Dung beetles, but not rodents, contribute to brown bear feces removal, disaggregation, and secondary seed dispersal

Seed dispersal by endozoochory is essential to plant dynamics, but once released in the feces, the seeds face a hostile environment that is not always favorable to germination. Indeed, feces may contain inhibitors, have high seed density, and be densely structured. However, feces visitors such as vertebrates and invertebrates may play an essential role in secondary seed dispersal (SSD) and can alleviate the chemical and physical constraints of the feces. Yet, their relative roles in the dispersal of small- and medium-sized seeds are not well documented. In this study, we designed a field experiment in the French Pyrénées mountains to disentangle the relative role of vertebrate and invertebrate on feces removal, disaggregation, and secondary dispersal of small- and medium-sized seeds. We thus used 30 brown bear (Ursus arctos) fresh feces and separated each of them into three sub-samples submitted to different treatments allowing total access of any visitor, access restricted to invertebrates, and no visitor access, respectively. We inserted eight raspberry (Rubus idaeus) and five blueberry (Vaccinium myrtillus) marked seeds in each sub-sample to assess SSD. In parallel, we used camera and pitfall traps to document the presence of vertebrate and invertebrate visitors, respectively. After ten days, we weighed the fecal matter remaining, counted the remaining seeds, and assessed the feces disaggregation based on visual examination and objective criteria. We observed a significant effect of invertebrates on feces removal, disaggregation, and secondary dispersal of both seed species. Vertebrates did not visit the feces. Dung beetles caught in pitfall traps appear as the main secondary seed dispersers and disaggregation agents in this area. We also pinpointed that diet composition and structure of brown bear feces affect dung beetle attraction and activities. Our study in a temperate mountainous area identifies dung beetles as key agents in the disaggregation of large feces and secondary dispersal of small- and medium-sized seeds, with no evidence of rodents. Diet composition and the fecal matter trapping the seeds affect seed fate by modulating dung beetle activity. By releasing variable fecal contents, omnivorous primary seed vectors have an even more complex effect on seed fate than expected.