The Ecology of Phytophthora ramorum and Resident Phytophthora in California Streams

Phytophthora spp. are regularly recovered from streams but their ecology in aquatic environments is not well understood. Phytophthora ramorum, invasive in California forests, where it causes of "Sudden Oak Death", persists in streams at times when sporulation in the canopy is absent, suggesting that it reproduces in the water. Streams are also inhabited by resident, clade 6 Phytophthora spp., believed to be primarily saprotrophic. Leaf litter is a major substrate for aquatic fungi, but senescence and decomposition could restrict its availability to an organism adapted as a pathogen, such as P. ramorum. It is also uncertain how litter quality affects colonization by resident, clade 6 Phytophthora spp., such as P. gonapodyides, to what extent such species contribute to leaf decomposition, and how the presence of a novel species affects these relationships. We conducted experiments to determine if differences of trophic specialization exist between these taxa that affect their survival and competition on stream leaf litter. P. ramorum effectively colonized fresh (live) rhododendron leaves but not those killed by freezing or drying, while clade 6 species colonized all leaf types. Both taxa were recovered from natural California bay leaf litter in streams. In stream experiments, P. ramorum colonized bay leaves rapidly but declined as rapidly and was succeeded by clade 6 species. Nevertheless, both taxa persisted in leaves over 16 weeks and substantial leaf decomposition. These results confirmed that clade 6 Phytophthora spp. are competent saprotrophs, and though P. ramorum could not colonize dead tissue, early colonization of suitable litter allowed it to survive at low levels in decomposing leaves. In controlled environment experiments, we found that both P. ramorum and P. gonapodyides effectively colonized and persisted on green and yellow (senescing) bay leaves. Only P. gonapodyides could also colonize and persist on brown (fully senesced and dried) leaves. Both Phytophthora spp. similarly accelerated the decomposition of green and yellow leaves compared with non-inoculated controls, but P. gonapodyides' colonization of brown leaves did not affect their decomposition rate. Finally, we identified a representative sample of Phytophthora and Pythium s.l. isolates collected from California bay leaves deployed in the aforementioned stream experiment by analyzing the internal transcribed spacer (ITS) region of the ribosomal DNA. Phytophthora chalmydospora, P. gonapodyides, and Phytopythium litorale were the most prevalent species but other species commonly encountered in environmental samples around the world also occurred. Phytophthora spp. colonized leaves within the first week of emersion and persisted throughout four months of in stream decomposition, while Phytopythium spp. became more prevalent as leaves decomposed. The picture that emerges is that Phytophthora are part of a diversity of oomycetes adapted to using plants as a substrate for growth, and covering a spectrum of trophic competence between pathogen and saprotroph, and that the presence of species adapted to the stream environment may to some extent mitigate the persistence and proliferation in streams of introduced species with less saprotrophic competence, such as P. ramorum.