The Biology of the Monotremes

368 Pages·1978·10.482 MB·English

by  Mervyn Griffiths (Auth.)

The Biology of
the Monotremes
M E R V YN G R I F F I T HS
Deakin, A. C. T.
2600, Australia
ACADEMIC PRESS New York San Francisco London 1978
A Subsidiary of Harcourt Brace Jovanovich, Publishers
Copyright © 1978, by Academic Press, Inc.
all rights reserved.
no part of this publication may be reproduced or
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ACADEMIC PRESS, INC.
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United Kingdom Edition published by
ACADEMIC PRESS, INC. (LONDON) LTD.
24/28 Oval Road, London NW1 7DX
Library of Congress Cataloging in Publication Data
Griffiths, Mervyn.
The biology of the monotremes.
Bibliography: p.
Includes index.
1. Monotremata. I. Title.
QL737.M7G74 599'.1 78-4818
ISBN 0-12-303850-2
PRINTED IN THE UNITED STATES OF AMERICA
Preface
Since their discovery in the late eighteenth century the monotremes—the
platypus and the echidna, with their melange of reptilian, mammalian, and
specialized characters—have held a fascination for zoologists, particularly those
interested in evolution. The outcome of that interest, until recently, has been a
literature concerned for the most part with anatomy and embryology. Over the
past twenty years, however, there has been an upsurge of research into the
physiology, biochemistry, ecology, ethology, and paleontology of the egg-laying
mammals. The catalyst for all this activity is the recent spate of publications from
paleontologists on the anatomy of extinct Mesozoic mammals whose cranial and
postcranial skeletons have been shown to have many characters in common with
those of the living monotremes. This has led some biologists to study the
monotremes from the possibly naive standpoint that an understanding of the
biology of Mesozoic mammals may result. Others study the monotremes for their
intrinsic interest as a taxon of mammals, probably of Mesozoic origin, which has
survived the vicissitudes of millions of years of existence during which their
relatives have gone to the wall; they seek answers to the questions of how these
survivors cope with their modern environments.
Whatever the standpoint, much has been achieved but the information is
available only in specialized journals or in theses housed in university libraries;
there has been no coordinated account of monotreme biology. This book is an
attempt to give an overall picture of what has been done and what is going on at
present; thus it is addressed to established research workers in different disciplines,
hopefully to young graduates to encourage them to undertake research on
monotremes, and to students and teachers concerned with life processes and
evolution of mammals.
As far as possible the information in each chapter has been considered under
the headings of Ornithorhynchus, Tachyglossus, and Zaglossus, the three living
genera of the monotremes. Occasionally it has been necessary to abandon that
arrangement, in part in Chapter 8 where embryos from Ornithorhynchus and
vii
viii Preface
Tachyglossus are used to give a sequential description of "monotreme" de
velopment, and completely so in Chapter 10.
My thanks go to numerous authors for permission to use their figures and
tables and I am particularly indebted to the following friends and colleagues:
Ederic Slater for the photography; Frank Knight for the artwork; Douglas Par-
sonson for the line drawings and graphs; Gutta Schoefl, John Calaby, Hugh
Tyndale-Biscoe, Tom Grant, Roslyn Bohringer, Murray Elliott, and Graeme
George for advice and information; Harry Frith for extension of museum, li
brary, and typing facilities at C.S.I.R.O. Division of Wildlife Research; Barbara
Staples and her staff for bibliographic research; Carol Todd who typed the
manuscript from my quasi-hand writing; Jim Menzies, Fathers May and Souris-
seau, and Gilles Telsfer for assistance in taking Zaglossus in the mountains of
Papua; Ray Leckie, Roy Coles, Leckie MacLean, and Terry Rutzou for skilled
technical assistance in the laboratory and in the bush; and to my daughter Mrs.
Garry Scott for assistance in checking the references.
Mervyn Griffiths
1
The Discovery and the General
Anatomy of the Monotremes
The order Monotremata of the subclass of the Mammalia known as the Pro-
totheria is made up of two families: Ornithorhynchidae (platypuses, two genera
Ornithorhynchus, and the fossil Obdurodon); and Tachyglossidae (echidnas, two
genera Tackyglossus, and Zaglossus).
ORNITHORHYNCHUS
Discovery
This beautiful little amphibious mammal, an inhabitant of freshwater streams,
lakes, and lagoons in eastern Australia, was first brought to the notice of
biologists by John Hunter, the Governor of the penal colony at Port Jackson in
New South Wales, who sent a skin and a drawing of the animal to the Literary
and Philosophical Society of Newcastle-upon-Tyne in 1798 (cited in Gilbert
Whitley, 1975). Home (1802a) relates just how Governor Hunter came by his
platypus:
The Natives sit upon the banks, with small wooden spears, and watch them everytime they
come to the surface, till they get a proper opportunity of striking them. This they do with
much dexterity; and frequently succeed in catching them in this way.
Governor Hunter saw a native watch one for above an hour before he attempted to spear it,
which he did through the neck and foreleg: when on shore, it used its claws with so much
force, that they were obliged to confine it between two pieces of board, while they were
cutting off the barbs of the spear, to disengage it.
Hunter's drawing (which is ghastly) was reproduced by David Collins (1802)
along with a description of the external characters of the animal. However, the
first description published was that by George Shaw (1799) in which he named
viii
2 l. The Discovery and the General Anatomy of the Monotremes
the animal Platypus anatinus. The name was changed to Ornithorhynchus
paradoxus by Blumenbach (1800), and an anatomical description using the name
O. paradoxus was published by Home (1802a). However, anatinus was deemed
to have priority, but not Platypus, so the animal is now known as Ornithorhyn
chus anatinus. It should be mentioned here that Home (1802a,b) was the first to
realize that platypuses and echidnas were closely related and although the
echidna had been discovered long before the platypus, the peculiar nature of the
anatomy of the monotremes was first discovered with Home's dissection of the
platypus.
External Features
The body of the platypus is streamlined (Fig. 1) and compressed dorsoven-
trally; the snout is prolonged into a muzzle shaped like the bill of a duck, and at
its hind end the platypus sports a tail like that of a beaver. The males are larger
than the females: the largest male I have taken weighed 2300 g and was 56 cm
long from tip of muzzle to tip of tail; the two largest females weighed 1300 and
1325 g and were 49.5 and 47.5 cm long, respectively. T. Grant (personal com
munication) caught a male 2350 g in weight. The males are testicond but can be
distinguished from adult females by the presence of a prominent sharp spur on
the medial side of the ankle in the former. Excretory and reproductive products
pass to the exterior through a cloacal aperture situated ventrally at the rostral end
of the tail in both sexes. There is no external pinna; the aural opening and the eye
are close together and are located dorsolaterally in a groove, the lips of which
come together and close off both eyes and ears when the animal is submerged.
Although the muzzle externally resembles the bill of a duck, internally it is
dissimilar. In Ornithorhynchus the muzzle is formed by two diverging "rostral
crura" (Wilson and Martin, 1893a), each of which consists of a long slender
Figure 1. Ornithorhynchus anatinus. Note backwardly directed frontal shield over forehead and
web of manus extending beyond the nails; hindlimbs trail and are used mainly as rudders.
Ornithorhynchus 3
extension of the premaxilla; the crura are inflected sharply anteriorly, forming
the limit of the bony rostrum. The crura, however, do not form the margin of the
muzzle since they are embedded in a vast plate of cartilage; the crura are sepa
rated widely (Fig. 5), the intercrural area being filled-in with cartilage, and their
lateral and anterior margins are also invested with cartilage forming the outer
most limits of the muzzle. In contradistinction the duck's bill is made of bone and
keratin.
The muzzle is covered by a delicate naked skin which at the caudal border is
carried back as a fold covering the anterior part of the face almost to the eyes.
The nostrils are located near the midline at the rostral end of the muzzle. Just
below the external opening of the nostril is a flap of skin which acts as a valve
when the animal dives, closing off the nostrils and thus eliminating sense of
smell under water. The mandibles are likewise covered with soft skin that is also
projected backwards over the throat, but this fold is divided into two at the
midline. These dorsal and ventral folds are known as the frontal shields. Both
snout and mandibular skin exhibits minute pores; these are the openings of sweat
gland ducts and are associated with collections of special sensory organs that are
distributed over the entire surface of the muzzle and frontal shields (see Chapter 7
for structure and function).
The platypus feeds in freshwater only and is largely a bottom feeder, swim
ming along and waggling its muzzle from side to side as it does so. The gape is
large and any food item snapped up or otherwise ingested is passed into a
capacious cheek-pouch on either side where it is stored in between dives. When
the pouches are full the food is transferred to the buccal cavity where it is
comminuted by the grinding action of keratinous horny grinding pads on the
upper and lower jaws (see also pp. 16, 56, 78). Since the eyes, ears, and olfac
tory organs are shut off from the outside world when underwater, any discrimi
nation about what is ingested must largely be due to tactile sense of the muzzle
(see p. 172).
The margins of the mandibles bear a series of keratinous serrations placed
transversely at right angles to the long axis at the posterior end of the mandible
but slanting forwards in the mandible's more rostral parts. The tongue is bipartite
consisting of a narrow elongated part housed in the hollow between the two
mandibles, and a raised oval-shaped portion housed at the posterior end of the
buccal cavity. The dorsal surface of the tongue is covered with backwardly
directed cuticular papillae and the oval portion bears two large forwardly directed
keratinous teeth at its laterorostral borders. These teeth are undoubtedly con
cerned with transferring and directing cheek-pouch contents to the grinding pads.
The body is covered by a pelage of coarse and fine hairs arranged, as in all
mammals, in bundles consisting of a principal hair and varying numbers of
neighboring hairs (Haupthaare and Nebenhaare of German authors). The princi
pal hairs are much longer than the fine ones and distally they are expanded into a
4 1. The Discovery and the General Anatomy of the Monotremes
narrow flattened leaf-shape. These principal hairs point backwards and lie flat on
the fine hairs beneath, thereby enhancing the insulative qualities of the pelt.
There has been controversy about the numbers of neighboring hairs surrounding
each principal hair and the numbers of bundles per unit area of skin in "normal"
platypuses (see Spencer and Sweet, 1899). Temple-Smith (1973) and Grant
(1976), however, have settled the matter since they found that platypus pelts
undergo moult involving even complete loss of principal hairs. This has a bearing
on thermoregulation since the pelt plays a major part in regulating heat loss (p.
126). The fur is thickest on the ventral surface of the body, next on the dorsal
surface, while that on the dorsal surface of the tail is sparse and coarse; the
ventral surface of the tail is practically naked skin. All these facts were known to
Home (1802a) who also noted the peculiar structure of the principal hairs. The
color of the fur in southeastern Australian platypuses is, in general, dark brown
on the back and a mixture of rufous brown and silvery grey on the venter. The
platypuses of northeastern Queensland are said to be of a rufous color on the
shoulders.
The skin is loosely attached to an extensive panniculus carnosus muscle that
confers a fantastic ability of the platypus to change its shape and wriggle out of
the firmest grasp.
The forelimbs are short and stoutly built; the digits of the pentadactyl manus
bear long nails and are webbed. The web occurs not only between the digits but is
carried forward well beyond the nails to form large fan-shaped paddles; these are
the main organs of propulsion in water. The hindlimbs are also webbed but they
simply trail and act as rudders when the platypus is swimming. The webs and
extensions of the forelimbs account for 13.5% of the total surface area of the
animal and play important roles in thermoregulation (p. 104). When out of the
water the platypus lives in a burrow dug into the bank of a river, pool, or creek.
When burrowing the web extensions are folded back and under so that the nails
form the most rostral part of the manus. This also takes place when the platypus
walks and runs.
Reproductive and Excretory Organs
The female reproductive organs consist of paired ovaries enclosed by paired
thin infundibular funnels, paired oviducts, paired uteri each of which communi
cates separately with a long median unpaired urogenital sinus. At the level of the
union of the uteri with the urogenital sinus the ureters from the kidneys enter the
sinus opposite the neck of the bladder which depends from its ventral surface.
The elongated urogenital sinus communicates with the cloaca; thus eggs, urine,
and feces pass out through the one cloacal sphincter, hence the word
Monotremata to describe the Order.
Ornithorhynchus 5
Only the left ovary and oviduct are functional; the right ovary exhibits oocytes
that never mature; however, the right oviduct while never as well-developed as
the left, exhibits uterine glands during the breeding season (p. 219). In the left
ovary mature oocytes achieve a diameter ofca. 4.3 mm and, along with their
follicular investments, are visible to the naked eye; an ovary with maturing
oocytes sticking out all over it gives one the impression of a bunch of grapes.
Home (1802a) discovered and described the essentials of the female reproduc
tive system and realized that it bore no resemblance to the reproductive systems
in mammals, nor could he find any resemblance of the platypus uterus to the
oviduct of birds. However, he did find a close resemblance of that organ to the
oviducts of 'Ovi-viviparous" lizards; he concluded that the platypus '4also is
oviviviparous in its mode of generation." In 1884 Caldwell (1884b) finally
showed that the platypus is oviparous (p. 209).
The ovaries of Ornithorhynchus are attached to the anteroventral faces of the
kidneys by a fold of peritoneum. The kidneys are nonlobulated structures, i.e.,
they are "kidney" shaped and have the typically mammalian blood supply and
drainage, consisting of renal artery and renal vein; there is no renal portal system
as in birds and reptiles (Hochstetter, 1896).
As mentioned above the males are testicond, the paired testes being suspended
posterior and ventral to the kidneys by mesorchial folds of the peritoneum.
Seminiferous tubules pass from the anterior end of the testis and join to form a
short rete that communicates with the ductuli efferentes (Temple-Smith, 1973).
Spermatozoa pass from the testes through the ductuli efferentes into the
epididymis, which consists of three regions: caput, corpus, and cauda. From the
cauda a short vas deferens conveys the sperm to the unpaired urogenital sinus
which is elongated as in the female. The penis depends ventrally from the
posterior end of the urogenital sinus and is housed in a thin-walled preputial sac
lying ventral to the cloacal chamber. The ventral surface of the latter is perforate
so that the erectile penis can pass through the cloaca and out to the exterior
through the cloacal aperture. These relationships are illustrated in Fig. 10, actu
ally a photograph of the reproductive system of a male echidna; that of the
platypus is practically the same. As Home (1802a) recognized, the urethra of the
penis communicates with the lumen of the urogenital sinus and that it conveys
sperm only, the urine being passed separately from the urogenital sinus into the
cloaca. Just why sperm do not do the same thing is not clear; possibly when the
penis is erect it also projects backwards into the sinus and blocks off the passage
to the cloaca thus forcing the sperm to enter the seminal urethra. The penis is
bifid distally, right and left portions terminating in a bulbous glans, each glans
bearing a group of evertible foliate papillae. Branches of the seminal urethra pass
to the exterior through these papillae (Temple-Smith, 1973). The penis is about
5-7 cm in length.
6 J. The Discovery and the General Anatomy of the Monotremes
Two types of accessory glands are present: paired Cowper's glands which
communicate by short ducts with the penile urethra, and a set of disseminate
tubular glands which encloses the urogenital sinus (p. 232).
Mammary Glands
Home (1802a) found "There is no appearance, that could be detected of
nipples; although the skin on the belly of the female was examined with the ut
most accuracy for that purpose." Twenty-four years later Meckelio (1826) found
two sets of ventrally located glands in female platypuses, one on each side of the
midline about halfway down the body; each set consisted of club-shaped lobules
that converged proximally and passed through the corium and skin to the ex
terior. The sets varied greatly in size from platypus to platypus. Meckel diag
nosed these as mammary glands but not everyone was convinced he was right:
Geoffroy (cited in Meckel, 1827) thought that the great variation in size ruled out
the possibility of them being mammary glands but Meckel stuck to his guns:
"Die Grosseverschiedenheit der Druse bei gleichem Alter und Grosse der In-
dividuen ist offenbar der beste Beweis fur die Ansicht, dass diese Druse zum
Zeugungssysteme gehore, und, in Verbindung mit den ubrigen Thatsachen, dass
die Brustdriise sey." A few years later his interpretation was confirmed by
Lieutenant the Hon. Lauderdale Maule of the 39th Regiment who communicated
his observations to the Zoological Society of London (Maule, 1832):
During the spring of 1831 being detached in the interior of New South Wales, I was at some
pains to discover the truths of the generally accepted belief, namely, that the female Platypus
lays eggs and suckles its young. By the care of a soldier of the 39th Regiment who was
stationed at a post on the Fish River, a mountain stream abounding with Platypi, several nests
of this shy and extraordinary animal were discovered.
A female and two young were taken from one of these nests; after keeping her
and the young for a couple of weeks she was accidentally killed. Upon skinning
her while she was still warm it was seen that milk oozed through the fur on her
ventral surface. This came from "two teats or canals," both of which contained
milk.
Considering the size of the animal the fully lactating glands are enormous. In
one platypus examined by Griffiths et al. (1973) measuring 43 cm from muzzle
to tail, the glands measured 13.5 cm in length stretching from axilla to groin, and
around the flank almost to the dorsal surface. Each of the lactating glands is
fan-shaped (Fig. 2) since the lobules are expanded distally but converge prox
imally to pass in the form of ducts through the abdominal musculature and skin to
appear at two patches obscured, as Maule noted, by the pelage of the ventral
surface. These patches or areolae have a well-defined morphology: the ducts
below the skin are distended into lacuna-like spaces reminiscent of storage cis
terns (Fig. 3). Peripheral to the distended ducts is a ring of convoluted glands, the