Heterodera cajani
(pigeon pea cyst nematode)

Life cycle

The development and life cycle of H. cajani were studied by Koshy and Swarup (1971c) on pigeon pea plants at an average soil temperature of 29°C (range 27-36°C). Second-stage juveniles (J2) penetrate the roots within 48 hours of inoculation. Both tap and lateral roots were penetrated, not necessarily near the root tips. Moulting began on the third day beginning from the anterior part and completing on the fourth day. Fourth-stage juveniles with well-developed reflexed ovaries were found on the tenth day. Adult lemon-shaped females were observed on the 12th day. Males were found on the 12th or 13th day. On the 14th day, many eggs were seen in the egg sacs as well as inside the white females. Second-stage juveniles were collected from soil as well as from cysts from which they hatched on the 16th day. A few males, apparently embedded in the egg mass, also emerged from the cysts. The white females turned yellowish from the 20th day onwards; the change from white to bright yellow took 8 days. The egg sac turned opaque and yellowish, occasionally purple. Brown cysts were noticed on the 38th day after inoculation. Although males are thought to be necessary for reproduction, females sometimes reproduced without them.

The life cycle was completed in 16 days at 29°C but during cooler conditions (10-25°C), the life-cycle took 45-80 days to complete (Koshy and Swarup, 1971c). On one crop of pigeon pea, 8-9 generations were recorded. Kalha and Edward (1979) studied the life cycle in Phaseolus mungo [Vigna mungo]. They found that juveniles took 3 days to penetrate the root and developed into males and females in 24 and 27 days, respectively.

Yadav and Walia (1989) found that H. cajani completes its life cycle on pigeon pea and Vigna aconitifolia in 23 days; on Vigna radiata in 26 days and on V. mungo and cowpea (V. unguiculata) in 29 days at a temperature of 24-39°C. On cowpea, Gupta and Edward (1974) found that the total time required by H. cajani to complete one generation was 13 days for males and 17 days for females and that in one growth season of the host lasting approximately 4 months, the nematode could produce up to 8 generations. As many as nine generations could be completed in 1 year under laboratory conditions. Two favourable periods for the multiplication of the nematode were during June-September and April-June in North India (Koshy and Swarup, 1971d).

A life table for H. cajani on pigeon pea at 25°C was developed by Singh and Sharma (1995b). Mortality rates were very high during egg and J2 stages prior to root penetration. Mortality of subsequent life stages was low and virtually constant. Egg laying began on the 23rd day and stopped on the 31st day after the start of the cohort. Mean generation time was 26.9 days and net reproductive rate 15.5 times per generation. The true intrinsic rate (rm) of natural increase indicated that a H. cajani population would multiply 1.107 times a day, and double itself in about 7 days.

Development and reproduction

H. cajani is primarily a parasite of roots. The adult females are lemon-shaped and sedentary in habit, and remain attached to roots semi-endoparasitically. Males are vermiform. Eggs may be retained inside the female body but many are laid in a gelatinous matrix forming egg sacs.

The optimum soil moisture content required for the development of H. cajani is between 35 and 45%. The number of cysts and final nematode population were higher when plants were irrigated twice in 24 h than once in either 24 or 48 h (Sharma and Trivedi, 1997). In pigeon pea, nematode multiplication is highest in sand and sandy loam soils due to the better development of plant roots (Walia, 1987).

Singh and Sharma (1994) studied the effects of constant and fluctuating temperatures on the development and reproduction of H. cajani on pigeon pea in growth chambers at 10, 15, 20, 25 and 30°C and in a greenhouse fluctuating between 22 and 38°C. Nematode penetration was greatest in roots at 25°C; there was no penetration at 10°C. The basal threshold temperature for development was calculated to be 11°C. Completion of one H. cajani generation required 17, 28, 35 and 66 days (323, 392, 315 and 264 degree-days) at 30, 25, 20 and 15°C, respectively, and 19 days (356 degree-days) at a fluctuating temperature. Survival was greater at 20 and 25°C than at 15 and 30°C. The greatest number of females (18 females per root) was produced at 25° females at 15°C. Nematode reproduction was 1.6 to 7.1 times greater at 25°C than at other temperatures. Equations were developed to predict nematode development rate, cumulative juvenile emergence from egg sacs and cysts, and population increases as influenced by temperature. Singh and Sharma (1995a) found that averaged across temperatures (20-32°C), the percentage of juveniles that penetrated roots was 34, 32, 9 and 4% at 24, 32, 16 and 40% soil moisture levels, respectively. Numbers of females per root system 4 weeks after infesting soil with J2 was 80 at 24%, 65 at 32%, 26 at 16%, and 39 at 40% soil moisture. Nematode reproduction was greatest at 24% soil moisture and 25°C. The Reproductive Factor was 19.4 at 24%, 15.2 at 32%, 5.7 at 16%, and 0.5 at 40% soil moisture level. Nematode penetration, development, and reproduction at different moisture levels were greater at 25 and 25-32° was retarded at 40% soil moisture and 20°C compared with that at 24 and 32% moisture levels and 25°C (Singh and Sharma, 1995a).

Yadav and Walia (1989) showed that larval penetration and multiplication was higher on pigeon pea, Sesbania bispinosa and Lablab purpureus than on cowpea, Vigna aconitifolia, Cyamopsis tetragonoloba and sesame. The fecundity of the nematode was not affected by the host.

Juvenile emergence

Factors affecting the emergence of juveniles were studied by Koshy and Swarup (1971b) and reviewed by Sharma and Sharma (1998).

Emergence from egg sacs is higher and more rapid than from white (young) or brown (mature) cysts (Sharma and Swarup, 1984; Sharma and Sharma, 1998). From white cysts, 50-80% of the juveniles emerged within 1 month at 25-30°C. 53% of the juveniles from brown cysts emerged at 25°C, 52% at 20°C and 5% at 15°C. About 48% of the juvebiles did not emerge even after incubation for 525 days at 25°C. These dormant juveniles were either free or within eggs in cysts. Juvenile emergence was greater from cysts produced on 30-day-old pigeon pea plants than from cysts produced on older plants. The pattern of J2 emergence in H. cajani is complex and temperature is a major, but not the only, important factor. Some of the encysted juvenile population undergoes diapause (Singh and Sharma, 1996).

No emergence occurs at 12 and 40°C. At fluctuating temperatures (15-40°C), the emergence of juveniles occurs in phases: 70-90% juveniles emerged in 5-7 months, followed by a short dormancy period of 2-4 months (Sharma and Swarup, 1984). It has been suggested that the nematodes have mechanisms of temperature-, host- and time-mediated delays which must have evolved gradually but have persisted because of their survival value (Singh and Sharma, 1996). Aeration does not appear to affect larval emergence but cysts exposed to light result in higher emergence than the cysts subjected to total darkness. Emergence occurs over a wide pH range, from 3.5-11.5; optimum at pH 10.5 (Singh and Sharma, 1996).

Hatching from cysts and egg sacs of six successive generations of H. cajani produced on cowpea during a single growing season in the greenhouse was compared in distilled water, soil leachate and host root diffusate by Gaur et al. (1992). Hatch from cysts but not egg sacs in the fifth and sixth generations, produced on senescing plants, showed a marked dependency on host root diffusate. The ratio of eggs in egg sacs to eggs in cysts decreased with each succeeding generation and a comparison between third and sixth generations indicated that, in the older generation, more lipid reserves are partitioned into the encysted J2 than into the J2 in egg sacs (Gaur et al., 1992).

Root leachates of host plants stimulated the larval hatch of H. cajani. Leachates collected from 2, 3 or 4-week-old plants or soil were more stimulatory than those from 1-week-old plants (Yadav and Walia, 1989).

Survival

Eggs within cysts are able to withstand extremes of desiccation; a maximum reduction of about 30% of viable eggs was recorded after 3 weeks exposure to 0% relative humidity (RH), which is similar to the reduction found in dry soil after storage of between 2 and 12 months. Cysts stored in moist soil for up to 12 months gave a greater percentage hatch in cowpea root diffusate (CRD) than those from air dried soil but the actual number of J2 emerging per cyst was lower. Eggs hatched during the first 4 months of storage in moist soil but only during the first 2 months in air dried soil (Gaur et al., 1996).

Pathogenicity

H. cajani juveniles were observed in the cortex of pigeon pea seedlings 48 h after inoculation. Movement was predominantly intracellular. Syncytia formed in the stelar region. Cells near the feeding site became angular with thickened cell walls. Giant cells had dense granular cytoplasm with 4-5 nuclei. There was extensive disruption of the xylem vessels. Juveniles which were established in the cortex developed mostly into males and those in the stelar region into females (Koshy and Swarup, 1980).

In glasshouse pot experiments with pigeon pea (Cajanus cajan), an initial density of 1.0 juvenile per cm³ soil resulted in a 14-24% reduction in plant height, root and shoot mass and leaf area. The tolerance limit for pod yield in field experiments was 2.6 eggs and juveniles of H. cajani per cm³ soil at sowing time (Sharma et al., 1993b).

H. cajani caused a reduction in bacterial nodule weight in Cyamopsis tetragonoloba at inoculum levels of 500 juveniles/plant and above. However, the actual functioning of the nodules was reduced at inoculum levels of 5 juveniles/plant and above. It is suggested that H. cajani infection causes an accumulation of ammonia in the roots of C. tetragonoloba leading to inactivation of nitrogenase and, consequently, a reduction in nitrogen fixation (Walia et al., 1989).

Various pathogenicity studies looking at plant growth parameters have been carried out on:
Vigna mungo (Devi and Gupta, 1988; Jain et al., 1994b); pigeon pea (Zaki and Bhatti, 1986c; Walia, 1987; Devi and Gupta, 1988; Sharma and Nene, 1988; Singh and Singh, 1995); sesame (Rana and Dalal, 1994);
cowpea (Aboul-Eid and Ghorab, 1974; Zaki and Bhatti, 1986c; Devi and Gupta, 1988); V. radiata (Devi and Gupta, 1988); V. aconitifolia (Zaki and Bhatti, 1986c); and Cyamopsis tetragonoloba (Walia and Bhatti, 1989).

The effects of H. cajani infestation on nitrogen, phosphorus and potassium levels in the roots and tops of pigeon pea and V. aconitifolia seedlings were studied by Zaki and Bhatti (1986b) and on the sugar content of Vigna sinensis [V. unguiculata] by Sethi and Sharma (1978) and Sharma and Sethi (1979a).

Races

Fourteen populations of H. cajani from different localities in seven districts of Uttar Pradesh (India) were tested on 9 hosts revealing the presence of 3 races: Race 1 reproduced on all the hosts tested; Race 2 did not reproduce on Cyamopsis tetragonoloba; Race 3 did not reproduce on C. tetragonoloba or Crotalaria juncea (Siddiqui and Mahmood, 1993).

Interactions with other plant pathogens

Interactions between H. cajani and the following pathogens have been studied:

Fusarium udum [Gibberella indica], on pigeon pea (Sharma and Nene, 1989; Singh et al., 1993c; Rai and Singh, 1996b; Siddiqui and Mahmood, 1999);
Fusarium solani, on cowpea (Varaprasad et al., 1987; Varaprasad and Kumar, 1991);
Rhizoctonia bataticola [Macrophomina phaseolina] (Walia and Gupta, 1986b), on Vigna mungo (Tiwari, 1998);
Rhizoctonia solani [Thanatephorus cucumeris], on cowpea (Walia and Gupta, 1986a);
Meloidogyne incognita, on pigeon pea (Siddiqui and Mahmood, 1999); on cowpea (Sharma and Sethi, 1976, 1978a, 1979b).

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Introduction

An integrated control approach involving summer ploughing, crop rotation, seed treatment, limited applications of chemicals and the use of resistant varieties should be adopted for the control of cyst nematodes (Yadav, 1986). After cyst nematodes have infested a field, it is practically impossible to eliminate them.

Chemical Control

Cyst nematodes are highly resistant to chemical control because the female, after death, transforms into a tough brown sac protecting the eggs which remain within.

Fensulfothion, when evaluated as a seed treatment for pigeon pea, reduced nematode populations, with high concentrations and long soaking period being the most effective (Zaki and Bhatti, 1986a). Seed soak treatments with dimethoate, acephate and quinalphos did not give effective control (Velayutham, 1988a).

Certain chemicals stimulate juvenile emergence and can be used with proper knowledge of the biology of the parasites to control them.

Experimental studies of various synthetic chemical treatments showing some control of H. cajani include the following:
Thiride gave better control than carbendazim, mancozeb and ziram on Vigna radiata in pot experiments (Mishra and Gupta, 1991);

The following non-synthetic treatments have also provided some control:
Essential oils of Mentha piperita, Ocimum sanctum, Cymbopogon martini, C. nardus, C. winterianus, C. flexuosus and O. basilicum (Gokte et al., 1993);
Root extract of Xanthium strumarium (Malik et al., 1987);
Green manures of Vigna radiata, cowpea (Vigna unguiculata), Crotalaria juncea and Sesbania bispinosa (Devi and Gupta, 1995); fenugreek (Trigonella foenum-graecum), wild methi (Senji species), berseem (Trifolium alexandrinum) and drum stick (Moringo pterygosperma) (Devi, 1997).
Powdered leaf extracts of Terminelia arjuna on pigeon pea (Singh and Singh, 1992); Argemone mexicana, Cannabis sativa, Datura metel, Nerium indicum (Mojumdar et al., 1989); and Solanum xanthocarpum (Bhatti et al., 1997);
Latex from Calotropis gigantea and Euphorbia pulcherrima, when applied as seed dressing to V. radiata (Gupta et al., 1999).
Oil cakes of neem, mustard and mahua (Rai and Singh, 1995, 1996a; Devi and Gupta, 1996).

Biological Control

Plant parasitic nematodes have many natural predators and parasites in the soil which provide opportunities for biological control.

Combinations of biocontrol agents and vesicular arbuscular mycorrhizal fungi have been used to manage the wilt disease complex of pigeon pea caused by H. cajani and Fusarium udum [Gibberella indica]: Bacillus subtilis, Bradyrhizobium japonicum and Glomus fasciculatum (Siddiqui and Mahmood, 1995a); Paecilomyces lilacinus, Verticillium chlamydosporium and Gigaspora margarita (Siddiqui and Mahmood, 1995b); and Trichoderma harzianum, V. chlamydosporium and Glomus mosseae (Siddiqui and Mahmood, 1996).

Resistant Varieties

The use of resistant varieties is the most economical method of controlling plant parasitic nematodes. A greenhouse technique to screen pigeon pea for resistance to H. cajani is described by Sharma et al. (1991).

Several screening progammes have been carried out to identify resistance to H. cajani in the following crops:
Pigeon pea and its wild relatives Cajanus platycarpus and others (Sharma et al., 1993c; Sharma, 1995; Singh and Singh, 1995; Elyas and Sharma, 1997; Siddiqui et al., 1998a);
Vigna radiata and V. mungo (Devi and Gupta, 1987; Siddiqui et al., 1999);
Cowpea, in which generally low levels of resistance have been reported (Sharma and Sethi, 1978b; Devi and Gupta, 1991; Balasubramanian et al., 1996);
Sesame, when none of 43 genotypes showed resistance (Rana and Dalal, 1993).

Cultural Practices

H. cajani has a very restricted host range and is mostly confined to the Fabaceae. Growing the host crop in rotations every 4-5 years with non-hosts can help to maintain populations below threshold levels. The significance of double crop (intercrop and sequential crop), single crop (rainy season crop fallow) and rotations on the densities of H. cajani and other nematodes was studied by Sharma et al. (1996b). Mean population densities of H. cajani were about eight times lower in single crop systems than in double crop systems, with pigeon pea as a component intercrop. Plots planted to sorghum, safflower and chickpea in the preceding year contained fewer H. cajani eggs and juveniles than did plots previously planted to pigeon pea, cowpea or Vigna radiata. Continuous cropping of sorghum in the rainy season and safflower in the post-rainy season markedly reduced the population density of H. cajani.

Intercropping sorghum with a tolerant pigeon pea cultivar could be effective in increasing the productivity of traditional production systems in H. cajani infested regions (Sharma et al., 1996b).