Ecological Archives E096-064-A1

Xubing Liu, Rampal S. Etienne, Minxia Liang, Yongfan Wang, and Shixiao Yu. 2015. Experimental evidence for an intraspecific Janzen-Connell effect mediated by soil biota. Ecology 96:662671.

Appendix A. Detailed description of how the eight focused traits could influence host–pathogen interactions.

SLA is often positively related to plant growth rate and leaf quality: individuals with larger SLA tend to grow faster and might be more susceptible to pathogens, as they have greater developmental and reproduction rates and invest less in adaptive immunity than slow-growing individuals (Cronin et al. 2010). Two indicators of past growth rates, adult wood density (higher wood density is accompanied by lower growth rate, Enquist et al. 1999) and successional status (late successional species have lower relative growth rate, Tilman and Cowan 1989) are negatively correlated with vulnerability of seedlings to pathogens (Augspurger and Kelly 1984). Seed size is positively correlated with pathogen attack: larger seeds were found to be more susceptible to pathogen attack than smaller ones (Pringle et al. 2007), although species with larger seed mass may offset disease-related losses during germination and establishment (Armstrong and Westoby 1993). Photosynthetic assimilation rate, a leaf trait associated with relative growth rate, is higher for light-demanding species than for shade-tolerant species (Kitajima 1994). Given that shade-intolerant species have faster growth rates and allocate fewer resources to fight pathogens and therefore may be more susceptible to disease than shade-tolerant species (Augspurger and Kelly 1984), individuals with higher photosynthetic capacity would suffer more intense pathogen mortality. LNC is closely correlated with mass-based maximum photosynthetic rate, and tends to correlate significantly with the nutrient availability in the soil (Cornelissen et al. 2003) which can also strongly influence soil pathogen abundance and richness.

Local pathogen levels may not only be affected by physiological and morphological traits, but also by characteristics relating to the abundance and spatial distribution of individuals, which could affect pathogen reservoir and transmission among host individuals. Heterogeneous spatial patterns of soil pathogen abundance guarantee the interspecific and intraspecific variation of the Janzen-Connell effect. It has previously been recognized that pathogenic activities and densities of soil organisms are regulated by a diverse range of spatial (reviewed by Ettema and Wardle 2002) and temporal (reviewed by Bardgett et al. 2005) scales. Environmental differences (e.g., soil type and nutrient), local species composition and historical processes and legacies among different populations can contribute to the spatial distribution of soil pathogens.

Locally abundant tree species are reported to experience greater negative density dependent effects than rare species (e.g., Webb and Peart 1999, Wills et al. 2006, Queenborough et al. 2007, but see Klironomos 2002, Mangan et al. 2012), which may "escape" density dependent mortality because they are less likely to encounter areas where conspecifics have accumulated many specialist enemies (pathogens and herbivores). Among different individuals of the same species (Ormosia glaberrima) in subtropical China, a locally rare species advantage was also found to be due to spatially unequal pathogen distributions: the negative plant-soil feedback caused by a host-specific pathogen was observed at a field site where O. glaberrima were locally common but not observed at another site with a single O. glaberrima tree (Liu et al. 2012). Larger host individuals are found to support more pathogen species (Miller 2012) and consequently increase the probability of encountering virulent ones. Individual size per se may increase pathogen richness by increasing rate of colonization by novel pathogens and population sizes of established pathogen species, and decreasing rates of pathogen extinction. Individual size may also influence pathogen richness through traits that correlated with plant size, including diversity of habitats embodied by the host (Clay and Kover 1996) and longevity of individuals and their tissues (Kikuzawa and Ackerly 1999). Because soil-borne pathogens have more limited dispersal than their hosts (Gilbert 2002), a given host individual may culture its own soil pathogens operating at a spatial scale commensurate with the area occupied by its canopy (McCarthy-Neumann and Kobe 2008), so encounters among host individuals are less likely with greater distance. Hence, we expect that the number of soil pathogens that two individual hosts share with each other should decline with increasing distance.

Literature cited

  1. Armstrong, D. P., and M. Westoby. 1993. Seedlings from large seeds tolerate defoliation better: a test using phylogenetically independent contrast. Ecology 74:1092-1100.
  2. Augspurger, C. K., and C. K. Kelly. 1984. Pathogen mortality of tropical tree seedlings: experimental studies of the effects of dispersal distance, seedling density, and light conditions. Oecologia 61:211-217.
  3. Bardgett, R. D., W. D. Bowman, R. Kaufmann, and S. K. Schmidt. 2005. A temporal approach to linking aboveground and belowground ecology. Trends in Ecology and Evolution 20:634-641.
  4. Clay, K., and P. Kover. 1996. Evolution and stasis in plant/pathogen associations. Ecology 77:997-1003.
  5. Cornelissen, J. H. C., S. Lavorel, E. Garnier, S. Diaz, N. Buchmann, and D. E. Gurvich. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51:335-380.
  6. Cronin, J. P., M. E. Welsh, M. G. Dekkers, S. T. Abercrombie, and C. E. Mitchell. 2010. Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13:1221-1232.
  7. Enquist, B., G. West, E. Charnov, and J. Brown. 1999. Allometric scaling of production and life-history variation in vascular plants. Nature 401:907-911.
  8. Ettema, C. H., and D. A. Wardle. 2002. Spatial soil ecology. Trends in Ecology and Evolution 17:177-183.
  9. Gilbert, G. S. 2002. Evolutionary ecology of plant diseases in natural systems. Annual Review of Phytopathology 40:13-43.
  10. Kikuzawa, K., and D. Ackerly. 1999. Significance of leaf longevity in plants. Plant Species Biology 14:39-45.
  11. Kitajima, K. 1994. Relative importance of photosynthetic traits and allocation patterns as correlates of seedling shade tolerance of 13 tropical trees. Oecologia 98:419-428.
  12. Klironomos, J. N. 2002. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67-70.
  13. Liu, Y., S. Yu, Z.-P. Xie, and C. Staehelin. 2012. Analysis of a negative plant-soil feedback in a subtropical monsoon forest. Journal of Ecology 100:1019-1028.
  14. Mangan, S. A., S. A. Schnitzer, E. A. Herre, K. M. L. Mack, M. C. Valencia, E. I. Sanchez, and J. D. Bever. 2010. Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752-755.
  15. McCarthy-Neumann, S., and R. K. Kobe. 2008. Tolerance of soil pathogens co-varies with shade tolerance across species of tropical tree seedlings. Ecology 89:1883-1892.
  16. Miller, Z. J. 2012. Fungal pathogen species richness: why do some plant species have more pathogens than others? American Naturalist 179:282-292.
  17. Pringle, E. G., P. Alvarez-Loayza, and J. Terborgh. 2007. Seed characteristics and susceptibility to pathogen attack in tree seeds of the Peruvian Amazon. Plant Ecology 193:211-222.
  18. Queenborough, S. A., D. F. Burslem, N. C. Garwood and R. Valencia. 2007. Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology 88:2248-2258.
  19. Tilman, D., and M. L. Cowan. 1989. Growth of old field herbs on a nitrogen gradient. Functional Ecology 3:425-438.
  20. Webb, C. O., and D. R. Peart. 1999. Seedling density dependence promotes coexistence of Bornean rain forest trees. Ecology 80:2006-2017.
  21. Wills, C., K .E. Harms, R. Condit, D. King, J. Thompson, F. He, et al. 2006. Nonrandom processes maintain diversity in tropical forests. Science 311:527-531.

[Back to E096-064]