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Home , Frangula californica, Phytophthora quercina, Prunus ilicifolia, Rhamnus crocea

Restoration outplantings of nursery-origin Californian flora are heavily infested with

Tyler B Bourret, HK Mehl, DM Rizzo, TJ Swiecki, EA Bernhardt & JM Hillman 6th SOD Symposium, June 23, 2016 Survey of potentially infested restoration sites

. Santa Clara Valley Water District (SCVWD) has routinely performed restoration with nursery-reared native Californian flora . Phytophthora species had been previously isolated from SCVWD outplantings & associated nurseries by Phytosphere (TJ Swiecki & EA Bernhardt), including P. tentaculata #5 on APHIS list of species to keep out of US . Broad survey of 31 sites by Rizzo lab (H. Mehl & T. Bourret) & Phytosphere Sep 2015 - May 2016

31 restoration sites sampled Sample site

San Jose 36 species

193 samples collected

Preference for symptomatic , especially known P. tentaculata hosts

~1 L soil +

Methods - soil sample processing & ID

Baited with green pears & Rhododendron Strains determined to species using morphotyping & ITS sequences Pythium s.l. was included but not reported (Mostly Phytopythium & Pythium s.s.)

# positive # Positive Plant species Common name # samples samples % samples sites # Psp. ► Aesculus californica Buckeye 2 1 50 1 1 ► Acer negundo Boxelder maple 5 3 60 2 2 193 total samples ► Alnus rhombifolia White Alder 2 1 50 1 1 ► Artemisia californica sagebrush 8 2 25 1 3 ► Artemisia douglasiana Mugwort 23 6 26 3 16 74 Phytophthora- Aster chilensis Chilean aster 3 0 0 0 0 positive ► Baccharis glutinosa Salt marsh baccharis 1 1 100 1 2 Baccharis pilularis Coyote brush 3 0 0 0 0 27 yielded more ► Baccharis salicifolia Mulefat 3 1 33 1 4 ► Ceanothus thyrsiflorus Blue blossom 1 1 100 1 3 than one species Clematis ligusticifolia Virgin's bower 2 0 0 0 0 ► Dead plant (unknown sp.) Empty planting site 8 2 25 2 2 ► Diplacus aurantiacus Sticky monkey 7 5 71 2 6 ► Euthamia occidentalis Goldenrod 3 2 67 2 1 ► californica Coffeeberry 9 2 22 2 2 Helenium bignonia Sneezeweed 1 0 0 0 0 ► arbutifolia Toyon 18 12 67 9 5 ► Juncus sp. Rush (unknown sp.) 6 5 83 4 7 36 plant species Lepechinia calycina Pitcher sage 1 0 0 0 0 ► Platanus racemosa Sycamore 7 1 14 1 2 ► Populus fremontii Fremont cottonwood 4 2 50 1 3 (28 associated with ► ilicifolia - 2 1 50 1 1 positive samples) ► Quercus agrifolia Coast live 19 5 26 3 5 ► Quercus douglasiana Blue oak 3 1 33 1 2 ► Quercus lobata Valley oak 12 4 33 1 3 Quercus sp. Oak (unknown sp.) 1 0 0 0 0 ► Quercus wislizenii Canyon live oak 1 1 100 1 1 crocea Redberry buckthorn 2 0 0 0 0 ► Rosa californica CA wild rose 13 7 54 4 6 ► Rubus ursinus CA blackberry 3 1 33 1 1 ► Salicornia pacifica Pickleweed 3 2 67 1 2 ► Salix sp. Willow (unknown sp.) 1 1 100 1 6 ► Sambucus mexicana Blue elderberry 12 4 33 4 4 Sambucus racemosa Mexican elderberry 2 0 0 0 0 ► Sambucus sp. Elderberry (unknown sp.) 1 1 100 1 2 ► Symphoricarpos laevigatus Snowberry 4 1 25 1 1 ► Phytophthora recovered ► Umbellularia californica Bay laurel 1 1 100 1 2 Plant species Common name # samples # positive samples # Psp. Phytophthora species list CAS, CHL, CRA, CRY, HYD, INU, LAC, MUL, PAR, PIN, POLxMAR, ROS, MUG, OAK, Artemisia douglasiana Mugwort 23 6 16 THE, THExAMN Juncus sp. Rush (unknown sp.) 6 5 7 CAC, CRY, EUR, INU, JUN, MUL, PIN Diplacus aurantiacus Sticky monkey flower 7 5 6 CAC, CRA, EUR, INU, MEG, PIN Rosa californica CA wild rose 12 6 6 CAC, CRA, MEG, QUM, RAM. RIP Salix sp. Willow (unknown sp.) 1 1 6 CRA, CRY, LAC, PSE, ROS, OAK Quercus agrifolia Coast live oak 19 5 5 CAC, CRA, OAK, SYR, WAL Heteromeles arbutifolia Toyon 18 12 5 CAC*, CRA, CRY, HED, OAK Baccharis salicifolia Mulefat 3 1 4 ASP, KELxCRY, ROS, OAK Sambucus mexicana Mexican elderberry 12 4 4 CRA, PAL, QUE, RAS Populus fremontii Fremont cottonwood 4 2 3 ACE, PSE, ROS Ceanothus thyrsiflorus Blue blossom 1 1 3 CAC, MUL, NIC Quercus lobata Valley oak 12 4 3 CAC, QUE, PSY Many species from Artemisia californica California sagebrush 8 2 3 CRA, INU, PAL Acer negundo Boxelder maple 5 3 2 CAC, MUL preferentially Coffeeberry 9 2 2 CAC, MUL sampled hosts: Quercus douglasiana Blue oak 3 1 2 CAC, OCC Dead plant (unknown sp.) Empty planting site 8 1 2 CAC, ROS - Mugwort Salicornia pacifica Pickleweed 3 2 2 HUM, HUMxINU - Toyon Baccharis glutinosa Salt marsh baccharis 1 1 2 MUL, OAK - Monkey flower Umbellularia californica Bay laurel 1 1 2 MUL, OCC Sambucus sp. Elderberry 1 1 2 MUL, ROS - Oak spp. Platanus racemosa Sycamore 7 1 2 ROS, OAK Aesculus californica Buckeye 2 1 1 CAC Also many species Alnus rhombifolia White Alder 2 1 1 CAC Euthamia occidentalis Goldenrod 3 2 1 CAC from: Holly-leaf cherry 2 1 1 CAC - Willow Rubus ursinus CA blackberry 3 1 1 CAC Symphoricarpos laevigatus Snowberry 4 1 1 CAC - Juncus sp. Quercus wislizenii Canyon live oak 1 1 1 PIN - Mulefat Aster chilensis Chilean aster 3 0 0 Baccharis pilularis Coyote brush 3 0 0 Clematis ligusticifolia Virgin's bower 2 0 0 Helenium bignonia Sneezeweed 1 0 0 Lepechinia calycina Pitcher sage 1 0 0 Quercus sp. Oak (unknown sp.) 1 0 0 Redberry buckthorn 2 0 0 Sambucus racemosa Red elderberry 2 0 0 P. acerina, ACE; P. asparagi, ASP; P. cactorum, CAC, P. chlamydospora, CHL; P. crassamura, CRA; P. europaea, EUR; P. hedraiandra, HED; P. hydropathica, HYD; P. humicola, HUM; P. humicola x inundata, HUMxINU; P. inundata, INU; P. sp. kelmania, KEL; P. lacustris, LAC; P. megasperma species complex, MEG; P. multivora, MUL; P. nicotianae, NIC; P. occultans, OCC; P. palmivora, PAL; P. parsiana, PAR; P. pini, PIN; P. polonica X aff. "Maryland 8," POLxMAR; P. pseudocryptogea , PCY; P. pseudosyringae, PSE; P. psychrophila, PSY; P. quercetorum, QUM; P. quercina, QUE; P. ramorum, RAM; P. riparia, RIP; P. rosacearum, ROS; P. syringae, SYR; P. taxon casuarina, CAS; P. taxon juncus (sp. nov.), JUN; P. taxon mugwort (sp. nov.), MUG; P. taxon oaksoil, OAK; P. taxon raspberry, RAS; P. taxon walnut, WAL; P. thermophila, THE; P. thermophila X amnicola, THExAMN *All Phytophthora positive samples included this Psp.

Phytophthora species recovered, by site

Total Positive % positive Site ID Year(s) planted Number Psp. Phytophthora spp. samples samples samples

GUAD6 2011-2012 3 3 100 13 CHL, CRA, HYD, INU, LAC, PAR, PCY, POLxMAR, ROS, CAS, OAK, THE, THExAMN GU1A 1994-1995 7 7 100 11 ACE, ASP, CRA, KEL, LAC, MUL, PCY, PSE, ROS, OAK, WAL UPC 2012 8 7 88 6 CAC, CRA, INU, MEG, PAL, PIN GRCE 2013 5 4 80 5 CAC, HED, MUL, PIN, OAK STMC 2002 10 8 80 5 CAC, MUL, PIN, PSY, QUE, OAK ADOB5 2008 12 6 50 4 CAC, MUL, NIC, RAS CARA 2012 11 4 36 4 CAC, EUR, MUL, PIN JACB 2009 6 2 33 3 CAC, MUL, OCC STSU 2012 4 2 50 3 CAC, CRA, HED COPAR 2006-8 5 3 60 3 EUR, MUL, JUN PAJ 2007-8 3 3 100 3 INU, RAM, RIP TOMA 2013 9 3 33 3 MUG, QUM, ROS P. cactorum most CSS 2011 8 3 38 2 CAC, PCY STRP 2002-2003 5 2 40 2 CAC, HED common and ADOB 2005 17 3 18 2 CAC, CRA widespread species PENT 2014 3 2 67 2 CRA, SYR COYM 1998-9 3 2 67 2 HUM, HUMxINU JACA 2009 8 1 12 1 CAC STWA 2013 2 2 100 1 CAC STWB 2013 3 1 33 1 CAC STWC 2013 5 2 40 1 CAC TAR 2008 4 1 25 1 CAC CCR2 1980’s 3 2 67 1 MUL CALE 2013 6 0 0 0 CCR3 1990’s 3 0 0 0 GCBH 2013 2 0 0 0 LEND1 2011 3 0 0 0 LEND2 2009 1 0 0 0 LEND3 2009 6 0 0 0 TIC 2010 4 0 0 0 TOCA 2012 8 0 0 0 P. acerina, ACE; P. asparagi, ASP; P. cactorum, CAC, P. chlamydospora, CHL; P. crassamura, CRA; P. europaea, EUR; P. hedraiandra, HED; P. hydropathica, HYD; P. humicola, HUM; P. humicola x inundata, HUMxINU; P. inundata, INU; P. sp. kelmania, KEL; P. lacustris, LAC; P. megasperma species complex, MEG; P. multivora, MUL; P. nicotianae, NIC; P. occultans, OCC; P. palmivora, PAL; P. parsiana, PAR; P. pini, PIN; P. polonica X aff. "Maryland 8," POLxMAR; P. pseudocryptogea , PCY; P. pseudosyringae, PSE; P. psychrophila, PSY; P. quercetorum, QUM; P. quercina, QUE; P. ramorum, RAM; P. riparia, RIP; P. rosacearum, ROS; P. syringae, SYR; P. taxon casuarina, CAS; P. taxon juncus (sp. nov.), JUN; P. taxon mugwort (sp. nov.), MUG; P. taxon oaksoil, OAK; P. taxon raspberry, RAS; P. taxon walnut, WAL; P. thermophila, THE; P. thermophila X amnicola, THExAMN Phytophthora species recovered, by site

Total Positive % positive Site ID Year(s) planted Number Psp. Phytophthora spp. samples samples samples

GUAD6 2011-2012 3 3 100 13 CHL, CRA, HYD, INU, LAC, PAR, PCY, POLxMAR, ROS, CAS, OAK, THE, THExAMN GU1A 1994-1995 7 7 100 11 ACE, ASP, CRA, KEL, LAC, MUL, PCY, PSE, ROS, OAK, WAL UPC 2012 8 7 88 6 CAC, CRA, INU, MEG, PAL, PIN GRCE 2013 5 4 80 5 CAC, HED, MUL, PIN, OAK STMC 2002 10 8 80 5 CAC, MUL, PIN, PSY, QUE, OAK ADOB5 2008 12 6 50 4 CAC, MUL, NIC, RAS CARA 2012 11 4 36 4 CAC, EUR, MUL, PIN JACB 2009 6 2 33 3 CAC, MUL, OCC STSU 2012 4 2 50 3 CAC, CRA, HED COPAR 2006-8 5 3 60 3 EUR, MUL, JUN PAJ 2007-8 3 3 100 3 INU, RAM, RIP TOMA 2013 9 3 33 3 MUG, QUM, ROS 19 species between CSS 2011 8 3 38 2 CAC, PCY STRP 2002-2003 5 2 40 2 CAC, HED two sites on the ADOB 2005 17 3 18 2 CAC, CRA Guadalupe river PENT 2014 3 2 67 2 CRA, SYR COYM 1998-9 3 2 67 2 HUM, HUMxINU JACA 2009 8 1 12 1 CAC STWA 2013 2 2 100 1 CAC STWB 2013 3 1 33 1 CAC STWC 2013 5 2 40 1 CAC TAR 2008 4 1 25 1 CAC CCR2 1980’s 3 2 67 1 MUL CALE 2013 6 0 0 0 CCR3 1990’s 3 0 0 0 GCBH 2013 2 0 0 0 LEND1 2011 3 0 0 0 LEND2 2009 1 0 0 0 LEND3 2009 6 0 0 0 TIC 2010 4 0 0 0 TOCA 2012 8 0 0 0 P. acerina, ACE; P. asparagi, ASP; P. cactorum, CAC, P. chlamydospora, CHL; P. crassamura, CRA; P. europaea, EUR; P. hedraiandra, HED; P. hydropathica, HYD; P. humicola, HUM; P. humicola x inundata, HUMxINU; P. inundata, INU; P. sp. kelmania, KEL; P. lacustris, LAC; P. megasperma species complex, MEG; P. multivora, MUL; P. nicotianae, NIC; P. occultans, OCC; P. palmivora, PAL; P. parsiana, PAR; P. pini, PIN; P. polonica X aff. "Maryland 8," POLxMAR; P. pseudocryptogea , PCY; P. pseudosyringae, PSE; P. psychrophila, PSY; P. quercetorum, QUM; P. quercina, QUE; P. ramorum, RAM; P. riparia, RIP; P. rosacearum, ROS; P. syringae, SYR; P. taxon casuarina, CAS; P. taxon juncus (sp. nov.), JUN; P. taxon mugwort (sp. nov.), MUG; P. taxon oaksoil, OAK; P. taxon raspberry, RAS; P. taxon walnut, WAL; P. thermophila, THE; P. thermophila X amnicola, THExAMN Juncus sp: P. multivora, P. pini Willow sp: P. crassamura, P. pseudocryptogea, P. lacustris, P. pseudosyringae, P. rosacearum, P. taxon oaksoil

Juncus sp: P. pseudocryptogea

Mugwort: P. chlamydospora, P. crassamura, P. hydropathica, P. inundata, P. lacustris, P. polonica Toyon: P. cactorum, P. X aff. "Maryland 8", P. taxon casuarina, P. thermophila X amnicola crassamura, P. hedraiandra All Phytophthora species # sites # Plant species Clade P. acerina 1 1 2 P. asparagi 1 1 6 38 Phytophthora species P. cactorum 15 16 1 P. chlamydospora 1 1 6 P. crassamura 5 7 6 P. europaea 2 2 7 P. hedraiandra 3 2 1 28 “good” species P. humicola 1 1 6 P. humicola X inundata 1 1 6 - 6 described since 2014 P. hydropathica 1 1 9 P. inundata 3 4 6 - 2 described since the P. lacustris 2 2 6 project started in August P. megasperma species complex 1 2 6 P. multivora 8 8 2 P. nicotianae 1 1 1 P. occultans 1 2 2 5 described but provisional P. palmivora 1 2 4 P. parsiana 1 1 9 P. pini 4 4 2 3 putative hybrids P. polonica X aff. "Maryland 8" 1 1 9 P. pseudocryptogea 3 4 8 P. pseudosyringae 1 2 3 2 novel species P. psychrophila 1 1 3 P. quercetorum 1 1 4 P. quercina 1 2 1 P. cactorum, P. multivora P. ramorum 1 1 8 P. riparia 1 1 6 and P. crassamura most P. rosacearum 3 7 6 P. syringae 1 1 8 widespread P. sp. kelmania 1 1 8 P. taxon casuarina 1 1 6 P. taxon juncus (sp. nov.) 1 1 ? P. taxon mugwort (sp. nov.) 1 1 ? P. taxon oaksoil 4 7 6 P. taxon raspberry 1 1 6 P. taxon walnut 1 1 6 P. thermophila 1 1 6 P. thermophila X amnicola 1 1 6

So many species

About 1/4 of the ~150 species of Phytophthora All subgeneric clades represented except 5 and 10

Big, lingering question: How many of our 38 species truly came from the nurseries?

Baiting a comparable amount of bulk soil from Big Sur forests resulted in 6 species (TBB, unpublished) A combined effort over more than a decade of nursery, landscape and riparian isolations across produced a list of ~60 species (Jung et al. 2014)

P. asparagi & P. crassamura from declining “maquis”

Declining native vegetation on Maddalena Archipelago (Scanu et al. 2015) Dieback of , Asparagus albus, Cistus sp., Juniperus phoenicea, J. oxycedrus, Pistacia lentiscus and Rhamnus alaternus Several species of Phytophthora associated P. asparagi most commonly isolated & most virulent on Juniperus seedlings P. crassamura and P. ornamentata described as novel species crassamura means “thick walled” (Scanu et al. 2015) Fig 1. Symptoms of decline on Mediterranean maquis vegetation caused by Phytophthora spp.: a. Dead and dying of Juniperus phoeniceae with abnormal production of epicormic shoots; b. Mature of Juniperus oxycedrus showing severe wilting and red discoloration; c. Young tree of J. oxycedrus with red/bronze colour of foliage over the entire crown; d. Basal phloem lesion on a juniper tree extending up from below ground level; e. Collar and rot on a young juniper tree; f. Extensive dieback and mortality of Pistacia lentiscus across site; g. Dieback and wilting of Asparagus albus. (Scanu et al. 2015) Phytophthora quercina Species first isolated from declining in Central & Southern Europe in the 1990s Most common Phytophthora in declining Central European oak forests, especially where trees die rapidly and in groups Declining Q. robur showing different levels of crown Fine-root pathogen, specific to the Quercus, but dieback and chlorosis (specific symptom on calcaric soils found in nursery soil with other plant species due to advanced fine root destructions caused by P. citricola and P. quercina). Aggressive on all Quercus species tested Balci et al. found a close relative, P. sp. ohioensis from eastern US oak stands, but P. quercina has not been isolated in APHIS ranked listed P. quercina as the #1 Phytophthora species of concern for introduction into the US Aggressiveness of P. quercina to Q. robur roots in a soil infestation test after 6 months; left: control, right: infested soil. P. quercina isolation in Santa Clara Co.

Isolated from four Valley Oaks (Q. lobata); site planted in 2002

Initial isolation is the only documented baiting of P. quercina by pear; subsequent isolations were only successful with Q. robur and Q. ilex leaf bait

This represents the first detection of P. quercina in the US, confirmed by USDA

Ongoing work

. Follow-up, including treatment of most critical areas (SCVWD & Phytosphere taking the lead) . Collaboration with “CalPhytos” working group and other researchers . Culture-independent techniques with frozen soil samples DNA has been extracted from most soil samples  DNA can be detected w/ specific primers in all samples tested . Systematic studies of interesting strains Two novel species of

Phytophthora were isolated Clade 7 Clade P. taxon juncus P. taxon mugwort

Neither could be unambiguously placed into a subgeneric clade, even with multiple (up to 6) loci 1 Clade The nature of the project raises important questions about their status as native or exotic pathogens Sporangia of P. taxon mugwort The big picture

. Increased regulations following SOD have been largely successful for foliar Phytophthora species, less so for soil-borne species . Move differently, symptoms less diagnostic . Regulated differently . Well-meaning environmental regulations may have led to poor choices for restoration in regards to root-associated Phytophthora  Choice of nursery-origin transplants rather than seeds or natural regeneration  Year-round irrigation of plants adapted to Mediterranean climates  Direct movement of soil for the purposes of moving unculturable plant-mutualistic microbes . Oomycete diversity remains undersampled at many scales Acknowledgments

Santa Clara Valley Water District & employees

Noah Luecke & Miles lab (CSUMB)

Rino Oguchi & Valerie Wuerz, UC Davis