[КГ
’ 1170-53092
EVOLUTION OF THE
_ ALIMENTARY SYSTEM IN
_ MYOMORPH RODENTS
_— М.М. VORONTSOV
_ TRANSLATED FROM RUSSIAN
f Published for the Smithsonian Institution and the National Science
Foundation, Washington, D.C. by the Indian National Scientific
| Documentation Centre, New Delhi.
1979
EVOLUTION OF THE
ALIMENTARY SYSTEM IN
MYOMORPH RODENTS
TT70-53092
EVOLUTION OF THE
Г ВЕ ТАБУ SYSTEM ПМ
МУОМОКРН RODENTS
(Evolyutsiya Pishchevari tel'noi Sistemy Gryzunov Mysheobraznye).
М. М. VORONTSOV
Izdatel'stvo "Nauka", Sibirskoe Otdelenie, Novsibirsk, 1967
TRANSLATED FROM RUSSIAN
Published for the Smithsonian Institution and the National Science
Foundation, Washington, D.C. by the Indian National Scientific
Documentation Centre, New Delhi.
1e7 9.
Contract NSF-C466
Available from the
U.S. Department of Commerce
National Technical Information Service
Springfield, Va. 22161
Translated and Published for the Smithsonian Institution in Accordance with
the Agreement with the National Science Foundation, Washington, D.C. by
the Indian National Scientific Documentation.Centre, Hillside Road, New
Delhi - 110012, India.
©) 1979 Indian National Scientific
Documentation Centre, New Delhi.
Translated, Printed and Published by INSDOC, New Delhi 110 012
DEDICATION
In memory of dear
Yuri Alexandrovich Orlov
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PREFACE
CONTENTS
INTRODUCTION
SPECIAL PART
CHAPTER |. Mechanism of Masticatory Movements and the
1.
De,
Evolution of Maxillary Apparatus
Structure and function of masticatory muscles
Mechanism and types of masticatory movements
in rodents
Functions of masticatory organs of rodents
Relationship of the exosomatic systems of the head
and skull and with each other. The main line of
_ transformation of the skull and maxillary apparatus
of Cricetidae
Paleontological and embryological proofs of the main
direction of evolution of the cranium of Cricetidae.
CHAPTER If. Evolution of the Dental System.
General notions, terminology
Types of masticatory movements and the structure
of molars
Change in the structure of the masticatory surface
of molars with the age, within the groups and between
the groups
11
_16
29
35
35
39
44
CHAPTER
Structure of the molar teeth of Cricetidae in connection
with their position in the system of Muroidea.
Transformation of molar teeth in the phylogenesis of
Cricetidae
. Structure of molar teeth of recent Cricetidde
Structure of the molar teeth of some rodents which
belonged sometime to Cricetinde (Мезотутае,
Tachyoryctinae, Myospalacinae, Lophiomyidde,
Platacanthomy inae) |
. Trends of dental specialisation of some primary
myomorph rodents. Homologous Gnd parallel variability
series in the dental system of rodents.
НГ. Evolution of other Org@ns of the Mouth Cavity
(Tongue Gnd Cheek Pouches)
1. Топаче
a) General outline of the tongue morphology in
mammals
b) Tonque structure in Cricetinde
-¢) Tonaue structure of some forms of Muroidea with
Ya
reference to the interrelations of Cricetinde with
allied subfamilies
Cheek pouches
CHAPTER IV. Evolution of Stomach
iis
op
Ceneral notions, terminology
On the physiology of digestion in the stomach.
Functional peculiarities of glandular and combined
stomachs, of nonchambered and multichambered
stomachs in rodents
Individual Gnd age variation in the structure of the
stomach
50
52
120
139
147
147
147
150
152
155
162
162
167
175
4. Stomach structure of Cricetinge
5. Data of the Ontogenesis of the stom@ch in Onychomys :
Modes of food specialization and secondary development
of protein nutrition in insectivorous hamsters.
6. Structure of the stom@ch in certain rodents belonging
to Cricetinae (Nesomyinge, Муозра!астав and
ophiomyidde)
7. Structure and trends of stomach specialisation in some
mainly, Myomorph rodents (Gerbillinae, Microtinga,
Muridae, Spalacidae, Glinoidea, Dipodoidea and Bathy-
ergoidea). Homologous and Parallel! Series of variability
in the rodent stom@ch structure
CHAPTER V. Evolution of Intestine
1. General concepts and terminology
2. Physiology of digestion т the intestine of rodents
3. Structure of the intestine in Cricetinae
4, Structure of the intestine of certain rodents relating
to Cricetinde (Nesomycinae, Myospalacinge,
Lophiomyidae)
5. Structure Gnd trends of the specialisation of the
intestine of some rodents mainly Myomorph rodents
(Gerbillinae, Microtinde, Muridae, Spalacidde,
‚ Bathyergoidea ап4 Geomyoidea)
CHAPTER VI. Evolution of Liver
CHAPTER VII. Ways of Food Specialisation and Evolution of the
Digestive System in Muroidea
CHAPTER VIII. Unequal Rates of Transformation of Oreans and the
Principle of Compensttion of Functions
1. Formetion of modern views upon the coordination of
the transformation of organs in phylogenesis, upon the
problems of specialisation and extinction
200
213
225
225
228
230
248
255
275
280
287
288
2. Uneaual rates of transformation of biologically
coordinated ordins in the process of specialization
3. The principle of compensation of functions. The
importance of unequal rates of transformation of organs
for despecialization
4, The Importance of unequal rates of organ-transformation
ап compensation of functions in ontogenesis
CHAPTER IX. Homologous Varia vility
1. Cytogenetic Ind molecular bases of homologous and
back mutations
2. Homology of characters and genotypes.Reversibility
of characters Gnd irreversibility of evolution.
3. Monophyly and possibility of parallel occurrence of
superspecific groups
4. Different levels of homology in different organs of a
united system
LITERATURE
299
307
311
315
317
319
323
326
327
PREFACE
This work is intended for specialists in the field of
Mammalian taxonomy, ecology, comparative anatomy and pa-
leontology. The extensive material drawn for study, also
yielded the possibility of arriving at certain general laws of
evolution. Special attention is paid to two problems: first to
homology, parallelism and convergence in the structure of the
rodent alimentary system, evaluation of the applicability of N.I.
Vavilov's taw of homologous series of inherited variability to
supergeneric taxa and secondly, to the problem of biological
coordinations, unequal rates of organic transformation in one
functionally-bound system and substantiation of the principle of
"compensation of functions" This second aspect of the general
biological part of this book is idealogically connected with the
studies of I.1.. Schmalhauzen. It seems that certain general
biological preblems discussed in this book may be of specific
interest not only to theriologists, but also to biologists with
other specialized interests in the problems of evolution.
In the course of his work on morphology and phylogeny of
rodents, the author has summed up the concepts on the cendi-
tions required for any ecological morphological, comparative
anatomical and phylogenetic studies.
$. Phylogenetically allied groups of forms as a whole
should be taken for the purpose of study. -In this work the sub-
family Cricetinae, the largest subfamily of mammals is studied.
taking the world fauna as a whole.
2. For explaining the degree of affinity, and the reasons
for the development of one or other characters, and for the dis-
parity in the instances of parallelism in development and con-
vergence, it is advisable to study the trend of evolution 1 the
strains allied to the group being studied. In this work repre-
i
sentatives oi the groups of Madagascar rodents (Nesomyinae),
gerbils, (Gerbillinae), voles (Microtinae), sokhors (Myospala-
cinae) and lophiomys (Lophiomyidae) are studied in full detail.
The structures of the alimentary system in some members of
mice (Muridae), dormice (Myoxidae), jerboas (Dipodidae), mole
rats (Spalacidae), bamboo rats (Rhizomyidae) and representa-
tives of other rodent orders ‘viz, gophers (Geomyidae) and
African sand rats and mole rats (Bathyergidae) are studied as
examples of parallel and convergent groups.
3. Itis highly desirable to make wee of the method of
"ternary parallelism" for revealing the history of development
of one or other characters: This method, recommended from
the time of E.Heckel in all text books, is very rarely used
owing to methodological difficulties and limited data.
The basic method employed in this work was comparative
anatomy. Wherever possible, the paleontological method is also
used and in controversial cases (proof for the secondary de-
velopment of an insectivorous type in Onychomys, etc) even the
embryological method of study is used for building a phylogenetic
group system. The phylogenetic system cannot be formed on the
basis of the study of the structure or the transformations of
individual characters in ecolegical morphological, comparative
anatomical or the phylogenetic series.
As this work is confined only to a review of the evolution
of digestive organs, the data on the position of any group in the
system of rodents contained in this book should be considered
only as data for building the system of rodents.
The conditions necessary for the phylogenetic study men-
tioned above may be fulfilled to some extent, because the author
had at his disposal more extensive material than the previous
research workers.
Rodents from the collections of the Zoological Institute,
Acad Sc., USSR at Leningrad and the Zoological Museum of the
Moscow State University have provided specimens for morpho-
logical studies. The fossil materials are described from the
collection of the Paleontology Institute, Acad. Sc. USSR, at
Moscow and Geological Paleontological Museum in the names of
А.Р. Pavlov and M. V. Pavlov of the Moscow Institute of Geologi-
cal Exploration.
South African specimens were furnished by Dr. D. Davis
(Plague Research Laboratory, Johannesburg), Madagascar speci-
mens by Prof. В. Mathey (Laboratorie de Zoologie et d'
Anatomie comparie, Universite de Lausanne) South American
specimens by Prof. Fr. Petter (Fr. Fetter, Museum National
d'Histoire Naturelle, Laboratoire des mammiferes et oiseaux,
Paris), U.S. and Mexican specimens by E. Hooper,(E T. Hooper.
Museum of Natural History, University of Michigan, Ann Arbor),
Brazilian specimens by Dr. Carvalho (C.T. Carvalho, Depart-
ments de Zoologia, Sao Paulo), P. South and Central American
specimens by Prof. P. Hershkovitz (Ph. Hershkovitz, Chicago
Natural History Museum) and South European specimens by Prof.
К. Zimmerman (Kl. Zimmermann, Institut fur spezielle Zoolo-
gie - und Zoologisches Museum der Humboldt-Unive rsitat Zu
Berlin). The list of species studied has lengthened considerably
thanks to the assistance of these foreign zoologists. The author
takes this opportunity to convey his deep gratitude to them.
Starting in this manner the author has tried to study the
maximum number of species of closely allied groups, to get an
idea of adaptive evolution of the entire group and not only the
comparative morphology of a random group of species, limited
by the size of such an extensive administrative territory as our
country. The structure of the digestive system of more than 300
species of rodents belonging to 19 subfamilies was studied. In the
study of most of the organs of the digestive system, the descrip-
tions are not uniformly detailed, owing to the large number of
objects of study. In Фе absence of data on the histology of the
alimentary tract it is easy to criticize the-author оп the ground that
the problems of homology of the dental system are dealt with
largely on the basis of topographic and not embryological analyses.
However, from the evolutionary point of view, the study of a wide
collection of species has specific advantages over comparative,
anatomical, histological and embryological analyses of some
species, For that reason, the author is indebted to B.S. Vino-
gradov, V.G. Heptner and N.V. Shibanov, who have awakened
his interest in the world fauna. So the study of groups is con-
sidered as an essential prerequisite for phylogenetic and syste -
matic studies.
Some sections were discussed with М.К. Vereshchagin, B.S.
Vinogradov, L.V. Ganeshina, V.G. Heptner, Г.М. Gromov, А.М.
Druzhinin, N.I. Kalabukov, V.V. Kucheruk, Yu.A. Labas, B.S.
Matveev, Р.Р. Strelkov, V.B. Sukhanov, К.К. Flerov, У.1.
iii
Tsalkin, Г.Г. Schmalhauzen, К.А. Учат and A.V. Yablokov.
Their advice and remarks, made at various stages of completion
of this work, were very valuable.
Work on this monograph was begun in the Mammalian
Laboratory of the Zoological Institute, Acad. Sci. USSR nearly
completed in 1961, completed and revised at Novosibirsk in the
Department of Evolution and Karyosystematics of the Institute of
Cytology and Genetics affiliated with the Siberian Branch of the
Acad. of Sciences, USSR.
iv
INTRODUCTION
The type and сс -osition of nutrition as well as the
methods for assimilating food reserves define the role of a
species within a community. Ecologists have already recognized
the relationship between the type of nutrition and the basic eco-
logical features of rodents: viz., the size of the individual
portions, mobility, nocturnal activity, reproduction and numerical
dynamics of population. They have also discovered the basic
laws linking the ty pe of nutrition of the species to its important
ecological features (Elton, 1942 Уогопоу, 194/ and Naumov,
1948). Nutrition and evolution of food specialization is one of the
most important problems of ecology. The considerable progress
that ecologists have made in the study of nutritional specializa-
tion, has been hampered by the nonavailability of elementary
information on the morphology of the digestive system.
The relationship between the type of nutrition and the
structure of rodents has been studied, generally based on
heterogeneous data at times related neither genetically nor eco-
logically (Luppa, 1956, 1958 b; Velichko, 1939a, 1939b; Velichko
and Mokeeva, 1949, Kulaeva, 1956; Nazarova, 1958, etc.).
Often, only the individual portions of the digestive system were
studied. These limited studies have beenof little value in deter -
mining the evolution of the entire systemof relevant organs. As
a break from ecology, as well as from the morphology of other
organs of the digestive system, a monograph devoted to the
comparative morphological description of the dental system of
rodents was made by Stehlin and Schaub (1950).
Against this background Tullberg's (1899) classical mono -
graph devoted to the problems of the system and phy logenesis of
rodents, remains, the best and unsurpassed study to date on the
structure of the digestive system of rodents. This monograph
unique inall respects, is the only work, wherein all the orgazs
of the digestive system are studied together. However, Tullberg
was primarily interested in the problems of phylogenesis and the
У
system of large taxa from family and above, in other words, in
the problems of megaevolution. Hence the problems of adaptive
evolution and adaptive radiation within the families, subfamilies
and genera were not studied by Tullberg. It is doubtful that these
problems could even have been raised at a time when very little
was known of the ecology of rodents, physiology of digestion and
even evolutionary morphology was not yet brought to a new level
by the studies of А. М. Severtsov and Р.Р. Sushkin. The question
of biological coordination was raised only in the thirties by Г.Г.
Schmalhausen. М.Г. Vavilov's Law of homologous series of
inherited variability (mostly on plants) was adopted at the same
time.
It was necessary to depend оп ecological and physiological
studies, for solving the problems of adaptive evolution of the
digestive system, the problems in establishing the homology and
parallelism in development, and the presence.or absence of
biological coordination. A series of ecological works by М.Р.
Naumov (1948), deserves the first mention,. helping to establish
a close relation between all aspects of the biology of rodents
(including even such phenomenon as the variation in number
which is important for man) and the exact type of nutrition.
A number of ecological studies onthe nutrition of rodents,
summarized by А.С. Уогопоу (1947) and М.Р. Naumov (1948)
saves the author from the unavoidable discussion of це tradi-
tional "ecological description" to the comparative anatomical
part of this work. The required references on works devoted to
the nutrition of one or more forms are givenin the text inthe
appropriate portions of the book.
A special chapter in the recent report of A.D. Slonim
(1962) is devoted to the physiology of digestion in mammals.
Hence the physiological survey antecedent to the corresponding
chapters of this work is also reduced to the minimum.
Thus, a study of the problems of adaptive evolution of the
digestive system logically results, fromthe works of the com-
parative anatomical school of thinking of A.N. Severtsov, P.P.
Sushkin, and I. I. Schmalhausen, and the evolutionary school of
thinking of М.Г. Vavilov mainly of the thirties and also from the
works of ecologists and ecological physiologists of the forties
and fifties. Finally, the recent achievements in the fields of
genetics and molecular biology made inthe early sixties, enable
us to use a new approach to the interpretation of the problems of
homological variability, polyphyly and reversibility of evolution.
vi
SPECIAL PART
! CHAPTER I
MECHANISM OF MASTICATORY MOVEMENTS AND EVOLUTION
OF MAXILLARY APPARATUS
The structure of the skull, masticatory muscles, and teeth
is determined by the general structural plan, depending upon the
gene stock of the given group and by the adaptability to the ргосезв-
ing of one or more food materials. The mechanism of masticatory
movements and some rules of transformation of the maxillary
apparatus and skull in rodents have been analyzed in earlier
investigations (Vorontsov, 1961Ъ, 19634; Vorontsov and Labas,
in litt).
I, Structure and Function of the Masticatory Muscles
The principal structural features of the masticatory muscles
are common for the entire superfamily, Muroidea. A unified
structural plan of the masticatory apparatus characterizes all
members of this most extensive group of mammals. But, within
the general structural plan, the adaptive characteristics of the
different types of nutrition are so different that they may radically
change the functional importance of some muscles.
The muscles of maxillary apparatus in Muroidea rodents
perform the following functions:
1. М. digastricus abducts the lower jaw and opens the mouth
2. М. transversus mandibulae to some extent pushes the
halves of the jaws and sets the lower incisor. Perhaps,
it acts simultaneously with m. pterygoideus externus and
пл. pterygoideus internus.
3, M. masseter lateralis (see Figs. 5 and 7), on the whole
adducts and partly moves the lower jaw forward. The
]
№ №. VORONTSOV
functions of individual segments of this muscle change
significantly depending on the adaptations to various types
of nutrition.
a) The pars anterior mainly moves the lower jaw forward.
In the carnivorous and seed-eating forms and in those burrowing
by incisor, it participates also in adducting the lower jaw. In the
seed-eating forms, including all voles (Microtinae), it practically
loses the function of adducting the jaw, and simply takes part in
longitudinal frontal displacement of the lower jaw. On transition
from a lipo-protein to a cellulose type of nutrition, this portion
strengthens (and the point of attachment changes). The basic
function is longitudinal grinding.
b) The para posterior adducts and partly moves the mandi-
ble. forward. With various types of nutrition it does not undergo
significant transformation in the ecological morphological series
of Muroidea. The main function is crushing of seeds and gnawing,
i.e., adduction of the lower jaw.
c) In the wild, seed-eating forms, and forms burrowing with
incigors, the pars profundus along with р. anterior of га. masseter
medialis mainly participates in adducting the lower jaw and barely
moves it forward. In the forms having cellulose type of nutrition,
it not only adducts the lower jaw, but also moves it forward. The
function is gripping and grawing.
4. М. masseter medialis dé¢presses and partly moves the
lower jaw forward.
a) The pars anterior adducts and barely moves the lower
jaw forward. The main function is gnawing and crushing seeds. On
transition from a protein-lipoid to a cellulose type of nutrition,
its function does not change, but the size is greatly reduced (see
Fig. 5).
b) The pars posterior adducts and pushes the lower jaw
partly back. In function it resembles m. temporalis.
5. М temporalis adducts and pushes the lower jaw, partly
back, bringing the articular head into the rear part of
the articular surface.
2
MASTIC ATORY MOVEMENTS IN RODENTS
6. M. pterygoideus consists of (see Fig. 4) two independent
muscles with different functions Both the pterygoideus
muscles push to a certain extent the rami of the lower
jaw.
a) М. pterygoideus еж{егпав` main function is the contrac -
++ 5u of the halves of the lower jaw, 1.е., transverse grinding
cvements; pushing the lower series of molar teeth inside in rela-
‘“-= ty the upper one; along with га. transversus mandibulae it
st. she lover incisors. In voles and zokhors (Myospalacinae), it
тстаоуев the articular head from the articular pit participating in
the preparation of gnawing movements, and partly moves the jaw
forward.
b) M. pterygoideus internus pulls the corner part of the
jaw inside and slightly forward and up; during this the upper por-
tion of the mandible with the lower row of molar teeth is pushed
externally with respect to the upper row of the molar, thereby
participating in the transverse grinding movements. In the voles
and zokhors this muscle takes part in moving the lower Jaw forward
i.e. ina longitudinal grinding movement.
2. Mechanism and Types of Masticatory Movements in Rodents
The type of masticatory movements and the structure of
-grinding surfaces are vitally important for the structure of the
cranium and teeth since these mainly determine the structure and
shape of cranium.
During the processing of food the mandible performs
complicated movements. The mandibular joint of rodents, possess-
ing three degrees of freedom causes simultaneous movement in
three interperpendicular directions. Composed of two inter-
perpendicular harmonic oscillatory movements of various
frequencies gives the trajectory of the movement in the shape of
an ellipse, an eight, a double eight and more complicated figures.
Very complicated trajectories corresponding to the movements of
the lower jaw are formed by the three interperpendicularly directed
harmonic oscillating movements. Any type of full movement can
be conditionally broken into its components. It is quite permissible
and very convenient to consider these components separately. The
3
№. №. VORONTSOV
general scheme of the types of lower jaw movements during the-
processing of food could not be found in the literature, though
references on the prevalence of one or the other type of masticatory
movements are made very often (Tullberg, 1899, Hinton, 1926;
Vinogradov, 1926; Ognev, 1940, 1947, 1948, 1950; Romer, 1938;
Lebedkina, 1949).
Morphological analysis helps distinguish the following types
of masticatory movements of the lower jaw :
1. Gnawing-adduction of lower jaw connected with the work-
ing of incisors on cracking nuts, seeds, holding and biting of food,
primary processing of twigged feed, and digging by incisors.
Mainly m. pterygoideus externus, p. posterior and p. profundus
гл. masseter lateralis, amd also (in seed-eating forms) р. anterior
m. masseter lateralis (in voles this muscle mainly works during
longitudinal grinding) take part in these movements. The oscilla-
tory movements of the lower jaw in the vertical plane around the
relatively fixed axis of the articulation of lower jaw with skull
predominate in this type.
Vinogradov (1926) has described in detail some special
adaptations of the maxillary apparatus of Rodentia relating to the
gnawing movements of the jaw, abducted forward. Meanwhile,
the gnawing movements of Rodentia take place in the front as well
as in the rear position; few having a fixed axis of maxillary lever,
The fixation of the axis of the maxillary lever is important
for the gnawing type of movements. This fixation is accomplished
in Carnivora (gripping type, resembling the gnawing type at the
rear portion of the jaw) by the hinge articulation of the jaw with
the skull and in the majority of rodents, by the stress of the arti-
culated head in fossa condyloidea. The processuss articularis,
directed backward, takes a more horizontal position. Its articulat-
ed head assumes a vertical position and the articulated pit is
displaced. This process of displacement of the articulated head
is most prominent when comparing the structure of the lower jaws
of piscivorous hamster (Ichthyomys), for which the process helping
in prey catching is of much importance to the ordinary hamster
(Cricetus) and herbivorous hamster (Neotoma) (Fig. 1).
MASTIC ATOR Y MOVEMENTS IN RODENTS
Fig.1: Position of the articular process and articular head, Left rami
of the lower jaws, lateral view (Orig). (a) Ichthyomys soderstro-
mi de Winton (gnawing -gripping type), (b) Cricetus cricetus Г.
(Inter mediate type with nearly equal development of gnawing -crush-
ing and grinding movements); (c) Neotoma cinerea Ord, (grinding
iype).
Special adaptations for the axial attachment of the maxillary
lever on gnawing are described earlier (Vorontsov 1963). ‘The
article states that the functions of gnawing and grinding are inde-
pendent of each other in the various groups of rodents.
2. The crushing of seeds basically resembles gnawing by
groups of operating muscles, since all the muscles adducting the
jaw are in action during this. Besides, there are slightly
circular, 8-shaped movements in the horizontal plane owing to
the contraction of m. pterygoideus internus in transversus mandi-
bulae, р. anterior, па. masseter lateralis and m. temporalis.
Crushing movements of the jaw are observed while buno-
dont rodents feed on seeds. Crushing movements combine with
gnawing since during crushing (as during gnawing) the angle of
deviation of the lower jaw from the position obtained when the
5
N.N, VORONTSOV
molars are touching, is of importance; the magnitude of this
angle is defined as the moment of force M, atithe end of the
lower incisor on gnawing and the moment of forces M2, Mz and
Мп on every tubercle of the lower molar teeth. During crushing
movements also, the avis -1,е., the articulation of the jaw with
skull remains slightly rm:obile. The process of grain crushing
combines with the adduction of the jaw and its insignificant dis-
piacement in the horizontal plane.
3. Grinding in transverse direction is effected by the
alternate contraction of the pterygoid muscles and па. trans-
versus mandibulee.
Grinding movements in transverse direction develop in
the seed-eating and very rarely, in the herbivorous forms.
According to Ognev (1940), the food of Duplicidentata, unlike
other rodents, is ground only in the transverse direction, and
in herbivorous forms including the crushing type grinding
movements are mainly in transverse direction. Tullberg (1899)
noticed circular movements of lower jaw in all members of
Sciuromorpha.
Advantages of transverse movements of jaw for seed eating
forms may be clearly explained thus: as it was shown (Vorontsov,
1963) that the gnawing -crushing movements of bunodonts are
related to the fixation of the lever, where the axis is the articu-
lation of jaw with skull; the axis remains undisturbed during
transverse movements of the lower jaw, and grinding movements
are accomplished in transverse direction simultaneously with
gnawing and crushing movements. in herbivorous forms, grind-
ing movements in tranaverse direction usually play an insigni-
ficant role while backward and forward grinding movements play
an important role.
Exceptional types of rodents are those which burrow with
incisors for which the axial fixation of maxillary leve™ 18 of
special significance. They grind in transverse direction though
they mainly feed on cellulose. Therefore the width of molar
teeth increases so much that it may be equa! to the length of
each tooth (Spalax, Rhizomys, Techyoryctes, Brachysromys
ramirohitra), The enamel crests of molar change from tfane~-
verse (Spalax) to an inclined position (Rhizomys) and, finally,
6
MASTICATORY MOVEMENTS IN RODENTS
to a position aimost along the axis of the dental rows ¢oechyor
yetes, Brachyutomys ramirohitra). As the transverse move -
ments of lower jaw are dominant the form of articulated head
becomes spherical. This can be clearly traced among the
Madagascan Cricetid Nesomyinae from Macrotarsomys to Вга-
Se ee =>
те cree оон пития питты eee
Since the function of the third (геаг) molars does not di-
minish while grinding in transverse direction, as observed in
the icxms having predominantly longitudinal movements of jaw,
МЗ and М. are never reduced in such rodents, but are equa! in
size if not bigger than the two primary molars. This can very
clearly be illustrated by comparing the teeth of two allied genera
of Madagascan cricetid Nesomyinae. One of them (Srachytar-
somys) is adapted to processing the cellulose food by longitudinal
movements of the jaw (the first molars are elongated and the last
ones are short, the teeth themselves are narrow and the enarel
crests are transversely arranged) and the cther (Brachyuromys
ramirohitra) - rhainly by transverse movements; thus the length
of each tooth Чоез not exceed its width, the width increases acd
the enamel crests are turned along the cranial axis. (See Figs.
75 and 76).
The grinding movements in transverse direction are pre-
dominant and the width of the molars are more or less equal to
their length not only in Myomorpha, but also in beaver, porcupine,
coypu, in which the gnawing movements are much extended on
processing the twig feed or digging of holes. In Hystricidae the
enamel crests are arranged transversely as well as obliquely and
almost longitudinally.
4. Grinding in the longitudinal direction is mainly accomp-
lished by p. anterior, m. masseter lateralis (forward motion of
the jaw) and m. temporalis (backward motion of the jaw). Grinding
movements in the longitudinal direction is predominant in herbi-
vorous forms. As shown by Tullberg, 1899, the processing of
food in Murinae, takes place by longitudinal and lateral movements
of the lower jaw and in Microtinae (Tullberg 1899; Hinton, 1926;
Орпеу, 1950) the mandible moves only longitudinally.
‘As shown by H.S. Lebedkina (1949), only the longitudinal
forward movement can be considered as the орегаН опа! movement
7
№. №. VORONTSOV
of masticatory muscles during the working of molars in voles.
Nevertheless, the grinding movements in longitudinal direction is
always associated with similar movements in transverse direc-
tion. The less prevalence of the transverse-grinding movements
in herbivorous animals can be explained as follows. In voles,
food is processed directly by tue enamel crests, dentinal areas
бо not actually take part in processing food. The grinding of
‘ood by molar teeth of voles in fact reduces to cutting and breaking
of the plant parts by the enamel crests (Lebedkina, 1949). In
this respect it is similar to the primary processing of food by
incisors and cam be compared with the working of a grater. That
18 why in forms whose food contains vegetative parts of plants
(Andinomys, Nectoma, Microtus, Lemmus) the length of enamel
crests increases because of the wide angle of the enamel prisms,
the increase (transverse) of width and the decrease (longitudinal)
of the length of the prisms.
The displacement should not be too large or too small
during the forward movement of jaw. The greater the displace-
ment, the greater the number of intersecting enamel crests
involved in grinding of food (Lebedkina, 1949). But when the
displacement of the lower jaw ie considerable ,the number of
intersecting enamel crests again decreases anda significant part
of the displacement of lower jaw may become idle. Since there
is a very small displacement, the frequency of longitudinal
movements of the lower jaw should increase for compensating the
slight grinding action resulting from the fewer number of inter-
secting enamel crests involved. Thus, it is clear that the trans -
formation of the dental system in series from seed-eating
hamsters to herbivorous hamsters and to voles, should bring
about a general increase in the relative length of the dental row,
and an increase in the number of the enamel crests and decrease
in the longitudinal wiath of the enamel prisms. An increase in
the angle of prisms, a general increase in the length of enamel
crests and also transformation of teeth from tubercular to flat-
crowned types and replacement of brachydont by hypsedont teeth
would also result,
With the small width of the teeth, the transverse displace-
ment already small in absolute value, may cause idie motiun and
an increase in the frequency of oscillatory movements о! jaw
becomes limited,
MASTICATORY MOVEMENTS IN RODENTS
During the longitudinal movements of jaw, the significant
(in absolute value) displacement will be, however, less than one
half or two thirds of the length of the molars. Thus we will get
the average amplitude and frequency of the oscillatory movements
which will give the maximum work, in unit time with the minimum
force.
Predominance of any type of movements leads to corres -
ponding changes in the structure of the jaw. So, two types of
motion of the lower jaw in processing food seem to be very
important fer voles, namely, longitudinal grinding and gnawing.
The length of the cutting edge of molar teeth increases in the
species having a predominantly longitudinal grinding movement by
of the enamel prisms (Midrotus, Lemmus, Myopus), and an
increase in the number of the loops of molars. (Microtus agrestis,
М. socialis paradoxus). Also the transition from the brachyodont
to hypsodont teeth is observed (Cl. rufocanus-Microt) and diastema
is short because of an increase in the length of the dental row
(excluding highly specialized forms such as muskrats). In species
having jaws where the grinding movement is predominant, the rows
of molars are somewhat short, diastema increases in length,
alveolar projection of the lower incisor approaches the articular
head of the lower jaw (Eliobius) and the lower part itself is elonga-
ted.
The length of M! increases, along with the general in-
crease in the length of the denta! row in forms having a longitudi-
nal - grinding movement where МЗ is generally many times.
shorter in them.
This is fully understood since, when the frontal advancement
of the jaw is insignificant, the main food falls on Ми, while М
is cut off from the action.
Strictly speaking, the process of crushing seeds and any
such hard matter occurs not only with the contraction of the lower
and the upper dental rows, but also when the displacement 18 small
with respect to one another by the rotary movements. It is
appropriate to compare the process of crushing food with the
pounding of grain in a mortar where the process is accomplished
by the pressure of the pestle (similar to the tubercle of the tooth)
9
N.N.VORONT SOV
as well.as by the rotary movements in the mortar. However,
grains can be broken, in a mortar but cannot be ground; a grater
is necessary for grinding. While reducing the food aubstance into
smailer bits on the grater, the pressure on the grinding object
plays a subordinate role in comparison with its displacement with
respect to the rubbing crests of the grater. The same is the
case when the food is processed by longitudinal-grinding move-
ments in Microtinae and some specialized Cricetinae (Andinomys,
Ne otoma).
The longitudinal (one row) or longitudinal transverse (two-
three row) arrangement of the roots of the teeth correspond to the
direction of the movements of the lower jaw. Itis interesting that
in Murinae, in which longitudinal and transverse movements ate
well developed the roots of the teeth are arranged in transverse
as well as ina longitudinal direction. Оп cheek-toaothed voles,
the roots of the molars have been arranged longitudinally. Even
when an additional third root appears in Clethrianomys, it is
arranged on the longitudinal plane only.
The shape and the position of the articular head is of great
significance for some movements of the lower jaw. Free dis-
placement of the articular head of the lower jaw in the longitudinal
direction along the fossa condyloidea is important for the grinding
type of movement. This is achieved by the relatively vertical
direction of the articular process and the horizontal position of
the articular head on it. This is accomplished by a sufficient
advancement of the mandibular row with respect to the maxillary
row having a considerable length of the dental rows in the species
where the grinding movements in the longitudinal direction are
predominant. The process of displacement of the articular head is
clearly seen by comparing the cheek-toothed and hypsodont voles
(Vorontsov, 1961Ъ).
5. A fifth type of jaw movement may also be observed
namely, the type of separated scissors.
In seed-eaters the halves of the lower jaw, loosely connected
between themselves, form the levers of the first order facilitating
the cracking of nuts. The anterior ends of the mandibles are
separated with the contraction of па. transversus mandibulae, т.
ptergoideus externus, and па. pterygoideus internus. This type
10
MASTIC ATORY MOVEMENTS IN RODENTS
of movement is not discussed here since it does not play an
important role in the evolution of the skull of rodents belonging
to the family Muridae.
3, Functions of the Mastication organs of Rodents
It was shown in earlier investigations (Vorontsov, 1961Ъ,
1962а, 1962b, 19734} that in the sced-eating forms, the main
type of movement is the move sent of the jaw in the vertical
plane (gnawing and crushing of seeds by the tubercles of molars);
whereas, in the herbivorous forms the main movements are
associated with grinding, i.e., the movements о! ihe jaw in the
horizontal plane in to-and fro directions. The process of the
division of the functions of gnawing and grinding (Vorontsov,
1962a) goes on independently in different groups. ‘The grinding
movements in the transverse direction are developed mostiy in
the seed-eating and rarely in the herbivorous rodents. The
grinding movements in the longitudinal direction prevail in the
herbivorous form except in the species which burrow with
incisors. The change in the points of attachment of P. anterior
and М. masseter laterlis оп the mandible results ina marked
development of the grinding movements in the longitudinal
direction from the seed-eating rodents to the herbivorous voles
(Vorontsov, 1962a).
Even in 1899 Tullberg had assumed that the circular
grinding movements was predominant in Murinae and longitudi-
nal grinding, in Microtinae. |
However, the functional consideration on the biomechanics
of the maxillary apparatus of rodents was described on the
basis of comparative anatomical study, unconfirmed by the
data of the specific physiological experiment. Only recently,
U.A. Labas developed a method of recording the masticatory
movements (mastication graph) of rodents in the laboratory of
A.D.Slonim, with the help of Holl's sensor device and magnet
activated in the lower jaw (Slonim, 1962, Labas 1963а).
The mechanical processing of food in practically all the
species under investigation, consists of consecutive stages of
gnawing and grinding which continuously alternate while eating
(Labas, 1963b; Vorontsov and Labas, т litt). While gnawing,
1]
М.М. VORONT SOV
the lower jaw moves in the longitudinally vertical plane, and
vhile grinding, the main movements are on the horizontal plane
inc ‘uding longitudinal as well as alternating transverse move-
ments, combined with the slight movement of the jaw in the
vertical plane.
The nature of the mastication graph was recorded while
eating hard food matter (seed and vegetative portions of plants,
dry bread, carrot, etc.) in all the species under study
iilistrates; first, the existence of two main types of the primary
vrocessing of food (gnawing and grinding) functionally different
and divided by time and secondly, great differences in the re-
lative duration and importance of these types in the various
species oi the rodents (Fig.2: and Table 1.2).
The vole occupies the first place according to the fre-
Guency of grinding movements, while the mice occupy the first
piace according to the frequency of gnawing movements. The
zsolden hamster is placed in an intermediate position between
the voles and the bunodont family of mice (see Tabie 1).
The gnawing movements are reduced to the biting of food
matter in the narrow skulled vole and gnawing of food is
virtually absent. In this manner, grinding plays the main
role.in the processing of food in field-voles. In gerbils, the
main burden of the processing of food matter rests on the in-
cisors and in mice gnawing assumes the significant role whereas
in bunodont hamsters belonging to Mesocricetus the role of
ee
gnawing and crushing movements is insignificant (see Table 2).
During gnawing and gripping of food, the oscillatory
movements of the lower jaw in the vertical and longitudinal
directions are frequent and uneven. The bunodont forms grind
the food particles gnawed off by the molars performing eight-
shaped movements in the three planes, including alternating
transverse motions of the jaw sometimes to the left and some-
times to the right. These unequal lateral movements are
evident in various species. They are easily observed by the
alternation of high and low waves on the mastication graph
recorded assymetrically by Holl's sensor device (Fig. 3).
MASTICATORY MOVEMENTS IN RODENTS
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MASTICATORY MOVEMENTS IN RODENTS
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Fig. 3: Mastication graph of white mouse recorded assymetrically by
Holl's sensor device placed on the skull. Left: recording during
gnawing of hard food matter (dry bread); centre luring grinding,
right; - while lapping water, below registration lime (1 sec. ).
After Labas,
The following main types of movements were observed on
the basis of the experimental data: by Labas (Vorontsov and
Labas, in litt. ).
Abducting - while storing food in the cheek pouches in
hamsters:
gnawing (also, possibly, crushing, which is difficult to
distinguish from gnawing on the recorded waves).
grinding, associated with movements in longitudinal
direction, particularly in voles it is strikingly expressed;
grinding - witha significant role of the transverse motion
of the jaw to the right and the left (prevails while grinding in
other species),
In this manner, the results of the comparative physiologi-
cal experiment principally confirm the assumptions regarding
the possible types of movements of the lower jaw made on the
basis of comparative morphological studies (Tullberg, 1899;
Vinogradov, 1926; Hinton, 1926; Lebedkina, 1949; Ognev, 1950;
Vorontsov, 1962a, 1962b, 19634).
The relationship of the exosomatic systems of the head
and skull and with each other. The main line of Transforma-
tion of the skull and Maxillary Apparatus of the Cricetidae.
If the division of organs into exosomatic and endosomatic
as proposed by A.N.Severtsov is applied, the skull is formed
under the strong influence of exosomatic (masticatory apparatus,
organs of smell, hearing and to some extent, sight) as well as
16
MASTICATORY MOVEMENTS IN RODENTS
endosomatic organs (the formation of the skull is greatly in-
fluenced by the brain). The long standing doubt аЪо..ё the brain:
or the muscles affecting the structure of the cranium wad
solved in the past by the majority of anatomists assuming it to
the musculature. The problem of the correlation of the gtruc-
ture of the sense organs with the shape of the cranium, ine
correlation between the structure of the capsular sections of
the cranium ana with the favourable solution of the bic-
mechanical problems of gripping and processing of food has act
been fully worked out.
Let us now consider certain tendencies in the transfor ma -
tion of the cranium of mice and voles, in the ecological series:
Ichthy omys-Oxymycterus -Orzyzomys -Peromyscus -Crice his ~.
Ne otoma -Andinomys -Clethrionomys-Microtus-Lemmus. Tris
series is characterized by a tendency towards the transition
from а purely protein diet, in Ichthyomys and Oxymeterus,
through а mixed type of diet characteristic of the majority of
mice and some primitive cheek-toocthed voles to an exclusively
cellulose diet, characteristic of t= hypsodont voles and
lemmings.
The relative size of the brain and the brain capsule of
the animals of this series diminishes during the transition
from those actively preying upon living objects to those feeding
on plants. The transition from feeding on proteins obtained
with difficulty to rich vegetative portions of plants leads toa
reduction of the olfactory organ, that plays a distinct, though
not a leading role in the life of seed-eating nodents (Ganeghinz ,
Gurtavoi, 1953), Ganeshina, Vorontsov, Chabovskii, 1957}.
The De velopment of simplification of the olfactory organ
is associated not only with the complication or simplification
of the ethmoturbinals which carry an olfactory epithelium, Sut
also with the increase or decrease in the relative volume of the
nasal cavity, as shown in insectivores (Ganeshina, Vorontsov
and Chabovskii, 1957), and consequently with a slight inflation
or elongation of the nasal part of the skull.
In view of the transition to low-calorie food, the as tivity
in voles (Naumov, 1948) and in certain herbivorous mice
(Hamilton, 1943} extends to nearly twenty four hours. ев are
17
М.М. УОВОМТ5ОУ
well developed in the noc arnal forms (Peromyscus), appreciably
reduced in Andinomys, Sigmodon, and the entire Microtinae..
The relative size of the eyeball also affects the structure of the
cranium toa definite degree. Although the width of the zygo-
matic arch is related not only to the size of the eye, but also to
the development ot the masticatory muscles, it is sometimes
possible to establish a specific relationship between the structure
of the orbital region of the skull and the size of the eye. Thus
in the line of the Dipodoidea from Sicista and Zapus to the рге-
sent Dipodidae, no special reinforcement of the masticatory
muscles is observed; Ба а sharp increase in the relative size of
the eyeball and relative width of the zygomatic arch is noticed.
The development of the tympanic region (bulla tympani and
bulla mastoidea) may result in a sharp change in the entire con-
figuration of the skull, particularly the brain capsule (Dipodidae,
He teromyidae, Ctenodactylidae, Gerbillinae). In some cases
hypertrophy of the tympanic region or the bony tube of the
external auditory meatus, as it was shown by Vorontsov (9963),
may facilitate the formation of unexpected connections between
the lower jaw and the skull. However, the variability of the
tympanic region is comparatively not very great within the
group of Cricetidae studied.
Of all the exsosomatic organs in the Cricetidae, the
structure of the masticatory organs has a decided influence on
the development of the cranium. However, this ‘influence™ is
very closely associated with the evolution of the functions of
other exsosomatic organs; the correlation between these systems
is so profound and "expedient" that this influence should not at
all be considered as a suppression of the functions of less
important organs by the leading organs.
The volume of the cranium is extremely great in pisci-
vorous Ichthyomys and Anatomys, Rheomys, Daptomys and other
rodents of the tribe Ichthyomyini that are allied toit. Their
food has a high-caloric value, procured with difficulty and
easily processible. The quick and sharp adduction of the lower
jaw in catching and gripping also plays a role in moving the
lower jawapart, The following changes take place in the
cranium because of the strong development of the muscles
adducting the lower jaw. The anterior part of the m. masseter
18
MASTIC ATORY MOVEMENTS IN RCDENTS
medialis, which moves the jaw forward and upward while
gripping the pray increases and the infraorbital foramen
through which this muscle passes, widens the fossa pterygoidews
lateralis is used for the attachment of M. pterygoideus and
accounts for 17-18% of the length of the skull: m. pterygoideus
internus is fixed toa large area, is fleshy and does not have «©
well marked tendinous layer by which it could be related to the
dynamic type producing abrupt, intense and sharp movements.
Owing to the ease of processing and the small quantity of
high-calorie food, the group of masticatory muscles, engaged in
grinding movements is poorly developed. The zygomatic arches,
to which are attached the posterior part of m. mass, lateralis,
р. posterior m. mass, medialis and through which passes m.
temporalis are very thin and poorly laid owing tc the reduction
of the masticatory muscles.
The size and thickness of the masseteric patch to which
is attached p. profundus m. mass. lateralis is extremely small.
The masseteric surface itself is : .cced ata slight angle to the
plane of the dental rows, and is а rected downward, to facilitate
the gripping function of p. profundus m. masa. lateralis.
The anterior part of m. masseter lateralis is attached to
a special, well-developed arm of the maxillary bone. The
anterior part of the lateral masticatory muscle in Ichthyomys
is attached along the lower edg= of the mandible (see Fig.7 a).
Such a construction leads to th> ‘act that muscles like р.
anterior та. lateralis, so adapted for the grinding of foodina
to and fro direction takes a greater part in the gripping and crush
ing of food than in grinding it by the longitudinal movements of the
lower jaw.
Of the sense organ Ichthy-rays, the organ of the sense
of touch is expressed as in many other aquatic mammals, thus
vibrissae are highly developed; the г innervating п. labialis
superior, branching {тс ~ th: powerful п. infraorbitaiis may
obviously, result als: зап increase in the size of the foramen
infraovbitale. But thi problem can be solved only after making
a special study of the ‹ -rrelation between the development of
vibrissae, the thickness of their innervating nerves and the size
of the foramen infraorbitale.
(
19
N.N.VORONTSOV
The skull of Oxymycterus differs from that of Ichthyomys
by a well developed nasal cavity. In_Oxymycterus the foramen
infraorbitale is enlarged, the fossa pterygoidea lateralis is
longitudinally elongated and the zygomatic arch is extraordi-
narily slender and poorly branched. The masseteric surface of
the maxillary bone is small (although greater than that in
Ichthyomys), thin, but to some extent directed more upwards and
forwards. Although the special process for the attachment of
p. anterior m. mass. lateralis is absent, this muscle is attached
from the lower side of the maxilla in Oxymycterus.
In Ichthyomys and Oxymycterus the masticatory surfaces
are not strictly parallel to the plane of the base of the skull, but
are directed slightly laterally in the upper and medially in the
lower rows of teeth. This indicates the possibility of some
lateral crushing type movement of the lower jaw while chewing
food. Actually, in these forms the mandible is not inserted
deeply in the skull; the articular depression is situated suffi-
ciently low, and the difference between its level and the level
of attachment of m. pterygoideus externus is not very great,
With such cranial structure and the attachment of muscles the
lower jaw moves insignificantly forward and downward and
shifts appreciably medially with the contraction of this muscle.
The skull of Oxymycterus and that of a group of genera
close to it (Lenoxus, Blarinomys and others) is characterized
by the strong development of the nasal section of the cranium.
This is associated with the intense development of the ethmo-
turbinal and correlates with an increase in the size (length and
breadth) of the nasal cavity. The complication of the organs of
smell in this group of insectivorous rodents results in an
increase in the size of the olfactory lobes of the brain, which
has a relation to the widening of the interorbital part of the skull
ihe ethmoturbinals are situated in the fore part and the olfactory
lobes of the brain in the posterior part of this section of the skull
The skulls of Ichthyomys and particularly, of Oxymycterus
are distinguished by the absence of the noticeable crest for the
_attachment of the masticatory muscle. This explains the re-
latively soft food (fish, insects, small invertebrates), taken by
these rodents in small quantity because of the high caloric value,
20
MASTICATORY MOVEMENTS IN RODENTS
The predominance of the cerebral section of the cranium ove
the facial section is also characteristic of Ichthyomys, and
Oxymycterus.
Substantial transformation of the skull is observed in the
series starting from the carnivorous rodents to the narrow
specialized forms of field-voles. A change over to the conti-
nuous intake of food with plenty of céllulose matter, anda
simplification of the nerve structure relative to the reduction of
the sense organs sharply decreases the size of the cranium.
The function of gripping and the retention of food which is
the main characteristic of Ichthyomys is replaced by the function
of processing a large quantity of coarse, low-calorie, cellulose
food matter which is the main characteristic of the field-voles
and other herbivorous mice. In general, starting with the
Neogene, this change of function is the most important moment
in the evolution, of the entire Myomorpha. It should be empha-
sized that the transition from protein toa cellulose diet needed
a sudden strengthening of the masticatory movements, resulting
in the greater development of all masticatory muscles. The
muscles adducting the lower jaw or producing gnawing motions
also begin to be dominant in field-voles in comparison with the
carnivorous or seed-eating mice. However, a general strength-
ening of the muscles suchas па. temporalis and р. anterior, па.
mass. medialis, is clearly noticeable, though insignificant in
comparison with the strengthening of the grinding movement
executed by the main group of masseteric muscles and
especially by p. anterior m. mass. lateralis.
Since the role of gripping of prey is reduced, the ever
decreasing part of the fibers of the p. anterior m. mass.
medialis passing through the foramen infraorbitale causes this
structure to become narrower. The point of attachment of part of
the fibers shifts forward and upward, so that during contraction
of the muscles the lower jaw moves not only upward, but to some
extent forward.
The fossa pterygoidea lateralis becomes short and deep but
in field-voles and zokors it even forms a pit oriented not along,
but across the cranial axis. In this series its length in relation
to that of the cranium decreases in the following manner :-
21
М.М. VORONTSOV
Oxymycterus nasutus_ 18-19
Ichthyomys soderstromi 17-18
Oryzomys meridensis 15-16
Reithrodontomys soderstromi 14-15
Cricetus cricetus 11-12
Andinomys edax У
Clethrionomys glareolus 7-8
Lemmus lemmus 5-6
М. pterygoideus internus, attached to the cranium of
lemmus ша smallarea, is pierced by tendinous fibers and
moves towards the static type of muscle, accomplishing long,
slow masticatory movements (Fig. 4).
The area of masseteric attachment on the maxillary in this
series sharply increases, moves forward and nearly takes a
perpendicular position with respect to the plane of the dental
series. This results in the change of motion of p. profundus га.
mass. lateralis, which changes froma vertical direction in the
primary members of the series to the inclined horizontal direc-
tion; that is, it takes part not only in the adduction of the lower
jaw but also in forward movement (Fig. 5).
The change in the position and shape of the masseteric area
is clearly observed in the series of Madagascan nesomyinae from
Macrotarsomys to Brachyoromys (Fig. 6).
The point of attachment of p. anterior m. mass. lateralis
shifts appreciably from the ventral side of the skull to the
lateral side and displaces upwards to some extent. In Cricetidae
we may observe a clearly marked tendency for the transfer of the
point of attachment of the anterior part of the external masticatory
muscles from the rear side of the lower margin of the angular
outgrowth to the internal side of the posterior margin of the jaw,
close to the notch between the angular and articular outgrowths
(Fig. 7). This leads to the most intensive development of the
grinding movements in the longitudinal direction and p. anterior
пл. mass. lateralis plays the most important role in these move-
ments, In general, this muscle is adapted mainly for longitudi-
22
MASTICATORY MOVEMENTS IN RODENTS
Fig. 4:
- Change in the points of attachment and functions of plerygoid
muscles. (a) Cricetus cricetus Г. ; (b) Меою та cinerea Ord, ;
(с) Micrélus agrestis Г,. ; (4) Myospalax fontanieri Milne -Edw,
Dotted line is the point of attachment of the.muscles on the lower
jaw; vertical, broken shaded portion is the point of attachment
of the muscles on the cranium; arrows show the direction of the
action of the pterygoid muscles; pte, pte' and Ме". are plerygot-
deus externus, its attachment to the cranium and 19 the jaw; pli,
pti! and pli'' are pterygoideus internus and its areas of allachment
to the cranium and the jaw, The pterygoideus externus primarily
takes part in the transverse displacement of the lower jaw, (а)
and later adducts of the posterior part of the jaw (cd) The plery-
goideus internus, primarily takes part in the abduction of the
lower jaw, and the insignificant forward tion for gnawing in
the posterior position (a), later takes part’in the forward motion
of the.jaw (c,d). Vorontsov (1963).
nally grinding movements; but in all hamsters it plays a definite
role while gnawing, crushing and gripping because of the attach-
ment of a large part of fibers on the ventral side of the jaw.
The change in the point of attachment of this muscle on the
posterior part of the lower jaw made it possible for the evolution
of herbivorous forms among hamsters. The loss of the lower
point of attachment of the anterior part of the lateral masticatory
muscle and the increase in the area of its attachment on the internal
side of the posterior margin of the lower jaw are the most
23
N.N. VORONTSOV
Fig. 5: Trans for mation of the functions of muscles, adducting the lower
jaw. (a) Ichthyomys soderstromi de Winton; (b) Cricetus cricetus
Г. ; (с) Negtoma.cinerea Ord, ; (а) Microtus agrestris L
The black portion shows the course of pars, anterior т. mass,
medialis; the shaded portion shows the course of pars profundus
т. mass. lateralis; the dotted line shows the point of attachment
of this muscle on the cranium. Right - diagrams showing the
action of muscles in the later members of the series. We se
a reduction in the relative size, and shifting of thc point of
attachment of p. anterior т. mass medialis upwards and back -
wards and that of the point of attachment of p. profundus т. mass.
lateralis on the skull forwards and upwards but on the jaw back -
wards and perpendicularly upwards (After Vorontsov (1963)).
important events in the evolution of Cricetidae which helped in the
emergence of the large group of the present-day voles.
W ith the change of the points of attachment of the muscle,
the field-voles lost their former functions of crushing food, and
developed a dental system to adapt to new habits. This, asa
matter of fact, is a unique feature that distinguishes hamsters
(Cricetinae) from field-voles (Microtinae).
Powerful development of the posterior part of р. anterior
m. mass. medialis, attached to the internal part of the zogymatic
24
Fig. 6:
MASTICATORY MOVEMENTS IN RODENTS
Mx ri т’ р”
Anterior part of the cranium of Madagascan cricetids, Nesomyi=
nae. Change in the position of masseteric area and suborbital
orifice can be seen. (a) Macrotarsomys bastardi Milne -Edw, et
Grandid; (5) Nesomys rufus Peters; (с) Gymnuromys roberti, РГ,
Major; (а) Eliurus tanala Е. Major; (e) Brachytarsomys albicauda
Giinth. ; (f) Brachyuromys betsileoensis Barti. ; (=) Brachyuromys-
tramirohitra, РЕ. Major; (f) Frontale; Mx - maxillare; М -пазще;
1, - lacrymae; fi - foramen infraorbitale; Im - Inter maxillare;
vi -ramus inferior; rs - ramus superior; mlsf' - point of altach-
ment of т. mass lateralis р - anterior; mip’ - point of attachment
of т. mass latcralis 5 - profundus, After Vorontsov (1963).
25
N.N.VORONTSOV
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MASTICATORY MOVEMENTS IN RODENTS
arch and filling a considerable part of the eye-socket, and the
increase in the size of p. posterior m. mass. lateralis (see Fig. 7}
lead to the strengthening and the widening of the zygomatic arches.
A clear trend toward an increase in size and widening, and the
attachment of zygomatic arches by the crests is observed in the
series under consideration.
In the series from Oryzomys - Peromyscus (except the
narrowly specialized Ichthyomys and Oxymeterus) to Microtinae,
the organs of sense, associated with the search of food, smell and
sight are greatly simplified. The ethmoturbinals are simplified
(Ganeshina and Gurtovoi, 1953), and sothe size of the olfactory
parts of the brain, and the volume of the nasal cavity and the
anterior section of the cranium decreases, and the interorbital
section of the cranium contracts. With the relative decrease in
the size of the eyeball in this series, the eye socket not only
decreases, but, the width of the eye increases with its reduction
because of the presence of the well developed, internal, masti-
catory muscles.
The structure of the interorbital space of the type found in
Oxymycterus, Oryzomys, Peromyscus, and others, that does not
meet all the new requirements, and rounded in the cross section,
is replaced by the structure having a strong interorbital crest of
the type found in Cricetus, Microtus and Lemmus, which success-
fully resist powerful forces developed by the masticatory muscies
with the adduction of the lower jaw.
In this series the masticatory surfaces of the upper and lower
molars become parallel to each other, which allows narrow and
perfect adaptations to the grinding of food solely in the longitudinal
direction. In the same series the level of the articular surface of
the temporal bone rises above the level of the skull base, with the
result that the lower jaw moves deeply into the cranium. On such
cranial structure, in. pterygoideus externus works on the abduction
of the posterior part of the jaw downwards and a little forward,
which is significant during the gnawing movements of the lower jaw
in the anterior position with unfixed axis of the maxillary lever.
The possibilities of the lateral movements of jaws are limited (see
Fig. 4).
27
N.N.VORONTSOV
The strengthening of the construction of the skull by addi-
tional crests for the attachment of the reinforced masticatory
muscle, increases the relative thickness of the cranial bones and
the appearance of new "costae of rigidity"' in the shape of inter-
orbital crests are observed inthis series. The tendency for a
decrease in the relative size of the cerebral part of the cranium
and an increase in the size of the facial part is observed.
The evolution of these features although less visual, but suffi-
ciently clear, is traced not only on slightly artificial ecological
series from Ichthyomys to Lemmus taken for analysis, but also on
more real comparative anatomical series. It is sufficient to take
for example, such series of hamsters аз : Phodopus -Cricetulus-
Cricetus, Oryzomys-Nectomys, Phyllotis-Euneomys-Auliscomys-
Chinchillula-Andinomys (Fig. 8), Holochilus-Sigmodon-
Reithrodon or series of field-voles Dolomys-~-Clethrionomys-
Ondatra-Microtus-Lemmus, to confirm the existence of the above
described course of transformation of correlatively connected
systems of the exosomatic organs of the head and the cranium
saaed
Fig. 8: Silhouettes of the cranium of hamsters from the trtbe >
Phyliotiini, The relative expansion and thickening of the eygo=
matic arch and reduction of the interorbital space is observed
in the series. (с) Phyllotis Watch. ; (b) Eune. ‘луз. Coues. ;
(с) Auliscomys Osgood; (а) Chinchliliula Thom. ; (e) Andimaomye
Thom, After Vorontsov (1963).
The line of development inthe comparative ana‘. mical
series corresponding to the ecology of the forms unde» study have
been established hbove; this series, however, can be -ecad inthe
direction as described above, as well as the cpposite way. To
prove the initial state is very necessary since the reduction of the
majority of sense organs is postulated as leading to the appearance
28
EVOLUTION OF CRICETD CR ANIUM
of widely spread and prospering groups and simplification of brain.
Let us take some paleontological and embryo logical data to prove
that these series must be read inthe same manner as they have
been summarized above.
5. Paleontological and Embryological Proofs of the Main
Direction of Evolution of the Cranium of Cricetidae.
The fragments of cranium of the paleogenic hamsters are
very rarely found while restoring them. The thin zygomatic arch
and the widely rounded and low-set foramen infraorbitale in the
cranium in well preserved oligocence Cricetodon incertum
Schlosser (from phosphorites of Kverci), is of interest.* The
masseteric space is situated ai'most parallel to the plane of the
cranial base (see Fig. 9,a 10,a) - sucha low position of its masse
teric space is not found in any of the latest members of Cricetidae.
The attachment point of p. anterior па. mass. lateralis is situated
onthe ventral side of the maxillary bone. The dental surface has
sharp tubercles and the exposure of dentinal fields is seen only on
the crowns of molars.
Fig. 9: The skull of some fossilized hamsters (front view). Contraction
and displacement of preorbital orifice (shown in black) and
displacement of masseteric space (attachment point of p. profun-
dosm, mass. lateralis is indicated by dots). (a) Cricetodon
incertum Schlosser (Oligocene), after Schaub (1925) with changes;
(6) Cricetops (aff.) affinis Arg. (Oligocene), org. ; (с) Cricetodon
gregovium Schaub (Miocene), after Schaub (1925) with changes;
ri ~ramus inferior arches of preorbital orifice; fi-foramen
infraorbitale; 7$ -romus superior, arches of preorbital orifice.
Afler Vorontsov (1963).
The large sized Cricetops, classified by Simpson (1945) in
a special tribe of Cricetopini stand apart from the paleoge nic
Cricetinae. Inthe well preserved skull of Cricetops (aff). affinis.
* The description is given after the figures of Schaub (1925).
29
М.М. VORONTSOV
Arg. (see Fig. 9,b 10,b) from the Oligocene for mations of the
Chelkar-Tenghiz lake (Kazhakstan), the features of the compara-
tively higher specializations are observed along with the primitive
features.
Fig. 10:
Structure of the anterior part of the zygomatic arch and the
attachment points of the masticatory muscle, in some fossilized
hamsters, side view, (a) Cricetodon incertum Schlosser (Oligo -
cene) after Schaub (1925) with changes; (5) Cricetops (aff. )
affinis. Arg. (Oligocene), orig. ; (c) Cricetodon minus Lartet
(Miocene), after Schaub (1925) with changes; (d) Criceton
gregarium Schaub (Miocene), after Schaub (1925) with changes;
(e) Cricetodon affine Schaub (Miocene), after Schaub (1926) with
‘Changes. Thick dots delineate the area of attachment of the
anterior part of pars anterior т. mass. medialis (pamm); fine
dots delineate masseteric space, the point of attachment of p.
profundus т. mass. lateralis. Legends as shown in Fig. 9.
After Vorontsov (1963).
The masseteric area, small in area and situated parallel to
the plane of the skull base, and the very wide, lowly situated
foramen infraorbitale (see Fig. 9b), are related to a number of
primitive indications. The zygomatic arches are not widely
arranged.
accounting for nearly 14-15% of the length of the cranium, M.
masseter lateralis, obviously, has not yet divided into three
portions.
30
Fossa pterygoidea lateralis is stretched longitudinally,
EVOLUTION OF GRICETID CR ANIUM
Meanwhile some features of Cricetops indicate further
specialization in the structure of the cranium as compared to the
Oligocene Cricetodon. In Cricetops (aff) affinis thick zypgomatic
arches are highly developed, greatly contracted intero. bital space
is fortified by paired crests and the facial section of cranium
prevail over cerebral section. These characteristics indicate a
substantial diver gence of Cricetinae already in upper Oligocene,
when the adaptations similar to the modern forms of Cricetus were
evolved along with the type of modern forms of Muroidea of
American hamsters, then represented by Cricetodon. However,
these facts, in our Opinion, cannot substantially change the above
developed concept concerning the main direction of the evolution of
the cranium of Cricetidae.
The excellent series of craniums of Cricetops collected by
the Mongolian paleontological expedition (collection of the Institute
of Paleontology, Middle or Upper Oligocene, Tatal - Hol, Mongo-
lia), mainly confirms the results of the study of the Chelkar -
Tenghiz specimen. Mongolian Cricetops from Tatal - Hol, belong-
ing, evidently to a new species, which has. not yet been described,
differ by the position of the attachment of m. mass, lateralis in
these hamsters; the masseteric space, serving as the attachment
of p. profundus па. mass. lateralis so far does not exist.
The cranium of the Miocene Cricetodon minus Lartet (from
Sansan), preserves the series of primitive characteristics.% The
description is given on the basis of the figure of Schaub (1925).
The zygomatic arches are tightly set and are thin, the masseteric
space is situated at a relatively lower level (see Fig. 10c) and p.
anterior m. mass. lateralis is attached to the ventral side of the
cranium, The cerebrat part of the cranium sharply prevails over
the facial portion. Fossa pterygoidea lateralis stretched longi-
tudinally accounts for 15-16% of the length of the skull (i.e. ,
approaches to Oryzomys in dimensions). The nasal cavity is
sufficiently well developed and resembles the nasal section of the
cranium of Oryzomys in outline. The gnawing surface of the upper
molars is slightly inclined outside (less than in Ichthyomys and
Oxymycterus). The crests for the attachment of the masticatory
muscle are not developed in the same way as in the fine forms of
‘modern Oryzomys, Peromyscus, Hesperomys, etc.;-but there is
‘* The description is given on the basis of the Figures of Schaub (1925).
31
N.N. VORONTSOV
a longitudinal crest on the basioccipitals for the attachment of
musclés, which lowers the head. Special costae of rigidity on the
interorbital part of the cranium are absent. The articujation of
the mandible with the cranium is situated at a significantly lower
level. The surface of the molars has sharp tubercles, but the
exposure of dentinal fields on the worn out teeth is seen not only
on the crowns of the tubercles but also in their bases and forma
loop- shaped figure (Schaub, 1925, Taf. I, Fig. 5). On the whole,
the craniums of Cricetodon minus and Cricetodon incertum stand
nearest to the modern hamsters of ''the generalized biological
type" like Oryzomys. These oldest forms differ greatly from the
narrowly specialized modern forms of Ichthyomys and Oxymyce-
terus and are far from the field-voles, like Andinomys,
Chinchillula and even Cricetus.
In the Miocene Cricetodon minus, the following changes
take place in comparison with oligocene Cr. incertum:foramen
infraorbitale reduces to some extent and moves upward, raising
the masseteric space. It is situated at a greater angle to the
plane of the cranial base and becomes more powerful (the position
of the masseteric space resembles that of the modern forms of
Oryzomys (Melanomys phaeopus Thom.). The molars have less
pointed tubercles.
Further development of these tendencies in the evolution
of the skull is found in the Miocene species, Cricetodon gregarium
(Schaub.). Compared to the former species, the foramen infra-
orbitale is highly contracted in Cr. gregarium, and with the widest
part of the preorbital orifice it moves upwards. The masseteric
space is widened and the zygomatic arch becomes more powerful.
The masseteric space itself is turned upwards and
forwards (see Fig. 9c, 10d).
Specializations of the skull in Cricetodon а ше (Schaub)
(see Fig. 10e) goes still further; the foramen infraorbitale
connects from below, its widest portion is situated at the level
of the lower boundary of nasale. The masseteric space moves
sharply up and forward, thereby resembling many modern ham-
sters, but the upper arch of the preorbital orifice is thinner than
in the latest forms having a similar structure of the masseteric
space. The dental system is brachyodont, having allloop- shaped
32
EVOLUTION OF CRICETD CRANIUM
gnawing surface of molars in the adults slightly resembling the
structure of molars of the modern forms of Nectomys. The
tubercle, to which p. anterior m. mass, lateralis is attached,
moves from the medial to the lateral side of the maxillary bone.
The lower pleistocene Allocr icetus* belong not to Cricetodontini
fossils but to the latest Cricetinitribe, possess the characteri-
stics of the cranium of the modern hamsters. The existence of
the powerful, and obviously, widely set zygomatic arches, a
strong and wide masseteric space directed forward and upward,
and a greatly contracted foramen infraorbitale from beiow, should
be noted,
This series cannot be treated as established since full
remnants of the skull, the lower jaw and the teeth are not found
in the fossils, But it may be said to be close to the primary
structure of the skull of the ancient forms of Cricetidae and its
evolution. It should be emphasized that the morphology of the
skull of the oldest forms of Cricetidae resembles that of Oryzomys
more, and hamsters closer to them, than those in the beginning af
the ecological series of Ichthyomys and Oxymycterus as suggested
above.
The above considerations on the evolution of the cranium
of hamsters and Cricetidae can be confirmed by the data on the
individual development of Cricetinae.
If we consider that the growth of the cerebral section of the
cranium prevails over the growth of the facial section in the early
stages of development then some characteristics of the cranium
of young modern hamsters**are close to the fossils and the
primitive forms of the modern Cricetinae.
Narrowly placed thin zygomatic arches, smaller deflection
of the masseteric space forward and upward, central position of
the point of attachment of р. anterior m. mass, lateralis,, wide
inter orbital space not fortified by crests.features which distinguish
the craniums of the young ones of Cricetus cricetus from the
craniums of adults confirm, the statements above on the primi-
tive and specialized characteristics in the cranium of hamsters.
* Description given according to the figures of Schaub (1930).
** Materials of the postembryonal development of the skull of Cricetus
cricetus and Phodopus sungorus served as the basis for studies.
33
М. М. VORONTSOV
However, in the cranium of the young Cricetus cricetus
(with a single cut M!) the features related to the characteristics
of specialization are observed. Foramen infraorbitale is almost
as narrow as in the individual adults, and fossa pterygoidea
lateralis is shorter than in the adult hamsters; the young Cr.
cricetus resemble field-voles by their shape. It may be asked
whether such a structure is not related to the herbivorous nature
of the young rodents compared with adult ones - a phenomenon not
yet understood.
On the whole, the fragments of data available on the Paleon-
tology and the postembryonal development of Cricetinae confirm
this system of transformation of the cranium of all forms of
Cricetinae and enable us to establish the structure of the cranium
close to the initial state in the modern forms of Cricetinae. The
structure of the cranium of the hamsters of the Oryzomys group
greatly resembles the ''archetype'' Cricetidae, suggested оп the
basis of the majority of features.
Ecological, morphological and functional anatomical analysis
of the structure of the cranium and the masticatory muscles,
supported by paleontological and embryological materials, enable
us to understand not only the adaptive significance of the features
widely used in classification but also to know the dynamics of
the transformation of these features in phylo- and ontogenesis,
and to trace their fate and to evaluate the significance of the
appearance of some new formations in the history of development.
CHAPTER II
EVOLUTION OF THE DENTAL SYSTEM
I, General Notions: Terminology
The dental system of rodents Muroidea is differentiated
only by two types of teeth, namely, incisors and real molars.
Premolars are not present. The space between incisors and
molars is occupied by intermaxillary and maxillary bones. The
space is free of teeth and is known as diastema. The incisors,
situated in the intermaxillary bones have a milk and permanent
sets. In hamsters the incisors change in the embryonal age. The
young ones of real hamsters are born with incisors; this is the
systematic distinction af Cricetus, Cricetulus, Mesocricetus and
Phodopus from all other Cricetidae. The molars are cut after a
few days of growth: starting with the first, then, the second and
the third molars. The dental formula of Cricetidae is constant:
M3 is absent in dwarf gerbil of the genus Desmodilliscus. *
il ша ‚ whereas in Muridae the number of molars may be re-
Heed +6 two (Hydromys, Neohydromys) and even to one in every
jaw (Mayermys).
The masticatory part i.e., the crown and the root part
resting in the bone, are distinguished m molar tooth. The teeth
having a low crown which does not enter into the bone, are called
brachyodont, the teeth having a crown of medium height, partially
. penetrating into the bone but with protective roots are called `
mesodont and the teeth having a high crown and reduced roots are
called hypsodont. Hypsodont molars grow during the entire life
of the animal. The chewing surface of molars may have sharp
tubercles, or flat tubercles, or may be practicaily plane. In
voles, the molar tooth not yet emerged has a tuberculate chewing
surface completely covered with an enamel layer. As abrasion
* М} is abseni in dwarf gerbil of the genus Desmodilliscus.
35
М. М. VORONTSOV
proceeds (first, on the tubercles) the dentinal fields bordering
along the edges on the enamel crests are exposed. Since the
thickness of the enamel is more than the thickness of dentine, the
enamel layers always protrude over the dentinal fields, forming
enamel crests. Attached to the so-called flat crowned tooth,
dentinal fields are arranged in one level and over them rise
enamel crests, forming a second level, The food matter is
ground with the mutual intersection of enamel crests of the upper
and the lower dental rows. Dentine serves as a matrix for the
cutting enamel portions and does not take part in grinding food.
A very complicated figure formed by the alternation of
enamel crests and dentinal fields, changing considerably with the
age of the animal, preserves the features peculiar to a given
taxonomical unit. Until now a unity does not exist in the nomen-
clature of basic and additional tubercles, protuberances, closed
islets of enamel, and other important systematic characteristics.
The best terminology for the teeth of water hamsters,
Nectomys was proposed by Hershkovitz (1944). However, like
most of the other English authors he gives anglisized Latin
terminology. Hershkovitz gives the meaning of the so-called
inlet corners, but the enamel islets enclosed in the dentinal area
is not named. Shotwell (1958) gave a successful system of
terms for closed, enameled islets and flexus for the fossils of
Mylagaullidae and Aplodontidae. In subsequent works on the
structure of the fossils of hamsters carried out by AMerican
authors, the terminology proposed by Hershkovitz (Hopper, 1945,
1957), (Hershkovitz, 1955, 1962) was widely used.
Full use of the terminology of Hershkovitz on the large
and varying materials somewhat impedes the conformation of
tooth parts. Therefore, the system of Hershkovitz was slightly
modified by using the nomenclature proposed by Shotwell for the
meaning of flexus and closed enameled spaces adding to it some
new Meanings.
The structure of the masticatory surface of the second
upper molar М2? (see Fig. 11,a) is nearest to the original plan
of the structure and it is constant.
36
ВМ:
DENTAL SYSTEM EVOLUTION
antfl antfld
msfld msstd
pfld mtfld
\ pstfla
sn es
b
ГА
Scheme of the structure and the adopted nomenclature of molar
teeth of Cricetidae. After Hershkovitz (1944) with changes and
additions. (a) Upper molars (antfl - anteroflexus, antfs -ащето-
fossa, antl-anterolop.; с. ant-anterior cingulum, с. post-poste -
rior cingulum, eac-exteroanterocone, Hc-hypocone, hfl-hypo-
y 2xus, hfs-hypofossa, tae-interoanterocone, Mc-metacone,
mtfl-metaflexus, mtfs-me'afossa, msst-mesostyle, pfl-para-
flexus, pafs-parafossa, Pc-paracone, Рус-ргоюсопе, prfl-pro- .
toflexus, pstl-posteroloph; (b) lower molars, antfld-anteroflexid,
cntfsal-anterofossetid, mtld-anteroflexid, antfsd-anterofossetid,
antld-anterolophid, с. anti-anterior cingulum, с. post-posterior
cingulum, eacd-exteroanteroconid, Hcd-hypoconid, hfld-hypo-
flexid, hfsd-hypofossetid, iacd-interoanteroconid, Mcd-metaco-
nid, mtfld-metaflexid, mtfsd-metafossetid, msstd-mesostylid,
pfld-paraflexid, prfsd-parafossetid, Pcd-paraconid, Руса-
protoconid, prfld-protoflexid, pstfld-postflexid, pstld-posterolo -
phid, antfld-anterolophiflexid, prcfld-procinguluflexid, hstd-
hypostilid.
37
М.М. УОВ ОМ TSOV
The main tubercles of teeth are termed cusps, supple-
mentary Ones, cingula; these cingula join with the cusps by
means of lophs. Flexuses, situated between tubercles are
named according to the arrangement of the tubercles, Ёе.,
hypoflexus when arranged in front of the hypocone, metaflexus
when situated before metacone, and so on. A slight rise in the
edge of the tooth between tubercles while grinding may lead to
the isolation of the flexus in the closed, enamel islet. This
fossa is named after the flexus from which it was tied off, е. в. ,
when it is tied off from anteroflexus it is called anterofossa,
when it is tied off from hypoflexus it is called hypofossa and so
on.
Two main tubercles anterior (protocone) and posterior
(hypocone) are distinctly seen from the lingual side of М“. In
iront of protocone the anteroloph may be well developed with
the formation of an outgrowth (sometimes called a heel) vallecula
(or flexus) occurring between anteroloph and protocone is named
protoflexus, and in case of snapping in the closed fossetus pro-
tofossa. Vallecula between protocone and hypocone is named
hypoflexus, and in case of its closure into fossa, hypofossa.
The structure of the molars from the labial side is
generally somewhat more complex than that from the lingual
side. The two labial tubercles that are always present are
called paracone (anterior) and metacone (posterior). In front of
the paracone, usually there is an additional tubercle connecting,
as detrition goes on, the crest with the axial elevated part of
the tooth is termei the anterior cingulum. There may also be
an additional tubercle between the paracone and metacone con-
necting the crest with the axial elevate4 part of tooth (it is
named mesostylus). Finally behind metacone the posterior
cingulum may be well developed. F lexus between the anterior
cingulum and paracone is called paraflexus, and fossa situated
at this place, parafossa. The depression between the paracone
and the spur of mesostylus is named mesoflexus and fossa,
mesofossa. The flexus between mesotyle and metacone is named
metaflexus, and fossa, metafossa. Finally the cavity between
the metacone and posterior cingulum is named postflexus and
fossa, postfossa, M3 is also characterized by the same plan
of structure but generally slightly simplified.
38
MOLAR TEETH STRUCTURE
M! in Cricetidae is complicated by the constant presence
of anterocone in front of protocone. As arule, ашегосопе is
subdivided into internal (intero-anterocone) and external (extero-
anterocone) in hamsters. The flexus dividing the internal and
external protocones, is called anteroflexus and the fossa formed
with the closure of this flexus is anterofossa.
The tubercles, flexuses and fossae of the lower molars
(see Fig. 11,b) are named the same way as the upper ones, but
with suffix "id' added in the end, (protoconid, protoflexid, pro-
tofossetid, etc. ).
(2) Types of masticatory movements and the structure of
molars
The main types of masticatory movements of rodents have
been discussed above (Chapter I) and some peculiarities of the
structure of the masticatory apparatus in connection with some
type of processing of the food have also been noted.
As already mentioned, gnawing movements of the incisors
in the rear position may be very close by its trajectory to the
crushing movements of the lower jaw. Processing of the seeds
on the tubercular teeth may be compared with the cutting with
pestle (tubercles) and mortar (corresponding flexus of the tooth).
Movements on the horizontal plane carried out by the jaw of
bunodont rodents are not great and, generally they have a some-
what circular pattern. The figure of the gnawing surface of the
lower molars is represented as the reflection of the correspond-
ing figure of the upper row of teeth, so that when the lower
dental row moves, the tubercles moving against the correspond-
ing tubercles of the upper row or vice versa form а flexus. A
similar structure of teeth limits very much the possibility of the
longitudinal displacement of dental rows with respect to each
other, but then it provides an extremely clcse contact of the
crushing surfaces of lower and upper dental rows. Since each
tubercle and the flexus of its tooth play the role of mortar and
pestle while processing the grains in the mouth, it can be fully
understood why the tubercles are generally found in a good
number on the molar teeth of the grain-eating rodents. This
process can very well be traced in the structure of the teeth of |
39
М. М. VORONT SOV
the grain-eating hamsters such as Rhipidomys, Reithrodontomys
and Peromyscus. Apparently, the three-row structure of tuber-
cles inthe forms of Muridae was also just a progressive feature
enabling it to be excluded from the Old World grain-eating buno-
dont, the mouse-like hamsters now available only in the New
World and Madagascar (if the Iranian form Calomyscus is not
considered).
The trajectory of.motion of the mandible depends toa
great extent on the mutual arrangement of tubercles with respect
to each other. The opposite arrangement of tubercles with
respect to each other is a characteristic (though varying in
degree) of all the real palearctic hamsters (Crietini) and parti-
cularly of the Central Asian hamsters, Phodopus having a pre-
dominance of transverse Movements of the mandible. For this
the width of the molars increases a little in real hamsters.
Since the role of МЗ during the processing of food matter is
significant (it is less than the role of M!, because of the smaller
length of the arc of trajectory described by M3 in comparison
with М! with the angle of deflection of the lower jaw to the
side remaining the same from the position of closed molars M3
of such forms is not greatly reduced. But since a strong trans-
verse displacement of the mandible in the case of a two-row
arrangement can lead to ‘idle’ motion' when the tubercles of the
lower row do not meet the corresponding flexures of the upper
row; the magnitude of lateral displacement of the lower jaw is
limited and so such arrangement of tubercles of molars in the
grain-eating forms of the family Crecitidae should be taken as
"inddaptive” (in the sense proposed by V.O. Kovalevskii).
When the arrangement of tubercles of the external and
internal rows is alternative with respect to each other
(Reithrodontomys, Peromyscus, Calomyscus, etc. ) the longi-
tudinal movement of the lower row with respect to the upper one
is dominant. In this case, when the mandible moves forward
1-2 tubercles in length, the particular tubercle is placed against
the corresponding flexus, whereas a vigorous transverse Mmove-
ment of the jaw may lead to sucha condition when tubercles will
be placed opposite tubercles and flexus opposite flexus. In this
longitudinally oriented type of crushing movements generally м1
and М“ are especially complicated whereas МЗ which ceases to
touch the lower molars when the movement of the lower jaw is
40
MOLAR TEETH STRUCTURE
insignificant, may be reduced. The relative width of the dental
row of the seed-eating forms with alternative arrangement of tuber.
cles is a little less than those with compressed masticatory surface
and with cellulose nutrition. The alternative type of arrangement
of tubercles of seed-eating rodents must be taken as adaptive.
A few forms of hamsters, changing Over to the carnivorous
type of nutrition (piscivorous Ichthyomys, Rheomys, Daptomys,
Anotomys etc., insectivorous Cxymycterus, Lenoxus, Blarino-~
mys), undergo the following transformations of molars:
higher caloric value of the animal food than seeds leads toa
decrease in the volume of the food consumed and its breaking up
does not require a thorough biomechanical processing because
of its reduced quantity and softness. Therefore, additional
tubercles of teeth (mesostylus, anterior and posterior cingula,
etc.) undergo reduction. The main biomechanical task, namely,
gripping and grasping of the prey, falls On incisors but the molars
possess sharper tubercles. A few tubercles of teeth (in compari-
sOn with seed-~eating forms) are situated Opposite, and the
relative width of the dental row increases. The opposite and
broad arrangement of tubercles facilitate grasping of the prey,
sometimes much larger animals because the force exerted by the
prey is directed longitudinally forward and the teeth holding the
prey are transversely arranged. It is easy to understand that
the alternative arrangement of tubercles and an increase in their
number (always associated with the decrease inthe relative height
of tubercles) would appear to be biomechanically disadvantageous
in this case. The reduction of the dental system оп the whole is
characteristic of the carnivorous forms of Cricetidae. This
reduction always begins from the molars, but in the insectivorous
forms the incisors may also be affected. Similar transformations
are also experienced by the dental system of the carnivorous
forms of Muridae. The opposite position of high tubercles of the
molars is characteristic of the African carnivorous mice,
Deomyinae. Apart from the carnivorous hamsters, reduction
of molars begins in the pisciverous mice, Hydromyinae (number
,of molars decreases from three to two and even One), and also
in insectivorous mice,.Rhynchomyinae. In Rhynchomys incisors
are also appreciably reduced.
41
М. М. VORONTSOV
Transition from the protein to the cellulose type of nutrition
is connected with the transformation of the function of maxillary
apparatus which tends, henceforth, to copy more and more the
work of the grater in its evolution. The dental system, developing
into the cellulose type of nutrition, loses the tubercular structure
of molars, and manifests significant exposures of the dentinal
fields fringed with the sharp enamel crests, which mutually
intersect while processing cellulose food. The biomechanical
advantage of longitudinal grinding movements of mandible
compared with the transverse movement is shown in Chapter I.
Depending on the prevalence of a particular type of movement,
enamel crests which are always situated across the direction of
the movement of dental rows are arranged accordingly: inthe
longitudinal type of masticatory movements the crests are
arranged longitudinally. This is quite clear from the comparison
of the structure of the teeth close to the family of the Madgascan
Cricetids, Brachyuromys and Brachytarsomys (see Fig. 75, 76).
Muroidea, following the main course of development of
grinding movements of mandible inthe rodents proceeded
through the development of the longitudinal grinding. Adaptation
to longitudinal grinding in the structure of the molars as
correctly noted by Hershkovitz (1955), proceeded in two direc~
tions namely, in the direction of the "terraced" and "plane"
forms of the gnawing surface of teeth (Fig. 12). The terraced
form of gnawing surface characteristic of many forms of Criceti-
dae (Holochilus, Nesomys, Gymnuromys, etc.), restricts the
lateral movements of the mandible by its structure and bio-~
mechanically provides an advantageous longitudinal grinding.
But, many hamsters (Chinchillula, Andinomys, Neotoma, etc.).
specialized in the cellulose type of nutrition and all field voles
(Microtinae) are characterized by having the "plane" form of
gnawing surface. Transformations in the structure of the masti-
catory muscles in field voles hawe made the movements of the
mandible impossible, and in hamsters specialized for the
cellulose type of nutrition, they should be considerably limited
(Vorontsov, 1963b). Prevalence of longitudinal grinding leads
to an increase in the relative length of the dental row and the
number of enamel loops. Ё is not difficult to note that the
increase inthe number of enamel loops, in the Opposite arrange-
ment of the tubercles, must cause a greater elongation of a tooth
42
MOLAR TEETH STR UCT URE
d
Fig.12: Degree of thickening of molars in Cricetidae. After Hershkovitz,
(1955). 1, protocone and protoconid; 3-paracone in the upper and
metaconid in the lower row; (a) scheme of the tuberculate masti-
р catory surface of hamsters; (5) scheme of terraced тл$Нсаюту
surface of hamsters; (с) scheme of thickened masticatory sur -
face \f Cricetidae; (а) terraced masticx.ory surface of the rivht,
upper dental rows of a young hamster, Holochilus magnus Hershk;
(e) thickened masticatory surface of the right, upper dental rows
of the young hamster, Holochilus brasiliensis Desm,
than inthe alternative arrangement; elongation of the dental row
itself cannot have its own limit. Inthe opposite arrangement
of tubercles that form enamel prisms, a greater part of the
longitudinal course of the dental row, seems to have free motion,
when the prism of the upper row is set against the flexus of the
lowér row (and vice versa). In this way, the opposite arrange~
ment of the derivative tubercles, i.e., enamel prisms is not
advantageous biomechanically. Actually, the opposite аггапве-
ment of the enamel prisms from the forms having a *plane®
gnawing surface is found only in hamster, Irenomys and in
field-voles less specialized inthe cellulose ;type of nutrition.
Alternate arrangement of enamel prisms is biochemically
advantageous and from the point of view of evolution it is
characteristic of the majority of herbivorous hamsters and
field-vples.
Three-row arrangement of tubercles in Muridae leads to
fusion of dentinal fields in most of the flat-crowned forms
(Nesokia, Otomyinae) in opposite manner and not in alternative
manner. In other words, absolute specialization to the seed-
eating type of nutrition (three-row arrangement of tubercles)
limits the possibility of transformations of molars, in the flat-
43
N.N.VORONTSOV
crowned shape of tooth biomechanically advantageous to the
cellulose type of nutrition. Maximum specialization in the direc~
tion of alternative arrangement of enamel fields is achieved in
the mice, Eropeplus (see Fig. 83c), whichis very far from those
perfect adaptations of the cellulose type of nutrition, which are
observed in Cricetidae.
Finally, the height of the crown increases with a sharp
increase in the quantity of coarse feed used: from brachydont,
(Cryzomys, Rhipidomys, Cricetus, Mesocricetus, Hesperomys,
etc.) the molars are transformed into mesodont (Neotomodon:
Neotoma, Phyllotis, Andinomys, Fibrini, etc.), and finally
acquire constant growth and become hypsodont (Lemmini,
Microti).
3. Change in the structure of the masticatory surface of
molars with the age, within the groups and between the
groups.
All forms of Cricetidae, at least in the early stages of
growth, have a 2-rowed tuberculate structure of the masticatory
surface of molars. Eventhe young forms of Microtinae retains
the tubercles inthe place of future prisms of molars (Cgnev,
1948, 1950). But the fate of these tubercles is very different
depending onthe type of the masticatory movements. The data
obtained by B.S. Matveev (1963), confirm, that :the number of
layers of the enamel organs of the rats correspond to the number
of tubercles of the adult. This. indicates that the tubercles of
the tooth ef the rodents, Muridae, are evidently not homologous
to the tubercles of the molars of marsupial, insectivorous and
carnivorous forms and thus the terms "protocone", "рагасопей,
"metacone" and so on, derived from the tritubercular theory of
Kopp-Csborn, may be used in relation to the teeth of the rodents
Only conditionally.
The thickness of the enamel layer at the top of the tubercles
is extremely varied in bunodont and brachydont forms. The
enamel layer оп the top of tubercles is very thick in Reithrodon-
tomys, Peromyscus, Rhipidomys and other seed~eating forms of
Cricetidae. Оп Ве other hand, the thickness of the enamel
layer On the top of the tubercles of voles and brachydont hamsters
is not much while the thickness of the enamel layer in the main
44
MOLAR TEETH STRUCTURE
tubercles of these forms is quite considerable. Therefore, the
juvenile tubercles of brachydont forms of Cricetida: wear Out in
the first days of independent nutrition of the animal whereas in
the seed eating hamsters the tubercles are retained for the
greater part of life. Informs with "'terraced'' masticatory
surface (Holochilus, Gymnuromys), -the thickness of the enamel
layer is not uniform in the internal and external sides of the tooth.
On one side the thickness of the enamel layers is at a higher level
than onthe other. As a result of uneven wearing of the juvenile
tubercles from different sides, the masticatory surface may not
have the terraced form.
The bunodont forms also do not have uniformly thick
enamel layers. Tubercles of the upper molars usually have a
thicker layer in the front than in the rear; tubercles of the lower
molars are characterized by a reverse ratio. On the upper and
the lower molars of the bunodont forms, tubercles are covered
by a thicker layer of enamel from the outer side than from the
inner. The difference: inthe thickness of the enamel covering
of tubercles leads to their automz‘ic sharpening as rubbing takes
place against the tuberculous sur’. «es and the tooth is retained in
the grown-up animals.
Young animals always possess relatively higher crown than
the adults of the same species (this, of course, does not concern
forms with real hypsodont tooth). According te the degree of
transition from a protein to a cellulose type of nutrition, the
tooth loses the tuberculous structure and attains a thick gnawing
surface, i.e., attains the characteristic of the adult tooth even
in early stages, or it changes from the brachydont to the Бурзо-
dont type, i.e., retains the characteristic of the young stage,
even in adults as in the animals of original forms. This contra-
diction in the directions of development of the molars (adult
feature while young and vice versa) takes place by a decrease
in the thickness of the enamel layer on the tips of the tubercles
and by the displacement of the juvenile stages of development
of tooth in the more grown up stage.
As expressed by Hooper (1957), the concept about the strict
constancy of the figure of the masticatory surface of the molars
formed by the alternation of enamel and dentinal parts is not
correct. The figure of the masticatory surface of the molar
45
М.М. VORONTSOV
tooth of the grown up animal greatly varies depending оп the
height of the so-called primary and supplementary tubercles
and their connecting crests (Fig.13).
af ve Be) tq eo We ый, i j
Fig.13: Sketch of the possible ways of link of mescstylus with mesoloph
paracone and ie2tacone. After Hooper (1957), with changes and
additions. (a) original state; (b -j) different types of link of
mesostylus with the neighboring loph and cone.
Let us trace the fate of the mesostylus at different combi~
nations of heights surrounding its cones and lophs:-
if the height of the mesoloph is a little less, equal ora
little more thanthe height of the mesostylus and the labial loph
extending from the mesostylus to paracone and metacone then
the mesostylus joins the exposed portion of the axial dentinal area
of tooth on grinding. (See Fig.13,e; for example Reithrodontomys
(Aprodon) tenuirostris, see Fig. 41, а);
if the height of the mesoloph is not only much more than
that of the labial loph extending from mesostylus to paracone
and metacone but also more than the height of the mesostylus
itself, then the mesostylus may remain with the independent
isolated tubercle (see Fig.13,a for example Reithrodontomys
(str. ) fulvescens, see Fig. 41,Ъ);
if the depth of the mesoflexus is much less than the depth
of the paraflexus and the metaflexus then оп grinding the meso~
stylus may merge with paracone (see Fig.13, b,c; for example,
Ichthyomys soderstrtmi, see Fig. 69 a; М! in Scotinomys
teguina, see Fig. 48, a);
if the depth of the mesoflexus from the labial side is tess
than from the medial side, then the mesostylus fusing with
рагасопе unlaces the fossetus covered by enamel i.e., meso-
46
MOLAR TEETH STRUCTURE
fossetus (see Fig.13, u, for example Neacomys spinosus,
Nectomys (s.str.). squamipes, see Fig. 33, 36,c);
if the depth of the metaflexus and the mesoflexus from the
labial side is less than from the medial side, then the mesostylus
joins from the labial side with paracone and matacone unlacing =
mesofossa and metafossa (see Fig.13, h,j; for example Nectomys
(Sigmodontomys) alfari, Scotinomys tequina, see Fig. 36,c, 48).
In individual cases, the flexures of the lingual and the
labial sides may join with each other. The figure of this type
is characterized more by flat-crowned mice (Muridae) and
sacculate rats (Geomyoidea) i.e., forms having a primarily
three~row arrangement of tubercles can algo be found in Criceti-
dae. 5o, in Nesomys rufus (see Fig. 71, a) paraflexus joins with
hy poflexus and in Bachyuromys ramirohitra parafossa joins
with hypoflexus (see Fig. 75а). The metaflexus in Brachytarsomys
albicauda, which is like the molars of the Madagascan field vole
may jOin with the hypoflexus. However, similar flexures extend-
ing across the entire tooth, are по! typical for Cricetidae.
Transformation of the molais from tuberculate to flat-
crowned is definitely associated with the relative thinning of the
enamel layer оп the rudiments of tubercles in the flat-crowned
forms. In field-vole this process attains extreme development.
Obviously the selection should have been in the direction of
elimination of individuals with early developed roots. The entire
variety of the structure of the molars of Cricetidae is connected
with the selection to retain the juvenile surface even On the adult
crown (in seed-eaters) ог to acquire an effaced masticatory gur~
face very early by the young animals while retaining the tall
crown during the whole life. In this way age variability of the
structure of the molars provides vast material for selection in
different directions.
In spite of a large number Of investigations carried out
chiefly on field-voles (Cgnev, 1948, 1950; Zimmermann, 1937,
1958, Stein, 1958, Kratochvil, 1959}, onthe significant range
of variability of molars, the idea about a small intraspecific
variability of the structure of molars still exists in systema~
tics. Meanwhile the intraspecific variability of the structure of
the molars in hamster is very much significant. In some forms,
47
N.N. VORONTSOV
even characteristics such as the presence and absence of вирр-
lementary tubercles vary widely. Thus, in Mesocricetus nowtani,
the mesostylid can exist оп M2, butit might be ina reduced form.
The variations in the figure of masticatory surface of the molars
formed by the differentiation of the enamel and dential fields
are more noticeable. A little more or less height of loph
cOnnecting separate tubercles of molars indifferent species of
Peromyscus gives different figures in different individuals while
grinding (Hooper, 1957).
The figure of the rnasticatory surface of МЗ is particularly
changed because of the fact that, as in field voles, this tooth
takes the least part in the process of crushing food (Voronstsov
1961Ь, 1963d). Small individual distinctions in the manner of
processing food, greater or smaller amplitude of displacement
of mandible and participation of M3 connected with it lead to
different degrees of wearing to the various parts of the tooth
while processing foodmatter causing different figures on the
masticatory surface.
Hooper (1957) in his work, dedicated to the study of
variability of the structure of molars of Peromyscus based on the
detailed study of the structure of the masticatory surface of
teeth in 1877 specimens of this genus, showed that the structure
of the first and second molars of the lower and upper rows
varies very greatly.
Thus in Peromyscus eremicug, the mesostylus is develop-
ed in 63% of the individuals on М1, in 21% on M@ and only in
19% оп M! and М“. Inthe same species the mesostylid is de-
veloped in 13% on Mj] in 6% on М2 but in 5% of individuals on
М, and М2. The mesostylus and the mesostylid are present both
on M! and М] in 7% and оп М2 and М? in less than 2% of the
individuals. Finally, the mesostylus and the mesostylid are
developed both on М} and M2 and М! and М? in less than 2%
animals. Similar data were received for mesoloph and meso-
lophid and hypostylus and hypostylid by Hooper for 17 species of
the genus Peromyscus.
The data of Hooper convincingly speak about the exceptional
range of the intraspecific variability of the structure of the
masticatory surface in small hamsters. Wide intraspecific and
48
MOLAR TEETH STRUCTURE
increasing variability of the structure of molars in field-voles
was convincingly shown by Ognev (1950) and Zejda (1960). These
materials must be applied carefully:to the systematic and
Paleontologic descriptions made exceptionally (or mainly) on
the basis of the morphological study of the dental system of
Single individuals. The materials of Hooper also show exception-
al plasticity of the dental structure which cannot serve-as а base
for the selection of forms with biomechanically advantageous
design Of tooth.
Peculiarities of nutrition and the manner of processing
food matter in different species are reflected to a great degree
оп the structure of the masticatory surface. Even small differ-
ences inthe degree of density and in the composition of food
matter lead to great changes in the form of the masticatory
surface as a result of distinction in the degree and direction of
grinding. Оп {Ве contrary, similarity in the type of nutrition and
in the manner of processing the food matter at he similar initial
plan of the structure leads to surprising example of parallelismSs
in the structure of the dental system.
A comparison of the variability of the dental system both _
between different species and different groups with that of the
organs of the digestive tube shows that the dental system is the
most labile of the organs of the digestive system. This fully
agrees with the principle of greater variability of the exosomatic
than the endosomatic organs observed by А. М. Severtsov. Sucha
variability of the dental system, providing material for differen~
tiation of forms must be applied with great careito the phylogene~
tic construction based chiefly on the morphological study of ;the
molar teeth.
While studying regional materials, many taxonomists did
not investigate the amplitude of the variability of the dental
System inthe whole group, and even introduced into the group
diagnosis the features not at all characteristic of the whole
group. This happened inthe сазе of hamsters; the tuberculate
structure of the molars of the palearctic genera was taken \unlike
flat-crown structure in field-voles) as a distinctive feature of the
this subfamily and introduced into the diagnosés (Vinogradov,
Argiropulo, 1940; Ognev, 1948; Vinogradov, Gromov, 1952).
49.
N.N.VORONTSOV
The structure of the dental system of the herbivorous
hamsters, Neotoma, Xenomys, Nelsonia, Chinchillus, Andino-
mys, Reithrodon, Sigmodon, etc. closely resembles the struc-
ture of molars of the primitive cheek-toothed field-voles belong-
ing to the Fibrini tribe. Adaptive radiation of the Madagascan
Cricetidae, Nesomyinae led to а surprising convergence and
parallelism inthe structure of molars with Other rodents. The
structure of the molars of Macrotarsomys highly resembles that
of Calomyscus; Brachyuromys ramirohitra is so similar to the
African Tachyoryctes by the structure of molars that Ellerman
(1941) and Hooper (1949) brought them to the closely allied
group; molars of EFliurus highly resemble Nesokia, Brachytarso~
mys of the primitive Microtinae, and Gymnurdmys conver gently
resembles Muscardinus by the structure of the molars. From
all these facts we may conclude that while using the data on the
structure of the dental system, for phylogenetic construction,
greatest care and ability to distinguish the cases of adaptive
raciation, parallelism and convergence are needed.
4. Structure of the molar teeth of Cricetidae in connection
with their position inthe system of Muroidea.
Disorderly arrangement of numerous tuberc'!:s of teeth in
the primitive specimens of the family Di» didae (Sicista,
Plesiosminthus~-Dipdoidea), mole-rats (Spalacidae) and bamboo-
rats (Rhizomyidae) is replaced by an orderly two-row (Cricetidae)
ог three-~row (Muridae) arrangement of tubercles in Muroidea.
This process of oligomerization of homologous paris of the tooth
(in a sense, introduced in the concept by V.A. Dogel) goes along
with the reduction of premolars in the same row. It cannot lead
to the reinforcement of masticatory movements of mandible and
to the restriction of its directions that take a very definite
trajectory (movements in the vertical plane while crushing seeds
and, finally, movements in the horizontal plane while processing
cellulose nutrition). This process of differentiation of masti-
catory movements in the same row leads to ‘he division of the
lateral masticatory muscle (M. mass. lateraiis) into three parts.
Orderly arrangement of tubercles (or Ге!” rudiments) and
the differentiation of lateral masticatory muscle are the distinct -
ive characteristics of the group Muroidea. Jhe only feature by
which this largest super family of memmals 5 divided 100 two
50
MOLAR TEETH IN MUROIDEA
main families, - Cricetidae and Muridae - is a two-row or a three~
row arrangement of the tubercles оп molars. A thorough study
of the morphology of hamsters and murines undertaken by us did
not indicate other features for the differentiation of these groups.
It is necessary to establish, whether this characteristic is
principally important, whether it offers a basis for the separation
of these groups as it is done by Vinogradov (1933), Vinogradov
and Arginopulo (1940), Vinogradov and Gromovy (1952), Simpson
(1945), Grasse and Dekeyser (1955) after Milier and Gidley (1918)
or else the large super family of Muroidea should be considered
as monotypic group of Muridae, following Ellerman (1940, 1941),
Ggnev (1948), Heptner (Heptner, Morozova, - Turova, Tsalkin,
1950) and many others.
The opposite arrangement of tubercles of molars in dwarf
gerbils (Gerbillinae) closely resembles those of Murinae as
correctly noticed by Stehlin and Schaub (1950), and in this way,
it is apparently similar to the original structure of the tooth for
the ancestors of murines. Some of the living specimens of
Murinae (Acomys, Steatomys) possess only incomplete set of
tubercles of the supplementary third row when according to
Stehlin and Schaub, the minute state is primary and not associated
with the secondary reduction ofthe supplementary row of the
tubercles.
In Geomyoidea, the three-row arrangement of tubercles on
the masticatory surface of the molars is found like in Murinae
(see Fig. 84a). However, many specimens of that superfamily
(Geomys, Heteromys) acquire flat-crown surface with the transi-
tion to the cellulose type of nutrition when the dentinal fields are
formed by the fusion of three tubercles of one transverse row
(see Fig. 84, b,c) 1.е., in the same way as in flat-crowned
Muridae (Nesokia, Malacomys, etc.).
Thus, the three-row arrangement of tubercles оп the
molars cannot be considered as a feature characteristic of
Muridae only.
Peculiar difficulties for separating Muridae from Cricetidae
are experienced while studying the structure of the molars of
African Ctomyinae. Molars of Ctomyinae are extremely far from
51
N.N.VORONTSOV
Cricetinae and Murinae. Their masticatory surface may 418 -
appear from the teeth of not only Murinae but also Cricetidae
having an opposite arrangement of tubercles which are characteri-~
stic of, say Gerbillinae. Until the study of embryonal 4еуе!ор-
ment of Otomyinae teeth is made the problem of regularity or
irregularity of the division of Muroidea into two large groups -
Muridae and Cricetidae - may not be finally solved. The func~
tional significance of a three~-row structure of teeth in Muridae
is extremely great. This form of the molars is better adapted to
the processing of seed food. Evidently, the biomechanically
advantageous structure of the teeth of Muridae was one of the
important progressive characteristics of this group which resulted
in liberating the muroid hamsters from the temperate and tropi-
cal zones of the Old World.
Оп the other hand, as it was already pointed out the three-
row opposite arrangement of tubercles is less advantageous, in
the transition from tuberculate to flat-crowned molars than the
two-row, alternate arrangement from which the teeth of the
progressive Microtinae are derived.
In this manner, specialization (progressive compared with
Cricetidae) of Muridae teeth for the seed-eating type of nutrition
was a factor which limited the possibility of adaptation of
Muroidea to the herbivorous type of nutrition. Onthe contrary,
the alternate two-row arrangement of tubercles оп the teeth, |
specialized for the seed~-eating type of nutrition of Cricetinae
and more primitive than that of Murinae, was the base from
where the teeth of advanced herbivorous hamsters and field-~-
voles could develop.
Thus, the differences inthe structure of the molar teeth
between Cricetidae and Muridae should be considered as а cha-
racteristic of paramount functional significance and the division
of Muroidea into Cricetidae and Muridae (this view is considered
by the author inthis work) is needed in further studies.
5. Transformation of Molar Teeth in the Phylogenesis
of Cricetidae.
Cligocene Melissiodontinae, whose position in the system
of Muroidea has not yet been explained, possess molars that have
52
TRANSFORMATION OF MOLAR TEETH
an extremely complex structure of masticatory surface. Tuber-
cles are not arranged in rows and their number exceeds the
known number for all real Cricetidae (Fig.14). Numerous tuber-~
cles are not high and the cavities between them are not suffi-
ciently marked which is biomechanically not advantageous. А.Т.
Argiropulo considers that Melissiodon possessed real quadri-
tubercular tooth with highly complicated Supplementary tuber -
cles and crests. Не thus described the structure of the molars
of Malissiodon”.
Fig.14: Structure of the masticatory surface of the molars of Melissiodon
quercyi Schaub. After Stehlin and Schaub (1950).
Right rows: (a) upper; (b) lower. Note the irregular arrangement
of tubercles. ы
"The quandritubercular molars of the mandible have а
nearly uniform length. The crown is divided by the enamel
crests into hollow pits. The connections of the tubercles are
designed in the plan, characteristic of hamsters, but greatly
modified. The unnamed tubercle of the lower first molar
(anteroconid-N.V.) is not long, unilobate or biolobate. The
* Here and hereafter, the description of Oligocene Cricetidae, given by
А.Т. Argiropulo, who was engaged in the study of Paleo tological Crice -
tidae, is cited. "Geological history and basic features of the evolution of
Cricetidae in the tertiary period" - this text within quotation marks are
taken from the incomplete description of Argtropulo, preserved in the
Zoological Institute of Academy of Sciences, USSR.
53
N.N.VORONTSOV
first upper molar is much elongated with a broad bilobate,
unnamed tubercle (exterpocone and interpocene - N.V.)®.
Traces of oligomerization of the number of tubercles and
their arrangement in a proper order are found in the majority
of the Oligocene Cricetidae.
According to Stehlin and Schaub (1950) Paracricetodon
(Fig. 15) known from the Stampa stage of turope is character -
ized by the most primitive structure of teeth. However,
Paracricetodon, and all other members of the Oligocene Crice-
tidae possessed a clearly marked two-row arrangement of
tubercles. Anterocone оп M’ is not divided into two tubercles
and M! has thus, five tubercles. The tubercles have been
arranged oppositely.
Fig.15: Structure of the masticatory surface of the molars of Paracrice-
todon spectabilis Schlosser. After Stehlin and Schaub (1950).
Right rows: (a) upper; (b) lower.
А.Г. Argiropulo observed:
"The specimens of Paracricetodon are, in general, close
to Cricetodon, but have a still more primitive structure of
molars than the oligocene species of Cricetodon, while in the
combination which does not repeat in other forms, the third
54
TRANSFORMATION OF MOLAR TEETH
lower molar is long at the independent posterior branch of
hypoconid. Protocones on M“ and МЗ are with the independent
branch {this branch usually remains connected with protocone
in Cricetodon).
The connecting crest is extremely short. The inner cavity
(bay) is superficial. A clear connection is observed in between
the posterior edgings Of the internal tubercles, (metaconid and
enteroconid}. Thus Paracricetodon stands very far from Cri-
cetodon by the structure of the upper molars than by the structural
features of the lower".
Oligocene specimens of the European genus of Cricetodon -
Cr. collatum Schaub, Cr. gerandianum Gervais and other species
of this genus (Fig.1lo) are also characterized by the opposite
arrangement of tubercles and five-tuberculate M
Fig.16: Structure of the masticatory surface of molars of Oligocene
Cricetodon. After Schaub (1925). Right rows: a, (с) Cricetodon
collatum. Schaub (a)-Upper, (с) lower; 6, d- Cr. gerandianumn
Gervais (b- upper, d- lower); e- Cr, hauberi Schaub (lower row).
А.Т. Argiropulo gives some distinguishing features of all
the forms of Oligocene Cricetodon:
(1) Tubercles of the lingual side (lower-row - N.V.) have
an elongated form, and the middle crests are usually moved
aside from the middle line of molars; (2) the spur of the meso~~™
55
N.N. VORONTSOV
stylid and the posterior branch of protoconid are well developed,
the rear branch of hypoconid is also well developed,in some of the
most ancient forms; (3) anterior supplementary tubercle on M]
(anteroconid-according to terminology - N.V.) has a generally
longitudinal loph; (4) metaconid often lies isolated.
As observed by Argiropulo, Cricetodon from the Stampa stage
have the most primitive structure of molars. From the seven species
of Cricetodon, known from the Stampa Stage "1 гее have developed
rear branches of protoconid, hypoconid and spur of mesostylid, in
these the branch of hypoconid does not develop and only in
Cricetodon huberi Schaub both these branches are not developed".
The structure of molars of Heterocricetodon, that is very dis-~-
tinct from Paracricetodon and especially Cricetodon indicates that
the Cligocene hamsters of Europe were highly represented by various
forms.
The masticatory surface of the molars of Heterocricetodon
(Fig.17) is compressed. The connection of tubercles of molars with
enamel crests is highly complex and somewhat resembles Pseudo-
theridomys in its form; M! has five tubercles. The opposite аггапяе-
ment of tubercles on the molars is retained in this genus.
Fig.17: Structure of the masticatory surface of molars of Heterocrice-
todon helbingi Schaub, After Stehlin and Schaub (1950) Right
rows: (a) upper; (6) lower. :
56
TRANSFORMATION OF MOLAR TEETH
The features of the structure of teeth of Heterocricetodonr
are characterized by А.Г. Argiropulo in the following manner:
"Elements of labial side (maxillary series- N,V.) form
elongated cross folds. Thus, onthe front molar there are six
cross folds formed by unnamed tubercles (anterocone-N.V.),
anterior branch of protocone, tiny crest of protocone (anterior
cigulum-N.V.), spur of mesostylus, crest of metacone and
posterior labial cingulum.
Large sized Cricetops from the upper Oligocene of
Kazakhstan and Mongolia possessed six-tuberculate M! and five-
tuberculate М1 (Fig. 18). The opposite arrangement of well
developed tubercles is very characteristic of this genus.
Fig.18: Structure of the masticatory suxface of molars of Cricetops
dor mitor Matth. at Gronger, After Stehiin and Schaub (1950). _
The posterior branch of protoconid, writes Argiropulo,
is in the form of a rear edging of trigonide and it has the shape of
a false spure of mesoStylid оп Mz and M3. Hypoconid has a
rudiment of the rear branch. The unnamed tubercles on М]
(anteroconid-N. V.) have a very simplified structure, and those
on M! are wide and bilobed (extero-and intero anterocones-N. V.).
According to the details of the structure of molars, Cricetops
stands totally by itself among other forms of Cricetidae, since a
mixture of the sufficiently primitive and more advanced charac-
57
N.N.VORONTSOV
teristics found in the forms of Neogene is discovered. For
example, the formation of a bilobed, unnamed tubercles on м1
(anterocone-N.V.) is never found in Oligocene Cricetidae and
noticed only in a fraction of the forms of Miocene; this feature
fully appears only in Pliocene and in recent forms. At the same
time the unnamed tubercle on М] (anteroconid-N. V.) appears to
be a highly primitive structure as seen in most of the earlier
forms of Cricetodon or in Paracricetodon.
Oligocene forms of Cricetidae of North-America and Asia
have many similarities in the structural plan (Argiropulo, 1940),
Eumys, Leidymys and Scottimus preserve the five-tubercular
structure of М1 and М]. However, Middle Oligocene Eumys is
characterized by well marked tubercular structure of the masti-
catory surface having almost an opposite arrangement of tuber-
cles onthe molars, and in the Middle Oligocene Leidymys this
tuberculation develops further, whereas the greatly compressed
masticatory surface is characterized by Late-Oligocene
Scottimus.
The molars of Eumys (Fig. 19} {в characterized by the
significant development of the supplementary tubercles and crests,
Anterocone is not divided into twotubercles, but from it a short
and high labial crest and a long sloping lingual crest branchs out
aside. Fromthe labial side, the crest, which can be connected
with anteroloph and pinch a small enamel socket, branches out
backwards from anterocone. The main tubercles of teeth are
placed oppositely. Mesostylus is well developed. The marginal
lingual crest connecting protocone and hypocone in such a way
that while grinding vigorously hypoflexus is transformed into
hypofossa, passing through the hypostylus. Posterior cingulum
is very well developed, postflexus goes deep into the body of
tooth. Posterior cingulum of M! and anterior cingulum of м2,
and posterior cingulum of M2 and anterior cingulum M2, and
posterior cingulum of М2 and anterior cingulum of М”, ава
matter of fact, form supplementary transverse rows of tubercles.
Tubercles of labial side of the upper dental row are arranged
notably opposite the lingual side of lower dental labial crest
which passes through hypostylid are well developed. Tubercles of
the lingual row of lower molars are slightly shifted forward with
respect to the tubercles of the labial row.
58
TRANSFORM ATION OF MOLAR TEETH
Fig. 19: Structure of the masticatory surface of molars of Eumys elegans
Leidy (White River, USA, Oligocene, from the collection of V,O.
Kovalevskii; Collection of Geological paleontological Museum
named after А.Р. and М.У. Pavlovs, at MGRI (Moscow Geologi-
cal Prospecting Institute) Orig. Right rows: (a) upper adultus;
(b) lower subabultus,
Upper molars of Scottimus (Fig. 20) retain the opposite
arrangement of tubercles; dentinal fields fuse together on each
side in pairs: the field of protocone with the field of hypocone,
and the field of paracone with the field of metacone; on the other
lower molars of Scottimus the tubercles of lingual and labial rows
are slightly displaced about each other which when the dentinal
fields fuse diagonally set the enamel crest right which passes
from the tubercles of the lingual row to those of the labial row.
Thus the fields of protoconid and enteroconid are connected.
С The structure of the upper molars of Scottimus resembles
the structure of those of the modern Central American hamsters,
Scotinomys; it is analogous to the selendont teeth of hoofed
animals. The shape of Scottinus molars indicates the significant
role of grinding mcvements of the mandible in transverse direc~
tion which is not characteristic of the overwhelming majority of
59
N.N.VORONTSOV
Fig, 20: Structure of the masticatory surface of the molars of Scottimus
lophatus Wood. After Wood (1937), from Stehlin and Schaub (1950)
Right rows: (a) upper; (b) lower.
modern Cricetidae. Similar "inadaptive® trend of specialization
of the dental system in Scottimus seems to us as the "dead end"
of evolution: actually we cannot derive the molars of subsequent
Cricetidae of America including Scotinomys from the teeth of
Scottinus.
Four genera in addition to Cricetops having highly special-~
ized dental system are known in the Upper-Cligocene deposits of
Asia. The most primitive of them by the structure of the dental
system is Eumysodon described from Agispe™ (Aral Sea).
The lower molars of Eumysodon have almost equal length
(Fig. 21), М] is slightly longer than М2 and M3. The crown 18
brachyodont. The masticatory surface is tuberculate (Eum. -
Crlovi Arg. ) or compressed (Eum. spurius Arg.) Anteroconid is
not divided into two tubercles. Anterior cingulum оп М] is
cOnnected with the anteréconid along the lingual side of tooth.
*'The question of the Oligocene Age of the idricoterie fauna of Agispe comes
in for any further proof. The structure of molars of Eumysodon, and
particularly lomys:and РАО 18 extremely peculiar. According to
the morphology of molars these forms are similar to the Miocene Crice -
tidae. According to the unpublished data of Г.К. Glickmann, the deposits
of Agispe may be related even to Middle Miocene. In "'Principles of
Paleontology" (1962) some authors relate the fauna of Agispe to the Late
Oligocene, while others, to the Early Miocene.
60
TR ANSFORM ATION OF MOLAR TEETH
Fig.21: Structure of the masticatory surface of molars of Eumysodon
orlovi Arg. and Eumysodon spuris Arg. Orig. (a) Eumysodon
orlovi Arg. , type, Mz - Му inf. sin., subad. , mirror reflection
(collection of the Institute of Paleontology, Acad, of Sciences,
USSR, №. :210-261 or 210-262, Agispe, Г. Miocene) orig. ;
(b) Eumysodon spurins Arg., type, М] - Mo inf; sin. ad., mirror
reflection (Collection of the Institute of: Paleontology, Acad. of
Sciences, USSR, No. 210-264, Agispe М. Miocene),
Protoflexid is separated by the elevated edge of enamel and
transforms into shallow protofossetid. Postflexid is less deep
than hypoflexid and metaflexid; on M, in Eum. spurius it is closed
into postfossetid. The enamel socket the trigin of which is not
clear, may be left in the dentinal field of hypoconid. Protoconid
grows a branch along the labial edge, and is directed backward,
Mesostylic is developed but оп grinding, it is fused with рага-
conid, pinching the mesoflexid. Inthe opinion of А.Т. Argiropulo
(in litt.) the presence of the branch of protoconid and the spur of
mesostylid at the same time, a characteristic of the lower-
Oligocene Cricetidae, should be considered as very primitive
features whereas the compressed form of the masticatory surface
of molars is the characteristic of the Neogene Cricetidae.
The features for adaptation to the cellulose type of nutrition
are traced back to the structure of the molar teeth of huge forms
61
N.N.VORONTSOV
of Cricetidae, Aralomys (Fig.22), known in the Upper-Cligocene
(?) deposits of the Aral Sea region. The crown is transitional
between brachyodont and mesodont. Anteroconid is not divided
into two tubercles and is poorly developed and lies apart. The
paraconid is isolated from anteraconid as well as from protoconid
fusing with each other by flexure formations of lingual and labial
sides. Hypoconid is exceptionally stretched forward. Сп Mbp,
the anterior cingulum is turned down to the protoconid and has a
well developed outgrowth from the lingual side. Са M3 this out-
growth is fused with the paraconid isolating the parafossetid.
The posterior cingulum is marked оп М} and Mo, its outgrowth
directed forward pinches the postfossetid. The postfossetid is
very shallow, wears off early and the dential field of the posterior
cingulum merges with the dential exposure of metaconid. Diagonal
direction of the enamel crest indicates the significant role of
transverge grinding movements of mandible. As noticed by А. 1.
Argiropulo, "inthe structure of the middle molar, Aralomys
does not even reveal the traces of such elements of archaic
complex structure, which are so common for the Cligocene
forms and partially found in Miocene also.
Fig.22: Structure of the masticatory surface of lower molars of Aralomys
gigas Arg. and Ar. glikmani Vorontz. After Vorontsov (1963 а).
(a) mirror reflection of left My - Mg Ar. glikmani Vorontz? lype
(collection of the Institute of Paleontology, Acad. Sciences, USSR,
No. 1978-1; (b) right My - Mzo0f Ar, gigas Arg., type (Collection
of Institute of Paleontology, Acad, of Sciences, USSR, No. 210-
263, Agispe; Г. Miocene ?
62
TRANSFORMATION OF MOLAR TEETH
Fi;,23: Structure of the masticatory surface of the lower molars of
Argyromys (= "Schaubeumys") aralensis Arg. and Arg.
(= "Schaubeumys"') woodi Arg. Orig, (a) Arg. aralensis Arg.
M1-M2, dext., subad,, type (collection of the Institute of
Paleontology, Асле. of Sciences USSR, No. 210-261 Agispe,
Г. Miocene?); (b) Arg. woodi Arg, М1-М2, sin, mirror reflec -
tion ad., type (collection of Ins. of Pal., Acad. of Sct, USSR),
No. 210-262, Agispe; Г. Miocene ?). ;
Argyromys Schaub ("Schaubeumys" Arg.) (Fig. 23) 4ез-
cribed from the same deposits as the previous genera was charace-
terized by the highly specialized dental system. The masticatory
surface of molars is compressed and the crown is mesodont.
Tubercles on the lower molars are situated alternately, which
leads to the diagonal fusing of dentinal fields. However, the front
dentinal fields were merged oppositely and in Argyromys aralensis
Arg. these were not joined with the tubercles occurring behind.
Anteréconid is shifted nearer to the labial side of the tooth, and
paraconid is greatly moved forward. As a result, a bi-tuberculate
structure of the anterior margin of M,, greatly resembling the
latest hamsters having developed ехёего- and interoanteroconid.
Paraflexid is moved much forward and is situated at the place of
the late developing anteroflexid. The well developed mesostylid
functionally plays the role of the paraconid; the paraconid carries
Out the function of the interoanterOconid, and the anteréconid, that
of the extero-anteroconid. In this way, the structural plan of М)
in Argyromys externally resembles the Neogone Cricetinae having
six-tuberculate М]. But this is similarly convergent, in as much
as the similar structures of the teeth are formed from different
63
N.N.VORONTSOV
rudiments. Са М) the paraconid also is greatly displaced forward
and the anterior cingulum is labially moved; dentinal fields of
these tubercles are arranged oppositely and in Arg. aralensis they
are not cOnnected with the tubercles that lie behind. Arg. Woodi
Arg. is characterized by a more and more compressed masticatory
surface; the postflexid may be closed into the post~-fossetid. Schaub
(1958) observes that the structure of the molars of Argyromys
resembles the structure of the masticatory surface of the Miocene
Anomalomys but Anomalomys possesses a higher crown anda
more compressed masticatory surface with highly developed fusion
of dentinal fields.
The width of the divergence of Cricetidae in the Late
Cligocene is particularly emphasized by the discovery of the strik-
ing Cricetid, Selenomys Matth. et Grand. (Fig. 24) from the
formations of Tatal-Gol in Mongolia, like the North American
Scottimus which lived at the same time and the latest Central
American Scottinomys, the dentinal fields of the upper dental row,
Fie. 24: Structure of the masticatory surface of Selenomys aff. mimicus —
я Matth. el Grand. Orig. (а) upper right row (collection of Inst. of
Paleont, Acad. of Sci. USSR No. 475 -511/3548. a
Mongolia; Olizocene); (b) ‘ower left row, mtrror reflection
(collection of Inst. of Paleon'., Acad. of Sci., USSR No. 475/
3823. Tatal-Gol, Mongolia; Oligocene).
64
TRANSFORMATION OF MOLAR TEETH
merge оп the lingual side and separately оп the labial side, after
which along the middle line or the margin of footh, the exposure
of dentine of the lingual and labial sides can merge with each other.
Аза result, the structure of the upper molars of Selenomys
imitates the selenodont teeth of the hoofed animals. Reduction of
the initial tuberculate structural plan in Selenomys went even
further than in Scottimus. As truly mentioned by Stehlin and
Schaub, (1950), the lower molars of Selenomys are even more
striking than the upper ones. М] has an undivided anteroconid;
the tubercles are arranged alternatively and the dentinal fields
merge diagonally. М> and M3 resemble each other and are dis-
tinct by "selenodont form".
Cn completing the review of the structure of the dental
system of Oligocene Cricetidae, let us mention that by the Late
Cligocene, the Cricetidae of Asia and America have already
achieved a great diversity in the structure of the dental system.
The majority of the forms possesses the tuberculate structure of
the tooth, whereas a number of forms of Cricetidae acquired
clearly a compressed masticatory surface and mesodont crown,
with the transition to a mixed nutrition.
Miocene Cricetidae, show an example of further complication
of the tuberculate structure of tooth, associated with further
specialization to the grain-eating type of nutrition, and the зрес!-
mens losing the tuberculate structure of tooth and gaining the 1оор-
shaped, field-vole like form of the masticatory surface of molars
are found among the Miocene Cricetidae. The compressed masti-~
catory surface of the molars is related to the transition from the
grain~-eating to the mixed type of nutrition and then to the ехсер-
tionally, grain-eating type of nutrition. This is caused by the
significant process of their settling down to land which began in
the Late Miocene.
Both the tendencies in the evolution of the Miocene Cricetidae,
namely further complication of the tuberculate structure of the
tooth and the compression of the masticatory surface of molars,
are well traced among the Miocene specimens of the polytypic
genus, Cricetidon (Fig. 25). Small forms of Cricetidae, Cricetodon
minus Lartet possess a hexatubercular structure of the first up™ :r
molars, but their tubercles have a strictly opposite arranger). tt.
Anteroconid is not divided into two tubercles (see Fig. 7", | +).
65
N.N.VORONTSOV
Structure of the masticatory surface of ‘nolars of Cricetodon.
After Schaub (1925). Right rows: a, g - Criceton haslachense
Schaub (a, МГ, g - M1-M2); В, В - Су. breve Schaub (b-M1,2, в.
М1-3); с, i-Cr. sansaniese Lartet (c-M1-3, }-М1 -з); 4, } - Cr.
gregarium Schaub (а - М1-3, }-М1-з); е, k - Су. minus Lartet
(е — M1-3, k - М1-3); f, 1 = Cr. larteti Schaub (f - M1-3, 1 -M1-3).
66
TRANSFORM ATION OF MOLAR TEETH
The initial stages of the division of anteroconid into two
tubercles - exte госопе and interocone - are observed in Criceto-
don sansaniense Lartet (see Fig.25, c.i.). In this respect Cr.
Sansaniense closely resembles the specimens of the modern sub-
genus Aprodon of North American Reithrodontomys hamsters. The
tendency towards the alternate arrangement of tubercles of tooth is
observed in Cr. sansaniense, as distinct from Cr. minus.
The hexatubercular structure of the upper as well as the
lower molars has a well marked alternate arrangement of tubercles
in Cricetodon gregarium (see Fig. 25, 4, j).
The forms of Cricetodon preserved in Miocene have a
Ppentatubercular first molar. (Cr. breve Schaub, Cr. haslachiense
Schaub and others) acquire alternate arrangement of tubercles of
molars (see Fig. 25, a,b,g,h).
Cricetodon larteti (see Fig.25, f, 1) having an alternate
arrangement of five tubercles on M! experiences a significant
compression of the masticatory surface and a characteristic
Zig -Zag~-shaped structure is formed on merging of the dentinal
fields.
_ Miocene Cricetidae of Hurope, Anomalomys (Fig. 26) already
possessed polyhypsodont (mesodont) crown and a compressed
masticatory surface of molars. The figure of dentinal fields
remotely resembles the modern Madagascan Brachyuromys betsi-
leoensis. Anomalomys, apparently possessed an undivided |
anterocOne and anteroconid and the tubercles of the lingual and
labial sides are appreciably displaced about each other, though not
alternately. Dentinal fields of upper molars get fused and fill the
gap in between forming numerous closed enamel islets. &namel
crests are arranged slantingly indicating the significant develop-
ment of circular movements of the mandible. Tubercles on the
lower molars are slightly displaced about each other. Dentinal
fields on М] and М2? fuse transversally rather than diagonally,
like the fusion of dentinal fields in Meriones, Nesokia and tliurus.
However, owing to the higher and thicker marginal layers of
enamel, pinching of the flexures and flexids and formation of small
enemeled fossettes and fossetids that get locked up within dentinal
fields take place. These make the pattern of the masticatory виг-
face look complicated.
67
N.N.VORONTSOV
Fig. 26: Structure of the masticatory surface of Anomalomys gaudryi
Gaillard. After Stehlin and Schaub (1950). Right rows: (a) upper;
(b) lower.
Primitive zokors, Prosiphneus possessing mesodont prismatic
molars, with a masticatory surface which is similar to that of the
primitive field-voles are also found in the Late Miocene of Asia.
The fauna of hamsters of Pliocene, a period having a special
significance in the evolution of Cricetidae and all Murvidea, соп-
tains specialized specimens of the ancient Oligocene branches a8
well as the young specimens of new, prospering group of Cri-
cetidae.
The Lower Pliocene fauna (the fauna of the hipparion epoch)
contained a large number of Cricetidae having progressive charac-
teristics in the structure of molars, which indicate a further speci-
alization of the cellulose type of nutrition.
The ancient Cricetodontini, which lived up to the Early
Pliocene, include a number of forms in Asia with a compressed
masticatory surface.
Paracricetulus Young retains the most primitive structure
(Fig. 27, а). Anterocone is not divided into two tips and the displace-
ment of tubercles of lingual and labial rows with respect to each
other is not significant. Compression of the masticatory surface
is expressed Only on sufficiently worn out teeth. According to
Schaub (1934) the primitive characteristics in the structure of
molar teeth are also retained by Neocricetodon Schaub.
68
TR ANSFORM ATION OF MOLAR TEETH
Fig,27: Structure of the masticatory surface of molars of the Pliocene
Cricetodontini.. After Schaub (1934). Right rows: (a) Paracrice -
tulus schaubi Young (M1-3); (b,c) Plesiodipus leci Young
(6 - M1-3, с - М2-3). =
Of all forms of Cricetodontini the Farly Pliocene Plesio-~
dipus Young (= Plesiocricetodon Shaub) (See fig. 27,b, с) posses8~
ed a dental system most specialized for cellulose nutrition. The
fusion of dentinal fields of this form of Cricetidae with compressed
masticatory surface takes place diagonally and the alternate
arrangement of tubercles is particularly well expressed on the
lower dental row. The crownis mesodont. Owing to the fusion
of the dentinal fields it is difficult to establish whether antero-
cone has been divided into two tubercles; but, judging from the
insignificant width of the front dentinal field on M!, the extere-
anterOcOne and the interoanterocone if present, would not be
far from each other. The figure of the masticatory surface
resembles that of the zokors and the primitive field-voles.
The Lower-Piocene specimen of the real hamsters of
Sinocricetus Schaub (Fig. 28, a, c) is characterized like all other
hamsters, 1) by paraflexus and metaflexus, which enter deeply
inside the tooth, are directed backwards from the front and
further deepen near the axial line of tooth, and 2) by meso- and
post-flexids which enter deeply into the tooth and are directed
forward from the back. As it gets worn out the elevated margi-~
nal part of these flexures fuse with the dentinal exposures of
69
М. М. VORONTSOV
Fig.28: Structure of the masticatory surface of the molars of Pliocene
Cricetini. Right rows: а, с - Sinocricetus zdanskyi Schaub, after
Schaub (1934) (a - M2, с - Mj~2); а - Nannocricetus mongolicus
Schaub (after Schaub, 1934) (М1 -2); 5-е: - Cricetus kormosi
Schaub (after Schaub, 1939); 6 - M1-3; e - М1-3; f - Lophocricetus
grubachi Schlosser (after Stehlin and Schaub, 1950) (Mj -3).
tubercles and pinch parae and metafossettes, and meso~ and
post-fossetids accordingly. These closed enamel islets are
very typical of Cricetini from Lower Pliocene to this day. The
tubercles onthe upper molars of Sinocricetus are arranged alter~
nately and the dentinal fields fused diagonally. The crown is
brachyodont, and the tuberculate structure of the surface of the
teeth is marked clearly in young mammals. Anterocone has
the traces of breaking into exteroanterocone and interoanterocone.
Nannocricetus, according, to the general structural plan of
molars, closely resembles Sinocricetus. Anterocone 18 sub-
divided into extero- and interoanteroconid. Alternate аггапзе-
ment of tubercle is clearly expressed. The fusion of dentinal
fields has taken place diagonally (see Fig.28, d).
The structure of the molar teeth of Cricetid, Pseudomeri-
ones Schaub (Fig.29,a,b) is peculiar. It is called во because
70
TR ANSFORMATION OF MOLAR TEETH
d
‘Fig. 29: ° The structure of the masticatory surface of molars of Psendomerio-
| nes. Anatolomys and Microtodon, After Schaub (1934). Right rows:
(a,b) Pseudomeriones abbreviatus Teilhard (a - M1-3;6 - М2);
(с) Anatolomys teilhardi Schaub (My -3); (d) Microtodon atovus
Schlosser (M1 -3).
of the close similarity in shape of molars with gerbils. Judging
from the width of the first dentinal field M! had intercone and
exteroanterocone. The tubercles of the upper dental row had
opposite arrangement. Flexures formed transversally but had
no slopes, which are characteristic of the majority of the pre-
sent day forms of Cricetini. Dentinal fields fused into pairs,
connect with each other along the middle line of tooth when
oppositely arranged juvenile tubercles begin to wear out. M3
is poorly developed and the length of M! exceeds the length of
M2 and M3 taken together. The crown is intermediate between
brachydont and ЕЕ The masticatory surface is сопз-
pressed.
Traces of the modern genus Cricetus are also well known
from the Lower Pliocene of Kurope. The early Pliocene form
of Cricetus kormosi Schaub (see Fig. 28, b,e) already possessed
molar teeth which closely resemble the modern specimens of this
genus. Anterocone and anteroconid are distinctly divided 110 `
two tubercles. The tubercles are arranged almost oppositely
but since the diagonal crests are situated higher than the trans-~
verse crests the fusion of dentinal fields in semiadults spread
diagonally. The greater depth of the flexures near the axial
part of the tooth in comparison with the marginal part results
(as they get worn out) in the separation of enamel islets ~-fossette,
surrounded by dentinal fields of oppositely placed tubercles. In
the old individuals with worn out teeth, the enamel islets may
i)!
N.N.VORONTSOV
disappear; dentinal fields of oppositely arranged tubercles fuse
in pairs and they are connected with each Other along the axial
line.
The members of the Karly Pliocene genus - Lophocricetus
were distinguished by brachyodont crown, elongated M+ and
short МЗ, which should be indicative of the prevalence of longi-
tudinally oriented movements of the mandible. The tubercles
of lower molars are placed alternately (see Fig.28, f). The
masticatory surface is compressed. Dentinal fields are fused
diagonally. Flexures are not forming a bend characteristic of
Cricetini. The external edge of the para and the metaflexids
is higher than the internal part; protective islets of enamel 1.е.,
parafossetid and metafossetid can be formed with detrition.
These are arranged quite differently here than in Cricetus owing
to the alternate arrangement of tubercles. The masticatory
surface of Lophocricetus differ from Cricetus by some features
of specialization to the cellulose type of nutrition.
Cricetidae of Anatolomys and Microtodon highly specia~
lized in the structure of the dental system for the cellulose type
of nutritidn existed inthe Karly Pliocene of Mongolia.
Species of Anatolomys (see Fig. 29c) were characterized
by brachyodont crown, compressed masticatory surface of the
molar teeth. Tubercles of lingual and labial sides of the lower
dental row are slightly displaced about each other and the dentinal
fields merge horizontally. M3 has quite a complex shape. The
dental row is elongated and the width of the teeth is much less
than their length.
Farly - Miocene Microtodon (see Fig. 29d) attained further
specialization for the cellulose type of nutrition by having а тево-
dont crown with a compressed masticatory surface On the molar
teeth, similar to the structure of teeth of cheek~-toothed field~
voles of Fibrini. Flexures from the lingual side is appreciably
deeper than those from the labial side. Dentinal fields, similar
to the worn out tubercles are arranged alternately.
In the Early Pliocene layer of North America, along with the
representatives of the ancient forms, .Eumyini-Copemys Macrogna*
thomys НаЙ- and the ancient forms of the modern genus Peramyscus
72
—
ТВ ANSFORMATION OF MOLAR TEETH
Gloger. These forms though differ in their specializations for the
seed-eating type of nutrition, do not substantially differ from the
modern bunodont of the American Cricetinae.
The structure of the masticatory surface of teeth of Middle~
Pliocene North American hamster of Pliotomodon Hoffmeister
(Fig. 30) closely resembles that of the molars of the modern
Central American Scotinomys. The division of anterocone into two
tubercles is well expressed. MDentinal fields of the lingual side
merge with each other and those of the labial side also merge with
each other. Onthe lower molars the tubercles are arranged
alternately and the dentinal field merges diagonally. The enamel
crests of lower molars are arranged diagonally, and almost longie
tudinally On the upper molars. A similar structure indicates the
significant role of transversely oriented masticatory movements
while processing the food.
Fig. 30: Structure of the masticatory surface of molar teeth of Pliotomodon
primitivus Hoffmeister. After Hoffmeister, 1945, from Stehlin
and Schaub (1950), Right rows: (a) M1-3; (b) Mj -3.
The first representatiyes of the advanced forms of the Muri-
dae group distinguished by the three-row arrangement of tubercles
On molars appear in the Early Pliocene of the Old World. These
are Parapodemus Schaub., Anthracomyg Schaub, Progonomys
73
N.N.VORONTSOV
Schaub and later Stephanomys Schaub and other genera. According
to Vorontsov (1960 b), the appearance of mice in the Old World
should have restricted these "radiation possibilities" of the seed-
eating forms of Cricetidae of the Old World.
In Late Pliocene there appear numerous representatives of
the present field-voles (Microtinae)-Synaptomys’Baird, Poamys
Matth., Microtoscoptes Schaub (from the Middle Pliocene),
Pliopotamus Hibbart, Ondatra Link, Neofiber True, Phenacomys
Merriam in North America, Mimomys Major in Palearctic and
Allophajomys Kormos, Lagurus Gloger and Ungaromys Kormos
in Europe. In this period there were a great number of represent-
atives of the modern genera of hamsters: Baiomys True Onycho-
mys Baird, Eligmodontia. Cuv. (Now only in South America),
Sigmodon Say et Ord, Neotoma Say et Ord, and also the fossils
of Parahodomys and Symmetrodontomys. A significant number
of forms of Cricetidae from Late Pliocene already possessed, a
compressed crown. The Cricetida Proreithrodon Ameghino,
belonging to the modern genus Reithrodon according to the data
of Hershkovitz (1955) existed in the Late Pliocene of South America.
Cbviously, in Late Pliocene the hamsters passed from North
America to the South along the then established bridge between the
Nearctic and Neogea Regions. `
The Pleistocene fauna of Cricetidae almost did not have
those genera which continued to live to this day. Transformation
of the dental system of Cricetidae in Pleistocene is closely connect~
ed with the adaptive radiation of Cricetidae in South America and
Madagascar. The dental system of Pleistocene hamsters of the
New World is very different. The bunodont seed~eating forms,
Peromyscus and Reithrodontomys having a highly complex struc-
ture of the masticatory surface and insectivorous forms, Oxymy-
cterus and Blarinomys having primitive opposite arrangement of
tubercles on molars, and forms having masticatory surface adapted
to the cellulose type of nutrition (Phyllotis, Reithrodon and
Holochilus) were represented here.
The ‘Pleistocone Asian representatives of Cricetini namely
Cricetinus (Fig. 3la, c) is almost characterized by the opposite
arrangement of ;tubercles On the upper molars and by alternate
arrangement оп the lower molars. During detrition the closed
74
TRANSFORMATION OF MOLAR TEETH
Fig. 31: Structure of the masticatory surface of the molar teeth of Pleisto-
cene Cricetini - Cricetinus and Allocricetus. After Schaub (1930),
Right rows: (a,c) Cricetinus varians Zdansky (a-M1-3; ¢-M} -3);
(b,d) Allocricetus bursae Schaub (b-M1-3, d-M 1-3).
enamel depressions characteristic of Cricetini are formed on the
upper molars, whereas оп the lower molars similar alveoli are
not formed, while dentinal fields merge diagonally. Ащегосопе is
not divided into two tubercles. Division of anterocoid into two
tubercles so far as itis possible to judge from the figure of highly
worn out tooth, was poorly marked. —
The characteristic features of the present forms of Cricetini
are expressed inthe structure of the teeth of European Pleistocene
hamsters of Allocricetus (see Fig. 3lb, а). Anterocone and
anternconid are divided into two tubercles. The tubercles On the
lower molars are arranged alternately, while the displacement of
the tubercles of lingual and labial rows with respect to each other
On the upper molars is sufficiently feebly expressed. Axial strip
of dentine on lower molars is very much displaced labially in
view of the fact that the lingual dentinal fields are greater than the
labial.
The structure of the molar teeth of the Pleistocene герге-.
sentatives of modern genera will be described in the part, discuss-~
ing the morphology of molars of modern hamsters.
The following principles are observed in the phylogenesis of
the dental system of Cricetinae from Cligocene to Pleistocene. For
the whole period of development of cricetids the dental system of
75
N.N.VORONTSOV
Cricetidae diverged sufficiently widely. From Cligocene to
Pliocene the main trend of specialization of dental system of Cri-~
cetinae was the adaptation to the processing of grains and associated
with this the complication of the tubercles, appearance of supple-~
mentary tubercles (mesostylus, hypostylus, etc.). However, the
forms with compressed masticatory surface, adapted to the сеЦа-
lose type of nutrition, are found among forms of Cricetidae now
in the lower Oligocene.
The grand process of stepping down to land which started in
Late Miocene led to the widening of areas, occupied by grassy-~
steppe associations (combinations) and to the. increase in number
of "niches" of herbivorous animalg. Tropical forests of Paleogene
were excluded from a greater part of the temperate zone of
Holarctic. Similar change would appear to have directed the еуо-
lution of Cricetidae and of course the majority of other groups of
herbivorous mammals, limiting the possibility of divergence of
bunodont seminivorous forms and created favorable conditions for
the emergence and wide radiation of herbivorous rodents having
compressed masticatory surface.
It should be noted that seeds do notinfrequently represent
harder food than some vegetative parts of the plants. The first
Ones are usually processed by rodents having unreduced hard enarnel
coverings of the tooth, while the second ones are processed by
enamel crests, lying onthe soft dentinal base. However, in.view of
the fact that cellulose food has less caloric value than protein,
rodents make use of the vegetative parts of the plants in an 1а-
comparably greater quantity than seeds. The cellulose for the
subsequent masceration and fermentation in stomach and intestine
needs more thorough mechanical processing than protein food. All
this leads to strong abrasion of tooth and in forms where cellulose
nutrition is predominant, the evolution is in the direction of select~
ion of individuals having a higher crown.
Therefore, starting from the second half of Miocene, the
dental system of Cricetidae evolves mainly in the direction of
creation of forms having a compressed masticatory surface, anda
mesodont and even hypsodont crown.
As it was shown above, longitudinal grinding and the соггев-
ponding form of molars characteristic of field-voles are biomecha-~-
76
MOLAR TEETH OF RECENT CRICETIN AE
nically most advantageous for the cellulose type of nutrition.
However, along with this adaptive trend of specialization of molars:
along which the evolution of the majority forms of Cricetidae рго-
ceeds, some genera acquire a pseudo~selencdont form of tooth, in
different periods independent of each other. Permitting the tuber-
culate structure of teeth of the seed-eating form to quickly trans ~
form into a compressed structure it does not seem to be evolution~
ally perspective, and is not concurrent with the forms, possessing
the structure of tooth, which resembles that of the field-voles and,
may be named as 'inadaptive' (in the view of V.O. Kovalevskii).
It should be noted that the only isolated forms of buno-
dont cricetids are left in pleistocene in the Palearctic but the
number of bunodont forms is very great in the New World.
6. Structure of Molar Teeth of Recent Cricetidae.
In Oryzomys (Fig. 32) the dental surfaces in adult indivi-
duals is tuberculate. The division of anterocone into two tuber -
cles is noticed only in young individuals. The thickness of the
enamel layer is not the same: it is more along the edges of the
tooth and less on the internal side of the tubercle. The thick-
ness of enamel is more оп the labial side of the upper molars
than on the lingual side; оп the lower molars the thickness of
enamel is more on the lingual than on the labial side. Sucha
structure leads to a durable preservation of the tuberculate and
then the terraced structure of tooth in adults and even in old
animals. 3
Internal sides of the tubercles are worn out most; the
height of the middle part of the tooth, situated along the axial
line, as well as the height of the tubercles are reduced with
detrition. Cwing to the unequal development of enamel On the
the metacone will be slightly taller than the protocone and the
hypocone, but the paraconid and the metaconid will be taller
than the protoconid and the hypoconid. Since the detrition of
enamel is uneven the dentinal fields are arranged in different
planes. The dentinal fields of the paracone and the metacone
are oriented towards the lingual side and turned back, and rise
much above their base while the dentinal fields of the protocone
and the hypocone are oriented towardg the labial slide and rise
77
N.N.VORONTSOV
very slightly above the base of the tubercles. The dentinal fields
of anterocone are oriented backwards. Accordingly, the dentinal
fields of the рага- and metaconids oriented towards the labial
side, turned towards the front and rise much above the base of
the tubercles, whereas the dentinal fields of protoconid and the
hypoconid are oriented towards the lingual side and irise
insignificantly above the level of the base of the tubercles.
Пе ntinal exposure of the anteroconid rises much above the other
dentinal fields and is oriented backwards.
From the labial side of the upper dental row passes the
marginal crest, which connects the tips of the exteroantero=
cOne, anterior cingulum, paracone, mesostylus, metacone and
posterior cingulum with each other. As the detrition of tooth
goes on, the flexures are pinched by this crest and enciosed in
the dentinal fields of tooth in the form of closed enamel islets.
Depending upon the greater or less height of tubercles and
enamel crest, and the depth of flexure, the latter are pinched
in different periods of time. First, the anteroflexus and the
postflexus are pinched, forming anterofosette the postfossete.
The depth of the postfossette is insignificant, and on further
detrition of tooth, this enamel ‘veolus disappears and the
dentinal fields of metac one and , osterior cingulum merge to-
gether. Further, with detrition the mesoflexus is pinched to
form mesofossette. Later highly deep paraflexus and meta~
flexus are closed to form parafossette and metafossette.
Ename! elevations on the lingual side of protoflexus and hypo-
flexus have a very smaii height. The tubercle on hypoflexus
18 well marked on M~ and М@; it may be патед as hypostylus .
In very old individuais protoflexus and hypoflexus can be
pinched into protofossette and hypofossette.
Unequal depth of parafossette and metafosseite formed
by detrition may result in the division oi these enamel alveoli
into fine, rarely shallow secondary alveoli; their origi» "aay
be traced rarely on highly worn out tooth. On МЗ, foxsettes
of lingual and labial sides may merge with each: othe:
The masticatory surface of М] is highly сотари лее by
the existence of anterofossetid, prosingulofossetid an ntere-
* According to the terminology af Hooper (1957) hyposiyius cov’ ‘aponds to
ectostylus and hypostylid, ectostylid. Our hypolophus correspeds to
endolophus, tut hypolophid, to endolophid.
78
MOLaR TEETH OF RECENT CRICETIN AE
Fig.32: Structure.of the masticatory surface of mouar teeih of Orvzomvs,
Right rows: (a,c) Orig. Отуготуз ($. sir.) couei Alston according
to specimens, from the collection of Institute of Zoology, Acad. Se.
USSR. , No. 38387, Mexico. , Chipas; (6, а) according io Hershkovi«-
{2 (1960) Oryzomys (Oecomys) bicolor Tomes; (a,b) Upper rows: о
(b,d) lower rows.
lophoflexid. Postfossetid and sometimes mesofossetid break
down into two alveoli formed by isolated enamel islets. Nypo-
stylid is well marked both оп М} and M2. Proto- and meta~
flexids which form proto~ and metafossetids are closed lastly.
M3 is not retuced and it is equal in length to M2; M3 is
slightly smaller than М2. The masticatory surface of upper
molars is somewhat inclined outside and that of lower molars»
inside of tooth. Tubercles of up*er and lower molars are
arranged in ап almost opposite manner, but dentinal fields
merge diagonally. Harshkovitz (1960) described the structure
of molars in the subgenus of Оесотуз.
Small hamsters, Neacomys (Fig. 33) are characteriz~
ed by the same structural planas in Gryzomys. They differ
from Oryzomys by a somewhat small size of M3 in compa-~
rison with М2.
The tubercular structure of molars is expressed more
prominantly in specimens of Rhipidomys (Fig. 34) than in Сгу-
zomys. Ежегоащегосопе and interoanterocone, and extero-
79
N.N.VORONTSOV
Fig.33: Structure of the masticatory surface of melars of Neacomys
spinosus Thom. , ad Institute of Zoology 39363. Peru Juliaca.
Upper right row. Orig.
Fig. 34: Structure of the masticatory surface of molars мо mys.
mastacalis Lunid subad,, zool. Museum, MGU №, $ ~ 61073,
Brazil, Orig. Right rows: (a) М1-3; (b) My .3.
and interoanteroconids are well expressed. М” is appr. cia-
bly smaller than M¢; M, is nearly equal to Mz. The general
structural plan ef Rhipidomys very much resembles Cry o-
mys, however flexures close into fossettes much later thanin
Стухотув.
80
MOLAR TEETH OF RECENT CRICETIN AE
The general structural plan of tooth, characteristic of
the group of genera close to Cryzomys, is well expressed
in Thomosomys (Fig.35). #xteroanterocone and interoantero-
cOne are separated from each other for along time. Antero-
flexus is separated into anterofossette later than the арреаг-
ance of parafossette and metafdéssette. Hypostylus is well
developed. &xteroanterocone and interoanterocone come
together but divided by a deep anteroflexid lately closing into
anterofossetid. МЗ is appreciably smaller than М”. M3 is
a bit shorter than М2. Thomasomys is a form having clearly
expressed tubercular structure of brachyodont crown, which
is retained almost throughout the life.
Fig.35: Structure of the masticatory surface of molars of Thomasomys
byrrhonotus. Thoms, ad., Zool. Museum MGU., No. 5 Brazil.
Orig. Right vows: (a) M1-3; (5) My 9.
Judged by the photographs of teeth (Gyldenstolpe, 1932),
Chilomys, Rhagomys, and Phaenomys are related to this
group of genera. All the three genera are characterized by
the tuberculate masticatory surface having strictly opposite
(Phaeconomys) or almost opposite (Chilomys, Rhagomys)
arrangement of tubercles and brachyodont crown. &xtero-
anterocone and interoanterocone are drawn nearer in Chilo-
mys, the distance between exteroanterocone and interoantero-
cOne increases in Phagomys and in Phaenomys they are so
81
М.М. VORON TSOV
much apart from each other as рагасопе is from protocone.
МЗ is smaller than М“ in all the three genera. In Rhagomys
and particularly in Qilomys M? is not very large.
The general structural plan of Nectomys molars may
have been evolved from the bunodont Rhipidomys»s, Thomaso -
mys and Oryzomys. -The tuberculate structure of the teeth in
Nectomys (Fig. 36) is not expressed or rather expressed only
in very young animals, which have not started independent
life. But even such young individuals have dentinal exposures,
joined diagonally (Hershkovitz, 1944). The enamel onthe
labial side of the upper and lingual side of the lower dental
rows és very thick and this leads to the formation of a com-
pressed terraced dental surface. The crown is brachyodont.
In the subgenus Sigmodontomys, even the traces of self-
dependence of exteroanterocOne and interoanterocone are
seen whereas inthe subgenus Nectomys в. str. the ащего-
flexus is closed and changed to anterofossette in the young
individuals. Anteroflexid closing with detrition of the tooth
into anterofossetid is seen in young individual of both the
‘subgenera. The distinctive feature of Nectomys is the
early constriction of flexures (flexures and flexids and Ёог -
mation of numerous closed enameled alveolate fossettes and
fossetids). In this manner a significant increase is obtain-
ed in the length of transversely oriented enamel crests which
intersect themselves during the longitudinal movements of
the mandible and help in grinding cellulose food. Terraced
surface of molars restrict most effectively transverse mOve-
ments of mandible. МЗ 18 much smaller than М2 and parti-
cularly the reduction of M~ is clearly expressed in the sub-~
genus Sigmodontomys. In our opinion (Vorontsov, 1963c),
reduction of МЗ is related to the decrease in the role of this
tooth during the development of longitudinally oriented grind-
ing movements of mandible.
The development of the terraced masticatory surface in
Nectomys, associated with a thicker layer of enamel on the
lingual side of the lower molars and оп the labial side of
upper molars leads to the fact that unlike Cryzomys the рго-
toflexus and hypoflexus, and protoflexid and hypoflexid are
left open for a long time and only in very old individuals they
82
MOLAR TEETH OF RECENT CRICETIN АЕ `
Fig, 36: Structure of the masticatory surface of Nectomys molars. After
Hershkovitz (1944,. Right rows: (a,b,c,g,h) М. ($. str. ат
bes Brants; (d,e,f, 1,8) М (Sigmodontomys) alfari Allen; (a,6,c,@
e, f) Upper rows: g,h, J wer rows; a,g,h,d,j juvents; b,h, ej)
subadults; b, f, adults,
close in the form of fossette. In our opinion, the less promi-
nent movements in comparison with the grinding movements,
must lead to a simplification of the tuberculate structure of the
tooth and this may be associated with the weak development of
hypostylus and hypostylid in Nectomys as compared to Oryzomys.
For the structure and development of the molars of Nectomys you
may also see Hershkovitz (1944).
According to the general structural plan of the molar -<teeth,
the genera discussed above, form а real group, and can be arrang~
ed in the following series according to {Не degree of adaptation to
83
N.N.VORONTSOV
the cellulose type of nutrition: Rhipidomys ~ Thomasosmys -»
О ryzomys > Nectomys.
Bunodont and brachyodont Central American hamsters,
Nyctomys (Fig. 37) have a structural plane of molar teeth thet is
close to Oryzomys. As in Cryzomys the tubercles of lingua! and
labial rows have unequal height. Orientation of dentinal fields of
individual tubercles resembles that in Oryzomys. Unlike the last
genus Nyctomys exteroanterocene and interoanterocene have been
brought together so much that not Only the anteroflexus but even
the anterofossette is not well expressed. Hypsostylid is express-~
ed very well.
Fig,37: Structure of the masticatory surface of molars of Nyctomys
sumichrasti decolorus True Orig, Right rows: (a) upper row;
(6) lower row, According to the specimen from the collection
of Zool Institut, Acad. of Sc. USSR, No. 39371, Central Amertea,
Gonduras, Las Flores,
Considerable height of lingual margin on the upper molars
and labial margin on lower molars leads to the early isolation of
flexures of these sides and to the formation of protofossette and
hypofossette, proto~-fossetid and hypo-fessetid. Tubercles are
arranged almost oppositely, and paracone is somewhat shifted
back with respect to protocone. Unequal! depth of flexures and
flexids leads to the formation of plural fossettes and fossetids.
84
MOLAR TEETH OF RECENT CRICETINAE
Thus, para- and metaflexures give two рага- and metafossettes
each on М! and МР. The intericr space of these closed areas is
oriented in longitudinally stretched islets of enamel. Orientation
of the ename! crests in transverse as well as longitudinal direc-
tion indicates that grinding movementé in this form, obviously,
take place in both transverse and iongitudinal direction.
МЗ is smaller than M“, but it cannot be considered as ге-
duced; M3 15 almost equal to Mj inlength. Osa Mj there is an
anterofossetid, indicating the fact that anter@conid was formed by
two tubercles.
The tuberculate structure of tooth in large-sized brachyodont
of the Central American hamster,. Tylomys* (Fig. 38). M? is,
Fig, 38: Structure of the тазИсшоту surface of Tylomys nudicaudus
Peters. Orig. Right upper row, According to the specimen
from the collection of Zool. Institute, Acad. of Sc., USSR,
No. 1545 Central America, Guatemala, Vera Paz,
even slightly bigger than M*, Exteroanterocone and interoantero~
cOne are divided by a deep fissure-~anteroflexus~-and widely set
apart; the distance between these tubercles is not less than the
distance between paracone and protocone. Tubercles of MI have
a strictly opposite arrangement. Cn M@ and M3, the tubercle of
the lingual row is slightly bent forward compared to that of the
labial row. Merging of dentinal fields takes place diagonally.
Flexures are very deep as a result of which the enameled alveoli
* Only the upper Central ruw of Tylomys wag studied.
85
М.М. УОВОМТ$ОУ
(fossettes) get pinched very late. Hypostylus is well developed.
More thickness of enamel along the edges of tooth and less along
the middle line leads to the situation that while grinding the central
part of tooth grinds quicker than the lateral parts, and thus the
two-row tuberculate structure of tooth is preserved for a long time
even in old forms.
Peromyscus, Baiomys and Reithrodontomys form ап _
independent group well separated from the previous genera by the
structure of the molars. The following are the characteristics in
the structure of the molars of this group:
alternate arrangement of well expressed tubercles;
five-tubercular structure of the first upper and lower molars
(in subgenus Aprodon of the genus Reithrodontomys the antero-~
cOne is divided into two tuberclés).
If the above developed conception on the biomechanical
significance of the tuberculate structure of tooth is considered in
the processing of seeds and food substances similar to them,
then the alternate arrangement of tubercles on molars of this
group should be regarded as an advanced feature, whereas the
undivided anterocone and anterOconid should be considered ав an
ancient feature thus giving evidence of the connections of the
Specimens of this group with Paleogene Cricetidae. Molars are
highly complicated by the formation of supplementary tubercles
(mesostylus and mesostylid, hypostylus and hypostylid, etc.) in
some representatives of this group of genera, paraflexus and
paraflexid, and metaflexus and metaflexid, are generally not
close‘ on the first two molars during the whole life.
The structure of molars is very simple in brachyodont Mexican
hamster, Baiomys (Fig. 39). Here the anterocone is wider than in
Calomyscus and along its front margin appears a shallow groove
which may be taken as anteroflexus. Dentinal exposures of ащфего-
cone in young animals are 8-shaped which gives evidence of the
starting division of anterocone into interoanterocone and ежегоап-
terocone. The posterior cingulum is absent on the upper molars
but mesostylus may be developed. МЗ is reduced to a less
degree than in Calomyseus. Alternate arrangement of tubercles is
well expressed. Anterocone is not. divided into two tubercles.
86
MOLAR TEETH OF RECENT CRICETIN AE
Fig, 39: Structure of the masticatory surface of molars of Baiomys,
After Packard (1960). Right rows: (a,c) B. taylor, Thom;
(5, а) В. musculus Merriam; (a,b) upper rows; c,d lower rows.
Hypostylid may be developed. During detrition, protoflexid, Буро-
flexid and later postflexid may be closed, but because of the
greater height of the tubercles this is only observed in old animals,
For the structure of molars of Baiomys see Packard (1960) also.
In the specimens of polytypic genus Peromyscus (Fig. 40),
the tuberculate structure of tooth becomes further developed.
Anterocone is relatively wide; sometimes along its front surface
there appears a groove, which may be homologized with an out-
growth of anteroflexus. The latter, however, is never closed to
form anterofossete. The closed enamel islets found in some forms
(Peromyscus oaxacensis) in between the dentinal field of ащего-
cOne are derivatives of flexure between anterocone and cingulum
anterior (Prosinguloflexus), prosingulofossette. The supplemen-
tary tubercles and crests connecting them with the main tubercles
of tooth are highly developed. The anterior cingulum is present
not Only on М2 but also on МИ. Mesostylus and hypostylus are often
developed. The posterior cingulum is situated close to metacone
and frequently merges with it. At least, either mesostylus or
hypostylus is positively developed on one of the teeth of the upper
row. Anteroconid is evidently divided into interoanteroconid and
exteroanteroconid. The posterior cingulum 18 always well deve~-
loped оп the first two lower molars. The supplementary tuber-~
cles = mesostylid and hypostylid. = and the crests connecting them
87
N.N.VORONTSVO
a b
Fig, 40: Structure of the masticatory surface of molar teeth of Peromyscus
zarhynchus Merriam. Orig. Right rows. According io the speci-
mens from the collection of Zoology, Insi., Acad., Sc. USSR
Ne. 39363, Mexico State Chiapas Pueblo Nuevo; а - upper row.
b - lower row.
with the axial part of the tooth are often developed. The number
and the degree of development of the supplementary tubercl es and
crests On the upper and lower teeth are extremely changeable
(Hooper, 1957). The thick development of the enamel layer along
the regional zones of the teeth also enables the preservation of
the tuberculate structure of teeth in old individuals. Tubercles of
the upper rew of molars are oriented backward and those of the
lower row forward. At the same time the dentinal exposures оп
the tubercles of the upper row оп labial side are oriented backward
and On lingual side outward and backward. The dentinal fields of
the lower dental row on the labial side are oriented inward and
forward, and those onthe lingual side, backward. МЗ is much
smaller than М2, but it is not во reduced as in the previous genus.
The rudiments of paracone, protocone, metacone and hypocone
and anterior cingulum are traced in M3, Alternate arrangement
of the tubercles is well expressed. See the paper of Hooper (1957)
for intraspecific and intrageneric variability of molars in Pero-
myscus.
The tuberculate structure of the tooth among the genera
discussed attains the highest development in Reithrodontomys es-
88
MOLAR TEETH OF RECENT CRICETIN AE
Fig,41: Structure of the masticatory surface of Reithrodontomys molars,
After Hooper (1952), Right rows: (a) В (Aprodon) tenuirostris,
Merrian b,d В. (5. str.) fulvescens. J. Alien; a,b - upper rows;
c,d - lower rows.
pecially in the subgenus Aprodon. “iolars of Reithrodontomys
(Fig. 41) very much resembles ti... isolars of Peromyscus in
structure, but МЗ and М; are more compiex than in Peromyscus.
Sometimes on МЗ, the paraflexus joins the hypoflexus and grows in
the opposite direction to enable the anterior cingulum merge with
the protocone. The posterior cingulum onthe upper molars is
not generally separated from metacone. Supplementary tubercles-~
mesOstylus and mesostylid, and hypostyius and hypostylid - are
generally well developed, but the crests (mesolophus, hypolophus,
etc.) connecting them with the axial part of tooth develop only in
old individuals.
The teeth of the specimens of the subgenus Aprodon are
highly specialized for the seed-eating type of nutrition. Extero-
anterocOne and interoanterocone are well developed. Supple-
mentary tubercles are excellently developed on upper and lower
molars. The posterior cingulum onthe upper molars is developed
and merges with the metacone only оп considerable detrition of
tooth. Alternate arrangement of tubercles is well expressed in
both the subgenera. For the structure of the molars of Reith-
rodontomys see the paper of Hooper (1952).
89
N.N.VORONTOS
Depending оп the degree of decrease in adaptability of the
dental system to the seed eating type of nutrition the above
described forms can be placed in the following series: Aprodon—
___Reithrodontomys в. str. > Peromyscus > Baiomys.
According to the structure of the molar teeth, Onychomys
(Fig. 42) relates to the described group of genera. Anterocone
is not divided into two tubercles. The posterior cingulum on
the upper molars is developed and it preserves its independence
for a longtime. Alternate arrangement of the tubercles is
poorly expressed, hypocone and metacone have almost an oppo-
site arrangement. The arrangement (almost opposite) of tuber-
cles оп molars facilitates the retention of the prey (Onychomys
has almost exceptionally insectivorous forms, Hall, 1946).
*vidently, Gnychomys acquired the opposite arrangement of the
tubercles for the second time with the secondary transition to
the insectivorous nutrition (it will be discussed in detail). M3
is extremely reduced. Tubercles of the lower molars are
situated somewhat more alternately than the upper. The tuber-
cles of the upper and the lower molars are extraordinarily
high. Supplementary tubercles are not developed generally.
Fig.42: Structure of the masticatory surface of molars of Onychomys _
leucogaster Wied, Orig, Right rows: Based on the specimens from
ithe collection of Zool Museum, MSU, №. S-645480, Canada,
Saskatchewan (a) upper row; (6) lower row.
90
MOLAR TEETH OF RECENT CRICETINAE
The structure of the molars of the forms of the genus
Calomyscus of muroid hamsters (Fig. 43), standing inique in
the system of Cricetinae greatly resembles Onychomys.
Fig. 43: Structure of the masticatory surface of molars of Calomyscus
baluchi. Orig, Right rows: According te specimen from the
collection of Zool, Museum, Mos. St, University Ма S-44255,
Baluchistan, Harboi (a) upper row; (b) lower row.
The teeth of Calomyscus are bunodont, and the crown is
brachyodnot, Anterocone is not divided into two tubercles
and is sufficiently narrow; mesostylus, posterior cingulum
and anterior cingulum are not expressed on Ml, (Absence
of posterior cingulum as it will be shown below, may be relat-
ec to the primary absence of this element as well as to its
inclusion in the composition of metacone). МЗ is highly ге-
duced. Anteroconid is slightly wider than anterocone, but
there is no basis to look for traces of exteroconid and antero-
conid just because it is slightly broader. The posterior cingu~
lum onthe lower molars is developed and mesostylid is not
present. Hypostylus and hypostylid are not marked. МЗ is
bigger than МЗ. Alternate arrangement of the tubercles is
clearly observed оп the upper and the lower molars. The
teeth of Calomyscus has a more compressed structure on bearing
out than those of Peromyscus and Reithrodontomys owing to
91
N.N.VORONTSOV
nearly equal thickness of the enamel on all the sides of the
tubercles. The compressed nature of the tuberculate structure
of molars alternate the arrangement of tubercles and the ear-
lier formation of compressed masticatory surface enable us to
consider the dental system of Calomyscus as less adaptive to
the protein type of nutrition than the other genera of the group
Peromyscus.
The hamsters of the genus Akodon (Fig. 44) are charac-
terized by tuberculate, brachyodont, dental system. Tubercles
are arranged almost oppositely (tubercles of the lingual row
are displaced slightly forward with respect to the tubercles of
the labial row). The posterior cingulum on the upper molars is
not expressed (merged with metacone?). Little thickness of
the enamel layer On the tips of the tubercles leads to a rather
Fig. 44: Structure of the masticatory surface of molars of Akodon arvico-
loides Wagn. Orig. Right rows: According to specimen from t
collection of Zool Mus., Moscow St. University No. S-61072,
Brazil (a) supper row; (b) lower row.
early exposure of dentine. The anterior cingulum, mesosty~
lus and hypostylus are usually developed but merge very early
with the main elements situated in front of them. #£xteroante~
rocone and interoanterocOne are well expressed in young indi-
viduals. &xteroanteroconid and interoanteroconid are brought
together to each other. The posterior cingulum is clearly
visible onthe lower molars. Postflexid is pinched very early
92
MOLAR TEETH OF RECENT CRICETINAE
and forms postfossetid МЗ is reduced, but M3 is not reduced,
and it is not smaller than M2 in length.
The group of genera (Oxymycterus, Lenoxus) related
to Akodon is characterized by a much simplified structure of .
the masticatory surface of molars. This simplification is ге-
lated to the adaptations to the insectivorous type of nutrition.
Adaptations to the gripping movements of mandible lead to
the loss of the multi-tuberculate structure of the tooth, cal-
culated On the prevalence of the crushing movements during
processing of seeds. A comparatively small number of main
tubercles have an opposite arrangement. А very simple вёгас-
ture of the masticatory surface (Fig. 45) is formed in old indivi-
duals during detrition.
a b
Fig.45: structure of the masticatory surfaceof molars of Notineys
negalonyx Waterh, Orig. Right rows:of old individual. According
to the specimen for the collection of the Museum of Natural
History т Paris-Ne. 1882, 2632, Chili (a) upper row; (b) lower row.
The masticatory surface of molars of Lenoxus (Fig. 46) is
sharply tuberculate, and crown brachyodont. The arrangement
of tubercles of the upper dental row is almost opposite, tuber-
cles of lingual row are slightly displaced forward with respect
to the tubercles of the labial row. &xteranterocone and intero-~-
93
N.N.VORONTSOV
Fig.46: Structure of the masticatory surface of molars of Lenoxus
apicalis boliviae. Orig.
апёегосопе are separated from each Other. The posterior cingue-
lum onthe upper molars is not prominent. Mesostylus and
mesolophus are developed. The anterior cingulum оп М1 is
approximated with paracone. Paraflexus and metaflexus are
very deep in their interior part whereas the exterior part of
these flexures are not deep. Therefore parafosette and meta-
fossette, directed longitudinally and arranged along the axial
line of tooth are formed early. M3 is very small. Tubercles
of the lingual row of the upper molars are projected outside, and
of the labial row, inside and backward, kxteroanteroconid and
interoanteroconid are approximated to each other. Hypostylid
and hypolophid, mesostylid and mesolophid are generally well
developed. The posterior cingulum оп lower molars is well
developed. Tubercles of the lingual row is exceptionally high
and their dentinal exposures are directed forward and outside.
Tubercles of the labial row of the lower molars are appreciably
below and their dentinal exposures are turned inside. МЗ is
shorter than M2 but not reduced.
The tuberculate structure of the teeth of Lenoxus almost
excludes the possibility of free mixing of the upper and the
lower dental rows with respect to each other in the horizontal
plane. When the dental rows are interlocked the closely situa-
ted exteroanteroconid and interoanteroconid are arranged in
94
MOLAR TEETH OF REGENT GCRICETIN AE
front of exterOanterOcOne and interoanterocone. Dentinal fields
of the anteroconid*rest against anteroflexus, tall exterocone
enters into protoflexid and short interoanterocone into paraflexid,
‘and во on. Mesoflexid is transformed early into posttussetid at
a very late stage
The structure of the molar teeth of the insectivorous hame
sters of Oxymycte.us (Fig.47) greatly resembles Lenoxus. Une
like Lenoxus the clesed, enamel alveoli of the upper molars
(fossettes) are arranged not along the middle line of the tooth
but somewhat labial:y. M3 is reduced still more than int the
previous genus. Anteroflexid and anteroflexus are not prominent:
a b
Fig. 47: Structure of masticatory surface of molars of Oxymycterus
rosettellatus Wagn. Orig. Right rows of old indtvidual: According .
to the specimen from the collection of Zool. Inst., Acad. of Sc.,
USSR. No. 6936, South America, Bahia (a) upper:row; (b) lower row. |
The extremely original structure of the molar teeth of
Scotinomys (Fig. 48) may be deduced from the structure of the
molars of Lenoxus. The tuberculate structure of tooth in
Scotinomys is marked less strikingly than in the previous two
genera. The crown in mesodont and the area of the dentinal
exposures are significant. Tubercles of the upper molars are
arranged almost oppositely. Interoanterocone is displaced for-
ward with respect to exteroanterocone. Tubercles of the lingual
95
М.М. VORONTSOV
Fig. 48: Structure of the masticatory surface of molars of Scotinomys
teguina trazuJ. Allen. Orig. Right rows: According to the
specimen from the collection of Zool. Inst. Acad, of Sc,', USSR
No. 39365, Central America, Costa Rica, lrazu (a) upper row;
(b) lower row.
and the labial rows are approximated with each other. Anterior
cingulum and mesostylus well developed, hypostylus not present.
Posterior cingulum not developed. Interlocking of enamel crests
nd dentinal exposures that pinch the extremely deep paraflexus
nd metaflexus into parafossette and metafossette take place
along the labial side of the upper molars. These enamel alveoli
are arranged along the axial line of the dental row and para~
fossette acquires the form of a crescent, projecting like little
‘horns’. Aga result a tooth very similar to the selenodont
oth of the hoofed animals is formed. Inthe lower molars
oercles of the lingual row are appreciably displaced forward
with respect to the tubercles of the labial row. Mesofossetid
‚па postfossetid are formed later than the formation of similar
alveoli onthe upper molars, and acquire the shape of a сге-
t appearing as horns inside. Anterior cingulum, mesosty-
11а and posterior cingulum are developed, hypostylid is not
present. Merging of dentinal fields and enamel crests on
lower molars takes place along the lingual side of the dental
row.
The selenodont structure of the dental row often appeared
in the phylogeny of Cricetidae: Scottimus, inthe Oligocene of
North America.
96
MOLAR TEETH OF RECENT CRICETINAE
Salenomys in Oligocene of Mongolia,
Pliotomodon, in Pliocene of North America, which was perhaps
related. to Scottinomys.
The structute of the molar teeth of the selenodont hamsters
indicates the significant role of thé transverse grinding move -
ments, biomechanically not as much advantageous, as the longi-
tudinal grinding movement. Evidently, a small percentage of
the selenodont hamsters is related to this in all the periods of
their geological history. These are dead ends of development
and adaptations to the masticatory systems.
As noticed by Stehlin and Schaub (1950) the structure of the
molars of Mystromys (F ig.49) resembles that of Cricetulus (Tsch-
erskia) trition; but(Vorontsov, 1966), this similarity may not be
Fig.49: Structure of the masticatory surface of molars of Mystromys
albicoudatus Wagn. Orig. Right rows: According to the specimen
from the collection of Zool. Inst. of Acad. of Sc., USSR, No.
39965, Union of South Africa, near Johannesburg (а) upper row;
(5) lower row.
considered as parallelism in the development of molars. Ежего-
anterocOne and interoanterocone are drawn very close to each other.
Tubercles of the lingual row of upper molars, including the intero-
anterocone are slightly shifted forward with respect to the tuber -~
cles of the labial row. Anterior cingulum mesostylus, mesolophus,
97
N.N. VORONTSOV
hypostylus, and hypolophus drawn apart from protocone are fairly
developed. The transverse length of anterolophus, mesolophus
and hypolophus is not much. Posterior cingulum is almost comp-
letely merged with metacone and postflexus is not expressed. Flex-
ures do not close themselves. The characteristic peculiarity of
the lower molars of Mystromys is the strong development of the
anterior cingulum which is directed longitudinally on M,; М” and
M, are fairly well developed. The crown is brachyodont and the
masticatory surface, tuberculate. Dentinal fields merge diagonally
оп detrition. For the structure of molars and family connections
of Mystromys see the other paper by the author (Vorontsov, 1966).
The structure of molars in the present Palearctic hamsters
(Cricetulus, Cricetus, Mesocricetus and Phodopus) can be deduced
from the morphology of molars of Neogene Cricetini-Sinocricetus,
Naunocricetus, and the Miocene specimen of the genus Cricetus.
In all forms of this group antervcone and anteroconid are divided
into two tubercles.
The mutual arrangement of tubercles of molars is very clear
in various species of the genus Cricetulus (Fig. 50). In the sub-
genus Tscherskia the tubercles of the lingual row of the upper molars
molars is slightly shifted forward with respect to the tubercles of
the labial row. The tip of the anterior cingulum joins the рага-
cone and mesostylus with metacone; these enamel crests pinch the
inner part of paraflexus and metaflexus deep into parafossette and
metafossette whereas the external parts of paraflexus and meta-
flexus remain open. The origin of metafossette is complex; it is
formed Only from the deeper inner part of metaflexus but also
from postflexus pinched by enamel labial crests connecting post~-
erior cingulum with metacone. Dential fields of the lingual row of
upper molars have the form of (in the initial stages of detrition)
little 'horns' turned outwards while dentinal fields of labial row
are loop-shaped.
The structure of the lower molars resembles the mirror
image of the structure of the upper molars, but closing of рага-
meso~ and postflexids takes place later than the closing of Йех-
ures in view of their greater depth. Postflexid is deep and wide
and widely separates metaconid from posterior cingulum. The
crecent form of dentinal exposures having its 'horns' directed
98
es
MOLAR TEETH OF RECENT GCRICETIN AE
Fig.50: Structure of ihe masticatory surface of molar teeth of Cricetulus
(Tscherskia) trition de т. Orig,. Right rows: According to the
Specimen from Primorye District, Kazan Region, Kraskino
(a) upper row; (b) lower row. |
inside is characteristic of the labial row, shifted much forward
with respect to tubercles of the lingual row.
Forms of the subgenus, Cricetulus s. str. acquire a сге-
cent form ofthe dentinal fields on the outer and the inner rows
of tubercles. The arrangement of the features of the tubercles
is not strictly opposite. However, because of the peculiarities
of detrition (tubercles of lingual row of upper and labial row of
lower molars are worn Out more from the back, and the tuber-=
cles of the labial row of upper and lingual row of lower molars
are worn Out from the front) dentinal fields of adults are
arranged opposite each other. Рага- and metafossettes are
arranged along the middle line of the row, enamel crests of
these alveoli and also anteroflexus are stretched along the middle
line of molars. A similar orientation of enamel crests indicates
the significant zole of transverse movements of mandible. Post-
erior cingulum is not well marked on upper molars. The teeth
are wide.
The structure of molars of Cricetus (Fig. 51) greatly resem-
bles the structure described above. Anterior cingulum on Mi
99
М.М. VORONTSOV
Fig.51: Structure of the masticatory surface of molar teeth of Cricetus
Cricetus L. Orig. Right rows: (a) upper; (b) lower.
stands very far from exteroanterocone. Рага- and metafossettes
are stretched longitudinally less than in Cricetus migratorius.
Mesostylus and mesolophus are well developed and separate meta-~-
fossette from metaflexus earlier than parafossette. Posterior
cingulum is fairly well developed on wide upper molars. М” is
a little shorter than МА, M3 and M2 are equal inlength. Arrange-
ment of tubercles is almost opposite. Anterior cingulum on М2
has a heel from the lingual side, which is much shorter than
Cricetulus.
Mesocricetus (Fig. 52) can be considered as the last number
of this series. Unlike the previous two genera anteroflexus closes
into anterofossetus, posterior cingulum оп the upper molars is
clearly marked and anterior cingulum оп М” does not have очё-
growths from the lingual side. There may be a small additional
rise to the front from the exteroanterocone. Mesostylid may be
developed on М> and M3. The marginal crest, connecting the
exteroanteroconid with the protoconid and the protoconid with the
hypostylid and the hypoconid may attain considerable height. How-~
ever, fossetids are observed only inold individuals. Arrangement
of tubercles of the upper molars is opposite and that of the lower
molars alternate. The rows of molars are relatively narrow.
190
MOLAR TEETH OF RECENT CRICETN МАЕ
Fig. 52: Structure of the masticatory surface of molars of Mesocricetus
newtoni Nekr, Right upper row. After Stehlin and Schauh (1950).
Molar teeth of Phodopus (Fig. 53), having almost the орро-
site arrangement of tubercles on the upper rows of Mesocricetus,
sharply differ from the teeth of Cricetulus, Cricetus and Мезо-
cricetus by the absence of parafossette and meta-fossette, which
is related to the shallow internal parts of paraflexures and meta-
flexures. Posterior ena on upper molars is hardly. developed.
Anterior cingulum оп М“ gives lingual sprout unlike in Mesocrice-
tus. Opposite fusion of dentinalfields and absence of closed enamel
alveoli of Phodopus are convergently similar to Meriones. By
the structure of the molars members of Phodopus are more adapt-~-
ive to the processing of cellulose food, than Cricetulus, Cricetus
and Mesocricetus and stand by themselves inthis group of genera.
By the degree of adaptability of the structure of teeth to the
cellulose type of nutrition, the modern forms of Cricetini can be
arranged in the following series: Cricetulus -* Cricetus —>
Mesocricetus —» Phodopus.
The structure of molars in Calomys, Eligomodontia, Zygo-
dontomys, Graomys, Phyllotis, Punomys, Irenomys, Chinchillula
and Andinomys is to a great extent, and sometimes, extremely
adapted to the cellulose type of nutrition. Original members of
this series (Colomys) still preserve bunodont teeth having a
brachyodont crown. The general characteristics of the specimens
of the entire group are as follow:
111
N.N. VORONTSOV
Fig.53: Structure of the masticatory surface of molars of Phodopus
sungorus sungorus Pall. Orig. Right rows: According to the
specimen from the neighborhood of Novenskoe village of the
Altai Region. (a) upper row; (b) lower row.
The presence Of exteroanterocone and interoanterOcone at
least in newly-born animals;
the significant reduction of supplementary tubercles and
crests: mesostylus, mesostylid, hypostylus, hypostylid, mesolo-
phus and mesolophid, hypolophus and hypolophid;
the flexures Ml, M4, М and М> (flexures and flexids) do
not usually close into fossettes and fossetids; compressed nature
of the masticatory surface is well expressed;
and the enamel crests are arranged transversally.
The presence of additional tubercles оп M,, situated in bet-
ween exteroanteroconid and protoconid is characteristic of the
structure of the molars in the described group of genera. Accord-
ing to the nomenclature of Hershkovitz (1962) this tubercle is
called the anterolabial stylid. Inthe young individuals of Phyllotis
micropus, Ph. sublimis and Euneomys chinchilloides this tubercle
is situated in amisolated manner. Frequently it is fused with
exteroanteroconid, to form along spur. It runs backwards from
the latter after developing specially in Andinomys, Chinchillula,
Eligmodontia and some forms of Phyllotis (Ph. griseoflavus, Ph.
micropus);
102
MOLAR TEETH OF RECENT CRICETIN АЕ
The structure of molar teeth of Phyllotiini is described by
Hershkovitz (1962).
Molars of Colomys have brachyodont crown with tuber-
culate masticatory surface (Fig. 54). Dentinal exposures in
adults are more poorly developed thanin Phyllotis. Because of
the unequal thickness of the enamel layer оп the external and in-
ternal sides of the tubercles of lingual and labial rows the tuber-
culate structure of tooth is retained not only in young and adult
forms but also in old individuals. Arrangement of tubercles and
dentinal fields on lower molars is strictly alternate, and on the
upper molars it is in between opposite and alternate. The first
molars are longer than the second molars and the second molars
are longer thanthe third. The highly characteristic additional
tubercle situated on М] in between protoconid and exteroantero-
сот usually merges with the latter. Traces of the division of
exterOanterOcOne, interoanterocone, exteroanteroconid and intero-
anteroconid are seen in young individuals.
Fig.54: Structure of the masticatory surjace of malars of Calomys sorrel -
la Thomas Orig. Right rows. According to the specimen from the
collection of Zool, Institute, Acad. ; of Sc., USSR No. 45385, 5,
Peru, Lircay (a) upper row; (b) lower row.
Molars of Hligmodontia (fig. 55) principally resemble Calo-
mys, although the dentinal exposures are slightly better develop-
ed. The spur, which connects the exter oanteroconid with supple-
mentary tubercles and almost closes up with protoconid is very
well developed.
103
М.М. VORONTSOV
Fig.56: Structure of the masticatory surface of the molars of Eligmodon =
tia typus. Е. Cuvier. Orig. Right rows. According to the speci-
men from the collection of Zool. Inst., Acad. of Sc., USSR №.
45375, Argentina; Neuquen Chosmalal (a) upper row; (b) lower
row,
The genus Pseudoryzomys described in 1959 by Hershkovitz
(1962) relates to these genera. Judging from the photographs and
descriptions (Hershkovitz, 1962) the molars of Pseudoryzomys
have clearly expressed tuberculate structure of the masticatory
surface. Tubercles on the upper molars are arranged oppositely
and-on the lower molars tubercles of the lingual row is slightly
displaced forward with respect to the tubercles of the labial
row. The spur highly characteristic of Phyllotini and connect-
ing the exteroanteroconid with the supplementary tubercles of
the lingual side is developed.
The masticatory surface of the molars is compressed in
Zygodontomys (Fig.56). The crownis brachyodont. Dentinal
fields which are derivative of the corresponding tubercles, are
arranged On the upper molars almost oppositely and on the
lower molars the dentinal fields of the lingual row are moved
forward with respect to the dentinal fields of the labial row.
De ntinal fields of exteroanterocone and interoanterocone are
merged with each other and only shallow anteroflexus and
considerable width of the first dentinal field of M! indicate
the differentiation of anterocone into two tubercles. Мево-
stylus on M! and M@ and anterior cingulum on М] are embr-
104
MOLAR TEETH OF RECENT CRICETIN AE
yOnic or in general they are not developed at all. Posterior
cingulum is not prominent (what the last dentinal field of
the labial row - a derivative of only a single metacone or
result of the merging of metacone with posterior cingulum --
гергезепёз cannot be taken for granted without the study of the
tooth development); M3 has two dentinal fields and is shorter
than М2. Mesostylid is poorly marked. Protoflexid on М]
may be closed into protofossetid during detrition. Ащшего-
flexid is not marked and the presence of extero-~and intero-
anterocoOnids can be judged only by the considerable width of
the anteroconid. M3 has two dentinal fields and is a bit
shorter than Mp2.
Fig.56: Structure of the masticatory surface of molare of Zygodonlomys
breicanda thomosi J, Allen. Orig. Right rows. According to
Specimens from the collection of Zoological Institute, Acad, uf
Sci, USSR, No. 45380, Venezuela, Rito Aurare (а) upper row;
(b) lower. row.
The crown is brachyodont and masticatory surface is
compressed in Phyllotig (Fig.57). #mbryonal tubercles have
a very thin layer of enamel on their own tips and so they are
quickly worn out arid become compressed. Thickness of the
enamel layer on the external and internal sides of the tubercles
of the lingual and labial rows is nearly the same. Therefore,
wearing-out conditions are the same for all parts of the tooth,
that retain the same height for a greater part of life. Arrange~
195
N.N. VORONTSOV
Fig.57: Structure of the masticatory surface of molars of Phyllotis
griseoflavus Waterh, Orig. Right rows: According to the speci-
mens from the collection of Zool. Inst., Acad, of Sc., USSR,
No. 45376, Paraguay, Gran Chaco (a) upper row; (b) lower row.
ment of dentinal fielas (tubercles) is almost opposite; on the
upper molars, the tubercles of the labial row, (but on the
lower Ones, those of the lingual row) are shifted forward.
Posterior cingulum onthe upper molars is not well expressed.
Anterior cingulum which often merges with the dentinal field
of рагасопе may be poorly developed on м2.
From the lower molars posterior cingulum may be de-
veloped оп М]. However, owing to the slight depth of post-
flexid it may quite closely fuse with metaconid. Molar teeth
of Phyllotis resemble the structure of the masticatory sur-
face of the less specialized specimens of the cheek-toothed
field-voles (Fibrini Hint.) Prometheomys, etc. Paraflexus and
protoflexus, metaflexus and hypoflexus standing against each
Other are зо close to each other that the portion of the crown
enclosed between them almost fully consists of two enamel
layers, divided by a small strip of dentine. These crosspieces
subdivide dentinal fields which highly resemble the structucture
of molars of the brachyodont field-voles.
The structure of molars in Galenomys (Fig.58) resembles
the structure described for Phyllotis.
106
MOLAR TEETH OF RECENT CRICETIN AE
Fig.58: Structure of the masticatory surface of molars of Galenomys
garleppi Thomas. Right rows. According to the photo of
Hershkovitz (1962) (a) upper row; (b) lower row..
Irenomys (Fig. 59) stands by itself amidst this group of
genera inthe structure of molars. Dentinal fields of the lingual
and labial sides are arranged strictly oppositely on the upper
molars and almost oppositely on the lower ones. Flexures of
the external and the internal sides almost adjoin with each Other-
only a narrow enamel partition separates them. Dentinal spaces
of any subsequent tubercle do practically not join with those of
the previous tubercle. Anterior cingulum and posterior cing.
are not well expressed. tach of the first molars have three
dentinal fields, and each of the second and the third have two
dentinal fields. The masticatory pattern is compressed and the
crown mesodont. The lateral edges of the dentinal field are
sharp. In our opinion the peculiar structure of Irenomys molars,
mostly resembling that of some Gerbillinae molars, does not,
however, give a basis for separation of Irenomys from other
forms of Phyllotini, (Hershkovitz, 1962). The spur on M] con-
necting exterOanteroconid with the arranged supplementary
tubercles in front of protoconid is highly developed in Irenomys.
Reduction of anterior cingulum and posterior cing. is marked
in Chincillula though feebly. In such a manner, the peculiarity
of adaptive evolution of the dental system of Irenomys originating
by imitation of the tooth of gerbils does not give a basis for the
sepazation of the genus Irenomys from the Phyllotini tribe.
107
N.N. VORONTSOV
Fig.59: Structure of the masticatory surface of molars of Irenomys
tarsalis philippi. Orig, Right rows: According to the specimens
from the collection of Zool Inst. of Acad. of Sc. , USSR, №.
45374, Chile, Blanquihue, Peulla (a) upper row; (b) lower row,
By the structure of molars Chinchillula occupies ап inter~-
mediate position between Irenomys and Andinomys. Anterior
cingulum and posterior cingulum are reduced similar to the
genus described above and Chinchillula; but the tubercles of
the lingual and the labial rows are out of line with respect to
each other (Fig.60). The spur moving to М] from exteroantero-
cOnid backward is very much developed and the crown is тево-
dont.
Andinomys (Fig. 61) achieves extreme degrees of adapta-
tion to the cellulose type of nutrition according to the structure
of molars among all Cricetinae (along with Neotoma). The
masticatory surface closely resembles Microtinae. The crown
is mesodont. Dentinal fields that are homologs of tubercles are
arranged alternately, and the dentinal fields merge diagonally.
Flexures are very deep and are so close to each other, that
the part of the crown enclosed between them, consists almost
entirely of two enamel layers divided by anarrow strip of 4еп-
tine. Enamel crests are directed transversally, which gives
evidence of the unusual development of the longitudinal grinding
movements of the mandible. The 'spur' moving to М] from
the exteroanteroconid backwards is very clearly marked. Anter-
ior cingulum and posterior cing. are developed on M2, М] and
108
MOLAR TEETH OF RECENT CRICETINAE
a b
Fig.60: Structure of the masticatory surface of ‘molars of Chinchillula
sahamae Thomas. Orig. Right rows: According to the specimen
from the collection of Zool. Inst; ,. Acad, of Sc, , USSR №.
45372, Peru, Arequipa, Cailloma (a) upper row; (b) lower row,
Fig.61: Structure of the masticatory surface of molars of Andinomys едах.
Thomas. Orig. Right rows. According to the specimen from the
collection of Zool. Inst, Acad. of Sc., USSR, No. 453681 Argenti+
= na, Huhui Province. (a) upper row; (b) lower row.
109
М.М. VORONTSOV
M2. Additional tubercles (ectostylid according to the termino-
logy of Hershkovitz, 1962) may be outlined on М] and M2 in
front of hypoconid. Сп М? anteroconid also merges with the
additional tubercle situated in front of protoconid and also forms
a "spur" directed backwards. The tendency for the formation
of additional tubercles and their merging with main tubercles
very strikingly expressed in Andonomys leads to an increase in
the length of the sectorial enameled crests.
Funeomys (Fig. 62) rather stands by itself from the group
of the genera under consideration. According to the structure of
the masticatory surface of the upper molars and of M2 and M3,
this genus having the same base can be approximated to Phyllotini
and Sigmodontini. The structure of М] is remarkable. An addi-
tional tubercle whichis, however, not connected with exteroantero-
conid by a "spur" but is connected with protoconid is developed in
front of protoconid. Self-dependence of extero-andrinteroantero-~
conids is preserved for a longtime. Their dentinal fields, merg-
ing with each other during the whole life remain isolated from
dentinal fields behind which lie proto- and metaconids. А similar
type of merging of dentinal fields is highly characteristic of the
primitive specimens of gerbils but is not absolutely found among
hamsters having a compressed masticatory surface.
Fig.62: Structure of the masticatory surface of molars of Euneomys =
chinchilloides PetersoniJ. Allen, Orig. Right rows. According
to the specimen from the collection of Zool. Inst., Acad. of Se.,
USSR №. 45369, Chile, Laguna Lazo (a) upper row; (b) lower row.
110
MOLAR TEETH OF RECENT CRICETIN AE
Cnthe whole, for the evolution of the.dental system of the
tribe Phyllotini, adaptibility to the processing of vegetative parts
of plants is characteristic of the majority of its specimens. Accord-
ing to the degree of adaptation of molar teeth to the processing of
cellulose food matter the specimens of the tribe can be arranged in
a following series: Calomys -» Pseudoryzomys -» Eligmodontia —
Galenomys —> Phyllotis > Chinchillula > Andinomys. The genus
Irenomys rather stands by itself, although it is close to Chinchillula.
Euneomys possibly forms an independent group associating РьуПо-
tini with Sigmodontini.
Sigmodon (including Sigmomys), Holochilus, Neotomys and
Reithrodon (including Proreithrodon) form a common group by
the structure of molars. The crown in all the specimens of this
group is brachyodont and the masticatory surface does not have
terraced (Holochilus) or compressed (Sigmodon, Reithrodon and
other genera) tubercles. Exteroanterocone and inter oanterocone
are developed in the newly born, and in individual cases in the
young animals also (Holochilus magnus Hershk). Supplementary
tubercles and crests (mesostylus, mesostylid, hypostylus, hypo-
stylid) are usually not developed. Unlike in Phyllotini flexures
and flexids often close into fossettes and tossetids, at least in
old individuals; it is associated with the rise of the marginal
layer of enamel; during detrition of this the enamel flexures close
into. isolated alveoli. The molars are broad and enamel crests
are frequently quite inclined (Sigmodon), and not directed strictly
transversally as in the majority of Phyllotiini. Flexures are
deeper (this is associated with considerable breadth of tooth as
well as the bending capacity of flexures and flexids), than in the
specimens of Р hyllotiini. By the structure of molars this group
of genera, being included by us in the tribe Sigmodontini is much
more homogenous than Phyllotiini. No member of Sigmodontini,
including Reithrodon does achieve such degrees of specialization
toithe cellulose type of nutrition as Andinomys of the group Phyllo-
tiini. However, among Sigmodontini, forms having tuberculate
masticatory surface are not found as among primitive forms of
Phyllotiini (Colomys, Hligmodontia), and, so a is
considered after Phyllotiini.
Forms of the genus Holochilus (Fig. 63) are characterized
by the terraced form of the masticatory surface. This form
111.
N.N. VORONTSOV
Fig.63: Structure of the masticatory surface of molars of Holochilus.
Right rows. According to the photo о} Hershkovite (1955),
(a,c) H. magnus Thomas; (b,d)'H. brasiliensis Hershk; (a, 6)
upper rows; (c,d) lower rows.
restricts transverse movements of mandible and permits lower
dental rows to move Only longitudinally. This adaptation indicates
a clear specialization of the dental system of Holochilus to the
cellulose type of nutrition. At the same time in Holochilug the
tuberculate structure of molars is expressed not Only in the newly
born but also in those which have started independent life. Denti-
nal fields of the lingual and the labial sides - homologs of the
с оггевропа1 пр tubercles ~ are situated considérably out of line
with respect to each other in H. magnus and arranged alternately
in H. brasiliensis. In H. brasiliensis the dentinal field of meta~
сопе has a protuberance from the labial side indicative of the
development of posterior cingulum, merged with metacone during
detrition. Mesostylus is developed in М7”. Frequently, paraflexus
closes into parafossetes and metafossetes also exists on M~ in H.
brasiliensis. М“? in Holochilus is slightly smaller or equal to М
but is narrowly noticeable.
Molars of Sigmodon (Fig. 64) are characterized Буа сопар-
ressed and not by a terraced form of masticatory surface. Enamel
crests are arranged in an inclined position which indicates the
great role of transverse movements of the mandible. Paraflexus
оп M@ and МЗ, meso-~ and postflexid on М| -Мз in adults and old
individuals, are locked into enamel alveoli (fossetus and fossetid).
112
MOLAR TEETH OF RECENT CRICETINAE
МЗ is slightly shorter and narrower than M@. Arrangement Of the
tubercles is almost opposite but in view of the greater depth and
bending capacity of flexus enamel crests have a significant
length. Inthe structure of molars Sigmodon is much more pri-
mitive than Holochilus, but Sigmodon even when young, loses the
tubercles and acquire a compressed masticatory surface unlike
Holochilus.
Fig.64: Structure of the masticatory surface of molars of Sigmodon ©
hispidus texianus Aud, et Bachm, Orig. Right rows, According
to the specimen from the collection of Zool. Mus, of Moscow St.
University No. S-65644, USA, Kansas (a) upper row; (b) lower
row.
The structure of molars of Reithrodon (Fig. 65) closely
resembles the structure of Sigmodon, but is distinct from it by
the alternate arrangement of dentinal fields - homologs of corres.
ponding tubercles - and nondiagonal arrangement of flexures. In
R. cuniculoides the molars are very wide, flexures have an
arched shape, and on МЗ and М? they close in (in the first ins -
tance from the labial side) the fossetids fairly early. In R.
typicus Waterh., the molars are narrower, flexures and enamel
crests are directed transversally, which indicates the increasing
role of the longitudinally-oriented grinding movements of the
mandible.
113
№.М. VORONTSOV
Fig.65: Structure of the masticatory surface of molars of Reithrouon,
Orig. Right rows: a,c: В. typicus Ищетй. ‚ according to the
specimen of Paris Museum of Natural History, №. 21-22, adull
individual; b,d, R. cunicaloides Waterh, according to the speci-
men of the Paris Museum of Natural History, No. 1883-182.
Older individuals (a,b) upper rows; (c,d) lower rows.
The alternate arrangement of tubercles in the members Of the
genus of Neotomys (Fig. 66) is clearly expressed. Like Holochilus
magnus all species of this genus preserve poorly developed ашего-
flexus, hardly subdividing the dentinal fields of exteroanterocone
and interoanterocone. The flexures and the corresponding enamel
crests are directed transeversally and not slantingly as inSigmodon
and Holochilus, which gives evidence of the increasing role of the
longitudinal grinding movements of the mandible. M3 is longer
than М2. and has a complex shape. Posterior cingulum on МЗ is
very well developed with an outgrowth on the lingual side, having
an almost independent dentinal field.
According to the degree of adaptation of molars to the cellu-
lose type of nutrition, Sigmodontini can be arranged in the follow-
114
MOLAR TEETH OF RECENT CRICETINAE
Fig.66: Structure of the masticatory surface of molars of Neotomys
ebriosus Thom, Right rows. According to the photo of Hershko -
vilz (1955) (a) upper row; (6) lower row.
ing order. Holochilus magnus -> H. brasiliensis —> Sigmodon —
Reithrodon -> Neotomys. The structure of the molars of Sigmo-
dontini has been described inthe paper of Hershkovitz (1955).
North American hamsters belonging to the tribe Neotomini
(Neotomodon, Neotoma, Nelsonia and Xenomys) attain highly per-
fect specializations to the cellulose type of nutrition.
The molars of Neotomodon (Fig. 67) have a compressed
masticatory surface. The crown is intermediate between brachyo-
dont and mesodont. Dentinal fields - homologs of corresponding
tubercles - are arranged alternately. The anterocone is, obviously,
not divided into two tubercles. Additional tubercles and crests are
not develooed. On М! and M@ and on the lower molars flexures
never close and form fossettes and fossetids. Flexures of internal
and external sides do not have a uniform depth: onthe upper molars
the depth of flexures of the lingual side is more than that of the
flexures of the labial side and on the lower molars it.is just орро-
site. The dental system of Neotomodon is not fully specialized for
the cellulose type of nutrition.
The molars of Neotoma, Nelsonia and Xenomys are highly
adapted to the processing of cellulose food. The mdlars of Neotoma
(Fig. 68) and the genera close to it with compressed masticatory
ВТБ
N.N.VORONTSOV
Fig.67: Structure of the masticatory surface of the upper molars of
Neotomodon alstoni Merriam, Right rows, After Hoffmeister
(1945)
Fig.68: Structure of the masticatory surface of molar teeth of Neoloma.
Orig. Right rows: a, dN. lepida Thomas, according to the spect-
men from the collection of Zool. Mus. Moscow St, University,
No. S-60168, USA, Utah State, Tuele b, е N. fuscipes Baird,
according to the specimen from the collection of Zool, Mus.,
Moscou St. University No. S-35352, USA California, Gilroy,
o,f №. albigula Hartley, according to the specimen from the
collection of 2001. Mus., Moscow St. University, №. S-60169,
USA, Arizona (a,b,c) upper rows; (Ч, е, /) lower rows.
116
MOLAR TEETH OF RECENT CRICETIN AE
surface having a prismatic structure are very close to the field-~
voles and zokors. The crown is mesodont, but almost hypsodont
when the rodents are young.
The young and the semi-~adult forms of Neotoma do not have
molars, but the bases of the prisms of molars are closed unlike the
real hypsodont Microtini and in individuals growing old there appear
roots without any special arrangement of maxillary bones. The
development of roots in Neotoma highly resembles Clethrionomys,
and considering the time the roots are laid and the degree of
development of roots, Neotoma is close to the most hypsodont
species of Clethrionomys to Cl. rufocanus. Evidently, Neotoma
and other genera close to it possessed unbroken anterocone. Flex-
ures Of external and internal sides enter deeply towards each other.
Оп the lower molars the dentinal fields of some forms of Neotoma
do not even merge with each other and lie isolated by enamel
constrictions remotely resembling thereby the structure of molars
of Ctomys. Unequal development of flexures and flexids leads to
the fact that the structure of molars of Neotoma convergently
resembles that of Myospalacinae. Dentinal fields of external and
internal sides are arranged alternately. The dental row is stretched.
longitudinally and the majority of enamel crests is directed trans-
versally indicating the prevalence of the longitudinally grinding
movements of the mandible.
By specialization to the cellulose type of nutrition, Neotoma
and the dloser genera resemble the South American hamster -
Andinomys and the most specialized forms of cheek~toothed field
voles (Fibrini). According to the degree of specialization to the
cellulose type of nutrition Neotomini can be arranged in the rv
following order:
INeotoma
Neotomodon | Xe nomys
Nelsonia
In all the above considered tribes of Cricetinae (except
some of Akodontini - Oxymycterus, Lenoxus, Blarinomys) there
was a tendency to the specialization of the dental system to the
cellulose type of nutrition. The adaptation of the dental system
in the piscivorous hamsters from the group Ichthyomyini (Ich-
117
N.N.VORONTSOV
thyomys, Rheomys, Anotomys, Daptomys, Neusticomys) start-
ed in a completely different direction.
Molars of Ichthyomys (Fig.69) compared to hunodont
Cryzomyini, undergo substantial changes: supplementary *
tubercles and crests are reduced and the main tubercles situat-
ed strictly insopposite direction achieve a significant height
in return and are widely placed. Anterocone is divided into
two tubercles. Molars have a significant width; М” is ге-
duced. Аз it has been pointed above, the opposite аггапре-
ment of the widely placed tubercles facilitates retention of the
prey for the force developed by the prey is directed longitudi-
nally forward and the holding tubercles are oriented transver-
sally.
Fig.69: Structure of the masticatory surface of molars of Ichthyomys
soderstromi de Winton. Orig. Right rows of an old individual.
According to the specimen from ti.e Paris Museum of Natural
History, No. 1932-2950. South America, Rio Blanco. Cacao
Cocha (a) upper row; (b) lower row,
The adaptive radiation is very wide in the structure of
the molars of Cricetinae. Within the subfamily almost а
whole variety of dental system characteristic of the entire
Cricetidae family is found: from the brachyodont sharp tuber -
118
MOLAR TEETH OF RECENT CRICETIN AE
culate tooth of зее4-еа пр and predatory hamsters to the
mesodont and almost hypsodont tooth having a compressed
masticatory surface like that of the field vole in herbivorous
hamsters. Depending оп the type of nutrition the bunodont
forms are characterized either by a masticatory surface
complicated by pointed tuberculate teeth with crests having
an alternate arrangement of tubercles (seed-eating Рего-
myscus, Reithrodontomys, etc.) or by one with compressed,
pointed tubercles having an opposite arrangement of tips
(insectivorous Oxymycterus, etc., piscivorous Ichthyomys,
etc.). Finally, the forms having a false selenodont type of
tooth (Scotinomys) appear as an exception among hamsters.
Practically not a single one of the above considered
tribes (except Ichthomyini) possesses a similar structure of
molars, or the same degree of specialization to any type of
nutrition. The features for adaptation to the cellulose type of
nutrition are observed inthe structure of molar teeth of some
forms existing in each of these groups.
Fach of these tribes can be easily characterized by the
tendency and range of variability in the structure of molars
than by the common features of the structure of masticatory
surface.
The variability series of the dental system within each
of these tribes, are the homologous variability series ассог4 -
ing to М.Т. Vavilov (1922).
Usually the members of a more progressive tribe attain
greater degrees of specialization to the cellulose type of nutri-
tion than the last forms of the previous tribes.
In many tribes individual genera occupy the same levels
of specialization to the cellulose type of nutrition and may
possess a very similar structure of molars. Farallelisms in
the structure of molar teeth are characteristic of not only the
members of different tribes of one subfamily but also inthe
forms of various subfamilies.
119
М.М. VORONTSOV
7. Structure of the Molar Teeth of Some Rodents, which
belonged sometimes to Cricetinae (Nesomyinae, Tachyory-
ctinae,Myospalacinae, Lophiomidae, and Platacanthomyinae)
a. Nesomyinae
Сп the basis of the study of the structure of the dental sys
tem of the Madagascan rodents, Stehlin and Schaub (1950) already
showed that tllerman's idea (1940, 1941) of dividing Nesomyi-
nae into five subfamilies had no base. The adaptive radiation of
Nesomyinae went too far and the teeth turned out to be the most
divergent of the organs inthis group. However, a detailed study
of the morphology of molars of Nesomyinae has helped to estab-
lish a single structural planin all members of this striking group
of animals.
The structure of molars of all modern forms of Nesomyi-
nae can be deduced from Macrotarsomys (Fig.70). Molars of
M. bastardi are tuberculate and the crown is brachyodont.
Anterocone is divided into exteroanterocone and interoantero~-
cone (Stehlin and Schaub, 1950, Fig. 257, S.174; see the figure
of teeth of young animals). However, anteroflexure is not deep
and the distance between these tubercles is not great, and with
grinding, their dentinal fields merge early during detrition.
Tubercles of the lingual side of upper molars and the labial
side of lower molars are slightly disposed forward with res-
Pect to opposite sides. The supplementary tubercles and
crests (mesostylus, mesolophus, etc.) are not developed.
Cingulum posterior is Seen on M2 in young individuals. Dur-
ing detrition the dentinal field of the posterior cingulum quickly
‘merges with the dentinal field of metacone. Alternate arrange-
ment of tubercles is clearly expressed onthe lower molars of
М] and M2, which generally have posterior cingulum; other
supplementary formations On lower molars are undeveloped.
M3 and in perticular, МЗ are reduced. The structure of the
molars of Macrotarsomys greatly resembles the structure of
those of Calomyscus Schaub (1934) even inclined to the idea
of close relationship between these two Series; later the same
author (Stehlin and Schaub, 1950) considered resemblance in
the structure of the molars of Macrotarsomys and Calomyscus
120
MOLAR TEETH OF NESOMYIN AE; BTC.
Fig, 70: ` Structure of the masticatory surface of molars of Macrotarosomys
bastardi Milne-Edw. et, Grandidier. Orig. Right rows: According
to the st specimen from the collection of the Paris Museum of
Natural History. No. 1912-134, Madagascar,
as ап example of Convergence: Schaub (Stehlin and Schaub,
1950) pays attention to the resemblance inthe structure of
molars between Macrotarsomys and the Miocene Cricetodon
minus Lartet. However, the division of anterocone into two
tubercles in Cr. minus was already expressed much more dis~
tinctly thanin in Macrotersomys. Similarity in the structure of
molar teeth of Macrotarsomys with the Miocene Cricetodontini
may be interpreted not as an example of convergence but as an
evidence of spontaneous genetic link between these groups. It
should not be forgotten that Madagascar was connected with the
mass of land of the Cld World only in Miocene (Termier H. et
G., 1952; Strakhav, 1948) and, evidently, the migration of
ancient Cricetidae to Madagascar (Vorontsov 1960Ъ) took place
in Pliocene when forms of Cricetodontini were existing in
Europe and Africa.
From the structure of the molars of Macrotarsomys we
find that the molars of Nesomys have a very complicated struc-
ture (Fig.71). The molars are tuberculate and the crown is
121
М. М. VORONTSOV
Е. 71: Structure of the masticatory surface of the molars of Nesomys
rufua Peters. Orig, Right rows. According to the specimen from
the collection of Zool, Mus. , Moscow State U niversity, №.
S-4293, Madagascar, Ampitambe forest, Betsileo (a) upper row:
(b) lower row.
brachyodont. The tubercles of the labial side of the upper and
the lingual side of the lower molars are much taller than the
compressed tubercles of the lingual side of the upper and the
labial side of the lower dental rows. Similar arrangement of
tubercles is as if it is a transition to the "terraced" form of
the masticatory surface characteristic of Gymnuromys. Antero-
cOne and protocone оп M!, and anterior eingulum and protocone
on M2 form a single dentinal field by fusion, paraflexure joins
with hypoflexure which is a characteristic feature of the struc-
ture of the dental system of the majority of Nesomyinae, never
found among the present Cricetinae. Mesostylus and posterior
cingulum are developed on upper molars. Mesoflexure and
postflexure are closed into shallow mesofossete and postfossete.
The structure of the masticatory surface of lower molars of
Nesomys is very complex, Anterior cingulum merges with para~
122
MOLAR TEETH OF NESOMYINAE, ЕТС.
conid, protoflexid joins with mesoflexid very early and then during
detrition they are pinched from the lingual and labial sides, and
form a single closed alveolus, with the fusion of protofossetid with
mesofossetid. Postfossetid is very big and, possibly, this alveolus
appeared not Only from postflexid but also by the constriction of the
deepest part of hypoflexid merged with postflexid. Mesostylid and
mesolophid are developed.
The structure of the front part of M, is exceptionally com-
plex, where there are four closed enamel alveoli in between the
dentinal field formed by anteroconid, protoconid, paraconid and
mesoOstylid. The two posterior alveoli may be homologized as
proto~ and mesofossetids, one of the frontal as parafossetid, and
the other, either as procingulofossetid or as anterofossetid. М” is
not reduced, but its size is less than М2; M3 is nearly equal to M2
and М}. The molars of Nesomys are relatively broad. The struc-
ture of the upper molars of Nesomys is functionally almost the same
as that of the molars of Rhipidomys, Reithrodontomys and other
typically seed-eating American hamsters.
The structure of the masticatory surface is very complicated
in Gymnuromys (Fig. 72) divided by Elterman (1941) into a special
subfamily of Gymnuromyinae. The masticatory surface 18 сопар-
ressed, the crownis mesodont, and the teeth are made of a great
number of frequently isolated plates of enamel having narrow denti-
nal exposures. The masticatory surface is of a terraced type.
Anterocone and protocone on M!, anterior cingulum and protocone
оп М“ and МЗ join to form a single dentinal field, paraflexure is
connected with hypoflexure, and protocone, as in Macrotarsomys
and Nesomys, does not move forward and is opposite to paracone.
Mesostylus, mesolophus and posterior cingulum attain extra- |
ordinary development: the size of the mesostylus-mesolophus
dentinal field is more than the dentinal field of metacone and are
nearly equal to the field of paracone. It is remarkable that while
additional tubercles are highly developed on labial side, the lingual
side remains made up of only protocone and hypocone. On M’, а
labially oriented outgrowth moves away from the paracone; this
outgrowth is a new formation not found in any other form of Cri-
cetidae. OnM! and М2 the flexures are generally closed into
fossettes. МЗ has an extremely complex form and homologization
of its elements is very difficult.
123
М.М. VORONTSOV
Fig.72: Structure of the masticatory surface of molars of Cymnuromys
roberti Е. Major Orig, Right rows. According to the specimen
from the collection of Paris Museum of Natural History No.
1897-538. Madagascar (a) upper row; (b) lower row.
The structure of the lower molars is more complex than the
upper molars. Ашщего- and paraconids оп М], and anterior cingu-
lum and paraconid оп M, and M3 form a horse~shoe shaped denti-
nal field; paraflexid first closes оп М], then оп М2 and later on
М. to form parafossetid. Protoflexid is connected with meso-
flexid and hypoflexid may be connected with postflexid (M), M2
and M3) and also with metaflexid (М2). Similar depressions which
cut the whole tooth transversally and have some inclination back-
ward from the labial edge to the lingual isolate the separate plates
of enamel and dentine. МЗ is not shorter and wider than M2. M3
is longer than М» and Mj. The structure of molars of Grymnuro-
mys adapted to the cellulose type of nutrition retains the common
structural plan of the molars of Nesomys. Functionally, the
dentinal system of Gymnuromys is convergent to the molars of
Muscardinus (Cliroidea) and Ctomys (Ctomyinae, Muridae).
124
MOLAR TEETH OF NESOMYINAE, ETC.
The structure of the molars of Eliurus (Fig. 73) is peculiar.
Flexures of external and internal sides are joined with each other,
the deep transverse hollows intersect teeth, thus separating denti-
nal fields. Tubercles are arranged oppositely and the dentinal
fields are fusedin pairs. The figure of the masticatory surface
highly resembles Nesokia (Murinae). The masticatory surface is
compressed. Homologization of the parts is very difficult. Sepa-
rate plates are formed of posterior cingulum and metacone
Fig.73: Structure of the masticatory surface of molars of Eliurus tanala
Е. Major. Orig. Right rows. According to the specimen from the
collection of Paris Museum of Natural History No. 1932 - 3517,
Madagascar (a) upper row; (b) lower row.
(posterior), Е (middle), exteroanterocone (М1) ог anterior
cingulum (M“ and M? ‚ anterior) from the labial side of the upper
dental row. The origin of the lingual side of the upper row of
plates is not clear; hypocone (rear plate), protocone (middle)
and interoanterocone (front) could take part in its formation. How;
ever, some displacement of the lingual edge of the front plate
and analogy with Nesomys, _4ymnuromys and other Nesomyinae
125
N.N.VORONTSOV
enable us to assume that the ;Вуросопе in general was not taking
any part in the formation of the posterior plate and its lingual
edge was formed by the outgrowth of posterior cingulum; hypocone
was taking part in the formation of the middle plate and protocone
in the formation of the front plate. Thus, according to this
hypothesis the front plate of М! in Eliurus is formed by three
tubercles (exteroanterocone, interoanterocone and protocone).
Postflexure - the only flexure, not connected with flexures
of the opposite side closes very easily into postfossette. The
anterior lobe of M, is cut from the front by a flexid, Homologi-
zation of the parts of the lower molars is difficult. Each of the
lower molars is formed by three transverse plates, enamel
crests as on the upper molars are oriented transversally which
indicates the prevalence of longitudinal movements of the man-
dible.
The change in the dental system in Brachyuromys betsileo-
ensis and Brachyuromys ramirohitra united without special
grounds in one genus, took place in another direction.
The features of the structural plan in Nesomys are still
observed in the structure of the molar teeth of Br. betsileoensis
(Fig. 74) while Br. betsileoensis represents a transitional form
from Nesomys to fo Brachyuromys remirohitra. The masticatory
surface of Br. betsileoensis molars is compressed and the crown
is brachyodont. Flexures of external and internal sides are not
merged with each other. Anterocone and protocone, and paracone
and mesostylus form common dentinal fields. The labial side
flexures are very much inclined to the back; the flexids of the
lingual side are oriented forward. Paraflexure and metaflexure
are closed into fossette with age; para- and metafossettes of M
may fuse with each other; during this the enamel crest of the newly
formed alveolus are oriented longitudinally (Stehlin and Schaub,
1950, Fig. 260). The usual type of the opposite arrangerhent of
flexures (paraflexid-protoflexid, metaflexid-hypoflexid) is
changed in the lower molars on account of the drastic shifting
oftubercles. The first dentinal field of M, is formed by the
fusion of anteroconid with paraconid; protoflexid.is fused with
parafossetid and placed opposite to mesoflexid, and hypoflexid
opposite to postflexid. On M, the anterior lobe is separated by
`
126
MOLAR TEETH OF NESOMYIN AE, ЕТС.
Fig.74: Structure of the masticatory surface of molars of Brachyuromys
betsileoensis Bartl. Orig, Right rows. According to the specimen
from the collection of Paris Museum of Natural History №.
‘45/ 1932. Madagascar (a) upper row; (b) lower row.
a deep flexid of the labial side, whereas on М> the anterior lobe
is separated by a deep flexure of the lingual side formed by the
fusion of mesoflexid with protofossetid; on М. this flexure is
closed into an alveolus having a Mixed origin. Slanting arrange-
ment of crests and the considerable width of molars of Br.
betsileoensis indicate the great specific weight of circular —
(composed of longitudinal and transverse) movements of the
mandible. mM! is shorter than M2, M, is as long as M>.
Further development of the structural plan of the dental
system of Nesomys into that of Br. betsileoensis is observed
inBrachyuromys ramirohitra (Fig. 75). The masticatory surface
is compressed, the crown is mesodont, the molars are excep-
tionally wide and the area of the dentinal fields is very large.
Each mvular tooth has more or less an oval shape and is cut by
slanting deep flexures or closed alveoli. Deep flexures of the
127
М.М. VORONTSOV
b
Fig.75: Structure of the masticatory surface of molars of Perachyuromys
таттоййта. Е. Major from Vorontosov (1963). Right rows,
According to the specinen from the collection of Zool. Inst.,
Moscow St, University No.. S-4299. Madagascar, Ampitambe,
forest, Betsileo (a) upper row; (b) lower row,
lingual side of м! апа М^, across the entire tooth are formed as
a result of the fusion of parafossette with hypoflexus: оп МЗ this
flexure is closed afresh also from the lingual side, forming a
deep enamel alveolus which may be named as parahypofossette.
Metafossette is very deep and intersects the whole tooth. The
lower molars also are intersected by inclined flexures and closed
alveoli, The first closed alveolus is formed by the fusion of
mesofossetid with hypoflexid; on M! this depression is closed
but the post- and hypofossetids contiguous to each other may
remain independent and may not merge into a single alveolus.
Each of the molars is n:arly equal to the other in size and М,
128
MOLAR ТЕБСТН OF NESOMYINAE, ЕТС.
and МЗ are not reduced. Extreme width of the molars, and
inclined (on M3 even longitudinal) disposition of the enamel
crests indicate the unusual development of the grinding movements
of the mandible in transverse direction. The structure of the
molars of Brachyuromys ramirohitra strikingly resembles the
African burrowing form, Tashyoryctes. The problem on the
interrelations of ;these forms will be discussed below.
The development of molars of Brachytarsomys (Fig. 76)
took place in an altogether different direction. Molar teeth in
the members of this genus have a compressed masticatory surface
and the crown is brachyodont. The figure of the masticatory
surface closely resembles field-vole; on the basis of this resemb-
lance, Ellerman (1941) related Brachytarsomys to Microtinae.
Dentinal fields have an alternate arrangement and their fusion
takes place diagonally. Some flexures of the external and the
Fig. 76: Structure of the masticatory surface of molars of Brachytarsomys
albicauda Gunth. from Vorontsov (1963) Right rows. According
to the specimen from the collection of Zool. Mus, , Moscow State
University, №. S-4289, Madagascar, Vinanitelo, Betsileo
(a) upper row; (b) lower row,
Ez9
N.N.VORONTSOV
internal sides are closed, separating the dentinal fields from one
another. Metaflexure on М! and M@ goes up to the lingual side;
on M3 the paraflexure joins with protoflexus and on M, meta-
flexure joins with protoflexid. Similar fusion of flexures of the
opposite sides (and these do not fuse each other as for example,
on Mj) are characteristic of all forms of Nesomyinae and retained
in Brachytarsomys also. Molars are drawn out in length; third
molars are much shorter than second. Enamel crests are orient-
ed transversely thus indicating the prevalence of the longitudinal
movements of the mandible. |
Out of the forms of Nesomyinae, only two (Macrotarsomys
and Nesomys) retain the tuberculate structure of the tooth,
while Gymnuromys, Eliurus, Brachyuromys and Brachytarsomys
acquire compressed masticatory surface adapted to the process -
ing of the cellulose food. However; among the present forms of
Cricetinae adaptation to the cellulose type of nutrition in various
tribes caused the appearance of forms highly similar to the form
of molars of field-voles, whereas among the Madagascar forms
of Nesomyinae only Brachytarsomys has a structure of the molars
similar to that of Microtinae. Thisis perhaps because Nesomyi-
nae represented the only rodents of Madagascar and their un-
limited adaptive radiation, (in Central-America, members of
Cricetinae were represented by a widespread and diverse group,
Hystricomorpha), resulted in the creation of forms, diversely
adapted to the cellulose type of nutrition.
The study of the structure of the dental system shows that
this group is genetically homogeneous and the evolution of the
dental system of the Madagascan Cricetidae can be schematically
illustrated in this way:
Brachyuromys ramirohitra
Comp. Cymnuromys
‘ reas Ellurus 6rachyuromys betsilecersis
Masticatory "4
Brachytorsomys
surface
Tube- WN2somys
= Macrotarsomys
130
MOLAR TEETH OF NESOMYIN AE, ETC.
Cricetinae may not have a different dental system than that
of Nesomyinae. Madagascan Cricetidae are genetically connected
with the ancient Cricetidae-Cricetodontini by the structure of
the teeth.
The main trend of specialization of the dental system of
Nesomyinae, like that of Cricetinae, was a transition from the
bunodont structure of the molars adapted to the cellulose type of
nutrition, to the compressed masticatory surface intersected by
numerous enamelcrests. Such formof molars is adapted to
the cellulose type of nutrition. However, in isolated cases, such
adaptation of teeth to the processing of cellulose food substance
was brought about in а more diverse form than in Cricetinae.
b. Tachyoryctinae
The striking resemblance in the structure of the molars of
Brachyuromys and Tachyoryctes was taken by some taxonomists
for deciding the genetic relationship of these forms. Ellerman
(1941) took Brachyuromys as the Brachyuromys group and related
it to the subfamily of Tachyoryotinae under the family Muridae
(Muroidea), Hooper (1949) related Tachyoryctes to Cricetinae
along with Brachyuromys.,
In fact the resemblance in the structure of Tachyoryctes
(Fig. 77) and Brachyuromys is very close. Tachyoryctes are
characterized by the compressed masticatory surface having a
strong development of dentinal exposures, hypsodont crown, wide
te eth and inclined (especially on upper molars) arrangement of
enamel crests. Each molar is intersected by two pairs of enamel
crests which surround the flexures or enamel alveoli. Marginal
layers of enamel reduce very much in thickness and the main
load falls onthe enamel crests of flexures and fossettes during
grinding of food.
However, as cOnvincingly shown by Stehlin and Schaub,
(1950), molars of Tachyoryctes are not homologous: to those of
Brachyuromys and represent the modification of the structural
plan of Theridomys, while the molars of Brachyuromys can be
traced out inthe structural plan of the teeth of Cricetinae. In
fact, the first de ntinal field of Brachyuromys, arranged in front
т 131
М. М. VORONT SOV
Fig.77: Structure of the masticatory surface of molars of Techyorscles
splendens Rupeel. Right rows: (a,b) according to Monmignaut,
1963; (b, d) Orig. ; (a,c) M1-2 and Mj -2 of a young specimen;
(а, а) upper and lower rows of adult according to the specimen
from the collection of Zool. Inst., Acad. of Sc., USSR, No.
70, -1922, (289). East Africa.
from a deep flexus is formed by anterocune and protocone, where-
аз рагасопе is arranged behind the flexus. In Tachyoryctes the
first-flexure is homologous to the second enamel alveolus of
Brachyuromys, so that the paracone lies in front of this depres-
sion.
The data of Stehlin and Schaub (1950) onthe homology of the
teeth of Tachyoryctes itself are most interesting. These authors
consider that in Tachyoryctes, like in rhizomys, Cannomys and
Spalax, the first molar is premolar, while the second and the
third molars are homologous to M, and M,, the real M3 ( and
M3) being absent. Unfortunately, the authors do not substantiate
this standpoint. If this point of view, is taken then Spalax,
Rhizomys, Cannomys and Tachyoryctes cannot in general be
related to Muroidea. However, the problem on the origin and
homologization of Tachyoryctes cannot be solved without embryo -
logical studies. It is possible that the resemblance in the struc~-
ture of molars of Tachyoryctes and Brachyuromys cannot be
considered as an example of extreme degree of convergence in
132
MOLAR TEETH OF NESOMYINAE, =TC.
the structure of the dental system of specimens of distant groups.
Judging from the figures of Major (1897), the teeth of young
Tachyoryctes are characterized by a disorderly arrangement of
the tubercles. The new data (Monmignaut, 1963) indicate the
two -row arrange ment of tubercles in young Tachyoryctes (Fig.
77). This indication bring themto other members of Cricetidae.
c. Myospalacinae
According to the structure of the molar teeth, zokers‘can
not be considered very different from Cricetinae nor connected
to them. The Miocene mesodont forms of Prosiphneus (Fig.78a)
and the modern hypsodont Myospalax (Fig. 78b) are characterized
Fig.78: Transformation of the dental system of zokors (Myospalacinae)
in phylogenesis from brachyodont to hypsodont. Tlic masticatory
surface of upper molars. Left rows: (a) Prosiphneus Т. le
Chardin (miocene), according to Stehlin and Schaub (1950):
(b) Myospalax psilurus Milne -Edw. (lalest species), Orig.
by the compressed and looped masticatory surface characte ristic
of the specialized Cricetidae and all Microtinae. The molars of
Myospalacinae are undoubtedly of the cricetid type with two -rowed
tubercles.
133
М.М. VORONTSOV
i. Lophiomyidae
The resemblance inthe structure of molars of Lophiomys
with Cricetus and Mesocricetus was the only characteristic, оп
the basis of which Winge (1924) and following him Grasse and
Dekeyser (1955) related Lophiomys (Fig. 79) to Cricetini, the
tribe of the palearctic hamsters. Molars are tuberculate and the
crownis brachyodont. Tubercles have an opposite arrangement.
The remarkable feature of Lophiomys is the possession of supple-
mentary tubercles in front of interoanterocone. Similar seven-
tuberculate structure of the first upper molar is not found in any
of the members of Muroidea. Inother respects the molars of
Lophiomys greatly resemble the teeth of the present palearctic
hamsters especially Mesocricetus, but unlike the latter in
Lophiomys anteroflexus is still not closed and the anterior cingu-
lum on М2 and МЗ has ап outgrowth from the lingual side. Meso-
stylid is not developed. Fossettes and fossetids exist not only on
the upper but also onthe lower teeth. The semilunar form of
dentinal exposures characteristic of Cricetinae is well expressed.
Fig.79: Structure of moiars of Lophiomys imhausi Milne Edw. Mastica-
tory surface of right rows: (a) upper; (b) lower, according to
Ellerman (1940); (с) profile of closed ruws according to Milne -
Edwards (1867).
134
MOLAR TEETH OF NESOMYINAE, ETC.
Resemblance in the structure of the teeth of Lophiomys and
present Cricetini is really very close. Stehlinand Schaub (1950)
consider that the dental system of Lophiomys, related, to the
tribe Lophiomyini of the subfamily of Cricetinae is genetically
linked with the dental system of Cricetini and represent the final
stage of specialization in the series Tscherskia » Cricetus s. str.
+ Cricetus > Mesocricetus = Lophiomys. Though the struc -
ture of the molar teeth of Lophiomys cannot contradict the relation
of Lophiomys to Cricetinae, this singular characteristic cannot be
taken as decisive for the final judgement on the state of Lophiomys
towards hamsters. If the unusual plasticity of the dental system,
its adaptiveness and wide-scale development of the phenomena of
parallelism and convergence, are not taken into account then the
forms such as Andinomys, Neotoma, Brachytarsomys can be
related to field-voles, mice, Eliurus and so on. It is well known
that such mistakes were committed by taxonomists just on the
basis of the study of the structure of only one dental system.
Seventubercules onthe Miof Lophiomys deserve special
cOnsideration. In Mesocricetus there appears а small additional
elevation from the anterior endof M!. However in Mesocricetus,
it is arranged in front of the exteroanterocone, while the addi-
tional tubercles on M! of Lophiomys are associated with intero-
anterocone. These tips are evidently not homologous to each
other and must have appeared independently.
Nothing is yet clear about the Origin of the anterocone.
According to some, the anterior tubercles of M! were formed
from the fusion of the last pseudomolar with the first molar, and
according to the others, the anterior tubercles of M* represent
new formation. Though this problem can be finally solved only
after detailed embryological studies, on the basis of the data
available on the phylogeny of the dental system of hamsters we
tend to support the second point of view.
Actually, the unpaired апёегасопе primarily appears in the
form of a short protuberence On the anterior margin of tooth.
Further it increases in height and then the division of protuberence
into two paired tubercles and the divergence of exter oanterocone
and interoanterocone towards the edges of tooth at the level of
other tubercles are observed. In most of the latest forms of
135
ay
М.М. VORONTSOV
аптегосопе and ежего- and interoanterocone the size is not
smaller than that of the maintubercles, namely, paracone, ргоёо-
cone, metacone and hypocone. It is interesting that in some of
the species, mesostylus undergoes the same fate.as mesolophus:
having appeared inthe form of a small tubercle, mesostylus, ina
few forms (Gymn_iromys), exceeds the size of the main tubercles.
Evidently it also happened with the anterior tubercles of M* (and
M,). . Independent appearance of the seventh tubercle in Lophiomys
and Mesocricetus shows that with the formation of the hexatuber -
culate M! the process of polymerization (according to the concept
of V.A. Dogel, 1954) of the homologous rudiments of tooth is
still not over. The anterior part of М! has been formed by the
inclusion of pseudomolar tooth whereas the species having One,
two or three additional tubercles have already been found among
the various Oligocene forms. Actually the division of anterocone
into two tubercles is met Only among the Neogene, Cricetidae,
and the forms having seventubercles are generally unknown in
fossilized state.
e. Platacanthomyinae
The structure and composition of the molars of Platacan-
thomys and Typhlomys undoubtedly, bring them closer to Criceti-
dae and clearly separate from Muridae. Unlike dormice (dental
formula i +; pm > ут +) pseudomolars are absent in
Platacanthomys and Typhlomys. It should be emphasized that in
a number of dormice the tendency for the reduction of pm’ is not
observed. The origin and homologization of dental parts of
Myoxidae are very difficult to study because of the extreme change
of the masticatory surface by a thick, enamel layer having crests
which do not wear off up to the dentine during the whole life of the
animal. There is no doubt that the peculiar dental system of
Platacanthomyinae cannot be deduced from the structural plan of
the molars of Myoxidae.
As convincingly shown by Stehlin and Schaub (1950), the
depressions intersecting the tooth of Platacanthomys teeth are
not homologous to those of Myoxidae. Molars of Platacanthomyi-
nae can be wholly deduced from the structural plan original to
Cricetidae,
136
MOLAR TEETH OF NESOMYINAE, ETC.
The molars of Platacanthomys (Fig. 80) have much in
common in the structure with the teeth of Gymnuromys: from the
lingual side only interoanterocone, protocone and hypocone are
developed whereas on the labial side there are exteroanterocone,
Paracone, mesostylus with mesolophus, metacone and posterior
cingulum. Hypoflexure is connected with mesoflexure (in Gymnu -
romys hypoflexure is joinéd with paraflexure). As detrition of
primary and secondary tubercles go on, the flexures join with
fossettes and fossetids, situated at some angle. The molars
have a compressed masticatory surface and the crown is brachyo-
dont. МЗ is only a little shorter than М? and well developed. The
structure of the molars of Platacanthomys like those of Gymnu-
romys present an example for solving the biomechanical problem
similar to Myoxidae in the same way, but on the basis of different
rudiments.
Fig.80: Structure of the masticatory surface of molars of Platacanthomys
Right rows. According to E llerman (1940) (a) upper row; (b) lower
row.
The molars of Typhlomys (Fig. 81) high, resemble
Platacanthomys in the arrangement and origin of dentinal fields,
flexures, fossettes, fossetids, etc., compressed nature of the
masticatory surface and the brachyodont state of the crown. How-
ever unlike the previous genus the molars of Typhlomys эге much
narrower but the enamel crests, surrounding the flexures,
ЭТ
М.М. VORONTSOV
Fig. 81: Structure of the masticatory surjace of molars of ТурШотуз.
Right rows. According to Ellerman (1940) (a) upper row; (b)
lower row, -
fossettes, flexids, and fossetids, are highly inclined. Narrowing
of the molars and similar inclination of enamel crests are observed
in the American forms of Napaeozapus (Zapadidae, Dipodoidea).
The case of Brachyuromys, where the almost longitudinal inc lined
position of the enamel crests, is associated with the intensification
of transversely oriented masticatory movements of the mandible,
increase in the width of molars and in the size of МЗ. In
Typhlomys, judging from the structure of molars, the longitudinal
movements of the mandible are prevalent, with the angle of inter-
section of enamel crests of the lower and the upper maxilla nearly
equal to 90° and accordingly МЗ is much shorter than M%
The structure of the molars does not give a basis for the
division of Platacanthomys and Typhlomys into two different
subfamilies, as proposed by Ognev (1947) and followed by Grasse
and Dekeyser (1955). The general structural plan of the molar
teeth of Platacanthomyinae is sharply distinguished from Myoxidae
and has a number of undisputable characteristics of relationship
with Cricetidae.
138
DENT AL SPECIALIS ATION
8. Trends of Dental Specialization of some Primary
‚ Myomorph Rodents. Homologous and Parallel
Variability series in the Dental System of Rodents
It was shown above that the main trend of dental specializa-
tion of Cricetinae (and Nesomyinae close to it) was the trans -
formation of the bunodont masticatory surface into the compressed
surface and the brachyodont crown into the mesodont.
A similar trend of the dental transformation is not charac:
teristic of Some hamsters, but widely spread among all rodents,
particularly Muroidae.
A series of transformation of the tuberculate brachyodont
tooth into hypsodont are established in the phylogenetic as well
as in the comparative -anatomical series.
Among the modern forms of Gerbillinae (Fig. 82) the
genera Gerbillus and Monodia, Taterillus, Taterina, and ~
Desmodilliscus retain the tuberculate structure of the molars,
Meriones are characterized by the compressed masticatory
surface with a brachyodont crown, and finally, Rhombomys
possess not only the compressed masticatory surface but also
the hypsodont crown. However, the opposite arrangement of
tubercles is retained in Meriones and Rhombomys and 50 the
enamel crests are found to be not so long as in Neotoma or in
Mic rotinae.
The old forms of Microtinae already possessed a compress-
ed masticatory surface. Transformation of the dental system
of Microtinae from Miocene till this day went on in the direction
of acquisition of hypsodont crown and increase in the number of
alternately arranged enamel prisms. The series of specializa-~
tion of the dental system of Microtinae for the cellulose type of
nutrition from the Miocene Mimomys to the modern Fibrini,
from Fibrini to Microti, from Fibrini to Lemmini from Clethrio-
‘nomys rutilus to Cl. rufocanus, from Microtus to Laqurus clearly
illustrate this trend of dental specialization of field-voles.
Transformation of the dental system in the phylogenesis _
of Myospalocinae, from the Miocene Prosiphneus to the modern
Myospalax took place in the same direction.
139
DENT AL SPECIALIS ATION
All these series of transformation are based on the two-
row tuberculate structural plan of molars which is common for
all forms of Cricetidae and can be considered as homologous
variability series (from the standpoint of N.I. Vavilov, 1922).
Since the main trend of variability and the original structural
plan is found to be common for individual homologous series,
the structure identical to minute details, of the given organ may
appear to facilitate adaptation to similar functions of the
members of different homologous series, which are situated at
the same stages of specialization. Hence, the teeth of Andinomys:
and Neotoma may be very identical to the teeth of field-voles
and hamsters, but the molars of Meriones are very much similar
to Phodopus. Without taking into account the homologous varia-
bility and the principle of N.I. Vavilov, (this periodic system
in biology) it is very easy to make gross phylogenetic mistakes
during the structural study of an individual organ.
Similar biomechanical problems of adaptation to the
cellulose type of nutrition in other rodents are solved ona
different morphological basis.
The three-row arrangement of tubercles in Muridae is one
of the progressive characteristics compared to those of Criceti-
dae by virtue of which Muridae displaced seed-eating bunodont
hamsters from a greater part of the Old World. The main
direction of specialization of the dental system of Muridae is a
Fig.82: Transformation of the dental system. .of'Gerbillinaé from brachyo -
dont to hypsodont, from sharp tubereutaté to flat -crowned. The
variability direction is homologotws to hamsters, field-voles and
zokors. Upper rows: a-t-structure of the masticatory surface;
j-1 profile of molars (schematically); a,b- according to Grasse
and Dekeyser (1965);.c -f- according to Wettstein ;1917); g-
according to Patter (1959); h-1 Orig. ; a-Gerbillus pyranidum
Geoffr. ; b- Monodia mouritaniae Halm de Balsac; c-_Taleirillus
kadugliensis Wattst. ; d-_Tateina lorenzi Wettst. ; e- Desmodillis -
cus brauneri Wattst. ; f- ~Talera rufa ига Wetts!; g- Tatera sp. from
Mesopotamia; h- Meriones meridianus Pall. According to the
specimen from the coilection of Zool. Mus. Moscow St. Uni-
versity №. S-28046, Turkmenia, Akhcha-Kaima, i- Rhombomys
opinus Licht. According to the specimen from the collection of
2001. Mus., Moscow St. University №. S-52284, Turkmenia,
North-western coast of Kapa Bogaz-Gol Bay, Bik -Tash; j - Gerbi-
Пиз; k- Meriones; 1- Rhombomys.
141
N.N.VORONTSOV
further complication of the tuberculate structure of the tooth.
But individual terminal branches of the widely radiating tree of
Muridae adapted to the cellulose type of nutrition for the second
time. Generally opposite, three-row arrangement of tubercles
led to the formation of a few forms of Muridae with flat-crowned ©
dentinal fields by means of the fusion of transverse rows of
tubercles (Nesokia, Olomys), whereas Cricetidae had usually
alternately arranged enamel fields formed by the diagonal
fusion. Even in Eropeplus, wherein the tubercles of the central
row have greatly shifted forward in relation to lateral rows, the
fusion of dentinal fields takes place in transverse rows and not
diagonally (Fig. 83).
Fig.83: Transformation of the dental.system in Muridae. In connection
with the transition from pr otein-lipoid to cellulose type of nulri-
tion, the masticatory su. rface becomes complex and the small
crust in elevated. Three-row arrangement of tubercles on upper
molars which is not homologous to the two -row structure of
Cricetidae leads to the fusion of all the three tubercles of trans -
verse row and not to the formation of loopshaped tooth of field -
veles. An example of convergence with field voles, Upper rous.
From Vorontsov (1962): (a) Hapalomys longicaudatus ; (b) Nesokia |
indica Gray et Ната; (с) Eropeplus canus; (а) Otomys tropicalis,
In the North-American Heteromyoidea, in which the three-
row arrangement of tubercles appears regardless of Muridae,
the compressed nature of the masticatory surface and the
formation of hypsodont molars in the series from Perognathus
to Heteromys and Geomys leads to the fusion of dentinal exposur-
es of the tubercles (Fig. 84).
142
DENTAL SPECIALIS ATION
Fig. 84: Dental transformation т а number of forms of Geomyodea:
‘Three -row arrangement of tubercles (convergence with mice)
corresponds to the seed -eating type of nutrition; the masticatory
surface is flattened the crown rises and enameled crests are
oriented transversely during the transition to the cellulose type
of nutrition. Upper rows. According to Grosse and Dekeyser
(1955) from Vorontsov (1962 b). (a) Perognathus; (b) Heteromys;
(c) Geomys. ;
The same tendency for flattening of the masticatory sur-
face and elevation of the crown in view of the transition from the
protein to the cellulose type of nutrition is observed in the series
of Dipodoidea (Fig. 85) from Sic ista to Zapus Napaeozapus,
Allactaga and Alactag ulus. Disorderly arrangement of tubercles
in Dipodoidea would appear close to the two-row arrangement of
tubercles of Cricetidae because of which the structure of molars
of the mesodont jerboas closely resembles the structure of the
molars of Cricetidae.
The teeth of Myoxidae (Fig. 86) are transformed on an
altogether different basis. Even the least specialized forms of
the modern Myoxidae possess a very thick layer of enamel on
_the surface of molars, complicated by transverse enamel
"owers".. The specialization of molar teeth of Myoxidae to the
cellulose type of nutrition in the series from Myomimus,
Eliomys and Dyromys to Glis and Muscardinus is marked by an
increase inithe number of transverse enamel columns from 4-5
to 7-8.
143
Fig. 85:
М. М. VORONTSOV
Туапз/от mation of the aenial system т a number of forms of
Dipodoidea, An example of dental transformation, similar to
Cricetidae. Upper rows: According to Grasse and Dekeyser
(1955) from Vorontsov (1962 b). (a) Sicista betulina Pall; (b)
Zapus hurisonicus Zimm; (с) Aliactaga euphratica Thom; (а)
lactogulus acontion Pail,
Trans for mation of the dental system of Myoxidae: In view of
the transition to the nuirition by a more coarse food substance the
number of transversely oriented crests of molars increases.
The direction of evolution resembles Cricetidae and Muroidea,
but ihe same biomechanical problem is solved by a different
method on the basis of outgrowths not homologous to each other.
An example of convergence with fieldwoles. Upper rows
(a - according to Ognev (1948); b-e- according to Grasse and
Dekeyser (1955), from Vorontsov (1962). (a) Myomimus persona-
tus Ogn. ; (b) Eliomys quercinus L. ; (с) Dyromys nitedula Pall. ;
(4) Glisglis 1,.; (e) Muscardinus avellanarius Г.
144
ig
CRICETINAE
S/IGMODON МЕОТОМА |} ANDINOMYS
GERBILLINAE
RHOMBOMYS
; NESOMYINAE
BRACHYUROMYS
BETSILEOENS/S \SRACHYTARSOMYS
ELLOBIUS PROMETHEOMY:
MIGRGTINAE
Li MURIDAE
i
nce | a
|
RATTUS \ORICETOMYS
EROPEPLUS OTOMYS
MYOXIDAE
SC ARDIMUS
Pe <
|
|
GEOMYIDAE |
CAVIA CHAETOMYS Ё
ae
Fig.87, Homologous and convergent variabilit molar teeth of rodents.
Series Cricetinae, Gerbillinae, А: ae Microtinae are homologous to
each other; series Cricetidae, Muridae i ar Geomyidae and Hystricomorpha
are convergent to each other. + Mygxidae,
i р
MYOMYMUS
DENTAL SPECILAIS ATION
The forms having a flat masticatory surface and an elevated
crown are also found among a few forms of Sciuromorpha
(Anomaluridae).
The tendency towards the formation of hypsodont teeth
having a flat masticatory surface is highly characteristic of
many forms of Hystricomorpha. In this regard Hystricomorpha-
an elder group than Myomorpha advanced further and the initial
stages of the tooth structure are found only ina few cases. Thus,
the tuberculate structure of molars is retained in the genus
Atherurus in Hystricidae while more highly organised Hystrix
possess a flat masticatory surface of molars.
Among these forms of Hystricomorpha, the members of
Hydrochoerus, that are most adaptive to the processing of
coarse vegetative portion of plants, possess hypsodont molars,
outwardly resembling the molars of field-voles, but sharply
distinguishing by the structural features, like individual prisms
are connected with each other by cement, while the prisms of
teeth in all hypsodont forms of Cricetidae are connected with
each other by enamel and dentine.
In this way, the process of transformation of brachyodont
tooth to hypsodont and flattering of tuberculate masticatory
surface (Fig. 87) are primarily observed in the structure of the
dental system of the different groups independent of each other.
These processes are associated with the independent transition of
various groups of rodents varying from the mixed type of nutri-
tion to the nutrition by vegetative portions of plants.
However in all these groups of rodents, similarly directed
process of formation of the hypsodont forms and flattening of the
masticatory surface undergoes starting from a different initial,
structural plan of tooth. As a result, similar stages of adapta-
tion in different series bear characteristics only of superficial
resemblance and they may be separated from each other without
any difficulty. Similar variability series should be related in
parallel.
Wide distribution of the phenomena of homologous varia
bility among Cricetidae compels one to come very carefully to
145
N.N.VORONTSOV
phylogenetic conclusions based only on the study of the dental
system. All cases of parallelisms in the development of the
dental system can. be separated only on comparative -morphologi
cal study of the other.systems of organs.
The maximum range of the individual and intragroup
variability of the dental system is fully in agreement with A.N.
Severtsov's point of view on'the great variability of exosomatic
organs (to which the dental system should be related) in compari -
son with the endosomatic organs.
146
CHAPTER III
EVOLUTION OF OTHER ORGANS OF THE MOUTH CAVITY
(THE TONGUE AND THE CHEEK POUCHES)
1. Tongue
а. General outline of the tongue morphology in mammals.
The tongue (lingua) in mammals is the longitudinally
stretched muscular body, covered with the connective tissue
membrane.
The transversely striped muscle, concentrated in three
fasciculi which pass in inter-perpendicular directions makes the
thickness. Mucus of the tongue membrane of the mouth cavity
(tunica mucosa s. tunica propria) passes onto the tongue from the
back and the sides.
The upper surface ог the back of the tongue (facies superior
5. dorsum linguae) and the lower surface (facies inferior) are
distinguished (Fig. 88). The lateral margins of the tongue are
known as margines laterales and the anterior margin as margo
anterior. The front portion of the tongue which is free is named
apex Tinguae, and the middle portion of the tongue, associated only
with the bottom of the mouth cavity, corpus linguae, while the
hind, last one-third of the tongue, having a free dorsum is called
the base or root (radix linguae). Corpus linguae on its facies
superior may have ап elevation-torus linguae. A crescent-shaped
fissure called the sulcus semilunaris linguae may be found in
front of the torus linguae-Papillae of the tongue on torus is not
expressed papillae filiformes s.p.p. conicales on torus are large
and, thus, the papillae of the corpus and apex linguae are sharply
distinguished from each other; the boundary between papillae
filiformes s.p.p. conicales of the apex and corpus linguae is called
called linea semilunaris. The boundary of apex and corpus linguae
is conditionally taken for crescent-fissure (or line).
147
N.N.VORONTSOV
sulc. med. ling b
m. lat.
= 54 = 2)
РЕЗ
Г М pp.tou! ор а
тах М corpus 2. 1 ae
чезу
к
р. clrcumy.
р.Р. lertic.
Fig.88: Tongue structure and the accepted nomenclature after Vorontsov
(1958 b). (a) view from above; (b) side view (schematically);
(c) boundary of the papillae layer m-muscles of the tongue.
apex 1. - apex lingulae; corpus 1. - corpus linguale; corsum 1. -
corsum linguale; fac. inf. - facies inferior linguale; m. ant. -
margo anterior; т. lat. - margo lateralis; р. circumv. - papi-
Пиз ctrcumvallatus; p.p. filif. - pappillae filiformes; р.р. fol. -
papillae foliatae; p.p. fungif. - papilae fungiformes;-p.p. lentic -
papillae lenticulares; radix 1. - radix linguae; sulc. med. ling. -
sulcus medianus linguae; sulc. semil. - sulcus semilunaris;
torus ling. - torus linguae.
The longitudinal fissure (sulcus medianus linguae) can pass
through the dorsum linguae in the apical part. The mucous
membrane with its internal layer is fused with the perimysium of
the tongue muscle. The muscular fibers of the tongue end
spontaneously in tunica mucosa.
The mucous membrane of dorsal part of the tongue and
sometimes of marginal zones (margins laterales et anterior) are
very thick-papillae of five types,
Papillae filiformes s.p.p. conicales are almost spread along
the whole dorsum of the tongue (only at the back pf pap. circum-
vallatae, they are displaced by lymphoid pap. lenticulares) and
can move on fac. inferior, where, however, they generally occur
in the marginal zone. Papillae filiformes of the apex are fine and
have a conical shape whereas those of the corpus have the common
form of leaflets or petals and are much bigger in size.
148
EVOLUTION OF TONGUE
Papillae filiformes do not have taste buds. They accomplish
definite functions while processing food; their direction is that of
the flow of food particles.
The special role of papillae fungiformes in myrmecophaga
and cheiroptera of the pollinizer of plants (for the tongue in the
latter, see the work of Jaegar, 1954) is not considered here. The
author does not stick to the division of papillae filiformes into
pap. pectinees,, pap. tricuspides etc. as adopted in some special
papers.
Papillae fungiformes are larger in size and spread only
along the papillary part of the apex linguae. Their number varies
very much in different species: in some it can reach up to 500, in
others papillae fungiformes are absent (some field-voles,
jerboae). The taste buds are located in papillae fungiformes. On
this basis, some authors (Ganeshina, Herman, in litt.; Matveev,
1960) see a direct correlation between the number of papillae
fungiformes and the degree of gustation. There is no unanimity
in the literature even on the problem of distribution of taste buds
in papillae fungiformes (Tonkov, 1933; Zavarzin, Schelkunov
1954, Shmalhauzen, 1947, and others).
1-15 papillae circumvallatae are present. in the root part
of the torus of mammals. There is only опе* рарШа circum-
vallatus in all Cricetinae. The taste buds are concentrated in
papillae circumvallatae.
Papillae foliatae are concentrated along the edges of the
tongue around the molar teeth. In many mammals including man
they are in reduced form. РарШае foliatae (called "lateral
organs'' by English authors) have taste buds.
Papillae lenticulares are located at the root of the tongue,
behind the papillae filiformes and papillae circumvallatae. Many
researchers do not even mention about the existence of pap.
lenticulares, while describing the tongue morphology.
* In the article devoted to the morphology of the tongue or palearctic
hamsters (Vorontsov, 1958b), it is wrongly pointed out that all forms of
Cricetidae have only one pap. circumvallatus, But Nesomyinae have
three,
149
М.М. VORONTSOV
b. Tongue structure м Cricetinae
The morphological study of the tongue of the palearctic
hamsters (Vorontsov, 1958b) has shown, that even the represent-
atives of such an ecologically uniform group as the present
palearctic hamsters (Cricetini) can considerably differ from
each other by the number and arrangement of the sensory
papillae and by other features of the tongue structure (Fig. 89).
The study of the tongue structure in palearctic Cricetinae
(Vorontsov, 1958b) and the comparison of the collected data with
the material already recorded on the Nearctic Cricetinae,
Microtinae, Gerbillinae and Muridae (Tuckerman, 1888; 1891
Tullberg, 1899; Sorintag, 1924) did not enable us to mark some
peculiar features in the tongue structure of palearctic Cricetinae,
characteristic of all the representatives of this group, and
separate them from the rest of the cricetinae studied.
The most interesting fact is the discovery of papillae
foliatae having a two-row arrangement, in Mesocricetus brandti
and М. Raddei. This important characteristic separates Meso-
cricetus from the rest of the species of Muroidea studied.
Difference by this characteristic is one of the arguments
against A I, Argiropulo (1933) for combining Mesocricetus Nehr.
and Cricetus (5. str.) Leske into one genus Cricetus,
Double number of papillae foliatae as against the usual
number, their two-row arrangement and to some extent a rela-
tively large number of papillae fungiformes separate Mesocricet-
us fromthe rest of the palearctic hamsters, Do these character-
istics not give yet another proof of the polyploid origin of
Mesocricetus ‘Sachs, 1952; Darlington, 1953) ?
The last assumption, of course, should not be taken to
interpret the polyploid origin (after Sachs and Darlington) of
Mesocricetus as a reSult of the hybridization of Cricetus and
Cricetulus.
It should be emphasized that the absence of a deep sulcus
semilunaris on the tongue of Mesocricetus raddei distinguishes
150
sVOLUTION OF TONGUE
2
°. Pa
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вы
cee
SB
e
ae,
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‘poe on
Je eve
The structure of the tongue of the palearctic hamsters. Semi-
schematic (After Vorontsov, 1958 b). (a,b) Cricetus cricetus L. ;
_(c,d,e) Mesocricetus raddei Мару. ; (f,g,h) Mesocricetus brandit
Nahr. ; (i,j,k) Cricetulus (Allocricetulus) eversmanni Brandt. ;
(1, m,n) Cricetulus (Tscherskia) triton de Winton; (0, р) Cricetulus
(s. str.) barabensis Pall. ; (a,r) Gricetulus (5. str.) migratoruis
Pall.; (s,t,u) Phodopus sungorus Pall. ; (v,x,w) Calomyscus
bailwardi Thom. (a, с, f, i, l,.0, s, q, v - dorsal view, 4, Е, },
т, 1, w - ventral view of the anterior part of tongue; b, e, h, К,
п, p, 7, и, x - Side view.)
151
М.М. VORONTSOV
itfrom М. brandtithus contradicting the opinion of Ellerman
(1941) about the monotypical nature of the genus Mesocricetus.
The myomorph hamsters (Calomyseus bailwardi) are
sharply distinguished from other palearctic hamsters by the
absence of papillae linticulares.
A comparison of the features of the tongue structure leads
to classify the following five groups among palearctic hamsters:
Е 1. Calomyscus bailwardi Thom.,
П. 2. Cricetulus (8. str.) barabensis Pall.
3. Cricetulus (8. str.) Ilongicaudatus Milne-Edw. ;
4. Cricetulus (3. str.) migratorius Pall.;
5. Cricetulus (Tscherskia) triton de Wint.;
6. Cricetus cricetus L.;
ПТ. 7. Cricetulus (Allocricetulus) eversmanni Вгапа+.;
8. Cricetulus (Allocricetulus) curtatus Gl. All.;
IV. 9. Phodopus sungorus Pall.;
У. 10. Mesdcricetus brandti Nehr.;
11. . Mesocricetus raddei Nehr.
с. Tongue structure of some forms of Muroidea with
reference to the interrelations of Cricetinae with
allied subfamilies.
The tongue structure is closely associated with the features
of the biomechanical processing of food, and the degree of
development of the gustatory papillae depends on the type of
nutrition. In the opinion of Ganeshina and German (in litt.) and
Matveev (1960), there exists a direct correlation between the
numbers of papillae fungiformes and the degree of development
of gustatory perception of the species. Papillae fungiformes are
numerous in view of the transition from protein food to the
cellulose nutrition in the forms, characterized by a limited
collection of high-calorie protein food. Papillae fungiformes
can be reduced with a changeover to the consumption of the wide
152
EVOLUTION OF TONGUE
collection of vegetative parts of the plants. This conformity is
traced by Ganeshina and German (in litt.) im some forms of
Murinae and Microtinae.
The significant interspecific variability of the number and
arrangement of papillae fungiformes, on the basis of their
development, does not enable us to express particular phylo-
genetic formations. The number and the degree of development
of papillae fungiformes are more constant.
How are the functions of the three types of gustatory
papillae divided? Judging from their arrangement it can be
assumed that the papillae fungiformes that are concentrated at
the tip and the dorsum of the tongue take part in the gustatory
perception of the food which is taken into the mouth. Papillae
foliatae, situated along the molar teeth differentiate the taste of
the food crushed by the teeth and papillae circumvallatae evaluate
the taste of the food crushed and soaked by saliva.
The number of papillae circumvallatae in rodents usually
ranges from one to three”.
All present forms of Sciuromorpha (representatives of the
old, predominantly seed-eating group of rodents) usually have
three papillae circumvallatae (Aplodontia Anomalurus, Sciurus,
Eutamias). The number of р. circumvallatae among Hystrico-
morphs decreases from three (Hystrix, Castor) to two (Cavia,
Erethizon, Chinchilla, Coelogenis, Myopotamus) when the
middle papillae is reduced.
The rodents which burrow with incisors, have strongly
developed torus linguae, which is evidently associated with the
pushing off of soil that has entered the mouth with the tongue.
Therefore, the main flow of the crushed food particles passes by
the side of the torus or over the p. vallatae but not over central
papilla. . Evidently it is related to the fact that the majority of
burrowing rodents, from different groups - Georychus
(Batheygidae-Bathyergomorpha), Myospalax (Myospalacinae-
Cricetidae-Myomorpha), Spalax (Spalacidae Myomorpha)
* According to Tullberg (1899) Pedetes. and Petauristg generally do not
have ‘papillae circumvallatae.
153
N.N.VORONTSOV
Rhizomys (Rhizomyidae-~Myomorpha) - possess two papillae
circumvallatae, whereas the central papilla is reduced in them.
Like all other non-burrowing members of the Geomyoidea group
(Hoteomyinae, Dipodemyinae), only Geomys has one central
circumvallate papilla.
The number of circumvallatae papillae in old Myomorph
group - Myoxsidae and Dipididea ~ is equaltothree. Among
Muroidea, Nesomyinae (Gymnuromys Macrotarsomys, Brachy-
uromys) have three circumvallate papillae. In a number of
Cricetidae in Myospalacinae the central papillae is reduced and two
circumvallate papilae are left behind, and in Cricetinae (Cricetus
Mesocricetus, Cricetulus, Phodopus, Mystromys, Peromyscus,
Calomyscus, Sigmodon, Neotoma) Gerbillinae (Gerbillus Merio-
nes, Rhombomys) and Microtinae (Clethrionomys, Prometheomys,
Lemmus, Lagurus, Dicrostonyx and others), two lateral papillae
are reduced and one central circumvallate papilla is left behind.
Only forms of Cricetomyinae have three circumvallate papillae,
among Muridae, whereas in the present Murinae (Rattus, Mus,
Apodemus, Aryicanthis) Nesokia, Micromys, Pogonamys and
others) there is only one circumvallate papilla.
In this manner, the oligomerization process of the number
of circumvallate papilla takes place inside the various groups of
rodents independent of each other. However the change in their
number is noticed only in big groups (from subfamily and above),
and within subfamilies and genera it is constant. That is why the
number of circumvallate papillae is an important systematic
characteristic, which gives evidence to the homogeneity of the
group Nesomyinae and the separation of Nesomyinae from Criceti~
nae. The number of circumvallate papillae separates Муовраа-
cinae both from Microtinae and Cricetinae to which they were
related by different classifications. At the same time, we think
that the agreement to the number of circumvallate papillae between
Myospalacinae and Spalacidae, is caused by the convergence,
associated with the burrowing life and cannot be considered as the
evidence of kinship of these proups. Similar tongue morphology in
such distant forms as Spalax and Georychus indicates definitely
that the convergence in the tongue structure in the forms which
burrows can go very far. Evidently, the resemblance in the
tongue structure and number of cir€umvallate papillae in Spalax
and Myospalax is caused by convergence.
154
EVOLUTION OF CHEEK POUCHES
Ia this connection, it is important to emphasize that the
Madagascar forms of Nesomyinae, in spite of the extreme breadth
of divergence, retain the same number of circumvallate papillae.
2. Cheek Pouches
Cheek pouches occur in various groups of rodents indepen-
dent of each other.
In the family, Sciuridae, cheek pouches are characteristic
of the representatives of the tribe Marrotini. They may not exist
or may only be slightly developed in Marmota (Grasse and Dekey-
ser, 1955). They exist in the members of other genera of this
tribe - Citellus, Cynomys, Tamias and Eutamias.
Cheek pouches are characteristic of the entire group of
Geomyoidea (Heteromys, Liomys, Perognathus, Microdipodops,
Dipodomys, Thomomys, Geomys, Pappogeomys, Cratogeomys,
Platygeomys, Orthogeomys, Heterogeomys, Macrogeomys,
Zygogeomys).
In the group Muroidea the cheek pouches appear, independent
of each other, in some forms of Cricetidae (Cricetus, Cricetulus,
Mesocricetus, Phodopus) and Muridae (Beamys, Saccostomus,
Cricetemys).
Among Hystricomorpha the cheek pouches are developed in
Cuniculus.
It is remarkable, that in all those groups the cheek pouches
are not homologous to each other.
Cheek pouches are poorly developed in Marmotini. The
cheek pouch is a growth of the lower part of the adoral cavity
and moves downwards away from the dental row. The posterior
part of the cheek pouches of Marmotini is drawn off by muscles
of which one moves downward and back and is attached to the
sternum, andthe other moves back horizontally and is attached
to the facies of muscles, which are attached to the front edge of
the shoulder blade (Fig. 90).
155
N.N. VORONTSOV
b
и
°
a
{
N
ACRES 1
Fig.90: Diagram showing attachment muscles of cheek pouches т
squirrel family (Marmotini, Sciuridae, Sciuromorpha), .Citellug
undulatus, Original: According to the specimen from the Eastern
Kazakhstan. Kalbin Altai. (a) ventral view; (b) side view.
The pouches for storing food are developed in Geomyoidea
in the form of special folds on the lower surface of the face and in
no way connected with the mouth cavity. These are blind pockets,
covered with hair from imside and are used only for bringing food
substance from the place, where food was found, to the nest
(Fig. 91).
Cheek pouches of present hamsters (Cricetini) attain an
unusual development. In inflated state they are stretched behind
shoulder blade. Cheek pouches are used by hamsters not merely
for storing the food substance. Cricetus cricetus takes the soil
out of the deep burrows to the surface (Zverev, 1931) with the
help of the cheek pouches. All forms of €ricetini use cheek
156
EVOLUTION OF CHEEK POUCHES
Fig.91: Topography of cheek pouches in Geomyoidea. View from the
ventral side, Original (a) Liomys pictus Thomas, Mexico,
Sinaloa; (b) Perognathus baileyi Merriam USA, Arizona; (c)
_ Dipodomys marriamt Mearni, USA New Mexico.
pouches while swimming; in water the hamsters inflate the cheek
pouches and swim, thus easily floating on the surface (we have
observed it outselves).
The young forms of Phodopus sungorus and Mesocricetus
auratus, still blind and hardly covered with wool, fill the cheek
pouches with such large things as sunflower seeds. Evidently,
in this manner, the animals, significantly increases the volume
of cheek pouches while still young.
Usually the food is collected in one of the cheek pouches
first and only whenthis is full itis collected inthe other. Itis
remarkable that only after the cheek pouches are free of food, the
hamsters start moving their shoulder and shoulder blade. For
the role of cheek pouches in storing food in hamsters see A.G.
Po nugaeva (1963).
In Cricetini cheek pouches are the growth of the posterior
part of the adoral cavity (Fig. 92). The hole of the cheek pouches
is situated in the diastema and blocked up by the jsphincter formed
by m. orbicularis oris. The :cheek pouch is coriaceaus, easily
stretchable organ, the internal surface of whichis covered with
horny epithelium. The empty cheek pouch is not very big, it
comes together owing to the contraction of the fibers of the trans-
versely striated muscle, longitudinally along its external surface;
the internal surface of the cheek pouch is folded when it comes
together. The folded growth of the internal surface fails into the
V5?
N.N.VORONTSOV
posterior part of the cheek pouch from the internal side near the
withdrawal point of the muscle inside the cheek pouch. Inthe
lateral and the lower parts of the mouth opening there is a groove
which leads to the cavity of the cheek pouch.
In Phodopus, unlike all other present forms of Cricetini,
the initial part of the external side of the cheek pouch is covered
from inside with small hair drawn inside.
The posterior part of the cheek pouch in Cricetini is drawn
off by one muscle which moves backwards and upwards, and is
attached near the lumbar vertebrae. This muscle, is evidently
the derivative of m. trapezius (Priddy and Brodie, 1948). The
muscle, which draws off the cheek pouch, envelops its posterior
part from the ventral and the medial sides.
Absence of cheek pouches should be marked not only in ali
American* and Madgascan forms of Cricetidae, but also in
Mystromys, Lophiomys and Calomyscus.
The strong development of the cheek pouches which could not
be taken as the evidence of the prolonged and independent evolu-
tion of Cricetus, Cricetulus Mesocricetus and Phodopus is, as a
matter of fact, one of the important characteristics, which com-
pels us to separate Mystromys, Lophiomys and Calomyscus from
the tribe, Cricetini.
In the family, Muridea the cheek pouches are developed
in the genera Beamys and Saccostomys of the supfamily Murinae
and in the monotypical subfamily Cricetomyinae. A representa-
tive of the last group of Cricetomys gambianus, named so
owing to the cheek pouches, indicating its similarity with the
hamster has been studied (Fig. 93).
* The poorly developed cheek pouches, or more exactly, the significant
increase in the size of the cavity situated between the cheek and molars
occur in some forms of Peromyscus. However, the degree of development
Gf the cheek pouch of Peromyscus is so insignificant in comparison wil”
that of Cricetini, that there 15 no doubt about the independent origin of
these formations in the Palearctic forms of Cricetini and the Ameria
forms of Peromyscus.
158
Fig. 92:
EVOLUTION OF CHEEK POUCHES
a
Diagram of muscle attachment of the cheek pouch in real hams -
ters (Cricetini, Cricetidae, Myomorpha). Phodopus sungorus
sungorus Pall. Original. According to the specimen from
Western Siberia. Novosibirsk region (a) view from above; (6)
side view,
Fig. 93:
2 b
Diagram of the muscle attachment of cheek pouches in mice
(Cricetomyinae, Muridae, Myomorpha), Cricetomys gambianis.
According to the specimen from Central Africa (a) view from
above; (b) side view.
Sg)
М.М. VORONTSOV
Cheek pouches are poorly developed in Cricetomys.
They have a blunt growth near the mouth cavity. The posterior
part of the cheek pouch is drawn off by one muscle, attached to
the cervical vertebrae. The problem of the origin of this
muscle, like that of the homologization of the muscle of the
cheek pouches in Marmotini and Cricetini, needs special study,
taking into account the innervation of this muscle.
Rodents having cheek pouches have a remarkable geo-
graphical distribution. The group Marmotini is undoubtedly,
associated with open spaces; the majority of the representatives,
except the Siberian Chipmonks, are found in steppes and semi-
desert regions.
The group Geomoidea is spread in steppes, semidesert,
desert and hilly, desert landscapes of North America.
The present hamsters (Cricetini) inhabit the steppes and
semi-desert regions of Palearctic.
The present mice (Murinae), possessing cheek pouches -
Saccostomus and Beamys - are found in steppes desert and
savanna of Africa. Only Cricetomyinae (a single species -
Cricetomys gambianis) from steppes, deserts and savanna of
Eastern and South-Eastern Africa penetrate into the humid and
tropical forests of Western Africa.
Paca (Cuniculus) is distributed in open arid landscapes
of central, and hilly parts of South America.
All these data on the geographical distribution of rodents
which are far from each other and which independently acquire
cheek pouches, indicate that the appearance of cheek pouches is
associated with living conditions in the open arid zones of the
globe having sharp variations of feeding conditions with seasons.
Cheek pouches help in storing food. It is not by coinci-
dence that, in the capacity of the food stored, the hamsters ©
occupy the first place among rodents and susliks the second
place while the mice, mole-rats, and certain field-voles occupy
generally much lower place. Storing of food, associated with
160
EVOLUTION OF CHEEK POUCHES
the development of cheek pouches leads to a great extent, to the
least dependence of the animals on unfavorable conditions of the
medium,
Slight variations in the number (associated also with the
storing of food for winter), which:are characteristic of hamsters
and resulting in the retardation of their evolution rate (Voro-
ntsov, 1960b) may, to some extent, depend on the presence of
extremely developed cheek pouches in Cricetini
161
CHAPTER IV
THE EVOLUTION OF STOMACH
1. General Notions, Terminology
Food falls into the stomach from the gullet which is a
deprivative of the ectoderm and is covered with horny epithelium.
It has endodermic origin and is lined with glandular epithelium
in most of the forms of Marsupialia and Eutheria.
The stomach (Venter), in its initial shape is a pouch-
shaped expansion which is connected to the esophagus above and
duodenum on the right. On the boundary between the esophagus
and stomach there is the ''border-line fold (Grenzfalte, as called
by German authors) representing the growth of the connective
tissue layer of the stomach and is lined with horny epithelium
(Brummer 1876; Luppa, 1956) from the side of the gullet as
well as the stomach.
At the opening between the gullet and the stomach the
thick muscular ring forms a cardiac sphincter (sphincter
cardia) which blocks the entrance of anything into the stomach,
on contraction of the muscle. There is a large thickening of
muscles at the opening between the stomach and the duodenum
which forms the phylorus sphincter (sphincter pylori).
The part of the stomach contiguous to the gullet is called
the cardiac portion (pars cardiaca or simply cardium); the
main part of the stomach arranged mainly posteriorly from the
cardium is called the fundic portion (р. fundica, or simply =
fundus); the narrow outlet is called the pyloric portion (p. pylo-
rica or pylorus). The types of main glands, correspond to the
division of the stomach in the one-chambered glandular stomach.
1 62
EVOLUTION OF STOMACH
Cardial glands producing mucous alkaline secretion occupy
a small area inthe cardium. These glands can be easily reduced
or displaced together with the border-line fold.
Fundic glands, which play a main role in the digestion of
protein food, are situated at the bottom of the stomach. They
are formed by remified glands. The gland cells produce gastric
juice - pepsin, chymosin and lipase, but the lining cells produce
hydrochloric acid. Fundic glands which may occupy a greater
or smaller surface area of the stomach, never disappear.
Pyloric glands, which produce an alkaline secretion con-
taining pepsin, are situated in the pyloric portion. These glands
may be displaced by the horny epithelium or generally reduced.
The surfaceof the glandular area of the stomach has
alveolate form; small elevations are called areas (aereae
gastricae), and shallow depressions, on the bottom of which
there are openings of glands, are named crypts (faveolae gas-
tricae).
Primarily the stomach in mammals is, a pouch-like ex-
pansion of the middle intestine. The part (primarily situated
between the gullet and the duodenum) adjacent to the liver is
called the minor curvature (curvatura minor); the caudal edge
of the stomach forms an arc of greater radius called the major
curvature (curvature major). As the stomach becomes more and
more complicated the gullet and the duodenum come close to
each other, and the radius of the minor curvature of stomach
decreases. The part of the stomach, situated on the left of the
cardium, is elevated forming a fornix (fornix ventriculi); the
pyloric part of the stomach also is elevated. As a result the
opening between the gullet and the stomach is situated more
caudally than many portions of the stomach.
The muscular membrane of the stomach consists of three
layers; external (longitudinal), middle (annular) and internal
(oblique). ‘The volume of the stomach in the non-inflated state
may significantly decrease on the contraction of the muscles.
Depending on the portion having less food, its volume reduces
to few times owing to the contraction of the gastric muscles.
1 63
У. М. VORONTSOV
АП sections of the stomach increase ог decrease proportionately
only during uniform inflation of the whole stomach by food or
contraction owing to its complete absence. The degree of
inflation and the state of contracted muscles determine the shape
of the stomach of the animal under study. That is why the size
of the blind pouch formed at the elevation of the fornix and the
pylorus changes completely. Attempts of some researchers to
judge the morphology of the stomach on the basis of superficial
morphology without studying its internal structure are supported
mainly by the ratio of the volumes of separate parts of stomach
and cannot be considered as convincing. Because of the signi-
ficant height of the glandular layer of the fundie part of the
stomach the bottom stretches the least and its volume varies less
than the remaining portions of the stomach.
Near the pyloric sphincter the pylorus is surrounded by a
powerfully developed muscular sphincter (constrictor antrium
pylori) which when contracts pushes the food from the stomach to
the duodenum. The powerful horny folds which play the role of
horny “teeth'' may be developed where the pyloric part of the
stomach is lined with the homny epithelium. Similar formation,
well known (Pernkopf, 1937) and most clearly expressed in
pangolin (Manis javanica) is not found so well expressed in some
rodents.
Non-chambered stomach may be subdivided by folds into,
sub-sections. Generally the angular fold (Plica angularis),
situated on the minor curvature of the stomach belgw (from be-
hind) the opening between the gullet and to its right , is very
clearly expressed. The division of the stomach into two portions,
characterized by real hamsters (Cricetini), is achieved by the
powerful development of plica angularis. To the left of the
opening between the gullet and stomach might develop a cardial
fold (plica cardialis) which separates the blind pouch, and this
pouch, is converted into an independent section of the stomach in
some sandworts (Arenaria). In front of the muscular pylorus
sphincter might develop a prepyloric fold (plica praepyloris)
which may. separate the pyloric section and convert it into an
independent chamber.
+ Here and later when there is a description of the stomach Ц 1s considered
from the dorsal side.
164
EVOLUTION OF STOMACH
The powerful development of the angular fold is generally
associated with the formation of an external deepening of the
constriction (isthmus). Similar recesses generally correspond
to other most important folds of the internal surface of the
stomach.
Depending on the epithelium which lines the internal
surface of the stomach, the following types of stomach are dis~
tinguished (Pernkopf, 1937, Jedenov, 1958);
horny (only in Monotremata among mammals it is
obviously, not homologous to the stomach of superior mammals
and represents the expansion of the gullet i.e., the derivative
of the anterior and not the middle intestine);
glandular (it is the initial stage of the superior mammals
and spread among Insectivora Chiroptera, Carnivora, Pinnipedia,
Prosimia, majority of Primates, some forms of the Cretacea,
Edentata, Sirenia, among rodents in all forms of Sciuromorpha
and Hystricomporpha, and in the suborder of Myomorpha among
all forms of Dipodiodea and Gliroidea);
combined, when a part of the stomach is lined with horny
epithelium having the origin of the gullet and the other part
is lined with glandular. This type appears in different groups of
the phytophagous mammals (Perissodactyla, Artiodoctyla,
Hyracidae, Macropodidae, Bradypodidae, and among rodents it
is spread in all Muroidea).
The stomach can be classified as simple, one-chambered,
or complex (two-, three-, four-, five-, and six-chambered)
types depending on the number of the sections. Generally the
process of isolation of the chambers proceeds along with the
formation of eipthelium of the stomach mixed according to types,
but in individual cases (Yablokov, 1958) the multi-chambered
stomach can also appear in forms having exceptionally glandular
covering of stomach (Ziphius-Odontoceti).
The notion about the fact that the two-chambered type of
stomach in rodents is found as an exception only in hamster
(Oppel, 1869, Pernkopf, 1937; Jedenov, 2958), is based on the
165
N.N. VORONTSOV
study of the limited number of forms: multi-chambered stomach
develops into various groups of Muscidea.
The isolated left portion of the complex stomach of the
rodents, lined with horny epithelium, similar to the rumen of
ruminants is named the prestomach. Bline growths, which
may be lined with horny as well as glandular diverticula branch
off from the corpus of the stomach. On the aperture of the di-
verticulum (oryphiceum diverticuli) may have special sphincter
(sphincter diverticali).
The surface of the horny portion of the stomach is covered
with folds particularly well expressed on the collapsed stomach.
Undoubtedly, these folds of horny epithelium, sometimes having
the form of thick horny protuberances moved by the stomach
muscles, have a definite significance in its motor system.
The surface of the horny portion of the stomach may in
extreme cases be strewn with papillae, lined with horny epi-
thelium, or powerfully developed villiferous layer. The muscle
enters the papillae, which may be mobile like the horny papillae,
of the rumen of some ruminants. An increase in the area covered
by horny epithelium is achieved with the development of
papillae and fibers.
Along the minor curvature of the stomach from gullet to
pylorus there exists an esophageal canal (sulcus oesophageus),
which is a narrow corridor on the surface of the minor curvature
of the stomach, with two longitudinal folds, having a muscular
base. In hoofed animals the edges of these folds may close,
forming a tube along which the milk and other food substances
which do not require special processing in the corneous portions
of the stomach, pass directly from the gullet into the glandular
portion of the stomach (Jedenov, 1958]. Most likely, the sulcus
aesophageus performs similar function in the stomach of the
rodents.
166
PHYSIOLOGY OF DIGESTION
2. Оп the Physiology of Digestion in the Stomach. Functional
Peculiarities of Glandular and Combined Stomachs, of
Nonchambered and Multichambered Stomachs in Rodents.
The physiological characteristics of digestion in the
stomach have not been studied much (Davenport and Yensen, 1949;
Davenport, Schnoebell and Chavre, 1950; Ambrus G.. Ambrus
М. and Harrison, 1953, Pravdina, 1958 a, 1958b). However
special studies of digestion in the glandular nonchambered ~
stomach in predatory animals in the combined one-chambered
stomach of horses, transitional to the multichambered combined
stomach of pigs, and in the multichambered stomach of rumi-
nants of hoofed animals (Pavlov, 1946; Verigo, 1906; Azimov,
Krinitsin and Popov, 1954.; Koshtoyants 1950) show the present
general regularities of the physiology of digestion closely asso-
ciated with the structure of the stomach. These data give us
an idea of the process of digestion in the stomach of the rodents.
The food lump from the mouth cavity moistened by saliva
falls into the stomach through the gullet. The process of diges-
tion can start in the mouth cavity itself where by the action of
amylase carbohydrates break up into polysaccharides. Breaking
up of carbohydrates stops in the stomach under the influence of
acidic medium.
The glandular stomach of mammals is strictly one-chamber-
ed. The fornix of the glandular type of stomach is never ex-
pressed. It becomes quite clear if we recall the features of
secretion of the main types of gastric glands. Cardial and
pyloric glands which never achieve’ such a concentration оп a
unit area as fundic glands, separate pepsin besides mucoid
secretion. However neither the cardial nor the pyloric arch
is capable of producing hydrochloric acid. Meanwhile pepsin
breaks up the protein only in acidic medium (optimum at pH =
1.5 -2.0). The food substance which came from the horny
cavity.and mixed with saliva, has a mild alkaline reaction.
Thus pepsin separated (in small quantities) by the cardial
* Exceptions are the Castors, in which the cardial glands produce not only
pepsin, but also HC} (Nasset 1953; Orlova, 1956). Possibly, the glands
of cardium т Castor originate from fundic glands, shifted to the minor
curvatuxe of the stomach.
1 67
N.N.VORONTSOV
glands acts only in acidic medium, which is formed by oxyntic
cells of the fundic glands, that secrete hydrochloric acid.
Whatever be the section separating the cardial part of the
stomach (secreting the ferment) from the fundal part (secreting
the activator of its action) it is not justified functionally. In an
exactly similar way the region of pyloric glands in the grandular
type of stomach has not been separated from fundic region. In
the same way, the pyloric glands secrete pepsin and are simi-
larly not capable of secreting acid. However the food, entering
from the fundal part of the stomach to pylorus, has already a
clearly marked acidic reaction, in which the pepsin of the ру1о-,
ric glands can act. Therefore, there may be an insignificant
degree of isolation of the pyloric region of the stomach from thé
fundal part in the glandular type of stomach but the separation
of the cardial part of the stomach from the fundal part is never
observed.
At the bottom of the stomach fundal glands play the main
role in splitting.proteins, as stated by the works of Г.Р. Pavlov
and his students. The number of fundal glands in a unit area of
the stomach is more than the number of cardial and pyloric
glands. They secrete the maximum quantity of pepsin, and only
they secrete hydrochloric acid - the medium necessary for the
action of pepsin.
Studies on domestic animals showed that in all phyto-
phagous mammals (rabits, horses, pigs and ruminants) the
gastric secretion flows continuously, whereas the predatory
animals the secretion starts only at the sight of the prey-
-while chasing the prey or even only after the first swallowing
movements (the feline species which catch prey from the
ambush). These features of gastric secretion in phytophagous
and predatory mammals are associated not only with the fact
that in the case of irregular nutrition, in the absence of food,
the continuous gastric secretion might result in self-digestion
of the walls of stomach but also with the fact that the frequency
of consumption, composition and caloric value of food substances,
with which the representatives of these main ecological groups
of mammals ‘feed on, are diverse.
Since protein food has a high caloric content only a
small quantity of such a food is required to be taken, and the
1 68
PHYSIOLOGY OF DIGESTION
process of food intake becomes less frequent. However, on
taking exceptionally or mainly protein food it is necessary to
have simultaneous secretion of a good quantity of highly con-
centrated secretion having ferments that split proteins.
Low caloris¢ value of the vegetative parts of the plants
requires a larger consumption of food in volume which even
the highly cagmplex digestive system of phytophagous mammals
can handle during one feeding. For attaining the necessary
colorie, therefore, the animal should eat round the clock.
An extremely low content of proteins in the vegetative parts of
the plants does not require a large quantity of concentrated
secretion for processing it. Utilization of an insignificant
quantity of proteins contained in this food is very important in
the case of the low-calorie cellulose food, and requires constant
secretion of a small quantity of gastric juice. It is interesting
that in the same forms (in horses) the protein products cause
an increase in the secretion of gastric juice whereas on
eating of mainly cellulose food (hay) the quantity of gastric
juice secreted is minimum (Azimov, Krinitsin, Popov, 1954).
According to the data of Г.Т. Pravdina (1958b) the gas-
tric juice containing maximum acidity in rodents is secreted
depending on the type of food specific for the given form: in
field-voles - cellulose, and in susliks and mice - protein food.
However, it is necessary to relate the data, acquired by a highly
perfect method with care.
Г... I. Pravdina (19588) studied the duration of the food
remaining in the stomach of common voles, social voles and
white mice. In all these species the grass (cellulose form)
remains in the stomach for 2 - 3.5 hours, while the grains
(protein form) remain up to 5.9 hours (Table 3). This phenome-
non to which Pravdina does not find explanations, is obviously
associated with the fact that the main breakdown of protein
takes place in the stomach, whereas the cellulose is subjected
to break down generally in caecum and colon.
Thé food, more specific for a given species stays longer
in the stomach than that less specific. However, in house
mice, and common filed-vole, also protein food (grain) remains
169
N.N. VORONTSOV
TABLE 3.
Duration of food substances remaining in the stomach in the rodents Muroidea
(according to Pravdina, 1958a), hour-min,
Species Grass Carrot Grain
a SE a a
Microtus socialis 3 - 00 4— 20 =
Microtus агса 1$ 3 -30 4 -40 5 -20
Mus musculus var, аЪ. 2 - 00 3 - 25 5 -55
in the stomach longer than cellulose (grass) food inspite of the
difference in the duration of remaining in the stomach.
Low calorie value of mainly the cellulose food brings about
the need to feed on round the clock. The quick passage of food
through the digestive canal in such herbivorous forms as field
voles, and the considerably greater duration of the stay of food
in the digestive canal of rodents having combined type of nutri-
tion (Table 4) (are associated with this. The experimental
data (Mokeeva, 1948) shows, that in the cellular form the food
stays longer than all in the blind and large portion of intestine,
combined type of nutrition stays in the stomach and small portion
of intestine.
It should, however, be noted that the duration of food
remaining in the digestive tract of the Asia Minor sandwort
twice longer than that of the gray hamster may depend not only
on the differences in the types of nutrition of these species but
also on the differences in the size of the animals and the lower
metabolic activity in larger forms of sandworts.
The insignificant role of the cardial and pyloric glands, in
the secretion of pepsin (in comparison with fundic glands)
explains, why exactly these glands are subjected to reduction
in many forms of phytophagous mammals. The reason for the
reduction of glandular lining of stomach is the decrease in the
role of protein food; the cellulose food is very coarse, and may
easily hurt the mucous membrane of the stomach.
170
PHYSIOLOGY OF DIGESTION
TABLE 4.
Duration of stay of food in the portions of digestive canal of rodents Muroidea.
(according to Mokeev, 1949)
Sp ecies Total duration of Relative duration of stay of food
stay of food in the in different portions,%
digestive canal
(hour)
stomach small blind and large
portion portions
Microtus socialis 37.0 6.8 12.2 81.0
Microtus arvalis 36 .0 8.3 Пе
Cricetulus migratorius 50.5 16.8 19.8 60.4
Meriones blackleri 149.0 26 .8 33.6 39.6
It is not clear why the reduction of the number of glands
in the stomach dissociated with the transition to the cellulose
type of nutrition results rot in the formation of mucous membrane
devoid of digestive glands, but in the replacement of the glandu-
lar lining of the stomach by the horny epithelium of esophageal
type.
The process of transformation of the glandular into the
combined stomach is closely associated with the transformation
of the one-chambered into the multichambered stomach. How-
ever, the division of the stomach into different parts starts a
little later than the formation of combined (according to the
types of epithelium) stomach.
With the formation of the combined type of stomach the
border line fold which primarily separates the horny epithelium
of the gullet from cardial glands, and which is situated in the
forms having glandular stomach, strictly at the opening between
the gullet and the stomach,moves into the stomach. The horny
171
М.М. VORONT SOV
epithelium of the esophageal type is spread into the cardial por-
tion of the stomach. According to the data of Luppa (1956), the
horny epithelium in rodents having combined type of stomach
is identical to epithelial lining of esophagus. The initial stages
of the process of spreading of the horny epithelium into the
stomach can be identified in Nesokia indica (see Fig. 116, a).
Nectomys squamipes (see Fig. 94,b) and Sigmodon hispidus
(see Fig.110). In the lamellident rat, Nesokia indica more
cardial glands are preserved in the stomach side by side with
the presence of horny epithelium in the left part.
The form of the combined type of stomach is prevalent
in rodents, wherein the horny epithelium completely replaces
the cardial glands from the left half of the stomach and the
border line folds divides the stomach into nearly two parts,
coming very close to the fundic glands. A similar shape of the
megalotis, Calomyscus bailwardi, etc. water-vole Arivicola
terrestris and the majority of sandworts.
The horny lining of the stomach serves as the surface of
that reservoir where infusaria and extensive specific bacterial
flora develop. According to the data of Kopperi (1935), a
symbiotic protistofauna appears in the multichambered stomach
of Cricetidae, which is qualitatively close to the fauna of the
stomach and the intestine of ruminants. With the help of
symbionts (the presence of bacteria in the combined stomach of
rodents is undoubtful), fermentation takes place for the ferments,
breaking down the cellulose (cellubiase) are not directly pr oduced
by mammals (Koshtoyants, 1950).
However, the bacterial flora and symbiotic protistofauna
of the digestive system can exist only in a weakly alkaline
medium, whereas these organisms are digested by pepsin in
acidic medium at the fundus of the stomach. Similarly a weakly
alkaline medium is created when the food moistened with saliva
enters the stomach. It is quite obvious that the isolation of the
horny portion of the stomach, where the weak alkaline medium
must be preserved from the glandular parts of the fundus ventri-
coli having strong acidic medium, is a condition which 187
necessary for the development of bacterial flora and symbiotic
r72
PHYSIOLOGY OF DIGESTION
protistofauna, i.e., a condition of assimilation with the organism
of cellulose food substances. That is why in various groups of
mammals and rodents the process of separation of the left part
begins in the independent portion (viz., the horny prestomach)
in view of the transition to the cellulose type of nutrition follows
ing the penetration of the horny part into the stomach.
Besides fermentation of cellulose symbionts help in the
intensive processes of grinding in the horny prestomach with the
help of horny columns, peristaltic and antiperistaltic contractions
of the stomach muscle and maceration of the coarse cellulose
food. These processes precede their fermentation.
The next stage of distribution of the horny epithelium in
the stomach is the displacement of the pyloric glands by it from
the pyloric portion of the stomach. The border line fold would
appear to be divided into two parts: the main part which separates
the fundic glands from the horny epithelium, and a small fold
near the opening between the stomach and the duodenum, where
the pyloric glands (Tullberg, 1899; Luppa, 1956) obviously
having no function may be retained in the narrow area between
the borderline fold and duodenum.
The nature of distribution of the pyloric glands (unlike the
cardial) plays a significant role in breaking down proteins.
Therefore, the process of keratinization of the pyloric portion
of the stomach is obviously associated primarily with a de-
crease in the role of protein food substances consumed by some
rodents adapted to the cellulose type of nutrition. The process
of keratinization of the final portion of the stomach is character-
istic of rodents, pangolins and some edentates and is not found
among hoofed mammals. The functional significance of the
formation of the horny lining of the pyloric portion of the stomach
may only be assumed, |
The horny epithelium in the pyloric portion of the stomach
seldom forms large bulges. These formations moved by the
powerful muscles of the pyloric sphincter, may have definite
role in the mechanical process of the coarse cellulose food.
The field voles having the pyloric portion not divided up
to the fundus (Microtus), may have a concentration of protein
73
N.N. VORONTSOV
particles in the fundic glands region when we find in the stomach
both the green parts of plants and seeds. But the cellulose food
substance re mains both in the anterior portion of the stomach in
pyloric portion. This observation, repeatedly checked in our
studies on northern field voles (Vorontsov, 1961Ъ), must be
explained physiologically, since the mechanism of dividing the
various food fractions is not clear according to their chemical
composition.
The entry of the fundic gland acid into the pyloric portion
considerably inhibits the cellulose fermentation in the horny
pyloric portion. The pyloric zone lined with the horny epithelium
is an independent zone in the hamster Peromyscus californicus
and field vole Prometheomys schaposchnikovi. This, to some
extent, limits the entry of hydrochloric acid of the gastric juice
into this section and facilitates the development of the bacterial
flora. Even the borderline fold which separates the horny portion
to some extent from the glandular portion is well developed in these
forms.
The separation of the fundic gland by the borderline fold on
the one hand and the considerable development-along the minor
curvature of the esophageal groove, on the other, clearly de-
marcate the fundus portion from the pyloric. In some rodents the
food passing through the fundic glands region may penetrate into the
pyloric portion through the esophageal groove or the place through
which it stretches along the minor curvature of the stomach. It is
interesting to note that the penetration of the horny epithelium to
the right half of the stomach, generally, begins only in the eso-
phageal groove along the minor curvature of the stomach. It is
well known that liquid food may pass through the esophageal groove
while passing through the cardial portion and sometimes even
through the other portions of the stomach. It is apparent that the
slightly alkaline saliva which favours the development of the Ъас+
terial flora and fauna may penetrate through the minor curvature
of the stomach into the pyloric portion where it creates conditions
for the existence of symbionts. However, this hypothesis is yet
to be proved experimentally. Even if the fermentation of cellulose
takes place in the horny pyloric portion, the conditions here are
not so favorable as in the "fore stomach". The main functions of
the horny pyloric portion are maceration and grinding of the cellur
lose food.
174
VARIABILITY OF STOMACH
Thus the basic tendency in the formation of the form and
function of the stomach in rodents is not strictly analogous to those
in ungulates. While the horny "fore stomach" of rodents is
analogous to the rumen, reticulum and omasum of ruminants and
the function of the fundal gland region is the same as that of
abomasum in ruminants, the horny pyloric-portion of the stomach
developing in some rodents does not have any analog among these
organs of the ungulates. 5
3. Individual and age variation in the structure of the stomach
The stomachs of 231 specimens of Clothrionomys glareolus
and 136 specimens of Clethrionomys nutilus have been studied. The
structure of the stomach of not only palearctic rodents but also
of 2-12 specimens were studied. As observed above, the ratio
of the volumes of the blind sac of the first stomach and the pyloric
portion depends on the amount of food contained in them and the
state of the animal at the time of fixation. These cannot be con-
sidered as individual differences, but should be taken into con-
sideration while studying the morphology of the stomach. Where-
ever possible sketches of the stomach are made with approximately
the same width of the stomach portions. However, the variation
is so great that we did not always succeed in getting a homo-
typal material. These features of the change in the form of the
stomach when it is full should be taken into consideration while
making use of the figures prepared for this work. Meanwhile, the
topography of the glands, the division of the stomach into portions
and the development of the borderline fold strictly constant in all
the individuals of this species - these were the characteristics
studied by us.
Agewise variations in the structure of the stomach were
studied by comparing the stomach of the new born, young and
adult forms of true cricetinae and field voles. The stomachs of the
new borns of true cricetinae and field voles have already been
divided into two portions, but, the blind sac and the pyloric
portion were relatively small compared to the fundal region.
Young animals, changing to independent nutrition possess well
developed fore stomach and pyloric portion. It is highly probable
that the increase in the volume of these portions is connected not
only with their late growth but also the strain caused by food con-
tained in them.
Lv 5
М.М. VORONT SOV
The embryos of Mesocricetus auratus measuring 10-12 mm
have a loopshaped curved stomach but it is not clearly divided
into two portions. The embryo of common voles measuring 6-8
mm also have a loopshaped curved, one-chambered stomach
where the fundal glands occupy most of the surface. These iso-
lated observations show the origin of the two-chambered stomach
in certain forms of Cricetidae from one-chambered stomach.
On the basis of the detailed e mbryological studies Pernkopft
(1931 and 1937) and Gerke (1956) have established that the multi-
chambered stomach of ruminants is formed by the division of an
originally one-chambered stomach, That have, thereby proved
that Aeby and Munk's view (see Gerke, 1956) that the horny
portion of the stomach is homologous to the lower portion of the
esophagus is erroneous. Our fragmental observations confirm
that Pernkopf's (1931 and 1937) and Gerke's (1956) views hold
good even for the rodents.
4. Stomach structure of Cricetinae
All members of Muroidea are characterized by the presence
of a horny epithelium on the stomach whereas the subfamily
Cricetinae, in this respect is similar to the remaining members
of the Muridae family. However, the ratio of the areas lined
with horny or glandular epithelia, one-chambered or multi-
chambered stomach - all these are highly variable features. The
characteristics of the stomach structure of the subfamily
Cricetinae have none of the characteristics of the representatives
of this large family.
The stomach of Oryzomys couesi (Fig.49a) is one-chambere
ed and fornix ventriculi is raised above the opening between the
gullet and the stomach. Thanks to the loopshaped bend of the
lesser curvature of the stomach the opening between the gullet
and the stomach and the opening between the duodenum and the
stomach are close to each other. The borderline fold starts
close to the right hand wall of the gullet and runs to the left. It
divides the horny and the glandular portions of the stomach into
two zones out of which the horny portion occupies a somewhat
larger area owing to the prominence of the fornices. There is
а prepyloric fold, well de veloped on the lesser curvature side of
the stomach. |
176
STOMACH STR UCT URE OF CRICETIN АЕ
The stomach of Nectomys squamipes (see Fig. 94b) has
a more primitive form than that of Oryzomis for it is sacculate,
the fornix ventriculi is only slightly above the opening of the
gullet; and the opening of the gullet and the outlet of the duodenum
are not close to each other. The borderline fold is shifted more
to the right than that in Oryzomys and passes along the right
wall of the gullet. However, the caecum is clear and the areas
lined with the horny and glandular epithelium are more or less
equal owing to the poor development of fornices. Fundic glands
line a large portion of fundus ventriculi, cardial glands remain
only on the boundary of the glandular portion of the stomach and
the well developed pyloric glands line the pylorus.
Fig,94: Stomach structure of hamsters, (a) Oryzomys couest Alston;
(b) Nectomys squamipes Brants, Original.
In Fig. 94-122 region of distribution of the glandular epithelium
is shown by vertical discontinuous dashes and the region of
distribution of horny epithelium with horizontal continuous lines,
Ventral view of the stomach is shown... Esophagus is shown at
the centre and duodenum on the left.
Further widening of the area occupied by the horny epithe-
lium, eminence of the fornix and individuation of the stomach
portions are observed in Calomyscus, Biom _ Re ithr od ontomys
and Peromyscus (Fig. 95).
Fig,95: Structure of the stomachs of hamsters of Reithrodontomyini and
Calomyscus. Original. (a) Calomyscus bailwardi Thom, ; (6)
Baiomys musculus Merriam; (c) Reithrodontomys megalotis
Baird; (d) ) Peromyscus $ (5. str.) leucopus Rafin; (e) Per.(s. str.)
maniculatus Wagn; @) Per (Haplomylomys) californicus Gam zl.
177
М.М. VORONTSOV
In_Calomyscus bailwardi (see Fig. 95,a) the fornix is
clearly noticeable perhaps with a weakly developed fold, separat-
ing the upper portion of the caecum, on its lesser curvature. The
esophagus and the duodenum are close to each other and there is
a clear isthmus between the horny and the glandular portions.
The borderline fold begins above the isthmus or on its right side,
then turns to the left and divides the stomach approximately along
the line on the right hand side of the esophagus. Owing to the
deve lopment of the fornix, the area lined by the horny epithelium
is slightly more than the glandular area, the fundic glands occupy
a considerable area and are highly raised close to the borderline
fold.
The structure of the stomach in Baiomys musculus (see
Fig. 95b) is very much similar to this. In Reithrodontomys
megalotis (see Fig. 95b and 96) the horny epithelium along the
lesser curvature penetrates farther and farther into the pylorus
portion, the plica angularis dividing the stomach into subdivisions
is well developed, and there is the plica cardialis which to some
extent separates the caecum of the fore stomach. In front of the
fundic gland region, the borderline fold has well developed uni-
serial villi, which at the fundic ventriculi attain a length of 3 mm.
These villi, demarcate the fundic region slightly from the side of
the gullet and the horny zone of the stomach.
' Species of the genus Peromyscus studied by us were charac-
terized by the horny epithelium spreading along the pyloric
portion. In Peromyscus (s. str.) leucopus and P. maniculatus
(see Fig. 95d, c) the fornix is very eminent thanks to the high
eminence of fornix ventriculi. A sharp increase in the size of
the horny forestomach and a high development of the isthmus and
plica angularis give the impression that the stomach is divided
into separate portions similar to the present palearctic
Fundic glands are found only ona small portion of the fundal
region.
The stomach of Peromyscus (Haplomylomys) californicus
(see Fig. 95, f, and 97) is still more complex. If the distribution
of the horny and the glandular epithelia is similar to those of the
representatives of the subgenus Peromyscus (s. str.), the form
178
Fig. 96:
STOM ACH STR UCTURE OF GRICETIN АЕ
Structure of the stomach of Reithrodontomys megalotis Baird.
The stomach is demarcated into horny and glandular portions
only slightly. Froin specimens from the collection of Zoological
Institute, Acad. of Sciences, USSR, №. 18878.
С - cardi; co - horny epithelium; dv ~ glindular diverticulum;
du - duodenum; fr - fornix ventriculi; gf - borderline fold beiween
horny and glandular portions of stomach; gf - borderline fold
between stomach and duodenum; gl - glandular epithelium;
isth - isthmus between the left and the right portions of the
stomach; т - section of the muscular layer; ое - esophagus;
od - oryphicium diverticuli; P - pylorus; pl. ang. - plica
angularis; pl. card. - plica cardialis; pl. praepyl. - plica
praepyloricus and pp - pars pyloricus.
of the stomach is considerably complex. Plica angularis is well
de veloped and the isthmus between the left and the right halves of
the stomach is very noticeables:but, it is not so much аз in
Cricetini and Microtini. The pyloric portion which gets trans -
formed into an independent portion of the stomach thanks to the
well developed plica praepylorica and the corresponding ring
shaped isthmus, is well developed in Cricetinae. Thus Peromys-
cus californicus has a stomach more or less three-chambered,
179
М.М. УОВОМТ SOV
ie)
Ue. ine
ен
ау 9
м, UW
ву: ах
(+.
жа
pl.ang
Fig.97: Stomach structure of Peromyscus (Haplomylomys) californicus
Cambell. Original. Stomach more or less three -chambered,
horny epithelium developed maximum and the glands concentrated
only in a small area of the fundus ventriculi, From the co-
llection of the 2001. Inst., Acad. of Sc., USSR, №. 18384.
For legends see Fig. 96.
where the first chamber is the horny fore stomach with a remark-
able caecum, the second is the glandular, fundal region and the
adjacent fundal region with corneous epithelium and the third is
the horny pylorus chamber with very well developed muscles of
the pyloric sphincter.
The stomach structure of the North American insectivorous
hamsters, Onychomys, differs sharply from that of Reithrodonto-
myini. Both the species of this genus namely, Оп. leucogaster
189
STOMACH STR UCT URE OF CRICETIN AE
(Fig. 98) and On. torridus have a true two-chambered stomach
not at all homologous to the two-chambered stomach of palearctic
Cricetini. The entire glandular portion is arranged in the special,
isolated, caecal portion of the stomach - glandular diverticulum,
The stomach of Onychomys is loop-shaped with caecum fornix of
medium height and is lined from oesophagus to duodenum with
horny epithelium forming folds, but in the pylorus region, there
are thick, horny highly segmented rugae. At the fundus ventri-
Fig.98: Stomach structure of insectivorous cricetins Onychomys leuco -
gaster Wied. Original. Corneous epithelium extends from
oesophagus to duodenum, the corneous portion of the зютлсй 15
divided into two portions by a fold and fundus glands are concen -
trated in the diverticulum. Convergence with the stomach of
Pangolins, Manis javanica and parallelism with the stomach
of the hamsters, Orymycterus. For legends see Fig. 96.
181
=
М.М. VORONT SOV
culi there is a small aperture (ozyphiceum diverticuli) leading to
the chamber lined completely with fundus type glandular epithe-
lium, The aperture is more or less at the center of the spherical
upper part of this cavity and has a musculature around it forming
a special diverticular sphincter. The small size of the aperture,
the special sphincter and the typical position show that food does
not enter into the diverticulum. In fact, the diverticulum ventri-
culi of the stomach of Onychomys is a gigantic gland where gastric
juice is produced. This juice enters the corneous portion through
the diverticular aperture and breaks down the proteins primarily.
The form of the stomach in Manis javanica (Pholidota) is
very similar. In the Javan forms of Pholidota, all the gastric
glands are concentrated in the diverticulum on the fundus ventri-
culi, from where the gastric juice enters into the stomach lined
with the corneous epithelium - (Pernkopf, 1937). The sphincter
muscles are well developed in the pyloric portion and they put
the corneous "radulae" made of corneous epithelium into action.
The radulae (which are very well developed in Myr mec ophaga)
grind the solid chitinous parts of insects before they enter the
thin mucous intestine.
It is well known that the role of insects (especially Ortho-
ptera) in the food of Onychomys is very important. A continuous
corneous stomach and the closing of the glandular portion intoa
special diverticulum are the prerequisites for the changeover toa
predominantly (Onychomys) or exclusively (Manis) insectivorous
nutrition.
A similar mode of nutrition, with the predominantly protein
food substances causes a powerful development of the proventri-
culus. Proventriculus is a characteristic exclusively of Insectivora
and Chiroptera, The glandular portion is well developed in ham-
sters like Oryzomys, Nectomys and Sigmodon.
However, the transition to feeding on adult insects (termites,
ants and Orthoptera) does not present any new requirements from
the chemism point of view of gastric secretion, but requires pro-
tection of the fine glandular lining of stomach from coarse chitinous
parts which are difficult to digest. This has given rise independent--
Ty to a process of cornification of the stomach and separation of
182
STOM ACH STRUCTURE OF CRICETIN AE
the glandular region intoa diverticulum. This is observed in groups
groups very different from one another, suchas pangolins and
Cricetinae.
A remarkable feature of the stomach of Onychomys is the
well developed corneous prominences, in the pyloric region
surrounded by powerful pyloric sphincter muscles, These process-
es cannot even be called corneous "teeth" as in the case of Manis
javanica and Myrmecophaga, but, it is undoubtful that these play a
decisive role in the grinding of chitinous residues of insects before
the chyme enters the stomach. Features of ontogenesis of
Onychomys's stomach will be described in the special part.
The loop-shaped stomach of Onychomys and well de veloped
fornix suggest that the hamsters can feed on insects as well as
cellulose food. According toSperry, (1929) and Hall, (1946)
Onychomys fed on cellulose food in winter.
The stomach structure of Onychomys separates this species
from other forms of North American Cricetinae, including Baiomys,
Reithrodontomys, and Peromyscus. it is grouped with them
because of certain similarities in the structure of the dental
system. The stomach structure of Akodon arenicola (Fig. 99) is
very primitive and comparable only to that of Oryzomys, Sigmodon
and Neotomys. The stomach is one-chambered and sacciform.,
Fornix ventriculi is feebly marked. The borderline fold is shifted
more to the right of oesophagus and the area lined with corneous
epithelium is somewhat larger than the glandular portion. A major
portion of this glandular zone is lined with fundic glands.
Fig.99: Stomach structure of Akodon arenicola Waterh. After Vorontsov.
In their stomach structure the South American insectivorous
hamsters, Oxymycterus, differ sharply from Akodon. Oxymycterus
just as Onychomys have a glandular diverticulum whose existence
was first mentioned by Tullberg (1899). He wrote :
183
N.N.VORONTSOV
"Internally the stomach of Oxymycterus is lined entirely with
corneous epithelium, while the glands are restricted to a special
thickening on the wall of the greater curvature of the stomach and
open into the fundus ventriculi through a small aperture" (Tullberg
1899, s. 251).
Figures (Taf. XLI, 23, 24) drawn by Tullberg are very
small and do not reveal the detailed structure of this noticeable
formation in the stomach of the rodents. In his report on the
digestive system of vertebrates Pernkopf (1937) redrew the
sketch drawn by Tullberg erroneously and did not at all notice
the diverticulum. He considered Oxymycterus rufus as a form
with highly reduced glandular epithelium and even considered
this species lower than the field voles. The author (Vorontsov,
1957) himself has committed this mistake by following Pernkopf.
The structure of the digestive system of a related species,
Oxymycterus nasutus, was studied (Fig. 100) and found very
similar, in as far as it can be judged from the schematic dia~
gram and brief description given by Tullberg, to Ox. rufus in its
stomach structure.
The stomach of Ox. nasutus is sacciform, fornix ventriculi
is not marked and the main stomach-chamber is lined from eso-
phagus to duodenum with corneous epithelium of esophageal ori-
gin. At the base, opposite to the opening between the esophagus
and the stomach, there is a small aperture leading into an iso-~
lated blind chamber, the glandular diverticulum. The entire wall
of the diverticulum is lined with considerably high fundic glands.
The aperture of the diverticulum (as distinct from that of Ony-
chomys) is on the left edge of its upper wall and is surrounded
by a circular system of muscles forming a sphincter. Ав in
Onychomys, the diverticulum of Oxymycterus presents a
gigantic gland in which gastric juice is produced. This juice is
periodically supplied to the corneous portion by opening the
sphincter. Here the juice breaks down the proteins.
Unlike Onychomys, the pyloric portion in Oxymycterus
does not have any special corneous prominence for grinding the
chitinous residue of insects and is not separated from the
remaining part of the stomach. The pyloric sphincter muscles
are not so prominent as in Onychomys.
184
STOMACH STR UCT URE OF CRICETIN АЕ
Fig.100: Stomach structure of insectivorous hamster Oxymycterus rufus
Desm. Original. Corneous epithelium developed from esophagus
to duodenum, one-chambered corneous stomach and glands
concentrated in the diverticulum. For legends see Fig. 96.
The absence of a blind sac of the first stomach suggests
that cellulose food plays a minor role in the nutrition of Охутус-
terus. This agrees with our views that Oxymycterus is found
in the subtropic zone, where small invertebrates are active all
the year round. Remnants of earth worms were found in the dis:
sected stomach of Oxymycterus nasutus.
Palearctic hamsters (Cricetulus, Cricetus, Mesocricetus,
Phodopus) and African Mystromys have a true two-chambered
stomach.
The stomach of Mystromys (Fig.101) is divided, into two
well marked chambers, by the isthmus. The large corneous
fore stomach is situated on the left of the oesophagus and the
185
М.М. VORONT SOV
Fig. 101: Stomach structure of African hamsters Mystromys albicaudatus
Wagn. The entire corneous portion of the stomach covered with
villi. (a) Dorsal view, Original; (b) Stomach structure ventral
view, after Vorontsov (1962 b). For legends see Fig. 96.
glandular portions of the stomach and by their development
widely separates these chambers from one another. The
corneous epithelium and the borderline fold separating it
penetrate into the right hand side of the stomach only along the
lesser curvature.
A remarkable feature which helps in distinguishing the
stomach of Mystromys from that of all the remaining members
of Cricetinae is the development of corneous columnar papillae
covering almost the entire surface of the corneous fore stomach
except a small portion in front of the borderline fold. The
papillae are oriented along the direction of the food flow. The
height of the papillae is 2~4 mm. They are especially abundant
below the opening between the esophagus and the stomach,
although their number in the blind sac of rumen is very high.
Development of papillae considerably increases the area of
the corneous epithelium of the stomach. Besides, the complex
surface of the rumen creates conditions favorable for the growth
of the bacterial flora in the stomach. An increase in the surface
of the forestomach is obtained in certain species by an increase
in the volume of the forestomach itself, in certain others
186 |
STOM ACH STR UCT URE OF CRICETIN AE
(Hypogeomys antimena, Nesomyinae) - by fhe formation of addi-
tional folds in the forestomach, in a third group (Ruminantia) -
by dividing the forestomach into separate chambers and in a {$
fourth group (Myospalax, Myospalacinae) by the formation of a
villose structure on the forestomach. Development of a papil-
lary lining on the corneous portion of the stomach in Mystromys
in an important new acquisition which particularly accelerates `
the fermentation of the cellulose food substance.
The special feature of the stomach structure in Mystromys
is still one of the facts, showing that it is erroneous to group
Mystromys and the present palearctic forms of Cricetini in one
tribe.
The stomach structure of true palearctic Cricetini is of the
same type. All the four genera of this group have an actually
two-chambered stomach. The difference in the stomach struc-
ture of the individual species is, as a rule, insignificant (Fig.
102).
The two-chambered stomach of Cricetus cricetus (see
Fig. 102,g) consists of а left corneous portion and a right glandu-
lar portion, more or less of the same size. A small portion of
the corneous epithelium extends into the glandular portion along
the minor curvature. Fundic glands occupy a considerable por-
tion of the base of the right chamber. The well developed and
distinct corneous forestomach and the large area lined with
glandular epithelium show that the stomach is meant for pro-
cessing both protein and cellulose food substances. This com-
pletely agrees with the data given by А.С. Voronov (1947) who
has shown that Cricetus cricetus is omnivorous.
In its structure, the stomach of Cricetulus (Tscherskia)
triton (see Fig. 102,b and 103) is similar to that of f Cricetus.
But it differs from that of Cricetus in certain minor features
like the position of the borderline fold. Besides the corneous
epithelium does not project into the right hand side chamber of
the stomach along the lesser curvature.
The stomach of Cricetulus (Allocricetulus) eversmanni
(see Fig. 102, а and 104) differs from that of the two previous
187
N.N.VORONTSOV
Fig.102: Stomach structure оу the present palearctice Cricetini.
Two -chambered stomach: reduction in the area occupied by the
glandular epithelium. From Vorontsov's work (1957, 1962 b).
For legends see Fig. 96.
(a) Cricetulus (Allocricetulous) eversmanni Brandt; (b) Cricetulus
(Tscherskia) triton der Winton; (с) Cricetulus ($. str.) migra-
torius Pall. ; (а) Cricetulus ($. str.) barabensis Pall. ; (e) Crice-
tulus (s. str. ) longicaudatus Milne Edw. ; (f) Cricetulus (s. str.)
kamensis Satunin; (g) Cricetus cricetus Г. ; (В) Mesocricetus
raddei Nehr. ; (i) Mesocricetus brandti Nehr. ; Gj) Phodopus
sungorus Pall. ; (k) Phodopus roborovskii Sehunin.
forms by the high development of the borderline fold in addition
to the peculiarities in the structure of the glandular chamber.
Fundic glands are located at the bottom and further above along
the greater curvature to the pylorus. The glandular surface in
front of the pylorus forms а fold - a temporary form of separat-
ing the fundic gland region from the pyloric. The pyloric sphinc-
ter muscle is well developed. In the pyloric sphincter region
the glands are very well developed along the lesser curvature.
In its stomach structure Cr. eversmanni is more adapted among
the palearctic Cricetinae for the protein type of nutrition. The
stomach structure of Cricetulus (Allocricetulus) curtatus is simi:
lar to that of Cricetulus (Allocricetulus) eversmanni.
A tendency of the corneous epithelium to penetrate to the
right hand side portion of the stomach is observed in members of
188
STOM ACH STRUCTURE OF CRICETIN AE
fu
gt
Fig. 103: Stomach structure of rat-like hamster (Cricetulus: -(Tstherskia)
triton de. Winton); Stomach - - actually two -chambered, the
corneous forestomach is separated from the glandular portion
by . deep isthmuses. For legends see Fig. 96.
the subgenus Cricetulus (s.str.) among Cr. barabensis - Cr.
longicaudatus - Cr, migratorius - Cr. kamensis (see Fig. «102,
c,d, е and f). The corneous epithelium penetrates fairly well to
the right hand portion of the stomach along the lesser curvature
of the stomach in the last species (Fig.105). A reduction in the
area occupied by the fundic glands is also observed.
`` The stomach of the three species of the genus Mesocrice-
tus viz., М. auratus, М. brandti (Fig. 106) and М- —radgei i (Fig.
189
N.N.VORONTSOV
Fig. 104: Stomach structure of Eversmann's hamster, Cricetulus
(Allocricetulus) eversmanni Brandt.
From the specimen from Zavolshye, Division of the stomach
into corneous and glandular portion is well expressed; well
developed borderline fold is shifted to the glandular portion,
which is divided into pyloric and fundus regions by pre -pyloric
fold, For legends see Fig. 96.
107) - studied are identical. Minor details in the topography of
the borderline fold which may shift slightly to the right glandular
portion vary from individual to individual. A feature of the
stomach of Mesocricetus is the considerable development of
folds increasing the area of the corneous epithelium in the
cricetinae described above.
In Phodopus sungorus (Fig. 108) the corneous epithelium
spreads less to the right hand portion of the stomach along the
lesser curvature of the stomach than in Cr, kamensis.
190
STOMACH STR UCT URE OF CRICETIN AE
Fig. 105: Stomach structure of Kama hamsters Cricetulus (5. str.) kamen-
sis Satunin, According to the typical specimen from Kama
(Central China) Original. The borderline fold is shifted ‘to the
pyloric portion, the corneous epithelium begins to displace the
glandular portion from the second half of the stomach, For
legends see Fig. 96.
Stomach in Ph. roborovskii (Fig. 109) in which the corneous
epithelium is distributed even along the pyloric portion, the
pyloric glands are absent and the fundic glands limited by the
borderline fold are concentrated only on a relatively small
portion of the fundus ventriculi, differs from this type of
stomach. On the basis of the stomach structure we stated
(Vorontsov, 1957, 1960a) that the cellulose food substances
should play an important role in the mode of nutrition of Ph.
roborovskii than in the life of Ph, sungorus.
These hypotheses were confirmed by the results of the
studies оп the nutrition of Ph. roborovskii carried. out Flint
(1960), who convincingly proved the major role of cellulose
in the food of Ph. roborovskii in comparison with Ph, sungorus.
According to the stomach structure Ph. roborovskii is an
extreme member of the order in the degree of adaptation to the
191
N.N. VORONTSOV
Cx: RASA
NS И get
—
Fig. 106: Stomach structure of Transcaucasian.hamster Mesocricetus
я brandti Мей’. Original. For legends see Ех. 96.
pl.ang
Fig. 107: Stomach structure of Precaucasian hamster Mesocricetus raddet
Nehr. According to a specimen obtained from the vicinity of
Khunsakh, Daghestan, Original. For legends see Fig. 96.
cellulose mode of nutrition among the palearctic hamsters just
as Peromyscus californicus among the American hamsters.
192
STOMACH STRUCTURE OF CRICETIN AE .
Fig. 108: Stomach structure of striped harrytfooted hamster Phodopus
sungorus Pall, According to a specimen from the vicinity of
Kokchetav, North Kazakhstan. Original. For legends see Fig. 96.
\\ pl.card
Fig.109: Stomach structure of the Roborovskii hamster Phodopus
roborouskii Satunin. According to the specimen from Mongolia.
Original, 193
N.N.VORONTSOV
Based on their stomach structure, the palearctic Cricetini
form a monolithic group, quite different not only from the
American hamsters but also from Calomyscus and Mystromys.
The stomach structure of Sigmodon (Fig. 110) is very
primitive. The stomach is one-chambered, the fornix ventri-
culi is above the oepning between the esophagus and the stomach,
The borderline fold begins on the right wall of the esophagus and
then turns to the left.* Of all the forms of Cricetinae studied
Sigmodon has the lowest degree of development of the corneous
epithelium in the stomach, But the stomach structure of
Sigmodon is similar to that of Oryzomys, Nectomys and Akodon
and differs greatly from the other members of the family
Cricetidae.
Fig.110: Stomach structure of the hamsters, Sigmodon hispidus Say et Ord,
From Vorontsov (19626).
Neotomodon and Neotoma attain a considerable degree of
specialization for the cellulose mode of nutrition. In Neotoma
albigula (Fig. 111, а) and Neotomodon alstoni (see Fig. 111, с)
the fornix is very eminent, the corneous epithelium spreads
along the entire phloric portion of the stomach and the glands
remain only on the bottom right half of the stomach. The-left
and right halves of the stomach are separated by a shallow
isthmus marking the tendency for the formation of separate
portions, the stomach, however, remaining one-chambered.
The region where fundic glands are concentrated is a little less
the pyloric portion of the stomach into an independent portion,
* Earlier, the author has indicated erroneously that the glandular lining of
_ the stomach in Sigmodon separates the corneous epithelium of esophagus
from the corneous epithelium of the stomach. The description and figures
`(1 and 2) are based on the study of the badly fixed specimens preserved т
° Sptrtt for more than 110 years. When new specimens were obtained, tt
was clear that the description made-in the year 1957 was inaccurate.
‘This mistake was rectified in the subsequent work (Vorontsov, 1962 b).
194
STOM ACH STR UCTURE OF CRICETIN AE
Fig.111: Stomach structure of a few forms of Neotomini Original.
(a) Neotoma albigula Hartley; (6) Neotoma Потапа Ord. ;
(с) Меою modon alstoni Merriam. 4
which, however, is less developed in this species than in
Peromyseus, californicus,
The structure of the stomach in Cricetinae is quite
diverse. Forms with primitive sacciform stomach withhighly-
developed glandular epithelium, adapted mostly for pfoetin
nutrition (Oryzomys), species with two-chambered stomach of
the type of Cricetus, adapted for the mixed type of nutrition and
finally, certain hamsters (Phodopus roborovskii, Peromyscus
californicus, Nestomodon and Neotoma), with their stomach
structure highly adapted for the cellulose type of nutrition are
found among the members of this subfamily. On the whole, the
hamster tribes are clearly separated from one another in the
plan of their stomach structure.
On the basis of the study on the stomach structure the
following groups may be distinguished :
I, Oryzomys, Neetomys, Akodon, Sigmodon.
Il, Calomyscus, Baiomys, Reithrodontomys, Peromyscus
ПТ. Neotoma, Neotomodon;
IV, Oxymycterus;
У. Onychomys
УТ. Cricetulus, Cricetus, Mesocricetus, Phodopus;
УП. Mystromys
495
М.М. УОВОМТ5ОУ
Homologous sets of changes in the structure of the stomach
associated with the process of adaptation to the cellulose type of
nutrition taking place independently in the majority of these
tribes, are observed within each of these groups. corresponding
generally to the tribes classified by us. Members of the
various tribes (Peromyscus maniculatus and Neotoma floridana)
may be on the same levels of specialization and have similar
stomach structure in the general basic plan of the structure. It
should be noted that such a similarity is more frequently met
with in the structure of the dental system than that of the
stomach,
Along with the basic tendency for transformation of the
stomach, associated with the transformation from the protein to
the cellulose type of nutrition, there exists yet another tendency
i.e., the tendency for transformation into insectivorous mode
of nutrition, connected with the formation of the glandular
diverticulum ventriculi of the stomach (Oxymycterus, Ony-
chomys). The modes of transformation of stomach associated
with the transition to the insectivorous type of nutrition will be
dealt with in the next section.
a Data on the Ontogenesis of the Stomach in Onychomys_
Modes of Food specialization and Secondary Develop-
ment of Protein Nutrition in Insectivorous Hamsters.
How did the diverticulum ventriculus of the stomach
develop in the insectivorous hamsters ? Studies of the embryo-
nic development of the stomach of Onychomys (Fig. 112} give
an answer to this question, И
We had embryos of Оп. leucogaster representing three
different stages of development as presented by Dr. Pfeifer of
the USA, They were obtained one and a half month after catch-
ing and fixation; fixation of embryos was excellent.
First stage of embryos : body length’ 17.4 - 17.6 mm,
stomach length - 4.4 mm, Fornix ventriculi already expressed
and stomach divided into two subsections. Corneous epithelium
ae
* Body length of embryos was measured by their projection in ihe natural
position in the uterus. Thus, this is less than the actual body lengih.
196
ONTOGENESIS OF STOMACH IN ONYCHOMYS
Ee. 112: Development of the glandular diverticulum ventriculus т т-
sectivorous hamsters Onychomys leucogaster Wied.
(a) stomach structure of the embryo. The glanduiar portion is
only faintly separated from the corneous portions, the form of
the stomach reminds us of the stomachs of Peromyscus and
Microtus ; (b) stomach structure of a fully grown individual. The
glandular diverticulum ventriculus is a complex gland into which
the food does not enter, the gastric juice is secreted into the
corneous portion of the stomach. From Vorontsov (1962 6),
lines the entire left half of the stomach as well as its pyloric
portion. Glands (of fundus only) are concentrated at the fundus
ventriculi. The corneous epithelium forms many well expressed
folds in the forestomach, Strong hornifications in the form of
ridges and corneous ''teeth" in the pyloric portion are still not
observed. Glandular diverticulum absent. The fundic glands
are separated from the corneous epithelium. by the borderline
fold which is only slightly bigger than that in rodents (adult
individuals) like Microtus or Peromyscus. The form of the
stomach of Onychomys еп embryo of this stage reminds us of the
stomach of the adult Peromyscus leucopus.
The second stage of the development of embryos (body >
length 19.0 mm and stomach length 4. 7 mm) does not differ
much from the preceding one. The borderline fold is more
developed than in the preceding stage, However, the fundic
gland region is still not separated from the corneous portion.
In the third embryonic stage (body length 27. 8 mm and
stomach length 5.9 mm) the stomach has externally the same
formas in the previous stage, differimg only very little from
197
N.N.VORONTSOV
the adult stomach. The borderline fold gets thickened and
covers half the entrance into the region of glandular epithelium.
The fundic glands which extend hither from the fundic gland
region are located along the lower side of the thickened border-
line fold. The upper side of the boundary fold is lined with
corneous epithelium, The muscular layer which forms the
sphincter of the diverticulum in adults penetrates into the
boundary fold. The third stage studied by us correspond to the
embryos 1-3 days before birth. Thus the final formation of
the diverticulum ventriculus in the stomach of Onychomys takes
place fairly late and it indicates the relatively insignificant
growth of this adaptation.
Consequently, the glandular diverticulum of the stomach of
Onychomys (and there are reasons to suggest that this is observed
even in the ontogenesis of Oxymycetrus) develops by the growth of
the boundary fold and spreading of fundic glands on its lower sur-
face. Thus, the development of adaptation for protein nutrition
in the insectivorous hamsters, Onychomys and Oxy mycetrus has
different basis than that in the seed-eating hamsters of the type
of Oryzomys.
The stomach with the extreme distribution of the corneous
equithelium and reduction of glands to a small area at the bottom
i.e. , stomach which has a form adapted to protein nutrition is
the initial form which the stomach of insectivorous hamsters,
Oxymycterus and Onychomys are formed. Hence, a very impor-
tant conclusion may be drawn that the protein nutrition in insecti-
vorous hamsters is a later acquisition and that these forms have
changed over to protein nutrition secondarily.
Let us remind you that the original form of the stomach of
Murodidea is a sacciform structure with preferential develop-
ment of glandular epithelium. Then the process of displacement
of‘the glandular epithelium by the corneous epithelium starts in
the different groups of Muridae independent of one another.
Besides this only a few extreme types of hamsters (Peromyscus,
Neotoma, Phodopus robovskii) have attained that stage in which
the glands are restricted only to a small portion of the fundus
ventriculi. This is that form of the stomach which is more
adapted to processing the cellulose food substance and is the base
from which the stomach of insectivorous hamsters has developed
as a result of a number of secondary transformations.
198
ONTOGENESIS OF STOMACH IN ONYCHOMYS
Development of the stomach in insectivorous hamsters is
a clear example of the law of irr evers ibility of evolution estab-
lished by L. Dollo more than half a century ago.
The question whether there is a secondary change over to
protein nutrition in insectivorous hamsters and formation of
glandular diverticulum as "a game of chance", i.e., peculiar
secondary adaptation of two or three genera of hamsters or even
the really insectivorous фуре* of nutrition cannot arise on the
basis of the primary stomach (adapted to protein nutrition) or
seed-eating hamsters. The last hypothesis, which is paradoxical
at the first sight, is apparently true. Let us remember that
the forms of stomach in hamsters feeding on mostly or exclusively
on insects have a corneous lining for a major portion of the
stomach and a separate glandular diverticulum whose glands
produce gastric juice. The thick corneous lining protects the
stomach wall from solid chitinous parts of insects. The stomach
wall, as a rule, has powerful horny projections (''teeth'), that
may additionally grind chitin. A similar stomach structure is
found in Myrmecophaga jubata (Xenarthra) Manis javanica
(Pholidota) and Onychomys and Oxymycterus (Rodentia) described
here. I is interesting to note that the diverticulum ventriculus
is not developed in all the pangolins; thus, Manis longicaudata
(Pernkopf 1937) has a one-chambered stomach, where the
glandular field separated by the boundary fold has not yet de-
veloped into a diverticulum.
Development of the glandular diverticulum in different
groups of true insectivorous mammals suggests that the stomach
of Manis javanica meets the specific functional requirements,
1.е., maximum development of glands producing proteolytic
enzymes with maximum protection of stomach from rough chiti-
nous remains of insects.
It follows from the above that the stomach of the primitive
seed-eating hamsters, in spite of the well developed glandular
areas, cannot be taken as the morphological base from which the
stomach of true insectivorous hamsters would have evolved,
because of the poorly protected inner stomach wall. On the
тории
* In ecology the term insectivorous type of nutrition means ны not only
' on insects but also on molluses and worms.
199
М.М. VORONTSOV
contrary the stomach of seed-eating rodents with well developed
corneous lining (but with reduced glandular layer) was the base
from where the stomach of Oxymycterus and Onychomys has
developed. Thus, the true msectivorous type of nutrition could
develop only (or mostly) in forms which are more or less
adapted earlier to cellulose nutrition in its stomach structure.
Thus, in Cricetinae along with the basic trend of transform
mation of the digestive system from protein to cellulose type of
nutrition individual forms may secondarily change over from
cellulose to protein type of nutrition, thereby solving the old
functional problem (of proteolysis) on a different morphological
basis. The mode of development of insectivorous nutrition in
Onychomys and Oxymycterus is one of the examples where the
dialectical law of "negation of negation" and ''spiral'' develop-
ment manifest themselves.
6. The Structure of Stomach in Certain Rodents belonging to
Cricetinae (Nesomyinae, Myospalacinae and Lophiomy idae
а. Nesomy тае
Adaptive radiation in the structure of the stomach of the
Madagascar Nesomyinae is quite wide, although all members of
this group retain the general plan of the stomach structure of
Muroidea i.e., with two types of epithelium (Fig. 113).
By its structure* and degree of specialization for cellulose
nutrition, the stomach of Gymnuromys roberti (see Fig. 113, а)
highly resembles Oryzomys couesi. This one-chambered struc-
ture has a short fornix and a more or less equal distribution of
corneous and glandular epithelia.
The stomach of Macrotarsomys bastardi and M. ingens (see
Fig.113b and c) do not differ structurally much from that of
Gymnuromys, but the specialization for cellulose nutrition has
advanced а little further in these species than in Gymnuromys,
which is expressed by a slightly higher degree of penetration of
the corneous epithelium to the left half of the stomach.
a r
* According to the figure and description given by Tullberg (1899).
200
STOMACH STR UCTURE OF NESOMYINAE, ВТС.
oO
Fig. 113: Structure of the stomach in the Madgascar Nesomyinae.
(a) according to Tullberg (1889); (b to h) Original (a - Gymnuromys.
roberti Е. Major; (b) Macrotarsomys bastardi Milne - Edw. et
Grandid; (с) Macrotarsomys ingens Petter; (а) Eliurus tanala F.
Major; (e) Eliurus туохтиз; (f) Brachyuromys betsileonsis
Bartl; (g) Brachytarsomys albicauda Gunth; and (h) Hypogeomys
antimena. -
The stomach structure of Eliurus tanala and El, myoxinus
(see Fig. 113 d and e) is close to that of these species. However,
fornix ventriculi is more prominent. In spite of the similarity
201
N,N.VORONTSOV
in the position of their border-line fold with that of Macrotarso-
mys, the region of distribution of the corneous epithelium is re-
latively more than that of the glandular epithelium. In El. myoxi-
nus, there is an isthmus separating the upper part of the left
helf of the stomach from the remaining corneous portion. ME,
tanala the well-developed borderline fold has a fimbria of the
lobes, reaching a height of 2 mm and increasing the degree of
separation of the corneous: subsection of the stomach from the
glandular. It is not the fundus but the pyloric glands which
attain the maximum development in the right half d the stomach.
In both the species the stomach surface is lined with well expres-
sed ridges in the pyloric region. This considerably increases
the area lined with pyloric glands. It is as if the region of
development of the pyloric sphincter musculature is drawn out
о the stomach thereby forming an annular blind fornix of
he stomach, where pyloric glands develop. The corneous
epithelium extend a Little to the right half of the stomach along
the lesser curvature.
Basically, the morphology of the stomach of Brachyuromys
netsileoensis (see Fig.113,f) belongs to the-group of species
described above. High development of plica cardiaca consider-
bly separates the blind sac of the left half of the stomach.
~“lica praepylorica is well marked and it separates the pyloric
portion of the stoma from its remaining glandular portion. The
ratio of the glandular and the corneous epithelia is similar to
that in Macrotarsomys and Eliurus. Unfortunately, we did not
study the internal organs of a close subgenus and spec ies, Bra-
chyuromys ramirohitra; but a comparison with Br. betsileoensis
would have been particularly interesting.
Brachytarsomys albicaudata (see Fig. 113,g) which among
the forms of Nesomyinae attains the maximum degree of specia-
lization of stomach for the cellulose type of nutrition differs
considerably from the above described species in its stomach
structure. The fornix of the stomach has attained an unprecer
dented development not only among the forms of Nesomy inae but
aiso among those of Cricetinae, Gerbillinae and even Microtinae.
The left part of the stomach lined with the corneous epithelium
is well developed. There is a deep notch separating the upper
one-third of the corneous forestomach into a blind sac on its
202
STOM ACH STR UCTURE OF NESOMYINAE, ETC.
upper part, on the lesser curvature side. At the portion where
esophagus opens into the stomach, the stomach is constricted £
for a considerable distance and this leads to an almost complete
separation of the right and left halves of the stomach.
Thus Brachytarsomys has a two-chambered stomach like
the present Cricetini. There are four deep notches and folds
having the form of the lobes of omasum of ruminants on the side
of the greater curvature in the isthmus region. Corneous epi-
thelium penetrates into the right half of the stomach along the
lesser and particularly, along the greater curvature.
The structure of the glandular portion of the stomach is
also equally complicated. The region where fundic glands are
distributed is large, and stretches not only along the fundus but
also along the lesser curvature of the stomach. The surface of
the glandular portion of the stomach is complicated by folds
increasing the area of distribution of glands, especially in the
pyloric region. The deep fold at the beginning of the pyloric
sphincter clearly separates the pylorus from the remaining
glandular parts. In fact, the pylorus is separated into an *
independent chamber. However, the pyloric glands are distri-
buted not only in the pylorus but also in the region of the lesser
curvature in the penultimate chamber of the stomach. The
stomach of Brachytarsomys may be considered four-chambered,
where the first chamber forms an enormous corneous "rumen",
second small chamber ''omasum'", also lined with corneous
epithelium, third large chamber, the region of distribution of
fundus and a portion of the pyloric glands and the fourth small
chamber-pylorus, lined only with pyloric glands.
The stomach structure of the inadequately studied Madagas-
car forms of Cricetinae, Hypogeomys antimena (See Fig. 113,h
and 114) is very peculiar: The stomach is two-chambered. The
corneous portion of the stomach is separated from the glandular
not so much by the development of a constriction more right of
the esophagus and plica angularis as by the formation of powerful
annular valve of the borderline fold. The corneous, forestomach
is well developed, its inner lining has strong corneous folds and
the upper part of the forestomach on the lesser curvature side is
set apart by a notch separating the blind sac. The borderline
203
N.N.VORONTSOV
Fig. 114: Structure of the stomach in the Madagascar Hypogeomys antimena,
For legends see Fig. 96.
fold runs along the lesser curvature upto plica angularis, where-
as at the middle portion it runs опа level with the esophagus
and at the bottom, in the greater curvature the region stretches
a little into the right half of the stomach. The borderline fold
along the lateral wall attains a height of up to 5-7 mm, while the
entire width of the isthmus of the stomach is only 10-12 mm. It
may be noted that the borderline fold in the isthmus region has
three dilations formed at the place where the borderline fold is
not sohigh. The first of these dilatations is near the lesser
curvature at the place where the corneous epithelium penetrates
into the right half of the stomach, the second, more or less in
the glandular epithelium and the borderline penetrates deepest
into the left glandular part of the stomach and the third one is
near the fundus ventriculi in the greater curvature region where
the second zone of penetration of the corneous epithelium to the
right half of the stomach is located.
204
STOM ACH STR UCT URE OF МЕЗОМ У1М АЕ. ETC.
The grooves described above lead into the right glandular
portion of the stomach whoSe structure is very remarkable. The
entire right half of the stomach is formed by thick folds covered
with well developed fundus and pyloric glands. These folds,
almost connected with each other, sometimes interlocking
together thereby Separating the glandular portion of the stomach.
In fact they divide:the glandular portion of the stomach into
several separate chambers, pockets and diverticula.
The lower groove of the borderline fold leads the food flow
to the region of the fundus glands. The degree of their develop-
ment is fully comparéble with the glandular diverticulum of
Onychomys and Oxymycterus. At the top, the region of distri-
bution (more precisely the zone of exclusive development) of the
fundic glands is limited by thick folds which hang down converg-
ingly from the dorsal and the ventral sides of the stomach. These
folds prevent the entry of food upwards, where the middle groove
is extended. The food mass which has entered the fundic gland
region through the lower groove is separated immediately after
the borderline fold into two canals - ventrofundal ( and dorso-
fundal (П) by an outgrowth of the fundic gland region of the
stomach. This outgrowth has on its upper right hand side a
small aperture, leading into a closed, separate cavity - the
glandular diverticulum (Ш. It is not homologous with the
glandular diverticuli of stomach of Onychomys and Oxymycterus,
as it is formed not from the thick corneous borderline fold, but
owing to the joining of the edges of the paired folds arising from
the fundic gland region of the stomach and lined with the glandu-
lar epithelium. The aperture of the diverticulum from which
gastric juice is secreted is situated at the point where the flow of
food particles is divided into ventro and dorsofundal, where the
food mass is acted upon by the first portions of, probably, the
highly concentrated gastric juice. The food which has entered
the lateral canals is also split up under the action of the gastric
juice secreted by the fundic glands as well as the secretions from
the diverticulum. The food as it comes out of these paired
canals meets the fold on the ventral side. Asa result of this the
food particles coming out of the ventrofundal canal gets diverted :
to the dorsal wall of the stomach where it gets mixed with the
mass coming out of the dorsofundal canal. This region (IV)
situated along the greater curvature of the stomach above its
205%
N.N.VORONTSOV
fundic gland region, is also lined with fundic glands. There isa
dilatation almost in closed folds limiting the region of fundic
glands on the dorsal side of the stomach below the place where
the stomach gets converted into duodenum. Through the dilata-
tion the food enters the pylorus, also subdivided by folds and
outgrowths, lined with pyloric glands, forming pouch-like cavi-
ties and grooves. Thanks to the thick outgrowth of the pylorus,
the food entering the pylorus from the lower and middle grooves,
moves mostly along the canal arranged along the greater curva-
ture of the stomach (УЦ.
The middle groove of the borderline fold, entering into the
glandular portion of the stomach, soon gets divided into paired
dorsal (У) and ventral (VI) canals. The region of these canals
is lined mostly with pyloric and at some places with cardial
glands. There is а small funnel-shaped recess leading to the
unpaired pocket (IV) lined with fundic glands beyond the region of
diverticulum in the folds separating the middle digestive tract
from the lower. However, a major part of the food flowing from
the middle grooves enters directly into the pylorus, where it
gets mixed with the food particles of the lower grooves coming
out of the IV section and enters the pyloric canal (УП) running
along the greater curvature of the stomach.
_ Finally, the food particles, falling into the right half of the
stomach through the upper groove, after plica angularis, are
directed by the thick fold hanging from the lesser curvature, into
the paired ventral and dorsal grooves (VIII and IX). Passing
smoothly through these grooves, the food particles fall into the
paired canals, running along the lesser curvature of the pylorus
(X and XJ), from where the food enters the intestine. The last
upper tract passes along those portions of the stomach, that are
completely devoid of fundic glands. Here, the proteins may be
subjected only to a weak splitting action by the enzymes of the
pyloric glands.
Apparently the upper alimentary tract serves as a canal
for protein-free food and the middle one - for mixed food, where-
as the lower one serves as a canal for protein food. A similar
hypothesis based on the undisputed ''selectivity'' of the separate
sections of the stomach for biochemically different food masses
has already been mentioned. |
206
STOM ACH STR UCT URE OF NESOMY!NAE, ETC.
The extremely complex and peculiar structure of the
stomach of Hypogeomys helps us consider it as a multifunctional
formation adapted for a highly perfect treatment of protein as
well as for cellulose food. It is highly probable that Hypogeomys
feeds on small invertebrates for a considerable part of the year.
The remarkable features of the stomach structure of this species
should draw the attention of the ecologists for the ‘study of
nutr ition of this relict form.
The special features of the stomach structure in Nesomy-
inae speak of the remarkable heterogeneity of this group. How-
ever, the remarkable features of the stomach structure in
Brochytarsomys, makes this species of Nesomyinae somewhat
closer to Microtinae. Similarity of Macrotarsomys, Gymnuro-
mys, Eliurus and Brachyuromys with Cricetinae, Microtinae,
Gerbillinae and Murinae in their stomach structure does not give
any basis to group any one of these species with any of the above
mentioned subfamilies.
According to the stomach structure Nesomyinae is divided
into three groups, clearly distinguished from one another
Г. Gymnuromys roberti; Macrotarsomys bastardi, М.
ingens, Eliurus tanala, El. myoxinus, Branchyuromys
betsileoensis.
Il, Brachytarsomys albicauda and
Ш. Hypogeomys antimena.
b. Myospalacinae.
Stomach structure of zokors is very peculiar and it compels
us to separate them from Microtinae, Cricetinae and Spalacidae
to which they are related by many authors. The stomach is
strictly one-chambered (unlike Cricetini and Microtinae) and
fornix ventriculi is raised. The inner surface of the stomach is
clearly divided, according to the tissues lining it, into three
portions. Blind sac and fornix are lined with multiple petaloid
villi reaching a height of 5-7 mm. The histological structure of
the Villi was not studied owing to the unsatisfactory fixing.
207
N.N.VORONTSOV
Macerated vegetative parts of plants and very frequently hair
are found in the villose portion of the stomach.
The villose portion gets sharply torn in the left part of
the esophagus and the entire cardial portion is lined with
corneous epithelium common in the Structure of Muroidea. The
corneous epithelium has the form of a sector with its center
at the place where the esophagus opens into the stomach and
with an arch in the form of a greater curvature (Fig. 115).
ake
pee a
Fig.115: Structure of the stomach of the zokor Myospalax myospalax
Laxmann. Original.
The borderline fold extends on the right side of the eso-
phagus. The usual glandular portion stretches behind this.
The deep plica praepylorica on the lesser curvature side
partially separates the pylorus from the fundus.
Presence of a villose portion in the stomach of Myospalax
is a peculiar feature of this rodent. Well developed villi con-
siderably increases the area of the fermenting-macerating cavity
208
STOM ACH STRUCTURE OF NESOMYINAE, ETC.
whose function is carried out by the blind sac of the corneous
forestomach.
In its stomach structure Myospalax sharply differs from
voles, hamsters and spalacids. However, the development of
corneous epithelium in the stomach is a feature peculiar to
-Muroidea. This, undoubtedly, speaks of the affinity of zokors
to Muroidea and suggests us to disagree with the opinion of Р.Р.
Gambaryan (in litt.) that zokor does not even belong to Myo-
morpha.
The stomach structure of the zokor was first described by
Milne-Edwards (1868-1874) in a monograph, in which a good
figure of the stomach of Myospalax fontanieri was given. From
this it is clear that the blind sac is lined with corneous epithe-
lium. However, neither the morphologists specially descr ibing
the stomach structure of rodents (Oppel. 1896 and Pernkopf,
1937). nor the zoologists (Wings, 1924; Hinton. 1926: Ognev,
1947, 1948; Vinogradov and Gramov. 1952) who have made use
of his work for describing the characteristics of zokors have
paid attention to the indications of Milne-Edwards.
c. Lophiomyidae
The stomach of Lophiomys was described by Milne-
Edwards (1867) who determined this species for the first time
and grouped it in a separate family, Lophiomyidae. F igures of
stomach not dissected from the dorsal side (Pl. VIII, 6). and
the inner surface of the stomach (Pl. [Х, 3,4) are given in the
work of Milne-Edwards. It is clear from the description and
figures that forms of Lophiomys have a five-chambered stomach
(an instance unprecedented in the rodents). It is surprising that
such a feature in the stomach structure of Lophiomys had es-
caped the attention of taxonomists. who included Lophiomys in
different groups of rodents, and the morphologists, who studied
the morphology of the stomach of mammals (Pernkopf, 1937).
The stomach of Lophiomys imhausi (Fig. 116, g) is ex-
tremely complicated. The es ophagus opens into a U-shaped
corneous forestomach which stretches not only to the left of the
gullet where there is a short fornix ventriculi. but also to the
209
М.М. VORONTSOV
Fig.116: Comparative -anatomical representation of some forms of
Muroidea, that illustrates the possible stages towards the
development of a five-chambered stomach in Lophiomys Original.
(a) Nesokia indica Gray. One-chambered combined stomach with
predominant development of the glandular epithelium; (b) Oryzo-
mys couesj Alston. One-chambered stomach with more or less
equal development of corneous and glandular eipthelia; (c) Cricetus
cricetus L, Two-chambered stomach with more or less equal
development of the corneous and glandular epithelia; (d) Phodopus
robonovskii Satunin. Two-chambered stomach with predominant
development of the corneous epithelium; (e) Peromyscus cali-
fornicus Gamb, The stomach is almost three -chambered with the
predominant development of the corneous epithelium; (f) Hypothe-
tical ancestral form of Lophiomys; (g) Stomach structure of
Lophiomys , imhausi Milne -Edw. I - V portions of stomach (see
text),
right of gullet where it gives rise to a secondary fornix ventri-
culi. Beyond the secondary fornix there is a sharp constriction
which leads to the next descending portion of the stomach (I)
also lined with corneous epithelium. A well developed alimentary
canal along which food may enter directly into the descending
portion passing through the forestomach stretches from the
lesser curvature of the stomach down to the second portion of
the stomach has a deep isthmus beyond which starts the ascend-
ing portion of the stomach (1) also lined with corneous epithe-
lium. The duodenum begins from this ascending portion.
On the dorsal side of the corneous forestomach there is a
dilatation leading to an isolated blind sac, i.e.. corneous diverti-
culum ventriculus of the stomach (V), analogous to a similar
formation in swine (Sus). Thus, the stomach of Lophiomys
has four chambers lined with corneous epithelium.
210
STOM ACH STRUCTURE OF NESOMYINAE, ETC.
The absolutely corneous forestomach (I chamber) is homo-
logous to the corneous forestomach of the present hamsters and
voles. However, unlike these forms Lophiomys has a part of
its stomach, situated between the esophagus and plica angularis
and isthmus, considerably drawn out and bent forward and
upward.
The isthmus between the corneous forestomach (J) and the
descending portion (II) of stomach is homologous to the common
isthmus in the two-chambered stomach of the present hamsters
and voles.
The descending portion (II) of the stomach in Lophiomys,
is apparently homologous to the corneous part of the fundic gland
region situated beyond the plica angularis and isthmus. and
anterior to plica praephylorica in such forms as Peromyscus
californicus and Prometheomys schaposchnikovi.
The isthmus between the descending (П) and the ascending
(11) portions of the stomach is apparently homologous to plica
praepylorica and the ascending part of the stomach of Lophiomys
is homologous to the pyloric portion of the stomach in Peromy-
scus californicus and Prometheomys schaposchnikovi.
There is a formation similar to the corneous diverticulum
ventriculus of the stomach (V) of Lophiomys in certain hamsters
and gerbils thanks to the considerable development of plica
postcardiaca, which constricts the blind sac of the forestomach.
However, this blind sac is not arranged asymmetrically in
gerbils, certain voles and hamsters, unlike in Lophiomys. The
corneous diverticulum ventriculi and isthmus, separating this
chamber from the forestomach in Lophiomys are not homologous
to the blind sacs of the stomachs in hamsters, gerbils and voles,
and isthmuses, separating these sacs from the forestomach.
There is a small orifice leading into a completely isolated
glandular diverticulum ventriculi (IV) lined with fundic glands
on the wall of the descending portion (II) close to its base on
the greater curvature side. The opening of the glandular diverti-
culum ventriculi is quite close to the place of termination of the
esophageal groove. The opening leading into the glandular
diverticulum ventriculi of the stomach in Lophiomys is so small
211
N.N.VORONTSOV
that food does not pass into this area and the protein foods are
treated with the gastric juice secreted by the glandular diverti-
culum ventriculi, which in fact is a gigantic gland. in the fundic
gland region of Il and III chambers of the stomach (lined with
corneous epithelium) into which it is secreted. However, the
relative size of the glandular diverticulum ventriculi of Lophio-
mys is negligible in comparison with the analogous formations
in the stomach of Onychomys and Oxymycterus.
The ecology of Lophiomys is not studied completely. We
may assume, on the basis of the stomach structure, that cellu-
lose food has an exclusive role in the nutrition of this species.
The five-chambered structure of the stomach in Lophiomys
represents the extreme (among all the rodents hitherto
studied) degree of adaptation to cellulose nutrition.
It is apparent that in their phylogeny Lophiomyidae should
have passed through several complicated stages of stomach.»
which may be illustrated by the comparative anatomical series
from Nesokia indica to Oryzomys couesi, then to Cricetomys
gambianus and Cricetus cricetus to Phodopus roborovskii, to
Peromyscus californicus and Prometheomys schaposchnikovi
(the last twoforms already have a more or less three-chambered
stomach). Displacement of portions II and III of the stomach
with respect to one another and the beginning of the formation
of the glandular diverticulum into the IV-chamber and blind sac
into a corneous diverticulum i.e., the V chamber of the stomach
the V chamber of the stomach probably marked the next stage in
the transformation of the stomach in the predecessors of Lophio-
myidae. This stage has not yet been discovered among the
modern rodents. However it is undoubtful that Lophiomyidae
should have passed through this stage (see F ig. 16f).
The truly five-chambered structure of the stomach and
other features in the structure of the skeleton and respiratory
organs clearly distinguish Lophiomys from Cricetidae, The
classification of Lophiomys into a separate family Lophiomy idae
as proposed early by Milne-Edwards, and later by Tullberg
(1899) and Ellerman (1940-and 1941) is fully valid from this
point of view. It should be noted that Milne-Edwards' compara-
212
{
STOM ACH STRUCTURE OF EARLY MYOMORPHS
tive anatomical reasons for separating Lophiomys were in-
comparably more profound than those of W inge (1924) Stehlian
and Schaub (1950), Grasse et Dekeyser (1955) and other authors
who related Lophiomys to Cricetinae and even to the tribe
Cricetini.
The combined type of stomach structure ~ presence of
corneous as well as glandular linings of the stomach - along with
various other characteristics enable us tc include Lophimyidae
in the subfamily Muroidae in which these extremely peculiar
rodents of Abyssinian plateau occupy a special position.
he The Structure and Trends of Stomach Specialization in
Some mainly, Mysmorph Rodents (Gerbillinae, Micro-
tinae, Murid2e, Spalacidae, Gliroidea, Dipodoidea
and Bathyergoidea) - Homologous and Parallel Series
of Variability in the Rodent Stomach Structure.
A basic trend in stomach specialization is the transforma-
tion of the one-chambered stomach into two- three- and even
five-chambered one and distribution of corneous epithelium,
displacing the cardial pyloric and, partially, fundic glands,
characteristic not only of Cricetinae, Nesomyinae and Lophio-
myidae but also the entire Muroidae. However, the range of
variability of stomach is quite different for different groups.
In Gerbillinae (F ig. 117) mostly the single chambered
stomach is prevalent. All members of Gerbillinae have a one-
chambered stomach with more or less equal development of
corneous and glandular portions. But even among the members
of this extremely homogeneous subfamily of rodents, there may
be forms with a stomach structure adapted in different degree to
a mixed (with considerable fractions of cellulose food) type of
nutrition. Fornix ventriculi and the isthmus separating the left
corneous half of the stomach from the right glandular half are
rather poorly marked in Gerbillus pyramidum and Tatera
indica and in Gerbillus dasyurus the plica postcardiaca separates
the blind sac of the carneous forestomach into an almost
independent chamber. ‘he isthmus between the corneous and
the glandular portions of the stomach is clearly expressed in
members of the genera Meriones, Psammomys, Brachiones
and Rhombomys ,but the process of extension a the corneous
213
N.N.VORONTSOV
Fig.117: Structure of stomach in Gerbillinae. Ventral view, schematic.
Stomach structure varies less in this subfamily. A tendency to
increase the area occupied by the corneous epithelium is observed
and the stomach begins separated into two chambers, From
Vorontsov (1962 b). (a) Gerbillus pyramidum Goeffr. ; (b) Gerbi-
llus dasyurus simoni Lataste; (c) Tatera indica Hardwicke; (а) _
Meriones (Paramerones) persicus Blanf; (e) Meriones ($. str.)
vinogradovi Heptner. ; (f) Meriones ($. str.) tamariscinus Pails:
(Е) Meriones (Pallas iomys s) unguiculatus Milne -E ~Edw. ; (h) Meriones
—-=—— —_— — + —
shawi Duvernoy; (j) Meriones (Pallasiomys) tristrami Thom. ;
(k) Meriones (Pallasiomys) 1 libycus Licht. ; (l) Meriones (Pallasio -
mys) ex yilmourus Gray. ; (m) Mer tones (Pallasiomys) crassus
Scully; (о) Psammom пу5 $ obesus Cretzsch. ; (р) (р) Brachiones _
— ———-
przewalskii Biichner ; (q) Rhombomys opimus Licht,
epithelium into the right half begins in Мег. vinogradovi, М.
tristrami and M. crassus. In these species the fornix ventri-
culi attains a considerable height and the stomach is divided into
separate portions -right and left halves of the stomach fairly
clearly. Thus, a number of specializations in the stomach
structure for mixed and cellulose type of nutrition are also
observed among the members of Gerbillinae. The stomach in
Gerbillinae represents by and large the stomach of seed-eating
214
STOMACH STR UCT URE OF EARLY MYOMORPHS
forms and those with mixed type of nutrition. Not even one of
the species of Gerbillinae studied is adapted mostly or exclusi-
vely for cellulose nutrition. By their stomach structure (as
well as by their basic ecological features) gerbils form a
surprisingly homogeneous group of rodents. In the stomach
structure of Gerbils there is not a single feature which separates
them from Cricetinae, Microtinae and Muridae.
Diversity in the stomach structure is much more in
Microtinae (Fig. 118). Certain forms of Fibrini: Dolomys
bogdanovi, Clethrionomys glareolus and certain forms of
ео Bavicols terrestria, Altiocola Altiocola (Aschizomys) te lemmi-
nus, (s. str. ) argentatus, Lagurus luteus, Lag. lagurus,
have a а with more ог less equally deve developed corneous
and glandular epithelia; the stomach in all the voles are two-
chambered: left chamber is always corneous while the right
chamber may be both corneous and mixed (glandulo - corneous).
In most of the voles the horny epithelium extends a little into
the right lalf of the stomach. This process of extension of the
corneous epithelium and its displacement by pyloric glands is
observed not only in different tribes of voles, Fibrini, Microtint
and Ellobiini but also among the different genera such as
Glethrionomys and Ellobius.
Maximum diversity in the degree of development of the
corneous and glandular epithelia is observed among the members
of Fibrini. The stomach structure of Dolomys bogdanovi
resembles that of the hamsters, like Baiomys musculus,
Calomyscus bailwardi or Reithrodontomys megalotis; the isth-
mus is not so well e3 expressed as in Cricetini and Microtini and
the corneous epithelium extends only toa small part in the right
half of the stomach. In Clethrionomys glareolus the stomach is
clearly divided into two chambers, but the distribution of the
corneous and the glandular epithelia remains the same as in
Dolomys. In Clethrionomys rutilus the corneous epithelium
extends into the right half of the ‘stomach and lines the entire
pyloric portion. Glands are restricted to a small area in the
fundic gland region. It is paradoxical that the sharp differences
in the stomach structure of Cl. glareolus and Cl. rutilus are
just the opposite of the differences in their ecological species
(For details see Vorontsov, 1961 b).
215
N.N.VORON TSOV
The stomach of Prometheomys schaposchinikovi is more
specialized for cellulose nutrition not only among the members
of Fibrini but also among the entire Microtinae. By its stomach
structure it highly resembles Peromyscus (Haplomylomys)
californicus. Plica postcardiaca (but not plica angularis as in
Pr, californicus) separates the blind sac of the corneous fore-
‘stomach to form ап independent chamber, plica angularis divides
the second chamber of the stomach, fundic glands are located
at the bottom, the corneous epithelium runs along the lesser
curvature of the chamber and the extensive pyloric portion lined
with only corneous epithelium, forms a third chamber of the
stomach.
The process of cornification of the pyloric portion is
observed in the tribe Ellobiini. The stomach in all the species
of the only genus of this tribe - Ellobius is strictly two-
chambered, In Ell. lutescens the corneous epithelium extends
into the pyloric portion along the lesser curvature before duo-
denum whereas there are pyloric glands up to the duodenum
along the greater curvature. A similar stage of penetration of
the corneous epithelium in to the right half of the stomach is
observed very rarely as it is apparent that immediately after
this stage the corneous epithelium spreads along the greater
curvature and the borderline fold restricts the fundic glands to
only a small portion in the fundic gland region.
Among all the species of rodents studied so far, this stage
of penetration of the corneous epithelium into the pyloric
portion, through which all species of Muroidea with stomach
specialization for cellulose type of nutrition have passed, is
found only in Ell, lutescens. In ЕЦ. talpinus the corneous epi-~ —
thelium is already distributed along the entire pyloric portion.
The pyloric glands separated from the corneous epithelium by
a small portion of the borderline folds are restricted only toa
small portion near duodenum around the pyloric sphincter, The
main part of the borderline fold separates the fundic gland
region from the corneous epithelium of the right half of the
stomach, In ЕП. talpinus the glands are distributed in a сопз1-
derably larger portion on the fundic gland region (see Fig. 118 g
and h),
216
STOM ACH STR UCTURE OF EARLY MYOMORPHS
Fig. 118: Structure of the stomach in Microtinae. Ventral view, schematic.
There is a tendency for the division of the stomach into two and
three chambers and considerable extension of the corneous epi-
thelium from the cardial to the pyloric portion of the stomach,
The series is homologous to the series of hamsters and Gerbils.
From Vorontsov (196265) (a) Arvicola terrestris Г. ; (b) Clethri-
onomys rufocanus Sund. ; (с) Lagurus luteus Evesmann; (а)
Lagurus lagurus Pall. ; (e) Alticola (Aschizomys) lemminus Mill. ;
(f) Altiocola ($. str. }argentatus Severtzov; (g) Ellobius lutescens
Thom. ; (В) Ellobius ttpinus Pall, ; (i) Ondatra zibethica L. ;
(j) Myopus schisticolor Lill. ; (Е) Lemmus amurensis Vinogr. ;
(1) Lemmus obensis Brandt. ; (т) Lemmus Chrysogaster J. Allen;
(п) Lemmus lemmus Г. ; (0) Dicrostonyx torquatus Pall. ; (р)
Dicrostonyx hudsonicus Pall. ; (4) Microtus (Chionomys) gud
Satunin; (r) Microtus (Phaiomys) carruthersi Thom, ; ($) Microtus
($. str.) hyperboreus Vinogr. ; (И Microtus ($. str.) ungurensis
Kastschenko; (u) Microtus (s. str.) tortis Buchner; (v) Promethe-
omys schaposchnikovi Satunin.
217
N.N.VORON TSOV
Cornification of the stomach and its complete division into
right and left halves takes place in the tribe Microtini also.
Stomach of Arvicola terrestris is less specialized. Its division
into two chambers is not so clear as in more specialized
Microtini for almost the entire right half of the stomach is lined
with glandular epithelium. Division of the stomach into two
chambers is marked better in Lagurus luteus, Lag. lagurus,
Alticola (Aschizomys)lemminus and Alticola (s. str.) argentatus
than in Агу. terrestris, but here the corneous epithelium pene-
trates into the pyloric portion (true, into a small portion) along
the lesser curvature of the stomach. The separation of the
right half of the stomach from the left is more marked in the
members of the genus Lagurus because of the development of
crest-like, long villi, preventing the entry of food into the
fundus portion, on the borderline fold in the region of the greater
curvature. Members of the large genus Microtus, highly adapted
to the requirements of the cellulose food are characterized by
the reduction of glands to a small area on the fundus region and
distribution of the corneous epithelium along the larger part of
the right half of the stomach. (Microtus (s. str.) (arvalis, M,
(в. str.) oeconomus, М. (s. str.) hyperboreus, M, (s. str.)
agrestis, М. (5. str.) urgurensis, М. (5. str.) fortis, М. (Chio-
nomys) gud, M. (Chionomys) nivalis and M. (Pyajomys) car-
ruthersi have a similar stomach structure. The borderline fold
in many of these species has villi similar to those developed in
Lagurus in the isthmus region. The fundic glands occupy a
somewhat larger portion in the stomach of Ondatra than in
Microtus.
The stomach structure of Lemmini is more uniform, All
the members of this tribe of voles highly adapted to cellulose
nutrition are characterized by the distribution of the corneous
epithelium even to the pyloric portion. A decrease in the area
occupied by the fundic glands and the division of the stomach into
left and right chambers are traced in Lemmini from Myopus
schisticolor, Lemmus amurensis and Г. obensis to Dicrostonyx
husdonicus and D. torquatus through L. chrysogaster and L.
lemmus.
Thus the trend in the transformation of stomach structure
for better adaptability to digest cellulose food and the morpho-
logical basis for solving this problem is similar for Cricetinae,
218
STOM ACH STR UCT URE OF EARLY MYOMOR PHS
Gerbillinae and Microtinae. Hence a number of variations in
the stomach structure of all the three subfamilies (and also
Nesomyinae) seem to us as homologous series of hereditary
variations. Let us recall that their dental system also shows a
number of homologous variations.
It is remarkable that the adaptation of the stomach to
cellulose nutrition in Muridae (unlike its dental system) is solved
on the same hereditary basis as in Cricetidae. It is clear that
veriations in the stomach structure not less than those observed
among Cricetinae may be expected among the members of this
largest group of rodents. Probably, examples of surprising
parallelism in the stomach structure even with such abnormal
forms as Mystromys and perhaps even with Onychomys as well
аз Oxymycterus may be found out. It is highly probable that
the insectivorous rodents-African Deomys and Phillipine Rhyn-
chomys - possess a stomach with glandular diverticulum of the
type found in Onychomys. Even the simple material examined in
Muridae, enables us to establish that a number of variations in
the stomach structure connected with the transition to cellulose
nutrition (Fig.119) are homologous to those of Muridae.
Fig. 119: Stomach structure of certain forms of Митаае. Ventral view,
schematic. Tendency for transformation of the one -chambered
stomach йо а two-chambered one and penetration of the corneous
epithelium from cardial to the pyloric portion. The series is
homologous to the series of hamsters, nesomyins, gerbils and
voles. 6 and e - after Luppa (1956) a, с, d and f - original from
Vorontsov (19626). (a) Nesokia indica Gray; (b) Rattus norvegicus
Berk. ; (с) Micromys minutus Pall. ; (а) Apodemus sylvaticus Г..;
(e) Apodemus agrarius Pall. ; (Г) Cricetomys gambianus. __
The stomach of the bandicoot rat Nesokia indica is the
least adapted to processing cellulose food. This is a one
chambered sacciform formation in which the corneous epithe-
lium only starts penetrating along the greater curvature of the
stomach. The stomach structure of Nesokia illustrates the very
initial stages in the penetration of the corneous epithelium
219
N.N.VORONTSOV
from esophagus to the left half of the stomach in all the members
of Muroidae studied in this connection.
Further penetration of the corneous epithelium into the
stomach and its distribution to the right portion of the stomach
and the eminence of fornix are observed in the one-chambered
stomachs of Rattus norvegicus, R. rattus and Micromys minutus.
The structure of their stomach highly resembles the stomach
structure of Sigmodon hispidus and Oryzomys couesi.
The stomach of Apodemus sylvaticus and Ap. flaviocollis
divided into two considerably independent portions by the isthmus
and plica angularis is the next stage in the adaptation to cellu-
lose nutrition. The left chamber lined with the corneous epithe-
lium is the forestomach, while the right one is lined entirely
with the glandular epithelium. This stage in the transformation
of the stomach of Muridae is homologous to Reithrodontomys
megalotis and Calomyscus bailwardli.
In Apodemus agrarius the corneous epithelium lines the
entire pyloric portion of the stomach, but the glands are con-
centrated only at the bottom of the right half of the stomach.
The shallow plica praepylorica partly separates the corneous
pyloric portion. Thus, the stomach of Ap. agrarius has three
chambers partly separated from one another. But this division
is not so clear as in Peromyscus (Haplomyomys californicus}.
According to the degree of reduction of the glandular epithelium
and distribution of the corneous epithelium, Ap. agrarius is
the form (among the forms of Muridae studied) most specialized
for cellulose nutrition.
However, actual separation of the corneous epithelium
from the glandular portion is achieved in the actually two-
chambered stomach of Cricetomys gambianus, in which the entire
right half of the stomach is lined with glandular epithelium. By
its degree of specialization for cellulose nutrition the stomach
structure of Cricetomys gambianus is homologous to the
stomach of Cricetus cricetus.
By the stomach structure, Spalacidae also highly re-
sembles the representatives of voles and hamsters highly adapted
220
STOM ACH STR UCT URE OF EARLY MYOMORPHS
to cellulose nutrition. Spalax giganteus, Spi microphthalmus
and Sp. leucodon studied by us, have a similar stomach structure
divided by a deep isthmus into two chambers (however, this
division is not so clear as in Cricetini) and the corneous epithe-
lium lines the entire left and a major portion of the right half
of the stomach, whereas the glands are concentrated only ina
small portion at the base. It is certain that Spalacidae in the
process of adaptation to cellulose type of nutrition must have
passed through all the stages through which the hamsters,voles
and rodents have passed (or which now remain as little adapted
forms).
The stomach structure of Spalax differs sharply from that
of Myospalax and also other fossorial rodents (Geomys and
Cryptomys). This enables us to confirm that the fossorial mode
of life is not reflected on the structure of their digestive system
and has not caused far reaching convergence. Consequently, the
structure of the digestive system may give substantial hints
at judging the genetic affinity of these forms.
Thus, the glandular and the corneous epithelia in the sto-
mach (which clearly distinguishes them from the remaining forms
of Myomorpha), the tendency for the transformation of the one-
chambered stomach into two-, three- or even five-chambered
and more considerable distribution of the corneous epithelium and
the replacement of the glandular epithelium by corneous
epithelium, are characteristic features of Muroidea (Cricetinae,
Lophiomyidae, Muridae and Spalacidae). The processes of
transformation from protein to cellulose type of nutrition taking
place independently in different subfamilies and tribes of this
large group of mammals lead to analogous morphological varia-
tions in the stomach otherwise determined everywhere on an
analogous genetic basis (on the basis of the general plan of the
Muroidean stomach structure) withthe development of glandular
and corneous epithelia. Similar basic trend of specialization and
the singular morphogenetic basis in the trend of the stomach
structure of these forms lead to the fact that the homologous
series of variation in the stomach structure are observed among
the members of these eroups. The similarity in the Series of
homological variability of the stomach structure of Muroidea is
important and makes it possible to ascertain apriori that there
existed a form with the Nesokia indica type of stomach earlier,
Zea,
N.N.VORONTSOV
if not at present. This suggests that there should be forms with
the stomach similar to that of Oxymycterus and Onychomys among
the insectivorous members of Myoidae of Austrialia, New Guinea
and perhaps the South-East Asian Islands.
М.Г. Vavilov's law of homologous hereditary variation ¢
series enables us not only to understand the trend of the process
of adaptation but also to foretell about the morphological forms
which will be created or are already created as a result of the
evolution of this group by studying a relatively limited number of
forms.
Homology of different organs of the.same digestive system
affects, at different phylogenetic levels : thus, the homological
series of variability in the dental system are observed within the
different families - Cricetidae (Cricetinae, Nesomyinae, Micro-
tinae, Myospalacinae and Gerbillinae), Muridae (Murinae,
Dendromyinae, Cricetomyinae, Otomyinae and Hydromyinae) and
Spalacidae - but not among these families, whereas the homo-
logous series of the variability in stomach structure is traced
already within all the subfamilies of Muridae and Spalacidae
(Fig. 120). Owing to the change-over from protein to cellulose
type of nutrition this phenomenon of different levels of homology
not only in the different organs but also in one system of organs
shows that the systems based on a limited number of traits should
be studied carefully. Besides the phenomenon of different levels
of homology in the different organs highly facilitates the struc-
turing of phylogenetic system, which will be dealt with ina
separate chapter.
The same problem is solved in a different morphogenetic
basis and therefore, differently in other rodent groups owing to
the change-over from protein to cellulose type of nutrition. Ina
number of forms of Dipodoidea the stomach generally remains
one-chambered and completely glandular.
The method of transformation of the stomach in Gliroidea
(Eig. 121) is very remarkable. In Muscardinus avellanarius (an
extreme member of Myoxidae) the one-chambered stomach gets
converted into a two-chambered glandular-corneous stomach not
by the penetration of the corneous epithelium from the esophagus
into the stomach and the division of the latter into two portions
222
PSAMMOMYS
RHOM BOM YS
BRACHYUROMYS
BETSILEOENSIS
ARVICOLA
мо
a)
? |?
| es = .
|AR AGRARIUS
ЕНСНУ$ DIROMYS =
GRYPTGMYS
Fig.120. Homologous and convergent series of the variability in the stomach of rodents. The Gerbillinae, Nesomyinae, Microtinae и ат La Е are Lie to
column, row corresponds to the variability of the systematic group. The side branches one another. The series Muroidae, Myoxidea and Bathyergoidea are convergent lo
@re placed in the upper sub -row; the basic line of development is shown in the lower one another. Ро ед mean that the given plan of structure cameol be applied to the
sub-row. A row shows only the specialization stages, modern representatives having modern members of this group? It means that all forms of this group are not эко
corresponding stomach structure are called phylogenetic. The series, Cricetinae, and the gives plan of structure may be observed among species not yer Chats
STOM ACH STR UCT URE OF EARLY MYOMOR PHS
Fig. 121: Stomach structure of certain forms of Myoxidae. Ventral view,
schematic, A two-chambered stomach is formed in Muscardinuss
avellanarius L. as a result of the bulging of oesophagus. An т-
example of the convergence with Muridae. This series is not -
homologous to the series of Muridae -(a) according to Tuliberg
(1899); (b,c and а) original, from Vorontsov (1962, b)).
(a) Glis glis L. ; (5) Dyromys nitedula Pall, ; (с) Eliomis guercinus
L. ; (а) Muscardinus avellanarius L. ; (b-o) bulbus vesophagicus.
but by a special dilatation of the posterior end of esophagus named
the bulbus esophagicus. This new formation is functionally апа-
logous to the corneous forestomach of Muroidea. Special trabe-
culae grow in the corneous forestomach of Muscardinus. They
get connected with each other and form a reticular globular
structure embedded in the bulbus oesophagicus and remains аз
if it were the inner wall of bulbus oesophagicus.
A tendency for the transformation of the one-chambered
sacciform stomach into a two-chambered one without the pene-
tration of the corneous epithelium from the esophagus to the
stomach (a series from Georychus to Cryptomys through Myos-
calops; Fig. 122) is observed among Bathyergoidae (studied for
learning the extent to which the fossorial mode of life affects the
structure of the internal organs in the different groups of rodents).
Fig. 122: Stomach structure of certain forms of Bathyergidae. Vieu from
the central side, schematic. Vertical broken dash line shows the
region lined with glandular epithelium. The white portion shows
region lined with villose epithelium. A tendency for the transfor -
mation of the saccular one-chambered stomach into a tuechamber -
ed one without the penetration of the conreous epithelium from
oesophigus to the stomach is observed. Ан example of conver -
gence with Muridae (a - according to Tullberg (1899) and b and с
original, from Vorontsov (1962 b)). ‘a) Georychus capensis; (b)
Myoscalops argentes and (c) Cryptomys damarensis Ogilby.
22/3
N.N.VORONTSOV
It is remarkable that a villose epithelium develops in the left
half of the stomach in Cryptomys convergent with Myospalax and
Tachyoryctes. Apparently the function of this portion consists
of trapping the soil particles entering the stomach along with
food, apart from maceration of cellulose.
The number of series of transformation of the stomach in
connection with the transformation from protein to cellulose
nutr ition will undoubtedly increase after studying the digestive
system of all the large groups of rodents.
However, in groups clearly separated from one another (in
the studied examples, from subfamilies and above) the same
degrees of adaptation in the different series have only surface
similarity, caused as a result of convergence and may be called
the parallel variability series.
When variability among the species of each group is very
high, their stomach structure, unlike their dental system, is less
variable and more stable (in their general features) for the
representatives of a relatively larger group of rodents. This fact
should draw the attention of taxonomists. It fully agrees with the
law of least variability of endosomatic organs in comparison
with exosomatic as proposed by А.М. Severtsov.
224
CHAPTER V
EVOLUTION OF INTESTINE
1. General concepts and terminology
The intestine is divided into a small and a large intestine.
The intestinal wall is formed of tunica mucosa (which varies
greatly depending on the position i.e., the beginning, middle or
end of the intestinal canal) tunica submucosa, tunica muscularis
and tunica зегоуа. The tunica muscularis is formed of inner
circular and outer longitudinal layers of smooth muscles.
The surface of the small intestine may have been compli-
cated by the presence of folds, (plica circulares) into which the
tunica submucosa enters. The surface of the small intestine is
lined with villi (villi intestinales) and the depressions between the
villi are called crypts. In many cases the degree of development
of villi determines the total area of the surface of the small
intestine. |
The so-called Lieberkuhn's glands are located deep in the
crypts. These glands produce an alkaline secretion which con-
tains a number of enzymes like, diastase, maltase, lactase,
invertase, lipase, enterokinase, erepsin, etc. Liéberkuhn's
glands in the large intestine do not secrete any enzymes (Zavarzin
and Schchelkunov, 1954), but produce only mucus.
The histological change in the transition of stomach into
intestine (the pyloric glands in the duodenum is replaced by
Briinner's glands which secrete serous - mucoid secretion) is
not very.clear in those rodents in which the pylorus is lined with
pyloric glands, The transition of the stomach into intestine is
very clear in those forms where the pylorus is lined completely
225
М.М. VORONTSOV
with the corneous epithelium. Here the corneous epithelium is
replaced by the glandular and a part of the borderline fold,
shifted from the oesophagus-stomach opening to the stomach-
duodenum opening passes through the same spot.
The small intestine consists of duodenum (intestinum duo-
denum) and jejunum-ileum (intestinum jejunum- ileum). Duodenum
is not suspended fromthe mesentary. Вгбппег!з glands are locat-
ed inside the duodenum. Hepatic duct and pancreas open шфо the
duodenum. Immediately after its emergence from pylorus, the
duodenum may have an enlargement - ampula duodeni = which is
very clear in such forms as Peromyscus californicus and
Eliurus myoxinus. The place of transition from duodenum to
jejunum-ileum is detected by the presence of mesentary and
absence of Briinner's glands. The number of villi and Lieberkiihn's
glands decreases from jejunum to ileum (the boundary between
them is highly arbitrary).
There is a bush-shaped ileocaecal valve (valvula ileo-
coecalis) at the junction of the small and large intestines to be
more precise, at the junction of ileum and caecum (in the majo-
rity of the rodents). The large intestine begins after the valve.
The large intestine consists of a caecurn (intestinum caecum)
and the large intestine proper has a very long colon which leads
into the rectum having transversely striated muscles on its:
wall.
The large intestine has an epithelium, similar in structure
to that of the small intestine. However, its glands (here mostly
goblet cells are present) secrete only a slightly alkaline mucous-
serous secretion which does not contain any enzymes.
A minor section of the initial portion of the ileum may get
considerably dilated to the diameter of caecum and forms the
ampulla (ampula coli) here. The groove through which food
from ileum may enter the colon through caecum stretches along
the inner wall of the ampula coli. Functionally ampula coli is
a part of the caecum and while measuring the length of the
caecum we have taken into consideration the length of the
caecum and ampula coli.
226
EVOLUTION OF INTESTINE
Ostium caeco-colicum may be isolated considerably from
colon or it may not be developed at all. The degree of develop-
ment of this valve is quite diverse in different species of
rodents.
There is a well developed isthmus at the junction of the
dilated ampula coli and the real colon in the large intenstine
but in individual cases a special valve separating the caecum
"functionally'' from the large intestine may also develop here.
In the majority of rodents the colon, immediately after
its emergence from ampula coli, forms spiral-shaped involution.
The number of coils in this large intestine spiral is constant for
each species. In Muroidea it varies from 0-1 to 11-12 coils.
These coils form the so-called colic spiral (It is called by the
name ''Colonspirale'' by German authors).
The ascending part of the colon, immediately after the
colic spiral is highly complicated in a majority of the herbivo-
rous rodents. Additional blind processes (ampulae coli
accessori) analogous to the caecum develop in some forms.
These additional blind projections may develop into additional
caeca in certain mammals - Marsupialia (Hall and Rewell, 1954)
and Hyracidae (Jacobshagen, 1937).
The inner surface of the ascending and transverse portions
of the large intestine is complicated by right series of spiral
folds (Plica obliquae). A narrow longitudinal foldless strip
along which food mass that does not require further bacterial
action may quickly run along one side of the intestine in the
region where the spiral folds are located.
The additional blind processes and spiral folds consider -
ably increase the absorptive surface area and give rise toa
blind section where fermentation and splitting of cellulose take
place under the action of bacteria.
Usually the caecum is more complicated. Its surface may
be increased by the development of blind sacs (sacculi caecales)
and appendix. In certain forms (Lagomorpha and Spalacidae) a
high fold having the form of a ''spiral valve'' which surprisingly
resembles the real spiral valve of Selyakhii and chondrostei.
ГАР
М. М. VORONTSOV
This ''spiral valve'' divides the caecum into а number of рог -
tions isolated from one another.
The structure of the caecum and the ascending part of the
colon do not vary within a species but varies from species to
species and genera and is of interest to taxonomists. Much
attention was paid to the structure of this portion and the re-
lative “evelopment of the portions of stomach while studying the
structure of the intestine and the length of the small intestine
(without ampula coli) and the large intestine (without ampula coli
and п the colic spiral uncoiled) was measured.
A comparison of the measurement of the relative length
of intestine in freshly killed samples kept in formalin and spirit
has shown that fixation and its degree do not have much effect
on the relative dimensions of the intestine. However the abso-
lute dimensions of the intestine depend greatly on fixation.
Hence the data on the ratio of the length of intestines to that of
the body given below should be taken only as preliminary data.
A study of the relative length variability of the vole intes-
tine (Vorontsov 196]a) has shown that the measurement error
and individual variations do not exceed ЕЕ. 5% while measur ing
small and large intestines and + 0.6% while measuring caeca.
However, the error in the determination of the relative length of
the intestine may go upto +7.5%. Mvyrcha (1964) has specially
studied the individual, age and sexual variability in the size of
the alimentary canal in Clethrionomys glareolus. By establish-
ing the considerable age and sexual variability of the absolute
size of the alimentary canals, Myrcha has proved that the ratio
of the length of the portions of intestine to the total length of the
_intestine is constant. Thus, according to him, the relative
length of the small intestine varies from 58.7 +0 61. 8% that of
large intestine from 25.1 to 27.6% and that of the caecum from
12.0 to 14.2%. The ratio of intestine length to body length
varies from 6.178 to 8.06 times (Myrcha 1964).
2. Physiology of Intestinal Digestion in Rodents.
The food enters the duodenum from the pylorus through the
pyloric sphincter. The pancreatic and hepatic ducts open into
the duodenum.
228
PHYSIOLOGY OF DIGESTION
The pancreatic gland secrets enzymes of which trypsin
and erepsin split up proteins and diastase and maltose hydrolyze
carbohydrates. Pancreatic juice is alkaline in reaction owing to
the large amount of sodium bicarbonate contained in it.
Trypsin hydrolyzes proteins not only into albumin and
peptones but also into aminoacids at a pH = 8.87. The food
matter passing out of the stomach has an acid reaction. Split-
ting up of proteins by pepsin ceases in the duodenum owing to
the alkaline medium and bile inhibiting the action of = psin on
trypsin and trypsin and erepsin take the place of pepsin.
Bile acid salts are the coferments of amylase and lipase
secreted by the pancreas.
Intestinal juice secreted by the glands of the small intes-
tine wall is alkaline in reaction and contains enterokinase (as
activator of trypsinogen), erepsin, lipase and some enzymes,
that hydrolyze carbohydrates (Ginetsinskii and Lebedinskii
1956; Koshtoyants, 1950 and Lappa 1958b).
Although the alkaline medium of the small intestine is
favorable for the development of bacteria, it is the protein, fat
and carbohydrate splitting enzymes secreted by the organism
itself that play the main part of digestion in this portion. Lactic
acid bacteria develop only in the lower portions of the small
intestine.
Digestive enzymes are generally absent in the secretion
of the simple tubular glands in the caecum and the large
intestine. It is well known that enzymes breaking down cellu-
lose are completely absent in the secretions of the mammalian
digestive glands (Koshtoyants, 1950). The slightly alkaline
carbonate solution secreted by the mucous membrane glands
of the large intestine and caecum creates conditions favorable
for the development of bacterial flora and symbiotic protozoan
fauna (Koshtoyants, 1950).
The enzymes secreted by symbionts break down cellulose
first into cellobiose and then into dextrose.
229
N.N. VORONTSOV
According to the data of M.A. Velichko and T.M.Mokeeva
(1949) anaerobic bacilli decompos ing cellulose, yeasts that
ferment glucose, coliform bacilli fermenting glucose and lactose
and bacteria of lactic and butyric fermentation are observed
among the microflora of caecum. Flora of the small intestine
completely disappears in the caecum.
Although the chief digestive enzymes of the small intes-
tine are secreted at the anterior part of the small intestine i.e.,
duodenum the splitting up of calorific food (proteins, fats
and carbyohydrates) continues even in the lower portions of the
small intestine. This decomposed food is absorbed here only.
Hence it is considered that the degree of the relative de-
velopment of small intestine reflects the role of caloric food.
chiefly proteins, in the nutrition of this species.
Decomposition of cellulose by symbionts requires the
development of special "fermenting-macerating chambers"
the function of which is carried out by the caecum and the blind
processes of the large intestine.
The large intestine and caecum have developed not only
on account of an increase in their absolute and relative lengths
but also because of the considerable complexity in their
structure. That is why the data on the relative length of the
large intestine and particularly the caecum give somewhat low
indexes of their real role in digestion.
33 The Structure of the Intestine in Cricetinae
In the relative development of the portions of intestine,
Cricetinae, is the most diverse group. The range of variability
of the relative dimensions of the intestine in Cricetinae is more
or less equal to the range of variability of the entire Cricetinae
family. Seed eating hamsters of the tribe Oryzomyini, protein-
eating Akodon, insectivorous Oxymycterus and Onychomys and
seed-eating Peromyscus are characterized by a considerable
relative length of the small intestine. It is the small intestine
that is reduced most in the members of the genus Mesocricetus.
The degree of development of any portion of the intestine varies
230
STR UCT URE OF INTESTINE IN CRICETIN AE
depending more on the mode of nutrition than on the systematic
position of the species (Table 5).
TABLE 5.
Relative dimensions and relative development of the portions of the |
intestine in certain Cricetinae (according to Vogontsov, 1962 b, with
certain additions).
Species Relative length of Ratio of the length of the
а portion to the intestine to the body
total length of the length
entire intestine, %
Small Large Caecum
Akodon arenicola 85 12 3 8.0
Oxymycterus nasutus 85 10 5 5.0
Nectomys squamipes 80 14 6 8.4
Oryzomys couesi 80 15 4 i
Охутус!егиз refus* 78 18 | 4 4.8
Peromyscus californicus 74 16 10 3.5
Onychomys leucogaster 74 20 6 5.0
Peromyscus leucopus ; 73 21 6 3.6
Sigmodon hispidus 70 20 10 6.7
Baiomys musculus 67 27 й 3.3
Calomyscus bailwardi_ 63 29 7/ 3.8
Mystromys albicaudatus 63 29 8 3.8
Cricetulus longicaudatus 63 28 9 325
Reithrodontomys megalotis 62 29 9 Bz.
Cricetulus migratorius 62 28 1] 4.1
Peromyscus maniculatus 61 29 11 a)
Cricetulus eversmanni 60 28 14 3.5
23)
М. М. VORONTSOV
Phodopus sungorus _ 60 27 13 3.6
Phodopus roborovskii 60 27 13 3.2
Neotoma albigula 59 21 20 3:2
Cricetus cricetus 58 32 10 6.4
Neotomodon alstoni ce) 10 6.5
Cricetulus barabensis 56 31 13 3.4
Cricetulus triton 55 36 10 3.7
Cricetulus kamensis 54 34 13 4.0
Mesocricetus raddei 50 40 10 6.9
Mesocricetus brandti 48 42 10 5.8
Neotoma floridana* 42 47 1 5.7
* As per the data of Tullberg (1899)
The intestine of Oryzomys couesi (Fig. 124, a) is 3-4 times
longer than its body. Its small intestine is 4 times longer than
the large intestine and caecum. Caecum is small, simple in
structure and has only one isthmus. Colic spiral has 1 - 1.5
coils. Large intestine is not complicated by additional digestive
caeca and ampullae and does not have any spiral fold on its inner
surface. Large intestine consists of an ascending, a very short
transverse and descending columns. These columns do not form
any complicated coils.
Intestine of herbivorous Nectomys squamipes (see Fig.
123 b) is 8. 4 times longer than its body. Small intestine, as in
the case of the previous species, is 4times longer than the large
intestine and caecum. Considerable elongation of the intestine
as a whole increases the relative (in comparison with the size of
the body) length of the large intestine and caecum. The caecum
itself is very wide, has 2-3 isthmuses and 2-3 sacculi. However,
its structure on the whole is very simple (see Fig. 131, b). Its
functional volume increases Owing to 10-16 ampullae coli at the
beginning of the ascending column of the colon.» Many ampullae
coli extend along one side of the ascending column of the colon
while plica obliquae run along its other side. A similar structure
#32
Fig. 123:
STRUCT URE OF INTESTINE IN CRICETIN AE
Structure of the large intestine and caecum of certain forms of
Oryzomyini. Original. (a) Oryzomys couesi Alston; (b) Nectomy's
squamipes Brants. Legends for Fig. 123 - 141.
amp - ampulla coli - blind process between the small intestine
and isthmus of caecum; атр. асс. - additional ampullae coli after
the colic spiral; app - appendix; cae - caecum; cae"-= additional
caecal process; col - colon; cosp - coli of the large intestinal
spiral; it - intestinum tenue, plo - plica obliquae of the large
intestine; т - rectum; sac - sacculus - caeca near the depression
between the small intestine and additional caecal cavilies;vc,. -
valvula coli - valve separating the real caecum from ampulla;
and vsp - valcula spiralis of caecum.
col
cae
27 б@Е
Structure of the large intestine and caecum of cerlain forms of
Reithrodontomyini and Calomyscus. Original. (a) Reithrodonto -
mys megalotis Baird; (b) Baiomys musculus Merriam, (с) Pero -
myscus (5. str.) енеорн$ Rafin;.(d) Peromyscus ($. str.) mani
culatus Wagn. ; (e) Peromyscus (Haplomylomys) californicus.
Gambell; (f) Calomyscus bailwardi Thom, For legend see Fig. 123.
253
N.N.VORONTSOV
of the initial portion of large intestine considerably compensates
for the poorly developed caecum. The transverse column of the
large intestine is short while the descending column runs more or
less straight.
By their structure and relative development of the portions
of intestine, the seed-eating Baiomys, Reithrodontomys, Pero-
myscus and Calomyscus (the intestine is 3.1 - 3. 8 times longer
than the body) form a unique group.
Intestine is Baiomys musculus (Fig. 124, b) is 3.3 times
longer than its body. The small intestine is twice longer than the
large intestine and caecum. The caecum is small, but fairly
wide and has only one isthmus (see Fig. 131, в). The large
intestine spiral has only а halfturn. The large intestine is devoid
of ampullae coli, ampullae, plicae obliquae and consists of an
ascending column with numerous small bends, a short transverse
column anda short but straight descending column.
The intestine of Reithrodontomys megalotis (see Fig. 124 a)
is 3, 7 times longer than its body. Small intestine is longer than
large intestine and caecum less than double the caecum, developed
more than that in the previous species and divided by three
isthmuses into four portions though not completely separated
from one another (See Fig. 131, e). The colon is not coiled at
its beginning, but has asmall dilatation - the ampulla. The
transverse column of the large intestine is short, while the
descending column is long and straight.
The intestine of Peromyscus (Haplomylomys) californicus
(see Fig. 124, b) is 3.5 times longer than its body. The small
intestine is thrice longer than the large intestine and caecum.
Caecum is wide, relatively long (10% of the length of the
intestine) and has 3-4 isthmuses partially dividing it into
chambers (see Fig. 131, j). The large intestine forms a large
ampulla - a continuation of the caecum - after the caecum.
Colic spiral and plicae obliquae are not developed in the ascending
column of the large intestine. Ascending, transverse and
descending columns have several bends.
Intestine length of Peromyscus (s. str.) leucopus (see
Fig. 124, с) is 3.6 times more than its body length. Small in-
234
STR UCT URE OF INTESTINE IN CRICETIN AE
testine is twice longer than the large intestine and caecum. The
caecum (see Fig. 131, h) is short, but has three deep isthmuses,
separating it into sacculi, on its posterior side. Colic spiral,
ampullae and plicae obliquae are not developed. The branches
of the large intestine does not have any bends.
Peromyscus (s. str. ) maniculatus (see Fig. 124d) is an
omnivorous species in comparison with P. leucopus, but the
cellulose food plays an important role in its nutrition. Hence
the caecum and the large intestine are well developed in this
species, but the relative length of the intestine, longer than the
body length only by 3.1 times, decreases. The small intestine
is only 1. 5 times longer than the large intestine and the caecum.
The caecum (see Fig. 131, i) has four isthmuses dividing it into
five chambers, incompletely separated from One another. The
large blind ampulla formed at the pointwhere the large intestine
emerges out from the caecum is a continuation of the large
intestine. After the ampullae, the colon runs forward and only
at a certain distance away from the caecum does not get spirally
coiled forming 1.5 coils. The ascending and transverse columns
have knee-shaped bends while the descending column is straight.
The caecum and the large intestine are more complicated
in Calomyscus bailwardi (See Fig. 124, e) than in Reithrodonto-
myini. Its small intestine is 2.4 times longer than the large
intestine and caecum, while the intestine itself is 3. 8 times
longer than its body. The caecum (see Fig. 131, d) is divided
into three portions by two isthmuses. The middle one is sub-
divided from the anterior side forming four sacculi in the middle
portion. The hind-portion of the caecum forms an appendix
having two bends. The anterior part of the caecum ends in an
ampulla-dilatation at the initial part of the large intestine.
Beyond the ampulla, the caecum is spirally coiled forming only
an incomplete coil. 'Plicae obliquae develop on the inner surface
of the ascending column situated beyond the colic spiral. The
ascending, transverse and descending columns of the large
intestine may be highly curved.
The characteristics of the intestine structure in Calomyscus
bailwardi somewhat distinguishes this genus from Baiamys,
Reithrodontomys and Peromyscus, but do not bring it closer to
the forms of Cricetini. It should be noted that the variations in
S255
N.N.VORONTSOV
the intestine structure of Calomyscus and Peromyscus are much
less than that between the undisputably allied genera, Nectomys
and Oryzomy Se
A reduction of the caecum and the large intestine and an
increase in the size of the small intestine are observed in the
insectivorous hamsters of the genus Onychomys - On. leucogaster
(see Fig. 125, a) and On. torridus. The intestine is 5 times
longer than its body and the small intestine thrice longer than
the large intestine and caecum. The small caecum (Fig. 131, r)
is incompletely divided into 3 subsections by 2 isthmuses. The
colon has no colic spiral and plicae obliquae on its inner surface.
Accessory sacculi are absent; but the ascending column may
have 1-2 bends.
Fig. 125: Structure of the large intestine and caecum of Onychomys,
Akodon Oxymycterus and Mystromys; а - according to Tullberg
(1899); a,b,c, and e - original. (a) Onychomys leucogaster
Wied; (b) Akodon arenicola Waterh, ; (с) Oxymyctlerus nastus
Waterh. ; (а) Oxymycterus rufus Desm, ; and (e) Mystromys
albicaudatus Wagn. For legcnds see Fig. 123.
The intestine as such is large in Akodon arenicola, but
its caecum and large intestine are reduced (see Fig. 125, b).
Its intestine is 8 times longer than its body, while the small
intestine is 5. 7 times (maximum among the forms of Cricetidae)
longer than the large intestine and caecum. The caecum is small
in size (see Fig. 131, c) and very simple in form. There is a
single isthmus separating the terminal* portion of caecum from
its body. Colic spiral, plicae obliquae of the large intestine and
sacculi are absent in this portion. The transverse colon may
have 1-2 bends.
236
STRUCT URE OF INTESTINE IN CRICETIN AE
Secondary* reduction of large intestine and caecum (is
more marked in the insectivorous hamster - Oxymycterus
nasutus (see Fig. 125 с). The intestine is 5 times longer than
its body, while the small intestine, just as in the previous case,
15 5. 7 times longer than the large intestine and caecum. How-
ever, in comparison with the body length, small intestine, large
intestine and caecum are shorter than those in Akodon. In Ox.
nasutus the caecum is a wide sac partially divided into 2 sub-
sections by a small isthmus. A thick ampulla which becomes
one with the caecum adjoins the caecum (see Fig. 131, а).
Plicae obliquae are present on the ascending colon. The small
intestine does not have any colic spiral and sacculi. The large
intestine is very simple in form, the ascending colon is some-
what dilated in comparison with the transverse and descending
colons,
According to the description and figures given by Tullberg
(1899), a further reduction in caecum is observed in Ox. rufus
(see Fig. 125, а). Caecum in this species is a small sacculus
without any additional isthmuses, plicae and sections (see Fig.
131, e). The large intestine does not have any plicae obliquae
and just as in the previous forms does not form colic spiral and
sacculi.
The intestine structure of Mystromys albicaudatus (see
Fig. 125, e) is very peculiar. It is 3. 8 times longer than the
its body while its small intestine is 2. 3 times longer than the
large intestine and the caecum. The caecum itself (see Fig.
eS. в) и relatively small in size and has two sections more ог
less separated from one another, which.in their turn are sub-
divided by isthmuses. A very large colic ampulla (ampulla
coli) with size more or less equal to that of the actual caecum
separated from it by an isthmus adjoins the caecum. This
ampulla has a number of additional pocket-like outgrowths consi-
derably increasing the functional volume of the caecum, along its
greater curvature.
The colon has a noticeable bend - colic spiral primodium -
after the ampulla. Both bends of this curvature has accessory
* It is shown above (Chapter IV Section 5) that the stomach of Onychomys
ts secondarily adapted for protein nutrition.
237
N.N.VORONTSOV
ampulla coli. Ascending and descending colons may have
additional bends.
Thus in the Mystromys hardly half the volume of the blind
part of the intestine is on the caecum, A similar development
of additional sacculi in the large intestine portion, when the
caecum itself has a relatively simple form (a characteristic not
found in forms of Cricetini), clearly distinguishes Mystromys
from all palearctic hamsters with which this genus was grouped
by earlier investigators.
A progressive complexity in the caecum and its analogs
and a decrease in the relative size of the large intestine are
observed among the New World hamsters - Cricetini - from
Phodopus and Cricetulus to Cricetus and Mesocricetus. While
there is a general similarity in the structure of stomach (except
Ph, roborovskii) and dental system, considerable radiation is
observed in the structure and corresponding development of the
parts of the intestine among the palearctic New World hamsters.
Intestine of Phodopus sungorus (Fig. 126, a), is 3. 6 times
longer than its body while that of Ph. roborovskii (see Fig. 126,
b), 3.7times. The relative sizes of the portions of the intestine
are the same for both the species : their small intestines are
1.5 times longer than their large intestines and caecum. The
structure of the caecum lying adjacent to the colon varies consi-
derably among these species. In Ph. sungorus the caecum is
divided into four portions not completely separated from one
another by isthmuses. A large ampulla of the colon (see Fig.
131, m) joins the caecum. In Ph. roborovskii (see Fig. 131, a)
the caecum is more distinctly divided into 3-4 chambers. Each
of these chambers has small sacculi along the lesser and
greater curvatures. In its turn the ampulla of the colon is
subdivided into three portions by two isthmuses. As a result
the total surface area of the caecum portion is much larger in
Ph. rogorovskii than in Ph. sungorus. Colic spiral and plicae
obligue of the ascending column are absent.
The large intestine and the caecum are considerably
complex in the genus Cricetulus.
238
STR UCT URE OF INTESTINE IN CRICETIN AE
Fig.126: Structure of the large intestine and caecum portions of hamsters
Phodopus and Cricetulus (s. str.) Original. (a) Phodopus sungo -
ти5. Pall. ; - (6) Photo ps roborovskit Satunin; г. Cricetulus (Ss. str)
“able of Се. (5. эт. ) longicaudatus is 3.5 times longer
than its body, while its small intestine is 2. 3 times longer than
the large intestine and caecum. The intestine of Cr. (5. эк.)
kamensis is 4times longer than its body, whereas the small
intestine is 1. 2 times longer than the large intestine and caecum.
In Cr. (5. str. ) migratorius the intestine is 4.1 times longer
than its body; but the small intestine and caecum are 2.1 times
longer. In Cr. longicaudatus the caecum is divided into several
portions, forming two bends of the caecum by 5-7 isthmusés.
Ampulla of the large intestine lies adjacent to it. Colic spiral
and plicae obliquae are absent in the large intestine (see Pes
126, c, d and e).
In Cr. kamensis (see Fig. 131, p) the caecum is compli-
cated by the development of a sacculus close to the openiny of
the small intestine and greater separation of the portions of the
239
N.N.VORONT SOV
intestine from one another. Colic spiral and plicae obliquae
are absent in the large intestine of this species.
The caecum is still more complicated in Cr. migratorius
(see Fig. 131, qh Here the caecu т is divided into 10-12
chambers by isthmuses. There is a large sacculus, clearly
distinct from the caecum close to the place where the small
intestine opens into the large. There is a fold penetrating deep
into the caecal cavity and separating a major portion of the
caecum from its entrance onthe anterior part of the caecum.
The colon does not have ampulla and accessory ampullae, but on
the other hand forms a colic spiral having two coils. The
ascending and the transverse colons are bent and highly coiled.
The stomach structure of the representatives of the sub-
genus Allocricetulus is close to that of the species of the sub-
genus Cricetulus (s. str.) described above. Intestine of
Cricetulus (Allocricetulus) eversmanni (Fig. 127, a) is 3.5
times longer than its body, while its small intestine is 1.5 times
longer than its large intestine and caecum. The caecum (See
Fig. 131, t) has a fairly complicated form and is divided into
9-10 chambers not completely separated from one another by
isthmuses. Colic spiral forming one coil lies next to the caecum
beyond which stretches the ampulla. Intestine, forming a part of
the colic spiral and caecum has the same diameter as that of
caecum and large intestine ampulla and is functionally the conti-
nuation of the caecum portion. Plica obliquae is not developed on
the ascending colon. The transverse colon is highly coiled.
The intestinal structure of Cricetulus (Tscherskia) triton
(see Fig. 127, b) differs considerably from those of the repre-
sentatives oi the genus Cricetulus described above. The length
of intestine is 3. 7 times more than the body length. Its small
intestine attains a iength 1. 2 times more than that of the large
intestine and the caecum (see Fig. 131, s) is complicated by the
formation of outgrowths and isthmuses along the greater and
lesser curvatures. The caecum is separated from the large
ampulla of the large intestine by a deep isthmus near the point
where the small intestine opens into the caecum. Along the inner
surface of this ampulla, there are 4 plicae obliquae (homologous
to the plicae obliquae of the large intestine) on the greater cur-
vature side. The large intestine forms a colic spiral having:
240
STR UCT URE OF INTESTINE IN CRICETIN AE
cae
Fig.127: Structure of large intestine and caecum portions of hamsters,
genus Cricelulus and subgenera Allocricetulus and Tscherskia
Original, (a) Cricetulus (Allocricetulus) eversmanni Brandt, and
(b) Cr. (Tscherskia) triton de Winton. For legends see Fig. 123.
0.5 -1 coil beyond the ampulla and there are 4 ampullae coli in
the ascending colon beyond the spiral. The latter attains consi -
derable size and its external surface is complicated by short
outgrowths. The transverse and descending colons may form 1-2
branches.
The intestine of Cricetus cricetus (Fig. 128, a) is 6. 4
times longer than its body, while its small intestine is |. 4 times
longer than its large intestine and caecum. The caecum is large
in size and has 8 chambers clearly separated from one another
by isthmuses. The ampulla, formed directly by colic spiral
having only a single incomplete coil lies adjacent to the caecum,
There are two more ampullae lying above this in the ascending
colon. The ascending and especially the transverse colons are
highly coiled and branched.
The small intestine is reduced to the maximum in the
members of the genus Mesocricetus. The intestine in М. brandt
is 5. 8 times longer than its body whereas in_\1. raddel, itis
6.9times. In М. raddei (see Fig. 128, b) the small intestine is
equal to the length of the large intestine and caecum while in
М. brandti (see Fig. 128, b) the small intestine constitute only
0. 92 of the length of the large intestine and caecum. There
are 12-14 blind projections increasing the caecal surfacc along
241
М. М. VORONTSOV
Ею. 128: Structure of the large intestine and caecum portions of the intes-
; tine т hamsters, Cricetus and Mesocricetus, Original.
(a) Cricetus cricetus L. ; (b) Mesocricetus brandti Hehr, ; (с)
Mesocricetus raddei Nahr For legends see Fig. 123.
из greater curvature in М. brandti. The caecum is followed by
а large ampulla. The colic spiral which forms a single incomp-
lete coil lies next to И. Two accessory ampullae coli develop
at thebeginning of the ascending column.
| The caecum is more complex in М. raddei (see Fig. 131,
i) Large sacculi considerably increasing the volume of caecum
develop along the greater curvature of the caecum on its dorsal
and ventral sides. The ampulla is small in size and the colic
spiral has hardly developed. Just as in the previous species
there are two sacculi in the ascending colon.
The structure of the intestine especially that of caecum,
naturally distinguishes Mesocricetus from Cricetus and enabies
one to determine the basic differences in the morphology of the
intestine between М. raddei and М. brandti which Ellerman
(1949) has grouped in a single species.
The structure of the intestine of Sigrnodon hispidus (Fig.
129) is very peculiar. Here the intestine is 6. 7 times longer than
its body and the small intestine 2. 3 times longe~ than the large
intestine and caecum. The caecum is small in size and has two
oends divided into 4 chambers by isthmuses and has a.long
242
STRUCT URE OF INTESTINE IN CRICETINAE
Fig. 129: Structure of large intestine and caecum of cotton hamster.
Sigmodon hispidus Say et Ord. Original. For legends see Fig,
123:
appendix. There are two large ampullae increasing the volume _
of caecum by 1. 5 times (see Fig. 131, у) lying adjacent to the
caecum. The caecum has 4 bends including the ampallae. The
colic spiral having 2-3 coils begins immediately after the ampull-
ae. One of the coils of this spiral has a wavy outer surfaces
which increases the area of the large intestine. The ascending
colon has several bends.
The most complicated caecum among Cricetinae is found
among the representatives of the genera Neotomodon and Neotoms
In Neotoma fioridana (Tuliberg 1899, Fig. 130, a) the in-
testine reaches a length 5. 7 times more than its body. The small
intestine forms only 0. 7 of the length of the large intestine and
the caecum, Among the entire Cricetinae, it is in this species
Fig. 130: Structure of the large intestine and the caecal portions of certain -
| forms о} Nectomini; (a) according Tullberg (1899), and (6 and с)
original, (a) Neotoma flovidana Ord, ; (b}) Neotoma albigula
‘Hertley and. (с) Neotoma alstoni Merriam: For legends see Fig.
123.
243
М. М. VORONTSOV
that the large intestine attains the maximum development. The
form of cacecum (Fig. 131, y) is not very complicated, and doubly
bent. There are many shallow blind processes along the greater
curvature. The colic spiral has several turns. Ampulla and
plica obliquae are absent on the large intestine. The ascending
colon is highly curled and has 6-8 bends, while the transverse
and descending colons are of the ordinary structure.
Of.all the members of the Cricetinae, it is Neotoma albi-
gula (see Fig. 130, b) which has the most developed caecum but
its large intestine is reduced. Its intestine is 3. 7 times longer
than its body while its small intestine is longer than its large
inte stine and caecum by 1.5 times. The caecum consists of 4
bends. Moreover the numerous sacculi and ampullae coli on
the caecum are sometimes considerably separated from its
body. The caecum has about eight portions clearly separated
from one another. These chambers in their turn have accessory
plicae, isthmuses and outgrowths (see Fig. 131,2). Colic spiral
has four coils. The ampulla which considerably increases the
size of caecum is in between the colic spiral and the caecum.
The ascending and transverse colons have several flexures.
The intestine of Neotomodon alstoni is similar to that
described above (see Fig. 130,b). Its intestine is 6. 5 times
longer than its body - while its small intestine is 1. 4 times
longer than the large intestine and the caecum has 3-4 bends
(see Fig. 131,2), The chambers are fairly well separated from
one another owing to the development of isthmuses. There is an
ampulla of large intestine which continues as the colic spiral
with 3 coils. The large intestine does not have plicae obliquae
and necessary ampulla coli. The ascending, transverse and
descending colons have several flexures.
The structuge of the intestine of Ichthyomys is not des-
cribed in detail. Thomas (1896) mentions that he caecum of
Ichthyomys is not well developed. This suits to the protein
nutrition of Ichthyomy s. It is undoubtful that the reduction of
caecum, inthis form is connected with the secondary transition
to exclusively protein nutrition.
The structure of the intestine is quite diverse in Cricetinae.
Different degrees of intestinal adaptation for protein (Onchomys,
244
STR UCT URE OF INTESTINE IN CRICETIN AE -
Oxymyceterus and Oryzomys), combined (Cricetini) and cellulose
(Neotoma and Neotomodon) types of nutrition are observed among
the hamsters.
Cricetini is divided into several groups on the basis of
the intestinal structure:
~
Г. Oryzomys
П. Nectomys,
ПТ. Akodon, Oxymycterus, Onychomys*
Baiomys, Reithrodontomys, Peromyscus, Calomyscus,
У. Mystromys,
VL Cricetulus (5. str. ), Allocricetulus, Tscherskia,
Cricetus, Mesocricetus;
УП. Sigmodon; and
VIII. Neotoma, Neotomodon.
A tendency for the reduction of small intestine and enlarge-
ment and complexity of large intestine and caecum are observed.
The large intestine and caecum are complicated as a result of
their elongation, formation of isthmuses, plicae, sacculi
increasing the volume of caecum, formation of colic spiral coils,
ampullae, plicae obliquae and accessory ampullae coli in the
large intestine (Fig.131). However, an identical, uniform 4е-
velopment of all these characteristics is not observed in any one
of the above described species.
It is certain that-the processes of transformation of intes-
tine, Owing to the adaptation to one particular type of nutrition,
took place independent of one another not only in the different
tribes but also inthe different genera. In certain forms the
homologous variability first changed certain features, while in
some others certain other features changed. In certain forms
adaptation to cellulose nutrition took place at equal levels.
Judging from the structure of the intestine, the basic trend in
the evolution of Cricetinae was a change over from protein nutri-
tion to cellulose nutrition through combined nutrition. Forms
secondarily adapted for protein nutrition have reduced the
caecum and well developed small intestine.
* According to the descriptions (Thomas 1896) the piscivorous hamsters
Ichthyomys with hardly developed caecum also belongs to this group of
genera,
245
М. М. VORONTSOV
246
STR UCT URE OF INTESTINE IN CRICETIN AE
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247
N.N.VORONTSOV
It is interesting that forms primarily adapted to predomi
nantly protein (seed-eating) type of nutrition have relatively
shorter intestine (Peromyscus 3. 4-4. | times longer than the
body). The length of the intestine increases depending upon the
extension of transition to mixed and predominantly cellulose type
of nutrition (Sigmodon hispidus - 6. 7; Cricetus cricetus - 6. 4;
Mesocricetus raddei - 6.9; Neotomodon alstoni - 6.5). But in
forms secondarily changed over to the protein type of nutrition
them relative length of the intestine becomes more than that in
primarily seed-eating forms (Onychomys and Oxymycterus - 50;
Akodon arenicola - 8. 0). Im forms highly adapted to cellulose
type of nutrition the length of the intestine may be reduced
(Neotoma floridana - 3.7; albigula - 3. 7).
4. Intestinal Structure of certain Rodents Relating to Cricetinae
(Nesomycinae, Myospalacinae, Lophiomidae).
а. Nesomyinae
Nesomyinae is a group very much referred to interrelated
development of sections and morphology of intestine. But the
features of the structure of intestine do not facilitate the separa-
tion of Nesomyinae from Cricetinae.
The features for adaptation to the cellulose type of nutri-
tion, reduction of small intestine and complication of caecum
and large intestine can be very well traced in a number of forms
of Nesomyinae (Fig. 132, 133; Table 6).
Macrotarsomys bastardi has an intestine which is only
2. 8 times longer than its body fand is remarkably shorter than
the intestine of most of the Cricetinae with protein nutrition.
Caecum is small in size and has a very simple form and only
one isthmus; its structure highly resembles that of Oryzomys
couesi. The caecum is adjoining an ampulla, which is followed
by the large intestine, that does not form any соШе spiral
ampullae and plicae obliquae (see Fig. 132, а; 133, а).
The intestine of М. ingens in its structure is close to the
intestine of M. bastardi, but has peculiarities which justify the
view of Petter (1959a) who had treated this form as an inde-
pendent species. The intestine of М. ingens is 3. 6 times longer
248
STRUCT URE OF INTESTINE IN NESOMYINAE, ETC.
---
at ad
(MEDS
a
р
Fig. 132: Structure of large intestine and caecum of the Madagascar
Nesomyinae; е - by Tullberg (1899) and the rest Orig.
(a) Macrotaysomys bastardi Milne -Edw. et Grandidier; (b)
Macaotarsomys ingens Petter; (с) Brachyuromys betsileoensts
Bartl. ; (а) Eliurus tanala F, Major; (е) Gymnuromys roberti;
(f) Eliurus myoximus; (g) Brachytarsomys albicauda Gtinth;
(h) Hypogoemys апНтепа. For legends see Fig. 123.
than its body while its small intestine is only 1. 3 times longer
than its large intestine and caecum. The relative size of the
caecum is close to those of М. bastardi; the caecum is simple
and resembles that of the previous species. However, the small
249
М.М. VORONTSOV
TABLE 6.
Relative dimensions and relative development of the sections of the
intestine in Nesomyinae (Original)
Relative length of the Relative length
portion with respect to of the intestine
Species the total length of the with respect to the
entire intestine body length
Small Large Caecum
Gymnuromys roberti! Lae Fae 6 8.8
Brachyuromys betsileoensis 68 26 6 7.2
Macrotarsomys bastardi 66 25 8 (2.8
Eliurus tanala 58 26 16 4.6
Macrotarsomys ingens 57 33 10° 3.6
Brachytarsomys albicauda 53 24 22 4.2
Hypogeomys antimena 48 43 9 -
Eliurus myoxinus 42 39 19 2.6
° Т. According to the data given by Tullberg (1899).
intestine entering into the large intestine and outlet of the ~
large intestine are close together. There is no ampulla. Addi-
tional sacculi of colic spiral also are absent. Spiral fold is
developed on the ascending colon (see Fig. 132, b and 133b).
The length of the intestine of Brachyuromys betsileoensis
exceeds its hody length by 7. 2 times and its small. intestine is
2.1 times longer than its large intestine and caecum. The cae-
cum is fairly wide for a short length and is divided into four
separate chambers. The large intestine does not have any
ampullae, accessory ampullae coli, colic spiral and plicae
obliquae (see Fig. 132, с and Fig. 133, с).
250
STRUCT URE OF INTESTINE IN NESOMYINAE, ETC.
amp
g h
Fig. 133: Caecum and its analogs т the Madasgascar Nesomyinae; h - by
_Tullberg (1899); and the rest - Original. Complication of the
caecum and its division into sections are traced. The series
is homologous to the hamsters, voles and mice. (a) Macrotar-
somys bastardi Milne-Edw. et Grandidier; (5) Macrotarsomys
ingens Petter; (с) Brachyuromys betsi leoensis Baril. ; (4)
Eliurus tanala F, Major; (e) Eliurus туохтиз; (f) Brachytarsomys
albicauda Gunth. ; (g) Hypogeomys antimena; (h) Gymmuromys _—
roberti. For legends see Fig. 123.
The intestine of Eliurus tanala is 4. 6 times longer than its
body while its small intestine is 1. 4 times longer than the
large intestine and caecum. The caecum is large in size but
slightly segmented. Ampulla is absent. Colon does not form a
251
N.N.VORONTSOV
spiral. Plicae obliquae are not developed on the large intestine
(see Fig. 132, d and Fig. 133, а).
The intestine of El. myoximus differs sharply from that
of El. tanala. Its intestine is 2. 6 times longer than its body
wheress its small intestine constitutes only 0. 7 of the length
of the large intestine and caecum. However, these figures
cannot speak of the extreme reduction of small intestine. The
duodenum is very well developed; its width is equal to or greater
than the width of the stomach. The jejunum ileum portion is
highly complicated owing to the formation of many plicae and
spiral involutions of the intestine which greatly increases the
area of the small intestine, even if it is short. The caecum 18
more complicated than in El. tanala and has three limbs sepa-
rated from one another by isthmuses. The caecum has five
chambers. Ampulla and colic spiral are absent. There is
a spiral valve on the ascending colon (see Fig. 132, f and Fig.
81
The differences in the intestinal structure of El. myoximus
and Е]. tanala are so great that it is expedient to group these
species in two different subgenera.
Further complication of the large intestine and caecum is
observed in Brachytarsomys albicaudata. The length of the in-
testine exceeds its body length by 4.2 times whereas that of the
small intestine, by 1.1 times. The caecum has three limbs.
The middle one of these three limbs is divided into 2 clearly
separated portions by an insthmus. There is a large caecum
close to the place from where the large intestine begins.
Ampulla and colic зр!та} are absent. There is a spiral valve on
the ascending colon (see Fig. 132, р and Fig. 133, f).
Large intestine attains maximum development in Hypogeo-
mys antimena. Here the small intestine is only 0.9 of the
length of the large intestine and caecum. The form of the
caecum highly resembles that of Brachytarsomys albicaudata,
but the branching of caecum is still more pronounced - it
consists of three chambers. Sacculus is absent near the
beginning of the large intestine. Ampulla and colic spiral are
absent. The large intestine is complicated in the ascending
colon by considerable development of spiral valve; there is a
252
STRUCT URE OF INTESTINE IN МЕЗОМУ АЕ, ЕТС.
dilation (ampulla coli accessorius) whose inner surface also is
lined by spiral valve at the initial portion of the.ascending colon.
Ascending. transverse and descending colons heéve bends in-
creasing the length of this portion of the intestine (see Fig. 132,b
and Fig. 133, g).
In Gymnuromys roberti (Tullberg 1899) the development
of the caecum takes place by an increase in its surface owing to
the formation of many blind pouch-like outgrowths along the
greater curvature and not by a division of the caecum into
chambers. The large intestine forms a colic spiral having one
coil (see Fig.132,e and Fig. 133 h).
A tendency for the adaptation of intestine for cellulose
nutrition is traced in Nesomyinae. It is realized on the same
morphological basis as in Cricetinae. The number of spec ializa-
tions of the intestine of Nesomyinae for cellulose nutrition are
homologous to that of hamster.
By its intestinal structure, the forms of Nesomyinae
represent a widely radiated, but undoubtedly closely related
group of forms of monophyletic origin.
b, Myospalacinae
The structure of the intestine in zokors is very peculiar
(Fig. 134,b). In Myospalax myospalax the intestine is 7 times
longer than its body. The small intestine forms 56% of the
length of the entire intestine, large intestine -34 and caecum -
10%
The caecum has 2-3 bends and is subdivided into about 16
well separated chambers by numerous isthmuses and properly
arranged plicae. However, in Myospalax these plicae on the
inner wall of caecum do not have the form of "spiral valve"
unlike in Spalax. A very large portion of the large intestine
forming 5-6 ampullae, functionally one with the caecum lies
adjoining the caecum. The large mtestine immediately after the
ampullae forms a colic spiral having 1.5-2 coils. Intestine in
the colic spiral is 2-3 times wider than the large intestine and
has up to 10-12 ampullae. The ascending, transverse and de-
scending colons have numerous flexures and has many bends,
253
М.М. VORONTSOV
Fig, 134: Structure of the large intestine and caecum of certain fossorial
rodents, Pay attention to the "spiral valve" in the caecum of
Spalax, Original, (a) Geomys sp. (Geomyidae); (b) Myospalax
myospalax Гахт. -(Myospalacinae, Cricetidae); (с ) Spalax
leucodon Giildenst (Spalacidae), For legends see Fig, 123.
Peculiarities in the structure of the caecum and the initial
part of the large intestine distinguish Myospalax from Criceti-
пае,: Microtinae and Spalacidae with which certain investigators
have groupédd the zokors. This throws light on tlh independent
nature of this peculiar group of rodents.
с. Lophiomy idae
Milne-Edwards (1867) has described the caecum structure
of Lophiomys imhausi and has given a figure of caecum in his
work.
From the figure of the caecum given by Milne-Edwards it
is seen that caecum has a fairly simple structure (Fig. 135). It
is arch shaped and not differentiated into sections by isthmuses
and folds. The volume of the caecum is half that of the stomach.
A plica separating the caecum from the colon develops at the
caecum - large mtestine opening. Just after the isthmus the
large intestine forms an ampulla which continues as the colic
spiral with one coil. The spiral forming portions:of the intestine’
are dilated before the ampulla formation.
254
STRUCT URE OF INTESTINE IN NESOMYINAE, ETC.
Fig.135: Structure of caecum of Lophiomys imhausi Milne-Edw, (Lophio-
myidae). After Milne -Edwards (1967). For legends see Fig. 123.
In the structure of the caecum and the initial portions of
the large intestine Lophiomys does not at all differ from either
Cricetinae or other members of Muroidea.
5 Structure and trends of the Specialization of the Intestine
of some Rodents, mainly Myomorph rodents (Gerbillinae
Microtinae, Muridae, Spalacidae, Bathyergoidea and ©
Geomyoidea).
Homologous and parallel series of variability of the rodent
intestine.
A number of changes in the structure of the intestine
undergone on account of the change over from protein to cellulose
nutrition are traced not only in Cricetinae and Nesomyinae, but
also in other rodents allied to hamsters and far removed from
them.
a. Gerbillinae
A tendency for reducing the small intestine and complicat-
ing the large intestine and са сот (Table 7) associated with the
change over of certain members of Gerbillinae (Rhombomys
opinus, etc.) to mostly cellulose nutrition is clearly traced in
the series of Gerbillinae from Gerbillus and Meriones to
Rhombomys and Psammomys.
Just as in Cricetinae, the transition of Gerbillinae to the
cellulose nutrition leads not only to a change in the relative
255
N.N. VORONTSOV
TABLE 7
Relative dimensions and relative development of the divisions of the intestine
in Gerbillinae (from Vorontsova, 1962 b).
Relative length of the portion Intestine
Species to the total length of the length -
entire intestine % body length
Small — [а9е Са- ~—_—sratio
intestine intestine cum,
Meriones shawi 73 17 и 5.0
Gerbillus pyramidum 72 22 6 Le:
Gerbillus dasyurus simoni 68 25 ‘4 5.4
Meriones persicus 67 19 14 4.6
Meriones tamariscinus 65 25 10 5.6
Brachiones przewalskii 64 22 14 5.4
Meriones erythrourus 63 28 9 3.4
Meriones libycus libycus 61 26 12 4.6
Meriones vinogradovi 57 31 12 4.5
Meriones meridianus 2 f 31 12 4.1
Мег опез unguiculatus 57 34 9 5
Meriones crassus swinhoei 56 31 13 4.1
Tatera indica 56 32 12 3.9
Meriones tristrami 55 30 12 3.5
Rhombomys opimus 54 35 11 5.2
Psammomys оБезиз_ 47 38 15 4.4
256
STRUCT URE ОЕ INTESTINE IN NESOMYINAE, ETC.
development of the intestine and complication of the large
intestine and caecum, but also to the development of an ampulla
and colic spiral. Increase im the volume of the caecum owing to
the ampulla of the large intestine is faintly expressed in
Meriones persicus and М. tristramiand well expressed in М.
vinogradovi, M. meridianus, Gerbillus pyramidum and Tatera
indica.
Colic spiral is developed in all members of Gerbillinae
and has 1-3 coils. The colic spiral has only one coil in Gerbil-
lus pyramidum, Tatera indica, Psammomys obesus, Rhombomys
opimus, Meriones erythrourus, M. unguiculatus, M. crassus
and М. melanurus. Ш М. vinogradovi, М. meridianus, М.
persicus, М. tamariscinus, М. tristrami and Brachiones
przewalskii the colic spiral has two coils whereas in Gerbillus_
dasyurus and Meriones shawi it has three coils.
While there is considerable similarity in the structure of
the intestine and in the trend of its variability between Cricetinae
and Gerbillinae, Gerbillinae are characterized by а considerably
low range of variability in the intestinal structure.
b. Microtinae
The tendency for the reduction of small intestine and
complication of large intestine and caecum is well a in
Microtinae - а group adapted to cellulose food.
It is remarkable that while there is similarity between
Cricetinae and Gerbillinae not only in the trend of variability
of intestine but also in the methods of morphological resolution
of the associated problems, Microtinae, which is even more pri-
mitive in these species, differs from Cricetinae and Gerbillinae
by its considerable specialization for cellulose nutrition.
Dolomys and Prometheomys of Microtinae more primitive from
the point of view of specializations of the intestine may top the
corresponding orders of Cricetinae and Gerbillinae in their
degree of mtestihal adaptation to cellulose nutrition.
The range of intergroup variability of the intestine is
wider in Microtinae (Table 8 and Fig. 136) than in Gerbillinae
and even Cricetinae.
257
М.М. VORONTSOV
TABLE 8
Relative sizes and correlative development of the sections of intestine of
Microtinae (After Vorontsov, 1962 b, with supplementaries) .
Relative length of the Intestine length-
portions with respect to body length
Species the total length of the ratio.
entire intestine, %
small large caecum
intes- int es—
tine tine Ste ee
Clethrionomys glareolus! 50 27 13 72
Dolomys bogdanovi 55 31 14 6.1
Prometheomys schaposchnikovi 55 28 17 6.3
Lemmus chrysogast er 55 31 14 7.4
Lemmus lemmus 54 29 17 6.9
Alticola argentatus 54 30 16 6.1
Dicrostonyx torquatus 51 37 i 7.8
Aschizomys lemminus 50 35 16 7.4
Microtus (Chionomys) gud. 50 92 18 6.3
Microtus (s.str.) oeconomus 59 ay 14 5.7
Ondatra zibethica 50 35 16 7.2
Ellobius talpinus 49 32 19 4.7
Ellobius lutescens 48 33 19 4.2
ЕЕ ve > : “rf
Lemmus amuirensis 48 45 7 =
Myopus schusticolor 48 45 8 92
Lagurus lagurus 47 33 19 5.9
Microtus (5.str. )ungurensis 47 35 19 4.1
Microtus (Phajomys)juldaschi 46 41 14 4.9
Arvicola terrestri 45 39 16 7.8
Microtus (s,str.) agrestis” 45 39 17 7.4
258
Fig. 136 mys) fuldaschi Savertz.; 1 - Microtus
The| (s. str.) oeconomus Pall. ; 1 - Microtus
com (s, sir.) fortis Buchner; п - Microtus
пота (s. str.) argentatus Severtz. ; p - Alticola
(199 щеиз Eversmann; у - Ellobius lutescens
ae Fig. 123.
a
ro
Fig.136. Caecum and initial portion of the large iniestine of Microtinae.
The s@ties is arranged according to the degree of increase in dimensions and
complexity of caecum; caecum and its analogs are shown in black. The series is
hamologous to the orders of Cricetinae, Nesomyinae and mice. After Vorontsov
(1962, 7a ). а - Dolomys bogdanovi Martino; b - Prometheomys schaposchnikovi
Satunin; с - Dicrostonyx torquatus Pall; а - Myopus-s¢histicolor Lill. ; e - Lemmus
amurensis Vinogr. ; f- Lemmus 1етти$ L.; g - Lemmus obensis Brants; h - Microtus
(chionomys) gud Satunin; i - Micaotus (Phajomys) fuldaschi Savertz.; j - Microtus
(Phajomys) carruthersi Thom; k - Microtus ($. str.) oeconomus Pall. ; 1 - Microtus
($. sir.) hyperboreus Vinogr. ; т - Microtus (s. str.) fortis Buchner; п - Microtus
(s. str.) ungurensis Kastschenko; о - Alticola (s. str.) argentatus Severtz. ; р - Alticola
{Aschizomys) lemminus Mill. ; 4 - Lagurus шеиз Eversmann;r - Ellobius lutescens
Thom. ;‘s - Ellobius talpinus. for legends see Fig, 123.
&
у
aa
~
\
ws
att ай
STRUCT URE OF INTESTINE IN NESOMYINAE, ETC.
Microtus (s.str.) arvalis? 44 38 18 6.3
Neofiber alleni_ 43 44 14 6.8
Microtus (s.str.) michnoi 41 ; ЗИ 22 5.8
Microtus (s.str.) hyperboreus 40 42 18 4.6
Lagurus luteus 39 47 14 7.5
2. According to the data given by Т. Bee (1899)
3. According to the data given Бу М.Р. Naumov (1948).
The volume of the large intestine and caecum of Microtinae
increases as a result of their various adaptations: simple
increase in the size of the c@ecum and the large intestine,
development of large ampullae, very complicated colic spiral,
spiral valves on the ascending colon, complication of the caecum 7
by the formation of additional blind pouches, ampulla coli and
isthmuses. It is interesting that a simultaneous development of
all these characteristics and generally an equal level of adapta-
tion to each one of theee features is not observed in any species
of Microtinae.
The structure of caecum and large intestine is simpler in
the ancient and primitive forms of Microtinae, Dolomys bogdano-
vi, Here the caecum has only four chambers slightly separated
from one another and adjoined by an ampulla and a three-coiled
colic spiral. Spiral valves develop on the ascending colon
(see Fig. 136, a).
In Prometheomys schaposclmikovi also belonging to the
primitive tribe of rhizodental voles, F ibrini the size and the
branching property of caecum into sacculations and outgrowths
greatly increase. Ampulla consisting of two chambers also
increases. However, the number of coils of the colic spiral is
reduced totwo. The degree of development of pepiral valves
remains unchanged (see Fig. 136, b).
259
N.N.VORONTSOV
Dicrostomyx torquatus - a member of the tribe Lemmimni -
has a very simple caecum consisting of three chambers. The
size of the caecum increases 1.5 - 2 times owing to the develop-
ment of two ampullae; colic spiral has four coils. Spiral valves
are absent on the ascending colon (See Fig. 136, c).
The caecum is very much complicated in Myopus schisti-
color, Here, it consists of 12-14 chambers and sacculations
adjomed by 4 ampullae of the large intestine. The 7-8 coiled
colic spiral stretches beyond the ampullae (see Fig. 136, d).
The structure of the caecum of the genus Lemmus (See
Fig. 136, e,f,g) is much simpler than that in Myopus. This
spirally twisted structure is divided into 10-14 chambers by
shallow isthmuses. There is only one large ampulla in the
intestine. However, if caecum and its analogs are considerably
less developed in Lemmus than in Myopus, the colic spiral is
very well developed and has 11-12 coils in Lemmus obensis.
The spiral valve is not well developed on the ascending colons
of L. amurensis and L. lemmus and is developed only in L.
obensis.
According to the degree of development of the caecum,
the forms of Lemmini examined are arranged in the following
order :
Dicrostonyx torquatus -» Lemmus amurensis —>
~L. Lemmus > L. obensis + Myopus schisticolor
According to the degree of development of the spiral valve
“in the large intestine, the same species are arranged in another
order.
Dicrost torquatus
Myopus schisticolor
L. amurensis
Г.. Lemmus
Г. obensis
According to the complexity of colic spiral and increase in |
the number of its coils, the same species are arranged in yet
another order.
260
—
SS ee an oan
ИИ
Cricetinae
Nesomyinae
Cerbillinae
стола
huridae
Dipodidae
Mystricomershe
SS ll Cricetinae
I i
a a ae Nesomyinae р
Cerbillinae
Microtinae
Muridae
Dipodidae
Fiz.138. Homologous and parallel series of variability in the correlative dimensions of
intestine in certain groups of rodents.
The series are arranged ( from left to right ) according to the degree of the
decrease in the relative dimensions of small intestine (white) and increase tn the
relative dimensions of large intestine (black) and caecum (horizontal hatching),
Pay attention to the greater width of the range of variability of Cricetinze and
Nesomyinae as compared with Gerbillinze and Microtinae|
STR UCT URE OF INTESTINE IN NESOMYIN АЕ, ETC.
Dicrost. torquatus > Myopus schisticolor >
-> Г. Lemmus ~ Г. amurensis > Г. obensis
These facts show the non-uniformity in the rate of trans-
for mation of the individual parts of the digestive system (Voront-
sov, 1961, a and 1963, e) within a closely related group of
forms.
A progressive complication of caecum and large intestine
is traced in the tribe Microtini in the central polytypic genus
of this tribe, Microtus.
In Microtus (Chionomys) gud (see Fig. 136, h) and М. (Ch.)
nivalis, the caecum has a wavy surface along the lesser curvature
and is partially divided only into 3-4 chambers by shallow isth-
muses. Ampullae are absent, colic spiral has three coils,
whereas a spiral valve develops in the large intestine. Caecum
is complicated in the subgenus Phajomys but here the spiral
valve is poorly developed. In М. (Phajomys) carruthersi the
caecum is complicated by the formation of many shallow ampulla
coli along the greater curvature. The ampullae which also have
small saccular outgrowths along the greater curvature increase
the size of the caecum. Colic spiral is absent. There are two
accessory ampullae coli at the initial portion of the ascending
colon. The spiral-valve runs along the inner wall of these
ampullae (see Fig. 136, }).
The saccular outgrowths along the greater curvature are
better developed in M(Ph) juldaschi than in the previous species.
Caecum has two bends. Ampulla is present. Colic spiral has
5-6 coils, but spiral valve is absent in the large intestine (see
Fig. 136,i).
The caecum is complicated in the subgenus Microtus (s. str)
as a result of its division into a number of chambers by isthmu-
ses.
The caecum тм М. (s.str.) oeconomus (see Fig. 136,k) is
divided into 13-14 chambers. Ampullae absent, colic spiral
with two coils. A slightly developed spiral valve is present
in the ascending colon.
261
N.N. VORONTSOV
The division of caecum (into 10-12 chambers) is better
expressed in М, (s.str.) hyperboreus than in the previous
species. Ampulla is present. Colic spiral has 4-5 coils, but
the spiral valve is poorly developed im the large intestine
(see Fig. 136, 1).
Caecum ш М. (s.str.) ungurensis has two bends and is
divided into about 14 chambers by isthmuses. Ampulla is
developed, but the colic spiral has only 2-3 coils. In the large
intestine the spiral valve is poorly developed (see Fig. 136, n)
In М. (3. str.) fortis also the caecum has two bends, but
here it is complicatéd by lateral saccular outgrowths (in agree-
ment with Mesocricetus raddei) which are considerably separated
from the "Ъо4у"' of the caecum. Ampulla is small and colic
spiral has only 4-5 coils. Spiral valve develops not only in the
ascending colon but also on the transverse colon (see Fig. 136,m).
Intestinal adaptation of the genus Alticola to cellulose
nutrition is reflected by the complication of the caecum and the
increase in its absolute and relative dimensions. Meanwhile,
the number of coils in the colic spiral does not exceed 3-4.
Spiral valve is absent in the large intestine. Ampulla is poorly
developed.
in Alt, (s.str.) argentatus the caecum is complicated by
many annular. isthmuses. Their position corresponds to the
interior of caecum dividing it into 25-30 chambers. Ampulla is
absent; colic spiral has coils. There is a fourth rudimentary
coil also (see Fig. 136,0).
In Microtinae the division of caecum by isthumses and
formation of sacculi reaches the maximum in Alt. (Aschizomys)
lemminus. The number of chambers and appendices goes up to
30-35. Some of these chambers are considerably separated
from the body of caecum. Here a small ampulla is present.
Colic spiral has three coils (see Fig. 136,p.
Among Microtini and the entire Microtinae, large intestine
and caecum achieve maximum development in Lagurus leuteus.
Intestine is 7.5 times longer than its body, whereas the small
intestine forms only 0.5 of the length of the large intestine and
2 62
STRUCT URE OF INTESTINE IN NESOMYINAE, ETC.
the caecum. Caecum is large in size and is divided into 22-25
chambers separated from one another by isthmuses and well
developed plicae of the inner surface of the intestine. There are
many ampullae coli and sacculi along the greater and lesser
curvatures of the stomach. Ampulla is present. Colic spiral
has only 2 coils. A spiral valve develops in the ascending colon
(see Fig. 136,q).
According to the degree of development of caecum the
forms of Microtini studied are arranged in the following order.
М. (Chionomys) gud -> М. (Phajomys) carruthersi 2-м.
(Ph). juldaschi-» М. (s.str.) oeconomus --» M.(s.str.
ungurensis --> М, (s.s str.) hyperboreus --> м. ils: str } $. artis |
--» Alticola (5. str.) argentalus --> Alt. (Aschizomys $) temininus
--> “Lagurus luteus.
The same species are arranged in anothex order according
to the degree of development of spiral valve in the large intes-
tine.
`М. (ph. ) Juldaschi
Alt. (5. str.) argentatus
Alt. (Aschizomys) lamminus
м. (Ch. ) gud
(ph. ) carruthersi М. (s. str.) cecon: ris
M. (s. str.) hyperboreus М. (s. str. ) fortis.
М. (s. str.) ungurensis
Lag. luteus
The same species form yet another order according to the
degree of the increase in the number of colic spiral coils.
М. (ph.) carruthersi — . (3. str.) oeconomus | _,
т luteus
М. (Ch. ) gud
2M, (5. str.) ungurensis Alt. (s. str. ) argentatus } >
Alt. (Aschiz) lemminus
M, (s. str.) hyperboreus
2 М. {s. str.) fortis > м. (Ph. ) juldaschi
2 63
М. М. VORONTSOV
АП these facts. show the high degree of non-uniformity in
the rate of transformation of the organs of the digestive system,
and may be considered as examples of the compensation of the
functions of one organ by another (Vorontsov) 1961 a, 1963 e).
The same tendency of specialization of the intestine for
cellulose nutrition is traced in the tribe Ellobiini also.
The intestine of Ellobius lutescens (see Fig. 136, r) is
4.2 times longer than its body, while its small intestine consti-
tutes only 0. 9 of the length of large intestine and caecum. The
caecum is divided into 10 chambers by isthmuses and forms some
projections and sacculi. Ampulla absent. Colic spiral has 4
coils. Spiral valve does not develop in the ascending colon. In
Ell. talpinus (see Fig. 136, a) the caecum is complicated by
bends: it has five bends; but sacculi are less developed than in
Ell, lutescens. In Ell. talpinus the relative length of the intes-
tine goes upto 4. 7 times. In other respects the intestine of
Ell, tal pinus is similar to that of ЕП. lutescens.
The sharp differences in the intestinal structure of
Ellobius and Prometheomys should be especially noted. Accord-
ing to the degree of intestinal adaptation for cellulose nutrition
Ellobiini form the following order.
Ellobius lutescens > ЕЦ. talpinus
с. Muridae
The family Muridae is more adapted to protein nutrition
than Cricetidae. However, a tendency for the specialization of
intestine for mixed nutrition with considerable amount of cellulose
is traced in this group, consisting mainly of seed-eating rodents
in spite of the fact that the number of species of this group
studied is limited (Table 9 and Fig. 137).
Among the species of Muridae studied by us and described
by Tullberg (1899) it is the Australian carnivorous rat Hydromys
chrysogaster (see Fig. 137, a), our bandicoot rat Nesokia
indica (see Fig. 137, b) and African mouse Dendromys meso-
melas (see Fig. 137, c) which have a very simple structure of
264
STR UCT URE OF INTESTINE IN NESOMYINAE, ЕТС.
TABLE 9
Relative dimensions and correlative development of the different
portions of intestine in certain Muridae (orig.)
Relative length of the portion Intestine length-body _
Species with respect to the total length length ratio.
of the entire intestine
Small Large Caecum
intestine intestine
Hydromys chrysogaster’ 86 11 3 6.8
Mus musculus” 74 19 7 6.0
Apodemus agrarius | 73 19 8 4.6
Chiropodomys penicillatus! 72 24 4 4.7
Nesokia indica 72 23 6 4.8
Dendromys mesomelas! 71 21 8 4.7
Cricetomys gambianus 66 28 6 3.9
Apodemus flavicol lis” 55 25 9 5.5
Conilurus penicillatus 64 28 8 =
Apodemys sylvaticus 60 29 10 3.8
Saccostomus lapidarius” 54 34 12 4.4
Otomys unisulcatus! 57 40 14 5.1
1) According to the data of T. Tullberg (1899).
2) According to N.P. Naumov (1948).
the caecum. The caecal structure of these species highly
resembles that of the insectivorous hamsters, Oxymycterus.
The large intestine is devoid of the colic spiral and spiral valves.
The simplified structure of caecum and large intestine conforms
to the mainly protein nutrition of Hydromys and Dendromys.
However, the highly simplified caecum and large intestine of
Nesokia, feeding mostly on the vegetative parts of the plants, may
be explained only as a manifestation of the non-uniformity in
the rates of transformation of the digestive organs. As a result
265
N.N.VORONTSOV
a b Е а е f
g h
Fig. 137: Structure of caecum and its analogs in certain forms of Muridae;
а, с, e- according to Tullberg (1899) and the rest -original.
Complication of caecum and its differentiation into sections are -
traced, The series is homologous to that of Cricetinae, Nesomy-
-=—-—
sylvaticus L. ; (В) Crecetomys gambianus.
of this the caecum and the large intestine of Nesokia are balanc-
ing organs (Vorontsov, 1961 a and 1963 e).
The caecum is somewhat complicated in Rattus norvegicus.
Here the caecum has two bends and is divided into three
chambers. The large intestine is devoid of ampulla, colic spiral
and spiral valves (see Fig. 137, e).
Large intestine and caecum are still more complicated in
the African Savanna cricetid, Saccostomus lapidartus. Colic
spiral forms one coil (see Fig. 137, f).
In the genus Apodemus, caecum and large intestine are
more developed in Ap. §ylvaticus (see Fig. 137, j). The caecum
has four bends and iis divided into 8 chambers by isthmuses.
Large intestine has an ampulla and a spiral valve. Colic spiral
is poorly developed.
The caecum is quite large in Cricetomys gambianus (see
Fig. 137, В). It is divided into 8 chambers to which the ampulla
of the large intestine is adjoined. The colic spiral and spiral
valves are not present in the large intestine.
Judging from the data given by Tullberg, (1899) the
caecum and the large intestine are better developed in Saccosto-
mus and especially in Otomys.
266
N.N.VORONTSOV
In Hydromys (Tullberg, 1899), the sharp increase in the
size of the small intestine and reduction of the caecum are,
apparently, associated with the secondary transition to the
predatory mode of nutrition (parallelism with Ichthyomys).
It is found that the range of variability in the structure of
the intestine of Muridae is almost the same as that in Cricetidae.
In the structure of the intestine of Muridae there are no
features that would permit us to contrast the members of
Muridae from Cricetid.
4. Spalacidae and Rhizomyidae
Convergence of the structure of intestine in burrowing
rodents.
Spalacidae and Rhizomyidae differ considerably from
Cricetidae, Lophiomyidae and Muridae in the structure of their
intestine.
A spiral fold dividing the caecum into 18-20 chambers,
almost fully separated from one another, is developed in the
caecum of Spalax. The structure of the caecum is Spalax (see
Fig. 134, с) is similar to that of Leporidae and very convergent -
ly resembles the form of the spiral valve ofthe intestine of
selyakhs and cartilaginous ganoid fishes. Large intestine has a
three-coiled colic spiral and spiral folds.
"Spiral valve" develops in the caecum of Rhizomyidae
also (Tullberg, 1899). Rhizomys also has a three coiled colic
spiral. Differences in the structure of the intestine of Myospalax
from that of Spalax and Rhizomys are as profound as the simi-
larity between the latter two genera.
Attention should be paid to the fact that in Bathvergidae
convergent with Spalacidae and Rhizomyidae, there appears (in
Cryptomys) а "spiral vaive" in its caecum.
Convergence caused by the burrowing way of life, is so
profound in rodents that it affects not only the locomotion system,
267
N.N.VORONTSOV
appearance and body proportion of the animal, but also the
digestive system. Convergence in the relative development of
the sections of the intestine in the distantly related and unrelated
forms of burrowing rodents (Table 10) living under similar
ecological conditions is of significance.
TABLE 10
Convergence in relative sizes and correlative development of the sections
of the intestine in borrowing rodents of Holcartic steppe regions.
Relative length of the portion Intestine length-body
Species and their with respect to the total length length ratio
systematic position of the entire intestine, %
Small Large Caecum
intestine intestine
Muroidea
Cricetidae
Myospalacinae
Myospalax
my ospalax 56 34 10 7.0
Spalacidae
Spalax microphtalmus 56 33 11 4.7
Spalax leucodon 55 34 11 4.5
Geomyoidea
_ Geomyidae
Geomys bulbivora 57 10 5-1
However, the convergence covers such superficial features
as correlative development of the sections of the intestine,
whereas the internal structure of the caecum and the large intes-
tine in such forms as Myospalax, Spalax and Geomys differ
considerably from one another.
Tullberg (1899) who has studied the intestine of Tachyory-
ctes does not mention anything about the "spiral valve" in the
caecum of this genus.
е. Muroidea
It is observed that a process of adaptation of the structure
of intestine for cellulose nutrition takes place independently of
268
INTESTINAL SPECIALIZATION IN OTHER MYOMOR PHS
One another inthe different subfamilies of the superfamily
Muroidea within this large group of rodents. There are several
series of homologous variability in the structure of the intestine
on account of the adaptation for cellulose nutrition (Cricetinae,
Nesomyinae, Myospalacinae, Gerbillinae, Microtinae and
Muridae). In Spalacidae and Rhizomyidae the adaptation of
intestine for cellulose nutrition is convergently different from
that in Cricetidae, Muridae and Lophiomyidae.
The author cannot draw a demarcating line between the
homologous series of each of the subfamilies of Muroidea. The
intestine structure of the series may define the range of varia-
bility and the degree of the tendency for protein or cellulose
nutrition (Fig. 138).
Along with the basic trend in intestine specialization -
reduction of small intestine and enlargement of caecum and large
intestine mastering of free niche of nutrition by certain forms
(Ichthyomys, Oxymycterus, Onychomys, etc. of Cricetinae and
Hydromys and allied genera of Muridae) leads them to a change
Over to protein nutrition. This results in the reduction of caecum
and large intestine and an enlargement of small intestine.
However, the basic trend in the intestine specialization of
Muroidea is the adaptation for cellulose nutrition.
f. Other Myomorpha (Dipodoidea and Myoxoidea)
Muroidea, in its intestinal structure, does not differ from
Dipodoidea. Complication and increase inthe relative size of
caecum and large intestine with change over from protein to
combined nutrition with considerable amount of cellulose о
11) is traced in the latter group also.
Myoxoidea differs considerably from Muroidea and
Dipodoidea in the absence of a caecum.
The genus Platacanthomys is allied to Myoxoidea in this
respect, Typhlomys (Thomas, 1896) has a poorly developed
caecum. It isjustly observed by Ellerman (1940) that reduction
of caecum may be so profound in certain Muroidea (Ichthyomys,
Oxymyceterus, Hydromys, etc.) that it is not clear whether the
reduction of caecum in Platacanthomys can be considered as a
feature which distinguishes this genus from Typhlomys.
269
N.N.VORONTSOV
TABLE 11
_ Relative size and correlative development of the different sections of intestine
in Dipodoidea. Calculated according to Tullberg's (1899) absolute data.
Relative length of the portion Intestine
with respect to the total length length-body
у of the entire intestine length ratio
Species Small Large Cae-
int estine intestine cum
Sicista subtilis 66 21 13 4.1
Dipus aegyptycus 64 25 7 Ta
Zapus hudsonicus 60 28 12 4.7
Allactaga faculus 60 30 10 TS
g. Bathyergomorpha and Hystricomorpha
A tendency for the adaptation of intestine for cellulose
nutrition is observed not only in the Myomorpha group but also
in other rodent groups.
A progressive enlargement of the large intestine and
caecum and complication of the caecum right up to the formation
of a spiral valve is observed in Cryptomys (Figs. 139 and 140;
and Table 12) of the ancient groups of rodents - fossorial Bathy-
ergomorpha (unlike Spalacidae and Myospalacinae, Bathyergidae
is not a monotypic group).
It is remarkable that in Cryptomys the complication of
caecum is associated with the reduction in the relative length of
the intestine as a whole.
It may be generalized that in the relatively more primitive
and ancient groups adaptation for cellulose nutrition takes place
mostly by an increase in the relative length of the entire intes-
tine, especially the large intestine. In progressive groups of
270
INTESTINAL SPECIALIZATION IN OTHER MYOMORPHS
,
Fig. 139: Structure of large intestine and caecum of certain Bathyergidae:
a and b after Tullberg (1899) с and 4 - original.
(a) Bathyergus martimus; (b) Georychus capensis; (c) Myoscalpos
argeutes; (а) Cryptomys damarensis Ogilby, For legend see
Fig, 123.
TABLE 12
Relative length and correlative development of the sections of
intestine of Bathyergidae.
Relative length of a section Intestine length -
Species to the total length of the body length ratio
intestine, %
Small Large Caecum
intestine —_ intestine
Myoscalops argentes 62 } 25 7 5.4
Georychus se 51 38 10 5-7
Bathyergus aoe oe 46 46 8 6.0
Cryptomys damarensis 36 46 18 4.2
1) According to Т. Tullberg’s (1899) data.
herbivorous rodents (in the tribe Microtini, Myospalacinae,
Spalacidae, etc. ) adaptation for cellulose nutrition is by a
complication in the form of the caecum and large intestine with
an intensification of their functions which leads to a secondary
reduction in the intestinal length.
271
N.N.VORONTSOV
TABLE 13
Relative length and correlative development of the sections of the intestine of
Hystricomorpha. Calculated on the basis of the absolute data of Tullberg (1899).
Relative length of the section — Intestine length-body
Species С the total length of the intestine, length ratio
Small Large Caecum
intestine, intestine.
Dasyprocta aguti 78 19 4 12.3
Atherura africana 78 18 4 12.9
Hystrix cristata 76 19 4 11.6
Myopotamus соуруз 76 17 8 16.9
Lagostomus trichodactylus 70 28 3 8.5
Hydrochoerus capibara 69 24 7 10.5
Coelogenys paca 67 29 3 31.0
Echinomys cayennensis 66 25 9 8.9
Nelomys antricola 62 32 6 #57
Abrocoma bennetti 62 31 6 12,2
Erethizon dorsatus 61 34 5 9.4
Spalacopus poeppigi 61 30 Woe 5.5
Cavia porcellus 59 35 й =
Octodon дедиз 59 34 8 7.3
Ctenomys magellanicus 57 32 11 755
Cannobatheomys amblyonyx 48 44 8 3.3
Chinchilla taniger 36 49 5 10.4
In the very old suborder of rodents, Hystricomorpha, the
intestine is adapted for cellulose nutrition not only by a compli-
cation of caecum (Fig. 141) but also by an increase in the length
of caecum and large intestine and an elongation of the entire
intestinal tract (Table 13).
РГ
INTESTINAL SPECIALIZATION IN OTHER MYOMOR PHS
Fig, 140: Caecum and its analogs in certain forms of Bathyergidae а and b,
after Tullberg (1899) c and d original, after Vorontsov (1962).
(a) Bathyergus martimis; (b) Georychu s capensis; (с) Myoscalops
argenies; (4) Cryplomys damar da maremsis. Ogilby. For legend see
Fig. 123.
ae pee
To Сы
k
Fig, 141: Caecum and its analogs in some members of the suborder
Hystricomorpha, According to Tullberg (1899). (a) Chinchilla
laniger; (b) Coelogenys раса; (с) Dasyprocta я (а) Сала. =
porcellus; (e) Cannobatheomys ambiyonyx; (f) Spalacopus poeppi-
gi; (в) Dolichotis patagonica; (№) Erethizon аотза!из; (i) Habraco -
ma benibeti; | 0) оз ¢ а: (Е) ) Glenomys и magellanicus: iO
see Fig. 123
273
М.М. VORONTSOV
Unlike the herbivorous Myomorpha the relative length of
the caecum in Hystricomorpha almost never attains a two digit
percent whereas, the relative length of intestine, as a rule, is
9-12 and in individual cases, 31 times more than the body length.
Thus, the forms of Hystricomorpha, convergent with those of
Myomorpha, solve the similar functional problem in a different
manner. It seems to us that the means adopted by Myomorpha
leading to the economy of construction material is progressive
and more perspective from the evolution point of view.
Thus the intestine of Rodents belonging to different groups
undergoes transformation independent of one another Owing to the
change over to cellulose nutrition. The series of intestinal
transformations within the entire suborder Myomorpha should be
considered homologous, whereas the orders Myomorpha and
Hystricomorpha are parallel to one another.
274
CHAPTER VI
EVOLUTION OF LIVER
The nature of division of the liver into lobes and the
presence or absence of the gall bladder are the specific features
of mammals. However, the morphology of liver of a majority of
wild mammalian species remains unstudied up to this day.
Morphologists do not give any functional explanation for the type
of the external structure of liver whereas the taxonomists over-
look this organ although they are also aware of the fact that the
structure of this gland in related forms (for example, Mus and
Rattus) may differ considerably and thereby give data on specific
phylogenetic structure.
The form and size of liver depend considerably on the
complete development of the adjoining organs: stomach, kidneys,
heart and even the lungs and also on the conditions of fixation of
the material. Hence attention was paid mainly to the correlative
development of the lobes and hepatic duct formation. It is also
well known (Schwartz, 1959) that the relative weight of the Nes
is correlated with the absolute size of the animals.
The liver (hepar) of rodents is divided into inner and outer
lobes (lobus sinister medialis, |. sinister lateralis, 1. dexter
medialis, 1. dexter lateralis) that are always paired. The gail
bladder (vesica fellea) usually lies between 1. dexter mediallis
and 1. sinister medialis. It usually unites the independent
quadrate lobe (1. quadratus) and in this case it lies between
1. Quadratus and 1. simister medialis.
On the ventral side these lobes are superimposed by a
three lobed caudate lobe (1. caudatus) which can be divided
basically into independent lobes; the spigelian lobe (1. spigelli
seu processus papillaris) lies оуег” 1. sinister lateralis;
* On examination of the liver from the caudal side.
275
N.N.VORONTSOV
processis ventricularis enters the lesser curvature of the sto-
mach along the sagittal line of the body and processus caudatus
lies on 1. dexter lateralis. From the ventral side of the form of
liver resembles those of the adjacent organs - stomach and
rodent kidney. There is a wide and shallow depression-
impressio gastrica оп |. sinister lateralis and impressio.
renalis on processus caudatus. Thus, the liver may consist of
8 (more or less equally developed) lobes and a gall bladder.
However, a reduction of the gall bladder as well as the number
of liver lobes is observed in many rodents.
The liver as a digestive gland secretes bile. Bile inhibits
the action of pepsin on tripsin thereby accelerating protein
digestion. Salts of bile acids serve as the coenzymes of amylase
and lipase. The alkaline reaction of bile faciiiiates emulsifica-
tion of fats, increases the surface of fatty droplets and facilitates
their contact with lipase. Finally bile facilitates the dissolution
of fatty acids.
In the entire carnivora and many rodents bile enters the
intestine from the gall bladder where it is concentrated quanti-
tatively and qualitatively (cystic bile contains only 80-86 percent
water).
There is no gall bladder in certain rodents and ungulates
with mainly cellulose nutrition.
What is the functional idea behind the presence or absence
of the gall bladder? It seems to us that the presence of the gall
bladder and the forms requiring the calorific proteo-lipoid food
is linked with the irregular entry of this food (for example, in
carnivores and seed-eating rodents). The irregular entry of
large amounts of fats and proteins demand the supply of a consi-
derably large amount of concentrated bile within a short period
of time. Let us remember that the pH of cystic bile is 6. 8
whereas that of hepatic bile is only 7.5 (Azimov et al. 1954).
Entry of low-calorie cellulose food is practically continuous
but it contains only an insignificant amount of fats and proteins.
In this case there could be a constant supply of less concentrated
bile which is close in composition to hepatic bile. Thus in forms
adapted mainly to cellulose nutrition, the gall bladder should
276
EVOLUTION OF LIVER
lose its function of concentration and storing of bile. This leads
to the total disappearance of the gall bladder in many rodents.
A majority of the American Cricetinae studied by us have
a gall bladder and an eight-lobed liver.
In Oryzomys flavescens the square lobe is one of the
largest liver lobes and gall bladder is present whereas in Or.
couesi gall bladder and square lobe are absent. It is possibie
that these species are artificially grouped into one genus.
The size of the square lobe is relatively large in Nectomys
squamipes but is less than that of Or. flavescens. A gradual
reduction in the size of the square lobe is observed in Oxymyc-
terus nasutus, Peromys cus oalifornicus, Baiomys musculus and
Onychomys leucogaster. Gall bladder is present in all these
forms.
The square lobe attains the maximum development in
Sigmodon hispidus in which it is subdivided by an isthmus into a
large (outer) and a small (inner) lobes. Gall bladder is present.
In Thomasomys dorsalis and Reithrodontomys megalotis,
gall bladder is present, but square lobe is absent whereas in
Akodon arenicola the gall bladder also is absent.
Calomyscus bailwardi, just as Reithrodontomys megalotis,
has a gall bladder but no square lobe. |
New world palearctic Cricetini are characterized by the
absence of square lobe. (Cricetulus longicaudatus hes a small
branching which may be a remnant of square lobe). Gall dviadder
is absent in the members of the entire Cricetini except
Mesocricetus (М. raddei М. bandti and M. auratus).
Gall bladder is absent in Cricetulus (5. str. ) longicaudatus,
Ч. (5. str.) migratorius; G. (5. str.) barabensis, G. (Tscherskia)
triton, Cricetus cricetus, Phodopus sungorus and Ph. reboroy-
skil.
A considerable increase of 1. dexter 'ateralis and a
noticeable decrease in the size of 1. caudatus, especially 1.
277
N.N.VORONTSOV
spigelli and proc. ventricularis, take place within the order of
Cricetini described above.
The gigantic 1-Spigelli and presence of gall bladder (square
lobe is absent) distinguish Mystromys albicaudatus clearly from
palearctic Cricetini.
All species of Microtinae studied by us retain gall bladder.
The square lobe was observed by us only in Prometheomys
schaposchnikovi (having a large size), Dolomys bogdonovi and
Alticola (Aschizomys) lemminus. It is present in Lemmus
obensis, Myopus schisticolor, Microtus (Chiconomys) gud, М.
(s. str.) michnoi, М. (5. str.) oeconomus,M, (s. str.) hyper-
boreus М. (Phajomys) caruthersi, Alticola argentatus, Lagurus
luteus and Ellobius talpinus. In its liver structure Microtinae
is a considerably more homogenous group than Cricetinae.
Gall bladder is developed in all the 17 species of Gerbilli-
nae studied by us. The square lobe of the liver is poorly
developed in certain forms of Gerbillinae (Gerbillus pyramidum,
Brachiones przewalskii, Meriones tamariscinus, М. pergicus,
М. crassus swinhoei, М. melanurus, М. shawi, Rhombomys
opimus, Psammomys obesus) whereas it is completely absent
in certain others (Meriones meridianus, М. erythrourus, М,
tristrami, М. unguiculatus, М. crassus charon, Gerbillus
dasyurus simoni and Tatera indica). By the liver structure
Gerbillinae forms a highly homogenous group.
Myospalax myospalax has a gall bladder. The size of
proc. ventricularis exceeds that of 1. spigelli and proc. caudatus
The square lobe is absent.
Reduction of the gall bladder and disappearance of indivi-
dual liver lobes are traced in the order of Muridae. Cricetomys
gambianusg has a gall bladder and а small square lobe. In
Nesokia indica, Pogonomys lepida and Conilurus penicillatus,
the gall bladder is absent, the square lobe is not developed and
proc, vemticularis and |. spigelli are highly reduced in size.
Reduction in the lobe structure is observed in other groups
of rodents also. Thus, Myoscalops argentes has a gall bladder,
small square lobe, small proc. ventricularis and reduced \.
278
VOLUTION OF LIVER
эре. The gall bladder is retained in Cryptomys damarensis,
but the square and spigelian lobes are absent.
Thus, a process of oligomerization’ (Dogel, 1954) of
homologous lobes and liver lobes takes place in the different
groups of rodents independent of one another, but in certain
forms the gall bladder may be reduced owing to the change over
to cellulose nutrition.
* The possibility for applying the phenomenon of oligomerization of homolo-
gous organs to the decrease in the lobulation of liver in mammals was
first argued by N.S, Lebedkina. While presenting the paper at the Scienti-
fic Council of the Institute of Animal Morphology, Acad. of Sc. , USSR. оп
13th Feb. 1953, N.S. Lebedkina said, 'the author writes: "А process of
oligomerization ( Dogel, 1954) of homologous lobes and liver lobes takes
place in the different groups of rodents independent of one another". But
it is difficult to agree with his view as Dogel has assumed the principle
of multiple laying of homologous organs as the essential prerequisite for
the very process of oligomerization. The vertebrate liver by its origin is
an unpaired intestinal outgrowth which gets branched secondarily. Dogel
himself ( page 41) writes "'As far as the digestive system is concerned, we -
did not consider the branches and outgrowths of intestine as separate
organs. Further (page 51) it is necessary to see whether we have before
us branching or actual multiplicity of organs (short hand record of the
conference of the Scientific Council of the Institute of Animal Morphology)"
N.S. Lebedkina did not pay attention to the fact that this observation of
V.A. Dogel relates to turbellaria. A wider explanation of the process of
oligomerization as understood by Milne -Edwards, who paid attention to
this phenomenon for the first time and by V.A. Dogel himself, appeals to
us more than the narrow explanation put forward by N.S. Lebedkina.
У.А. Dogel studies oligomerization in detail in such irregularly shaped
animals, as Mollusca. In particular, Dogel examines, as instances of
oligomerization, not only the reduction of liver lobes in the Mollusca,
Placophora ( Dogel, 1954) (page 119) but also decreases in the number of
mammary glands in mammals. Meanwhile, it is well known that these
glands are formed by the division of the portions of the ''mammary line''
laid out as a single formation. Hence we are inclined to consider it
permissible to include such instances as the decrease in the number of
lobes of liver and lungs under the phenomenon of oligomerization.
279
GENERAL PART
CHAPTER УП
Weys of Food Specialization and Evolution of*the
Digestive System in Muroidea.
On the basis of the study of Muroidea intestinal structure,
it may be concluded that the basic evolutionary trend in Muroidea
and a majority of other phytophagous mammals, starting from
the early miocene, was a change over from proteo-lipid to
cellulose nutrition. This change in the type of nutrition was
highly accelerated by the large settlement in the land taking
place in pliocene (Vorontsov, 1959a, 1959b, 1960b, 1960c,
1961с, 1962a, 1962b and 1963b).
The change over from protein nutrition to cellulose nutri-
tion signifies a transition from the high-calorie, food substances
available with difficulty (seeds, small invertebrates) to low-
calorie substances easily accessible (vegetative parts of plants).
The change over from protein to cellulose nutrition leads to a
decrease in the size of the individual portion and decrease in the
mobility of the animals (Naumov, 1948), increase in the total
volume of food required, transition from necturnal activity
(Oryzomys Rhipidomys, Peromyscus, Calomyscus and other
members of Cricetinae, Clethrionomys rutilus of Microtinae
and Gerbillus and many Meriones of Gerbillinae) to continuous
or diurnal activity (Sigmodon hispidus of Cricetinae, Microtus
and Clethrionomys rutilus of Microtinae and Rhombomys of
Gerbillinae). This change over leads to the disappearance of the
instinct to’store food (Naumov, 1948 and Vorontsov 1956, 1961b) |
and to « change over from closed biotopes (characteristic of
Cricetinae - Oryzomys, Thomasomys, Rhipidomys, Peromyscus,
etc. ; Microtinae - Clethrionomys; Rodents - Apodemus, Rattus,
Dendromys, etc.; Dipodidae - Sicista substidis and Zapus
280
FOOD AND ALIMENTARY SYSTEM
hudsonicus) to open (typical Cricetinae - Cricetus, Cricetulus,
Mesocricetus, Rhodopus, Andinomys, Reithrodon, etc. ;
Microtinae - Microtus, Lemmus, Lagurus, etc. ; Rodents -
Nesokia, Otomys, etc. and majority of Dipodidae.
With the reduction in the mobility the locomotor organs
are reduced, relative length of the limbs, especially the hind
limbs, is reduced and the tail gets shortened (series of Criceti-
nae from Peromyscus, Thomasomys, Oryzomys to_Sigmodon,
Andinomys, Cricetus, ee series of Microtinae from
Dolomys, Clethrionomys glareolus to Microtus, Lagurus and
Lemmus; and series of Rodents from_Apodemus and Rattus to
Nesokia).
With the simplification in the search for food, the sensitive
organs beginning with the organs of smell, vision and taste
(Matveev, 1960, and Ganeshina and Grutovoi, 1953; Ganeshina,
Vorontsov and Chabovskii, 1957) and the size of the olfactory and
the optic lobes of the brain and cerebellum get reduced
(Matveev, 1960).
On the basis of the comparative ecological and morphologi-
cal studies of the digestive system of different rodents it may be
said that with the change over from protein to cellulose nutrition
the digestive system undergoes the following changes : -
1. With the increase in the total amount of food required
the entire set of muscles associated with chewing becomes
stronger (series from Cricetinae to Microtinae; series, from
Oryzomys to Nectomys, from Phyllotis to Andinomys, from
Peromyscus and Calomyscus to Cricetus, from Neotomodon to
Neotoma, etc. of Cricetinae, series from Clethrioniomys to
Microtus and Lemmus of Microtinae and series from Apodemus
to Rattus and Nesokia) (see Chapter I, 1-4).
2. Crushing of seeds (analogous with mortar) is suitable
for crushing the seeds biomechanically whereas grinding
(analogous with grinder) is suitable for grinding cellulose food.
On the basis of this crushing and pressing movement, the jaw
movements are divided into gnawing and grinding (Chapter I,
ааа)
281
N.N.VORONTSVQ
Division of the gnawing and grinding functions (Chapter I,
3) leads to differentiation of па. masseter lateralis into three
portions of which pars anterior (Chapter I, 4) attains the
maximum development. M, masster lateralis is still not
differentiated in Gliroidea and Dipodoidea. Oligoene Cricetidae
(Cricetops affinis) also, apparently, possessed а nondifferentiat -
ed m. masseter lateralis. Decrease in the role of catching the
prey leads to a reduction of р. anterior гп. masseter medialis
and constriction of the foramen infraorbitale through which
stretches this muscle. This regularity is traced in the evoluticn
of Cricetodontini from Oligocene to Miocene (Chapter I, 5)
and in the New World Cricetidae it is observed in the series
Ichthyomys -Oxymycterus -Oryzomys -Cricetus -Clethrionomys-~
Microtus-Lemmus (Chapter I, 4).
Deepening and shortening of fossa pterygoidea lateralis
are observed in this series; messeter area of maxilla highly
increases and is moved forward and upward (series of fossil
Cricetidae from Oligocene to Miocene and series of New World
Muroidea from Ichthyomys to Microtus).
Thus, р. profundus m. masseter lateralis takes part not
only in the adduction of mandible but also in pushing it forward
(Vorontsov, 1963).
3. Molars of bunodontia are compressed and owing to the
mastication of a large amount of coarse cellulose food substance
they acquire the capacity for constant growth, loose their roots,
and thus change (Chapter Ц, 2) into hypsodont dentition from
brachyodont (series of fossil forms of Cricetodontini from
bunodont Oligocene species to lophodont Upper Miocene species;
series of fossil forms of Microtinae from Mimmomys to Lemmus
(Chapter II, 5); series of New World Cricetinae from Oryzomys _
to Neotomys, from Akodon to Zygodontomys, from Holochilus
magnus to Н. brasiliensis, Sigmodon and Reithrodon, from
Phyllotis to lrenomys and Andinomys from Neotomodon to
Neotoma (Chapter Il, 6); series of New World forms of Micro-
tinae from Fibrini to Microtini and Lemmini, from Clethriono-
mys rutilus to Cl. rufocanus (Chapter Il, 8); series of Gerbillinae
from Gerbillus and Monodia to hypsodont Rhombomys through
Meriones and Psammomys (Chapter II, 8); series of zokors,
from Miocene Prosiphneus to New World forms of Myospalax
282
FOOD AND ALIMENTARY SYSTEM
(Chapter II, 7c) and series of Muridae from Hapalomys to
-Otomys through Nesokia and Eropeplus (Chapter H, 8}. Сопуег-
gent with Muroidea, the series of variability in the dental system
are known in Dipodoidea (from Sicista and Zapus to Allactaga and
Alactagulus), in Gliroidea (from Dyromys and Eliomys to
Muscardinus), in Geomyoidea (from Perognathus to Heteromys
and Geomys), in Hystricidae (from Atherurus and Hystrix) and
other groups of rodents (Chapter I, 8).
4. The masticatory surface of the molars is complicated
by an increase in the number of enamel crown ridges which are
always oriented across the direction of masticatory movements.
Most forms of Myomorpha and Hystricomorpha, except certain
forms which make burrows with their incisors have longitudinal
grinding movements, for which (Chapter II, 2) the enamel crowns
are oriented transversely (Microtinae, Neotoma, Andinomys
Reithrodon, etc. of Cricetinae; Rhombomys of Gerbillinea;
Nesokia and Otomys of Muridae, etc.). The relative length
of the molars increases (series of Cricetinae from Oryzomys to
Neotoma and series of Microtinae from Clethrionomys to Micro-
tus, Lagurus, Lemmus and Dicrostonyx). If the grinding is in
transverse direction the enamel crowns are oriented longitudi-
nally, width of molars increases and МЗ attains the size of М".
(Tachyoryctes and Brachyuromys ramirohitra).
5. The articulated head of the mandible takes a horizontal
position from the vertical one (series of Cricetinae from
Ichthyomys to Cricetus and Neotoma and series of Mic rotinae
and Clethrionomys rutilus to Microtus).
6. The sensitive papillae of the tongue (papillae fungi -
formes, papillae foliatae and papillae circumvallatae) are
subjected to reduction. P. circumvallatae including three still
present in the entire forms of Dipodoidea and Gliroidea, whereas
in Muroidea, these three papillae are retained only in Nesomyi-
nae and CricetOmyinae, Its number is reduced to two in
Myospalacinae and one (Chapter III, 1) in the entire Cricetinae,
Microtinae, Gerbillinae and Murinae.
7. The size of the entire alimentary canal (Chapter IV-V)
increases Owing to the considerable increase in the amount of
food required.
283
N.N.VORONTSOV
8. In the stomach, the area lined by the corneous epi-
thelium increases, the boundary fold between the corneous and
the glandular portions is shifted to the pyloric portion and finally
the glands are restricted to only a small portion of the fundus
ventriculi. The one-chambered stomach is converted into a
two-, three- or even five-chambered one. The first portion
lined only with the corneous epithelium and analogous to the
rumen of ruminants plays the role of a "fermenter" in the initial
cellulose digestion. Similar series in the stomach structure
are traced among cricetinae from Neotomys and Sigmodon to
Phodopus roborovskii, Neotoma cinerea and Peromyscus
californicus (Vorontsov, 1957); among Microtinae from Ayicola,
Lagurus, Alticola to Ondatra, Lemmus, Microtus and Promethe-
omys through Ellobius lutescens and Ell. talpinus; among
Muridae from Nesokia to Cricetomys and Ap. agrarius through
Rattus and Apodemus sylvaticus and among Muroidea from
Cricetidae to Lophiomyidae. A tendency for the formation of a
two-chambered stomach is observed among other groups of
rodents also evenat the expense of other rudiments. Thus the
formation of an additional section of the stomach by the dilation
of the rear part of the Oesophagus is observed in the series
Myoxidae, from Glis,Dyromys and Eliomys to Muscardinus. A
similar two-chambered stomach of the dormouse is not homo-
logous to the two-chambered stomach of Muridae. We observe
a series convergent with Muroidea by its stomach structure in
Bathyergoidea (from Georychus and Myoscalops to Cryptomys)
(see Chapter IV).
9. The relative length of the small intestine decreases,
whereas the relative size of the large intestine and caecum
increases.
10. The caecum not only increases in size, but also is
complicated by the formation of small pockets and isthmuses and
in extreme cases its surface increases owing to the folds which
have the form of actual spiral valve (Spalax and Cryptomys).
Such are the series of Cricetinae from Oryzomys to Nectomys,
from Phodopus to Mesocricetus, from Neotoma floridana to
N. albigula and Neotomodon (Chapter V, 3); series of Microtinae
from Dolomys to Alticola and Lagurus (Chapter V, 5,b) series
of Muridae from Nesokia and Rattus to Apodemus and Cricetomys
(Chapter V, 5, c) and series of Bathyergidae from Bathyergus
and Georychus to Myoscalops and Cryptomys (Chapter V, 5, g).
3 284
FOOD AND ALIMENT ARY SYSTEM
11. The surface of the large intestine increases by a
simple elongation of the intestine and by the formation of
accessory spiral folds on its inner surface and accessory
ampullae coli (Chapter V, 3-5).
12. The number of coils in the spiral of the large intestine
at its emergence from caecum increases. The size of the large
intestine also increases. The number of coils in the spiral may
attain 4 in Cricetinae (Neotoma), 2 in Gerbillinae (Meriones) 2
in Muridae (Apodemus) 6 in Bathyergidae (Cryptomys) and 10-12
in Microtinae (Lemmus and Ondatra) (Chapter V, 3-5).
13. The eight lobed liver (Oryzomys, Nectomys, Pero-
myscus, Oxymycterus, Sigmodon, Akodon, Onychomys, etc. of
Cricetinae, Promethemys, Dolomys, etc. of Microtinae,
Brachiones and many Members of Gerbillinae and Cricetomys of
Muridae) is transformed into a seven-lobed one (Reithrodonto-
mys, Calomyscus, Cricetilus, Mesocricetus, etc., of Criceti-
nae, Myopus, Lemmus, etc. of Microtinae, certain forms of
Meriones of Gerbillinae, Apodemus €onilurus, Pogonomys and
Nesokia of Muridae).
The gall bladder is usually present in species with
irregular nutrition of high-calorie proteo-lipoid food requiring
concentrated supply of large amount of bile. With the change
over to feeding on low-calorie food and consequently the frequent
demand for mostly cellulose food, a continuous supply of bile
is required, which may lead to the reduction of gall bladder
(Cricetus, Cricetulus, Phodopus of Cricetinae and Rattus and
Nesokia of Muridae) (see Chapter VI).
Morphological series of transition from proteo -lipoid
nutrition to cellulose nutrition is determined for Cricetinae
(from Rhipidomys to Neotoma and Andinomys), Gerbillinae
(from Gerbillus to Rhombomys), Microtinae (from Fibrini to
Microtini and Lemmini) Muridae (from Micromys to Nesokia
and Apodemus ‘agrarius), Dipodidae (from Sicista and Allactaga)
and Myaxidae (from Dyromys to Muscardimus).
In addition to the basic trend in the evolution (transition
to cellulose nutrition). Myroidea as well as other groups of
285
N.N.VORONTSOV
rodents may Occupy the niche of animals adapted exclusively to
protein nutrition. This reverse trend in the specialization is
especially clear under conditions of isolation and unsaturated
biocoenosis. InSouth America in Pliocene Cricetinae occupied
the niche of the insectivores which were absent there and gave
rise to a series of insectivorous forms (Oxymycterus, Lenokus
and Blarinomys) and also of the small piscivorous carnovores
of the type Micropotdmogale -Potamogale -Chrinonectes
(Ichthyomys, Rheomys and Anotomys). Muridae of Indo-Malayan
region which occupied the niche of fine piscivorous carnivores
(Bayankamys, Hydromys, Parahydromys, Crossomys,
Pseudohydromys, Neohydromys, Mayermys, Chrotomys and
Celaenomys) had also undergone the same fate. The peculiari-
ties in the structure and the development of the digestive system
of the insectivorous Cricetinae show that the American
Oxymycterus, Onychomys and others have secondarily changed
from cellulose to protein nutrition (Chapter IV, 5).
Between the extreme trends of specialization basic with
highly perfected adaptations for cellulose nutrition and just the
opposite trends with adaptations for protein nutrition (here,
there are primarily proteinic forms of the type Oryzomys and
those secondarily adapted for this type of nutrition Ichthyomyini,
Oxymycterus, etc.) there are many species and genera, adapted
for cellulose nutrition. However, the basic trend in the evo-
lution of Muroidea was transition from proteinic and proteoe
cellulose to cellulose nutrition.
286
CHAPTER VIII
Unequal Rates of the Transformation of Organs and the
Principle of Compensation of Functions ;
The problems of interrelationship of organs, development
of this interrelationship and specialization and extinction
assOciated with it, form the important parts in the study of
evolution. Inspite of the fact that morphologists, paleontologists
and evolutionists have paid attention to these problems, the
problem of the transformation of the correlated systems of
organisms still remains as one of the least studied problems in
biology.
Solution to the most important biological problems at the
cell level and the submicroscopic structure of the cell drew the
attention of biologists from the problems of transformation of
organs, their coadaptations and. evolution and phylogenesis was
treated somewhat like a “secondary science". Meanwhile the
idea behind the understanding of the laws of molecular and
cellular biology lie in the fact that by knowing the processes at
some elementary level, we may pass on to the understanding
and control of the processes of development of science at the
level of tissues, organs, the organisms themselves and their
society. The logic of the development of science is such
that the present rapid progress in the field of molecular biology
should inevitably deal with the solution of the problems of
evolution studied by the phylogeneticists, zoologists, paleonto-
logists and botanists. Unfortunately the intensity of research in
the field of biology is at present little, but the 'rate of evolution'
of these sciences is still not sufficiently high.
I. I. Schmalhausen's (1938) remark that the problem of
integration has so far been an almost absolutely untouched
problem is correct and it still remains to be so. As observed
287
N.N.VORONTSQV
by I. I. Schmalhausen (1938), "it is necessary to study the
factors that determine the coordination of parts in the phylo-
genetic transformations of the organism". He considered the
method of development of the entire connecting Mechanism and
its role in further evolution as very important. This is an
unbroken chain of problems of considerable theoretical and
practical signficance not yet solved completely (pages 4, 5,
Г.Г. Schmalhausen). The question of the so-called biological
coordinations (Schmalhausen, 1938) belongs to the group of the
least studied aspects of this problem.
Е Formation of Modern Views upon the Coordination of the
Transformation of Organs in Phylogenesis, upon the
Problems of Specialization and Extinction,
According to the classic notion, enunciated by Cuvier,
when there is a change in the habitat, the organs of a system
are transformed more or less in the same direction. I.I.
Schmalhausen (1939b, page 84) has expressed this point of view
thus:
"Biological coordination limits the possible changes in the
Organism by biologically agreeable changes of individual organs,
i.e., by changes permissible by the given specific medium. If
organ A directly related to a certain factor (for example, to
herbaceous food) of a given medium (say, steppes) changes ina
definite direction owing to a change in the climate or in the
transition to any more specialized food (for example, a change
over to feeding on succulent vegetation with constant increase in
the arid nature and transformation of the steppe into a semi-
desert), organ B, related to the same factor should change
strictly in the same way.
According to this point of view, the biological coordinations
restrict the possible independent change in an individual organ
of the given system (Schmalhausen 1936b, page 85).
Adaptation of an organism to a restricted habitat permits
only certain main trends of evolution of the organism, namely,
only further specialization, i.e., adaptation for special condi-
tions within a more restricted habitat. The more the network
of biological coordination is complicated, the better the organism
288
VIEWS ON TR ANSFORM ATION
is adapted to the struggle for existence, but at the same time it
looses its plasticity, i.e., the possibility for readjustment if
there is any change in the habitat. During specialization, there
develops a complex, and hence, the strong bond between the
organism and the habitat. The organism becomes (in its
evolution) completely dependent on the given habitat, and going
out of this becomes a problem for it. Blind alleys of evolution
are created thus.
The following important aspects of the modern theory of
evOlution and morphological and phylogenetic researches are
based on these concepts of coordinated transformation of organs
when there is a change in the habitat :-
possible reconstruction of the entire organism from its
separate fragments,
loss of plasticity due to specialization,
specialization leading to the creation of blind alleys of
evolution, and to extinction, and
the fact that these specialized forms cannot form the basis
of new branches of development.
How did these concepts originate and develop?
It was G. Cuvier, who for the first time made а syste- _
matic study on the correlations which play an important positive
role in the development of comparative anatomy especially in
paleontology. The very idea of putting a question on the inter-
relationship and interdependence of the organs on one another
was extremely progressive.
The organs of an animal form a unified system, whose
Parts depend on One another and act and react with respect to
one another. Hence it is difficult to observe a change in one
without corresponding changes in all the remaining parts
(quotation from 1.1. Schmalhausen, page 8, 1938).
In his "A discussion on the cataclysms on the surface of
the globe" (page 130) Cuvier (1812) wrote :
289
N.N.VORONTSOV
"Any organized creature forms a single whole, closed
system, whose parts correspond to One another and act with the
same final aim by mutual influence. None of these parts can
change without changing other parts and consequently each of
these parts taken separately directs and determines all others.
Thus, as I have said elsewhere, if the intestine of an
animal is so built that it can digest only meat, its jaws should be
so designed as to shallow the prey, its claws to grasp and to
tear, its teeth - to cut and split, its locomotor system - to
chase and catch its prey, its sense organs - to detect the prey
from a great distance and nature equips its brain with the neces-
Sary instinct so that it can hide and trap its victims.
Uiving from his observations the form ofa law, Cuvier
(in the same book, page 132) wrote :
"In short the shape of a tooth entails the shape of an
articulated head, shape of scapula and shape of claws just as
the properties of a curve follows from the equation ofa curve".
Further (page 134) he wrote : "One such mark (of artiodactyls-
М. У. ) reveals to the observer the shape of teeth, jaw, vertebrae,
all bones of legs, shoulder and pelvis of a recently extinct
animal. This feature is more reliable than all the features of
the Zodiac".
Cuvier (in the same book, page 135) observed that "there
is some constant interrelationship between two organs which
may seem quite alien and the gradation of their shapes inevitably
corresponds to one another even when we cannot account for
their relationship" (spacing out given by us - N. V.).
Later (1859, 1868 and 1875) Charles Darwin forwarded a
new evolution concept in his study on the correlations, which
was reviewed by him in connection with his study on the laws of
variability. Thus Cuvier's basically static idea on the inter-
relationship of organs within an organism has turned out to be a
theory, dynamic in spirit, on the interrelated and interdependent
variations of organs in the process of evolution.
А.М. Severtsov (1931 and 1939) and Г.Т. Schmalhausen
(1938, 1939a and 1939b) after L. Plate (1913) divided the
290
VIEWS ON. TR ANSFORMATION
phenomenon on correlative variability into two g р5 namely,
actual correlations -interdependent, cocrdinatei d velopment of
organs in ontogenesis and coordinations-variation according to
the relation, between the organs developing independent of one
another and on a third organ in onto- and phylogenesis. As
I. 1. Schmalhausen (1939a) observes, Cuvier relates most of
the examples of 'correlations' to coordinations.
Charles Darwin (1875) actually made a distinction between
correlations and coordinations and while studying the difference
between these groups of phenomena had especially studied the
strictly correlative variation.
However, subsequent research workers extended Darwin's
conclusions on the laws of correlative variations fully even to
coordinative variability. The indistinct demarcations between
correlation and coordination suggested by Darwin (1859) paved
the way for criticisms of his teachings. Thus G. Spencer (1864)
found in the coincidence of coordinated variations of organs one
of his basic rejoinders to the natural selection theory and a
decisive argument in favour of Lamarckism. In fact in his
later statement (1875) on the theory of correlations, Darwin
more frequently, than in 1859, had recourse to Lamarckian
‘disuse of organs' in answering the criticism of Spencer.
Е. Cope (1884) put forward his "law of non-specialization'
according to which new groups may develop only from non-
specialized members of the parental groups. Developing the
concepts of Cope, 5. Dapiere formed the ‘law of specialization
of phylogenetic branches'. He emphasized (page 164 and 165)
that 'specialization does not affect the entire organism as a
whole. It covers one organ or a group of organs more or less
closely related functionally. That is why frequently it seems as
if specialization does not have any actual aim except gradual
perfection of one specific function - swimming, flying, jumping,
running, etc. '.
S. Dapiere (1915) relates specialization with extinction
of group and considers (page 172) that 'under no circumstances
is specialization a condition for the developm ent and longevity
of branches but, on the contrary, serves as a senile feature
which precedes their imminent extinction.
291
N.N.VORONTSOV
5. Dapiere, just like many other paleontologists consider ~-
ed that Darwinism cannot solve the problems of extinction
(page 186). 'The struggle for existence is decisively insufficient
to explain the extinction of species'. Instead of Darwin's
interpretation, Dapiere has put forward a theory, according to
which each phylogenetic branch has to pass through the develop~
ment stages, youth, which corresponds to a low level of зресйа -
lization and ageing stage which corresponds to a high level of
specialization. The latter stage, according to Dapiere,
'ргерагез! the extinction of group. The Cope~-Dapiere theory on
extinction, as a result of narrow specialization, was a logical
development and continuation of the study on coordinated trans -
formation of organs in phylogeneébis.
L. Plate (1913), who has put forward the concept of
'phyletic correlations’ corresponding to Severtsov's "coordina -
tions", considered that during the transformation of “complex
coadaptations" "a large number of elements change step by step
in a definite direction and often simultaneously" (Plate 1908,
page 350).
A similar concept on more or less uniform and unidirec-
tional transformation of organs in the process of specialization,
or on the close coordination of this transformation and on the
fact that this coordination narrows down the potential adaptability
of the organism and leads to extinction of the group is prevalent
until now (Franz 1935: and Schmalhausen, 1938, 1939a, 1939b,
1946).
Even in olden days naturalists had paid attention to the
occurrence of noncorrelation in the structure of organs of one
biological trend and later, with the development of ideas of
evolution and some irregularities in the rates of transformation
of organs. First examples of the manifestation of incomplete
correlations was given even by Aristotle.
S. Cuvier in 1812 observes that "the necessity for a
more complex digestive system for species whose dental system
is less perfect is fully understood" (Cuvier 1937, page 133).
However, this observation just like a slightly abandoned obser -
vation gets lost among the large number of conclusions and
facts, given by Cuvier in favour of the idea of direct coordination
of organs.
292
VIEWS ON TR ANSFORM ATION
The law of compensation was formed by М. У. Gete (1957)
in 1795 and published in the "first sketch of the general intro-
duction to comparative anatomy derived from osteology". Не
expressed it thus :
"Nothing can be added to one part without at the same time
removing something from another and vice-versa".
Т.Г. Kanaev (1957) rightly observes that Gete's idea of
compensation, is, in essence, close to the law of conservation
of matter and energy. A little later the same idea was put
forward under the name "compensation of growth" by Zhoffrua
St. Hilaire (1830).
Considering the ideas of Gete and Z. St. Hilaire Charles
Darwin (1859) has expressed the correct idea that,
"Certain instances of compensation given here as well as
similar and certain other factors may be grouped under a wider
principle, namely, a tendency for natural selection is to
constantly observe an economy with respect to all parts of
organization" (Charles Darwin, collected works, vol. Ш, 1939
page 377, 378).
However paradoxical it may be, neither the ideas of pre-
Darwinian naturalists nor those of Darwin himself had the least
influence on the formation of the ideas about coordinated trans -
formation of the system of organs, in connection with the new
requirements of the habitat put forward in the post-Darwinian
period. It is possible that this disregard for Gete's ideas was a
"relatiatory reaction" of qualified experts to the old naturalists
and philosophers on naive formulations supported hardly by any
actual data.
L. Dollo (1895) was the first to pay attention to the fact
that the phylogenetic series of forms proposed by paleontologists
and Darwinists were, in essence, not direct series. Studying
the phylogenesis of dipnoi fishes, he emphasized that the series,
formed on the basis of certain features, cannot correspond to
the series, formed onthe basis of the study of the structure of
other features. Dollo showed that the phylogenetic series known
to us are not direct series of the forms and are formed on the
293
N.N.VORONTSOV
basis of the study of a limited n@mber of features in the lateral
branches of the original stock. He put forward the concept of
"crisscrossing of specialization” for characterizing the pheno-
mena of the non-coincidence of the series formed on the basis of
the study of different features.
Dollo's concept of 'crisscrossing of specialization’ was
developed by O. Abel (1929) who wrote :
"Contrasts in the interpretations of different authors on
the position in the series of different fossil forms of one stock
is mainly due to the fact that during the formation and deepening
of our knowledge of the morphology of individual forms it was
proved that a number of series of specialization change with
respect to different organs. So we take an entirely different
genetic gruuping, it we take organ A with its degree of зресза -
lization as the basis for the formation of series, than if we select
another organ В for which the sequence of specialization is quite
different".
Abel at first criticized Cuvier's correlation theory and
indicated many mistakes, committed by the paleontologists, who
reconstructed the whole organism оп the basis о! the study of its
fragments, starting from Cuvier's correlation theory without
considering the phenomena of "€risscrossing of specialization".
However, many examples of the "crisscrossing of specia-~
lization" relate to different groups of phenomena not distinguished
by Abel. These included the crisscrossings of specialization of
different functionally unrelated systems of organs (Series of
adaptations inthe groups of Cetacea of the families Balaenidae
and Balenopteridae, built on the basis of the structure of cervical
vertebrae which do not correspond to the series of specialization
of the fore limbs) as well as crisscrossings of the specializations
of individual traits in the phylogenesis of an organ (structure of
molars of the fossil rhinoceros, Rhinocerotidae).
Abel paid attention also to the non-uniformity in the rates
of transformation of individual traits in phylogenesis. However,
he started from the false notion that a trait once developed in
phylogenesis cannot return to the original state. Non-uniformity
in so broad an interpretation of the law of irreversibility of
294
,
VIEWS ON TR ANSFORM ATION
evolution put forward by L. Dollo was shown even by P.P.
Sushkin (1915) and subsequently by С.Г. Ognev (1945). N.I.
Vavilov (1922) foretold the possible emergence of homologous
mutations iri allied groups and based оп the researches of репе-
ticists, marked the reversibility of the process of emergence of
new traits. Abel bypassed these works and proposed the appli-
cation of the phenomenon of "crisscrossing of specialization"
for establishing the geneological tree whether we are concerned
with the direct phylogenetic series (when crisscrossing of
specialization is absent) or the lateral branches of this geneologi-
cal tree (when crisscrossing of specialization is :present). These
concepts of Abel оп the application of crisscrossing of speciali-~
zation is graphically represented in Fig. 142.
Fig, 142: Chart of Abel's concepts on possible application of "crisscrossing
of specialization" for the formation of the phylogenetic tree.
After Vorontsov (1963, е). A,B,C,D,E and F- individual trails:
I, primitive state of these traits: П- specialized state of these
traits; 1,2,3, and 4- species with primitive or specialized trails.
There is no crisscrossing of specialization among the species
1,2 and 4 (direct phylogenetic series) species 2 and 3 with
crisscrossingwf specialization at least one of these species
should be on the lateral branch of the phylogenetic tree.
A Remane (1956) has severely criticized the method of
forming the phylogenetic charts On the basis of the presence or
absence of "crisscrossing of specialization". Meanwhile, it is
undisputable that the idea of non-uniformity of the rate of trans-
formation of individual features and organs in phylogenesis laid
down in Abel's concepts оп crisscrossing of Specialization, are
undoubtedly reliable and progressive.
One can Only be surprised at the fact that during 30 years
after the publication of Abel's book, his ideas are rarely made
295
N.N.¥VORONTSOV
use of and, have not yet been used essentially in phylogenetic
researches. Е
А.М. Severtsov, apparently, could not consider Abels'
concept On "crisscrossing of specialization" since the first
addition of his "Morphological regularities of Evolution" (1931)
came out soon after Abel's "Palaeobiology and History of Origin"
(1929).
While studying the phylogenesis of the family, Equidae,
A.N. Severtsov explains the simultaneous. and parallel varia-
tions of the different systems of organs (skull, teeth and
limbs) "as the condition that the animals referred to are
simultaneously adapted for different types of changes taking
place parallely in the surrounding medium." He emphasizes that
there are instances of transformation of organs taking place not
simultaneously but successively "in different, tunctionally un-
related systems of organs".
The problem on non-uniformity in the rates of transforma-
tion of organs was not studied by Severtsov's school. Teachings
of 1,1. Schmalhausen (1939а, 1939b, and 1946) onthe adaptation-
mor phosis and its forms and biological coordinations were further
developments of the views of Cope, Depiere, and Severtsov on the
coordinated transformation of ongans of single biological function.
According to Schamalhausen (1946, page 471) telomorphosis
is a specialization of organism, associated with the transition
from a more general to a specialized, more limited environment.
Besides there is unilateral development of certain organs and
partial reduction of others. Progressive differentiation is restrict:
ed by those parts of the organism, which are connected with pecu-
liar conditions of the given environment. The organization as a
whole is at a fairly low level or experiences some simplification.
Here specialization covers mainly the organs of nutrition and food
catching as well as means of locomotion.
Ав Т.Г. Schmalhausen (1946, page 473)observes "in раги-
cular, the biologically coordinated adaptations are characteristics
of allomorphosis and even more for telomorphosis combination of
the changes is explained by the relation of the с gans with certain
general factors of the environment*,
296
VIEWS ON TR ANSFORM ATION
Reviewing the relation between the specialization of the
organism and the problem of extinction, Т.Г. Schmalhausen
(1946, page 475) writes :
"Specialized organisms are strongly connected with the
limited environment and hence lose their plasticity. Telomorpho-
sis closes many possibilities of further evolution. Hence even
the question of progressive specialization of organisms is close to
the question of its extinction. Unilateral specialization is, in
fact, related to a real danger of extinction. This does not mean
that specialization leads to extinction owing to inevitable internal
factors".
А ‚мау out from such a "blind alley" caused by specialization,
according to Г.Г. Schmalhausen (1940, page 484), 15 a regression
of the slightly specialized organs leading to relative despecializat-
ion. Whenthere are quick changes inthe environment it is арра-
rent that only degeneration may, at times, save the organism
from extinction".
Thus, unlike Е, Cope, 5. Depiere and others, I.1.Schmal -
hausen sees possible means for further evolution of forms with
highly specialized organs.
B.C. Matveev (1940, page 391) emphasizes that геаггапре-
ment of ontogenesis is an important means for Overspecialization
of species adapted to limited environmental conditions.
"For such specializations, the means for further evolution
during the rearrangement of all features of organization to
Others, frequently inversely proportional to the environment, is
not closed. A complete rearrangement Of organization in another
direction is quite possible in those stages of ontogenesis when the
process of morphogenesis is not yet complete" (underlined by
B.S. Matveev).
Summing up our discussion of the views on the coordinated
nature of transformation of organs in phyloOgenesis, it may be
concluded that biology till today abounds in views which state that
when there is a change in the conditions of the habitat, the organs
of a system (in biological coordination with one another) get
transformed more or less synchroOnizingly in the same direction).
Рот
N.N.VORON TSOY
These biological coordinations limit the possibility for indepen-
dent variation in the individual organ of a given system (or
systems, in biological coordination). A similar "total" specia-
lization of al! the biologically coordinated organs leads to loss
in ecological plasticity, creation of blind alieys of evolution and
extinction. That is why specialized forms cannot form the basis
of new branches of development. Hence we may draw the practi-
cal conclusion whether it is possible to reconstruct the entire
organism from its separate fragments on the basis of the pre~
sence of more or less strictly coordinated n=ture in the trans:
formation of organs.
Is it so?
The author published a review of these concepts in 1961 and
1963 (Vorontsov, 196ta, 19614 and 1903e). Our interpretation of the
non-uniformity in the rate of transformation of organs was support-
ed by Е.Г. Lukin (1964), B.S. Matveev (1966) and A.V. Yablokov
(1966).
It should be noted that Lukin (1964) has put the questionina
wider perspective. His articles (196la and 1903e) deal with the
non-uniformity of the rates of transformation of organs belonging
to one biologically coordinated system. E.I. Lukin considers the
phenomenon of non-uniformity in the rates of transformation appli-
cable to the different systems of organs, often not directly coordi~
nated with one another biologically. Such an approach is cloge to
Abel's approach (see above).
According to E.], Lukin (1964, page 1118) "retardation of
any systems and adaptations may be liquidated in the process of
further evolution, but is retained in.a number of instances. The
reascns for retaining them may be : a) compensation of the poorly
developed lagging systems by other systems and adaptations, b)
ensuring divergence with other groups as a result of retardation
of certain systems and adaptations suitable for the given group of
animals and c) development of new correlations of the lagging
systems and adaptations with mor quickly developing systems and
adaptations if it is not visibly reflected on the general adaptability
of organisms."
Sinc: this book deals with organs of one biologically со-
ordinated system, Only the phenomena connected with the evolution
of organs © this systern shali be discussed further. Without deny-
<
~4IG
UNEQUAL RATES OF TRANSFORM ATION
ing the possibility for a wider interpretation of the phenomena of
non-uniformity in the rate of transformation of Organs proposed
by Е.Г. Lukin (1964), we restrict ourselves to reviewing the regu-
larities in the phylogenetic transformation of organs of One system.
Ze Unequal Rates of Transformation of Biologically Coordinat-
ed Страпз in the Process of Specialization.
Starting from the traditional point of view given above, it
may be expected that equal degree of specialization of each portion
of the digestive system in forms, most adapted to One or the Other
mode of nutrition (Fig. 143). Meanwhile, a study of the rodent
digestive system shows that the individual organs of species may
be at completely different levels of specialization (Vorontsov, 1957,
190la, 1961Ъ, 1962a and 1962b) and the series of specialization оп
the basis of the study of One Organ do not correspond to the series
оп the basis of other organs of portions of the digestive system.
~
$
и Ay
3 x
= YY
5 3
= 1-2
Е © с,
= AS
tos
S oe
Ся oS
5 ва
= & be
5 Ss
Cy x
le
Fig, 143: Chaat of equal rates of transformation of biologically coordinated
system of digestive organs. Vorontsov (1961 а). t- tecth,
s- stomach, 1- liver, c- caecum and cs- colic spiral of large
intestine. Left-extreme degree of adaplation for proteo -lipoid
nutrition: brachyodont, one-chambered glandular stomach.
eight -lobed liver with gall bladder, poorly developed caecum,
large intestine colic spiral having 0-1 lurn, Right-extreme
degree of specialization for cellulose nutrition, hypsodont,
prism-shaped molars, multichambered stomach with predomt-
nance of corneous epithelium, six-lobed liver without gall
bladder, complex caecum with spiral valve, large intestinal
colic spiral with 9-10 coils; center -inter mediate types of
structure, A,B,C, and О hypothetical forms with synchronized
transformation of digestive organs. (a) Protein nutrition:
(b) Cellulose nutrition. |
Absence of complete coordination between the stomach
structure and the corresponding development of the sections of the
intestine have already been observed (Vorontsov, 1957) in certain
forms of Cricetinae. Alarge number of examples of the unequal
299
N.N.VORONTSOV
rates of transformation of the digestive organs (Fig. 144, П) is
observed in the widely divergent ancient group of Cricetinae.
Fig, 144:
Cp Cg № Rn As
Ре Phr,Aa Ns № Sh NF
oe
>
a”
oe
И аи
mY
Е ae
Ва =
9—4 Ф
| oo
3 ih 1s)
я >
Е ane
° oO -
© wre
a 5
fay
=———-—-
300
UNEQUAL RATES OF TRANSFORMATION
Mostly herbivorous Sigmodon hipidus has highly specializ-
ed teeth, initiating the molar structure of Microtinae. Sigmodon
has in its large intestine accessory ampullae coli-ampullae and
complex spiral of large intestine but in its morphology of stomach
and liver this is the most primitive species among all the forms
of Cricetinae studied. |
Among the entire Cricetinae it is the seed-eating brachyo-
dont, Peromyscus californicus that is characterized by the most
complex three-chambered stomach, homologous to the stomach
of Prometheomys, which is adapted to digest the cellulose food.
In its structure of the dental system and caecum, Necto-~
mys squamipes is the form that is most adapted among all the
members of Oryzomyini to cellulose nutrition. However, by its
stomach structure, N. squamipes is more adapted to proteo-
lipoid nutrition than the seed-eating Oryzomys as such.
The structure of molars of Neotomodon alstoni is less
adapted to cellulose nutrition than of Neotoma, but the stomach
structure and development of caecum in Neotomodon is more
suitable for cellulose nutrition than in Neotoma floridana and
even 1п М. albigula. However, by the large intestinal structure,
Neotoma is more adapted to cellulose nutrition than Neotomodon.
Teeth and liver structure as well as the correlative develop-~
ment Of the sections of the intestine are quite identical inthe ham-
sters Phodopus sungorus and Ph. roborovskii, whereas the sto-~-
mach of the latter species is more adapted to taking the vegetative
parts of the plants. 7
It would seem as if the bunodont teeth and the simple caecum
of Lophiomys imhausi are mostly for proteolipoid nutrition,
whereas its five-chambered stomach with well developed cor neous
portions shows that this species is perfectly adapted to cellulose
nutrition.
Considerable variability of the dental system is observed in
the forms of the subfamily (Gerbillinae from.brachyodont, clearly
bunodont (Monodia and Gerbillus) to brachyodont, but with simpli- |
fied masticatory surfaces (Meriones) and finally to hypsodont
with simplified masticatory surface and constant growth of the
301
N.N.VORONTSOV
prismatic molars (Rhombomys), Meanwhile the stomach struc-
ture and correlative portions of the intestine of this series do not
vary practically.
Highly specialized lemmings (Lemmus) have highly compli-
cated prism shaped teeth constantly growing throughout their life,
the number of coils in the large intestine spiral goes up to 10 but
the stomach and caecum of lemmings, unlike many Other forms
of Microtinae, are not highly specialized for cellulose nutrition
(Fig. 145 B).
Fig. 145: Unequal rales of the transformation of digestive system and
compensation of functions in Microtinae, After Vorontsor (1961, a).
A- Prometheomys, B- Lemmus: (a) masticatory surface M1;
(b) stomach (corneous epithelium is shown crosshatched); (с)
caecum: (d) colic spiral of large intesine (cosp). Arrows indi-
cate the direction from less specialized to more specialized
Structure,
UNEQUAL RATES OF TRANSFORMATION
The primitive Microtinae, Prometheomys schaposchnikovi
have sirople brachyodont teeth, its large intestine spiral hus
only 2 «oils whereas the caecum is considerably large in Size.
By its stomach structure this is the most specialized species 1п
the whoie of Microtinae (see Fig. 145 A).
The simple structure of caecum in Lemmini is compensat-
ed by the elongation of the entire intestine. The complete struc
ture of caecum compensates for the relatively short length of
“the intestine as such. The highly complicated colic spiral of
Cndatra zibethica compensates the function of the relatively
simple caecum of this species.
It is well known that Apodemus aquarius differs consider -
ably from mostly seed~-eating Ap. sylvaticus and Ap. flavicollis
in its cellulose jutrition. However the caecum is less develop-
ed in Ap. aquarius than in Ap. flavicollis and Ap. sylvaticus
(this wis estad\ished even by N. P. Naumov 1948); meanwhile,
by its stemach structure, which fully agrees with the ecology
of these species, Ap. aquarius is more adapted for digesting
cellulose food than Ap. sylvaticus (Fig. 146).
Highly unequal rates of transformation of the different
organs Of the digestive system may be observed in Nesokia indica
(Fig. 144,1140). By the structure of its dental system, this form
feeding mostly on the underground parts of the plants, is more
adapted to cellulose nutrition than the other members of Murinae.
Stomach and caecum of Nesokia indica are more adapted to ©
protein nutrition than in all other members of Muroidea (1),
whereas reduction of all gall bladder and square lobe shows that
the process Ot adaptation of liver to cellulose nutrition has аа-
vanced iurther. |
In the groups Dipodoidea the structure of molars varies
from bunodont with low crown (Sicista) to the type of teeth with
simple masticatory surface and prism shaped molars, crown is
raised from brachyodont to mesodont (Allactaga, Alactagulus,
Pygerethmus). Meanwhile a highly similar stomach structure
of the glandular type adapted to protein nutrition is а character-~
istic feature ot Dipodoidea, when certain forms have chanyed
Over almost exclusively to cellulose nutrition (Fygerethmus).
303
N.N.VORONTSOV
Ml
Fig, 146: Unequal rates of transformation of the organs of digestive system
and compensation Of functions in Muridae. After Vorontsov
(1963 e), I- Structure of the masticatgry surface of molars;
П- Slomach structure, horizontal crosshatched lines indicale
corneous epilhelium and vertical lines - glandular epilhelinm;
Ш- Relative development of the sections of intestine, horizontal
crosshatched lines - small intestine vertical crosshatched lines -
small intestine vertical crosshatched lines - large intestine
marked in black - caecum; the numhers show the relative length
to the total length of the intestine (%); and IV- caecum structure.
Lefl-structure of organs adapted for proteolipoid nutrition, right -
for cellulose nutrition Aq - Apodemus agrarius, As - Apodemius
sylvaticus, Cy - cricelomys gambianus and М; - Nesokia indica.
М.У. Clkova (1960), studying the structure of intestinal
tract in certain species of rodents, has arrived at similar
conclusions :
"Insufficient development of one or the other component
of the structure constituting the surface of mucOsa of any por-
tion is compensated by the development of other components of
the structure leading to an increase inthe surface. Thus, in-
sufficient area of the surface of mucosa may be compensated by
greater height of glands; short length of One or the Other section
by the large diameter of lumen, insufficient height of glands",
by the development of outgrowths, folds etc." (page 234).
304
UNEQUAL RATES OF TRANSFORMATION
The number of examples of the unequal rates of transforma-
tion of organs Of the digestive system may increase considerably
when any group of rodents is analyzed in detail. A study of the
digestive system of rodents and even other mammals shows the
universal nature of the given phenomenon-different levels of spe-
cialization of the individual links of the single system of digestive
organs. We may state that in the different groups of rodents,
changes in the mode of nutrition reflect on the different organs of
the digestive system. Unequal degree of specialization of the
different organs of the digestive system is, apparently, related to
the hereditarily caused stability of certain organs and liability of
Other Organs.
In rodents, digestion of cellulose food includes basically the
grinding and crushing of-the vegetative parts of the plants by teeth,
maceration and fermentation in the corneous "proventriculus", .
caecum and large intestine. A more thorough crushing of foed
Simplifies its maceration and fermentation may make up for the
cellulose food less thoroughly treated mechanically inthe mouth
cavity.
Examples of unequal rates of transformation of organs, in
biological coerdination, may be met with not only in the study of
the digestive system. In burrowing rodents the fore~-limbs as
well as the incisors with which they stir up the soil are зёгепр-
thened. In all fossorial rodents both incisors and fore limbs are
strengthened in comparison with their closely related forms;how-
ever, the development of one part always leads to the development
of another. In Spalacidae (Spalax) incisors are more powerfully
developed than in zokors (Myospalax), whereas the paw of zokor
is provided with well developed claws (Fig. 147). The same
relation between the structure of incisors and front-limb claws
is Observed also in fossorial voles and lemmings. In mole-
voles (Ellebius) the incisors are hypertrophized whereas the fore-
claws are sOmewhat larger than in forms less specialized for
burrowing (Microtus, Glethrinomys). In long~clawed mole-vole
(Prometheomys) the reverse relation-front paw claws-well
developed whereas the incisors are Only insignificantly enlarged
(Fig. 148).
Jaeckel (1957) observes that in cephalopoda there exists
a relation between the development of siphon and velum - organs
305
М.М, VORONTSOV
Fig. 147: Compensation of the function of fossorial organs. After Voronrsov
с). А +i» Shalacidae (Spalax), В - in zokor (Myospalax).
vial burrows with its inctsors, the claws are poorly
bul if i. burrows with the claws, the mcisors aré poorly
Lovi-skhull, right-fore paws, АЦ figures are т the
of the jet propulsion locomotion of these forms. Species with
strong siphon and well developed apparatus for closing the mouth
slits possess poorly developed velum, whereas species with well
developed membrane between the claws are characterized by
small siphon and poorly developed apparatus for closing the
mantle slit.
М.Г. Kalabukhov turned the author's attention to the
unequal rates of development of functional shifts in the intensity
of metabolism and ensuring its maintenance of respiration and
blood circulation. He writes :
"With hypoxia observed while climbing mountains the
same result, namely facilitating the tissue respiration (in spite
of the low pressure of oxygen in the atmosphere) is obtained by
altogether different means in closely related forms, for example
in the mountain and plain specimens of the same species or
306
UNEQUAL RATES OF TRANSFORMATION
Fig, 148: Compensation о} functions of burrowing organs. After Vorontsov
(1963 e). A - т mole-voles (Ellobius), В - in long-clawed mole -
voles (Prometheomys). 1 the animal burrows with its incisors,
the claws are ill developed and if it burrows with its claws the
incisors are ill developed. Left-skull, right-fore paws. All the
figures are in the same scale.
closely related species. The forms living on high mountains are
perfectly adapted to this hypoxia, (the level of its cellular meta -
bolism is relatively low...) in those living at medium high
mountains this compensation is provided by increased haemo -
globin content in the blood and finally, animals living in plains
in the first period of ''acclimatization"' to hypoxia react by
increasing the rate of blood circulation then only by increasing
the number of erythrocytes in blood, ''*
ar The Principle of Compensation of Functions. Importance
of Unequal Rates of Transformation of Organs for
Despecialization.,
In all the instances described above we have encountered
the phenomenon of compensation of functions of one organ of the
given system by another of the same system. It seems to us
that this phenomenon is one of the types of phylogenetic varia-
* М Г. Kalabukhov, Verbal statement.
57
N.N.VORONTSOV
tions of the organs and should find a place in Severtsov's classi-
fication system of the principles of similar variations (Severt-
sov, 1939).
By the principle of compensation of functions is meant the
ee ewe w= ee ee ee ee ee ce re ee ee ee ee ee as SS eee ee ee
phenomena of phylogenetic variability of organs of one system,
in which a quick and complete (in the sense of narrow specializa-
tion) variation of certain organs owing to environmental
ee ne ee ee es ee ee SO, ae Se -->--[[--Ь —— ee wae eae SSS ee
requirements compensates the long lag in the rates of the deve -
me me a a ee a ee ae ae es eS = ee
whereas intensification of the functions of another organ of the
same system may not set in at all or alternatively the intensi-
fication of the functions of the latter organ will take place at
slow speed, Unlike the principle of physiological substitution
of organs, formulated by О.М. Fedotov (1927), the compensat -
ing organ does not acquire any new functions during this, but
only intensifies its characteristic functions earlier.
Unequal rates of transformation of organs and the compen -
sation phenomenon, as is evident from a literary review were
widely known to zoologists. The concept of "reverse biological
coordination put forward by I. I. Schmalhausen (1939b and 1946)
is close to the group of phenomena being described.
It is important to note that, in nature, along with the close
correlation of organs, to which the biologists first pay their
attention, there exists a certain fraction of ''freedom", relative
independence and absence of complete correlation between <
organs; this enables the organism to adapt itself to any change
in the environmental conditions quickly most economically and
in shortest means.
It is remarkable that extreme degrees of specialization
= -----------------_-------------
digestive system even in such forms as lemmings that are highly
a ee ee eee ee
UNEQUAL RATES OF TRANSFORMATION
specialized and passing through a period of decline. This.
indicates that even highly adapted stenobathic forms are not _
conditions. Thanks to the unequal rates of transformation of |
organs there remains in these species some less specialized
features which when there is a change in the environmental
conditions, may develop in a direction opposite to that in which
the compensating organs have developed earlier. When there is
such a change in the ecological condition, the compensated organ
may become the compensating one and vice versa.
Protein nutrition (seeds and small invertebrates) is mostly
a characteristic of the primitive forms of Cricetinae (Oryzomys,
etc.). Sharp bunodont teeth and stomach predominantly covered
with glandular epithelium match this type of nutrition. Many
hamsters have passed on to mixed and then purely cellulose
nutrition. In certain forms a similar change in nutrition has
caused, inthe first instance, a simplification of the surface of
molars, with the retention of the initial form of the stomach
thelium develops in the stomach and the glands are restricted
only to a small portion of the fundus ventriculi,' whereas the den-
——_— =
roborovskii, etc.). When there is a change in the ecological
conditions owing to the penetration of hamsters into a region
where insectivorous mammals are absent, certain forms
Onychomis) secondarily pass on to proteo -lipoid nutrition
(Vorontsov, 1959a, 1962a and 1962b). Presence of corneous
epithelium in stomach, inherited from herbivorous forms
enabled these species to be specialized for insectivorous nutri -
tion, as the corneous epithelium protects the stomach from
coarse chitinous parts, In Oxymycterus and Onychomys the
fundus glands are separated into special diverticulum ventriculi
of the stomach, which is in fact a large gland producing gastric
juice. In these forms the glandular diverticulum compensates
the less distribution of the glandular fields along the stomach
walls. The dental system of the herbivorous ancestors of the
insectivorous hamsters had, in their times, almost remained
unchanged and its lagging should be compensated by an intensi -
fication of maceration and fermentation functions of the horny
stomach. When there 15 a change in the ecological conditions,
309
N.N,VORONTSOV
this lag in the development of dental system enables the ham-
sters of the group Oxymycterus, Blarinomys and Onychomys to
quickly adapt themselves to insectivorous nutrition, i.e., to
secondarily pass over to proteo-lipoid nutrition.
The widespread unequal rates of organ-transformation,
with a change in the habitat conditions and the compensation of
functions enable us to consider these phenomena as regularities
of general biological importance. We did not succeed in finding
in general not even a single instance of synchronized transforma -
tion of all the organs of a system in the investigated material.
High specialization of all organs of a given system to the
present day conditions, if such a specialization exists, generally
would have created conditions for the flourishing of this group
at present, but it would also have made this group nonprospective
in evolution plan. Ё is well known that radically new forms
originate from animals of the so-called ''generalized"' biological
type and not from highly specialized forms. Meanwhile, uni-
versal biological forms are always adapted to particular ecologi-
cal conditions and may, often, not only be eurybathic, but also
stenobathic. This stenobenthic nature is achieved by high specia-
lization of certain links of a system of organs, whereas the
remaining organs of the same system remain slighly specialized,
The principle of compensation established above is applicable
here. Similar stenobenthic, but highly specialized forms where
the functions of certain organs are compensated by other organs
of the same system may subsequently, when there is a change
in life condition,be perspective from the evolution point of view,
while the organs of the given system specialized earlier will be
subjected to specialization.
When there is a change in the direction of specialization,
the organs of the given system that were conservative (for
development in one direction) earlier, may turn out to be more
tended to the development in another direction; they will be
quickly and more narrowly specialized than the organs of the
same system that are narrowly specialized (in another direction),
These newly specialized organs may compensate the imperfec -
tions in the functions of other organs, which have played earlier
the paramount role in the life of the organism and the activity
of the given system, ensuring thereby conditions for the survival
310
UNEQUAL RATES OF TR ANSFORMATION
and flourishing of the group in the new ecological conditions.
We should remember that the more vigorously the given organ
functions, the lesser its variability, and the less the functioning
organs are characterized by the maximum variability range.
Starting from this long -known proposition, it may be considered
that the variability of the organs to be compensated should be
more than that of the compensating ones; considerable range of
variability of the organs to be compensated facilitates their
transformation: when there is a change in the ecological condi-
tions.
It does not follow from this that the unequal rates of
organ-transformation prevent the onward course of evolution
and specialization of organisms. Inspite of the unequal rates of
transformation, the organs of the digestive system of herbivorous
group of Microtinae derived from Cricetinae, are distinguished
by the narrow specialization features. The most primitive
forms of Microtinae (Fibrini) is ‘more adapted to feeding on
coarse food than the primitive forms of Cricetinae most specia -
lized forms of Microtinae (Microtini and Gemmini) are more
only as a general tendency while comparing the entire digestive
system as such and not while studying its individual organs,
which, by virtue of the unequal rates of transformation, may be
in quite different levels or degrees of specialization.
a Importance of Unequal Rates of Organ-Transformation
and Compensation of Functions in Ontogenesis.
Ecologists' concepts of the degree of eurybenthic and
stenobenthic nature of the species are fairly schematic. They
become still more schematic at the hands of ecological morpho-
logists, sometimes reducing morphological series to ecological
series, and wishing to see compiete correlation of the former
with the latter.
Meanwhile the life conditions of the species are quite
diverse, These are not the same for young, adult and old
individuals, but vary cunsiderably with seasons, vary within the
same season of different years and vary considerably in different
parts of the area,
311
N.N.VORONTSOV
To what extent does the range of intraspecific variability
of morphological structures in all its forms (depending on age,
season, geography, etc.) correspond to the extremely wide
range of variability of ecological conditions? To avery small
extent, is the answer. Geographic, seasonal and even age
intraspecific variability in the nutrition of rust-colored
voles fully coincides with the interspecific var м
nutrition of these forms when they have а common habitat
(Vorontsov, 1961Ь). Besides, the geographic variability of the
digestive system within these species has a negligible range.
Even in the same zone, and the same season of different years,
the nutrition of a species may vary in the way distantly related
forms of different ecological groups as a whole vary. Inthe
districts near Moscow, during September and December, seeds
were found in 77.1% of stomachs and plants - only in 14.3% of
stomachs Cl, glareolus, which according to the nutrition
spectrum is close to the nutrition of such seed - -eating species,
as Apodemus sylvatious (Seed in 94. 3% of stomachs and plants
in 14.6% of stomachs, М.Р. Naumovy 1948) and in the period
November -December of the snowless winter of 1954, in the
same districts, seeds were observed in only 15.0% of stomachs,
whereas plants were observed in 77. 5% of the individuals
studied (Vorontsov, 1961b) which according to the nutrition
spectrum is close to such herbivorous species as Microtus
socialis (seeds in 19.1% of stomachs and plants in 97.6%, М.Р.
= —щЩ
Naumov, 1948). In summer, ae food of тан вов mice
— ee oe = =, —= ee ae ee ee
they oy on vegetable materials.
In all these instances the digestive system should ensure
the processing and digestion of these quite different food
materials. Undoubtedly there should be some physiological
mechanism for regulating the digestion of the biochemically
different food materials. It is similarly undoubtful that the
morphological structure of the digestive organsis adapted to a
larger or lesser extent to thenatural changes in the life condi -
tions, expressed clearly by a change in the type of nutrition.
That is why it is well assumed that the unequal rates of
the transformation of organs of the digestive system serves not
ae
UNEQUAL RATES OF TR ANSFORM ATION
only as a reflection of the phylogenetic history of the species,
but also as an adaptation for the seasonal variability of environ-
mental factors. It is possible that, in the life of an organism,
the organ 'А' may compensate the function of organ Bina
season, whereas in another season organ B may compensate
the function of the organ A.
If this assumption is right, the unequal rates of organ-
transformation should be expressed less in forms living for a
long time under the same environmental conditions, without
seasonal fluctuations, than in forms living under conditions
where the seasonal fluctuations are clearly expressed.
If the specialization of an organ of the digestive system is
fairly high, the unequal rates of organ-transformation only
creates conditions for the multifunctional action of the entire
system.
In this sense it may be said that the phenomena of the
unequal rates of organ transformation and compensation of
functions serve as the morphological basis of the potential
adaptability of the species, not only in phylogenesis, but also in
ontogenesis.
From this it follows that the phenomena described here
should be taken into consideration also for acclimatization.
Actually, the niche similar to the native place should be selected
for a species for acclimatization, without the consideration of
the phenomena of compensation. This considerably decreases
the number of species recommended for introduction. On the
other hand it is necessary to consider the wide morphological
basis of the potential adaptability of species as a result of which
the species often considerably change their habits and become
pests under the new conditions, after entering into the new niche.
The degree of unequal rates of organ-transformation is an
index for determining the potential damage spectrum while study -
ing the pests.
Thus, unequal rates of organ-transformation not only
facilitate adaptation to a change in the habitat conditions in
phylogenesis, but also enable to get used to the different possible
313
N.N.VORONTSOV
groups of food in the life of an organism. The same unequal
rates and compensation of functions lie at the root of such eco-
logical phenomena, as seasonal and geographical change in the
life conditions.
It should be emphasized that forms, similar or approxi-
mately similar in the structure of their digestive system may
differ from one another in the type of their nutrition. The struc-
ture of the digestive system of the genera Cricetulus, Allocricetu-
lus, Cricetus and Mesocricetus is very similar; but Allocricetu-
lus and Cricetulus barabensis are carnivorous, whereas Meso-
cricetus is mostly herbivorous. As V.D.-Spanovskaya ( 1961)
observes, though all fishes of the genus Gobio are ''morphologi-
cally similar'' some of them are stenophagous in their mode of
nutrition, others are euryphagous (page 1522). Examples of
Similar genus are fairly numerous and may be Seen in any group
of animals.
Thus, unequal rates of organ-transformation and compen-
sation of functions provide quick and economical means of the
adaptation of an organism to the changes in the habitat conditions
both in phylogenesis and ontogenesis.
The unequal rates of organ-transformation and compen-
sation of functions serve as the biological and morphological
basis of the phenomena of eurybenthic and stenobenthic nature.
The ''generalized'' forms prospective from the point of view of
evolution are adapted to the concrete conditions of the present
lay by the compensation of functions.
The unequal rates of organ-transformation and the principle
of the compensation of functions, in fact, lead to a more general
law namely, the nature by selection creates ''perfect adaptations"
by more economical and brief means.
While judging the structure of the organism on the basis of
the study of its parts and paleontological reconstructions,
morphology and particularly paleontology should be taken into
consideration along with the unequal rates of organ-transforma-
tion in the process of adaptation.
CHAPTER IX
Homologous variability
Many examples of homologous series of variability are
given in Chapters II-VI of this work. It is expedient to discuss
the considerable material on the homologous variability of the
digestive organs not only from the point of view of comparative
anatomy and evolution- morphology but also from that of genetics.
The law of homologous series of inherited variability put
forward by N.I. Vavilov in 1922 is rightly considered by many a
biologist as an analog of D.I, Mendeleev's periodic system of
chemical elements. N.I. Davilov's law enables us to foretell the
presence and properties of not-yet-described forms of a second
series, living under conditions similar to the homologous forms of
the first series (Table 14) after studying a series of homologous
variability of one species (or genus) and observing the homologous
series of variability of another allied species or genus.
TABLE 14
М.1. Vavilov's system of homologous series of variability (original) .
Systematic Niche.
category
ао ey
|
и ЕН le agli Ke el oko
т Ke 32 с2 02 5 Е? с? 2 р jy 5 2 м2 м2
315
N.N.VORONTSOV
After establishing the complete series of variability within
the group (genus and species) Ifrom А! to N! and observing
that a few forms inhabiting the niches 5, 8, 11 and 12 of the series
from AZ to N@ of the allied group II are not yet studied, we may
predict their basic morphological and ecological properties and
confirm that if group II also occupies niches 5, 8, 1] and 12 as
group I the similarity among the forms living in similar niches
will be quite triking. Thus the very existence as well as the
peculiarities of forms E2, НА, К? and L“ not yet discovered may
be predicted. The characteristics of the extreme members of
the series not yet studied may be predicted less authentically.
Thus characteristics and existence of forms I> and К? of group
III may be predicted on the basis of the comparison between the
series С3-МЗ and C!-M! as well as C“-M*. However, in spite
of the presence of such niches forms A>, B3 and N may be
absent. This may be caused by a general decrease in the range
of variability of group III, for example, as a result of the preced-
ing inhabitance under more uniform conditions and loss of genes
leading to extreme significant manifestation of certain traits,
i.e., аз a result of stabilizing selection
А quite similar interpretation follows fromN.I. Vavilov's
studies. In its original form М.Г. Vavilov's laws of homologous
series of inherited variability plays an exclusive role. Like the
chemists of later XIX and early XX centuries, the biologists
could predict the existence of undiscovered ecotypes, races,
species and genera and to describe their characteristics.
Analogy of N.I. Vavilov's law with D.I. Mendeleev's system
goes further. О.Г. Mendeleev discovered the phenomenon of
periodicity in the properties of elements, but did not explain the
reason for this phenomenon. Only the discovery of atomic struc-
ture in the early XX century (E. Rutherford, J. Thompson and
N. Bor) revealed that the periodicity in the characters of elements
depends on the structure of the electronic shell of atoms. In
1922 N.I. Vavilov could not even explain the cause of the ''periodi-
city" in the characters of the members of the homologous series.
Later N.I. Vavilov (1939, page 138, 139) wrote "According
to us the nature of this homologous variability consists first of
all in the affinity and unity in the genetic structure of the related
species and genera. On the other hand it is the result of the
316
HOMOLOGOUS У ARI ABILITY
environment, and selection in a particular direction, under
specific conditions." He continues further ''New profound genetic
studies, have of course, hetped us to deepen our understanding of
the phenomena of variability and to differentiate them. Ш certain
cases, they have among them a similarity of genes and in other
cases their phylogenetic characters.
Lys Cytogenetic and molecular bases of homologous and
back mutations.
Progress in the field of evolutionary genetics in the late
thirties enabled us to indicate that on the basis of similar pheno-
typic changes of allied species and genera there may be similarity.
in their genotypes. The homologous nature of genes in the allied
species of Drosophila was established. It was algo shown that
considerable portions of the chromosomes in different species
may have similar genes (Dobzhansky, 1937). At present it is
known that allied species may differ from one another only by a
small number of genes, and genetic isolation between these
species may be maintained by another grouping of the genic
material by intra- and interchromosomal translocations.
Homology of genes in allied forms results in the formation
of different homologous species among the newly formed muta -
tions. Living in similar niches (for example, in the different
islands and continents and subjected to similar effect of selection
these species give homologous forms, belonging to one and the
same "group" of Vavilov's system.
It is difficult to establish homology between mutations
yielding similar phenotypic effect. It is well known, for example,
that the formation of the brown pigment in the ommatidia of
insects' eyes is determined by a chain of reactions: tryptophan
formylkynurenine*kynurenine = oxykinurenine + pigment
(Wagner and Mitchell, 1958). Mutations destroying any of this
chain of reactions lead to similar phenotypic effect. However,
these mutations act at different stages of pigment synthesis.
Recessive mutation blocks formylkynurenine and kynurenine
synthesis in the homozygote of vermilion (v/v) and oxy kynurenine
in the homozygote of cinnabar (cn/cn). Mutation in the indivi-
duals of scarlet with genotype st/st blocks kynurenine and oxy -
&ynurenine synthesis. Cardinal recessive mutation in the
317
М.М. УОВОМТЗОУ
homozygote cd/cd leads to blocking of the extreme parts of the
reaction-breaks formylknurenine and pigment from oxykynure-
nine. All these mutations were observed,in Drosophila melano-
‘gaster (Wagner and Mitchell, 1958). It is remarkable that
mutation of vermilion arises in other species of Drosophila also
Dr. simulans. Dr. pseudoobscura, Dr. affinis and Dr. virilis.
Mutation of cinnabar is known also for Dr. affinis and Dr.
virilis and mutation of scarlet and cardinal are described for
Dr. virilis.
A break in the synthesis of oxykynurenine from kynurenine
is observed even in the mutants of other groups of insects -
in Diptera (Phryne-fenestris, ) Ghalcididae (Habrobracon), and
even in Bombycidae (Bombyx mori), i.e., in most of the
species of insects studied genetically. Whether the mechanism
of suppression of oxykynurenine synthesis is homologous in very
remote systematic species is not yet known.
Genetics at present does not give a definite answer to this
question. On the one hand it is well known that biosynthesis of
certain aminoacids (histidine, arginine) takes place in the same
way in very remote organisms, as Escherichia coli and
Neurospora, and on the other the biosynthesis of one and the |
same compounds (lysine, for example) may be realized by
different methods (Wagner and Mitchell, 1958).
The process of development of back mutations (Timofeev-
Resovskii, 1927, 1929, 1934) plays a major role in homologous
variability. However till recently it was not sure that back
mutation was manifested by previous phenocopy. Recent experi-
mental studies have shown that back mutations, in fact comple-
tely repeat the course and is not a phenocopy but genocopy.
Yanofsky (1960) obtained mutation of the gene governing the
synthesis of the enzyme tryptophafle synthetase in Escherichia
coli - Mutation change of itidividual nucleotides of the triplet
coding the synthesis of any aminoacid (G-Guanine, С -Cytocine,
U-Uracil and A-Adenine) was observed in the subsequent
generations. |
These experimental data which caused a keen interest
among molecular scientists failed to draw the attention of
evolutionists. As it is well known, the difference in some amino-
318
HOMOLOGY OF CHARACTERS AND GENOTYPES
СОС Gigeine}
UG (Glutamic acid) GUC (Arginine)
DUG CURA -GUG GUG vuc
(¥gline) (Alanine) (Glycine) (Glycine) (Serine)
acids serves as the basis for the specificity of proteins which is
a phenomenon of great evolutionary significance.
Experiments on the mutability of gene, governing the
synthesis of tryptophane synthetase have shown that reversibility
of code is possible. Possibility for the development of identical
triplets (triplet GUG, coding the synthesis of glycine may arise
both from the triplet AUG coding the glutamic acid synthesis and
triplet GUC coding arginine synthesis) also deserves special
attention, Thus it is experimentally proved that organisms
having a certain common characteristic may arise from two
organisms different in this characteristic (and according to the
cOde of these characteristics).
Let us remember that Ingram (1959) ha_ shown, on
anomalous haemoglobin ot man, that one mutation causes а
change in one aminoacid in the protein molecule. This change
in aminoacids leads to considerable changes in the individual's
character (for the selective significance of these changes, see-
Efroimson, 1964).
Thus recent data show that homological mutations are
possible in genotypically different forms (for example, in differ -
ent species). Besides, they show the reversibility of mutations
and that of back mutations are possible in genotypically different
forms.
a2: Homology of characters and genotypes. Reversibility
of characters and irreversibility of evolution.
Just as there is a large discontinuity between the studies
of research scientists of micro- and magaevolutionary processes
in the evolution biology, so also is there an equally vast gap
between the studies of molecular and evolutionary biologists.
319
М.М. VORONTSOV
It should be hoped that in the near future, all round attempts will
be made to bridge the gap. However, much sacrifice has to be
made before trying this. The author is aware of the fact that
while trying to cross the bridge between the data of molecular
genetics and those of the ancestors of evolution-comparative
anatomy and paleontology, he finds himself not as a builder, but
as an unwary traveler who has fallen into this abyss.
The concept of homology of organs and their parts develop-
ed in comparative anatomy, describes only the phenomenology of
events. The data of comparative anatomy, throwing light only
on the later stages of ontogenesis, do not give a causal analysis
of the phenomenon of homology, although these may be decisive
in judging the divergent or convergent origin of any formation.
It should be emphasized that the concepts of "homology"
and "homologous elements" used in the special part of this work
is based on the phenomenological approach to the same extent as
other works on evolutionary morphology.
What do we mean by saying that an organ of a species is
homologous to the organ of another species? We start only from
the topographic aspects, usually supported by a comparative
embryological analysis. At the moment there is no connection
between the comparative anatomy concept of "homology" and the
genetic concept of "homology". Apparently, it may be suggested
that anatomical homology depends on genetic homology. The
possibility of the existence of homologous groups of genes govern
governing the development of homologous organs in allied
species and genera may be considered.
What is to be done with the systematically remote groups ?
Is it possible to say that the development of notochord of an
appendicularian, a lancelet, ‘а shark and а rat is regulated by
homologous genes retained even in terrestrial vertebrates? We
cannot give a precise answer to this question. It is perfectly
clearl, however, that the comparative anatomists should un-
consciously stick to such a point of view.
A considerable number of mutations causing similar pheno-
typic effect on individuals of highly remote systematic groups
are known. Higher primates are distinguished from majority of
320
HOMOLOGY OF CHARACTERS AND GENOTY PES
the mammals studied by the presence of uric acid in their urine,
whereas in other mammals the urine mostly contains allantoin.
These differences are connected with the corresponding differen-
ces in the structure and functioning of the kidney membrane.
However, in one of the species of dogs - Dalmatian - the excre-
tion of uric acid considerably increases and that of allantoin
decreases (Wagner and Mitchell, 1958).
Mutations changing the basic structural plan, characteri-
stic of the representatives of a high ranking taxonomic group
should draw the special attention of evolution morphologists.
A few examples are given below.
Mutation of tetraptera causes in flies (members of the
order Diptera) the formation of four wings - a character of
another order. The mutants in this gene are characterized
also by an increase in the number of body segments, 1. е., in
this character it goes beyond the limits ot the class of insects.
This mutation takes place in different species of the genera
Drosophila (Hoddington, 1964).
Mutation of aristapedia changes not only the segmentation
of limbs in diptera (five segmented claw to four segmented
claw i.e., one of;the characters of the order Diptera is lost),
but also may lead to the conversion of antenna into a limb.
This mutation is found in different species of Dvosophila and
Musca.
Metanephros (Wagner and Mitchell, 1958) does not develor
in the homozygote of Denford, short-tailed mouse strains,
i.e., one of the important characters distinguishing terre-
strial vertebrates-amniotes from the aquatic vertebrates -
Anamunia.
The number of similar examples of mutations dealing
with the principles of the organisation of animals may increase
greatly. Such mutations are known among ichneumon flies,
diptera (Drosophila and Musca), silkworms, mice, rats,
goldcolored hamsters i.e., for all animals well studied geneti-
cally, The fact that homologous mutations, changing the
cardinal characters, develop in different species, genera and
even families is more remarkable.
321
М. М. УОВОМТ 50У
This enables us to propose that the homology of the
genotype forms the basis for morphological homology and
homologous genes may be found in the members of systemati-
cally remote groups of animals.
Existence of back mutations leads us to the conclusions
about the possible reversibility of characters in phylogenesis,
and repeatedly occurring characters may be homologous before
they disappear. All these data confirm the correctness of the
suggestion by Р.Р. Sushkin (1915) who assumed that there was
a possible reversibility of characters in phylogenesis.
P.P. Sushkin (1915) correctly projected against the
extraordinary interpretation of the law of nonreversibility of
evolution put forward by Luis Dollo. Nonreversibility of evo-
lution does not exclude the possibility of repeated return of
characteristics disappeared earlier.
Does not the recognition of the possible reversibility of
characters in phylogenesis signify the recognition of the
reversibility of the evolutionary process? No; even the allied
species do not differ from one another in a number of charac-
ters. Even a change in certain genes on account of correla-
tions, pleiotropism and interrelation of genes leads to substan-
tial changes in the individual's phenotypes, cont rolled by
selection, Populations and not individuals evolve, selecting
not individual characters but their complex, controlled not
by a selection of genes but gene complexes. That is why back
mutation by a given character may lead to repeated development
of this gene, but not the genotype as a whole and repeated
appearance of the given character, but not the phenotype as a
whole.
Repeated development of mutation and even repeated
appearance of conditions of selection, favoring its retention
and accumulation are reliable statistically but repeated
appearance of gene complexes once disappeared and phenotypes
once lost are not reliable. Irreversibility of evolution is a
statistical process.
322
SUPERSPECIFIC GROUPS
3. Monophbyly and the possibility of Parallel
Occurrence of Superspecific Groups.
Strict monophyly presupposes that all members of a
given taxon are derived from а commgn ancestral species.
Such a concept was not reviewed even though a good number of
data on the polyphyletic origin of groups, considered earlier
as monophyletic have been collected in the last one and a half
decade.
Institution of polyphyly became, perhaps, the order of
the day. It is acknowledged that Glires is a collective group
and has two orders, Lagomorpha and Rodentia. The question
on the polyphyletic origin of Cetacea and its division into orders
My sticeti and Odontoceti 15 in the stage of discussion. Not
only the collective nature of the group Edentata (which is
classified with orders, Palaeanodonta, Pilosa and Cingulata)
but also the polyphyly of Pinnipedia is being discussed. Notions
on the polyphyletic origin of mammals and reptiles are wide
spread.
If subsequently the concept of "strict monophyly" is
applied to all taxa above the family, we will soon come to the
conclusion that all the large systematic groups of the animal
kingdom have originated polyphyletically.
It is believed that there is no actual basis at the moment
for applying the concept of "strict monophyly". It is clear that
the general homologous genes are retained in the allied species,
genera and families. These homologous genes may mutate
homologically.
Under similar conditions of existence (not necessarily in
homologous niche only) the selection trend will be similar and
leads to retention of homclogous mutations developed in forms
which have differed’ earlier in other characters.
The change in the conditions of existence at the end of
Paleozoic era and general "drying of earth" facilitated the
elimination of semiacquatic forms associated with water (re-
Production, cutaneous and pulmonary respiration, acquatic
stage in development) led to reproduction independent of the
323
М.М. МОВОМТЗОУ
acquatic medium (emergence of amniotes), protection of skin
from drying (appearance of scales, reduction of glarids, reduc-
tion of cutaneous respiration with compensating complex struc-
ture of lungs), perfection of locomotion, etc. The entire,
closely allied system of characters distinguishing the reptiles
from amphibians is the result of the selection of innumerable
combinations of repeated occurrence of mutations. Naturally
the transition from amphibian "level of organization" to the
reptile one was not simultaneous in all its characters. Seymou-
ria in its many characters, formed an odd combination of the
features of both the classes (Schmalhausen, 1964b), some
amphibian characters and some of colylosauria were retained.
Schmalhausen (1964b) considers the origin of ichthyosaurs from
embolomeri as independent. Thus the gap at the reptélian level
of organization is filled at least by two different amphibian
groups. However, it is significant that both these groups are
derived only from one of the branches of development of
amphibia, namely anthracosaurs, It is certain that the members
of one line of amphibia possessed a considerable number of
homologous genes. Homologous mutation of these genes and
free directions of selection led to a parallel "gap" in the
different descendants of anthrocosaurs at the reptilian level.
Cooling off towards the end of Mesozoic era and increase of
moisture led to similar selection to different groups of verte-
brates. In the descendents of the much diverged branches of
reptiles-aves and mammals - a heat protecting coat developed
convergently. They acquired a constant body temperature and a
four -chambered heart; one of their aortic arches was reduced
and the respiratory organs became highly complicated.
Reptiles belonging to one of the branches (Theromorpha),
apparently made several attempts to attain the level of warm-
bloodedness. But, owing to the generality in the genetic compo-
sition, all the descendants of this group with beastly characters
are considered mammals. It is undoubtful that the mammalian
level was achieved in certain places. When there is divergence
of species in special characters (adaptation in the narrow sense)
the generality in the gene composition of the diverged forms
may, apparently, be retained for long. Transition to another
"adaptive zone" (Simpson, 1948) - aromorphosis - may affect
not one, but many species, possibly, belonging to different
324
SUPERSPECIFIC GROUPS
families of the class. As a result of aromorphosis, selection of
homologous mutations leads to the emergence of forms so well
distinguished in the cardinal features of organization that we may
take them to be а new order or even class. However inthis
case, it will be hardly right to speak of the polyphyletic origin
of groups. The very possibility of homologous mutation and
parallel development of descendents of the groups divergent
sometime was due to similarity in their genotypes, 1е., in the
final analysis on the commonness of origin.
I. I. Schmalhau'’sen (1947, page 191, 192) cautioned about
the extraordinary increase of "strict monophyly”.
"Monophyly should not be understood ina very narrow
sense. Concrete organisms evolve into a great number of
individuals, among which there takes place constant differentia -
tion. This entire mass аз a rule, continues to develop under
similar (in general) biological conditions, and consequently,
parallely. Hence all these individual stocks, branches, allied
strains, etc. which were discussed...... are not branches and
individual strains, but a group of branches of innumerable
number of parallel (in general) strains, which we present only as
branches for simplicity and clarity. Underlying such branches,
let there be always a group (and not individual) of в inter -
breeding individuals even at the depth of stock".
It is believed that one is competent to speak of the poly-
phyletic origin of forms of any taxon only if these are derived
from two different taxa of the same systematic rank, for example,
a branch of mammals evolved from reptiles and the other,
directly from amphibia. Polyphyly cannot be taken under the
same conditions when it is established that the forms of a high
ranking taxon are derived from two forms of a low ranking taxon
(associated with one another in a high ranking taxon). For
example, in our view, one should nat speak of polyphyletic origin
of the order Pinnipedia on the basis of the fact that the different
families of Pinnipedia were perhaps derived, from the different
families of the order Carnivora. In the latter case we can talk
of only parallelism and not polyphyly. It is believed that a
clear demarcation of these concepts and final denial of "strict
monophyly" will help in bringing clarity to phylogenetic
researches.
325
N.N. VORONTSOV
4. Different levels of homology in different organs
of a united system
A substantial conclusion that can be drawn on the basis of
the study of the series of variability of different organs in the
rodent digestive system consists in establishing different levels
of homology in the different organs of a svstem.
Thus the homologous series of variability in the dental
system were observed only within the families (Cricetidae -
Cricetinae, Gerbillinae, Nesomyinae, Microtinae, Myospalaci-
nae; Muridae - Мигшае, Hydromyinae, Dendromyinae,
Cricetomyinae) and orders of allied families (Cricetidae and
Muridae) are parallel, but not homologous. In other words, the
structure of molar teeth of the forms of Muridae not yet des-
cribed should not be predicted on the basis of the study of the
order of Cricetidae.
As far as the stomach structure is concerned, the homo-
logous series of variability are observed within the subfamilies
(Muroidea - Cricetidae, Muridae, Spalacidae and Lophiomyidae).
In this case, after studying the series of variability of
stomachs of Cricetidae, the stomach structure of the forms of
Muridae that have not been studied in this connection, but the
stomach structure of Dipoideae, cannot be predicted.
Thus it may be expected that if Phillipinian Rhynchomys
and African Deomys actually feed on insects (like Oxymcterus
and Onychomys of Cricetinae), a major portion of their stomach
should be lined with corneous epithelium and the fundus glands
are locked within the glandular diverticulum.
The different levels of homology are, of course, connected
with the change in the control of genes over the characters in
evolution does not take place simultaneously. А portion of the
homologous genes remains; the homologous mutations also
remain. Besides, a portion of the genes, governing other
organs may be replaced, the mutations again occurring in them
will not be homologous to those in the ancestral group.
The establishment of different levels of homology while
studying homologous, parallel, and convergent variability may
substantially facilitate classification.
326
LITERATURE
Azimov, G.L, О. Ya. Krinitsyn and М.Е. Popov,
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