One possible
explanation of this is that the average annual production of corpora albicantia increases with age and
as this has a very important bearing on the question of age-determination it must now be dealt with.

Other considerations being equal the formation of ' old ' corpora albicantia should lag about 3 years
(strictly three sampling periods) behind the production of ' young ' corpora, but should take place at
the same rate. The regression line describing the rate of accumulation of ' old ' corpora should there-
fore have a slope of 1 -o. In fact the regression line (calculated by the method of least squares and ignoring
the first six points) is described by y = — 3-433 + 0-885*, when y is the number of 'old' corpora
albicantia, and x is the total number of corpora albicantia. This gives an intercept on the x-axis at
3-88, suggesting that if 'young' corpora take three sampling periods to regress to 'old', then the
annual increment in the first 3 years after puberty averages about 1-3. We know that there are in the
material 88 females in their first pregnancy, and these had a mean number of 1-420 ±0-146 corpora,
which is in close agreement. The intersection of the two curves in Text-fig. 21 is at 8-9 corpora, when
4-45 recent corpora and 4-45 ' old ' corpora have formed. This implies that during the time it takes for
4-45 ' old ' corpora to accumulate a further 4-45 ' young ' and ' medium ' corpora are formed and that
' old ' corpora are being added at about the same rate as ' young ' corpora are formed. This suggests
that ' young ' corpora form at the rate of about 1 -48 per year.

The average number of recent corpora then increases from 4-45 at this intersection to 5-8 when
a total of 20 corpora have accumulated and to 7 when a total of 30 corpora have accumulated,
and so on. This apparently corresponds to increases in the annual rate of production of corpora
from 1-3 just after puberty to approximately 1-5, 1-9 and 2-3 at later ages. In terms of the number of
ovulations per 2-year cycle it implies a 50% increase over this age range from about 3 to over 4-5, that
is more than one extra ovulation per cycle.

There is some evidence that the frequency of dizygotic twinning increases with age as a result of
multiple ovulations (Kimura, 1957), but only by a few per cent. Accessory corpora lutea amount to
only about 4% of all corpora lutea and multiple ovulations increase only slightly with age (see p. 454).
Nor is there any evidence for any other kind of increase in the ovulation rate. The percentage of
mature females with corpora lutea in the ovaries remains remarkably constant with increasing age
(Text-fig. 52).

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA

379

7 8 9 IO II 12 13

TOTAL NUMBER OF CORPORA

Text-fig. 21. Changes in the mean number of 'old' (white circles) and recent ('young' and 'medium')
corpora albicantia (black circles), with increasing corpora numbers.

20 30 40

TOTAL NUMBER OF CORPORA

Text-fig. 22. Changes in the mean number of 'old' corpora albicantia with increasing corpora numbers.

Two possible explanations of this rise in the number of recent corpora albicantia associated with
increasing age could be advanced. One is that there is a progressive human error in the counts, a
tendency to overestimate the number of recent corpora as the total number of corpora increases. This
can be checked and does not account for this large increase.

Another explanation is that the rate of regression becomes progressively slower with age, the duration
of the ' young ' and ' medium ' stages being longer and the number of corpora in these stages increasing.
It is possible to apply a test to this hypothesis, because if the rate of regression is slower then the

380 DISCOVERY REPORTS

size of corpora albicantia of similar ages should be greater in older whales. Dr Mackintosh has shown
me some unpublished figures he worked out for the average sizes of corpora albicantia, based on a
large number of measurements. He was able to show that the average size of the nth. largest corpus
albicans does in fact increase with age, that is, with increasing corpora number. For example, when
there are 10 corpora albicantia the tenth largest is smaller than the tenth largest when there are
20 corpora albicantia. This finding has been inexplicable up to now, because the most obvious inter-
pretation, that the size of the corpus luteum and therefore of its products increases with age, is known
to be inapplicable (see p. 357). I am indebted to Dr Mackintosh for enabling me to refer to this work.

It appears then that this apparent increase in the rate of ovulation is due to the lengthening of the
period occupied by the regression of the corpus albicans in older whales. A correction has, therefore,
been made, by assuming that ' old ' corpora albicantia accumulate at the same rate as ' young ' corpora
albicantia form. This assumption is valid if the duration of the regression period is constant and there
is no human error in the counts of recent corpora, and no increase in the rate of ovulation. The last
qualification is not quite correct, but may be ignored for the moment.

A corrected regression line of slope 1 -o was, therefore, drawn through the intersection point of the
two curves shown in Text-fig. 21, giving an intersect on the x-axis of 4*45, and an estimate for the
average annual increment of corpora of 1-48. This figure is likely to be a little high because it does not
allow for any increase in the regression period while the first nine corpora are accumulating; nor are
we justified in assuming that there is no increase in the ovulation rate with age. There is in fact a
slight rise in the incidence of multiple ovulations. Taking into account all the evidence the best
estimate of the average annual rate of accumulation is between 1-4 and 1-5.

Taking the duration of the ' young ' and ' medium ' stages in the regression of corpora to be about
1 and 2 years respectively, the mean sizes of the corpus luteum, ' young ', ' medium ' and ' old ' corpora
albicantia, may be plotted on semi-logarithmic paper. For both diameter and weight the initial
regression is very rapid, corresponding to the change from glandular tissue to collagen, and is suc-
ceeded by slower regression which is apparently exponential (that is to say, the points fall on a straight
line) until the fully regressed stage is reached.

Corpora aberrantia

In addition to the types of normal corpora albicantia and corpora lutea, which have been described
and shown to represent stages in the regression of ovulation and pregnancy corpora lutea, a very small
number of other corpora are present in fin-whale ovaries.

During the examination of the 1953/54 ovaries four unusual types of pigmented bodies were identi-
fied. One very distinct type, small and bright orange-yellow in colour, is more properly a corpus
atreticum and is not considered to represent a former corpus luteum. The other three main types
have yellow or buff pigmentation. They were termed corpora aberrantia and distinguished by the
adjectives ' yellow ', ' buff-cellular ' and ' yellow and white '. In the routine examinations of part of the
1955/56 collection further observations were made on the incidence of these types. Out of a total of
2655 corpora albicantia and corpora aberrantia (corpora atretica excluded) only 37 (or 1-4%) were
corpora aberrantia. The 'yellow' type comprises 0-7%, 'buff-cellular' o-6% and 'yellow and white'
o-i%. They were present in 34 out of 273 pairs of ovaries (12-5%).

All appear to have developed from ruptured follicles (Text-fig. 236 and c), but it is difficult to
establish the cause of their formation and their fate is uncertain.

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA

38i

' Yellow ' corpora aberrantia
The size range of 17 corpora of this type is from 1-3 to 3-3 cm. in mean diameter, average 2-12 cm.
They range in colour from a uniform bright lemon-yellow to primrose-yellow in both fresh and fixed
material. In shape they are usually irregular or amoeboid, suggesting a collapsed follicle which has
re-expanded only slightly, and often have a conspicuous stigma (Text-fig. 23 a).

In histological preparations of formalin- or Bouin-fixed material, paraffin embedded, they are seen
to consist of a homogeneous collagenous matrix (staining blue in Mallory, green in Masson's trichrome,
and pink in Haematoxylin and Eosin) with uniformly scattered vacuoles representing dissolved lipoids.
In material which has been fixed in Zenker-formol (Helly) and post-osmicated (PI. VII, fig. 3),
darkly stained lipoid material is seen to be distributed in discrete globules throughout the matrix,
but there are concentrations of lipoid material at the periphery. In contrast to the normal corpus
albicans the outline is very definite and there is no penetration by blood vessels into the lobes of
the corpus.

'.;'■

Text-fig. 23. Morphology of corpora aberrantia (a-c) and corpora atretica (d-i).

' Buff-cellular ' corpora aberrantia
The mean size of fifteen corpora of this type is 2-14 cm., ranging from 1-3 to 3-2 cm. in diameter.
Macroscopically the colour is a pale buff with a slightly darker layer next to the trabeculae marking
the folding of the original follicle and dividing the corpus into narrow compartments or cells (Text-
fig. 236). These corpora are very similar to the 'yellow' corpora aberrantia in histological structure,
but differ in their more regular outline and in the distribution of the pigment. They are thrown into
many small, meandrine folds reminiscent of a miniature corpus luteum and like the corpus luteum
give the impression of a re-expansion to occupy a roughly spheroidal or ovoidal shape. As in the
other corpora aberrantia there is very little vascularization and the blood vessels are confined to the
narrow trabeculae. In histological preparations the pigmentation is heavier in a layer adjacent to the
trabeculae.

' Yellow and zvhite ' corpora aberrantia

The size range of three corpora of this type is 2-2-2-5 cm., with a mean diameter of 2-3 cm. The colour
is white, with a deep orange-yellow pigment outlining the folds of the original follicle wall (Text-
fig. 23c). The pigment zone may be more extensive in parts, which then resemble the 'yellow' corpus
aberrans. The outline in the three specimens available is more regular than that of the ' yellow ' corpus
aberrans but less regular than the 'buff-cellular' type. Histologically they are seen to be similar to
the other two aberrant types, but have a much narrower and more densely pigmented zone near the
trabeculae (PI. VII, figs. 4, 6). As in these others the few blood vessels present are confined to the
trabeculae.

382 DISCOVERY REPORTS

One must conclude that these three types of aberrant corpora are very similar in size and structure
and, therefore, in their origin and fate. In fact they may represent stages in the regression of one type.
It is noticeable that all are more or less avascular bodies and appear to have undergone a type of lipid
hyaline degeneration which is probably a direct result of the deficient vascularization.

It is not possible to say with certainty whether they persist as well-pigmented bodies for a long or
short period. Nor is it known at which part of the breeding cycle they are formed, but they do not
represent corpora lutea of pregnancy. All three types are found in females at puberty in addition to
the more usual corpora albicantia. It seems likely that in fully mature females they form during or
prior to the resting period and possibly again as accessory corpora lutea at the start of pregnancy.
These bodies are present in 38-4± 19-0% of resting females and i3'2±7*4% of pregnant females, but
this difference is not quite significant at the 95 % level. In the first half of pregnancy (foetus 0-1 m.
long) 45 ±30% had one or two such bodies in the ovaries, and in the second half of pregnancy (foetus
larger than 1 m.) only 7- 1 ± 5 -8 % had corpora aberrantia in the ovaries. Of those females with foetuses
longer than 2 m. only 1-7 ±3 -7% had such corpora. Of eleven lactating females none had such
corpora aberrantia; some lactating females have anomalous corpora which are like corpora albicantia
in their gross morphology but resemble corpora aberrantia in their histology. These observations
suggest that their longevity as corpora aberrantia is probably little more than a year, and if some are
formed at the same time as the corpus luteum of pregnancy then their life is only about 6 months.
Their scarcity in terms of total corpora (1-4%) and their relative abundance in terms of the proportion
of ovaries showing them (12-5%) supports this contention. In view of the fact that 38-4±i9#o% of
resting females had corpora aberrantia in the ovaries, but no lactating females had them, it would
seem likely that these resting females had ovulated recently.

Corpora aberrantia are unlike corpora albicantia in their morphology, but the appearance of the
collagen is similar to the pigmented collagen of corpora albicantia, except that it is much more heavily
laden with lipids and pigment and the distribution of lipoid material is different. In view of their
collagenous nature they cannot be regarded as functional, but are regressing bodies.

Corner, Bartelmetz and Hartman (1936) concluded that the corpora aberrantia, which they
described in the rhesus monkey, were probably formed at the same time as corpora lutea of the cycle
or of pregnancy. The whale corpora aberrantia now described are different from those described by
Corner, Bartelmetz and Hartman which retain recognizable granulosa lutein cells and have a very
noticeable network of capillaries. The latter are also much larger relative to the true corpora lutea
than are the whale corpora aberrantia. These authors' type 3 corpora aberrantia appear to be very
similar to the whale corpora atretica to be described below.

In most respects but size, the whale corpora aberrantia appear to agree with the description by
Dubreuil and Riviere (1947, p. 83 and fig. 27, 1) of the ' mode de degenerescence lipoide ' in the human
ovary.

Corpora atretica

In addition to the corpora lutea, corpora albicantia and corpora aberrantia, there are in fin-whale
ovaries a number of small, bright orange-pigmented bodies. Laurie (1937, p. 244) described occasional
yellow bodies in blue-whale ovaries. These were small (1-0x0-3 cm-) and located deep in the ovary
as compared with the other types of corpora which are most superficial. They were described as
corpora atretica, the relics of atretic follicles. In the sample of fin-whale ovaries with altogether
2655 corpora lutea, albicantia and aberrantia there were a further 5% of corpora atretica. The
greatest numbers were found in resting females (maximum 4) and in pregnant females with a foetus
1-3 m. long (maximum 8). In contrast to the corpora aberrantia no significant differences were found
in the percentage occurrence of corpora atretica at different stages of the sexual cycle.

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 383

The mean diameter of those measured was 1-27 ±0-14 cm., but the modal diameter is 075 cm.
and the true mean diameter is probably less than 1 cm.

All stages in the formation of these bodies have been observed, from a relatively large follicle
(maximum 3-5 cm.) with slightly folded walls and a bright orange lining, through similar follicle stages,
becoming more and more collapsed, and finally to small (4 mm.) stellate bodies or thin compressed
orange streaks (Text-fig. 23 d-h). These undoubted chronological stages confirm that these bodies are
corpora atretica. They have, therefore, been ignored in making the routine counts of corpora for
purposes of age-determination (p. 466). There are also collagenous unpigmented corpora atretica in
which the original follicle wall can be identified (Text-fig. 23 i).

The histology of one such pigmented body is illustrated in PI. VII, figs. 5, 7. This shows it to be

composed of tissue heavily laden with lipoid globules, but with very little collagenous material.

It also shows the folding of the original follicle wall. These corpora atretica appear to be homologous

with the 'corps lipoides' or 'formations spongiocytaires ' of the human ovary described by

Dubreuil and Riviere (1947, p. 83 and fig. 26 I). The third kind of atypical corpus of the rhesus

monkey described by Corner, Bartelmetz and Hartman (1936) also appears to be in this category.

It is largely composed of clear lipid-filled cells believed to be derived from the theca interna,

but there is also a distinct zone of darker cells which appear to be granulosa cells. Brambell (1956,

p. 501) described the corpora lutea atretica found in various mammals and states that, according to

the majority of authors, these corpora originate by hypertrophy and hyperplasia of the cells of the

theca interna after degeneration of the membrana granulosa. Owing to the small amount of whale

material which has been examined histologically, it is not possible to say definitely whether whale

corpora atretica are composed mainly of transformed theca interna cells or are developed from the

granulosa layer.

Conclusions

Old, non-functional corpora lutea are termed corpora albicantia although the majority are still
pigmented. There is no significant difference in the mean size of corpora albicantia of pregnant,
non-pregnant and lactating females, which have a mean diameter of 2-5 cm. and a mean weight of
about 10 g. The relation between weight and diameter for corpora albicantia is the same as that for
corpora lutea and there is no significant alteration in density as a result of the changes in composition,
appearance, and histology.

The morphological types of corpora albicantia correspond to the types of corpora lutea and in
particular the incidence of vesicular or radiate corpora albicantia is not significantly different from
the proportion of vesicular corpora lutea. This confirms that the incidence of vesicular corpora lutea
of ovulation is not appreciably different from the incidence of vesicular corpora lutea of pregnancy.

Three age-groups of corpora albicantia have been identified on the basis of anatomical and histo-
logical changes. 'Young' corpora albicantia have a mean diameter of 4-01 cm. and a weight of 41 g.;
the values for 'medium' corpora albicantia are 2-94 cm. and 15 g.; and for 'old' corpora 2-01 cm.
and 5 g. The latter group has been shown to represent the final stage of regression when the corpus
largely consists of unpigmented collagen.

Evidence which is considered to be conclusive has been presented showing that the corpora persist
throughout the life of the individual. It appears that corpora lutea regress by a constant proportion
of their initial size to a final size which is directly related to the initial size. Only the remnants of those
corpora lutea originally under 3 cm. in diameter are likely to be missed in the routine examination of
5-mm. slices. This means that no more than 1 % of ovulations are unrepresented by corpora albicantia
large enough to be recorded in the conditions of the routine examination, and for practical purposes
of employing corpora counts for age-determinations this may be regarded as negligible.

384 DISCOVERY REPORTS

Some evidence bearing on the rate of accumulation of corpora albicantia is provided by examination
of the absolute and relative numbers of these three types of corpora albicantia. There are no significant
differences between the mean numbers of ' young ' corpora albicantia in pregnant and non-pregnant
females, nor between samples taken in consecutive years, the mean value being 1-54. Large variations
in the mortality rates of populations of fin whales apparently have no significant effect on the rate of
formation of corpora albicantia. It follows that if there are differences in the rate of accumulation
they must be slight. The mean number of 'medium' corpora albicantia is 3-22, giving a ratio of
' young ' to ' medium ' corpora of 1 : 2. The average duration of the ' medium ' stage is probably about
twice as long as that of the ' young ' stage and it is concluded that the ' young ' corpora probably
represent one year's increment, and on average take about 3 years to regress to ' old ' corpora, which
after the first few years accumulate at the same rate as the ' young ' corpora. The mean number of
' young ' and ' medium ' corpora apparently increases with increasing total corpora number. Evidence
is presented which strongly suggests that this is the result of a progressive retardation in the regression
of corpora with increasing age of the female. Taking this into account the corrected estimate of the
mean annual increment of corpora albicantia is between 1-4 and 1-5 although the possibility that
this is in error by a factor of 2 cannot be excluded.

The possibility of gross morphological differences between corpora albicantia derived from corpora
lutea of pregnancy and ovulation respectively, as suggested by Robins (1954) and Van Lennep (1950)
has been examined and rejected. Peters (1939) claimed to have found such a macroscopically
recognizable difference, based on differences in the colour and texture of the gland, in the arrange-
ment of the connective tissue and the trabeculae. Although he examined 27 pairs of blue-whale ovaries
and 57 pairs of fin-whale ovaries, with altogether 500 corpora, his counts establishing the proportions
of the two groups of corpora are based on only 4 pairs of blue-whale ovaries (with 75 corpora in all)
and 7 pairs of fin-whale ovaries (with altogether 97 corpora). He states that the darker group repre-
sent corpora of pregnancy and the lighter-coloured are corpora of the cycle. Since every corpus of
pregnancy corresponds to a breeding period, and, therefore, on average to 2 years of life, the average
number of ovulations per cycle can be obtained from the ratio of pregnancy corpora to ovulation
corpora. For instance, if this ratio is 1 : 1 then there will be two ovulations per cycle. Peters's actual
values for blue and fin whales are respectively 1 -9 and 1 -8 ovulations in 2 years.

Unfortunately Peters did not give precise details of these differences in his paper, but promised
that they would be given in a later paper which was not completed before his death. No macroscopic
difference attributable to different origin has been observed in the present material although several
thousand corpora have been examined in detail. The only clear distinction which has emerged is that
which is the result of age changes in the corpora. The differences between recent ('young' and
'medium') and 'old' corpora are similar to those indicated by Peters as distinguishing corpora of
pregnancy and ovulation respectively.

It is instructive to assume that recent and ' old ' corpora are derived from corpora lutea of pregnancy
and ovulation respectively and see what figure is obtained for the rate of ovulation. The mean number
of corpora albicantia per female in the 1953/54 an<^ I955/5° samples is 9-7. From Text-fig. 21 the
mean numbers of recent and 'old' corpora albicantia at this corpora number are 4-6 and 5-1 respec-
tively, giving a ratio of i:i-i and, according to Peters's hypothesis, an assumed 2-1 ovulations per
2-year cycle. The agreement with Peters's estimate of i-8 is rather close when it is recalled that Peters's
sample only contained seven whales and would have a correspondingly large variance. It is the author's
opinion that this is probably the basis of Peters's estimate and this assumption, that recent and ' old '
corpora are of different origin, is known to be incorrect.

It may be possible to identify corpora albicantia derived from corpora lutea of ovulation and
pregnancy by quantitative histological examination. The rate of regression of corpora albicantia

CORPORA ALBICANTIA, CORPORA ABERRANTIA AND CORPORA ATRETICA 385

appears to be related to changes in the thickness of the walls of the blood vessels. The relative thickness
of the vessel walls may be a better quantitative index of the age of a corpus than is its diameter. Since
the initial diameter of the corpus luteum of ovulation is only about two-thirds that of the corpus
luteum of pregnancy, it is likely that for a given vessel-wall thickness the ratio of the percentage thick-
ness of the vessel wall to the diameter of the corpus will be higher for those corpora albicantia derived
from corpora lutea of pregnancy than for corpora lutea of ovulation and could perhaps be used to
differentiate them. This is the only distinctive character which appears likely.

There are two other types of corpora which are found in fin-whale ovaries. These are the corpora
aberrantia and corpora atretica. The former comprise 1-4% of all corpora albicantia and aberrantia
and appear to develop invariably from ruptured follicles. They are more heavily pigmented than
corpora albicantia and are also characterized by the absence of blood vessels from the lobes of ' luteal '
tissue. Their frequency in different phases of the 2-year breeding cycle suggests that there is an ovulatory
period at the end of lactation or the beginning of the 'resting' period when they are formed. These
corpora are included in the routine counts of corpora albicantia for purposes of age-determination.
The corpora atretica are formed from unruptured atretic follicles and are easily distinguished from
true corpora lutea, albicantia or aberrantia. They are not included in the routine counts of corpora.

We have now dealt with the ovaries and the formation and subsequent history of the corpus luteum.
It has been established that the corpora albicantia persist throughout the life of the female and from
the numbers at the different stages of regression it appears that they accumulate at the rate of approxi-
mately 1-4-1-5 per year although the possibility of 0-7-0-75 per year cannot be excluded.

In the next part of this paper the accumulation of corpora albicantia up to the attainment of physical
maturity will be discussed. Then the annual cycle and life-history of the fin whale will be described
and the probable time and rate of ovulation will be discussed with a view to obtaining a second inde-
pendent estimate of the annual increment of corpora and also of the range of variation.

ACCUMULATION OF CORPORA UP TO THE ATTAINMENT

OF PHYSICAL MATURITY

The evidence presented in the preceding section suggests that the average rate of ovulation in a stock
of whales does not vary appreciably from year to year or in different areas, but little has been said
about the amount of variation shown by individual females. An examination of the accumulation of
corpora up to a fixed point in the life-cycle, the attainment of physical maturity, is of relevance to this
problem and gives us some additional evidence.

The frequency of corpora in early baleen groups

It is shown below (p. 41 1) that, on average, females ovulate 1-42 times before becoming pregnant for
the first time. In studying the amount of individual variation in the rate of accumulation of corpora,
up to what is presumably a fairly regular age, the initial variation in the number of corpora in early
age-groups, caused by the spread of ages at puberty, must be taken into account.

In the fin whale the evidence suggests that the majority of females ovulate for the first time at ages
ranging from 3 to 8 years (see below, p. 407). Thus an 8-year-old female may be primiparous with one
corpus luteum in the ovaries or have been mature for several years, with a correspondingly greater
number of corpora in the ovaries. In any one age-group there can, therefore, be quite a wide range
of corpora frequencies depending on the individual ages at puberty.

Hylen et al. (1955) give the frequencies of numbers of corpora in the ovaries of sexually mature
female fin whales in baleen age-groups II-V. A description of this method of ageing may be seen in

papers by Ruud (1940, 1945) and Ruud and Jonsgard (1950).

8-2

386 DISCOVERY REPORTS

Sexual maturity in female fin whales is attained on average between baleen groups III and IV, with
small numbers maturing in groups II and V. Consequently, the frequency distribution of corpora
numbers in group V may be slightly truncated in the lower numbers, but will represent fairly
accurately the frequency distribution of corpora numbers within early age-groups (Text-fig. 27) and
can be compared with the frequency distribution of corpora at the attainment of physical maturity.
Hylen et al. (1955) point out that baleen group V probably includes animals from more than one year
class because it includes females with rather high corpora numbers. They suggest that 5-7-5% of
individuals placed in group V are certainly older than 5 years of age, although the participation of
older year classes may be greater than this. The mean number of corpora in baleen group V is 5-607
and, on the assumption that the average increment of corpora is 1-4-1-5 per year, the average age of
group V would seem to be some 4 years later than puberty, suggesting, if puberty usually occurs in
groups III and IV, that it includes several year classes.

A similar conclusion is reached on comparing ear-plug ages with baleen groups (see Text-fig. 55,
p. 467).

The number of corpora at the attainment of physical maturity

Growth in body length is accomplished in mammals by intercalary growth of the vertebrae, which
occurs, as in other bones, at the zones of cartilage joining the epiphyses to the diaphyses. A whale is
said to have attained physical maturity when the epiphyses are fused to the centra along the entire
length of the vertebral column. When this happens linear growth of the vertebral column ceases,
although growth in other dimensions may continue and the skull may continue to grow slightly. It has
been shown that fusion of the epiphyses begins at both ends of the vertebral column and proceeds
inwards. This process is more rapid from the tail end than from the head end so that fusion is usually
completed in the anterior thoracic region, generally at the level of the fourth and fifth thoracic
vertebrae.

Wheeler (1930, p. 411) showed that in female fin whales physical maturity is reached when about
15 corpora lutea and albicantia have accumulated in the ovaries. Peters (1939) came to a similar
conclusion, but Brinkmann (1948) and Nishiwaki (1950 a, 1952) concluded that the threshold of
physical maturity was correlated with the accumulation of respectively 13 and 11-5 corpora. These
discrepancies are probably the result of the application of different criteria of physical maturity, which
will be discussed presently. Chittleborough (19556, p. 321) suggested that physical maturity in the
humpback whale coincides with the accumulation of some 30 corpora in the ovaries, but his criteria
(Chittleborough, 1955 a) differ from those of other workers and his relative growth curve (19556,
fig. 3) suggests that linear growth ceases when about 15-20 corpora have accumulated. The material
of Symons and Weston (1958), although very sparse, suggests that physical maturity in the humpback
whale is attained when between 8 and 20 corpora have accumulated and the criteria of maturity which
they adopted are those used by the ' Discovery ' Committee and the National Institute of Oceano-
graphy. Laurie (1937, p. 236) found a similar correlation in blue whales, physical maturity being
attained at about 11-12 corpora.

'This accumulation of such a regular number of corpora lutea at such a landmark as physical
maturity seems to leave no doubt not only that the corpora lutea persist up to and well beyond the
age at which physical maturity is reached but also that the accumulation takes place at a fairly steady
rate. It can also perhaps be argued that the ossification of the vertebral epiphyses and the accumulation
of corpora lutea could scarcely keep in step with one another in this way except in their relation to the
age of the whale, and that therefore the females normally become physically mature at a fixed age in
either species after the attainment of sexual maturity (Mackintosh, 1942, p. 221).'

ACCUMULATION OF CORPORA UP TO ATTAINMENT OF PHYSICAL MATURITY 387
The body length at sexual maturity appears to be a fairly constant proportion of the body length at
physical maturity, and has been shown to average 85-1% (range 80-0-88-5, a = 3-14, V = 3-69) for
a number of cetacean species for which data were available (Laws, 19566). Recent work on pinnipeds
confirms that the age at sexual maturity in this group is related to the growth-rate, and it appears that
those species which are precocious sexually also show precocious physical maturity (Laws, 19566,
1959c). However, it seems unlikely that physical maturity is necessarily attained at a firmly fixed
number of years after sexual maturity, but rather that there is a similar spread, as in the age at puberty,
over a few years.

Since Wheeler (1930) first demonstrated the correlation between physical maturity and corpora
number a large amount of extra material has been collected and it seems worth while briefly to re-
examine the relationship.

Material and methods

Wheeler (1930) had data on physical maturity and corpora number from 171 sexually mature female
fin whales. In the present material there are 925 sexually mature females for which data on the
progress of physical maturity are available, including 642 physically immature females and 283 mature.

This material was accumulated between 1929 and 1949 and I have not included more recent data
because the present sample is sufficient to demonstrate the closeness of the correlation. Further
material could hardly improve the correlation, but might even increase the variation by adding to the
human errors (a further six workers being involved). I am indebted to my colleague Dr R. H. Clarke,
who had classified and tabulated this material and who kindly placed his material and a preliminary
analysis of the data in my hands.

Some explanation of the procedure followed is desirable. Ideally it would be useful to have for
each whale as complete data as possible over the whole length of the vertebral column, but for
practical reasons this is impossible. On floating factory ships and to a lesser degree at shore stations
there is only a very short period during the working up of the whale (from the time when the meat is
removed from the backbone until the vertebrae are sawn up and put into the cookers), when it is
possible to examine the vertebral column.

Observers are, therefore, instructed to examine the crucial vertebrae first, namely the fourth and
fifth thoracics. If these are unfused they then try the posterior thoracics and if these are still unfused
and time permits, then a lumbar vertebra, and if necessary a caudal vertebra, is examined. The rib
sockets and chevron bones are useful guides to the different regions. If an epiphysis is unfused a note
is made as to whether the cartilage is thick or thin, and if fused, whether the join is visible or invisible.
The vertebra is then classed as one of four categories according to the state of fusion—' unfused thick
cartilage ' (UTC), ' unfused thin cartilage ' (UFC), ' fused join visible ' (FJV) and ' fused join invisible '
(FJI). These categories are illustrated in Text-figure 24. Because the epiphysis has a separate blood
supply from the centrum these two parts are sometimes differently coloured, either the epiphysis or
the centrum being engorged with blood. This means that the line of fusion can then be picked out
even in the fourth class (FJI).

The observations on which this section is based have been made by no less than nine different
workers and this naturally results in an increase in the amount of variation. There are two main
sources of error: first, in the counts of ovarian corpora, some workers record ' doubtful ' corpora much
more frequently than others, and the ovaries on which the counts were made were sliced by hand,
a method which is likely to lead to small errors of omission. Secondly, and probably more important,
are the variations in individual techniques of examining the vertebral column. Attention has already
been drawn to the discrepancies between the results of the examination of fin whales by Wheeler
(1930) and Peters (1939) on the one hand, and Brinkmann (1948) and Nishiwaki (1950a, 1952) on the

388 DISCOVERY REPORTS

other, and as regards humpback whales to the divergence of the results of Chittleborough (1955 6) and
Symons and Weston (1958). It is thought that the techniques used by the 'Discovery' Committee
and later by the National Institute of Oceanography have been fairly well standardized and that in
the present material individual differences in interpretation are reasonably small.

There is, however, a basic cause of variation which must now be mentioned. Fusion of the epiphyses
to the centrum progresses from the centre to the periphery (Text-fig. 24) which means that the
determination of the state of fusion depends to some extent on the depth at which the line of fusion
is examined and is, therefore, influenced by the tools used to examine the vertebrae. When a knife
is used the cut is necessarily superficial; with a hand-axe or adze the cut is deeper, but more superficial
than the section exposed by use of a felling axe. Other things being equal, the more superficial the
examination, the later will be the apparent attainment of physical maturity.

UTC

UFC

FJV

FJI

Text-fig. 24. Diagram showing stages of epiphyseal fusion. Above, sagittal section of centrum and epiphysis; below,
appearance of tangential chips. The first example of FJI shows how the blood may indicate the line of fusion.

Results
In analysing the data, certain simple conventions have been followed.

(a) As regards the classification of individual vertebrae, fused join visible (FJV) is counted as fully
fused. Although the fact that the join is visible means that there is a thin layer of cartilage at the
periphery, this layer is not always continuous (e.g. Wheeler, 1930, PI. V, fig. 2) and usually there is com-
plete fusion in the less superficial parts (Text-fig. 24). Purves and Mountford (1959) have mistakenly
assumed this class to be unfused, but have used the figure of 14-15 corpora at the threshold of physical
maturity (which is dependent on the FJV classification being classed as fused). Wheeler (1930,
pp. 407, 408) also counted FJV as fused. If the FJV group is classed as unfused it naturally raises the
threshold of physical maturity in terms of corpora number, as the ovaries associated with Purves and
Mountford's ear-plugs show.

(b) Five stages of fusion are recognized. (1) Some or all of caudal vertebrae unfused; lumbar and
thoracic vertebrae unfused. (1-2) Caudal vertebrae not seen; thoracic and lumbar vertebrae unfused.
(2) Caudal vertebrae fused; some or all lumbar vertebrae fused; thoracic vertebrae unfused. (3)
Caudal, lumbar and posterior thoracic vertebrae (11-15) fused; anterior thoracics unfused. (4)
Anterior thoracic vertebrae (3-5) fused. The material, classified into these stages, is set out in Table 5.

(c) In classifying the observations in this way it has been assumed first, that if a vertebra is recorded
as FJV then the eighth vertebra forward of it will certainly be unfused, and secondly, that if a vertebra
is recorded as UTC then the fourth vertebra posterior to it will still be unfused. These assumptions

ACCUMULATION OF CORPORA UP TO ATTAINMENT OF PHYSICAL MATURITY 389

Table 5. Progressive stages in the fusion of the vertebral epiphyses in
relation to corpora numbers
Stages of physical maturity

■\

Immature

Smoothed

No. of
corpora

, *

1\/Jatijre

r
I

1-2

Total

Immature

Mature

103

94-0

i-o

—

8V25

0-25

—

78-75

— ■

—

6175

—

49"25

—

47-75

■ —

—

44-75

0-25

33-25

i-o

24'5

2-25

24-0

3-o

22-5

4"25

i8-S

6-5

H75

6-75

—

J3-25

975

—

9-5

17-25

—

5-o

19-0

—

3"25

15-75

—

2-0

1375

—

175

1325

—

i-75

16-25

— .

—

i-o

1675

—

0-25

12-25

—

- —

—

10-25

—

1 i-o

—

1 1 75

—

0-25

7-5

—

o-5

9"25

—

0-25

8-75

3°

—

7-25

—

8-o

— .

—

7-0

—

4-0

— .

—

375

—

5-5

—

— ■

—

4'75

—

4-0

—

4-0

—

2-25

—

— ■

—

o-75

—

o-5

—

°"5

—

o-5

—

0-25

—

o-5

—

i-o

—

°-5

—

■ —

—

5°

—

■ —

—

— .

—

0-25

—

o-5

—

0-5

—

0-5

are based on the condition of the vertebral column in some 23 whales for which fuller records are
available, and enable the progress of fusion to be fixed more accurately.

For example, if only lumbar and/or caudal vertebrae are observed and lumbar 10 is FJV then
lumbar 2 (eight in advance) is assumed to be unfused, which puts this whale in stage 2. On the other
hand, if lumbar 15 is UTC then caudal 4 is assumed to be unfused, thus altering the classification
from stage 1-2 to stage 1.

Stages 1-3 are regarded as physically immature, stages 2 and 3 approaching maturity and stage 4
whales are physically mature. It should be noted that this represents the average progress of fusion
with completion of linear growth in the anterior thoracic region, but there are a few exceptional whales
in which fusion appears to be completed in the middle or posterior thoracic region. It should also be
pointed out that the determination of physical maturity is less easy and less certain than the identifica-
tion of immaturity because the latter is dependent on any one unfused epiphysis, whereas a whale
might be classed as stage 4, and therefore mature, although the posterior thoracics were still unfused.
However, the good correlation between number of corpora and the attainment of physical maturity
suggests that errors are actually small.

Table 6. Mean lengths of area II females in relation to numbers of corpora

No. of

Size of

Average

No. of

Size of

Average

corpora

sample

length

corpora

sample

length

133

669

73'1

107

687

73-2

69-9

73-2

70-6

72-6

71-1

73'°

72-2

73-°

72-0

72-8

72-9

74-2

72-6

74-0

73'1

>20

187

73-0

727

Total

1233

In Text-fig. 25 a smoothed curve indicating the increase in the mean length at increasing corpora
numbers is shown. This is based on 1233 sexually mature females taken in the antarctic area II, that
is, presumably from the same stock but over a period of years (Table 6). The mean length at physical
maturity in this sample is 73-0 ft. Purves and Mountford (1959) with a smaller sample from area I
obtained a figure of 72-9 ft. which is in close agreement.1 As they point out, their sample may contain
a mixture of populations (Brown, 1954), and the present sample is composite in respect of time.

For comparison with this curve of relative linear growth the frequency distributions of corpora
numbers at different stages in the progress of epiphysial fusion are also shown in this figure. The
' immature ' group includes stage 1 and 1-2 ; the group ' approaching maturity ' is composed of stages 2
and 3, and the physically mature group is stage 4.

The 'immature' group in which, it will be remembered, fusion has not progressed further than
the caudal region, corresponds to the period of fastest growth. The average growth is from 66-9 ft.
at one corpus luteum or corpus albicans to 72-5 ft. at the mid-point (8-5 corpora) where the ' immature '
group overlaps the group 'approaching maturity'. The average amount of subsequent growth to
maturity is only 0-5 ft. and is mainly confined to the thoracic region.

In Table 5 and Text-fig. 26 the smoothed frequency distributions of corpora numbers for physically
immature (stages 1-3) and physically mature (stage 4) females are drawn. These curves intersect at
14-3 corpora.

1 Their value for a small area II sample is much higher.

ACCUMULATION OF CORPORA UP TO ATTAINMENT OF PHYSICAL MATURITY 391

At the overlap there are 3 1 physically mature females with 14 corpora or less and 23 immature females

with 15 corpora or more. Considering these 54 individuals as a normal frequency distribution with a

mean value corresponding to the average number of corpora at the threshold of physical maturity, the

O 70

APPROACHING MATURITY

HTm

IS 20 25

NUMBER OF CORPORA

Text-fig. 25. Smoothed curve showing increase in body length with increasing corpora number, together
with frequency distributions of corpora numbers at progressive stages of epiphysial fusion.

IOO

>•
o

z> 50

PHYSICALLY IMMATURE
PHYSICALLY MATURE

15 20 25 30 35

NUMBER OF CORPORA

Text-fig. 26. Smoothed frequency distributions of corpora numbers in physically
immature and physically mature females.

mean is 14-0 with a standard deviation of 3-94. This is slightly lower than the value at the intersection
point (14-3) and is influenced by the effect of mortality on the populations from which the sample is
taken. The effect of mortality would be to steepen the right-hand part and to decrease the slope of the
left-hand part (as in Text-fig. 27), so that the intersection point is a slightly better indication of the
mean number of corpora on the attainment of physical maturity. A further confirmation of the close-

392 DISCOVERY REPORTS

ness of the correlation is that, of 53 individuals with 14 or 15 corpora, 26 are physically immature
and 27 are mature.

The mean number of corpora at physical maturity is now concluded to be 14-3, and is in close
agreement with the findings of Wheeler (1930) and Peters (1939), which were based on smaller samples.

Comparisons between the number of corpora in young age groups

and at physical maturity
In Text-fig. 27 the frequency distributions of corpora numbers at baleen group V (mean number 5-6)
and at the threshold of physical maturity (mean number 14-0) are illustrated. For comparison both
curves have been converted to percentage frequencies for there is a great discrepancy in the size of
the samples. The curves are based on 405 females in baleen group V and only 54 at the threshold of
physical maturity. They have been arranged so that the modal number of corpora (5 in the case of
baleen group V, and 14-3, the intersect, in the case of the group at physical maturity) corresponds to
o and the corpora numbers have been converted to values relative to the mode. It is then apparent
that the frequency distributions are very similar in shape, the agreement between the right-hand
parts of the curves being particularly close. The discrepancy between the left-hand slopes is largely
due to the truncation of the group V frequency curve as mentioned above (p. 386). The standard
deviations for the curves are 3-30 for group V and 3-94 at physical maturity, and they are in reasonably
close agreement. If the two extremes in the frequency at physical maturity (at 1 and 28 corpora) are
eliminated the standard deviation becomes 3.00.

We may conclude that the range of variation in corpora numbers at baleen group V is similar to
that obtaining at the threshold of physical maturity. It has been suggested that baleen group V
includes several year classes and cannot, therefore, represent the range of variation at one specific
age, which must be less than this sample shows. Similarly, the group at physical maturity is unlikely
to represent a single year class, or even a single age class relative to sexual maturity, but it is not possible
to say over how many year classes it is spread and therefore impossible to estimate the probable
increase in variation by comparing these two samples.

It would seem to be clear, however, from the small variance at the threshold of physical maturity
that there is little variation in the average number accumulated annually by individual whales. In the
simplest case linear growth is a decelerating process which begins before sexual maturity and ceases a
number of years later. The corpora accumulate annually and the range of variation in the number
present at the threshold of physical maturity depends first, on the individual variation in the age at
sexual maturity, secondly on the time taken to reach physical maturity and thirdly on the cumulative
variation in the annual production of corpora. In this case there can be very little individual variation
in the average annual rate of corpora production, because almost all the variation can be accounted for
by the age spread at puberty (see below, p. 407). This argument assumes that the accumulation of
corpora and ossification of the epiphyses are independent physiological processes. It should be pointed
out, however, that oestrogen production (by follicles, corpus luteum and placenta) is associated with
each ovulation and pregnancy. One of the biological actions of oestrogens is to delay the ossification of
epiphyses in mammals, so that the number of such cycles might well have a direct effect, independent
of chronological age, on the attainment of physical maturity. According to this hypothesis females
ovulating less frequently than the average would attain physical maturity at an earlier age than those
with a higher rate of ovulation, and the frequency distribution of corpora at the attainment of physical
maturity might be very similar to that obtained in the present study. If there is such a direct correla-
tion between rate of ovulation and age at maturity then the amount of variation at physical maturity
will nevertheless reflect the extent of annual variations between individuals.

ACCUMULATION OF CORPORA UP TO ATTAINMENT OF PHYSICAL MATURITY 393
Probably neither hypothesis alone is entirely correct and the actual mechanism is likely to be very
complicated. In the absence of a sufficiency of marked whales of known age it is unlikely that a
satisfactory explanation can be found, but the available evidence suggests that there is a very regular
annual increment of corpora in individuals and that the variation in the number of corpora at the
threshold of physical maturity is mainly influenced by the spread in the ages at which sexual and
physical maturity are attained, and partly by the variation in the annual production of corpora in
individuals.

>
o

111

w
&

z
u
o

<£

<= BALEEN GROUP 3£
— PHYSICAL MATURITY

-8

-5 -4 -3 -2 -I O +1 +2 +3 +4 +5
RELATIVE NUMBER OF CORPORA

+7 +8

Text-fig. 27. Frequency distribution of corpora at two stages of the life-cycle compared.

The fact that, despite the possible sources of error in the collecting of the data, there is so good a
correlation between corpora accumulation and physical maturity points to a rather regular annual rate
of accumulation of corpora. This is difficult to account for if the female fin whale is polyoestrous
with an average of three ovulations (representing a range of say 1-6 ovulations) per breeding season.
This individual variation in the rate of ovulation would alone account for the variance in the number
of corpora at physical maturity, without taking account of the age spread at sexual and physical
maturity or the possibility of human error. Chittleborough (1955 b, p. 56) presents data which strongly
suggest that ' the mean number of ovulations per female humpback during the ovulatory period was
only slightly above one'. But if, as seems likely, some two laminations of the ear-plug represent one
year (Laws and Purves, 1956; Nishiwaki, 1957; Purves and Mountford, 1959) then the female
humpback accumulates about 2-4 corpora on average during each 2-year breeding cycle (Symons and
Weston, 1958). That is to say, there is more than one ovulatory period. It has been shown above
that newly mature female fin whales, which might be expected to be less successful breeders than
multiparous females, have on average only 1-42 ovulations (range 1-4) before becoming pregnant.

In the following sections the reproductive cycle of the fin whale is re-examined in order to find an
explanation of the regular rate of ovulation and it is concluded that the female fin whale is probably
not polyoestrous as has been assumed by all previous workers. A preliminary announcement of this
finding was made in 1956 (Laws, 1956a).

9-2

394 DISCOVERY REPORTS

THE REPRODUCTIVE CYCLE

Introduction

The framework of the study of the reproductive cycle of the fin whale was laid down by Mackintosh and
Wheeler (1929) in their classic work on blue and fin whales, and most of their conclusions still stand.
They showed that the season of pairing and parturition extends over a protracted period in the southern
winter with a peak in June and July ; that pregnancy occupies about 1 1 months ; and that a lactation
period of about 7 months was usually followed by a resting period lasting until the next pairing
season, so that there is usually only one pregnancy in 2 years. They did, however, note that exception-
ally two pregnancies may follow in quick succession as a result of a successful post-partum ovulation
in early lactation.

Mackintosh (1942), in summarizing work up to that time, found no reason for altering these initial
conclusions as to the interval between pregnancies, but drew attention to a marked increase in the
percentage of pregnant females and suggested that this might represent a reaction to whaling. He also
stated that there was some evidence that females simultaneously pregnant and lactating were less rare
than formerly. He discussed the growth to sexual maturity and concluded that ' while the estimate of
two years as the normal period from birth to sexual maturity is not proved, it is unlikely to be more
than three years ' (p. 225). The evidence on which this conclusion was based was mainly the incidence
of unweaned calves and modes in the length frequency distribution of immature whales (Mackintosh
and Wheeler, 1929) ; on the distinction of separate sets of scars indicating migrations in young whales
(Wheeler, 1930) ; and on the recovery of a single female fin whale marked as a calf, which 3 years later
was much larger than the mean length at sexual maturity.

This estimate of the average age at sexual maturity was later revised to 3 and then 4 years as a result
of age-determinations made on baleen plates (Ruud, 1940, 1945; Nishiwaki, 1952; Hylen et al. 1955)
and as a result of the study of the ear-plug to 5-6 years (Purves and Mountford, 1959).

There is now reason to believe that the average age at sexual maturity, although about 5 years
in this species is not fixed, but varies slightly with the condition of the stock (Laws, in press)
perhaps acting through the food supply. Among wild mammal populations this is perhaps best
documented for deer on ranges of differing carrying capacity (Morton and Cheatum, 1946; Cheatum
and Severinghaus, 1950). Laws (19566) has suggested that this may be the result of a higher
level of nutrition stimulating bodily growth so that the size threshold for reproduction is reached at an
earlier age. It is, therefore, unwise to assume that either the average age or the average length at
sexual maturity are unvarying. As regards the length at sexual maturity, Mackintosh (1942) revised
slightly the original estimate of Mackintosh and Wheeler (1929) of 65-57 ft- f°r area H females to
65-24 ft., mainly for samples also from area II. Brinkmann (1948) whose material was also mainly
from area II obtained a figure of 65-35 ft- These estimates are all in close agreement. Mackintosh
(1942) gave 63-0 ft. as the mean length of male fin whales at sexual maturity.

Mackintosh (1942) discussed the important question as to whether whales are monoestrous or
polyoestrous. He concluded that ovulation is spontaneous and that, although the evidence is not
conclusive, it strongly suggests that whales are polyoestrous. He remarks : ' If it were found, contrary
to expectation, that whales were in fact monoestrous, the determination of age from corpora lutea
numbers would of course be enormously simplified' (p. 222).

Chittleborough's (19556) data on the humpback whale suggest that in the great majority of indivi-
duals there is only one ovulation during the ovulatory period, but that this is a case of later poly-
oestrous cycles being suppressed because the first ovulation is successful, so that it is effectively
monoestrous. However, there is evidence (p. 393) that in the humpback whale there are on average

THE REPRODUCTIVE CYCLE 395

probably two to three ovulations per 2-year cycle, which means, if correct, that there must usually
be more than one ovulatory period in the course of the 2-year cycle. Chittleborough is the only
worker who has been able to carrv out extensive studies on a large whalebone whale in low latitudes
during the winter, that is near the breeding grounds during the breeding season. His direct observa-
tions confirm the inferences about the breeding season and gestation period of humpback whales
made from records of foetal lengths (e.g. Matthews, 1937). This is encouraging and suggests that
such an approach should give fairly accurate results for other species (Laws, 1959a).

It has been necessary in parts of the following account to draw analogies with other mammals, but
owing to the practical difficulties of verifying such points as, for example, the duration of the corpus
luteum of the cycle in the whale, this approach is unavoidable.

The sex ratio

Mackintosh (1942, tables 21 and 22) gives records of the sex of 13,379 fin-whale foetuses and
119,385 post-natal fin whales. The foetal records show a significant difference in the proportions of
the sexes (52-0% male, s.e. of the percentage 0-19), and the other records show an even greater
preponderance of males (54-5%, S.E. of the percentage 0-02).

. The interpretation of the second figure is difficult. Lactating females are under-represented on the
antarctic whaling grounds and, as their taking has been prohibited for many years, even less well
represented in the catch. Conversely, there has probably been some selection by the whalers of
females because of their larger size, and the minimum size limits give greater protection to the males
(see Laws, i960). Mackintosh (1942, p. 267) concludes that there are slightly more males than
females.

The breeding season

The breeding season is here defined as the period of pairing and parturition. Since pregnancy extends
over almost a year these two activities take place at the same season of the year. It is clear from the
wide variation in foetal lengths in any one month that it is a protracted period. In fact, conceptions
occur and calves may be born in almost every month of the year, but most of this activity is confined
to a relatively short period. There are several methods by which we can obtain an estimate of the
monthly frequency of pairing.

The male reproductive cycle

The mating season depends to some extent on the cycle of activity of the males. Thus if, in the male,
rut is short and well-marked, the season of pairing will probably also be well-defined and the season
of parturition limited. This relationship is very clear in the pinnipedia, in some of which the pairing
season is confined to two months or less (Laws 1956c).

In investigating the male reproductive cycle of fin whales little direct evidence is available because
of the inaccessibility of the breeding population and we must resort to indirect methods (as in the
case of females).

Histological evidence

One method is to attempt to distinguish a cycle of activity in the gonads, but here again there are
difficulties. A point which has not perhaps been sufficiently emphasized by previous workers is that
the epithelium of the seminiferous tubules is more sensitive to post-mortem changes than most other
tissues. These changes often take the form of extensive desquamation, of at least the superficial
layers, which is similar to natural and experimentally induced testis degeneration.

In most pelagically caught animals the time from death to the examination is about 5-10 hr. and

396 DISCOVERY REPORTS

whales under 3 hr. post-mortem are rare on factory ships or land stations. The insulating layer of
blubber probably accelerates post-mortem changes. Chittleborough has studied the histology of
humpback-whale testes from animals in breeding condition, but the material shows signs of post-
mortem degenerative changes, with the result that even his material does not present a clear picture
of full spermatogenesis (Chittleborough, 19556, PI. 1, fig. 4). In most cases it has been found possible
to diagnose a male in full breeding condition or in complete anoestrus, but it is not possible to describe
the more gradual histological changes accompanying the approach to or regression from full breeding
activity as was possible with well-fixed material collected from seals immediately after death (Laws,
1956c). A preliminary examination is sufficient to show that most male fin whales examined in the

MONTHS

250

200

5
<

150

IOO

S AFRICA

ANTARCTIC

J A S

MONTHS

Text-fig. 28. Annual cycle of testis activity in the male. Above, activity expressed as arbitrary scale of values, based on
histological appearance; below, measurements of mean diameters of seminiferous tubules; from Antarctic and South Africa.

Antarctic are in full anoestrus, but there are some individuals in which the seminiferous tubules present
a more active picture.

Since detailed histological examination and description is not rewarding, a subjective classification
into five arbitrary stages of activity has been made using the sectioned material on which Mackintosh
and Wheeler (1929) based their account of the male cycle. This includes 86 specimens, mostly from
January and February, but including all months except June. On the basis of the overall microscopic
appearance the material has been divided into five classes — o, 1, 2, 3 and 4, ranging from complete
anoestrus to full activity. The monthly mean according to this scale of values has been calculated and
the results are set out in Table 7 and Text-fig. 28. Almost all the pelagic material collected in recent
years is from January and February and the great majority of specimens fall into group o as in the
earlier material ; it has not, therefore, been included.

THE REPRODUCTIVE CYCLE 397

Smears of testes and epididymides from 17 mature fin whales were examined by A. H. Laurie
and F. D. Ommanney at Durban, South Africa (unpublished work). This material was collected in
June, July and August and spermatozoa were present in all except two specimens.

Table 7. Arbitrary classification of testis samples according to activity

Arbitrary classification

* , Arbitrary

1234 mean

3 2 0-4

Sample

Month

size

January

February

March

—

April

—

May

—

June

—

July

—

August

—

September

—

October

November

—

December

—

Total

2 — 0-2

I — 2

I — 2-2

4-oj

1 3-0

4 2'0

2 2 I 1-8

2 — — — 07

3 2 1-4
2 1 — 1-3

13 12 8 3

From this examination it appears that the period of maximum testicular activity extends from about
April to July or August with peak activity probably in May and June, and it is at a minimum in
January and February. Owing to the scarcity of material from March to October it is not possible
to say more than this.

Variations in the diameter of the seminiferous tubules

Individuals of many species of mammals show a seasonal cycle in the diameter of the seminiferous
tubules, correlated with histological changes in the contents of the tubules (Laws, 1956c). The
seminiferous tubules are narrow in anoestrus, enlarge just before the breeding season and shrink again
afterwards. Whales might be expected to show a similar cycle of growth and regression, but the full
extent of these changes appears to be masked by the amount of chronological variation in the indivi-
dual cycles. Chittleborough (19550) for instance, could demonstrate no change in testis weight or in
the diameter of the seminiferous tubules of humpback whales taken over a period of 4I months from
June to October, but Omura (1953) and Symons and Weston (1958) found the testis weight to be lower
in antarctic specimens than those in Chittleborough's sample. These authors also state that the testes
of humpback whales taken in February present an inactive appearance when examined histologically.

As explained above, whale testis material is often badly fixed and shows degenerative changes. In
measuring the diameter of the seminiferous tubules only material which showed no obvious shrinkage
of the tubules has been accepted. This limits the material to samples from 95 mature male fin whales,
the histological appearance of the tubule contents being the criterion of maturity adopted. As the
testis of males approaching puberty probably presents an appearance similar to that in inactive
mature males, it is possible that some immature males have been included inadvertently, but these are
unlikely to have much effect on the general conclusions.

For each of these 95 whales the mean tubule diameter was calculated from a random sample of
20 tubules, except for a small minority in which only 10-15 were measured. Measurements were
made with a graduated scale on projected histological sections and only roughly circular tubule
sections were measured across two diameters at right angles ; this helped to make the samples random
and ensured that the full tubule diameter was measured.

398 DISCOVERY REPORTS

Table 8. Summary of records of the diameter of seminiferous tubules of
antarctic male fin zvhales by months

Month

Mean
diameter (ji)

Range (ft)

Sample
size

October
November

164
154

144-183

110-188

7
22

December

155

126-179

January
February
March i

H3
140

99-199

1 1 2-200

30
16

April -
May J

165

1 3 1-24 1

The results are shown in Text-figs. 28 and 29 and summarized in Table 8. Taking first the antarctic
samples it will be seen that, although there is a wide range of variation in tubule diameters, the monthly
mean value progressively declines from 164// in October to 140// in February. This continued
decrease in the tubule diameter strongly suggests that the testes of male fin whales taken in the
Antarctic from October to February are regressing following a season of activity at an earlier period.
Clarke (1956) found a closely similar decrease in monthly mean tubule diameters in male sperm whales
taken in the vicinity of the Azores (from 161 // in June to 134/^ in September and 144 fi in October).

After February there is apparently an increase in the tubule diameters. The monthly mean for
March is 208 fi, but this is probably too high, being the average of only two whales, and probably over-
influenced by the high value for one of them (tubule diameter 241 //, the largest tubule diameter
measured). The lower of these two values (tubule diameter 175 //) was from a specimen in which the
tubules were in early spermatogenesis and, therefore, probably enlarging prior to the breeding season.
The other specimen had a number of degenerating spermatids in the lumen and may have been either
approaching rut, or immediately post-rut. An observation of the extent of diatom infection might
have helped to place this very interesting animal (see below), but unfortunately no notes were made
on this point in the field. If the seven specimens for March, April, and May are taken together they
suggest a mean diameter of about 165 /i in April.

Turning now to the testis tubule diameters for the eight mature males from Saldanha Bay, South
Africa, taken in July, August and September (Text-fig. 28) it will be observed that only two have
tubules above 140 ju in diameter, which is very much lower than expected. These few specimens
suggest a possible decline in tubule diameter over this period but the August and September means
are below the lowest monthly mean values in the antarctic samples. Referring again to the arbitrary
scale of testis activity based on the histological appearance of the seminiferous epithelium it will be
seen that these testes from July, August, and September are more active than those from later months.
The most probable explanation of the discrepancy is that the post-mortem and post-fixation treatment
has been different, and has produced greater shrinkage in the South African material. It will, how-
ever, be remembered that only fin-whale material showing no obvious shrinkage has been used. It is
relevant to note that the frequency distribution of humpback-whale tubule diameters, measured by
Chittleborough (1955a, fig. 10), is almost the same as that for fin whales. These are compared in
Text-fig. 29 A and C, and it will be noticed that two fin-whale values are higher than the highest value
for humpback whales. The present material was Bouin-fixed or formol-saline fixed whereas Chittle-
borough's material was fixed in Susa or formol-saline. The different fixation should not in itself
produce very marked differences in shrinkage, and most shrinkage occurs in pre-embedding prepara-
tions (Baker, 1958). Symons and Weston (1958) also give a mean tubule diameter for a sample of

THE REPRODUCTIVE CYCLE 399

eleven humpback whales taken in February which is higher than that for Chittleborough's sample.
In fact the maximum diameter they found was 290 11 which seems very high, but their sections were
cut from frozen material without embedding, so the shrinkage would be expected to be much less
than in paraffin-embedded material. We are comparing here anoestrous fin and humpback whales with
humpback whales in rut and one would expect the latter to show much higher values with identical
treatment.

In pinnipeds of at least four widely different genera the tubule diameters in rut are about 220 11 and
shrink to less than 140^ in anoestrus (Laws, 1956c, fig. 7; McLaren, 1958, fig. 3; Mansfield, 1958,
fig. 15). The antarctic fin-whale material suggests that there is a similar range in whales. In this
material anoestrous tubules are about 140// in diameter (Text-fig. 28) and the largest measured
(241 11) was either approaching rut or taken immediately after.

250

200

150

100

0 510 15 2005 O
FREQUENCY

IO 15 20

Text-fig. 29. Measurements of seminiferous tubules. A, humpback whale, West Australia; B, fin whale, South Africa;
C, fin whale, antarctic; D, E, and F, means ± 20- and s.e. for antarctic fin whales classified as to diatom infection; D, recent
arrivals; E, heavy diatom infection, South Georgia; F, heavy infection, antarctic pelagic.

It seems probable then that the fin-whale material from South Africa and the humpback-whale
material from Australia has undergone much greater shrinkage than the antarctic material, so that
the testis tubule diameters cannot be directly compared. It is also possible, however, that the South
African material gives a true picture, relative to the antarctic material, and that there is a decrease
in average tubule diameter from July to September, followed by an enlargement associated with the
southward migration. This possibility is discussed later (p. 453). It seems clear, when the evidence
is combined, that there is a very definite cycle of activity in the male fin whale. It should be noted
that the bulk of the fin-whale population is in the Antarctic during the months covered by the samples
because at this time they must feed in antarctic waters (Mackintosh and Brown, 1956, fig. 2; Marr,
1956). It can safely be assumed that, so far as it goes, the material gives a true picture of the male
sexual cycle.

The individual rate of regression in tubule diameter is actually greater than Text-fig. 28 suggests,
because of the smoothing effect of the continued arrival in the Antarctic of males from lower latitudes.
Even in January and February there are some males with seminiferous tubules about 200 p in mean
diameter and it seems likely that these are recent arrivals. Is there any way of confirming this? Hart
(1935) showed that the presence of a thick diatom film on the surface of the body can be taken to
indicate that a whale has been in antarctic waters for at least a month, and conversely, the absence

4oo DISCOVERY REPORTS

of a diatom film or the presence only of small patches on the jaw is characteristic of whales which have

only recently entered the colder waters.

Records of both the extent and heaviness of diatom infection and of the mean diameter of the
seminiferous tubules, are available for a number of fin whales from South Georgia and the pelagic
whaling grounds. When doubtful cases have been eliminated the sample for which precise information
is available is reduced to only 43 male fin whales.

Table 9. Summary of information on the diameters of the testis tubules of 43 male fin zvhales

classified by means of diatom infection

Heavy diatom

Recent arrivals

South Georgia

Pelagic

Sample size

Mean diameter (/<)

173

152

140

Range

(149-201)

(127-183)

(119-171)

1973

18-64

15-40

S.E.

5-20

4-98

3-85

For 13 recent arrivals with little or no diatom infection, the mean tubule diameter is 173 /^; for
fourteen whales taken at South Georgia with heavy diatom infection which had, therefore, been in the
Antarctic for several weeks the mean tubule diameter is 152//. For 16 with heavy diatom infection,
taken pelagically much further south, which had presumably been in colder water even longer than
the last group, the mean tubule diameter is 140//. There is a similar range of variation in all three
samples (Table 9), suggesting that the rate of regression is fairly constant.

These mean values plus or minus za and 2 s.e. are shown in Table 9 and Text-fig. 29 D-F, and
it will be seen that the mean values for the tubule diameter in recent arrivals and in animals which
have been south of the antarctic convergence for some time are significantly different. These values
may be compared in the same figure with the frequencies of tubule diameters in the larger unclassified
sample (Text-fig. 29 C). There are two modes in this frequency distribution, the higher of which is
now seen to correspond to recent arrivals in the Antarctic in which the tubules are still shrinking, and
the lower mode represents males in which the tubules are almost fully regressed. The mean diameter
of fully regressed tubules in mature fin whales is probably about 140 /i, for material fixed and embedded
in this way. The last phrase is an important qualification.

These results may be compared with the mean diameter of the testis tubules of 13 immature fin
whales, which is 79 /i (range 47-113 //). This is almost identical with the findings of Chittleborough
(1955a) for the humpback whale and close to the figures given by Clarke (1956) for the sperm whale.
One specimen, taken in October, which appears to be approaching puberty has a mean tubule
diameter of 102// (open tubules 122 fi; closed 82//), which is again close to Chittleborough's figures.
It is difficult to reconcile this with the apparent extensive shrinkage of the tubules of mature hump-
back whales in rut, but whether this shrinkage is postulated or not, it does not affect the general
conclusions given below.

This brief discussion of testis histology is sufficient to establish that there is an annual cycle of
testis activity in the male fin whale. The season when the majority are in active spermatogenesis
probably extends over the period April-September, with most activity in April, May, June and July.
It is in these months that the majority of conceptions should occur. Nevertheless, the presence of
some males in January, February and March which have testis tubules up to 200 ft in diameter
suggests that successful pairings can occur in almost any month.

THE REPRODUCTIVE CYCLE 401

The follicular cycle in females

The cycle of follicular activity in female fin whales has been discussed in an earlier section of this

paper. In adult females there are usually large numbers of resting or regressing follicles, often of

large size, and this makes any attempt to demonstrate a cycle of follicular activity difficult owing to the

limited period for which data are available.

This difficulty can be overcome by considering only the size of the largest follicle in fin whale

females approaching puberty. In the present material there are 62 pairs of ovaries from immature

females at this stage of the life-cycle, and the results obtained were described on pp. 346-47, Table 2,

and Text-fig. 3. It was concluded that immature females ovulate for the first time between June

and November (possibly also December) and that from January to May the ovarian activity is at a

minimum. It will be shown (p. 411) that the annual cycle of immature females is retarded relative

to that of mature females and this evidence, therefore, supports the inferences about the season of

pairing drawn from evidence from the male cycle and from a consideration of foetal lengths (see

below).

Pregnancy and foetal growth

If the rate of foetal growth is known with reasonable accuracy then it should be possible to obtain an
estimate of the frequency distribution of pairings and conceptions by examining the foetal length
records, as was done by Mackintosh and Wheeler (1929, pp. 426-7) for blue and fin whales. However,
small errors in the estimated curve of foetal growth can lead to quite large errors in the calculation
of the frequency distribution of conceptions. For this reason it is necessary to obtain an average curve
of foetal growth which is reasonably accurate, before going on to use this to determine the monthly
frequency of pairing. It is also necessary to show to what extent the length frequencies of foetuses
in the sample examined may be taken to be representative of the foetal length frequencies in the
population sampled, and the extent of the differences, if any.

In a recent paper (1959 a) I reviewed earlier work on the problem and went on to examine the rates
of foetal growth in three Odontocete species and five Balaenopterids. The material for the fin whale
included length records of 956 foetuses from South Africa (5), South Georgia (268) and from the
pelagic whaling grounds (683). I found that the method developed by Huggett and Widdas (195 1)
for dealing with foetal length and weight data appears to hold good for the Odontocete species
studied and to a limited extent for the Balaenopterid species. In particular this method provides
for an objective estimate of the length of the initial period of very slow growth (before the placental
circulation is fully established?) which is impossible by means of freehand extrapolation. In the
Balaenopterid species growth after this initial period is linear as in the Odontocetes, but unlike this
group, the phase of linear growth appears to be superseded by a phase of exponential growth in the
second half of pregnancy. My (1959 a) conclusions about foetal growth in length in the fin whale are
presented and summarized in Table 10 and Text-fig. 30, and the original paper should be consulted
for further details. The average duration of gestation in this species is estimated to be n J months
(early June to mid-May). This evidence of the mean date of pairing agrees very well with the evidence
from the male sexual cycle and reasonably well with the ovarian cycle in females approaching puberty.
It is shown below (p. 41 1) that the beginning of pregnancy in primiparous females is later than the
average date of conception in multiparous females.

The explanation of the relatively large variation in the foetal lengths in the monthly samples is
undoubtedly that the pairing season both for primiparous females and multiparous females extends
over several months, as will be shown below.

The frequency distributions of foetal lengths in the monthly samples were examined in the above

402 DISCOVERY REPORTS

paper (Laws, 1959 a) and it was shown that the samples taken in the Antarctic in the period of 5 months
from October to February may be considered to be representative of the progress of foetal growth,
but that differential migration out of the area affects the validity of the samples from March onwards.
A similar differential migration into the area in spring means that very early embryos (less than one
month post-conception) will tend to be absent in antarctic samples. The effect of this would be most
marked in the earlier months, prior to November, for which in any case very few length records are
available.

It is estimated that, in addition to the 956 foetuses recorded in Table io, little more than 50 (some
5%) would have to be added to the lower size groups of the frequency distributions for October and

J JASONDJ FMA

MONTHS

Text-fig. 30. Mean curve of foetal growth and monthly foetal length frequencies of southern
hemisphere fin whales; class interval 0-2 m.

November, and the higher size groups of the March and April samples, to overcome this bias. The
effect of this small error on the frequency distribution of pairing, which is now to be calculated, means
that the pairing frequencies for the early months of the breeding season and for the late months will be
slightly under- rep resented. This is thought to have a negligible effect on the shape of the pairing curve.
The effect of individual variation in growth-rates must also be considered. Zemskiy (19500) states
that male and female foetuses grow at different rates. Kimura (1957, p. 113) studied the difference
in length between twins of different sexes, but found that in 57 % of cases there was no difference,
and the remainder were almost equally divided between pairs in which the female was larger and pairs
in which the male was larger. No distinction as to sex need, therefore, be made in studying foetal growth.
We are concerned here with the average growth of large numbers, so individual variations in the
growth-rate need not be considered in drawing up an average growth curve. When foetal lengths are

THE REPRODUCTIVE CYCLE 403

Table 10. Growth in length of southern hemisphere fin-whale embryos

Size of

Mean

Fitted

Month

sample

length (tn.)

2 S.E.

curve

12 June

—

o-oo

Mid-July

—

o-io

Mid-August

—

0-30

Mid-September

—

o-55

Mid-October

0-809

0-I58

0-80

Mid-November

1-069

0-128

1-07

Mid-December

142

1-377

0-I2I

i-33

Mid-January

271

1-775

0-II2

1-82

Mid- February

284

2-620

0-I28

2-55

Mid-March

165

3-056

0-188

3-4°

Mid-April

4-128

I>154

4-70

Mid-May

—

6-40

Total

956

—

used to determine the pairing season, individual variations will have the effect of slightly extending it.
It should be noted that this effect tends to cancel out the effect produced by the under-representation
of very small embryos and very large foetuses in the sample.

It has now been shown that, for the purpose of establishing the frequency of conceptions in the fin
whale, the foetuses for which data are available (956 in number) may be taken to be a representative
sample. For the reasons given above any errors are likely to be small.

The pairing season and the season of parturition

The evidence which has been considered above strongly suggests that the majority of pairings in the
southern hemisphere fin whale take place during the period April-July. It is now possible to obtain
a more precise idea of the relative frequency of pairing by examining the foetal length data, using the
method employed by Mackintosh and Wheeler (1929, p. 427, fig. 146).

First, the 956 foetal lengths were plotted according to the dates on which they were taken. The mean
curve of growth in foetal length (Table 10, Text-fig. 30) was then drawn and similar curves constructed
at lateral intervals of one month. The foetuses which lie between two of these growth curves can then
be referred to the monthly periods in which they were conceived. The effect on the results of uneven
sampling and individual variation in the rate of growth have already been discussed (p. 402) and it was
concluded that these influences tended to neutralize each other.

All the foetal length records have been referred to the various monthly periods of conception, for
example 12 June- 11 July, and the frequency distribution of conceptions, determined in this way, is
shown in Table 11. The actual frequencies have been converted to percentage frequencies and are
plotted graphically in Text-fig. 31. It will be seen that although 12 June is estimated to be the mean
date of conception, the distribution of pairings about this mean date is not symmetrical, but skewed,
so that the modal frequency occurs earlier than the mean. This curve of the frequency of pairing is
in close agreement with the conclusions reached from consideration of the male sexual cycle, and of
the ovarian cycle of females near puberty. It is estimated that 77% of foetuses are conceived in the
4 monthly periods between April and August; only about 14% of all foetuses are conceived in the
7 monthly periods from September to April, and only about 6% in the 5 months between October
and March. This demonstrates that there is a limited season in the female extending over 4-5 months
during which most conceptions occur, but it will be noted that some foetuses may be conceived in
every month of the year except February.

4°4 DISCOVERY REPORTS

It has already been shown that the duration of the gestation period is about n| months. A curve
showing the seasonal distribution of calving has, therefore, been constructed by advancing the curve
of conceptions by 3 weeks (Text-fig. 31).

So far we have been concerned with the pairing season averaged from data collected over a number
of years. It would be interesting to know the possible variation in the timing of the pairing season from
year to year.

Text-fig. 31. Monthly percentage frequency of pairing (full line) and calving (broken line) of 956 pregnant females.

Table 11. Estimated frequency of conceptions in southern hemisphere fin whales,
based on 956 records of foetal length

Conceptions

Monthly period

No.

Percentage

January/February

February/March

o-i

March/April

2-4

April/May

196

20-5

May/June

249

26-0

June/July

180

18-8

July/August

116

I2-I

August/September

8-5

September/October

5-4

October/November

3-8

November/December

i-8

December/January

°'5

Total

956

99-9

Our material collected by biologists is inadequate for this purpose, but there is information on
foetal lengths of fin whales in the International Whaling Statistics covering the period 1925-58 and
comprising many thousands of records. These measurements are not as accurate as those made by
biologists which were used to elucidate the curve of foetal growth and the average pairing season.
As Brinkmann (1948) has pointed out, small foetuses tend to be missed so that in the earlier months
the mean foetal lengths given in the International Whaling Statistics are higher than expected in a
true sample. However, we are interested in relative differences from year to year and the absolute
lengths are not important in this connexion.

In Text-fig. 32 the mean monthly foetal lengths given in the International Whaling Statistics have
been converted from feet to metres, and are plotted against the respective whaling seasons. The records

THE REPRODUCTIVE CYCLE 4°5

for 192=5-30 are averaged and there is a gap between 1940 and 1945 corresponding to the reduced
whaling activity during the war. Only 4 months (December-March) are considered, because the
samples from other months are small, and no mean value is given for December 1932 because there
were only eight individuals in this sample. From 1934 onwards the samples are large (usually from
a hundred to over a thousand).

It will be seen that in the three decades covered by the material there has been no significant
progressive change in the mean monthly foetal lengths for December and January. The values for
March and perhaps February suggest that the rate of foetal growth may have increased slightly. There
have, however, been variations from year to year, although the pattern of the curves for the different
months is not always the same, indicating that some of these variations are not significant. There are
seasons when monthly mean foetal lengths deviate significantly from the monthly mean for the whole

z
<

3 -

2 -

I -

OA — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — i — 1
1925 1930 1935 1940 1945

YEARS

Text-fig. 32. Variation in the mean monthly foetal lengths over the period 1925-58 (from International

Whaling Statistics, Sandefjord).

period. In January 1935 and February 1953 for instance, where there is a large deviation from the
overall mean for the period, the calculation of the mean ±2 S.E. shows that these particular values
deviate significantly by more than 0-25 m. and about 0-5 m. respectively, from the means for the full
period.

Deviations of this order could represent displacements of the mean date of conception of about
i-2| weeks (from Text-fig. 30), but a number of complicating factors need to be considered in
assessing this temporal deviation. Have there, for instance, been any changes during this 30-year
period in the rates of foetal growth ? Have changes in the age structure of the populations of mature
females been sufficient to produce an apparent change in the pairing season? It is not possible to
provide conclusive answers to these questions, but such changes would probably be progressive and
would not account for variations from year to year. It may be that a slight increase in the rate of foetal
growth, and a shift towards lower ages in the age structure of the mature females, could produce an
apparent advancement or retardation of the pairing season.

On the evidence available it seems probable that there has been no progressive change in the pairing

406 DISCOVERY REPORTS

season, and that annual variations in the mean date of pairing have been within the extreme range of
±2^ weeks, during the period for which data are available. It is possible that variations in the spatial
distribution of the catches are partly responsible for these fluctuations, that is to say, the timing of the
pairing season or the foetal growth-rate may be slightly different in the different oceans, but it seems
more likely that climatic factors are at work. A year when pack-ice was late in retreating might retard
the southward and northward migrations and delay the pairing season. Dawbin (1956) has shown that
at Cook Strait, New Zealand, the mid-point of the northward migration of humpback whales is 5 July.
In 36 seasons the maximum variation has been from 21 June to 29 July, that is about 5 weeks. This
is in quite close agreement with the conclusions about the annual variations in the monthly mean
sizes of fin-whale foetuses. It is a problem which might well repay further study.

Sexual maturity
Strictly speaking the term sexual maturity should be applied to the peak period of reproductive
performance when fertility and reproductive rate are at a maximum. In the literature on whales the
attainment of sexual maturity is understood to refer to that part of the life-cycle when females first
ovulate and males first produce sperm. Although it thus corresponds more accurately to puberty,
because of its wide use the term sexual maturity is retained here, although it is not strictly correct.

The mean length at sexual maturity

Various estimates of the length at the attainment of maturity of female southern hemisphere fin whales
have been made, all of which correspond rather closely. Mackintosh and Wheeler (1929) estimated
the mean length of the female at sexual maturity to be 65 ft. 7 in. This was later amended by Mackin-
tosh (1942) to 65 ft. 3 in., using the same data as well as additional records accumulated up to 1941.
Brinkmann (1948) concluded that the mean length at sexual maturity is 65-66 ft.

Estimates of the mean length of the female at sexual maturity made by Japanese workers range
from 67 to 68 ft. (Nishiwaki, 1950; Nishiwaki and Hayashi, 1950; Nishiwaki and Oye, 1951), but the
figure of 64 ft. given by Nishiwaki (1957, p. 30) does not agree with these earlier estimates. The
apparent discrepancy between the results of Japanese and European workers is accounted for by the
fact that the former take the average length at sexual maturity as the length when 75 % of females are
sexually mature. (Their reasons for this procedure are not clear.) When recalculated by taking the
length at which 50% are mature and 50% immature, the mean length is seen to be about 65 ft.
(Nishiwaki, 1950, fig. 226) and conforms closely with the other estimates obtained in this way. The
European material is mainly from antarctic areas II and III, whereas the Japanese material is mainly

Table 12. Length frequencies of sexually immature and mature fin whale females
Length (ft.) Immature Mature

5°

137

169

Total 389

756

THE REPRODUCTIVE CYCLE 407

from area V. This close agreement between material from different areas of the Antarctic is
particularly interesting in view of the much lower size at sexual maturity of northern hemisphere fin
whales (Jonsgard, 1952; Pike, 1953) and the reported difference between the lengths at maturity of
this species in the North Pacific and in the East China Sea (Miyazaki, 1958); also in antarctic areas I
and II (Purves and Mountford, 1959).

The question of the mean length of the female fin whale at sexual maturity has been re-examined
using the material available to Mackintosh (1942) and in addition several hundred observations made
up to 1954 on behalf of the ' Discovery ' Committee and the National Institute of Oceanography. This
new material increases the number of records of immature and mature females between 60 and 71 ft.
from 402 to 1 145. The data are presented in Table 12. In Text-fig. 33 these length frequencies,
smoothed by threes, are shown and it will be seen that the intersection of the curves for sexually
immature and mature females is at 65-25 ft. There are 80 sexually mature females below the inter-
section point and 86 sexually immature females above. Taking the lengths of these 166 individuals

100

>- 100

-- IMMATURE
— MATURE

LENGTH IN FEET

Text-fig. 33. Smoothed length frequencies of
sexually immature and sexually mature females.

2 3 4 5 6 7 8

AGE FROM EAR -PLUG (YEARS)

Text-fig. 34. Percentage of sexually mature
females in successive age groups.

as a normal frequency distribution with a mean value corresponding to the average length at puberty,
the mean is 65-41 ft. (standard deviation 2-07, standard error 0-16). This is in close agreement with the
value of the intersection point of the curves. The mean length at puberty is therefore taken to be
65-25 ft. The larger sample has extended the range of overlap by a few feet from 61-69 to 60-71 ft.,
but the mean length at sexual maturity remains identical with the earlier estimate of Mackintosh. It
should be remembered that this mean length is derived from material representing several areas.

The diagnosis of sexually mature males is not so easy, nor so precise. It depends either on histo-
logical criteria or on consideration of the size of the testis. The estimate given by Mackintosh (1942)
is based on 770 sexually immature and mature males up to 69 ft. in length, and his figure of 63 ft. is
accepted here, because the new material did not necessitate revision of his estimate for the female.

The age at sexual maturity
Earlier estimates of the age of female fin whales at sexual maturity have been discussed in the introduc-
tion to this paper (pp. 334-38). These were based on the occurrence of modal groups in analyses of
length frequencies, and on methods of age-determination, such as baleen plate, crystalline lens, etc.

4o8 DISCOVERY REPORTS

Nishiwaki (1957) re-examined this question by comparing the number of laminations in the ear-
plug with the number of corpora in the ovaries of 34 antarctic fin whales. He found that 10 laminations
corresponded to one corpus albicans and, assuming that laminae are laid down at the rate of two per
year, concluded that sexual maturity is attained at 4-5 years. This estimate agrees with his previously
published estimate based on other methods (Nishiwaki, 1952). It appears from his fig. 3 that he used
six records of immature females (with no corpora) in fitting his regression line, and this would result
in a figure for the age at sexual maturity which is slightly low.

Purves and Mountford (1959) correlated sexual maturity with lamination number for a large sample
of antarctic fin whales and found that in the female approximately 12 laminations were laid down at
sexual maturity. They based this estimate on the youngest pregnant females in their sample, and on
their growth curve showing the number of laminae corresponding to the average length at sexual
maturity which they assume to be 66 ft. (Actually 65-25 ft. is the best estimate.) They conclude that
the age of the female fin whale at sexual maturity is 5-6 years.

Not all females become pregnant at the first ovulation and there is usually a gap of several months
between first and second ovulations (see below, p. 416). If all sexually mature females (including those
at puberty which have ovulated without becoming pregnant) are examined, a more precise estimate of
the age at puberty should be possible.

The ovaries relating to the ear-plugs examined by Purves and Mountford (1959) have now been
examined and a brief preliminary account of the findings is helpful at this point. A more detailed
account based on a much larger sample of ear-plugs and ovaries now being examined by the author
will be published at a later date and may lead to slight modification of the results now put forward.
Females are taken to be sexually immature if there is no corpus luteum or corpus albicans in the
ovaries ; they are sexually mature if the ovaries contain one or more corpora.

Table 1 3 . Frequency of sexually immature and mature female fin whales in different age groups

Number Percentage

Estimated
age (yrs.)

j
Immature

5
6

7
8

Mature

r
Immature

Mature

ioo-o

o-o

71-4

28-6

78-6

214

53-8

46-2

222

77-8

12-5

87-5

o-o

1000

o-o

ioo-o

3
6

7
7
8

9 — 5

The results of this study are set out in Table 13 and Text-fig. 34. The estimated ages of individual
females are taken from Purves and Mountford (1959, table A) and the material has been confined to
area I as their sample from area II is rather small.

In Text-fig. 34 the curve shows the percentage frequency of sexually mature females in different
age-groups up to 9 years. The age corresponding to 50% of mature females is about 5 years, which is
taken to be the average age at sexual maturity. This is in fairly good agreement with the conclusions
of Purves and Mountford (1959); the age above which the majority of females were pregnant was
estimated to be about 6 years, but the antarctic catch is taken in January, February and March, and
these females would, on average have ovulated during the breeding season (July), that is some
7 months previously, giving an estimate for the age at sexual maturity of about 5-4 years.

Although the average age at maturity is here taken to be 5 years, Text-fig. 34 shows that some 3 -year-

THE REPRODUCTIVE CYCLE 4°9

old females are sexually mature, while some sexually immature whales are as old as 7 years, a range of
5 years. The full range for the population is probably greater than this small sample indicates.

As regards the male fin whale, Laws and Purves (1956) compared testis weights and ear-plug
laminations of a small sample of northern hemisphere animals. They concluded that sexual maturity
is attained at 4-6 years. Purves and Mountford (1959) show that the estimated length at sexual maturity
(taken to be 63 ft.) corresponds to nine laminations on their growth curve for body length, that is, to
4I years. Sexual maturity in the male appears, therefore, to be attained at a slightly lower age than
in the female.

These estimates of age at sexual maturity are based on an assumed bi-annual rate of lamina forma-
tion. Although this appears probable for adult fin whales (see below, p. 467), it is possible that the
incremental rate is less regular in immature whales (Chittleborough, 1959, fig. 4), and the laminations
are difficult to read. This will probably not greatly affect the estimate of the average age at sexual
maturity, but means that the range of ages at which sexual maturity is attained may perhaps be greater.

NEWLY MATURE FEMALES

The mammary gland
Positive identification of newly mature females is made possible in the field by the characteristic
appearance (gross and microscopic) of the mammary gland. This is the only group of mature females
for which the precise reproductive status is known with certainty. The location of the mammary
glands of baleen whales and their anatomy and histology are described by Lillie (191 5), Mackintosh and
Wheeler (1929), Heyerdahl (1930), Ommanney (1932), van Lennep and van Utrecht (1953) and
Chittleborough (1958).

In sexually immature female fin whales the mammary gland is usually not more than 3 cm. deep
(mean 2-2 cm.) at the widest part (Text-fig. 35) and is pale pinkish white in colour. It is composed
mainly of a mass of connective tissue in which a few small lacteal ducts and blood vessels are seen,
and the alveoli are only slightly developed (Mackintosh and Wheeler, 1929, fig. 135).

The glands of females in their first pregnancy (usually with only one corpus luteum and no corpus
albicans in the ovaries) are very similar in gross and microscopic appearance to those of immature
females and are 3 cm. thick, or less, in the majority (mean 2-9 cm., range 1-6 cm.). The development
of the lobules may be slightly greater than in the immature gland, but less than in the resting condition,
and the colour remains a pinkish white.

A preliminary study suggested that the mammary gland increases in thickness from the immature
level of about 2 cm. to about 4-5 cm. at each ovulation preceding the first pregnancy, and shrinks
again to the former level in anoestrus or pregnancy. This would account for the few thicker mammary
glands at puberty and the first pregnancy; in spite of their greater depth they retain the immature
appearance. Unfortunately the material is insufficient for statistical treatment. There is no evidence
for an increase in the thickness of the mammary gland during pregnancy, at least up to the time when
the foetus has attained a length of 4-5 m., which is thought to be about a month before parturition
(Laws, 19590). One first-pregnancy female with a foetus 6-4 m. long (which must have been very
near term) had mammary glands only 2 cm. thick. Van Lennep and van Utrecht (1953) remark that,
' In contrast to many other mammals the alveoli do not develop until the end of pregnancy '. Chittle-
borough (1958) found that in humpback whales which were very close to the time of parturition the
lobules and alveoli were well developed and colostrum was present in most cases. It is considered
unlikely that in fin whales mammary gland development and the secretion of colostrum begin until
after they have left the Antarctic on the northward breeding migration.

4io DISCOVERY REPORTS

Lactating females with one corpus albicans in the ovaries will be in their first lactation and in the
material there are seven such records. The criterion of full lactation which is adopted here is discussed
below (p. 444). During the first lactation the gland undergoes an apparently irreversible change;
it may enlarge to over 20 cm. in thickness (mean 16-1 cm., range 8-24 cm.) and although it involutes
after weaning (or death) of the calf it does not revert to the former immature condition.

In females which have previously experienced at least one lactation period the mammary glands are
either immediately post-lactation in condition or what Mackintosh and Wheeler (1929) termed
'resting' or 'intermediate' between this condition and lactation (see below, p. 444). The mammary
glands are then usually more than 3 cm. deep (from 2-5 to 14 cm., Text-fig. 35) and there are brown
lobes of coiled ducts set in a thick connective tissue framework (Mackintosh and Wheeler, 1929,

- 15

10 20 o 10 so o 10

PUBERTY PREGNANCY LACTATION

PRIMIPAROUS

SECOND FULL

PREGNANCY LACTATION

END OF

LACTATION

MULTIPAROUS -

Text-fig. 35. Frequency distribution of mammary gland depth in several groups of female fin whales.

fig. 138; van Lennep and van Utrecht, 1953, fig. 1). Apart from the usually greater thickness, the colour
and appearance of ' resting ' or ' intermediate ' mammary glands is quite different from that of the
gland which has not yet been functional. The gross appearance of the mammary gland in section is,
therefore, considered to be a reliable criterion of nulliparous or primiparous females.

The first pregnancy

There are 88 pregnant fin whale females in the material which can be classed as primiparous on the
grounds outlined above. This figure includes only those individuals for which data on both mammary
development and ovaries are available; it excludes females known to be primiparous because they
are pregnant with only one corpus luteum and no corpus albicans in the ovaries, but for which no
data on the mammary gland condition are available. Of these females, 60 (68%) had one corpus
luteum and no corpus albicans, 20 (23 %) had one corpus luteum and one corpus albicans, 7 (8 %) had
one corpus luteum and two corpora albicantia, and one (1 %) had one corpus luteum and three corpora
albicantia. They had, therefore, become pregnant for the first time at the first, second, third, or fourth

NEWLY MATURE FEMALES 411

ovulation and in this class the mean number of ovulations preceding conception was 1-42. Owing to
the small size of the sample the variance is quite large. It is of interest that in primiparous females
any corpora albicantia will represent unsuccessful ovulations.

MONTHS

Text-fig. 36. Monthly mean foetal lengths for all pregnant females (solid line) and
for primiparous females (dotted line).

0,1,2, C. A.

J F

M J J A

MONTHS

Text-fig. 37. Monthly frequencies of conception for different classes of pregnant females. P, , first pregnancy diagnosed
from mammary glands; o, 1, 2 and 0-1, number of corpora albicantia. The mean conception dates ± 2 S.E. are indicated.

There are conspicuous differences in the timing of the pregnancy of primiparous females compared
with multiparous females. In Text-fig. 36 the mean monthly foetal lengths for all pregnant females
and for females known to be primiparous, from examination of the mammary glands, are set out for
comparison. The rates of growth of both groups of foetuses appear to be similar, but the first-pregnancy
'oetuses seem to be retarded by about a month compared with those of multiparous females.

4i2 DISCOVERY REPORTS

The monthly frequencies of conception for newly mature females can be estimated by relating the
individual foetal lengths to the mean curve of growth as was done previously for all pregnant females
(p. 403). This involves the assumption that the rate of foetal growth is the same in primiparous females
as in multiparous females; it is thought to be a reasonable premiss and there is no evidence to the
contrary. The conception periods estimated in this way for several groups of newly mature females
are shown in Text-fig. 37. The classes of newly mature females for which conception dates have been
calculated are as follows: (1) Primiparous females with one corpus luteum and up to three corpora
albicantia in the ovaries. Examination of the mammary glands is used to diagnose a first pregnancy
in this case. They will be referred to as ' primiparous ' females. (2) Females known to be primiparous
because they are pregnant with a corpus luteum but no corpus albicans in the ovaries, that is, they
conceived at the first ovulation. This group includes females for which there is no mammary gland
data; it will be referred to as the 'o corpus albicans' group. (3) Females probably in their first or
second pregnancy with a corpus luteum and one or two corpora albicantia ; to be referred to as the
' 1 corpus albicans ' and ' 2 corpora albicantia ' groups.

The frequency of conceptions of the ' primiparous ' group of (88) newly mature females is shown in
Text-fig. 37, centre (Pj. The frequency curve is fairly symmetrical, with mean, modal and median
dates all approximating to late July (respectively 22, 26 and 21 July). It will be remembered that the
conception curve for all females was markedly skewed towards earlier months. The combined con-
ception frequencies of the ' o corpus albicans ' and ' 1 corpus albicans ' groups has been plotted in
the same figure for comparison with the ' primiparous ' group. This is a larger sample (151) and shows
a closely similar frequency distribution to the 'primiparous' group, the mean, modal and median
dates being very close to these values for the 'primiparous' group (respectively 21, 26 and 19 July).
For the purpose of determining the monthly frequency of multiparous conceptions it will, therefore,
be assumed that the ' 0-1 corpora albicantia ' group is equivalent to all first pregnancies (below, p. 425).
This means that the samples of primiparous and multiparous females need not be restricted to those
females for which mammary gland data are available, but only to those for which the results of examina-
tion of the ovaries are available. The number of pregnant females for which foetal length records and
ovarian data are available is 845, of which 151, or 17-9%, are taken to be in the first pregnancy.

Although the frequency curve of '0-1 corpora albicantia' conceptions is reasonably symmetrical,
there is a conspicuous subsidiary peak of conceptions in May and it is instructive to plot the ' o corpus
albicans' and ' 1 corpus albicans' groups separately for comparison. In Text-fig. 37 (top), the con-
ception frequencies of these two groups are plotted and also the conception curve for the ' 2 corpora
albicantia' group. The distribution of the 'o corpus albicans' conception frequencies is very
symmetrical with a sharp peak in July (mean and median dates, 23 July ; mode 26 July). When the
conception curve for the ' 1 corpus albicans ' group is examined, the mean and median dates are found
to be at the middle of July (18 July and 12 July, respectively), and the curve is skewed with the mode
in May, two months earlier than the peak number of ' o corpus albicans ' conceptions. This mode is
clearly responsible for the subsidiary peak in the ' 0-1 corpora albicantia ' conception curve. It will
be seen that this advancement of the peak conception date is also characteristic of the ' 2 corpora
albicantia ' group, in which it is slightly more marked. When similar curves are plotted for later corpora
albicantia groups the proportion of conceptions in April/May is seen to show a marked increase in the
'3 corpora albicantia' group and in later groups this becomes the peak month. Wheeler (1930) from
his examination of the frequency of numbers of corpora concluded that in the first sexual season the
majority of females become pregnant at the first ovulation, while in subsequent seasons unsuccessful
ovulations usually precede pregnancy. In explanation he suggested that whales nearing puberty tend
to stay near the breeding areas, or at any rate do not make a long southward migration, so that they

NEWLY MATURE FEMALES 413

are first to be impregnated, while older females arrive on the breeding grounds later, after one or more
unsuccessful ovulations. In fact it is now known that the pubertal females migrate and conceive later
than the mature females. The tendency for the advancement of the pairing season with increasing age
is further discussed below (p. 427).

Growth in length just after puberty

Females in the ' o corpus albicans ' group form a distinct, narrow, and relatively uniform class of
animals. For this group of females it is possible to study the rate of growth over almost a year by
comparing the maternal growth with the growth of the foetus. The average curve of foetal growth in
length of the fin whale has been established with reasonable accuracy (p. 403), and may be used as an
absolute time-scale over the period of gestation.

Text-fig. 38.

Ol 234 5678 9 IO II 12

JASONDJFMAMJJ

GESTATION PERIOD (MONTHS)

Probable growth in length during first pregnancy of females which conceived
at the first ovulation.

The mean length at conception is taken to be 65-25 ft. (see above, p. 406), but this may be a slightly
high (or low) value because females which become pregnant at the first ovulation may be shorter (or
longer) than those which ovulate unsuccessfully for the first time.

The mean lengths of 86 primiparous females in the 'o corpus albicans' group are set out in
Table 14, according to the month of pregnancy, and in Text-fig. 38 the smoothed maternal lengths
are plotted against the months of pregnancy, taking July as the mean period of conception. A growth
curve has been fitted by inspection to these points taking its origin at a length of 65-25 ft. at conception.
There is no statistical justification for fitting an approximately sigmoid curve to the points, but with
the exception of the second point, which represents a small sample, the lightly smoothed mean lengths
do not show large fluctuations and it is reasonable to suppose that the average curve which has been
drawn does approximate to the true growth curve (Text-fig. 38). It is significant that the supposed
maternal increase in growth-rate begins about 6-7 months after conception ; it is at this time that the
exponential phase of foetal growth begins (p. 401, Text-fig. 30) and this increased growth is related
to the short annual period of intensive feeding. A mass curve of this kind is likely to reduce
apparent changes in the growth rate. It is likely, therefore, though not proven, that fin whales
experience a period of increased growth in length, similar to the increase in weight known to take
place on the antarctic feeding grounds (Ash, 1956). Probably all fin whales show a similar rapid
seasonal increase in length on the feeding grounds, which yearly becomes smaller and smaller until
physical maturity is attained. These data suggest that just after puberty the average rate of growth is
between 2 and 4 ft. a year, probably just over 3 ft.

4'4 DISCOVERY REPORTS

Table 14. Growth of the 'o corpus albicans' group of females during the first pregnancy

Length (ft.)

Duration of
pregnancy Sample

Smoothed

(months) size

Range

Mean

(threes

0-1 2

(63

0-67-5)

65-3

—

1-2 2

(69

0-71-0)

70-0

66-5

2-3 1

—

62-0

65-6

3-4 7

(63

o-66-o)

64-9

65-8

4-5 6

(62

5-70-0)

67-4

66-2

5-6 16

(62-0-70-0)

66-3

66-2

6-7 15

(60-0-78-0)

66-3

66-4

7-8 5

(64-

0-71-0)

66-8

8-9 20

(63-

0-72-0)

67-7

677

9-10 8

(67

0-70-0)

68-3

67-9

io-n 3

(61

0-72-0)

677

68-4

c. II 1

71-0

— —

rable 15. Mean length and variation in six

groups of newly mature ft

male

Mean

Number

length

2 S.E.

A Puberty

166

65-25*

2-07

0-32

1 Ovulation

B Primiparous

66-9

266

0-58

C Nulliparous

66-8

2-90

1-04

B + C

121

669

273

0-50

D Lactating or Resting

68-5

2-40

o-86

2 Ovulations

E Nulliparous and Primiparous

68-2

2-81

0-99

F Second pregnancy

689

2-36

1-03

* This is the intersection of the length frequency distributions of immature and mature females; the standard deviation
and standard error are calculated from the frequency distribution of the overlapping group (see Text-fig. 33).

Further information about the average rate of growth in length in the period following puberty can
be obtained by considering the average lengths of these and other groups of females known to be
recently mature. The means plus or minus one standard deviation and two standard errors are given
for each of five groups of recently mature females in Table 15 and plotted in Text-fig. 39. The groups
comprise (a) females at puberty ; females which have ovulated once and are (b) primiparous, (c) nulli-
parous, or (d) lactating or resting; females which have ovulated twice and are (e) nulliparous or
primiparous, (/) in the second pregnancy. (In the groups (d) and (e) the two categories comprising
the group have been amalgamated so as to increase the size of the sample for statistical treatment.)
With the exception of the nulliparous females, these all represent individuals which became
pregnant at the first ovulation and are presumed on average to have attained puberty in July
(that is, as primiparous 'o corpus albicans' females). The average date of the other observations is
mid-February. The probable mean growth curve of first pregnancy, 'o corpus albicans' females
(from Text-fig. 38) has been drawn in as an unbroken line. It passes close to the mean length of
the primiparous ' o corpus albicans ' group (B) and through the mean of the nulliparous ' 1 corpus
albicans ' group (C). Females in their first lactation, or first resting period with one corpus albicans (D)
will be on average a year older than the primiparous 'o corpus albicans' group, and have been
plotted in the second year following puberty. It is possible that a very small proportion of the resting
females in this group may be older.

NEWLY MATURE FEMALES 41S

The mean growth curve has been continued as a broken line, increasing very slightly from June to
December and then increasing again during the second feeding season after puberty. At 2 years after
puberty the mean length is shown as 69-6 ft. If the average rate of ovulation is 1-4 per year (below
p. 465) then 2 years after puberty there are expected to be on average 2-8 corpora and from Text-
fig. 25 the mean length at 2-8 corpora is 69-6 ft. The growth previous to puberty is also suggested as
a broken line, to indicate that in the feeding season before puberty growth is more rapid, as is probable
in the primiparous feeding females. If this line of argument is correct, then puberty usually succeeds
both a period of rapid growth, and a northward migration when day length is increasing (see below,
p. 421).

72 -1 A - - BC - — DF-

'jvTa mJJaSONDJFMAMJJASONDJFMAMJ

MONTHS

FEEDING PAIRING

FEEDING PARTURITION

FEEDING

Text-fig. 39. Growth of newly mature females indicated by mean length ± a, ±2 s.E. A, at puberty; B, first pregnancy,
o corpus albicans ;C, one nulliparous ovulation ; D, first lactation or resting period; F, second pregnancy, 1 corpus albicans.
See text for explanation.

The position of the remaining group, of females in their second pregnancy with one corpus
albicans and resting mammary glands (F), must now be discussed. These are females which have
become pregnant again at the first ovulation after the termination of the first pregnancy. It seems
most probable that the origin of this second pregnancy is either a post-partum ovulation (shown below,
p. 429, to be a normal feature of the reproductive cycle in female fin whales and some other species)
and or an ovulation following the termination of lactation upon loss of the calf. It is, however, certain
that some, possibly all, of these first-lactation females do not experience a post-partum ovulatory
period and that some or all of them are a year older than has been indicated in Text-fig. 39. It is only
possible to diagnose accurately the reproductive history of those females in the first lactation or
resting period which have only one corpus albicans in the ovaries. None of the individuals in this
group has, by definition, experienced a post-partum ovulation. Those with more than one corpus
in the ovaries might possibly be in the second lactation or resting period, but there are undoubtedly
many females in their first lactation or resting period which have more than one corpus albicans in
their ovaries and some of these may well have experienced a post-partum ovulatory period. The fact

416 DISCOVERY REPORTS

that the mean of this second-pregnancy group is so close to the mean length of females in their first
lactation or resting period, suggests that the original assumption is correct and that this group is
correctly placed in Text-fig. 39.

The variance in length in each group is rather large (standard deviations 2-3 ft.). The dotted lines
in Text-fig. 39 represent the mean plus or minus 6 in. and this represents the probable range of error
in the mean curve taking into account the values of two standard errors of the mean lengths at puberty,
some months later (groups (b) and (c) combined), and over a year later (groups (d) and (e) combined).

The first ovulations
We have seen that prior to the first pregnancy there may be from one to four ovulations, with a mean
number of about 1-42. There are two important questions which we must now attempt to answer.
First, is ovulation spontaneous or is it induced by the stimulus of coition? Secondly, what is the
length of the oestrous cycle and the interval between successive ovulations ; that is to say is the fin
whale polyoestrous or monoestrous?

Ovulation is probably spontaneous as in ungulates and most other mammals (Eckstein, 1949).
Mackintosh and Wheeler (1929, p. 381) describe the vaginal band which is present in about 21 % of
immature females. This structure is so placed that it is almost certain to be ruptured when mating
occurs and up to 1957 no intact vaginal bands had been observed in parous females. Wheeler (1930,
p. 413) mentions the case of a female fin whale with immature mammary glands, an unbroken vaginal
band and one corpus albicans in the ovaries ; a similar case was recorded by Mackintosh and Wheeler
(1929, p. 390), and there have been a few later unpublished records of females in a similar condition.
This is a rarely observed condition because, of a hundred females at puberty, about 70 become pregnant
at the first ovulation, and only about 21 % of the remainder would have a vaginal band ; this means that
less than about 6% of females which have ovulated only once can be expected to have an unbroken
vaginal band. The presence of corpora in the ovaries of females with unbroken vaginal bands would
appear to be conclusive evidence of spontaneous ovulation. However, in 1958 D. F. S. Raitt, a
biologist making observations and collections for the National Institute of Oceanography, reported
a pregnant fin whale which had an unbroken vaginal band. ' One case appeared to be an example
of a virgin ovulation. This was a 69 ft. fin... .The vaginal band was intact, though rather slack,
the mammary gland was 4-5 cm. deep and a 10 ft. n ins. male foetus was found. The ovaries were
obtained and one had an apparently functional corpus luteum (unpublished report). In spite of
this one exceptional record it is considered that the several other cases of virgin ovulations associated
with unbroken vaginal bands are evidence that ovulation is spontaneous. Some additional support
for this assumption is provided by the relatively high proportion of non-pregnant females in antarctic
waters which have recently ovulated (pp. 418 and 436), although mating behaviour has been very
rarely observed.

It has been shown that some 68 % of newly mature female fin whales become pregnant at the first
ovulation. Furthermore, a large proportion of newly mature females, taken in the Antarctic several
months after the pairing season, have ovulated only once and regression of the corpus albicans
representing that ovulation is already advanced (mean diameter 4-4 cm.), indicating that it represents
a monoestrous cycle, and not the first of a series of polyoestrous cycles. The great majority of fin whale
females, if not all, are, therefore, effectively monoestrous in their first sexual season. Some 32%
of females in their first pregnancy had ovulated more than once before becoming pregnant. It is not
possible to say how long the oestrous cycle in the fin whale is, but it is probably about 16-23 days
as in ungulates (Eckstein, 1949) or longer; it is very unlikely to be shorter than this. Then, if the
female fin whale is polyoestrous in the first sexual season the curves of the monthly frequency of

NEWLY MATURE FEMALES 4'7

conceptions for the ' o corpus albicans ' group and the ' primiparous ' animals with 0-3 corpora albicantia
(diagnosed from mammary gland inspection) should differ. The latter group might be expected to
show more conceptions in the later months. In fact a comparison of these curves (Text-fig. 37) shows
that they are almost identical.

Curves showing the frequency of conception in those females which had ovulated twice or more
before the current pregnancy have already been presented (Text-fig. 37). The ' 1 corpus albicans ' group
was shown to be in advance of the ' o corpus albicans ' group in this respect, whereas, if fin whale
females are polyoestrous it would be expected to be slightly later. The ' 2 corpora albicantia ' group
shows a similar advancement.

The majority of the ' 1 corpus albicans ' group will probably be primiparous, but some of this group
may be individuals which are in the second pregnancy, having failed to complete the first pregnancy.
In this event the second ovulation, leading to the current pregnancy, would probably have occurred
earlier in the pairing season than the first ovulation (' o corpus albicans ' group) as is the tendency in
muciparous females.

Others may be females which became pregnant a second time as a result of a post-partum ovulation
(see p. 429) following the successful completion of the first pregnancy. If pregnancy were to last
ill months in primiparous females, as in multiparous females, and this ovulation is about 3-4 weeks
post-partum then the group would tend to conceive about the end of July. This would partly counter
the effect of earlier mating of females in which the first pregnancy had been prematurely terminated.
The evidence presented above, although not conclusive, suggests that at puberty there is a single
ovulation and that if pregnancy does not intervene the female usually goes into anoestrus without
further ovulatory cycles. It is possible that a small proportion of females do experience up to three or
four polyoestrous cycles, but this is thought to be unlikely.

Chittleborough (19556, p. 3 18) implies that this is also true of the humpback whale. He states that
some female humpback whales become pregnant at the first ovulation, but that the ovaries of a number
of nulliparous females 'contained one (or sometimes two) corpora albicantia' and these females
'would probably have become pregnant for the first time during their second ovulatory season'.
Presumably regression of the corpora albicantia was well advanced in these females and the follicles
were not undergoing pro-oestrus enlargement. The mean length of these females was about a foot
more than the mean length at puberty which also suggests, as in the fin whale (Text-fig. 39 C), that
puberty occurred some months earlier.

Certain evidence, now to be presented, shows that puberty may be attained outside the usual pairing
season, and that in this case also the cycle at puberty is monoestrous.

In the material there are 10 virgin females which have a corpus luteum of ovulation in the ovaries.
In seven of these animals (taken between November and February) this was the result of the first
ovulation at puberty; in one (20 January) it represented the second ovulation, and in two others
(11 November, 18 January) it was a product of the third ovulation. These are diagnosed as virgin
ovulations from the virgin appearance of the mammary gland, and the absence of any embryo in the
uterus. Only 2-4% of all pregnancies are estimated to begin in the 4 months November-February

(Table 11).

In one of these females (taken on 29 December) regression had begun but the corpus was still 7 cm.
in diameter. The others were taken between 15 November and 14 February, and the corpora lutea
ranged in size from 6 to 13 cm. The mean diameter was 8-8 cm., which is slightly higher than the mean
diameter of the corpus luteum of ovulation, but well within the probable range of variation of the
mean (8-28 ±0-82 cm., above, p. 356). It is well below the mean diameter of the corpus luteum of
pregnancy ( 1 1 -44 ± o- 1 5 cm.). This supports the diagnoses of recent ovulations. In the three nulliparous

4i8 DISCOVERY REPORTS

females which had ovulated more than once the diameters of the largest corpora albicantia were
4*5 > 3 '3 and 3 cm- respectively, suggesting that there had been quite a long interval between the last
two ovulations and that they do not represent successive ovulations in a polyoestrous ovulatory cycle.

The estimated pairing season for the ' o corpus albicans ' group is April-November (inclusive)
(Text-fig. 37). The present material shows that puberty can be attained and the first ovulation take
place several months before or after the normal pairing season for this group. March is the only
month for which there is no record or estimate of a female fin whale reaching puberty.

For six of these females observations on the extent of the diatom film were made. In three of them
there was no diatom infection (two in January, one in February); in one (November) it was incipient;
in one moderate (November); and in one it was heavy (December). The latter record relates to the
female in which the recent corpus luteum had just begun to regress. As the diatom film is acquired in
antarctic waters these limited data suggest that the corpora lutea of ovulation in these whales formed
during or just after the southern migration.

IV-*

. IUU

111

" /■

•

a.
u.

UI 5

50-

• •

•

• •
•

•

a O H

1 1 1 1
J F M

MONTHS

v-* n

i i
J F

MONTHS

Text-fig. 40. a, Size of largest corpus albicans of 14 nulliparous females without a corpus luteum; antarctic material. (Black
circles, only corpus albicans; white circles, largest of two or more corpora albicantia.) b, Monthly frequency of ovulation of
41 pubertal females taken in the Antarctic.

Certain other evidence supports this hypothesis. There are records of the size of the largest corpus
albicans in a number of pubertal nulliparous females taken in the Antarctic. In Text-fig. 40, a, the
diameters of 14 such corpora (from ovaries in which there are no active corpora lutea) are plotted
according to the date of collection. They show an apparent decline in size, probably representing
the shrinkage associated with regression. The sizes of these corpora suggest that most of them were
derived from corpora lutea of ovulation which formed as late as November, December, or January.
The ovaries of these females do not contain follicles undergoing pro-oestrus-enlargement and this
confirms that these corpora do not represent the first ovulation in a series of dioestrous cycles.

If we now examine the entire group of pubertal nulliparous females (which incorporates animals
not included in the discussion above because there were no records of corpora size for them) we can
obtain a better estimate of the time of ovulation. This material comes from each of the 6 months
November-April and for each month the percentage of animals in this group which have an apparently
active corpus luteum of ovulation in the ovaries (as opposed to those in which the ovaries contain one
or more corpora albicantia) has been calculated. This is shown in Table 16 and graphically in Text-
fig. 40, b. A single record for 29 December is the animal mentioned above in which the corpus luteum
had only just begun to regress and had characteristics of both corpus luteum and corpus albicans.

NEWLY MATURE FEMALES 419

This has been placed in December as a corpus luteum of ovulation and in January as a corpus
albicans.

The paucity of records in the early months does not permit a precise estimate of the peak time of
ovulation during this period, and the purpose is merely to show that there is an ovulatory period in
this group of pubertal females which is well outside the main breeding period (see also pp. 403-6),
From the evidence presented in Text-fig. 40, it is presumed that before January the majority of
pubertal females present in the Antarctic have recently ovulated, and that after January the ovaries of
the majority contain young regressing corpora albicantia from recent ovulations. This evidence also
suggests that an ovulatory period is associated with the southern migration which probably takes place
in the majority of this group in November, December, and January, but may be slightly earlier or
later.

Table 16. Monthly frequency of ovulation of pubertal female fin whales taken in the antarctic

Corpus albicans

Total ovulated

nulliparous

females

Corpus

luteum

of ovulatioi

No.

Percentage

November

100

December

100

January

5°

February

March

April

Total

—

No.

Percentage

5( + i*)

5°

100

30( + i*)
* This record has been included as corpus luteum and corpus albicans; see text p. 418.

One anomalous pubertal female has not been included in Text-fig. 40, a, for reasons given below,
but is included in Text-fig. 40, b. This individual was taken on 24 January and had one corpus
aberrans in each ovary (see p. 380), measuring 2-5 and 2-3 cm. in diameter. The largest follicle was
3-5 cm. in diameter and there were several follicles about 3 cm. in size, in each ovary. This female
had not yet acquired a diatom film and is, therefore, presumed to have recently completed a southern
migration during which ovulations took place which led to the formation of corpora aberrantia. It
does not invalidate the conclusions put forward above.

The monthly variation in size of the largest follicle in the ovaries of females approaching puberty
(over 63 ft. in length) has been discussed above (p. 346, Table 2, Text-fig. 3). In conjunction with the
foregoing evidence it is significant that the largest follicles are found in females of this group taken
in the Antarctic in November. The mean size of the largest follicle in three individuals taken in
November is 3-3 cm., and the absolute maximum size of follicles in immature females was about 5 cm.
for one of these November animals. From January to May the monthly mean maximal follicle size
is about 1 cm. or less. The large size of the November follicles suggests pro-oestrus enlargement which
might or might not have been followed by maturation and ovulation.

For the present it is sufficient to show that ovulations can occur outside the recognized pairing
season, and that then also there is a single ovulation, almost invariably unsuccessful probably because
the majority of males are not then in breeding condition. There is no evidence for a succession of
several ovulations at intervals of a month or less. The evidence presented below (p. 438) suggests that
this is also true of multiparous females which ovulate outside the usual breeding season.

One other separate piece of evidence which is inconclusive when considered alone, but which
appears to fit this hypothesis better than any other, remains to be discussed. In Text-fig. 41 the mean
length, plus or minus one standard deviation and two standard errors, is set out for two groups of newly

420 DISCOVERY REPORTS

mature females which have ovulated only once (A) or twice (B). These data are presented in Table 15,
groups B + C and group E respectively. The probable range of error of the estimated mean growth
curve for females which attain puberty in the breeding season at a mean length of 65-25 ft. (from
Text-fig. 39) is also shown by the dotted lines. The mean date of sampling is mid-February.

When the mean length of the once-ovulated group is compared with that of the twice-ovulated
group there is seen to be a difference of 1-3 ft. The standard error of the difference between these two
means is 0-554, which means that the difference is statistically significant. If the twice-ovulated group

72-

AB, B2

71 -

T 1

70-

uj 69 J

...a--

68-

,: \

I
F
O

g 67^

Vy 1

66-

65-

a ■'"

64-

■ 1 1 1 1 1 1 1 ' 1 1

— 1 — 1 — 1 — 1 — 1 — 1 — 1 — 1 — i — i — 1 — 1 — 1 —

1 >

MAMJJASONDJ FMAMJJASON DJ FMAMJ

MONTHS

PAIRING

Text-fig. 41. Growth of newly mature females. The mean lengths ±<r and 2 s.E. of nulliparous or primiparous females which
had ovulated twice (Bj, B2) are duplicated one year apart for comparison with the growth curve of once-ovulated, nulliparous
or primiparous females (A). See text for explanation.

attained puberty and ovulated at about the same time as the once-ovulated group it is very unlikely
that there would be such a discrepancy between the mean lengths of the two samples. The mean
values for the once-ovulated females which were primiparous or nulliparous (Text-fig. 39 B and C)
are in very close agreement with each other.

If the twice-ovulated group is plotted a year later (B2) its mean length (68-2 ft.) is seen to be close
to the length (68-5 ft.) of the group of females known to be in their first lactation or resting period
(Table 15). That is to say, pregnant females in the '1 corpus albicans' group probably become
pregnant about a year later than the 'o corpus albicans' group. The mean length of the twice-
ovulated group under consideration coincides with the estimated lower limit of the growth curve of
the 'o corpus albicans' group of pregnant females (Text-fig. 41, curve a---a) which on average attain
puberty and pair in July. The estimated time of pairing of the ' 1 corpus albicans ' group is also July
(Text-fig. 37), when this lower curve (a---a) has attained a length of nearly 68 ft., which is nearly 3 ft.
more than the mean length at puberty. It will be remembered that the growth in length in the first
year after puberty was taken to be just over 3 ft. The origin of this curve (a---a) at the mean length at
puberty is in October, some months after the peak pairing season, but having regard to the length
variance of the group concerned they could well have attained puberty as late as December or January.

NEWLY MATURE FEMALES 421

The question is now, when the first ovulation of the ' 1 corpus albicans ' group of pregnant females
occurred. This could have been at the time when the average length and age at puberty was reached,
or possibly at an average length of about 68 ft. just before the second ovulation which led to the
current pregnancy. It seems most probable, taking into account all the evidence discussed in the
preceding pages, that the pregnant ' 1 corpus albicans ' group is composed of females which attain
puberty at a later date than the pregnant ' o corpus albicans ' group, during or just after the south-
ward migration, say in December or January. Pubertal females which were taken in the period
November-February and are discussed above (p. 417) belong to this group. After one ovulation they
probably go into anoestrus and conceive on average in July at the next ovulation after the northward
migration to the breeding grounds.

Puberty and its relation to the migratory cycle
It has been shown that the gross structure of the mammary gland is diagnostic of nulliparous or
primiparous female fin whales. This enables certain groups of pubertal or newly mature females to be
defined and distinguished, and simplifies investigation of events at this stage of the life-cycle. It is
estimated that, on average, puberty is attained at an age of about 5 years (range 3-8 years), corres-
ponding to an average length of 65-25 ft. The standard deviation of the mean length at puberty is
2-07 ft. which means that 95% of females should attain puberty between about 61 and 69 ft., and
67% between 63 and 67 ft. Asdell (1946, p. 10) states that of the factors associated with puberty
length is much less variable than age, and this is true of the fin whale also. Laws (19566) has shown
that there is a very close relation between growth and sexual maturity in whales as in other mammals.
For 10 species of cetaceans the mean length at puberty expressed as a percentage of the mean length
of physically mature animals averages 85-1 % (a = 3-14, V = 3-69). It should be mentioned that the
true length variance at puberty (and in other age-groups) in the fin whale is probably rather less than
that given. Errors in length measurement are undoubtedly relatively large; the dragging of a 60-ton
whale up the slipway against gravity and friction might be expected to extend the whale by an amount
which should vary according to the post-mortem history. The true mean length at puberty is, there-
fore, even less variable than the figures given above suggest. The average rate of growth at puberty
is about 3 ft. a year, and in the majority of females puberty is preceded by a period of intensive feeding
in the Antarctic, when growth is probably rapid and follicular development may be stimulated by the
improved nutritive state. Maximum fertility is probably not reached until after the attainment of
physical maturity (p. 456).

Ovulation is almost certainly spontaneous, and about 70% of females become pregnant at the first
ovulation. The curve of monthly frequencies of conceptions is very symmetrical for this group, and
the pairing season, which apparently extends from April to October or November, is later in the year
than the pairing period of multiparous females.

A number of nulliparous females are found in the Antarctic between December and April which have
only one corpus albicans in the ovaries. Thus a single ovulation appears to be the rule in the first
ovulatory period even in the absence of conception. Furthermore, it is found that in general females
which become primiparous at the second ovulation conceive earlier in the year than those females which
become primiparous at the first ovulation. This also suggests a monoestrous cycle at puberty, for if
there were two or three cycles in succession females which conceive at the second or third ovulation
should in general pair rather later than females which become pregnant at the first ovulation.

The evidence strongly suggests that there is a second, subsidiary, period when females which did
not attain puberty in the pairing season (April-November) ovulate during or just after the migration
to the antarctic feeding grounds. Pubertal females are found in antarctic waters which have recently

422 DISCOVERY REPORTS

ovulated, with a corpus luteum of ovulation in the ovaries, and have not yet acquired a diatom film.
The most recently formed corpora albicantia in the ovaries of other nulliparous females taken in
antarctic waters appear to have been derived from corpora lutea formed as late as November, December,
or January, and this is associated with a decline in the percentage of pubertal females with corpora
lutea of ovulation in the ovaries from January onwards. This subsidiary ovulatory period also repre-
sents a monoestrous cycle and rarely, if ever, initiates a pregnancy. A period of anoestrus succeeds,
and the next ovulation, which probably follows a northward migration, occurs in April-November
when this group of females have probably attained on average a length of about 68 ft. This ovulation
is usually succeeded by pregnancy.

The type of sexual cycle described in this short summary is very different from the type of cycle
which has previously been assumed to apply to cetacea. Hitherto it has been assumed that whales
have a series of polyoestrous cycles during a single protracted ovulatory period. It has been assumed
that an individual female may experience several dioestrous cycles at intervals until interrupted by
pregnancy or anoestrus. The new evidence about the fin whale suggests that this species is not usually
polyoestrous but rather that it is seasonally monoestrous, and further evidence is presented in a later
part of this paper (p. 425) which shows that the annual cycle of multiparous female fin whales is also
characterized by two ovulatory periods, which probably represent two monoestrous cycles.

If the arguments put forward above are valid then there are two seasons of the year at which fin
whale females may attain puberty. The majority, probably about 70%, ovulate for the first time in
winter during the usual pairing season (April-November) after a northward migration, and the others
probably attain puberty and ovulate for the first time in spring and summer (September?) (October-
February), after a southward migration. This is a very unexpected conclusion and it is worth looking
into possible exteroceptive factors which may be responsible.

A majority of mammals (insectivores, rodents, non-ruminant ungulates and carnivores) are spring
breeders and, as Marshall (1922) pointed out, they appear to be sensitive to increasing light. A minority
(the ruminant ungulates) are autumn and winter breeders and would appear to be sensitive to de-
creasing amounts of light; others appear to be uninfluenced by seasonal changes in the amount of
light. Other factors such as temperature, humidity, food, etc. are also important.

' The various factors which affect the time of the appearance of puberty probably act through the
pituitary-gonad mechanism. Such exteroceptive factors, too... as the length of daylight changes
during the course of the year which cause the onset of the breeding season will accelerate or retard
the age of puberty according as the normal age for puberty in the individual falls before or after this
season ' (Hammond and Marshall, 1952, p. 824). Thus for certain breeds of sheep the breeding season
extends from September to March and those lambs born early in the season will be longer in arriving
at the age of puberty than those born later in the season. In sheep there is neither a fixed age at
puberty nor a fixed time of year for the first heat (J. Hammond, Jr., 1944). Sexual activity begins at
a minimal age of about 6 months, and with increasing age the threshold of stimulation required to
produce the first oestrous cycle falls, until by about 10 months it reaches the adult level. The sheep
responds to decreasing light, and as day length decreases so the intensity of stimulation increases.
It is maximal at the middle of the breeding season which corresponds to the minimal age at first heat
(about 6 months). If this age is reached later in the breeding season the intensity of stimulation is not
sufficient to bring about oestrus, and puberty is not attained until the next breeding season when the
animal may be over a year old (Hammond and Marshall, 1952, p. 824).

A similar mechanism appears to be operative in the case of the fin whale except that this species
probably responds to increasing light, attains puberty at a much greater age and, owing to the
migratory habits, experiences two periods of increasing day length each year instead of one (see below).

NEWLY MATURE FEMALES 423

In most terrestrial mammals the migratory movements, if any, are restricted by geographical or
physical barriers. The scale of migration is greatest in those animals, such as fish, birds, bats, seals
and whales, which live in a continuous medium and are less restricted in their movements by such
barriers. Whales appear to undertake longer migrations than other aquatic mammals. Some seals
migrate over a latitude range of about 250: the migratory range of the northern fur seal (Callorhinns
ursinus) is from about 350 N. to about 6o° N. (Kenyon and Wilke, 1953), and the harp seal (Phoca
groenlandica) travels between 450 N. and about 700 N. (Nansen, 1925), although some individuals
may cover a greater distance. On the other hand, the humpback whale regularly migrates between
the breeding area in about 150 S. latitude and the antarctic feeding zone at about 66° S. (Dawbin,
1956, p. 193). The grey whale (Eschrichtius glaucas) migrates between a feeding area in the North
Pacific at about 6o° N. and a very restricted breeding area centred on lower California in latitude
250 N. (Gilmore, 1955). The fin whale undertakes similar annual migrations, though the evidence is

Text-fig. 42. Above, monthly changes in day length (sunrise to sunset) at latitudes 200 S. and 6o° S. Below, estimated
monthly changes in day length experienced by whales migrating between 20° S. and 6o° S.

not so complete (see above, p. 339), and in its breeding range the fin whale is probably more widely
dispersed than the humpback. One result of these migrations is that the fin whale, and other whales,
are subjected each year to two periods of increasing daylight hours and two periods when day lengths
are decreasing. Animals which do not migrate experience only one period of increase, and one of
decrease, in day lengths.

Let us assume for present purposes that the fin whale migrates between a breeding area, centred on
about 200 S. latitude, and a feeding area which is for the most part south of 6o° S. Let us also assume
that the migration between these latitudes takes about a month. The change in the length of day which
would be experienced by animals migrating north or south in each month is shown in Text-fig. 42.
From this it is evident that animals migrating north in April, May, June, July, August and September
should experience increasing lengths of day with the maximum rate of increase influencing animals
migrating between the beginning and end of July and amounting to some 5 hr. Animals migrating
southwards in September, October, November, December, January and February should also
experience increasing daylight hours with a maximum rate of increase in November and December.
It can be shown that two cycles of increasing photo-periods would also be experienced if we assume
alternative latitudinal movements, such as between 150 S. and 650 S., 300 S. and 6o° S., 400 S. and

DL
13

424 DISCOVERY REPORTS

6o° S., and so on. If it is assumed that each migration takes longer than a month, then the changes in
day length also show two periods of increasing photo-period. Animals remaining at any one latitude
in the southern hemisphere are subject to increasing lengths of day from July to December, though
the rates of increase are in general much smaller than those experienced on migration.

We may now turn to the question of when females approaching the age of puberty make their
northern migration. Mackintosh (1942) discussed the monthly frequency of immature females on
the feeding grounds. He shows that both at South Georgia and on the pelagic whaling grounds the
average length of the catches falls, and the proportion of immature females in the catches (calculated
from the mean length of puberty) increases in the later part of the summer season. Although this
change in the composition of the catches is more marked in blue whales than in fin whales, it suggests
that immature female fin whales arrive at and probably depart from the antarctic feeding grounds
later than the adult females. A similar conclusion was reached by Hjort, Lie and Ruud (1935) and
by Ottestad (1938).

Mackintosh and Brown (1956, fig. 2, table 1) show that the population of large baleen whales (blue,
fin and humpback) in antarctic waters is at its peak in February, but there are still large numbers
present in March and April. Thus, expressed as whales observed per hundred miles steamed, there
were 9-9 in February, 7-2 in March and 3-6 in April. Allowing for the area of ice-free water in three
surface temperature zones the calculated population in April is rather more than half that present in
February. The sampling in May and June, when the estimated population south of the Antarctic
Convergence is higher, is considered by the authors to be unsatisfactory and unrepresentative of the
Antarctic as a whole. Nevertheless an appreciable number of whales are probably still present in these
months and the great majority of these are likely to be fin whales both because fin whale populations
are larger than the stocks of the other species and because the feeding season for blue and humpback
whales is in advance of the season for fin whales (Mackintosh, 1942).

If we are correct in assuming that a large proportion of this rearguard are immature females, then
the main northward migration of fin whale females approaching maturity probably takes place from
April onwards. They will be subjected to maximal stimulus from increasing day length on migration
during July (Text-fig. 42). This is the peak month of pairing for those females which become pregnant
at the first ovulation (Text-fig. 37). Animals migrating northwards in May and June and in August
and September will also be subject to increasing day lengths although the rate of increase will be
smaller. It may be significant that the curve showing the frequency of ovulations in the ' o corpus
albicans ' group of primiparous females closely parallels the hypothetical curve showing the rate of
increase of day length with migration. The small percentage of ovulations in April (2-5%), which is
unexpected on theoretical grounds, is possibly attributable to the working of an inherent cycle and also
to the effect of individual variations in the rate of foetal growth on the estimated frequency of pairing
(see p. 403). The small percentage of successful ovulations in October and November may perhaps be
attributed to this effect, and partly perhaps to animals which experience increasing day lengths only
on arrival at the breeding zone (see next paragraph). Similarly 95 % of successful pairings at the second
ovulation are estimated to take place in the 5 months May-September.

Animals migrating north before May will experience decreasing day lengths on migration. Then, if
they remain in any one latitude zone, they will continue to experience decreasing day lengths until
the end of June, when day length will increase again. Animals which migrate northwards after
September (which are unlikely to be more than a very small fraction of the population) will experience
decreasing day lengths on migration, and then increasing day lengths on arriving at say 200 S., the
rate of increase decreasing until December, after which they will again be subject to decreasing day
lengths. By far the greatest change in day lengths occurs during the migratory phase.

NEWLY MATURE FEMALES 425

According to this hypothesis animals approaching the age of puberty, which migrate northwards
at such a time or at such an age that the postulated ' threshold of stimulation ' is not quite attained
(see p. 422) should not attain puberty until they are next subjected to increasing day lengths. For the
great majority, if not all, of these animals this will be during the next southward migration to the
feeding grounds. Animals migrating southwards in the 6 months from September to February (which
includes almost all individuals) will be subjected to increasing day lengths, and animals making this
migration in November will experience the greatest change in day length. It is again significant that
the incidence of recent ovulations in nulliparous females in antarctic waters appears to be highest in
November and December, falling to zero in March and April (Text-fig. 40). It has also been shown
above that animals taken with corpora lutea of ovulation in the ovaries have only recently completed
the southward migration.

So far only the influence of light has been considered, but the effects of seasonal feeding and tempera-
ture changes are probably also important. Thus, a period of heavy feeding precedes the northward
migration and undoubtedly influences the time of puberty. These factors will be discussed again in
relation to the adult reproductive cycle. There may also be other less obvious influences at present
unsuspected and owing to the lack of precise information about the timing and duration of the
migrations of fin whales it is not possible to treat this subject in more detail. It is possible, for instance,
that the duration of northward and southward migrations may differ, and the speed of migration no
doubt varies for different classes of whales. The curves showing the spread in time of conception may
also be less precise than has been assumed, owing to individual variations in foetal growth.

This hypothesis has been developed to show that the observed facts relating to the reproductive
cycle at puberty are in close agreement with the two periods of increasing day lengths related to
migrations between the breeding and feeding areas. This does not mean that other factors may not
influence the timing of the cycle. Thus, in some mammals which have two breeding seasons the first,
in the spring, follows a period of increasing day length, and the second follows a period of decreasing
day length in the autumn (Eckstein and Zuckerman, 1956). Nevertheless, the thesis that in the fin
whale the response to increasing light is the primary exteroceptive factor in the regulation of an
inherent sexual cycle appears to be reasonable.

MULTIPAROUS FEMALES
The pairing season and the calving season
The curve showing the monthly frequency of conceptions of pregnant females in the 'o corpus
albicans ' and ' 1 corpus albicans ' groups combined is very close to that for females known to be in
the first pregnancy by reason of the state of the mammary gland (p. 409, Text-fig. 37). For the purpose
of determining the pairing season of multiparous females it is, therefore, assumed that all females with
three or more corpora in the ovaries are multiparous. A small proportion of primiparous females will
be included in this group since 9 % of primiparous females have been found to have three or more
corpora lutea and corpora albicantia in the ovaries. This will have a negligible effect on the resulting
curve showing the seasonal frequency of pairing.

There are in the material 694 pregnant females which have three or more corpora in the ovaries and
for which there are foetal length records. The seasonal frequency of pairing was estimated for this
group by relating foetal lengths to the mean curve of foetal growth as was done for all females (p. 403,
Text-fig. 31) and for selected groups of newly mature females (p. 412, Text-fig. 37). In this way
foetuses have been divided into groups conceived in the periods 12 June- 11 July, 12 July- 11 August,
etc. The estimated frequencies of conceptions in the different monthly periods are set out in Table 17

13-2

426

DISCOVERY REPORTS

Table 17. Estimated frequency of conceptions in multiparous southern hemisphere
fin whales, based on 694 records of foetal length

Conceptions

Period

No.

Percentage

January/February

o-o

February/March

o-o

March/April

2-9

April/May

164

23-6

May/June

191

27-5

June/July

131

18-8

July/August

9-1

August/September

5°

7-2

September/October

4-9

October/November

3-6

November/December

i-8

December/January

o-6

Total

694

ioo-o

MONTHS

Text-fig. 43. Monthly percentage frequency of pairing (full line) and calving (broken line) of 694
multiparous females (with 3 or more corpora in the ovaries).

and shown graphically in Text-fig. 43. The peak pairing season is from April to July, as opposed to
May to September in primiparous females, and the mean date of conception for multiparous females
(20 June), is a month in advance of the estimated mean date of conception for primiparous females
(21/22 July). The multiparous curve is skewed with a long 'tail' from July to December, whereas
the primiparous curve is much more symmetrical about the mean, so it is better to compare the median
dates. The median pairing of multiparous females (8 June) is then seen to be about 6 weeks in advance
of the median date for primiparous females (21 July). It should also be pointed out that the beginning
of the steep rise in the multiparous curve of conceptions is actually about half a month later, that is to
say in May, if half-monthly periods are considered. Of the 164 foetuses estimated to have been con-
ceived between 12 April and 1 1 May, 98 were conceived in the second half of the period, so that only
about 90 foetuses were conceived earlier than the beginning of May. These amount to about 13%
of all multiparous conceptions.

Evidence given above suggests that the majority of females, if not all, experience a monoestrous
cycle in their first sexual season. There is unfortunately very little information on this point for
multiparous females. F. D. Ommanney and A. H. Laurie, who examined whales at Durban, South

MULTIPAROUS FEMALES 427

Africa in June, July and August 1930, recorded details of 16 mature female fin whales. Of these, two
were ' resting' but had large maturing follicles up to 5 cm., one was lactating and two were pregnant.
Eight had recently ovulated and another probably had recently ovulated; no embryos were found.
Two had recent corpora lutea in the ovaries, but it was not possible to ascertain whether they were
pregnant or not.

The two ' resting ' females and the eight or nine whales which had recently ovulated were probably
migrating northwards. The appearance and size of the other corpora in these ovaries suggests that in
each case these represent either monoestrous cycles or the first of a series of dioestrous cycles. They
had not been preceded by recent unsuccessful ovulations. The average size of the largest follicle in these
females was only 37 cm., which is very similar to the average maximum follicle size (3-8 ±0-53 cm.)

J J A S
MONTHS

Text-fig. 44. Relation between month of conception and maternal age. Thin line, mean body length; thick line, resultant;
broken line, mean number of corpora. A, all pregnant females ; B, multiparous females.

in the ' recently ovulated ' group from antarctic waters (p. 348). This close agreement suggests that the
follicles are not maturing in preparation for a subsequent ovulation, but may be regressing following
the current ovulation. It is interesting that three of the recently ovulated females examined at Durban
had experienced multiple ovulations.

This material, while not providing very strong support for the thesis of monoestrous cycles, does
not contradict it.

The multiparous group may contain some 40 year classes. It has already been mentioned that the
' 3 corpora albicantia ' group conceptions tend to be earlier than those of the ' o, 1 and 2 corpora
albicantia' groups. One may ask whether individual females tend to conceive at a slightly earlier date
each year so that in general the oldest females are the first to ovulate each breeding season. We are
in a position to compare the average ages of females conceiving in each month by using corpora

438 DISCOVERY REPORTS

number and body length as indications of age. These two characters are shown in Table 18 and have
been plotted in Text-fig. 44. The 'resultant' of these two curves gives a smoothed relative age
distribution (thick line).

In the upper graph all sexually mature females are included. The mean age is highest for the mothers
of foetuses conceived in March/ April, declines through April/May conceptions and levels off in later
months. The mothers of foetuses conceived in the July/August period appear to have the lowest
average age, though this is perhaps unduly depressed by the low average length for this month.
DArcy Thompson (1952, p. 175) found a correlation between the size of the mother and the size
of the foetus in a sample from a given month, and remarked that this suggested a very considerable
growth of the mother during pregnancy. This correlation should, however, be found if, as has been
shown above, the older and larger females tend to conceive at an earlier date than younger, and in
general smaller, females. In any one month the foetuses of these older females would tend to be older,
and therefore larger than those of young females.

Table 18. Relation betzveen

time of

conception and maternal age

• (as expressed by

corpora numbers and

body length)

March/

Aprilj

May]

Junej

July!

August 1

September] October] i\

Jovembe

Period of conception April

May

June

July

August

September

October

November 1

~)ecembe

All pregnant females

Mean no. of corpora 18-7

12-9

8-8

9-4

8-7

8-4

8-6

10-9

5-8

Mean length (ft.) 73-3

71-9

7i-3

71-0

697

70-8

71-1

7°-5

7i-5

Sample size 20

170

223

159

101

Pregnant females with 3 or more

corpora

Mean no. of corpora 18-7

I3'3

10-2

u-3

13-5

n-4

12-5

14- 1

6-6

Mean length (ft.) 73-3

71-4

71-9

71-8

72-3

71-9

72-2

Sample size 20

164

191

J31

5°

In the lower graph primiparous females are excluded by omitting the ' o and 1 corpora albicantia '
groups from the calculations. The average age of females conceiving in March/April is again the
highest, but from May onwards the average age per conception month is more or less unchanged,
although there is a tendency for the average age to increase slightly up to September and October.
The November sample is small.

We may conclude then that for multiparous females in general age does not influence the time at
which conception occurs, although in the oldest females this appears to be important. Those which
mate in March and April are much older than those females which pair in later months. This point
will be of some importance when we come to consider the role of light as an exteroceptive factor
controlling the sexual cycle of multiparous females (p. 450).

The average duration of the gestation period is about 11 \ months and a curve showing the seasonal
distribution of calving has therefore been constructed by advancing the curve of conceptions by three
weeks (Text-fig. 43). This assumes that the rate of pre-natal mortality is the same for all foetuses
whatever the month of conception. It has been shown that the month of conception is partly related
to maternal age, but we do not know whether there are differential pre-natal mortality rates related to
maternal age. This factor may influence the shape of the estimated curve of conception frequencies
but probably not appreciably, and Text-fig. 43 is thought to give a good idea of the frequency of
births, which reaches a peak in April/May.

MULTIPAROUS FEMALES 429

POST-PARTUM HEAT

It has not been possible to study post-partum females directly, and we are again restricted to drawing
inferences from material collected in the Antarctic. Events during lactation are difficult to establish,
because lactating whales are now protected and therefore appear in the catches each year only in
small numbers. The present material includes 129 lactating female fin whales examined at South
Georgia (in earlier years) and on the pelagic whaling grounds.

Females simultaneously pregnant and lactating
For several Balaenopterid species there are records of females which are simultaneously pregnant and
lactating. This appears to be of most common occurrence in the minke whale. Jonsgard (1951) found
that in this species lactating females were invariably pregnant, and only 4-5 % of mature females were
neither pregnant nor lactating. Omura and Sakiura (1956) also concluded that the majority of minke
whales in Japanese waters become pregnant as a result of a post-partum ovulation. Chittleborough
(1958) gives data obtained by Norwegian workers on the incidence of pregnancy in lactating hump-
back whales and Symons and Weston (1958) give a few more records. In this combined sample there
are 23 lactating females of which nine, or 39% were simultaneously pregnant. Chittleborough also
points out that there are very few females in the resting condition. There appear to be no published
records of blue whales which were simultaneously pregnant and lactating, but there are in the records
of the National Institute of Oceanography references to two female blue whales which were pregnant
while lactating. This is evidently a very rare condition in the blue whale.

As regards the fin whale Hinton (1925, p. 124) refers to four fin whales which were simultaneously
lactating and pregnant, and Mackintosh and Wheeler (1929) stated that, although there were a few
records of lactating females which were pregnant, none of the lactating whales examined by ' Discovery '
Investigations at South Georgia was concurrently pregnant. They concluded that such cases are
extremely rare, but ' might arise if a female were impregnated near the end of a long period of lacta-
tion ' (p. 431). Wheeler (1930, p. 414) stated that seven out of 199 pregnant whales were also lactating,
and suggested that a post-partum ovulation may sometimes take place. In later seasons, as we shall
see, about one-fifth of lactating females examined at South Georgia were found to be simultaneously
pregnant, and Mackintosh (1942, p. 224) stated that there was some evidence that 'the occurrence of
whales simultaneously pregnant and lactating is also less rare than in former years '. Ruud (1945, p. 58)
remarked that 'nursing females with a foetus seem to be unknown', and Brinkmann (1948, p. 36)
gave details of a lactating fin whale with a 77-cm. foetus. He drew attention to the fact that no such
case had, so far as was known, been previously recorded. This appears to be the first detailed record
to be published, although at that time at least ten such females had been examined by 'Discovery'
Investigations (Table 19).

There are in the present material 129 lactating female fin whales examined between 1925 and 1958.
Of these 15, or n-6% were simultaneously lactating and pregnant (Table 19). This material has been
subdivided into four groups, the first two representing the work of ' Discovery ' Investigations at
South Georgia and the next groups representing the work undertaken by ' Discovery ' Investigations
and the National Institute of Oceanography in pelagic expeditions.

Some explanation of the meaning of this grouping is called for. At South Georgia up to the end of
the 1926/27 season, no lactating female had been recorded which was also known to be pregnant.
In January 1928 the first female which was simultaneously lactating and pregnant was recorded and
following this a much higher number of such females were found amounting to some 20% of all
lactating females examined. In the pelagic operations no females pregnant while lactating were found

430 DISCOVERY REPORTS

in 1939/40 and 1940/41, nor in the early post-war years, but in 1953/54 °f f°ur lactating females ex-
amined two were found to be simultaneously pregnant, and in subsequent seasons a further three
were recorded.

It is often said that females cannot be pregnant and suckling a calf at the same time, and the presence
of milk has been explained as a premature development of the gland. The Scientific Subcommittee of
the International Whaling Commission recently found it necessary to state that ' pregnant whales can
be simultaneously lactating and accompanied by a calf (International Commission on Whaling,
Seventh Report of the Commission, 1956. Appendix IV, Report of the Scientific Subcommittee, p. 22).
Chittleborough (1958, p. 15) also suggests that lactation may be overlooked in pregnant females. It
seems probable that lactation was overlooked in pregnant females in the pelagic samples up to 1952.
At South Georgia in 1925-28, however, there was probably a real absence of lactating pregnant
females (see p. 459).

Table 19. Proportion of lactating females which are simultaneously pregnant or recently ovulated

Lactating and pregnant Lactating and ovulation

Samples

Total
lactating

Lactating
only

No.

* ,

Percentage

{

No.

Percentage

South Georgia

1925-28

4-8

1928-31

19-6

Pelagic

I939-S2

3°

3-3

1953-58

15-6

ii-i

* Percentage calculated from columns 2 and 5 only, because lactating and pregnant females do not ovulate.

If we accept this explanation then the figure of 11 -6% for the proportion of lactating female fin
whales which are pregnant is too low. A more realistic figure is obtained if we eliminate the data
which are thought to be unrepresentative, and use only those from 1928-31 and 1953-58. In this
reduced sample there are 78 lactating females, of which 14, or 17-9%, are simultaneously pregnant.
The standard error of this percentage is 4-34, which means that the true percentage of lactating females
which are simultaneously pregnant probably lies between 9-2 and 26-6%. It is unfortunate that the
small size of the sample does not permit a closer estimate than this. It must also be pointed out that
the proportion of lactating females which become pregnant may vary from year to year and may
increase in response to exploitation. A discussion of the incidence of corpora lutea of ovulation in
lactating females will be postponed until the next section (on the post-lactation ovulation) for reasons
which will then be apparent.

For the 15 lactating females which were pregnant the foetal lengths are known. They range from

0-31 to 4-4 m.; two-thirds of them are between 1 and 2 m. in length, and the mean foetal length is

1-71 m., corresponding to a foetal age of 7 months. Mackintosh and Wheeler (1929), on the basis of

an examination of the sizes of calves and growth of the baleen, concluded that lactation lasts for

6 or 7 months; it is also shown below on other grounds that the calf is suckled for about 7 months.

The foetuses of females which are lactating must, therefore, have been conceived at a post-partum

ovulation.

Evidence from the sizes of corpora albicantia

Almost a fifth of lactating female fin whales appear to be pregnant as a result of a post-partum
ovulation. The question now arises whether only about one-fifth of mature females experience a post-
partum heat, or whether the majority of mature females experience a post-partum heat, but only
about one in five become pregnant, possibly owing to low fertility at this stage of the cycle.

It will be remembered that there is a group of recently mature females in the first lactation or post-

MULTIPAROUS FEMALES 431

lactation stages of the sexual cycle which have ovulated once only (Table 15). Thus in the first lactation
period a substantial proportion of females do not experience a post-partum ovulation, and in these
females there is only one corpus albicans, derived from the former corpus luteum of pregnancy. This
suggests that the first of the two postulates in the previous paragraph, namely that only a small
proportion of females experience a post-partum heat, is correct. It is, however, possible that the
sexual cycle of primiparous females differs in this respect from that of multiparous females (i.e. that
they are less fertile) and the evidence now to be presented suggests that this is so and that the majority
of multiparous females experience a post-partum heat.

This evidence concerns first, the sizes of corpora in the ovaries of lactating, ' resting ' and pregnant
females, and secondly, the morphology and histology of certain corpora in the ovaries of lactating females.

Measurements of corpora diameters made at South Georgia between 1925 and 193 1 comprise the
only consistent series which contains a fairly large number of lactating females. The methods of
measurement adopted by later workers vary, and since the methods were standardized in 1954 only
a relatively small number (32) of lactating females have been examined. Although the pelagic data
nearly double the size of the sample they also increase the variability, and only the South Georgia
material is used in the following discussion. Females which are simultaneously lactating and pregnant
are not included, for obvious reasons, and the remainder of the females for which corpora measure-
ments are available have been split into three groups according to whether they are pregnant, lactating,
or ' resting '. The frequency distributions of the diameters of the largest, second largest, third largest,
...up to the sixth largest corpora albicantia, have been obtained. From these the mean diameters
and standard errors have been calculated and are shown in Table 20.

Table 20. Mean diameter ±2 s.E. of corpus luteum and six largest corpora albicantia in the ovaries of
201 pregnant, 48 lactating and 59 'resting' females. The size of the corpus luteum is based upon a
much larger sample (p. 356)

Corpora albicantia

Sexual Corpus r — * >

condition luteum 123456

Pregnant 11-4410-15 5-04 + 0-13 4-0510-11 3-5910-11 3-4310-13 3-13 +0-19 3-0110-20

Lactating — 5-5810-20 4-3310-22 4-1510-18 3-3610-20 3-2810-31 3-0010-53

'Resting' — 5-5710-26 4-4210-22 3-98 + 0-24 3-6210-20 3-2010-20 3-1010-31

In Text-fig. 45 the results are presented graphically and each group has been plotted twice so as
to cover two reproductive cycles, or four years. It should be noted that this represents the average
reproductive pattern. Some of the pregnant group will, however, be animals which conceived as a
result of a post-partum ovulation, and therefore did not pass through the lactating and resting stages
before becoming pregnant as in the majority of cases. Furthermore, the group of resting females
includes some which have recently ovulated (see below, p. 436) and have a young corpus albicans in
the early rapid phase of regression, while in others this most recently formed corpus albicans has
undergone a much longer period of regression. These variations are a complication in the interpreta-
tion of the size distribution of corpora albicantia in this group.

One assumption is made, that with increasing age the corpus albicans progressively shrinks in size.
Consequently, if say the third largest corpus albicans in one group is larger than the third largest
corpus in the preceding group then the former cannot have been derived from the latter. Similarly,
if these two corpora are equal in size then one is unlikely to have been derived from the other because
it should have regressed by an appreciable amount in the intervening months. It is necessary again
to emphasize that the corpus luteum of pregnancy in the fin whale is much larger than the corpus
luteum of ovulation (11-44 cm- as compared with 8-28 cm.). Therefore, among corpora albicantia of

432 DISCOVERY REPORTS

similar age, those derived from corpora lutea of pregnancy should be larger on average than those

which are products of the regression of corpora lutea of ovulation.

Let us now attempt to trace the regression of corpora albicantia through successive phases of the
sexual cycle. The lines joining corpora in Text-fig. 45 present the conclusions; corpora known or
presumed to be derived from pregnancy corpora lutea are shown as black rectangles (shaded in the
case of resting females), and those presumed to represent ovulations are shown as white rectangles.
The evidence on which these conclusions are based is as follows.

120

2
<

R P

STAGE OF CYCLE

Text-fig. 45. Mean diameters + 2 S.E. of corpus luteum, and six largest corpora albicantia of pregnant, lactating1,
and ' resting ' females plotted to a time scale so as to represent two sexual cycles. See text for explanation.

The mean size of the largest corpus albicans in lactating females is 5-58 cm.; the mean size of the
largest corpus albicans in lactating females which are also pregnant (not given in Table 20) is 5-61 cm.,
and in ' resting ' females it is 5-57 cm. These mean sizes are not significantly different, and if we suppose
that there has been not more than one post-partum ovulation in lactating pregnant females, then
their largest corpus albicans must represent the corpus luteum of the previous pregnancy. The
largest corpus albicans in non-pregnant lactating females and resting females is presumed (because
of its closely similar size) also to represent the previous corpus luteum of pregnancy.

In pregnant females the largest corpus albicans must either represent the corpus luteum of the
previous pregnancy, or an unsuccessful ovulation before the current pregnancy. The latter case is
unlikely, because it would mean that the second largest corpus albicans of pregnant females represents
the largest corpus albicans of resting females, and has undergone rapid regression. It would also
mean that the fin whale is polyoestrous, with on average two ovulations in the breeding season, the
second of which leads to pregnancy, whereas the evidence points to a seasonally monoestrous cycle.

1 The lactating females are in late lactation (p. 445), so close to the resting stage.

MULTIPAROUS FEMALES 433

Moreover, if the species were polyoestrous, then in pregnant females the corpus albicans derived
from the corpus luteum of the previous pregnancy, in which regression should now be proceeding
at a much slower rate than at the beginning of regression, would then appear to have undergone much
greater shrinkage than a young corpus albicans from the first of the hypothetical two recent dioestrous
cycles. In fact the ovulation which preceded that which led to the current pregnancy almost certainly
occurred at the beginning of the resting period, and is probably represented by the second largest
corpus albicans in pregnant females (see below).

Now, if there is no post-partum ovulation in the majority of females and if those which do have
a post-partum heat usually become pregnant as a result, the second largest corpus albicans of non-
pregnant, lactating females should represent the further regression of the largest corpus albicans in
pregnant females. This also gives an acceptable rate of regression.

The third largest corpus albicans of lactating females should then be derived from the third largest
corpus of pregnant females (that is, the second largest corpus albicans, since the largest corpus is the
corpus luteum). It will be apparent from the figure that this is unlikely. The mean size of the third
largest corpus albicans of lactating females is actually about i mm. greater than that of the third largest
corpus of pregnant females and, taking into account the 95 % confidence limits, the maximum probable
rate of regression would be less than 2 mm. over a period of about 1 1 months. This is much too slow,
and we must conclude that the third largest corpus albicans in lactating females is the product of
the regression of an ovulation in the period between parturition and the latter part of the lactation
period. As we know that lactating females which are pregnant must have conceived at a post-partum
ovulation, it is probable that this third largest corpus albicans of non-pregnant lactating females also
represents a post-partum ovulation. In seven months it is presumed to have decreased in diameter by
50% (on average from 8-28 to 4-15 cm.) and in volume by about 87% (Text-fig. 8). This compares
with a decrease in the diameter of the regressing corpus luteum of pregnancy of 5 1 % ( 1 1 -44 to 5 -58 cm.)
and a decrease in volume of about 88%, over a slightly longer period. This close agreement between
observed and inferred rates of regression strongly supports the conclusion that post-partum oestrus
is a regular feature in the sexual cycle of the majority, if not of all multiparous fin whale females.

The fourth largest corpus albicans of lactating females is, therefore, likely to be derived from the
second largest corpus albicans of pregnant females, and this gives a reasonable amount of shrinkage
(about 7 mm. in diameter), associated with regression over about 11 months.

Let us now consider the resting females. Although this anticipates the next part of this paper, it is
more convenient to complete this discussion of the regression of corpora before turning to other points.
It has been shown that the largest corpus albicans in lactating females represents the former corpus
luteum of pregnancy, and it has been suggested that this is also the derivation of the largest corpus
in resting females. In the next section it is shown that the group of resting females includes some
which have recently ovulated, the ovaries containing an active corpus luteum, or a body partly
resembling a corpus luteum and partly a corpus albicans ; and others with a very large recent corpus
albicans. In this group the largest corpus albicans in some individuals will represent the former corpus
luteum, with a mean size slightly less than the largest corpus albicans in lactating females ; in other
' resting ' individuals the largest corpus albicans will be the product of a recent post-lactation ovulation.
Similarly, the size frequency distribution of the second largest corpus albicans in resting females will
include some which represent the previous corpus luteum of pregnancy, and some which are derived
from a recent ovulation. The effect of this should be to make the largest corpus albicans larger, and the
second largest corpus albicans smaller, than they should be when regression of the recently formed
corpus albicans is more advanced. In pregnant females there is no recently formed corpus albicans,
and the expected separation between the second and third largest corpora albicantia is found.

14-

434 DISCOVERY REPORTS

The second largest corpus albicans in resting females, therefore, represents a recent ovulation at
the beginning of the resting period (see below, p. 436, for other evidence of this ovulatory period),
which should have a mean diameter larger by probably about 1-2 mm. (The largest corpus albicans
in resting females appears to be approximately 1-2 mm. larger than expected by comparison with the
largest corpus in lactating females.) The third and fourth largest corpora are then seen to be derived
from the second and third largest corpora of lactating females, and become in turn the third and
fourth largest corpora albicantia of pregnant females, when they again show a relatively close size
grouping as do the second and third corpora of lactating females. Only in the fourth largest corpus
albicans in resting females has the line indicating regression not been drawn to the mean, but it is
within the 95 % confidence limits. In all other corpora groups the suggested regression lines are drawn
through the means, and give a consistent picture of rates of regression in size.

The second largest corpus albicans of pregnant females is now seen to be derived from the second
largest corpus albicans in resting females. If this resulted from an ovulation at the beginning of the
resting period, then it has decreased in size from 8-28 cm. in diameter to 4-05 cm. in about a year
(from the beginning of the resting period to the eighth month of pregnancy), that is by 5 1 % . This is
not in close agreement with the estimated average percentage shrinkage of corpus luteum of pregnancy
(51%), and post-partum corpus luteum of ovulation (50%), over a shorter period of time. It is
possible that the size regression of corpora albicantia is slower during pregnancy than during the
lactation or resting phases of the cycle. This is borne out by the regression in size of the largest corpus
albicans in primiparous females (which will represent an ovulation). When plotted according to the
time-scale established for foetal length, this declines from 5-3 cm. at the beginning of pregnancy to
about 4-1 cm. at term, and would explain the apparent discrepancy noted above.

A further point to be made is the relation of the fourth largest corpus albicans in resting females to
corpora albicantia in other groups. If we assume, for the purpose of the argument, that there is no
post-lactation ovulation in the fin whale, then the second and third corpora albicantia of resting females
should be derived from the second and third corpora albicantia of lactating females. This means that
the fourth largest corpus albicans of resting females does not fit into the pattern nearly so well ; its
mean diameter is 3-62 cm., larger than the size of the fourth corpus albicans of lactating females
(3-36 cm.), from which it should be derived according to this hypothesis. Together with the inde-
pendent evidence to be described below (p. 436) this indicates that a post-lactation ovulation is a
regular feature of the fin whale cycle.

Anomalous corpora albicantia of lactating females
Four lactating females were examined in 1953/54. Of these, two were simultaneously pregnant, and
one (no. 17 17) was primiparous with one corpus albicans representing the previous corpus luteum
of pregnancy. The fourth (no. 636), which was the only normal multiparous lactating female examined,
had 15 corpora albicantia in the ovaries, the largest of which was of the usual type, measuring 3-7 cm.
in mean diameter, and probably represented the previous corpus luteum of pregnancy. It was similar
in appearance to the single corpus albicans in no. 17 17, and to the corpora albicantia in other primi-
parous lactating females examined later. There was one anomalous corpus albicans in the ovaries of
no. 636, of a type which had not previously been observed in non-lactating females (Text-fig. 466).
This measured 3-4 cm. in mean diameter.

Subsequently, a further 18 non-pregnant lactating females and two pregnant lactating females were
examined. The corpora albicantia in the four pregnant lactating females were all of the normal type,
but of the 18 ' lactating only ' females (excluding two primiparous females with only one corpus albicans
of the normal type) nine, or 50%, possessed one of the anomalous corpora.

MULTIPAROUS FEMALES 435

This type of corpus albicans is found exclusively in lactating females and differs from the more
usual corpus albicans, both in its morphology and in its histology. The morphology is similar to that
of a corpus luteum of ovulation (Text-fig. 5) ; the mural luteal tissue tends to be thin and usually has
a relatively simple folded pattern, and not the very complicated arrangement associated with the
full growth and expansion of the corpus luteum. The central connective tissue core is correspondingly
simple, and clearly shows its derivation from the original cavity of the collapsed follicle. But the most
conspicuous feature is the colouring. This is usually a pale yellow or yellow-buff in colour, as com-
pared with the usually darker brown of the majority of the corpora albicantia. In this respect they
are similar to the corpora aberrantia which have been described above (p. 380), and which represent
former corpora lutea of ovulation. This gross resemblance is confirmed by the histological appearance.
The difference between this anomalous type of corpus albicans and normal corpora albicantia is
best seen in osmic-treated material (PI. V, fig. 5, cf. PI. V, fig. 6). In normal corpora albicantia
the osmic-staining lipoid material is evenly distributed in the hyaline collagen representing the former
glandular tissue, and is in granular form. In the anomalous corpora the lipoid material is usually in
the form of discrete globules of varying sizes. Where the globules are large the lipoid material occurs
at the periphery after fixation, and surrounds a central vacuole which was presumably fluid-filled

Text-fig. 46. Morphology of anomalous corpora of lactating females.

before treatment. There are also lipoid deposits in granular form as in the normal type of corpus
albicans, and these granules are more abundant in the peripheral parts of the corpus. The arrange-
ment of lipoid material around fluid-filled vacuoles is very similar to the condition of some of the
corpora aberrantia and atretica (see PI. VII, figs. 6, 7).

This similarity between the anomalous corpora albicantia of lactating females and the corpora
aberrantia and atretica is suggestive, and it is probable that these anomalous corpora represent
ovulations during lactation. The relative age of these corpora (as indicated by the amount of vasculariza-
tion for instance) appears to be very similar to the age of normal ' young ' corpora albicantia, from which
they differ mainly in the arrangement of the lipoid material. In view of this they do not represent recent
ovulations, towards the end of lactation, but probably are the products of post-partum ovulations.

The mean diameter of nine of these anomalous corpora was 3-8 cm. Considering the small size of
the sample, and the fact that the method of measuring may be slightly different, this is quite close to the
mean size of the third largest corpus (4-15 cm.) in the sample of lactating females from South Georgia,
which on other grounds was assumed to be from a post-partum ovulation. In the period of approxi-
mately seven months since its formation it had regressed by 5 1 % in diameter, which was shown to be in
close agreement with the rate of regression of the former corpus luteum of pregnancy during lactation.

About 1 8 % of lactating females are simultaneously pregnant, and of the remaining lactating females
about half are presumed (on histological grounds) to have experienced a post-partum ovulation.
Combining these data suggests that at least 60% of multiparous females experience a post-partum
ovulation. No allowance has been made for the possible variance of these small samples, which is
particularly large in respect of the incidence of anomalous corpora.

436 DISCOVERY REPORTS

These anomalous corpora are very similar histologically to the corpora aberrantia described above
(p. 380), but in size and gross morphology resemble normal corpora albicantia more closely. Like
the corpora aberrantia they probably represent former corpora lutea of ovulation which have under-
gone an aberrant type of regression. Not all corpora lutea of ovulation undergo this type of regression.
Nulliparous females, for instance, usually have normal 'young' corpora albicantia which cannot
certainly be distinguished from the single corpus albicans in primiparous lactating or resting
females.

Thus, it seems likely that more than two-thirds of multiparous females, possibly all, experience a
post-partum ovulation. Indeed, the size distribution of corpora described above could not be expected
to show such a clear pattern if only two-thirds of females experience a post-partum ovulation. In
primiparous females, however, there is evidence that a substantial number do not have a post-partum
ovulation.

Ovulation after abortion, stillbirth, or loss of calf

Chittleborough (1958) has examined six female humpback whales which showed anatomical
evidence of a recent birth, but in which the mammary gland was involuting, suggesting that the calf
had been lost at, or just after, birth. In five of these ovarian activity had recommenced; in three cases
mature follicles were present; in another ovulation had just occurred and in the fifth a developing
corpus luteum indicated a recent ovulation. This is compatible with a normal post-partum ovulation
since these calves were presumably very young, and a post-partum ovulation seems to be a not un-
common feature of the sexual cycle of the female humpback whale.

As regards the possibility of ovulation after the premature termination of pregnancy, another of
Chittleborough's observations is of interest. One of over seventy female humpback whales in late
pregnancy had a regressing corpus luteum and one mature follicle 4-8 cm. in diameter. This suggests
that the initiation of pro-oestrus changes is dependent on the regression of the corpus luteum of
pregnancy. It is unlikely that the fin whale is different in this respect. A further possibility is that
ovulation might closely follow abortion or foetal death in mid-pregnancy if this is also associated
with regression of the corpus luteum of pregnancy. It has been shown that there is a follicular cycle
during pregnancy in fin whales, with peak activity corresponding to a foetal length of 1-2 m. (p. 348).
The follicles enlarge at this time, but maturation and ovulation are suppressed owing to the presence
of an active corpus luteum. If for any reason, such as an abortion or foetal death, the corpus luteum
ceased to be functional at this stage of the cycle it might no longer suppress follicular maturation, and
ovulation might follow.

Kimura (1957) reports on a case of fin whale triplets in which two (measuring 19 ft. 8 in. and
15 ft. o in.) were necrotic and one (5 ft. 2 in.) was normal. This would seem to be a case of foetal
death of twins, followed by a further ovulation which initiated a second pregnancy, but it is not possible
to say what was the interval between the death of the twins and the new conception. It may have been
quite short, but alternatively the further ovulation may have been delayed until the next ovulatory
period. The latter would seem to be the more probable sequence.

We may conclude that the loss of a near-term foetus, a stillbirth, or the loss of a young calf, will
probably be followed by an oestrous cycle comparable with normal post-partum heat. The termination
of pregnancy by foetal death or abortion at an earlier stage will most likely be followed by ovulation
at the next ovulatory period.

Post-lactation heat

In the humpback whale the lactation period lasts io| months, weaning occurs on average at the end
of June and the majority of females are in oestrus between July and September, with pro-oestrus most
common in July. The female is not usually in anoestrus after lactation, and in some cases there is

MULTIPAROUS FEMALES 437

a recrudescence of ovarian activity before the end of lactation. Chittleborough (1958), found that in
this species 18% of females in late lactation had maturing follicles or had recently ovulated.

In the fin whale the lactation period is shorter, and weaning probably occurs on average in December
(see below, p. 446); pairings are not frequent until May. There is, however, strong evidence to show
that, as in the humpback whale, there is an ovulatory period just after lactation, and that some females
may undergo oestrous changes and ovulate in late lactation. Some 20 % of female fin whales in late
lactation have maturing follicles in the ovaries (over 3 cm. in diameter (Text-fig. 4)), and some 5%
(4-6±4-2) of lactating females have recently ovulated, as evidenced by the presence of a corpus
luteum of ovulation in the ovaries (Table 19). This is in close agreement with Chittleborough's
findings in late-lactation humpback whales.

The majority of lactating fin whales found in antarctic waters are in late lactation, and are very near
to the time of weaning. This is discussed in more detail in the next section (p. 445). The evidence as
to the size of the calf at weaning, the foetal age in pregnant lactating females, and the lower incidence
of diatom infection, all points to this conclusion.

As Mackintosh and Wheeler (1929) showed, the period of lactation is succeeded by a ' resting ' period
of anoestrus which lasts until the following winter. However, when we examine the records for females
taken in the Antarctic which are neither lactating nor pregnant, and which should, therefore, be in the
Vesting' condition, we find that a proportion of them have recently ovulated. So as to minimize the
possibility of including pregnant females (perhaps with small foetuses, or aborted foetuses) in this
sample, the material on which the following discussion is based is restricted to whales which were
examined personally by the biologists. Where a corpus luteum was seen but no foetus or embryo was
found the uterus was searched. Although some females in early pregnancy may be included in this
sample, their numbers must be very small.

The greatest numbers of recent ovulations are recorded from January (Table 22), a month in which
it is estimated that very few conceptions occur (Text-fig. 31). Apart from the care taken to include
only those females in which it is reasonably certain that no embryo was present there are two facts
which confirm the validity of the sample. The evidence of the mean size of the corpus luteum in these
whales, which is significantly smaller than the mean size of the corpus luteum of pregnant females
(p. 356), and the mean size of the largest follicle, which is significantly greater than the mean size of
the largest follicle of pregnant females (p. 348) confirm that most, if not all, of these recent ovulations
are correctly diagnosed.

In the material up to 1958 there are 465 non-pregnant, non-lactating females which fulfil these
conditions and of these 59 or 127% had recently ovulated before death. This figure needs some
adjustment, because the discrepancy between the early period of the investigation at South Georgia
and the later seasons suggests that in the early seasons at South Georgia recent ovulations may have
been under-represented. Thus, in the four seasons 1924-28, some 55 non-pregnant, non-lactating
females are recorded, but no recent ovulations; in the three seasons 1928-31 eight out of 51 such
females had a corpus luteum of ovulation in the ovaries (157%). If these 55 records are eliminated
there are 410 non-pregnant, non-lactating females, of which 59 or 14^3-5% are deemed to have
had a corpus luteum of ovulation in the ovaries at the time of capture. It makes little difference
to the argument below whether or not we restrict the sample in this way. Another fact which should
be recalled is that, although the mean size of the largest follicle of ' resting ' females is similar to
that of lactating females (Text-fig. 4), the maximum follicle size of 'resting' females is 8 cm., only
slightly less than the largest follicles in recently ovulated females, whereas the maximum follicle size
in the sample of lactating females was about 5 cm. This suggests that some ' resting ' females are in an
immediately post-oestrus condition. Although there are a number of 'resting' females which have a

438 DISCOVERY REPORTS

corpus albicans in the early stages of regression, occasionally with some yellow glandular tissue
remaining, in no case is such a young corpus albicans associated with a corpus luteum of ovulation.
This is valid evidence for a monoestrous cycle at this time, as in females at puberty (p. 416).

The records of the incidence of diatom infection show that the ovulation which gives rise to this
corpus luteum occurs at about the time of the entry into antarctic waters of the so-called ' resting '
females. Diatom infection has been assessed as absent, incipient, moderate, and extensive, and the
results are shown for 268 lactating, recently ovulated or 'resting' females in Table 21. Females in
which the diatom film is absent or incipient have probably been south of the Antarctic Convergence
for a month or less (Hart, 1935). Of lactating females 70-9 ± 10-5 % fell into one or other of these two
categories, and of recently ovulated females 7i*4±iS"3%. In contrast to this low incidence of diatoms
in lactating and recently ovulated females, only 46-2±8-2% of 'resting' females fell into these two
categories. This difference is statistically significant at the 95 % level.

These figures strongly suggest that this ovulation occurs at or very soon after the end of lactation,
and the approximately 5 % of lactating females which had recently ovulated presumably represent
a premature ovulation at this time as in the humpback whale.

Table 21. Incidence of diatom infection in three classes of fin whale females

Lactating

Ovulation

Resting

A _

Diatoms

No.

Percentage

No.

Percentage

No.

Percentag

Absent
Incipient
Moderate
Extensive

38
23
13
12

44-2
26-7
15-0
14-0

7
6

Si-4

20-0
I7-I

n-4

37
31
3°
49

25-2

2I-I

20'4

33-3

Total

99-9

147

ioo-o

Table 22. Monthly frequency of recent ovulations in mature non-pregnant,
non- lactating fin whale females {Antarctic)

October

November

December

January

February

March

April

Total

Resting

35i

Ovulations

Total

126

106

410

Percentage

ovulations

25-0

33'3

26-3

21-4

8-5

8-8

o-o

14-4

2 S.E.

43-2

18-0

H-3

7-3

5-4

6-4

—

3'5

It is now possible to test the hypothesis that female fin whales experience a monoestrous cycle at
the time when they are weaning or have just weaned the calf, shortly after entering antarctic waters,
by examining the monthly incidence of recent ovulations in the Antarctic. This is set out in Table 22
for a sample of 410 non-pregnant, non-lactating fin whales, taken between October and April over
a number of years. The proportion of females with a corpus luteum of ovulation in each month declines
from one-third in November to none in April. The standard errors of these percentages have also
been calculated, and the results are shown graphically in Text-fig. 47. Owing to the small size of the
monthly samples the standard errors are large, and the only samples which show a significant dif-
ference in the incidence of ovulations in successive months are those from January and February,
March and April. However, when the percentages and standard errors are considered as a whole the
decline from November to April cannot be disputed.

A straight line has been fitted to these points by inspection, and extrapolated to give a value for
September. The justification for extrapolating for the September value will become apparent during
the ensuing discussion. There is, of course, no certainty that a straight line best describes the monthly

MULTIPAROUS FEMALES 439

incidence of ovulations, and it is possible that a sigmoidal curve, or an irregular curve, as well as giving
a better fit, might be nearer to the truth. Calculations have, therefore, also been made using a sigmoid
curve to estimate the monthly incidence of ovulations, and also using the actual means of the samples.
It makes little difference to the following discussion which fit is adopted, and the straight line shown
in Text-fig. 47 is used below, because it probably gives the most likely value for September.

It is supposed that the numbers of fin whales south of the Antarctic Convergence are at a minimum
in July and August and then build up to a maximum in say February (see Mackintosh, 1942, p. 270;
Mackintosh and Brown, 1956, fig. 2; and evidence from the catch statistics). The numbers of non-
pregnant, non-lactating females in the Antarctic will follow a similar pattern though later in time
(Text-fig. 48 b). According to the hypothesis under consideration, these females ovulate either shortly
before or soon after their entry into the Antarctic population. A small proportion of the fin whale
population probably overwinters in antarctic waters (Hart, 1935, p. 276; Mackintosh, 1942, p. 250),
and it follows that apart from these, all non-pregnant, non-lactating females present in the antarctic

111

£T
UJ

au -
70-

60-

50-

40-

30 -

20-

10 -
O -

1 1 —

— 1 —

^w-

SONDJ FMAM

MONTHS

Text-fig. 47. Monthly percentages ( ± 2 s.E.) of recent ovulations in antarctic waters.

in September should have ovulated recently. In the following months there will be an increasing
influx of new arrivals which are expected to ovulate just before, on arrival, or soon after arrival, but
in successive months there will also be an increasing accumulation of females which have been in
antarctic waters for some time, and have ovulated some time before. It is, therefore, to be expected
that the monthly proportion of recent ovulations would decline as the number of truly 'resting'
females in the population increases, and this is in fact what the actual figures show.

It has been pointed out that in September all but the small proportion of non-pregnant females
which have remained south of the Antarctic Convergence during the winter months, or have migrated
into the Antarctic before September, should have recently ovulated. In fact Text-fig. 47 shows less
than half of these females to have a corpus luteum of ovulation. So far we have not considered the
length of life of the active corpus luteum of the cycle, but this is an important factor which will affect
the figures for the incidence of ovulations. Thus, if the corpus luteum persists in a recognizably active
form for a month, the figures given in Table 22 and Text-fig. 47 will represent the monthly frequency
of ovulation, but if, for example, the corpus luteum persists for only 2 weeks after entry into the whaling
grounds, then the observed frequencies of corpora lutea of ovulation must be doubled to give the true

monthly frequency of ovulation. This would give an estimate of 92% for the incidence of ovulations
in September, which is probably nearer the true proportion.

The life of the corpus luteum of the cycle as in other mammals is likely to be nearer half a month
than a month. Thus, Eckstein (1949, p. 400) remarks that: 'The life span of the c.l. in different
species is remarkably uniform and independent of body size. The range of variability encountered is
about 10-20 days (the upper limit being represented by the cow), but in the great majority of animals
it is probably of the order of only 10-15 days.' Harrison (1948, p. 323) also states that regression
begins 10-18 days after ovulation. There is no reason for supposing that pseudo-pregnancy is a feature
of the reproductive cycle of whales, and there are several good reasons for supposing that it is not.
While definite proof is lacking it is highly probable that the corpus luteum of ovulation in the whale
persists in a recognizably active state for a period of between 15 and 20 days.

Table 23. Monthly percentage of adult females pregnant ; South Georgia 1925-31,

pelagic 1932-52

South Georgia Pelagic

, * , , * ,

Month No. % No. %

September 1 (ioo-o) — —

October 40 85-0 — —

November 86 77-9 — —

December m 82-0 131 79-4

January 134 70-1 336 64-3

February 81 49-4 320 67-8

March 65 32-3 239 51-9

April 30 26-7 72 7-0

May 2 (5°'°) — —

550 64-9 1098 607

We may now proceed to test the hypothesis concerning this post-lactation ovulation, using some
actual figures to compare the cumulative curve of ovulations with the increase in the population of
' resting ' females in antarctic waters. The results of these calculations are presented in Table 24 and
illustrated in Text-fig. 49.

As a basis for the calculations it has been assumed that the catch at South Georgia in the eight
seasons 1927-35 gives a reasonably accurate picture of the monthly variation in numbers of the
antarctic fin whale population. The figures for the pelagic catch cannot be used, because in recent
seasons there have been no catches before December or January ; and in earlier years the catches are
not considered to be representative of the population present, because of the selection of the more
valuable blue whale, so that the earlier months are under-represented (see Mackintosh, 1942). The
calculations have been repeated for the eight post-war seasons, 1948-54, 1955-57, at South Georgia
(the season 1954-55 being excluded, because it was clearly anomalous with peak catches of fin whales
in October and November). The results are similar to those for the earlier period.

The monthly percentage of females in the catch is fairly constant, and on average slightly less than
50%, though it varies between 40-54% (from Mackintosh, 1942, table 25). The catch at South
Georgia in 1927-35 is here taken to represent the variation in numbers of females. The monthly
percentage of immature females (Table 24, column (2)) is taken from Mackintosh (1942, table 26b),
and an arbitrary figure allowed for September. This permits the approximate numbers of mature
females to be calculated (column (3)). The monthly percentage of non-pregnant mature females in
the catch (shown in column (4)), is obtained from Table 23, Text-fig. 48 a and enables the catch of
non-pregnant mature females to be estimated (Table 24, Text-fig. 486). The monthly percentage of

MULTIPAROUS FEMALES

441

Table 24. Monthly frequencies of non-pregnant mature females at South Georgia (1927-35) and the
estimated cumulative frequencies of ovulations in this class assuming a corpus luteum life of 15 or 20 days.
See text for explanation

C.L.O.

15 days

C.L.O.

20 days

No. non-

No. of

No. mature

pregnant

ovulations

No. of

Percentage

from (1)

Percentage

from (3)

Percentage

from (5)

ovulations

Cumulative

ovulations

Cumulative

Month

Catch

immature

and (2)

non-pregnant

and (4)

ovulations

and (6)

(7)X2

frequency

(7)x i'5

frequency

(1)

(2)

(3)

(4)

(5)

(6)

(7)

(8)

(9)

(10)

(")

September

195

(20-0)

156

(10-0)

(46)

1 1

October

1348

24-1

1013

150

152

122

136

102

November

1930

15-2

1637

22'I

362

121

242

378

181

283

December

2919

18-6

2376

18-0

428

1 11

222

600

166

449

January

37H

30-7

2574

29-9

77°

154

308

908

231

680

February

2136

44'5

1185

50-6

600

■3

156

1064

117

797

March

879

46-0

475

67-7

322

831

April

208

33'3

139

73'3

102

831

100

> 30-

7\\

' \ s

/ \ ^

\ x

£20-

/ I
A 1

\ \

/ J

\ \

111

\ V

\ *>

\ s

zio-

V N

/ /

\ \

/ J

/ /'

r> -

1 : — 1 — — — r— — — r

r— - —

D J F

MONTHS

O N

D J
MONTHS
b

Text-fig. 48. a, Monthly '% pregnant', South Georgia 1925-31 (full line), pelagic 1932-52 (broken line), b. Monthly
frequency of pregnant (full line) and non-pregnant females (broken line) in the South Georgia catches 1927-35.

recent ovulations (uncorrected for the active life of the corpus luteum), is then obtained as described
above (Text-fig. 47), and the number of recent ovulations observed in each month (column (7)) is
obtained by applying these percentages to the estimated number of non-pregnant females in the catch.
The question of the proportion of lactating whales in the monthly samples is discussed in the next
section (p. 448), and it is shown that there are relatively large numbers at South Georgia from
December onwards, but that very few enter the pelagic grounds until January or February, having
weaned the calf before entering colder waters. Those lactating females which do enter the catches are
either about to wean, are weaning, or have just weaned, the calf (see below, p. 445). For present
purposes lactating females are, therefore, included in the non-pregnant group. Columns (8) and (10)
show the estimated numbers of ovulations on the assumption that the corpus luteum is recognizable
as such in females taken on the whaling grounds for 15 or 20 days respectively, and in columns (9)
and (11) the cumulative frequencies of recent ovulations are shown.

If we are correct in postulating that new arrivals to the non-pregnant fin whale female population
in the Antarctic ovulate and then enter the true 'resting' state, then the cumulative figures for the
number of ovulations should correspond to the build-up of the antarctic population of 'resting
females. Unfortunately, we have no data on the actual numbers of animals in the population, but for
present purposes we may assume that the monthly catches correspond to the relative abundance in
the sea. The catching intensity is probably rather less at the beginning and end of the whaling season,
but this does not affect the general argument. In Text-fig. 49 the catch of non-pregnant females is

15-2

442 DISCOVERY REPORTS

compared with the estimated cumulative frequencies of ovulations, the upper limit of the shaded
portion representing a corpus luteum life of 15 days and the lower representing a life of 20 days. It is
apparent that there is a reasonably good correlation between these curves, and a cumulative curve of
ovulations may be taken to represent the entry of 'resting' females into the antarctic population.

The best agreement is obtained if the centre of the shaded area, corresponding to a corpus luteum
life of 17-18 days, is used. Up to January there is fairly close agreement, but after this the numbers
of non-pregnant adult females in South Georgia waters fall off. Probably very small numbers arrive
in the Antarctic after March.

1000-

>
u

ui
a.

500

D J

MONTHS

Text-fig. 49. Thick line, catch of non-pregnant females, South Georgia 1927-35, from Text-fig. 48. Shaded area represents
estimated cumulative frequency of ovulation for corpus luteum life of 15-20 days. See text for explanation.

According to these calculations 50% of non-pregnant females are south of the Antarctic Convergence
by mid-December, and almost all have arrived by the end of March. As regards the true monthly
frequency of this summer ovulation, December may, therefore, be considered as the median month.
This is in reasonably close agreement with the cycle of ovarian activity in pregnant females, which
shows a peak in November/December (see p. 348, Text-fig. 4). Pregnant females enter antarctic
waters about a month in advance of non-pregnant females (Text-fig. 486), and it would seem that
in this class also ovarian activity is correlated with the southward migration. It will also be remembered
that a similar correlation was demonstrated for some nulliparous females at puberty. We will return
to this interesting point later (p. 450).

The main purpose of this brief discussion has been to show that the estimated cumulative frequency
of ovulations corresponds fairly closely with the ascending limb of the curve showing the catches of
non-pregnant mature fin whale females at South Georgia, and therefore supports the hypothesis put
forward above concerning an end-of-lactation, or post-lactation, ovulation. The catch statistics show
that the peak in the pelagic catch of fin whales is usually a month later than the peak numbers at
South Georgia. This island ' occupies a peculiar position where Antarctic conditions extend into a

MULTIPAROUS FEMALES 443

comparatively low latitude, and Fin whales may be plentiful there before they have reached the
higher latitudes elsewhere. It is not until about the New Year that the big herds of Fin whales make
their appearance on the pelagic grounds' (Mackintosh, 1942, p. 272, and his tables 23 and 24).
Rayner (1940, p. 261) showed that fin whales marked near Shag Rocks (just west of South Georgia)
were not taken by the South Georgia whalers, but some were taken further south on the pelagic
grounds. Fin whales marked and recovered on the South Georgia whaling grounds are found to
belong to migrating herds which stop to feed in these waters, averaging about 15 days in the area.

Similar calculations may be made, basing them on an arbitrary pelagic population, the monthly
frequency curve being similar to that for South Georgia, but attaining peak numbers a little later.
There is again close agreement between the ascending limb of this curve and the cumulative frequency
of ovulations estimated from it, and the cumulative curve again attains the 50% level just before mid-
December.

This hypothesis is not entirely satisfactory in detail. A point which may be raised is that if, as a rule,
non-pregnant females ovulate after arriving in antarctic waters, then more cases of very recent ovula-
tions should have been observed, in which the follicle is still in the initial collapsed state, or the corpus
luteum is in the initial phases of development (see p. 354, Text-fig. 5 a) and has not filled out. Let us
suppose that this initial stage lasts about 8 days as in certain ungulates (Harrison, 1948, p. 315). Then
if ovulations occur on the whaling grounds some 44% of observed corpora lutea of ovulation are
expected to be in this initial phase. Allowing for the large standard error of this percentage a minimum
of 16 out of the 59 corpora lutea recorded should have been in this condition. The very early stages,
more easily recognizable to observers, should be proportionately fewer. Since the present investiga-
tion began in 1954 only 10 recent ovulations have been recorded, and two of these were in the early
stages, with the corpus luteum presenting a folded and unexpanded appearance, the original follicle
cavity still being discernible (Text-fig. 56). This suggests that they were less than a week old.
A number of the early records also note that the corpus luteum looks very young, but fuller details
are lacking. It is, therefore, uncertain whether the earliest post-ovulation stages have been observed
in antarctic waters, and it is likely that this ovulation usually occurs just before the entry of these
females into the whaling grounds. Some 80% of lactating females are believed to wean their calves
before they appear on the pelagic grounds (see p. 450).

It is clear that this problem of the precise relationship of the summer ovulatory period to the
lactating and ' resting' phases of the sexual cycle is complex. There can, however, be little doubt that
in the fin whale there is as a rule an ovulatory period at the end of, or just after, lactation as in the
humpback whale. In contrast to the humpback whale, and related to the shorter duration of lactation,
this ovulation in the fin whale occurs during or after a southward migration to the Antarctic, instead
of being associated with a northward movement to warm waters.

Almost without exception it appears to be an unsuccessful ovulation, but there are a few foetuses
estimated to have been conceived at this time, in some cases possibly in antarctic waters (p. 403).
There are also a few observations of pairing between baleen whales in polar waters in summer.
Nishiwaki and Hayashi (1950) described copulation of two humpback whales in antarctic waters in
January, and a similar observation was made from a whale catcher by a British Whaling Inspector
(J. E. P. Brass) in December 1934, in 6o° S., 950 E. ' I also had the experience of seeing two whales
copulating. The pair came to the surface on their sides with flippers securely interlaced' (MS. notes).
Unfortunately he gives no details and does not record the species. There are other closely similar,
but less reliable accounts by whalers of fin and blue whales seen in coition in antarctic waters. Hinton
(1925) refers to reports by whalers of pairing observed in the summer months in the North Atlantic
(fin and blue whales off the Finmark coast, pp. 1 18-19, 141). These accounts strongly suggest that

444 DISCOVERY REPORTS

in Balaenopterids not only oestrus and ovulation, but occasionally mating and conception, may occur
in polar waters in the summer months. It would appear that at most only about 6% of all conceptions
occur in this way (Table n, October-March conceptions). This is correlated with the observation
that the great majority of male fin whales examined in antarctic waters are found to be in full anoestrus

(P- 396)-

The lactation period

Text-fig. 35 (p. 410) illustrates the cycle of activity of the mammary gland. Attention has already been
drawn to the relative thinness of the mammary glands of nulliparous and primiparous females, and to
the fact that after its expansion during the first lactation period the mammary gland does not return to its
former size, but decreases to a depth of about 5 cm. in primiparous ' resting ' females and in second-
pregnancy females. This figure also suggests that in lactating multiparous females the mammary
gland is rather thicker than in primiparous females, although the data are too small to allow definite
conclusions to be drawn.

In multiparous females the mammary gland in full lactation averages 20 cm. in depth (range
10-30 cm.); the lobules of glandular tissue with expanded alveoli are large, and the connective tissue
is arranged as relatively thin supporting septa. In pregnant females and ' resting ' females which have
experienced at least one lactation period, the glands are either involuted or intermediate between this
condition and the lactating condition. The 'intermediate' glands are then about 7-1 1 cm. thick,
brownish in colour with large lobes of alveolar tissue and relatively small amounts of connective tissue
(Mackintosh and Wheeler, 1929, fig. 137). In the involuted mammary gland the brownish alveolar
lobes are smaller than in the ' intermediate ' gland, and the connective tissue framework is corre-
spondingly more conspicuous (Mackintosh and Wheeler, 1929, fig. 138); the thickness of the gland is
usually from 4 to 8 cm. There is little chance of confusing a gland in this condition with an immature
gland, because both thickness and colour are usually very different.

Another group is shown in Text-fig. 35, which has been termed the 'end of lactation' group, and
some explanation is necessary. Chittleborough (1958) noted that after lactation has ended, when
involution of the gland is well-marked, there may be liquid in the lacteal ducts, which is usually a
whitish or turbid yellowish thin fluid. There are 22 fin whales in the present material which have
mammary glands in this condition. They are considered to be involuting after the successful termina-
tion of lactation or following loss of the calf. They range in thickness from 7 to 17 cm. (mean 1 1 -i cm.)
and are shown in Text-fig. 35 as an 'end of lactation' group.

It will be noted that the upper part of the histograms showing mammary gland depth are closely
similar in both the ' resting ' and pregnant groups of females, and overlap the values for the ' end of
lactation' group, and even the two lowest values in the lactating group. This is to be expected in the
case of the resting group which normally follow on after weaning; the thicker glands in the pregnant
group must similarly be considered to represent females which became pregnant at a post-partum
or post-lactation ovulation. The estimated foetal ages for these females agree with this interpretation.

The criterion of lactation adopted here is the presence, in the mammary glands or ducts, of milk
which is apparently normal in colour and consistency. Usually the appearance of the cut gland is
also diagnostic. The quantity of milk present is not important, because it will vary according to the time
elapsed since the calf was last fed. As was noted above the presence of milk is usually, but not invariably,
associated with mammary glands which are thicker than those of non-lactating females (Text-fig. 35).

However, the presence of milk or gross appearance of the gland are not completely valid criteria
of lactation because some females diagnosed as being in full lactation are found, on histological
examination, to have stopped active secretion of milk. Van Lennep and van Utrecht (1953) have shown
that of 69 females (mainly blue and fin whales) said on these grounds to be lactating, histological

MULTIPAROUS FEMALES 445

criteria showed that a substantial proportion were either not lactating or were in a doubtful condition.
Chittleborough (1958) has also distinguished on histological grounds two groups of females, each
with apparently normal milk in the glands. When the cells lining the alveoli were actively secreting
the female was classified as still suckling a calf, but if the lacteal ducts contained milk and the alveolar
cells were no longer secreting, then it was considered that ' the female had either recently lost, was
weaning, or had just finished weaning the calf, and that the apparently normal milk present in the
ducts was a residuum which would shortly have disappeared' (p. 7).

Of the 69 females examined by van Lennep and van Utrecht (1953) four humpback whales and
a sperm whale should be excluded from the present discussion because in these species the calf is
usually weaned in low latitudes. Of the remaining 64 fin and blue whales, 41 were held to be lactating,
six definitely not lactating, and 17 could not be definitely assigned to either of the first two groups.
In some of the material in the third group fixation was bad; some of these whales were thought to
be weaning the calf; and at least two were thought to be pathological. We are not likely to be far
wrong if we assume that about half of the females in the doubtful group were weaning the calf. Then
for 41 females known to be lactating there are 14 which are thought to have just ceased to secrete
milk, that is about 25 %. Even if the doubtful group is excluded, there is a minimum of 6 out of 47
(or 12-8%) which were no longer secreting milk. On the west Australian coast Chittleborough (1958)
found 23 % (5 out of 22) of female humpback whales with milk in the glands to be in this condition.
Lactating females appear in the catches off the west Australian coast shortly before weaning, and the
period after secretion has ceased when normal milk is still present in the glands, is almost certainly
very short. It is interesting to note that the lactating female fin whales taken in antarctic waters have
probably been on the whaling grounds for less than a month, possibly only for 2 weeks. This con-
clusion receives support from the results of the analysis of the incidence of diatom infection (Table 21).
In some 71 % of lactating females diatoms are absent or incipient, showing that the majority of lactating
females in the sample have entered the Antarctic recently, probably less than a month before their

capture (Hart, 1935).

Further support comes from an analysis of the foetal lengths of those lactating females which are
also pregnant. The work of Mackintosh and Wheeler (1929) strongly suggested that the lactation
period was about 6-7 months, and this estimate cannot be very far out. In fact it is in very close
agreement with the conclusions reached below. The average foetal length will give us the average
foetal age for this class of females, and will enable us to see how near this group of females is to
weaning the calf. It is reasonable to assume that the lactation period is no longer in pregnant lactating
females than in non-pregnant lactating females, and that in other respects the behaviour of these two

groups is similar.

There are 15 fin whale females in the material which are concurrently pregnant and lactating. The
foetal lengths range from 3-1 to 4-4 m. with a mean length of 1-69 m., and a median length of 1-58 m.,
corresponding to foetal ages of 7-3 and 7-1 months. Of these 15 foetuses, 12 are between 1 m. and
3 m. in length; the largest at 4-4 m. is equivalent to a foetal age of 10 months, and the two smallest
measuring 31 cm. and 76 cm. represent ages of 2-3 months and 4 months respectively. If these three
foetuses are excluded then the mean length, i-66 m., corresponds to a foetal age of 6-95 months, which
is probably a better estimate.

The foetuses of lactating females are conceived at a post-partum ovulation, which on average
follows closely on the mean calving date at the end of May (p. 403). The lactating females are very
near weaning time and allowing about 7 months for the length of the lactation period (to account for
the mean foetal age) suggests weaning at the end of December. Mackintosh and Wheeler (1929,
pp. 431-7) estimated that the average length of the calf at weaning is probably about 12 m. in the

446 DISCOVERY REPORTS

southern hemisphere fin whale. This estimate was based on an apparent increase in the rate of growth
of the baleen plates at weaning, and on the sizes of the largest suckling calves and the smallest inde-
pendent calves. There is no additional information to give us cause to modify this estimate, although
it should be noted that Chittleborough (1958) found no such increase in the growth of baleen in the
humpback whale. By plotting the lengths of small fin whales against the time of capture Mackintosh
and Wheeler were able to extend their average curve of foetal growth to the lactation period, and
found that it attained the level of 12 m. in the first week in December. In the same way they estimated
that in the blue whale weaning occurs at an average length of 16 m., which in this species also is
attained in December. These authors, therefore, assumed that weaning occurs on average in Decem-
ber, and they pointed out that in each of these species there is a regular influx to South Georgia
waters, mainly from January onwards, of small whales, many of which have probably just recently
been weaned.

A short paper by Ash (1956) also suggests that weaning occurs on average in December. He
expressed the increase in fatness of fin whales by plotting the blubber ratio (average blubber thickness
in cm. /length of whale in feet) against time. The rate of fattening is fairly constant during the 10-week
period covered by the data. Males and non-pregnant females are represented by curves which are
almost identical; the curve for pregnant females is well above the curve for non-pregnant females,
but is nearly parallel to it, and lactating females are seen to be very lean. The average blubber ratio
of the five lactating females given by Ash is 0-279. If we assume for the reasons given above that
lactating females are very near to weaning, then this figure is probably very close to the average
blubber ratio for non-pregnant females when they first enter the antarctic population (because the
non-pregnant group is largely, if not entirely, composed of post-lactation females). When the fatness
curve for non-pregnant females is extrapolated backwards in time to a value of 0-279, tms *s found to
correspond to the third week of December. This evidence again suggests December as the average
month of weaning.

It will also be remembered that the cumulative curve of ovulations which is held to correspond to
the change from lactation to the 'resting' phase reaches the 50% level in December (p. 442).

These several estimates all suggest December as the average month of weaning for the southern
hemisphere fin whale. However, when we examine the incidence of lactating females on the whaling
grounds, we find that rather small numbers of lactating females figure in the catches for the early part
of the season, and are at a maximum towards the end of the season. Thus, at South Georgia, between
1925 and 1931, out of 459 females examined closely, 68 or 14-8% were found to contain apparently
normal milk in the mammary glands, but when the monthly proportion of lactating females is examined
there are found to be about 5 % of mature females in October and November, rising to 44% in March
(Text-fig. 50). If weaning occurs on average in December, then most lactating females should be
taken in the early part of the season, and by March very few unweaned calves should be left. The fact
that the bulk of lactating females in the catches are taken late in the season strongly suggests that in
the earlier months lactating females do not enter the whaling grounds in representative numbers, but
in fact wean their calves before entering colder waters.

Mackintosh and Wheeler (1929) also commented on the fact that the behaviour of lactating females
as a class differs from that of non-lactating females. They also suggest that for part of the nursing
period the lactating females are segregated from the main herds, so that not all lactating females appear
on the whaling grounds. These authors suggest that lactating females are slower on migration than
non-lactating females, and this is borne out by Chittleborough's observations on humpback whales
(^SS) P- 222)- Mackintosh and Wheeler (1929) point out that the killing of females accompanied by
a calf is prohibited in the Falkland Islands Dependencies; according to the whalers young calves are

MULTIPAROUS FEMALES 447

rarely seen in the Dependencies, though relatively common off the South African coasts (p. 433).
They also believe that in some cases ' the calf is weaned on the small and rather scarce krill ' in South
African waters 'and remains in the northerly regions for the first summer' (p. 437).

It is not at all improbable that fin whale calves should be weaned in regions which are not very rich
in plankton. Thus, we can be certain that humpback whale calves are almost invariably weaned at the
end of a northward migration, in waters relatively poor in plankton (Chittleborough, 1958). The minke
whale provides a better parallel with the fin whale. Lactating female minke whales are not found
in the Arctic, although they are found in Lofoten waters in small numbers, and Jonsgard (195 1)
suggested that most are weaned before they immigrate to Norwegian waters from lower latitudes.

It is suggested that in the fin whale the calf is weaned on average in December, and that in the
majority of cases weaning occurs north of the antarctic whaling grounds, if not north of the Antarctic

a.
hi

1 1 1 1 1 1

A -

" -

B^=

D J F

MONTHS

Text-fig. 50. Monthly percentage frequency ( + 2 S.E.) of lactating females in the South Georgia catches (A),

and the pelagic catches (B) of mature females.

Convergence. It is clear that (even if we allow that lactating females are under-represented in the
catches owing to the prohibition on their capture), lactating females are not present on the whaling
grounds in representative numbers in the early part of the season. This hypothesis explains why no
very early post-ovulation stages in the development of the corpus luteum have been recovered in the
Antarctic (p. 443), because if weaning and the post-lactation ovulation usually occur to the north of
the whaling grounds, then the very early post-ovulation stages might well be unrepresented or very
under-represented on the whaling grounds.

Some lactating females are, however, taken on the whaling grounds, although the evidence pre-
sented above suggests that in a large proportion of these the secretion of milk has actually ceased.
It may well be that some of the others have also weaned their calves very recently, but that the process
of milk secretion has not yet ceased. In this connexion it may be thought to be significant that, in
explaining infractions of paragraph 3 of the Schedule to the International Whaling Convention, 1946
(which prohibits the taking of calves or females accompanied by calves), the gunners almost invariably
state that no calf was seen. They are heavily penalized for taking lactating whales, but their denials
have some support from the evidence given here.

A further point, which should now be discussed, concerns the difference in the incidence of lactating

448 DISCOVERY REPORTS

females in the catches at South Georgia and on the pelagic whaling grounds. The South Georgia figures
are based on the biological investigations made during the period 1925-31, and the pelagic figures
are from 1939-54 (see Table 25, 'Percentage lactating'). Both samples relate to times and places
at which the taking of females accompanied by calves was prohibited. The pelagic sample relates to
the 5 months December-April, and the overall proportion of mature females found to be lactating is
3-3 ± 1-08 % ; during these 5 months at South Georgia the proportion lactating was 18-9 ±4-3 %. While
it is possible that the enforcement of this prohibition was less rigorous at South Georgia in 1925-31
than in British pelagic expeditions from 1939 onwards, it seems possible that such a great difference
in the incidence of lactating females in the catches reflects a real difference in the proportion of
lactating females in these two populations. If true it would mean that lactating females appear in
South Georgia waters in relatively greater numbers than on the pelagic whaling grounds further south.

So far we have expressed the occurrence of lactating females in the catches as a percentage of the
total mature females. This is open to the criticism that lactating females are protected to a degree
which may well vary with time and place. Text-fig. 50 at first gives the impression that the peak influx
of lactating females is later in South Georgia waters than on the pelagic whaling grounds, but this is
misleading. It is possible to obtain a much more accurate impression of the seasonal and numerical
incidence of lactating females on these two whaling grounds, by applying the percentage figures for
lactating females to figures of the total catches of mature females, and thus to obtain estimates of the
numbers of lactating females in the catches in different months. The method is similar to that employed
when examining the numbers of recent ovulations in antarctic waters (p. 440). The same figures are
used for the percentage immature and the source of the data on percentage lactating is given above.

The basic figures used for the catches are for the period 1927-35 for South Georgia (as before) and
1945-47 for the pelagic catches. Data on the latter period are used because they include catches made
in December and April. The results are presented in Table 25 and Text-fig. 51, and are to be regarded
as approximations for demonstration purposes rather than as precise values. Thus the validity of the
early and late catches cannot be checked but should not affect the main conclusions.

Table 25. Estimated monthly frequencies of lactating females in the catches at South
Georgia and on the pelagic whaling grounds

South Georgia, eight seasons 1927-35

Pelagic, two seaso?ts, 1945-47

Percentage

No.

Percentage

No.

Percentage

No.

Percentage

No.

Month

Catch

immature

mature

lactating

Catch

immature

mature

lactating

September

!95

(20-0)

156

o-o

—

October

1348

24-1

1013

5'4

—

November

1930

15-2

1637

3-6

15-2

—

December

2919

18-6

2376

n-8

280

2129

18-6

J733

o-93

January

37H

307

2574

12-5

322

5861

3°7

4062

2-3

February

2136

44"5

1185

19-6

232

6274

44-5

3482

6-o

209

March

879

46-0

475

44'4

211

5284

46-0

2853

1-9

April

208

33-3

139

20-8

995

33-3

664

2-1

In Text-fig. 51a curve has been drawn which shows the expected monthly incidence of weaning.
This curve is the same shape as the curve of calving frequencies (Text-fig. 31), but is displaced in time
by about seven months, so that the mean value occurs in December (as estimated above), and the
mode is, therefore, at the end of November. Differential growth between birth and weaning should
affect the shape of this curve, though not the mode and mean, but it has not been possible to allow
for this. The estimated numbers of lactating females in the catches are shown in the same figure for
comparison. It will be seen that peak numbers of lactating females were taken in South Georgia

MULTIPAROUS FEMALES 449

waters in January, and entered the pelagic catches in peak numbers in February. The ascending limb
of the pelagic curve actually appears to be about one to two months later than the ascending part of
the curve for South Georgia. In drawing this figure the scale, on which the estimated numbers of
lactating females have been plotted, has been so arranged that the descending limb of these curves
is in advance of the descending limb of the upper curve (which shows the approximate expected
frequency of weaning), by about 2 weeks to a month. This is in order to allow for the fact that lactating
females taken in antarctic waters are on average estimated to be only 2-4 weeks in advance of weaning.
The high value for March in the South Georgia curve reflects the high percentage frequency of

z
<

<
UJ
10

-2

J F

MONTHS

Text-fig. 51. Above: A, estimated frequency of weaning; B, monthly incidence of lactating females in South Georgia
catches, and C, in pelagic catches. Below: average monthly sea surface temperatures in South Georgia waters and on the
pelagic whaling grounds.

lactating females in the sample for this month (Text-fig. 50) ; it may well be too high. Even so the
slope of the descending limb of the South Georgia curve is fairly close to that of the expected curve.

In explanation of these results, it is suggested that the southward migration of females with suckling
calves is dependent on, and limited by, seasonal changes in the temperature of the sea. In latitudes
from 560 S. to 66° S. the average sea surface temperature is at a maximum in February (Mackintosh,
1946, fig. 11), when it is 1-20 C. higher than in December or earlier. The average surface temperature
for March is also much higher than the December value and somewhat higher than the January surface
temperature. Also, the summer rise in the surface temperatures appears not to begin until early
January in higher latitudes (64°-66° S.) owing to the presence of sea ice.

In Text-fig. 5 1 the average monthly sea surface temperatures for South Georgia and the pelagic
whaling grounds are plotted for comparison with the curves showing the relative frequency of

45Q DISCOVERY REPORTS

occurrence of lactating females in the catches. The temperature curve for South Georgia has been
constructed from information given by Mackintosh (1946) ; the average latitude of the pelagic whaling
grounds is assumed to be about 620 S. (see Mackintosh, 1942, fig. 2), and the monthly sea surface
temperatures for this latitude are taken from Mackintosh (1946, fig. 11).

Comparison of these sea temperature curves with the curves showing the relative monthly frequencies
of lactating females in the catches strongly suggests that the movements of females with suckling
calves are closely dependent on environmental temperatures. It appears that the influx of lactating
females to the whaling grounds may begin when sea surface temperatures rise above about o° C, as
suggested by the broken vertical lines in Text-fig. 5 1 . This apparently occurs about 5-6 weeks earlier
in South Georgia waters than on the pelagic whaling grounds. The figures suggest that over 50% of
females enter South Georgia waters after they have weaned their calves, mostly before January, and
that probably over 80% wean their calves before they reach the pelagic whaling grounds further south.
It was concluded above, that the majority of those lactating females which do penetrate to the whaling
grounds later in the season are either very near to the time of weaning, are in process of weaning, or
have just weaned the calf.

It is not possible to demonstrate a significant difference in the percentages of lactating females in
the pelagic sample at different latitudes, because of the variation in the position of the isotherms in
different sectors of the Antarctic. Thus, south of the Atlantic Ocean in January the o° C. isotherm
lies at about 580 S., but south of the Indian Ocean this isotherm is at about 65° S. in January. If the
material is subdivided into sectors then the samples are rather too small for statistical analysis to yield
significant results.

The conclusions reached in this section are of some importance in connexion with the occurrence
of the post-lactation ovulation, because if for the majority of females weaning of the calf and ovulation
occur north of the whaling grounds, then the chances of finding very early post-ovulatory stages in
the development of the corpus luteum are greatly reduced (see p. 443). They are also important in
relation to the supposed danger to the stock of killing lactating females. If the majority of lactating
females do not enter the whaling grounds until the calf is weaned, and if those which do are very
close to the time of weaning, then the effect on the stock of killing lactating females will not be so
drastic as was previously thought.

The Sexual cycle and its relation to the migratory cycle
In an earlier paper, on foetal growth in whales, it was suggested that the explanation of the con-
spicuous differences in the gestation periods and curves of foetal growth of baleen and toothed whales,
was to be found in the discontinuous feeding and the migratory cycle of baleen whales (Laws, 1959 a,

PP- 304-5)-

In a preceding section of this paper (p. 421) it was also shown that the sexual cycle of newly mature
females was rather closely related to the migratory cycle, and a possible causative and regulatory
factor was suggested. The further evidence which has now been presented shows that a similar
correlation is found in multiparous females. This may now be discussed in detail.

The main pairing season for multiparous females is found to extend from April to July, as compared
with the period May-September for primiparous females, and the median dates of conception are
respectively 8 June and 21 July. Another point of difference is that the frequency curve of multiparous
conceptions is skewed, with a long ' tail ' from July to December, whereas the primiparous curve is
more symmetrical.

If we accept the hypothesis that the sexual cycle in the fin whale is regulated by the change in day
lengths related to and caused by the long migrations between low and high latitudes (p. 423), the

MULTIPAROUS FEMALES 45'

advancement of the pairing season in multiparous females is clearly related to the fact that the north-
ward migration of mature females is earlier than that of immature females. Thus, there is an increasing
proportion of immature females in the catches towards the later part of the antarctic whaling season,
which suggests that immature females migrate into, and move out of, antarctic waters later in the
season than mature females. Only 13 % of multiparous conceptions are estimated to occur earlier than
the beginning of May and this figure is almost certainly too high, because the method of estimation
takes no account of variations in the rate of foetal growth. This has the effect of extending the
estimated period of conceptions. Thus, in calculating the frequency of conceptions, a faster growing
foetus would appear to have been conceived earlier than one which grew more slowly, whereas in fact
both might have been conceived at the same time.

According to Text-fig. 42 (p. 423) the earliest period in which whales migrating northwards should
experience increasing day lengths is late April-May, and this is in very close agreement with the
estimated frequency of conceptions. The latest month during which fin whales can migrate northwards,
and yet be subjected to increasing day lengths, is seen to be September, although few if any animals
migrate northwards at this time. From July to November or December, animals remaining in one
latitude zone in the southern hemisphere will experience increasing day lengths (Text-fig. 42) ; this
extends over most of the period covered by the ' tail ' of multiparous conceptions. It is interesting that
in the apparently non-migratory female sperm whale pairing occurs in spring (Matthews, 1938;
Clarke, 1956), that is at a season of increasing photo-period.

It is not, however, necessary to show that all conceptions follow a period of increasing day lengths,
because it has been shown that a post-partum ovulation is a regular feature of the sexual cycle. The
factors governing this post-partum ovulation are uncertain, but it is likely that interoceptive factors
relating to the end of pregnancy, the regression of the corpus luteum of pregnancy, and loss of the
placenta are responsible. In this event conceptions occurring before May could represent a successful
post-partum ovulation, for a calf conceived in May would on average be born 11 J months later in
April, so that the mother could experience a post-partum heat and mate again in April. In this
connexion it will be remembered that the average age of females which conceive in April is apparently
very much higher than in later months.

It seems likely that the ' tail ' of the pairing curve of multiparous females is largely caused by such
post-partum conceptions, and it is perhaps significant that in the closely related blue whale the
frequency curve of conceptions obtained from foetal length records is not skewed in this way (Laws
and Purves, 1956, fig. 11). In the blue whale post-partum conceptions are not a regular feature of the
sexual cycle (p. 429).

We may conclude that the pairing season of multiparous females is closely related to, and perhaps
regulated by the increasing day lengths associated with the northward migration from antarctic waters
to subtropical and tropical waters. For multiparous females in general, age does not influence the
time at which ovulation and conception occur, although the oldest females show a strong tendency
to mate early in the season. No convincing explanation of this anomaly suggests itself. It may be
relevant that in these older females linear growth is very slow, or has ceased, so that they may not
need to remain on the feeding grounds for as long as younger, faster-growing females and can migrate
north somewhat earlier.

Detailed examination of the size distribution of corpora albicantia in females in the different phases
of the sexual cycle provides strong evidence that the majority of, if not all, adult females experience
a post-partum ovulation. It has been shown, however, that a substantial proportion of primiparous
females do not experience a post-partum ovulation. The evidence discussed above does not allow a
precise estimate of the proportion of females in which the post-partum ovulation initiates another

452 DISCOVERY REPORTS

pregnancy. Some 18% of lactating females in the present material are found to be simultaneously
pregnant, but the variance of this percentage is large (s.E. = 4-34) which means that the true pro-
portion probably lies between 9 and 27%. It may be argued that if a post-partum ovulation is of
regular occurrence, then more females should be simultaneously lactating and pregnant. It is, how-
ever, quite likely that females are relatively infertile at the post-partum cycle, as compared with the
ovulation at the end of the 'resting' period which initiates pregnancy in the majority of females.
It is well known that a number of animals, including man, are less fertile during lactation. Similarly,
interoceptive factors may govern the initiation of an oestrous cycle after stillbirths and possibly after
abortions.

Perhaps the most unexpected result of the present investigation is the evidence for an end-of-
lactation or post-lactation oestrous cycle in the fin whale. This is of regular occurrence in the humpback
whale, but in this species it occurs in low latitudes. In the fin whale the lactation period is shorter,
and a post-lactation ovulation occurs during the migration to the antarctic feeding grounds and is
associated with increasing photo-periods. Females taken in antarctic waters with an active corpus
luteum of ovulation in the ovaries, denoting a recent ovulation, show a. very low incidence of diatom
infection, suggesting that they have only recently moved into antarctic waters.

It has been suggested that the southward movement of females with calves is in general restricted
to regions where the sea surface temperature is above o° C. Weaning of the calf occurs on average in
December, but probably owing to the unfavourable environmental conditions less than half of the
lactating females in that sector enter South Georgia waters, and probably less than one-fifth enter the
pelagic whaling grounds further south, over a month later. The majority of females, therefore,
experience the post-lactation oestrous cycle before attaining the latitude of the pelagic whaling grounds
(on average about 61-62 °S.). Almost all lactating females which are present in antarctic waters are
very near to the time of weaning, are weaning, or have recently weaned the calf. Many of the lactating
females passing through South Georgia waters probably experience a post-lactation oestrus while
migrating from the latitude of South Georgia to the pelagic whaling grounds further south.

The few lactating females which penetrate to high latitudes late in the whaling season probably
enter oestrus at the end of lactation, but the earliest stages in the development of the corpus luteum
which have been accurately noted in antarctic waters, were estimated to be about one week post-
ovulation. As only ten such corpora lutea of ovulation have been noted since the recent investigations
began, it is not surprising that no very early stages in the development of the corpus luteum have been
recorded as yet. In the earlier records some corpora lutea are noted as 'very young', but it is not
known whether any of the very earliest stages after the rupture of the follicle and early development
of the corpus luteum have been observed. On rare occasions mating has been observed in antarctic
waters.

The temporal distribution of these post-lactation ovulations has been investigated, and it is found
that very few if any occur before September, that mid-December is the average date, and that no
recent corpora lutea are found after March.

It is significant that at the same time as this post-lactation oestrous cycle, pregnant females also
experience an ovarian cycle, following a southward movement to antarctic waters. In pregnant
females there is a cycle of follicular activity which is at a maximum (expressed as maximum follicle
size, and as numbers over 3 cm. in diameter), in December, or November/December. The follicles
increase in size, but maturation is suppressed owing to the presence of the corpus luteum of pregnancy.
The timing of this cycle is again in close agreement with the hypothesis that pro-oestrus is initiated
during a period of increasing day lengths related to the southward migration.

The post-lactation oestrous cycle initiates a pregnancy only very infrequently (in an estimated 5 % of

MULTIPAROUS FEMALES 453

cases). This is probably because there is a single restricted sexual season in the male fin whale.
Evidence given above shows that the male sexual season extends in the main from April to July, and
is reflected by the data on the frequency of pairing. It agrees with the hypothesis put forward to
explain the factors regulating the female cycle. Almost invariably the seminiferous tubules of males
are still regressing on arrival in antarctic waters, but full anoestrus is attained soon after arrival.

It is not immediately clear why the male should not experience a sexual season during or following
the southern migration as do the females, but there is an important difference between the sexes
which may go a long way towards explaining this. The female fin whale is monoestrous and produces
ova at infrequent intervals, but in the males it is probable that, as in some other animals, production of
sperm is continuous over a period of several months. If we assume a ' refractory period ' just after
the sexual season (as in fact occurs in female dioestrous cycles), then increasing day lengths would not
initiate a further sexual season if they occurred during this ' refractory period '.

Such a refractory period has been shown to characterize the testis cycle of seasonally breeding male
birds (Marshall, 1950, 1951). It is defined as ' that period of the avian testis cycle when the tubules are
in a state of post-spermatogenetic lipoidal metamorphosis and before the newly regenerated Leydig
cells of the interstitium have become sufficiently lipoidal and mature to respond to neuro-hormonal
influences initiated by natural factors in the environment'.
' This seems to be the most likely explanation, but it is also possible that the testes of male fin whales,
stimulated by increasing day lengths on migration, undergo a short recrudescence of activity. If this
were so, then it might be expected that more females would become pregnant following the post-
lactation ovulation. In juvenile birds, the testis tubules have not produced spermatozoa, and the
lipoid Leydig cells are still developing and receptive to stimuli ; it is possible that some pubertal male
fin whales are similarly receptive to day-length changes during the southern migration, as are pubertal
females. In this case some pubertal females might be expected to mate successfully with pubertal
males at this time. The disadvantage of such matings is clear; it would mean that larger numbers of
calves would be born at a time when the females must seek out food in the colder southern waters.
If it is disadvantageous for several-months old unweaned calves to enter antarctic waters then it is
clearly very disadvantageous for births to occur in antarctic or sub-antarctic waters.

Marshall (1942) has reviewed the evidence bearing on the role of exteroceptive factors in sexual
periodicity. He concludes that in all species of mammals there is an internal sexual rhythm ' which
is presumably dependent upon an endocrine cycle but that this is usually, though not always, adjusted
to external seasonal change. That the recurrence of the sexual periods is not due entirely to endocrine
factors is shown especially clearly by those individuals which belong to species or breeds that ordinarily
have only one sexual season annually, yet can be induced to have two seasons by transferring them
across the equator from one hemisphere to the other. '

The evidence which has been presented strongly suggests that the ovulatory cycles of fin whales
are monoestrous cycles. This conclusion is strongly supported by the evidence as to the limited
variation in the rate of accumulation of corpora albicantia presented earlier. Further support for this
view will be demonstrated below, when the average annual rate of ovulation, estimated from just
such a seasonally monoestrous cycle as has now been described, is found to be in very close agree-
ment with the independent estimate of the average annual rate of ovulation given earlier in this
paper (p. 385), and with the rates of ovulation suggested by comparison with other methods of age-
determination.

454

DISCOVERY REPORTS

Variation of fertility with age
It has been shown that the female fin whale experiences a seasonally monoestrous sexual cycle. If this
is true then variations in the rate of production of ova will be mainly related to the incidence of
multiple ovulations, or to the percentage of females ovulating at each ovulatory period, rather than
to variations in the number of dioestrous cycles in each ovulatory period.

Multiple ovulations
The varying incidence of multiple ovulations with age in the present material is shown in Table 26.
For different numbers of corpora albicantia are shown the numbers of females with more than one
corpus luteum in the ovaries. The incidence of multiple ovulations appears to increase with increasing
numbers of corpora albicantia (and therefore with increasing age), but there is a significant difference
only between the first two groups. It seems probable that there is a real increase in the occurrence of
multiple ovulations, because Kimura (1957, fig. 10) shows, for a much larger sample, that the frequency
of dizygotic twins similarly increases with age from about o-i % (at 1-5 corpora) to 6-25% (at 30-35
corpora). The average incidence of multiple ovulations in the present material is 2-i6±o-82%. So
far we have not considered the variations in actual numbers of ovulations in cases of multiple ovulation.
In different cases of multiple ovulations the number of corpora lutea produced varies from 2 to 13
(in the present material). There are 22 females with 2 corpora lutea, 3 with 3 corpora lutea, 1 with
4 corpora lutea and 1 with 13 corpora lutea.

Table 26.

No. of

corpora

albicantia

0-4

5-9
10-14

15-19

20-24
25-29
30-34
35-39
40-44

45-49
5°-54
Total

Variation in incidence of multiple ovulations with age

(number of corpora albicantia)

Total

ovaries with

corpora lutea

490
281
178
128
76

49
29

15
3
2

Multiple
ovulations

1
7
5
6

Percentage

multiple

ovulations

0-20
249
2-81
4-69
6-58

6-oo

2 S.E.

0-40
i-86
2-47

374

57°

672

1252

2-16

0-82

Table 27. Details of multiple ovulation in which 13 ova were shed and 5 foetuses developed

Ovary 1

Ovary 11

-1
Cavity

Cavity

Weight

Diameter

diameter

Weight

Diameter

diameter

C.L. no.

(lb.)

(cm.)

c.l. no.

(lb.)

(cm.)

H-5

—

13-0

8-0

12-0

6-5

io-o

—

10-5

—

9-0

3-3

io-o

6-5

7-0

4-5

9"5

4'5

7-0

4'5

9-0

—

7-5

5"5

—

7"5

2-5

—

MULTIPAROUS FEMALES 455

The appearance of the corpora lutea in the case where there were four simultaneous ovulations is
illustrated in Text-fig. 10 a. The female which had 13 corpora lutea in the ovaries was examined by
Dr R. H. Clarke on 25 February 1948 in 6i° 14' S., 870 25' E., and measured 78-5 ft. in length. This
female carried 5 male foetuses of lengths 2-03, 2-26, 2-28, 2-54, and 2-67 m., the first of which was
necrotic, the others healthy. There were 16 corpora albicantia in the ovaries and details of the
13 corpora lutea are given in Table 27. It will be seen that none of the corpora lutea is of very
small size, ranging from 7 to 14-5 cm. in diameter, and all would therefore be expected to leave a
permanent record in the ovaries (p. 375).

Making due allowance for these supernumerary corpora lutea it is estimated that on average
1 -034 corpora lutea are formed each ovulatory cycle, that is to say the proportion of extra ovulations is
3 -4 ±1-02%. With a smaller sample (part of the present sample) in which the corpora lutea were
examined in detail the proportion of accessory corpora lutea was 3*7% (p. 361).

Proportion of females in oestrus or pregnancy
Another aspect of the variation in sexual activity with age can be studied by examining, for successive
groups of corpora numbers, the percentage of adult females which show one or more active corpora
lutea in the ovaries. The majority of these females will be pregnant, but a small proportion are in a

100

z
u

250
s

NUMBER IN SAMPLE
776 416 268 192 116 67 42 20 3 2 5

100

NUMBER IN SAMPLE
490 281 178 128 76 49 29 IS 3 2 I

A 1 h

O 5 10 15 20 25 30 35 40 45 50 55
NUMBER OF CORPORA

O 5 10 15 20 2 5 30 35 40 45 50 55
NUMBER OF CORPORA

Text-fig. 52. a, Percentage of mature females which have an active corpus luteum in the ovaries.
b, Percentage of these corpora lutea which represent pregnancies.

post-oestrus condition following a recent unsuccessful ovulation (p. 437). Owing to differential
migration, mortality, etc., the figures obtained will not exactly represent the true proportion of females
which are still experiencing oestrous cycles, but will give a picture of the relative variation in activity
with age.

The results are shown in Text-fig. 52 a, in which data on 1907 mature females examined between
1925 and 1954 are utilized. For successive age groups (expressed as corpora numbers) the percentages
of mature females with corpora lutea are shown. The vertical range represents the percentages ± 2 S.E.,
and the results for the last three groups have been combined so as to increase the size of the sample.

Over this range of ages the percentage frequency of pregnancy or post-oestrus stages does not vary
significantly, but taking the figures as a whole it would seem that fertility increases very slightly up to
an age corresponding to 40-50 corpora (estimated to be about 35-40 years; see pp. 465-66), after
which it may decline.

A proportion of these females have ovulated recently without becoming pregnant, and it is, there-
fore, interesting to see whether the percentage of unsuccessful ovulations varies with age. There are
1252 females in the material which have corpora lutea in the ovaries, and these are again divided into
successive age groups according to corpora number. For each age group the proportion known to be
pregnant, because a foetus was noted, has been calculated. Some few pregnant females in which the
17 DL

456 DISCOVERY REPORTS

foetus was missed may have been included in the non-pregnant group, but this will not greatly affect
the results, and in any case the relative incidence of pregnancies is what we are here concerned with.
The percentages pregnant ± 2 s.E. are shown in Text-fig. 52 b, and the results for the last four age
groups have been combined to increase the size of the sample.

There is again no statistically significant difference in the incidence of successful ovulations, but
considering the results as a whole it would appear that the youngest females show a slightly lower
fertility, that fertility is at a maximum at ages corresponding to 1 5-30 corpora (that is about 1 5-25 years,
see p. 466), after which the proportion of successful ovulations appears to decline. This is in agreement
with the generalization made by Hammond (1952, p. 656) that the time of submaximal fertility
corresponds to the time during which the skeleton is completing its full growth, because as we have
seen in the fin whale, ossification of the vertebral epiphyses is completed when 14-15 corpora have
accumulated in the ovaries.

There are no data on which to base an accurate estimate of pre-natal mortality, which is another
factor in fecundity. This includes all females which conceive, but fail to complete pregnancy success-
fully, owing to absorption or abortion of the embryo or foetus. In sheep, losses from these causes
average 2-4%, but in cows they are higher, averaging 10% (Hammond, 1952, p. 703). It is likely that
in whales the average incidence of pre-natal mortality is very low, possibly as low as the average figure
quoted above for sheep.

The climacteric which occurs in some mammals, and is perhaps most marked in man, marks the
end of active sexual life and is, therefore, the inverse of the developmental process of puberty. It is
of rare occurrence in natural populations. Taking into account all the evidence presented above, it is
clear that there is no real climacteric in fin whales, at least up to the ages represented in the sample.
It is significant that the oldest female (according to the number of corpora which had accumulated in
the ovaries) was pregnant. It does, however, seem that there is a slight tendency for fertility to be
reduced at ages in excess of about 30-40 years (that is when 35-50 corpora have accumulated, see

P- 466)-

Variations in fertility with time

Mackintosh (1942, p. 223) referring to blue and fin whales remarked that, 'the percentage of adult
females which are pregnant has been increasing in a remarkable degree year by year, as if the actual
rate of breeding were becoming faster '. He suggested that this was conceivably a reaction to whaling.
Since then additional material has become available.

In order to make use of material collected by non-biologists, so as to keep the available samples as
large as possible, all females with an active corpus luteum in the ovaries have been assumed to be
pregnant whether or not an embryo or foetus is found. If this procedure were not adopted, then the
sample would have to be restricted to females of which the uterus has been carefully searched. This
would greatly reduce the size of the sample and would eliminate all samples provided by the whaling
companies.

The term ' percentage pregnant ' means, therefore, the proportion of adult females in the catches
which had an active corpus luteum in the ovaries. The actual ' percentage pregnant ' will be lower than
this by about 8-10%, because as shown above a proportion of those females which have active corpora
lutea in the ovaries are not pregnant, but have recently ovulated.

It should be emphasized that the term ' percentage pregnant ' refers to the catches only, and applies to
the total population in a relative way. This is due to the fact that a large proportion of lactating females
delay the southward migration into antarctic waters (p. 450), and because of this, and also because of the
prohibition on the taking of lactating females, this group is under-represented in the catches. This may
partly explain the lower values for the South Georgia catches, where more lactating females are taken.

MULTIPAROUS FEMALES 457

Another factor influencing the apparent percentage pregnant is the mortality rate. Non-pregnant
mature females taken in antarctic waters will on average be about a year older than pregnant females,
because most females become pregnant at the first ovulation and do not join the non-pregnant group
until a year later. Thus, even if lactating females were fully represented in the samples and the actual
average pregnancy rate for individual females was 50% (that is, one pregnancy every 2 years), the
apparent ' percentage pregnant ' of the population as a whole, resulting from an annual adult mortality
rate of, say, 20% should be 55*5%. For every 100 pregnant females there would be only 80 non-preg-
nant, because 20 females die in the intervening year. However, even if the effects of high mortality rates
are allowed for, the variation between the values for the apparent ' percentage pregnant ' is considerable,
and probably represents a real change in fertility. This might be caused by increased fertility at post-
partum or post-lactation ovulations, and to a small extent perhaps by reduced pre-natal mortality.

It has been shown above that the youngest females have a lower fertility rate, and that fertility is
maximal at about 15-25 years, after which it appears to fall slightly. If the age-composition of the
population has changed then this would affect the percentage pregnant, but only to a very slight and
possibly not appreciable extent.

100

z
<

5 SOl

BLUE WHALE- ALL AREAS

£ IOO

£ SO

-n-*-«-

FIN WHALE-AREA II o

AREAS m+K«

1930

1935

-1 — i — 1 — r
1940

-1 1 1 1 r-

1945

1950

1955

I960

Text-fig. 53. Pregnancy rates of mature females in different seasons and areas.

Table 28. Variations in the 'pregnancy rate' in the catches of adult females over a number of years

Blue Fin Blue Fin

South
Georgia

Pelagic

South
Georgia

Area 11

Areas

III + IV

Pelagic

Area

Area 11

Areas
III + IV

Season

1925/26
1926/27
1927/28
1928/29
1929/30
1930/31
I93I/32
1932/33
1933/34
1934/35
1935/36
1936/37
1937/38
1938/39
I939/40
1940/41

Per- Per- Per- Per- Per-

No. centage No. centage No. centage No. centage No. centage

— — — — 72 46 — — — —
30 40 — — 18 56 — — — —

— — — — 12 42 — — — —
27 41 — — 74 69

9 55 — — 188 69 — — — —

25 76 — — 70 76 — — — —

— — 184

— — 25

563

407

342

401

506

Season

1945/46
1946/47
1947/48
1948/49
1949/50
1950/51
1951/52
1952/53
1953/54
1954/55
1955/56
1956/57
1957/58
1958/59

Per- Per- Per- Per-

No. centage No. centage No. centage No. centage

190

479
377
347
239
278
142
134
121
68

54
68
54
68

75
77
73
73

284

—

■ —

—

180

—

165

130

163

108

69 185

79 294

71 333

— 184

79
72

118

174
363

84
86
86

222
164

77
80

With these reservations in mind the variations from year to year in the ' percentage pregnant ' may
be briefly discussed. In Table 28 the full results are shown, and in Text-fig. 53 some of these values
are plotted.

The pelagic values for blue whales are combined for all areas, because individual areas show a
similar pattern. This indicates an apparent increase in fertility in pre-war years levelling-out at about

458 DISCOVERY REPORTS

80% pregnant. The great reduction in the intensity of whaling during the war years is apparently
correlated with a fall in the percentage pregnant to the original low level of the early 1930's. Then, in
post-war years, there was a similar increase in fertility up to the 1950/51 season, though it seems that
the maximum fertility is lower than in pre-war years. Sampling difficulties may be responsible for
this change, because pregnant females are more abundant in the catches early in the season (see above)
and the later season for blue whales in recent years would be expected to result in a potentially lower
' percentage pregnant '. The catches of blue whales have declined greatly in post-war years and samples
after 1954/55 have been too small to use for this purpose.

The data for fin whales follow a similar pattern and the values for area 11 and areas m and iv have
been plotted separately in Text-fig. 53. Areas m and iv have a similar history of exploitation, beginning
long after area 11 (Text-fig. 54).

The 'pregnancy rate' for the South Georgia fin whale catches rose from about 50% in 1925/26 to
70% or more at the beginning of the 1930's. At this time the annual catches of both fin and blue
whales in area 11 were increasing (Text-fig. 54) (geographically South Georgia is within area 11). The
pregnancy rate for area 11 fin whales had risen to about 80% by 1940/41, after some years of high
catches in this area (Text-fig. 54), but in 1945/46 after the greatly reduced catches of the war years

I960

Text-fig. 54. Antarctic catches of fin whales from 1909/10 to 1957/58 according to the whaling areas.

had fallen to 32%. This season was rather an abnormal one and the sample may have been less
representative of the stock than in later seasons, but bearing in mind the additional evidence from
blue whales, it does seem reasonable to conclude that the real pregnancy rate was low. By 1950/51,
after several seasons of sustained heavy exploitation (Text-fig. 54), the 'percentage pregnant' was
above 80%. This would appear to be the maximal response of which the fin whale was capable, for
in later seasons (1955/56-1958/59) even after larger catches the percentage pregnant was stable at
about 80%. The apparent decrease in the pregnancy rate in 1958/59 is disturbing, but may not be
real, and it is too early to assess its full significance. Owing to differential sampling as mentioned
above, a 'pregnancy rate' of 80% is probably equivalent to a real pregnancy rate of about 60%.

Similarly in areas in and iv the 'pregnancy rate' appears to have stabilized in post-war years at
rather more than 80%. A very small sample from area m in 1932/33 suggests a very much lower
pregnancy rate, but little confidence can be attached to this figure.

In area 1 the ' percentage pregnant ' was round about 70-80% from 1955-58 when very large catches
were being made in this area. Area I was a sanctuary up to 1955/56, so that according to the hypothesis
that fertility is lower in natural conditions and rises with increasing fishing mortality, the ' percentage

MULTIPAROUS FEMALES 459

pregnant ' might have been expected to be low in the season 1955/56. There is, however, some evidence
from whale marking of interchange of whales between this region and area II, so that the area 1 whales
were probably not a completely unexploited stock before whaling operations began in this area.

What is the most likely mechanism causing such changes in the pregnancy rate? Lack (1954) has
surveyed the factors which operate to limit the numbers of mammals. He suggests four density-
dependent factors that might be important; food shortage, disease, predation, and, as a secondary
factor dependent on food, behaviour. It seems probable that the availability of food is the primary
factor limiting the numbers of baleen whales under natural conditions, though man, as a predator,
has now largely taken over this role. Food-supply limits numbers by its effect on mortality rates (by
starvation) ; also in several species of mammals, and especially in deer, the birth-rate has been found
to vary with the food-supply (Cowan, 1950; Severinghaus, 195 1 ; Morton and Cheatum, 1946; Cheatum
and Severinghaus, 1950). The food-supply is density-dependent and so is the birth-rate. It is sug-
gested that the observed rise in the pregnancy rate of fin and blue whales associated with increased
exploitation by man is a response to decreased population density acting through the food-supply.
It is a limited response which in the fin and blue whales evidently produced its maximum effect by
the early 1950's and has since been fairly stable.

It is hoped that a fuller discussion of this apparent relation between fertility and intensity of whaling
can be given in a later paper. For the present it is sufficient to show that the bulk of the present
material comes from samples collected when the fertility was probably maximal. For periods when
the 'percentage pregnant' was appreciably lower than 70-80% (that is, the samples for 1924-28,
1932/33, and 1945/46), the sexual cycle may well have been slightly different from that which has
been described above. In particular the percentage of post-partum conceptions may have been lower.
This suggestion receives some support from the South Georgia data, because in the period 1924-28
the proportion of lactating females pregnant was very much lower than in 1928-31 (Table 19). See
also pp. 430, 437.

If there was a real difference in the sexual cycle for periods when the catches of whales were less,
then the annual rate of ovulation may have been slightly different at these times. The difference
would not, however, be sufficient to have an appreciable effect on age-determination by means of
corpora lutea and corpora albicantia, which is discussed in the following section.

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA

The Rate of Accumulation of Corpora Albicantia

It has been shown above that with negligible exceptions the corpora albicantia in fin whale ovaries,
which represent previous ovulations or pregnancies, persist throughout life in a form which is readily
visible to macroscopic examination. This persistence on a macroscopic scale is related to the large
initial size of the whale corpus luteum, in conjunction with the fact that the corpus luteum usually
regresses to a constant fraction of its initial size. The mean diameter of fully regressed corpora
albicantia is 2-01 cm. and very few shrink to less than 1 cm. in diameter.

By using a slicing machine to cut 5-mm. thick slices of the ovaries, the number of corpora in each
pair of ovaries can be determined with precision, and the errors in counting are small. Earlier samples
of ovaries were sliced by hand and although the errors will inevitably be greater the results from this
period are unlikely to be much in error, probably not more than ±5-10%. The numbers of corpora
in the ovaries will give us an estimate of the relative age of the female, and if it is possible to determine
the average rate of accumulation of corpora, then actual ages may be estimated with a degree of
confidence which depends on the variation in the age at puberty and the variability in the average

460 DISCOVERY REPORTS

rate of accumulation. We are now in a position to give an estimate of the average annual rate of
accumulation of corpora, and to compare ages determined in this way with ages determined by other
independent methods.

Types of corpora albicantia

Three age groups of corpora albicantia have been identified on the basis of gross anatomical appearance,
and confirmed by histological examination (p. 366). The mean diameters of these groups in order of
increasing age are 4-01 cm., 2-94 cm., and 2-01 cm. These three groups represent stages of regression,
and in the ovaries there are on average about 1-54 of the youngest corpora albicantia and 3-22 of the
next age group. The number in the oldest group is cumulative, and bears a direct relation to the
total number of corpora in the ovaries. That is to say, the first two groups represent stages of
regression, while the third group represents the accumulation of fully regressed corpora albicantia
which increase in numbers with age.

If the first two groups represent successive stages of regression, their relative frequency of occur-
rence should represent the relative length of time taken for each stage of regression. It is found that
the ratio of ' young ' to ' medium ' corpora albicantia is almost exactly 1 : 2 and it appears that together
they occupy about three years. The ' young ' corpora albicantia, therefore, represent about one year's
accumulation, and ' medium ' corpora two years. The average annual rate of accumulation of corpora,
therefore, appears to be about 1-5-1-6, but a correction (explained on p. 380) is necessary because
the process of regression lasts longer in older animals, so that there are more ' young ' and ' medium '
corpora in the higher corpora groups, that is at higher ages. This suggests that 1 -4-1-5 is a more
accurate value for the annual increment of corpora.1 It is found that newly mature females ovulate
on average about 1-42 times before becoming pregnant.

The sexual cycle

Evidence has been presented in this paper which strongly suggests that the female fin whale has a
seasonally monoestrous type of sexual cycle. It has been shown that in the majority of females there
are three ovulatory periods, two of which (a post-partum oestrus and a post-resting oestrus) usually
occur in low latitudes in the southern winter, during or after a northward migration ; and the other
(a post-lactation oestrus), usually occurs in higher latitudes in the southern summer, during or after
a southward migration. With the present data it is not possible to show conclusively that these ovula-
tory periods are invariably monoestrous, but the material available strongly suggests that this is so.
The evidence for newly mature females is perhaps the most conclusive. Even if female fin whales
are not invariably monoestrous there is certainly a very strong tendency towards the monoestrous
condition, similar perhaps to that which has been demonstrated, for example, in certain species of
Equidae and Bovidae (Eckstein and Zuckerman, 1956, pp. 238, 245).

In this connexion it is of interest that Chittleborough (1954) has shown just such a strong tendency
to monoestrus in the humpback whale during the breeding season. Thus, he finds that the mean
number of ovulations for a female humpback whale during its ovulatory period (in Australian waters)
is only slightly over one. It is possible that the monoestrous condition in the fin whale is more apparent
than real, and that there is in fact a polyoestrous cycle in which the first ovulation is almost invariably
successful. However, in an ovulatory period, such as the post-lactation oestrus of the fin whale, when
males are out of breeding condition, the polyoestrous cycles should not be suppressed. The evidence
on this point, both in females at puberty and in adult females, is strongly in favour of monoestrous
cycles in fin whales at each of the three ovulatory periods. This evidence precludes more than a slight
tendency towards polyoestry.

1 From the evidence of the corpora albicantia the possibility that the rate is only 0-7-0-75 cannot be excluded (see p. 385).

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA 461

Given a seasonally monoestrous sexual cycle it is possible to estimate the average annual rate of
ovulation. It should be made clear that this evidence is completely independent of the other estimate
of the rate of ovulation given in this paper. Thus, ignoring for the moment post-partum and post-
lactation conceptions and assuming that all females experience a post-partum and post-lactation
oestrus, there would on average be three ovulations in two years, or 1-5 a year. The effect of post-
partum conceptions and post-lactation conceptions will be to alter this estimate as follows.

The incidence of the post-partum ovulation and the percentage of conceptions resulting from it are
the points on which there is most uncertainty. Calculations have, therefore, been made for six
different alternatives, in which it is assumed that the incidence of post-partum ovulations is either
100 or 80%, and three alternatives are assumed for the proportion of successful post-partum ovula-
tions, namely 9, 18, or 27%. The post-resting ovulation is assumed to be 100% successful, and the
post-lactation ovulation is assumed to be only 5 % successful. An allowance of 3 % is made in respect
of multiple ovulations. Evidence has been given earlier supporting a high incidence of post-partum
ovulations (pp. 429-36); the alternative proportions of post-partum conceptions are based on the
average incidence plus or minus 2 s.E. (p. 430); reasons have been given for assuming a low incidence
of post-lactation conceptions (p. 443), and the frequency of multiple ovulations has been discussed.

The calculations are presented in Table 29, and because in calculating the average annual rate the
starting-point in the 2-year cycle is important, three hypothetical 2-year periods are covered.

In the first case the 2-year cycle is assumed to commence in late pregnancy, so that the first ovulation
occurs at the post-partum oestrus. Then, in the first column it is assumed that all females ovulate
shortly after parturition and that 9% conceive at this time. Then 91% will enter anoestrus until the
post-lactation ovulation, at which 5% of them will conceive, so that 87% of the original numbers are
left to ovulate again at the end of the resting period. It is assumed that these become pregnant and
do not ovulate again for nearly a year. An allowance must be made for those females which become
pregnant at the first post-partum ovulation in this cycle. They will ovulate again at the end of this
pregnancy, and 91% of them (because 9% are assumed to become pregnant again), will ovulate
once more at the end of lactation. These figures should include all the ovulations in this 2-year period.
When allowance is made for multiple ovulations by adding 3%, the mean value for this case is
1-518 ovulations per year.

The other columns are worked out in the same way, the results varying with the basic assumptions.

In the next set of calculations (Table 29 B, column 1), the 2-year sexual cycle is assumed to com-
mence just before the winter post-resting ovulation. All females are assumed to ovulate at this stage of
the cycle, becoming pregnant for nearly a year when, as in the case set out in the first column, all
experience a post-partum ovulation, and 9% conceive at this ovulation. The remaining 91% ovulate
again at the end of lactation, and 5% of them are assumed to become pregnant again. The 2-year
period ends before another ovulatory period is due. A correction is again made to allow for multiple
ovulations, and the mean value for this set of premisses is 1-499.

In the third group of calculations (Table 29 C, column 1) the sexual cycle is assumed to begin just
before the post-lactation ovulation, when all ovulate with 5% conceiving. Thus, 95% are left to
ovulate at the post-resting ovulation, when they become pregnant again and ovulate post-partum
just before this arbitrary 2-year period ends. The other 5 % which became pregnant at the first post-
lactation oestrus should experience a post-partum ovulation at the end of the first year when 9 % of
them (that is, about 0-45 % of the original sample) should again become pregnant. This leaves 4-55 %
to ovulate again at the end of lactation, when they are all assumed to become pregnant (because this
ovulation should occur in winter, in low latitudes, when males in breeding condition are present).
After an adjustment for the occurrence of multiple ovulations, the mean value is estimated to be 1-543.

462

DISCOVERY REPORTS

Table 29. Calculation of average annual rate of ovulation. Three 2-year periods are considered, beginning
with a post-partum oestrus (a), a post-resting oestrus (b), and a post-lactation oestrus (c). See text for
explanation

ioo% post-partum ovulation 80% post-partum ovulation

1.
2.
3-
4-

Ovulatory periods

9%P.L.

l8%P.L.

27% P.L.

9% p-L-

18% P.L.

27% P-

Beginning with

post-partum

oestrus

Winter (post-partum)

1 -ooo

o-8oo

Summer (post-lactation) 5 % success

0-910

0-820

0-730

0-910

0-820

0-730

Winter (post-resting) 100% success

0-865

0-779

0-694

0-865

0-779

0-694

Winter (post-partum)

0-090

0-180

0-270

0-072

0-144

0-216

Summer (post-lactation)

0-082

0-148

0-197

0-082

0-147

0-197

Multiple ovulations (3 %)

Annual rate of ovulation

2-947
0-088

3-Q35
i-5i8

2-927
0-088

3-QI5
1-508

2-891

0-087

2-978
1-489

2-729
0-082

2-811

1-406

B. Beginning with post-resting oestrus

1. Winter (post-resting) 100% success

2. Winter (post-partum)

3. Summer (post-lactation) 5 % success

Multiple ovulations (3%)

Annual rate of ovulation

2-910

0-087

2-997
1-499

2-820
0-085

2-905
J-453

2-730
0-082

2-8l2
1-406

2-710

0-081

2-791
1-396

C. Beginning with post-lactation oestrus

1. Summer (post-lactation) 5% success

2. Winter (post-resting) 100% success

3. Summer (post-partum)

4. Winter (post-lactation) 100% success

5. Winter (post-partum)

Multiple ovulations (3 %)

Annual rate of ovulation

Total
Average

4-56o
1-520

4-5°2
1-501

4-434
1-478

4-242
1-414

2-690
0-081

2-771
1-386

2-620
0-079

2-699
!-35o

4"J74
i-39i

2-637
0-079

2-716
1-358

1 -ooo

o-8oo

o-Soo

0-910

0-820

0-730

0-910

0-820

0-730

2-530

0-076
2-606
1-303

1 -ooo

0-950
0-050

0-046

0-950

0-950
0-050

0-041

0-950

0-950
0-050
0-037
0-950

0-950

0-040
0-046
0-760

0-950

0-040
0-041
0-760

0-950

0-040
0-037
0-760

2996

0-090

2991

0-090

2-987

0-090

2-796

0-084

2-791

0-084

2-787
0-084

3-086

0-081

3-077

2-880

2-875

2-871

!-543

J-54i

J-539

1-440

1-438

1-436

Average of A,

i-5i8
1-499

J'543

B and c

1-508

J-453
i-54i

1-489
1-406
!-539

1-406
1-396
1-440

1-386

!-35°
i-438

i-358

i-3°3
1-436

4-097
1-366

This procedure has been followed for the other assumed rates of post-partum ovulations and post-
partum conceptions, and the resulting annual values are averaged. The six mean values finally obtained
vary from 1-366 to 1-520, which means that if the assumptions cover almost all the possible range of
variation in the incidence of ovulations, the annual rate is between about 1-35 and 1-55. Some of these
assumptions are considered to be more likely than others ; it is thought to be probable that the incidence
of post-partum ovulations lies between 80% and 100% (probably nearer to 80%), and that the propor-
tion conceiving at this ovulation is about 18%. Taking the average of columns 2 and 5 in the final
line of Table 29 gives a figure which meets these conditions and suggests an average annual rate of

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA 463

ovulation of 1-446. Assuming the incidence of post-partum ovulations to be nearer to 80%, we may
adopt a figure of about 1-43 ovulations per year. Even if the incidence of post-partum ovulations is as
low as 60%, which is improbable, the average annual increment (for 18% pregnant/lactating) is 1-282.

If the fin whale is not strictly monoestrous, but only shows a strong tendency to this condition,
then the average annual rate of ovulation will be slightly higher than this estimate. An average of
i-i ovulations per ovulatory period (excluding multiple ovulations) would raise the estimate from
1-43 to 1-57, but in the absence of supporting evidence this possibility has not been allowed for in
adopting an estimate of 1-43.

There are now two independent estimates based on the evidence presented in the present paper,
which are in fairly close agreement, namely about 1-4-1-5 (p. 385) and about 1-43. Allowing for
possible causes of variation or sources of error it is considered that the average annual rate of ovulation
in the southern hemisphere fin whale is i-43±o-i. In calculating ages from the numbers of corpora
albicantia in the ovaries the annual rate of accumulation is taken to be 1-43 corpora albicantia. In
general estimates of relative individual ages, post-puberty, are likely to be accurate to within ±7%
(namely ±1-4 corpora, that is, 1 year, in 14 years)1.

Recovered whale marks

A long-term programme of whale-marking was initiated in 1934-35 by ' Discovery ' Investigations, and
continued after the war by the National Institute of Oceanography and other interested bodies in
Norway, Japan, Russia, Australia, and New Zealand, with the support of the International Whaling
Commission and the Whaling Companies (Brown, 1954; Chittleborough and Godfrey, 1957; Clarke
and Brown, 1957; Dawbin, 1956a; Mackintosh, 1942; Rayner, 1940).

One of the objects of this marking programme was to provide a check on methods of age-determina-
tion. Unfortunately, however, there are difficulties which are peculiar to whale research. It is not
possible to capture whales, mark them and then release them as in marking fish, seals, and other
animals. Whale-marking is effected by firing a numbered metal tube into the dorsal muscle of the
free-swimming animal — a costly operation. One consequence of this is that it has not so far been
possible to confine marking to one particular known age-class (e.g. the calves), nor is it possible to
determine the age or size of individual whales at the time of marking. In any case measurements of
body length are very variable, even within a single age-class, and estimates of size in the water are
usually inaccurate.

Up to the season 1958/59 about 5000 fin whales had been marked in antarctic waters and 373 marked
whales had been recovered up to 1 958/59, one of which had a minimum age (from marking to recapture)
of 24 years.

Unfortunately only 10 of these recoveries were also accompanied by material (the ovaries) enabling
us to make an attempt to check this method of age-determination. The reason for this very low figure
(only 4% of the females from which marks were recovered), is that usually the processing of the carcass
is well advanced before the mark is found. A fair proportion of the marks are not found until the
cookers are cleaned some hours, or days, after processing.

1 A rate of ovulation of 0-7-0-75, suggested as a possible alternative (p. 385) appears to be incompatible with the
evidence of the sexual cycle. Such a low rate is only possible if the cycle is markedly different from that described here.
Thus, it would be necessary to accept much lower ovulation rates at the post-partum and post-lactation periods (of the
order of only 10-30 %) in order to bring the ovulation rate into line with a value of 0-7-0-75. It is possible that the
incidence of post-partum ovulations is lower than has been assumed ; the crucial evidence for this relates to the relative
sizes and rates of regression of corpora albicantia (pp. 430-4, and especially p. 433). The assumption of a high incidence
of post-lactation ovulations is thought to be well-founded (see pp. 436-44). The evidence considered as a whole favours
the higher rate of ovulation.

18 DI-

464 DISCOVERY REPORTS

We have then, 10 whales (all except one marked between 1934 and 1937) for which a minimum age
is known and for which data on the number of corpora in the ovaries are available. Particulars of
these whales are given in Table 30. What is it possible to say about these data?

For these individuals the mean period between marking and recovery is 13-8 years (ranging from
2 to 24 years) and the mean number of corpora is 15-7 (ranging from 3 to 40). If fin whales are marked
on average at about the time of puberty (when corpora begin to accumulate) then these data suggest
the mean increment of corpora is likely to be about 1-14 per year. If, on the other hand, they tend to
be younger or older than this stage when marked, then the average annual increment of corpora is
likely to be respectively more or less than 1-14, with the reservations imposed by the small size of the
sample. (It is, however, interesting that the sample is equally divided between whales less than, or
more than 15 years from marking to recovery. The 'apparent' annual increment is the same in both
groups, namely 1*14.)

Table 30. Particulars of ten

marked female fin whales from

which the ovaries

have been recovered {see text)

Length

Mark

Date

Number of

of whale

no.

marked

recorded

Years

C.L. + C.A.

(ft-)

Condition

696

11 Dec. 1934

26 Feb. 1 94 1

6-21

Non-pregnant

11991
1203 \

18 Jan. 1935

2 Mar. 1954

19-12

Pregnant, foetus 2-35 m.

1300!

35°7

26 Feb. 1935

18 Jan. 1956

20-89

Pregnant, foetus 4-33 m.

4938

21 Dec. 1935

13 Jan. 1948

12-06

Pregnant, foetus 2-77 m.

7972

4 Jan. 1937

19 Feb. 1948

11-13

Pregnant, foetus 3-35 m.

6818

9 Jan- J937

28 Jan. 1954

17-05

Pregnant, foetus 3-35 m.

10504

21 Dec. 1937

16 Mar. 1940

2-23

Pregnant, foetus 3-95 m.

2627

27 Dec. 1934

20 Jan. 1959

24-06

Pregnant

*6i37

22 Mar. 1936

4 Feb. 1958

21-87

Pregnant, foetus 2-77 m.

12870

7 Nov. 1955

29 Jan. 1959

3-23

Pregnant or recent ovulation

Total

I37-85

157

Mean

13-8

15-7

* Total excluding no. 6137

115-98

146

Mean

excluding no. 6137

12-89

16-2

There is some evidence bearing on the question of whether female fin whales are marked on average
before or after puberty. There are 24 female fin whales marked in the pre-war operations which were
recovered either in the same season (o-group) or a year later (1 -group), for which the lengths at recovery
were known (Rayner, 1940). The mean length at marking should be below the mean length (plus
2 s.E. of the mean) of the animals in this sample. It is known that the mean length of southern hemi-
sphere female fin whales at sexual maturity is 65-25 ±0-32 ft. (p. 407). The mean length of the o-group
and 1 -group sample is 65 -42 ±2- 18 ft. (mean and two standard errors), and this figure is probably
a little high. It is well known that length measurements made on floating factories tend to be slightly
higher than control measurements made by biologists, and the effect of the minimum length regulations
might be to exclude some of the smaller females from the o-group and 1 -group recoveries. It has
been shown that the average rate of growth at the period corresponding to these lengths is rapid,
amounting to some 3 ft. per year (p. 413), which has the effect of minimizing errors in estimating the
age at marking. It is, therefore, probable that the mean age of these whales at marking was a little
less than the mean age at puberty, say half a year, because the sample includes roughly equal numbers
of o-group and 1 -group females. The length variation (±2-18 ft.) corresponds to an age variation of

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA 465

±0-67 years, assuming that growth is at the rate of just over 3 ft. a year at this part of the growth

curve.

It appears then that about 157 corpora accumulate in from 12-63 to J 3*97 Years (i3"3±°,67 years),
that is, at a rate of about 1 -24 to 1 • 1 2 per year. So far it has been assumed that the ten mark recoveries
with ovary data are a random sample from the population. This is probable, but the variance for such
a small sample is large, and the true mean rate of accumulation may be higher or lower than this
figure. There is also another source of error which must be mentioned.

In the confusion of work on the deck of a whale factory ship there is a possibility that ovaries may
sometimes be collected by mistake from the wrong whale. It seems likely that this was the case with
mark number 6137. The female from which this came was 22 years from marking to recapture, but
the ovaries which accompanied this mark contained only one corpus luteum and 10 corpora albicantia.
The baleen plates had the appearance of those of a young whale. It seems probable that this was such
a case of mistaken identity, because by a remarkable coincidence two marks were recovered that same
day, on the same factory ship, by the same man, both from female fin whales of identical lengths.
For one (mark no. 12673) tne mar^ is notecl as having been 'found in the dorsal muscle'; for the
other (mark no. 6137) there is no note of the location of the mark. Now, if a mark was found in the
dorsal muscle it is probable that the ovaries would be obtainable as well. It is, therefore, possible that
the ovaries were actually from the whale which bore mark no. 12673, which was only 3-22 years from
marking to recovery. This would raise the mean annual rate of accumulation calculated in this way
to 1-30-1-46 corpora. In view of this uncertainty it will probably be best to ignore the doubtful
record and to repeat the calculations for the 9 mark recoveries about which no doubts have been
raised. Then it is estimated that in about 12-39^0-67 years on average some 16-2 corpora have
accumulated, that is about 1-24-1-38 per year (or 1-31 ±0-07).

Two other females shown in this table (nos. 1199/1203/1300, and no. 7972) are at first sight
incompatible with a rate of ovulation of i-43±o-i per year, but it should be emphasized that this
is a mean value. Even if ovulations in these two were at the rate of 1 -4 a year, then the apparent
discrepancies in the mark data can be explained by assuming that these females matured late (at 1 1 years
and 8 years respectively). If the rate of ovulation were lower then puberty could have been attained

earlier.

We can have little confidence in this evidence from the recovery of marked females, which is
inconclusive (owing to the small size of the sample), but does not necessarily disagree with the esti-
mated average increment of 1-43 ±o-i corpora per year, obtained from studies of the ovaries and the
reproductive cycle. This is the best we can do with the limited data. In view of the difficulty of
recovering whale marks together with other data, it seems unlikely that a precise confirmation of this
method of age-determination for the fin whale (or of any method) will be obtained for many years,
(but see footnote p. 470).

Age-determination
For average growth curves or for population studies the corpora counts may be used to determine
the post-pubertal age using the estimated figure of 1-43 ±o-i for the average annual rate of accumula-
tion. For animals which have not attained puberty the method cannot of course be used.

The estimated age at puberty averages 5 years (p. 407), varying in individuals at least from 3 to
8 years in a small sample, and the extreme range is probably greater. There will, therefore, be a con-
siderable variation in individual ages estimated in this way, according to whether the female became
mature at an early or a late age. A simple calculation shows that this variation alone would result in
a variation of ±4 corpora at a given absolute age. This is in reasonably close agreement with the

18-2

466 DISCOVERY REPORTS

frequency curves for the number of corpora in baleen group v females, and for the number of corpora
at the attainment of physical maturity. Thus, in the curve showing the number of corpora at the
attainment of physical maturity (Text-fig. 27), 81 % are in the range ±4 corpora about the mean. As
pointed out earlier (p. 392) it is unlikely that all females attain physical maturity at exactly the same
age, or even at exactly the same number of years after puberty. The discrepancy between the
estimated range of variation in a single year class and the actual range of variation at the attainment
of physical maturity is probably largely to be explained in this way. Also, the mean age and the age
range at puberty may be slightly greater than our small sample suggests; ear-plug laminations may
not always be formed biannually in immature females; and a further fact to be allowed for is the
incidence of multiple ovulations (p. 454).

The close agreement between the expected frequency distribution of ovarian corpora, as calculated
from the age variation at puberty, and the actual frequency distribution at physical maturity, supports
the earlier conclusion (p. 384) that there is very little variation in the annual rate of ovulation and
accumulation of corpora. This is further evidence against the conception of a polyoestrous sexual
cycle in which, during an ovulatory period, a variable number of ovulations may precede that which
initiates pregnancy.

It is considered that the number of corpora in the ovaries of a fin whale female, of any particular
age, will probably be within the range of the mean number of corpora expected at that age ±4; this
corresponds to an estimated age which will probably vary from the true age by up to ±3 years. In
exceptional cases the apparent age may differ from the true age by more than this. For instance, the
combined effect of an early puberty and a number of multiple ovulations would be considerable.

For estimating individual ages the number of ovarian corpora excluding corpora atretica (p. 382)
and pathological bodies (p. 343), is divided by 1-43, and to the result is added 5 years, to allow for the
immature period. For animals taken in the Antarctic half a year is then subtracted. Thus first pregnancy
females taken in the Antarctic with an average of 1-43 corpora are on average estimated to be 5 \ years
old. The result should then give the probable age to ±3 years with about 90% accuracy. For example,
a female with 28 corpora in the ovaries is estimated to be 19 ±3 years old.

In using the counts of ovarian corpora to determine the age for purposes of average growth curves,
population studies, etc., this individual variation can safely be ignored, because in a large sample
individual variations caused by early or late puberty, multiple ovulations, etc. will counterbalance
each other.

Comparison with other methods
The method of age-determination based on the external ridges of the baleen plates which was
developed by Ruud (1940 and later papers) has already been referred to (pp. 335-37). Unfortunately
this method is limited in application to the younger age groups, and is, therefore, complementary to
the method based on the ovaries of mature females. Over the range of ages where the methods over-
lap, the latest work of Ruud (1958) suggests that the annual rate of accumulation of corpora, according
to the ages determined from baleen records, is about i-6. This is in fairly close agreement with the
present estimate (1-43^0-1 corpora per year).

After the present work had begun a new method of age-determination was suggested by Purves
(1955). This arose out of studies on the physiology of hearing in Cetacea, in the course of which it
was found that the ear-plug in the external auditory meatus of baleen whales is of a laminated structure.
The core of the plug consists of a number of concentric laminations which follow the curvature of the
so-called 'glove-finger'. Each lamination consists of epidermal elements derived from the zona
corneum of the 'glove-finger'. From the presence of imperfectly keratinized epithelium in each

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA 467

lamination it seemed that the growth of the epidermis is arrested at regular intervals. It was assumed
that the period of arrested growth corresponds to the migratory periods (when the physiological
demands of active swimming coincide with complete absence of food), so that each lamination repre-
sents a growth period of approximately six months. Later Purves and Mountford (1959, p. 137) stated
that ' It is very doubtful whether environmental conditions have any direct influence on the time of
formation of the laminae of the ear plug in whales, although nutritional conditions may to some extent
determine their thickness. Since there is strong evidence [not given by them] that lamina formation
is an inherent moulting cycle it is very probable that it takes place whether the whale migrates or not.
If the rate of moulting can be established the ear plug would probably be a more accurate age indicator
than the fish scale.'

Comparison of ages estimated in this way from the ear-plug with the corresponding baleen plates
for a small sample of North Atlantic fin whales (Laws and Purves, 1956), suggested that the hypothesis

EAR -PLUG AGE (YRS.)

Text-fig. 55. Comparison of the ages of individual fin whales estimated from baleen plates and ear-plugs

(white, North Atlantic; black, Antarctic).

of a biannual formation of laminations was correct. This agreement between baleen plates and ear-
plugs was partly confirmed with a small additional sample of antarctic fin whale material collected
in 1955-56. The ear-plug ages of this sample (estimated on the basis of two laminations per year) are
given by Purves and Mountford (1959) to whom the material was made available. Professor J. T.
Ruud and Mr Age Jonsgard (Statens Institutt for Hvalforskning, Oslo) kindly undertook the examina-
tion of the baleen plates. In Text-fig. 55 the ear-plug ages are plotted against the ages estimated from
the baleen plates. If the age-determinations by these two methods are in exact agreement then the
points should fall on the 450 line which is shown. It is apparent that there is fairly close though not
exact agreement between these two methods for the first 4-5 years, after which baleen plate ages
(owing to wear at the tip of the plates) are supposed to be minimum values. Chittleborough (1959)
finds similar agreement between baleen plates and ear-plugs of humpback whales.

Purves (1958) and Purves and Mountford (1959) used the assumption that about 1-4 corpora are
accumulated annually in the ovaries of fin whales (Laws, 1956a) to confirm the assumed biannual
rate of lamina formation in sexually mature females. Some 14-15 corpora accumulate in the ovaries
between puberty and physical maturity, and this period is, therefore, estimated to be 10 years (but
see p. 388, where attention is drawn to an error in this work). About 12 laminations were found at

468 DISCOVERY REPORTS

sexual maturity and about 32 at physical maturity, corresponding to an incremental rate of approxi-
mately two a year. It was also found that the mean curve of growth in body length gave lengths at the
1 2th and 32nd laminations which were close to the previously estimated lengths at sexual maturity
and physical maturity.

So far the best evidence for the biannual formation of ear-plug laminations, therefore, comes from
this check against the ovaries, using the figure of 1-4 for the annual increment of corpora. The nature
of the fin-whale sexual cycle, particularly of the female, which was discussed earlier in this paper
suggests additional strong circumstantial evidence in favour of a biannual cycle of lamina formation.
It also suggests a possible exteroceptive factor responsible for the regular formation of the laminations.
Owing to the migratory cycle, most fin whales are usually subjected each year to two periods of
increasing day lengths. In the female these are associated with oestrus (incompletely suppressed during
pregnancy). In the male it appears that the period of increasing day lengths associated with the spring
migration does not initiate a second period of sexual activity, because, it was suggested, of the long
period of spermatogenesis which precedes this migration and is followed by a refractory period. This
is paralleled by the suppression of oestrus in pregnant females.

One of the most characteristic features of oestrus is the cornification of the vaginal and other
epithelia. It seems possible that the growth cycle of the ear-plug is in fact related to the migratory
cycle as was initially assumed, not because of arrested growth associated with the expenditure of
energy on migration, but because of a biannual hormonal cycle associated with and regulated by
varying day lengths. According to this hypothesis there is during each migration a rise in the amounts
of circulating oestrogens in both male and female, which results in the formation of a keratinized layer.

This hypothesis explains lamina formation in adults satisfactorily, but little is known of the migra-
tions of immature fin whales and the early laminations are the most difficult to interpret. This inter-
pretation for adults is to some degree independent of the estimated figure for the annual increment
of corpora, so that the ear-plug age estimates are at least partly independent of the ovaries.

Purves and Mountford (1959) give the ages, estimated from ear-plugs, of samples of fin whales,
and the ovaries of the females in these samples have been examined by the present author. Individual
ages have been estimated from the corpora numbers in the way described above (p. 466). In Text-
fig. 56 the ages estimated from ear-plugs are plotted against the ages estimated from the ovaries for
in individuals. The 45 ° line shown corresponds to an exact agreement between the two methods.

It is expected that, owing to individual errors in the estimates based on corpora numbers (related
in the main to the variation in the age at puberty), the majority of the ovarian ages should lie within
± 3 years of the regression line representing exact agreement. It is assumed that the ages estimated
from the ear-plug laminations are accurate, although some plugs are difficult to read and may give
inaccurate results. Also the interpretation of immature laminations is doubtful. Purves and Mount-
ford (1959) estimate the maximum error by this method to be ±2 years. In Text-fig. 57, the variation
of ovary ages about the theoretical mean regression line is shown. This curve was constructed by
drawing in other oblique lines parallel to the original regression line, displaced laterally at yearly
intervals. The total number of points lying within each pair of lines was obtained and plotted to show
the frequency distribution about the assumed mean. The results are near to expectation; 72% of the
estimated ovarian ages lie within ±3 years, and 82% within ±4 years of the regression line showing
an exact correlation, and the extreme range is ±12 years. Only seven values lie outside the range
±6 years and it is probable that the five extreme values represent combined errors of the two methods.
The results are in close agreement with the distribution of corpora at physical maturity, shown in
Text-fig. 27. It should be noted that there is a group of points in Text-fig. 56, for which the ovarian
ages are too high. This is because 5 years is taken as the age at puberty, and some nine of these records

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA 469

(indicated by a dotted line) are probably from females which attained puberty earlier than 5 years.
If it were possible to allow for this the frequency distribution in Text-fig. 57 would be slightly more
symmetrical.

30
i/i

UJ
%

o 20

or.

IO 20 30

OVARY AGE (YRS)

Text-fig. 56. Comparison of the ages of individual female fin whales estimated from ear-plugs and ovaries.

-10

-5 O +5

RELATIVE AGE IN YEARS

+IO

Text-fig. 57. Frequency distribution of ovary ages about the regression line shown in Text-fig. 56.

This brief comparison with other methods of age-determination supports the conclusions about the
rate of ovulation and the accumulation of corpora reached in this paper. Ovarian counts may be
used with confidence to estimate the ages of mature female fin whales.

Ages determined independently by the three most important methods in use for baleen whales
(ovarian corpora, baleen plates, and ear-plugs) are in reasonably close agreement, but all three methods
have been criticized on the grounds that it has not yet been possible to check any of them against

47° DISCOVERY REPORTS

animals of known age. If the validity of any one of the methods could be confirmed by reference to
known-age animals, then, in view of the agreement between the results obtained separately by the
other methods, it could be taken that all three methods are valid for studies of the age-composition
of the catches. In the 25 years since effective whale-marking began, only 10 marked fin whales have
been recovered together with material enabling age-determinations to be made. It seems unlikely that
there will be any great increase in such recoveries in the near future, and for the time being the sample
now available is the only independent check on age1. The estimated annual increment of corpora
and the figure suggested by these marked females are very similar, but owing to the small size of
the sample the apparently quite close agreement is not conclusive. There can, however, be no reason-
able doubt that the ovaries provide reliable estimates of age, and that the ear-plugs and baleen plates
(with some reservations) are also reliable.

One important qualification is called for. The estimated ages are greatly dependent on the method
of examination. In this respect the counts of ovarian corpora are perhaps least liable to error. The
interpretation of baleen plates is difficult, and the same applies to the ear-plug. In this connexion
reference must be made to the recently published papers of Ohsumi, Nishiwaki and Hibiya (1958)
and Nishiwaki, Ichihara and Osumi (1958). These authors, by plotting lamination number against
corpora number, and assuming two laminations are laid down each year, obtain a figure of 0-8-0-9
for the average annual increment of corpora in northern and southern hemisphere fin whales. Their
results differ in this and other respects from Nishiwaki (1957), Purves and Mountford (1959) and the
present paper. It seems likely that interpretations of the ear-plug laminations differ (and/or counts
of corpora), and a standardization of methods is desirable.

n . , Applications

Survival curves

Having shown that the corpora albicantia persist throughout life and accumulate at a regular rate,
it is possible to use corpora counts, made on samples of the antarctic catches since 1925, to investigate
the changing age structure.

A full detailed treatment of this subject would be out of place here, but to indicate the possibilities
let us take as an example the data for the two seasons 1939/40 and 1940/41, for Antarctic area n
(o° to 700 W.). For this period there are corpora counts relating to 389 adult females, 170 from the
season 1939/40 and 219 from 1940/41. Brown (1954) has shown that there is little dispersal between
the different whaling areas, but suggests that there may be a significant interchange between areas 1
and 11. Virtually no whaling had been carried out in area 1, prior to 1955/56 and it may be assumed
for present purposes that the whales in area 11 constitute a stock which is separate from the other areas.

This sample from area 11 (1939-41) has been chosen because it is fairly large and of the samples
available is probably least influenced by changes in the size of the catches. The age composition of
post-war samples is affected by the low level of catching between 1940 and 1945. From Text-fig. 54
it would appear that for the effect of fluctuating catches to be minimal the most suitable samples
should come from area 1 in 1955/56, area 111 before 1934, area iv before 1937, and area v before 1930.
If the populations of fin whales in the different areas are distinct and isolated (though not in a genetical
sense) such samples might enable estimates of the natural mortality rates of adult females to be made.
Unfortunately adequate samples meeting these conditions are not forthcoming.

Three possible methods of constructing survival curves have been examined and although, owing
to sampling difficulties none of them is really satisfactory, they can be used to compare the changes
in the stocks from year to year in a relative way.

1 Since this was written there has in fact been an increase in the number of such recoveries in Japanese factory ships.

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA 471

First, we could assume that mortality is constant with respect to age, so that the decline in numbers
is logarithmic. A regression line is fitted to the logarithms of the corpora albicantia or age frequencies
and, if it can be assumed that the age composition of the catch is fully representative of the population
being studied, the slope of this line is e~zt, the survival rate, and z is the instantaneous mortality rate,
including both fishing mortality and natural mortality. If working in annual age groups then t = 1
but with corpora albicantia t is assumed to be 1-43.

This method was used by Purves and Mountford (1959), with reservations, for their fin whale data.
The method used by Hylen et al. (1955) requires similar assumptions. It seems, however, that in
view of the limitations of our samples this method is not applicable and gives a spurious impression
of accuracy. Our present knowledge of the relation between the catch and the real population is
sufficient to indicate only that confident estimates of absolute mortality rates cannot be given by these
methods (nor, so far, by other methods). A detailed discussion of the sampling problem cannot be
given here, though a short discussion of some relevant problems will be found in a paper by Laws
(i960). However, some of the more important factors which are relevant must be briefly mentioned
at this point.

An important problem is related to the segregation of the stocks on the Antarctic whaling-grounds.
Laws (i960) has discussed geographical segregation and segregation in time.

The catches show a definite pattern of body size segregation by longitude, when mean lengths are
plotted by 10° sectors of longitude, perhaps related to food and oceanographic conditions. This may
reflect a geographical segregation by age, which would have important implications for the analysis of
age distribution in the catches from different parts of the whaling-grounds.

Fin whales migrate to the antarctic feeding-grounds at different times according to age, sex and
reproductive status. The whaling operations, on which we depend for our samples, do not extend over
the whole of the summer months when whales are on the feeding-grounds and in recent years the
whaling season has become much shorter and generally later. This means that the different age groups
in the population are not equally vulnerable to whaling, because they are at risk for different periods.
In the fin and blue whales the oldest animals appear on the feeding-grounds first, younger animals
next and the youngest last of all. The period when samples are taken may therefore have a profound
effect on their age composition. For example, if separate survival curves are constructed for monthly
samples taken in November, December, January, February and March the slope is found to be steeper
with the progression of the season. Because the older animals tend to arrive on the grounds earlier
they may be at risk longer and some of the younger animals arrive after the whaling operations have
ceased, so that there may tend to be a bias towards older animals in the age-composition of the catches.
An example of this type of selection can be seen in samples from area 11 in 1939-41 (Text-fig. 58),
and from area 1 in 1955/56 and 1956/57 (Laws, in press).

In exploited stocks of fish it can usually be assumed that recruitment, although varying from year
to year, does not change progressively over a number of years in response to exploitation. Although
brood strength fluctuations affect the scatter about a curve they do not alter the slope. In whales which
bear a single young, recruitment is very closely related to the number of adult females (fluctuating
within rather narrow limits) so that in general changes in the size of the stock of adult females will be
accompanied by similar changes in the number of recruits. Such changes will affect the slope of the
catch curves; the effect of reduced recruitment will be to produce a lower apparent mortality rate.

A further difficulty is that in a long-lived animal changes in overall mortality rates only become
gradually apparent as new year classes enter the exploited part of the population. If there is no dif-
ferential selection of animals in respect of age, above a certain size governed by the minimum length
regulations, the relative age-composition of the mature population should change only slowly and the

472 DISCOVERY REPORTS

effect of varying intensity of whaling should show initially only at the ages when animals enter the
catches. It should take many years for these changes to work their way through the age structure of
the population, for the catches of fin whales may be drawn from as many as fifty year groups. Marks
have been recovered from antarctic fin whales as long as 26 years after marking (the first effective
marking was carried out in 1932/33).

Thus even if the catch were a random sample of the stock in the sea important changes could take
place in the stock without being detected by the calculation of instantaneous mortality rates derived
from a regression line fitted to the catch curve. This method will give only a crude approximation to
mortality rates operating over a period of years, and mortality rates derived in this way may be mis-
leading when applied to current situations.

The catch per unit effort gives an index of abundance of the stock. In estimating current mortality
rates the most satisfactory treatment would perhaps be to convert the sizes of year classes at two
known times to comparable values, by applying effort values so as to obtain density indices for different
age groups. Estimates of mortality can then be made from pairs of successive years for different year
classes fully recruited to the exploited part of the stock. Unfortunately, the unit of effort in whaling
is not stable owing to increasing catcher efficiency (see Laws, in press) and it has not yet been
possible to calibrate these changes in effort so that they can be used to estimate mortality rates. This
is potentially the most accurate approach, though sampling difficulties and changing recruitment
again pose serious problems.

A method which will give us some indication of changing mortality rates is to construct time-
specific survival curves by smoothing the frequency distribution of corpora numbers (Table 31) more
or less heavily, according to the size of the sample. The resulting curve is converted by a graphical
method to an age frequency distribution by finding the values corresponding to 1-43, 2-86, 4-29
corpora up to 52-91 corpora (equivalent to post-pubertal ages of \ year, \\ years, z\ years and
37^ years). An additional 5 years must be allowed for the immature period, making the ages 5^, 6|,
7^ and up to 42^ years (Table 32).

Direct observation of the age structure of juveniles is not possible by this or any other method
because of the minimum size limit, which means that early year classes are absent or not fully repre-
sented in the catches. An indirect method must, therefore, be used to estimate the recruitment to the
population.

The data given in Table 32 show a total of 2681 females. For present purposes it may be presumed
that fertility does not change with age (see p. 454). The conception rate is taken to be 1-18 per 2-year
cycle, assuming 18% post-partum ovulations (p. 430), that is 0-59 per year. No allowance is made
for post-lactation conceptions, or for twins, because it is thought that post-natal survival of these
groups is low. On this basis 2681 adult females represent 1582 conceptions. The foetal sex ratio was
shown to be 52% male: 48% female so these females are estimated to carry 759 female foetuses.
Let us allow 10% prenatal mortality to cover foetal deaths from conception to birth and maternal
deaths from mid-pregnancy to parturition. This figure is based on an assumed 5% foetal mortality
and about 12% maternal deaths, the latter estimated from table 32. (An assumed stable population
of 2681 mature females has a recruitment at puberty of 325 or 12%, which should be balanced by
a corresponding number of deaths.) Then 683 female calves are expected to be born, the earlier
qualifying remarks about sampling being understood to apply. These data indicate that total immature
mortality assuming a stable population is 52-4%. If the population from which this sample is derived
was decreasing then the immature mortality would be higher than this value.

This 'apparent' survival curve is plotted on a logarithmic scale in Text-fig. 58. The logarithmic
scale has the advantage that a straight line implies equal rates of survival (or mortality) with respect

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA 473

to age. The curve is similar to the diagonal type of Pearl and Miner (1955) and Deevey (1947), but
it represents both natural and fishing mortality. A prominent bump in the curve from 20 to 35 years
suggests some bias towards older females in the sample as might be expected in view of the tendency
(mentioned above) for older animals to be over-represented in the samples. This is a further warning

Table 3 1 . Frequency distribution of corpora, and apparent survivors up to an age
corresponding to 55 corpora. Area II, 1939-41.

Smoothed

frequency

No. 0

10 (time

Survivors

No. of

x 10 (time

Survivors

corpora Frequency specific)

(dynamic)

corpora

Frequency

specific)

(dynamic)

350

389

5°

310

350

3°

280

329

244

295

236

275

210

250

186

222

168

211

138

190

128

182

100

166

104

159

—

147

—

140

—

130

119

—

113

—

103

—

5°

—

— ■

—

Total

389

—

Table 3:

2. Apparent survival data

for area

11 fin whale females prior to

1940

Survivors

■>

Age

Survivors

Age

Survivors

Age

Time

•v

Time

(yr.)

specific

Dynamic

(yr.)

specific

Dynamic

iyr.)

specific Dynami

325

370

3i£

23 11

280

33°

19!

32j

16 6

245

290

20J

33*

10-5 6

210

256

21*

34i

7-0 6

180

225

22i

35*

4-8 5

io£

142

200

23i

36*

3-° 5

135

182

24*

37i

3-° 4

12*

120

162

25*

3«i

2-5 4

i3i

io5

148

26!

38-5

39*

2-0 4

137

27J

4°l

i-6 4

*si

122

28J

41!

1-4 2

i6i

ii3

29i

42i

1-2 2

i7i

100

3°£

43!

1-0 0

Totals 2681 3361

19-2

474 DISCOVERY REPORTS

against reading too much into the apparent survival curve and against describing the age structure

by a single regression line.

A third method of constructing an apparent survival curve is the dynamic method which assumes
that the sample represents the ages at death. In the present case the sample represents deaths due to
whaling and does not take into account natural mortality. However, the adult natural mortality rates
of fin whales should be very low to counterbalance the low reproductive rate and long life-span and
are probably constant over most of the age range. If we accept the fact that sampling difficulties
mean that estimates of absolute mortality rates derived from survival curves are unreliable and not
contemporary, we can still expect to obtain limited information on changes in the stocks by comparing
the shapes of apparent survival curves. While it is true that neither method is really satisfactory this
is thought to be preferable to calculating instantaneous mortality rates from the slope of a single

IOOO

500

IOO

O
>

AREA H 1939-1941

- 1 —
30

AGE IN YEARS

Text-fig. 58. Time specific survival curve for female fin whales. See text for method of construction.

regression line. For this purpose dynamic survival curves appear to be more desirable. Bias towards
the catching of older animals (see above) will be shown in the dynamic curves as lower survival rates
or higher mortality rates (which is correct) rather than as higher survival or lower mortality as in time
specific curves.

Dynamic survival data for the mature females is given in Table 32. These are derived from the
counts of corpora albicantia in the following way. There are 389 individuals in the sample and all of
these have survived to an age corresponding to one corpus luteum or corpus albicans; there are
39 individuals in the 1 -corpus group, from which it is inferred that only 350 survive to the 2-corpora
group; 21 individuals in the 2-corpora group are then subtracted to give the number which survive
to the 3-corpora group, in this case 329; and so on up to the 55-corpora group when there is no sur-
vivor. These data are converted to actual age data as before by finding the values corresponding to
1-43, 2-86, etc. corpora and the result is set out in Table 32 and Text-fig. 59. Recruitment at birth

475

AGE-DETERMINATION BY MEANS OF THE OVARIAN CORPORA
is calculated as before to be 857 indicating a total immature mortality from birth to 5 years of about
53'3%> a verY similar result to that given by the time specific method.

This apparent survival curve again approximates to the diagonal type (Text-fig. 59). Mortality
appears to be higher in the early segment of the curve and increases again after 25-26 years. Between
9 and 26 years the survival curve plotted on a logarithmic scale is almost exactly linear, that is to say
the decline in numbers is exponential. For this segment of the curve the apparent rate is e 00973 or
90-8%, corresponding to an annual mortality rate of 9-2%.

One of the central problems of whale research is to define and distinguish the different populations
being sampled ; a complementary problem concerns the extent to which the samples from the catches
are representative of the actual population in the sea. Until more progress is made in the solution of
these problems it would seem that population studies will lack precision.

1000

500

100

a.
o
>

>
a

20 30

AGE IN YEARS

Text-fig. 59. Dynamic survival curve for female fin whales. See text for method of construction.

Growth curves
The relation between length and corpora number for area 11 females has already been discussed
(Table 6, Text-fig. 25). The average length at physical maturity was there taken to be 73 ft., which
was the average length of 187 females which had more than 20 corpora in the ovaries. Nishiwaki,
Ichihara and Osumi (1958) suggest that after the attainment of physical maturity there is a slight
decrease in body length and the present material also suggests this, although the shrinkage is evidently
slight and there is no statistical support for it. The relative growth curve in Text-fig. 25 was, therefore,
fitted to the average lengths at different corpora numbers so that it attained 73 ft. at 14-3 corpora.

This smoothed curve may be converted to a length-at-age curve in the same way as the age structure
of a sample was obtained (p. 466). The lengths corresponding to 1-43, 2-86, 4-29 corpora, etc., are
equivalent to post-pubertal ages of about \ year, i\ years, 2 \ years, etc., and as before an additional
5 years is added to allow for the immature period (Table 33).

476 DISCOVERY REPORTS

In Text-fig. 60 these length-at-age data are plotted. In addition the estimated mean length at
puberty (65-25 ft. at 5 years) and the estimated mean length at weaning (39 ft. at 7 months) are shown.
The pre-natal growth is known from the previous studies (Laws, 1959 a; and above, Text-fig. 30).
Conception is taken to be 0-93 years before birth.

Table 33. Length-at-age data for female fin whales {see text)

Age

Stage of life-cycle

Body length (ft.)

Birth

20-80

7 months

Weaning

39-00

5 years

Puberty

65-25

52 years

—

67-80

6| years

—

69-70

7! years

—

70-80

8£ years

—

71-60

9 I years

—

72-20

10J years

—

72-50

n| years

—

72-70

12 J years

—

72-85

13 J years

—

72-95

14! years

Physical maturity

73-00

> 15 years

—

73-00

The von Bertalanffy equation (von Bertalanffy, 1938; Beverton and Holt, 1957) has been fitted to
the length-at-age data for mature females in area 11 (Table 33), 5J years and over, obtained from the
smoothed curve showing average lengths at different corpora numbers. This gives a theoretical curve
in which lt = Lco(i — e~kU~'o)), and a good fit is obtained for values at estimated ages above 5 years.
It is shown in Text-fig. 60 as a continuous line for which Lx = 73-0 ft., K = 0-450, and t0 = 0-368.
The parameter t is the post-conception age in years. This theoretical curve has been extrapolated
backwards to t = 3-93, that is equivalent to a post-natal age of 3 years.

80
^ 70-

h-
UJ

S 60

x 50

i 40
ui

30
>
o

o 20

PHYSICAL MATURITY

-O O— — O 1 I o-

PUBERTY,

lt=73O(j-e"0450(,"0368))

^WEANING

BIRTH

■25-0

2000c

150 x

y-
O

100 -J

5-0 *

I 2 3 4 5 6 7 8 9 IO II 12 13 14 15 >I5

AGE IN YEARS

Text-fig. 60. Length-at-age curve for female fin whales, Antarctic area II.

This growth curve has been completed by inserting the foetal growth curve already obtained, with
a mean neo-natal length of 20-8 ft. This leaves the segment of the curve from birth to 3 years to be
completed, but we have an approximate value for the length at weaning (39 ft. ; Mackintosh and
Wheeler, 1929), and the age at weaning has been established as about 7 months (p. 445). This has
been used to complete the growth curve and agrees quite well with expectation. The equation

SUMMARY 477

/ _ y^-o (i—e~ °'45" -°-368)) gives values, for the ages corresponding to birth and weaning, of
16-3 and 297 ft. respectively. These are quite close to the observed values and the accelerated
growth towards the end of gestation and during the lactation period is, as it were, superimposed on
the theoretical curve.

The existence of such a close correspondence between the theoretical curve and the observed values
makes for additional confidence in the figure of 1 -43 for the estimated annual increment of corpora.

There is, however, one discrepancy which will have been noticed in Text-fig. 60. The estimated
value for the mean length at puberty (65-25 ft.), which has been inserted at a point corresponding to
an age at puberty of 5 years, is not in agreement with the theoretical curve derived from the von
Bertalanfly equation (which in fact gives a value of 67-02 ft. at this age). This requires some explanation.

Although growth in body length has here been described by a smooth curve, it almost certainly
occurs in a series of steps related to the periods of intensive summer feeding in antarctic waters, and
partial winter fasting in low latitudes. This was discussed especially for newly mature females, when
it was concluded that there was probably a rapid acceleration of growth associated with the summer
feeding period (Text-fig. 38). The values from which the theoretical curve has been calculated are mean
lengths for females taken during the same period of the year in antarctic waters when feeding on krill,
and are therefore directly comparable. The value for the mean length at puberty was inferred from
the length frequency distributions of immature and mature females, and is not, therefore, comparable
with the other values. The estimated mean age at puberty obtained by a similar method is 5 years, and
therefore represents the time of year when growth is thought to be minimal. This partly explains
why the length at puberty calculated in this way is below the theoretical curve. Another reason for
this is that the data on length and corpora numbers apply to the area 11 sample only, whereas the
mean length at puberty was calculated from all available data, representing several areas. There is
reason to believe that the length at puberty in area 11 may be slightly higher than the general level
in the Antarctic (see also p. 407).

SUMMARY

1 . This paper is concerned primarily with female fin whales, Balaenoptera physalus (Linn.), and is
based on several thousand whales examined in antarctic waters by or on behalf of 'Discovery'
Investigations between 1925 and 1949 and on behalf of the National Institute of Oceanography from
195 1 onwards.

2. In an introductory section, previous work on the reproductive cycle, migratory cycle, growth
and age of baleen whales is briefly reviewed.

The main part of the paper falls into three parts. The first deals mainly with the detailed structure
of the ovaries, the evidence for the persistence of corpora albicantia, and the estimated annual rate of
accumulation ; the second part describes the annual sexual cycle, and provides a further independent
estimate of the rate of ovulation ; the last section is concerned with age-determination by means of
the ovarian corpora, and some examples are given to illustrate the application and value of the method.

3. The mean paired ovary weights of immature, non-pregnant mature and pregnant females are
respectively 0-97, 1-97, and 3-14 kg. The increased weight of the ovaries of pregnant females is only
partly explained by the development of the corpus luteum. Increased vascularization, and increased
follicle size and numbers probably account for the rest. The maximum paired weight of fin whale
ovaries was 52 kg., but these were probably in a pathological condition.

4. The morphology and anatomical relations of immature and adult ovaries are briefly described.

5. Primary follicles begin to develop in the last 2-3 months of gestation; they are numerous in the
cortex of the ovaries of immature females, but are very sparsely distributed in the cortex in sexually

478 DISCOVERY REPORTS

mature females. In the majority of immature females the largest follicle is less than i cm. in diameter,
but at the approach of puberty the mean maximum follicle size rises to about 3 cm. or more between
June and November.

In mature females the mean maximum follicle size is greatest in the 'recently ovulated' class
(3 -8 ± 0-53 cm.), and is lower in pregnant, lactating, and ' resting ' females (respectively 278 ± o- 1 5 cm.,
1 -93 ±0-34 cm. and 1-93+0-29 cm.). The existence of a cycle of follicular activity has been demon-
strated in pregnant females, reaching a peak in mid-pregnancy (November/December). At this time
the follicles enlarge, but do not mature, owing to the presence of the active corpus luteum. No acces-
sory corpora lutea form during pregnancy as happens in some other mammals. From the follicle
sizes it appears that there are periods of follicular activity in early lactation and at the end of lactation.

6. Ovulation probably occurs when the follicle attains a diameter of about 7 cm., collapsing to
about 4 cm. immediately after ovulation and then, as the corpus luteum forms, increasing to 8-28 ±
0-82 cm. in the corpus luteum of the cycle, or to 11-44 + 0-15 cm. if pregnancy supervenes. There is
no reason to suppose that pseudopregnancy occurs. It is possible that there is a slight tendency for
the right ovary to ovulate more frequently than the left in baleen whales, but the data for blue and
fin whales do not show a significant difference. There is a marked tendency for ovulation to occur in
the vicinity of the anterior pole of the ovary. The mean weight of the corpus luteum of ovulation is
0-375 kg. (range 3-4 g.-i-5 kg.) and the mean weight of the corpus luteum of pregnancy is o-88i kg.
(range 0-2-2-4 kg-)- Various morphological types of corpora lutea are described and related to the
modes of formation; vesicular corpora lutea constitute 17-1% of all corpora lutea. Accessory corpora
lutea comprised only 3 -7 % of all corpora lutea examined ; they have a mean diameter of 3 -88 ± o-8o cm.
and a weight of about 45 g. The size ranges of corpora lutea of ovulation and pregnancy are large, so
that these bodies cannot be distinguished from one another on the basis of size, and no certain diag-
nostic features have been found.

7. There is no significant difference in the mean size of corpora albicantia in the ovaries of pregnant,
lactating, and 'resting' females; they have a mean diameter of 2-5 cm. and a mean weight of about
10 g. The various morphological types of corpora lutea are reflected by the corpora albicantia and,
in particular, the incidence of vesicular or radiate corpora albicantia is not significantly different from
the proportion of vesicular corpora lutea.

It appears that corpora lutea regress to a constant proportion of their initial size, and as this is large
they remain visible throughout life.

Three age groups of corpora albicantia have been identified on the basis of anatomical and histo-
logical changes associated with regression. 'Young' corpora albicantia have a mean diameter of
4-01 cm. and a weight of 41 g. ; the values for 'medium' corpora albicantia are 2-94 cm. and 15 g.,
and for 'old' corpora albicantia 2-01 cm. and 5 g.

The ratio of ' young ' to ' medium ' corpora albicantia in the ovaries is 1 : 2 and it is shown that the
' young ' corpora albicantia probably represent one year's increment of corpora and take about three
years to regress to 'old' corpora albicantia. From this it can be calculated that the mean annual
increment of corpora is probably about 1-4-1-5 (although there is a possibility that the rate is only half
this value), and as the corpora persist throughout life, counts of them may be used to determine age.

8. Two other structures in the ovaries are described, the corpora aberrantia and the corpora
atretica. The former are included in the corpora counts (as corpora albicantia) for the purpose of age-
determination, but the latter are ignored.

9. It has been possible to confirm earlier work on the correlation between the attainment of physical
maturity and the accumulation of 14-15 corpora lutea and corpora albicantia. The frequency distribu-
tion of the number of corpora shortly after puberty (baleen group v), and at the threshold of physical

SUMMARY 479

maturity, have been compared. These frequency curves are found to be very similar in shape and
range, with standard deviations of respectively 3-3 and 3-94 corpora. This amount of variation is
almost entirely explained by the spread in the ages at puberty, and suggests that there is a very regular
annual increment of corpora, which is difficult to explain on the basis of a polyoestrous sexual cycle.

10. Histological examination of a series of fin whale testes indicates that the period of maximum
activity extends from about April to July and is minimal in January and February. The seminiferous
tubules undergo a seasonal variation in diameter, decreasing progressively from 164// in October to
140 n in February and rising again to 165 // in April. The maximum diameter recorded (241 /i) was
from March. Reference to the incidence of diatom film (which is absent in lower latitudes), indicates
that on entering antarctic waters the tubule diameter is about 170 //, falling to 140 ft when the diatom
film is well developed. In immature males the tubule diameter averaged 79^ and in one near to
puberty 102 ft.

11. A mean curve of foetal growth is given and from this the conception dates of individual
foetuses can be estimated. 12 June is estimated to be the mean date of pairing, but the frequency-
distribution of conceptions is skewed, with a peak in May /June. It is estimated that 77 % of foetuses are
conceived between April and August, and only about 6% between October and March. As the gesta-
tion period is about 1 1 ^ months the frequency distribution of births can easily be obtained. Annual
variations in the timing of the breeding season are discussed.

12. Earlier estimates of the mean length of the female at puberty (65-25 ft.) have been confirmed
on the larger samples now available; the standard deviation of the length at puberty is 2-07 ft., but
this is influenced by the post-mortem history of individuals and the variance in life is probably much
less. The average age at puberty based on ear-plug ages and ovarian examination is estimated to be
about 5 years, ranging from 3 to 8 years in the relatively small sample available.

13. The state of the mammary gland is used to diagnose nulliparous and primiparous females. Of
88 females pregnant for the first time 68 % had only one corpus luteum and only 9 % had more than
two corpora. The mean number of ovulations preceding conception was 1-42.

The pairing season of primiparous females was estimated, like that for all females, from foetal
length data, and it is found that the median date of pairing is about 21 July. That is about 4-6 weeks
later than multiparous females, and the frequency curve of conceptions is symmetrical, not skewed.

The rate of growth in length for females in their first pregnancy can be determined, employing
foetal age as a time-scale. The average female grows from 65-25 ft. to about 68-69 ft- during the twelve
months following puberty. There appears to be a marked increase in the growth-rate related to the
short annual period of intensive feeding. The growth in the following year has also been studied.

14. Evidence is presented which suggests that ovulation is spontaneous. It appears that at puberty
there is a single ovulation, and if the female is not successfully mated she goes into anoestrus without
experiencing further ovulatory cycles at this time. Although puberty is normally attained in July, it
may also be attained outside the normal pairing season, mainly in November, December, and January.
Then also there is a monoestrous cycle, but it is almost invariably unsuccessful because, it is believed,
the males are sexually inactive at this time.

The relation of puberty to the migratory cycle is discussed. In the majority of females puberty is
preceded by a period of intensive feeding in the Antarctic, when growth is probably rapid, but the
main exteroceptive factor bringing about the first ovulation appears to be the period of increasing day
lengths associated with the northward migration. There is a second, subsidiary period when other
females attain puberty in December, after a southward migration, during which they also experience
increasing day lengths. It is suggested that puberty is initiated by a combination of age and increasing
day lengths, the light threshold becoming lower with increasing age.

48o DISCOVERY REPORTS

15. The pairing season of multiparous females is investigated as before from foetal length data.
The peak conception period is from April to July, with 8 June as the median date of pairing, and the
curve is skewed, with a long tail from July to December. Less than 13 % of all multiparous conceptions
are estimated to take place before May. The average age of females pairing in March and April is
much higher than for later months but, apart from this older group and the primiparous group, age
does not influence the conception date.

16. Data on the incidence of females which are concurrently lactating and pregnant are given, and
suggest that some 18% of females conceive at a post-partum ovulation. Evidence is presented which
suggests that nearly all multiparous females experience a post-partum heat, and that a proportion of
primiparous females do not. This is inferred from the relative sizes of the corpora albicantia in
different classes of mature females, and from the presence in the ovaries of lactating females of
anomalous corpora which resemble corpora aberrantia in their histology.

Loss of a near-term foetus, a stillbirth, or loss of a young calf, is probably followed by an oestrous
cycle comparable with normal post-partum heat. The termination of pregnancy at an earlier stage is
probably followed by ovulation at the ovulatory period which would normally occur next.

17. A small proportion of females in late lactation are found to have recently ovulated, and some
14% of 'resting' females are also found to have ovulated recently and to have a corpus luteum of
ovulation in the ovaries. The incidence of diatom film is low in both lactating and recently-ovulated
females, suggesting that they are females which have only recently entered antarctic waters, and that
they have therefore ovulated either during or just after the southward migration.

The incidence of recent ovulations in antarctic waters is not constant throughout the summer
months, but falls progressively from October/November to April. Evidence is presented which
strongly suggests that almost all fin whale females experience a post-lactation ovulation, and a theoretical
curve based on this hypothesis, which indicates the entry of post-lactation females into the antarctic
summer population, is in close agreement with one showing the monthly antarctic catch. It is
concluded that 50 % of non-pregnant mature females are south of the Antarctic Convergence by mid-
December, and that December is the average time of the post-lactation ovulation. This is in agree-
ment with the time of the suppressed oestrous cycle of pregnant females, and suggests that identical
exteroceptive factors are responsible for the regulation of this cycle in these two classes of females.
Very few pregnancies are initiated at this time, mainly owing to the absence of sexually active males.

18. The cyclical activity of the mammary glands is briefly described. The criterion of lactation
which is adopted is the presence of apparently normal milk in the glands, but this is not completely
valid because it has been shown that probably about 25 % of such females in antarctic waters have
recently ceased to secrete milk and are weaning, or have just weaned, the calf. The average month of
weaning is estimated to be December, and the lactation period is about 7 months. The incidence of
diatom film, and the ages of foetuses in females simultaneously lactating and pregnant, suggest that
these females do not usually enter antarctic waters until they are just about to wean the calf.

The relative abundance of lactating females in antarctic waters in different months is examined, and
it is concluded that they are not present in representative numbers in the early part of the whaling
season. It is suggested that the southward migration of females with suckling calves is dependent on,
and limited by, seasonal changes in sea temperature, and that the critical surface temperature is about
o° C. Thus, the influx of lactating females is earlier at South Georgia than on the pelagic whaling
grounds further south ; probably over 50% of females wean their calves before entering South Georgia
waters, and over 80% do so before they enter the pelagic whaling grounds.

19. The relation of the sexual cycle to the migratory cycle is discussed. It is suggested that, as in
females at puberty, the biannual ovulatory periods are primarily related to the twice-yearly period of

SUMMARY 481

increasing day lengths associated with the north and south migrations. Animals remaining in one
latitude or undertaking small migrations are only subjected to one period of increasing and one of
decreasing day lengths annually.

This hypothesis agrees both generally and in detail with the type of female sexual cycle outlined
above, but for males it is necessary to assume that a refractory period follows the extended winter
period of sperm production, as in some male birds, and that the spring migration does not initiate a
second period of rut.

The evidence strongly suggests that the female fin whale is not polyoestrous, as earlier workers
have assumed, but seasonally monoestrous.

20. An explanation of the assumed biannual formation of ear-plug laminations is advanced. It
seems likely that the biannual hormonal cycle, regulated by changes in day lengths associated with
the long migrations, may be responsible. Thus during each migration there is a rise in the amounts
of circulating oestrogens, associated with oestrus, and it is suggested that this is responsible for the
formation of a keratinous layer in the epithelium contributing to the growth of the ear-plug.

21. The possibility of variation in fertility with age is examined. It is shown that with increasing
age there is probably a slight increase in the occurrence of multiple ovulations. Details are given of one
case in which 13 corpora lutea were formed as a result of a multiple ovulation, but this is exceptional.
In 22 out of 27 cases of multiple ovulation only two corpora lutea were formed.

The proportion of sexually active females in different age groups has also been examined, and
it is shown that age changes in fertility are slight; the youngest females show slightly lower fertility,
which is probably maximal at ages of about 1 5-25 years, and may decline at ages in excess of about
30-40 years.

Evidence is presented which suggests that up to a point fertility is directly proportional to the intensity
of whaling, and has increased to a maximum level above which it appears that no further increase is
possible in this species. The conclusions reached in this paper about the incidence of, for example, post-
partum conceptions, probably apply to fin whale populations in which fertility is maximal. With
post-partum conceptions assumed to be 18%, the average conception rate per female is 0-59 per year.

22. The annual rate of ovulation can be calculated from the type of sexual cycle which has now
been established. These calculations suggest an annual rate of ovulation of 1-43, which is very close
to the higher estimate obtained from a consideration of the regression of corpora albicantia. Allowing
for possible causes of error it is concluded that the average annual increment of corpora is 1-43 ±o-i.

No firm evidence about the rate of accumulation can be obtained from the recovery of whale marks
together with ovaries for 1 o female fin whales, owing to the small size of this sample and the uncertainty
about the age at marking.

23. For estimating individual ages of females taken in the Antarctic the number of corpora is
divided by 1-43 and to the result is added 4! years to allow for the immature period. Allowing for the
variation in the age at puberty, the accuracy of the method is such that about 90% of females should
be within ± 3 years of the estimate.

Ages determined in this way are in close agreement with the results obtained by other methods,
namely baleen plates and ear-plugs. When individual ear-plug ages are plotted against the corre-
sponding ovarian ages, it is found that 72 % of the latter lie within ± 3 years of the regression line
showing an exact correlation, and are symmetrically distributed; 82% He within ±4 years.

In drawing up survival curves or growth curves based on large samples the variation in individual
ages becomes unimportant.

24. Survival curves are given for area 11 females which, when plotted logarithmically, approximate
to the diagonal type, and this implies a more or less constant mortality with respect to age. It appears

4g2 DISCOVERY REPORTS

that total immature mortality up to 5 years amounted to about 53 % if the population which the sample
represents can be assumed to be stable.

The relation between the catches and the age structure of the population is briefly discussed, and it
is shown that for the segment of the dynamic curve between 9 and 26 years, corresponding to a period
when fishing mortality was relatively small, the annual adult mortality rate was probably about 9-2%.
The oldest animals in this sample are estimated to have been 42I years old, and it is suggested that
the specific longevity of the female fin whale is likely to be about 50 years.

25. Length-at-age data for area 11 females above 5 years of age are presented, the ages estimated
from corpora counts. The von Bertalanffy growth equation has been fitted to this data. This
gives a theoretical curve for which lt = 73-0 (i-e -Msa-o-aw)), anc\ corresponds very closely to the
observed mean values. This curve has been extrapolated back to 3 years, and is completed by including
observed values for foetal growth and the estimated length at age corresponding to weaning. It
provides additional evidence of the validity of ovarian corpora counts for age-determination.

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Maynard, C. J., 1888. Notes on the anatomical structure of three species of gannets. Contr. Sci. vol. 1 (4), pp. 151— 3.
Mizue, K. and Murata, T., 1951. Biological investigation on the whales caught by the Japanese Antarctic whaling fleets season

1949-50. Sci. Rep. Whales Res. Inst., Tokyo, no. 6, pp. 73-131.

Miyazaki, I., 1958. Fin whales and whaling operations in the East China Sea. Norsk Hvalfangsttid. 47 Arg. (1), pp. 21-6.

Morch, J. A., 191 1. On the natural history of whalebone whales. Proc. Zool. Soc. Lond. pp. 661-70.

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Mossman, H. W. and Judas, I., 1949. Accessory corpora lutea, lutein cell origin, and the ovarian cycle in the Canadian porcupine.
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Neal, E. G. and Harrison, R. J., 1958. Reproduction in the European badger (Meles meles L.). Trans. Zool. Soc. Lond.
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Nelson, W. O., 1929. Oestrus during pregnancy. Science, vol. lxx, p. 543.

Nishiwaki, M., 1950a. Determination of the age of Antarctic blue and fin whales by the colour changes in crystalline lens. Sci.
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19506. Age characteristics in baleen plates. Sci. Rep. Whales Res. Inst., Tokyo, no. 4, pp. 162-83.

1951- On the periodic mark on the baleen plates as the sign of annual growth. Sci. Rep. Whales Res. Inst., Tokyo, no. 6,

PP- I33-52-

1952. On the age determination of Mystacoceti, chiefly blue and fin whales. Sci. Rep. Whales Res. Inst., Tokyo, no. 7,

pp. 87-119.

1957. Age characteristics of ear plugs of whales. Sci. Rep. Whales Res. Inst., Tokyo, no. 12, pp. 23-32.

Nishiwaki, M. and Hayashi, K., 1950. Biological survey of fin and blue whales taken in the Antarctic season 1947-48 by the

Japanese fleet . Sci. Rep. Whales Res. Inst., Tokyo, no, 3, pp. 132-90.
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Res. Inst., Tokyo, no. 13, pp. 155-70.
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Ohno, M. and Fujino, K., 1952. Biological investigation on the whales caught by the Japanese Antarctic whaling fleets, season

1950/51. Sci. Rep. Whales Res. Inst., Tokyo, no. 7, pp. 125-88.
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1953- Biological study on humpback whales in the Antarctic whaling areas IV and v. Sci. Rep. Whales Res. Inst., Tokyo,

no. 8, pp. 81-102.

Omura, H. and Sakiura, H., 1956. Studies on the little piked whale from the coast of Japan. Sci. Rep. Whales Res. Inst.,

Tokyo, no. 11, pp. 1-37.
Ottestad, Per, 1938. Variations in the size distribution of southern blue and fin whales. Hvalrad. Skr. nr. 18, pp. 49-68.
Pearl, R. and Miner, J. R., 1935. Experimental studies on the duration of life. XIV. The comparative mortality of certain lower

organisms. Quart. Rev. Biol. vol. x, pp. 60-79.
Pearson, O. P., 1949. Reproduction of a South American rodent, the mountain viscacha. Amer. J. Anat. vol. 84 (1),

PP- H3-73-
Perry, J. S., 1953. The reproduction of the African elephant, Loxodonta africana. Phil. Trans. B, vol. ccxxxvn, pp. 93-149.
Peters, N., 1939. Vber Grosse, Wachstum und Alter des Blauwales (Balaenoptera musculus (L.)) und Finnwales (Balaenoptera

physalus (L.)). Zool. Anz. vol. cxxvn, pp. 193-204.
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486 DISCOVERY REPORTS

Pike, G. C, 1953. Preliminary report on the growth of finback whales from the coast of British Columbia. Norsk Hvalfangsttid.

42Arg. (1), pp. 11-15.
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1958- The use of the ear plug in age determination in whales. Proc. XV th Internat. Congr. Zool., sect, in, pp. 305-7.

Purves, P. E. and Mountford, M. D., 1959. Ear plug laminations in relation to the age composition of a population of fin whales

(Balaenoptera physalus). Bull. Brit. Mus. (Nat. Hist.), Zool. vol. v (6), pp. 123-62.
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pp. 65-100. Academic Press, N.Y.
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vol. xix (1), pp. 115-36.
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pp. 201-3.
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phenomena. Trans. Roy. Soc. Edinb. vol. lii, p. 303.
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pp. 97-110.
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1945. Further studies on the structure of the baleen plates and their application to age determination. Hvalrad. Skr.

nr. 29, pp. 1-69.

1958. The use of baleen plates in age determination of whales. Proc. XVth Internat. Congr. Zool., sect, in, pp. 302-33.

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Severinghaus, C. W., 1951. A study of productivity and mortality of corralled deer. J. Wildlife Mgmt. vol. xv, pp. 73-80.
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1956. Some remarks on gestation and birth in cetacea and other aquatic mammals. Hvalrad. Skr. nr. 41, pp. 1-62.

Swezy, O., 1933. Ovogenesis and its relation to the hypophysis; the effect of pregnancy, hypophysectomy and hormone administra-
tion on the ovary of the rat. Science Press, Lancaster, Philadelphia, p. 72.

Swezy, O. and Evans, H. M., 1930. Ovarian changes in the rat. Science, vol. lxxi, p. 46.

Symons, H. W. and Weston, R. D., 1958. Studies on the humpback whale (Megaptera nodosa) in the Bellingshausen Sea.

Norsk Hvalfangsttid. 47 Arg. (2), pp. 53-81.
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vol. xlix (6), pp. 460-3.
Wheeler, J. F. G., 1930. The age of fin whales at physical maturity with a note on multiple ovulations. Discovery Rep. vol. II,

PP- 4°3"34-

I934- On the stock of zvhales at South Georgia. Discovery Rep. vol. IX, pp. 351-72.

Williams, S. M., Carrigus, U. S., Norton, H. W. and Nalbandov, A. V., 1956. The occurrence of estrus in pregnant ewes.

J. Anim. Sci. vol. xv (4), pp. 978-83.
Wynne-Edwards, V. C, 1939. Intermittent breeding in the fulmar Fulmarus glacialis (L.), with some general observations on

non-breeding sea-birds. Proc. Zool. Soc. Lond. vol. cxix, p. 127.
Zemskiy, V. A., 1950a. [Some aspects of the biology of reproduction of certain species of antarctic whalebone whales.] Bull. Soc.

Nat. Moscou, N.S. Biol. Sect. vol. lv (2), pp. 1-10.
19506. [Material for the study of the embryonic development of Balaenoptera physalus L.] Bull. Soc. Nat. Moscou,

N.S. Biol. Sect. vol. lv (6), pp. 15-20.

* These papers also appear in Collected Reprints of the National Institute of Oceanography.

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PLATE IV

Fig. i. Section of a typical corpus luteum of pregnancy (bar = i cm.).

Fig. 2. Photomicrograph of a thick cleared section of a corpus luteum

to show vascular and avascular septa (bar = i mm.).
Fig. 3. Photomicrograph of corpus luteum of a pregnant female; foetus

0-47 m; fixed Zenker-formol, post-osmicated, not counterstained

(bar = 200/1).
Fig. 4. Photomicrograph of corpus luteum of a pregnant female, foetus

2-47 m; treatment as in fig. 3 (bar = 200 fi).
Fig. 5. Photomicrograph of corpus luteum of a pregnant female; foetus
' 5- iS m; treatment as in fig. 3 (bar = 500/.).

Fie. 6. Photomicrograph of ovarian cortex of immature female, body
length 54 feet, showing primary follicles; fixed Bouin, stained
Masson's Trichrome (bar = 200/t).

DISCOVERY REPORTS, VOL. XXXI

PLATE IV

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PLATE V

Fig. i. Section of a typical 'young' corpus albicans (bar = I cm.).
Fig. 2. Photomicrograph of 'young' corpus albicans, fixed Zenker-

formol, post-osmicated, not counterstained (bar = i mm.).
Fig. 3. Photomicrograph of 'medium' corpus albicans, treatment as

fig. 2 (bar = 1 mm.).
Fig. 4. Photomicrograph of 'medium' corpus albicans, fixed Bouin,

stained Masson's Trichrome (bar = 1 mm.).
Fig. 5. Photomicrograph of anomalous corpus albicans from lactating

female (Text-fig. 46 c), treatment as fig. 2 (bar = 200/1).

Fig. 6. Photomicrograph of corpus albicans shown in fig. 3 to show
arrangement of lipoids (bar = 200/1).

DISCOVERY REPORTS, VOL. XXXI

PLATE V

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PLATE VI

Fig. i. Section of typical 'old' corpus albicans (bar = i cm.).

Fig. 2. Photomicrograph of old corpus albicans; fixed Zenker-formol,
post-osmicated, not counterstained (bar = 200/1).

Fig. 3. Photomicrograph of typical radiate corpus albicans ; fixed Bouin,
stained Haematoxylin and eosin (bar = 1 mm.).

Fig. 4. Photomicrograph of old corpus albicans, treatment as fig. 2
(bar = 1 mm.).

Fig. 5. Photomicrograph of old corpus albicans; treatment as fig. 2
(bar = 1 mm.).

Fig. 6. Photomicrograph of old corpus albicans; treatment as fig. 2

(bar = 1 mm.).
Fig. 7. Photomicrograph of old corpus albicans; treatment as fig. 2

(bar = 1 mm.).

DISCOVERY REPORTS, VOL. XXXI

PLATE VI

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PLATE VII

Fig. i . Photomicrograph of old corpus albicans ; fixed Bouin, stained
Haematoxylin and eosin (bar = 0-5 mm.).

Fig. 2. Photomicrograph of old corpus albicans, fixed Bouin, stained
Van Gieson (bar = 1 mm.).

Fig. 3. Photomicrograph of corpus aberrans (Text-fig. 23 a); fixed
Zenker-formol, post osmicated, not counterstained (bar = 0-5 mm.).

Fig. 4. Photomicrograph of corpus aberrans (Text-fig. 23 c); fixed Bouin,
stained Masson's Trichrome (bar = 200//).

Fig. 5. Photomicrograph of corpus atreticum (Text-fig. 23^/); treatment
as fig. 3 (bar = 1 mm.).

Fig. 6. Photomicrograph of corpus aberrans shown in fig. 4, but treat-
ment as fig. 3 (bar = 200//).

Fig. 7. Photomicrograph of part of corpus atreticum shown in fig. 5
(bar = 200//).

DISCOVERY REPORTS, VOL. XXXI

PLATE VI!

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