AMER. ZOOL., 17:335-342 (1977).
Skeletal Tissues in Sharks
MELVIN L. MOSS
Department of Anatomy, Columbia University, New York, New York 10032
SYNOPSIS Recent data on shark skeletal tissues have been reviewed. It is now reasonably
certain that shark teeth and denticles are covered with a true ectodermal enamel, although
the outer layer of these structures is structurally complex, consisting of both calcified
ectodermal enamel and uncalcified areas of ectomesenchymal origin. The intradermal
base of these structures most probably consists of acellular bone. The structural array of
apatite crystallites in the teeth seems strongly correlated with the specific shape and
function of individual teeth.
The calcified cartilage of sharks differs significantly from that of other vertebrates, not
only in its composition, but in the fact that the areas of calcification are composed of many
vital and non-hypertrophic cells. Recent studies of the mineralization processes of other
vertebrate tissues suggest a possible explanation for the classically described differential
patterns of calcification of shark cartilages, but the specific details in elasmobranchs are as
yet unknown, as indeed are many other aspects of their skeletal tissues whose future
investigation would surely be useful in the elucidation of the general processes of
vertebrate skeletal tissue mineralization.
INTRODUCTION
The general characteristics of skeletal
tissues in sharks are well known: a cartilaginous endoskeleton that is partially
calcified, a continuously succeeding intraoral dentition and a generalized distribution of dermal denticles (variously
termed placoid scales or odontodes). Both
the intraoral teeth and dermal denticles
(and their derivatives) consist of essentially
homologous tissues, composed chiefly of
dentin, covered with a harder outer layer
and attached to subepithelial tissues by
means of a basal calcified tissue.
There is consensual agreement about all
these statements, as well as the further
point that the cartilaginous endoskeleton
of recent and fossil elasmobranchs is derived from phylogenetically ancestral
forms possessed of osseous endoskeletal
tissues.
Beyond this, controversy exists about
several matters concerning the nature and
significance of several skeletal tissues in
sharks, both recent and fossil. This paper
This work was aided by the Plastic Surgery Research Fund, The Presbyterian Hospital, New York,
Dr. George F. Crikelair, Director, and by the Polly
Annenberg Levee Charitable Trust.
does not attempt a monographic review of
these topics, but rather a brief review of
the more recent data that suggest a resolution of several of these almost classical
problems as well as a delineation of areas
of fruitful further work. It is explicitly
stated that I am not an ichthyologist, but
rather one interested in the more general
attributes of calcified tissues and calcification processes. A recent excellent review of
this topic has been presented by a worker
well able to represent the ichthyological
viewpoint (Applegate, 1967).
THE ENAMEL PROBLEM
It is agreed that all vertebrate teeth form
as the result of homologous processes, the
mutually inductive interaction between an
overlying ectoderm and an underlying
core of neural crest derived (ectomesenchymal) tissues (Moss, 1969). These two
tissues typically form an essentially cone
shaped mass, with the ectomesenchymal
core enveloped by a doubled layer of ectoderm. The innermost of these epithelial
layers is called the inner enamel
epithelium and typically undergoes
cytodifferentiation from a low cuboidal
form to a tall columnar one coincident
335
336
MELVIN L. MOSS
with its role in the active production and
secretion of the organic matrix of the
enamel, the hard outermost covering of
the crowns of the teeth. The dentin is
formed by odontoblasts, differentiated
from the ectomesenchyme. In tetrapods
initial dentinogenesis always precedes
elaboration of the immediately external
enamel matrix (see Slavkin, 1974, for a
recent review and an advanced discussion).
The outer layer of both teleost and
elasmobranch teeth (and I consider them
homologous for the purposes of this discussion) is thin and structurally less uniform than that of tetrapod teeth. However, by light microscopy, the organic matrix of this outermost layer is formed first,
followed by the matrix of the subjacent
dentin, the reverse of the sequence in
tetrapods. Nevertheless, the inner enamel
epithelium undergoes cytodifferentiation
that appears homologous with that observed in teeth of tetrapods. These seemingly contradictory data understandably
led to two opposing views on the nature of
the outer layer of dental tissue.
On the basis of the seemingly constantly
centripetal deposition of organic matrix,
one group claimed that the first formed,
outermost layer was a product of the odontoblasts alone and, hence, was a variety of
dentin, variously termed durodentin,
mesodermal enamel, enameloid, among
other terms. The second group, primarily
but not exclusively on the basis of the
observations of undoubted cytodifferentiation of the inner enamel
epithelium claimed that the tissue was a
true ectodermal enamel. This subject has
been reviewed extensively (Applebaum,
1942; Applegate, 1967; Kemp and Park,
1974; Kerr, 1950; Moss, 1964, 1968a,
19686, 1969, 1970; Moss et al., 1964; 0rvig, 1967).
With respect to the structure of this
outer layer, I earlier suggested that it be
termed a "fibrous enamel," in an attempt
to define a tissue layer that contained obviously uncalcified, vertically oriented zones
interspersed as a minor component in a
calcified tissue.
The past few years have finally produced data, derived from the use of elec-
tron microscopy and autoradiography capable of resolving this problem and, as might
be expected, the thesis and antithesis are
synthesized in a way satisfactory to both
schools of thought in that both were partially correct. With these techniques it is
now unequivocal that the inner enamel
epithelial cells possess all of the typical
structural properties associated with structural protein production and transport,
and indeed are forming the organic matrix
of an ectodermal enamel (Herold, 1974),
which covers the coronal surfaces of the
teeth (Herold, 1975). Applegate (1967)
notes other supporting data. The structure
of the outer layer is now clear from the
elegant work of Kemp and Park (1974).
Their data show that the outer layer is
penetrated by vertically directed interdigitating strands of uncalcified tissues
undoubtedly ectomesenchymal (pulpal)
origin, while the "alternating" calcified
areas were of ectodermal origin. Hence, if
we consider only the calcified portions of
the outer layer alone, this tissue is ectodermal enamel, but if we consider the
outer capping layer as a whole, it is of a
mixed origin (Kemp and Park, 1974). This
finding supports the earlier data of Kerr,
1950, who felt that both ameloblasts and
odontoblasts jointly contributed to the
production of the enamel.
The most critical data are those of Andrevicci and Blumen (1971) and of Shellis
and Miles (1974). Studying teleost hshes,
the two groups of workers found that both
ameloblasts and odontoblasts contributed
to the organic matrix of the outer layer of
the teeth, findings clearly supportive of
and explicable within the context of those
of Kemp and Park, 1974. Parenthetically,
our earlier analysis of the proteins of this
outer layer, in which we claimed to find an
epithelial protein (Moss et al., 1964), have
been supported by the more recent work
of Shellis (1975).
In summary, it is now clear that the
outer layer of shark teeth does contain a
calcified component whose organic matrix
is derived from ameloblastic activity and
that this tissue component is a true ectodermal enamel. Further, considered as a
whole, the outer layer is a composite, also
337
SKELETAL TISSUES
containing variable amounts of uncalcified
tissues of mesodermal origin. It is no
longer possible to maintain that enamel
does not exist on teeth below the tetrapods
as, for example, does Bergot (1975) despite his explicit recognition of the protein
secretory types of cytodifferentiation of
the inner enamel epithelium.
Clearly established also is the claim that
enamel is an ancient vertebrate tissue, presumably equally as old as bone and dentin,
and calcified cartilage (although the latter
may indeed be even older, cf. infra.). We
now perceive that tetrapods did not create
enamel de novo but rather the ability to so
structurally array their odontoblasts and
ameloblasts as to reduce (but not eliminate) the structural intermixture of ectomesenchymal organic matrices in the
enamel layer.
FUNCTIONAL SIGNIFICANCE OF TOOTH STRUCTURE
It has been shown recently that the hydroxyapatite in the enamel of shark teeth
has a relatively high fluoride content (Ripa
et al, 1972; M0ller et al., 1975) and that
there is a well-defined pattern of crystallite
orientation (Ripar et al., 1972). These data
provide a conceptual substrate for the excellent work of Preuschaft et al. (1974) and
ofReif(1973).
It has long been recognized that it is
possible to classify shark teeth by their
external shape; some being conical, others
flat, with a spectrum of intermediate types
(see Schaeffer, 1967, for descriptions of
cladodont and hybodont teeth, and Applegate, 1967). Using instead a dichotomous division of (a) and (/3) teeth, Preuschaft et al. (1974) note that both groups of
teeth can occur in different locations of a
single jaw of a given species (see Applegate, 1976). However, (a) tooth crystallites
are arrayed to resist compressive loadings
while the Q3) tooth enamels are arrayed to
resist tension. Further, these microscopic
arrays are well correlated with the gross,
external morphology of the individual
tooth. It would appear that the introduction of biomechanical considerations and
of corresponding structural arrays of
enamel crystallites will be more useful in
the future for comprehension of shark
tooth functions than will purely descriptive
techniques.
Taxonomy is not a topic I feel qualified
to discuss authoritatively, but some comments may be helpful for those who are.
The data immediately preceding on
enamel crystallite array seemingly do not
lend themselves easily to be used as
taxonomic criteria in themselves. While it
was once felt that the histologic structure
of the dentin could be so used (Thomasset,
1928, 1930), more recently this claim has
been challenged by Radinsky (1969). It
would appear to me that the gross morphology, number and arrangement of the
teeth (cf. Grady, 1970), and other details of
their gross structure (vascular foramina,
etc.) could also serve usefully as taxonomic
criteria (see Casier, 1961, and this paper
for references to his other excellent papers).
Non-oral tooth-like structures, dermal
denticles, and their several derivatives
have been reviewed morphologically by
Applegate (1967), who noted also the relative value of these several structures for
taxonomic purposes. Little new information is available, and from the viewpoint of
calcification processes, these structures can
add nothing unique to the data and concepts presented above for the teeth.
BONE IN SHARKS
Despite the total absence of osseous tissues in the shark endoskeleton, bone does
exist in the base (or pedicle) of the teeth
and dermal denticles (see Moss, 1970).
This fact was noted by Miles (1971), and
earlier by Zangerl (1966) in fossil sharks,
while 0rvig(1951) cited earlier reports of a
"bone-like" tissue in the arculia of some
fossil selachians. The inability of others to
find osteocytes here (Applegate, 1967) is
accounted for by the transitory nature of
these cells in what is an acellular bone
tissue (Moss, 1970).
The fact that bone tissue is present in
recent, and fossil, sharks clearly indicates
that these "cartilaginous" fishes do not lack
osteogenetic ability on a total organismic
338
MELVIN L. MOSS
level, nor can the cartilaginous endoskeleton exist on the basis of an intrinsic
(genomic) inability of scleroblastic cells to
differentiate into functional osteoblasts
everywhere in the shark body. This being so,
we can consider that the selection between
chondro- and osteogenesis may possibly
reflect regional, epigenetic factors. To the
extent that this is so, I can perceive that the
shark may well serve as an excellent model
for future studies of the specific factors
related to modulation of skeletogenic cells.
CALCIFIED CARTILAGE
The topic of possible epigenetic regulation of specific types of skeletal tissues may
be pursued further with respect to the
endoskeleton. The phylogeny of sharks
has been well reviewed (0rvig, 1951;
Schaeffer, 1967; Miles, 1971). Although
0rvig (1951) claims an "affinity" between
Placoderms and Elasmobranchs, Schaeffer
(1967) feels that such a derivation is "less
secure . . .," while Miles (1971) states that
"the elasmobranch and holocephalan
lineages apparently diverged after the
basal elasmobranchiomorph stock separated into the placoderm and chondrichthyan lines of evolution." This is a critical
point since it is reasonable to believe that
the placoderm endoskeleton possessed, at
least, some perichondral bone (0rvig,
1951). If the elasmobranchs were derived
from placoderms, then their scleroblasts
lost the ability to form endoskeletal bone,
but not dermal bone (in association with
teeth).
However .this may be, Schaeffer (1967)
feels that it is "evident that the calcified
endoskeleton must have been inherited
from more primitive gnathostomes." Yet,
it seems that this ability of cartilage to
calcify was not necessarily a property of all
of the endoskeletal cartilage since "the
calcified centra may have been preceded
phylogenetically by uncalcified ones . . ."
(Schaeffer, 1967).
There is an argument, now classical,
concerning the significance of elasmobranch cartilage, some holding that its
presence indicates a neotenic process
(Romer, 1963), while other held for ver-
tebrate cartilage as phylogenetically (as
well as ontogenetically) preceding the appearance of bone (Denison, 1963; see
Moss, 1968a, 19686, for a review). In so far
as the fossil record permits, the latter view
seems correct, with respect to the endoskeleton.
In recent sharks, calcification of cartilage is found typically and extensively in
the vertebral column and in the jaws. In
the former, the calcifications are found
deep within the cartilaginous mass, while
in the latter site, the hydroxyapatite deposits characteristically form a continuous
series of subsurface plaques, which seem to
serve as points of attachment of uncalcified
perichondral collagen fiber bundles. It is
almost as if these calcified plaques served
as "staples."
On the basis of their shape, Applegate
(1967) terms the calcified areas of the jaw
cartilage (as well as the calcified areas of
the neural and hemal arches) "tesserae."
As that author acknowledges, this term has
another, more common significance in
paleontologic studies of fossil fish dermal
bone tissues. I must demur from Applegate's (1967) usage and urge that this term
remain restricted to its current usage to
avoid unnecessary confusion between
dermal skeleton and calcified cartilage.
One point of potentially great significance is noted in these areas of shark
calcification; they are composed of a
densely cellular cartilage whose cells appear both of "normal size" (in comparison
with those of the very sparsely cellular
non-calcified cartilage) and furthermore
these chondrocytes appear to be vital (see
also Halstead, 1974). Interestingly, Applegate (1967) presents some evidence to
suggest rapid turnover of the apatite in
these same areas. Any student of tetrapod
endochondral bone formation knows that
calcification of these latter cartilages is associated with both chondrocytic hypertrophy and death. Something radically different occurs in shark cartilage, making it
certain that there can be no unitary description of vertebrate cartilaginous calcification. This is an area of investigation
that surely will repay future study.
Turning next to the patterns of calcifica-
SKELETAL TISSUES
tion in the vertebral column, Schaeffer
(1967) notes that there has been a
phylogenetic replacement of a continuous
notochord by individual calcified centra. It
has long been noted that there are at least
three distinct patterns of calcifications observed in these cartilaginous vertebrae (see
Ridewood, 1921; Devillers, 1954; and Bertin, 1958, for an especially comprehensive
bibliography). While it has been usual to
claim that these calcification patterns have
taxonomic value, in some elasmobranchs
the type of calcification pattern is age dependent (cf. Devillers, 1954). To date no
explanation has been offered to suggest a
basis for these different patterns; again a
point of interest to students of vertebrate
skeletal tissues and worthy of further
study. It has been denied that these patterns of calcifications of vertebral centra
are of taxonomic value; and a current
classification of their patterns is nonphyletic (Applegate, 1967).
In addition to these problems related to
the gross pattern of calcifications, there are
those concerning the specific array of crystallites; globular, prismatic or "aveolar"
(cf. 0rvig, 1951, 1967). Applegate claims,
without further evidence, that the calcification of recent shark centra is "aveolar."
The globular type seems similar to that
observed in developing mammalian dentin
and 0rvig (op. cit.) held these to be related
to the formation of "calcospherites." This
might not be of such significance if it were
not for the claim that the globular array
represents a more primitive mode that has
evolved phylogenetically into the prismatic
(cf. 0rvig, 1951, 1967; Halstead, 1973,
1974; see also Denison, 1963; Hall, 1975;
Miles, 1971). While this concept has gained
some support, I remain troubled by the
matter. Careful reading of 0rvig (1951)
shows that he agrees that the globular
array represents Liesegang rings, and
further he agrees there that the globular
phase of calcification is but the first step in
the same process that leads to prismatic
calcification (as it does in recent mammalian dentins). In addition to the doubts I
expressed earlier concerning the possibility that geological factors might play a role
in the production of "globular" calcifica-
339
tion in fossilized (and possibly remineralized) cartilages, more recent data
on the nature of the processes associated
with the initial stages of mammalian
mineralization provide a possible solution
to this vexing matter.
The processes of skeletogenesis have
been well reviewed recently by Hall (1975).
With respect to the initiation of mineralization it seems clear now that the extracellular sites of initiation of calcium phosphate
salt deposition occur within membrane
bound "matrix vesicles," produced and
secreted by the scleroblastic cells; these
have been seen in mammalian intramembranous osteogenesis, in calcifying
cartilage and dentin (Anderson, 1973;
Slavkin, 1974), as well as in articular cartilage (Freeman, 1974). After the first nucleation, possibly of an amorphous calcium
phosphate, the membrane of the vesicle
breaks down and subsequent transformation into hydroxyapatite occurs. It has
been postulated that these sites serve as a
site of formation of spherulites of calcification (cf. Anderson, 1973). Subsequently,
and as these centers of calcification
coalesce and grow, the spherical array is
capable of transformation into a prismatic
pattern. Although beyond the scope of this
paper, the reader is invited to review the
more recent developments relating to calcification processes before ascribing definitive phylogenetic significance to any particular pattern of crystallite array in shark
calcified cartilage (see Wadkins et al.,
1974).
Sharks provide yet other problems relating to their calcified cartilages. Earlier
work noted that the serum calcium and
phosphorous concentrations of sharks approximate those of bony vertebrates
(Urist, 1961, 1964); yet, there is no detailed study of skeletal tissue physiology of
sharks, as there has been of other fishes
(Simmons, 1971). What is certain is that
the internal conditions of the body as a
whole of sharks, in relation to both bone
and calcified cartilage formation, differs
significantly from that of other recent vertebrates, although we do not understand
the meaning of these differences.
Moreover, the biochemical constitution of
340
MELVIN L. MOSS
shark cartilage differs in several ways from does not establish a fundamental alteration
that of tetrapods (Matthews, 1966; Matth- in the potential, intrinsic (genomic) ability
ews, 1972), but as yet the significance of of the elasmobranch scleroblasts to modthese differences in terms of the site, type ulate into osteoblasts.
and cellularity of calcified cartilage in the
In the case of invertebrate cartilages
sharks is unknown.
which normally never calcify, appropriate
The role of the teeth, denticles and (in vitro) alterations of environmental (excalcified cartilage in the mineral trinsic) conditions will permit such calmetabolism of the shark is as yet not cifications to occur (Eilberg etal., 1975a, b).
known in detail. We noted earlier that the An increasing body of data has permitted
quantity of mineral salts in calcified shark the recent postulation of a newer view of
cartilage was essentially equivalent to that the potential regulatory roles of extracellufound in vertebrate bone (Moss, 1965). It lar epigenetic factors in skeletogenic dehas been suggested that both resorbed velopmental processes (L0vtrup, 1974;
denticles as well as the calcified areas of Slavkin et al., 1975). In this context, it is
cartilage might play a role in mineral possible to suggest that some combination
homeostasis in sharks (Applegate, 1967). I, of the specific biochemical (biophysical)
however, will suggest, subject to correction factors in the shark cartilage per se, or in
when definitive data are presented in the the perichondral tissues, is epigenetically
future, that the shark, like the teleosts, capable of regulating the shark scleroblasts
does not normally utilize his skeletal tissues to inhibit an osteoblastic differentiation,
for this role, but rather the environmental which these same cells are still potentially
waters he lives in (Moss, 1965). The func- capable of undergoing. Surely the prestions related to protection, digestion, and ence of bone in the dermal skeleton
biomechanics remain for the same skeletal suggests that this is not a matter regulated
by such organismic factors as serum contissues to fulfill.
centrations of mineral ions, hormones, etc.
Again, the shark gives promise of being
SOME PHVLOGENETIC CONSIDERATIONS
the animal of choice in future studies of
The nature of shark skeletal tissues these intriguing questions whose resoluposes some interesting phylogenetic ques- tions have implications beyond the sharks
tions. As noted above, the chondral state of alone.
the elasmobranch endoskeleton was once
believed to "prove" that cartilage preceded
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