Crotalaria As a Cover Crop for Nematode Management: a Review†

CROTALARIA AS A COVER CROP FOR NEMATODE MANAGEMENT: A REVIEW†

Koon-Hui Wang, B. S. Sipes, and D. P. Schmitt Department of Plant and Environmental Protection Sciences, 3190 Maile Way, University of Hawaii, Honolulu, HI 96822-2279, U.S.A. Current address of senior author: Department of Entomology and Nematology, University of Florida, P.O. Box. 110620, Gainesville, FL 32611-0620, U.S.A. koon- [email protected].

ABSTRACT

Wang, K.-H., B. S. Sipes, and D. P. Schmitt. 2002. Crotalaria as a cover crop for nematode management: A review. Nematropica 32:35-57. Much of the research on Crotalaria has focused on nematode suppression in agricultural production systems. Crotalaria is a poor host to many plant-parasitic nematodes including Meloidogyne spp., Rotylenchulus reniformis, Radopholus similis, Belonolaimus longicaudatus, and Heterodera glycines. It is also a poor or non-host to a large group of other pests and pathogens, is competitive with weeds without becoming a weed, grows vigorously to provide good ground coverage for soil erosion control, fixes nitrogen, and is a green manure. However, most Crotalaria species are susceptible to Pratylenchus spp., Helicotylenchus sp., Scutellonema sp., and Criconemella spp. The objectives of this review are to summa- rize the knowledge of the efficacy of Crotalaria spp. for plant-parasitic nematode management, de- scribe the mechanisms of nematode suppression, and outline prospects for using this crop effectively. Crotalaria species are used as preplant cover crops, intercrops, or soil amendments. Variation in nematode suppression by different Crotalaria cropping systems is discussed. The major impediment to using Crotalaria is its short-term effect in agricultural production systems. Integrating other pest management strategies with Crotalaria could offer promising nematode management approaches. Key words: Allelopathy, Crotalaria juncea, nematode antagonistic fungi, plant-parasitic nematodes, sunn hemp.

RESUMEN

Wang, K.-H., B. S. Sipes, and D. P. Schmitt. 2002. Uso de Crotalaria como cultivo de cobertura para el manejo de nematodo: Una revision. Nematrópica 32:35-57. Gran parte de la investigación en Crotalaria ha sido enfocada sobre la supresión de nematodos en sistemas de producción agrícola. Crotalaria es una hospedera inadecuada para muchos nematodos parásitos de plantas entre los cuales se incluyen Meloidogyne spp., Rotylenchulus reniformis, Radopholus similis, Belonolaimus longicaudatus, y Heterodera glycines. Un gran número de otros tipos de plagas y pató- genos no logran hospedarse en ella, compite con malezas sin llegar a ser una maleza, crece vigorosa- mente proporcionando una buena cobertura del suelo que lo protege contra la erosión, fija nitrógeno, y es un abono verde. Sin embargo, muchas especies de Crotalaria son susceptibles a Pra- tylenchus spp., Helicotylenchus sp., Scutellonema sp., y Criconemella spp. Esta revisión tiene como objetivos resumir el conocimiento actual sobre la eficiencia de Crotalaria spp. para el manejo de nematodos fitoparásitos, describir los mechanismos de la supresión de nematodos, y esquematizar perspectivas para el uso de este cultivo eficientemente. Las especies de Crotalaria son usadas como cultivos de cobertura presiembra, cultivo intercalado o emiendas de suelo. Se discute la variación en la supresión de nematodos por diferentes sistemas de cultivos de Crotalaria. El mayor obstáculo para el uso de Cro-

†This paper is a contribution from the College of Tropical Agriculture and Human Resources, University of Hawaii, Honolulu, Journal Series No. 4584.

36 NEMATROPICA Vol. 32, No. 1, 2002

talaria es su efecto a corto plazo en los sitemas de producción agrícola. La integración de otras estra- tegias de manejo de plagas con Crotalaria podría ofrecer soluciones promisorias para el manejo de nematodo. Palabras claves: Alelopatía, Crotalaria juncea, hongos antagonista de nematodos, nematodos fitoparási- tos.

INTRODUCTION mation of the horn-forming membranes of the hoof. Crotalaria dura Wood & Evans Crotalaria possesses many characteris- causes pulmonary and liver diseases in tics of a cover crop, being a poor or non- horses and cirrhosis of the liver in cattle; C. host for a large group of pests and patho- retusa causes cirrhosis of the liver in humans gens, competitive with weeds without and cattle in Jaimaica; C. maypurensis HBK becoming a weed, growing vigorously to is suspected of losses in cattle in Guyana provide good ground coverage, perform- (Purseglove, 1974); and C. spectabilis Roth. ing symbiosis with rhizobium to fix nitro- is toxic to livestock and can become a nox- gen, and being a green manure. This ious weed (Good et al., 1965). review will focus on growing Crotalaria for Fortunately, numerous species are not nematode management, and will provide toxic to livestock (Rotar and Joy, 1983), an overview of the advantages and poten- including C. juncea, commonly known as tial problems of this plant as a cover crop, sunn hemp. It probably originated in India, a description of the mechanisms of nema- is the fastest growing of the Crotalaria spe- tode suppression, and prospects for using cies, and is very effective at competitively this crop effectively to suppress plant-para- displacing weeds (Purseglove, 1974). It is sitic nematodes. hardy, drought-resistant, and grows on almost all soil types. Although adapted to Crotalaria hot climates, the plant will endure slight frost. It is the most important fiber crop in Crotalaria belongs to Fabaceae L. (syn. India and is now widely grown as a green Leguminosae Juss.) and contains about manure in Indonesia, Zimbabwe, Malay- 550 species (Purseglove, 1974). Growth sia, Taiwan, Thailand, and China (Rotar habits vary from shrubs to herbs and the and Joy, 1983). Crotalaria juncea was used in genus is common in the tropics and sub- the manufacture of products such as tropics, with the greatest number of spe- twines, cords, fishing nets, sacks, and rope cies occurring in Africa. One of the soles for shoes and sandals (Purseglove, important fiber and green manure crops is 1974). In addition, since rhizobia that nod- Crotalaria juncea L. Several other economi- ulate C. juncea are present in most soils, cally important species are C. intermedia soil nitrogen improvement is expected Kotschy, C. mucronata Desv (syn. C. striata (National Research Council, 1979). As a DC.), and C. retusa L., which are grown as green manure crop, the plants can be green manures, forages, and ornamentals. tilled into the soil 2 months after planting Many species of Crotalaria contain alka- to increase the soil organic matter. There- loids toxic to animals. For example, C. fore, C. juncea is grown in rotation with burkeana Benth causes crotalism (styfsiekte) rice, maize, tobacco, cotton, sugar cane, in cattle in South Africa, an acute inflam- pineapples (Hawaii), coffee (Brazil) and in

Crotalaria for nematode management: Wang et al. 37

orchard crops (Purseglove, 1974). Its seeds 150 to 165 kg/ha of nitrogen and 7 t/ha have been fed to pigs in Zimbabwe and air-dry organic matter at 60 days of growth horses in the former Soviet Union without under favorable conditions (Rotar and Joy, harm to the animals (Purseglove, 1974). 1983). In southwestern Alabama, plants Crotalaria juncea ‘Tropic Sun’, devel- grown for 9 to 12 weeks will produce 5.9 t/ oped for use as a green manure, was ha dry-matter and 126 kg N/ha (Reeves released in 1982 by the National Resources et al., 1996). Leaving the residue on the soil of Conservation Seirra (NRCS), formerly surface over winter resulted in the release the Soil Conservation Service, and Univer- of 75 to 80 kg N/ha (Reeves et al., 1996). sity of Hawaii (Rotar and Joy, 1983). The The crop has a few pest and pathogen source of the germplasm is uncertain, but problems. Major diseases of C. juncea are it was probably collected by the Pineapple Fusarium wilt caused by Fusarium udum var. Research Institute in Hawaii since it was crotalariae and anthracnose caused by Col- conducting research on Crotalaria species. lectotrichum curvatum (Purseglove, 1974). In 1958, NRCS and University of Hawaii In Brazil, the only disease reported on the purchased seeds of Crotalaria from a crop is Ceratocystes ﬁmbriata (National farmer who was growing it as a cover crop Research Council, 1979). The three most on the island of Kauai. This germplasm serious insect pests for C. juncea are larvae was used to develop ‘Tropic Sun’. The of the sunn hemp moth, Utetheisa pulchella, Agricultural Research Service’s Poisonous the stem borer, Laspeyresia pseudonectis, and Plant Laboratory and the University of the pod borers (Purseglove, 1974). Crota- Hawaii determined that seeds of this culti- laria juncea was also a host to stink bug, var were not toxic to livestock, and that the Nezara viridula and African sorghum head plant was resistant to root-knot nematodes bug, Eurystylus oldi (Davis, 1964; Malden (Rotar and Joy, 1983). and Ratnadass, 1998). In the tropics, ‘Tropic Sun’ grows and produces seed year round at elevations of NEMATODE POPULATION 0 to 300 m, and in summer up to 600 m. It SUPPRESSION BY CROTALARIA is grown in Guam and Puerto Rico under conditions similar to Hawaii. In the conti- Suppression of plant-parasitic nema- nental United States, C. juncea is adapted todes by Crotalaria spp. has been known for to spring and summer planting in the decades. Godfrey (1928) noted that South and Southwest (Rotar and Joy, 1983) C. juncea had few root galls from infection and can be grown as a winter cover crop in with Meloidogyne spp. Most of the plant-par- Alabama (Reeves et al., 1996). It is suitable asitic nematodes suppressed by Crotalaria as a green manure crop as far north as are sedentary endoparasitic nematodes. Maryland, but may not seed well north of These include Meloidogyne spp. (Good et al., 30° latitude. 1965; McSorley et al., 1994a; Taylor, 1985), ‘Tropic Sun’ is a rapidly growing crop Heterodera glycines (Rodríguez-Kábana et al., that is good for use as a green manure and 1992b) and Rotylenchulus reniformis (Robin- for adding organic matter and nitrogen to son et al., 1998; Araya and Caswell-Chen, the soil. It suppresses weeds, slows soil ero- 1994a). Some migratory nematodes such sion, and reduces root-knot nematodes as Belonolaimus longicaudatus (Reddy et al., populations (Rotar and Joy, 1983). When 1986), Paratrichodorous minor, Xiphinema plowed under at early bloom stage, nitro- americanum (Good et al., 1965; Brodie et al., gen recovery is the highest. It can produce 1970), and Radopholus similis (Birchﬁeld 38 NEMATROPICA Vol. 32, No. 1, 2002

and Bristline, 1956) were also suppressed as effective as fallow, differences between by Crotalaria spp. (Table 1). Most of the those two treatments were not statistically plant-parasitic nematodes that are not sup- significant. pressed by Crotalaria are migratory nema- Crotalaria species demonstrated variable todes, including Helicotylenchus spp., Meso- resistance against different nematodes. For criconema xenoplax, P. minor, Pratylenchus example, C. juncea supported moderate spp., Radopholus similis, Scutellonema spp. infection by M. javanica, whereas C. inter- and X. americanum (Table 2). media exhibited greater resistance, and Among the species tested, C. spectabilis C. paulina Schrank and C. spectabilis showed and C. juncea are most frequently studied. high resistance (Daulton, 1955; Martin, These plants have been used as preplant 1956). Similarly, C. breviflora DC., C. lan- cover crops, intercrops, and soil amend- ceolata E. Meyer and C. mucronata are very ments. The suppressive effect of Crotalaria resistant, C. retusa, C. grantiana Harv., C. spec- on nematodes is variable for all the appli- tabilis and C. juncea are intermediate, and cation methods (Table 1). As suggested by C. striata and C. paulina are less resistant to McSorley (2002), this variation could be R. reniformis (Silva et al., 1989b). Different due to genetic variation within the nema- susceptibility of Crotalaria species to Praty- tode species, crop cultivars, cropping sea- lenchus and Helicotylenchus spp. was also son, field history, cover cropping system, observed. Population densities of P. coffeae concurrent field practices or edaphic fac- on tea were suppressed by Crotalaria (Vis- tors including various biological compo- ser and Vythilingam, 1959) but P. zea can nents associated with the Crotalaria rhizo- penetrate roots of C. breviflora, C. spectabilis, sphere or soil amendment. Accordingly, C. retusa, and C. juncea, and P. brachyurus variation in nematode suppression by dif- can penetrate roots of C. juncea and C. spec- ferent Crotalaria application methods will tabilis at a lower rate than those penetrat- be discussed. ing roots of Sorghum bicolor, a standard host Preplant cover crop: In general, when Cro- for Pratylenchus (Silva et al., 1989a). Bio- talaria was used as a preplant cover crop, it mass production of several species of Crota- suppressed population growth of most laria, including C. paulina, C. pycnostachya, plant-parasitic nematodes except Pratylen- and C. striata, was reduced by P. zeae (Desae- chus spp. and Helicotylenchus spp. (Desae- ger and Rao, 2001). However, C. mucronata ger and Rao, 2000; Johnson and Campbell, suppressed P. zeae and P. brachyurus (Endo, 1980). Several studies demonstrated that 1959) and C. usaromoensis decreased P. bra- Crotalaria suppressed Meloidogyne spp. bet- chyurus population densities and improve ter than nematicides, because it continued pineapple yield. In another case, P. bra- to suppress the nematode population chyurus survived in soil planted with C. jun- development after a host was planted cea, but did not multiply (Charchar and (Huang et al., 1981; Aguillera et al., 1984; Huang, 1981). Sharma and Scolari, 1984). Crotalaria jun- Most reports have indicated that C. spec- cea suppressed R. reniformis population tabilis suppressed Meloidogyne spp. How- densities better than weed cover when ever, a majority of the tests for Crotalaria planted immediately after pineapple, with were conducted in tropical or subtropical a nematode reproductive factor of 0.16 areas where Crotalaria is well adapted. A and 1.59 respectively (Wang, 2000). greenhouse experiment showed that C. Although Johnson and Campbell (1980) spectabilis was not resistant to M. hapla suggested that Crotalaria treatment was not (Good et al., 1965), a nematode more com- Crotalaria for nematode management: Wang et al. 39 , 1989b , 1989a , 1989a , 1989b et al. et al. et al. et al. Visser and Vythilingam, 1959 Visser and Vythilingam, 1960 Chitwood and Toung, Desaeger and Rao, 1999 Desaeger and Rao, 2000 Silva Shepherd and Barker, 1993 Shepherd and Barker, Desaeger and Rao, 1999 Shepherd and Barker, 1993 Shepherd and Barker, Shepherd and Barker, 1993 Shepherd and Barker, on on on M. javanica M. javanica M. javanica Reduced nematodes on tea more efficiently than fallow. Reduced nematode population densities. Román, 1964 Nematode invaded roots but no nematode reproduction. No nematodes were recovered from soil or roots. Decreased nematode populations before and after maize planting compared to weed fallow. No nematodes detected.No nematodes detected. Santos and Ruano, 1987 Silva Low numbers compared to those in sorghum. No nematodes recovered after 4 months. Desaeger and Rao, 1999 Non-host of these nematodes.Suppressed damage of Netcher and Sikora, 1990 tobacco. Non-host of these nematodes.Suppressed damage of Netcher and Sikora, 1990; tobacco. No nematodes recovered after 4 months. Desaeger and Rao, 1999 No nematodes were detected. Silva Poor host. Silva No nematodes recovered after 4 months. Desaeger and Rao, 1999 Suppressed damage of Resistant. Santos and Ruano, 1987 tobacco. Resistant. Santos and Ruano, 1987 mixed with

Pratylenchus , M. javanica M. javanica M. javanica zea P. M. javanica M. javanica M. javanica M. javanica M. javanica M. javanica , , race 3, , , , , race 3, , race 3, M. javanica spp. Poor host in tobacco fields of Florida. 1942 Bratley, spp. on citrus (Asiatic spp. Low root gall index. 1928 Godfrey, zea brachyurus Meloidogyne Meloidogyne javanica coffeae R. reniformis Meloidogyne M. incognita M. incognita pyroid citrus nematode) M. incognita R. reniformis P. M. incognita M. incognita M. javanica M. incognita M. javanica M. incognita M. incognita R. reniformis M. incognita M. javanica P. Meloidogyne M. incognita spp. on plant-parasitic nematodes management. Crotalaria rap crop Host testing Host testing Host testing T Host testing in field soilPreplant cover crop for maize of Majority Field testHost testing Ectoparasitic nematodes Effectively reduced nematode numbers. Ochse and Brewton, 1954 Host testing Host testing Host testing Host testing Preplant cover crop for tobacco Host testing Preplant cover crop for tobacco Host testing Host testing Host testing Host testing Preplant cover crop for tobacco Host testing Host testing Host testing sp. able 1. Examples of positive effects Species Crotalaria Experimental conditions nematode Target Results References T C. agatiflora C. breviflora C. breviflora C. endecaphylla C. fulva C. grahamiana C. greenway C. grantiana C. grantiana C. incana C. intermedia C. juncea 40 NEMATROPICA Vol. 32, No. 1, 2002 , 1989b et al. , 1998 , 1991; Robinson et al. , 1989 , 1990a , 1990b , 1989c et al. et al. et al. et al. et al. , 1998; Silva ang, 2000 Sipes and Arakaki, 1997 Jasy and Koshy, 1994 Jasy and Koshy, Robinson Caswell et al. Charles, 1995 Shepherd and Barker, 1993 Shepherd and Barker, W Silva McSorley, 1999 McSorley, Silva Silva Araya and Caswell-Chen, 1994a Silva to M. javanica reproduction but no extracted by mist cham- infected plants. at least as well fallow. M. javanica M. javanica Reduced nematode numbers on taro and increased taro corm weight better than continuous taro planting. Suppressed damage by Lethal at dilution of 1:5 24 hours after incubating the nematodes in extract. Suppressed population densities on cotton. Reduced the nematode population densities better than carbofuran treatment and increased banana yield. tobacco. Reduced nematode population density compared to fallow. Low numbers compared to those in sorghum. Poor host, limited penetration, reduced R. reniformis Only occasional egg masses observed on M. incognita Highly efficient in suppressing the nematode. Smaller giant cells; fewer cells per female; giant cells showed granular, dense cytoplasm, with small number of nuclei; large vacuoles frequently absent. Some ber were significantly lower than that from the tomato. Penetrate the roots but cannot develop into adult 45 days after inoculation. Survived but failed to multiply. Charchar and Huang, 1981 galls observed and no juveniles found in soil; , , M. java- , R. similis , zea P. , M. incognita , spp. on plant-parasitic nematodes management. brachyurus brachyurus Crotalaria M. javanica M. javanica Radopholus similis M. incognita R. reniformis R. reniformis Helicotylenchus multicinctus Hoplolaimus indicus Rotylenchulus reniformis M. arenaria M. exigua M. javanica M. javanica M. javanica P. P. nica Preplant cover crop for taro Preplant cover crop for tobacco Leaf extract Preplant cover crop for cotton Preplant cover crop for pineapple Intercropping with banana Host testing Host testing Host testing Host testing Host testing Host testing Host testing Host testing able 1. (Continued) Examples of positive effects T Species Experimental conditions nematode Target Results References C. juncea Crotalaria for nematode management: Wang et al. 41 , 1974 , 1989a, b , 1989a, b et al. et al. et al. Endo, 1959 Murphy 1975 Brodie and Murphy, Moura, 1991 Moura, 1995 Desaeger and Rao, 1999 Gonzaga and Ferraz, 1994 Peacock, 1957 rotation in brachyurus P. C. juncea planting reduced these root recovered after 4 recovered after 4 months. Desaeger and Rao, 1999 below detectable levels in 1 -1 -1 was cultivated. Soil amend- No nematode detected. Silva No nematodes recovered after 4 months. Desaeger and Rao, 1999 No nematode detected.Reduced populations of Reduced the population densities of M. incognita to 3 years. Depends on the initial population density. Combination of 6-week fallow and Silva C. mucronata nematode population densities to almost undetectable levels on tomato and improved tomato yield. 1 juvenile g a former sugarcane field reduced the nematode population densities. todes on sugar cane. A two-year corn and 1 juvenile g months. Did not allow nematodes to reproduce. Gonzaga and Ferraz, 1994 Resistant.Poor host. Santos and Ruano, 1987 Endo, 1959 No nematodes recovered after 4 months. Desaeger and Rao, 1999 No egg masses were found on bean plants grown in the same pots after C. paulina ment did not suppress the nematode but enhanced bean growth. Life cycle not completed. Gonzaga and Ferraz, 1994; No nematodes recovered after 4 months. Desaeger and Rao, 1999 spp. Reduced the resurgence of these nema- Para- , R. reniformis R. reniformis M. javanica brachyurus , , Pratylechus P. zea zea , brachyurus P. P. M. javanica P. M. javanica M. javanica M. javanica M. javanica M. javanica M. javanica , , , race 3, , , , , , , , spp., spp. on plant-parasitic nematodes management. brachyurus brachyurus brachyurus Crotalaria M. incognita M. incognita M. incognita P. M. incognita christiei trichodorous M. incognita M. incognita Meloidogyne M. incognita P. M. incognita M. incognita Pratylenchus zeae P. M. incognita M. incognita M. incognita Host testing Host testing Preplant cover crop Preplant cover crop Preplant cover crop Host testingHost testing Ectoparasitic nematodes Effectively reduced nematode numbers Ochse and Brewton, 1954 Crop rotation Crop rotation Host testing Host testing Host testing Host testing Host testing Host testing Host testing and amendment effect Host testing Host testing able 1. (Continued) Examples of positive effects C. mucronata C. ochroleuca C. juncea C. laburnifolia C. lanceolata C. pallida C. paulina T Species Experimental conditions nematode Target Results References 42 NEMATROPICA Vol. 32, No. 1, 2002 , , et al. et al. , 1992a et al. , 1994 , 1965; Taylor, 1985 , 1965; Taylor, , 1965; Reddy , 1965; Taylor , 1965; Taylor , 1989a , 1989b , 1989c , 1989a , 1989b , 1989c et al. et al. et al. et al. et al. et al. et al. et al. et al. et al. 1986; Taylor, 1985 1986; Taylor, Anwar Carneiro and Carneiro, 1982; Good Sharma and Scolari, 1984 Good Sasser, 1954 Sasser, Silva Sasser, 1954 Sasser, 1985 Silva . . Meloidogyne Meloidogyne were lower than those after fal- No root gall symptoms.Fewer nematodes invaded, development was delayed, and fecundity low. Rodríguez-Kábana Resistant.No galls or egg masses were observed. 1999 McSorley, High degree of resistance and low root galling. Santos and Ruano, 1987 No nematode detected.Poor host.Reproductive factors of these nematodes on bean and corn planted after C. paulina low treatment. Silva Silva No egg masses were observed.High degree of resistance and low root galling. McSorley and Dickson, 1995 No nematodes recovered after 4 months. Desaeger and Rao, 1999 Penetrated the roots but did not develop to adult 45 days after inoculation. No nematode detected.Poor host.High resistance and low root galling. Good Silva Silva Penetrate the roots but cannot develop into adult 45 days after inoculation. , M. java- , M. java- and M. javanica M. javanica zea C. ornata P. M. javanica , , M. incognita race 3 and race 1 and 3, , spp. Resistant to five species of spp. Resistant to five species of , race 1, spp. on plant-parasitic nematodes management. brachyurus brachyurus brachyurus Crotalaria M. arenaria M. incognita M. incognita nica M. arenaria M. incognita nica M. incognita M. arenaria R. reniformis Combination of P. M. incognita M. javanica H. dihystera Meloidogyne M. javanica P. R. reniformis Meloidogyne M. arenaria M. javanica P. Host testing Host testing Host testing Host testing Host testing Host testing Host testing Preplant cover crop followed by bean and corn Host testing Host testing Host testingHost testing Host testing Ectoparasitic nematodes Effectively reduced nematode number. Ochse and Brewton, 1954 Host testing Host testing Host testing Host testing Host testing Host testing able 1. (Continued) Examples of positive effects C. recta C. retusa T Species Experimental conditions nematode Target C. spectabilis Results References C. paulina Crotalaria for nematode management: Wang et al. 43 , , et al. et al. , 1994b , 1981 , 1981 , 1965; Brodie et al. , 1989a , 1989b , 1989c; Silva et al. et al. et al. et al. et al. et al. Huang Almeida and Campos, 1991a, b. McSorley Huang Silva Shepherd and Barker, 1993 Shepherd and Barker, 1970 Rhoades, 1964 Good Navarro, 1968 1990b Silva spp. on Meloidogyne was grown for 8 M. javanica detected in okra on carrot; numbers in the soil 6 C. spectabilis M. incognita M. incognita M. exigua Reduced months prior to okra. No galls were formed and greatly reduced months after planting. No nematodes detected in coffee roots 23 months after planting. Suppressed the nematode only in short season crop, squash, but still increased eggplant yield compared to peanut rotation. increased carrot yield compared to rotation with tomato. Suppressed damage of Low numbers compared to those in sorghum. Poor host.Almost no roots when Silva tobacco. compared to fallowed plots. Reduced nematode population densities in subsequent tomato field, enhanced tomato growth. Reduced nematode population densities in soil. Few galls and no egg masses.No reproduction. Martin, 1958 Birchfield and Bristline, 1956 Penetrated the roots but did not develop to adult; smaller giant cells and fewer giant cells per female; showed dense cytoplasm, with few granular, nuclei; large vacuoles frequently absent. sp. , , Xiphinema , Pratylenchus R. reniformis zea sp., P. , spp. Reduced populations of spp. on plant-parasitic nematodes management. brachyurus Crotalaria M. incognita M. exigua M. arenaria M. javanica Helicotylenchus R. reniformis M. incognita Meloidogyne americanum Paratrichodorus minor Belonolaimus longicaudatus M. javanica Radopholus similis P. M. javanica Preplant cover crop for tomato Preplant to coffee Crop rotation with squash and eggplant in two cropping seasons Preplant cover crop for tobacco Host testing Crop rotation with okra Preplant cover crop for snap bean Preplant cover crop Combination of Preplant cover crop Host testing Host testing Host testing Host testing able 1. (Continued) Examples of positive effects T Species Experimental conditions nematode Target Results References C. spectabilis 44 NEMATROPICA Vol. 32, No. 1, 2002 , 1992a et al. , 1965 , 1995 , 1989a , 1989b et al. et al. et al. et al. alle Guérout, 1969 Mian and Rodríguez-Kábana, 1982 Rich and Rahi, 1995 V McBeth and Taylor, 1944 McBeth and Taylor,

C. spectabilis No nematode detected.No reproduction.Poor host.Non-host.Decreased nematode population densities and improved pineapple yield. Silva Birchﬁeld and Bristline, 1956 Silva Netcher and Sikora, 1990 No nematodes recovered after 4 months. Desaeger and Rao, 1999 Reduced root galling on squash, nematicidal efﬁcacy of amendments directly correlated with N content of the amendments. Mixture at 1% level suppressed nematode reproduction better than non- amended soil. Mixture at 2% level almost completely suppressed nematode egg mass production but phytotoxic to tomato. Life cycle not completed.Resistant.Nematode population levels reduced and fresh weight of soybean increased. Peacock, 1957 Santos and Ruano, 1987 was interplanted in peach orchards for 2 years. High degree of resistance. Good M. javan- zea P. M. javanica M. javanica , , , race 3 and spp. Nematodes controlled after spp. No galls developed. Rodríguez-Kábana spp. on plant-parasitic nematodes management. brachyurus brachyurus Crotalaria R. similis R. reniformis M. incognita P. M. incognita M. arenaria M. incognita P. M. incognita M. incognita ica H. glycines Meloidogyne Meloidogyne M. arenaria rap crop Host testing Host testing Host testing Crop rotation with pineapple Host testing Soil amendment Ground seed amendment Host testing Host testing Host testing Host testing Interplanted T Soil amendment able 1. (Continued) Examples of positive effects C. usaramoensis C. usaramoensis C. vallicola T Species Experimental conditions nematode Target Results References C. striata C. spectabilis Crotalaria for nematode management: Wang et al. 45 , 1974 , 2000 , 1993 et al. et al. et al. an der Linde, 1956 Luc Desaeger and Rao, 2000 V Martin, 1958 Inomoto, 1994 Wilson and Caveness, 1980 Murphy Martin, 1958

zeae Sor-

P. . sefaensis P. spp. but increased soil after 4 months. Desaeger and Rao, 1999 soil after 4 months. Desaeger and Rao, 1999 -1 -1 to damaging level on pine- . Meloidogyne brachyurus Control P. apple in Ivory Coast. As susceptible as maize. Desaeger and Rao, 2001 As susceptible as maize. Desaeger and Rao, 2001 Increased population densities of to a level that can limit growth of maize. These nematodes from South Africa were found penetrating and reproduc- ing in roots. Data were not quantiﬁed. Roots almost totally galled, but few egg masses found. As susceptible as maize.5000 nematodes L Desaeger and Rao, 2001 Galls visible.Nematode numbers recovered not different from that in a standard host, ghum bicolor Not effective against As susceptible as maize.Increased nematode population densities. Galls readily found.Roots almost totally galled but no egg Martin, 1958 masses found. As susceptible as maize. Desaeger and Rao, 2001 5000 nematodes L Martin, 1958 Desaeger and Rao, 2001 , sp. As susceptible as maize. Desaeger and Rao, 2001 sp. As susceptible as maize. Desaeger and Rao, 2001

acrita M. javan- , var thamesi, Scutellonema Scutellonema acrita acrita sp., sp.,

X. americanum , var. var. var. var. spp. Not effective for nematode control. Ijani subsp. M. incognita brachyurus brachyurus , P. P. , , spp. on plant-parasitic nematodes management. zeae, P. brachyurus zeae, P. brachyurus zeae, P. zeae zeae brachyurus brachyurus zeae and P. richodoridae richodoridae Pratylenchus brachyurus Helicotylenchus P. M. arenaria P. M. hapla Pratylenchus zeae Helicotylenchus M. javanica M. hapla M. incognita T P. ica Radopholus similis Pratylenchus sefaensis P. P. M. incognita M. hapla P. Meloidogyne T Crotalaria Host testing Host testing Host testing Host testing Preplant cover crop for maize Host testing Host testing Host testing Host testing Host testing Host testing Preplant cover crop Host testing Preplant cover crop Host testing Host testing Host testing Preplant cover crop in microplot Host testing sp. Intercrop able 2. Examples of negative or no effects SpeciesCrotalaria Experimental conditions nematode Target Results References C. agatiflora C. incana C. juncea C. paulina T C. grahamiana C. laburnifolia C. mucronata C. ochroleuca 46 NEMATROPICA Vol. 32, No. 1, 2002 , 1998 , 1981 , 1965 et al. et al. et al. Johnson and Campbell, 1980 Johnson and Campbell, 1980 Jaehn and Rebel, 1984 Huang Robinson Good Buente and Mueller, 1997 Buente and Mueller, . -tomato -tomato spp. suffi- H. dihystera , heavy root gall- Crotalaria Crotalaria for 8 months prior Meloidogyne M. hapla spp. C. spectabilis Supported large numbers of these nematodes after 4 years of cropping sequence. No effect.As susceptible as maize. Desaeger and Rao, 2001 1992 Whittington and Zehr, Did not reduce ciently to meet USA certification regulation after 4 years of rotation. Did not reduce nematode infection on coffee sufficiently and did not improve coffee yield. to okra, with no effect on Pratylenchus ing, sausage-shaped larvae found. Planted Did not reduce the nematode population densities sufficiently to protect following tomato crop. Good host.Not resistant to 1989 Jordaan and Waele, sp. As susceptible as maize. Desaeger and Rao, 2001

M. java- zeae and P. , Scutellonema Paratrichodorus spp. on plant-parasitic nematodes management. sp.,

brachyurus spp., spp. Supported high population densities of P. brachyurus Crotalaria P. and , zeae zeae Criconemella xenoplax Helicotylenchus minor P. M. javanica Criconemella nica Pratylenchus Meloidogyne incognita H. dihystera M. incognita P. M. hapla Intercrop with peach Host testing Host testing Intercrop with coffee Crop rotation with tomato Preplant cover crop Crop rotation with tomato Crop rotation with okra Preplant cover crop in microplot Host testing Host testing able 2. (Continued) Examples of negative or no effects T Species Experimental conditions nematode Target ResultsC. striata References C. spectabilis C. pancira C. retusa C. sphaerocarpa Crotalaria for nematode management: Wang et al. 47

monly found in temperate regions. How- cies next to the row of another. There has ever, in South Africa, C. spectabilis allowed been little research on nematode popula- M. hapla penetration but not reproduction tions when intercropping Crotalaria with (van der Linde, 1956). Even though C. specta- cash crops. Successful examples of using bilis suppressed most Meloidogyne spp., it Crotalaria as an intercrop against plant-para- did not reduce M. incognita and M. javan- sitic nematodes were reported for peach ica population densities sufficiently to meet and banana orchards (McBeth and Taylor, USA certification regulation after 4 years 1944; Charles, 1995). However, Crotalaria of Crotalaria-tomato rotation (Johnson and intercropped with peach had no effect on Campbell, 1980). However, C. spectabilis, as Mesocriconema spp. (Whittington and Zehr, a preplant cover crop in Florida, sup- 1992) and C. spectabilis intercropped with pressed R. similis successfully (Birchfield coffee did not suppress M. incognita (Jaehn and Bistline, 1956). Duration of planting and Rebel, 1984). This practice is con- and field history might affect Crotalaria strained by the competition in growth performance. For instance, 1 or 2 years of between the cash crops and cover crops. C. mucronata in land previously cropped to Desaeger and Rao (2001) proposed to native pasture or okra, respectively, were intercrop C. grahamiana with other legumi- required to achieve suppression of M. incog- nous cover crops such as Sesbania sesban and nita population densities below detectable Tephrosia vogelii as these latter legumes are levels (Murphy et al., 1974). Duration of good hosts to Meloidogyne but poor hosts to crop growth after soil incorporation of Pratylenchus and Helicotylenchus. They found C. spectabilis also influenced nematode con- that intercropping S. sesban and T. vogelii trol. Reduction of numbers of M. arenaria with Crotalaria did not reduce the numbers was adequate for squash but not eggplant of the vermiform stage of Meloidogyne but which is a longer-term crop planted after did reduce nematode egg mass production C. spectabilis (McSorley et al., 1994b). Nev- as compared to broadcast cropping of ertheless, C. spectabilis still increased egg- S. sesban and T. vogelii individually (Desae- plant fruit weight compared to that ger, 2001). However, intercropping with following peanut. The effect of C. juncea C. grahamiana resulted in higher P. zeae pop- on Radopholus similis varied and may be ulation densities than in cropping S. sesban related to the method of cover crop appli- and T. vogelii alone (Desaeger, 2001). cation (Inomoto, 1994; Jasy and Koshy, Wang (2000) intercropped C. juncea 1994). When C. juncea was applied as a pre- with pineapple and then alternated the plant cover crop without soil incorpora- C. juncea and pineapple planting bed in tion, it failed to suppress R. similis (Inomoto, the next cropping cycle. This cropping sys- 1994), but was effective when its leaf extract tem is similar to using Crotalaria as a pre- was tested against the nematode (Jasy and plant cover crop for pineapple except that Koshy, 1994). In another case, population Crotalaria was planted for a longer period densities of P. brachyurus increased consid- of time. When pineapple was planted into erably on M. mucronata after 3 years, but the previously C. juncea-intercropped plots, was not detectable if soil was fallow for 6 R. reniformis population densities, egg pro- weeks prior to C. mucronata planting (Bro- duction and mobility were lower than that die and Murphy, 1975). in the previously weedy fallow plots (Wang, Intercropping: Intercropping refers to 2000). After one C. juncea-pineapple inter- spatially mixed plantings of species in a cropping cycle (23 months), C. juncea field, usually by planting a row of one spe- enhanced bacterivorous nematode popula- 48 NEMATROPICA Vol. 32, No. 1, 2002

tion densities and nematode-trapping fun- logarithm (=2.1416). The criteria for host gal propagules compared to weedy fallow plant resistance are 1) failure of the nema- or pineapple beds (Wang, 2000), indicat- tode to live inside the host or early nema- ing that microbial activities against R. reni- tode death in the host, 2) decreased formis may have been enhanced. production of eggs, or 3) inhibition of Soil Amendment: Incorporating biomass nematode growth or development. can play an important role in nematode The mode of resistance in Crotalaria suppression. Most Crotalaria preplant cover against different nematodes varies among crops were followed by soil incorporation plant and nematode species. Meloidogyne of the biomass and subsequent reduction javanica is less attracted to C. spectabilis of plant-parasitic nematode numbers. roots as compare to tomato roots (Silva However, incorporation of C. paulina bio- et al., 1989c). The life cycle of M. incognita mass did not suppress M. incognita better was not completed in the roots of C. striata than allowing the biomass to remain on and C. retusa (Peacock, 1957). Development top of the ground as mulch (Gonzaga and of M. arenaria, M. incognita, and M. javanica Ferraz, 1994). Rich and Rahi (1995) found in the roots of C. spectabilis was arrested at that soil amended with C. spectabilis seeds the sausage-shaped late J2 stage (Good suppressed M. incognita and M. javanica et al., 1965). Although the Meloidogyne spp. better than non-amended soil. juveniles were able to penetrate the roots of C. spectabilis, C. juncea, C. retusa and MECHANISMS OF NEMATODE C. paulina, none of them become adults SUPPRESSION within 45 days after inoculation (Silva et al., 1989c). In other studies nematodes devel- Cover crops such as Crotalaria reduce oped but produced few eggs (Rich and plant-parasitic nematode populations by: Rahi, 1995; McSorley, 1999). Giant cells of 1) acting as a nonhost or a poor host C. spectabilis and C. juncea induced by (Rodríguez-Kábana et al., 1988, 1989, 1990, M. javanica were granular, had dense cyto- 1992b, 1994), 2) producing allelochemi- plasm, few nuclei, lacked large vacuoles, cals that are toxic or inhibitory (Haroon and were smaller and fewer compared to and G. C. Smart, 1983; Gommers and Bak- those in tomato roots (Silva et al., 1990b). ker, 1988; A Halbrendt, 1996), 3) provid- Penetration of M. javanica into roots of ing a niche for antagonistic flora and C. juncea was suppressed (Araya and fauna (Linford, 1937; Evans et al., 1988; Caswell-Chen, 1994b). Although C. juncea Caswell et al., 1990; Kloepper et al., 1991), supports M. javanica reproduction to some and 4) trapping the nematode (Gallaher extent, galls did not develop (Araya and et al., 1991; Gardner and Caswell-Chen, Caswell-Chen, 1994a). However, this effect 1994; LaMondia, 1996). can vary among nematode populations Poor or Non-host Effects: A non-host to a and species. One population of M. javanica nematode species is a plant in which the from South Africa penetrated and repro- nematode fails to reproduce (Trudgill, duced on C. juncea, whereas only 5 out of 9 1991). Seinhorst (1967) defined a poor populations of M. incognita var. acrita pene- host as having low a and M in the popula- trated and reproduced on C. juncea (van -a tion increase equation, Pf = M(1-e ), where der Linde, 1956). Crotalaria juncea Pf is the final population, M is the maxi- allowed R. reniformis infection but the nem- mum nematode population, a is the maxi- atode did not develop (Silva et al., 1990b) mum multiplication rate, e is the natural or reproduce (Caswell et al., 1991). How- Crotalaria for nematode management: Wang et al. 49

ever, when the observation time was pro- of the nitrogenous amendments contain longed, R. reniformis developed to female chitin. When added to the soil, enhanced and eggs were produced, but at a slower soil chitinase activities could result in dis- rate than on a good host, cowpea (Wang, tortion of the chitin layer of the nematode 2000a). eggshell (Rodríguez-Kábana, 1986). Mech- Allelopathic Effects: Allelopathy was origi- anisms involved in the action of low C/N nally designated for plant-plant and plant- ratio remain complex. microorganism biochemical interactions Enhancement of Nematode Antagonistists: (Rice, 1984). Secondary plant metabolites Nematode antagonist is a general term for are suspected as the allelopathic com- parasites, predators, pathogens, competi- pound against nematodes. Several plant tors, and other organisms that repel, inhibit, allelochemicals have effectively suppressed or kill plant-parasitic nematodes. Antago- phytopathogens, including nematodes, with nists, most likely favored by selected cover minimal environmental impact (Soler- crops, include fungal egg parasites, trapping Serratosa et al., 1996). fungi, endoparasitic fungi, fungal parasites Crotalaria spp. produce pyrrolizidine of females, endomycorrhizal fungi, plant- alkaloids and monocrotaline which have health promoting rhizobacteria, and obli- high vertebrate toxicity and could poten- gate bacterial parasites (Sikora, 1992). Other tially be toxic to nematodes (Rich and antagonists including mites, collembola, Rahi, 1995). Upon exposure of root-knot tardigrades, oligochaetes, predatory nema- nematode juveniles to monocrotaline solu- todes, turbellarians, and protozoans that tions, their bodies began to jerk (Fassuli- reduce nematode population densities are otis and Skucas, 1969). Infectivity of seldom discussed because data relevant to treated nematodes is therefore reduced. their management are insufficient (Sikora, Crotalaria juncea leaf extract was lethal to 1992). For practical plant-parasitic nema- R. similis at dilutions of 1:5 within 24 hours tode control to be successful in agricul- (Jasy and Koshy, 1994). Crotalaria juncea tural soils, the antagonists need the ability leaf leachate essentially stopped move- to proliferate under intensive farming ment of R. reniformis (Wang, 2000a). How- practices (Morgan-Jones and Rodríguez- ever, Fassuliotis and Skucas (1969) did not Kábana, 1987). find a relationship between the pyrrolizi- There are several hypotheses on how dine-containing plants and root-knot nem- cover crops can enhance nematode-antag- atode resistance. onistic activities. Linford (1937) specu- It is possible that the low C/N ratio of lated that incorporation of organic matter Crotalaria may also contribute to its allelo- provides an environment that favors popu- pathic effect against nematodes (Fassuli- lation growth and activities of nematopha- otis and Skucas, 1969; Rich and Rahi, gous fungi. A series of ecological events may 1995). The nematicidal efficacy of C. specta- be involved. The decomposing organic bilis used as a soil amendment was related material is a significant event because the to the nitrogen content of the amendment bacteria which proliferate after organic (Mian and Rodríguez-Kábana, 1982). matter incorporation become a food base Materials with very low C/N or high con- for microbiovorous nematodes. In turn, tent of ammonia will either result in plas- these nematodes serve as a food source for molysis of nematodes, or proliferation of nematophagous fungi (van den Boogert nematophagous fungi due to the release of et al., 1994b). For example, incorporation NH4+-N (Rodríguez-Kábana, 1986). Some of C. juncea enhanced Acrobeloides bodenhei- 50 NEMATROPICA Vol. 32, No. 1, 2002

meri, one of the most susceptible bacteri- dates from Crotalaria spp. were selective for vorous nematodes to parasitism by Hirsutella microbial species antagonistic to phyto- rhossiliensis (a nematode-endoparasitic fun- pathogenic fungi and nematodes (Rodrí- gus) (Venette et al., 1997). guez-Kábana and Klopper, 1998). Mycostasis, the inability of fungal Nematode-trapping fungi are a major spores to germinate in natural soils when group of nematode antagonists that can be temperature and moisture condition are enhanced by incorporation of residues of favorable for germination, may also be C. juncea (Wang, 2000). These fungi have involved in the enhancement of nematode been categorized into two groups: parasitic antagonistic fungi following the incorpora- and saprophytic (Cooke, 1963). The tion of organic matter (Stirling, 1991). saprophytic group consists of predators Nematode-trapping fungal activity is characterized by sticky three-dimensional enhanced when N is limiting (Barron, networks and non-spontaneous trap for- 1982). During the early stages of incorpo- mation. These fungi have a saprophytic ration of organic matter into the soil, the and a predatory (trap formation) phase. In C/N ratio increases. This high C concen- the presence of nematodes, or even exu- tration may aid spore germination (Ko and dates and homogenates of nematodes, Lockwood, 1967). trap formation is induced (Nordbring- Leguminous crops enhance nematoph- Hertz, 1973). The parasitic group consists agous fungi better than other crops. Root- of nematode-trapping fungi that form con- knot symptoms were reduced more by stricting rings, adhesive knobs, or adhesive alfalfa amendments in a 4-year microplot branches. These fungi form traps sponta- test than by chemical fertilization of plots neously, and thus are more effective trap- (Mankau, 1968). Meloidogyne incognita was pers. Among these two groups of nematode- suppressed in soil amended with alfalfa trapping fungi, the population densities of inoculated with Arthrobotrys conoides (Al- parasitic fungi are more likely to be Hazmi et al., 1982). Microplots amended enhanced by organic matter due to the with alfalfa meal increased nematode-trap- rich microbial flora and fauna (Gray, 1983). ping fungal activity of two efficient nema- The nematode trapping by these fungi are tode-trapping fungal species, A. dactyloides not nematode species- or trophic group- and Dactylellina ellipsospora (van den Boogert specific, therefore the enhancement of et al., 1994a). Pea enhanced the densities nematode-trapping fungi by organic mat- and species diversity of nematode-trapping ter incorporation should lead to increased fungi more than white mustard or barley trapping of plant-parasitic nematodes (Jans- (Persmark and Jansson, 1997). In addi- son and Nordbring-Hertz, 1980). tion, formation of conidial traps of nema- Soil amended with C. juncea to give a tode-trapping fungi was more prevalent in 1:100 (w:w) concentration, enhanced para- the pea rhizosphere than in root-free soil sitic nematode-trapping fungi, nematode (Persmark and Nordbring-Hertz, 1997). egg parasitic fungi, vermiform stage para- Being a legume, Crotalaria juncea has sites, and bacterivorous nematode popula- characteristics that may make the crop use- tion densities more efficiently than soil ful for nematode antagonism. For exam- amended with chopped pineapple tissues ple, C. juncea has soil enzymatic activity or non-amended soil (Wang, 2000). Crota- correlated with microbial activity and sup- laria juncea amendment enhanced the pressiveness to soil borne plant pathogens population densities of nematode-trapping (Quiroga-Madrigal et al., 1999). Plant exu- fungi and the percentage of eggs parasit- Crotalaria for nematode management: Wang et al. 51

ized by the fungi. Enhancement of nema- alkaloids and monocrotaline are released tode-trapping fungi was most effective in from Crotalaria tissues upon decomposi- soils that had not been treated with 1,3- tion (Rich and Rahi, 1995). Soil solariza- dichloropropene for at least 5 months tion could enhance the “biofumigation” (Wang, 2000). Suppression of R. reniformis process. Nematodes will be affected by the by C. juncea amendment was correlated sublethal heat in conjunction with the with parasitic nematode-trapping fungi, nematicidal effects from Crotalaria. fungal egg parasites, and bacterivorous Chemical nematicides should be nematodes (Wang, 2000). Nematode-trap- avoided in a cropping system if the objective ping fungi population densities were is to enhance nematode-antagonistic micro- higher in C. juncea planted plots than weed organisms in the cropping system. Several fallow plots (Wang, 2000). However, four studies have demonstrated the destructive months after removal of C. juncea, and effect of fumigation treatments to nematode replacement with pineapple plants, the antagonistic microorganisms. For example, population densities of nematode-trapping formaldehyde treatment increased the mul- fungi greatly decreased (Wang, 2000b). tiplication of Heterodera avenae as compared to non-fumigated nematode-suppressive PROSPECTS soil after the chemical degenerated in Roth- amstead (Kerry et al., 1995). Preplant treat- Nematode management is rarely suc- ment with metam sodium, methyl bromide, cessful in the long term with unitactic methyl iodide, or formaldehyde reduced approaches. It is important to integrate suppressiveness of soil against H. schachtii multiple-tactics into a strategy. Crotalaria (Westphal and Becker, 1999). Crotalaria jun- offers the potential to be one of the tactics. cea amendments failed to enhance nema- Some Crotalaria species are potential cover tode-trapping fungi populations in soils that crops for managing several important plant- were recently treated with 1,3-dichloropro- parasitic nematodes including Meloidogyne pane (Wang, 2000). spp. and R. reniformis. Unfortunately, the We hypothesize that intercropping Cro- residual effects are short term (a few talaria with a longer term cash crop will months). Crotalaria, a poor host, generally allow the nematode-antagonisitc microor- helps reduce nematode population densi- ganisms associated with Crotalaria to estab- ties, but the number of nematodes will lish after one cycle of the cash crop. resurge on subsequent host crops. The Previous research had demonstrated that damage threshold level, especially on C. juncea could enhance nematode-trap- longer-term crops, will often be reached or ping fungi activities in the rhizosphere exceeded (McSorley et al., 1994b). This sce- (Wang, 2000). However, development of nario strongly suggests that integrating the microbial populations to a density needed Crotalaria rotation system with other nema- to control nematodes has occurred only tode management strategies is necessary. under perennial crops or those grown in Among the possibilities for integration are monocultures (Kerry, 1987). Prolonged crop resistance, enhanced crop tolerance, culture of Crotalaria in an intercropping sys- selection for fast growing crop varieties, soil tem enhanced the nematode suppressive solarization, and biological control. effect in both peach (McBeth and Taylor, Solarization of soil amended with Crota- 1944) and pineapple systems (Wang, 2000). laria tissues may enhance nematode con- Another approach worth exploring is trol over either tactic alone. Pyrrolizidine the search for biocontrol agents compati- 52 NEMATROPICA Vol. 32, No. 1, 2002

ble with Crotalaria cropping systems. Intro- AL-HAZMI, A. S., D. P. SCHMITT, and J. N. SASSER. duction of biocontrol agents to manage 1982. Population dynamics of Meloidogyne incog- plant-parasitic nematode has met with lim- nita on corn grown in soil infested with Arthrobot- rys conoides. Journal of Nematology 14:44-50. ited success in the field (Stirling, 1991). ALMEIDA, V. F., and V. P. CAMPOS. 1991a. Reprodu- This might be due to microbiostasis prop- tividade de Meloidogyne exigua em plantas antago- erties of the soil (Ho and Ko, 1986) and nistas e em culturas de interesse econômico. the legume rhizosphere may overcome Nematologia Brasileira 15: 24-29. fungistasis against the nematode-trapping ALMEIDA, V. F., and V. P. CAMPOS. 1991b. Alternân- cia de culturas e sobrevivência de Meloidogyne ex- fungi better than that of root-free soil igua em áreas de cafezal infestado e erradicado. (Persmark and Nordbring-Hertz, 1997). Nematologia Brasileira 15:30-42. Although several attempts have failed to ANWAR, S. A., D. L. TRUDGILL, and M. S. PHIL- enhance some nematophagous fungi by LIPS. 1994. The contribution of variation in in- Crotalaria (Venette et al., 1997), in situ nema- vasion and development rates of Meloidogyne incognita to host status differences. Nematologi- tode-antagonistic microorganisms associ- ca 40:579-586. ated with the Crotalaria rhizosphere and ARAYA, M., and E. P. CASWELL-CHEN. 1994a. Host Crotalaria amended soils have not been status of Crotalaria juncea, Sesamum indicum, Doli- studied in depth. Such research might chos lablab, and Elymus glaucus to Meloidogyne jav- improve the prospect of prolonging the anica. Journal of Nematology 26:492-497. ARAYA, M., and E. P. CASWELL-CHEN. 1994b. Pene- nematode suppressive effect of Crotalaria tration of Crotalaria juncea, Dolichos lablab and Ses- cropping systems. amum indicum roots by Meloidogyne javanica. In summary, Crotalaria, besides being Journal of Nematology 26:238-240. an efficient green manure, is a poor host BARRON, G. L. 1982. Nematode-destroying fungi. to many important plant-parasitic nema- Pp. 533-551 in R. G. Burns and J. H. Slater, eds. Experimental Microbiologial Ecology. Blackwell todes, producing allelopathic compound Scientific Publications, Oxford, U.K. toxic to nematodes, and is able to enhance BIRCHFIELD, W., and F. BISTLINE. 1956. Cover crop some nematode-antagonisitc microorgan- in relation to the burrowing nematode, Radopho- isms. Therefore using Crotalaria as a cover lus similis. Plant Disease Reporter 40:398-399. crop may offer alternatives to nematicides. BRATLEY, H. E. 1942. Weed host plants of the nematode found in the three year tobacco rotation. Integrating the use of Crotalaria with other Proceeding of Soil Science Society of Florida pest management strategies offers promise 4:118-120. for the development of new sustainable BRODIE, B. B., J. M. GOOD, and C. A. JAWORSKI. agricultural cropping systems. 1970. Population dynamics of plant nematodes in cultivated soil: effect of summer cover crops in old agricultural land. Journal of Nematology ACKNOWLEDGMENT 2:147-148. BRODIE, B. B., and W. S. MURPHY. 1975. Population The authors thank Drs. Robert McSor- dynamics of plant nematodes as affected by com- ley and Johan Desaeger for providing new binations of fallow and cropping sequence. Jour- information and reviewing the paper, and nal of Nematology 7:91-92. BUENTE, R., and J. MUELLER. 1997. Influence of Drs. Maria Mendes and Roseangela Oliveira resistant oil radish genotypes on the population for literature translation. dynamics of Meloidogyne hapla and M. incognita. Zeitschrift fuer Pflanzenkrankheiten und Pflan- zenschutz 103:527-534. LITERATURE CITED CARNEIRO, R. G., and CARNEIRO, R. M. D. G. AGUILLERA, M. M., S. MATSUOKA, and O. T. IDO. 1982. Selecao preliminar de plantas para rota- 1984. Efeitos da adubação verde com Crotalaria cao de culturas em areas infestadas por M. incog- juncea sobre nematóides e a produção de cana- nita nos anos de 1979 e 1980. Reuniao de de-açucar. Nematologia Brasileira 8: 25-26. Nematologia 6:141-148. Crotalaria for nematode management: Wang et al. 53

CASWELL, E. P., J. DEFRANK, W. J. APT, and C.-S. FASSULIOTIS, G., and G. P. SKUCAS. 1969. The ef- TANG. 1991. Influence of nonhost plants on fect of pyrrolizidine alkaloid ester and plants population decline of Rotylenchulus reniformis. containing pyrrolizidine on Meloidogyne incognita Journal of Nematology 23:91-98. acrita. Journal of Nematology 1:287-288. CASWELL, E. P., J.-L. SARAH, and W. J. APT. 1990. GALLAHER, R. N., R. McSORLEY, and D. W. DICK- Nematode parasites of pineapple. Pp. 519-537 in SON. 1991. Nematode densities associated with M. Luc, R. A. Sikora, and J. Bridge, eds. Plant-Par- corn and sorghum cropping systems in Florida. asitic Nematodes in Subtropical and Tropical Ag- Supplement to Journal of Nematology 23:668- riculture. CAB International, Wallingford, UK. 672. CHARCHAR, J. M., and C. S. HUANG. 1981. Host GARDNER, J., and E. P. CASWELL-CHEN. 1994. range of Pratylenchus brachyurus: 3. Different spe- Raphanus sativus, Sinapis alba, Fagopyrum esculen- cies. Fitopathologia Brasileira 6:469-474. tum as hosts to Meloidogyne incognita, Meloidogyne CHARLES, J. S. K. 1995. Effect of intercropping an- javanica, and Plasmodiophora brassicae. Supple- tagonistic crops against nematodes in banana. ment to Journal of Nematology 26:756-760. Annals of Plant Protection Sciences 3:185-187. GUÉROUT, R. 1969. Action des plantes ameliorantes CHITWOOD, B. G., and M. C. TOUNG. 1960. Host- en culture ananas. III. Bilan Nématologique parasite interactions of the Asiatic pyroid citrus Fruits outre mer. 24:436-443. nema. Plant Disease Reporter 44:848-854. GODFREY, G. H. 1928. Legumes as rotation and trap COOKE, R. C. 1963. Ecological characteristics of crops for pineapple fields. Experiment Station nematode-trapping fungi Hyphomycetes. Annu- of the Association of Hawaiian Pineapple Can- al Review of Applied Biology 52:431-437. ners Bulletin 10:3-21. DAULTON, R. A. C. 1955. Progress on eelworm con- GOMMERS, F. J., and J. BAKKER. 1988. Physiological trol experiments. Rhodesian Tobacco 11:21-27. diseases induced by plant responses or products. DAVIS, C. J. 1964. The introduction, propagation, lib- Pp. 3-22 in G. O. Poinar Jr., and H.-B. Jansson, eration, and establishment of parasites to con- eds. Diseases of Nematodes., Vol. I,. CRC Press trol Nezara oviridula variety smaragdula Inc., Boca Raton, FL, U.S.A. (Fabricius) in Hawaii (Heteroptera: Pentatomi- GONZAGA, V., and S. FERRAZ. 1994. Control of Me- dae). Proceeding of Hawaiian Entomological loidogyne incognita race 3 by some plant species Society 18:369-375. with or without incorporation of the above DESAEGER, J., and M. R. RAO. 1999. The root-knot ground plant parts into the soil. Nematologia nematode problem in sesbania fallow and scope Brasileira 18:42-49. for managing it in western Kenya. Agroforestry GOOD, J. M., N. A. MINTON, and C. A. JAWORSKI. Systems 47:273-288. 1965. Relative susceptibility of selected cover DESAEGER, J., and M. R. RAO. 2000. Parasitic nema- crops and Coastal Bermudagrass to plant nematode populations in natural fallows and im- todes. Phytopathology 55:1026-1030. proved cover crops and their effects on HALBRENDT, J. M. 1996. Allelopathy in the manage- subsequent crops in Kenya. Field Crops Re- ment of plant-parasitic nematodes. Journal of search 65:41-56. Nematology 28:8-14. DESAEGER, J. 2001. Implications of plant-parasitic HAROON, S., and J. G. C. SMART. 1983. Effects of nematodes for improved fallows in Africa. Dis- Pangola digitgrass on Meloidogyne arenaria, M. ja- sertation. Katholieke Universiteit Leuven, Bel- vanica, and M. hapla. Journal of Nematology gium. 15:649-650. DESAEGER, J., and M. R. RAO. 2001. The potential HO, W.-C., and W.-H. KO. 1986. Microbiostasis by nu- of mixed covers of Sesbania, Tephrosia and Crota- trient deficiency shown in natural and synthetic laria to minimise nematode problems on subse- soils. Journal of General Microbiology 132:2807- quent crops. Field Crops Research 70:111-125. 2815. ENDO, B. Y. 1959. Responses of root-lesion nema- HUANG, C. S., J. M. CHARCHAR, and R. C. V. TE- todes, Pratylenchus brachyurus and P. zea, to vari- NENTE. 1981. Control of root-knot nematode ous plants and soil types. Phytopathology 49:417- (Meloidogyne incognita) in carrot (Daucus carota) 421. through rotation. Fitopathologia Brasileira EVANS, D. O., R. J. JOY, and C. L. CHIA. 1988. Cover 5:329-336. crops for orchards in Hawaii. Research Exten- HUANG, C. S., R. C. V. TENENTE, F. C. C. DA SILVA, sion Series 094. College of Tropical Agriculture and J. A. R. LARA. 1981. Effect of Crotalaria spect- and Human Resources, University of Hawaii, abilis and two nematicides on numbers of Meloido- Honolulu, HI, U.S.A. gyne incognita and Helicotylenchus dihystera. 27:1-5. 54 NEMATROPICA Vol. 32, No. 1, 2002

IJANI, A. S. M., R. B. MABAGALA, and M. S. NCHIM- LINFORD, M. B. 1937. Stimulated activity of natural BI. 2000. Efficacy of different control methods enemies of nematodes. Science 85:123-124. applied separately and in combination in man- LUC, M., R. A. SIKORA, and J. BRIDGE. 1993. Intro- aging root-knot nematodes (Meloidogyne spp.) duction: Reflections on nematology in subtropical on common beans. European Journal of Plant and tropical agriculture. Pp. xi-xvii in M. Luc, R. Pathology 106:1-10. A. Sikora, and J. Bridge, eds. Plant parasitic nema- INOMOTO, M. M. 1994. Host reaction of some plant todes in subtropical and tropical agriculture, 2nd species to the burrowing nematode. Nematolo- ed. CAB International, Wallingford, UK. gia Brasileira 18:21-27. MALDEN, J. M., and A. RATNADASS. 1998. Crotalaria JAEHN, A. 1984. Recuperação de lavoura cafeeira re- juncea (Fabaceae) cited for the first time as alter- cepada, com utilização de Crotalaria spectabilis, native host of Eurystylus oldi important pest of torta de mamona e nematicidas, em ãrea infesta- sorghum and ricinus (Hem., Miridae). Bulletin da por Meloidogyne incognita. Nematologia de la Societe Entomologique de France 103:272. Brasileira 8:257-264. MANKAU, R. 1968. Reduction of root-knot disease JAEHN, A., and E. K. REBEL. 1984. Uso de palha de with organic amendments under semifield con- café, leguminosas e nematicida em mudas de ca- ditions. Plant Disease Reporter 52:315-319. feeiro, plantadas em ãrea infestada por Meloido- MARTIN, G. C. 1956. The common root-knot nema- gyne incognita. Nematologia Brasileira 8:309-317. tode, Meloidogyne javanica, and crop rotation. JANSSON, H. B., and B. NORDBRING-HERTZ. 1980. 2. Showy Crotalaria (C. spectabilis). Rhodesian Interaction between nematophagous fungi and Farmer 27:35. plant-parasitic nematodes: attraction, induction MARTIN, G. C. 1958. Root-knot nematodes (Meloidog- of trap formation and capture. Nematologica yne spp.) in the Federation of Rhodesia and 26: 383-389. Nyasaland. Nematologica 3:332-349. JASY, T., and P. K. KOSHY. 1994. Effect of certain leaf McBETH, C. W., and A. L. TAYLOR. 1944. Immune extracts and leaves of Glyricidia maculata, (H. B. and resistant cover crops valuable in root-knot- & K) Steud. as green manure on Radopholus simi- infested peach orchards. American Society of lis. Indian Journal of Nematology 22:117-121. Horticultural Science Proceeding 45:158-166. JOHNSON, A. W., and G. M. CAMPBELL. 1980. Man- McSORLEY, R. 1999. Host suitability of potential cov- aging nematode population densities on tomato er crops for root-knot nematodes. Supplement transplants (Lycopersicon esculentum) using crop to the Journal of Nematology 31:619-623. rotation and a nematicide. Journal of Nematolo- McSORLEY, R. 2001. Multiple cropping systems for gy 12:6-19. nematode management: A review. Soil and Crop JORDAAN, E. M., and D. DEWAELE. 1989. Host sta- Science Society of Florida Proceedings 60:132- tus of five weed species and their effects on 142. Pratylenchus zeae infestation of maize. Journal of McSORLEY, R., and D. W. DICKSON. 1995. Effect of Nematology 20:620-624. tropical rotation crops on Meloidogyne incognita KERRY, B. R. 1987. Biological control. In R. H. Brown and other plant-parasitic nematodes. Supple- and B. R. Kerry, eds. Principles and Practice of ment to the Journal of Nematology 27:535-544. Nematode Control in Crops. Academic Press, McSORLEY, R., D. W. DICKSON, and J. A. BRITO. Sydney, Australia. 1994a. Host status of selected tropical rotation KERRY, B. R., D. H. CRUMP, and F. IRVING. 1995. crops to four populations of root-knot nema- Some aspects of biological control of cyst nematodes. Nematropica 24:45-53. todes. Biocontrol 1:5-14. McSORLEY, R., D. W. DICKSON, J. A. BRITO, T. E. KLOEPPER, J. W., R. RODRÍGUEZ-KÁBANA, J. A. HEWLETT, and J. J. FREDERICK. 1994b. Effects McINROY, and D. J. COLLINS. 1991. Analysis of of tropical rotation crops on Meloidogyne arenaria populations and physiological characterization population densities and vegetable yields in mi- of microorganisms in rhizospheres of plants croplots. Journal of Nematology 26:175-181. with antagonistic properties to phytopathogen- MIAN, I. H., and R. RODRÍGUEZ-KÁBANA. 1982. ic nematodes. Plant and Soil 136:95-102. Survey of the nematicidal properties of some or- KO, W.-H., and J. L. LOCKWOOD. 1967. Soil fung- ganic materials available in Alabama USA as istasis: relation to fungal spore nutrition. Phyto- amendments to soil for control of Meloidogyne pathology 57:894-901. arenaria. Nematropica 12: 235-246. LAMONDIA, J. A. 1996. Trap crops and population MORGAN-JONES, G., and R. RODRÍGUEZ-KÁBA- management of Globodera tabacum tabacum. Jour- NA. 1987. Fungal biocontrol for the manage- nal of Nematology 28:238-243. ment of nematodes. Pp. 94-99 in J. A. Veech, and Crotalaria for nematode management: Wang et al. 55

D. W. Dickson eds. Vistas on Nematology. Soci- in Auburn, Alabama. Nematropica 29:129 (ab- ety of Nematologists, Hyattsville, U.S.A. stract). MOURA, R. M. 1991. Two years of crop rotation on REDDY, K. C., A. R. SOFFES, G. M. PRINE, and R. A. sugarcane fields to control root-knot part I; Ef- DUNN. 1986. Tropical legumes for green ma- fect of the treatments on the nematode popula- nure: II. Nematode populations and their effects tion. Nematologia Brasileira 15:1-7. on succeeding crop yields. Agronomy Journal MOURA, R. M. 1995. Two years of crop rotation on 78:5-10. sugar cane fields to control root-knot nema- REEVES, D. W., Z. MANSOER, and C. W. WOOD. todes. II. Comments on the method and reflexes 1996. Suitability of sunn hemp as an alternative on cane and sugar production. Fitopatologia legume cover crop. in Proceedings of the New Brasileira 20:597-600. Technology and Conservation Tillage 96(7):125- MURPHY, W. S., B. B. BRODIE, and J. M. GOOD. 130. University of Tennessee Agricultural Exper- 1974. Population dynamics of plant nematodes iment Station, TN, U.S.A. in cultivated soil: Effects of combinations of RHOADES, H. L. 1964. Effect of Crotalaria spectabilis cropping systems and nematicides. Journal of and Sesbania exaltata on plant nematode popula- Nematology 6:103-107. tions and subsequent yield of snap beans and NATIONAL RESEARCH COUNCIL. 1979. Tropical le- cabbage. Proceedings of the Florida State Horti- gumes: resources for the future. National Acade- cultural Society 77:233-237. my of Science, Washington, D.C. pp. 272-278. RICE, E. L. 1984. Allelopathy. Academic Press, New NAVARRO, R. 1968. Rotacion de cultivos para el con- York, NY, U.S.A. trol de nematodos fitoparasiticos en el Valle del RICH, J. R., and G. S. RAHI. 1995. Suppression of Me- Cauca. Soil and Crop Science Society of Florida loidogyne javanica and M. incognita on tomato 28:276-279. with ground seed of castor, Crotalaria, hairy indi- NETCHER, C., and R. A. SIKORA. 1990. Nematode go and wheat. Nematoropica 25:159-164. parasites of vegetables. P. 251 in M. Luc, R. A. ROBINSON, A. F., C. G. COOK, and A. C. BRIDGES. Sikora, and J. Bridge, eds. Plant Parasitic Nema- 1998. Comparative reproduction of Rotylenchulus todes in Subtropical and Tropical Agriculture. reniformis and Meloidogyne incognita race 3 on CAB International, Wallingford, U.K. kenaf and sunn hemp grown in rotation with NORDBRING-HERTZ, B. 1973. Peptide-induced cotton. Nematropica 28:143 (abstract). morphogenisis in the nematode-trapping fun- RODRÍGUEZ-KÁBANA, R. 1986. Organic and inor- gus Arthrobotrys oligospora. Physiology of Plant ganic nitrogen amendments to soil as nematode 29:223-233. suppressants. Journal of Nematology 18:129-135. OCHSE, J. J., and W. S. BREWTON. 1954. Prelimi- RODRÍGUEZ-KÁBANA, R., and J. W. KLOEPPER. nary report on Crotalaria versus nematodes. 1998. Cropping systems and the enhancement Florida Horticulture Society Proceedings of microbial activities antagonistic to nema- 67:218-219. todes. Nematropica 28:144 (abstract). PEACOCK, F. C. 1957. Studies on root-knot nema- RODRÍGUEZ-KÁBANA, R., N. KOKALIS-BURELLE, todes of the genus Meloidogyne in the Gold Coast. D. G. ROBERTSON, P. S. KING, and L. W. I. Comparative development on susceptible and WELLS. 1994. Rotations with coastal burmuda- resistant host species. Nematologica 2:76-84. grass, cotton, and bahiagrass for management of PERSMARK, L., and H.-B. JANSSON. 1997. Nemato- Meloidogyne arenaria and southern blight in pea- phagous fungi in the rhizosphere of agricultural nut. Supplement to Journal of Nematology crops. Federation of European Microbiological 26:665-668. Societies Microbiology Ecology 22:303-312. RODRÍGUEZ-KÁBANA, R., J. PINOCHET, D. G. PERSMARK, L., and B. NORDBRING-HERTZ. 1997. ROBERTSON, C. F. WEAVER, and P. S. KING. Conidial trap formation of nematode-trapping 1992a. Horsebean (Canavalia ensiformis) and fungi in soil and soil extracts. Federation of Eu- Crotalaria (Crotalaria spectabilis) for the manage- ropean Microbiological Societies Microbiology ment of Meloidogyne spp. Nematropica 22:29-35. Ecology 22:313-323. RODRÍGUEZ-KÁBANA, R., J. PINOCHET, D. G. ROB- PURSEGLOVE, J. W. 1974. Tropical crops: Dicotylen- ERTSON, and L. W. WELLS. 1992b. Crop rota- dons. Longman Group Limited, London. tion studies with velvetbean (Mucuna deeringiana) QUIROGA-MADRIGAL, R. RODRÍGUEZ-KÁBANA, for the management of Meloidogyne spp. Supple- D. G. ROBERTSON, C. F. WEAVER, and P. S. ment to Journal of Nematology 24:662-668. KING. 1999. Nematode populations and enzy- RODRÍGUEZ-KÁBANA, R., D. G. ROBERTSON, L. matic activity in rhizospheres of tropical legumes WELLS, P. S. KING, and C. F. WEAVER. 1989. 56 NEMATROPICA Vol. 32, No. 1, 2002

Crops uncommon to Alabama for the manage- SILVA, G. S., S. FERRAZ, and J. M. SANTOS. 1990a. ment of Meloidogyne arenaria in peanut. Supple- Effect of Crotalaria spp. on Meloidogyne javanica, ment to Journal of Nematology 21:712-716. Meloidogyne incognita race 3 and Meloidogyne ex- RODRÍGUEZ-KÁBANA, R., C. F. WEAVER, D. G. ROB- igua. Fitopatologia Brasileira 15:94-95. ERTSON, and H. IVEY. 1988. Bahiagrass for the SILVA, G. S., S. FERRAZ, and J. M. SANTOS. 1990b. His- management of Meloidogyne arenaria in peanut. topathology of Crotalaria roots infected with Meloid- Annals of Applied Nematology 2:110-114. ogyne javanica. Fitopatologia Brasileira 15:46-47. RODRÍGUEZ-KÁBANA, R., D. B. WEAVER, D. G. SIPES, B. S., and A. S. ARAKAKI. 1997. Root-knot ROBERTSON, P. S. KING, and E. L. CARDEN. nematode management in dryland taro with 1990. Sorghum in rotation with soybean for the tropical cover crops. Supplement to Journal of management of cyst and root-knot nematodes. Nematology 29:721-724. Nematropica 20:111-119. SOLER-SERRATOSA, A., N. KOKALIS-BURELLE, R. ROMÁN, J. 1964. Immunity of sugarcane to the reni- RODRIGUEZ-KABANA, C. F. WEAVER, and P. S. form nematode. Journal of Agriculture, Univer- KING. 1996. Allelochemicals for control of plant- sity of Pueto Rico 48:162-163. parasitic nematodes. Nematropica 26:57-71. ROTAR, P. P., and R. J. JOY. 1983. ‘Tropic Sun’ sunn STIRLING, G. R. 1991. Biological Control of Plant hemp, Crotalaria juncea L. Research Extension Parasitic Nematodes. CAB International, Bris- Series 036. College of Tropical Agriculture and bane, Australia. Human Resources, University of Hawaii, Hono- TAYLOR, S. G. 1985. Interactions between six warm- lulu, HI, U.S.A. season legumes and three species of root-knot SANTOS, M. A., and O. RUANO. 1987. Reação de nematodes. Journal of Nematology 17:367-370. plantas usadas como adubos verdes a Meloidogyne TRUDGILL, D. L. 1991. Resistance to and tolerance incognita raça 3 e M. javanica. Nematologia of plant parasitic nematodes in plants. Annual Brasileira 11:184-197. Review of Phytopathology 29:167-192. SASSER, J. N. 1954. Identiﬁcation and host-parasite VALLE, L. A. C., S. FERRAZ, and W. P. DIAS. 1995. Ef- relationships of certain root-knot nematodes fect of legumes used as green manure on Hetero- (Meloidogyne spp.). Maryland Agriculture Experi- dera glycines. Nematropica 25:106-107 (Abstract). ment Station Technical Bulletin A:77. VAN DEN BOOGERT, P. H. J. F., H. VELVIS, C. H. SEINHORST, J. W. 1967. The relationships between ETTEMA, and L. A. BOUWMAN. 1994a. The population increase and population density in role of organic matter in the population dynam- plant parasitic nematodes, III and IV. Nemato- ics of the endoparasitic nematophagous fungus, logica 13:429-442. Drechmaria coniospora in microcrosms. Nemato- SHARMA, R. D., and D. D. G. SCOLARI. 1984. Efﬁ- logica 7:139-145. ciency of green manure and crop rotation in the VAN DEN BOOGERT, P. H. J. F., H. VELVIS, C. H. control of nematodes under Savannah condi- ETTEMA, and L. A. BOUWMAN. 1994b. The tions. Nematologia Brasileira 8:193-212. role of organic matter in the population dynam- SHEPHERD, J. A., and K. R. BARKER. 1993. Nematode ics of the endoparasitic nematophagus fungus parasites of tobacco. Pp. 493-518 in M. Luc, R. A. Drechmeria coniospora in microcosms. Nematolog- Sikora and J. Bridge, eds. Plant Parasitic Nema- ica 40:249-257. todes in Subtropical and Tropical Agriculture, VAN DER LINDE, W. J. 1956. The Meloidogyne prob- 2nd ed. CAB International, Wallingford, UK. lem in South Africa. Nematologica 1:177-183. SIKORA, R. A. 1992. Management of the antagonistic VENETTE, R. C., F. A. M. MONSTAFA, and H. FER- potential in agricultural ecosystems for the bio- RIS. 1997. Trophic interactions between bacteri- logical control of plant parasitic nematodes. An- al-feeding nematodes in plant rhizospheres and nual Review of Phytopathology 30:245-247. the nematophagus fungus Hirsutella rhossiliensis SILVA, G. S., S. FERRAZ, and J. M. SANTOS. 1989a. to suppress Heterodera schachtii. Plant and Soil Resistência de espécies de Crotalaria a Pratylen- 191:213-223. chus brachyurus e P. zeae. 13:81-86. VISSER, T., and M. K. VYTHILINGAM. 1959. The ef- SILVA, G. S., S. FERRAZ, and J. M. SANTOS. 1989b. fect of marigolds and some other crops on the Resistencia de especies de Crotalaria a Rotylenchu- Pratylenchus and Meloidogyne populations in tea lus reniformis. 13:87-92. soil. Tea Quarter 30:30-38. SILVA, G. S., S. FERRAZ, and J. M. SANTOS. 1989c. WANG, K.-H. 2000. Management of Rotylenchulus reni- Atraçâo, penetraçâo e desenvolvimento de lar- formis in Hawaiian pineapple with tropical cover vas de Meloidogyne javanica em raízes de Crotalar- crops. Dissertation, University of Hawaii at ia spp. 13:151-163. Manoa, Honolulu, HI, U.S.A. Crotalaria for nematode management: Wang et al. 57

WANG, K.-H., B. S. Sipes, and D. P. Schmitt. 2002a. Heterodera schachtii in a California ﬁeld. Phytopa- Suppression of Rotylenchulus reniformis by Crota- thology 89:434-440. laria juncea, Brassica napus, and Tagetes erecta. WHITTINGTON, D. P., and E. I. ZEHR. 1992. Popula- Nematropica 31:237-251. tions of Criconemella xenoplax on peach interplant- WANG, K.-H., B. S. Sipes, and D. P. Schmitt. 2002b. ed with certain herbaceous plants. Supplement to Management of Rotylenchulus reniformis in pine- Journal of Nematology 24:688-692. apple, Ananas comosus, by intercycle cover crops. WILSON, G. F., and F. E. CAVENESS. 1980. The ef- Journal of Nematology 34:(in press). fects of rotation crops on the survival of root- WESTPHAL, A., and J. O. BECKER. 1999. Biological knot, root lesion and spiral nematodes. Nemat- suppression and natural population decline of ropica 10:56-61.

Received: Accepted for publication: 14.VII.2001 21.IX.2001 Recibido: Aceptado para publicacion: