Colletotrichum cliviae Y.L. Yang, Zuo Y. Liu, K.D. Hyde & L. Cai, 2009

California Pest Rating for

Colletotrichum cliviae Y.L. Yang, Zuo Y. Liu, K.D. Hyde & L. Cai, 2009

PEST RATING: B

PEST RATING PROFILE

Initiating Event:

On October 17, 2017, diseased leaves of variegated croton plants (Codiaeum variegata) exhibiting leaf spotting symptoms, were collected from a nursery in San Diego, by San Diego County officials and sent to the CDFA Plant Pathology Laboratory for diagnoses. The shipment of croton plants had originated from Florida. On November 20, 2017, Suzanne Latham, CDFA plant pathologist, identified the pathogen, Collectotrichum cliviae, as the cause for the disease. Furthermore, during 2015-2016, CDFA detections of anthracnose disease of Cymbidium sp., Aglaonema sp., and Dieffenbachia sp. plants in nurseries in San Diego County in California, were attributed to Colletotrichum cf. cliviae (‘cf’ in biological terminology means ‘a significant resemblance to’). Those detections initiated, and were included in, a pest rating assessment for the closely similar species, C. cliviae, which was eventually given a permanent B-rating. However, those detections were recently shown to be, instead, C. aracearum (Kennedy, 2017; Latham, 2017). The recent detection of C. cliviae in San Diego marked the first record of this pathogen in California. Consequently, the infected plants were treated by the nursery and are to be periodically re-inspected (Walber, 2017). The risk of the introduction and establishment of C. cliviae, and its current rating in California are re-evaluated here.

History & Status:

Background: Colletotrichum cliviae causes anthracnose and leaf blight disease in its host plants. The fungal pathogen was originally reported from Clivia miniata (clivia/flame/bush/kaffir lily) leaves growing in Yunnan Province, China and reported as not being host-specific (Yang et al., 2009). Since then, C. cliviae has been found on few tropical and subtropical hosts from China, India, Brazil, and recently, from the USA (California).

Hosts: Arundina graminifolia (Bamboo orchid), Camellia sinensis (tea plant), Clivia miniata (Kaffir lily), Capsicum annuum (pepper), Capsicum sp., Cymbidium hookerianum (orchid), C. pendulum, Glycine max (soybean), Mangifera indica (mango) Phaseolus sp. (bean), Ricinus communis (castor), Saccharum sp., Zamioculcas zamiifolia (Barbieri et al., 2017; Chowpadda et al., 2014; Diao et al., 2017; Farr & Rossman, 2016; Lui et al., 2015; Saini et al., 2017; Sharma et al., 2014; Vieira et al., 2014; Yang et al., 2009; Zhang & Li, 2017). The recent host, Codiaeum variegata (variegated croton) is added to this list (see ‘Initiating Event’).

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. Colletotrichum cliviae produce dark brown to black, ellipsoid lesions in orchid leaves of Cymbidium hookerianum and Arundina graminifolia. The lesions contain pale yellow conidial (spore) masses (Yang et al., 2011).

Damage Potential: Anthracnose disease caused by Colletotrichum cliviae can result in reduced plant quality and growth, fruit production and marketability. Estimates of yield/crop loss due to this pathogen have not been reported. However, in California, nursery and greenhouse production of orchids, croton, and other host plants would be 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 cliviae 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; South America: Brazil (Farr & Rossman, 2016; Liu et al., 2015; Vieira et al., 2014; Yang et al., 2011).

Official Control: Colletotrichum cliviae is reportable to the USDA.

California Distribution: Colletotrichum cliviae is not established in California.

California Interceptions: Only one interception from Florida is recorded (see ‘Initiating Event).

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

Consequences of Introduction:

1) Climate/Host Interaction: Similar to other species of Colletotrichum, C. cliviae 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.

Evaluate if the pest would have suitable hosts and climate to establish in California.

Score: 2

– 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.

2) Known Pest Host Range: Presently, the host range of Colletotrichum cliviae is limited to few plant species in eight different families – mainly economically important orchid, mango, and nursery ornamentals.

Evaluate the host range of the pest.

Score: 1

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

– Medium (2) has a moderate host range.

– High (3) has a wide host range.

3) Pest Dispersal Potential: 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.

Evaluate the natural and artificial dispersal potential of the pest.

Score: 3

– 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.

4) Economic Impact: Under suitable, wet climates, the pathogen could lower plant growth, fruit production and value and trigger the loss of markets. Nursery orchids and ornamentals, and mango production could be negatively affected.

Evaluate the economic impact of the pest to California using the criteria below.

Economic Impact: A, B, C

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.

Economic Impact Score: 3

– 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.

5) Environmental Impact: The pathogen could significantly impact cultural practices or home garden plantings.

Evaluate the environmental impact of the pest on California using the criteria below.

Environmental Impact: E

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

B. The pest could directly affect threatened or endangered species.

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

D. The pest could trigger additional official or private treatment programs.

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

Environmental Impact Score: 2

– 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.

**Consequences of Introduction to California for Colletotrichum cliviae: Medium (11)**

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 cliviae to California = (11).

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 Not established in California (-1).

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 = 11.

Uncertainty:

None.

Conclusion and Rating Justification:

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

References:

Diao, Y.-Z., C. Zhang, F. Liu, W. –Z, Wang, L. Liu, L. Cai,, and X. –L. Liu. 2017. Colletotrichum species causing anthracnose disease of chili in China. Persoonia 38: 20-37.

Barbieri, M. C., G., M. Ciampi-Guillardi, S. R. G. Moraes, S. M. Bonaldo, F. Rogerio, R. R. Linhares, and N. S. Massola Jr. 2017. First report of Colletotrichum cliviae causing anthracnose on soybean in Brazil. Plant Disease 101: 1677.

Chowpadda, P., C. S. Chethana, R. P. Pant, and P. D. Bridge. 2014. Multilocus gene phylogeny reveals occurrence of Colletotrichum cymbidiicola and C. cliviae on orchids in north east India. Journal of Plant Pathology 96: 327-334.

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

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

Kennedy, A. 2017. Email from A. H. Kennedy, Molecular Biologist, National Identification Services, USDA APHIS PPQ PM to John Chitambar, CDFA, sent: August 29, 2017, 12:54 pm.

Latham, S. 2017. Email from A. H. Kennedy, Molecular Biologist, National Identification Services, USDA APHIS PPQ PM to Suzanne Latham, CDFA, sent: August 18, 2017, 12:11 pm.

Liu, F., B. S. Weir, U. Damm, P. W. Crous, Y. Wang, B. Liu, M. Wang, M. Zhang, and L. Cai. 2015. Unravelling Colletotrichum species associated with Camellia: employing ApMat and GS loci to resolve species in the C. gloeosporioides complex. Persoonia 35: 63-86. http://dx.doi.org/10.3767/003158515X687597.

Saini, T. J., S. G. Gupta, and R. Anandalakshmi. 2017. Detection of chili anthracnose caused by Colletotrichum cliviae in India. Australasian Plant Disease Notes 12: 33.

Sharma G., A. K. Pinnaka, and B. D. Shenoy. 2013. ITS-based diversity of Colletotrichum from India. Current Research in Environmental & Applied Mycology 3: 194–220.

Vieira, W.A.S., S. J. Michereff, M. A. de Morais, Jr., K. D. Hyde, and M. P. S. Camara. 2014. Endophytic species of Colletotrichum associated with mango in northeastern Brazil. Fungal Diversity 67: 181-202.

Walber, T. 2017. Email from G. Hernandez, San Diego County Department of Agriculture/Weights & Measures to T. Walber, CDFA Interior Pest Exclusion. Dated: December 01, 2017, 11:28:29 am.

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.

Yang, Y., L. Cai, Z. Yu, Z. Liu, and K. D. Hyde. 2011. Colletotrichum species on Orchidaceae in southwest China. Cryptogamie, Mycologie, 2011, 32 (3): 229-253.

Yang, Y.L., Z. Y. Liu, L. Cai, K. D. Hyde, Z. N. Yu, and E. H. C. McKenzie. 2009. Colletotrichum anthracnose of Amaryllidaceae. Fungal Diversity 39: 123-146.

Zhou, Z., and Y. L. Li. 2017. First report of Colletotrichum cliviae causing anthracnose on Zamioculcas zamiifolia in Henan Province, China. Plant Disease 101(5): 838.

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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