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Biocontrol introduction

Target pest: Clematis vitalba (Ranunculales: Ranunculaceae), old man's beard

Agent introduced: Longididymella clematidis (Pleosporales: Didymellaceae) = Didymella clematidis, Phoma clematidina, old man's beard leaf fungus

Imported:

1990

Import source:

Washington, USA

Import notes:

Gourlay et al. (2000) - after extensive laboratory tests for virulence and host specificity to C. vitalba, a single isolate of L. clematidis [as Phoma clematidina, subsequently reclassified as Didymella clematidis and then Longididymella clematidis - see Woudenberg et al. (2009) and Hou et al. (2020) entries in 'General comments' section] from Clematis ligusticifolia, that was collected in Washington State, USA, was selected for release in New Zealand. A weakly pathogenic form of L. clematidis was already present in New Zealand. An application for release of the fungus was made in 1996 and approved, and the fungus introduced in that year.

Gourlay (2008) - a selected strain of this fungus was introduced from USA by the Department of Scientific and Industrial Research in 1990 as a biocontrol agent; other less virulent strains were already present in the country.

Released:

1996

Release details:

Landcare Research (1998a, 1998c, 1999d, 2000c) - eleven releases were made in the year to Jul 1998 (taking the total number of releases at that time to 15, made throughout New Zealand), 12 in the year Aug 1998 - Aug 1999, 15 in the year Sep 1999 - Aug 2000.

Gourlay et al. (2000) - the new virulent strain of L. clematidis was introduced in 1996; it has now been released at 23 sites in New Zealand.

Gourlay (2008) - first releases were in summer of 1996; widespread releases began in spring 1997.

Establishment:

Landcare Research (1999b, 1999c) - Longididymella clematidis has dispersed surprising quickly. This year infected plants were seen in many places (e.g. Auckland, Otago, and the West Coast) that are all some distance (as much as 200 km) from the nearest known release sites. The fungus is now established in all old man’s beard-infested regions.

Gourlay et al. (2000) - establishment of the virulent strain L. clematidis has been confirmed at 11 of the 23 release sites and this strain has spread rapidly throughout the country.

Landcare Research (2001d) - common.

Gourlay (2008), Landcare Research (2008c) - a molecular study has not found any evidence that the strain that was deliberately released is still present in New Zealand.

Landcare Research (2021b) - the deliberately released strain did not persist and is believed to have been outcompeted by native fungi.

Impacts on target:

Landcare Research (1998b) - so far, the impact of L. clematidis has exceeded expectations; at some sites in the Manawatu-Wanganui region of the North Island, all C. vitalba plants had blackened, dead and dying leaves and stems, and it looked as though whole vines had been killed. Badly infected vines have not set any seed, and many of the seed heads that did form were destroyed by the fungus.

Landcare Research (1999c) - Longididymella clematidis is causing noticeable damage at many of the damper sites.

Gourlay et al. (2000) - at several of the release sites, L. clematidis has caused extensive leaf necrosis, leaf fall, and stem dieback of C. vitalba.

Landcare Research (2001d) - often causes obvious damage.

Landcare Research (2005e) - old man’s beard leaf fungus is common and sometimes causes obvious damage, especially in autumn, but can exist as a symptomless endophyte. [NB: the strain deliberately released was introduced as Phoma clematidina but was subsequently reclassified as Longididymella clematidis, and is not the endophytic strain/species - see Landcare Research (2008c) entry below in this section.]

Paynter et al. (2006) - insecticide and fungicide exclusion experiments were performed in the field near Blenheim in the South Island between September 2003 and April 2004 to determine the impact, both separately and in combination, of two biological control agents, L. clematidis and a leaf-mining fly, Phytomyza vitalbae, released against C. vitalba. Although both agents were common on non-treated plants, they damaged only a small fraction of the total leaf area, with most damage occurring in late autumn after the main period of stem growth. There was no impact on growth and only a minor reduction in percentage cover (8-10%) of non-treated plants. Most of the damage to leaves was caused by P. vitalbae; disease symptoms were generally only expressed late in the growing season, when leaves were senescent, and were correlated with P. vitalbae damage. Longididymella clematidis alone appears insufficiently pathogenic to cause disease symptoms during the main growing season of C. vitalba. In this study, 3.94% of leaves of non-treated plants were recorded with L. clematidis symptoms, compared to 14.28% in a study at Mangaweka (central North Island) in January 2004.

Gourlay (2008) - initially caused considerable damage, but has since become rare and has probably died out. Minor damage caused by the less virulent strains is commonly seen.

Landcare Research (2008c) - a molecular study has shown that there are multiple strains of the fungus currently known as Phoma clematidina in New Zealand, that some may in fact be different species and that one unexpected strain exists in the leaves of C. vitalba as an endophyte without causing disease symptoms. [The strain deliberately introduced into New Zealand was introduced as P. clematidina but has since been reclassified as Longididymella clematidis – see Woudenberg et al. (2009) and Hou et al. (2020) entries in 'General comments' section.] It is possible that endophytes are protecting C. vitalba from attack by pathogenic fungi and that this is the reason the deliberately introduced strain has become rare or died out.

Landcare Research (2016d) - it is possible that the released strain was outcompeted by other fungi on old man's beard, some of which studies have shown occur as symptomless endophytes that may confer disease resistance to the plant.

Impacts on non-targets:

Gourlay et al. (2000) - in initial host range tests carried out prior to the application to release L. clematidis, small lesions were formed on petioles of Clematis paniculata and C. quadribracteolata [both endemic species], leaf spots on C. montana [an exotic ornamental species] and necrotic spots on three weed Ranunculus species. Further tests were carried out against 16 endemic Clematis species and 16 endemic Ranunculus species; minor spotting occurred on leaves of some plants but no pycnidia were formed on any species.

Landcare Research (2006b) - surveys for non-target attack have found small lesions and rot on several native Clematis species attributed to Phoma clematidina. While this was predicted from host-testing of the deliberately released strain [considered at the time to be Phoma clematidina but since reclassified as Longididymella clematidis - see Woudenberg et al. (2009) and Hou et al. (2020) entries in 'General comments' section] it is suspected that there is more than one fungal species involved and the minor non-target attack could be due to the original accidentally introduced strain/species. Molecular studies are underway to differentiate strains of the fungus [see Landcare Research (2008c) and Paynter (2008) entries below in this section].

Gourlay (2008) - Longididymella clematidis was expected to possibly cause slight damage to some of the ornamental Clematis species that are closely related to old man’s beard. No other plants were believed to be at risk.

Landcare Research (2008c) - a molecular study has shown no evidence of the deliberately released strain of L. clematidis attacking native Clematis species.

Paynter (2008) - minor non-target damage was predicted for the old man’s beard fungus on closely-related ornamental Clematis. Studies have shown that fungi found damaging native and ornamental Clematis are not the strain/species deliberately released against old man’s beard [as Phoma clematidina but since reclassified as Longididymella clematidis - see Landcare Research (2006b) entry above in this section] and in fact there is no evidence that this fungus is still present in New Zealand.

General comments:

Woudenberg et al. (2009) - multiple taxa are present within the morphological variation understood to represent Phoma clematidina. A study to assess the diversity of P. clematidina by means of DNA sequence comparisons showed three distinct groups which are elevated to species level. One of these is described as Didymella clematidis. Due to the presence of only two-celled conidia both in vitro and in vivo, the anamorph [asexual] stage of D. clematidis (previously considered to be Phoma clematidina) is classified in the genus Ascochyta. This species has been released in New Zealand as a biological control agent of Clematis vitalba.

Hou et al. (2020) - Didymella clematidis is shown to be part of a fully supported clade that is distant from Didymella and distinct from other known genera in family Didymellaceae and is consequently reclassified in a newly introduced genus as Longididymella clematidis.

References

Gourlay AH, Wittenberg R, Hill RL, Spiers AG, Fowler SV (2000). The biological control programme against Clematis vitalba in New Zealand. In Proceedings of the X international symposium on biological control of weeds 2000 (pp. 799-806). Montana State University Bozeman, Montana, USA. https://bugwoodcloud.org/ibiocontrol/proceedings/pdf/10_709-718.pdf

Gourlay H (2008). Old man's beard fungus: Phoma clematidina. The Biological Control of Weeds Book - Te Whakapau Taru: A New Zealand Guide (Landcare Research) [Updated 2021] https://www.landcareresearch.co.nz/discover-our-research/biodiversity-biosecurity/weed-biocontrol/projects-agents/biocontrol-agents/old-mans-beard-leaf-fungus/

Hou LW, Groenewald JZ, Pfenning LH, Yarden O, Crous PW, Cai L (2020). The phoma-like dilemma. Studies in Mycology 96: 309-396 https://doi.org/10.1016/j.simyco.2020.05.001

Landcare Research (1998a). Quarantine graduates - where are they now? Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 1997/98. July 1998, 4: 10-11 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp98.pdf

Landcare Research (1998b). Old man's beard wars - the agents strike back. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 1997/98. July 1998, 4: 4-5 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp98.pdf

Landcare Research (1998c). Control agents released in 1997/98. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 1997/98. July 1998, 4: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp98.pdf

Landcare Research (1999b). Old man's beard project goes ahead in leaps and bounds. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 1998/1999. August 1999, 5: 4-5 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp99.pdf

Landcare Research (1999c). Quarantine graduates - where are they now? Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 1998/1999. August 1999, 5: 12-13 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp99.pdf

Landcare Research (1999d). Control agents released in 1998/99. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 1998/1999. August 1999, 5: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp99.pdf

Landcare Research (2000c). Control agents released in 1999/00. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 1999/2000. August 2000, 6: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp00.pdf

Landcare Research (2001d). Who's who in biological control of weeds? Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 2000/2001. August 2001, 7: 14-15 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp01.pdf

Landcare Research (2005e). Who's who in the biological control of weeds. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 2001/2002. August 2002, 8: 14-15 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp02.pdf

Landcare Research (2006b). Are they behaving themselves? What’s New In Biological Control of Weeds? Annual Review. August 2006, 37: 6-7 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew37.pdf

Landcare Research (2008c). Fascinating fungal findings. What’s New In Biological Control of Weeds? November 2008, 46: 3-4 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew46.pdf

Landcare Research (2016d). What's happening with old man's beard? Weed Biocontrol: What's New? 76: 4-5 http://www.landcareresearch.co.nz/publications/newsletters/biological-control-of-weeds/issue-76

Landcare Research (2021b). Old man's beard agents show promise. Weed Biocontrol: What's New? 95, Feb 2021 https://www.landcareresearch.co.nz/publications/weed-biocontrol/weed-biocontrol-articles/old-mans-beard-agents-show-promise

Paynter Q (2008). How safe are biocontrol agents for weeds? The Biologial Control of Weeds Book. https://www.landcareresearch.co.nz/assets/Discover-Our-Research/Biosecurity/Biocontrol-ecology-of-weeds/3-applications/How_Safe_are_Biological_Control_Agents.pdf

Paynter Q, Waipara N, Peterson P, Hona S, Fowler S, Gianotti A, Wilkie P (2006). The impact of two introduced biocontrol agents, Phytomyza vitalbae and Phoma clematidina, on Clematis vitalba in New Zealand. Biological Control 36: 350-357 https://doi.org/10.1016/j.biocontrol.2005.09.011

Woudenberg JHC, Aveskamp MM, de Gruyter J, Spiers AG, Crous PW (2009). Multiple Didymella teleomorphs are linked to the Phoma clematidina morphotype. Persoonia - Molecular Phylogeny and Evolution of Fungi 22: 56-62