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A review of Cannabis diseases

J. M. McPartland

AMRITA, 53 Washington Street, Middlebury, VT, 05753, USA

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    McPartland, J. M., 1996.  A review of Cannabis diseases. Journal of the International Hemp Association 3(1): 19-23.
    Diseases of Cannabis are caused by organisms or abiotic sources.   Organisms include fungi (first and foremost), nematodes, parasitic plants, bacteria, and viruses.  Abiotic (non-living) causes include nutrient deficiencies, pollutants and genetic diseases.  Different diseases prevail in different crops (e.g., drug cultivars versus fiber cultivars).  Disease prevalence is also modulated by geography and climate.  The claim that Cannabis has no diseases is not correct, Cannabis suffers over 100 diseases, but less than a dozen are serious.   Serious diseases include gray mold, hemp canker, damping off, assorted leaf spots, blights, stem cankers, root rots, nematode diseases, broomrape, macro- and micronutrient deficiencies, and genetic diseases.  Environmentally stressed plants become predisposed to diseases.  Stress incudes drought, insufficient light, untoward temperatures, or growing plants in monoculture.

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Introduction
   Despite the oft-repeated quote, "hemp has no enemies" (Dewey 1914), Cannabis suffers many diseases.  Agrios (1988) estimates 11% of fiber crops are lost to diseases.  This statistic does not include insect injury.  Disease, by definition, is continued irritation damage by a causal factor (be it an organism or the environment).  In contrast, injury is due to a transient causal factor.  Insects are transient, they cause feeding injury, not disease.  Insects will be the subject of our next review.

Figure 1. Shapes and sizes of some organisms associated with Cannabis (adapted from Agrios, 1988)

Cucumber Mosaic virus
Aphid
stylet
Fungus
mycelium Mycoplasma-like organisms
Tobacco Mosaic virus
Head of Nematode
Nucleolus
Bacteria
Nucleus

    Organisms that cause continued irritation (disease) include viruses, bacteria, fungi, parasitic plants, and nematodes (Figure 1).  Plant diseases are almost always caused by fungi and rarely caused by bacteria.  In people this fungi-to-bacteria ratio is reversed.  Few Cannabis diseases can be transmitted to humans, but there are exceptions (McPartland, 1994).
    Some diseases prevail in Cannabis fiber and oil seed crops, other diseases predominate in drug crops.  Disease prevalence varies geographically.   For instance, many virus diseases are limited by the range of their insect vectors.   Disease prevalence shifts between greenhouse crops and outdoor crops.  Disease prevalence alters as plants grow from seedlings to flowering adults.  (Table 1).

Table 1.  Common Cannabis diseases

Seedling diseases	Flower & leaf diseases, outdoors	Flower & leaf, diseases, indoors	Stem & branch diseases	Root diseases
Damping-off fungi Storage fungi Genetic sterility	Gray mold Yellow and Brown leaf spots Downy mildew Olive leaf spot Nutritional diseases Brown blight Bacterial leaf diseases	Nutritional diseases Pink rot Gray mold Powdery mildew Brown blight Virus diseases	Gray mold Hemp canker Fusarium canker Fusarium wilt Stem nema Charcoal rot Anthracnose Striatura ulcerosa Dodder	Fusarium root rot Root knot nema Broomrape Rhizoc root rot Sclerotium rot Cyst nema

    Three lists of Cannabis diseases have been collated recently.  McPartland (1991) lists diseases by their common names (American Phytopathological Society URL address : http://www.scisoc.org).   This list is unweighted—severe and epidemic diseases are presented next to rare and benign diseases without differentiation.  Termorshuizen (1991) lists diseases by their causal organisms, alphabetically.  His discussion is weighted by disease severity and organized geographically.  But he is not entirely critical of old taxonomy.  Gutberlet & Karus (1995) list diseases by their causal organisms, taxonomically.  Their list is not weighted by disease severity nor critical of taxonomy.  The taxonomy of Cannabis pathogens has been ignored since the 1930s.  Concerning fungi alone, the scientific literature cites 400+ taxa as Cannabis pathogens.  Research reveals many of these species are misidentifications or taxonomic synonyms (McPartland 1995 a-e).  After a name-by-name review, McPartland (1992) determined the 400+ taxa represent about 88 true species of Cannabis fungal pathogens.
    This review is presented taxonomically, weighted by severity.   Discussion is organized primarily for fiber crops and geographically centered in Europe.  The review does not discuss control measures.

Fungi
   As mentioned above, at least 88 species of fungi attack Cannabis and more are being discovered every year (McPartland & Hughes 1994, McPartland & Cubeta 1996).  By far the most significant is gray mold, caused by Botrytis cinerea (teleomorph Botryotinia fuckeliana).   B. cinerea thrives in temperate regions with high humidity and cool to moderate temperatures.  Under these conditions gray mold can reach epidemic proportions and completely destroy a Cannabis crop within a week (Barloy & Pelhate 1962). B. cinerea attacks many crop plants and weed species worldwide.
    Gray mold presents in three scenarios, depending on plant maturity and cultivar.  Seedlings succumb to damping off, discussed below.  In fiber cultivars gray mold presents as a stem disease.  It arises as a gray-brown mat of mycelium which becomes covered by masses of conidia (fungal spores).  Stems become chlorotic at margins of the mat.  Enzymes released by B. cinerea reduce stems to soft shredded cankers.  Stems often snap at canker sites.  Gray mold may encircle and girdle stems, wilting everything above the canker.  Fiber varieties become more susceptible after canopy closure.  In field experiments in the Netherlands the disease was found from the beginning of July (Van der Werf and Van Geel, 1994).  Van der Werf et al. (1995) note Hungarian Kompolti Hibrid TC is more susceptible to gray mold than other fiber varieties.  Dempsey (1975) says the Russian cultivars JUS-1 and JUS-7 are resistant, but these may no longer be available (de Meijer 1995).
    In drug cultivars, gray mold infests flowering tops.  Large moisture-retaining female buds are most susceptible.  Fan leaflets first turn yellow and wilt, then pistils begin to brown.  Whole inflorescences soon become enveloped in a fuzzy gray mycelium then degrade into a gray-brown slime.  Drug varieties are most susceptible during flowering near harvest time.  Dense tightly-packed buds of Cannabis afghanica Clarke tend to hold moisture and easily rot (Clarke 1987).  Afghan cultivars evolved in very arid conditions and have no resistance to gray mold.  This unfavorable trait is often expressed in hybrids that have only a small percentage of C. afghanica Clarke heritage.
    For the second most important disease, Termorshuizen (1991) lists hemp canker.  This diease is caused by Sclerotinia sclerotiorum.  The fungus primarily attacks fiber cultivars in Europe, but it has caused up to 40% losses in North America (Hockey 1927) and damaged hemp in Australia (Synnott 1941) and Tasmania (Lisson & Mendham 1995).  Hemp canker has also appeared on drug cultivars in India (Bilgrami et al. 1981).  Symptoms begin as watersoaked lesions on stems and branches of plants nearing maturity.  The lesions collapse into cankers and become darkly discolored.  Affected areas take on a shredded appearance and the pith becomes filled with a white cottony mycelium.  Plants remain in this condition or wilt and fall over.  By September large black sclerotia develop on the stem surface or within pith of dead stalks.
    Damping off fungi kill seeds in soil or seedlings shortly after they emerge from the soil.  Fungi invade stems of seedlings at the soil line, causing a brown watery soft rot, then the plants topple over.  Most damping off is caused by two Protoctistan Pythium species (technically they are o–mycetes, not fungi), P. aphanidermatum and P. ultimum.  Several fungi also cause damping off—Rhizoctonia solani, Botrytis cinerea, Macrophomina phaseolina, and several Fusarium species, F. solani, F. oxysporum, F. sulphurem, F. avenaceum, F. graminearum.  Together they make damping off a ubiquitous problem, attacking all cultivars of Cannabis (Bush Doctor 1985).
    The two most common leaf spot diseases are yellow leaf spot caused by two Septoria species (McPartland 1995d), and brown leaf spot caused by about eight Phoma and Ascochyta species (McPartland 1995c).  These diseases rarely kill plants but sharply reduce crop yields.  Two common diseases of fiber varieties are downy mildew, caused by two Pseudoperonospora species, and olive leaf spot caused by a Pseudocercospora species and a Cercospora species.  Pink rot, caused by Trichothecium roseum, has recently killed greenhouse-grown drug cultivars and seems to be on the rise.  Less frequently seen but equally virulent diseases include brown blight (caused by two Alternaria and two Stemphylium species), anthracnose (caused by two Colletotrichum species) and white leaf spot (caused by Phomopsis ganjae).  Powdery mildews, black mildews, and rusts are caused by high-visibility fungi, but rarely cause serious problems (McPartland 1983).
    Some leaf disease fungi also infest stems, especially Trichothecium roseum, Phoma, Stemphylium, Colletotrichum, and Phomopsis species.   The most serious causes of stem cankers are Fusarium species—F. graminearum and F. avenaceum occur in cooler climates, F. sulphureum and F. sambucinum in warmer climates.
    Some root rots cause serious losses.  Barloy & Pelhate (1962) considered root rot caused by Fusarium solani the worst disease of hemp in France.   Pandotra & Sastry (1967) report a virulent strain of Rhizoctonia solani destroying 80% of drug plants in northern India.  Root rot by Sclerotium rolfsii predominates in southern temperate zones and the tropics, on both fiber and drug cultivars (Ferri 1961).
    Above-ground symptoms of root rots are hard to distinguish from wilt diseases.  Three wilt diseases are important—fusarium wilt caused by two forms of Fusarium oxysporum, verticillium wilt caused by two Verticillium species, and premature wilt (also called charcoal rot) caused by Macrophomina phaseolina.   Fusarium wilt received attention as a potential biocontrol to eliminate illegal marijuana plantations (Hildebrand & McCain 1978, Noviello et al. 1990).   Wilt diseases are more severe in Cannabis fields harboring root-wounding nematodes or broomrape.

Nematodes
   Nematodes are tiny roundworms, also called eelworms.  Nematodes are not closely related to earthworms.  Built on a much smaller and simpler scale, they have no respiratory nor circulatory systems.  Their nervous system is so simple it can be described at the level of individual cells.  Caenorhabditis elegans, for instance, has exactly 302 neurons.
    Crop damage by nematodes is underrated due to their small size and the unseen (mostly underground) nature of their pathology.  Above-ground symptoms consist of stunting, reduced yield and insipient wilting (drooping of leaves during midday with recovery at night).  Farmers may misinterpret symptoms as mineral deficiencies or drought, mysteriously arising despite adequate nutrients and moisture.  These symptoms do not occur uniformly across a field, but in pockets of scattered infestation.   Below-ground symptoms are more distinctive, including root knots or galls.   Six nematodes are known to infest Cannabis. All species attack roots except one.
    Root knot nematodes embed themselves in roots and induce plants to form giant cells or syncytia.  Syncytia swell into root galls and stimulate formation of adventitious rootlets, creating a bushy root.  Compound galls arise on larger roots forming "root knots": hypertrophied roots with a rough surface.  The southern root knot nematode, Meloidogyne incognita, has been reported on fiber cultivars in Europe, the former USSR, Brazil, and the southern US (Goody et al. 1965). M. incognita is the most widely distributed Meloidogyne spp. worldwide, and attacks hundreds of hosts.  Two other species are rarely reported, the northern root knot nematode Meliodogyne hapla (Norton 1966; de Meijer 1995) and the Java root knot nematode Meloidogyne javanica (Decker 1972).
    The stem nematode, Ditylenchus dipsaci, uniquely lives above the ground and does not infest roots.  Initial symptoms arise in stems, branches and leaf petioles, which swell and become chlorotic.  Stems subsequently become twisted and distorted with shortened internodes.  Plants are stunted. D. dipsaci is found in North America, southern Africa, Australia, and temperate areas of Asia.  But Cannabis disease has only been described from fiber varieties in Europe (Mezzetti 1951).   Other nematodes are rarely reported: cyst nematodes (Heterodera schachtii, H. humuli), needle nematodes (Paralongidorus maximus), and root lesion nematodes (Pratylenchus penetrans).

Parasitic Plants
   Plants from two genera are genuine Cannabis para-sites.  They sink specialized roots (haustoria) into the host’s xylem and phloem to withdraw fluids and nu-trients.  Broomrapes seem to be the worst.   Dewey (1914) calls branched broomrape (Orobanche ramosa) "the only really serious enemy to hemp."  Barloy & Pelhate (1962) consider a combi-nation of O. ramosa and Fusarium solani the greatest threat to Cannabis cultivation in southern France.  Broomrapes do most of their damage underground, their haustoria provide portholes for root rot fungi.  Only briefly do broomrapes send shoots above ground, which quickly flower and set seed.  Rarely Orobanche aegyptiaca and Orobanche cernua have been cited on fiber and drug cultivars.
    Dodder, in contrast to broomrape, sinks haustoria into above-ground parts.  Five species have been reported, mostly Cuscuta campestris (on drug cultivars in the US and fiber varieties in Europe) and Cuscuta europea (on fiber cultivars in Europe).  Dodder arises as conspicuous tangles of glabrous yellow filaments, bearing vernacular names such as "gold thread," "hair weed," "devil’s ringlet," and "love vine."  They twine themselves around stems and branches.  Robust specimens girdle branches and pull down hosts.  Dodder, like broomrape, can vector viruses.

Viruses
   Viruses rarely kill Cannabis. They only exist and replicate in living plants.  Viruses can, however, seriously reduce yields.  Once acquired, they are nearly impossible to eradicate.  Viruses invade all parts of plants.  Pollen and seed infections transmit viruses to subsequent generations.
    Five viral syndromes are described in the literature.  In addition to these naturally-occurring infections, Hartowicz et al. (1971) screened 22 common plant viruses for their ability to infect wild hemp.  Over half the viruses could infect Cannabis.
   The hemp streak virus (HSV) is frequently cited on fiber cultivars in Europe.  Foliar symptoms begin as a pale green chlorosis.   Chlorotic areas soon develop into a series of interveinal yellow streaks or chevron-stripes.  Some-times brown necrotic flecks appear, each fleck surrounded by a pale green halo.  Flecks appear along the margins and tips of older leaves and often coalesce.  Streak symptoms predominate in moist weather, flecks appear during dry weather.  Leaf margins become wrinkled and leaf tips roll upward, leaflets curl into spirals.  Whole plants assume a "wavy wilt" appearance.
    The hemp mozaic virus has been described on fiber cultivars in Europe and drug cultivars in Pakistan.  Symptoms were described as a gray leaf mosaics.   Three other viruses have been cited on European hemp—the alfalfa mozaic virus (=lucerne mozaic virus), cucumber mozaic virus, and the arabis mozaic virus.  Many insects transmit these viruses as they feed from plant to plant.  According to Ceapoiu (1958), the worst vectors of Cannabis viruses are bhang aphids (Phorodon cannabis), greenhouse whiteflies (Trialeudodes vaporariorum), onion thrips (Thrips tabaci) and green peach aphids (Myzus persicae).

Bacteria and MLOs
   The Cannabis literature concerning bacteria is confused.  Dozens of bacteria have been cited, a morass of misidentifications and taxonomic synonyms.  Species of hemp rettors and marijuana rotters have leaked into the literature, but they do not cause disease in live plants.   Mutualistic species also appear.  Kosslak & Bohlool (1983) isolated Azospirillum brasilense and A. lipoferum from the rhizosphere of marijuana plants growing in Hawaii.  These diazotrophic bacteria live on the surface of plant roots where they fix nitrogen for their host.  Diazotrophic bacteria have been sprayed on plants to serve as "biofertilizers" (Fokkema & Heuvel 1986).
    Only four species of true pathogenic bacteria (with one species split into four pathovarieties) cause disease in living Cannabis plants.  Bacterial blight by Pseudomonas syringae pv. cannabina seems to be the most common problem.  Symptoms resemble those caused by brown leaf spot, a fungal disease.   Bacterial blight has only been described on fiber cultivars in Europe. Striatura ulcerosa produces similar symptoms on stems and is caused by a similar species, Pseudomonas syringae pv. mori.  It, too, is limited to fiber varieties in Europe.  Uncommon diseases include crown gall by Agrobacterium tumefaciens, bacterial wilt by Erwinia tracheiphila, xanthomonas leaf spot by Xanthomonas campestris pv. cannabis, and a mycoplasma-like object described by Phatak et al. (1975).

Abiotic diseases
   Diseases from abiotic (non-living) causes often arise suddenly.  They usually resemble diseases caused by living organisms.   Some abiotic diseases have unknown causes, such as "grandine" of hemp.   Abiotic problems also predispose plants to other diseases.  Drought-stressed plants, for instance, become much more susceptible to fungal cankers (McPartland & Schoeneweiss 1984).
    The most common abiotic diseases are nutrient deficiencies (Frank 1988).  Generally, deficiencies of mobile nutrients (N, P, K, Mg, B, Mb) begin in large leaves at the bottom of plants.  Shortages of less mobile nutrients (Mn, Zn, Ca, S, Fe, Cu) usually begin in young leaves near the top.
    Pollutants take their toll.  Sulfur dioxide causes interveinal leaf chlorosis and hydrogen fluoride causes a complete chlorosis in Cannabis (Goidýnich 1959).  Sharma & Mann (1984) found C. sativa ssp. indica near a Himalayan highway suffering chlorosis and necrosis.  Automobile-polluted plants produced fewer stomates but more trichomes per leaf area.  Because of increased trichome density, Sharma & Mann thought auto pollution increased THC production.
    Genetic diseases are common.  BÛcsa (1958) describes some consequences of inbred hemp e.g. short stature (only 68% the height of normal hemp), shortened lifespan (vegetative growth 9 weeks shorter than normal plants), production of sterile seeds, and increased susceptibility to fungal diseases.   Crescini (1956) describes plant fasciation, ramification of stems, and strange pinnate phyllotaxy in mutagenic, inbred hemp.  Borodina & Migal (1987) illustrate flower fasciation and other teratologies in monoecious plants.  Lai (1985) describes the deleterious effects of inbreeding on yield of fiber and seed.  Sitnik (1981) says "yellow stem" disease in the Ukraine is genetic, caused by a monogenic recessive mutation.  The gene involved has a pleiotropic effect on plant yields, it decreases biomass, fiber and seed production.

 

References

• Agrios, G. 1988. Plant Pathology, 3rd Ed.  Academic Press, N.Y. 803 pp.
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• Bilgrami, K., S. Jamaluddin and M. A. Rizwi 1981. Fungi of India: Part II, Host index and addenda.  Today & Tomarrow’s Printers and Publishers, New Delhi. 128 pp.
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• McPartland, J. M. 1995e. Cannabis pathogens XII: lumper’s row. Mycotaxon 54:273-279.
• McPartland, J. M. and M. A. Cubeta 1996.  New species, combinations, host associations and location records of fungi associated with hemp (Cannabis sativa L.).   manuscript submitted to Mycological Research.
• McPartland, J. M. and S. Hughes 1994. Cannabis pathogens VII: a new species, Schiffnerula cannabis. Mycologia 86: 867-869.
• McPartland, J. M. and D. F. Schoeneweiss 1984.  Hyphal morphology of Botryosphaeria dothidea in vessels of unstressed and drought-stressed Betula alba. Phytopathology 74: 358-362.
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• Sharma, G. K. and S. K. Mann 1984.  Variation in vegetative growth and trichomes in Cannabis sativa L. (marihuana) in response to environmental pollution. J. Tennessee Academy of Science 59: 38-40.
• Sitnik, V. P. 1981.  Inheritance of charcters controlled by the pleiotropic effect of the gene for yellow stem in hemp. Selektsiya i Semenovodstvo No. 47: 46-49.
• Synnott, K. [Ed.] 1941.  Plant diseases.  Notes contributed by the biological branch. Agricultural Gazette of New South Wales 52(7): 369-371, 384; 52(8): 435-438.
• Termorshuizen, A. J. 1991.  Literatuuronderzoek over ziekten bij nieuwe potenti‘le gewassen. IPO-DLO Rapport No. 91-08, Instituut voor Planteziektenkundig Onderzoek, Wageningen, The Netherlands. 18 pp.
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-excerpted from Biocontrol of Cannabis diseases and pests due in 1997.

Cannabis stem cross section (courtesy of VIR)

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