Yu Liu and Fangliang He
The Janzen-Connell (JC) hypothesis, proposed by Janzen (1970) and Connell (1971), stipulates that host-specific natural enemies near adult trees inhibit the establishment and later success of conspecific seedlings in the vicinity of adults, thereby releasing space for establishment of other tree species and thus promoting tree species coexistence (i.e., the JC effect). Soil pathogens, being dispersal-limited and host-specific, meet the critical prerequisites for natural enemies to induce the JC effect. Note that herbivores, including seed predators, were also proposed as an agent inducing the JC effect in Janzen’s original paper, but herbivore satiation after heavy seed rain (e.g., ‘mast seeding’) and indiscriminate attack by herbivores on seedlings of all species are inconsistent with the JC hypothesis. Therefore, we focus our review exclusively on the pathogen-induced JC effect. Despite the widespread appreciation of the JC hypothesis in explaining the maintenance of tree species diversity since it was proposed over 40 years ago, contradictory results for the JC effect have been obtained and its contribution to maintaining biodiversity remains controversial.
Our review adopts insights from the framework of the classic plant disease triangle (i.e., occurrence of a plant disease requires a virulent pathogen encountering its susceptible host plant under an environment conducive to disease development), which has been widely studied in crop diseases. Increasing attention has recently been paid to environmental factors in forest pathology, and we propose to link the disease triangle with the JC effect to address environmental factors which may obscure the detection of the JC effect. Through reviewing the literature, we present evidence that the intensity of the JC effect depends on the conditions where and when the specific pathogens and host plants occur as predicted by the disease triangle; in other words, the effect is context-dependent. Together with such context-dependence, the role of the JC effect in maintaining tree species biodiversity is expected to change under current climate change (e.g., elevated temperature and drought). Thus the importance of taking into account the indirect effects of climate change on tree species diversity should be highlighted in future studies (due to the changed JC effect), besides exploring the direct impacts of climate change on tree species (e.g., physiological stress).