Dr Terry Mabbett recalls the discovery and spread of Phytophthora ramorum in the UK and asks what the details of that crisis may tell us about the road ahead for Phytophthora pluvialis, now that its presence has been confirmed across Britain.

I FIRST put pen to paper on Phytophthora ramorum in February and April 2004 for Forestry and British Timber. The first UK finding of P. ramorum was on evergreen Viburnum tinus at a garden centre in Sussex in February 2002, while the first mature tree confirmed with the disease was a North American native broadleaf, a southern red oak (Quercus falcata) found in November 2003, also in Sussex. 

By April 2004, additional plant hosts were being chalked up at a frightening frequency, with the pathogen and disease already out of control on understorey Rhododendron ponticum. Confirmed tree hosts included Castanea sativa (sweet chestnut), Quercus ilex (holm oak), Fagus sylvatica (common beech) and Acer pseudoplatanus (sycamore), although no-one foresaw the fate awaiting Japanese larch (Larix kaempferi) at the hands of P. ramorum in 2009.

READ MORE: What is Phytophthora Pluvialis? Everything we know so far

This was because all eyes were still on a perceived high risk for English oak after P. ramorum, albeit as a different genetic lineage, decimated North American native trees including Quercus agrifolia (coast live oak), Quercus kelloggii (California black oak) and Notholithocarpus densiflorus (tan oak) in woodlands along the Pacific Northwest coast. In those early days, the disease was dubbed ‘sudden oak death’, appropriately shortened to SOD by Tony Burt, editor of Forestry and British Timber. 

Almost 20 years later we are now confronted with Phytophthora pluvialis infecting plantation conifer trees. This time round, hindsight allows us to compare P. pluvialis in real time with P. ramorum over the last two decades. First indications offer an unnerving sense of déjà vu.

NOMENCLATURE AND HISTORY

P. ramorum and P. pluvialis are relatively recent additions to the Phytophthora stable. The first report of P. ramorum was in 1995 from the USA, where the pathogen was already killing large numbers of tan oak trees in the Pacific Northwest. As North American lineage NA1, the pathogen was eventually documented in 2000 as a new species of Phytophthora, called Phytophthora ramorum. 

At the same time, a range of disease symptoms on evergreen shrubs in European plant nurseries were casually assigned to an ‘unknown species of Phytophthora’. Only after P. ramorum was exported to the UK from the Netherlands and Germany, and subsequently identified on a Viburnum plant in a Sussex garden centre, was the EU1 genetic lineage of Phytophthora ramorum finally decoded and documented.

Forestry Journal: hades of a past pandemic caused by Phytophthora ramorum? Will we see this again? Japanese larch is seen here changing to the wrong shade at the wrong time due to a foliar blight caused by P. ramorum. Will western hemlock and Douglas fir be in the firing line this time round from Phytophthora pluvialis?hades of a past pandemic caused by Phytophthora ramorum? Will we see this again? Japanese larch is seen here changing to the wrong shade at the wrong time due to a foliar blight caused by P. ramorum. Will western hemlock and Douglas fir be in the firing line this time round from Phytophthora pluvialis?

The first report of P. pluvialis as a primary plant pathogen came in 2013 from Oregon on Douglas fir (Pseudotsuga menziesii) and tan oak (Notholithocarpus densiflorus), then in 2014 in New Zealand as red needle cast disease on radiata pine (Pinus radiata). 

Numerous Phytophthora species have been genetically sequenced for assignment to a specific Phytophthora ITS (internal transcribed spacer) clade. P. ramorum is in Clade 8c and P. pluvialis is in Clade 3, alongside other Phytophthora species, some of which are also present in the UK. 

Many Phytophthora species are extremely difficult to distinguish from each other without the use of these state-of-the-art genetic tools. As such, it is not unusual for a ‘new’ species to have been rattling around for some time, especially in the plant nursery trade, without the relevant in-country plant health authorities realising its existence. 

This is essentially what happened to the EU1 genetic lineage of P. ramorum which was circulating in the European plant nursery trade, on evergreen shrub species like Rhododendron ponticum and Viburnum tinus, as an ‘unknown Phytophthora’ in the mid 1990s. The ‘unknown Phytophthora’ escaped scrutiny until turning up in the UK circa 2000 on hardy, evergreen nursery stock imported from Europe. Eventually identified as P. ramorum, the pathogen subsequently escaped into the wider UK environment and exploded into a full-blown plant disease pandemic along the western flank of the British Isles. 

The encounter between P. ramorum and Rhododendron ponticum proved instrumental in initiating and sustaining the pandemic. Foliage of this evergreen, understorey shrub proved to be a highly efficacious sporulation template, assisted by the mild maritime climatic conditions which enabled the host plant to grow and the plant pathogen to reproduce throughout the year.   

But the biggest blow was yet to come, following infection of Japanese larch after P. ramorum apparently jumped species from R. ponticum. Among the very first Japanese larch trees identified with infection were on an FC-managed estate at Plym in Devon in 2009, from where Forest Research scientists reported catastrophic levels of infection. Japanese larch was acting as a terminal host and a highly effective sporulation host for the Phytophthora pathogen. Spores released from diseased larch foliage had already initiated dieback and bole cankers in a wide range of non-sporulating coniferous and broadleaved host trees that were either part of the understorey or present in stands next to the infected Larix kaempferi.

‘ORIGIN’ AND HOST RANGE, SPREAD AND DISTRIBUTION

The first report of Phytophthora pluvialis was in September 2021 on western hemlock and Douglas fir in woodland in south-east Cornwall. Infected sites in Devon and Cumbria, and further infected sites in Cornwall, were announced in mid November. DEFRA and the Forestry Commission announced (27 November, 2021) a new community forest for Cumbria that will see thousands of trees planted along the west coast. The area appears to coincide very closely with the FC’s Notice No. 3/ Demarcated Area No. 3 (26 November, 2021), relating to the recent finding of Phytophthora pluvialis in Cumbria. Presumably, this means the project will be forced to reassess the chosen planting mix, especially if it was scheduled to include western hemlock and Douglas fir.

Forestry Journal: Rhododendron ponticum looks as pretty as a picture, but the exotic evergreen understorey shrub was instrumental in the loss of Japanese larch to Phytophthora ramorum.Rhododendron ponticum looks as pretty as a picture, but the exotic evergreen understorey shrub was instrumental in the loss of Japanese larch to Phytophthora ramorum.

When Scottish Forestry announced on 19 November 2021 that targeted inspections were underway in Scotland as a precautionary measure, you could almost sense what was coming next. They clearly did not have to look very far, because seven days later it was announced that this new disease had been found on trees at Loch Carron in the north-west of the country, although the report failed to say what the affected tree species were.

However, Lorna Slater, Scottish government minister for green skills, circular economy and biodiversity, said: “We are asking the forestry industry and landowners to help tackle this pathogen and avoid its spread. Please check the health of western hemlock and Douglas fir trees on your land,” indicating these same two conifers found with the disease in England were the ones of immediate concern in Scotland.

Forestry Journal: Lorna SlaterLorna Slater

Phytophthora pluvialis has only been recorded in the USA and New Zealand. Neither is believed to be the ‘centre of diversity’. How the pathogen found its way into the UK to infect trees over such a wide area as Cornwall and Devon, Cumbria, and north-west Scotland is clearly up for discussion, but I would not mind betting that, like P. ramorum, and irrespective of its centre of diversity, P. pluvialis arrived on the back of plant trade with Europe, courtesy the ‘Alexandre Dumas doctrine’ (all for one and one for all) permitting free trade in goods, services, pests and diseases. At least 14 outbreaks had been identified by the last week of November, suggesting the disease could have entered the UK on multiple occasions and has been here for some time.

P. ramorum has managed to collect a massive plant host range even by Phytophthora standards, with over 150 recorded hosts covering tens of different plant families. California bay laurel (Umbellularia californica) and Rhododendron ponticum have played pivotal roles in the reproduction, spread and survival of P. ramorum in the USA and British Isles. As evergreen understorey shrub species, their broad leaves offer an ideal, year-round sporulation template for pathogen and disease. Tan oak (Notholithocarpus densiflorus) is probably the most affected mature tree in the US, with Japanese larch the equivalent in the UK. 

Until its discovery in Cornwall, P. pluvialis was documented as a pathogen of Douglas fir (Pseudotsuga menziesii), western hemlock (Tsuga heterophylla), tan oak and Monterey (radiata) pine (Pinus radiata). The Forestry Commission also mentions Pinus strobus (eastern white pine/Weymouth pine) and Pinus patula (Mexican weeping pine) in the plant host profile of P. pluvialis, while the UK Plant Register lists both of these species as major hosts of P. pluvialis. 

READ MORE: Could Phytophthora pluvialis pulverise UK forestry? - Dr Terry Mabbett

Relatively recent research in New Zealand to which the FC/UK Plant Register presumably refers says: “Phytophthora pluvialis has been shown to be a foliar pathogen of various species of Pinaceae in North America and New Zealand where it has been primarily associated with red needle cast on Pinus radiata, and on Pseudotsuga menziesii, but it has also been isolated from Pinus patula and Pinus strobus.” However, there is no mention of P. pluvialis being pathogenic to these species. 

Compared to the same stage in the game with P. ramorum, it had already clocked up an impressive host range numbering dozens of different species. Eight years on from its identification in Oregon in 2013, the recorded host range of P. pluvialis remains relatively restricted, but New Zealand scientists say: “The rapid host diversification between closely related isolates of P. pluvialis in New Zealand suggests this pathogen has the potential to infect a broader range of hosts than is currently recognised.”

Experience shows pathogens gaining entry to and establishing in new environments seek out, infect and colonise plant host species not previously affected, irrespective of whether they were present in previously established environments.  The behaviour of P. ramorum in the UK with respect to plant host range provides a clear example. 

Forestry Journal: A basal stem (trunk) lesion on a western hemlock tree from which Phytophthora pluvialis was isolated.A basal stem (trunk) lesion on a western hemlock tree from which Phytophthora pluvialis was isolated.

The FC says it has identified western hemlock and Douglas fir as host plants of Phytophthora pluvialis in the UK, but there will be other possible target species with implications for rapid spread and containment failure, as happened with P. ramorum. Obvious candidates include native Pinus sylvestris (Scots pine), especially given the high susceptibility of Pinus radiata in New Zealand. 

Castanea sativa (sweet chestnut) is another one to watch. Like tan oak, it belongs to the plant family Fagaceae and is recorded as a terminal and sporulation host of P. ramorum. Castanea sativa is quite closely related to tan oak, which the leaves closely resemble although the fruit and seeds are more like the acorns of true oaks. Let’s not forget Rhododendron ponticum and all Larix species, given the plant host profile of P. ramorum, and Fagus sylvatica, given the high perceived risk to this native tree species from Phytophthora kernoviae, which is genetically close to P. ramorum.

UK plant health authorities may see fit to conduct comprehensive laboratory investigations into the susceptibility of key potential tree and shrub hosts as they did for P. ramorum in the first few years of the new millennium. Such trials can throw up frightening possibilities, but these may subsequently come to nothing much under field conditions. For instance, in 2005, Forest Research scientists carried out lab trials to assess the infection potential of P. ramorum on 23 broadleaves and 11 conifers. Douglas fir and Sitka spruce were subsequently shown to be among the most susceptible under laboratory conditions. 

Later, there were instances of field infections when Douglas fir and Sitka spruce were found growing close to high sporulation plant hosts like R. ponticum. However, P. ramorum has thankfully not yet posed an economic problem for either of these premium softwood timber trees. No larch species were included in the study, which is unfortunate as it might have flagged up what would befall the hapless Japanese larch at the hands of P. ramorum four years later in 2009.

DISEASE DIMENSIONS

P. pluvialis infection of conifers in Oregon and New Zealand is mostly restricted to the needle blight and needle cast symptoms and disease dimensions of this pathogen. Cankers observed on main stems, branches, stem collars and roots hardly feature in published papers and reports, which describe the situation as follows: Infection (of Pinus radiata) appears to be limited to the needles, with no recoveries of Phytophthora pluvialis having been made from the roots, stems or branches. 

In western Oregon, P. pluvialis is commonly associated with lower-canopy needle loss in dense, humid, closed-canopy forest plantations and natural stands, with suggestions that P. pluvialis might reduce the success of Douglas fir seedlings under dense stands of mature trees. Needle infection of Douglas fir was subsequently reported in both Oregon and New Zealand, causing chlorotic needle mottling, new growth dieback and canker development on the Douglas fir seedlings.

Forestry Journal: Phytophthora pluvialis appears to have gone straight for the jugular of UK commercial forestry with a terminal stem canker disease on plantation conifers like western hemlock, shown here.Phytophthora pluvialis appears to have gone straight for the jugular of UK commercial forestry with a terminal stem canker disease on plantation conifers like western hemlock, shown here.

Detailed information on the disease found in Cornwall, Devon and Cumbria is still sparse and understandably so, although several distinct threads to pathogen and disease are already apparent. Pictures released by the Forestry Commission/Forest Research illustrating diseased stands, trees and tree parts all feature western hemlock. 
Specific symptoms on mature trees include resinous cankers on main stems, shoots, twigs and root collars, as well as on natural regeneration (seedling trees of western hemlock). Mature western hemlock trees are pictured showing dieback and bare lower branches, with dead natural regeneration in the understorey. Despite Douglas fir being documented as a host, the pictorial evidence to illustrate this is yet to appear. Nothing has yet been said by the UK plant health authorities to indicate what the sporulation hosts of P. pluvialis could be.

All in all, the main disease dimension recorded so far in the UK appears to be stem and branch canker on mature western hemlock. This is in stark contrast to P. pluvialis on equivalent age and stage Douglas fir in Oregon and New Zealand, where needle blight and needle cast predominate. Perhaps this is more evidence showing how Phytophthora pathogens may behave completely differently in ‘new’ environmental situations.

COMMERCIAL IMPLICATIONS

The implications for commercial forestry in the UK are impossible to predict at this point, although the disease is apparently affecting two of our remaining premium commercial softwood timber trees. This is acutely dangerous at the current time because we have essentially lost any long-term benefits of other premium commercial softwoods such as Corsican pine (to Dothistroma needle blight) and Japanese larch (to P. ramorum). 

It’s not so much about the amount of conifer plantation forest immediately at risk, because Douglas fir and western hemlock only account for around 50,000 hectares, with Douglas fir at 46,000 hectares having the most prominent profile. However, timber quality also matters, especially for Douglas fir, and that could well be lost. Also, species options for commercial conifer planting are dwindling all the time, with Norway spruce and (heaven forbid) Sitka spruce at risk from the establishment and apparent spread of Ips typographus. 

Of foremost concern with Phytophthora pluvialis is the number of outbreaks already identified in a short space of time (especially to anyone recalling 2009 and the first finding of P. ramorum on Japanese larch in the English West Country, rapidly followed by the disease spreading right up the western flank of the British Isles).

What’s more, P. pluvialis and its disease manifestations appear to have gone straight for the commercial jugular of UK forestry by targeting a pair of premium softwood timber trees, unlike P. ramorum, which spent the first six or seven years of its time in the UK taking a bite out of all sorts of weird and wonderful trees and shrubs like southern beech (Nothofagus) and witch hazel (Hamamelis), before homing in on poor Japanese larch. 

DISEASE PROGRESSION

The first outbreak of the disease was reported in mid-October 2021 in Cornwall. As has been the case with many previous outbreaks of ‘new’ pests and diseases, these reports from the Forestry Commission were remarkably coy about location, with county or at best nearest large town as far as they were prepared to go. However, according to a report in The Times, the woodland site where P. pluvialis was first found is close to the National Trust’s Lanhydrock Estate. 

Following this first report, additional outbreaks, said to number around 12 in total, were identified in east Cornwall/west Devon, west Cumbria and north-west Scotland. The Forestry Commission introduced additional demarcated areas with movement restrictions on materials capable of spreading the disease. 

Forestry Journal: Western hemlock regeneration under its own mature canopy for which the commercial conifer is famed.Western hemlock regeneration under its own mature canopy for which the commercial conifer is famed.

The demarcated area for the original outbreak in Cornwall has been extended twice to currently cover a significantly enlarged area now 100 km in width. The demarcated area for west Cumbria has been extended once. All notices now include an additional restriction on the felling of susceptible material within the demarcated areas, unless the FC has been notified in advance.

Scottish Forestry duly announced the Plant Health (Phytophthora pluvialis) (Scotland Demarcated Area No. 1) notices covering the area around Loch Carron lying north of the Kyle of Lochalsh, which became effective on 15 December, 2021.

WALES COMPLETES JIGSAW

Any lingering hopes that Wales might escape Phytophthora pluvialis were finally dashed on 13 December 2021 when the Welsh government announced its first case at Dyfi Forest, Gwynedd. P. pluvialis is now established along the entire western maritime flank of the British Isles, with a distribution that mirrors the main infection of Japanese larch with P. ramorum.