Introduction

Chickpea (Cicer arietinum L.) is the fourth most important legume grown in the world after soybeans, peanuts, and beans (^{FAOSTAT, 2021}). Its grains contain fibers, proteins, vitamins, carbohydrates, mineral salts, unsaturated fatty acids, and ß-carotene and are a source of protein in human and animal food supplementation (^{Souza, 2019}). There are reports of cultivation in 55 countries, with a total production of 17.19 million t (^{FAOSTAT, 2021}). The world average yield is approximately 1.2 t ha^-1; however, some countries reach higher values, such as Israel (6.04 t ha^-1), China (5.2 t ha^-1), and Moldova (3.9 t ha^-1) (^{Avelar et al., 2018}).

In Brazil, domestic consumption and production are considered low, but in recent years, due to its nutritional characteristics and changes/trends in the patterns of food consumption, the demand for chickpea grains has grown. However, it is still necessary to import a large part of the quantity consumed in the domestic market, most of which comes from Mexico and Argentina (^{Artiaga et al., 2015}), with amounts close to 8,000 t per year (^{Avelar et al., 2018}). This new scenario gives chickpea an important role as an economic option for planting in the second summer harvest (known as safrinha in Portuguese and meaning "little harvest") in the Brazilian Cerrado biome, which takes advantage of the drought tolerance ability of this species to grow despite little rainfall (^{Artiaga et al., 2015}).

The many species of plant-parasitic nematodes (PPN) are among the constraints that can cause impairments to chickpea production; some of these species include root-knot nematodes (Meloidogyne javanica, M. incognita, and M. artiella), cyst nematode (Heterodera ciceri), and the root-lesion nematode (Pratylenchus spp.) (^{Castillo et al., 2008}; ^{Zwart et al., 2019}). Characterization studies in various parts of the world show that most chickpea genotypes are normally susceptible (^{Zwart et al., 2019}). However, there are few reports of chickpea genotypes with nematode tolerance (^{Ali & Ahmad, 2000}; ^{Ansari et al., 2004}; ^{Hassan & Devi, 2004}; ^{Chakraborty et al., 2016}; ^{Sumita, 2017}), making more studies in this area necessary.

PPN also damage soybeans, with Heterodera glycines as one of the most harmful species due to its wide geographic distribution. However, in recent years, mainly in the Midwest region of Brazil, as well as in other regions, damages were registered and also attributed to the root-lesion nematode, Pratylenchus brachyurus, a polyphagous species (^{Cruz et al., 2020}) that colonizes even grasses such as maize and pastures.

Heterodera glycines can also colonize other plants like sunn hemp (Crotalaria juncea), pigeon pea (Cajanus cajan) (^{Valle et al., 1996}), common bean (Phaseolus vulgaris), azuki bean (Vigna angularis), and mung bean (Vigna radiata) (^{Rossi & Ferraz, 2001}). ^{Poromarto and Nelson (2010)} verified that chickpea was a poor host of H. glycines race 3; however, there are no studies on H. glycines race 5. ^{Cardoso et al. (2019)} evaluated the resistance of Crotalaria ochroleuca to races 1, 2, 3, 5, 6, and 14 of H. glycines, and verified that it was resistant to races 1, 2 and 5, but was susceptible to race 3 and showed varied reactions to races 6 and 14. Due to the increase in the cultivated areas of chickpea in succession to soybeans in the Brazilian Midwest, research on these two PPN species becomes important. Thus, the objective of this study was to evaluate the population dynamics of Heterodera glycines race 5 and Pratylenchus brachyurus in a succession crop of soybean and chickpea.

Materials and methods

The experiment was carried out in Campos Novos dos Parecis, a municipality in the state of Mato Grosso, Brazil, from February to May 2017, in a field area naturally infested with the species Heterodera glycines race 5 and Pratylenchus brachyurus. The regional climate according to the Köppen classification is tropical with a dry winter and rainy summer, CWB type. The weather of the summer season in the Cerrado biome is characterized by a semi-humid tropical climate, with average temperatures of 25°C and annual precipitation of 1,677 mm. Six chickpea cultivars, BRS Aleppo, BRS Cícero, Jamu 96, BRS Cristalino, BRS Toro, and BRS Kalifa, were evaluated. The sowing occurred on February 24, 2017.

The experiment was conducted in an area of 60 ha (10 ha per cultivar), previously cultivated with a susceptible soybean cultivar, in a completely randomized design with three replicates. Soil and plant samples were collected at regular intervals of about 30 d on March 24, April 24, and May 25. For each replicate, five soil samples of 500-600 g and roots were collected using equidistant georeferenced points. All the samples were identified, extracted, and quantified in the Nematology Laboratory of Embrapa Vegetables, Brasília - DF.

The H. glycines and P. brachyurus species were identified according to their morphologic characteristics (^{Gonzaga, 2006}; ^{Mekete et al., 2012}). The identification of H. glycines race 5 was performed with the differentiating host test according to ^{Riggs and Schmitt (1988)}.

The extraction of second-stage juveniles and cists of H. glycines, as well as juveniles and adults of P. brachyurus from the soil samples, was performed using the rapid centrifugal-flotation technique, employing a sucrose solution, in accordance with ^{Jenkins (1964)}. The extraction of PPN associated with roots was performed using the method of Hussey and Barker, modified by Bonetti and Ferraz in accordance with ^{Wilcken et al. (2010)}. After the extractions, the quantification of the nematodes was performed with a Peters chamber and the visualization was made under a trinocular stereoscopic microscope (model Eclipse 80i, Nikon, Melville, NY, USA) in accordance with ^{Bellé et al. (2017)}.

The following response variables were evaluated: number of viable cysts of H. glycines /150 cm³ of soil (NVCS), number of nonviable cists of H. glycines/150 cm³ of soil (NNVCS), number of juveniles of second stage (J2) of H. glycines/150 cm³ of soil (NJ2HS), number of juveniles and adults of P. brachyurus/'150 cm³ of soil (NJAPS), and number of juveniles and adults of P. brachyurus/g of fresh roots (NJAPR). The data were subjected to variance and regression analyses using the Genes statistical program (^{Cruz, 2016}).

Results and discussion

There was no effect of the cultivars on the response variables evaluated. On the contrary, statistical differences were observed for the source of variation - date of collection or sampling time for all the evaluated variables, except for the number of juveniles and adults of Pratylenchus in roots (NJAPR). Table 1 indicates that the population levels of P. brachyurus per g of roots remained constant. There was also no interaction between the cultivars and sampling times -collection (CxCL) (Tab. 1), indicating that the population dynamics of the studied nematode species was not affected by any of these factors (cultivars and times).

Regarding the number of viable cysts of H. glycines/150 cm³ of soil (NVCS), a significant reduction in the population was observed during the chickpea crop cycle (Fig. 1), regardless of the cultivar used.

FIGURE 1 Number of viable cysts of Heterodera glycines /1 50 cm³ of soil according to the collection intervals (30, 60, and 90 d after sowing). 

An increase in the number of nonviable cysts of H. glycines /150 cm³ of soil (NNVCS) was observed according to the sampling times (CL) (Fig. 2), regardless of the chickpea cultivar.

FIGURE 2 Number of nonviable cysts of Heterodera glycines /1 50 cm³ of soil according to the collection intervals (30, 60, and 90 d after sowing). 

As for the number of juveniles of second stage (J2) of H. glycines/150 cm³ of soil (NJ2HS), among all the evaluated cultivars, there was a reduction of population levels from 57.64 to 16.67 (Fig. 3).

FIGURE 3 Number of juveniles of second stage (J2) of Heterodera glycines /150 cm³ of soil according to the collection intervals (30, 60, and 90 d after sowing). 

The increase in the number of nonviable cysts, the reduction of viable cysts, and the reduction in the number of these PPN in the soil may be due to the hatching of juveniles of H. glycines race 5 and the absence of a host plant in the area for a period that prevented the reinfection and continuity of its life cycle (^{Cardoso et al., 2019}). This result shows that chickpea is not a host of H. glycines race 5 and that it can be indicated for crop rotation or succession with soybeans in the areas infested with this race. This is a significant finding, as there are no similar studies in the literature.

The number of juveniles and adults of P. brachyurus/'150 cm³ of soil (NJAPS) was maintained during the first 60 d of the cycle, with a subsequent sharp reduction observed from 35.42 to 10.42 between the samplings collected at 60 and 90 d of the cycle (Fig. 4). However, as previously verified, the population per g of roots remained high in all the samples. This reduction in the population of P. brachyurus in the soil, considering that the chickpea vegetative cycle is close to 110 d, was probably because this nematode is a migrating endoparasite that prefers roots to soil. When plants are expanding their canopy in an area with a large initial population of nematodes in the soil, it is usual for migration to occur with more intensity as the roots are also developing. At the end of the crop cycle, there will be a new migration to the soil, with a subsequent search for host plants (^{Puerari et al., 2020}).

FIGURE 4 Number of juveniles of second stage (J2) and adults of Pratylenchus brachyurus /150 cm³ of soil according to the collection intervals (30, 60, and 90 d after sowing). 

^{Santos (2019)} evaluated these same six cultivars in a naturally infested field with the presence of M. javanica for their resistance to P. brachyurus, finding a marked differentiation in terms of their susceptibility. Nevertheless, this author estimated only the reproduction factor (RF) based on the rate between the initial population at the time of the sowing and the final nematode population in the soil. That study verified that the cultivar Jamu 96 maintained the same population of P. brachyurus in both periods, i.e., showing a reproduction factor equal to 1; BRS Cicero showed a reproduction factor of 0.95 and all the others had RFs ranging from 0.43 to 0.65. The initial population level of P. brachyurus in the soil may be a determinant factor to the degree of resistance of the cultivars; since the population in this study was considered very high, it may have resulted in a greater nematode pressure, making it impossible to verify differences in the resistance levels of the cultivars.

^{Santos (2019)} demonstrated that these chickpea cultivars showed resistance to M. javanica in a naturally infested field with a mixed population of M. javanica and P. brachyurus. However, ^{Bernardes Neto et al. (2019)} evaluated the same cultivars in a greenhouse trial and considered them susceptible to M. incognita and M. enterolobii, which are also important for both chickpeas and soybeans.

Among the most widespread control methods for PPN are the use of nematicides, crop rotation, antagonistic plants, organic matter, fallowing, soil fumigation, solarization, and use of genetic resistance (^{Ravichandra, 2014}; ^{Cruz et al., 2020}). Crop rotation with non-host plant species for a sufficient period to allow the decomposition of infested residues reduces the viability and association of the pathogen, especially in the no-tillage system (^{Cruz et al., 2020}). It also increases beneficial soil organisms and minimizes the impact of root diseases (^{Cruz et al., 2020}).

To evaluate the response of different plant species to H. glycines and to better understand what crops could be recommended in rotation or succession or as green manure for soybeans, ^{Sanches (2001)} evaluated two species ofvelvet bean (Mucuna pruriens and Mucuna utilis) for reaction to races 2, 3, 4, 5 and 14 of H glycines and verified that both are not hosts of this nematode. Evaluating the response of several species used as green manure or cover crops to race 3 of this nematode, ^{Valle et al. (1996)} found that sunn hemp (Crotalaria juncea), pigeon pea (Cajanus cajan), azuki beans (Vigna angularis), and mungo beans (Vigna radiata) are hosts that can multiply these PPN. The susceptibility of azuki and mungo beans was also verified by ^{Rossi and Ferraz (2001)}, who also found susceptibility in common beans (Phaseolus vulgaris) and white lupine (Lupinus albus L.) to race 3 of this nematode.

In addition to cultivated plants, H. glycines can also be found in weeds. ^{Venkatesh et al. (2000)} evaluated 22 weed species from 13 families of dicotyledonous as alternative hosts of H. glycines in a greenhouse in Ohio, USA, and found that the red dead-nettle (Lamium purpureum), common henbit (Lamium amplexicaule), field pennycress (Thlaspi arvense) and shepherd purse (Capsella bursapastoris) were hosts. A greater reproduction of race 1 and a low reproduction of race 6 were found in red dead-nettle. For race 3, the highest level of reproduction occurred in red dead-nettle, field pennycress, and common henbit (^{Venkatesh et al., 2000}).

^{Poromarto and Nelson (2010)} found that the chickpea was not an efficient host of H. glycines race 3, although it allowed the multiplication of a small number of this nematode. However, ^{Cardoso et al. (2019)}, who evaluated the resistance of rattlepod (Crotalaria ochroleuca) to races 1, 2, 3, 5, 6, and 14 of H. glycines, found that this plant species was resistant to races 1, 2, and 5 but was susceptible to race 3 and showed varied reactions to races 6 and 14.

The identification of these H. glycines races is important since prior to this research, no study had identified resistance of this plant to race 5 of this nematode.

Conclusions

There was a reduction in the population levels of Heterodera glycines race 5 throughout the cycle of chickpeas, indicating that it is possible to grow this species in a succession crop with soybeans in the presence of this nematode.

Due to the maintenance of the population of Pratylenchus brachyurus in the roots throughout the chickpea cycle, crop rotation of soybean with chickpeas would not be recommended for fields infested with this nematode.