Conspecific and heterospecific neighbors significantly affected ontogenetic tree mortality (Zhu et al., 2015). However, neighbors in different life stages than the focal tree showed inconsistent effects. In our study, we found that conspecific earlier and later stage neighbors had opposite effects on juvenile mortality. Heterospecific same and later stage neighbors also had opposing effects on sapling mortality. The later stage neighbors were the only group whose singular effect was mostly consistent with the effect of all neighbors combined. In short, failing to consider some life stages of neighbors might result in concluding that related environmental factors are more consequential than neighbor effects.
Mortality attributed to conspecific negative density dependence is significantly widespread in the sapling stage, but this effect weakens as the tree grows (Zhu et al., 2015; Yao et al., 2020). Meanwhile, heterospecific neighbors reduce tree mortality throughout all life stages. Previous studies have shown that mortality due to conspecific negative density dependence is caused by specialized natural enemies and/or intraspecific competition for resources (Janzen, 1970; Connell, 1971; Zhu et al., 2015). Saplings, as the earliest life stage, suffer to a greater degree from natural enemy damage and from intraspecific competition than do older trees (Weiner, 1990). Therefore, saplings are more strongly impacted by conspecific neighbors. This result is consistent with findings of previous studies showing that density-dependent survival at the seedling and sapling stages plays a significant role in fostering tree species coexistence and maintaining diversity in forests (Bai et al., 2012; Johnson et al., 2014; Lin et al., 2014; Yan et al., 2015; Yao et al., 2020). Unlike conspecific neighbors, denser heterospecific neighbors can effectively hinder the spread of specific natural enemies and reduce objective tree mortality (Wills and Green, 1995; Peters, 2003). This herd protection has also been found in other studies on conspecific negative density dependence (CNDD) (Comita and Engelbrecht, 2009; Zhu et al., 2015; Yao et al., 2020). Furthermore, heterospecific neighbors have a negative correlation with adult tree mortality. This result indicates that heterospecific trees survive better around adult trees, which consequently promotes species coexistence.
Clumping of conspecific later stage and heterospecific same stage neighbors contributes the most to sapling mortality. Saplings are the youngest trees in this study. They are more susceptible to natural enemies and are less competitive. Saplings could be subject to invasion upon the crowding of conspecific later stage neighbors because the neighbors could spread specific natural enemies, while also having asymmetric advantages in the competition for resources (Weiner, 1990; Clark and Clark, 1992; Uriarte et al., 2004; Yao et al., 2020). Consequently, conspecific later stage neighbors are the major contributor of all conspecific neighborhood effects to sapling mortality. In addition, conspecific later stage neighbors comprise the largest component of conspecific neighbors (Fig.S1). Thus, conspecific neighbors cause sapling mortality altogether (Fig. 3a), but this effect can be attributed mainly to conspecific later stage neighbors. This may also be why most studies on CNDD have found that the clumping of conspecific neighbors causes sapling mortality (Bai et al., 2012; Lin et al., 2014; Yan et al., 2015; Yao et al., 2020), even though these studies did not distinguish among conspecific neighbors’ life stage. In contrast, clumping of heterospecific later stage neighbors could reduce sapling mortality by hindering the spread of specific natural enemies (Peters, 2003). However, heterospecific sapling neighbors demonstrate the opposite effect, increasing focal sapling mortality. For one, herd protection is weakened in same stage heterospecific neighbors (Ramage et al., 2017), and they also have symmetric advantages in the competition for light resources, which can result in greater sapling mortality (Comita and Engelbrecht, 2009; Rüger et al., 2009; Bai et al., 2012; Piao et al., 2013).
Conspecific earlier and later stage neighbors show opposing effects on juvenile mortality, and this conflict destabilizes the overall conspecific neighbor effect. Conspecific earlier stage neighbors for juveniles are saplings. They usually smaller and weaker than juveniles. Therefore, they hardly influence juvenile mortality (Weiner, 1990). However, that conspecific sapling neighbors are clumped demonstrates that this habitat is suitable for regeneration (Grubb, 1977; Silvertown, 2004; Pérez-Ramos et al., 2012). The mortality of juveniles decreases correspondingly, and consequently, conspecific saplings significantly and negatively affect juvenile mortality. In contrast, adults are at a later stage than juveniles. As mentioned above, they could also spread specific natural enemies and they have asymmetric competitive advantages compared to juveniles. However, juveniles are more adept at resisting natural enemies and asymmetric competition than are saplings (Boege and Marquis, 2005; DeMalach et al., 2016; Yao et al., 2020). Therefore, the positive effect of conspecific adult neighbors on juvenile mortality is weaker than it is on saplings. Furthermore, due to the weaker positive effect of conspecific adult neighbors and the counteraction of conspecific sapling neighbors, the overall conspecific neighbor effect on juvenile mortality is offset by these opposing effects. In our study, we could not even detect an overall conspecific neighbor effect on juvenile mortality (Fig. 3b). Again, overlooking the life stages of neighbors when measuring their effect on focal tree mortality can result in a biased, incomplete conclusion.
Clumping of earlier stage conspecific neighbors suggests that an adult trees is healthy with a low chance of mortality. In our study, we found that when more conspecific earlier stage neighbors were clumped around the focal adult tree, its mortality was lower. Adult trees are generally surrounded by offspring due to dispersal limitation (Vincent et al., 2011). The healthier the focal adult tree, the stronger its offspring will be and the more likely that they will survive into the next life stage (Moles et al., 2004; Sanín et al., 2013). In general, the healthy adult tree is unlikely to die. Thus, the more the conspecific earlier stage neighbors assemble in clumps, the healthier the adult tree will be. In a previous study, Hou et al. (2004) also found that earlier stage neighbors exhibited clumped distributions to a greater degree around living adult trees than dead ones. Lastly, although we considered the effects of environmental filtering on tree mortality by including some environmental factors in the analysis, other environmental factors that could have contributed to clumping of earlier stage conspecific neighbors and adult tree survival, such as canopy light, were excluded (Dechnik-Vázquez et al., 2016; Liu et al., 2017).
Environmental filtering is a vital process contributing to tree mortality across complex topographies (Wang et al., 2012; Yao et al., 2020). The topography of the Tiantong plot is rough (Yang et al., 2011; Fang et al., 2017). There are two parallel valleys with north-south direction in the Tiantong plot (Fig. 1). These two valleys make it so that convexity is an important environmental variable in the Tiantong plot (Fang et al., 2017). In our study, trees tended to have a higher probability of mortality in low convexity habitats across all life stages. This may be because trees in lower convexity habitats might be disturbed more easily and get less light. Remember that light conditions are always reduced from a south to a north slope. Thus, juveniles occurring toward a north slope suffer higher mortality than juveniles near a south slope. In addition, initial tree size is always a strong predictor for tree survival (Wang et al., 2012; Ma et al., 2013; Wu et al., 2017). We also detected this effect across all life stages.
Environmental variables might have indirectly affected tree mortality through their correlations with the distributions of large neighbors. In this study, we classified the neighbors into different ontogenetic life stages. We found that removing some later stage neighbors from the analysis allowed the effects of some environment variables to become significant. These environment variables were found to correlate with the variables of these later stage neighbors (Fig.S2). Thus, this correlation reflects that the distribution of large individuals is influenced by environmental variables (Wang et al., 2012; Yao et al., 2020), so environmental variables likely affected tree mortality indirectly through neighborhood effects.
Our study proved that both conspecific and heterospecific neighbors play a major role in tree mortality (Peters, 2003; Zhu et al., 2015). However, these influences differ based on the life stage of the neighbors. Conspecific earlier stage neighbors generally have effects on decreasing focal tree mortality because their clumping either reflects that the focal tree is healthy or that the micro-habitat is suitable for focal tree survival. In contrast, conspecific later stage neighbors have effects on increasing focal tree mortality through CNDD. Furthermore, these opposing effects could minimize the overall conspecific neighbor effect. Due to herd protection, the assembling of heterospecific later stage neighbors could reduce focal tree mortality. In addition, large tree neighbors always dominate the neighborhood effects. At the same time, some environmental variables are closely correlated with the distribution of large trees. This correlation could result in the neighborhood effect on tree mortality partially including an indirect environmental effect. Overall, these results suggest that there are multiple mechanisms at play among neighbors at different life stages in ontogenetic tree mortality, and thereby they highlight the necessity for dividing neighbors into different life stages when assessing the overall neighborhood effect contributing to species coexistence.