Enamel microwear in caviomorph rodents

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

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

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 information (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

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 hippopotamus, 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

* Correspondent: [email protected]

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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 relationship 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-magnification microwear method to obtain data on microwear, and we evaluated whether microwear features covary with the dietary categories (using univariate and multivariate statistical techniques). 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

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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, Thrichomys, 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

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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

Fruitleaf

3, 8, 10, 16, 18, 21

Fruit, seeds, browse, leaves

Terrestrial; scatter-horde

Fruitleaf

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

Fruits, seeds, nuts, leaves Unknown

Terrestrial; scatter-horde Unknown

Fruitleaf

3, 4, 7, 8, 10, 18

Grasses, grass inflorescences

Terrestrial; construct surface runways in soil

Grassleaf

7, 8, 17, 22

Grasses, aquatic plants

Semiaquatic

Grassleaf

3, 7, 8, 10, 15, 16, 17

Grasses, stems, roots, bulbs, bark, leaves

Fossorial

Grassleaf

2, 3, 13, 20, 22, 23, 26

Fruits, nuts Seeds, fruits, nuts

Terrestrial

Fruitseed Fruitseed

1, 3, 7, 9, 10, 12, 26 3, 17, 22, 26

Grass, stems, leaves, roots, bark, aquatic vegetation

Semiaquatic

Fruitleaf

3, 8, 15, 27

Grass, any vegetation Grasses, herbivore

Terrestrial; burrows Terrestrial

Grassleaf Grassleaf

3, 4, 25 5, 8, 11, 15, 17, 21, 22

Cavioidea Agoutidae Cuniculus paca Dasyproctidae Dasyprocta Neoreomys* Caviidae Cavia Hydrochoeridae Hydrochoeris Octodontoidea Ctenomyidae Ctenomys Echimyidae Proechimys Thrichomys Myocastoridae Myocastor

Chinchilloidea Chinchillidae Chinchilla Lagidium

a References: 1) Adler 2000; 2) Altuna et al. 1998; 3) Arends and McNab 2001; 4) Corte´s et al. 2002a; 5) Corte´s 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) Pe´rez 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.

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

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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.

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

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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. Hardobject 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 multivariate 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. 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.

0.00

44.40 44.40 30.00 75.00 33.30 62.50 50.00 44.40 11.10 14.30 11.10 25.00 0.00

71.40

0.00 0.00 0.00 0.00 11.10 0.00 25.00 0.00 0.00 0.00 10.00 0.00 0.00

0.00

11.10 44.4 40.00 0.00 11.10 12.50 0.00 44.40 11.10 0.00 11.10 25.00 100.00 (13, 84)

(1.91) (1.00)

(1.70) (0.35)

2.07 (0.05) 0.00 1.75 (0.10) 0.36 (0.75) 2.01 (0.05) 1.36 (1.60) 1.86 (0.05) 1.00 (1.44) 8.01 (0.000) 14.78 (4.27) 1.87 (0.05) 30.57 (12.24)

(13, 84)

(0.94)

(3.98)

1.75 (0.10) 1.14 (1.18)

28.60

44.4 11.1 20.00 25.00 44.4 25.00 25.00 55.6 77.8 85.7 20.00 25.00 0.00 (1.80) (2.20) (2.94) (2.02) (1.48) (2.20) (0.96) (1.48) (1.00) (1.35) (2.00) (1.08) (0.70) (13, 84) 2.77 3.88 3.15 3.88 3.22 3.31 2.75 2.00 1.33 1.14 3.65 0.54 3.00 1.99 (0.17)

0.06 0.00 0.00 0.00 0.00 2.50 0.00 0.00 0.00 0.36 0.00 0.00 0.00 1.59 (1.77) (1.14) (1.42) (2.00) (3.99) (0.15)

2.27 0.89 0.90 1.00 2.61 0.05 0.00 0.83 0.17 0.00 0.60 0.50 0.00 1.82 (3.74) (2.11) (3.13) (3.40) (3.65) (2.51) (3.12) (2.50) (3.15) (2.51) (2.98) (2.25) (3.18) (13, 84) 5.39 3.83 2.40 4.00 5.33 2.40 4.13 2.22 1.61 0.86 5.25 3.75 2.25 3.12 (1.58) (1.22) (.632) (0.25) (0.73) (0.52) (0.86) (0.77) (1.67) (0.52) (0.16) (1.18) (2.12) (13, 84) 1.00 1.33 0.30 0.13 0.44 0.27 0.75 0.56 0.56 1.00 0.05 0.88 3.50 1.17 (8.13) (4.34) (5.71) (5.27) (4.91) (4.96) (1.47) (7.61) (7.11) (4.96) (5.54) (5.48) (7.07) (13, 84) 16.38 13.94 12.15 15.25 8.77 8.70 9.50 13.44 26.61 29.14 7.45 7.75 29.50 9.50 (7.79) (28.9) (12.17) (16.02) (16.47) (14.70) (13.69) (9.14) (12.67) (14.7) (35.14) (15.67) (44.55) (13, 84) 16.38 44.55 30.40 27.25 27.05 24.36 24.50 20.16 27.27 29.07 46.40 39.00 40.50 20.33

6

9 9 10 4 9 11 4 9 9 7 10 4 2

Coendou Cuniculus Dasyprocta Myocastor Thrichomys Proechimys guyannensis Proechimys brevicauda Proechimys cuvieri Hydrochoeris Cavia Ctenomys Chinchilla Lagidium ANOVA grand mean (d.f. [between groups, within groups]) F (significance [P,]) Fossil taxon Neoreomys australis

Diet group

Fruitleaf Fruitleaf Fruitleaf Fruitleaf Fruitseed Fruitseed Fruitseed Fruitseed Grassleaf Grassleaf Grassleaf Grassleaf Grassleaf

% hypercoarse scratches % coarse scratches % fine scratches Average no. gouges Average no. small puncture pits Average no. large puncture pits Average no. large pits Average no. cross scratches Average no. scratches n

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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Taxon

RESULTS

Average no. small pits

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 univariate and discriminant analyses. We performed a 1-way ANOVA to evaluate whether variable 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 probability of making a type I error with the Mann–Whitney U pairwise 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 discriminant 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 categories 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 unknown and was then subsequently classified into a dietary group by the model. The diet of the extinct rodent Neoreomys was reconstructed by treating the extinct taxon as an unknown in the analysis. The microwear profile of Neoreomys was generated in the same way as for extant caviomorphs and was based on both the mean and percentage scores of the individuals.

% mixed scratches

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TABLE 2.—Microwear data for extant and extinct caviomorph rodents. Averages are given as means (SD).

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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, Pc ¼ P. cuvieri, Pb ¼ P. brevicauda, M ¼ Myocastor, Ag ¼ Cuniculus, 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.

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

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— 0.140

Chinchilla

— 0.511 0.357

Ctenomys

— 0.296 0.742 0.033

Cavia

Grassleaf

Fruitleaf

0.352 0.399 0.368 0.660

a

— — 0.286 — 0.407 0.485 — 0.513 0.852 0.386 — — 0.198 — — 0.766

Thrichomys Proechimys guyannensis P. brevicauda P. cuvieri Coendou Cuniculus Dasyprocta Myocastor Hydrochoeris Cavia Ctenomys Chinchilla Lagidium Fruitseed

Two-tailed significance is reported. Using the Dunn–Sidak method to correct for experimentwise error rate, no comparisons were found to be significant.

— 0.756 0.275 0.791 0.027

Hydrochoeris Myocastor Dasyprocta Cuniculus Coendou P. cuvieri P. brevicauda Proechimys guyannensis Thrichomys Taxa Group

TABLE 3.—Mann–Whitney U-test for coded scratch texture ranks within dietary groups.a

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—

Lagidium

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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.

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

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TABLE 4.—Dominant microwear signal, principal component analysis (PCA), with taxa arranged by increasing score on PC1. PCA scores are mean (SE). Taxon Cavia Lagidium Hydrochoeris Proechimys cuvieri P. guyannensis Chinchilla P. brevicauda Dasyprocta Cuniculus Myocastor Coendou Ctenomys Thrichomys

PCA axis 1 scores 1.25 1.19 0.96 0.23 0.01 0.02 0.03 0.05 0.14 0.25 0.59 0.67 0.85

(0.29) (0.14) (0.13) (0.19) (0.15) (0.23) (0.24) (0.38) (0.23) (0.53) (0.25) (0.26) (0.48)

Diet group Grassleaf Grassleaf Grassleaf Fruitseed Fruitseed Grassleaf Fruitseed Fruitleaf Fruitleaf Fruitleaf Fruitleaf Grassleaf Fruitseed

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; chisquare 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

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 Neoreomys australis 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 ¼ fruit–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

4 0 0

0 4 0

0 0 5

100 100 100

4

5

F-L F-S G-L Total

4

13

Taxon

Discriminant score

Dietary category

Hydrochoeris Ctenomys Lagidium Chinchilla Cavia Cuniculus Myocastor Dasyprocta Coendou Proechimys cuvieri P. brevicauda Thrichomys P. guyannensis Neoreomys

17.99571 17.73593 17.36286 16.83331 15.88239 5.15392 5.34501 5.40925 5.54652 13.96034 16.03833 16.86027 17.49657 27.52555

Grassleaf Grassleaf Grassleaf Grassleaf Grassleaf Fruitleaf Fruitleaf Fruitleaf Fruitleaf Fruitleaf Fruitseed Fruitseed Fruitseed Fruitseeda

a

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

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

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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 coarsewear 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

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large pits, and many gouges; all of these features suggest hardobject processing. Unlike primates or duikers where ‘‘hardobject 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 lanigera evaluated 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 (Corte´s 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 (Corte´s 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 (Pe´rez 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 seedpredation signal were likely due to differences in seed

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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 (punare´s) all are known seed predators and we expected to see a strong hard-object processing signal (Streilein 1982). Fecal samples of P. brevicauda indicate 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 coarsewear 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. cuvieri preferred 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. Punare´s (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 punare´s 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 hardobject processing signal seen in Thrichomys would suggest that punare´s 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 dependent 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

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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

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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; Pe´rez 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. Cavia tunnels in surface soil and eats grass flowers (Redford and Eisenberg 1992), both of which could contribute to the coarsewear 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 studies 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 (hypsodonty) 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, Neoreomys 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

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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 informative 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 paleoenvironmental 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 understanding 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.

LITERATURE CITED ADLER, G. H. 2000. Tropical tree diversity, forest structure and the demography of a frugivorous rodent, the spiny rat (Proechimys semispinosus). Journal of Zoology (London) 250:57–74. ADLER, G. H., D. C. TOMBLIN, AND D. T. LAMBERT. 1998. Ecology of two species of echimyid rodents (Hoplomys gymnurus and Proechimys semispinosus) in central Panama´. Journal of Tropical Ecology 14:711–717.

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ALTUNA, C. A., L. D. BACIAGALUPE, AND S. CORTE. 1998. Foodhandling and feces reingestion in Ctenomys pearsoni (Rodentia, Ctenomyidae). Acta Theriologica 43:433–437. ARENDS, A., AND B. K. MCNAB. 2001. The comparative energetics of ‘caviomorph’ rodents. Comparative Biochemistry and Physiology, A. Comparative Physiology 130:105–122. BOURLIE`RE, F. 1973. The comparative ecology of rain forest mammals in Africa and tropical America: some introductory remarks. Pp. 279–292 in Tropical forest ecosystems in Africa and South America (B. J. Meggers, E. S. Ayensu, and W. D. Duckworth, eds.). Smithsonian Institution Press, Washington, D.C. CANDELA, A. M. 2004. A new giant porcupine (Rodentia, Erethizondontidae) from the late Miocene of Argentina. Journal of Vertebrate Paleontology 24:732–741. CORTE´S, A., E. MIRANDA, AND J. E. JIME´NEZ. 2002a. Seasonal food habits of the endangered long-tailed chinchilla (Chinchilla lanigera): the effect of precipitation. Mammalian Biology 67:167–175. CORTE´S, A., J. R. RAU, E. MIRANDA, AND J. E. JIME´NEZ. 2002b. Ha´bitos alimenticos de Lagidium viscacia y Abrocoma cinera: roedores sinto´picos en ambientes altoandinos del norte de Chile. Revista Chilena de Historia Natural 75:583–593. CROFT, D. A., J. J. FLYNN, AND A. R. WYSS. 2004. Notoungulata and Litopterna of the early Miocene Chucal Fauna, northern Chile. Fieldiana: Geology (New Series) 50:1–52. DUBOST, G. 1988. Ecology and social life of the acouchy, Myoprocta exilis, comparison with the orange-rumped agouti, Dasyprocta leporine. Journal of Zoology (London) 214:107–123. DUBOST, G., O. HENRY, AND P. COMMIZOLI. 2005. Seasonality of reproduction in the three largest terrestrial rodents of French Guiana forest. Mammalian Biology 70:93–109. EISENBERG, J. F. 1989. Mammals of the Neotropics: the northern Neotropics. University of Chicago Press, Chicago, Illinois. EISENBERG, J. F., AND K. H. REDFORD. 1999. Mammals of the Neotropics: the central Neotropics. University of Chicago Press, Chicago, Illinois. EMMONS, L. H. 1982. Ecology of Proechimys (Rodentia, Echimyidae) in south-eastern Peru. Tropical Ecology 23:280–290. EMMONS, L. H., AND F. FEER. 1997. Neotropical rainforest mammals: a field guide. 2nd ed. University of Chicago Press, Chicago, Illinois. FERANEC, R. S. 2003. Stable isotopes, hypsodonty, and the paleodiet of Hemiauchenia (Mammalia: Camelidae): a morphological specialization creating ecological generalization. Paleobiology 29:230–242. FIELDS, R. W. 1957. Hystricomorph rodents from the late Miocene of Colombia, South America. University of California Publications in Geological Sciences 32:273–404. FLYNN, J. J., AND C. C. SWISHER III. 1995. Cenozoic South American Land Mammal Ages: correlation to global geochronologies. Pp. 317–333 in Geochronology, time scales, and global stratigraphic correlation (W. A. Berggren, D. V. Kent, M.-P. Aubry, and J. Hardenbol, eds.). Special Publication 54, SEPM (Society for Sedimentary Geology). FLYNN, J. J., AND A. R. WYSS. 1998. Recent advances in South American mammalian paleontology. Trends in Ecology and Evolution 13:449–454. FLYNN, J. J., A. R. WYSS, D. A. CROFT, AND R. CHARRIER. 2003. The Tinguiririca Fauna, Chile: biochronology, paleoecology, biogeography, and a new earliest Oligocene South American Land Mammal ‘Age.’ Palaeogeography, Palaeoclimatology, Palaeoecology 195:229–259. FORGET, P. M. 1991. Scatterhording of Astrocaryum paramaca by Proechimys in French Guiana: comparison with Myoprocta exilis. Tropical Ecology 32:155–167.

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Submitted 5 October 2006. Accepted 28 September 2007. Associate Editor was Craig L. Frank.

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APPENDIX I Probabilities of group membership from discriminant function analysis of microwear variables. Taxon

Group

Conditional probability

Posterior probability

Cuniculus Dasyprocta Myocastor Coendou P. guyannensis P. brevicauda P. cuvieri Thrichomys Hydrochoeris Lagidium Cavia Ctenomys Chinchilla Neoreomys

Fruitleaf Fruitleaf Fruitleaf Fruitleaf Fruitseed Fruitseed Fruitseed Fruitseed Grassleaf Grassleaf Grassleaf Grassleaf Grassleaf Fruitseed

0.830 0.827 0.241 0.868 0.310 0.235 0.104 0.415 0.704 0.730 0.249 0.832 0.947 0.000

1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00 1.00

APPENDIX II Microwear 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 tucotuco (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

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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 coarsewear 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 hardobject 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 hardobject 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 hardobject 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.