C 2005)
Journal of Mammalian Evolution, Vol. 12, Nos. 3/4, December 2005 (
DOI: 10.1007/s10914-005-6968-8
Incisor Schmelzmuster Diversity in South America’s Oldest
Rodent Fauna and Early Caviomorph History
Thomas Martin1
Investigation of the enamel microstructure of 20 isolated rodent incisors from the ?Eocene Santa
Rosa local fauna (Peru) yielded exclusively schmelzmuster with multiserial Hunter–Schreger
bands (HSB). All three subtypes of multiserial HSB with parallel, acute angular, and rectangular
interprismatic matrix (IPM) that were previously reported for caviomorph rodents are present.
Two lower incisors with rectangular IPM can be attributed to the Octodontoidea, a caviomorph
superfamily exhibiting this highly derived enamel type. The plesiomorphic pauciserial condition
that characterizes early Paleogene rodents such as North American Ischyromyoidea (including
“Franimorpha”) has not been detected. It is therefore probable that the founder populations of
South American Caviomorpha already possessed a derived incisor schmelzmuster with multiserial
HSB that is shared with African Thryonomyoidea. Because on the North American continent a
possible stem-lineage representative of Caviomorpha with multiserial HSB has never been detected,
incisor enamel microstructure supports the hypothesis of an African origin of Caviomorpha from
a common ancestor shared with Thryonomyoidea.
KEY WORDS: Caviomorpha, enamel microstructure, Eocene, Peru, Santa Rosa.
INTRODUCTION
The recently discovered ?Eocene Santa Rosa locality in Peru (Campbell, 2004) has yielded
the oldest rodents in South America that are known to date. On the basis of several fragmentary dentaries and more than 200 isolated molars and premolars, Frailey and Campbell
(2004) described a diverse caviomorph rodent fauna consisting of at least six genera and
nine species that can be referred to the Families Erethizontidae, Agoutidae, and Echimyidae. A large number of isolated incisors have been collected from the Santa Rosa locality
that cannot be assigned to the generic or specific level using gross morphology, but unequivocally are attributable to Rodentia based on shape and enamel distribution. In terms
of gross morphology, isolated rodent incisors are of little value for taxonomic and phylogenetic studies because they have a rather uniform shape. However, rodent incisors can
provide important information at the microstructural level of the enamel.
Rodent incisor enamel microstructure is a powerful tool for rodent systematics and
phylogeny (Korvenkontio, 1934; Wahlert, 1968; Boyde, 1978; Koenigswald, 1985; Martin,
1 Forschungsinstitut
Senckenberg, Senckenberganlage 25, 60325 Frankfurt am Main, Germany. E-mail:
[email protected]
405
C 2005 Springer Science+Business Media, Inc.
1064-7554/05/1200-0405/0 406
Martin
1992, 1993, 1997; Kalthoff, 2000). As mammalian enamel in general, rodent incisor
enamel is formed from hydroxyapatite crystallites that are bundled into rodlike structures, the enamel prisms (P). These prisms have a diameter of approximately 5 µm. They
originate at the enamel–dentine junction (EDJ) and run through the entire thickness of the
tissue to the outer enamel surface (OES). The second structural element of the enamel is
the interprismatic matrix (IPM), in which the crystallites are oriented in parallel but are
not bundled. IPM may run parallel, at an acute angle, or rectangular to the long axes of
the prisms. The plesiomorphic condition for therians is a single layer of radial enamel in
which all prisms run parallel to each other in a straight course or slightly bent from the
EDJ to the OES. In most medium to large sized placentals, the prisms are arranged in decussating layers, the Hunter–Schreger bands (HSB), which are interpreted as an adaptation
to strengthen the enamel when the chewing stress is increased (Koenigswald et al., 1987;
Pfretzschner, 1988, 1994; Rensberger, 1997). Small mammals, such as most lipotyphlans,
usually lack HSB; rodents are an important exception and have well-developed HSB in their
molars and their highly specialized incisors (Korvenkontio, 1934; Wahlert, 1968; Boyde,
1978; Koenigswald, 1980, 2004; Martin, 1992, 1997). Rodent incisor enamel with very few
exceptions is double-layered, with the portio externa (PE) formed by radial enamel and the
portio interna (PI) by HSB.
Within a HSB, the prisms run parallel to each other and in adjacent HSB they decussate
at a high angle. Three basic types of HSB occur in rodent incisors: pauciserial, uniserial,
and multiserial HSB (Korvenkontio, 1934; Wahlert, 1968, 1989; Martin, 1992, 1993, 1997).
Pauciserial HSB are plesiomorphic within Rodentia and are restricted to Paleogene groups
such as Ischyromyoidea and early ctenodactyloids. Uniserial and multiserial HSB are
derived. In uniserial enamel, each HSB is formed by a single prism layer. This enamel type
occurs only in rodents where it is found in Myomorpha and Sciuromorpha (Korvenkontio,
1934; Wahlert, 1968; Koenigswald, 1980; Kalthoff, 2000). Multiserial HSB characterize
the South American Caviomorpha, African Thryonomyoidea, derived ctenodactylids, and
pedetids. They are slightly thicker than pauciserial HSB but structurally more derived in
having a thinner IPM that does not surround each individual prism and mostly runs at a
certain angle to the prism long axes. In the most derived multiserial HSB that are found
in Octodontoidea, IPM runs at a right angle to the prisms. Other derived characters of
multiserial enamel are steeply inclined HSB, transition zones between the HSB, oval prisms
cross-sections in the PI, and lancet shaped prisms cross-sections in the PE (Korvenkontio,
1934; Wahlert, 1968, 1984; Martin, 1992, 1993, 1997).
In an earlier study, the enamel microstructure of six isolated rodent incisors from
Santa Rosa was examined (Martin, 2004). Among two upper and four lower incisors
from three size classes, all three subtypes of multiserial HSB were detected that had been
previously reported for caviomorph rodents (with parallel, acute angled, and rectangular
IPM). While the more plesiomorphic subtypes may belong either to Erethizontidae or
Agoutidae (both families are represented by molars), the most derived rectangular IPM
represents a synapomorphic character of Octodontoidea (to which the Echimyidae belong
that are represented by molars in the Santa Rosa fauna). Since that investigation, a larger
sample of 20 isolated insisors has became available which provide and extended basis for
documenting the schmelzmuster diversity in the Santa Rosa Fauna. Of particular interest was
the question whether additional plesiomorphic (pauciserial) enamel types could be found
in the Santa Rosa rodent fauna, because of their relevance to the long-standing controversy
Incisor Schmelzmuster Diversity
407
about the origin of South American caviomorphs. Wood and Patterson repeatedly advocated
a North or Middle American origin of caviomorphs from Ischyromyoidea (“Franimorpha,”
certainly a paraphyletic group; Wood and Patterson, 1959; Wood, 1981, 1985; Patterson
and Wood, 1982), while Lavocat (1969, 1971, 1974, 1976) favored an origin from African
hystricognathous Thryonomoidea (“Phiomorpha”). The North American Ischyromyoidea
are characterized by a plesiomorphic schmelzmuster with pauciserial HSB, but all known
South American caviomorphs exclusively have a derived schmelzmuster with multiserial
HSB (Martin, 1992, 1994, 2004). This large sample of rodent incisors probably predating all
others on that continent provides a good opportunity to test the hypothesis that the earliest
caviomorphs already possessed schmelzmuster with multiserial HSB and that rodents with
pauciserial HSB never reached South America.
MATERIALS AND METHODS
Enamel preparation technique has been described in detail elsewhere (Martin, 1992,
1993). Rodent incisors were embedded in polyester resin and cut in longitudinal and crosssections. Samples were ground, polished, and subsequently etched with 2 N hydrochloric
acid for 2–4 s to make morphological details visible. After rinsing and drying, samples
were sputtercoated with gold and studied with a scanning electron microscope (SEM) at
magnifications between 350× and 2000×. The enamel samples are housed in the author’s
enamel collection under the reference numbers given (MA plus number). For a glossary of
terms see Koenigswald and Sander (1997) and Martin (1999).
Rodent incisors (Fig. 1) studied from the ?Eocene Santa Rosa locality, Natural History
Museum of Los Angeles County (LACM) locality 6789 (collected by K. E. Campbell, C. D.
Frailey, and L. Romero-Pitman in 1995 and 1998), lower incisors: LACM 149406 (right),
MA 272; LACM 149409 (right), MA 273; LACM 149411 (right), MA 275; LACM 149414
(left), MA 281; LACM 149415 (right), MA 265; LACM 149416 (right), MA 284; LACM
149419 (left), MA 277; upper incisors: LACM 149405 (left), MA 271; LACM 149407
(left), MA 269; LACM 149408 (right), MA 274; LACM 149410 (left), MA 270; LACM
149412 (left), MA 276; LACM 149413 (right), MA 283; LACM 149417 (right), MA 282;
LACM 149418 (left), MA 280; LACM 149420 (right), MA 279; LACM 149421 (right),
MA 268; LACM 149422 (left), MA 278; LACM 149423 (left), MA 266; LACM 149424
(left), MA 267.
RESULTS
The investigated sample comprises 13 upper and 7 lower incisors that can roughly
be divided in four size classes. The smallest incisor has an anterior–posterior diameter of
0.98 mm and the largest of 3.52 mm. The cross-sections (Fig. 1) of the incisors exhibit a
considerable variability and indicate a higher taxonomic diversity than suggested by the
size classes. One upper incisor (LACM 149408) has a groove on the lateral side of the
enamel cover.
All incisors that have been studied have a schmelzmuster with multiserial HSB. Three
subtypes of multiserial HSB have been detected with parallel, acute angular, and rectangular
IPM, all of which are typical for caviomorph rodents. The majority of incisors (all 13 uppers
and 2 lowers) have multiserial HSB with parallel to slightly angular IPM (Table I; parallel
408
Martin
Fig. 1. Incisor cross-sections of Santa Rosa caviomorph rodents (A–L, upper; M–R, lower incisors).
(A) LACM 149408 (MA 274); (B) LACM 149423 (MA 266); (C) LACM 149413 (MA 283); (D)
LACM 149421 (MA 269); (E) LACM 149417 (MA 282); (F) LACM 149424 (MA 267); (G) LACM
149410 (MA 270); (H) LACM 149418 (MA 280); (I) LACM 149422 (MA 278); (J) LACM 149412
(MA 276); (K) LACM 149405 (MA 271); (L) LACM 149407 (MA 269); (M) LACM 149411 (MA
275); (N) LACM 149415 (MA 265); (O) LACM 149406 (MA 272); (P) LACM 149416 (MA 284);
(Q) LACM 149409 (MA 273) [Octodontoidea]; (R) LACM 149414 (MA 281) [Octodontoidea].
and parallel to acute angular IPM is considered one subtype). In this enamel subtype
(Figs. 2 and 3), the IPM is comparatively thick and IPM crystallites run parallel or at
a very low angle (less than 10◦ ) to the long axes of the prisms. This IPM orientation
makes it difficult to differentiate IPM and prisms in longitudinal and cross-sections. HSB
appear less regular than in the subtypes with acute angular or rectangular IPM and often
are slightly sigmoidally bent (visible in longitudinal section). Despite these plesiomorphic
characters, this multiserial enamel subtype is clearly distinct from the pauciserial condition
in the presence of transition zones between HSB, a thinner IPM that does not surround
each single prism, oval (PI), or lancet-shaped (PE) prisms cross-sections, and more steeply
inclined HSB. LACM 149408, an upper incisor with a lateral groove on the enamel cover
Incisor Schmelzmuster Diversity
409
Table I. Incisor Enamel Characters of the Studied Specimens from Santa Rosa
Specimen
number
LACM 149421
LACM 149417
LACM 149423
LACM 149424
LACM 149407
Prisms Inclination Enamel Percentage
PE
per
of
thickness
of PE
prism
◦
Incisor Schmelzmuster HSB HSB ( )
(µm)
thickness inclination (◦ )
Upper
Upper
Upper
Upper
Upper
Multiserial
Multiserial
Multiserial
Multiserial
Multiserial
3–5
3–4
3–6
3–4
2–5
40
25
20
15
25
95
110
125
225
65
30
20
15
20
25–30
55
55
55
55
45
LACM 149412 Upper
Multiserial
3–5
35
85
30
70
LACM 149408 Upper
Multiserial
3–5
25
225
20
55
LACM 149410 Upper
Multiserial
3–4
20
235
20
70
LACM 149413 Upper
Multiserial
3–4
20
225
20
60
LACM 149405 Upper
Multiserial
2–3
30
110
25
55
LACM 149418 Upper
Multiserial
3–5
20
255
15
65
LACM 149420 Upper
Multiserial
3–4
25
270
15
55
LACM 149422 Upper
Multiserial
2–5
35
90
25
?
LACM 149416 Lower
Multiserial
3–4
45
115
15
45
LACM 149419 Lower
Multiserial
3–4
40
110
20
?
LACM 149406
LACM 149411
LACM 149415
LACM 149409
LACM 149414
Multiserial
Multiserial
Multiserial
Multiserial
Multiserial
3
3–6
3–5
3–4
3–5
40
35
25
30
30
95
265
225
180
230
20
15
20
15
20
55
65
55
65
65
Lower
Lower
Lower
Lower
Lower
IPM
in PI
(angle)
Parallel
Parallel
Parallel
Parallel
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Parallel
to acute
Acute
Acute
Acute
Right
Right
belongs to this group. A similar incisor with a lateral groove, most probably belonging to
the same species, was studied in the previous survey (Martin, 2004) and had the same HSB
subtype with parallel to slightly angular IPM.
Three lower incisors have multiserial HSB with acute angular IPM that anastomoses
between the prisms (Table I; Fig. 4). The angle between IPM crystallite orientation and
the long axis of the prisms is as much as 45◦ . The higher the angle between IPM and the
long axes of the prisms, the more regular and less sigmoidally bent the HSB appear in
longitudinal section. In contrast to the parallel to slightly angular IPM subtye, prisms and
IPM can be easily distinguished. In the cross-sections, the regularly anastomosing IPM is
clearly visible.
Two lower incisors have multiserial HSB with IPM that runs at a very high angle to
the long axes of the prisms (Table I, Fig. 5). In LACM 149409, the IPM is oriented at a
right angle to the prism long axes. IPM forms plates (“inter-row sheets”) between the prism
rows that anastomose only infrequently as is evident in cross-section (Fig. 5D). In LACM
149414, the angle between IPM crystallites and prisms is slightly less than 90◦ , but IPM
410
Martin
Fig. 2. Scanning electron micrographs of caviomorph (LACM 149423 [MA 266]) upper incisor enamel
from Santa Rosa with parallel IPM in the PI. In all sections, EDJ is to the right and in longitudinal
sections tip of the incisor is to the top. Scale bar equals 10 µm. (A) Overview of longitudinal section;
(B) Detail of PI in longitudinal section. IPM runs parallel to the long axes of the prisms; (C) overview
of cross-section; (D) detail of PI in cross-section.
forms plates between the prism rows and anastomoses only occasionally. In both incisors,
the HSB appear regular and straight in longitudinal section.
DISCUSSION
The ?Eocene Santa Rosa local fauna yielded what are probably the oldest known
rodents from South America. The fauna therefore provides important evidence for the
question of the origin and early diversification of caviomorph rodents on the continent.
During the late Mesozoic and most of the Cenozoic, South America was an island continent
with a highly endemic fauna lacking rodents (Simpson, 1980). The hitherto oldest South
Incisor Schmelzmuster Diversity
411
Fig. 3. Scanning electron micrographs of caviomorph (LACM 149407 [MA 269]) upper incisor
enamel from Santa Rosa with parallel to acute angular IPM in the PI. In all sections, EDJ is to the
right and in longitudinal sections tip of the incisor is to the top. Scale bar equals 10 µm. (A) Overview
of longitudinal section; (B) detail of PI in longitudinal section. IPM runs at a slight angle to the long
axes of the prisms; (C) overview of cross-section; (D) detail of PI in cross-section.
American rodents are from the Deseadan South American Land Mammal Age which was
originally regarded as early Oligocene but is now considered as late Oligocene to early
Miocene (MacFadden et al., 1985) or late early Oligocene to early Miocene (Marshall
et al., 1986). Recently, a mandible of a supposed dasyproctid has been reported from preDeseadan strata of Tinguiririca (Chile) that have been dated radiometrically at 31.5 Ma, and
possibly extend back to ∼37.5 Ma (early Oligocene or late Eocene) (Wyss et al., 1993).
There is a long-standing debate about the origin of South American caviomorph
rodents, and two classic hypotheses have been put forward. Either the rodents are descendants of North American Ischyromyoidea (“Franimorpha”; Wood and Patterson, 1959;
412
Martin
Fig. 4. Scanning electron micrographs of caviomorph lower incisor enamel from Santa Rosa with
acute angular IPM in the PI. In all sections, EDJ is to the right and in longitudinal sections tip of the
incisor is to the top. Scale bar equals 10 µm. (A) Overview of longitudinal section (LACM 149406
[MA 272]); (B) detail of PI in longitudinal section (LACM 149411 [MA 275]) (IPM runs at an acute
angle (about 45◦ ) to the long axes of the prisms); (C) overview of cross-section (LACM 149406 [MA
272]); (D) detail of PI in cross-section (LACM 149411 [MA 275]).
Wood, 1981, 1985; Patterson and Wood, 1982) or African Thryonomyoidea (“Phiomorpha”; Lavocat, 1969, 1971, 1974, 1976). Stressing the importance of enamel microstructure,
Martin (1992, 1994) explicitly argued for a common origin of Caviomorpha and African
Thryonomyoidea (probably from Asian stem-lineage hystricognaths), because both share
the same derived multiserial schmelzmuster in the incisors. North and Middle American
Ischyromyoidea are characterized by plesiomorphic schmelzmuster with pauciserial HSB,
and no evidence of evolution of the multiserial condition has been detected in that group.
Neither the hypothesis of an Asian origin of hystricognath rodents and subsequent migration
Incisor Schmelzmuster Diversity
413
Fig. 5. Scanning electron micrographs of octodontoid (LACM 149409 [MA 273]) lower incisor enamel
from Santa Rosa with rectangular IPM in the PI. In all sections, EDJ is to the right and in longitudinal
sections tip of the incisor is to the top. Scale bar equals 10 µm. (A) Overview of longitudinal section;
(B) detail of PI in longitudinal section showing plate-like IPM that runs at a right angle to the prism
long axes; (C) overview of cross-section. The crack caused by the grinding and polishing procedure
runs straight in the PE (radial enamel) and follows the wavy arrangement of prism cross-sections in
the HSB of PE; (D) detail of PI in cross-section. IPM forms “interrow sheets” between the prism rows
and anastomoses infrequently.
via North America (Hussain et al., 1978) nor Australia and Antarctica (Houle, 1999) to
South America route are not supported by the fossil record, because hystricognath rodents
have been found neither in North America nor in Australia and Antarctica.
Incisor enamel character polarity (pauciserial—plesiomorphic, multiserial—derived)
is clearly evident from outgroup comparison and biomechanical considerations. A pauciserial schmelzmuster characterizes early Paleogene rodents and has not been found in any
Neogene rodent (Korvenkontio, 1934; Wahlert, 1968; Martin, 1992, 1993, 1997, 1999).
414
Martin
The pauciserial HSB in the incisor enamel of early rodents structurally resemble the earliest known eutherian HSB, which occurred in widely disparate lineages, such as early
Paleogene Arctocyonidae (Koenigswald et al., 1987), Tillodontia (Koenigswald, 1997),
Primates (Clemens and Koenigswald, 1991), Creodonta (Stefen, 1997), and early Gliriformes (Martin, 2004). A cladistic analysis of Paleogene rodents based on dental characters
(Marivaux et al., 2004) corroborated the plesiomorphic condition of the schmelzmuster
with pauciserial HSB. Biomechanically, HSB are interpreted as strengthening devices and
crack-propagation inhibitors (providing a “plywood-effect”; Lehner and Plenck, 1936;
Pfretzschner, 1988, 1994; Koenigswald and Pfretzschner, 1991). IPM that runs at an acute
or right angle to the prisms as in multiserial HSB provides additional strengthening in the
third direction. Thus biomechanical considerations provide an independent line of evidence
for the derived condition of the schmelzmuster with multiserial HSB.
The Santa Rosan rodents are crucial evidence because they hold valuable information
on the evolutionary history of caviomorph schmelzmuster. The results of an earlier study
(Martin, 2004) that detected all three subtypes of multiserial HSB with parallel, acute
angular, and rectangular IPM were fully corroborated by the much larger sample studied
here. It is of particular importance that no plesiomorphic schmelzmuster with pauciserial
HSB was detected in the Santa Rosa rodent fauna. The absence of incisors exhibiting
pauciserial HSB provides strong support for the hypothesis that the founder population of
the South American caviomorphs already possessed a multiserial schmelzmuster (Martin,
1992, 2004). Multiserial HSB with acute angular IPM have been detected in Late Eocene
“Phiomorpha” (Martin, 1993) from Bir el Ater in Algeria (Jaeger et al., 1985), and the
oldest African multiserial HSB with rectangular, plate-like IPM have been reported from
late Eocene/early Oligocene “Phiomorpha” of the Fayum depression (Martin, 1992). In the
North American continent no rodent incisors with multiserial HSB have been found in strata
that were deposited before the emergence of the Panama land bridge and the subsequent
great faunal interchange.
Among the mainly isolated rodent molars from Santa Rosa, Frailey and Campbell
(2004) distinguish six genera with at least nine species in the three families Erethizontidae,
Agoutidae, and Echimyidae. The presence of these families accords with the evidence from
incisor enamel microstructure. The majority of incisors (70%; 15 from the new study and
3 from the former) belong to the plesiomorphic multiserial subtype with parallel to slightly
angular IPM, and 15% (three from the new study and one from the former) have acute
angular IPM in the HSB; both subtypes are present in Erethizontidae and Agoutidae.
Rectangular, plate-like IPM in the PI is a synapomorphy of Octodontoidea (Martin,
1992, 1994) and the occurrence of this enamel type in two incisors of the new sample
corroborates the presence of that superfamily (to which the Echimyidae belong) in the
Santa Rosa local fauna. The more plesiomorphic subtypes of multiserial HSB with parallel
or acute angular IPM are represented by the majority (18) of incisors studied here. If the
six previously studied incisors (Martin, 2004) are taken into consideration, the percentage
of incisors with rectangular IPM (four) is 15% (N = 26). This is not congruent with the
ratio of molars that Frailey and Campbell (2004) attribute to the Echimyidae (about 50% of
the sample). This may be caused by sampling bias or indicate that some of the Santa Rosa
(basal) Octodontoidea retained a more plesiomorphic schmelzmuster. In a broad survey of
caviomorph incisor enamel microstructure, Martin (1992) found in Echimyidae (and other
Octodontoidea) exclusively rectangular IPM in the PI of upper and lower incisors with
Incisor Schmelzmuster Diversity
415
one exception, a lower incisor of Sallamys sp. indet. from the Deseadan of Salla (Bolivia)
which had acute angular IPM (about 45◦ ). Because the Santa Rosa local fauna most probably
predates that of the Oligocene Salla beds, it can be expected that the Santa Rosa rodents
exhibit more plesiomorphic characters. On the basis of the advanced molar morphology of
the Santa Rosan Caviomorpha, Frailey and Campbell (2004) proposed a new hypothesis
for caviomorph origin from an ancient Gondwanan stock that was separated by the breakup
of Gondwanaland. However, this hypothesis is neither supported by molecular evidence
(e.g., Huchon and Douzery, 2001) nor a recent cladistic analysis of early Paleogene rodents
based on dental characters (Marivaux et al., 2004).
CONCLUSION
The presence of exclusively derived schmelzmuster with multiserial HSB and the
absence of plesiomorphic schmelzmuster with pauciserial HSB in the incisors of the putatively oldest South American rodents favor an origin of Caviomorpha and Thryonomyoidea
from a common (probably Asian) ancestry and contradicts an origin from North or Middle
American Ischyromyoidea. The diversity of Santa Rosan rodents and incisor schmelzmuster
can be best explained by either several waves of immigration from Africa by rafting or, in
the case of a single immigration event, a probable pre-Santa Rosan evolutionary history
of rodents in South America. An immigration of (pre-)hystricognath rodents possessing
schmelzmuster with multiserial HSB from Asia via the Bering strait and North America
to South America is unlikely, because no derived incisor schmelzmuster with multiserial
HSB have been found among the well-studied North American Paleogene rodents. The fact
that cheek teeth suggest a higher percentage of octodontoids (about 50%) in the Santa Rosa
fauna than does incisor microstructure (15%), is probably due to a sampling bias or to the
retention of a more plesiomorphic character state in the enamel in some octodontoid taxa
from this fauna.
ACKNOWLEDGMENTS
This paper is dedicated to Bill Clemens in acknowledgment of his enthusiasm and
long-lasting interest in enamel microstructure studies. I thank David Polly for the invitation
to contribute to this Festschrift and his editorial work. K. E. Campbell, Los Angeles County
Museum, provided the rodent incisors from Santa Rosa for study. W. v. Koenigswald
and an anonymous reviewer provided constructive critical comments. M. Bulang-Lörcher
drew Fig. 1 and W. Müller (both Berlin) assisted at the SEM and provided photographical
prints. This study was supported by a Heisenberg grant (Ma 1643/5-2) from the Deutsche
Forschungsgemeinschaft (DFG).
LITERATURE CITED
Boyde, A. (1978). Development of the structure of the enamel on the incisor teeth in the three classical subordinal
groups of the Rodentia. In: Development, Function and Evolution of Teeth, P. M. Butler and K. A. Josey,
eds., pp. 43–58, Academic Press, London.
Campbell, K. E., ed. (in press). The Paleogene Mammalian Fauna of Santa Rosa, Amazonian Peru, Natural History
Museum of Los Angeles County, Science Series 40: 1–163.
Clemens, W. A., and Koenigswald, W. V. (1991). Purgatorius, plesiadapiforms, and evolution of Hunter–Schreger
bands. J. Vertebr. Paleontol. 11(Suppl.): 43A.
416
Martin
Frailey, C. D., and Campbell, K. E. (2004). The Rodents of the Santa Rosa Local Fauna. In: The Paleogene
Mammalian Fauna of Santa Rosa, Amazonian Peru, K. E. Campbell Jr., ed., Natural History Museum of Los
Angeles County, Science Series 40: 71–130.
Houle, A. (1999). The origin of platyrrhines: An evaluation of the Antarctic scenario and the floating island model.
Am. J. Phys. Anthropol. 109: 541–559.
Huchon, D., and Douzery, E. J. P. (2001). From the Old World to the New World: A molecular chronicle of the
phylogeny and biogeography of hystricognath rodents. Mol. Phylogenet. Evol. 20: 238–251.
Hussain, S. T., de Bruijn, H., and Leinders, J. M. (1978). Middle Eocene rodents from the Kala Chitta Range
(Punjab, Pakistan) III. Proc. Kon. Ned. Akad. Wetensch. B 81: 101–112.
Jaeger, J. J., Denys, C., and Coiffait, B. (1985). New Phiomorpha and Anomaluridae from the late Eocene of
North-West Africa: Phylogenetic implications. In: Evolutionary Relationships Among Rodents, W. P. Luckett
and J.-L. Hartenberger, eds., pp. 567–588, Plenum, New York.
Kalthoff, D. C. (2000). Die Schmelzmikrostruktur in den Inzisiven der hamsterartigen Nagetiere und anderer
Myomorpha (Rodentia, Mammalia). Palaeontographica A 259: 1–193.
Koenigswald, W. v. (1980). Schmelzmuster und Morphologie in den Molaren der Arvicolidae (Rodentia). Abh.
senckenberg. naturforsch. Ges. 539: 1–129.
Koenigswald, W. v. (1985). Evolutionary trends in the enamel of rodent incisors. In: Evolutionary Relationships
Among Rodents, W. P. Luckett and J.-L. Hartenberger, eds., pp. 403–422, Plenum, New York.
Koenigswald, W. v. (1997). Brief survey of enamel diversity at the schmelzmuster level in Cenozoic placental
mammals. In: Tooth Enamel Microstructure, W. v. Koenigswald and P. M. Sander, eds., pp. 137–161,
Balkema, Rotterdam.
Koenigswald, W. v. (2004). Enamel microstructure of rodent molars, classification and parallelisms, with a
note on the systematic affiliation of the enigmatic Eocene rodent Protoptychus. J. Mamm. Evol. 11: 127–
142.
Koenigswald, W. v., and Pfretzschner, H. U. (1991). Biomechanics in the enamel of mammalian teeth. In:
Constructional Morphology and Biomechanics, N. Schmidt-Kittler and K. Vogel, eds., pp. 113–125, SpringerVerlag, Berlin.
Koenigswald, W. v., Rensberger, J. M., and Pfretzschner, H. U. (1987). Changes in the tooth enamel of early
Paleocene mammals allowing increased diet diversity. Nature 328: 150–152.
Koenigswald, W. v., and Sander, P. M. (1997). Glossary of terms used for enamel microstructures. In: Tooth
Enamel Microstructure, W. v. Koenigswald and P. M. Sander, eds., pp. 267–280, Balkema, Rotterdam.
Korvenkontio, V. A. (1934). Mikroskopische Untersuchungen an Nagerincisiven, unter Hinweis auf die
Schmelzstruktur der Backenzähne. Ann. Zool. Soc. Zool.-Bot. Fenn. Vanamo 2: 1–274.
Lavocat, R. (1969). La systématique des rongeurs hystricomorphes et la dérive des continents. C. R. Acad. Sci.,
Paris D 269: 1496–1497.
Lavocat, R. (1971). Affinités systématiques des caviomorphes et des phiomorphes et origine africaine des
caviomorphes. An. Acad. Bras. Cienc. 43(Suppl.): 515–522.
Lavocat, R. (1974). The interrelationships between the African and South American rodents and their bearing on
the problem of the origin of South American monkeys. J. Hum. Evol. 3: 323–326.
Lavocat, R. (1976). Rongeurs caviomorphes de l’ Oligocène de Bolivie. II. Rongeurs du bassin Déséadien de
Salla-Luribay. Palaeovertebrata 7: 15–90.
Lehner, J., and Plenk, H. (1936). Die Zähne. In: Handbuch der mikroskopischen Anatomie des Menschen 5/3, W.
v. Möllendorff, ed., pp. 447–708, Springer-Verlag, Berlin.
MacFadden, B., Campbell, K. E., Cifelli, R. L., Siles, O., Johnson, N. M., Naeser, C. W., and Zeitler, P. K. (1985).
Magnetic polarity stratigraphy and mammalian fauna of the Deseadan (late Oligocene-early Miocene) Salla
beds of northern Bolivia. J. Geol. 93: 223–250.
Marivaux, L., Vianey-Liaud, M., and Jaeger, J. J. (2004): High-level phylogeny of early Tertiary rodents: Dental
evidence. Zool. J. Linn. Soc. 142: 105–134.
Marshall, L. G., Cifelli, R. L., Drake, R. E., and Curtis, G. H. (1986). Vertebrate paleontology, geology, and
geochronology of the Tapera de Lopez and Scarrit Pocket, Chubut Province, Argentina. J. Paleontol. 60:
920–951.
Martin, T. (1992). Schmelzmikrostruktur in den Inzisiven alt- und neuweltlicher hystricognather Nagetiere.
Palaeovertebrata, Mém. extra. 1–168.
Martin, T. (1993). Early rodent incisor enamel evolution: Phylogenetic implications. J. Mamm. Evol. 1: 227–253.
Martin, T. (1994). African origin of caviomorph rodents is indicated by incisor enamel microstructure. Paleobiology 20: 5–13.
Martin, T. (1997). Incisor enamel microstructure and systematics in rodents. In: Tooth Enamel Microstructure, W.
v. Koenigswald and P. M. Sander, eds., pp. 163–175, Balkema, Rotterdam.
Martin, T. (1999). Evolution of incisor enamel microstructure in Theridomyidae (Rodentia). J. Vertebr. Paleontol.
19: 550-565.
Martin, T. (2004). Evolution of incisor enamel microstructure in Lagomorpha. J. Vertebr. Paleontol. 24: 411–426.
Incisor Schmelzmuster Diversity
417
Martin, T. (2004). Incisor enamel microstructure of South America’s earliest rodents: Implications for caviomorph
origin and diversification. In: The Paleogene Mammalian Fauna of Santa Rosa, Amazonian Peru, K. E.
Campbell Jr., ed., Natural History Museum of Los Angeles County, Science Series 40: 131–140.
Patterson, B., and Wood, A. E. (1982). Rodents from the Deseadan Oligocene of Bolivia and the relationships of
the Caviomorpha. Bull. Mus. Comp. Zool. 149: 371–543.
Pfretzschner, H. U. (1988). Structural reinforcement and crack propagation in enamel. In: Teeth Revisited:
Proceedings of the VIIth International Symposium on Dental Morphology, Paris 1986, D. E. Russell, J.P. Santoro, and D. Sigogneau-Russell, eds., Mém. Mus. natn. Hist. nat., Paris, (sér. C) 53: 133–144.
Pfretzschner, H. U. (1994). Biomechanik der Schmelzmikrostruktur in den Backenzähnen von Großsäugern.
Palaeontographica A 234: 1–88.
Rensberger, J. M. (1997). Mechanical adaptation in enamel. In: Tooth Enamel Microstructure, W. v. Koenigswald
and P. M. Sander, eds., pp. 237–257, Balkema, Rotterdam.
Simpson, G. G. (1980). Splendid Isolation: The Curious History of South American Mammals, Yale University
Press, New Haven, CT.
Stefen, C. (1997). Differentiations in Hunter–Schreger bands of carnivores. In: Tooth Enamel Microstructure, W.
V. Koenigswald and P. M. Sander, eds., pp. 123–136, Balkema, Rotterdam.
Wahlert, J. H. (1968). Variability of rodent incisor enamel as viewed in thin section, and the microstructure of the
enamel in fossil and Recent rodent groups. Brev. Mus. Comp. Zool. 309: 1–18.
Wahlert, J. H. (1984). Hystricomorphs, the oldest branch of the Rodentia. Ann. N. Y. Acad. Sci. 435: 356–357.
Wahlert, J. H. (1989). The three types of incisor enamel in rodens. In: Papers on Fossil Rodents in Honor of
Albert Elmer Wood, C. C. Black and M. R. Dawson, eds., pp. 7–16, Natural History Museum of Los Angeles
County, Science Series 33.
Wood, A. E. (1981). The origin of the caviomorph rodents from a source in middle America: A clue to the area of
origin of the platyrrhine primates. In: Evolutionary Relationships of the New World Monkeys and Continental
Drift, R. L. Ciochon and A. B. Chiarelli, eds., pp. 79–91, Plenum, New York.
Wood, A. E. (1985). The relationships, origin, and dispersal of the hystricognathous rodents. In: Evolutionary
Relationships Among Rodents, W. P. Luckett and J.-L. Hartenberger, eds., pp. 475–513, Plenum, New York.
Wood, A. E., and Patterson, B. (1959). The rodents of the Deseadan Oligocene of Patagonia and the beginnings
of South American rodent evolution. Bull. Mus. Comp. Zool. 120: 282–428.
Wyss, A. E., Flynn, J. F., Norell, M. A., Swisher, C. C., III, Charrier, R., Novacek, M. J., and McKenna, M. C.
(1993). South America’s earliest rodent and recognition of a new interval of mammalian evolution. Nature
365: 434–437.