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Enamel microstructure in lemuridae (mammalia primates) Assessment of variability.

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Enamel Microstructure in Lemuridae (Mammalia, Primates):
Assessment of Variability
Department of Biological Anthropology and Anatomy, Duke University
Medical Center, Durham, North Carolina 27710
Strepsirhini, Enamel prisms, Hunter-Schreger
This study describes the molar enamel microstructure of
seven lemurid primates: Hapalemur griseus, Varecia variegata, Lemur catta,
Lemur macaco, Lemur fulvus rufus, Lemur fulvus fulvus, and Lemur fulvus
albifrons. Contrary to earlier accounts, which reported little or no prism
decussation in lemurid enamel, both Lemur and Varecia molars contain a
prominent inner layer of decussating prisms (Hunter-Schreger bands), in
addition to an outer radial prism layer, and a thin, nonprismatic enamel
surface layer. In contrast, Hapalemur enamel consists entirely of radial and,
near the surface, nonprismatic enamel. In addition, for all species, prism
packing patterns differ according to depth from the tooth surface, and for all
species but Varecia (which also has the thinnest enamel of any lemurid),
average prism area increases from the enamel-dentine junction to the surface;
this may be a de-dopmental solution to the problem of accommodating a .
Arc a with enamel deposited from a fixed number of cells.’ +
larger outer sur.
Finally, con
g some previous reports, Pattern 1 prisms predomiaate’a
only in the rl -*t ;.iperficial prismatic enamel. In the deeper enamel, prism
cross-sections include both closed (Pattern 1) and arc-shaped (Pattern 2 or,
most commonly, Pattern 3). This sequence of depth-related pattern change is
repeated in all taxa. It should also be emphasized that all taxa can exhibit all
three prism patterns in their mature enamel. The high degree of quantitative
and qualitative variation in prism size, shape, and packing suggests that
these features should be used cautiously in phylogenetic studies.
Hapalemur is distinguished from the other lemurids by unique, medially
constricted or rectangular prism cross-sections at an intermediate depth and
the absence of prism decussation, but, without further assessment of character polarity, these differences do not clarify lemurid phylogenetic relations.
Some characters of enamel microstructure may represent synapomorphies
of Lemuridae, or of clades within Lemuridae, but homoplasy is likely to
be common. Homoplasy of enamel characters may reflect functional constraints. 0 1994 Wiley-Liss, Inc.
The microstructure of primate dental
enamel, like other aspects of tooth morphology, contains data about the phylogeny and
functional morphology of primates. Researchers seeking phylogenetic information
for the most part have focused on enamel
prism cross-sectiona1 patterns (e.g*, Boyde
and Martin, 1982,
1987; Carter,
1922; Dumont, 1993; Gantt, 1980, 1983,
0 1994 WILEY-LISS,
1986; Gantt et al., 1977; Martin et al., 1988;
Shellis and Poole, 1977). Most have attempted to distinguish taxonomically diagnostic prism patterns that might elucidate
Received January 19,1994; accepted May 30,1994.
Address reprint requests to Mary C. Maas, Box 3170, Duke
UniversityMedical Center, Durham, NC 27710.
phylogenetic relations of problematic fossils
or clarify questions of origin or relationships
of higher taxonomic groups. Problems with
interpreting the results of these studies
have arisen, however, because of variation
in enamel microstructure, particularly
within individuals. In investigations of primate enamel, some initial assessments that
seemed to yield phylogenetically useful data
(Gantt et al., 1977; Gantt, 1979, 1980) have
been contradicted (Boyde and Martin, 1982,
1984b; Martin et al., 1988; Vrba and Grine,
1978). These latter studies demonstrated
that variation in enamel microstructure is
substantial and must be a major consideration in any attempts to use microstructural
data in systematics.
Most reports of strepsirhine enamel structure are based on single species (and in some
cases single specimens) (Gantt, 1980; Martin et al., 1988; Shellis, 1984; Shellis and
Poole, 1977). Not surprisingly, there are
conflicting accounts of strepsirhine prism
patterns and other microstructural characters. To date, there have been no comprehensive taxonomic surveys of enamel structure within this diverse group of primates,
and there have been detailed studies of only
two species, Daubentonia madagascarensis
(Shellis and Poole, 1979; Koenigswald and
Pfretzschner, 1987) and Otolemur crassicaudatus (Maas, 1993b). A fuller documentation of strepsirhine enamel structure has
relevance not only for understanding phylogenetic relations within the group, but for
studies of phylogenetic relations of early
Tertiary prosimian-grade primates. However, before enamel structure can be used to
address these issues, the nature of variation
within individuals, within taxa, and between taxa must be clarified and conflicting
reports of strepsirhine enamel patterns resolved. For example, we need to know
whether different descriptions of strepsirhine enamel represent artifacts of preparation or intrinsic structural variation.
Likewise, we need to consider how variation
is expressed within teeth, among individuals, and among species and a t different, hierarchical levels of complexity. Finally, we
need to determine which aspects of primate
enamel structure are most appropriate for
addressing different aspects of biology, including phylogeny and function.
This study documents enamel microstructural variation in molar teeth of one group of
strepsirhines, the Lemuridae. Lemurids are
among the most taxonomically and ecologically diverse of the strepsirhines, and, although their taxonomy and systematics are
not fully resolved’, they are the group on
which most reports of strepsirhine microstructure are based. The aims of this study
are to present an accurate description of lemurid molar enamel microstructure and to
discuss the nature and implications of
enamel variation within the group.
Two important properties of enamel are
durability and structural complexity. Durability (which assures its preservation in the
fossil record) is largely a function of its high
mineral content (95% by weight). The structural complexity of enamel reflects its development.
Enamel structure can be viewed hierarchically (Koenigswald and Clemens, 1992;
Koenigswald et al., 1993). Thus, from smallest to largest units, enamel within a single
tooth is comprised of crystallites, prisms,
enamel types (arrangement and orientation
of groups of prisms), and Schmelzmuster
‘Currently there is a lack of consensus in lemurid systematics.
Independent studies have proposed generic distinction of Lemur
catta and other Lemur species: Simons and Rumpler (1988)
named the L. fuluus-L. macaeo-L. rubriuenter-L. mongoz-L.
caronatus group =Eulemur“;Groves and Eaglen (1988) designated the same group “Petterus.”TattersalI and Koopman (1989)
argued that both Petterus and Eulemur are junior synonyms of
Prosimia Boddaert, 1785. Most recently, Tattersall and
Schwartz (1991) have suggested that the genus Lemur includes
all Lemuridae except Hapalemur, although currently most workers recognize the distinction between Varecia uariegata and Lemur spp. by separate generic designations (Petter et al., 1977).
Lepilemur is currently considered distinct from other lemurs at
the family level (e.g., Groves and Eaglen, 1988; Tattersall, 1982;
Tattersall and Schwartz, 1991),but the position ofHapaZemur is
less clear. Hapalemur is generally included in Lemuridae, but
whereas some recognize a close relationship between Hapalemur
and Lemur catta (Groves and Eaglen, 1988; Simons and Rumpler, 19881, others argue that Hapalemur is sister group to a
clade consisting oflemur (includingthe Lemur fuluus group) and
Varecia (Tattersall and Schwartz, 1991). Because of the lack of
consensus, I follow a conservative approach here and use the
generic designation Lemur for all lemurids but Varecia and
(arrangement and organization of enamel venes between bodies of longitudinally
types within a tooth). Crystallites, the aligned prisms (Boyde, 1964; Boyde and
smallest structural units, may show regular Martin, 1984b; Gantt, 1986). Pattern 3
patterns of variation in orientation. These prisms, like Pattern 2 prisms, have cerviform the major regions of crystallite discon- cally incomplete boundaries, but, like Pattinuity known as prism boundaries, which tern 1prisms, are packed in horizontally offdemarcate enamel prisms and interpris- set rows. Boyde (1964; Boyde and Martin,
matic enamel. Minor regions of crystallite 1984b) described three variants of Pattern
discontinuity have been termed “enamel 3: 3A, 3B, and 3C. These differ primarily in
seams” (Lester and Koenigswald, 1989) and the degree of cervical closure of prism
occur within prism bodies (see arrow, Fig. boundaries and in the amount of interpris6 0 . They appear to be associated develop- matic enamel between adjacent prisms.
mentally with a central ridge on the Tomes However, the variations on the three-patprocess (secretory process of the ameloblast) tern scheme have not been thoroughly docu(Lester and Koenigswald, 1989).Among pri- mented (Boyde, 1964; Boyde and Martin,
mates, seams have been reported in human 1984b; Gantt, 1980, 1983, 1986; Shellis,
deciduous teeth (Lester and Koenigswald, 1984). Moreover, intermediate forms of the
1989) and galago molars (Maas, 1993b).
three basic patterns are common, and any
The next hierarchical level of enamel or- tooth is likely to contain all three (Martin et
ganization defined by Koenigswald and col- al., 1988).
Enamel tubules are an additional feature
leagues (Koenigswald and Clemens, 1992;
Koenigswald et al., 1993), the prism, is com- of the prism level of organization. They are
monly used in mammalian systematics. linear structures of controversial origin (see
Most systematists follow Boyde’s (e.g., 1964, Boyde and Lester, 1984), which are gener1971) scheme of three major prism patterns, ally confined to prism bodies. In some but
which is based on observations of developing not all cases, enamel tubules are continuous
enamel but is typically applied to mature with dentine tubules, which are prominent
(fully mineralized) enamel. The attributes histological features of dentine (Lester et al.,
used to classify prisms pertain to their mor- 1987). Tubules are common in marsupial
phology viewed in cross-section (perpendicu- enamel, where they generally extend from
lar to the prism long axis) and include com- the enamel-dentine junction (EDJ) to the
pleteness of prism boundaries, packing tooth surface, but in primates they occur
arrangement of adjacent prisms, and the less frequently and more typically end close
relative proportions of prismatic and inter- to the EDJ (see arrow, Fig. 11).
The next hierarchical level of enamel
prismatic enamel. Pattern 1 prisms have
complete, typically circular boundaries, are structure defined by Koenigswald and colpacked so that prisms in one row are offset leagues (Koenigswald and Clemens, 1992;
from prisms in the adjacent rows, and usu- Koenigswald et al., 19931, the enamel type,
ally are separated by relatively broad inter- concerns the arrangement and orientation
prismatic regions. In Pattern 2 enamel, the of groups of prisms. Enamel types include
prism boundaries are discontinuous to- radial enamel, where prism long axes are
wards the cervix (root-crownjunction) of the more or less parallel to one another in their
tooth, and prisms are arranged in longitudi- course from the EDJ to the tooth surface,
nal (apicocervical) columns; thus, viewed in and decussating enamel, where prisms are
cross-section, prisms in adjacent rows are arranged in bundles with different orientaaligned, and interprismatic enamel is apico- tions. A single plane of section thus intercervically continuous between adjacent cepts long axes of prisms in adjacent bunprisms (see arrows, Fig. 6B). In the variant dles at different angles. These adjacent
of Pattern 2 enamel most commonly seen in decussation zones are designated parazones
primates, interprismatic enamel is not re- and diazones, depending on whether prism
stricted to inter-row sheets (as is typical of long axes are largely parallel or perpendicuungulates with Pattern 2 prisms) but inter- lar to the section plane. When sectioned
specimens are viewed under incident light,
parazones and diazones appear as alternating light and dark bands, termed HunterSchreger bands (HSB). Decussating enamels vary according to several criteria: 1)the
number of prisms contained in each decussation zone, 2) the amount of cuspal inclination of zones, from the EDJ to the tooth surface, 3) the angles between prisms in
adjacent parazones and diazones, 4)
whether boundaries between zones are
abrupt or occur across a transitional zone
several prisms wide, and 5) the complexity
of zones, including patterns of zone bifurcation. Zone bifurcation occurs when some
prisms within a zone abruptly change direction (Koenigswald and Clemens, 1992). A
third enamel type is nonprismatic enamel,
where C-axes of most crystallites are parallel to one another, without the regular
changes in orientation that demarcate
prism boundaries.
The next hierarchical level, the Schmelzmuster, is the level of organization that describes the arrangement and distribution of
enamel types within a tooth (Koenigswald
and Clemens, 1992; Koenigswald et al.,
1993). For example, a tooth may contain an
inner zone of decussating enamel and an
outer zone of radial enamel, or a tooth may
consist entirely of a single enamel type.
Likewise, the distribution of enamel types
may be uniform or may differ among parts of
the tooth.
This study will examine lemurid microstructure at the levels of Schmelzmuster,
enamel types, prisms, and crystallites. The
focus is on variation within and between
taxa a t each hierarchical level.
Dental specimens used in this study consisted of upper and lower molars extracted
from 16 lemurid cadavers. The specimens
were obtained from the Duke University
Primate Center (DUPC) and represent
seven species and subspecies: Hapalemur
griseus, Varecia variegata rufus, Lemur
catta, Lemur macaco, Lemur fulvus rufus,
Lemur fulvus fulvus, and Lemur fulvus albifrom (Table 1).The teeth were prepared, as
outlined below, to document Schmelzmuster, enamel types, and prism morphology.
TABLE 1. Lemurid saecimens included in this study
Hapalemur grisew
Hapalemur griseus
Varecia uariegata rubra
Varecia uariegata rubra
Lemur catta
Lemur catta
Lemur catta
Lemur macaco macaco
Lemur fuluus rufus
Lemur fuluus rufus
Lemur fuluus rufus
Lemur fuluus fuluus
Lemur fuluus f u l u w
Lemur fuluus futuw
Lemur fuluus albifruns
Lemur fuluus albifrons
Age (years)
DUPC’ 1326
DUPC 1317
DUPC 1127
DUPC 1363
DUPC 1183
DUPC 1242
DUPC 1020
DUPC 1268
DUPC 1192
DUPC 1021
DUPC 1239
DUPC 1202
DUPC 1266
D U E 1196
DUPC 1189
DUPC 1265
DUF’C, Duke University Primate Center.
For study of Schmelzmuster and enamel
types, two pairs of occluding upper and
lower molars from each individual were embedded in epoxy resin (Epo-Tek; Epoxy
Technology, Inc., Billerica, MA) and sectioned, following procedures described previously (Maas, 1993b). One pair was sectioned mesiodistally, in two planes: 1)
through the buccal cusps and (Fig. 1A,B,
a-a’) and 2) through the lingual cusps (Fig.
1A,B, b-b’). The second pair was sectioned
orthogonal to the first, in two buccolingual
planes: 1) through the mesial cusps (Fig.
lA,B, c-c‘) and 2) through the distal cusps
(Fig. 1A,B, d-d’). In all cases, planes of section were oriented perpendicular to the cervical plane (root-crownjunction) of the tooth
(see Fig. 1C). The sectioned specimens were
mounted on scanning electron microscope
(SEM) stubs, polished with 800 and 1,200
grit silicon carbide abrasive paper and 0.05
p,m alumina powder, lightly etched in 5%
HC1 for 10 seconds, and examined in a JEOL
35-C SEM. Sections were photographed a t
low magnification ( 2 0 0 ~for
) preparation of
photomontages of entire sectioned teeth,
and a t higher magnification (1,000-2,000~)
for two-dimensional measurement of angles
of orientation of HSB, enamel prisms, and
crystallites. Descriptions and measurements are based on buccolingual and mesiodistal sections of both upper and lower molars.
Orientations of radial prisms and decussation zones were measured as the two-di-
- d'
- \
Surface-Tangential Sectior
Fig. 1. Oblique occlusal views of (A) upper and (B)
lower right first molars of Lemur fulvus rufus, illustrating orientation of four planes of section: a-a', b b ' , c x ' ,
and d-d'. The gray box in B illustrates location of surface-tangential sections, which is enlarged in the inset
to illustrate the relationship of estimated ameloblast
secretory area (dashed hexagons) to prism cross-sectional area (solid arcades). C illustrates lower molar
section d-d' and the location of major structural features relative to the plane of section.
mensional angle between their long axes
and the EDJ. Degree of decussation was estimated as the two-dimensional angle between the preferred orientation of prism
long axes in the centers of adjacent parazones and diazones. The distribution of
enamel types was observed under incident
light, where HSB and radial enamel can be
distinguished by their different reflective
properties. The thickness of each enamel
type was measured perpendicular to the
EDJ and recorded as a proportion of total
enamel thickness a t the point of measurement.
To assess depth-related variation in prism
cross-sectional morphology, surface-tangential facets were prepared on the buccal surfaces of first or second lower molars (Fig.
1B). The facets were ground with 800 and
1,200 grit silicon carbide abrasive paper until a dentine window was exposed at the center of the facet. This allowed documentation
of prism cross-sections at three depths, relative to the outer tooth surface: superficial,
intermediate, and deep. Superficial enamel
was represented around the outer one-third
of the facet circumference, intermediate
enamel around the middle one-third of the
facet circumference, and deep enamel in the
inner one-third, surrounding the central
dentine window (this method introduces
some sectioning artifact, because prisms a t
different positions on the facet are unlikely
to be sectioned precisely perpendicular to
their long axes). The ground facets were polished with 0.05 pm alumina powder. The
specimens then were cleaned and etched
lightly with acid (5% HC1 for 10 seconds).
The etched specimens were sputter-coated
and then examined and photographed in the
SEM. Two micrographs (2,OOOx) were made
at each enamel depth.
Prism areas (PA) and estimated ameloblast secretory areas (ASA) were measured
for ten prisms selected randomly from each
micrograph (see Maas, 1993b). PA is the
area contained within a prism boundary (for
Pattern 2 and Pattern 3 prisms, the cervical
prism boundary was estimated by a line connecting the two sides of the prism boundary). Estimated ASA is the area of a hexagon
drawn to enclose one prism body and onehalf of the surrounding interprismatic
enamel (see Boyde, 1964; Fortelius, 1985).
PA and ASA were traced directly from micrographs onto acetate overlays and measured using a computerized digitizing program (Sigmascan; Jandel Scientific, San
Rafael, CA). An index of prism area to estimated ameloblast secretory area (PAIASA x
100) was calculated for each of the prism
and estimated ameloblast area measurements. This index is a measure of the relative amounts of prismatic and interprismatic enamel. The higher the index, the
smaller the proportion of interprismatic
Statistical analyses of prism parameters
included single classification analysis of
variance (ANOVA) and nonparametric
Kruskal-Wallis tests (SAS, 1987; Sokal and
Rohlf, 1981)for several levels ofvariation: 1)
among depths for each individual, 2) among
depths for each species (individuals pooled),
3) among individuals of each species, for
each enamel depth (except L. macaco, where
n = 11, and 4) among species (individuals
pooled), for each enamel depth. Significant
pairs were identified by multiple comparisons procedures, using Tukey’s studentized
range test (SAS, 1987). The more conservative nonparametric Kruskal-Wallis test was
used in addition to the parametric ANOVA
because some variables did not meet all the
criteria for analysis of variance.
Schmeizmuster and enamel types
Figures 2 and 3 illustrate the molar
Schmelzmuster for each of the seven taxa.
The figures show nonocclusal surfaces (buccal slope of hypoconid or lingual slope of entoconid), where the full thickness of enamel
is preserved. Hapalemur molar enamel consists primarily of radial enamel, with a thin
Fig. 2. Micrographsof buccolinguallysectioned molars
(sectiond-d’; see Fig. lB, C). EDJ at bottom in all micrographs. A Hapalemur griseus, DUPC 1317, lingual
slope entoconid (occlusal at right), LM,.B: Vureciu variegatu, DUPC 1363, buccal slope hypoconid (occlusal at
leR), RM,. C: Lemur cattu, D W C 1183, lingual slope
entoconid (occlusal at right), LM,. D: Lemur macuco,
DWC 1268, buccal slope hypoconid (occlusal at leR),
RM,. Note orientations of decussating prisms in parazones (p) and diazones (d) in E D . Scale bar, 100 km.
Fig. 3. Micrographs of buccolingually sectioned molars. EDJ at bottom. A. Lemur fuluus rufus, DUPC 1192,
lingual slope entoconid (occlusal at right), RM,. B Lemur fuluus fuluus, DUPC 1202, lingual slope entoconid
(occlusal at left), LM,. C: Lemurfuluus albifmns, D W C
1265, lingual slope entoconid (occlusal at left), LM,.
Note relative proportions of radial enamel (r) and parazones (p) and diazones (d) of decussating enamel. Scale
bar, 100 km.
zone of nonprismatic enamel near the surface but no evidence of prism decussation
(Fig. 2A). In contrast, the Lemur spp. and
Varecia Schmelzmusters consist of three
enamel types. From the surface to the EDJ,
these are nonprismatic enamel (a very small
component of the Schmelzmuster, most
prominent towards the root but typically absent or negligible at more occlusal surfaces),
radial enamel, and decussating enamel
(HSB) (Figs. 2B-D, 3A-C). This arrangement of enamel types is typical of both upper
and lower molars, although the proportions
of radial and decussating enamel vary
among species (see Varecia, Lemur catta
and L. macaco vs. L. fulvus subspp. below).
In general, the distribution of enamel types
is uniform throughout a single tooth (i.e.,
throughout mesial, distal, buccal, and lingual aspects, cusp tips, and basins), but in
some cases a particular plane of section may
obscure the Schmelzmuster. Therefore, care
was taken to examine specimens in a variety
of sectioning planes and using both light microscopy and SEM.
In Lemur and Varecia, HSB typically have
a slight cuspal inclination, forming angles of
70-80" with the EDJ. Towards the cervix,
the enamel is thinner and HSB are more
nearly perpendicular (90") to the EDJ. The
arrangement of HSB in Lemur and Varecia
is simple, with none showing bifurcation of
zones. Numbers of prisms per zone range
from 4-8, with variation within individual
teeth. The change in prism orientation between parazones and diazones is gradual,
occurring across a transitional band 2-3
prisms wide (Figs. 4, 5). The maximum difference in prism orientation between adjacent zones ranges from 30-50" but varies
within single teeth. The transitions between
zones are most distinct in Lemur catta and
Varecia, which also have, on average,
slightly narrower decussation zones (4-6
prisms wide) than Lemur macaco or Lemur
The Schmelzmuster of all subspecies of
Lemur fulvus can be distinguished from
those of Varecia, Lemur catta, and Lemur
macaco by the proportions of radial enamel
and decussating enamel. In Lemur fulvus,
decussation zones are restricted to the inner
50-70% of the enamel (see Fig. 3) (except at
cusp tips and wear facets, where the outer
nonprismatic and radial enamel presumably are worn away). In Varecia, Lemur
catta, and Lemur macaco, decussating
enamel comprises a much larger proportion
of the total enamel thickness (approximately 90%) (see Fig. 2B-D). Varecia has a
molar Schmelzmuster most similar to that
of Lemur catta. Varecia also has the largest
Fig. 4. Micrographs of buccolingually sectioned molars, illustrating orientation of decussating prisms in
parazones (p) and diazones (d). A Varecia variegata
DUPC 1363, buccal slope hypoconid, RM,. B Lemur
catta, DUPC 1183, lingual slope entoconid, LM,. C : Lemur Macaco, DUPC 1268, buccal slope hypoconid, RM,.
Scale bar, 10 pm.
Fig. 5. Micrographs of buccolingually sectioned molars, illustrating orientation of decussating prisms in
parazones (p) and diazones (d). A Lemur fuluus rufus,
DUPC 1192, lingual slope entoconid, RM,. B: Lemur
fuluus fuluus, DUPC 1202, lingual slope entoconid, LM,.
C: Lemur fuluus albifrons, DUPC 1265, lingual slope
entoconid, LM,.Scale bar, 10 pm.
molars and thinnest enamel of all taxa included in this study; Varecia molar enamel
thickness is only 50-75% that of Lemur or
Hapalemur, measured perpendicular to the
EDJ at homologous regions.
Prisms and crystallites
Figures 6-12 illustrate prism cross-sections for each species. Each species shows
considerable variation in prism shape and
packing arrangement, even within a single
field of view, but the most distinct and consistent differences in prism pattern are between superficial prismatic enamel, where
closed prisms (Pattern 1) predominate, and
intermediate and deep enamel, where open
prisms (Pattern 2
' or Pattern 3) predominate. It should be emphasized, however,
that all three prism patterns can occur in
adjacent areas, at any enamel depth; thus,
Pattern 1 prisms can be found in intermediate and deep enamel, though on average less
frequently than open prisms. In some cases,
the orientation of prisms relative to the surface-tangential plane appears to differ between depths. This can be seen most clearly
in the different orientation of crystallite
long axes relative to the surface. This may
be an artifact of the preparation of surfacetangential sections or reflect intrinsic variation in prism orientation due to prism decussation.
In most cases, open-boundary prisms,
whether Pattern 2 or Pattern 3, are separated from one another by relatively broad
regions of interprismatic enamel. Thus, the
Pattern 3 prisms conform to Boyde's (1964)
Pattern 3C, and the lemurid Pattern 2
prisms differ from Boyde's Pattern 2A,
where interprismatic enamel is restricted to
broad inter-row sheets. The angles between
crystallites in interprismatic and prismatic
enamel range from 30-60", regardless of
prism pattern.
In many instances, Pattern 2 and Pattern
3 arrangements were difficult to distin-
Fig. 6 . Hapalemurgriseus, DUPC 1317, LM,.Surfacetangential sections illustrating prism packing arrangements for superficial(A),intermediate(B), and deep (C)
enamel. Arrows in B indicate apico-cervically oriented
regions of interprismatic enamel, typical of Pattern 2
enamel. Arrow in C indicates an enamel seam. Occlusal
towards top. Scale bar, 10 pm.
Fig. 7. Varecia uariegata, DUPC 1127, LM,.Surfacetangential sections illustrating prism packing arrangements for superficial (A),intermediate (B), and deep (C)
enamel. Occlusal towards top. Scale bar, 10 pm.
Fig. 8. Lemur catta, DUPC 1183, LM,. Surface-tangential sections illustrating prism packing arrangements for superficial (A), intermediate (B), and deep (C)
enamel. Occlusal towards top. Scale bar, 10 pm.
Fig. 9. Lemur macaco, DUPC 1268, LM,. Surface-tangential sections illustrating prism packing arrangements for superficial (A),intermediate (B), and deep ( C )
enamel. Occlusal towards top. Scale bar, 10 pm.
23 1
Fig. 10. Lemur fulvus rufus, DUPC 1192, LM,. Surface-tangential sections illustrating prism packing arrangements for superficial (A), intermediate (B), and
deep ( C )enamel. Scale bar, 10 pm.
Fig. 11. Lemur fuluus fuluus, DUPC 1202, RM,. Surface-tangential sections illustrating prism packing arrangements for superficial (A), intermediate (B), and
deep (C) enamel. Arrow in C indicates cross-section of an
enamel tubule. Note frequency of enamel tubules in
deep enamel. Occlusal towards top. Scale bar, 10 pm.
Fig. 12. Lemur fuluus albifrons, DUPC 1265, RM,.
Surface-tangential sections illustrating prism packing
arrangements for superficial (A), intermediate (B), and
deep (C) enamel. Occlusal towards top. Scale bar, 10 pm.
guish. In part this is because of variation in and Kruskal-Wallis tests, P < 0.01). This
prism orientation in regions of decussating was the case both for tests among depths for
enamel. The Pattern 2 packing arrangement single individuals and for tests among
was most clearly seen in the intermediate, depths for each species (with values for conradial enamel of Hapalemur (Fig. 6B) but specific individuals pooled). Similar patwas found in other taxa as well.
terns of depth-related variation in prism
Enamel seams were observed in deep size are also reported for other mammalian
enamel of Hapalemur (see arrow, Fig. 6C) species (e.g., Fosse, 1968; Grine et al., 1986,
but were not evident unequivocally in any 1987; Maas 1993b, in press), which points to
other taxa. Enamel tubules, which in cross- the importance of comparing homologous
section appear as small, dark holes within depths when making interspecific compariprism bodies, are common in the deep sons of prism size and shape.
enamel ofLemur fulvus (see Figs. lOC, 11C,
Results of comparisons among conspecific
12C) but were observed infrequently in sur- individuals at homologous depths have more
face-tangential preparations of Lemur catta, serious implications for phylogenetic studVarecia, and Hapalemur. They were not ies. Significant differences between conspefound in Lemur macaco and were not seen in cific individuals were found in five of 54 poslongitudinal preparations.
sible cases (comparisons for each variable at
Lemurid prism cross-sections vary accord- each enamel depth for each of the six species
ing to shape as well as packing pattern. In represented by more than a single individLemur spp. and Varecia molars, most ual): for Lemur catta deep enamel PA and
prisms are round or ovoid in cross-section, ASA (ANOVA and Kruskal-Wallis test,
although prisms with more angular apices P < 0.051, Lemur fulvus albifrons superfialso occur (see Figs. 7-12). There are differ- cial and intermediate enamel ASA (ANOVA
ences in the completeness (degree of cervical and Kruskal-Wallis test, P < 0.05), and Leclosure) of prism boundaries, but there is no mur fulvus fulvus intermediate enamel ASA
regular pattern to this variation, which (ANOVA
sometimes is seen between adjacent prisms P < 0.05). This amount of conspecific indiin a single field of view. In Hapalemur, some vidual variation, while not large, is greater
superficial enamel shows a pattern of than what would, in most biological studies,
“prisms within prisms” (Fig. 6A), but in gen- be expected from chance alone and suggests
eral Hapalemur superficial and deep prism that, for lemurids, statistical tests of becross-sections conform to the predominately tween-species differences in metrical paovoid shape seen in other lemurids. In con- rameters may not be very informative. This
trast, the intermediate enamel of Hapale- is, in fact, the case. While both ANOVA and
mur is very distinctive (Fig. 6B). These Kruskal-Wallis tests demonstrate signifiprism cross-sections show greater apico-cer- cant among-species differences for all pavical distention than prisms of the other le- rameters a t all depths (individuals pooled
murids. Most have a “waisted,” or medially for each species), multiple comparisons tests
constricted, appearance; others have show that these significant differences perstraight sides and appear either rectangu- tain to different pairs of species, depending
lar, with parallel sides and flat apical ends, on the enamel depth and the metrical paor triangular.
rameter (Table 2).
As might be expected from the within-speSome of the variation in prism paramecies variation in prism packing pattern and ters, both interspecific and intraspecific, unshape, there also is considerable within-spe- doubtedly reflects differences in the orientacies metrical variation in prism size. This tion of prism axes relative to the plane of the
variation is expressed at two levels: among surface-tangential section. This is in part
different enamel depths within individuals because of prism decussation and in part beand species and between conspecific individ- cause of sectioning artifact: a prism perpenuals a t the same enamel depth. For all spe- dicular to the EDJ, even if it pursues a
cies but Vureciu, the three parameters (PA, straight course to the surface, will intercept
ASA, and the PNASA index) differed signif- a plane tangential to the surface at slightly
icantly among enamel depths (both ANOVA different angles at different enamel depths,
TABLE 2. Significant species pairs (P < 0.05) based on multiple comparisons (Tukey's studentized range test) for prism
cross-sectional parameters PA (prism area), ASA (estimated ameloblast secretory area) and PAIASA'
Deep enamel
Intermediate enamel
Superficial enamel
LFA-LM; L F A - W L F F - W
'See text for discussionofprism parameters.Abbreviations: HG, Hapalemurgriseus;LC,Lemur catta; LFA,Lemurfulvus albifrons; LFF,Lemur
fuluus fuluus; LFR, Lemur fuluus rufus; LM,Lemur macaco; W, Varecia uariegata.
TABLE 3. Species values for PA (prism area), ASA (estimated ameloblast secretory area) and PAIASA x 100'
Hapalemur grisew (n = 2)
Varecia uariegata uariegata (n = 2)
Lemur catta (n = 3)
Lemur macaco macaw (n = 1)
Lemur fulvus rufus (n = 3)
Lemur fuluus fuluus (n = 3)
Lemur fuluus albifrons (n = 2)
PA (pm2)
ASA (prn')
PNASA x 100
See text for explanationof prism parameters.Means are based on measurement of ten prisms and surroundingestimated ameloblast secretory
areas for each of n individuals.Abbreviations: S, Superficial;I, Intermediate;D, Deep.
owing to the difference in radius of curvature of the EDJ and the tooth surface.
While keeping in mind the intraspecific
individual variation, the patterns of species
averages of metrical parameters do shed
some light on the nature of variation in lemurid microstructure. Species values for
PA, ASA, and the PNASA index are reported in Table 3. As expected, given the
intraspecific variation, standard deviations
are large for all parameters, and there is
considerable overlap in values, not only
among depths but among species. For most
taxa, PA and ASA show an average size in-
crease from deep to superficial enamel (Fig.
13).Varecza,which has the thinnest enamel,
is an exception. It shows little difference in
average PA and ASA among enamel depths.
Hapalemur, which has enamel comparable
in thickness to Lemur spp., shows a deep to
superficial size increase in average ASA but
not PA. Among enamel depths, the average
PAIASA index is greatest for superficial
enamel in Lemur spp. but not Varecia and
Hapalemur. Among the seven taxa, the
range of prism areas is 8-29 pm2, corresponding to a range of prism diameters of
3.5-6 pm. Estimated ameloblast secretory
Fig. 13. Average species values for prism parameters PA (prism area), ASA (estimated ameloblast
secretory area), and the index PNASA x 100. The relative amount of interprismatic enamel varies
inversely with the index value. S = Superficial enamel; I = Intermediate enamel; D = Deep enamel. See
text for further explanation.
area ranges from 19-50 pm2, and the proportion of prismatic enamel (PNASA)
ranges from 32-74%.
mammals with prismatic enamel, absence of
HSB due to evolutionary reversal has been
documented in at least one group, Cetacea
(Ishiyama, 1987; Maas and Thewissen, in
press). Alternatively, prism decussation
The Schmelzmuster of lemurid molars is may be derived for lemurids. It has been
more complex than previously reported. suggested that prism decussation, which
With the exception of Hapalemur, decussat- serves the biomechanical function of a
ing, radial, and nonprismatic enamel are all crack-stopping mechanism, evolved indepresent, contradicting previous reports of pendently in many lineages of mammals, in
Lemur enamel that described absence of de- response to increased chewing stresses assocussation (Boyde and Martin, 1982, 1984b) ciated with increase in body size (Koenigor little or no decussation (Shellis, 1984). swald et al., 1987). The absence of decussaThe differences between Hapalemur and tion only in Hapalemur griseus, the smallest
other lemurids also reflects greater be- of the lemurids, provides some support for
tween-species variation in Schmelzmuster the idea of independent evolution of decusthan previously appreciated.
sation within the larger-bodied lemurids.
The phylogenetic implications of within- Decussation may have evolved indepenfamily variation in Schmelzmuster and dently in other strepsirhine lineages as well,
enamel types are uncertain, since the char- as suggested by the presence of decussation
acter polarities of enamel types currently in the relatively large-bodied Propithecus
are unknown for Lemuridae, for Strep- (Shellis, 1984) and the absence of decussasirhini, and for Primates. Decussation may tion in the smaller Otolemur (Maas 1993b).
be primitive for lemurids. If so, the absence If HSB were absent in the last common anof HSB in Hapalemur would represent an cestor of lemurids and other strepsirhines,
evolutionary reversal. Although radial decussation could represent either a synapoenamel is almost certainly primitive for morphy of a Varecia-Lemur clade, according
to the phylogenetic hypothesis of Tattersall
and Schwartz (1991), or an instance of parallel evolution if, as others have suggested
(Groves and Eaglen, 1988; Simons and
Rumpler, 1988), Hapalemur and Lemur
cattu are sister taxa. It would not be surprising to find that some enamel characters, like
many other characters of lemurid morphology and behavior, exhibit homoplasy, particularly since this is the case in other groups
of mammals. The question then arises as to
the extent that the distribution of enamel
characters reflects functional constraints,
and what the evolutionary history of this
structure-function complex is within the Lemuridae, and within Strepsirhini, and Primates.
As with descriptions of lemurid Schmelzmuster, previously published reports of lemur prism patterns offer conflicting interpretations. Boyde and Martin (1982,
1984a,b, 1987) reported predominance of
Pattern 1 prisms, Shellis (1984; Shellis and
Poole, 1977) described Lemur sp. enamel as
a variant of Pattern 3, and Gantt (1980) described Lemur sp. enamel prisms as opensided and transitional between Pattern 1
and Pattern 3 prisms. In the specimens reported here, Pattern 1 prisms clearly predominate only in the superficial enamel of
lemurid molars, and prisms with open
boundaries are common in deeper enamel.
In the case ofLemur and Varecia, these open
prisms most commonly show a Pattern 3 arrangement, whereas Pattern 2 prisms are
more common in Hapalemur. In all cases,
prisms are widely separated by interprismatic enamel, as indicated by the relatively
low PAIASA indices. This high proportion of
interprismatic enamel may be primitive for
mammals with prismatic enamel (Koenigswald and Clemens, 1992; Kozawa, 1984;
Sahni, 1979, 1987). None of the lemurids
showed any of what are probably the more
derived prism pattern variants, where interprismatic regions are more restricted (i.e.,
the keyhole-shaped prisms of Pattern 3A,
where interprismatic enamel is restricted to
prism tail regions, or Pattern 2A, where interprismatic enamel is restricted to interrow sheets and the angle between prismatic
and interprismatic crystallites is close to 900).
The observation that all three prism patterns occur in all lemurids studied here,
sometimes within a single field of view, is
not surprising. This heterogeneity of prism
packing arrangements has been reported for
many other primates, including humans,
macaques, and a variety of New World monkeys (Boyde, 1964; Boyde and Martin, 1987).
It is probably typical of primates, as well as
many other mammals.
In light of the common occurrence of Pattern 2 and Pattern 3 prisms in all but the
superficial level of lemurid molar enamel,
the claim that strepsirhines are characterized by Pattern 1 enamel (Martin et al.,
1988) should be abandoned. This, along with
the fact that Pattern 2 and 3 prisms also are
present in molar enamel of Otolemur (Maas,
1993b), Nycticebus, Perodicticis (Shellis,
1984), Propithecus (Shellis, 1984; Boyde and
Martin, 1987), and Daubentonia (Shellis
and Poole, 1979; Martin et al., 1988), indicates that there is no support for the suggestion that the distribution of prism patterns
might provide evidence for either a
anthropoid dichotomy (Martin et al., 1988).
As is the case with Schmelzmuster, use of
prism patterns in phylogenetic studies requires determination of character polarities.
Some have assumed that closed (Pattern 1)
prisms are primitive for mammals, based on
knowledge of the distribution of Pattern 1
prisms in some living groups (e.g., Boyde
and Martin, 1984a). However, Pattern 1
prisms have been shown to be derived for
Multituberculata (Krause and Carlson,
19871, and a report of open prisms in a dryolestid eupantothere, a primitive Cretaceous mammal (Lester and Koenigswald,
1989), suggests that open prisms may in fact
be primitive for therian mammals as well.
As pointed out by Koenigswald and Clemens
(1992), determination of character polarity
for prism patterns is complicated by the fact
that a given pattern can include apparently
primitive and very derived variants. Thus,
Pattern 3 enamel includes the open prisms
of the dryolestid eupantothere as well as the
almost certainly derived Pattern 3A keyhole
pattern of human enamel. Furthermore, the
character transformation sequence among
variants of a given prism pattern (e.g., Pattern 3C to 3B to 3A) or among prism patterns (e.g., Pattern 1 to Pattern 2 or Pattern
3) has yet to be demonstrated.
The ubiquitous occurrence of open prisms
in the lemurids studied here does provide
some support for the notion that open
prisms are primitive for Lemuridae, though
this has yet to be tested by out-group comparisons. In any event, open prisms are
clearly more widely distributed among
strepsirhine taxa than previously thought
and may well be primitive for strepsirhines,
if not primates.
In this context, the enamel microstructure
of various early Tertiary primates is of considerable interest. Not only might it elucidate character states of primitive primate
enamel, but such data also are relevant to
the issue of the relationships of various
Eocene primate groups to living haplorhines
and strepsirhines. Gantt (1980) reported
that a number of early Eocene primates
(Necrolemur, Adapis, Smilodectes, and
Notharctus) were characterized by Pattern 1
prisms. However, it is possible that Gantt’s
study sampled only the superficial enamel,
a region where, as has been shown here,
Pattern 1 prisms are common, even for taxa
where open prisms predominate at deeper
levels. Gantt’s preliminary survey therefore
cannot be considered conclusive.
Prism shape also has received some attention in phylogenetic studies, although generally less than prism packing patterns. For
example, prism cross-sections may appear
apico-cervically distended or compressed,
and their shapes may vary in angularity and
symmetry. Qualitative differences in prism
shape (rounded-ovoid,rectangular, triangular) were used to distinguish between
prisms of colobines and cercopithecines and
among various hominoids (Dostal, 1989;
Dostal and Zapfe, 1986; Dostal et al., 1985).
Martin et al. (1988:259) noted a “so far
unique inverted V shape to the prism outline” of the callitrichid primate Leontopithecus. In the case of lemurids, the distinctive
medially constricted prism cross-sections of
Hapalemur intermediate enamel appear to
be yet another instance of a unique prism
shape. If this does represent an autapomor-
phy of Hapalemur, however, it is of little
significance for lemurid or strepsirhine systematics.
In terms of phylogenetic significance,
quantitative assessments of differences in
lemurid prism shape are even more problematic than qualitative assessments. Statistical analyses of prism shape variables
have proved difficult for some taxa, largely
because of the heterogeneity of variances of
shape parameters (Grine et al., 1986,1987).
Moreover, the utility of quantitative analyses of prism shape in systematics has been
questioned, again largely because of the heterogeneity in prism shape in some species
(Koenigswald and Clemens, 1992; Maas, in
press). Quantitative prism shape analyses
are particularly problematic for decussating
enamel, where differences in prism orientation add an additional component of variation which can confound two-dimensional
shape analysis (Maas, in press; Maas and
Thewissen, in press). Likewise, differences
in sectioning planes among specimens may
influence prism shape comparisons (Maas,
1993b), and prism shape also can be affected
by etching regime (e.g., Martin et al., 1988).
For whatever reasons, the magnitude and
nature of within-species variation in prism
parameters for the lemurids studied here
precluded meaningful statistical analyses of
species differences. Nevertheless, some interesting trends were apparent when only
species averages were considered. The increase in average area of estimated ameloblast secretion from the EDJ to the tooth
surface, seen in all lemurids except Varecia,
most likely reflects increase in tooth area
from the EDJ to the surface (e.g., Fosse,
1964, 1968): estimated ameloblast secretion
area increases from the EDJ to the outer
surface of the tooth because these differentsized surfaces must be covered by enamel
deposited by the same number of ameloblasts. Varecia, which has the thinnest
enamel of any of the taxa studied and therefore presumably the least depth-related difference in enamel area, does not show this
size-depth relationship.
In sum, metrical variation in size or shape
of enamel prisms and ameloblasts appears
to have little systematic significance a t the
generic or specific level, at least for Lemuridae. Although the sample sizes for all taxa
were small (1-3 individuals), it is unlikely
that larger sample sizes would add any discriminating power to these variables, given
the high individual variability in prism parameters and the extensive overlap in values among taxa. In some other mammalian
groups, most notably Multituberculata,
prism size variation has been shown to be
useful systematically a t higher taxonomic
levels (e.g., Krause and Carlson, 19871, but
it has yet to be shown that this is the case for
The systematic significance of prism features such as enamel seams and enamel tubules in lemurids is unclear. Of the taxa
studied here, seams were observed unequivocally only in the deep enamel of Hapalemur. Enamel seams have been observed in
Otolemur crassicaudatus as well (Maas,
199313). Seams are common in chiropteran
enamel (Lester and Hand, 1987) and may be
a fairly common component of primitive
prismatic and nonprismatic enamels (Lester
and Koenigswald, 1989; Koenigswald and
Clemens, 1992). As noted above, identification of tubules in cross-sectional preparations is sometimes problematic, and thus
the apparent absence of tubules in some
specimens examined here is not definitive.
Shellis and Poole (1977), for example, found
that in Lemur sp., tubules could be observed
in thin section preparations but not in the
SEM. In this study, tubules were fairly common in cross-sections of deep enamel of Lemur fulvus and Lemur catta and very close
to the EDJ in Hapalemur. Shellis and Poole
(1977) described Propithecus enamel and
noted that tubules frequently appeared to
extend to the tooth surface. This does not
appear to be the case for lemurids.
Although we cannot assess polarity of
prism patterns or enamel types from the
data reported here, microstructure is consistent with the interpretation, based on some
other morphological criteria (Tattersall and
Schwartz, 19911, that Lemur spp. and Varecia are distinct from Hapalemur. Moreover,
there are no characters of enamel microstructure shared between Lemur catta and
Hapalemur to the exclusion of the other lemurids. Koenigswald and colleagues (Koe-
nigswald and Clemens, 1992; Koenigswald
et al., 1993) have suggested that there is an
inverse relationship between the hierarchical levels of structural complexity and taxonomic rank. They propose that the most
complex structural levels (enamel types,
Schmelzmuster) are useful in species and
generic distinctions, whereas the least complex levels (crystallites, prisms) are most diagnostic at the taxonomic level of the family
or order. The theoretical basis of this is unclear, but this analysis of lemurid enamel,
where Hapalemur is most clearly distinguished from Lemur spp. and Varecia on the
basis of Schmelzmuster, appears to be another case of this phenomenon.
It is particularly important to understand
that although enamel microstructural characters may in some cases be useful in testing
phylogenetic hypotheses, this is not always
the case. Care must be taken to define character states so as to facilitate distinction of
homoplasies from shared derived characters. The traditional definitions of enamel
characters are a first step but not, in themselves, adequate for this task.
The Hapalemur Schmelzmuster, which
consists almost entirely of radial enamel,
with a thin surface layer of nonprismatic
enamel, is different from that of the other
lemurids studied. The Schmelzmuster of Lemur spp. and Varecia contains an additional, prominent inner layer of decussating
enamel (HSB). In Lemur fulvus subspp.,
HSB comprise a smaller proportion of the
total enamel thickness than in Lemur catta,
Lemur macaco, and Varecia, but this difference in Schmelzmuster is much less pronounced than that which distinguishes &mur spp. and Varecia from Hapalemur. All
lemurids are characterized by an open (Pattern 2 or Pattern 3) prism pattern. Previous
reports that Lemur enamel consists of Pattern 1 prisms are based on incomplete sampling of lemur enamel. Pattern 1prisms are
predominant a t the surface of enamel of lemurids, but Pattern 2, or, most commonly,
Pattern 3 prisms are found a t deeper levels.
The Pattern 2 arrangement is most pronounced in Hapalemur molars, where, at in-
termediate depths, prisms also have a
unique, medially constricted cross-sectional
Although this study demonstrates similarity in enamel microstructure among Lemur spp. and Varecia and the distinctiveness of Hapalemur, the phylogenetic
significance of the distribution of enamel
microstructural features depends on interpretation of character polarity. Thus,
whether radial enamel or HSB is primitive
for Lemuridae or for Strepsirhini would affect phylogenetic interpretations based on
Schmelzmuster. Likewise, open prisms may
be an autapomorphy of Lemuridae or primitive for the group.
To begin to resolve questions of character
polarity and character transformation in lemurid enamel microstructure, one must
first identify appropriate outgroups, which,
for Lemuridae, is not an easy task (Eaglen,
1983). Previously suggested candidates include Indriidae (e.g., Eaglen, 1983; Groves,
1974), Cheirogaleidae (e.g., Charles-Dominique and Martin, 1970; Eaglen, 1983; Yoder, 1994), and the fossil Adapidae (e.g.,
Beard et al., 1988; Eaglen, 1983; Gregory,
1920; Szalay and Delson, 1979). Currently,
little or nothing is known of enamel microstructure in any of these groups, but a survey of enamel microstructure of these and
other strepsirhine taxa could resolve the
question of polarity of enamel characters.
Whether this information would in turn
help resolve phylogenetic questions is less
certain, however, given the likelihood of homoplasy in enamel characters. There is a
growing body of evidence that the distribution of some enamel microstructure characters reflects functional, as well as phylogenetic constraints (e.g., Koenigswald et al.,
1987; Maas, 1992, 1993a,b; Stern et al.,
1989).Although enamel microstructure may
not clarify phylogenetic questions for this
group of mammals, an understanding of the
distribution of enamel characters, within a
phylogenetic context, could provide important insight into the evolution of this structure-function complex.
I thank J. Muennig for photographic
work, D. Overdorff and A. Yoder for discus-
sion of strepsirhine systematics, and R.F.
Kay, P. Ungar, and two anonymous reviewers for comments on an earlier draft of this
paper. This research was supported by BNS
9020788 from the National Science Foundation.
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mammalia, primate, lemuridae, enamel, assessment, microstructure, variability
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