Colletotrichum fructicola | Pest Rating Proposals and Final Ratings

California Pest Rating for

Colletotrichum fructicola Prihastuti, L. Cai & K. D. Hyde, 2009

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

On March 29, 2016, a shipment of Chinese evergreen (Aglaonema sp.) cuttings showing leaf spotting symptoms and destined to a nursery in San Luis Obispo County, was intercepted and sampled by San Luis Obispo County Agricultural officials. The shipment had originated in Costa Rica. Diseased plant samples were sent to the CDFA Plant Diagnostics Branch for diagnosis. Suzanne Latham, CDFA plant pathologist, identified the anthracnose and fruit rot pathogen, Colletotrichum fructicola, as the cause for the disease. This species was first detected within California on August 26, 2015, in mango fruit shipped from Puerto Rico and intercepted by the California Dog Team. The fruit shipment was destined to a private citizen in Sacramento County. The identity of the fungal pathogen was confirmed on August 18, 2015, by the USDA National Identification Services at Beltsville, Maryland. Several detections of C. fructicola followed the initial find: on August 14, 2015, in Cymbidium orchid leaves from a nursery in San Diego County; on August 19, 2015, on mango fruit from Florida and destined for Stanislaus County; on November 9, 2015, in Dracaena massangeana cuttings from Costa Rica and destined to a nursery in San Diego County; on March 15, 2016, in black sapote fruit from Florida and destined to a private citizen in Los Angeles County. In all these cases, subsequent to the detection of C. fructicola, all fruit and plant shipments/nursery stock were either destroyed or rejected from entering California. Currently, C. fructicola has a temporary ‘Q’ rating. The risk of introduction and establishment of this pathogen in California is assessed and a permanent rating is proposed herein.

History & Status:

Background: Colletotrichum fructicola was originally reported to be associated with coffee berries (Coffea arabica) in northern Thailand (Prihastuti et al., 2009) and as a leaf endophyte from Central America (as C. ignotum). Since then, C. fructicola has been found on several tropical and subtropical hosts from diverse geographical regions. In the USA, C. fructicola was reported in 2012 from Florida and North Carolina on strawberry crown and apple fruit respectively (Weir et al., 2012). During 2015-16, the pathogen was also detected in California associated with several quarantine nursery plant/fruit shipments and regulatory nursery samples.

The pathogen is a distinct fungus species belonging to the vastly morphological and physiological variable C. gloeosporioides complex and is generally identified from other species of the complex only by gene sequencing. However, C. ignotum and Glomerella cingulata var. minor are synonyms of C. fructicola (Prihastuti et al., 2009; Rojas et al., 2010; Weir et al, 2012).

Hosts: Aglaonema sp. (Chinese evergreen), Annona reticulata (custard apple), A. squamosa (sugar apples), Artocarpus heterophyllus (jackfruit), Coffea arabica (coffee), Coffea sp., Camellia japonica (Japanese camellia), Camellia sinensis (tea), Camellia sp., Capsicum frutescens (chili pepper), Carica papaya (papaya), Cestrum parqui (green cestrum), Citrullus vulgaris (watermelon), Citrus limon (lemon), C. reticulata (Mandarin orange), C. sinensis (sweet orange), Citrus x paradisi, Crinum asiaticum (spider lily), Cucumis sativus (cucumber), Cymbidium sp. (orchid), Dendrobium sp. (orchid), Dioscorea alata (purple yam), D. rotundata (white yam), Diospyros nigra (black sapote), Dracaena massangeana (corn plant/cornstalk Dracaena), Epidendrum sp. (orchid), Ficus carica (common fig), F. edulis (fig), F. pumila (creeping fig), Fortunella margarita (oval kumquat) Fragaria ananassa (strawberry), Limonium sinuatum (statice), Limonium sp., Lobularia maritima (sweet alyssum), Lupinus angustifolius (blue lupine), Lycopersicon esculentum (tomato), Lycium chinensis (boxthorn), Malus domestica (apple), M. sylvestris (crab apple), Mangifera indica (mango), Matthiola incana (stock), Medicago polymorpha (burclover), Musa acuminata (edible banana), Nerium oleander (oleander), Nicotiana tabacum (tobacco), Passiflora edulis (passion fruit), Persea americana (avocado), Phalaenopsis sp. (moth orchid), Phormium tenax (flax), Portulaca oleracea (little hogweed/common purslane), Psidium guajava (guava), Pyrus bretschneideri (Chinese white pear), P. pyrifolia (pear), Saccolabium sp. (orchid), Tetragastris panamensis, Theobroma cacao (cocoa), Vanda sp. (orchid) (Farr & Rossman, 2016; Li et al., 2014; Prihastuti et al., 2009; Wang et al., 2016, Weir et al., 2012; Zhang et al., 2015).

Symptoms: Generally, Colletotrichum-infected host plants exhibit symptoms of anthracnose which include dark brown leaf, stem and fruit spots, fruit rot, and wilting of leaves which often result in dieback and reduction in plant quality. In China, early stages of the disease in pear was characterized by the presence of black spots on young fruit which was always followed by severe bitter rot in matured fruit, and less than 1 mm black spots on leaves resulting in severe defoliation and loss of fruit (Jiang et al., 2014; Zhang et al., 2015). Anthracnose symptoms on tobacco leaves initiate as discrete, yellow-green spots which coalesce into larger lesions with white centers and dark brown margins (Wang et al., 2016).

Damage Potential: Anthracnose disease caused by Colletotrichum fructicola can result in reduced plant quality and growth, fruit production and marketability. In China, sudden outbreaks of the disease resulted in severe defoliation and a loss of pear fruit quality and yield resulting in fresh market losses ranging from 60-90% which, in 2008, were estimated at US$150 million. (Li, et al., 2013; Zhang, et al., 2015). In 2014, also in China, 90% of tobacco leaves on ~2% plants in a 3-ha commercial tobacco field were infected with C. fructicola (Wang, et al., 2016). In California, nursery production of potted host plants or in greenhouses are particularly at risk as nursery conditions are often conducive to infection by Colletotrichum species. In California’s cultivated fields, disease development may be sporadic as it is affected by levels of pathogen inoculum and environmental conditions.

Disease Cycle: It is likely that Colletotrichum fructicola has a similar life cycle to that of other Colletotrichum species and survives between crops during winter as mycelium on plant residue in soil, on infected plants, and on seeds. During active growth, the pathogen produces masses of hyphae (stromata) which bear conidiophores, on the plant surface. Conidia (spores) are produced at the tips of the conidiophores and disseminated by wind, rain, cultivation tools, equipment, and field workers. Conidia are transmitted to host plants. Humid, wet, rainy weather is necessary for infection to occur. These requirements in particular may limit the occurrence of the pathogen in California fields and subsequently, the pathogen may be more of a problem under controlled environments of greenhouses. Conidia germinate, penetrate host tissue by means of specialized hyphae (appresoria) and invade host tissue.

Transmission: Wind, wind-driven rain, cultivation tools, and human contact.

Worldwide Distribution: Asia: China, India, Israel, Japan, Korea, Thailand; Africa: Angola, Nigeria; Europe: United Kingdom; North America: Canada, Panama, USA (California, Florida, North Carolina); Australia (Farr & Rossman, 2016; Li et al., 2014; Prihastuti et al., 2009; Wang et al., 2016, Weir et al., 2012; Zhang et al., 2015).

Official Control: In California C. fructicola is an actionable, Q-rated pathogen, and infected plant material is subject to destruction or rejection.

California Distribution: Colletotrichum fructicola was detected in a nursery in San Diego County (see “Initiating Event”).

California Interceptions: During 2015-16, Colletotrichum fructicola has been intercepted several times mainly in shipments of mango and black sapote fruits, Dracaena and Chinese evergreen cuttings that originated in Costa Rica, Puerto Rico, and Florida (see ‘Initiating event’).

The risk Colletotrichum fructicola would pose to California is evaluated below.

Consequences of Introduction:

1) Climate/Host Interaction: Evaluate if the pest would have suitable hosts and climate to establish in California. Score:

– Low (1) Not likely to establish in California; or likely to establish in very limited areas.

– Medium (2) may be able to establish in a larger but limited part of California.

– High (3) likely to establish a widespread distribution in California.

Risk is Medium (2) – Similar to other species of Colletotrichum, C. fructicola requires humid, wet, rainy weather for conidia to infect host plants. This environmental requirement may limit the ability of the pathogen to fully establish and spread under dry field conditions in California.

2) Known Pest Host Range: Evaluate the host range of the pest. Score:

– Low (1) has a very limited host range.

– Medium (2) has a moderate host range.

– High (3) has a wide host range.

Risk is High (3) – The host range of Colletotrichum fructicola is relatively wide and diverse and includes several tropical and subtropical plants, as well as agricultural and ornamental crops grown in California.

3) Pest Dispersal Potential: Evaluate the natural and artificial dispersal potential of the pest. Score:

– Low (1) does not have high reproductive or dispersal potential.

– Medium (2) has either high reproductive or dispersal potential.

– High (3) has both high reproduction and dispersal potential.

Risk is High (3) – The pathogen has high reproductive potential and conidia are produced successively. They are transmitted by wind, wind-driven rain, cultivation tools, and human contact however conidial germination and plant infection require long, wet periods.

4) Economic Impact: Evaluate the economic impact of the pest to California using the criteria below. Score:

A. The pest could lower crop yield.

B. The pest could lower crop value (includes increasing crop production costs).

C. The pest could trigger the loss of markets (includes quarantines).

D. The pest could negatively change normal cultural practices.

E. The pest can vector, or is vectored, by another pestiferous organism.

F. The organism is injurious or poisonous to agriculturally important animals.

G. The organism can interfere with the delivery or supply of water for agricultural uses.

– Low (1) causes 0 or 1 of these impacts.

– Medium (2) causes 2 of these impacts.

– High (3) causes 3 or more of these impacts.

Risk is High (3) –Under suitable, wet climates, the pathogen could lower plant growth, fruit production and value and trigger the loss of markets.

5) Environmental Impact: Evaluate the environmental impact of the pest on California using the criteria below.

The pest could have a significant environmental impact such as lowering biodiversity, disrupting natural communities, or changing ecosystem processes.

The pest could directly affect threatened or endangered species.

The pest could impact threatened or endangered species by disrupting critical habitats.

The pest could trigger additional official or private treatment programs.

The pest significantly impacts cultural practices, home/urban gardening or ornamental plantings.

Score the pest for Environmental Impact. Score:

– Low (1) causes none of the above to occur.

– Medium (2) causes one of the above to occur.

– High (3) causes two or more of the above to occur.

Risk is Medium (2) – The pathogen could significantly impact cultural practices or home garden plantings.

Consequences of Introduction to California for Colletotrichum fructicola:

Add up the total score and include it here. (Score)

-Low = 5-8 points

-Medium = 9-12 points

–High = 13-15 points

Total points obtained on evaluation of consequences of introduction of Colletotrichum fructicola to California = (13).

6) Post Entry Distribution and Survey Information: Evaluate the known distribution in California. Only official records identified by a taxonomic expert and supported by voucher specimens deposited in natural history collections should be considered. Pest incursions that have been eradicated, are under eradication, or have been delimited with no further detections should not be included. (Score)

-Not established (0) Pest never detected in California, or known only from incursions.

–Low (-1) Pest has a localized distribution in California, or is established in one suitable climate/host area (region).

-Medium (-2) Pest is widespread in California but not fully established in the endangered area, or pest established in two contiguous suitable climate/host areas.

-High (-3) Pest has fully established in the endangered area, or pest is reported in more than two contiguous or non-contiguous suitable climate/host areas.

Evaluation is Low (-1) – Colletotrichum fructicola was detected in a nursery in San Diego County.

Final Score:

7) The final score is the consequences of introduction score minus the post entry distribution and survey information score: (Score)

Final Score: Score of Consequences of Introduction – Score of Post Entry Distribution and Survey Information = 12.

Uncertainty:

Periodic surveys need to be conducted to confirm the presence/absence of C. fructicola in commercial and private production regions within California. Subsequent results may alter the herein proposed rating for the pathogen.

Conclusion and Rating Justification:

Based on the evidence provided above the proposed rating for the anthracnose pathogen, Colletotrichum fructicola is B.

References:

CABI. 2016. Colletotrichum fructicola basic datasheet report. Crop Protection Compendium. www.cabi.org/cpc/

Farr, D. F., & A. Y. Rossman. Fungal databases, systematic mycology and microbiology laboratory, ARS, USDA. Retrieved April 3, 2016, from

http://nt.ars-grin.gov/fungaldatabases/

J. Jiang, Zhai, H. Li, Z. Wang, Y. Chen, N. Hong, G. Wang, G. N. Chofong, and W. Xu. 2014. Identification and characterization of Colletotrichum fructicola causing black spots on young fruits related to bitter rot of pear (Pyrus bretschneideri Rehd.) in China. Crop Protection 58:41-48.

Li, H.N., Jiang, J.J., Hong, N., Wang, G.-P., and Xu, W.X. 2013. First Report of Colletotrichum fructicola Causing Bitter Rot of Pear (Pyrus bretschneideri) in China. Plant Disease 97:1000. http://dx.doi.org/10.1094/PDIS-01-13-0084-PDN.

Prihastuti, H., L. Cai, H. Chen, E. H. C. McKenzie, and K. D. Hyde. 2009. Characterization of Colletotrichum species associated with coffee berries in northern Thailand. Fungal Diversity 39: 89-109.

Wang, H. C., Y. F. Huang, Q. Chen, M. S. Wang, H. Q. Xia, S. H. Shang, and C. Q. Zhang. 2016. Anthracnose caused by Colletotrichum fructicola on tobacco (Nicotiana tabacum) in China. Plant Disease (posted on line March 8, 2016). http://dx.doi.org/10.1094/PDIS-06-15-0724-PDN.

Weir, B. S., P. R. Johnston, and U. Damm. 2012. The Colletotrichum gloeosporioides species complex. Studies in Mycology, 73:115-180. DOI:10.3114/sim0011.

P. F. Zhang, L. F. Zhai, X. K. Zhang, X. Z. Huang, N. Hong, W. Xu, and G. Wang. Characterization of Colletotrichum fructicola, a new causal agent of leaf black spot disease of sandy pear (Pyrus pyrifolia). European Journal of Plant Pathology 143:651-662.

Responsible Party:

John J. Chitambar, Primary Plant Pathologist/Nematologist, California Department of Food and Agriculture, 3294 Meadowview Road, Sacramento, CA 95832. Phone: 916-262-1110, plant.health[@]cdfa.ca.gov.

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