enamel microwear in caviomorph rodents

14
ENAMEL MICROWEAR IN CAVIOMORPH RODENTS K. E. BETH TOWNSEND* AND DARIN A. CROFT Department of Anatomy, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA We developed a new data set of enamel microwear for extant caviomorph rodents (i.e., South American hystricognaths) and inferred the diet of an extinct taxon, Neoreomys australis, from data on microwear. To evaluate frequencies of wear features (pits and scratches) in caviomorphs, we employed low-magnification microwear, which has been used successfully by others to distinguish among the diets of ungulates, primates, and sciurid rodents. We developed 3 broad dietary categories for caviomorphs based on behavioral observations reported in the literature: fruit–leaf, fruit–seed, and grass–leaf. Caviomorphs in general all exhibited wear features indicative of processing hard objects (e.g., seed predation, eating hard fruits, and consuming exogenous grit). Among our grass–leaf group, we identified an exogenous-grit subgroup that included fossorial and dust-bathing taxa. We used a discriminant function analysis of wear features to examine post hoc classification of the caviomorph taxa into the 3 dietary categories. Ours is the 1st study to quantify the distribution of microwear features among modern caviomorph rodents; it has the potential to clarify the diets of modern forms that have little behavioral data as well as to infer the diets of extinct species. Key words: caviomorph rodents, diet groups, dietary inference, hypsodonty, microwear, paleodiets During its long period of isolation, the mammalian fauna of South America included numerous endemic lineages and radiations, most of which are now extinct. The caviomorph rodents of South America were arguably the most successful group to survive the stresses of both environmental changes and competition from North American mammals after the Plio–Pleistocene faunal interchange (Flynn and Wyss 1998; Simpson 1980; Webb 1978, 1991). The caviomorphs are a diverse radiation of rodents that fill niches typically occupied by nonrodents (e.g., small forest deer, hyraxes, pygmy hippo- potamus, and rabbits) on other continents (Bourlie `re 1973; Dubost 1988; Mares and Ojeda 1982). Caviomorpha, as a group, mostly includes large neotropical forms; no species weigh ,90 g and the largest living rodent, the capybara (Hydrochoeris) is a caviomorph (Dubost 1988; Mora et al. 2003). Dietary information for living caviomorph rodents is generally limited to isolated reports of feeding behavior for 1 or a few individuals and is not based upon long-term studies that can indicate dietary variation due to seasonality, geography, or other limiting factors. Most caviomorph rodents are generally cryptic, do not live in gregarious social groups, and are difficult to observe in the wild (Dubost 1988). Consequently, unlike most primates and ungulates, which have well-known dietary ecologies, caviomorph rodents have not been categorized into broad dietary groups. Placing these rodents into broad dietary categories allows researchers to assess trophic diversity patterns among caviomorphs and to evaluate trophic structures within their corresponding mammal communities. Establishing a series of ecologically meaningful dietary categories for modern caviomorph rodents also facilitates dietary inference for extinct caviomorphs. Rodents are an important element of late Paleogene and Neogene South American fossil mammal faunas and they can provide important paleoecological and biostratigraphic in- formation (Flynn et al. 2003; Kramarz and Bellosi 2005; Pascual and Ortiz Jaureguizar 1990; Tauber 1997; Vucetich 1986; Vucetich et al. 1999). Extinct caviomorphs have been the subject of numerous taxonomic studies, but there have been few paleobiological studies (Flynn et al. 2003; Walton 1997). These latter studies are hampered by the paucity of natural history and functional data for living taxa (Emmons and Feer 1997; Mares and Ojeda 1982; Rensberger 1978). Crown height (hypsodonty) has been used as a proxy for diet in fossil rodents, suggesting that rodents with tall tooth crowns ate more-abrasive foods than those with shorter crowns (Kay and Madden 1997; Vianney-Liaud 1991; Williams and Kay 2001). Both abrasive diets (grazing) and grit have been shown to play an important role in the evolution of tall crowns for rodents and ungulates; hypsodonty in rodents also has been used to infer paleoenvironments (Croft et al. 2004; Flynn et al. 2003; Janis 1988; Kramarz and Bellosi 2005; Vianney-Liaud 1991; Williams and Kay 2001). Nevertheless, a hypsodont * Correspondent: [email protected] Ó 2008 American Society of Mammalogists www.mammalogy.org Journal of Mammalogy, 89(3):729–742, 2008 729

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ENAMEL MICROWEAR IN CAVIOMORPH RODENTS

K. E. BETH TOWNSEND* AND DARIN A. CROFT

Department of Anatomy, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA

We developed a new data set of enamel microwear for extant caviomorph rodents (i.e., South American

hystricognaths) and inferred the diet of an extinct taxon, Neoreomys australis, from data on microwear. To

evaluate frequencies of wear features (pits and scratches) in caviomorphs, we employed low-magnification

microwear, which has been used successfully by others to distinguish among the diets of ungulates, primates, and

sciurid rodents. We developed 3 broad dietary categories for caviomorphs based on behavioral observations

reported in the literature: fruit–leaf, fruit–seed, and grass–leaf. Caviomorphs in general all exhibited wear features

indicative of processing hard objects (e.g., seed predation, eating hard fruits, and consuming exogenous grit).

Among our grass–leaf group, we identified an exogenous-grit subgroup that included fossorial and dust-bathing

taxa. We used a discriminant function analysis of wear features to examine post hoc classification of the

caviomorph taxa into the 3 dietary categories. Ours is the 1st study to quantify the distribution of microwear

features among modern caviomorph rodents; it has the potential to clarify the diets of modern forms that have

little behavioral data as well as to infer the diets of extinct species.

Key words: caviomorph rodents, diet groups, dietary inference, hypsodonty, microwear, paleodiets

During its long period of isolation, the mammalian fauna of

South America included numerous endemic lineages and

radiations, most of which are now extinct. The caviomorph

rodents of South America were arguably the most successful

group to survive the stresses of both environmental changes

and competition from North American mammals after the

Plio–Pleistocene faunal interchange (Flynn and Wyss 1998;

Simpson 1980; Webb 1978, 1991). The caviomorphs are

a diverse radiation of rodents that fill niches typically occupied

by nonrodents (e.g., small forest deer, hyraxes, pygmy hippo-

potamus, and rabbits) on other continents (Bourliere 1973;

Dubost 1988; Mares and Ojeda 1982). Caviomorpha, as a group,

mostly includes large neotropical forms; no species weigh ,90 g

and the largest living rodent, the capybara (Hydrochoeris) is

a caviomorph (Dubost 1988; Mora et al. 2003).

Dietary information for living caviomorph rodents is

generally limited to isolated reports of feeding behavior for 1

or a few individuals and is not based upon long-term studies

that can indicate dietary variation due to seasonality,

geography, or other limiting factors. Most caviomorph rodents

are generally cryptic, do not live in gregarious social groups,

and are difficult to observe in the wild (Dubost 1988).

Consequently, unlike most primates and ungulates, which have

well-known dietary ecologies, caviomorph rodents have not

been categorized into broad dietary groups. Placing these

rodents into broad dietary categories allows researchers to

assess trophic diversity patterns among caviomorphs and to

evaluate trophic structures within their corresponding mammal

communities. Establishing a series of ecologically meaningful

dietary categories for modern caviomorph rodents also

facilitates dietary inference for extinct caviomorphs.

Rodents are an important element of late Paleogene and

Neogene South American fossil mammal faunas and they can

provide important paleoecological and biostratigraphic in-

formation (Flynn et al. 2003; Kramarz and Bellosi 2005;

Pascual and Ortiz Jaureguizar 1990; Tauber 1997; Vucetich

1986; Vucetich et al. 1999). Extinct caviomorphs have been the

subject of numerous taxonomic studies, but there have been

few paleobiological studies (Flynn et al. 2003; Walton 1997).

These latter studies are hampered by the paucity of natural

history and functional data for living taxa (Emmons and Feer

1997; Mares and Ojeda 1982; Rensberger 1978).

Crown height (hypsodonty) has been used as a proxy for diet

in fossil rodents, suggesting that rodents with tall tooth crowns

ate more-abrasive foods than those with shorter crowns (Kay

and Madden 1997; Vianney-Liaud 1991; Williams and Kay

2001). Both abrasive diets (grazing) and grit have been shown

to play an important role in the evolution of tall crowns for

rodents and ungulates; hypsodonty in rodents also has been

used to infer paleoenvironments (Croft et al. 2004; Flynn et al.

2003; Janis 1988; Kramarz and Bellosi 2005; Vianney-Liaud

1991; Williams and Kay 2001). Nevertheless, a hypsodont

* Correspondent: [email protected]

� 2008 American Society of Mammalogistswww.mammalogy.org

Journal of Mammalogy, 89(3):729–742, 2008

729

dentition does not necessarily restrict an animal to eating

abrasive foods. In North American Neogene llamas and South

American Miocene notoungulates, the evolution of hypsodonty

apparently widened the dietary niches of these animals,

allowing for a more generalized diet that could accommodate

seasonal changes in food availability (Feranec 2003; Townsend

and Croft 2005, 2008).

The aim of this study was to use dental evidence from

microwear to categorize caviomorph rodents into broad dietary

categories. Then, using microwear data collected from the teeth

of extinct rodents, we can infer their diets by placing them in 1

of the dietary categories developed here. Because the relation-

ship between hypsodonty and diet in rodents is unclear, we

chose to use analysis of enamel microwear. Microwear studies

evaluate the pits and scratches left on the enamel surface of

teeth by the food an animal eats. Numerous methods have been

developed to evaluate microwear, primarily with the objective

of assessing the diets of extinct mammals (e.g., Solounias and

Semprebon 2002; Teaford et al. 1996; Ungar 1998; Walker

et al. 1978). Because long-term socioecological studies on

caviomorphs are rare, the evaluation of enamel microwear also

has the potential to confirm isolated reports of dietary behavior.

In this study, we strive to characterize the diets of a set of

extant caviomorph rodents by assessing enamel microwear

features of the molar teeth. We 1st evaluated ecological and

behavioral data for a group of extant caviomorphs and then we

generated broad dietary categories that would be useful for

classifying fossil rodent diets. We then used a low-magnifica-

tion microwear method to obtain data on microwear, and we

evaluated whether microwear features covary with the dietary

categories (using univariate and multivariate statistical tech-

niques). Finally, we used this data set to infer the diet of a fossil

rodent and we evaluated its use for further paleodietary

inference.

MATERIALS AND METHODS

Diets of rodents.—Rodents exhibit a range of dietary habits;

some are specialized herbivores, whereas others eat insects,

fish, and small land vertebrates, and many are considered

omnivorous (Eisenberg and Redford 1999; Emmons and Feer

1997; Nowak 1999). Among caviomorph rodents, herbivory

appears to be the dominant feeding strategy, although some

forms will eat small amounts of animal matter, mainly insects

(Emmons 1982; Henry 1999; Herskovitz 1972; Mares and

Ojeda 1982; Woods 1982).

Some caviomorph genera are particularly speciose (e.g.,

spiny rats [Proechimys]) and lack precise dietary data for all

constituent species. In Table 1, we have compiled dietary data

for the rodent taxa evaluated in this study. Most of these data

are for genera because data for species were not available.

These data were used to construct broad dietary categories that

were applicable to modern and fossil rodents. Some taxa are

fossorial (tuco-tucos [Ctenomys]) and others are known to bury

their food in what is known as ‘‘scatter-hoarding’’ behavior

(agoutis [Dasyprocta] and pacas [Cuniculus]); these species

therefore may consume exogenous grit. Because microwear

from grit could skew our dietary interpretations, we took

substrate use into account when evaluating the data on

microwear. When data were available, we considered seasonal

changes in diet as significant criteria for assigning taxa to

dietary categories for analysis.

We developed 3 broad dietary categories based primarily on

reports of observed dietary behavior in wild caviomorphs:

fruit–leaf, fruit–seed, and grass–leaf consumers. Of these

categories, the fruit–leaf and fruit–seed categories represent

a continuum of seed consumption or predation. Leaves, soft

fruit pulp, seeds, bark, twigs, and animal material comprise the

diets of taxa in the fruit–leaf group (Emmons and Feer 1997;

Woods et al. 1992; see Table 1). Taxa in the fruit–seed group

feed mainly on seeds and rely on seeds as a major food source,

although they are known to eat other fruits and plant parts as

well (Emmons 1982; Henry 1997; Streilein 1982). Taxa in the

grass–leaf group ate mainly grasses and leafy plants.

Samples and variables.—Fourteen species of caviomorph

rodents were evaluated in this study, 13 extant and 1 extinct

(Table 1). The extant sample includes 97 individuals from 9

families, all from the collections of the Carnegie Museum of

Natural History, Pittsburgh, Pennsylvania. Our sample of the

extinct dasyproctid Neoreomys comes from the late early

Miocene (16.3–17.5 million years ago [mya]—Flynn and

Swisher 1995) Santa Cruz Formation of Patagonian Argentina;

specimens were examined at The Field Museum, Chicago,

Illinois. We limited the sample of extant rodents to taxa with

relatively well-known diets; some of the ecological data are

from individuals in captivity, but most of the dietary data are

from field observations of feeding behaviors, stomach contents

of wild-caught individuals, or fecal samples. We limited the

sample to individuals in which M2 has erupted.

Occlusal patterns.—A wide variety of occlusal patterns are

represented in this sample. Hydrochoeris and Cavia have

laminar plates that are joined by cement (Fig. 1A; Hillson

1986). Chinchilla and Lagidium exhibit tall plates of enamel

that are not joined by cement (Hillson 1986). Ctenomys has

a crown with a single enamel ring outlining the occlusal surface

(Fig. 1B). Some caviomorphs, including Proechimys, Thrich-omys, and Myocastor, have occlusal patterns formed by

infoldings of enamel from the sides of the crown, similar to

what is seen in porcupines, Coendou (Fig. 1C; Hillson 1986).

Because of the difference in occlusal patterns, the region of

interest for microwear varied somewhat with taxon (see below).

Previous studies have successfully compared microwear on

teeth with different occlusal morphologies (Green et al. 2005;

Solounias and Semprebon 2002) and we therefore do not think

this poses a problem for analysis of microwear in rodents.

Data on microwear.—Data were collected from upper 2nd

molars, which were primarily used to compile the data set on

extant taxa. In the case of Ctenomys, the lower 2nd molar was

used when upper molars were not available; the lingual portion

of the single enamel band was read.

Studies of microwear in primates and ungulates have shown

that the dietary signal is consistent across both maxillary and

mandibular 2nd molars (Green et al. 2005; Semprebon et al.

2004). Although these studies did not include rodents, the cheek

730 JOURNAL OF MAMMALOGY Vol. 89, No. 3

toothrow of extant rodents is effectively homodont, especially in

caviomorphs, with minor differences in size among the molars

and single premolar (if present). This suggests that the functional

differences among these elements would not obscure or skew any

dietary signal on any particular tooth. Both mandibular and

maxillary specimens were used for the extinct Neoreomys and

data were collected on the anteroloph–posteroloph region of the

upper molars and the anterolophid–posterolophid region of the

lower molars. Clear epoxy casts were made of the occlusal

surfaces for both the extant and extinct caviomorphs and

microwear features were read from these casts.

All microwear features were read in a 0.3-mm2 standard area

at 70� magnification using a Leica MZ 12.5 light microscope

(Microscopy & Scientific Instruments, Bannockburn, Illinois).

The standard area or region of interest was delimited digitally

on a computer screen based on measurements made using

a stage micrometer. The imaging software Q-Capture version

2.7.3 (QImaging, Surrey, British Columbia, Canada) was used

to digitize the tooth images using a 5-megapixel camera

(QImaging Micropublisher 5.0 RTV; QImaging) and to transfer

the 70�-magnified image to the computer monitor for

assessment. Microwear features were counted on the computer

screen in the region of interest. Because of the small size of

rodent molars, the region of interest in this study was smaller

and the magnification was greater than that used in previous

low-magnification studies of microwear on samples of modern

TABLE 1.—Classification, diet, and substrate use of caviomorph rodents evaluated in this study. Taxonomy follows Huchon and Douzery (2001)

and McKenna and Bell (1997). The fossil taxon is indicated by an asterisk (*).

Taxon Diet

Substrate and food

storage and acquisition Dietary class Dietary referencea

Order Rodentia

Suborder Hystricognathi

Infraorder Caviomorpha

Erethizontidae

Coendou Seeds, herbivore,

frugivore

Arboreal Fruit�leaf 3, 8, 10, 16, 18, 21

Cavioidea

Agoutidae

Cuniculus paca Fruit, seeds, browse,

leaves

Terrestrial;

scatter-horde

Fruit�leaf 3, 6, 7, 8, 10, 14, 17, 18, 19, 22, 24

Dasyproctidae

Dasyprocta Fruits, seeds, nuts,

leaves

Terrestrial;

scatter-horde

Fruit�leaf 3, 4, 7, 8, 10, 18

Neoreomys* Unknown Unknown

Caviidae

Cavia Grasses, grass

inflorescences

Terrestrial; construct

surface runways in soil

Grass�leaf 7, 8, 17, 22

Hydrochoeridae

Hydrochoeris Grasses, aquatic

plants

Semiaquatic Grass�leaf 3, 7, 8, 10, 15, 16, 17

Octodontoidea

Ctenomyidae

Ctenomys Grasses, stems, roots,

bulbs, bark, leaves

Fossorial Grass�leaf 2, 3, 13, 20, 22, 23, 26

Echimyidae

Proechimys Fruits, nuts Terrestrial Fruit�seed 1, 3, 7, 9, 10, 12, 26

Thrichomys Seeds, fruits, nuts Fruit�seed 3, 17, 22, 26

Myocastoridae

Myocastor Grass, stems, leaves,

roots, bark, aquatic

vegetation

Semiaquatic Fruit�leaf 3, 8, 15, 27

Chinchilloidea

Chinchillidae

Chinchilla Grass, any vegetation Terrestrial; burrows Grass�leaf 3, 4, 25

Lagidium Grasses, herbivore Terrestrial Grass�leaf 5, 8, 11, 15, 17, 21, 22

a References: 1) Adler 2000; 2) Altuna et al. 1998; 3) Arends and McNab 2001; 4) Cortes et al. 2002a; 5) Cortes et al. 2002b; 6) Dubost et al. 2005; 7) Eisenberg 1989; 8) Eisenberg and

Redford 1999; 9) Emmons 1982; 10) Emmons and Feer 1997; 11) Galende et al. 1998; 12) Henry 1997; 13) Justo et al. 2003; 14) Laska et al. 2003; 15) Mares et al. 1989; 16) Mones and

Ojasti 1986; 17) Nowak 1999; 18) Peres 1999; 19) Perez 1992; 20) Puig et al. 1999; 21) Puig et al. 1998; 22) Redford and Eisenberg 1992; 23) Rosi et al. 2003; 24) Smythe 1986; 25)

Sportno et al. 2004; 26) Streilien 1982; 27) Woods et al. 1992.

June 2008 731TOWNSEND AND CROFT—ENAMEL MICROWEAR IN CAVIOMORPHS

and fossil ungulates and primates (Godfrey et al. 2004, 2005;

Semprebon et al. 2004; Solounias and Semprebon 2002;

Townsend and Croft 2005). We also wanted to maintain

a measurement standard that was comparable to similar studies

of microwear on squirrels (Nelson et al. 2005).

Variables.—Microwear features were counted twice, once

on the anteroloph or anterolophid and again on the posteroloph

or posterolophid (Fig. 1). Seven microwear features were

evaluated for each specimen: number of small pits; number of

scratches; number of large pits; number of cross scratches;

scratch texture (fine, coarse, mixed, or hypercoarse); number

of puncture pits; and number of gouges (Fig. 2). The size of

puncture pits was also recorded (small, medium, or large).

When an enamel plate or ring was read instead, 2 areas along

the same enamel plate were read. Scratch textures were coded

as fine, coarse, a mixture of fine and coarse, or hypercoarse. In

previous studies evaluating ungulates and primates, small pits

were combined with large and puncture pits for a ‘‘total pit’’count that was averaged for comparison across taxa (Godfrey

et al. 2004; Solounias and Semprebon 2002). We chose to

evaluate the small pits separately from other types of pits in

order to assess their utility as a dietary microwear feature.

Previous authors have developed 2 summary terms to

describe microwear signatures, coarse and fine wear, that have

been used to characterize the distribution of wear features for

a taxon (Godfrey et al. 2004; Green et al. 2005; Semprebon

et al. 2004; Solounias and Semprebon 2002). Features that

leave rough impressions on the enamel, such as large pits,

puncture pits, coarse scratches, and gouges, generally define

coarse wear. In contrast, fine scratches, few to no large pits,

gouges, and puncture pits define a fine wear signature. Hard-

object feeding or processing is another term that has been used

to describe both ungulate and primate seed predators; this term

implies coarse wear, and is characterized by a predominance of

puncture pits (Godfrey et al. 2004). These terms are used

throughout the remainder of this report to describe general

trends in microwear signatures.

Analyses.—Graphical evaluation and univariate and multi-

variate statistical analyses were used to assess the correlation

between microwear features and diet. The 1st series of analyses

were used to evaluate consistency in microwear variables

among taxa within dietary groups. Further testing explored

differences in microwear features among the 3 dietary groups.

FIG. 1.—Variation in occlusal morphology of 2nd upper molars in

3 representative caviomorphs: A) Cavia, B) Ctenomys, and C)

generalized erethizontid molar, adapted from Candela (2004). Dashed

boxes indicate areas where microwear was read on each type of

occlusal morphology. For all taxa with lophate teeth (Cuniculus,

Dasyprocta, Coendou, Proechimys, Thrichomys, and Myocastor) the

protocone region of the anteroloph and the hypocone region of the

posteroloph were read. In Hydrochoeris, Cavia, Chinchilla, and

Lagidium data were collected along the buccolingual surface of the

enamel plate. In Ctenomys, data were collected on the lingual edge of

the tooth. In all illustrations, the thick line represents the enamel band.

FIG. 2.—Digital photographs (taken at 70� magnification) of caviomorph microwear. A) Proechimys guyannensis, B) Hydrochoeris,

C) Dasyprocta, D) Cavia, E) Ctenomys, and F) Neoreomys (extinct). Microwear features illustrated on this figure are as follows: G ¼ gouge,

PP ¼ puncture pit, SPP ¼ small puncture pit, FS ¼ fine scratch, CS ¼ coarse scratch, SP ¼ small pit, HC ¼ hypercoarse scratch.

732 JOURNAL OF MAMMALOGY Vol. 89, No. 3

Graphs were generated and statistical tests were run on SPSS

11 for Mac OS X (SPSS, Chicago, Illinois).

Two types of variables were evaluated: averaged individual

data (e.g., average number of small pits for each specimen of

Cavia) and averaged individual per taxon data (e.g., average

number of small pits for all individuals of the taxon Cavia).

Averaged individual data and individual coded scratch textures

were used in the 1-way analysis of variance (ANOVA), Mann–

Whitney U-test, and principal component analysis (PCA). The

averaged individual per taxon data were used for all other

analyses. The individual coded scratch textures were evaluated

as percentages per taxon for subsequent evaluation in univar-

iate and discriminant analyses.

We performed a 1-way ANOVA to evaluate whether vari-

able means were significantly different among the 13 extant

caviomorph taxa. We used the Mann–Whitney U-statistic to

assess if the scratch texture data differed significantly among

taxa within the 3 dietary groups. In order to control the prob-

ability of making a type I error with the Mann–Whitney Upairwise comparisons, we performed a Dunn–Sidak correction

to reduce the experimentwise error rate.

We performed a PCA to explore variation in microwear

features among extant caviomorphs. An unrotated PCA of the

trait correlation matrix was run for microwear variables of all

individuals in the data set on extant caviomorphs. This allowed

us to identify the dominant microwear features in the data and

assess the dietary spectrum occupied by the extant rodents.

A discriminant function analysis of the newly defined dietary

groups was run to classify individuals into broad dietary groups

(fruit–leaf, fruit–seed, and grass–leaf) and to generate a dis-

criminant model that could be used to reconstruct the diets of

extinct caviomorphs. The goal of this analysis was to determine

those microwear features that characterize broad dietary cate-

gories and to evaluate the placement of some taxa into those

categories based upon their scores from the model. Using

a jackknifed classification method to evaluate the discriminant

model, we tested whether the modern caviomorph taxa were

correctly classified into their dietary groups. We ran 13 separate

discriminant analyses where 1 taxon was treated as an un-

known and was then subsequently classified into a dietary

group by the model. The diet of the extinct rodent Neoreomyswas reconstructed by treating the extinct taxon as an unknown

in the analysis. The microwear profile of Neoreomys was gener-

ated in the same way as for extant caviomorphs and was based

on both the mean and percentage scores of the individuals.

RESULTS

Overview of data on microwear.—Microwear features

visible in the region of interest included fine, coarse, and

hypercoarse scratches, small pits, gouges, large pits, and

puncture pits of large and small size (Fig. 2). The caviomorphs

overlapped each other in the average number of small pits;

Cuniculus, Chinchilla, Ctenomys, and Lagidium exhibited the

most small pits and Coendou exhibited the fewest (Table 2;

Fig. 3). There was also some degree of overlap in the average

number of scratches among the caviomorphs, although Hydro-

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June 2008 733TOWNSEND AND CROFT—ENAMEL MICROWEAR IN CAVIOMORPHS

choeris, Cavia, and Lagidium exhibited very high average

numbers of scratches. Microwear features typical of coarse

wear such as gouges, large pits, and puncture pits were present

in high numbers among most caviomorphs, but Cavia,

Lagidium, and Proechimys brevicauda lacked large puncture

pits (Fig. 3). All taxa exhibited both fine and coarse scratch

textures except Lagidium, which displayed only coarse

scratches. Three taxa, Thrichomys, P. brevicauda, and

Ctenomys, had individuals that displayed hypercoarse scratch

textures. A bivariate plot of scratches versus pits (Fig. 4) shows

that scratches (x-axis) are effective in separating the frugivores

from 3 of the grass–leaf consumers (Hydrochoeris, Cavia, and

Lagidium). Average number of small pits (y axis) did not

discriminate along a dietary spectrum; Ctenomys, Chinchilla,

Cuniculus, and Lagidium had the highest frequencies of small

pits.

Analysis of variance and Mann–Whitney U-test.—The

1-way ANOVAs showed significant differences among all taxa

for average number of small pits, scratches, cross scratches,

large pits, large puncture pits, small puncture pits, and gouges

(Table 2). The average number of scratches per individual per

taxon showed the greatest differences among taxa (P ,

0.0001). Because these variables were significantly different

among taxa of different diets, we evaluated their diagnostic

utility further via multivariate analyses below.

Scratch textures were evaluated using a nonparametric test

for categorical data. The Mann–Whitney U-test for differences

in scratch textures between pairs of taxa in the 3 broad dietary

groups showed no significant differences among taxa in the

fruit–seed and fruit–leaf groups (Table 3). There was

a significant difference in scratch textures between 2 pairs of

taxa in the grass–leaf group: Hydrochoeris–Lagidium and

Cavia–Lagidium. Using the Dunn–Sidak Bonferroni method

(Sokal and Rohlf 1995) for correcting experimentwise type 1

error, these comparisons were shown to be not significant.

Scratch texture was used as a variable for subsequent analyses

because it proved homogenous within the other dietary groups.

Principal component analysis.—Using PCA, we evaluated

the dominant microwear signal in the data. Four components

explained 67.2% of the original variation in the data. The 1st

component (PC1) explained 25.3% of the variation, almost

one-third of the variance (Fig. 5). The 2nd through 4th

components each explained between 16% and 12% of the

variation. We used the 1st component axis to evaluate the

diagnostic utility of the microwear features. Taxa with high

positive scores on this axis have a coarse-wear signature

including (in decreasing order of importance) many large pits,

many large puncture pits, and many gouges (Table 4; Fig. 5).

Species with high negative scores have fewer coarse-wear

features but have more scratches overall, more cross scratches,

and more scratches of coarse texture (Table 4; Fig. 5). Of the 8

variables used in this analysis, 6 had relatively high loadings

on PC1, and 2—average number of small pits per taxon and

average number of small puncture pits per taxon—had

extremely low loadings. This axis describes a dietary spectrum

from hard-object feeders (at the high positive end) to grass

consumers and folivores (near the negative end; Fig. 5). On the

FIG. 3.—Box plots illustrating the distribution of the 6 quantitative

microwear variables among the 3 dietary groups. The plots show the

median, interquartile range, and outliers for each taxon. Dark gray

bars represent the fruit–seed group, white bars represent the fruit–

leaf group, and light gray bars represent the grass–leaf group. Outliers

are denoted by asterisks and open circles. The x-axis (taxon) for

each graph is coded: T ¼ Thrichomys, Pg ¼ Proechimys guyannensis,

Pc¼ P. cuvieri, Pb¼ P. brevicauda, M¼Myocastor, Ag¼Cuniculus,

D ¼ Dasyprocta, Co ¼ Coendou, L ¼ Lagidium, H ¼ Hydrochoeris,

Ca ¼ Cavia, Ct ¼ Ctenomys, Ch ¼ Chinchilla. The y axis for all

variables represents the average number of that variable per taxon.

FIG. 4.—Bivariate plot of the average number of scratches versus

pits. Note that the grazing subgroup (Hydrochoeris, Cavia, and

Lagidium) separates from the frugivores and exogenous-grit subgroup

(Ctenomys and Chinchilla) along the scratch axis. Filled circles

represent the fruit–seed group, open circles represent the fruit–leaf

group, and diamonds represent the grass–leaf group.

734 JOURNAL OF MAMMALOGY Vol. 89, No. 3

positive end of the spectrum the differences among scores is

not as great. The 2nd component (PC2) explained 15.58% of

the variation in the data; all variables loaded positively and

contrasted little in their loadings (Fig. 5). The remaining

components, PC3 and PC4, did not show strong contrasts

among microwear variables.

Discriminant function analysis.—We applied discriminant

function analysis to the data set to evaluate whether the

TA

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FIG. 5.—Principal component analysis of extant caviomorph

rodents based on the correlation matrix of 8 variables and 97 cases.

A) Plot of principal component 2 (PC2) versus PC1; most individuals

toward group interiors were removed to provide a clearer view of the

dietary groups. Note the separation of the fruit–leaf (open circle) and

fruit–seed (filled circles) groups from the grazing subgroup (open

diamonds, dotted line). Note also the position of the exogenous-grit

subgroup (filled diamonds, dotted line). The grazers have more

scratches and cross scratches, whereas the other taxa are characterized

by more coarse-wear features. B) Loadings on PC1; note the contrast

between scratch variables and pit variables. C) Loadings on PC2; note

the clustering of most of variables toward the positive end.

June 2008 735TOWNSEND AND CROFT—ENAMEL MICROWEAR IN CAVIOMORPHS

variables could be used to classify caviomorphs by diet. We

removed the variable ‘‘average number of small puncture pits’’because only 7 individuals in the data set exhibited small

puncture pits and this variable did not differ among the dietary

groups in previous analyses. Two canonical discriminant

functions captured 100% of the variation in the data; chi-

square tests of the significance of variance explained by the 1st

function (DF1; using Wilks’ lambda) yielded P-values , 0.05.

DF1 explained 99.4% of the variance in the data and its axis

separated the 2 groups of frugivores from the grass–leaf group

(Fig. 6). The 2nd function (DF2) separated the fruit–leaf group

from both the grass–leaf and fruit–seed groups (Fig. 6). There

was no overlap in the group centroids or in the taxa among the

3 groups, as illustrated by a 100% post hoc classification of the

original cases (Fig. 6). The jackknife classification procedure

resulted in no misclassifications of individual taxa into their

dietary groups (Table 5).

The variable ‘‘average number of scratches’’ had the largest

absolute correlation with DF1 (loading negatively), as did

average number of cross scratches, percentage of fine scratches,

percentage of coarse scratches, and average number of small

pits. Taxa with high positive scores on DF1 had more puncture

pits, gouges, large pits, hypercoarse scratches, and mixed

scratches (Fig. 5; Table 5). Taxa that loaded highest on this

function were the frugivores, with the fruit–seed consumers

(Proechimys and Thrichomys) having the highest scores. The

fruit–leaf consumers had lower positive scores because of

fewer ‘‘coarse-wear’’ features and more scratches of different

textures. DF1 separated grass–leaf consumers from the

frugivores by higher frequencies of small pits, scratches of

all kinds, and scratches with coarser texture. Puncture pits and

gouges were more frequent among frugivores than the grass–

leaf consumers. DF2 separated the fruit–leaf group from the

grass–leaf and fruit–seed groups. In contrast to the fruit–leaf

group, the taxa in the grass–leaf and fruit–seed groups had

more scratch features. The grass–leaf group has the highest

frequency of scratch features of all of the caviomorph taxa. The

conditional probabilities for each taxon being placed in the

correct group were all quite high and the posterior probability

for each taxon was 1.00 (Appendix I); this is also indicated by

the 100% post hoc classification success of the model.

The model classified the fossil taxon, Neoreomys, into the

fruit–seed group, with a 0.00 conditional probability of that

TABLE 4.—Dominant microwear signal, principal component

analysis (PCA), with taxa arranged by increasing score on PC1.

PCA scores are mean (SE).

Taxon PCA axis 1 scores Diet group

Cavia �1.25 (0.29) Grass�leaf

Lagidium �1.19 (0.14) Grass�leaf

Hydrochoeris �0.96 (0.13) Grass�leaf

Proechimys cuvieri �0.23 (0.19) Fruit�seed

P. guyannensis 0.01 (0.15) Fruit�seed

Chinchilla 0.02 (0.23) Grass�leaf

P. brevicauda 0.03 (0.24) Fruit�seed

Dasyprocta 0.05 (0.38) Fruit�leaf

Cuniculus 0.14 (0.23) Fruit�leaf

Myocastor 0.25 (0.53) Fruit�leaf

Coendou 0.59 (0.25) Fruit�leaf

Ctenomys 0.67 (0.26) Grass�leaf

Thrichomys 0.85 (0.48) Fruit�seed

FIG. 6.—Plot of the first 2 discriminant functions from an analysis

of diets of caviomorphs using microwear features. The model classified

all extant taxa by dietary group correctly. The fossil rodent Neoreomysaustralis plots between the fruit–seed and fruit–leaf groups.

TABLE 5.—Jackknifed classification matrix and discriminant scores

of extant caviomorph taxa on the 1st discriminant function. F-L ¼fruit–leaf, F-S ¼ fruit–seed, G-L ¼ grass–leaf. The score for the Santa

Cruz fossil rodent Neoreomys is included with the classification

provided by the model.

F-L F-S G-L % correct

F-L 4 0 0 100

F-S 0 4 0 100

G-L 0 0 5 100

Total 4 4 5 13

Taxon Discriminant score Dietary category

Hydrochoeris �17.99571 Grass�leaf

Ctenomys �17.73593 Grass�leaf

Lagidium �17.36286 Grass�leaf

Chinchilla �16.83331 Grass�leaf

Cavia �15.88239 Grass�leaf

Cuniculus 5.15392 Fruit�leaf

Myocastor 5.34501 Fruit�leaf

Dasyprocta 5.40925 Fruit�leaf

Coendou 5.54652 Fruit�leaf

Proechimys cuvieri 13.96034 Fruit�leaf

P. brevicauda 16.03833 Fruit�seed

Thrichomys 16.86027 Fruit�seed

P. guyannensis 17.49657 Fruit�seed

Neoreomys 27.52555 Fruit�seeda

a The model classified Neoreomys into the fruit–seed group with a 0.00 probability.

736 JOURNAL OF MAMMALOGY Vol. 89, No. 3

score being placed in the fruit–seed group. Neoreomys fell out

beyond the extant seed consumers on DF1 because of a very

high positive score on that function (Table 5).

DISCUSSION

The classic microwear variables ‘‘average pits’’ and

‘‘average number of scratches’’ did not provide the stark

dietary signal apparent in studies of microwear in ungulates and

primates (e.g., the traditional browser and grazer split among

ungulates or the ‘‘trophic triangle’’ seen in primates [Fig. 4;

Godfrey et al. 2004; Solounias and Semprebon 2002]). The

caviomorph rodents are unusual in that the average small pit

count was high (.40 small pits) for some taxa in the grass–leaf

category; in other groups, grass-consuming herbivores tend to

have lower pit counts (Godfrey et al. 2004; Semprebon et al.

2004; Solounias and Semprebon 2002). The discriminant

function analysis showed that the 3 groups are internally

consistent, although some taxa stood out within each group.

Detailed descriptions of the microwear profiles associated with

each dietary group are given in Appendix II.

The differences in low-magnification microwear patterns are

subtler among caviomorph rodents than those reported for

ungulates and primates. In these other groups, the dominant

presence of either pits or scratches allows for easy distinction

among frugivores, folivores, and hard-object specialists or

between browsers and grazers (Godfrey et al. 2004; Green et al.

2005; Semprebon et al. 2004; Solounias and Semprebon 2002).

Small pit and total scratch frequencies did separate frugivorous

caviomorphs from grazing ones in a bivariate plot, but detailed

dietary behaviors could be discerned only by evaluating

frequencies of other coarse-wear features (e.g., puncture pits

and large pits).

Presumed diets of extant caviomorphs were well supported

by the microwear data and the discriminant model. Lagidium,

Cavia, and Hydrochoeris are all grazers; these 3 taxa were

characterized by microwear profiles with the highest scratch

frequencies. Viscachas (Lagidium) have a diet dominated by

grasses (89%—Puig et al. 1998). Capybaras (Hydrochoeris)

are committed grazers that requires open grassy fields for

feeding (Mones and Ojasti 1986). Cavies (Cavia) are reported

to be grazers as well, but this taxon will eat grass flowers; these

have small seeds, likely accounting for the small puncture pits

(Table 2; Eisenberg 1989; Eisenberg and Redford 1999;

Nowak 1999; Redford and Eisenberg 1992). Cavia spends

time close to the ground and is known to tunnel through the

uppermost layers of soft soil (Eisenberg 1989; Eisenberg and

Redford 1999; Nowak 1999; Redford and Eisenberg 1992); it

would therefore be expected to exhibit some kind of coarse-

wear signal caused by ingested exogenous grit. The grazing

features apparently masked any signal from exogenous grit

because Cavia exhibited few coarse-wear features such as large

pits, gouges, and small puncture pits. Tuco-tucos (Ctenomys)

are reported to consume as much as 80% grasses (Justo et al.

2003; Rosi et al. 2003). Tuco-tucos had a microwear profile

with the highest small pit counts of all caviomorphs sampled,

very few scratches, very few cross scratches, high numbers of

large pits, and many gouges; all of these features suggest hard-

object processing. Unlike primates or duikers where ‘‘hard-

object processing’’ indicates seed predation or eating fruits with

tough pericarps, it is likely that the tuco-tuco is consuming

exogenous grit during burrowing because it is known to

‘‘chisel-tooth dig’’ (i.e., excavate with the incisors) in hard soils

(Mora et al. 2003; Spotorno et al. 2004; Vassallo 1998). Food

cleaning has been reported for tuco-tucos, where little soil has

been found in stomach contents (Altuna et al. 1998), but

examination of our data suggests that much exogenous grit is

consumed.

The microwear of the 4 individuals of Chinchilla lanigeraevaluated in this study did not suggest a grass-dominated diet,

but pointed toward hard-object processing. It has been reported

that chinchillas show no interest in eating seeds or pods and

few puncture pits were observed in this taxon, so it is unlikely

that we are getting a signal indicating seed predation (Cortes

et al. 2002a). We interpret this microwear as an indicator of

exogenous grit because chinchillas are known to burrow and

dust bathe (Spotorno et al. 2004). C. lanigera is reported to

have a seasonally varied diet (Cortes et al. 2002a); it is

therefore possible that the specimens examined were collected

during a period when fewer grasses and more soft plants and

fruits were being consumed.

Of the fruit–leaf consumers, Coendou has the highest degree

of hard-object processing; it is reported to eat seeds, twigs, and

bark, along with fruits and leaves (Emmons and Feer 1997).

Cuniculus exhibited a microwear profile consistent with the

frugivore pattern in primates (Godfrey et al. 2004; Semprebon

et al. 2004). Because pacas are forest-floor foragers and are

known to consume tubers, the gouging seen in the enamel may

be an exogenous-grit signal. Pacas do eat seeds, but cannot

open them with their incisors and will only eat the softer inner

parts of seeds that have been pried open by other animals

(Perez 1992). Primate frugivores that are seed predators tend to

have more coarse-wear features such as hypercoarse scratches

and, of particular importance, puncture pits (Semprebon et al.

2004). Cuniculus does have a large number of coarse scratches,

but it has no hypercoarse scratches and very few puncture pits

(Table 2). Coypus (Myocastor) spend a great deal of time in the

water and burrow into the banks of rivers and other waterways

(Woods et al. 1992). The coarse-wear features seen on the teeth

of the coypus are not likely indicative of an exogenous-grit

signal and probably indicate a slight degree of hard-object

processing (Woods et al. 1992). Coypus have been reported to

eat bark along with leaves, roots, and stems and are considered

generalists with tendencies towards folivory (Woods et al.

1992). The folivore signal was not as strong in the coypus as

what was seen in the grass–leaf consumers and was likely

masked by the coarse wear found on the occlusal surface.

Cuniculuss (Dasyprocta) are known hard-object specialists that

use their strong anterior dentition to open seeds and tough fruits

(Henry 1999). The microwear profile for agoutis had very few

puncture pits (Table 2) but it did exhibit high frequencies of

coarse and mixed scratches, as would be expected for a primate

or ungulate seed predator. These differences in the seed-

predation signal were likely due to differences in seed

June 2008 737TOWNSEND AND CROFT—ENAMEL MICROWEAR IN CAVIOMORPHS

processing: primates and ungulates open tough fruits, nuts, and

seeds with their molar teeth, whereas Dasyprocta uses the

incisors (Henry 1999). In the fruit–seed group, Proechimys(spiny rats) and Thrichomys (punares) all are known seed

predators and we expected to see a strong hard-object pro-

cessing signal (Streilein 1982). Fecal samples of P. brevicaudaindicate that it eats seeds, stems, fruit parts, and fungus

(Emmons 1982; Emmons and Feer 1997). P. brevicauda is

known to eat palm nuts and wind-dispersed seeds that are only

found on the ground (Emmons 1982); therefore, the coarse-

wear features in this species (and, by analogy, the other spiny

rats in our sample) could be due to both seed consumption and

exogenous grit. Emmons (1982) noted that a high proportion of

the stomach contents of P. brevicauda consisted of fungi, but it

is not possible at this time to determine the wear signal left

from fungivory. Henry (1997, 1999) noted that P. cuvieripreferred the soft pulp of fruits. The microwear profile of these

spiny rats certainly supports their known dietary habits of fruit

consumption as do their scores on PC1. Punares (Thrichomys)

are known to eat seeds preferentially and they live in the arid

habitats of the Caatinga in Brazil, which could also contribute

to their microwear signal (Streilein 1982). It is likely that

punares feed on seeds to a greater degree than do the spiny rats

because they had the profile with the highest frequencies of

coarse-wear features. Proechimys, like Dasyprocta, uses its

anterior dentition to open seeds, but Emmons (1982:287)

commented that Proechimys may not be an efficient seed

predator (in terms of eating the entire seed) noting that ‘‘the

morphology of the echimyid jaw is poorly adapted for scooping

hard materials.’’ Henry (1997, 1999) echoed this statement in

regards to P. cuvieri. If this is the case, and spiny rats cannot

access tough seeds, it may have had some effect on the

microwear seen in Proechimys. In contrast, the strong hard-

object processing signal seen in Thrichomys would suggest that

punares masticate seeds using primarily the molar teeth.

The low-magnification microwear method has been shown

to pick up dietary subtleties among species within the same

genus (e.g., Alouatta—Semprebon et al. 2004). Spiny rats are

a highly speciose group, and multiple species can be found in

very close proximity because their food resources are de-

pendent on highly productive microhabitats (Emmons 1982;

Emmons and Feer 1997; Patton and Gardner 1972). This is

reflected in very small home ranges that are characterized by

high densities of food. Within these microhabitats, however, it

appears that these animals are eating similar foods because

species of Proechimys are known to have very similar diets

from 1 locality to another (Adler 2000; Adler et al. 1998;

Emmons 1982; Henry 1997, 1999). Examination of our data on

microwear supports the hypothesis that species of spiny rats

have similar food preferences.

Substrate signal or seed predation?—All of the frugivorous

rodents in our study are reported to eat seeds to some degree.

Many of these taxa are terrestrial as well and it has been

established that coarse-wear features are present in all taxa. It is

essential to determine whether microwear profiles dominated

by coarse-wear features represent seed predation or hard-object

feeding, or both, or the effects of substrate (i.e., exogenous

grit); this is especially important when making inferences about

paleoenvironments using dietary reconstructions based on

microwear.

Recent low-magnification microwear work on squirrels

showed that the average number of pits and coarse features is

useful in distinguishing among frugivorous tree squirrels and

ground squirrels (Nelson et al. 2005). The study of microwear

in squirrels suggested that ground squirrels exhibited more

coarse-wear features due to more exogenous grit in their diets,

along with seeds and insects with tough exoskeletons (Nelson

et al. 2005). In primates, the intensity of seed predation is

reflected by the frequency of puncture pits and a spectrum

ranging from no seed consumption to heavy or ‘‘exceptional’’seed predation is apparent (Semprebon et al. 2004). The

recognition of such a spectrum has to do with the extraordinary

behavioral literature on primates combined with large dental

samples available for numerous species. The literature on diets

of caviomorphs is not as extensive as that of primates. Using

the primate model, where the frequency of puncture pits is

correlated with the degree of seed predation, we can make

similar statements about the degree of seed predation in

caviomorph rodents.

Most of the caviomorphs in our study are terrestrial and

a coarse-wear signal was represented in all taxa, ranging from

slight to dominant (Tables 1 and 2). The strongest coarse-wear

signals were found in Thrichomys, Ctenomys, Coendou, and

Myocastor. Of these, Ctenomys is the only form that lives most

of its life underground and is known to feed predominantly on

grasses (Altuna et al. 1998; Puig et al. 1999; Rosi et al. 2003).

Because the microwear profile of Ctenomys showed few

puncture pits (0.60 average pits per individual per taxon), we

are confident that the coarse-wear signal is due to substrate use.

Thrichomys is restricted to the semiarid Brazilian Caatinga

(Redford and Eisenberg 1992; Streilein 1982), and it could be

argued that an exogenous-grit signal is present due to living in

a dry habitat with more dust on food items. Given the strong

behavioral evidence for seed consumption by Thrichomys and

the very high number of puncture pits, we are confident that its

coarse-wear signal is due to seeds (Table 2). Coendou,

a porcupine, is the only arboreal form evaluated in our study.

Coendou is known to eat bark and twigs and is restricted to

humid forest (Eisenberg and Redford 1999; Emmons and Feer

1997); its microwear is clearly due to feeding on hard objects,

probably including seeds, since it had the 2nd highest

frequency of large puncture pits. Although dietary data for

the semiaquatic Myocastor are sparse, bark consumption has

been reported for this genus (Woods et al. 1992), and we

attribute the coarse wear to eating tough plant parts. The

puncture pits present in the profile of Myocastor might suggest

it eats seeds as well, but with such a small sample (n ¼ 4) it

would be tenuous to attribute these pits to seed predation.

The remaining terrestrial frugivores did not have microwear

dominated by coarse wear. The frugivorous spiny rats,

Proechimys, are terrestrial seed predators, but their microwear

profile was not coarse enough to be attributed to either grit or

seeds (Table 2). Dasyprocta, the agouti, is known to bury its

food in a scatter-hoarding behavior and then retrieve it during

738 JOURNAL OF MAMMALOGY Vol. 89, No. 3

times of food scarcity (Henry 1999). Therefore, we expected to

see a grit signal in Dasyprocta but did not. Cuniculus, the paca,

forages on the ground, but will eat only the soft inner portions

of tough fruits (Dubost et al. 2005). It is unclear whether the

slight coarse wear (especially few puncture pits) seen in

Cuniculus could be attributed to eating food from the ground or

to minimal hard-object processing. Because caviomorphs do

much seed processing with their incisors (Emmons 1982;

Henry 1997, 1999; Perez 1992), it is challenging to accurately

assess this behavior based on microwear of the cheek teeth.

Taxa in the grass–leaf group show evidence of coarse wear.

Hydrochoeris, Lagidium, Cavia, and Chinchilla exhibited

gouging, large pits, and a few large puncture pits. Considering

that Hydrochoeris grazes on both dry and wet grass, it is likely

that this animal may be picking up grit on grass blades. Caviatunnels in surface soil and eats grass flowers (Redford and

Eisenberg 1992), both of which could contribute to the coarse-

wear signal seen in this animal. Chinchilla is a known dust

bather and burrows (Spotorno et al. 2004), so it is likely that

exogenous grit affects its microwear. Lagidium is another

committed grazer living in arid habitats and could be

consuming grit on grass as well (Puig et al. 1998).

Paleodietary inference.—Quantitative paleobiological stud-

ies of neotropical rodents are few and have primarily been based

on inference with extant forms (e.g., Kay and Madden 1997;

Scott 1905; Walton 1997). Scott (1905) noted resemblances

among the teeth of Neoreomys, Capromys, Myocastor, and

Cuniculus and suggested that Neoreomys might be a remnant

form of the ancestral stock from which all of these lineages

descended. Fields (1957) stated that Neoreomys huilensis from

the La Venta Fauna (11.8–13.8 mya—Flynn and Swisher 1995)

could be related to Myocastor, based upon similarities in the

lower dentition. Based on analogy with living rodents, Kay and

Madden (1997) listed N. huilensis as a small-seed consumer.

Other authors have noted the similarities in molar occlusal

morphology between Neoreomys and living dasyproctids,

implying that it may have been a forest-floor dweller exhibiting

similar dietary behaviors (Fig. 2; Kramarz and Bellosi 2005;

Walton 1997). Dietary inferences for fossil caviomorphs based

upon analogies with modern forms and crown height (hyp-

sodonty) have been used to inform paleoenvironmental

reconstructions (Flynn et al. 2003; Kramarz and Bellosi 2005).

Although our discriminant model assigned a 0.00 probability

to the placement of Neoreomys in the fruit–seed category,

microwear indicative of frugivory was apparent on its occlusal

surface. As with other studies of microwear, scratches proved

to be the most diagnostic variable discriminating between

folivores and frugivores, and browsers and grazers (Godfrey

et al. 2004; Solounias and Hayek 1993; Solounias and

Semprebon 2002). Based on scratch frequency alone, Neo-reomys certainly was not a grazer; the remaining microwear

features resemble those of Dasyprocta. Expanded studies of

extant and extinct taxa may permit more detailed dietary

inferences for Neoreomys.

Studies of microwear using low-magnification microscopy

hold great promise for correlating dietary behavior of rodents

with wear signatures. Examination of our data shows that

recognizable dietary categories exist among caviomorph

rodents and that microwear can be used to classify taxa into

these categories. In evaluating habits such as seed predation,

greater sample sizes are needed to more accurately distinguish

the exogenous-grit signal from the hard-object processing

signal in frugivorous caviomorphs. For taxa with few dietary

data such as Thrichomys and Coendou, our studies of

microwear have confirmed reported dietary behavior. Unlike

features of microwear in primates and ungulates, individual

features other than scratches are apparently not very in-

formative for inferring diet in caviomorphs but yield insights

when considered together (although this may change with

greater sample sizes and additional taxa, particularly for

arboreal rodents).

The utility of our data set for paleodietary and paleoenvi-

ronmental inference is clear. The microwear profile of

Neoreomys is similar to that of Dasyprocta, suggesting that it

was some kind of frugivore; assessment of more specimens

could verify that it was a seed predator as suggested for the

species N. huilensis from La Venta (Kay and Madden 1997).

When diet is used to infer paleohabitats, studies of microwear

such as ours would be a useful approach to ensure accurate

dietary reconstructions. Furthermore, studies of microwear

underscore the importance of museum collections as sources of

ecological data, particularly because mammalian osteological

collections are generally used for taxonomic or functional

studies.

The data set that we have developed will be expanded in

future studies by adding more taxa and more specimens per

taxon. Additional variables such as incisor microwear would

further clarify food processing and consumption patterns in

caviomorphs. Nevertheless, this data set is valuable for under-

standing the diversity of modern caviomorph diets and shows

potential for interpreting the diets of fossil rodents.

ACKNOWLEDGMENTS

Funding for this study was provided by Case Western Reserve

University School of Medicine. We are grateful to both the Carnegie

Museum of Natural History and The Field Museum for access to

modern and fossil specimens. We thank J. Wible and S. McLaren

for access to specimens at the Carnegie Museum of Natural History;

S. McLaren was extremely helpful in setting up specimens for

molding. W. Simpson of The Field Museum was especially helpful in

suggesting ideas for preparing fossil specimens for molding. We also

thank the Department of Vertebrate Paleontology at the Cleveland

Museum of Natural History for allowing us to use space in the fossil

preparation laboratory for molding and casting; D. Chapman provided

valuable insights in this regard. Discussions with G. Semprebon about

microwear methods were very insightful.

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Associate Editor was Craig L. Frank.

June 2008 741TOWNSEND AND CROFT—ENAMEL MICROWEAR IN CAVIOMORPHS

APPENDIX IIMicrowear Profiles for Dietary Groups

Grass–leaf group.—Within the grass–leaf consumers 2 subgroups

were apparent: grazers and exogenous-grit consumers. High scratch

frequencies and few to no puncture pits defined the grazer subgroup

(Hydrochoeris, Lagidium, and Cavia), although this subgroup did

have other coarse-wear features (Table 2). These taxa lie at the

‘‘scratch’’ end of the 1st principal component axis, suggesting a diet

composed of more abrasives than that of the other caviomorph taxa

(Table 4). Hydrochoeris exhibited a microwear profile indicative of

a diet dominated by grasses: high frequencies of scratches that are

mostly fine in texture and few coarse-wear features (Table 2).

Lagidium had a high number of small pits, the highest frequency of

scratches of all caviomorph taxa sampled, and all scratches were

coarse in texture; other than scratch texture, this taxon exhibited few

coarse-wear features. Cavia exhibited almost equal frequencies of pits

and scratches (Table 2); most of the scratches were fine in texture and

this taxon exhibited few coarse-wear features.

Ctenomys and Chinchilla comprised the exogenous-grit subgroup

and exhibited microwear profiles defined by coarse-wear features and

fewer scratches. A bivariate plot of average scratch frequency and

average small pit frequency shows that these 2 taxa fall well within the

range of the fruit–seed and fruit–leaf consumers (Fig. 4). The tuco-

tuco (Ctenomys) had the 2nd highest positive score on the 1st principal

component axis, suggesting hard-object processing. Chinchilla also

exhibited both low scratch and cross-scratch frequencies and high

small and large pit counts; it scored positively on principal component

1 (PC1), indicating fewer scratch features (Fig. 5).

Fruit–seed group.—The fruit–seed consumer group is composed of

3 species of Proechimys (which exhibit a consistent microwear profile)

and the punare (Thrichomys). As a group, they had relatively high

small pit counts (more than 20) and rather low scratch counts

(frequencies of both scratches and cross scratches; Table 2). The

presence and high numbers of large pits and gouges suggest seeds in

the diet, particularly in Thrichomys, which exhibited high puncture-pit

and large-pit frequencies (Table 2). Proechimys guyannensis also

exhibited small puncture pits and displayed the greatest number of

these pits among the 3 caviomorph taxa that had this feature (the

others being Coendou and Cavia). The presence of small pits in this

species suggests seed pits, which have been noted in both ungulate and

primate taxa; Proechimys is known to horde seeds for later

consumption (Forget 1991; Godfrey et al. 2004; Semprebon et al.

2004; Solounias and Semprebon 2002). The spiny rats exhibited

a range of scratch textures; Proechimys did not exhibit hypercoarse

scratches, but these were seen in Thrichomys. Coarse scratch textures

were a dominant feature in Proechimys, as evidenced by the

percentages of both coarse and mixed (both fine and coarse scratches)

textures apparent in their microwear profiles. The 3 species of

Proechimys did not fall near the hard-object processing end of PC1,

indicating that they had lower large-pit, gouge, and puncture-pit scores

than other hard-object feeders (Table 4; Fig. 5). The punare

(Thrichomys) had the highest PC1 score, indicating that it was

a definitive hard-object feeder (Table 4; Fig. 5). The most outstanding

feature of the microwear profile of the punare is that it had the highest

frequency of large puncture pits of all the caviomorph taxa in this

sample and it is the only taxon to exhibit hypercoarse scratches.

Fruit–leaf group.—All of the members of the fruit–leaf group

except Coendou exhibited a microwear profile consistent with

frugivory, as noted in both primate and ungulate microwear studies:

high frequencies of small pits and low frequencies of scratches. This

group had high frequencies of large pits, large puncture pits, and

gouges, with low frequencies of scratches and cross scratches. The

fruit–leaf consumers scored positively on PC1, indicating more coarse-

wear features than grass–leaf and fruit–seed consumers (Table 4; Fig.

5). The paca (Cuniculus) scored near the middle of PC1 between the

coarse-wear and grazing ends of the microwear spectrum, indicating

that it had fewer large pits and puncture pits than other more hard-

object feeders and fewer scratches than seen in the grass consumers.

The paca did exhibit a large number of gouges and large pits, many of

them along the edges of the enamel bands (Fig. 2). The agouti

(Dasyprocta) had low scratch values, low pit values, and high numbers

of large pits and gouges present, all features seen in frugivores (Table

2; Godfrey et al. 2004; Solounias and Semprebon 2002). The PC1 score

for the agouti was in the middle range, indicating that it was not a hard-

object specialist. The coypu (Myocastor) exhibited a microwear profile

similar to that of Cuniculus or Dasyprocta. In addition to exhibiting

high pit values and low scratch values, the coypu also exhibited a high

number of large pits, large puncture pits, and gouges. Most individuals

(75%) exhibited a mixed scratch texture signature (both fine and coarse

scratches). Myocastor scored on the positive end of PC1, reflecting the

higher frequency of large pits, gouges, and puncture pits on its enamel.

The arboreal porcupine (Coendou) exhibited the fewest pits and

scratches of the fruit–seed consumer group and these features were

represented with equal frequencies. The arboreal porcupine had the

highest number of large pits among all taxa represented in the study and

had the highest number of puncture pits relative to other members in its

dietary group (Table 2). It also exhibited an equal number of fine and

mixed scratch textures, and a few individuals exhibited only coarse

scratches. On PC1, Coendou scored high on the positive end of the

spectrum, with high counts of coarse-wear features, suggesting hard-

object processing (Table 4; Fig. 5).

Fossil taxon: Neoreomys.—The microwear of Neoreomys was most

similar to that of the agouti (Dasyprocta) in terms of small-pit and

scratch frequencies; it was classified by the discriminant function as

a member of the fruit–seed group. However, the conditional probability

of this classification using the extant caviomorph model is 0.00. This

result is apparent from the bivariate plot of the 2 discriminant functions

(Fig. 6) that Neoreomys falls beyond the fruit–leaf and fruit–seed group

on both the 1st and 2nd axes. The frequencies of coarse-wear features

are lower than those exhibited by members of the fruit–seed group.

These results should be considered preliminary because our sample of

Neoreomys is relatively small.

APPENDIX IProbabilities of group membership from discriminant function

analysis of microwear variables.

Taxon Group

Conditional

probability

Posterior

probability

Cuniculus Fruit�leaf 0.830 1.00

Dasyprocta Fruit�leaf 0.827 1.00

Myocastor Fruit�leaf 0.241 1.00

Coendou Fruit�leaf 0.868 1.00

P. guyannensis Fruit�seed 0.310 1.00

P. brevicauda Fruit�seed 0.235 1.00

P. cuvieri Fruit�seed 0.104 1.00

Thrichomys Fruit�seed 0.415 1.00

Hydrochoeris Grass�leaf 0.704 1.00

Lagidium Grass�leaf 0.730 1.00

Cavia Grass�leaf 0.249 1.00

Ctenomys Grass�leaf 0.832 1.00

Chinchilla Grass�leaf 0.947 1.00

Neoreomys Fruit�seed 0.000 1.00

742 JOURNAL OF MAMMALOGY Vol. 89, No. 3