Astronauts of the Nematode World:An Aerial View of Foliar Nematode Biology, Epidemiology, and Host Range
Lisa M. Kohl USDA-APHIS-PPQ, Center for Plant Health Science and Technology, Plant Epidemiology and Risk Analysis Laboratory, Raleigh, NC 27606
Kohl, L. M. 2011. Astronauts of the Nematode World: An Aerial View of Foliar Nematode Biology, Epidemiology, and Host Range. APSnet Features. doi:10.1094/APSnetFeature-2011-0111.
Foliar nematodes (Aphelenchoides fragariae, A. ritzemabosi, and A. besseyi) are pathogens of ornamental crops in greenhouse and nursery production, and may infect some field crops, as well. Foliar nematodes migrate over plant surfaces through films of water to enter the stomates of leaves, causing vein-delimited lesions on leaf tissue. This review covers research on the identification, biology, epidemiology, and management of foliar nematodes, and also provides a new compilation of plant hosts that includes over 700 different plant species.
Foliar nematodes (Aphelenchoides spp.) are increasingly widespread pathogens of ornamental plants grown in greenhouses, nurseries, and in the landscape. There are three species of economic importance on ornamentals: Aphelenchoides fragariae (Ritzema Bos, 1891) Christie, 1932; Aphelenchoides ritzemabosi (Schwartz, 1911) Steiner and Buhrer, 1932; and Aphelenchoides besseyi Christie, 1942. Aphelenchoides fragariae is found in a diverse range of plants, including ferns, bedding plants, and herbaceous perennials, and has been reported across the United States (5,44,74). Aphelenchoides ritzemabosi also attacks a large range of ornamental plant species, but is rarely found on ferns and is commonly reported from Europe (29,69), although neither species is limited to a specific continent. Aphelenchoides besseyi is the least common of the three species in ornamentals, and is an economically important pathogen of rice (7). Aphelenchoides besseyi is often found in warmer climates while A. ritzemabosi and A. fragariae are more commonly associated with temperate climates, even though the two latter species are found in both tropical and temperate localities (76). While all three species infect a wide variety of ornamental and field crop plants, this review focuses mainly on ornamental plants grown for aesthetic value and infection by A. fragariae and A. ritzemabosi, the two species that most commonly infect ornamental plants.
Foliar nematodes infect the leaves of plants by migrating up plant stems and entering the stomates of leaves (70). Because migration occurs in water, infection is favored by plant surfaces recently moistened by dew, rain, or overhead irrigation. Foliar nematodes feed primarily endoparasitically and occasionally ectoparasitically on plant tissue, depending on the environment and type of plant host (76). During endoparasitic feeding within leaves, foliar nematodes cause brown to black, or chlorotic, vein-delimited angular lesions that can become necrotic with age (7) (Fig. 1). The response of host plants is variable. When the leaves of some woody ornamental plants, such as Lantana camara, become heavily infected, foliar lesons develop, followed by defoliation (Fig. 2). In other plants, such as Heuchera sanguinea, the infected leaves eventually turn necrotic and die. Older infected leaf tissue of Hosta spp. and Helianthus spp. drops out leaving a shot-hole or tattered appearance. Because ornamentals are sold for their aesthetic value, infected plants are often unsaleable, making foliar nematode damage very costly for ornamental growers.
Fig. 1 (A). Vein-delimited angular lesions resulting from foliar nematode infection of Salvia sp.
Fig. 1 (B). Vein-delimited angular lesions resulting from foliar nematode infection of Buddleja sp.
Fig. 2. Defoliation of Lantana camara as a result of foliar nematode infection.
The genus Aphelenchoides Fischer, 1894, contains many ubiquitous fungal feeding nematode species, as well as species that are parasites of insects and plants (14). The nematodes in this genus may represent a more primitive type of nematode evolutionarily, because they often can feed on both fungi and plants, and plant parasitic nematodes of the genus have a very wide host range compared to other plant pathogenic nematodes (11).
Adult nematodes in the genus Aphelenchoides are vermiform and about 1 mm in length (55). Aphelenchoides species can be differentiated from most plant parasitic nematode taxa by the presence of a very large metacarpus, a finely annulated cuticle, an offset lip region (Fig. 3), a lateral field that contains two to four lines (Fig. 4), and a tapering, conical tail end that is either rounded or has a mucro (14) (Fig. 5).
Fig. 3. Scanning electron micrograph of an Aphelenchoides fragariae head showing the mouth opening surrounded by the slightly protruding labia (lips).
Fig. 4. Scanning electron micrograph showing A. fragariae annulations and lateral field containing a narrow band with two incisures, as indicated by arrows.
Fig. 5. Tail of A. fragariae male. Notice the prominent spicules. The tip of the tail is curved as a result of the fixation process.
Aphelenchoides fragariae was first described when E. A. Ormerod sent infected strawberry plants to Ritzema Bos in England in 1890 (19). The strawberry plants were stunted and deformed so that the crown and lateral branches resembled a cauliflower, which caused Bos to describe the plants as suffering from "cauliflower disease." Bos named the nematodes causing this disease Aphelenchoides fragariae in 1891 (19).
Aphelenchoides ritzemabosi had been detected in chrysanthemums suffering from "eelworm disease" as early as 1890, but the nematode was confused with other Aphelenchoides species possessing similar morphology, until Schwartz characterized it as A. ritzemabosi in 1911 (19). Even after A. ritzemabosi was identified as a separate species, A. ritzemabosi was still confused with A. fragariae due to morphological similarities between the two species (13). Aphelenchoides fragariae has two lateral lines and a tail ending in a blunt point, while A. ritzemabosi has a lateral field with four lines and a tail ending in two to four processes (14).
Aphelenchoides besseyi was described by Christie in 1942 (14). This species is often associated with rice plants; A. besseyi causes "white tip" disease of rice in Japan and the southern United States (15). While the most economically significant plant host for A. besseyi is rice, this nematode has also been recorded on many ornamental plant hosts (18). Aphelenchoides besseyi can be distinguished from other Aphelenchoides species by having a lateral field with four lines, a stellate mucro at the tail (14), and shorter postvulvar uterine sac than A. ritzemabosi (54).
Molecular tools can also be used to identify Aphelenchoides species. Ribosomal DNA is used to differentiate A. besseyi and A. fragariae from several other Aphelenchoides species, including A. nechaleos, A. paranechaleos, A. composticola, A. bicaudatus, and A. arachidis (24). Chizhov et al. (4) inferred the phylogenetic relationships of A. fragariae, A. ritzemabosi, and A. besseyi to several other Aphelenchoides species, and found that plant parasitic species of Aphelenchoides grouped together in two clades. A PCR diagnostic assay has been developed to detect A. fragariae in infected plant tissue (22), and this PCR assay proved more accurate than a traditional water extraction method (44).
There are over 700 associated host species of foliar nematodes from at least 85 different plant families (5,18,29,35,74). The term "associated host" is used here because Koch’s postulates were not always performed. An updated compilation of reported associated hosts of Aphelenchoides fragariae, A. ritzemabosi, and A. besseyi is summarized in Table 1. This compilation consolidates associated host lists from around the world, including records from North America, South America, Europe, Asia, and Oceania. The earliest of these lists was published in 1936 (5), and Table 1 includes 135 hosts from this list. Table 1 also includes Goodey (18), who listed 308 plant hosts for Aphelenchoides in The Nematode Parasites of Plants Catalogued under their Hosts, 76 plant hosts from Juhl (29) in Denmark, and 83 host plants from Knight (35,36) in New Zealand. Plant names in lists have been updated to reflect updated taxonomy. Thus, Table 1 will be of value to diagnostic clinics, researchers, government agencies, and growers who need to know what plants are susceptible to foliar nematode infestation.
The updated host plant list reveals an expansive foliar nematode host range. A large number of associated plant hosts are members of the plant families Asteraceae, Ranunculaceae, Scrophulariaceae, Primulaceae, Lamiaceae, and Liliaceae, and foliar nematodes also infect members of such diverse plant families as Agavaceae, Pinaceae, Poaceae, Orchidaceae, Cactaceae, and Crassulaceae. It is also interesting to note that while there are very few reports of A. ritzemabosi and A. besseyi infecting ferns, there are numerous reports of A. fragariae infecting ferns in the families Dryopteridaceae, Pteridaceae, and Aspleniaceae.
The expanded host list reveals host diversity, which is one reason why foliar nematode control is very challenging. Foliar nematodes can quickly spread throughout greenhouses, infesting many different kinds of plants that are being grown close to one another. Management can be especially difficult when small numbers of rare, high-value plants such as exotic ferns or tropical plants are grown. In these cases growers are often reluctant to discard infected plants because of their value, and theses plants remain as a source of nematodes. Growers who buy and ship large quantities of plants also risk bringing asymptomatic plants into their operations and can end up contaminating multiple blocks of numerous and varied plants.
Water plays a crucial role in the movement and dispersal of foliar nematodes. Dew, rainfall, or overhead irrigation provide moisture for the water films in which foliar nematodes migrate (40) to reach leaves. Wallace (70) observed that A. ritzemabosi adults moved more rapidly in thick water films that immersed epidermal hairs, similar to what would be found on the underside of wet leaves.
Aphelenchoides spp. enter and exit leaf tissue through stomata on the leaf undersurface (64,70). Wallace (70) observed adults of A. ritzemabosi entering plant tissue through open stomata on the underside of chrysanthemum leaves. He observed a nematode feeling the stomate with its head and then inserting its head into the opening while moving the rest of its body back and forth until the worm had fully entered the stomate. Wallace (70) also demonstrated that nematodes emerge from stomata by differentially coating upper and lower leaf surfaces with petroleum jelly. Nematodes emerged in large numbers from leaves that had no petroleum jelly, and when petroleum jelly was applied only to the upper leaf surface. However, fewer nematodes emerged when the lower leaf surface was coated, because most stomata are located on the leaf underside (70).
Klinger (34) observed that foliar nematodes were attracted to the tactile stimulus of stomate-shaped slits. The nematodes were not attracted to oxygen, but they were attracted to carbon dioxide gas, which would normally emerge from stomata at night as a result of cellular respiration in the plant. At night there could also be a film of dew over the surface of plant leaves that would allow the nematodes to migrate to stomata.
After adult and fourth-stage juvenile nematodes enter through leaf stomata, feeding and reproduction occurs within the leaf tissue. The nematodes feed within the mesophyll and epidermis of the leaf (69), piercing neighboring cells with their stylets to feed (64). Eggs are laid within healthy, green sections of the leaf tissues (71). The endoparasitic feeding results in the collapse of the spongy parenchyma and palisade cells, which causes the leaf tissue to turn brown (69). Nematodes also feed ectoparasitically on stems, buds and flowers (56).
The life cycle is very similar in both A. ritzemabosi and A. fragariae. Males are required for reproduction, and once females are fertilized they are able to lay eggs even after emergence from months of dormancy in an anhydrobiotic state (16). Strümpel (64) observed populations of A. fragariae in Lorraine begonia at 18°C, and determined that each females laid approximately 32 eggs, and that eggs hatched in 4 days. The second stage juveniles reached reproductive maturity in six to seven days. Each A. ritzemabosi female lays an average of 25 to 35 eggs in a cluster (71). Stewart (61) observed that A. ritzemabosi could complete its life cycle in 14 days, with five days being required for embryonic development, and maturation occurring after another five days; Wallace (71) and French (16) reported similar generation times. These observations reveal that foliar nematode populations can rapidly increase within leaf tissue, with thousands of nematodes per gram of leaf tissue produced within two months.
Adult and fourth-stage juveniles are able to overwinter in an anhydrobiotic state within desiccated plant tissue and can survive for several months up to three years (7). The adult and fourth-stage juveniles have been shown to overwinter in dried leaves, dormant buds, but not in plant roots (17,27). Nematodes may be more likely to survive in a dormant state when bare soil is dry, but less likely to survive in moist soil, especially at moisture levels at 30% field capacity and greater (17,20,67). Jagdale and Grewal (27) found live nematodes in rhizosphere soil associated with overwintering hosta plants, but did not state if leaf fragments, which would have served as a reservoir for foliar nematodes, were present in their samples.
Foliar nematodes are often dispersed throughout greenhouses and nurseries by splashing water (40). Overheard irrigation allows foliar nematodes to be carried in water droplets to neighboring, uninfected plants. Foliar nematodes can also spread from the direct contact of an infected leaf with uninfected plant tissue. There have been reports of foliar nematodes traveling along weed leaves to infect new plants, being carried in seeds, and within infected leaves that have dehisced and fallen onto uninfected plant tissue (40).
Szczygiel (66) studied populations of A. fragariae in field-grown strawberry plants in Poland and determined that the population density of the nematodes in plant parts increased from November to December, and then decreased in January and remained low through the spring. He theorized that the population was responding to changes in the atmospheric temperature and humidity. When Szczygiel and Hasior (68) repeated similar experiments in 1967 and 1968, they observed that populations of A. ritzemabosi and A. fragariae increased during the early spring and late fall when the air temperature was low and relative humidity was high (68). Yamada and Takakura (77) examined populations of A. fragariae in lilies in Japan, and determined that the nematode populations increased in leaves during the rainy season.
Epidemiology studies of foliar nematodes are limited, and more research needs to be conducted on the spatial and temporal distribution of foliar nematodes in order to better understand their population dynamics, and to develop more effective management tactics.
Foliar nematode management is very challenging. Because foliar nematodes are disseminated by splashing water, a common recommendation is to avoid overhead irrigation. This is often difficult to accomplish when costly overhead irrigation systems are already in place for large sections of greenhouse space, and in outdoor nurseries where rain can spread foliar nematodes, even in the absence of overhead irrigation.
Some chrysanthemum cultivars have foliar nematode resistance (21). These cultivars have leaves that rapidly become necrotic, which quickly surrounds the nematodes with dead cells, thereby reducing feeding on green tissue and egg laying (72). However, no breeding work has been done to produce foliar nematode resistant chrysanthemum plants using this information. Even if there were breeding programs to produce plants resistant to foliar nematodes, it would not be feasible to introduce resistance into all of the hundreds of plant species that are susceptible to foliar nematodes.
In the past, chemical treatments such as oxamyl and parathion were used for effective management of foliar nematodes (28). However, due to environmental concerns and toxicity, these chemicals are no longer available, and modern chemical control methods have variable results. Chemical treatments may kill nematodes in water suspensions, but then fail to kill nematodes within infected leaves (25). The miticide chlorfenapyr is currently labeled for foliar nematode control on greenhouse ornamentals. Chlorfenapyr is reported to be effective for reducing foliar nematode populations in thin-leaved plants such as anemone (51) but is less effective in crops with thicker leaves such as lantana (73). Several insecticides have also been tested for control of foliar nematodes on ornamentals with similar variable results (38). These results reveal that current chemical treatments have varied success for controlling foliar nematodes because the chemicals are unable to fully penetrate leaf tissue in many plant species. Therefore, it is likely that the most effective chemical controls will be those that are truly systemic within the plant.
An alternative method for killing nematodes within leaf tissue is by soaking infected plants in hot water. Staniland (60) concluded that A. ritzemabosi could be killed in chrysanthemum stock plants soaked in water at 46°C for five minutes. Jagdade and Grewal (26) found that submerging infected hostas in 90°C water in the spring or autumn could greatly reduce A. fragariae populations. Because hot water treatment is labor intensive, and there can be negative effects on plant growth, this method is only used as a last resort in commercial settings, or for treating high value plants.
While we understand much of the basic biology of Aphelenchoides, there is still a great deal of research that needs to be done to better understand Aphelenchoides epidemiology, and to develop improved methods for their suppression in greenhouse and nursery settings. We need a better understanding of intra- and inter-plant nematode distribution, dispersal of foliar nematodes in ornamental plant production systems, and a better understanding of the infection process in order to develop improved integrated management strategies. Breeding programs can improve nematode resistance in a small number of ornamental plant species, but may be impractical on a large scale because the host range for Aphelenchoides is so diverse. Therefore, research efforts should focus on developing methods to prevent inoculum spread from infected plants, improving and utilizing chemical controls, as well as development of biological controls, sanitation techniques, and other strategies to limit the negative impact of Aphelenchoides.
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Table 1. Reported plant hosts of Aphelenchoides fragariae, A. ritzemabosi, and A. besseyi. Helpful hint: Use your browser’s "Find" function and search by family or genus to quickly find a host of interest.