Zurich Open Repository and Archive. Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics

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1 University of Zurich Zurich Open Repository and Archive Winterthurerstr. 0 CH-0 Zurich Year: 00 Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics Kaiser, T M; Brasch, J; Castell, J C; Schulz, E; Clauss, M Kaiser, T M; Brasch, J; Castell, J C; Schulz, E; Clauss, M (00). Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics. Mammalian Biology - Zeitschrift fur Saugetierkunde, ():-. Postprint available at: Posted at the Zurich Open Repository and Archive, University of Zurich. Originally published at: Mammalian Biology - Zeitschrift fur Saugetierkunde 00, ():-.

2 RH: Increased dental wear in captive ruminants Tooth wear in captive wild ruminant species differs from that of free-ranging conspecifics Thomas M. Kaiser, Juliane Brasch, Johanna C. Castell, Ellen Schulz, Marcus Clauss 0 Biozentrum Grindel and Zoological Museum, University of Hamburg, Martin-Luther- King-Platz, 0 Hamburg, Germany Zoological Institute and Museum, University Greifswald, Johann-Sebastian-Bach- Str. -, Greifswald, Germany Institute of Animal Physiology, Physiological Chemistry and Animal Nutrition, University of Munich, Schoenleutnerstr., Oberschleissheim, Germany Division of Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstr. 0, 0 Zurich, Switzerland Correspondence should be directed to T. M. Kaiser, ++ 0 ; thomas.kaiser@uni-hamburg.de

3 0 0 Abstract The mesowear method evaluates the wear patterns of herbivore cheek teeth by visually evaluating the facet development of the occlusal surfaces. It thus allows classification of most herbivorous ungulates into browsers, grazers or intermediate feeders, due to the fact that in grazers, tooth wear is characterized by a comparatively high degree of abrasion, most probably due to the presence of silicacious phytoliths in grasses, a higher amount of dust and grit adhering to their forage, or both. It has been suggested that excessive tooth wear could be a particularly limiting factor in the husbandry of captive large browsing species, and major tooth wear was demonstrated in captive as compared to free-ranging giraffe. If this increased tooth wear in captivity was an effect of feeding type and diets fed, then it would be expected that other browsing species are affected in a similar manner. In order to test this hypothesis, we investigated the dental mesowear pattern in captive individuals of ruminant species and compared the results to data on free-ranging animals. Compared to free-ranging populations, captive browsers show a significantly more abrasion-dominated tooth wear signal. The reverse applies to captive grazers, which tend to show a less abrasion-dominated wear in captivity. Captive ruminants were generally more homogenous in their wear signature than free-ranging ruminants. If grit contamination in the natural habitat is a major cause of dental wear in grazers, then diets in captivity, although similar in botanical composition, most likely contain less abrasives due to feeding hygiene. If dental wear is one of the major factors limiting longevity, then captive grazers should achieve longer lifespans than both captive browsers and free-ranging grazers. In particular with respect to browsers, the results suggest that captive feeding regimes could be improved.

4 Key words: nutrition, tooth wear, browser, grazer, roughage, browse, alfalfa, pelleted compound feed 0 0 Introduction Free-ranging herbivores are usually classified as grazers, browsers or intermediate feeders (Clauss et al., 00). Fortelius and Solounias (000) demonstrated that dental wear patterns mostly correspond to these feeding types. Dental wear is basically induced by two components food-to-tooth contact (abrasion) and tooth-to-tooth contact (attrition). Because abrasiveness varies with food source, the wear pattern can be more attrition-dominated or more abrasiondominated. The mesowear scoring method analyses the wear patterns of herbivore molar teeth by visually evaluating the facet development of the occlusal surfaces (Fortelius and Solounias, 000). The method has proven to be a powerful tool for reconstructing dietary traits of herbivorous ungulates (Kaiser et al., 000), and is mainly used in palaeontological reconstructions of the biology of extinct species (Franz-Odendaal et al., 00; Kaiser and Fortelius, 00; Kaiser and Croitor, 00; Mihlbachler and Solounias, 00; Schulz et al., 00; Semprebon and Rivals, 00) or of whole palaeoecosystems (Kaiser and Rössner, 00; Rivals et al., 00). The method classifies animals into browsers, grazers or intermediate feeders, due to the fact that in grazers, tooth wear is characterized by a high degree of abrasion, most probably due to the presence of silicacious phytoliths in grasses (Baker et al., ; Healy and Ludwig, ; Sanson et al., 00), while the amount of dust and grit adhering to vegetation may increase abrasiveness of both grass and browse, in particular in arid or high altitude habitats. The increased abrasiveness of grazer diets

5 0 0 is regarded as the evolutionary driver of hypsodonty, i.e. the high-crowned teeth of grazing species, as opposed to the brachydont (low-crowned) teeth of browsing species. Browsing species can afford low-crowned teeth because their natural forage contains little or no abrasive components (Janis and Fortelius, ). Evidently, there is less need to reconstruct the diet of extant herbivores, which is mostly known from direct observations or ingesta or faecal analyses (e.g. Gagnon and Chew, 000), by mesowear patterns; yet, extensive datasets on the wear pattern of extant, freeranging herbivores exist as reference bases for the classification of extinct animals (Fortelius and Solounias, 000). These databases can be used to analyse dental wear patterns in free-ranging animals in comparison to captive specimens. For large herbivores, it has been suggested that excessive tooth wear should be a major limiting factor in the husbandry of captive browsing species (Clauss and Dierenfeld, 00), and for a prominent browser species, the giraffe (Giraffa camelopardalis), it has been demonstrated that captive individuals differ systematically in their tooth wear pattern from free-ranging conspecifics (Clauss et al., 00). The giraffe shows a more severe, grazer-type, abrasion-dominated wear pattern in captivity. Should this difference be an effect of feeding type and diets fed in captivity, as suggested by Clauss et al. (00), then it would be expected that not only the giraffe, but also other browsing species are affected in a similar manner. In order to test this hypothesis, we investigated the dental mesowear pattern in captive individuals of ruminant species and compared the results to data on free-ranging specimens.

6 MATERIALS AND METHODS 0 Material Museum specimens of zoo ruminants of seven German zoological museums were investigated, comprising individuals (that had died between 0 and ) of species (Table ). Species were assigned to the grazer, browser or intermediate feeding type according to Hofmann (; ), Gagnon and Chew (000) and Sponheimer et al. (00). Animals whose origin was not stated in the museum records were not included in the study. Information contained in museum records on the origin, sex, age and date of death were noted, but were not consistently given, making distinctions other than captive or free-ranging origin difficult. Museum specimens were carefully cleaned, and a negative mold of one upper premolar-molar tooth row was made using PROVIL novo Putty regular set (Heraeus Kulzer, Hanau, Germany) polysiloxane dental molding putty. Subsequently, positive casts of the teeth rows were produced by filling the molds with epoxy resin Injektionsharz EP (Reckli-Chemiewerkstoff, Herne, Germany). The use of molds is a prerogative for such a study, in order to have continuous access to tooth casts, and to be able to investigate tooth forms from different locations under standardized conditions. 0 Mesowear method The mesowear method was developed by Fortelius and Solounias (000) and is based on facet development of cheek tooth occlusal surfaces. The degree of facet development reflects the relative proportions of tooth-to-tooth contact (attrition) and food to tooth contact (abrasion). Attrition creates facets while abrasion obliterates

7 them. The entire surface of the teeth is affected by tooth wear but mesowear analysis has focused on the buccal cutting edges of the enamel where the buccal wall (ectoloph) meets the occlusal surface. The mesowear method treats ungulate tooth wear as two variables: occlusal relief and cusp shape. Occlusal relief (OR) is classified as high (h) or low (l), depending on how high the cusps rise above the valley between them. The second mesowear variable, cusp shape, includes scored attributes: sharp (s), round (r) and blunt (b) according to the degree of facet development (Fig. ). Figure here 0 0 Mesowear scoring Only upper post canine dentitions were investigated, because as yet, there is no consistent comparative mesowear dataset available for the lower jaw dentition of ruminants. Only permanent teeth were scored. Unworn teeth and teeth in early wear (occlusal surface not yet entirely exposed to wear) were excluded from this study, because when too little wear is involved, no stable mesowear equilibrium can be established. Also, dental specimens in very late wear were excluded as suggested by Fortelius and Solounias (000). We used molar wear as a measure of discrimination of very old and very young individuals, because absolute individual ages were unknown in all wild animals and the majority of captive animals, and because wear stages allow for selection of specimens in the same dental functional stage independent from the degree of hypsodonty and the absolute amount of wear involved. Wear stages considered in this study thus centre around the primary molar functional stage of a species. In brachydont species (hypsodonty index <.) wear stages - (Fig. ) were considered. These include teeth with dentine exposed at all

8 cusps and all dentine fields isolated (stage ), theeth with at least but less then dentine fields connected (stage ) and teeth with all dentine fields connected, at least one infundibulum still open or both infundibula connected (stage ). In mesodont species (. < hypsodonty index <.) stages - (Fig. ) were scored. Stage includes teeth with both infundibula closed, isolated and complex in shape. In hypsodont species (hypsodonty index >.) only stages and were considered. Figure here 0 0 Both the second and the third molar were scored, following feasibility tests on three extant ruminant species (Franz-Odendaal and Kaiser, 00) and the procedure applied to giraffes (Clauss et al., 00). After excluding unworn teeth, specimens in earliest and latest wear and those with secondarily broken cusp apices, the available upper post canine sample comprised dental specimens. Only the sharpest of the two cusps of a cheek tooth was scored, in order to be consistent with the comparative data by Fortelius and Solounias (000). In addition to established mesowear convention, a combined mesowear score was computed from each captive and wild population similar to Mihlbachler and Solounias (00), Rivals and Semprebon (00) and Semprebon and Rivals (00). A combination of high relief and sharp cusps was assigned a score of 0, a combination of high relief and round cusp was assigned a score of, a combination of low relief and sharp cusp was assigned a score of, a combination of low relief and round cusp was assigned a score of and a combination of low relief and blunt cusp was assigned a score of. In this convention, a score of 0 represents the most attrition dominated mesowear signature, while a score of would represent the most abrasion dominated signature. Individual scores were averaged and a mean score was

9 calculated for each species in the captive and the wild population. Scores thus indicate the over all abrasiveness of the diet a species had to cope with. Percentages of mesowear variables of the wild populations were taken from the literature (Fortelius and Solounias, 000) and absolute counts of mesowear variables as needed for the computation of scores were taken from the original data of Fortelius and Solounias (000), which were courteously provided to T. M. Kaiser by the authors. New, yet unpublished comparative mesowear data were gathered of a small number of individuals representing two species, Connochaetes gnou and Oryx gazella gazella. 0 0 Statistical analysis The mesowear parameter frequencies were calculated for free-ranging and captive individuals of each species, and subsequently the difference in score (freerange minus captive). Data on sex and age at death were not included in the analysis. Score differences between free-ranging and captive populations were plotted against the hypsodonty index after Janis () and the body mass after Janis (0). Differences between the feeding types were tested by Kruskal-Wallis test and subsequent U-tests with Dunn Sidak adjustment for ordinal data (mesowear scores) and by ANOVA and subsequent post hoc tests with Dunn Sidak adjustment for percentages. Differences between the scores within feeding types were tested by Wilcoxon tests. Correlations were tested by bivariate correlation analysis (Spearman). All statistical analyses were performed using SPSS.0 (SPSS Inc., Chicago, IL, USA). The significance level was set to 0.0.

10 0 0 RESULTS Mesowear scorings are listed per species in Table ; high occlusal reliefs prevailed over low reliefs in all browsers and intermediate feeders. Those browsers showing differences between wild and captive populations all had higher proportions of low reliefs in the captive population. Among the intermediate feeders, two species (Antidorcas marsupialis and Boselaphus tragocamelus) had higher reliefs in the captive population. Among the free-ranging grazers the American plains bison (Bison bison) had 00% low cusps, while in the captive population most specimens (%) had high reliefs. Damaliscus lunatus was the second species of wild grazers that had lower relief scorings (0%) in the wild compared to the captive population where there were no low reliefs. With the only exception of Tragelaphus strepsicerosi, sharp cusps prevailed in all free-ranging browsers while round apices prevailed in all captive browsers. Among free-ranging browsers, blunt cusps were only represented in Capreolus capreolus (%). In the captive populations they were represented in species. Free-ranging intermediate feeders showed balanced relations of sharp and round cusps, with at least % and never more than % (Antodorcas marsupialis) in each category. The only exception here was Boselaphus tragocamelus, which had 00% round cusps. Three of four captive intermediate feeders had more round at the expense of sharp cusps. Again Boselaphus tragocamelus was the exception in being the only species with less round, but considerably more sharp (%) and also some blunt cusps (%) in the captive population. Three grazers had more sharp cusps (% - % higher) in the captive sample while two had less sharp cusps (% - 0% lower). Blunt cusps prevailed in none of the captive grazer populations and never exceeded % (Hippotragus niger), while in the free-ranging populations blunt cusps prevailed in

11 0 Bison bison (%) and made up at least 0% in two other species (Connochaetes taurinus and Damaliscus lunatus). 0 Table here Free-ranging ruminants differed in their mesowear score between the feeding types (Kruskal-Wallis p=0.00), with no difference between browsers and intermediate feeders (p=0.), a trend for a higher score in grazers than in intermediate feeders (p=0.0), and significantly higher scores in grazers than in browsers (p=0.00). Free-ranging animals also differed in the proportion of sharp cusps between the feeding types (ANOVA p=0.00), again with no difference between browsers and intermediate feeders (p=0.) or between intermediate feeders and grazers (p=0.0), but with a significantly higher proportion of sharp cusps in browsers as compared with grazers (p=0.00). Differences in the proportion of round cusps (ANOVA p=0.0) and blunt cusps (ANOVA p=0.0) only tended towards significance between the feeding types. In contrast, there were no differences between the feeding types in the captive animals; in particular, the mesowear score did not differ (Kruskal-Wallis p=0.0). 0 Browsing species mostly had higher mesowear scores in captivity than in the wild (Fig. ), and this difference was significant between the populations (p=0.0). In contrast, five out of eight grazers had lower scores in captivity than in the wild; the difference was, however, not significant for this feeding type (p=0.) nor for the intermediate feeders (p=0.). Among the browsers, the only exception was Tragelaphus strepsiceros (TT), which had a slightly lower score in captivity. This species was already shown by Fortelius and Solounias (000) to have a rather 0

12 0 abrasive diet in the wild. The intermediate feeders showed a similar trend as the browsers, but less pronounced. Only in Boselaphus tragocamelus (Btr) were scores lower in the captive as compared with the wild sample. The latter species must also be regarded as a non-typical intermediate feeder, as is indicated by the classification of the species as an outlier by Fortelius and Solounias (000). Solounias and Semprebon (00) found high scratch ratios in the microwear signature of this species, which indicated that Boselaphus tragocamelus has a rather abrasive diet in the wild; lower scores in captivity may indicate a similar pattern as observed in typical grazers. Note that the total range of mesowear scores, in particular with regards to very high scores, is lower in captivity (the grey shaded area in Fig. ) than in the wild. Quartile ranges of scores in free-ranging (0.-.) and captive specimens (0.-.) indicate that captive specimens are generally more homogenous in their signature than wild specimens (Table ). 0 Figure here When calculating the mean difference in mesowear scores (free-ranging minus captivity), it was evident that browsers had lowest and grazers the highest values, with intermediate feeders in-between (Fig. ). There was a significant difference between the feeding types with respect to the mesowear score difference (Kruskal- Wallis p=0.00). Browsers had a significantly lower score difference than grazers (p=0.00); and the intermediate feeders were intermediate, with a nearly significant difference to browsers (p=0.0; limit for significance with Dunn Sidak adjustment 0.0) or grazers (p=0.). This indicates that the diet of captive browsers was generally more abrasive compared to the free-ranging browsers. Numerically, the grazer score was 0. higher in the wild, indicating that some grazers in captivity

13 received a less abrasive diet compared to the wild. Quartile ranges of score differences indicate less variability between free-ranging and captive browsers ( ) and intermediate feeders ( ) as compared to grazers ( ). Figure here 0 Plotting difference score versus hypsodonty index (from Janis ) separates the major feeding traits along the hypsodonty gradient, with browsers between. and., and grazers between (Syncerus caffer) and. (Damaliscus lunatus) (Fig. ). The difference in score was positively correlated to the hypsodonty index (R=0., p<0.00). Figure here In contrast, the difference in mesowear score was not correlated (p=0.) to the average body mass of the species taken from Janis (0) (Fig. ). Figure here 0 DISCUSSION This study demonstrates a significant difference in the tooth wear pattern between free-ranging and captive ruminants. Compared to free-ranging populations, most

14 0 0 captive browsers show a much more abrasion-dominated dental wear signal. The reverse applies to captive grazers, which tend to show a less abrasion-dominated wear signature in captivity than in the wild. Intermediate feeders are intermediate. The diet in captivity thus seems to obliterate differences in dental wear patterns between the feeding types, which differed significantly in the free-ranging but not in the captive populations. The range of diets offered in captivity evidently does not span the range consumed in the wild, not for the extreme grazers, and in particular not for the browsers. Diets in captivity therefore can be roughly characterized as undifferentiated diets levelling the impact of dietary abrasiveness on the animals dentitions. There are some limitations to this study. Although an effect of age was indirectly controlled for by the exclusion of particularly worn teeth, an age bias between the two populations cannot be ruled out with absolute certainty. Nevertheless, general qualitative differences in the mesowear parameters, such as the fact that in giraffe, Clauss et al. (00) found that the proportion of sharp cusps was not influenced by tooth position in captive giraffes, are indicative of fundamental differences in tooth wear and not only differences in wear degree due to age. The evident conclusion is that this difference must be a result of the difference in diets ingested by the freeranging and captive populations. Another limitation of this study is that individual feeding records for the captive animals investigated were generally unavailable. In order to achieve a sufficient sample size, individuals had to be included that had been kept in captivity between 0-, with the majority of animals between 0-0. Therefore, a direct conclusion for a particular feeding regime cannot be made, and it cannot be stated with certainty whether our findings are representative for ruminants recently or

15 0 0 currently kept at zoological institutions. However, for giraffe, Clauss et al. (00) documented that the diets generally in use during the major period of sampling (0-0) were, if published feeding recommendations of the times are compared, not specifically different from current diets in European zoos. With few exceptions, the captive signal of intermediate feeders was only slightly shifted towards the more abrasion-dominated end of the mesowear continuum. This indicates that this feeding group experiences the least degree of difference in dietary abrasiveness between the wild and captivity. Whatever the botanical differences, the abrasiveness of diets fed in captivity appears to resemble the abrasiveness encountered by the intermediate feeders of this study quite closely. In contrast, the two extreme feeding types show differences between the wild and captivity that indicate considerable differences in the abrasiveness faced in the two environments. Grazers are generally considered less sensitive to abrasives in their diet, and in captivity, this group appears less prone to feeding problems compared to browsers (Clauss et al., 00). Grazing species have an increased dental resistance towards abrasives in the diet as reflected by increased tooth crown height (Fortelius, ; Janis, ), and specific shearing adaptations in the occlusal pattern (Archer and Sanson, 00). In a comparison of three macropod species, enamel hardness was greater in the grazers than in the browsing species (Palamara et al., ); however, for ruminants no such data are available to date. Abrasiveness of the diet may have two general sources. The cell walls of monocotyledons may contain a high concentration of silica phytoliths (Kaufman et al., ; Carnelli et al., 00), the abrasiveness of which is considered as an adaptive response to overgrazing by ungulates (Baker et al., ; McNaughton et al., ). In contrast to monocotyledons, dicotyledons have fewer silica phytoliths, so that browsing

16 0 0 ungulates encounter less endogenous abrasives when compared to grazers. Feeding grazers with a grass hay-dominated diet is common practice in zoo animal husbandry (Lintzenich and Ward, ). Grass hay in zoo diets is mostly not gathered from the natural habitat of the species fed, nor is it grown in the same climate zone. McNaughton et al. () summarize literature data that indicate that cultivated forages contain distinctively less silica than Serengeti grasses. Since all zoological Institutions that provided material to this study are situated in the temperate climate zone, it must be considered likely that the grass hay fed to the animals investigated had lower concentrations of silica. A recent exploratory study (Sanson et al., 00) revealed that isolated silica phytoliths are softer than enamel tissue. The authors concluded that the dental wear pattern typical for grazers might not be related to the abrasiveness of phytoliths but rather to the exogenous grit and dust deposited on consumed plants. Although this work is controversial (Merceron et al., 00), and although an experimental study has shown that an increased silica content of monocot species reduces the plant acceptability by a herbivore (Massey et al., 00), it nevertheless indicates that contamination of food plants by exogenous grit has probably been severely underestimated as a source of abrasives in free-ranging ungulates. The effect of grit has, so far, only been investigated once in several populations of Australian sheep, in which tooth wear was a direct function of the amount of soil ingested (Healy and Ludwig, ). A very general relationship seems to be established between the amount of exogenous grit in the natural habitat and water availability. Generally, more grit should accumulate on plants in dry environments. Kaiser and Rössner (00) positively tested this hypothesis in Miocene environments of Southern Germany by showing that browsing ruminants in a humid wetland environment had

17 0 0 less abrasion-dominated mesowear signatures than contemporaneous communities from adjacent karst environments. Climate proxy studies by Kaiser and Schulz (00) indicate that this relationship also applies to zebra habitats in Sub-Saharan Africa, where plains zebras (Equus quagga) from dryer habitats had a more abrasion dominated mesowear signature than the same species in more humid environments. Forages fed in captivity, even if similar in botanical composition, most likely contain less grit than the food of many wild ruminants, as they usually do not originate from arid regions and are harvested with professional agricultural techniques that aim to minimize soil contamination. Additionally, food presentation practice in zoos usually comprises measures against the contamination of feedstuffs with grit or soil (Martin Jurado et al., 00). These factors most likely explain the observation that in several grazers, more abrasion was evident in free-ranging animals. From a clinical point of view, a less abrasion-dominated tooth wear pattern does not appear problematic. On the contrary, if one accepts that dental wear is one of the major factors limiting longevity (Robinson, ; Verstraete et al., ; Kojola et al., ), then a logical hypothesis deriving from this study would be that on average, captive grazers should achieve longer lifespans than both captive browsers on the one and free-ranging grazers on the other hand. In contrast, the findings in browsing ruminants are more alarming. Irrespective of body mass (Fig. ), the browsers investigated showed wear patterns indicative of a more abrasive diet in captivity than in the wild. The only exception was the greater kudu, a browser (Gagnon and Chew, 000; Sponheimer et al., 00) whose natural mesowear pattern already indicates a comparatively high proportion of abrasive dietary elements (Fortelius and Solounias, 000). Thus, the results support the hypothesis forwarded in Clauss et al. (00) that not only captive giraffe, but many

18 0 0 other captive browsing ruminants show abnormal dental wear patterns due to a higher proportion of abrasive elements in the diets offered to these species. Two questions arise from these findings: what are the causes for the increased abrasiveness in captive browsers diets, and are there any potential adverse clinical consequences? One evident cause for a discrepancy in abrasiveness between the diet of free-ranging and captive browsers could be the feeding of grass hay to these species. In moose, for example, a survey revealed that of facilities (%) offered grass hay but only (%) used lucerne hay (Clauss, 000). In giraffe, a European diet survey showed that % of 0 respondents were offering grass hay regularly (in addition to lucerne hay) to their giraffe; in two facilities, grass hay was the only roughage used (Hummel et al., 00). Similar data for other browsers is missing, to our knowledge. In general, the use of lucerne hay is advocated in browsing species (Lintzenich and Ward, ). Even if grass hay cannot be regarded as the sole culprit for the increased dental wear in browsers documented in this study, its use is to be discouraged with respect to its potentially detrimental effect of tooth wear in these species. Another likely candidate for the introduction of abrasive elements into the diets of captive browsers are pelleted compound feeds in general. Clauss et al. (00) documented that whereas silicate levels (measured as acid insoluble ash) are low in lucerne and dicot foliage, they are considerably higher in grass products as well as pelleted compound feeds used in captive giraffe and other zoo herbivores. Whether this is due to the inclusion of monocot material into pelleted feeds, the silicate content in mineral premixes, or the inclusion of high-silica components for technical reasons (to enhance material flow in the pelleting machines) remains to be investigated as well as a feasible potential to reduce the apparent abrasiveness of many current pelleted feed compounds, should this ever be

19 0 0 aimed at. In browsers, grit adhesion as a reason for excessive tooth wear appears less likely than in grazers, as most browsers are not fed at ground level in zoos. The clinical relevance of the observed increased tooth wear in captive browsers can also only be speculated upon. There is limited evidence that the teeth of browsers are less adapted to the comminution of zoo diets than the teeth of grazers (Hummel et al., 00), and excessive wear might exacerbate this situation. No comparative data exists to test the evident hypothesis that captive browsers should have, on average, shorter life spans than captive grazers of comparable body size, due to their abnormal tooth wear. Detailed studies on the effect of tooth wear on food and energy intake exist in two species only, the red deer (Cervus elaphus) and the koala (Phascolarctos cinereus). Pérez-Barbería and Gordon () demonstrated that in red deer, increased tooth wear was correlated with lower voluntary food intake and less effective food comminution; therefore, even if digestibility itself was not affected, digestible energy intake decreased. In the long run, this would lead to a loss of body condition. Skogland () and Kojola et al. () had already found a lower body condition in wild reindeer populations with high tooth wear. In correspondence to this concept, Martin Jurado et al. (00) found that captive wild ruminants with excessive tooth wear were often in a bad nutritional state and showed serous atrophy of body fat stores at necropsy, a sign of energy depletion. In captive giraffe, serous fat atrophy is a well-recognized problem (Fowler, ; Junge and Bradley, ; Clauss et al., 00; Potter and Clauss, 00), and excessive tooth wear has been stated explicitly as one of the potential, contributing factors (Enqvist et al., 00; Clauss et al., 00). In free-ranging koalas, animals compensate for increasing tooth wear by increasing feeding time, chewing intensity, and leaf intake (Logan and Sanson, 00); however, the authors speculated that these

20 0 compensatory mechanisms would have to fall short at some advanced stage of wear. Thus, although direct evidence is lacking, some negative consequences of the increased tooth wear in captive browsing ruminants can be suspected. Browsing ruminants have for a long time been considered more difficult to maintain in captivity than grazers (Renecker, 00; Clauss et al., 00; Clauss and Dierenfeld, 00), and the low abrasiveness found in their natural diet might be one other reason to ensure a consistent supply of browse material as the bulk feed for these animals, as e. g. facilitated by the use of browse plantations and particular preservation techniques for times of low browse availability (Hatt and Clauss, 00; Höllerl et al., 00; Schlegel et al., 00). The use of diets that result, especially in browsing species, in a non-natural tooth wear pattern, might also have an influence on the potential survival of individuals that are released in re-stocking programmes. Animals that are released into the wild with an abnormal tooth wear might be less fit for survival in their natural habitat; even if the animals then feed on their natural diet, an abrasion-induced high tooth wear cannot be reversed. The question whether similar effects can be demonstrated in other captive browsing species, such as tapirs or browsing rhinoceroses, remains to be investigated. 0 Acknowledgments: We thank the following museum collections for providing access to ruminant skull specimens in their care: Zoological Institute and Museum, Copenhagen, Zoological Museum, Universität Hamburg, Forschungsinstitut und Naturmuseum Senckenberg, Frankfurt, Museum für Naturkunde Berlin, Staatliches Museum für Naturkunde Stuttgart, Naturwissenschaftliche Staatssammlungen München, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn,

21 0 0 Institute of Palaeoanatomy, Domestication Research and History of Veterinary Medicine, Ludwig-Maximilians-University Munich. We thank the Deutsche Forschungsgesmeinschaft (DFG) for generously supporting this work (KA /- and CL /-). TMK and ES thank Regine Brandenburg and Erika Becker for technical assistance in casting, scoring and data base management. We are further grateful to Nikos Solounias (New York) and Mikael Fortelius (Helsinki) for sharing their original mesowear counts from Fortelius and Solounias (000) with TMK. MC thanks Sandra Henkel-Zuber, Corinna and Klaus Vestner, Anne Weiss, and Marthe and Manfred Clauss for their hospitality during the travel stage of this project. The comments of two anonymous referees improved the quality of this manuscript. 0

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29 Table. Mesowear scoring of upper molars and in wild and captive ruminants investigated in this study. For an explanation of scoring parameters, see Fig.. Figure. The mesowear variables (Fortelius and Solounias, 000) of a brachydont cheek tooth (upper left second molar; free-ranging male moose (Alces alces) ZMH- from Vänersborg, Sweden). The occlusal relief (OR) may be scored high (h) or low (l), the cusp shape (CS) is classified as sharp (s), round (r) and blunt (b). 0 Figure. Scheme for the grading of dental wear stage used to decide whether a specimen was included or excluded in the study. Due to differential wear depending on hypsodonty of the tooth, different grades were included for brachydont, mesodont or hypsodont species. 0 Figure. Comparison of mesowear scores of individual species. Note that the range of mesowear scores, in particular with regards to very high scores, is lower in captivity (the grey shaded area) than in the wild. Browsers in captivity show a more abrasion dominated mesowear signal (high score). Captive grazers show the reverse trend. Scores of wild ranging species computed based on original mesowear counts from Fortelius and Solounias (000). BR = browsers, IM = intermediate feeders, GR = grazers. Browsers: Alces alces (AA), Capreolus capreolus (CC), Giraffa camelopardalis (GC), Odocoileus hemionus (OH), Odocoileus virginianus (OV), Okapia johnstoni (OJ), Tragelaphus euryceros (TE), Tragelaphus scriptus (TS), Tragelaphus strepsiceros (TT).

30 Intermediate-feeders: Aepyceros melampus (Me), Antidorcas marsupialis (Ma), Boselaphus tragocamelus (Btr), Capricornis sumatraensis (Ca), Cervus elaphus canadensis (Cec), Gazella granti (Gg), Gazella thomsoni (Gt), Ovibos moschatus (Om), Taurotragus oryx (To), Tragelaphus angasi (Ta). Grazers: Alcelaphus buselaphus (ab), Bison bison (bb), Connochaetes gnou (cg), Connochaetes taurinus (ct), Damaliscus lunatus (dl), Hippotragus equinus (he), Hippotragus niger (hn), Kobus ellipsiprymnus (ke), Oryx gazella gazella (og), Redunca redunca (rr), Syncerus caffer (sc). 0 Figure. Mean difference in scores according to feeding type. Note that the diet of captive browsers was generally more abrasive compared to the free-ranging browsers. The grazer average score indicated that grazers in captivity had to cope with a less abrasive diet. BR = browsers, IM = intermediate feeders, GR = grazers. Figure.. Difference in scores versus hypsodonty index (from Janis ) separates the major feeding traits along the hypsodonty gradient with browsers and grazers at the extremes. Note the increase in score difference with increase in hypsodonty. BR = browsers, IM = intermediate feeders, GR = grazers. 0 Figure.. Difference in score versus body mass (after Janis 0). Note that the difference in mesowear score is not related to the average body mass of the species. BR = browsers, IM = intermediate feeders, GR = grazers.