Botanic gardens and plant pathogens: a risk-based approach at the Royal Botanic Garden Edinburgh
DOI:
https://doi.org/10.24823/Sibbaldia.2020.293Abstract
Introduced and emerging plant diseases as a result of live plant movements are increasingly recognised as a global environmental and economic threat. This presents a fundamental challenge to botanic gardens and other ex situ plant conservation organisations: how to continue this important work while recognising and mitigating the plant health risks. The approach taken by the Royal Botanic Garden Edinburgh is presented as a case study, showing how we have reduced ecological and evolutionary opportunities for pests in ex situ conservation and are monitoring the success of these efforts. We have developed protocols in quarantine and horticultural practice, expanded visitor engagement and public education, and taken a precautionary approach towards plant distribution supported by in-house diagnostics and working closely with statutory authorities. We hope that by sharing activities as well as difficulties, botanic gardens can acknowledge and address the new biosecurity landscape.
References
ADAME-ÁLVAREZ, R.-M., MENDIOLA-SOTO, J. &
HEIL, M. (2014). Order of arrival shifts endophytepathogen
interactions in bean from resistance
induction to disease facilitation. FEMS microbiology
letters, 355(2): 100–107.
ARNOLD, A.E. (2003). Fungal endophytes limit
pathogen damage in a tropical tree. Proceedings
of the National Academy of Sciences, 100(26):
15649–15654.
BARHAM, E., SHARROCK, S., LANE, C. & BAKER,
R. (2015). An International Plant Sentinel Network.
Sibbaldia, 13: 83–98.
BEBBER, D.P., HOLMES, T. & GURR, S.J. (2014).
The global spread of crop pests and pathogens.
Global Ecology and Biogeography, 23(12):
1398–1407.
BRASIER, C. (2008). The biosecurity threat to the
UK and global environment from international
trade in plants. Plant Pathology, 57(5): 792–808.
BRASIER, C. & WEBBER, J. (2010). Plant
pathology: sudden larch death. Nature, 466(7308):
824–825.
BUSBY, P.E., PEAY, K.G. & NEWCOMBE, G. (2015).
Common foliar fungi of Populus trichocarpa modify
Melampsora rust disease severity. New Phytologist,
209(4): 1681–1692.
BUSBY, P.E., RIDOUT, M. & NEWCOMBE, G. (2016).
Fungal endophytes: modifiers of plant disease.
Plant Molecular Biology, 90(6): 645–655.
CHEAH, L.-H., MARSH, A.T., MCNEILL, M.R. &
HEDDERLEY, D.I. (2009). Evaluation of disinfectant
products for microbial decontamination of
imported used footwear. New Zealand Plant
Protection, 62: 130–135.
CORLETT, R.T. (2016). Plant diversity in a changing
world: Status, trends, and conservation needs. Plant
Diversity, 38(1): 10–16.
DESPREZ-LOUSTAU, M., ROBIN, C., BUEE, M.,
COURTECUISSE, R., GARBAYE, J., SUFFERT,
F., SACHE, I. & RIZZO, D. (2007). The fungal
dimension of biological invasions. Trends In Ecology
& Evolution, 22(9): 472–480.
DESPREZ-LOUSTAU, M.-L., AGUAYO, J., DUTECH,
C., HAYDEN, K.J., HUSSON, C., JAKUSHKIN, B.,
MARÇAIS, B., PIOU, D., ROBIN, C. & VACHER, C.
(2015). An evolutionary ecology perspective to
address forest pathology challenges of today and
tomorrow. Annals of Forest Science, 73: 45–67.
DESPREZ-LOUSTAU, M.-L., COURTECUISSE,
R., ROBIN, C., HUSSON, C., MOREAU,
P.-A., BLANCARD, D., SELOSSE, M.-A.,
LUNG-ESCARMANT, B., PIOU, D. & SACHE, I.
(2009). Species diversity and drivers of spread of
alien fungi (sensu lato) in Europe with a particular
focus on France. Biological Invasions, 12(1): 157–172.
ELLIOT, M., MEAGHER, T.R., HARRIS, C., SEARLE,
K., PURSE, B.V. & SCHLENZIG, A. (2013). The
epidemiology of Phytophthora ramorum and P.
kernoviae at two historic gardens in Scotland. In:
FRANKEL, S.J., KLIEJUNAS, J.T., PALMIERI, K.M. &
ALEXANDER, J.M. (tech. co-ords), Proceedings of the
Sudden Oak Death Fifth Science Symposium, June
19-22, 2012, Petaluma, CA, USA. US Department
of Agriculture, Forest Service, Pacific Southwest
Research Station, Albany, CA, pp. 23–32.
ENNOS, R.A. (2015). Resilience of forests to
pathogens: an evolutionary ecology perspective.
Forestry, 88(1): 41–52.
ERWIN, D.C. & RIBEIRO, O.K. (1996). Phytophthora
Diseases Worldwide. APS Press, St. Paul, MN.
ESCHEN, R., BRITTON, K., BROCKERHOFF, E.,
BURGESS, T., DALLEY, V., EPANCHIN-NIELL, R.S.,
GUPTA, K., HARDY, G., HUANG, Y., KENIS, M.,
KIMANI, E., LI, H.-M. ET AL. (2015). International
variation in phytosanitary legislation and
regulations governing importation of plants
for planting. Environmental Science & Policy, 51:
228–237.
EUROPEAN PARLIAMENT AND COUNCIL OF
THE EUROPEAN UNION (2016). Regulation
(EU) 2016/2031 of the European Parliament of
the Council of 26 October 2016 on protective
measures against pests of plants, amending
Regulations (EU) No 228/2013, (EU) No 652/2014
138 | Katherine Hayden
and (EU) No 1143/2014 of the European
Parliament and of the Council and repealing
Council Directives 69/464/EEC, 74/647/EEC, 93/85/
EEC, 98/57/EC, 2000/29/EC, 2006/91/EC and
2007/33/EC. 2016/2031. Available online: https://
eur-lex.europa.eu/legal-content/EN/TXT/HTML/?
uri=CELEX:32016R2031&from=EN (accessed July
2019).
FISHER, M.C., HENK, D.A., BRIGGS, C.J.,
BROWNSTEIN, J.S., MADOFF, L.C., MCCRAW, S.L.
& GURR, S.J. (2012). Emerging fungal threats
to animal, plant and ecosystem health. Nature,
484(7393): 186–194.
GILBERT, G. (2002). Evolutionary ecology of plant
diseases in natural ecosystems. Annual Review of
Phytopathology, 40: 13–43.
HARRIS, A.R. & WEBBER, J.F. (2016). Sporulation
potential, symptom expression and detection of
Phytophthora ramorum on larch needles and other
foliar hosts. Plant Pathology, 65(9): 1441–1451.
IPPC (1997). International Plant Protection
Convention, p. 18. Available online: www.
ippc.int/static/media/files/publication/
en/2019/02/1329129099_ippc_2011-12-01_
reformatted.pdf (accessed July 2019).
LEIFERT, C. & CASSELLS, A.C. (2001). Microbial
hazards in plant tissue and cell cultures. In Vitro
Cellular & Developmental Biology – Plant, 37(2):
133–138.
LIEBHOLD, A.M., BROCKERHOFF, E.G., GARRETT,
L.J., PARKE, J.L. & BRITTON, K.O. (2012). Live
plant imports: the major pathway for forest insect
and pathogen invasions of the US. Frontiers in
Ecology and the Environment, 10(3): 135–143.
MARCHETTI, V., MANCIANTI, F., CARDINI, G. &
LUCHETTI, E. (2006). Evaluation of fungicidal
efficacy of benzalkonium chloride (Steramina G
u.v.) and Virkon-S against Microsporum canis for
environmental disinfection. Veterinary Research
Communications, 30(3): 255–261.
MCDONNELL, G. & RUSSELL, A.D. (1999).
Antiseptics and disinfectants: activity, action, and
resistance. Clinical Microbiology Reviews, 12(1):
147–179.
MOUNCE, R., SMITH, P. & BROCKINGTON, S.
(2017). Ex situ conservation of plant diversity in
the world’s botanic gardens. Nature Plants, 3(10):
795–802.
PARKE, J.L. & GRÜNWALD, N.J. (2012). A
systems approach for management of pests and
pathogens of nursery crops. Plant Disease, 96(9):
1236–1244.
PIMM, S.L. & RAVEN, P.H. (2017). The fate of the
world’s plants. Trends in Ecology & Evolution, 32(5):
317–320.
POWER, A.G. & MITCHELL, C.E. (2004). Pathogen
spillover in disease epidemics. The American
Naturalist, 164(s5): S79–S89.
ROONEY-LATHAM, S., BLOMQUIST, C.L., KOSTA,
K.L., GUO, Y.Y., WOODS, P.W. & SORIANO, M.C.
(2018). Phytophthora species are common
on nursery stock grown for restoration and
revegetation purposes in California. Plant Disease.
doi.org/10.1094/PDIS-01-18-0167-RE.
ROY, B.A., ALEXANDER, H.M., DAVIDSON, J.,
CAMPBELL, F.T., BURDON, J.J., SNIEZKO, R.
& BRASIER, C. (2014). Increasing forest loss
worldwide from invasive pests requires new
trade regulations. Frontiers in Ecology and the
Environment, 12(8): 457–465.
ROYAL BOTANIC GARDEN EDINBURGH (2018).
Catalogue of the Living Collections. Available online:
https://data.rbge.org.uk/search/livingcollection
(accessed July 2019).
SANTINI, A., GHELARDINI, L., DE PACE,
C., DESPREZ-LOUSTAU, M.L., CAPRETTI,
P., CHANDELIER, A., CECH, T., CHIRA, D.,
DIAMANDIS, S., GAITNIEKIS, T., HANTULA,
J., HOLDENRIEDER, O. ET AL. (2013).
Biogeographical patterns and determinants of
invasion by forest pathogens in Europe. New
Phytologist, 197(1): 238–250.
SIKES, B.A., BUFFORD, J.L., HULME, P.E., COOPER,
J.A., JOHNSTON, P.R. & DUNCAN, R.P. (2018).
Import volumes and biosecurity interventions
shape the arrival rate of fungal pathogens. PLOS
Biology, 16(5): e2006025.
SIMBERLOFF, D. (2009). The role of propagule
pressure in biological invasions. Annual Review of
Ecology, Evolution, and Systematics, 40(1): 81–102.
SIMS, L., TJOSVOLD, S., CHAMBERS, D. &
GARBELOTTO, M. (2019). Control of Phytophthora
species in plant stock for habitat restoration
through best management practices. Plant
Pathology, 68(1): 196–204.
STERGIOPOULOS, I. & GORDON, T.R. (2014).Cryptic fungal infections: the hidden agenda of
plant pathogens. Frontiers in Plant Science, 5. doi.
org/10.3389/fpls.2014.00506.
SUSLOW, K. (2007). Recommended industry
best management practices for the prevention
of Phytophthora ramorum introduction in nursery
operations. In: FRANKEL, S.J., KLIEJUNAS, J.T. &
PALMIERI, K.M. (tech. co-ords), Proceedings of the
Sudden Oak Death Third Science Symposium, March
5, 2007, Santa Rosa, CA, USA. US Department
of Agriculture, Forest Service, Pacific Southwest
Research Station, Albany, CA, pp. 115–128..
HEIL, M. (2014). Order of arrival shifts endophytepathogen
interactions in bean from resistance
induction to disease facilitation. FEMS microbiology
letters, 355(2): 100–107.
ARNOLD, A.E. (2003). Fungal endophytes limit
pathogen damage in a tropical tree. Proceedings
of the National Academy of Sciences, 100(26):
15649–15654.
BARHAM, E., SHARROCK, S., LANE, C. & BAKER,
R. (2015). An International Plant Sentinel Network.
Sibbaldia, 13: 83–98.
BEBBER, D.P., HOLMES, T. & GURR, S.J. (2014).
The global spread of crop pests and pathogens.
Global Ecology and Biogeography, 23(12):
1398–1407.
BRASIER, C. (2008). The biosecurity threat to the
UK and global environment from international
trade in plants. Plant Pathology, 57(5): 792–808.
BRASIER, C. & WEBBER, J. (2010). Plant
pathology: sudden larch death. Nature, 466(7308):
824–825.
BUSBY, P.E., PEAY, K.G. & NEWCOMBE, G. (2015).
Common foliar fungi of Populus trichocarpa modify
Melampsora rust disease severity. New Phytologist,
209(4): 1681–1692.
BUSBY, P.E., RIDOUT, M. & NEWCOMBE, G. (2016).
Fungal endophytes: modifiers of plant disease.
Plant Molecular Biology, 90(6): 645–655.
CHEAH, L.-H., MARSH, A.T., MCNEILL, M.R. &
HEDDERLEY, D.I. (2009). Evaluation of disinfectant
products for microbial decontamination of
imported used footwear. New Zealand Plant
Protection, 62: 130–135.
CORLETT, R.T. (2016). Plant diversity in a changing
world: Status, trends, and conservation needs. Plant
Diversity, 38(1): 10–16.
DESPREZ-LOUSTAU, M., ROBIN, C., BUEE, M.,
COURTECUISSE, R., GARBAYE, J., SUFFERT,
F., SACHE, I. & RIZZO, D. (2007). The fungal
dimension of biological invasions. Trends In Ecology
& Evolution, 22(9): 472–480.
DESPREZ-LOUSTAU, M.-L., AGUAYO, J., DUTECH,
C., HAYDEN, K.J., HUSSON, C., JAKUSHKIN, B.,
MARÇAIS, B., PIOU, D., ROBIN, C. & VACHER, C.
(2015). An evolutionary ecology perspective to
address forest pathology challenges of today and
tomorrow. Annals of Forest Science, 73: 45–67.
DESPREZ-LOUSTAU, M.-L., COURTECUISSE,
R., ROBIN, C., HUSSON, C., MOREAU,
P.-A., BLANCARD, D., SELOSSE, M.-A.,
LUNG-ESCARMANT, B., PIOU, D. & SACHE, I.
(2009). Species diversity and drivers of spread of
alien fungi (sensu lato) in Europe with a particular
focus on France. Biological Invasions, 12(1): 157–172.
ELLIOT, M., MEAGHER, T.R., HARRIS, C., SEARLE,
K., PURSE, B.V. & SCHLENZIG, A. (2013). The
epidemiology of Phytophthora ramorum and P.
kernoviae at two historic gardens in Scotland. In:
FRANKEL, S.J., KLIEJUNAS, J.T., PALMIERI, K.M. &
ALEXANDER, J.M. (tech. co-ords), Proceedings of the
Sudden Oak Death Fifth Science Symposium, June
19-22, 2012, Petaluma, CA, USA. US Department
of Agriculture, Forest Service, Pacific Southwest
Research Station, Albany, CA, pp. 23–32.
ENNOS, R.A. (2015). Resilience of forests to
pathogens: an evolutionary ecology perspective.
Forestry, 88(1): 41–52.
ERWIN, D.C. & RIBEIRO, O.K. (1996). Phytophthora
Diseases Worldwide. APS Press, St. Paul, MN.
ESCHEN, R., BRITTON, K., BROCKERHOFF, E.,
BURGESS, T., DALLEY, V., EPANCHIN-NIELL, R.S.,
GUPTA, K., HARDY, G., HUANG, Y., KENIS, M.,
KIMANI, E., LI, H.-M. ET AL. (2015). International
variation in phytosanitary legislation and
regulations governing importation of plants
for planting. Environmental Science & Policy, 51:
228–237.
EUROPEAN PARLIAMENT AND COUNCIL OF
THE EUROPEAN UNION (2016). Regulation
(EU) 2016/2031 of the European Parliament of
the Council of 26 October 2016 on protective
measures against pests of plants, amending
Regulations (EU) No 228/2013, (EU) No 652/2014
138 | Katherine Hayden
and (EU) No 1143/2014 of the European
Parliament and of the Council and repealing
Council Directives 69/464/EEC, 74/647/EEC, 93/85/
EEC, 98/57/EC, 2000/29/EC, 2006/91/EC and
2007/33/EC. 2016/2031. Available online: https://
eur-lex.europa.eu/legal-content/EN/TXT/HTML/?
uri=CELEX:32016R2031&from=EN (accessed July
2019).
FISHER, M.C., HENK, D.A., BRIGGS, C.J.,
BROWNSTEIN, J.S., MADOFF, L.C., MCCRAW, S.L.
& GURR, S.J. (2012). Emerging fungal threats
to animal, plant and ecosystem health. Nature,
484(7393): 186–194.
GILBERT, G. (2002). Evolutionary ecology of plant
diseases in natural ecosystems. Annual Review of
Phytopathology, 40: 13–43.
HARRIS, A.R. & WEBBER, J.F. (2016). Sporulation
potential, symptom expression and detection of
Phytophthora ramorum on larch needles and other
foliar hosts. Plant Pathology, 65(9): 1441–1451.
IPPC (1997). International Plant Protection
Convention, p. 18. Available online: www.
ippc.int/static/media/files/publication/
en/2019/02/1329129099_ippc_2011-12-01_
reformatted.pdf (accessed July 2019).
LEIFERT, C. & CASSELLS, A.C. (2001). Microbial
hazards in plant tissue and cell cultures. In Vitro
Cellular & Developmental Biology – Plant, 37(2):
133–138.
LIEBHOLD, A.M., BROCKERHOFF, E.G., GARRETT,
L.J., PARKE, J.L. & BRITTON, K.O. (2012). Live
plant imports: the major pathway for forest insect
and pathogen invasions of the US. Frontiers in
Ecology and the Environment, 10(3): 135–143.
MARCHETTI, V., MANCIANTI, F., CARDINI, G. &
LUCHETTI, E. (2006). Evaluation of fungicidal
efficacy of benzalkonium chloride (Steramina G
u.v.) and Virkon-S against Microsporum canis for
environmental disinfection. Veterinary Research
Communications, 30(3): 255–261.
MCDONNELL, G. & RUSSELL, A.D. (1999).
Antiseptics and disinfectants: activity, action, and
resistance. Clinical Microbiology Reviews, 12(1):
147–179.
MOUNCE, R., SMITH, P. & BROCKINGTON, S.
(2017). Ex situ conservation of plant diversity in
the world’s botanic gardens. Nature Plants, 3(10):
795–802.
PARKE, J.L. & GRÜNWALD, N.J. (2012). A
systems approach for management of pests and
pathogens of nursery crops. Plant Disease, 96(9):
1236–1244.
PIMM, S.L. & RAVEN, P.H. (2017). The fate of the
world’s plants. Trends in Ecology & Evolution, 32(5):
317–320.
POWER, A.G. & MITCHELL, C.E. (2004). Pathogen
spillover in disease epidemics. The American
Naturalist, 164(s5): S79–S89.
ROONEY-LATHAM, S., BLOMQUIST, C.L., KOSTA,
K.L., GUO, Y.Y., WOODS, P.W. & SORIANO, M.C.
(2018). Phytophthora species are common
on nursery stock grown for restoration and
revegetation purposes in California. Plant Disease.
doi.org/10.1094/PDIS-01-18-0167-RE.
ROY, B.A., ALEXANDER, H.M., DAVIDSON, J.,
CAMPBELL, F.T., BURDON, J.J., SNIEZKO, R.
& BRASIER, C. (2014). Increasing forest loss
worldwide from invasive pests requires new
trade regulations. Frontiers in Ecology and the
Environment, 12(8): 457–465.
ROYAL BOTANIC GARDEN EDINBURGH (2018).
Catalogue of the Living Collections. Available online:
https://data.rbge.org.uk/search/livingcollection
(accessed July 2019).
SANTINI, A., GHELARDINI, L., DE PACE,
C., DESPREZ-LOUSTAU, M.L., CAPRETTI,
P., CHANDELIER, A., CECH, T., CHIRA, D.,
DIAMANDIS, S., GAITNIEKIS, T., HANTULA,
J., HOLDENRIEDER, O. ET AL. (2013).
Biogeographical patterns and determinants of
invasion by forest pathogens in Europe. New
Phytologist, 197(1): 238–250.
SIKES, B.A., BUFFORD, J.L., HULME, P.E., COOPER,
J.A., JOHNSTON, P.R. & DUNCAN, R.P. (2018).
Import volumes and biosecurity interventions
shape the arrival rate of fungal pathogens. PLOS
Biology, 16(5): e2006025.
SIMBERLOFF, D. (2009). The role of propagule
pressure in biological invasions. Annual Review of
Ecology, Evolution, and Systematics, 40(1): 81–102.
SIMS, L., TJOSVOLD, S., CHAMBERS, D. &
GARBELOTTO, M. (2019). Control of Phytophthora
species in plant stock for habitat restoration
through best management practices. Plant
Pathology, 68(1): 196–204.
STERGIOPOULOS, I. & GORDON, T.R. (2014).Cryptic fungal infections: the hidden agenda of
plant pathogens. Frontiers in Plant Science, 5. doi.
org/10.3389/fpls.2014.00506.
SUSLOW, K. (2007). Recommended industry
best management practices for the prevention
of Phytophthora ramorum introduction in nursery
operations. In: FRANKEL, S.J., KLIEJUNAS, J.T. &
PALMIERI, K.M. (tech. co-ords), Proceedings of the
Sudden Oak Death Third Science Symposium, March
5, 2007, Santa Rosa, CA, USA. US Department
of Agriculture, Forest Service, Pacific Southwest
Research Station, Albany, CA, pp. 115–128..
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How to Cite
Botanic gardens and plant pathogens: a risk-based approach at the Royal Botanic Garden Edinburgh. (2020). Sibbaldia: The International Journal of Botanic Garden Horticulture, 18, 127-139. https://doi.org/10.24823/Sibbaldia.2020.293
