''Bursaphelenchus xylophilus'', commonly known as pine wood nematode or pine wilt nematode (PWN), is a species of

nematode The nematodes ( or grc-gre, Νηματώδη; la, Nematoda) or roundworms constitute the phylum Nematoda (also called Nemathelminthes), with plant-Parasitism, parasitic nematodes also known as eelworms. They are a diverse animal phylum inhab ...

that infects trees in the ''Pinus'' genus of coniferous trees and causes the disease

pine wilt ''Bursaphelenchus xylophilus'', commonly known as pine wood nematode or pine wilt nematode (PWN), is a species of nematode that infects trees in the ''Pinus'' genus of coniferous trees and causes the disease pine wilt.''Bursaphelenchus xylophilus''.
Nemaplex. UC Davis. While native to North America, it spread in the early 20th century to

Japan Japan ( ja, 日本, or , and formally , ''Nihonkoku'') is an island country in East Asia. It is situated in the northwest Pacific Ocean, and is bordered on the west by the Sea of Japan, while extending from the Sea of Okhotsk in the north ...

and in the latter half of the century to other areas of

Asia Asia (, ) is one of the world's most notable geographical regions, which is either considered a continent in its own right or a subcontinent of Eurasia, which shares the continental landmass of Afro-Eurasia with Africa. Asia covers an area ...

, including

China China, officially the People's Republic of China (PRC), is a country in East Asia. It is the world's most populous country, with a population exceeding 1.4 billion, slightly ahead of India. China spans the equivalent of five time zones and ...

Taiwan Taiwan, officially the Republic of China (ROC), is a country in East Asia, at the junction of the East and South China Seas in the northwestern Pacific Ocean, with the People's Republic of China (PRC) to the northwest, Japan to the nort ...

, and

Korea Korea ( ko, 한국, or , ) is a peninsular region in East Asia. Since 1945, it has been divided at or near the 38th parallel, with North Korea (Democratic People's Republic of Korea) comprising its northern half and South Korea (Republic o ...

, as well as to

Europe Europe is a large peninsula conventionally considered a continent in its own right because of its great physical size and the weight of its history and traditions. Europe is also considered a Continent#Subcontinents, subcontinent of Eurasia ...

, including

Portugal Portugal, officially the Portuguese Republic ( pt, República Portuguesa, links=yes ), is a country whose mainland is located on the Iberian Peninsula of Southwestern Europe, and whose territory also includes the Atlantic archipelagos of ...

and

Spain , image_flag = Bandera de España.svg , image_coat = Escudo de España (mazonado).svg , national_motto = ''Plus ultra'' (Latin)(English: "Further Beyond") , national_anthem = (English: "Royal March") , i ...

History

Pine mortality in Japan was first reported by Munemoto Yano (矢野宗幹) in

Nagasaki prefecture is a Prefectures of Japan, prefecture of Japan located on the island of Kyūshū. Nagasaki Prefecture has a population of 1,314,078 (1 June 2020) and has a geographic area of 4,130 Square kilometre, km2 (1,594 sq mi). Nagasaki Prefecture borders ...

in 1905. The nematode was first discovered in the timber of longleaf pine (''Pinus palustris'') in

Louisiana Louisiana , group=pronunciation (French: ''La Louisiane'') is a state in the Deep South and South Central regions of the United States. It is the 20th-smallest by area and the 25th most populous of the 50 U.S. states. Louisiana is borde ...

United States The United States of America (U.S.A. or USA), commonly known as the United States (U.S. or US) or America, is a country primarily located in North America. It consists of 50 states, a federal district, five major unincorporated territorie ...

. Steiner and Burhrer reported that the nematode was a new species, and they named it ''Aphelenchoides xylophilus'' in 1934. In 1969, Japanese plant pathologists Tomoya Kiyohara (清原友也) and Yozan Tokushige (徳重陽山) discovered many unfamiliar nematodes on dead pine trees around the

Kyushu is the third-largest island of Japan's five main islands and the most southerly of the four largest islands ( i.e. excluding Okinawa). In the past, it has been known as , and . The historical regional name referred to Kyushu and its surroun ...

islands in Japan. Then, they experimentally inoculated the nematode to healthy pine and other conifer trees and observed them. The healthy pine trees were killed—especially Japanese red pine ('' Pinus densiflora'') and Japanese Black pine (''P. thunbergii''). However,

Jack pine Jack pine (''Pinus banksiana'') is an eastern North American pine. Its native range in Canada is east of the Rocky Mountains from the Mackenzie River in the Northwest Territories to Cape Breton Island in Nova Scotia, and the north-central and ...

(''P. banksiana''), Loblolly pine (''P. taeda''), Sugi redwood (''Cryptomeria japonica''), and

Hinoki cypress ''Chamaecyparis obtusa'' (Japanese cypress, hinoki cypress or hinoki; ja, 檜 or , ) is a species of cypress native to central Japan in East Asia, and widely cultivated in the temperate northern hemisphere for its high-quality timber and orname ...

(''Chamaecyparis obtusa'') trees were able to survive. In 1971, the researchers concluded that the nematode was the pathogen was the primary contributor to the high mortality of Japanese pine trees. In 1972, Yasuharu Mamiya (真宮靖治) and Kiyohara incorrectly claimed that the nematode was a new species, which they named Bursaphelenchus lignicolous. A 1981 reclassification united the American and Japanese forms as ''B. xylophilus''. Pine wilt nematode epidemics have occurred in Japan, particularly during warm, dry summers.Dwinell, L. D. and W. R. Nickle. (1989)
An Overview of the Pine Wood Nematode Ban in North America.
Gen. Tech. Rep. SE-55. Asheville, North Carolina: USDA, Forest Service, Southeastern Forest Experiment Station.Suzuki, K. 2002
Pine Wilt Disease: a threat to pine forest in Europe.
''Dendrobiology'' 48, 71-74. In the late 1970s and 1980s, the nematode was observed to have spread to other countries of Asia outside of Japan, including

, and

, and later observed in

, including

and

. The forests of Portugal have been particularly impacted, as the most abundant species, the

maritime pine ''Pinus pinaster'', the maritime pine or cluster pine, is a pine native to the south Atlantic Europe region and parts of the western Mediterranean. It is a hard, fast growing pine bearing small seeds with large wings. Description ''Pinus pinast ...

, comprising almost two-thirds of all trees, is susceptible to the nematode. In the 1990s, further spread of the nematode was reported in

Mexico Mexico (Spanish: México), officially the United Mexican States, is a country in the southern portion of North America. It is bordered to the north by the United States; to the south and west by the Pacific Ocean; to the southeast by Guatema ...

and

Nigeria Nigeria ( ), , ig, Naìjíríyà, yo, Nàìjíríà, pcm, Naijá , ff, Naajeeriya, kcg, Naijeriya officially the Federal Republic of Nigeria, is a country in West Africa. It is situated between the Sahel to the north and the Gulf o ...

. Many factors have contributed to the global spread of the nematode, including human activities, in particular infested timber exports, as well as

climate change In common usage, climate change describes global warming—the ongoing increase in global average temperature—and its effects on Earth's climate system. Climate change in a broader sense also includes previous long-term changes to E ...

and

ecological disturbance In ecology, a disturbance is a temporary change in environmental conditions that causes a pronounced change in an ecosystem. Disturbances often act quickly and with great effect, to alter the physical structure or arrangement of biotic and abiotic ...

Morphology

Species of the genus ''

Bursaphelenchus __NOTOC__ ''Bursaphelenchus'' is a genus of nematodes (roundworms) in the order Aphelenchida. Most are obligate mycophages, but some feed on wood, with two species, the red ring nematode (''B. cocophilus'') and the pine wood nematode (''B. xylop ...

'' are difficult to distinguish because they are similar in

morphology Morphology, from the Greek and meaning "study of shape", may refer to: Disciplines *Morphology (archaeology), study of the shapes or forms of artifacts *Morphology (astronomy), study of the shape of astronomical objects such as nebulae, galaxies, ...

. A positive identification can be made with molecular analyses such as restriction fragment length polymorphism (RFLP). ''B. xylophilus'' is distinguished by three characteristics: the spicule is flattened into a disc-shaped ''cucullus'' at the tip, the front vulval lip is flap-like, and the tail of the female is rounded.

Life cycle

The pine wilt nematode has a typical nematode life cycle, with four juvenile stages and an adult stage with both male and female individuals that

reproduce sexually Sexual reproduction is a type of reproduction that involves a complex life cycle in which a gamete ( haploid reproductive cells, such as a sperm or egg cell) with a single set of chromosomes combines with another gamete to produce a zygote tha ...

. The mycophagous phase of the life cycle takes place in dead or dying wood, where the nematodes live and feed upon

fungi A fungus ( : fungi or funguses) is any member of the group of eukaryotic organisms that includes microorganisms such as yeasts and molds, as well as the more familiar mushrooms. These organisms are classified as a kingdom, separately from ...

, rather than the wood itself. The nematode cannot travel outside of the wood independently; it must be transported by an insect vector. ''B. xylophilus'' has the shortest life cycle of any known parasitic nematode. In laboratory studies in which it is cultured on fungal media, its life cycle is completed in four days. In nature it reproduces most rapidly in the summer, producing large numbers of individuals that spread throughout the resin canal system of susceptible pines, into the trunk, the branches, and the roots. If living tree cells are no longer available the parasite feeds and reproduces on the fungal

hypha A hypha (; ) is a long, branching, filamentous structure of a fungus, oomycete, or actinobacterium. In most fungi, hyphae are the main mode of vegetative growth, and are collectively called a mycelium. Structure A hypha consists of one or ...

e growing in the resin canals. While the nematode becomes inactive during the fall and winter, they survive in pine trees through

overwintering Overwintering is the process by which some organisms pass through or wait out the winter season, or pass through that period of the year when "winter" conditions (cold or sub-zero temperatures, ice, snow, limited food supplies) make normal activi ...

Digestion

Several cellulose binding proteins are predicted by Kikuchi et al 2009. These are similar to the hosts' own

expansin Expansins are a family of closely related nonenzymatic proteins found in the plant cell wall, with important roles in plant cell growth, fruit softening, abscission, emergence of root hairs, pollen tube invasion of the stigma and style, meristem fun ...

Vectors

When the nematode was detected, the '' sawyer beetle'' was frequently found on dead pine trees, proving an important vector of the nematode, and that the nematode infected healthy pine trees.Katsura MORIMOTO. and Atsushi Iwasaki(1972) Role of ''Monochamus alternatus'' as a vector of ''Bursaphelenchus lignicolous'']. Journal of the Japanese forestry society（日本林学会誌）54(6): 177-183. The nematodes drop off the beetle, and infect healthy pine trees when the adult beetles eat the young pine branches. The pine wilt nematode is spread by a number of

bark beetle A bark beetle is the common name for the subfamily of beetles Scolytinae. Previously, this was considered a distinct family (Scolytidae), but is now understood to be a specialized clade of the "true weevil" family (Curculionidae). Although the ...

s and wood borers, typically associated with the genus ''

Monochamus ''Monochamus'' is a genus of longhorn beetles found throughout the world. They are commonly known as sawyer beetles or sawyers, as their larvae bore into dead or dying trees, especially conifersThe Free Dictionary (TFD) (2008)Genus Monochamus Re ...

'' of pine sawyers. Pine sawyers lay their eggs in the bark of dead timber. The growing

larva A larva (; plural larvae ) is a distinct juvenile form many animals undergo before metamorphosis into adults. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle. The ...

feeds on the wood and

pupa A pupa ( la, pupa, "doll"; plural: ''pupae'') is the life stage of some insects undergoing transformation between immature and mature stages. Insects that go through a pupal stage are holometabolous: they go through four distinct stages in their ...

tes in the resulting cavity. Nematodes of the third juvenile stage congregate in the cavity around the pupa, molt into the fourth juvenile stage, and invade the

trachea The trachea, also known as the windpipe, is a Cartilage, cartilaginous tube that connects the larynx to the bronchi of the lungs, allowing the passage of air, and so is present in almost all air-breathing animals with lungs. The trachea extends ...

of the adult beetle. During this dispersive stage, the beetle transports the nematode to other trees. File:Monochamus alternatus.jpg, ''Monochamus alternatus'' main vector in Japan. File:Monochamus saltuarius.jpg, ''M. saltuarius'', secondary vector in Japan. File:Monochamus galloprovincialis male up.JPG, ''M. galloprovincialis'', main vector in Europe

Mechanism of wilt and spread

The mechanism from initial nematode infection to the resultant death of the pine tree is not fully understood. The ultimate death of the tree is caused by the nematode's inhibition of the uptake of water. Small air pockets created by the nematode lead to air embolisms in the xylem tissue which prevents water movement. The embolism does not make

tylose Tyloses are outgrowths/extragrouth on parenchyma cells of xylem vessels of secondary heartwood. When the plant is stressed by drought or infection, tyloses will fall from the sides of the cells and "dam" up the vascular tissue to prevent furth ...

or clog the nematode or pine cell. The cause of cavitation and non-reversible embolism is not fully understood. In primary transmission, when the beetle feeds on a susceptible host pine, the pine wilt nematode enters the tree and feeds on the epithelial cells which line the resin ducts. This is referred to as the phytophagous phase of the nematode, and it results in pine wilt disease. Water transport in the tissues of the infested tree is disrupted, and the disease can manifest within as little as a few weeks. Signs include browning of the needles or yellowing of the leaves, and the tree may die within two to three months.

Grade of resistance

Furuno(1982)Tooshiu FURUNO. (1982) Studies on the Insect Damage upon the Pine-species imported in Japan : (No.7) On the Withering of the pines by the Pine Wilt. Bulletin of

Kyoto University , mottoeng = Freedom of academic culture , established = , type = National university, Public (National) , endowment = ¥ 316 billion (2.4 1000000000 (number), billion USD) , faculty = 3,480 (Teaching Staff) , administrative_staff ...

Forests 54, 16-30. observed standing pine trees in Japanese forest and ranked their resistance to pine wood nematode. The "high resistance" pines are rarely killed by the nematode, but young saplings or trees in weakened condition may succumb. ;High resistance :'' Pinus taeda'', ''P. elliottii'', ''P. palustris'', ''P. rigida'', ''P. taiwanensis'' ;Moderate resistance : ''P. strobus'', ''P. massoniana'', ''P. resinosa'', ''P. tabulaeformis'', ''P. banksiana'', ''P. contorta'', ''P. thumb''×''P. masso'' ;Moderate susceptibility : ''P. bungeana'', ''P. monticola'', ''P. parviflora'', ''P. strobiformis'', ''P. densiflora'', ''P. pinaster'', ''P. sylvestris'', ''P. ponderosa'', ''P. rudis'', ''P. pseudostrobus'', ''P. oocarpa'', ''P. radiata, ''P. greggii'' ;High susceptibility : ''P. koraiensis'', ''P. leiophylla'', ''P. luchuensis'', ''P. thunbergii'', ''P. nigra'', ''P. mugo'', ''P. khasya'', ''P. muricata''

Ongoing initiatives in Europe

The

European Commission The European Commission (EC) is the executive of the European Union (EU). It operates as a cabinet government, with 27 members of the Commission (informally known as "Commissioners") headed by a President. It includes an administrative body o ...

has enacted protective measures against species harmful to plants. Specific policies targeting ''B. xylophilus'' in Portugal were enacted in 2006 before a 2012 expansion to all

European Union The European Union (EU) is a supranational political and economic union of member states that are located primarily in Europe. The union has a total area of and an estimated total population of about 447million. The EU has often been des ...

member states. In 2015, emergency measures further expanded the definition of susceptible wood.

Management in the field

In Japan, scientists and forestry officials believe the most effective preventative technique is the removal of sawyer beetles, the vector of the nematode. The sawyers like to spawn near dying or dead pine trees, so it is advised to cut down these trees until next spring. The timber is subsequently chipped, burned or sprayed with insecticide to kill the sawyer larvae and pupae in the wood. The adult sawyers go out from the timber in late spring or early summer. They start eating young pine growth and spread the nematodes to the tree. Consequently, it is beneficial to kill the adult sawyers at this time to prevent the nematode infection to other trees. In Japan,

organophosphorus compound Organophosphorus compounds are organic compounds containing phosphorus. They are used primarily in pest control as an alternative to chlorinated hydrocarbons that persist in the environment. Some organophosphorus compounds are highly effective in ...

s and neonicotinoids like fenitrothion,

malathion Malathion is an organophosphate insecticide which acts as an acetylcholinesterase inhibitor. In the USSR, it was known as carbophos, in New Zealand and Australia as maldison and in South Africa as mercaptothion. Pesticide use Malathion is a pesti ...

, acetamiprid, and

thiacloprid Thiacloprid is an insecticide of the neonicotinoid class. Its mechanism of action is similar to other neonicotinoids and involves disruption of the insect's nervous system by stimulating nicotinic acetylcholine receptors. Thiacloprid was develop ...

are typically used to treat the adult sawyers. However, many environmentalists are opposed to the use of neonicotinoid-based insecticides. Bioinsecticides are another potential method to treat the sawyers that is currently being researched. Entomopathogenic fungus,

woodpeckers Woodpeckers are part of the bird family Picidae, which also includes the piculets, wrynecks, and sapsuckers. Members of this family are found worldwide, except for Australia, New Guinea, New Zealand, Madagascar, and the extreme polar regions. M ...

, and some parasitoid or prey insects are being investigated. Embargoes have been placed on untreated lumber from the United States and Canada to prevent the unintentional spread of this disease. Management practices have concentrated on preventing the spread of the nematode. Infected trees are cut and either burned or chipped, soft wood timber is stripped of its bark to prevent oviposition by vectors, and all lumber shipped overseas is either fumigated or kiln-dried. Despite these preventative measures the nematode has been confirmed in Portugal, and may yet spread further in Europe. File:Fenitrothion Structural Formulae .V.1.svg, fenitrotion (organophosphorus compound) File:Malathion.png, malathion (organophosphorus compound) File:Acetamiprid Structural Formulae V.1.svg, acetamiprid (neonicotinoid) File:Thiacloprid structure.svg, thiacloprid (neonicotinoid) File:Great Spotted woodpecker.jpg, Great spotted woodpecker In Japan, some nematocides are used to prevent the disease. For example, morantel, mesulfenfos, levamisole, emamectin, milbemectin, and

thionazin Thionazin is a chemical compound used in nematicide A nematicide is a type of chemical pesticide used to kill plant-parasitic nematodes. Nematicides have tended to be broad-spectrum toxicants possessing high volatility or other properties promoti ...

. Some biopesticides are also being studied, but they remain in the experimental stage. Inoculating infected trees with

nematophagous fungus Nematophagous fungi are carnivorous fungi specialized in trapping and digesting nematodes. Around 160 species are known. There exist both species that live inside the nematodes from the beginning and others that catch them, mostly with glue tra ...

may be a potential treatment for the disease.Mamiya, Y.; Hiratsuka, M.; Murata, M. (2005
Ability of wood-decay fungi to prey on the pinewood nematode, ''Bursaphelenchus xylophilus'' (Steiner et Buhrer) Nickle
日本線虫学会誌35(1): 21-30. File:ネマノーン (483707052).jpg, Nematocide applied to a tree File:Levamisole2.svg, Levamisole File:Emamectins.svg, Emamectin File:Milbemectin structure.svg, Milbemectin File:Thionazin.svg, Thionazin

Gallery

Bursaphelenchus xylophilus male tail.jpg, Pointed tail end of the male Austrian pine with wilt large.jpg, Austrian pine with pine wilt Cross-cutting of Austrian pine that has been affected with pine wilt.png, A cross-section of an affected Austrian pine Three Scots pines with pine wilt.png, Affected Scots pines on a Christmas tree farm

References

External links

(Japanese)

(Japanese)

(Japanese)

prey beetle, hope to decrease sawyers

Parasitoid beetle, hope to decrease sawyers {{DEFAULTSORT:Bursaphelenchus Xylophilus Aphelenchida