Could Phytophthora pluvialis pulverise UK forestry? - Dr Terry Mabbett

WITH 65 shopping days to Christmas, an unwelcome new arrival was announced by the Forestry Commission (FC) – and with impeccable seasonal timing, because Phytophthora pluvialis, found for the first time on conifers in Cornish woodland, is closely aligned with our own Phytophthora ilicis, a pathogen of the much-revered English holly. 

Phytophthora pluvialis wasn’t on my radar and there is no reason why it should have been, given the species is a relatively recent and geographically-obscure ‘invention’. It was first reported in Oregon in the Pacific North West on Douglas fir (Pseudotsuga menziesii) and tanoak (Notholithocarpus densiflorus) in 2013, and subsequently in 2014, causing red needle cast on Pinus radiata (Radiata pine) in New Zealand. 

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

Huge numbers of Phytophthora species stalk planet earth, causing disease in a wide range of plants from tomatoes to trees, including angiosperms (broadleaves) and gymnosperms (conifers). Scores of different Phytophthora species have been described, with many more still waiting to be discovered. Given the number involved, there is a clear need to group Phytophthora species according to their most common characteristics.

This is based on DNA sequencing using internal transcribed spacer (ITS) sequences. Phytophthora pluvialis is in ITS Clade 3 along with: 
• P. ilicis – causes a leaf and twig blight in a number of Ilex species including Ilex aquifolium (English holly). Present in the UK, according to CABI
• P. pseudosyringae – causes root and collar rot disease in a number of broadleaf species with Nothofagus (southern beech) more susceptible than most. Present in the UK, according to CABI
• P. nemorosa – causes leaf blight and shoot dieback in some evergreen trees including coast redwood. Not present in the UK, according to CABI
• P. psychrophila – leaf and stem pathogen of European oak and Ilex (holly) species. This Phytophthora species is not recorded as present in the UK.

The commonality of these ITS Clade 3 species is genetic, determined by DNA sequences in the respective genomes, but there are common phenotypic characteristics as well, with semi-papillate sporangia (singular sporangium) as a key one of note for budding mycologists with magnification at their fingertips.

PHYTOPHTHORA PLUVIALIS IN SOUTH-WEST ENGLAND

With characteristic aplomb, the FC and Forest Research announced the first finding of this fungus-like Phytophthora pluvialis pathogen in woodland in Cornwall in September, and said this was the first report in Europe. They are unsure as to whether this pathogen is the direct cause of the disease symptoms observed on Douglas fir and western hemlock (Tsuga heterophylla).

A combined force of the FC, Forest Research and Animal and Plant Health Agency (APHA) officers is conducting further surveillance and diagnostic analysis to understand more about the pathogen and to ensure any required and available control measures are undertaken promptly to prevent further spread.

Symptomatic details of the disease on Douglas fir and western hemlock are not documented in the initial press release, but UK chief plant health officer Nicola Spence is quoted as saying: “I urge all sectors to support efforts to tackle this pathogen by checking the health of western hemlock and Douglas fir trees. Key symptoms to look for are lesions on the stem, branch or roots.” 

This general range covers some symptoms observed in Oregon, the USA and New Zealand. However, the absence of any request for observers to inspect foliage presumably rules out the discovery in Cornwall of needle blight and/or needle cast, both common symptomatic features of disease caused by P. pluvialis in Oregon and New Zealand.

Given that the finding in Cornwall was made in September, and since the plant health authorities are unsure as to whether the symptoms of disease are directly caused by Phytophthora pluvialis, it would appear that Koch’s postulates had not yet been satisfied when the initial FC press release was published in late October.

Developed in the 19th century, Robert Koch’s postulates are four criteria designed to assess whether a micro-organism causes a disease. The four criteria are: (1) The micro-organism must be found in diseased but not healthy individuals; (2) The micro-organism must be cultured from the diseased individual; (3) Inoculation of a healthy individual with the cultured micro-organism must recapitulate the disease; and finally (4) The micro-organism must be re-isolated from the inoculated, diseased individual and matched to the original micro-organism. 

The FC has introduced a demarcated area in Cornwall to restrict the movement of materials capable of spreading the disease. The Plant Health (Phytophthora pluvialis) (Demarcated Area No.1) Notice, which came into effect on 27 October prohibits the movement of any wood, isolated bark and trees (including live trees, felled or fallen trees, fruit, seeds, leaves or foliage) of the genus Tsuga, Pseudotsuga, Pinus and Notholithocarpus, that has originated within the demarcated area. 

The demarcated area occupies a part of south-east Cornwall stretching approximately 15 km from north to south and 15 km from east to west. It includes the towns of Bodmin, Lostwithiel and Liskegard, with St Austell and Looe just outside. The area doesn’t appear to meet the ocean at any point.

NATURE OF THE RISK POSED

So what do the plant health authorities consider to be the nature and magnitude of risk from this newly-arrived pathogen to our trees, woodland and forests? The FC wasted no time in carrying out a pest-risk analysis, the most significant sections of which are:

• Criterion: Probability of establishment of the pest in Great Britain territory, or the specific parts of Great Britain 

Answer: Note that this pest is established elsewhere in countries with climates similar to those found in Great Britain (e.g. Oregon and southern Washington state in the USA; New Zealand including parts of the South Island).
• Criterion: Probability of spread of the pest in Great Britain territory, or the specific part(s) of Great Britain. 
Answer: Yes. Environmental factors such as high rainfall in Great Britain are considered favourable for the pest. The means by which P. pluvialis is disseminated are not well known, though spread via water splash and similar means is plausible. Therefore there are unlikely to be natural barriers against spread in Great Britain. Suitable hosts (e.g. Pseudotsuga menziesii – Douglas fir) are widespread in Great Britain.
• Criterion: Potential economic, social and environmental impact of the pest 
Answer: Yes. Yield and quality losses: In particular this pathogen causes premature needle drop in infected conifers. These are recorded yield losses in its current range. Similar levels of damage could be expected in Great Britain.

The truth is that no one really knows, because Phytophthora pathogens like P. pluvialis are entirely unpredictable, as previous experience with Phytophthora ramorum shows.

After circulating unidentified within European plant nurseries, the EU 1 genetic lineage of P. ramorum arrived in UK on imported hardy nursery stock including viburnum and rhododendron, most probably from the Netherlands and Germany. It subsequently swept through the UK nursery trade but was also recorded in the wider environment on a range of broadleaf trees, though not in great numbers. Tree species affected included white-flowering horse chestnut, sweet chestnut, English oak, Turkey oak, holm oak, sycamore, North American red oak, European beech and southern beech. 

Meanwhile, the North American lineage NA1 had decimated native North American true oaks and tanoaks in the Pacific Northwest and it was assumed the EU 1 lineage would do the same to native English oak trees in UK. As such, the stem necrosis disease caused by P. ramorum was duly dubbed sudden oak death (SOD), as in North America. 

Phytophthora ramorum subsequently found rhododendron ponticum a genial sporulation host from where it jumped onto the hapless Japanese larch, which offered even greater infection potential as a dual sporulation/terminal tree host. The rest is well documented.

Sudden oak death (SOD) became sudden larch death (SLD) as the disease quickly removed Japanese larch as a premium timber tree from the UK commercial forest species portfolio. 

None of this had been imagined let alone predicted after the very first finding of Phytophthora ramorum on viburnum at a garden centre in Sussex in February 2002, and the first finding on a mature tree in November 2003, also in Sussex, on a 100-year old North American red oak. Despite P. ramorum being found infecting Japanese larch in Brittany, France in 2017, mature trees in the wider European environment as a whole remain largely unscathed.

IMPLICATIONS FOR TREE SPECIES AND FOREST/WOODLAND ECOSYSTEMS IN UK 

To get a better idea of what this pathogen and its disease could mean for particular tree species, woodland ecosystems and commercial forestry in the UK, we can take a closer look at what is already documented in the Pacific North West (USA) and New Zealand.

Susceptible species

Conifers – Observations made in both Oregon and New Zealand show conifers as the most susceptible group of trees to P. pluvialis. Douglas fir and western hemlock (both natives of the Pacific Northwest) were rapidly identified as key plant hosts of P. pluvialis in Oregon. In New Zealand Radiata pine was initially most severely affected although disease, described as ‘red needle cast’ of radiata pine, was subsequently found on Douglas fir. 

According to the FC, mature Douglas fir and western hemlock are the two species of conifer identified with disease in the affected Cornish woodland. Both Douglas fir and western Hemlock are key commercial conifers in the UK, particularly following the demise of premium timber tree species like Corsican pine and Japanese larch, doomed to eventual commercial extinction by Dothistroma and P. ramorum respectively. The latest Forestry Statistics (2021) record 46,000 ha of Douglas fir in Great Britain – England (25,000 ha), Scotland (12,000 ha) and Wales (9,000 ha).

Pinus radiata (radiata pine) is not grown commercially in the UK and is unlikely to be planted on a large scale in future, irrespective of P. pluvialis, due to its high susceptibility to Dothistroma needle blight.

Broadleaves – Native North American tan oak Notholithocarpus is the broadleaf most frequently mentioned in relation to P. pluvialis in the Pacific Northwest. Tanoaks are few and far between in UK, found in botanic gardens and on other arboriculture sites. However, the Notholithocarpus genus is transitional between chestnuts (Castanea spp.) and true oaks (Quercus spp.), with flowers which look like chestnuts and fruits similar to those of true oaks. 

Phytophthora ramorum appears to be tightening its grip on sweet chestnut (Castanea sativa) in Britain. Between 2015 and 2020 Forest Research reported 68 sites where sweet chestnut was found with P. ramorum and almost entirely in Cornwall and Devon.

Phytophthora species thrive in moist humid conditions. This has certainly been the experience in UK where pandemic potential of P. ramorum has been unleashed up the maritime western flank of the British Isles. There is no reason to suspect that it will be any different for P. pluvialis if the moisture-loving fungus-like pathogen spreads from the present focus of infection in Cornwall.

POTENTIAL SPREAD

Work will soon be underway to determine ways and means of pathogen and disease spread, but indications from Oregon do not make for comfortable reading. Following the first findings of the pathogen in association with twig and stem cankers on tanoak in 2013 in mixed tanoak/Douglas fir stands P. pluvialis inoculum was recovered from soil, streams and canopy drip. If Phytophthora spores are present in water drips which fall from needles and branches high in the canopies of tall conifer trees, then spore inoculum will almost certainly be carried in water droplets picked up and spread by wind movements. Movement in air-currents looks a likely mode of spread of P. ramorum from the south-west England peninsula and across the Bristol channel into South Wales.

FORESTRY SYSTEMS

Researchers in Oregon report Douglas fir seedlings developing needle-blight symptoms when exposed to infection under 20-30 year-old Douglas fir tree plantations. Douglas fir is most frequently mentioned in relation to needle blight on seedling conifers in both Oregon and New Zealand. As such, it could pose a real threat to forest nurseries, although Douglas fir does not generally feature in the UK Christmas tree industry. And P. pluvialis would clearly present a threat to mixed woodland where Douglas fir is a component and natural regeneration is required to sustain the forest system. In this context, implications for western hemlock are even more serious because western hemlock is one of the conifers that can regenerate freely under mature canopies. 

Observations and reports of tree-disease symptoms caused by P. pluvialis to conifers in Oregon and New Zealand focus on needle blight and needle cast, with stem cankers on mature trees invariably absent from accounts and discussions. The needle cast symptom on Douglas fir in Oregon is described as bare lower branches, coupled with abundant green or yellow needles covering the ground beneath the trees.

In contrast, the picture posted by the FC's initial press release in October features a well-grown if not mature western hemlock tree suffering from a large stem canker with classic Phytophthora signs and symptoms – wet necrosis and cankerous bark, oozing and bleeding from the affected area and apparently well on the way to encircling and ring-barking the tree with all the signs of terminal tree disease.

SHRINKING OPTIONS FOR CONIFERS

Phytophthora pluvialis could be the latest in a line of pathogens restricting the range of conifers planted in UK commercial forestry. Corsican pine and Japanese larch are essentially out for the count due to Dothistroma and P. ramorum. But the fall-out does not stop there, because the authorities tend to talk purely about larch when reporting P. ramorum. Although the majority of disease has been recorded on Japanese larch, this tendency to lump all larch together could lead to European larch and Hybrid larch being lost by default. However, David Gwillam at Prees Heath Forest Nurseries in Shropshire says his customers are planting European larch, not in pure stands but in mixtures, with Douglas fir and western red cedar.

READ MORE: Phytophthora Pluvialis: New tree disease found in Scotland for the first time

Dothistroma continues to spread its plant-host wings to infect lodgepole pine and native Scot’s pine. David Gwillam says the frequency of Dothiostroma in the wider environment has hit plantings of lodgepole pine but thankfully not Scot’s pine.
The recent discovery of Ips typographus on at least five sites across Kent and East Sussex raises a question mark over Norway spruce (the primary spruce host of Ips typographus) and with fewer – but very real – fears for Sitka spruce (a recorded host of I. typographus), accounting for over half of the commercial softwood plantation in UK.

WORST AND BEST-CASE SCENARIOUS FOR P. PLUVIALIS

The worst-case scenario is P. pluvialis inflicting on Douglas fir and/or Western Hemlock what P. ramorum did to Japanese larch or turning its attention to a tree species that is not currently on the radar of research scientists in Oregon, New Zealand or Cornwall.

Phytophthora ramorum spent its first seven years in the UK, taking bites out of scores of different tree and shrub species before deciding to tear the heart out of Japanese larch, starting in 2009. 

The best-case scenario for P. pluvialis is retreat into relative obscurity like Phytophthora kernoviae which arrived in UK as an alien pathogen around the same time as P. ramorum and with a similar tree host range and tree-disease dimensions. Phytophthora kernoviae appears to have disappeared from the radar, although it is still regarded as a potentially serious threat especially to beech trees. Let’s hope the situation for P. pluvialis pans out like P. kernoviae and not P. ramorum, with taxonomists forced to consider a name change from ‘pluvialis’ to ‘pulveralis’.

AUTHOR'S NOTES

Sporangium: a sac which contains and carries asexual spores. In the Phytophthora genus these asexual spores are motile zoospores.

Papilla: a small bud-like and generally translucent swelling of the wall of a sporangium, which on breaking is the exit point of zoospores contained therein.

Semi-papillate: refers to sporangia with papilla which are shallow and less nipple-like than the fully papillate sporangial structures. Sporangia of Phytophthora pluvialis and its most closely related species produce semi-papillate sporangia.

NOTE: This article was originally published before some recent developments.