Epidemiology and integrated control of Nacobbus aberranson tomato in Mexico
Jairo CRISTÓBAL-ALEJO 1, Gustavo MORA-AGUILERA 2, Rosa H. MANZANILLA-LÓPEZ 3,∗,Nahúm MARBÁN-MÉNDOZA 4, Prometeo SÁNCHEZ-GARCIA 5,
Ignacio CID DEL PRADO-VERA 2 and Ken EVANS 3
1 Instituto Tecnológico de Conkal, Km 16.3 Antigua Carretera Mérida-Motul, Conkal, Yucatán, CP 97345, México2 Programa de Fitosanidad, Colegio de Postgraduados, Km 36.5 Carretera México-Texcoco, Montecillos,
4 Dpto. de Parasitología Agrícola, Universidad Autónoma Chapingo, Edo. Méx. C.P. 56230, México5 Programa de Edafología, Colegio de Postgraduados, Km 36.5 Carretera México-Texcoco,
Edo. Méx. C.P. 56230, México
Received: 7 January 2005; revised: 18 July 2006Accepted for publication: 18 July 2006
Summary – Population densities, population fluctuations, yield loss and disease incidence caused by Nacobbus aberrans on tomato(Lycopersicon esculentum) were studied, using an epidemiological approach, in a field experiment that included three different controlregimes: an integrated control (IC) scheme, which included fertilisation, nematicide (ethoprop) and chicken manure; a technical control(TC) scheme, based on the best local practices of fertilisation and use of carbofuran for nematode control; and a check treatment (AC),with no application of fertilisers or nematicide. At least three generations of N. aberrans occurred through the cropping season andthe numbers of galls/plant and females/g of root through the crop season were used to define the area under a disease progress curve(AUDPC). The variables b−1 (Weibull’s apparent infection rate), AUDPC and Yf (final disease incidence) indicated less crop damageunder the IC scheme than under the other two schemes (TC and AC). The IC scheme resulted in increased plant height (41-49%),foliage dry weight (37-53%) and stem diameter (31-41%) compared with the TC and AC schemes. Tomato yields in IC surpassed thosefrom TC and AC by 34 and 83%, respectively, while TC exceeded AC by 73%. The yield loss attributed to N. aberrans was 12, 29 and83% in IC, TC and AC, respectively. The IC scheme improved commercial production by 20 and 81% in comparison to the TC andAC schemes. This was largely due to effective control of the initial inoculum density, which affects the first generation of the nematodepopulation; control of this generation is essential for avoidance of yield loss. The first generation is completed during the period 0-60dat (days after transplanting), i.e., during the critical stages of flowering, fruit initiation and fruit set (40, 50 and 60 dat). Data on plantperformance taken every 10 days were used to derive a multiple point model for calculation of production loss.
In Mexico, tomato exports, valued at more than 310million US dollars (Anon., 2000), are an important sourceof foreign income. Most tomato and vegetable productionis used for local consumption but, because of their rela-tively high value in Mexican markets, small farmers preferto grow tomatoes as cash crops. Galling of the root systemby the ‘false root-knot nematode’, Nacobbus aberrans(Thorne, 1935) Thorne & Allen, 1944, is one of the mostlimiting diseases for tomato production in Mexico (Cruzet al., 1987). This disease reaches extreme importance
on the crop in the municipality of Tecamachalco (Puebla,Mexico), where the nematode can cause 50-100% yieldloss (Zamudio, 1987). As a result, crops can be abandonedas unprofitable and the contaminated land remains unsuit-able for growing tomatoes for some years.
Nacobbus aberrans has spread over most of the arableland of the municipality of Tecamachalco (ca 300 ha arebadly infested), and the need of local farmers to main-tain production, and thereby income, by using new ar-eas of land means that there is a constant threat of its
further dissemination. Not knowing how to treat the dis-ease, farmers often make improper use of nematicides orother pesticides. Previous attempts have been made lo-cally to control this disease on tomato, chilli pepper (Cap-sicum annuum L.), and beans (Phaseolus vulgaris L.),using nematicides, genetic resistance, manures, solarisa-tion, and organic amendments (Zamudio, 1987; Silva,1989; Gómez, 1991; Cid del Prado et al., 1997; Cristóbal-Alejo et al., 2001a; Yáñez-Juárez et al., 2001; Franco-Navarro et al., 2002). However, no specific guidelinesare available and the problem of controlling the nema-tode has not been resolved. This is due partly to a lackof basic local information about the biology of the nema-tode, such as its population dynamics, ecology and epi-demiology. Therefore, a study was made to investigatethe population densities and population fluctuations of N.aberrans, the incidence of the disease that it causes, andits effects on tomato, Lycopersicon esculentum Mill., cv.Rio Grande, vigour and yield in field conditions when ap-plying three different control schemes: integrated control(IC, including fertilisation, nematicide and chicken ma-nure), technical control (TC, based on local practices),and a check treatment (AC, with no application of fer-tiliser, nematicides or chicken manure). The study wasintended to identify the best control scheme, and to im-prove the measures taken locally against the nematode,as well as improving our understanding of the dynam-ics of the relationship between the nematode and thecrop.
Materials and methods
ESTABLISHMENT OF THE EXPERIMENT
The experimental area (Tecamachalco, Mexico) is lo-cated at latitude 18◦53′32′′ north and longitude 97◦44′22′′west, at an elevation of 2012 m above sea level. Localconditions include minimum and maximum average tem-peratures of 3.5 and 29.5◦C, and an average annual pre-cipitation of 606 mm. The experiment was made on 1ha of land, naturally infested with N. aberrans, duringthe spring-summer season of 1999. The soil consisted of48.8% sand, 22.0% silt and 29.24% clay, pH 7.5 and or-ganic matter content 1.21%. The land was prepared forplanting the tomato crop by harrowing twice at right an-gles, followed by ploughing, to even out distribution of thenematode in the area occupied by the experiment. In or-der to assess the spatial distribution of the nematode, soilsamples were taken to a depth of 20 cm in a systematic
zigzag pattern of ten cores (200-300 g each) from eachof a total of 12 plots of 6 × 12 m, thus providing a bulksample of ca 3 kg of soil per plot (McSorley, 1987). Theinitial population density of N. aberrans in each plot wasestimated in a bio-assay. For this, two 1-month-old tomatoseedlings (cv. Rio Grande) were transplanted into 20 cmdiam. plastic pots filled with 2.5 kg of soil. After 45 days,the plants were washed free of soil and the number of gallson each counted. The number of galls ranged from 23 to33 per plant, with no significant differences between ex-perimental units (Tukey, P = 0.05). Thus, the distributionof the inoculum in the soil was considered to be accept-ably uniform. A second set of samples, taken in the sameway as the first but to a depth of 30 cm, allowed a soilphysico-chemical analysis to be made and the optimumnutrient application required for the crop to reach a poten-tial production of 30 tonnes ha−1 to be calculated (Etchev-ers et al., 1994). From this analysis, the fertilisation for-mula 210-88-00 (kg ha−1 N, P, K) was determined. Thenitrogen was added in three doses: at transplanting, andat 45 and 75 days after transplanting (dat). Phosphoruswas added only at transplanting. The three managementschemes were established in a randomised block designwith four replications. Plots, consisting of six ridges (each1 m wide by 12 m long), were planted with 1-month-oldtomato seedlings of cv. Rio Grande, of the Saladette type.The IC treatment consisted of application of the calcu-lated dose of fertiliser as described before; ethoprop gel(68% Mocap®) was applied at 7 kg active substance (a.s.)ha−1 in a band 10 cm from the plants, after a light irriga-tion, at transplanting and 20 dat; and 10 ton ha−1 of ho-mogenised, matured (i.e., allowed to stand for 12 monthsbefore use) chicken manure was applied in a band at thebase of the furrow 30 days before transplanting. The lat-ter supplemented chemical fertilisation and improved soilstructure and may bring about a nematode suppressive ef-fect (Mankau, 1962, 1963; Handelsman & Stabb, 1996).The TC scheme consisted of the best local practices andincluded use of fertiliser (150, 100 and 100 kg ha−1 of N,P, K, respectively) and 1 l ha−1 of carbofuran 27.5% (Fu-radan 300 T®) applied to plants at 15, 30 and 60 dat. Forthe check treatment (AC), no nematicides and no chem-ical or organic fertilisers were used as crops are some-times grown under these conditions in this area, and sucha treatment would provide a clear demonstration of thebenefits of nematode management strategies under suchconditions. Cultural practices and control of other pestsand pathogens were carried out according to conventionallocal methods for all three management strategies.
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CROP VIGOUR AND PRODUCTION AND NEMATODE
COUNTS
Every 10 days for 15 weeks, four plants were takenfrom the outer rows of each plot. A single randomlyselected plant from the four that were taken was usedto determine the population density of nematodes inthe roots. After roots had been washed, cut into 1 cmsections and thoroughly mixed, a 1 g subsample perplant was blended and the third- (J3) and fourth-stagejuveniles (J4) and the obese females within it werecounted. Determination and counting of the stages ofthe nematode were made at a magnificaction of 40×using a stereomicroscope. The numbers of galls per plantwere counted and the data used as an estimate of diseaseincidence through the crop season (McSorley, 1987). Atthe same time as taking plant samples, soil samplesconsisting of ten cores were taken midway between plantsfrom the outer rows to a depth of 20-30 cm (totalling500 g of soil/replicate). The procedures described byAyoub (1980) were employed to extract the nematodesfrom soil and roots. The sieving flotation-centrifugationtechnique was used to extract second-stage juveniles (J2),J3 and J4 from 200 ml of soil per sample (using sieves ofmeshes 212, 106, 53 and 30 µm). Soil temperature wasmeasured at a depth of 20 cm during the development ofthe crop using Tiny Talk Temperature Loggers® (Gemini,Chichester, UK) (Manzanilla-López, 1997).
Fifteen plants, selected at random from the two cen-tral rows of each plot at harvest time, were used to esti-mate crop vigour and yield by measuring the followingvariables: plant height, foliage dry weight, stem diame-ter, total production, and commercial production. The datawere subjected to analyses of variance and comparison ofmeans using Tukey’s HSD test (P = 0.05; Steel & Torrie,1986).
EPIDEMIC CHARACTERISATION AND STATISTICAL
ANALYSIS
The numbers of galls per plant and of obese females perg of root that were estimated every 10 days were used tomodel the disease progress curve and population densityover time. The area under the disease progress curve(AUDPC) was calculated using the trapezoidal integrationmethod (Campbell & Madden, 1990), and the rate ofapparent infection was estimated as the b−1 parameterof the Weibull model, in which Y (disease incidence) =1 − e{−(t/b)c}, where e is the base of natural logarithms,t is the time measured in days, b is the reciprocal of the
rate of disease increase, and c is an index determinedby the shape of the curve (Pennypeker et al., 1980;Thal et al., 1984). The AUDPC and b−1 parameter wereused as estimators of epidemic intensity based on thenumber of galls per plant. In both cases, the estimatorswere obtained using SAS procedures (Anon., 1988). Forthe b−1 parameter, a non-linear procedure (NLIN) andDudd algorithms were used. The AUDPC and b−1 werealso calculated based on the population curves of obesefemales (density per g of root). The numbers of galls perplant evaluated at the last commercial harvest were used toestimate the final disease incidence (Yf ). The parametersAUDPC, b−1 and Yf were subjected to analysis ofvariance followed by a multiple comparison of meansusing Tukey’s HSD test (P = 0.05).
PRODUCTION LOSS MODELS
Models were built using a multiple regression of theform: Y = b0 + b1x1 + b2x2 + b3x3 + bnxn, whereY is the commercial yield (i.e., fruit of marketablequality), b0 is the intercept parameter or ‘theoreticalproduction’ sensu Zadoks and Schein (1979), and b1
to bn are parameters that estimate the effect of gallincidence on fruit production measured at different stagesof crop phenology. Gall incidence, x1−n, was measuredon different dates, beginning 10 days after transplantingand continuing up to the last harvest. By reference to thedegree of galling of the plants in the AC treatment, therelative percentage incidence of galling in each treatmenton each date was calculated and also used to estimatemodel parameters.
A multiple point model (Madden, 1983; Teng, 1984;Campbell & Madden, 1990) was constructed using gallincidence during crop growth to estimate epidemic inten-sity at specific stages of crop phenology (Duncan & Fer-ris, 1983; Noling, 1987). A matrix of 12 observations, theresult of averaging the disease incidence and yield of 15plants per plot, was used to build the model, which con-sisted of the commercial (i.e., marketable) yield as thedependent variable (Y ) and ten incidence measurementsover time as independent variables (x1−10) per treatmentand replicate. Percentage data were transformed for nor-mality by taking the arc-sin of the square root (Steel &Torrie, 1986). The Stepwise method of the GLM (gener-alised linear model) procedure of SAS (1988) was usedto adjust the models, selecting those that satisfied a rel-atively high R2, and also based on the general signifi-cance of the model and where the number of parame-
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Fig. 1. Population densities of juveniles of Nacobbus aberrans on tomato (Lycopersicon esculentum cv. Rio Grande) under three controlschemes. A: Second-stage juveniles (J2) per 200 ml of soil; B: Third- and fourth-stage juveniles (J3 and J4) per 200 ml of soil. IC =Integrated Control, TC = Technical Control, AC = Check.
ters (p) gave a Cp-Mallow ≈ p, which gives the modelgood stability when used predictively (Freund & Littell,1991).
Results
POPULATION DENSITY
The population density of the nematodes in the soiland roots fluctuated during the cultivation cycle in all ofthe treatments (Figs 1, 2). Three overlapping generationsof N. aberrans can be identified through the cultivationcycle. These correspond approximately to the periods0-60, 60-100, and 100-130 dat, periods that show differentpeaks of juveniles in soil and roots (Figs 1A, B; 2A) andobese females in roots (Fig. 2B). Although some J3 andJ4 were detected in soil as early as the first day aftertransplanting the crop, the J2 numbers peaked at 20, 75, 95and 115 dat (Fig. 1A), while the J3 and J4 numbers peaked
at 20, 80 and 100 dat (Fig. 1B). Blended root samplesshowed that the J3 and J4 were abundant (>100 g−1
root) in the AC at 20 dat (Fig. 2A). Population peaks ofobese females (Fig. 2B) occurred at 30, 70-80 and 110dat. All of the treatments showed a decrease in numbersof nematodes in soil and roots at the end of crop growth(Figs 1, 2).
CHARACTERISATION OF EPIDEMICS
The general trend was of peaks in the numbers of obesefemales and galls starting at 20 dat (Figs 2B; 3). The finalphases of the first and second generations of the nematodepopulation produced increments at 70 and 90 dat. Thesepeaks, particularly for the numbers of galls, were lower inthe IC (Fig. 3).
The b−1 parameter of the Weibull disease progressmodel explained at least 94% of the experimental varia-tion during 0-50 dat (Table 1). The fit for the completedisease cycle (110 dat) was poor (r2 � 0.62) because
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Fig. 2. Nacobbus aberrans population densities on tomato roots (Lycopersicon esculentum cv. Rio Grande) under three control schemes.A: Third- (J3) and fourth- (J4) stage juveniles per g of root; B: Obese females per g of root. IC = Integrated Control, TC = TechnicalControl, AC = Check.
of the peaks of damage mentioned above (Table 1). Inaddition, the AUDPC and Yf were calculated, so allow-ing us to define the intensity of the epidemics for thewhole cultivation cycle. The IC treatment showed a lessintense epidemic than the other treatments according toall of the models (P = 0.05), whilst the AC treatmenthad the highest epidemic intensity (Table 2). The AUDPCfor the numbers of obese females/g of root also showedthat IC allowed nematode development but that this treat-ment achieved the greatest degree of control (P = 0.05)(Table 2).
EFFECTS OF TREATMENTS ON VIGOUR AND CROP
PRODUCTION
The beneficial effects of IC resulted in greater plantvigour throughout crop development as estimated fromplant height, foliage dry weight, and stem diameter (P =
0.01) (Fig. 4). In reducing epidemic intensity, the ICtreatment increased plant height by 41 and 49.6%, foliagedry weight by 36.9 and 53.1%, and stem diameter by31.1 and 41% with respect to the TC and AC treatments,respectively. TC exceeded AC in plant height and foliagedry weight, but not in stem diameter (P = 0.05) (Fig. 4).
Similar total yields were obtained in treatments IC andTC, which exceeded AC by 78.7 and 74.7%, respectively(P = 0.05) (Fig. 5). However, marketable productionin IC exceeded that in TC and AC by 33.9 and 82.0%,respectively, and TC exceeded AC by 72.8%.
PRODUCTION LOSS MODELS
The best multiple point model for calculating commer-cial production loss caused by N. aberrans on the tomatocv. Rio Grande, was Y = 15.505 − 0.045 × 4 − 0.045 ×5 − 0.024 × 6, which had an R2 of 0.83 (P < 0.05) and a
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Fig. 3. Partial temporal progress curves of disease on tomato, Lycopersicon esculentum cv. Rio Grande (up to 50 days aftertransplanting), caused by Nacobbus aberrans (values are means of four replicates per treatment). IC = Integrated Control, TC =Technical Control, AC = Check.
Table 1. Nacobbus aberrans epidemics on tomato (Lycopersicon esculentum cv. Rio Grande) under three different control schemes.Coefficient of determination (r2), mean square of error (MSE) and apparent infection rate (b−1) values for partial epidemics (50 daysafter transplanting) and complete epidemics (110 days after transplanting) as estimated by the Weibull model.
Treatment Replicate Weibull model
50 days after transplanting 110 days after transplanting
IC = Integrated Control; TC = Technical Control; AC = Check; r2 = coefficient of determination; MSE = mean square of error(variance) of the estimated apparent infection rate; b−1 = progress of apparent infection rate obtained from the reciprocal of the b
parameter of the Weibull model.
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Table 2. Effect of control schemes on three parameters of the temporal progress of disease on tomato (Lycopersicon esculentum cv. RioGrande) caused by Nacobbus aberrans in Tecamachalco (Mexico).
Disease parameter Number of galls per plant Females per g of root
IC TC AC IC TC AC
Yf (%) 64.0 b 71.0 a 71.0 a – – –b−1 0.039 b 0.085 a 0.083 a – – –AUDPC 1525 b 2830 a 3263 a 1282 c 2733 b 3220 a
Yf = Final incidence (110 days after transplanting); b−1 = rate of apparent infection (reciprocal of the b parameter of the Weibullmodel) 50 days after transplanting; AUDPC = area below the disease progress curve 110 days after transplanting; IC = IntegratedControl; TC = Technical Control; AC = Check.
Note: numbers with the same letters in the same row are not significantly different (Tukey, P = 0.05).
Fig. 4. Tomato (Lycopersicon esculentum cv. Rio Grande) vigour estimates under three control schemes for Nacobbus aberrans. IC =Integrated Control, TC = Technical Control, AC = Check. Bars with the same letter are not significantly different (Tukey, P = 0.05).
Cp of Mallow of 6.38. In this model, Y corresponds to theestimated production and ×4, ×5, and ×6 represent theestimates of damage (i.e., degree of galling) caused by thenematode at 40, 50, and 60 dat, coinciding with the pheno-logical periods of flowering, fruit initiation, and fruit set,respectively (Fig. 3). From this model, the theoretical pro-duction (sensu Zadoks & Schein, 1979) was estimated, fora damage level equal to zero, at 1.03 kg plant−1. From thisestimate and with a sowing density of 20 000 plants ha−1,a theoretically achievable yield of 20 673 kg ha−1 was cal-culated.
The experimental treatments produced average totalyields of 0.991 kg plant−1 (18 253 kg ha−1), 0.729 kgplant−1 (14 593 kg ha−1) and 0.174 kg plant−1 (3497 kg
ha−1) in IC, TC and AC, respectively. Thus, the estimatedproduction losses on tomato caused by N. aberrans, cal-culated from the theoretical maximum possible produc-tion and the average production achieved with the dif-ferent treatments, were 0.121 kg plant−1 (2420 kg ha−1)
with IC, 0.304 kg plant−1 (6080 kg ha−1) with TC and0.858 kg plant−1 (17 176 kg ha−1) with AC, which corre-spond to 11.7, 29.4 and 83.1%, respectively.
Discussion
There are few studies of disease progress and yield losscaused by N. aberrans (Manzanilla-López et al., 2002).Otazú et al. (1985) determined the progress curve of N.
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Fig. 5. Effects of three different systems of management of Nacobbus aberrans on the production of tomato cv. Rio Grande. IC =Integrated Control, TC = Technical Control, AC = Check. Bars with the same letters are not statistically different (Tukey, α = 0.05).
aberrans infection on potato during the growing season.However, the present work is the first report of the useof epidemiological models and management schemes toestimate production losses due to N. aberrans on tomatocrops under field conditions. Others have made estimatesbased on different treatments under glasshouse conditions(Costilla & Gómez, 1981) or on the traditional criteriaof chemical control based mainly on different dosagesof nematicides and intensity of control (Zamudio, 1987;Franco et al., 1993a, b). The critical period for controllingthe nematode is during its first generation (0-60 dat),and the damage in our experiment was estimated best bymeasuring the damage caused by N. aberrans between 40and 50 dat, i.e., when the crop is at the stage of floweringand fruit initiation.
The decrease in numbers of nematodes in soil androots at the end of crop growth found in all treatmentsis a behaviour already reported by Gómez (1991) andCid del Prado et al. (1996a). This phenomenon seemedto be due to the decline of the crop, the consequentdisintegration of the roots, and the invasion of secondarydisease organisms, such that less nutritious tissue wasavailable for the nematodes. The first peak of obesefemales corresponded to the inoculum of J3 and J4 andimmature females already present in the field beforethe crop was transplanted and responsible for the gallsthat developed on the plants in the bio-assay. Figure1B clearly shows the presence of J3 and J4 in the soil
at transplanting, a feature reported previously for thispathosystem (Manzanilla-López, 1997).
More generations may occur immediately if alternativecrop hosts or weeds follow a tomato crop (Cid del Pradoet al., 1996b, 1997). Also, it has been observed thatthe nematode is able to survive without any host forat least one year under field conditions as J3 and J4(Cristóbal-Alejo et al., 2001b). These two stages cantolerate gradual dehydration over 15-30 days (Manzanilla-López & Pérez-Vera, 1999) and host absence for up toa year (Manzanilla-López, unpubl.) better than other lifestages. This may explain why, at the time of transplanting,only J3 and J4 (4-6 nematodes/200 ml) were found in thesoil (Fig. 1B), despite efforts to recover J2 through sievingtechniques. Thus, from the present work, it seems that J3and J4 represent the main inoculum for the progress ofepidemics, and this is the first report that demonstrates theimportance of these juvenile stages under field conditions.These stages must, therefore, be the principal target for thepurposes of achieving an effective control of crop damageand management of the nematode.
The chemical control in IC at the begining of the cropseason was presumably the cause of the lowered peak innumbers of J2 (Fig. 1A), thereby reducing the impact ofthe initial inoculum of the nematode and helping to reducethe numbers of the first generation of obese females (Figs2B; 3).
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The overall beneficial effects of IC must have been dueto the two main components (i.e., nematicides and fertilis-ers, both chemical and organic), which influence the ef-fective initial inoculum (estimated through Y0) by reduc-ing nematode densities and also improve host nutrition.Later, IC also reduced the values of the epidemic intensityparameters (AUDPC, b−1, and Yf ). The positive effectsof addition of chicken manure might be at least partlydue to their restrictive effect on nematode development(Rodríguez-Kábana, 1986; Zavaleta-Mejía, 1986). How-ever, as with other types of amendment, it is important tostudy the effects of the amendment on various physico-chemical processes in the soil and on soil pH (Etcheverset al., 1989). Its effects on nematode antagonistic organ-isms (Mankau, 1962, 1963; Wallace, 1983) and the opti-mum period of application could also be important. Theapplication of nematicide in this experiment, especiallyat the time of transplanting, did reduce the initial inocu-lum, but it would be informative to study the frequency ofapplication, dose, and alternative chemical products, andto make cost-benefit analyses, to determine the most ef-fective strategy (Chew, 1995; Barker & Koenning, 1998;Yáñez et al., 2001).
Conclusions
Epidemiological models to assess disease progress havebeen built for few species of plant-parasitic nematodes.This is partly due to the lack of studies that includedata on nematode population dynamics related to cropphenology, and this is especially true for Nacobbus. Inthe present study, information has been generated on thepopulation dynamics of N. aberrans on tomato plantsunder field conditions in a comparison of treatmentsdesigned to increase production and to reduce the effectof the nematode on yield. At least three generationsof N. aberrans seemed to occur through the croppingseason and J3 and J4 were the main inoculum for theprogress of epidemics. The critical period for controllingthe nematode is probably during the first generation(0-60 dat).
The epidemiological models for the disease causedby the nematode on tomato crops, revealed that thenumber of galls per plant and females per g of rootthrough the crop season were the most practical andsuitable variables for definition of the area under adisease progress curve (AUDPC). The variables b−1
(Weibull’s apparent infection rate), AUDPC and Yf (finaldisease incidence) indicated less crop damage under
the IC scheme than under the other two schemes (TCand AC) (P = 0.05). However, comparison with ACalso showed that chemical control only reduces thenumbers of nematodes for a short period without exertingpermanent control. Therefore, this could still permit amajor loss in production but, by using the additionalmeasures included in IC, such large losses are avoided,thus diminishing the impact of the disease (Chávez,1995; Chew, 1995; Cid del Prado et al., 1997). Theepidemiological approach used in the present study helpedto assess the impact of the different control practices andtheir potential for increasing production and reducing thenematode population in infested soils. The results shouldhelp in planning and implementing improved controlstrategies. The IC programme would allow the disease tobe managed in a sustainable production system and toincrease crop yield (Téliz, 1992) in infested soils, thusreducing the area of land abandoned by small farmersbecause of infestation of the soil by N. aberrans and theconsequent poor crop yields.
Acknowledgements
The first author thanks CONACYT (Mexico) for finan-cial support through the development of the research, andManuel Rodríguez, the cooperating farmer. RothamstedResearch receives grant-aided support from the Biotech-nology and Biological Sciences Research Council of theUnited Kingdom.
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