<oo/ogica/ Journal of the Ltnnean Soczely ( 1 989), 95: 3 I 1-334. With 1 I figures
Enamel ultrastructure and masticatory
function in molars of the American opossum,
Didelphis virginiana
DORIS STERN* AND A. W. CROMPTON
Department of Biology, Harvard University, Cambridge, M A 02138, U.S.A.
AND
ZIEDONIS SKOBE
Forsyth Dental Center, Boston, M A 02115, U.S.A.
Received December 1987, accepted for publication May 1988
Maxillary and mandibular molars of the American opossum, Didelphis u i r p i a n a L., werc viewed in
the scanning electron microscope (SEM) after acid-etching or after cutting and acid-rtching.
Observations were made on enamel prism patterns as they relate to functional properties of the tooth
at a particular site. Molars at different stages of wear were also observed under a dissecting
microscope; worn surfaces were correlated with function and enamel ultrastructure. Pounding
surfaces of molar cusps wear more rapidly than near-vertical shearing surfaces or crushing basins (i.e.
the trigon and talonid basin). Pounding surfaces are subjected to abrasion by food and arc not
normally involved in tooth-tooth contact. Near-vertical shearing surfaces and basins used for crushing
do experience tooth-tooth contact, but are surprisingly more resistant to wear. Prisms at pounding
sites approach the occlusal surface at a near 90' angle and are surrounded with very thick
interprismatic ( I P ) enamel parallel to the occlusal surface of the tooth. T h e pounding pattern is
prescnt at tips of cusps and at occlusal surfaces of ridges of the tooth. At near-vertical shearing
surfaces, the prisms approach the outer surface obliquely and are surrounded with I P crystals which
are perpendicular to the vertical surface. T h e angle between prismatic and I P enamel in these
patterns is 60-90" in a cervical to occlusal direction. I n basins of the tooth used principally for
crushing and some shearing, IP enamel is perpendicular to the changing slope of the basin and the
prisms are usually at a 55-65" angle to the I P enamel. When the pounding and shearing-crushing
patterns meet a t a ridge, a distinct seam is observed. Pounding forces occur parallel to the long axis of
the prisms and perpendicular to the thick I P enamel (i.e. perpendicular to the long axis of the IP
crystals) lying on either side of the prisms. Shearing and crushing forces occur at a n oblique angle to
the prism, and interprismatic enamel is more evenly distributed about the prism. A spiral pattern is
found at the bottoms of the trigon and talonid basins, but not at the bottom of the trigonid which is a
non-occluding basin. I t is concluded that the differential rates of wear of the enamel surfaces are
necessary in maintaining the sharp cutting edges and effective crushing basins of the tribosphenic
molar, and the ultrastructural arrangements of the enamel prisms are of functional significance.
KEY WORDS:---Opossum
molars prisms.
-
enamel
structure
function
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wear
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mastication - tribosphenic
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*Present address: Forsyth Dental Center, 40 T h e Fenway, Boston, MA 021 15.
002+4082/89/040311+ 24 S03.00/0
31 1
01989 T h e Linnean
Society of London
CONTEN'I'S
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Ultrastructural fraturrs of enamel .
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Stages of mastication ,
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Functions of the molars
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Material and mcthods .
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IJncut surfaces
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Slices arid cubes .
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Mapping of sites .
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Tooth wrar .
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'1'tiic.knrss measurements .
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P I P angles a n d angle of prisms to surface . .
Krsults
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F,ffi.cts 01. wcar
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Enamel ultrastructure .
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Enamrl thickness .
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Alignment and arrangement of prisms .
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Discussion .
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1)ilierential wcar .
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Enamel ultrastructure and wcar .
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Aprismatir enamel
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Enamel thickness .
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Drntinal peaks
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Angle of prisnis t o interprismatic enamel ,
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Solution to a problcm, and its c o t ~ s c q ~ ~ c ~ i c,c s
Conclusions .
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Acknowlcdgcnients
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Abbre\.iations used i n trxt and figures .
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I ntroduc.tion
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I N I RODUC I ION
Except for studies by von Koenigswald (1982) on enamel structure in the
molars of arvicolid rodents and one by Rensberger & van Koenigswald (1980) in
rhinoceroses, previous studies have not correlated enamel prism patterns to
functional aspects of the teeth. In his study of the Arvicolidae, von Koenigswald
( 1982) concluded that the distribution of enamel patterns, and enamel thickness,
were related to the mechanical eficiency of the molars. Prisms of leading and
trailing edges of enamel were arranged so that a masticatory stress pattern was
rellected. The lamellar arrangement of decussating prisms appeared in areas
where most resistance to stress was needed, and the radial pattern of parallel
prisms appeared at the outer surfaces of sharp cutting edges. Rensberger & von
Kaenigswald ( 1980) i n their study of rhinoceros enamel structure correlated the
vertical orientation of decussating groups of prisms (Hunter-Schrcger bands) to
the evolution of hypsodonty. They showed experimentally that the modified
arrangement of prisms was more resistant to wear, and appeared at sites of the
tooth where occlusal pressures were greatest. Both studies focussed on herbivorous
dentitions with highly derived enamel patterns.
The opossum is a n omnivorous marsupial with tribosphenic molars that have
changed little from those of the earliest therians from the lower Cretaceous
(Kermack, Lees & Mussett, 1965; Clemens, 1971; Crompton & KielanJaworowska, 1978). This type of molar, in sharp contrast to pre-tribosphenic
molars of earlier mammals, is characterized by the ability to shear, crush, and
pound (see Function3 qf the molars, below). Since diverse molar patterns of modern
mammals are all derived from the basic tribosphenic pattern (Crompton &
OPOSSUM ENAMEL
313
Hiiemae, 1969; Butler, 1972), it is essential to determine the organization and
structure-function correlates of enamel in a living mammal that has retained the
tribosphenic pat tern.
The purpose ofthe present study is to describe, in the American opossum, the
arrangement and structure-function relationships of enamel prisms at sites of the
molars where the functions differ.
Ullrastructural f e a Lures o f enamel
The enamel of Dzdelflhis is prismatic (Tomes, 1897, 1906; Boyde & Lester, 1967)
as is all mammalian enamel (see Boyde, 1964 for a comparative study), with the
rxception of some of the Cetaceans (Ishiyama, 1984). T h e following facts about
mammalian enamel are generally agreed upon (reviewed by Osborn, 198 1 ) .
Enamel prisms are composed of hydroxyapatite crystallites which are more or less
parallel to each other. Crystallites of prisms differ in orientation from those of
interprismatic enamel, often by as much as 90". A space, or prism sheath, either
partially or completely surrounds the enamel prism where there is an abrupt
change in orientation of crystallites. Near the dentin-enamel junction (DEJ), a
small amount (0.5-5 p m ) of aprismatic or structureless enamel is laid down
during development before prismatic enamel is formed. After the prismatic layer,
enamel which is nearly or completely structureless is deposited near the outer
surface of the tooth (Gwinnett, 1966, 1967; Bhaskar, 1987). T h e prismless enamel
is deposited when the ameloblast is either forming its Tomes' process at the
beginning of enamel secretion, or just retracting the Tomes' process during the
maturation phase of amelogenesis.
The prisms of the enamel in the opossum do not decussate relative to one
another (Tomes, 1898, 1906; Boyde, 1964), i.e. they d o not form Hunter-Schreger
bands where groups of prisms are tilted relative to a neighbouring group as in
more advanced mammals (herbivores: Fortelius, 1984; Boyde & Fortelius, 1986;
human: Stern & Skobe, 1985; cat and dog: Skobe, Prostak & 'lrombly, 1985;
primates: Lavelle, Shellis & Poole, 1977), or a uniserial type of enamel where one
row of prisms is tilted 90" relative to a neighbouring row (rodents: Boyde, 1964,
1978; von Koenigswald, 1982). The primitive type of parallel prismatic enamel is
found in all marsupials except the wombat (Tomes, 1906), and in the following
placental mammals: bats (Friant, 1964; Lester & Hand, 1987), and some
primitive insectivores (moles, shrews, hedgehogs), rodents Cjerboas), primates
(lemurs) (Boyde, 1964), and hyraxes (Carter, 1920), but the structure-function
relationship of this simple type of prism organization has not been addressed.
&ages o f mastication
The first stage of the mastication of resistant foods is puncture-crushing; this
stage involves tooth-food-tooth contact (Crompton & Hiiemae, 1970), and the
predominant movement of the active side of the mandible is vertical or orthal
(Hiiemae, 1978). During the puncture-crushing stage, the food is punctured as
long as the cusp tips are relatively sharp; when the cusps are blunted, the
principal action of the cusps is one of fracturing or softening the food. During the
second stage (shearing-crushing), shearing occurs at the near-vertical surfaces of
the cusps and ridges and always involves tooth-tooth contact as the surfaces slide
314
D. S T E R N E T A L
by each other. Crushing occurs in the trigon and talonid basins (Crompton &
Hiiemae, 1970), and initially involves tooth-food-tooth contact. Food is
compressed and triturated into smaller pieces, and tooth-tooth contact occurs
when full occlusion is reached (Crompton & Hiiemae, 1969, 1970; Hiiemae,
1978).
Functions of Ihe molars
The actions during food reduction have been generally defined in terms of
tooth morphology, the direction of tooth movement, occlusal pressure during
tooth-food or tooth-tooth contact and the effects on food (Rensberger, 1973; Kay
& Hiiemae, 1974; Rosenberger & Kinzey, 1976). In Didelphis, the masticatory
functions are defined by us as follows:
1. Puncturing-involves tips of cusps and food contact. This action results in
size reduction of hard food particles and occurs during the first stage of
mastication (Crompton & Hiiemae, 1970; Hiiemae, 1978; Oron & Crompton,
1985). Occlusal pressure is high because the area of tooth-food contact is small
(Rensberger, 1973).
2. Pounding-involves blunter surfaces such as horizontal surfaces of ridges and
food, or well-worn cusps and food. Pounding occurs at both stages of mastication,
since holding or grasping of food by the horizontal surfaces of teeth during
shearing (Crompton & Sita-Lumsden, 1970; Osborn & Lumsden, 1978) can be
considered a gentle form of pounding. Occlusal force per unit area is likely lower
than in puncturing because the area of tooth-food contact is greater.
3. Shearing-occurs as near-vertical surfaces of the teeth slide by each other.
Horizontal surfaces grasp and hold the food as two points on apposing crescentic
surfaces move toward each other (Crompton & Sita-Lumsden, 1970); necessarily
involves tooth-tooth contact, and the reduction of food particles. Occlusal
pressure is high as the leading edges of the shearing surfaces narrowly miss each
other (Rensberger, 1973).
4. Crushing-involves a cusp occluding in a basin, with the result that food is
compressed. The term shearing-crushing is used to describe a combined action:
shearing as the edge of a cusp (i.e. the protocone or hypoconid) slides down the
edge of the occluding basin, followed by crushing as the cusp contacts the bottom
of the basin. Occlusal pressure per unit area is low in the basin because the area of
contact between the tooth surfaces is large (Rensberger, 1973).
MATERIAL AND MF,'I'HOIX
Uncut surfaces
Five maxillary and four mandibular molars extracted from dried or formalinfixed specimens (a total offour different specimens), were soaked for two hours in
a 2.504, sodium hypochlorite solution. After rinsing, the teeth were etched in loo/,
perchloric acid for 15 seconds, rinsed, dried, sputter-coated with 20 nm palladium
gold, and photographed in a JEOL-SMU3 scanning electron microscope. In
addition, three jaw quadrants were treated as above and surveyed to determine
the consistency of enamel patterns, but not photographed.
Two teeth each were soaked overnight in 2.5% NaOCl or soaked in I N K O H
OPOSSUM E N A M E L
315
in 50°, ethanol to observe the effect, ifany, on the organic material in the enamel.
'lhese molars were then acid-etched and processed, as above.
Slices and cubes
Two lower molars were cut longitudinally with a Buehler Isomet saw equipped
with a diamond blade, polished with 400 and then 600 grit sandpaper, and etched
as above before viewing in SEM. Five samples were cut into 100 p m sections, four
i n a mesial-distal and one in a buccal-lingual direction. Blocks were cut from the
l00ym sections with a razor blade near the protoconid and from the talonid
basin, so that the enamel could be viewed from several directions. The small
blocks were not polished but were dipped quickly four times in 10% perchloric
acid and rinsed before being mounted on aluminium stubs.
Mapping o f site;,
Drawings were made of whole or cut molars and letters were assigned to areas
so that high magnification micrographs could be correlated to the gross
morphology of the teeth. Some montages were made at low magnification (SEM)
for the same purpose of carefully mapping the sites.
Tooth wear
Molars at different stages of wear, from 12 skulls of Didelphis-virginiana, were
observed under a dissecting microscope. Drawings of occlusal views of three
maxillas and three mandibles were made through the use of a camera lucida;
regions of worn enamel were noted. Patterns of enamel ultrastructure were
correlated with jaw movement (as determined by Crompton & Hiiemae, 1970)
and tooth wear.
Thickness measurements
From a total of 250 SEM micrographs, enamel thickness was measured
whenever the entire thickness was included in the photograph (about 30 of the
250). The thickness was measured as a perpendicular line from the DEJ to the
outer enamel surface. All measurements were corrected for magnifications, but
could not be corrected for attrition since this study did not include baseline
measurements of unworn molars.
P: IP angles and angle of prisms to surface
The angle of prism (P) to interprismatic (IP) enamel was taken as the acute
angle between them, Twenty-eight measurements were made from longitudinal
sections at various sites of the molars. The angle of the prism to a functional
surface was taken as the acute angle between the prism and a line drawn parallel
to the functional surface. These angles were measured (with a protractor) from
longitudinal sections in 26 micrographs; they must be taken as rough
measurements since no attempt was made to standardize the angle of P and IP to
the cut surface.
D. SI'ERN B'T A L
316
B
L
'RIOR
AN1
Figure 1. A, Diagram oftwo upper right molars and one lower left molar of Didelphis uirginiana. 'I'ips of
cusps are marked with circles, vertical shearing surfaces are portrayed with hatchrd patterns, and
shearing aspects of shearing-crushing sites (basin areas) have a stippled design. Pounding occurs a1
tips of rusps and along the ridges represented by dense black lines on thr ncrlusal surfaces. Crushing
occurs i n the centre of the trigon and talonid basins, and is encircled in this diagram. See Kesults, first
paragraph. (Modified from Crompwn (Ir Hiiemae, 1970; Crompton, 1971; and Bown & Kraus,
1979.) B, Diagram of occlusal view of two upper right molars and two lower left molars with worn
surfaces shaded in. Krlative positions have been shifted from the natural occlusal alignment. T h e
wear shown on the four teeth was observed in onc specimen; third molars display a moderate amount
of wear arid second molars are well-worn. Vertical surfaces of teeth used for shearing, and basins used
for shearing-crushing are tlic least worn sites.
RESULTS
A diagram of two left upper molars and a right lower molar is shown in Fig. 1 A
with functional surfaces shaded in. By superimposing the maxillary arid
mandibular molars so that the numbers match, occluding surfaces can be
visualized (Crompton & Hiiemae, 1969; Crompton, 1971; Bown & Kraus, 1979).
T h e remainder of the crown does not occlude with another tooth and serves a
pounding function. A seam, which separates two different patterns of the molars,
runs along the rims of the three basins (trigon, trigonid and talonid) and also
along the occlusal surfaces of the metacrista and the ridge joining the stylar cusps
of the upper molars.
OPOSSUM ENAMEL
317
Efects of wear
Moderately and well-worn molars are shown in Fig. 1B. Tips of cusps are worn
flat by tooth-food abrasion, but sharp edges to the shearing surfaces are retained
and the talonid and trigon basins show little wear despite tooth-tooth contact.
Wear appears first at the tips of cusps (e.g. paraconid-top of micrograph, Fig. 2A;
entoconid-Fig. 2B) and then spreads along the seams, such as the one that goes
around the talonid basin (see posterior portions of two lower molars in Fig. 1B).
The upper molars begin showing wear at horizontal aspects of the two main
shearing surfaces along the paracrista and the metacrista. Cusp "c" on the stylar
ridge (Fig. 1A) begins to wear before the stylocone; cusps of the trigonid wear very
rapidly. Basins in which cusps occlude (right side of Fig. 2B) show little wear a t a
gross level except at the rims, but the non-occluding basin of the trigonid wears
rapidly from the tips of the three cusps downward and eventually becomes
obliterated.
Enamel ultrastructure
Different enamel patterns are encountered on surfaces with different functions.
Pounding pattern
Patterns at puncturing and pounding surfaces are similar.
Puncturing occurs at tips of cusps when they are still relatively sharp. At these
sites, prisms approach the occlusal surface of the tooth at a near 90" and are
surrounded by thick interprismatic (IP) enamel (Fig. 2C, D) which is parallel to
the occlusal surface of the tooth. If a worn cusp is viewed occlusally, the following
is seen: the I P enamel is especially thick on two sides of the prism, but not as
prominent on the edges of the prism which are closer to and farther from the
dentin-enamel junction (DEJ), i.e. the tapered edges of the oval as seen in crosssection of the prisms. Prisms closest to the DEJ often appear circular (arrow,
Fig. 2C) instead of oval in transverse section, and are surrounded on all four sides
by thick IP enamel.
Pounding occurs at tips of blunted cusps such as the entoconid (Fig. 2B, E)
where a broad, flat expanse of enamel is found on both sides of the seam after a
substantial amount of wear. Pounding also occurs at horizontal surfaces of ridges
such as that distal to the metaconid (Fig. 2F) and the ridge mesial to the
entoconid (Fig. 3A). At areas of thick enamel, the prisms tilt slightly more than
90" relative to the horizontal surface of the tooth (left side of Fig. 2E, top of
Fig. 2F, and left side of Fig. 3A), especially further from the dentin in a lateral or
mtward direction. The ridges shown in Figs2F and 3A juxtapose shearing
surfaces 5 and 6, respectively (Fig. 1A). Figure 2E is a high magnification of the
worn area of the entoconid (Fig. 2B) where the dentin is just showing through at
the tapered (top) edge. The fact that dentin is standing proud of the enamel is an
:ffect of the acid etchant, which preferentially removes the enamel crystals and
lot the dentin crystals which are more protected by organic material in the dentin
matrix. Before etching, the dentin was exposed at the worn surfaces, but not
jtanding higher than the enamel. Spikes of dentin, an unusual feature of exposed
jentin, are aligned at the surface where the enamel has begun to wear off. Notice
he different patterns on each side of the spikes or seam in Fig. 2E; on the left side
Figure 2. A, Occlusal view of paraconid (cusp) and the paracristid (ridge) displaying a moderate
amount ofwear (dentin is black in micrograph). Outer area ofrusp (top ofmicrograph) shows thicker
enamel of a pounding surface. The ridge of the rusp displays wear at its horizontal aspect due to a
pounding artion and the outer edge or slope of thr ridgr (arrow) shows attrition due to thr shearing (if
the paracristid of the lower molar against the metacrista of the upper molar. Scale bar =500 pm.
B, Occlusal view of entoconid which has been worn flat d u e to a pounding actiori. T h e dark area is
dentin. Numbers refer to figures which arc higher magnifirations ofthose sites. 'I'he entoconid bordrrs
shearing surface 6 (Fig. I , lower molar). T h e talonid basin ('I'B) is seen i n thr right side of the
micrograph; some shearing artion ocrurs at the edge of the right (buccal) sidc of the cusp. p = prism.
Srale bar=500pm. C, T h e pounding pattern on the buccal side of the entoconid (see Fig. 2B) in
occlusal view. Notice the thirk interprismatic (IP) enamel, rrystallitcs of which are oriented parallel
to the occlusal surlice. Arrow points to rirrular prism near the DEJ surrounded by I P mamel. Srale
bat-= 5.0 pm. D, T h e pounding pattrrn from the buccal side of the entoconid (see Pig. 28) at a higher
magnification. Arrow points to round prism close to the DEJ which is surrounded on all sides with IP
enamel. d =dentin. Scalc b a r = 10 p i . E, Worn surfacc of thc mcsial sidc of the entoconid (see
Fig. 28). The modified pounding pattern is towards the left in tht- micrograph, and the shedringcrushing pattern is towards the right. Notice the dentinal peaks (arrows) where thr two patterns meet.
Holes within some of the prisms are tubular arras. Scale bar= 10 pm. F, Distal tip of the metacmnid of
a lower right molar. T h e pounding pattrrn (top) and the shearing pattern (bottom) come togcthcr to
h r m a scani. d = dentin. Scale bar = 25 pm.
OPOSSUM ENAMEL
319
Figure 3. A, Orclusal view of enamc.1 just mesial to the entoconid. A seam is visible where the
pounding p a t m n (left) and the shearing-crushing pattern (right) come together. T h e seam probably
widens during drying of the tooth, but does represent a disrontinuity or abrupt change of enamel
patterns. Scale bar = 50 pm. B, High magnification of the distal slope of the entoconid. Notice the
tubule (arrow) projecting from the centre o f a prism. T h e function at this particular site is pounding.
i p = interprismatic enamel, p = prism. Scale bar = 5 pm. C, Posterior, and obliquely occlusal, view of
the anterior cingulum of an upper right third molar (see Fig. 4).T h e pounding pattern is obvious on
the occlusal surface of the cingulum; the vertical-shearing pattern is at the lower portion of the
micrograph, even though this is not a functional shearing surface. Notice the sharp edge (arrow)
formed as the pounding surfaw is abraded. d = dentin. Scale bar = 50 pm. D, Antero-occlusal view of
the area of the cingulum where two upper molars contact each other (black arrow). T h e pounding
pattern at the occlusal surfarc is twisted slightly in a buccal-lingual direction. T h e pattern on the
vertical surface appears similar to a pounding pattern, exrept the I P crystallites (arrowhead) are
perpendicular to the vertical surface. d = dentin. Scale bar = 20 pm.
is the pounding pattern with thick IP enamel aligned parallel to the occlusal
surface, and on the right side is a modified pounding pattern where the prisms are
more tilted relative to the occlusal surface. Seams are also visible in Figs 2F and
3A. A high magnification of the pounding surface is seen in Fig. 3B. T h e prisms
are oblique to the occlusal surface, but the I P enamel is parallel to the surface.
Enamel tubules, usually a feature of primitive enamel 0.Tomes, 1849; Boyde,
1964), are seen in this micrograph; one of the tubules is projecting from the centre
of a prism. (The visibility of enamel tubules did not seem to depend on the length
of time the tooth was soaked in NaOCl, or whether or not the tooth was treated
with 1N KOH in 50% ethanol.) T h e horizontal plane of a shearing surface
(anterior part ofshearing surface 1 , Fig. 1) is also seen in Figs 3C and 3D; both are
part of the anterior cingulum of the upper molar. T h e diagram in Fig. 4 shows
where on the upper molar these areas are taken. Pounding patterns are obvious
on horizontal surfaces of both areas and the shearing pattern is exposed at the
bottom of Fig. 3C as the result of abrasion by food. A sharp edge (arrow, Fig. 3C)
D. SI'EKN E 7 At.
320
occlusol
I.'igurc 4.Drawing to illustrate orientation ol'aIras of'thc anterior cingulum shown in Fig. 3C,
n).
is formed as the pounding and shearing surfaces wear. An especially worn area of
the mesial side of the paraconid, the paracristid, is shown in Fig. 5A (see low
magnification, Fig. 2A); a combined pounding/shearing pattern is seen at the
occlusal surface as some of the vertical and horizontal planes of that slope are
worn away, but not at a differential rate necessary to maintain a sharp edge.
Shelearing pallern
In order to determine the prismatic and interprismatic arrangement of a nearvertical shearing surface, small blocks were cut from a 100 pm mesial-distal
section of a molar and the individual surfaces were inspected. One of these blocks,
cut from near the top of the protoconid (mesial aspect), is seen in Fig. 5B. The
arrow (Fig. 5B) denotes an area of outer enamel that is relatively free of prisms.
'I'he vertical shearing surface (vs) of that block appears to be made up of round
profiles which are actually not prisms, but are territories of aprismatic enamel; as
shown at a higher magnification in Fig. 5C, small portions of prisms 'peak'
through the abundant aprismatic crystals. Since the outer (mesial, distal, buccal,
or lingual) edges of the molars generally are composed of thick enamel (Fig. 5D)
and a thick layer ofaprismatic enamel (or poorly defined prisms) appears at the
outer surface, the vertical shearing edge often appears 'barnacle-like' as in
Fig. 5C. The pounding pattern is seen towards the right of the micrograph in
Fig. 5R; that face of the block is parallel to and just under the pounding surface of
the cusp. A summary diagram to illustrate the orientation of prisms and
interprismatic enamel of pounding and shearing surfaces, such as those of the
metacrista arid paracristid (surface 2, Fig. IA), is seen in Fig. 6. Prisms approach
the shearing surface obliquely and the pounding surface perpendicularly;
OPOSSUM ENAMEL
32 1
Figure 5. A, Occlusal view of the paracristid, one of the main shearing surfaces of the lower molar
(Fig. 1A). Notice the pounding pattern near the dentin. Arrows point to vertical-shearing pattern at
the worn edge of the ridge. Scale bar= 30 pm. B, Block of enamel cut from the mesial side of the
protoconid. The pounding pattern is at the right in the micrograph, and is on a cut surface which is
parallel to and just under the occlusal surface. Notice the ‘barnacle-like’ appearance of the verticalshearing surface (vs). Arrow points to the aprismatic layer (or one of poorly-defined prisms).
pdzpounding pattern. Scalr bar= 50 p n , C, Higher magnification of the vertical shcaring surface
seen in Fig. 5B. ‘Barnacle-like’appearance is due to aprismatic (AP) layer ofcrystallites. Some prisms
(arrows] are pecking through the AP layer. Notice the round profilcs which probably denotr the area
occupied by one ameloblast. Scale bar = 20 pm. D, Posterior side of the tooth, behind the talonid
basin, taken from a 100pm section of a lower right molar. Notice the undulating path of the prisms
from the DEJ; arrows point to slight changes in path of one prism. I P enamel is abundant and
perpendicular to the outer vertical surface. Incremental growth lines (arrowhead) are easily visible in
the area of poorly-defined prisms (pdp). d=dentin. Scale bar= 50 pm.
interprismatic crystallites are parallel to the pounding surface and perpendicular
t o the shearing surface.
Shearing-crushing pattern
This enamel pattern is characterized by prisms that tilt relative to the occlusal
surface (Fig. 7A,far right side, and Fig. 7B) and, at the base of the trigon (Fig. 7B)
and talonid basin (Fig. 7C),form a spiral. The talonid spiral is not as tight as that
in the trigon. T h e interprismatic enamel crystallites change orientation to remain
more perpendicular to the concave or convex surfaces of the basins, and are not
oriented parallel to the horizontal plane of the tooth as in the pounding pattern.
A block was cut from the base of the talonid basin, and is shown from the
occlusal surface (Fig. 7C) and four cut sides (Fig. 7D-G).T h e width (mesial side)
of the rectangle (Fig. 7D) exhibits a radial arrangement (as seen by von
OPOSSUM ENAMEL
Figure 7. A, Occlusal view of buccal side of entoconid. l'his is a lower magnification, but same area
from which Fig. ?C, L) are takcn. Notice the pounding pattern (arrow) near the dentin which changes
to a modified pounding pattern (double arrows) closer to the talonid basin, and to the shearingcrushing pattern as the surfacc slopes into thc basin (far right). (See shearing surfarr 6, lower molar,
Fig. 1A.) Scale b a r 5 2 0 pm. B, Spiral near base of trigori in uppcr right first molar. '1 his pattern is
similar to a shearing pattern in that prisms are at an angle to the surface and tilt occlusally, and I P
enamel is not very prominent after acid-etching. The spiral arrangement is unique to the trigon and
talonid basin. Scale b a r = 30 pm. C, Ocrlusal virw of enamel block taken from talonid basin. Notice
thr spiral which is not as tight as that sccn i n Fig. 7R. d = dcntin. Scale b a r = 30 pm. D, O n e of the r u t
edges of the block (Fig. 7C) cxhihiting a radial arrangement of prisms which is diffcrcnt from the
pounding pattern (see Results). d = dentin, oc = orrlusal. Scale bar = 30 pm. E, Long and short r u t
edges of the block shown in Fig. 7C. T h r short side exhibits the tangential arrangement as described
by von Koenigswald (1982); see Results section. Scale h a r =3 0 p r n . F, Drawing of the same cube
sh(iwing the radial ( r ) and tangential ( t ) arrangement orprisms (white, i n small squares) and IP (dots
or dashes) enamel. G , 'l'he long cut side of the block near thc spiral (Fig. 7C, upper left quadrant of
photograph). A combination of radial arid tangential prism patterns are observed. d = dentin,
r = radial, t = tangcntial (see Fig. 7F). Scale bar = 50 pm.
323
324
D. STERN E T AL.
Figure 8 A, High magnification of the shearing-crushing pattern from the mesial side of the talonid
basin. Arrow shows direction or prism crystallites, and circles denote IP crystallites almost
perpendicular to the surface. Scale bar=tipm. B, Area of talonid basin which is not as warn as in
Fig. 8A. Notice the ‘barnacle-like’ effect of AP crystallites. Crystallites of prisms ‘peeking’ through
(arrows) are oriented at various angles. a p = aprismatic enamel. Scale bar= 10pm.
Transitional patterns
The modified pounding pattern has features of both the pounding and shearing
patterns, and is seen when the enamel is worn tangentially (arrow, Fig. 5A) or is
leading into a basin (double arrows, Fig. 7A) to become a shearing-crushing
pattern. Near the worn, exposed dentin of the entoconid (Fig. 7A), the pounding
pattern is present on the basin side of the seam but farther from the dentin, it
becomes a modified pounding pattern where the prisms are at a greater angle to
the surface and IP enamel remains abundant (double arrows).
From the descriptions of enamel patterns listed above, it is clear that the
orientation of prisms and IP enamel is not constant relative to the surface of the
dentin. The functional patterns are shown in diagrammatic form in Fig. 9 as they
relate to the gross morphology of the tooth. The blocks shown in Figs5B and
7C-G can be related to this diagram.
Enamel thickness
As one would expect, thick enamel occurs at the main shearing surfaces.
Enamel within the trigon, trigonid and talonid basin, is generally thinner (nine
measurements, 20-150 pm, average =64 pm) than enamel at an outer (mesial,
distal, buccal, or lingual) surface of the tooth (23 measurements, 140-250 pm,
OPOSSUM ENAMEL
325
---
POSTERO-LINGUAL VIEW
OF PROTOCONID
Figure 9. Drawing showing the three enamel prism patterns; the cusp is drawn as if a long section of
enamel were removed (boxed inset). T h e pounding pattern is seen at the occlusal (horizontal) surface
of the cusp. The right sidc shows thc path of the prisms toward the vertical shearing (vs) surface, and
the left side shows the path of the prisms toward the surface of the trigonid. T h e cube from the talonid
basin displays the spiral of the shearing-crushing pattern.
average = 163 pm). The thinner areas of enamel correspond to the stippled
patterns in Fig. 1A with the exceptions of the sides of the protocristid and the
entoconid, and near the cusps of the paracone and metacone. Notice that on the
20 pm thick dorsal ledge of the trigonid (Fig. lOA), the prisms near the DEJ are
completely surrounded with IP enamel as they are in the right and left sides of
Fig. 2E. In Fig. 5D, the thickness of the enamel posterior to the talonid basin
(shearing surface 4,Fig. 1A) is about 250 pm thick. T h e trigonid (Fig. 10A) is a
non-occluding basin and the enamel pattern differs somewhat from that found in
the trigon (Fig. 7B); a spiral is not seen, and I P enamel is not as perpendicular to
the surface of the basin, since it does not appear to etch away to the same extent as
I P enamel in the trigon (Fig. 7B) and talonid basin (Fig. 7C).
A ~ i g n m e nand
~ arrangement of prisms
In practically all areas of the molars, prisms of the enamel are parallel to each
other (Figs 2C, D, 5D, 7A) except at a very steep slope on the buccal side of the
entoconid (Fig. 10B; see Fig. 2B for low magnification). O n this slope, a pattern
reminiscent of Hunter-Schreger bands of more evolutionarily advanced enamel is
Figure 10. h,'l'rigonid basin (towards the bottom of micrograph) of thc lower molar. R'Gtice thc
dorsal ledgr (arrows) ofenamel with prisms surrounded by IP enamel. 11' enamel is morr obvious in
this pattcrn, which iiccurs i n a non-orrluding surfacr. Srdlr bar= 20 pin. B, B u i ~ a side
l
idr n ~ w i i n i d
(see Fig. 213) leading into talonid basin. Appearance ofbands is due to the undulating course ofprisms
towards the ocrlusal surfare. Blark arrows points to pattern I (Boyde, 1964) prisms and whitr arrow
points to pattern 2 (Roydr, 1964) prisms. Scale har=30 pm. Cl, High magnification of prismatic ( P )
and interprismatic ( I P ) enamrl, as sren in a longitudinal section, at a lateral (outer) side ofthe tooth.
Angle between P and 11' crystallites is about 75'. Scale b a r = 5 pm.
OPOSSUM ENAMEL
327
P:IP
750
- prisrnotic enornel
-----
CRUSHING
BASIN
interprismotic enamel
Figure 11. Diagram summarizing angle relationships of P and 1P crystallites at shearing, pounding
and crushing sites. At the shearing surfaces, P:IP varies from about 60' cervically to 90' occlusally and
I P remains parallel to the occlusal (dorsal or ventral) surface. In basins, P:IP is about 55-65", I P
remains perpendicular to the changing slope of the basin, and the prisms maintain a cuspal tilt. A line
drawn on the small tooth (A-A') shows where the cut would be to give a curve with the above shape
when viewed in longitudinal section.
seen (Fig. 10B). This pattern appears to shift between pattern 1 (black arrow,
Fig. 10B) and pattern 2 (white arrow, Fig. 10B) (Boyde, 1964) of etched enamel
prisms. In Boyde's pattern 1, the prisms appear circular in transverse section and
are completely surrounded with I P enamel. In Boyde's pattern 2, the prisms are
horseshoe-shaped and I P enamel is thicker on two sides of the prisms. I t should be
noted that Boyde's patterns classify prisms as they are viewed transverse to the
long prism axis (or as close to this as possible), but the view in Fig. 10B is of a
natural unfiled surface going down the slope of a shearing-crushing basin.
The angle between the prisms and I P enamel a t the lateral (outer) edge of a
tooth (Fig. 5D) varies from about 60" in a cervical direction, relative to a
horizontal axis, to about 90" at the occlusal tip. The relationship of prisms to I P
enamel is seen in Fig. 1OC where the angle between the two is about 75". At the
outer surfaces, the I P enamel remains fairly perpendicular to the vertical edge of
the tooth, but the prism changes its orientation with respect to I P enamel as it
undulates away from the DEJ and toward the occlusal surface. I n areas of thinner
enamel, i.e. in the basins, the I P enamel remains fairly perpendicular to the
changing slope of the outer surface, and the prisms are directed occlusally
(i.e. dorsally or ventrally) towards the cusps or ridges of the teeth. The angle
between prisms and I P enamel is about 55"-65" in the concave or convex areas
(Fig. 9). The relationships observed in this study are summarized in
diagrammatic form in Fig. 1 1.
328
D. STERN E T AI..
DISCUSSION
Dzferential wear
Surfaces of the opossum molar involved in tooth-food contact wear more
rapidly than those involved in tooth-tooth contact. In functional terms, pounding
and puncturing surfaces wear more quickly than shearing and crushing surfaces.
These differential rates of wear appear to be independent of occlusal pressures
(Butler, 1972; Rensberger, 1973). The present study, however, revealed a
consistent relationship between enamel prism patterns and functional surfaces.
T h e fact that tips of cusps and ridges wear more rapidly than their sides is an
advantage to the organism, since sharp shearing edges can be maintained. If rates
of wear were the same for both patterns, pointed cusps and rounded edges to
shearing surfaces would be maintained and the shearing capacity of the
tribosphenic molar would be reduced. Cusps have to be flattened somewhat in
order for vertical shearing surfaces to acquire sharp leading edges. The
maintenance of these shearing edges is critical to the functioning of the complex
tribosphenic molars (Crompton, 197 1).
Enamel ultrastructure and wear
Pounding pattern
The rapidly wearing surfaces (tips of cusps, trigonid basin rim, and the stylar
shelfi are characterized by the pounding pattern (FigsZD, E, F, 3C, D, 5B).
Compressive forces at pounding surfaces are resisted by the smallest diameter of
the prism. Prisms are aligned in rows at pounding surfaces, not staggered as in
hcxagonal packing (Boyde, 1964); this arrangement enables the IP enamel also to
be well-aligned. Crystallites of the I P enamel, parallel to the occlusal surface, may
be the dominant factor in absorbing compressive forces. Few studies have been
conducted on strength-testing of enamel and nothing has been reported on
primitive enamel. T h e studies reported present varying results (see Waters, 1980)
except for the common tendency for compressive strength to be greater where
prisms were oriented across the long axis (as I P enamel is in the pounding
pattern) of the specimen. Therefore, the occlusal compressive forces may not be as
responsible for wearing of the pounding surface as the abrasion due to food
(Rensberger, 1973). In addition, if tubules occur more frequently within prisms
and along their long axes (J. Tomes, 1849; Boyde & Lester, 1967, 1984), then
prisms might be worn away rapidly because of the discontinuities (Boyde, 1984).
Boyde (1984) and Boyde & Fortelius (1986) have also shown that parallel
elements are less resistant to abrasion than perpendicular ones. Those studies
discussed prisms as parallel and perpendicular elements, but if we can extrapolate
to enamel without Hunter-Schreger bands, the thick IP enamel becomes the
element parallel to the abraded surface. These may be two reasons
(discontinuities presented by tubules within prisms, and parallel interprismatic
enamel) for the relatively rapid erosion of the pounding pattern.
Shearing pattern
Longer-wearing vertical surfaces (bottom of Fig. 3C and Fig. 5C) are
characterized by patterns in which the prisms approach the surface at an oblique
angle and I P crystallites are perpendicular to the shearing force. Aprismatic (AP)
OPOSSUM ENAMEL
329
enamel, which appears in varying amounts at most surfaces ofall teeth (Gwinnett,
1966, 1967; Bhaskar, 1986), seems to be especially abundant on some vertical
shearing surfaces (Fig. 5B) of the opossum molar. Aprismatic crystallites are
oriented perpendicular to the shearing surface, similar to the I P crystallites
(Gwinnett, 1967).
Unworn shearing surfaces are characterized by aprismatic enamel that has a
‘barnacle-like’ appearance (Fig. 5C). Although the present study did not
concentrate on the extent and appearance of AP enamel, i t was obvious that AP
enamel is more abundant on lateral aspects of the tooth (i.e. any side) where thick
enamel occurs. Newly-erupted or -occluded teeth were not examined, so that we
cannot judge how much AP enamel was worn away by attrition, or what
orientation AP crystallites assumed, if present, at tips of cusps.
Shearing-crushing pattern
Prisms of shearing-crushing basins (Fig. 7B, C) meet shearing and crushing
forces at an oblique angle. The spiral patterns at the centres of the trigon and
talonid basin must add durability to the crushing basins, since they are intact
when much of the enamel on the occlusal surfaces of teeth have disappeared
(Fig. 1B). T h e crushing pattern (Fig. 7B, C) can be explained in terms of the
radial and tangential patterns (Fig. 7D-G) (as defined by von Koenigswald,
1982); a single arrangement of P and I P enamel (with respect to the angle
between the two, and with respect to the angle between the prism and the DEJ),
when twisted about the vertical axis of the tooth, forms a spiral. A radial or
tangential pattern is observed depending on the orientation of the prism to the cut
surface (Fig. 7F).
The block shown in Fig. 7C-G demonstrates that the shearing-crushing pattern
viewed internally is not the same as the pounding pattern just below a cusp
(Fig.5B), but the difference lies in the arrangement of prismatic and
interprismatic elements. If there were a constant angle between the prisms and I P
enamel or between the prisms and the dentin, then one of the cut sides of the
shearing-crushing pattern (Fig. 7D-G) would be the same as the pounding
pattern at the cusp (Fig. 2C). The alignment of P and IP enamel changes as one
proceeds away from the centre of the trigon or talonid basin, and also away from
the DEJ (Figs 5A, 7A) of thick enamel towards the outer surface of the tooth.
The spiral arrangement also represents a geometric solution to the problem of
filling in a fissure and maintaining the tilt of the prisms towards the basin rim; the
fissures or basins are the last areas to develop during amelogenesis. Matrix
formation and mineralization begin at the tips of cusps and proceed down the
sides or down the slopes of cusps (Bhaskar, 1986). It is interesting to compare this
spiral arrangement to that in the tapir (Boyde, 1986; fig. 52) and that in the
human (Skobe & Stern, 1980; fig. 3 ) . I n both instances, the spiral was observed at
or near the tips of cusps; the difference in position of the spiral in the opossum
molars may be due to whether or not Hunter-Schreger bands are present, but this
is speculative.
Aprismatic enamel
The poorly-defined prisms (Fig. 5B, D ) and circular profiles at the outer surface
of the tooth (Fig. 5B) are not yet fully understood by enamel microanatomists,
330
D. WERN 87 AL.
except for the fact that P:IP crystallites change proportions as the Tomes' process
is retracted prior to the maturation stage of amelogenesis. A circular profile
(Fig. 5B) probably represents the territory of one ameloblast, and also indicates
that the aprismatic enamel is not entirely without pattern. I t is understood that
enamel crystallites are oriented perpendicular to the apical membrane of the
secreting ameloblast (Skobe, 1977; Simmelink, 1982).
Enamel thickness
The significance of having thinner enamel, at areas of basin rims where there is
no tooth-tooth contact (Fig. 2A, bottom ofFig. 2F) is not clear, but may simply be
that it is not needed in those areas. Thicker enamel is found at areas of basin rims
where tooth-tooth contact is made, i.e. near the paracone and metacone, and the
entoconid (Fig. 1A; Fig. 2B).
Dentinal peaks
The function of the dentinal peaks seen in Fig. 2E is not clear. They are
probably bundles of von Korffs fibers (Bhaskar, 1986); the fact that they are
aligned along the seam, make it inviting to postulate that they may serve as a
signal to ameloblasts to change patterns during amelogenesis. These peaks were
also observed in areas of the upper molar near the metacrista.
Angle of prisms to interprismatic enamel
Another variable of the main patterns is the angle of the P to IP enamel. Along
a thick lateral edge (Fig. 5D) P:IP varied from about 60" cervically to 85-90"
occlusally (Figs 5D and lOC, respectively). If I P enamel remains perpendicular to
the side of the tooth, and the course of the prisms is an undulating one toward the
cusp, then P:IP will change in a cervical-occlusal direction (Fig. 1 1 ) . This
undulation is also responsible for the appearance of patterns 1 and 2 (Boyde,
1964) on the slope of the entoconid (Fig. 5D) leading into the talonid basin. For
the thinner enamel lining inner concave or convex surfaces, the angle of P:IP
averaged 55-65" and was more variable. This can be explained by the fact that
concave inner areas change more drastically in slope than the fairly vertical sides
of the teeth; I P enamel remains perpendicular to the changing slope but varies
with respect to the horizontal aspect and the prisms maintain a cuspal tilt
(Fig. 1 1 ) . The shearing-crushing pattern shows some changes by varying P:IP
angles, thinness of enamel, and the prism arrangement in the centre of the basins,
but has stayed within the limits of a primitive enamel (thick I P enamel, but no
Hunter-Schreger bands).
Solution to a problem, and its consequence5
It is generally true that I P areas dominate most patterns of primitive enamel
(Figs 2C, 5D). In more advanced mammalian enamel, I P areas do not usually
dominate the patterns (Boyde, 1964) and greater strength is maintained by the
fact that the prisms decussate and forces are more easily dissipated (Waters, 1980;
von Koenigswald, 1982). Primitive enamel must satisfy functional needs with less
OPOSSUM ENAMEL
33 1
diversity of pattern since prism paths are more limited in extent of transverse
movement around the longitudinal axis of the tooth (see Skobe & Stern, 1980)
than in more evolutionarily advanced mammalian enamel with decussating
prisms. The opossum molar appears to have reached a satisfactory solution by
presenting a prism arrangement to pounding surfaces which wears rapidly, and a
perpendicular face which is very resistant to shearing forces. T h e result is
interesting, since the plane of one is determined by the plane of the other; the
pounding surface is the other face of the shearing surface.
The fact that I P crystallites are usually perpendicular to the shearing and
shearing-crushing surfaccs means they will etch more readily in acid conditions
(Johnson, Poole & Tyler, 1971) as, for example, when fruit or berries are ingested,
and more of the prism component will be maintained. The patterns in Figs 7C
and 8A, of prisms angulated to the surface, would seem to be effective
topographically in the shearing or abrading of food.
Prisms within the trigonid appear to be more normal to the dorsal surface; they
do not approach the basin at a large angle, and more I P enamel is visible
(Fig. 10A). The trigonid wears away almost as quickly as the cusps (Fig. IB), and
does not have the long life associated with the talonid basin or the trigon. T h e
trigonid is a non-occluding surface, so the functional patterns associated with the
occluding basins are not necessary in this area.
One of the surprising results of this study is the consistent relationship of thc
pounding pattern with the surfaces that exhibit much abrasion in very worn
teeth. We feel that this phenomenon is explained by results of Boyde's (1984)
study (also Boyde & Fortelius, 1986):
1. The parallel I P elements are not very resistant to abrasion, perhaps being
worn away in groups of crystallites.
2. Enamel tubules within prisms present discontinuities which cause the
prisms to abrade quickly.
3. The seam between two different patterns also presents a discontinuity
which is more susceptible to abrasion.
CONCLUSIONS
There are three main patterns of enamel seen in the opossum molars: 1,
pounding; 2, shearing; 3, shearing-crushing. The main elements of differing
functional patterns are: 1, the angles of P and I P enamel to the functional surface;
2, the angle of P and I P enamel to each other; 3, the alignment of prisms; 4,the
thickness of the enamel.
Features of primitive enamel such as dentinal peaks along the DEJ, seams
where two patterns meet, and enamel tubules may serve functional purposes.
Because the pounding pattern erodes more quickly than the shearing pattern,
we suggest that these arrangements represent a selective advantage for the
organism to exploit additional shearing surfaces (Crompton,197 1 ) . The differential
rates of wear may be responsible for the success of the tribosphenic molar.
ACKNO\.2;LEDGEMENI'S
We wish to acknowledge the artistic talents of M r Laszlo Meszoly. This project
was supported by N I H training grant 5-T32-GM07 1 1 7 to Harvard University
332
D. STERN E T AL.
(D. Stern) and NIDR grants DE 07894 (to A. W. Crompton and D. Stern) and
DE 04230 (to Z. Skobe).
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Y
l
I
ABBREVIAIIONS USED IN T E X T AND FIGURES
AP Aprismatic
D Dentin
DEJ Dentin-enamel junction
E Enamel
I P Interprismatic enamel
P Prism/prismatic enamel
PDP Poorly-defined prism
R Radial arrangement
T Tangential arrangement
ac anterior cingulum
B buccal
c cusp “c”
end entoconid
hyd hypoconid
hyld hypoconulid
L lingual
mc metacrista
me metacone
med metaconid
mt me tast yle
pa paracone
pad paraconid
pcd paracristid
pr protocone
prd protoconid
ptd protocristid
sty stylocone
TB talonid basin
T G trigon
T G D trigonid
334
D. SI'EKN E'T A I .
ADDENDUM
After submitting this manuscript, we became aware of a publication by Young,
McCowan & Daley (Scanning Microscopy, I : 1925-1934, 1987) in which they
described the structure-function relationship in enamel of the koala. A difference
bctween leading and trailing edges of these folivorous molars was found in regard
to enamel ultrastructure (angle of prism to functional surface) and enamel
thickness.