DENTAL ABNORMALITIES OF EIGHT WILD QINLING GIANT PANDAS (AILUROPODA MELANOLEUCA QINLINGENSIS), SHAANXI PROVINCE, Author(s): Yipeng Jin, Si Chen, Yanqiao Chao, Tianchun Pu, Hongqian Xu, Xiaobin Liu, Kaihui Zhao, Yonggang Nie, Wei Wei, and Degui Lin Source: Journal of Wildlife Diseases, 51(4):849-859. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/2014-12-289 URL: http://www.bioone.org/doi/full/10.7589/2014-12-289

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. DOI: 10.7589/2014-12-289 Journal of Wildlife Diseases, 51(4), 2015, pp. 849–859 # Wildlife Disease Association 2015

DENTAL ABNORMALITIES OF EIGHT WILD QINLING GIANT PANDAS (AILUROPODA MELANOLEUCA QINLINGENSIS), SHAANXI PROVINCE, CHINA

Yipeng Jin,1 Si Chen,1 Yanqiao Chao,1,5 Tianchun Pu,2 Hongqian Xu,1 Xiaobin Liu,3 Kaihui Zhao,3 Yonggang Nie,4 Wei Wei,4 and Degui Lin1,5 1 Clinical Department, College of Veterinary Medicine, China Agricultural University, Haidian District, Yuanmingyuan Xi Lu #2, 100193, People’s Republic of China 2 Beijing , , Wai Dajie #137, Beijing 100044, People’s Republic of China 3 China Foping National Nature Reserve, Hanzhong, Foping Heti Jie #48, Shaanxi 723400, People’s Republic of China 4 Institue of Zoology Chinese Academy of Sciences, Haidian District, Beichen Xi Lu #1, Building #5, Beijing 100049, People’s Republic of China 5 Corresponding authors (email: [email protected] [D.L.]; [email protected] [Y.C.])

ABSTRACT: Eight adult (six male and two female) wild Qinling giant pandas (Ailuropoda melanoleuca qinlingensis) from China National Foping Nature Reserve were tracked, and their dental data collected and recorded from October 2010 to April 2014. Each panda had dental abnormalities of varying severity. Dental wear and fracture were the most common conditions. Absent teeth were common, with premolars missing most often. Mild caries were present in five molar teeth between two animals. Different degrees of dental plaque and calculus occurred in all animals but without severe periodontal disease. Two animals with severe dental abnormalities died due to intestinal problems. Large segments of bamboo were found in their intestinal tracts, and intestinal perforation and ulcers were evident, indicating dental abnormalities can be an important factor in the health of wild giant pandas and may lead to death. Further research with larger sample sizes of wild and captive giant pandas will be required to substantiate the relationship between dental abnormalities and mortality in giant pandas. Key words: Dental abnormalities, dental fracture, periodontal disease, tooth wear, wild .

INTRODUCTION Ailuropoda melanoleuca sichuanensis, are recognized on the basis of cranial features, Dental health, especially in wild animals, color patterns, and genetics (Wan et al. is important for survival. Without proper 2003, 2005). The Qinling subspecies, A. m. treatment, dental abnormalities may lead to qinlingensis, lives only in the Qinling oral pain, difficulty foraging or hunting, and Mountains in Shaanxi Province and has anorexia (Wallach and Boever 1983; Bel- seven regional populations, totaling 273 lows 2004; Holmstrom et al. 2004). Sec- pandas (Lu et al. 2001; Liu et al. 2002, ondary complications, such as malnutrition; 2009; Hu and Wei, 2004; Feng et al. 2009). gastrointestinal, cardiovascular, and renal The panda population in these mountains diseases, isolation from feeding territory, has a unique distribution pattern and and other systemic disorders can be fatal evolutionary history. They are different (Wallach and Boever 1983; Stromquist et al. from the mainstream population of A. m. 2009; Jin et al. 2012). Although dentistry is sichuanensis in morphology and molecular well practiced in veterinary science, most biology (Lu et al. 2001; Loucks et al. 2003; research and practice are focused on Wan et al. 2003, 2005; Liu et al. 2009). companion and domestic animals. System- Nonetheless, the habits and diet of Qinling atic studies on wild giant pandas (Ailur- pandas are similar to the pandas in opoda melanoleuca) are rare (Wenker et al. Sichuan. They are territorial, solitary 1999; Hu 2001; Stromquist et al. 2009; Jin animals in the wild (Schaller et al. 1985; et al. 2012). Tang 1992). The average lifespan of a wild Two subspecies of giant panda, Ailur- giant panda is about 20 yr, compared with opoda melanoleuca qinlingensis and 25–30 yr for captive giant pandas (Hu

849 850 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 4, OCTOBER 2015

2001; Jin et al., 2012). They primarily routine physical examinations, blood and fecal spend their lives roaming and feeding in sample collections, GPS collar fitting, or collar % check and battery change. Pistol systems (Dan- bamboo forests. The diet is 95–99 Inject, Børkop, Denmark) were used for bamboo and occasionally other vegetation remote drug delivery for immobilization. We or carcasses of small animals (Schaller et al. used 3-mL darts with 2.0340-mm, plain 1985, 1989; Tang 1992; Hu 2001). Because needles to inject a mixture of dexmedetomi- bamboo is poor in nutrients, giant pandas dine and zolazepam-tiletamine intramuscularly must eat large amounts and different kinds into the lateral hip region. The anesthetic formulation was 8 mg/kg dexmedetomidine of bamboo to fulfill essential nutrient (Dexdomitor, Orion Cooperation and Orion requirements. They spend about 14 h/ Pharm, Espoo, Finland) and 2 mg/kg zolaze- d consuming 12–38 kg of bamboo (Reid et pam-tiletamine (Zoletil 100 Injectable Anes- al. 1989; Schaller et al. 1989; Tang 1992; thetic/Sedative for Dogs, Cats, Zoo, and Wild Loucks et al. 2003). animals, Virbac Pty. Ltd., New South Wales, Australia; Mainka and He 1993; Jin et A normal adult giant panda has 42 teeth, al. 2012; Reed et al. 2012). The anesthetic including incisors (I), canines (C), premolars protocol was derived from previous anesthetic (P), and molars (M) with a dental formula of data, experience, and the animals’ body condi- 2 (I 3/3, C 1/1, P 4/4, M 2/3; Huang 1993). tion. The duration of anesthesia was approxi- Captive Sichuan giant pandas at Beijing Zoo mately 60 min, allowing for physical examina- tions, sample collecting, dental examination, have a high prevalence of dental caries, tooth and dental radiology. The general health status wear, and tooth loss (Jin et al. 2012). of all pandas is summarized in Table 1. Here, we report a systematic dental case study of wild Qinling giant pandas. We Dental examination evaluated the complete dental and peri- Y.J. conducted all dental examinations and odontal status of wild Qinling giant pandas, radiology. Results were recorded on a dental compared results with captive giant pandas examination chart modified for giant pandas and other bear (Ursidae) species, and (see Appendix). Three categories with nine reveal the importance of dental health for indices were evaluated for each tooth and graded accordingly. The first category was oral giant panda survival in the wild. hygiene, which includes the plaque index (PI) and calculus index (CI). The second was tooth MATERIALS AND METHODS abnormalities, which includes the tooth fracture index (Fr), tooth wear index (W), caries index, Study animals and immobilization discoloration, tooth absence, supernumerary, This is a joint research project lead by the and pulp exposure (PE). The third category was China National Foping Nature Reserve and the surrounding periodontal structures, which China Agriculture University, Department of includes gingival index, periodontal index, Veterinary Medicine, approved by the China mobility index (M), and furcation involvement National Foping Nature Reserve Committee. index. For a detailed index system for evaluation From November 2010 to April 2014, eight wild and grading, see Appendix. adult Qinling giant pandas (six males and two The overall occlusion was evaluated and females) were tracked at the China National recorded. Periodontal pocket depth was mea- Foping Nature Reserve (33u339to 33u469N, sured with a dental explorer probe (Jorvet- 107u419to 107u559E) in Shaanxi Province as 937cn-Explorer/Probe 23/12, Jorgensen Labo- a routine procedure to assess this endangered ratories Inc., Loveland, Colorado, USA; Bel- species’ health status and to check the GPS lows 2004; Holmstrom et al. 2004), and the device and battery. Dental inspection is added deepest single site was recorded. A dental as a comprehensive examination for assessing decay was defined as a discolored area of the the health of the pandas. Seven of these tooth surface in which a dental probe could be animals were tracked by using their original inserted and when removed had slight re- GPS collars (custom made by Zhongke Xintong sistance (Harvey 1985; Bellows 2004; Holm- Information and Technology Co., Ltd., Shenz- strom et al. 2004; Stromquist et al. 2009). A hen, China). One animal’s collar was lost, and decayed tooth has a rough and coarse inner the panda was tracked and recollared. Three surface of the cavity. Tooth wear was classified (pandas 1, 5, and 8) were tracked and examined according to the progressive loss in the overall again in 2014. All animals were immobilized for surface of the tooth in all planes (mainly, the JIN ET AL.—DENTAL HEALTH OF WILD GIANT PANDAS 851

TABLE 1. General information describing eight wild Qinling giant pandas (Ailuropoda melanoleuca qinlingensis) from the China National Foping Nature Reserve, Shaanxi Province, China. Pandas were tracked, and dental data were collected and recorded October 2010–April 2014.a

Pocket Date of Age Existing health depth Other examination ID (yr) Sex problems Occlusion (mm) pH comments

7 March 2007 1 7–8 M Scars on face See other 1 8.6 Complicated fracture and neck comments of 304 and mandible 16 December 2010 2 8–10 M Scars on face Normal 2 8.3 None and neck 6 March 2011 3 5–6 F None Normal ,1 8.7 None 28 February 2011 4 14–16 M Massive intestinal Normal 1 8.4 Severe tooth wear ulcers, malnu- and fractures trition and death 8 March 2011 5 7–9 F None Base narrow 2 8.2 None 21 January 2011 6 7–8 M Scars on face Normal 1–2 8.4 Fracture of maxillary and neck incisors December 12 2010 7 13–14 M Scars on face Normal 2 8.1 None and neck 12 March 2011 8 19–20 M Scars on face Normal ,1 8.5 Collar was lost, and neck recollared 22 February 2014 1 10–11 M Scars on face Normal 3 8.4 Healed mandibular and neck fracture 2 March 2014 5 10–12 F Alert with infant, Base narrow 2 8.3 Severe tooth wear on great weight loss all lingual sides of mandibular canines 4 March 2014 8 10–11 M Colon perforation, Normal 2 8.1 Severe tooth wear, peritonitis, septice- fractures and mia, malnutrition, pulpitis death Average pH value 8.4 a ID 5 animal identification number; M 5 male; F 5 female. occlusal, lingual, and buccal), which results in Dental radiology a smooth and fine surface. Teeth were defined Dental radiology was performed on all teeth by as absent when all tooth structures, including using a portable intraoral dental radiology crown and root, were absent during oral exam machine (ADX4000 Digital Radiography System, and on dental radiographs (Harvey 1985; Dexcowin Co., Ltd., Seoul, Korea). The sensor of Bellows 2004; Holmstrom et al. 2004; Strom- the portable digital x-ray machine is small; so quist et al. 2009). Dental plaque was evaluated several small images were needed for a complete by applying a thin layer of plaque disclosing x-ray image of one tooth. All teeth and periodon- agent (iC Plaque; iM3 Pty. Ltd. Australia, tal structures were evaluated (Fig. 1B), and Lane Cove, New South Wales, Australia) on findings were compared with the dental exami- the tooth surface and graded accordingly nation findings. Statistical analysis was done by using Statistical Product and Service Solutions (Fig. 1A). Oral pH was measured by using (SPSS China, Shanghai, China) for correlations a portable pH meter (FiveGo pH Meter, between all indexes, age, and sex. Mettler-Toledo Inc., Columbus, Ohio, USA). The pH measurements were taken three times, and the average was recorded. The RESULTS Appendix shows all indices inspected and the Study animals grading scales used. The tooth numbering system used is the modified Triadan system The estimated age for study animals (Floyd 1991). ranged 5–20 yr at the time of examination. 852 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 4, OCTOBER 2015

FIGURE 1. Examples of dental abnormalities observed in Qinling giant pandas (Ailuropoda melanoleuca qinlingensis) examined at the China National Foping Nature Reserve, Shaanxi Province, China, November 2012–April 2014. (A) Plaque examination of female panda 5 by using plaque disclosing agent. Note mild dental plaque and calculus. (B) Dental radiology showing moderate tooth wear on lower right premolars JIN ET AL.—DENTAL HEALTH OF WILD GIANT PANDAS 853

Ages were estimated based on the time of (I5265) had plaque. Canines, premolars, collar fitting, dental condition, animal’s and molars were the most affected (100% appearance, health status, and individual of 32 canine; 79.7% of 102 premolars; history. All animals bred naturally in the 100% of 80 molars). Incisors were the wild. One male (panda 4) had massive least affected. (PI1, n534; PI2, n517). intestinal ulcers that caused severe mal- Most teeth had PI2 (n5125); 48.5% of nutrition and died soon after examination. teeth had calculus (n5163). Molars were All six male pandas had scar tissue on the most affected (88%;CI1,n560; CI2, facial and neck area, probably due to n510). No teeth were graded CI3. No fighting during mating season. statistical correlation was found between Pandas 1, 5, and 8 were tracked and plaque and calculus prevalence. Detailed examined again in 2014. Panda 5 had dental examination results of 2011 are a nursing juvenile and had lost significant summarized in Table 2. weight since the 2011 examination. Panda 8 had severe health problems (Table 1) Tooth abnormalities and died 8 d after return to the reservation All animals had oligodontia, and 10% of base. Postmortem examination revealed teeth were absent (n533). Absent teeth death was due to peritonitis and septice- include 101, 103, 201, 301, 303, 401, 105, mia. Existing health problems and general 106, 205, 206, 305, 306, 405, and 406. condition for other pandas are summa- First premolars were the most frequently rized in Table 1. absent teeth (n518). No supernumerary teeth were found. Seven of eight pandas General dental examination had tooth discoloration. Incisors were the We examined 303 teeth. The average most affected (20%, n519). pH value was 8.4. Panda 5 had a base Six pandas (five males and a female) had narrow occlusion causing severe wear on tooth fractures. All fractures occurred on the lingual side of all mandibular canines incisors and canines (n532 and n521), and incisors (Fig. 1C). Panda 1 had and canines had the highest prevalence a complicated fracture on tooth 304 (66%), with grade Fr1 being the most (Fig. 1D). Panda 6 had a fractured maxilla common (n513). Of incisors, 33% were due to trauma (Fig. 1E). Existing health fractured (n532). No statistical correla- problems and general comments are tions were found between fracture, tooth summarized in Table 1. discoloration, and PE, but all Fr3 and Fr4 teeth showed discoloration and visible Oral hygiene pulpitis. Various degrees of plaque and calculus No pandas had tooth caries during 2010 were found in all pandas; 78.9% of teeth to 2011.

r (teeth 407 and 408; see Appendix) without pulp exposure. (C) Female panda 5 with base narrow occlusion that caused tooth wear on the lingual side of 104 and 204. Severe tooth wear was also observed on all maxillary and mandibular incisors. (D) Male panda 1 with fracture on 304 and mild tooth wear on all mandibular incisors and upper incisors, 103, 202, and 203. Chip fracture is evident on tooth 101. Teeth 102 and 201 were shorter than other upper incisors, indicating a complicated tooth fracture. (E) Male panda 6 with maxilla fracture. Teeth 103, 203, and 204 showed tooth wear W2. Tooth 104 was significantly shorter than 204, indicating complicated tooth fracture. (F) Male panda 4 with severe tooth wear on maxillary premolar and molars. (G) Radiography shows relatively symmetrical tooth wear pattern of panda 1. Tooth 305 is absent, and the data point is omitted. (H) White arrow indicates radiolucent area of the furcational bone of panda 8. Black arrow points to lucency due to decalcification and loss of a portion of the occlusal crown, consistent with tooth decay on tooth 407. 854 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 4, OCTOBER 2015

TABLE 2. Results of dental examinations for eight Qinling giant pandas (Ailuropoda melanoleuca qinlingensis) from the China National Foping Nature Reserve, Shaanxi Province, China, 2011. See Appendix for explanation of grade and categories of dental problems.

No. of teeth

Prevalence of Total Dental problems Teeth type Grade 1 Grade 2 Grade 3 Grade 4 Total abnormalities (%)a prevalence (%)b

Plaque Incisors 34 17 0 N/Ac 51 53 78.9 Canines 2 22 8 N/A 32 100 Premolar 31 39 32 N/A 102 79.7 Molar 0 47 33 N/A 80 100 Calculus Incisors 3 0 0 N/A 3 3 48.5 Canines 21 1 0 N/A 22 69 Premolar 49 19 0 N/A 68 53.1 Molar 60 10 0 N/A 70 87 Fracture Incisors 7 9 8 8 32 33 15.8 Canines 13 1 3 4 21 66 Tooth wear Incisors 17 35 31 N/A 83 86 88.1 Canines 28 0 1 N/A 29 91 Premolar 82 19 5 N/A 106 82.5 Molar 31 36 11 N/A 78 97 Discoloration Incisors N/A N/A N/A N/A 19 20 8.6 Canines N/A N/A N/A N/A 6 19 Premolar N/A N/A N/A N/A 2 1.6 Molar N/A N/A N/A N/A 2 2 Absence of teeth Incisors N/A N/A N/A N/A 11 11 9.8 Premolar N/A N/A N/A N/A 22 17.2 Gingivitis Incisors 12 4 1 N/A 17 17 9.5 Canines 3 1 0 N/A 4 12 Premolar 9 2 0 N/A 11 8.6 Periodontitis Incisors 1 0 0 N/A 1 1 0.3 a Affected teeth/total number of the same type of tooth3100 (e.g., prevalence of caries of incisors5No. of incisors with caries/total No. of incisors58/85510%). b Total number of affected teeth/total number of teeth3100. c N/A 5 not applicable.

All pandas had different degrees of tooth periodontitis on 201. No furcation in- wear, involving 88.1% of teeth (n5296). volvement was found. Incisors were the most worn: 20% of incisors were graded W1 (n517), 41% (n535) were Dental condition in 2014 for three pandas graded W2, and 37% (n531) were graded When pandas 1, 5, and 8 were reexamined W3 (Fig. 1F). Canines and premolars were in 2014, all had increased severity of tooth the least worn. Tooth wear for all animals discoloration. Pandas 1 and 8 had additional was charted. Radiology indicated tooth wear tooth loss and fracture; pandas 5 and 8 had patterns for each panda were relatively caries in the grooves of the molar occlusal symmetrical (Fig. 1G). surface but with no advancement in peri- odontal pocket depth. The periodontal Periodontal examination pocket depths were advanced to 3 mm in Six pandas (all males) had mild gingivitis panda 1. Panda 5 had more severely worn affecting the incisors, canines, and pre- mandibular canines due to base narrow molars (n517, n54, and n511). All occlusion, and a tooth mobility of M1 on 205. animals had normal periodontal pocket Only panda 8 showed furcation involvement depth (0–2 mm), and no teeth showed on 407. Comparison of dental abnormality any mobility. Only one panda had mild findings are summarized in Table 3. JIN ET AL.—DENTAL HEALTH OF WILD GIANT PANDAS 855

TABLE 3. Comparison of dental examination records for three Qinling giant pandas (Ailuropoda melanoleuca qinlingensis) examined in 2011 and again in 2014. Data represent number of teeth affected (% of teeth of that type affected).

Dental problems Year ID Incisor Canine Premolar Molar Total

Teeth absent 2011 1 0 0 1 (6) 0 1 (2) 2014 1 5 (42) 0 2 (12) 0 7 (17) 2011 5 0 0 1 (6) 0 1 (2) 2014 5 0 0 1 (6) 0 1 (2) 2011 8 0 0 4 (25) 0 4 (10) 2014 8 2 (17) 0 5 (31) 0 7 (17) Discoloration 2011 1 1 (8) 0 0 0 1 (2) 2014 1 1 (8) 2 (50) 0 0 3 (7) 2011 5 3 (25) 0 0 0 3 (7) 2014 5 9 (75) 0 0 0 9 (21) 2014 8 2 (16) 4 (100) 2 (12) 4 (40) 12 (29) Caries 2014 5 0 0 0 2 (20) 2 (5) 2014 8 0 0 0 3 (30) 3 (7) Fracture 2011 1 2 (16) 2 (50) 0 0 4 (10) 2014 1 4 (33) 4 (100) 0 0 8 (19) 2014 5 5 (42) 3 (75) 0 0 8 (19) 2011 8 4 (33) 4 (100) 0 0 8 (19) 2014 8 4 (33) 4 (100) 0 0 8 (19) Tooth wear 2011 1 10 (83) 4 (100) 15 (94) 8 (80) 37 (88) 2014 1 12 (100) 4 (100) 15 (94) 10 (100) 41 (97) 2011 5 12 (100) 4 (100) 12 (75) 10 (100) 38 (91) 2014 5 8 (67) 3 (75) 14 (87) 10 (100) 35 (83)b 2011 8 12 (100) 4 (100) 14 (87) 10 (100) 40 (95) 2014 8 11 (92) 4 (100) 14 (87) 10 (100) 39 (93)b Gingivitis 2011 1 0 2 (50) 0 0 2 (5) 2014 1 1 (8) 0 0 0 1 (2) 2014 5 6 (50) 4 (100) 14 (87) 10 (100) 34 (81) 2011 8 12 (100) 4 (100) 8 (50) 10 (100) 34 (81) 2014 8 12 (100) 4 (100) 9 (56) 10 (100) 35 (83) Periodontitis 2014 5 2 (17) 0 0 0 2 (5) 2014 8 2 (17) 4 (100) 2 (12) 0 8 (19) Furcation involvement 2014 8 0 0 1 (6) 0 1 (2) Mobility 2014 5 0 0 1 (6) 0 1 (2) a ID 5 animal identification number. b Total tooth wear numbers in 2014 are less than 2011 because some teeth were missing.

Radiology Radiographic evidence of tooth decay Dental radiology findings were consis- was found on five molar teeth between tent with the dental examination results. two animals in 2014. No unerupted teeth were detected, and little evidence of periodontal diseases was DISCUSSION found. Radiographic changes were consis- In this systematic study of dental abnor- tent with pulpitis and apical periodontitis malities of wild Qinling giant pandas, we on canines, premolars, and molars. One found that all pandas had various degrees furcation involvement on tooth 407 was of dental abnormalities. Dental attrition evident (Fig. 1H). Damage of the enamel due to tooth wear was the most common caused by tooth wear was found on all abnormality. Tooth fractures were also severely damaged teeth, including inci- common, with canines and incisors being sors, canines, premolars, and molars. the most fractured teeth. Maxillary and 856 JOURNAL OF WILDLIFE DISEASES, VOL. 51, NO. 4, OCTOBER 2015 mandibular fractures were also found, but Tooth fracture and mandibular and tooth caries were rare. Periodontal disease maxillary bone fractures were common in was not found, but calculus and plaque wild pandas. The uniquely shaped canine varied with pandas and progressed over teeth were the most fractured, followed by time. Oligodontia was also common. incisors. Although they prefer tender Dental health is important for panda bamboo shoots and leaves, death and survival in the wild. Although, no statisti- regeneration of bamboo or a harsh season cal correlation between dental health and means pandas in the wild may have to eat mortality was found (likely due to the tough stems (Johnson et al. 1988; Reid et small sample size), both pandas that died al. 1989; Reid and Jinchu 1991; Liu et al. during the study had poor dental condi- 2002), causing trauma to their teeth. tion, systemic health problems, and mal- During mating season, males fight for nutrition before death. Poor dental health mates and better territories (Schaller et al. could cause anorexia, which would result 1985; Hu 2001). We observed that when in decreased bamboo intake and cause they fight, they bite their opponent’s neck malnutrition and weakness. A weak wild and face, locking teeth and throwing their panda will lose in territorial fights and be heads back and forth. Such behavior can forced to live in areas with low bamboo result in canine tooth fracture and maxilla density. With limited bamboo resources, or mandibular fractures (Fig. 1D, E). the animal would have to eat tough When compared with captive panda in bamboo stems to survive. Ingested bam- Beijing Zoo and other bear species, the wild boo fragments with sharp edges could giant panda’s diet contains more bamboo cause ulcers or perforation of the digestive and less sugar (Manville 1990; Tang 1992; tract, causing gastrointestinal disorders Hu 2001; Holmstrom et al. 2004; Zhang and other systematic problems and, final- 2004; Stromquist et al. 2009; Jin et al. 2012). ly, lead to death. Thus, deteriorating They are also younger than average age dental health in wild giant pandas could during examination, with more alkaline be life-threatening. saliva similar to Swedish brown bears Despite its taxonomic classification as (Ursus arctos; Stromquist et al. 2009). a carnivore, wild giant pandas are primar- Moreover, all captive giant pandas at the ily herbivorous, with a diet consisting of Beijing Zoo were Sichuan pandas, with 95–99% bamboo (Reid and Jinchu 1991; smaller skulls and smaller teeth that have Tang 1992; Huang 1993). However, they deeper and more uneven grooves (Wan et retain the digestive system of a carnivore, al. 2005; Liu et al. 2009; Jin et al. 2012); they and thus derive little energy and little also do not fight for mates or territory. protein from the consumption of bamboo These anatomic, dietary, behavioral, and (Hu 2001; Wan et al. 2003). Because the physiologic differences may explain the wild diet is low in nutrition, it is important for Qinling pandas’ fewer dental caries, greater a wild giant panda to keep its digestive tooth wear, and more severe tooth fractures tract full. An average wild giant panda eats compared with captive giant pandas and 9–14 kg of bamboo shoots for at least 14 h some other bear species. Similar to the a day (Reid et al. 1989; Reid and Jinchu captive panda study by Jin et al. (2012), all 1991; Tang 1992). Constant chewing and wild Qinling pandas had different degrees extensive use of the teeth result in severe of dental plaque and mild to moderate tooth wear (Fig. 1F). Tooth wear in most calculus, with increasing severity with age. wild pandas was symmetrical, indicating Serious periodontal disease was not found, that tooth wear may be mostly mechanical, because the flavonoid compound in bam- and wild giant pandas alternate the usage boo can act as an antiseptic and antioxidant; of their teeth, resulting in a symmetrical the bamboo fibers also can brush the tooth chewing pattern (Fig. 1G). surface preventing the formation of plaque JIN ET AL.—DENTAL HEALTH OF WILD GIANT PANDAS 857 and calculus (Tang 1992; Sato et al. 1996; Huang W. 1993. The skull, mandible and dentition of Williams et al. 2004; Zhang 2004; Jin et al. giant pandas (Ailuropoda): Morphological char- acters and their evolutionary implications. Ver- 2012). Oligodontia was common in wild tebr Palasiat 31:191–207. giant pandas as in captive giant pandas, with Jin Y, Lin W, Huang S, Zhang C, Pu T, Ma W, Lin D. first premolars being the most frequently 2012. Dental abnormalities in eight captive giant missing teeth (Jin et al. 2012). Further pandas (Ailuropoda melanoleuca) in China. research is needed to determine the reason J Comp Pathol 146:357–364. Johnson KG, Schaller GB, Jinchu H. 1988. Re- for the absence of the first premolar. sponses of giant pandas to a bamboo die-off. Natl Limitations of this study include the Geogr Res 4:161–177. small sample size of wild Qinling giant Liu S, Chen Y, Zhang M. 2009. Morphological and pandas. Dental plaque samples were not functional aspects of giant panda (Ailuropoda collected owing to equipment and legisla- melanoleuca) dentition from the Qinling Moun- tains. Acta Theriol Sin 29:332–337. tive constrains. We could not achieve long- Liu X, Skidmore AK, Wang T, Yong Y, Prins HHT. term follow up on all eight wild giant 2002. Giant panda movements in Foping Nature pandas. Our findings may have important Reserve, China. 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APPENDIX: CHART USED FOR QINLING GIANT PANDAS (AILUROPODA MELANOLEUCA QINLINGENSIS) DENTAL EXAMINATION