Ebook Plant Nematology (2nd edition): Part 2

Continued part 1, part 2 of ebook Plant Nematology (2nd edition) provide readers with content about: quantitative nematology and management; plant growth and population dynamics; distribution patterns and sampling; international plant health – putting legislation into practice; biological and cultural management; nematode resistance in crops; genetic engineering for resistance; chemical control of nematodes;...

10 Plant Growth and Population Dynamics* CORRIE H SCHOMAKER** AND THOMAS H BEEN Wageningen University and Research Centre, Plant Research International, The Netherlands and Biology Department, Ghent University, Belgium 10.1 10.2 10.3 10.4 10.5 10.6 10.7 10.8 10.9 Introduction Relationships of Nematodes with Plants Predictors of Yield Reduction 10.3.1 Symptoms 10.3.2 Pre-plant density (Pi) 10.3.3 Multiplication Different Response Variables of Nematodes Stem Nematodes (Ditylenchus dipsaci) Root-invading Nematodes 10.6.1 A simple model for nematode density and plant weight 10.6.2 Mechanisms of growth reduction 10.6.3 T and m as measures of tolerance 10.6.4 Growth reduction in perennial plants Effect of Nematicides 10.7.1 Nematistatics (= nematistats) 10.7.2 Contact nematicides Validation of the Model Population Dynamics 10.9.1 Nematodes with one generation per season 10.9.2 Nematodes with more than one generation 10.9.3 The effect of nematode damage and rooted area on population dynamics 10.9.3.1 Resistance 10.9.3.2 Population decline in the absence of hosts 302 302 303 303 304 304 305 305 307 309 311 312 315 319 319 321 321 322 323 324 325 326 329 * A revision of Schomaker, C.H and Been, T.H (2006) Plant growth and population dynamics In: Perry, R.N and Moens, M (eds) Plant Nematology, 1st edn CAB International, Wallingford, UK ** Corresponding author: corrie.schomaker@wur.nl © CAB International 2013 Plant Nematology, 2nd edn (eds R Perry and M Moens) 301 10.1 Introduction The main purpose of quantitative nematological research is to achieve an optimal economical protection of crops against plant-parasitic nematodes To accomplish this, the costs of control measures must be adjusted to the costs of the expected yield reduction compared to the yield in a situation without the need for control Such an adjustment requires quantitative knowledge of: The relationship between a measure for the nematode activity (in practice mostly their population density at the time of planting) and plant response The population dynamics of nematodes in the presence of food sources (of different quality) and in the absence of food The effect of control measures on plant response and nematode population dynamics The control measures may range from pesticide treatment, crop rotation and cultivation of crops that vary in suitability as a food source for nematodes Cost/benefit of the control measures 10.2 Relationships of Nematodes with Plants The majority of species of plant-parasitic nematodes live on or around plant roots (see Chapter 8) Nematode species can be divided into four types according to the plant parts they infest: (i) species that form galls in ovaries and other above-ground plant parts, e.g Anguina tritici in wheat; (ii) leaf nematodes (Aphelenchoides) infesting leaf buds and causing malformations and necrosis in leaves of many ornamental plants and in strawberries; (iii) stem nematodes (Ditylenchus dipsaci) causing malformations, swellings, growth reduction and dry rot in above- and underground parts of plant stems such as onions, bulbs, rye, wheat, beet, potatoes and red clover; and (iv) root nematodes causing growth reduction in whole plants and malformations in underground plant parts (Meloidogyne spp., Rotylenchus uniformis), root necrosis and growth reduction (Pratylenchus penetrans, Tylenchulus semipenetrans) or growth reduction without any symptoms (Globodera rostochiensis, G pallida, Tylenchorhynchus dubius) In most cases of infestations by stem and root nematodes, the nematodes were already present in the soil at the time of planting Damage in red clover and lucerne often is the result of seed infested with stem nematodes Stem nematodes introduced into a field with infested onion seed are not known to reach densities that are high enough to cause immediate visible infestations The introduction of nematodes on planting material such as bulbs and tubers and the spread of nematodes by machinery and other vectors is discussed in detail in Chapter 11 Bursaphelenchus cocophilus in coconut and oil palm and B xylophilus in various pine species are unusual Both are transmitted by a beetle In fact, several species of beetle support the life cycle of B xylophilus: pine sawyer beetles (Monochamus spp.) transport the nematodes to the pine trees where they feed on blue stain fungi Bark beetles help to introduce the blue stain fungi into the trees and thus allow the nematodes to feed and multiply Bursaphelenchus xylophilus (and possibly one or two other species) can feed on live trees as well as fungi 302 C.H Schomaker and T.H Been 10.3 Predictors of Yield Reduction 10.3.1 Symptoms Figure 10.1 gives some examples of visible symptoms of nematode infestations Some of them are very conspicuous but others are hardly visible In some cases visible symptoms in plants can be used as a measure of yield reduction For example, symptoms of nematode infestations in above- and underground parts of the stem are often easy to recognize, and yield reduction is closely related to the extent of the phenomena Some root nematodes inflict conspicuous deterioration in roots or underground plant parts: Meloidogyne spp cause root knots, and species of Longidorus and Xiphinema are responsible for bent, swollen root tips If these plant parts are marketable products, the symptoms are closely related to yield reduction If not, the relationship between symptoms and yield is much more complex A B C D E F Fig 10.1 Visual symptoms of nematode attack A: Meloidogyne incognita on tomato roots B: Ditylenchus dipsaci in onions C: Deformations in potatoes caused by Pratylenchus spp D: Meloidogyne in carrots E: Meloidogyne in table beets F: Deformation in sugar beet caused by trichodorids Plant Growth and Population Dynamics 303 By contrast, other nematode species cause hardly any specific or recognizable symptoms and yet reduce yields severely For example, P penetrans causes root necrosis, and low to medium numbers of cyst nematodes, T dubius, R uniformis, Helicotylenchus spp., P crenatus and P neglectus cause no, or hardly any, symptoms, yet these species can cause considerable growth reduction in the plants they attack Longidorus elongatus in some cases causes swollen root tips and a smaller root weight, but does not affect the above-ground plant parts Therefore, in general, visible symptoms of nematode infestation can seldom be used as a measure for growth and yield reduction 10.3.2 Pre-plant density (Pi) Only leaf and bud nematodes and Bursaphelenchus spp can multiply fast enough to cause considerable damage very shortly after the first infection, even at very low densities For these species, damage or yield reduction is almost independent of the numbers of nematodes at the time of planting (Pi) To control these nematodes, all sources of infection, such as infested plants, must be removed and breeding material must be free from nematodes By contrast, the multiplication of most root nematodes is relatively slow, even on good hosts Root nematodes only cause yield reduction when harmful densities are already present in the soil at the time of planting of a sensitive crop On a small scale, root nematodes are distributed in the soil according to a negative binomial distribution with an aggregation coefficient (k) larger than 40 for most nematode species This distribution is regular enough to assume that growing plant roots are continuously exposed to the attack of a nematode population with about the same density and, therefore, that the growth of annual plants (or the growth of perennial plants during the first year) is retarded at a constant rate 10.3.3 Multiplication Nematode damage to plants can have some influence on nematode multiplication but only when large nematode densities reduce the food source (often the root system) in sensitive plants Conversely, multiplication of nematodes is of little importance to the growth and yield reduction they cause; the same amount of yield reduction may occur in resistant (non-host) and susceptible plants Examples are G pallida and G rostochiensis, causing the same damage in resistant and susceptible potato cultivars (Fig 10.2), Meloidodyne naasi and M hapla damaging beet during the first months after sowing, and damage by stem nematodes in flax, yellow lupin, maize and sun spurge In these latter crops, marked yield reductions or growth aberrations have been found without any nematodes being detected in the plants Therefore, the host status of a plant and its susceptibility to damage must be treated as independent qualities The reason for this independence is that only a very small part of the damage caused by nematodes is caused by food withdrawal from host plants and the main part by the biochemical and mechanical disruptions that nematodes bring about in plants 304 C.H Schomaker and T.H Been Tuber dry weight (t ha–1) 16 12 0.0 0.1 1.0 10.0 Pi (juveniles g–1 soil) Observations Bintje Observations Santé 100.0 1000.0 Model Bintje; m = 0.43 Model Santé; m = 0.43 Fig 10.2 The potato cultivars Bintje (susceptible) and Santé (resistant) were grown in a field infested with Globodera pallida Although the yield potential of Santé (11.9 t ha−1) is greater than that of Bintje (10.6 t ha−1), the effect of the nematodes on tuber dry weight is the same: both cultivars have a relative minimum yield (m) of 0.43 and a tolerance limit T of 18 juveniles g−1 of soil (L Molendijk, unpublished data.) 10.4 Different Response Variables of Nematodes Crop returns are reduced by nematode attack as a result of reduction of crop weight per unit area, which is mostly equivalent to average weight of marketable product per plant, and reduction of the value of the product per unit weight For example, carrots attacked by root-knot nematodes (Meloidogyne spp.) may be worthless because of branching and deformation of the taproot (Fig 10.1D), although they have the same weight per unit area as carrots without nematodes Onions of normal weight but infected with a few stem nematodes (D dipsaci) at harvest will, nevertheless, be lost in storage Attack of potatoes by G rostochiensis and G pallida not only reduces potato tuber weight but also may reduce tuber size However, small and medium densities of potato cyst nematodes attacking potatoes and almost all root-infesting nematodes attacking crop plants of which the above-ground parts are harvested, hardly ever affect the value per unit weight of harvested product Therefore, prediction of crop reduction by these nematodes can, in general, be based on models of the relation between nematode density at planting (Pi) and average weight of single plants (y) at harvest In the following sections, the term ‘yield’ will be avoided The yield in the agronomic sense must be derived from individual plant weights 10.5 Stem Nematodes (Ditylenchus dipsaci) To construct a model of the relationship between initial population density (immediately before planting), Pi, and the proportion, y, of uninfected plants (onions, flower Plant Growth and Population Dynamics 305 bulbs), a theory is required concerning the mechanisms involved The theory has to be translated into a mathematic model so that it can be tested In fact, a mathematical analogue of the theory is formulated To test or validate the mathematical model (and the theory), it is compared with mathematical patterns that are distinguishable in data derived from observations At the same time, the values of system parameters are estimated under various experimental conditions Pi and y are called system variables because they have different values in each experiment, in contrast to system parameters, which are constants They have only one value in a certain experiment but they can vary between experiments because of changes in external conditions Seinhorst (1986) presented a competition model for the relationship between stem nematode densities (Pi) and the proportion of infested onion plants As only nematode-free onions are marketable and the degree of infestation of single plants is irrelevant, only infested and non-infested onions were distinguished To formulate the model, three assumptions were needed: The average nematode is the same at all densities This means that initial population density (Pi) does not affect the average size or activity of the nematodes Nematodes not affect each other’s behaviour They not attract or repel each other directly or indirectly Nematodes are distributed randomly over the plants in a certain small area It is postulated that at Pi = a proportion d of the onion plants is infected and that, therefore, a proportion − d is left non-infected Then, at density Pi = 2, a proportion d of already damaged plants is attacked (which has no additional effect as onions, once attacked, are worthless), plus a proportion d of the still non-infected proportion (1 − d) So at Pi = a proportion d + d(1 − d) onions is attacked and – d − d(1 − d) = (1 − d) − d(1 − d) = (1 − d)2 of the plants is left non-infected At Pi = 3, again a proportion d of already damaged onions is damaged, which has no effect, and a proportion d of the non-infected plants (1 − d)2 is attacked Summing it all up, we see that at Pi = the proportion of infected onions amounts to d + d(1 − d)2 and that the proportion of non-infected onions is – d − d(1 − d)2 = (1 − d) – (1 − d)2 = (1 − d)3 Schematically: Population density, Pi = Proportion of infected onions Proportion of non-infected onions P d d + d(1 − d) d + d(1 − d) + d(1 − d)2 1−d − {d + d(1 − d)} = (1 − d)2 − {d + d(1 − d) + d(1 − d )2} = (1 − d)3 (1 − d)P In general: a nematode density Pi = P leaves a proportion y = (1 – d)P = zP (10.1) of the onions non-infected In Eqn 10.1 P is an integer, y is a variable (like Pi) and z is a parameter The parameter z must be estimated The expected value of z and its variance must be estimated in field experiments; the population density Pi can be estimated by taking soil samples with an appropriate sampling method (see Chapter 11) In Fig 10.3 values of y (= zPi) are plotted for three different values of z The values of y are not plotted against Pi, but against log Pi This log-transformation of Pi not 306 C.H Schomaker and T.H Been 1.2 1.0 Yield (y) 0.8 0.6 0.4 0.2 0.0 0.1 10 100 Initial population density P (juveniles g–1 soil) z = 0.99 z = 0.97 1000 z = 0.95 Fig 10.3 Yield relation for stem nematodes according to equation y (= z Pi) with three different values for z (z = 0.99, 0.97 and 0.95) The smaller z, the greater the activity of the nematodes and the smaller the yield only has the advantage that the shape of the curves is the same for all z, but also that, if Pi is estimated by counting nematodes from a soil sample, the variance of log Pi is constant (and independent of Pi), provided that Pi is not very small The value of the parameter z is determined by conditions that influence the efficiency of nematodes in finding and penetrating plants In patchy infestations of stem nematodes these conditions for attack appear to be more favourable in the centre of the patch than towards the borders This results in an increase of z with increase of the distance from this centre and, thus, in persistency of the patchiness The model also applies when nematodes spread from randomly distributed infested plants to neighbouring ones, leading to overlapping patches of infested plants 10.6 Root-invading Nematodes Root-knot nematodes, Pratylenchus spp and cyst nematodes are considered to be the most important tylench root-invading nematodes Although some of these nematodes, especially root-knot nematodes, can also inflict qualitative damage in underground plant parts, they generally reduce crop yield in a less direct way than stem nematodes Often there are no visible symptoms Only the rate of growth and development of attacked plants is reduced, resulting in lower weight compared to plants without nematodes To put it simply: in plants with nematodes the same thing happens later In exceptional cases, nematode-infested plants reach the same final weight as plants without nematodes, but at a later stage In general, such a delay results in ripening of the crop being prevented by external conditions at the end of the plant growing season Plant Growth and Population Dynamics 307 Seinhorst (1986) based a growth model on two simple concepts: (i) the nature of the plant (an element that increases in weight over time); and (ii) the nature of the plant-parasitic nematode (elements that reduce the rate of increase of plant weight and, in principle, the more so the larger the population density) To formulate the model for root nematodes three extra assumptions must be added to those made for stem nematodes (Section 10.5): Root-infesting nematodes are distributed randomly in the soil Nematodes enter the roots of plants randomly in space and time Therefore, the average number of nematodes entering per quantity of root and time is constant This number is proportional to the nematode density P (number of nematodes per unit weight or volume of soil) The growth rate of plants at a given time t after planting is the increase in total weight per unit time (dy/dt) Let this growth rate be r0 for plants without nematodes and rP for plants at nematode density P According to Fig 10.4, r0 = tan(a) = Dy/Dt0 and rP = tan(b) = Dy/DtP Thus, for plants of the same total weight (and, therefore, of different age) with nematode density P and without nematodes, the ratio rP /r0 is constant during the growing period Therefore, rP /r0 = t0/tP (10.2) Weight (y) The relationship between population density of the nematodes and its total effect on the growth rate of the plants accords with Eqn 10.1 Equation 10.1 is a continuous function for £ P £ ¥ There is one complication: all accurate observations on the relationship between the population density P of various nematode species and weight of various plant species indicate that there must be a maximum density, T, Δy α β Δt0 ΔtP Δy Time (t) Without nematodes With nematodes Fig 10.4 Growth curves of plants without nematodes and with nematodes at density P; y = plant weight and t = time after planting The variables t0 and tP are the times that plants without nematodes and at density P need to reach the same total weight y, respectively; r0 = tan(α) = Δy/Δt0 and rP = tan(β) = Δy/ΔtP are the growth rates of plants without nematodes and at nematode density P, respectively 308 C.H Schomaker and T.H Been below which the nematodes not reduce plant weight Therefore, Eqn 10.1 is adapted by replacing P by P − T and we have to deal with a discontinuous function In practice the transition between P > T and P £ T will be smoother than it is in theory Further, only in very few experiments were large nematode densities able to reduce plant weight to zero, whilst growth rates of attacked plants were never reduced to zero Therefore, a second adaptation in Eqn 10.1 was the introduction of the minimum relative growth rate k = rP/r0 for P → ¥ The equation constituting the growth model for plants attacked by root nematodes then becomes: rP/r0 = k + (1 – k) · zP–T for P > T rP/r0 = for P £ T (10.3) and T, z and k are parameters (constants); rP, r0 and P are variables The parameters z and k are constants smaller than The value of the parameter k is independent of nematode density and time after planting but may vary between experiments Growth curves of plants for different nematode densities can be derived from a growth curve of plants without nematodes with the help of Eqns 10.2 and 10.3 These curves may vary in shape but they must answer two conditions: (i) they must be continuous; and (ii) the growth rate must decrease continuously from shortly after planting The frequently used logistic growth curve complies with these conditions Figure 10.5 gives an impression of the three-dimensional model with axes for total plant weight y, relative nematode density P/T and time t after planting From the model it can be deduced that nematodes reduce growth rates of plants by the production of a growth-reducing substance only during penetration in the roots but not when they have settled This hypothesis is supported by Schans (1993), who observed stomatal closure in potato plants infested by G pallida during the time of penetration and concluded that disturbance of cell development just behind the root tips interferes with the production of abscisic acid, which is known to act as a messenger for stomatal closure Because of the constant number of nematodes penetrating per unit quantity of root and per unit duration of time, the growth-reducing stimulus will then remain constant per unit weight of plant For nematodes that not move once they have initiated a feeding site within the root, such as root-knot and cyst nematodes, zP can be interpreted as the proportion of the food source that is left unoccupied by nematodes at density P For species that are mobile during their whole life cycle, − zP is a measure of the ratio between the feeding times at density P and the maximum feeding times at P → ¥ Therefore, − zP is proportional to a hypothetical growth-reducing substance that nematodes bring into the plants during penetration The parameter k means that nematodes cannot stop plant growth completely and that, even at very large nematode densities, some growth is left: rP/r0 = k 10.6.1 A simple model for nematode density and plant weight The model described in Section 10.5 makes good biological sense but is not easy to use in everyday nematological practice The primary results of experiments are almost Plant Growth and Population Dynamics 309 A 70 Plant dry weight (y) 60 50 40 30 20 10 Time (t ) in weeks B C 70 16 33 Pi (juveniles g–1 soil) 70 60 60 50 50 Plant dry weight (y) Plant dry weight (y) 70 148 314 665 40 30 20 30 20 10 10 40 0 Time (t in weeks) 20 55 148 403 Pi (juveniles g–1 soil) Fig 10.5 Surface plots of the three-dimensional model (Eqns 10.2 and 10.3) representing the relation between weight, the relative nematode density P/T and time t after planting: A, at 230 degrees rotation; B, at degree rotation, showing the relation between plant weight and t at different nematode densities; C, at 270 degrees rotation, showing the relation between plant weight and Pi always weights of plants attacked by known nematode densities at a given time after sowing or planting To investigate whether these relationships are in accordance with the growth model, they must be compared with cross-sections orthogonal to the time axis (Fig 10.5), through growth curves of plants for ranges of densities P/T and different values of k If we describe these cross-sections mathematically, they appear to be in close accordance with Eqn 10.4: y = m + (1 – m) · zP–T for P > T y=1 for P £ T 310 (10.4) C.H Schomaker and T.H Been ... 1.46 2. 68 1 .22 1.10 1.46 1.83 0 .24 0.49 12. 15 11.99 11.18 11. 02 9 .24 5.61 2. 66 1.06 s2tot = 19.45 12. 48 12. 48 12. 47 12. 46 12. 41 12. 39 12. 36 12. 29 12. 22 12. 20 12. 19 11.79 11.78 11.67 11.33 11 .27 ... 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 1 .2 1 .2 1.3 1.3 1.5 1.6 1.7 2. 0 2. 3 2. 4 2. 4 4.1 4 .2 4.7 6 .2 6.5 6.9 7 .2 7.3 13.8 15.5 16.3 17.5 24 .6... 1.94 1.97 2. 06 2. 16 2. 28 2. 39 2. 51 2. 52 2.58 2. 65 12. 44 0.08 12. 23 0.06 11.75 0. 32 11.13 0.01 9.44 0.04 5 .23 0.14 2. 66 0.00 1 .24 0.03 s2 = 0.1147 0.14 1.38 0.36 2. 27 0.64 4.33 0.85 7. 12 1 .20 15.71