Hemicycliophora arenaria Raski, 1958

California Pest Rating for

Citrus sheath nematode

Pest Rating: B

PEST RATING PROFILE

Initiating Event:

None. The current status and rating of Hemicycliophora arenaria is assessed.

History & Status:

Background: The citrus sheath nematode, Hemicycliophora arenaria, was first reported in 1957 as an unknown species parasitizing rough lemon seedlings in a grower’s nursery in the Coachella Valley, near Mecca, southern California (Van Gundy, 1957). The effect on seedling roots was noteworthy due to symptoms of ‘peculiar galling’ produced in infected plants, quite unlike those caused by the root-knot nematode. Soon after, in 1964, the same species was found in a citrus ranch approximately 2 miles from the original site in Riverside County and on citrus land in Imperial County. All properties were planted with citrus trees from a commercial nursery located near Niland in Imperial County, approximately 40 miles from the original site in Riverside County. This nursery had been planted on virgin desert soil and failed due to lack of moisture, and consequently, was abandoned in 1956. Surveys were conducted by the CDFA at that time to establish origin and extent of spread of the nematode species. In 1965, H. arenaria was found in a number of soil samples collected from cheese bush, a California native plant, growing in a virgin desert region about one mile north of the original abandoned nursery. At about the same time, the nematode species was also found on cheese bush in another native situation near Palm Springs, about 30 miles northwest from the infestation in Mecca. Additionally, another California native plant, coyote melon, was experimentally shown to be a host of the nematode species (McElroy & Van Gundy, 1967). In 1971, H. arenaria was found in soil and root samples collected from roadside cheese bush plants near the entrance of a desert state park in San Diego County. These detections indicated that H. arenaria is indigenous to native plants in low and high elevation deserts of California and had been spread with citrus nursery stock from the abandoned nursery planting near Niland. The species was assigned an ‘A’ rating because of its limited distribution and demonstrated potential for injury to citrus and vegetables (discussed below), and the infested sites were placed under a county “hold-order” quarantine. This action restricted the movement of all soil, bare-rooted plants and equipment with soil. Also, at the time of its discovery the citrus sheath nematode in California was of great concern to other state trading partners thereby making quarantine action necessary. In 2006, in statewide, USDA APHIS CAPS-sponsored surveys, CDFA once again detected H. arenaria in lemon and grapefruit soils in Imperial County (Chitambar, 2008).

Hemicycliophora arenaria was named and described by Raski (1958). Since its original discovery, the citrus sheath nematode had only been reported from California until more than 25 years later, when it was also reported from Australia and southern Argentina (Chitambar & Subbotin, 2014; Reay, 1984; Brugni & Chaves, 1994).

Hemicycliophora arenaria is a plant parasitic nematode species whose females feed ectoparasitically on host plant roots and lay their eggs singly in the soil. Each egg has a gelatinous coating that makes it adhere to soil and roots. The optimum range for reproduction is 30-32.5°C with 32.5°C being the optimum. Within this temperature, the nematode completes a life cycle of 15-18 days. Males do not feed and are not required for reproduction, which can be parthenogenetic. Almost no reproduction occurs at 20°C and at 35°C reproduction is greatly reduced. Furthermore, reproduction is greatest in sandy soils. Reproduction was determined to be greatest on tomato grown in 90% sand, 5% silt, and 5% clay, and at the original detection site in the Coachella Valley, the soil comprised 75% sand, 9% silt and 16% clay (Van Gundy & Rackham, 1961; Maggenti, 1981). The nematode also requires adequate aeration and maybe killed by reduced aeration caused by prolonged irrigation cycles. This preference of high temperature and sandy soils explains the very limited distribution of the citrus sheath nematode within desert regions of California, where it was discovered to be endemic on native desert plants namely, cheese bush and coyote melon (McElroy et al. 1966; McElroy & Van Gundy, 1967). Subsequently, the citrus sheath nematode gained economic importance as a parasite of agricultural crops with the reclamation of southern California deserts (Maggenti, 1981).

Hosts: Citrus is the main host. Citrus limonia (Rough lemon), C. aurantifolia (West Indian lime), C. limon (Dorshapo sweet lemon), C. reticulata (Cleopatra mandarin), C. taiwanica (Taiwanica), Severinia buxifolia, Solanum lycopersicum (Rutgers tomato), Vigna sinensis (blackeye bean), Capsicum frutescens var. grossum (pepper), Apium graveolens (celery), Cucurbita moschata (squash) (Van Gundy, 1959; Van Gundy & Rackham, 1961; Van Gundy & McElroy, 1969), Hymenoclea salsola (syn. Ambrosia salsola; cheesebush), Cucurbita palmata (coyote melon), and Vitis vinifera (Tokay grape) (McElroy et al. 1966; McElroy & Van Gundy, 1967). Moura & Almeida (1982) found this species in sugar-cane field. Reay (1984) reports the following hosts from Australia: Auraucaria bidwillii, Acacia euthycarpa, A. gracilifolia, A. continua, A. myrtifolia, A. paradoxa, A. pycnantha, Banksia marginata, B. ornata, Callitris preisii, Eucalyptus anceps, E. baxteri, E. fasciculosa, E. foecunda, E. goniocalyx, E. incrassata, E. maculata, E. obliqua, E. odorata, E. oleosa, E. socialis, E. vitrea, Macrozamia spiralis, cycad, Melaleuca acuminata, M. lanceolata, and M. uncinata, Pteridium esculentum, bracken, Xanthorrhoea quadrangulata, and Austrocedrus chilensis.

Symptoms: Plants infected by H. arenaria are easily recognized by swellings or galls produced on lateral and terminal roots. Unlike galls formed along the length of roots parasitized by root-knot nematodes, galls caused by H. arenaria are produced at the tips of lateral and terminal roots. The nematodes remain tightly attached to freshly dug roots and are visible through a hand lens (McElroy & Van Gundy, 1967).

Damage Potential: Feeding of H. arenaria results in the production of galls at tips of lateral and terminal roots, as well as a reduction in the number of feeder roots and top growth. The growth of rough lemon seedlings in H. arenaria infested soil at 30°C for 5 months was reduced by 36% in comparison to seedlings in non-infested soil. Dry weight of tomato plants was reduced by 28%, and a 10-20% yield reduction in field-grown tomato and squash occurred at the original locality in Mecca, California. Growth of citrus and tomato was reduced from 12% at 25°C to 37% at 30°C (McElroy & Van Gundy, 1967, 1968; Van Gundy & Rackham, 1961). Significant damage may affect citrus production under climates suitable for the development of the nematode species.

Transmission: Infested rootstock, rooted plants, soil, irrigation and run-off water, cultivation tools and equipment that can move infested soil and plant roots to non-infested sites.

Worldwide Distribution: Oceania: Australia (South Australia, New South Wales, Queensland); North America: USA (California); South America: Argentina, Brazil (Brugni & Chaves, 1994; Reay, 1984; Van Gundy, 1957; McElroy & Van Gundy, 1967; Moura & Almeida, 1982).

Official Control: Hemicycliophora arenaria is on the ‘Harmful Organism Lists’ for Honduras, Republic of Korea, and Taiwan (USDA PCIT, 2016). Within the USA, Florida has listed H. arenaria as a plant pest of quarantine significance and potentially subject to quarantine action (FDACS, 2016).

California Distribution: Limited desert regions within Imperial, Riverside and San Diego Counties.

California Interceptions: Hemicycliophora arenaria has never been detected in intercepted plant and soil shipments to California.

The risk citrus sheath nematode 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). Hemicycliophora arenaria is naturally endemic to limited hot desert regions within Imperial, Riverside and San Diego Counties. Within those regions it has been found naturally infesting coyote melon and cheese bush which are indigenous desert plants commonly found in the sandy washes and stream beds in the Coachella and Imperial valleys and provide a reservoir of nematodes for infesting plantings in non-infested soils. High soil temperatures and coarse soils are needed for the nematode to develop and affect plant growth and production. Agricultural host plants grown under those climate conditions are likely to establish and further spread the nematode to non-infested regions particularly in reclaimed desert regions of southern California.

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

-Low (1) has a very limited host range

-Medium (2) has a moderate host range

– High (3) has a wide host range.

Risk is Medium (2). Hemicycliophora arenaria has a moderate host range which includes citrus as the main host, also tomato and other vegetable plants, and grape (Tokay variety). California native desert plants, cheese bush and coyote melon are hosts of the nematode species in California.

3) Pest Dispersal Potential: Evaluate the dispersal potential of the pest:

-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). Hemicycliophora arenaria has high reproduction and is dispersed primarily by movement of infested rootstock, plant roots, soil, irrigation and run-off water, cultivation tools and equipment that can move infested soil and plant roots to non-infested sites.

4) Economic Impact: Evaluate the economic impact of the pest to California using these criteria:

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 by other states or countries)

D. The pest could negatively change normal production 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 climates for infestations of the citrus sheath nematode, crop yield and value could be lowered. Reductions of 36% growth of rough lemon seedlings in H. arenaria infested soil at 30°C has been reported. Also, reported was 28% reduction in dry weight of tomato plants and 10-20% yield reduction in field-grown tomato and squash. Growth of citrus and tomato was reduced from 12% at 25°C to 37% at 30°C. The nematode may also spread along the flow of irrigation water in a field, thereby, requiring change in normal irrigation and cultural practices. The original detection of H. arenaria in California resulted in establishment of quarantines by other states and to date, the citrus sheath nematode is a quarantine regulated pest in Florida. Therefore, a ‘High’ rating is given here for the potential economic impact of H. arenaria.

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

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. Significantly impacting cultural practices, home/urban gardening or ornamental plantings.

Score the pest for Environmental Impact:

– 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). Under favorable conditions of warm to hot soil temperatures and coarse textured soils, the citrus sheath nematode could significantly impact home and commercial urban plantings and cultural practices.

Consequences of Introduction to California for Common Name: Score

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 to California = 12.

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 Low (-1): Hemicycliophora arenaria is established in limited hot desert regions within Imperial, Riverside and San Diego Counties.

Final 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 presented above, the proposed pest rating for the citrus sheath nematode, Hemicycliophora arenaria is B.

References:

Brugni, N., and E. Chaves. 1994. Criconemoides from a cypress forest of South Argentina. Nematologica 40: 467-473.

CABI. 2016. Hemicycliophora arenaria (sheath nematode). http://www.cabi.org/cpc/datasheet/46685 .

Chitambar, J. J. 2008. Status of ten quarantine “A” nematode pests in California. California Plant Pest and Disease Report 24: 62-75.

Chitambar, J. J. and S. A. Subbotin. 2014. Systematics of the sheath nematodes of the superfamily Hemicycliophoroidea. Nematology Monographs and Perspectives, Vol. 10 (Series Editors: D. J. Hunt and R. N. Perry). The Netherlands, Leiden, Brill, 2014. 732 p.

FDACS. 2016. Florida summary of plant protection regulations updated June 2016. Florida Department of Agriculture and Consumer Services Division of Plant Industry. http://nationalplantboard.org/wp-content/uploads/docs/summaries/florida.pdf .

Maggenti, A. 1981. General Nematology. Springer-Verlag New York, Inc. 372 p.

McElroy, F. D., and S. D. Van Gundy. 1967. The sheath nematode. The California Citrograph 52, 379-384.

McElroy, F. D., and S. D. Van Gundy. 1968. Observations on the feeding process of Hemicycliophora arenaria. Phytopathology 58: 1558-1565.

McElroy, F. D., S. A. Sher, and S. D. Van Gundy. 1966. The sheath nematode, Hemicycliophora arenaria, a native to California soils. Plant Disease Reporter 40: 581-583.

Moura, R. M., and A. V. Almeida. 1982. Preliminary studies on the occurrence of phytonematodes associated with sugarcane in areas of low productivity in Pernambuco State. Nematologia Brasileira 5: 213-220.

Raski, D. J. 1958. Four new species of Hemicycliophora de Man, 1921, with further observations on H. brevis Thorne, 1955 (Nematoda: Criconematidae). Proceedings of the Helminthological Society of Washington 25: 125-131.

Reay, F. 1984. Plant nematodes from Australia: new records of Hemicycliophoroidea (Nematoda: Tylenchida). Australasian Plant Pathology 13: 8-11.

USDA PCIT. 2016. USDA Phytosanitary Certificate Issuance & Tracking System. September 27, 2016. https://pcit.aphis.usda.gov/PExD/faces/ReportHarmOrgs.jsp.

Van Gundy, S. D. 1957. The first report of a species of Hemicycliophora attacking citrus roots. Plant Disease Reporter 41: 1016-1018.

Van Gundy, S. D. 1959. The life history of Hemicycliophora arenaria Raski (Nematoda: Criconematidae). Proceedings of the Helminthological Society of Washington 26: 67-72.

Van Gundy, S. D. and R. L. Rackham. 1961. Studies on the biology and pathogenicity of Hemicycliophora arenaria. Phytopathology 51: 393-397.

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.

Comment Period: CLOSED

Oct 25 – Dec 9, 2016

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