Indirect restoration of ecological interactions: reintroduction of a dung-beetle associated primate increases the recruitment of large seeds

Abstract

The biased loss of large and medium frugivores alters seed dispersal and plant regeneration. Species reintroductions have been proposed as a strategy to reverse the consequences of species loss. However, reintroductions effects on ecological processes are seldom accessed, which hinders the comprehension of reintroductions’ potential to reestablish functioning ecosystems. In this study, we investigate the effect of howler monkey (Alouatta guariba) reintroduction in the plant regeneration of Tijuca National Park (TNP), a highly defaunated Atlantic Forest fragment. Howlers are medium sized folivore-frugivore primates, whose large clumped defecations attract dung beetles. Dung beetles bury seeds present in howlers’ feces, a process known as secondary seed dispersal. Thus, we expect that the fate of seeds dispersed by howlers will differ from those dispersed by the other frugivores present in the Park. We followed the fate of seeds between 3 and 14mm in diameter in three steps of the seed dispersal loop, each consisting of a different experiment. First, we estimated secondary seed dispersal and burial depth probabilities according to the frugivores’ defecation pattern; then, predation probability in different burial depths and defecation patterns; and, finally, recruitment probability in different burial depths. Considering the final result of the three experiments, the howlers’ reintroduction affected positively the regeneration of large seeds. 3mm seeds did not benefit as much because they weren’t frequently predated at shallower depths and couldn’t recruit when deeply buried. Seeds larger than 3mm reached more frequently the seedling stage when dispersed by howlers than when dispersed by other animals present in the Park. Thus, howler monkey reintroduction in defaunated areas, consisting mainly of smaller frugivores, whose defecation pattern doesn’t attract dung beetles as frequently, improves the regeneration of large seeds. We hope that this study will stimulate the resuming of howler reintroduction in TNP, as well as new howler reintroductions in defaunated areas.