Based on continuous field investigations and camera-trap surveys from July 2012 to November 2018, we found that eight of the 20 dens were used by female giant pandas for birthing and rearing cubs. A total of 8 713 days of camera trapping were accumulated in the den sites, with total trapping time on the animal trail along the ridge of 74 283 days over 5.5 years. A total of 732 independent effective photos were taken by the infrared camera traps monitoring the giant panda dens, with 19 species of mammals and birds, belonging to six orders and 14 families, found to visit these dens (See Table 1, Figure 2).
Species No. of sites (n) No. of independent photos (n) Relative abundance index Protection category MAMMALIA Primates I Cercopithecidae 1. Rhinopithecus roxellana 1 2 0.02 I, EN, T, A Carnivora I Ursidae 2. Ursus thibetanus 1 2 0.02 II, VU, A II Ailuropodidae 3. Ailuropoda melanoleuca 3 130 1.49 I, VU, T, A Ⅲ Mustelidae 4. Martes flavigula 1 1 0.01 II, LC, C Ⅳ Viverridae 5. Paguma larvata 5 22 0.25 Ⅲ, LC, C Ⅴ Felidae 6. Prionailurus bengalensis 1 1 0.15 Ⅲ, LC, B Artiodactyla I Suidae 7. Sus scrofa 2 3 0.03 Ⅲ, LC II Cervidae 8. Muntiacus reevesi 1 1 0.01 Ⅲ, LC, T Ⅲ Bovidae 9. Budorcas bedfordi 3 15 0.17 I, VU, T, B 10. Naemorhedus griseus 1 1 0.01 II, VU, A Rodentia I Sciuridae 11. Tamiops swinhoei 1 2 0.02 Ⅲ, LC 12. Sciurotamias davidianus 9 355 4.07 Ⅲ, LC, T 13. Petaurista alborufus 3 25 0.29 Ⅲ, LC, T II Hystricidae 14. Hystrix brachyuran 2 6 0.07 Ⅲ, LC AVES Galliformes I Phasianidae 15. Tragopan temminckii 5 11 0.13 II, LC 16. Chrysolophus pictus 1 2 0.02 II, LC, T Passeriformes I Turdidae 17. Myophonus caeruleus 3 7 0.08 LC 18. Zoothera dauma 1 1 0.01 Ⅲ, LC II Timaliidae 19. Garrulax elliotii 1 1 0.01 Ⅲ, LC, T * Rat 9 144 1.65 Ⅲ, LC I: National Key Protected Species (Class I); II: National Key Protected Species (Class II); III: Species listed in “The List of Territorial Wildlife of National Protected Beneficial or Valuable Species for Economic and Scientific Research”. T: Endemic to China; LC: Least Concern; EN: Endangered; VU: Vulnerable; NT: Near Threatened; A, B, and C represent species listed in Appendix I, II, and III of CITES, respectively. *: Some rodents (rat) could not be given a species identification and are listed as a separate term.
Table 1. List of mammals and birds visiting giant panda dens recorded by camera traps in our study area
Figure 2. Important sympatric species recorded by infrared camera traps in giant panda dens in Foping National Nature Reserve
A total of eight birthing or cub-rearing events were recorded in the maternal dens during our survey. One event was well recorded by the infrared camera, lasting 21 days from the birth of a cub by a female giant panda in the den on 11 September until 02 October 2016. The female giant panda did not leave the den for the first five days after the cub was born. However, the time and frequency of the female leaving the den to forage or drink gradually increased from days 5 to 15 after the birth, and then remained stable after 15 days (Figure 3). To ensure the safety of the cubs, the average time that a mother left a den for foraging or drinking was 1.90±0.26 h.
We found that the probability of a den being visited by female giant pandas during the breeding season was negatively correlated with the presence of carnivores in the dens and the vicinity. The RAI of the presence of carnivores in the giant panda dens was 6.83±3.28. Female giant pandas also avoided using dens in areas that had a high RAI of Asian black bears (Wilcoxon rank sum test: W=153, P<0.05) and yellow-throated martens (Wilcoxon rank sum test: W=82.5, P<0.001). However, no obvious differences in the RAI of leopard cats were found between used and unused dens (Wilcoxon rank sum test: W=243, P=0.7347) (Figure 1B–D).
Four ungulate species utilized the giant panda dens for rest and shelter from the rain, including wild boars (Sus scrofa), Chinese muntjacs (Muntiacus reevesi), Chinese gorals (Naemorhedus griseus), and golden takins (Budorcas bedfordi) (Figure 2). In addition, based on the camera-trap photos, golden takins also licked the cliff-face of the dens for salt (three times) and pushed their heads into the dens (four times) (Figure 2). The RAI was 12.45±4.78 for the ungulates, which only appeared in dens unused by the female giant pandas, similar to the carnivores.
Interestingly, maternal giant pandas were not averse to the activity of rodents or terrestrial birds in or around the dens. The RAI of rodents and terrestrial birds was significantly higher in the used dens (164.91±5.54) than in the unused dens (51.90±17.45). Predators not only kill giant panda cubs but also prey on rodents and terrestrial birds. The frequent occurrence of these animals in and around giant panda dens may indicate the presence of fewer carnivores, and thus better suitability for pandas. The DSI of the used dens was significantly higher than that of the unused dens (Wilcoxon rank sum test: W=45, P<0.001) (Figure 4).
Impact of sympatric carnivores on den selection of wild giant pandas
- Received Date: 2019-12-18
- Accepted Date: 2020-04-10
- Available Online: 2020-04-16
- Publish Date: 2020-05-01
- Ailuropoda melanoleuca /
- Interspecific interference competition /
- Dens /
- Den suitability index
Abstract: Interspecific killing is a primary reason for the low survival rates of some animal species. The giant panda (Ailuropoda melanoleuca) is an altricial eutherian mammal and thus, in comparison to other infants, panda cubs are highly vulnerable, which may significantly influence the selection of breeding sites by females. Here, we used infrared camera traps to monitor giant panda dens for 5.5 years in Foping National Nature Reserve (FNNR) to determine how interspecific factors affect den selection by wild female pandas. Results indicated that Asian black bears (Ursus thibetanus), yellow-throated martens (Martes flavigula), leopard cats (Prionailurus bengalensis), and masked palm civets (Paguma larvata) visited the dens frequently, and the presence of these species negatively influenced den selection by female pandas. Interestingly, the presence of rodents and terrestrial birds appeared to indicate den safety, and female giant pandas were not averse and even preferred dens with a high abundance index of rodents and terrestrial birds. The den suitability index (DSI) was a reliable tool for evaluating whether dens were suitable for female giant pandas to give birth to and rear cubs, with preference for dens with high DSI values. This study increases our understanding of the den selection criteria of female giant pandas and the main threats to the survival of their cubs, thus providing important guidance for the conservation and management of this species.#Authors contributed equally to this work
|Citation:||Xin-Lei Lai, Wen-Liang Zhou, Hua-Lei Gao, Meng Wang, Kai Gao, Bao-Wei Zhang, Fu-Wen Wei, Yong-Gang Nie. Impact of sympatric carnivores on den selection of wild giant pandas[J]. Zoological Research, 2020, 41(3): 273-280. doi: 10.24272/j.issn.2095-8137.2020.027|