NC 2512. In comparison, P. brachyurus suppressed M . hapla on Hicks and NC 95, ..... cultivar 'NC 95' by infection of Meloidogyne a1'ena,.ia on M. hapla.
Chapter 42
Interactions with Other Nematodes
J.
D.
EISENBACK AND G.
D.
GRIFFIN
Assistant Professor, Department of Plant Pathology, Physiology and Weed Science, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061. Nematologist, USDA ARS, Forage and Range Research Laboratory, Utah State University, Logan, UT 84322-6300.
One of the most important roles of nematodes in the host-parasite relationships between soil borne pathogens and plants is in disease complexes. Such complexes extend beyond the interaction(s) of nematodes with organisms of other phyla to include the relationship between nematode species. The presence of two or more plantparasitic nematodes parasitizing a single plant cultivar is a common occurrence in nature. The nematode community is dynamic; its members are constantly interacting with each other as well as with other organisms. Communities of plant-parasitic nematodes are generally polyspecific, and many different factors are responsible for the diversity of the community and relative success of the individual in the community. Widespread dispersal, polyphagous nature, persistence in the soil, and weak interspecific competition of nematodes enhance community diversity (42). Plant-parasitic nematodes rarely occur in monospecific communities. The occurrence of a particular species in an environment is related to its dissemination, the climate, edaphic factors, host suitability, fecundity, survival adaptations, and interactions with other organisms, including nematodes (40,42) . However, most nematological research involves the effects of a single nematode species on a particular crop plant. Of course, the effects of one species on a particular crop plant must be identified in order to compare the effects of concomitant populations. In some cases, a single nematode species may dominate, especially if the species is better adapted to a host-parasite relationship or to the given ecological conditions. Species of plant-parasitic nematodes can interact ecologically or etiologically. Ecological interactions affect the repro-
ductive capacity of the individual nematode populations; etiological interactions alter the development of plant disease. Ecology and etiology of the interaction are related because numbers of nematodes are often correlated with the amount of disease (42). However, nematode reproduction is not always related to the susceptibility of the plant to damage, and the two aspects of the interaction may behave independently. Thus, nematode-nematode interactions should be examined from both approaches. The host plant response to a plant-parasitic nematode may be altered by the presence of another nematode. One nematode may enhance the development and reproduction of another nematode on a host, and a reverse effect may be observed on a different host (30,51). Two or more nematode species may act independently and have no effect on parasitism and reproduction (53) and disease expression (31) of another nematode. ECOLOGICAL INTERACTIONS
Nematode-nematode interactions may be beneficial or detrimental to one or all nematodes involved, or they may have no effect. However, such interactions are usually antagonistic to at least one of the individual species. When the reproductive capacity of a nematode is greater under monospecific conditions than under polyspecific conditions, competition occurs between species (4). An antagonistic interaction can be caused by spatial competition, physical alteration or destruction of feeding sites, or a decrease in the suitability of the host caused by a physiological change (40). The principle of competitive exclusion states that two closely related species cannot occupy the same ecological niche (16). 313
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Each species can function by itself in a particular niche, but when the two are together they interact until one species usually dominates. The species that dominates has a competitive advantage. Competition, however, may be density and time dependent and is related to persistence, pathogenicity, and host suitability (4). The competitive exclusion principle is difficult to apply to communities of plantparasitic nematodes because the different niches in the soil environment are dynamic and not easily defined or delineated. Furthermore, other factors may cause exclusions. Also, interactions may occur between species in close proximity even though they occupy different niches (4 , 40). When the competition among individuals in a species is greater than the competition between species, two species can cohabit (4). Occasionally, beneficial interactions occur between two nematode species because of the results of a mechanical or physiological alteration of the pla.nt that makes it a more suitable host. Physiological changes may also enhance nutrition or reduce resistance of the host to the parasite (40). Ectoparasites: Ectoparasites can be divided into different groups according to their feeding habits. One group remains completely outside the root tissues and feeds only on epidermal cells and root hairs; members are referred to as 'browsers' (5). Association with the host is usually short term and not specialized. Members of another group of ectoparasites may be short-term feeders, but the anterior portion of their heads may penetrate into the cortical tissues of some hosts. A more specialized group of ectoparasites remains completely outside of the root tissue, but the parasitic relationship with the plant is more complex than with the epidermal feeding ectoparasites; members of this group have relatively long stylets, feed on cells below the epidermis, and often incite hypertrophy and hyperplasia. The degree of competition between species within the ectoparasites is affected by the mode of parasitism. The primitive host-parasite relationships are usually less competitive than the more specialized relationships (29,30,38).
Greenhouse experiments with six varieties of bermudagrass demonstrated that more competition occurred between Tylenchorhynchus martini and Criconemella ornata than between T. martini and Belonolaimus longicaudatus or C. ornata and B. longicaudatus. However, reactions varied according to cultivar (29), but competition for feeding sites occurred more between species that fed superficially. Some nematodes may be related in their ability to compete for feeding sites with other species. Belonolaimus longicaudatus is more pathogenic on corn than is Dolichodorus heterocephalus, inhibiting D. heterocephalus reproduction. D. heterocephalus did not interfere with B. longicaudatus reproduction (47). The interaction between ectoparasites may be affected by host suitability. Paratylenchus projectus reproduction was suppressed by Helicotylenchus pseudorobustus and Criconemella similis on soybean. Soybean is a poor host for P. projectus, a moderately good host for H. pseudorobustus, and a good host for C. similis (34). Environmental factors and population density modify the competition between ectoparasites. Paratylenchus neoarnblycephalus and Criconernoides xenoplax showed different antagonisms to each other at 20 C and 26 C. This is expected, since the optimum temperature for P . neoamblycephalus is 20 C, whereas 26 C is optimum for C. xenoplax (3).
Ectoparasites can interact so that one or both species are stimulated. Reproduction of concomitant populations of Hoplolairnus columbus and Scutellonema brachyururn on cotton was mutually stimulated after 90 days in greenhouse experiments (33). Ectoparasite.\ยท and migratory endoparasites: Movement of migratory endoparasitic nematodes through the root tissues alters root morphology and physiology and is generally antagonistic to ectoparasitic nematodes (1,6,44). However, the suitability of the host to a nematode is important in the interactions. Reproduction of Tylenchorhynchus martini was suppressed by Pratylenchus penetram on red clover which is a good host for both species (6). However, no interaction was observed with Tylenchorhynchus agri and P. penetrans on creeping bentgrass, a poor host for P. penetrans and an excellent host for T. agri (51). Paratrichodorus
Nematode Interactions: Eisenback, Griffin minor and Pratylenchus zeae were mutually stimulatory on several varieties of corn, and positive interactions occurred between P. minor and Pratylenchus brachyurus on several soybean cultivars (30). Small changes in host suitability have been suggested for the increase in the reproduction rate of certain nematodes; the exact mechanisms involved are unknown. Interactions between nematodes may be time dependent. The reproduction of Pratylenchus penetrans on red clover was suppressed by Tylenchorhynchus agri after 3 months in a greenhouse experiment, but P. penetrans overcame the suppression after 5 months (1). Translocatable factors may alter the attractiveness of the roots to nematodes. In experiments utilizing plants with divided root systems, Tylenchorhynchus claytoni induced physiological changes in the host that inhibited penetration by P. penetrans by 25-90% on tobacco cultivar WS 117. This may have been a temporary inhibition, since these tests were only several days in duration and long-term interactions were not determined (35). Ectoparasites and sedentary endoparasites: Ectoparasites and sedentary endoparasitic nematodes occupy different niches and coexist on the same plant with and without any interaction (38). The interactions can be suppressive or stimulatory, depending upon the mechanisms involved. Reproduction of the sedentary endoparasite can be suppressed by the ectoparasite by indirect or direct competition for feeding sites. The number of feeding sites for the endoparasite can be reduced if the endoparasite penetrates at the preferred feeding site of the ectoparasite. Ectoparasites can also indirectly reduce the number of feeding sites available to the endoparasite by damaging the root system. An example of this is shown by the competition between Paratrichodorus minor and Meloidogyne naasi. P. minor feeds near the root tips, competes for feeding sites, and inhibits M. naasi on creeping bentgrass
(52). Sedentary endoparasitic nematodes can suppress the ectoparasites even though they are separated by host tissue. The mechanisms of inhibition are probably physiological rather than mechanical.
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Sometimes domination by either species is related to environmental or edaphic factors. Meloidogyne hapla antagonized Xiphinema americanum on alfalfa in field tests lasting 4 years. This may have been caused by M. hapla limiting the number of feeding sites; however, changes in the physiology of the alfalfa may have changed the suitability of the host to X. americanum (39). Hoplolaimus galeatus increased from undetectable levels and gradually replaced Meloidogyne incognita as the dominant plant-parasitic nematode species during six growing seasons in a cotton field (2). There may also be a mutual stimulatory effect on reproduction between nematode species. Meloidogyne incognita increased the reproduction of Hoplolaimus columbus on cotton after 90 days in a greenhouse (33), and Meloidogyne hapla enhanced reproduction of Criconemoides xenoplax on concord grape (49). In comparison, the ectoparasite Scutellonema brachyurum stinmlated reproduction of the sedentary endoparasite M. incognita on cotton (33). The mechanisms involved have been suggested to be primarily physiological, but the precise mechanisms involved are not known. Migratory endoparasites: Migratory endoparasitic nematode species generally utilize the same feeding sites and are competitive with each other. The suitability of the host plays an important role in the interaction of concomitant populations. In greenhouse studies, Pratylenchus penetrans was antagonistic to Pratylenchus alieni, whereas P. alieni caused an increase in the ratio of females to males of P. penetrans (14). Interactions between two nematode species may be affected by climatic or edaphic factors. Radopholus similis and Pratylenchus coffeae were mutually suppressive on citrus after 10-15 months, but soil texture favored one of the species; P. coffeae dominated in fine textured soils, whereas, R. similis dominated in coarse textured soils (41). Migratory endoparasitic and sedentary endoparasites: Migratory endoparasitic nematodes move through root tissues and generally disturb feeding by sedentary endoparasitic nematodes. A Meloidogyne spp. was suppressed by Pratylenchus major on pineapple (23), Pratylenchus brachyurus dominated
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M eloidogyne incognita on cotton ( 17), and Pratylenchus spp. were more competitive than M. incognita on tobacco (18). An explanation for this may be that migratory endoparasites often penetrate the root faster and thus inhibit penetration by the sedentary species ( 17,55); however, host suitability may be related to penetration rates. Good hosts allow faster penetration than less suitable hosts; hence , sedentary endoparasites may stimulate or suppress penetration by the migratory species (15). Tomato is a better host for M . incognita than P. brachyurus, and prior inoculation with M. incognita suppressed penetration by P. brachyurus. Cotton is a good host for P. brachyurus and a poor host forM. incognita but prior infection by M . incognita stimulated penetration by P . brachyurus ( 17). Interactions between species may be affected by the extent of the period of nematode cohabitation. Meloidogyne naasi did not overcome initial inhibition by Pratylenchus penetrans on creeping bentgrass until after 10 months (51). However, P. penetrans was not suppressed by Meloidogyne incognita on red clover until after a 5month cohabitation period (I) . Invasion and reproduction of Ditylenchus dipsaci and Heterodera schachtii in sugarbeet was not affected by combined inoculations, apparently because of differences in nematode biology and tissue specificity (20). Timing of the inoculations can artificially affect nematode interactions. M . incognita inoculated on grape 1 month before Pratylenchus vulnus significantly inhibited reproduction by P . vulnus after 150 days. In simultaneous inoculations, however, inhibition of P. vulnus did not occur until after 250 days (9).
Sedentary endoparasites are considered to be more advanced parasites than the migratory species. They establish a more complex relationship with the plant and greatly alter the physiology of the host. The altered physiology may increase or decrease the suitability of the host to the migratory parasites ; Pratylenchus penetrans and Meloidogyne incognita were mutually suppressive in a greenhouse study (13). Translocatable factors induced by M. incognita in split-root experiments greatly inhibited P. penetrans. However, the antagonism
factor that was induced by P. penetrans toward M. incognita was not translocatable and was probably more closely associated with a disruption of feeding sites. Competition between species is affected by host suitability. Pratylenchus brachyurus and M. incognita were mutually suppressiVe on M. incognita susceptible tobacco cultivar NC 2326; P. brachyurus had no effect on M. incognita susceptible cultivar Hicks, but M. incognita inhibited P. brachyurus. M. incognita stimulated P . brachyurus on root-knot resistant cultivars NC 95 and NC 2512. In comparison , P. brachyurus suppressed M . hapla on Hicks and NC 95, but had no effect on NC 2326 and NC 2512. M . hapla inhibited P. brachyurus on Hicks and NC 2326, but had no effect on NC 95 and NC 2512. (31). Resistance to M eloidogyne hapla in a cultivar of alfalfa was reduced by prior infection by Ditylenchus dipsaci (19). fhe effect of nematode interactions on host suitability is also density dependent. Low and high numbers of Meloidogyne incognita caused decreases of the number of Pratylenchus penetrans eggs deposited by 37 % and 57%, respectively (8 ,9). Migratory and sedentary endoparasites do not always interact negatively but sometimes interact in a stimulatory manner. The reproduction of Pratylenchus brachyurus on tobacco was stimula ted by Meloidogyne incognita (31 ), and Meloidogyne naasi stimulated Pratylenchus penetrans on creeping bentgrass (51). Sedentary endoparasites: Sedentary endoparasites are highly specialized parasites. Competition between two sedentary endoparasitic species is generally mutually suppressive because of the competition for available feeding sites (40) and physiological alterations; however, neutral and stimulatory interactions also occur (48,50). Two or more species of Meloidogyne are commonly found together in the same field, root system, or gall (36). Factors other than competition are also important in the domination of a particular species. Temperature and other climatic factors are important because certain species are more common in cooler climates and others are better adapted to warmer clima tes.
Nematode Interactions: Eisenbach, Griffin Meloidogyne incognita dominated Meloidogyne javanica and Meloidogyne hapla at high temperatures, but M. javanica suppressed M. incognita and M. hapla at cool temperatures (36). Ninety per cent of the females were M. incognita and 10% were M. hapla in simultaneous inoculations of M. incognita and M. hapla at high temperatures. Only 57% of the females were M. incognita at low temperatures. M. hapla suppressed M. incognita on M. incognita resistant tobacco cultivars NC 95 and NC 2512 at moderate temperatures (31 ).
Competition between species is also density dependent (32). Meloidogyne incognita penetrated the roots faster than Meloidogyne hapla in simultaneous inoculations, occupying all of the infection sites that were then destroyed by the hypersensitive reaction (31 ). Likewise, prior inoculation of M. incognita on Meloidogyne arenaria-susceptible soybean resulted in a decrease in gall and egg mass production by M. arenaria (24). However, prior inoculation of M . incognita-resistant tobacco with M. arenaria or M. hapla masked the resistance toM. incognita ( 12). M. hapla inoculated on tomato 20 days before Heterodera schachtii inhibited reproduction of the cyst nematode. In simultaneous inoculations, H. schachtii suppressed M. hapla (21 ). Interactions have been reported where a neutral effect was obtained. No interactions occurred in simultaneous inoculations of Meloidogyne incognita and Heterodera cajani on cowpea in the greenhouse (50). Similar results were 23 found with M. hapla and H. schachtii on sugarbeet. However, prior inoculation of M. hapla on sugarbeet stimulated H. schachtii (26,28). The relationship between cyst and root-knot nematodes is density and time dependent (50). Low populations of M. incognita had no effect on Heterodera glycines in microplot studies with soybean, yet high populations suppressed cyst nematodes early in the season and stimulated them late in the season (48). Prior inoculation of Heterodera schachtii on sugarbeet in the greenhouse suppressed Meloidogyne hapla, whereas prior infection by M. hapla stimulated H. schachtii (26,28). Double inoculations of M. hapla on sugarbeet had little effect on each other, whereas
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double inoculations of H. schachtii were synergistic (27). Temperature can affect the interaction between Meloidogyne and Heterodera. In simultaneous inoculations of M. hapla and H. schachtii, the inhibition of M. hapla by H. schachtii on tomato increased as the plant growth temperatures were raised (21 ). Interactions may also be density dependent as well as time dependent. In field studies, low levels of Rotylenchulus reniformis inhibited Meloidogyne incognita on sweet potato, whereas M. incognita had no affect on R. reniformis. High levels of M. incognita, however, suppressed R. reniformis, and R. reniformis had no effect on the root-knot nematode. Each species was capable of suppressing the other and becoming the dominant species (54). Nacobbus aberrans interacted with Meloidogyne hapla and H eterodera schachtii on sugarbeet and, over time, was antagonistic to the reproduction of Heterodera and Meloidogyne, particularly Meloidogyne (25). Conversely, reproduction by N. aberrans was not affected by the presence of the other two genera. Nacobbus was considered less aggressive than root-knot or cyst nematodes. ETIOLOGICAL INTERACTIONS
In most studies, a single nematode entity is found responsible for plant disease symptoms (40). However, since nematodes are usually found in polyspecific communities (42), it can be expected that nematodes would interact with each other and alter the course of the disease. If the amount of disease caused by both nematodes is less than their combined effects acting alone, the interaction is negative; if it is more, the interaction is positive (synergistic); and if it is the same, there is no interaction (neutral or additive). Neutral interactions: Instances where two or more species of plant-parasitic nematodes have shown neither a negative or positive effect on plant growth usually occur where the nematode species differ in the plant tissue they parasitized. Interactions, however, may have gone undetected because the investigator failed to consider the effect(s) of different inoculum or population density levels, age
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of plant at time of inoculation, or time or inoculation or the type of host. A combination of Heterodera glycines and Meloidogyne incognita reduced the growth of soybean from slightly less to slightly more than the additive effect of both nematodes, depending on inoculum densities (48). Although the mean height of tobacco plants, susceptible to Meloidogyne incognita, Meloidogyne hapla, and Pratylenchus brachyurus, was depressed from simultaneous inoculation of the three nematode species, the fresh top weights were not significantly different and root-knot nematodes increased root weights (30). A combination of Pratylenchus penetrans and Tylenchorhynchus martini failed to reduce the growth of red clover and alfalfa below that of P. penetrans alone. A combination of Ditylenchus dipsaci and Heterodera schachtii did not increase the susceptibility of sugarbeet to either nematode (20). Negative interactions: Less disease occurs when there is strong competition between nematode species. Although this type of relationship does not represent the usual nematode-nematode interaction, there have been reported cases where one species limits the virulence of another species on a plant. One explanation given for this relationship is that a less pathogenic species reduces the number of infection loci and feedings sites available to the more pathogenic nematode species ( 10, 11 ). There are probably other factors involved in this relationship, such as physiological changes occurring within the plant. Suppression of the growth of tomato was less when exposed to Meloidogyne incognita and Pratylenchus penetrans than when exposed to M. incognita alone ( 13). Similar results were observed with M. incognita and Rotylenchulus reniformis on blackgram (37) and grape (46) . Positive interactions: The reason for one species of nematode being able to predispose a plant species to another species of nematode in a synergistic reaction is not fully understood. It may be due to an increase in susceptibility to invasion or host suitability (45) or to some other factor that brings about a physiological reaction in the plant to greater or total susceptibility. Combinations of Heterodera schachtii and Meloidogyne hapla suppressed tomato
root growth by 65, 64, and 61% below that of uninoculated controls and single inoculations of either M. hapla or H. schachtii, respectively (22). Similar results were obtained with Meloidogyne javanica and M. incognita on Hicks tobacco (43). The reaction of two or more nematode species on a plant may or may not be positive depending on the period of exposure. Combined inoculations of H. schachtii, M. hapla, and Nacobbus aberrans, significantly suppressed the growth of sugarbeet (25). A similar situation was found on creeping bentgrass (51). Single inoculations of Tylenchorhynchus agri or Pratylenchus penetrans inhibited plant root growth, but shoot growth was suppressed only when combined inoculation of the two nematode species was made. However, the greatest root growth suppression of creeping bentgrass occurred when T. agri or Paratrichodorus minor inoculation preceded that of Meloidogyne naasi by 3 weeks (52). A combination of Ditylenchus dipsaci and Meloidogyne hapla synergistically reduced the growth of 'Ranger' alfalfa, susceptible to both nematodes (18). A combination of the two nematodes did not affect the resistance or susceptibility of alfalfa to D. dipsaci, but reduced the resistance of 'Vernal 298' to M. hapla. Similar results were obtained on tobacco; either Meloidogyne arenaria or M. hapla reduced the resistance of NC95 toM. incognita race 1 ( 12). CONCLUSIONS
Since more than one species of plantparasitic nematode species are usually found associated with the growth of a given plant cultivar, it is apparent that one may suspect a positive or negative relationship occurring between nematode species in relation to associated plant growth, nematode pathogenicity, and nematode population dynamics. Concomitant populations of nematodes can interact with each other to affect their reproductive capability, and their interaction can alter the etiology of plant disease. Most studies on nematode interactions have been qualitative and provide limited information. It is, therefore, impossible to determine with any degree of accuracy how a given nematode-nematode relationship will affect plant growth and nematode
Nematode Interactions: Eisenbach, Griffin reproduction without an understanding of the host-parasite relationship, differences in the degree of virulence between nematode species, and the effect of environmental factors on the nematode-nematode-plant association. Although these preliminary experiments reported herein are useful, more interactions may have bee n found if different levels of variables had been used. Therefore, interpretations of the d ata is not easy and the development of conclusions about nematode-nematode inte ractions is difficult. The following general conclusions can be made in summarizing this complex subject: l. Ne matode-nematode interactions can be approached from two interrelated aspects of ecology or etiology. 2. Interactions can be stimulatory, neutral, or detrimental to one or both species. 3. Competition between nematode species generally is weak. 4. Competition between species can restrict the distribution of some species. 5. Competition is more severe between species with similar feeding habits. 6. Competitive advantage increases as the host-parasite relationship becomes more complex. Hence, the endoparasites are more competitive than the ectoparasites, and the sedentary endoparasites are more competitive than the migratory endopa rasites. 7. Competition between species may be density and time dependent. 8. Competition can be modified by environmental factors which are difficult to separate from competition. 9. Host suitability is a key factor in interactions and often is responsible for one species being dominant. lO. Mechanisms of competition may include mechanical destruction or physical occupation of feeding sites or induced ph ysiological changes in the host's suitability or attractiveness. 1l. Generally, the amount of disease caused by two or more nem atode species is additive or slightly less than their combined effects of each alone, but sometimes it can be more than additive. 12. Strong competitors cause less disease in combination with another species than from single nematode-plant associations.
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13. Most nematode-nematode interactions which result in more disease in combination than in single nematodeplant associations involve a sedentary endoparasite. 14. Nematode-nematode interactions can become more complex when other organisms are also involved in the etiology of the disease. 15. Interactions among nematodes are important in nature and more precise experiments are needed if their effects on plant growth are to be quantified. LI T ERATURE CITED I.
Amosu,
J.
0., and D. P. Taylor. 1975 . Interaction of
Meloidogyne hapla, Pratylenchus penetrans a nd Tylmchorhynchus agri on Ken land red clover, Trifolium pratense. Indian J o urnal
of Nematology 4:124-131. 2. Bird, G. W .. 0. L. Brooks, and C. E. Perry. I 974. Dynamics o f co ncom itant fie ld populations of H opioi.dimu.< columbus and M eloidogyne incognita. J ou rnal of Nem atology 6: 190-1 94. 3. Bra un , A. L., H. Mojtahedi , and B. F. Lownsbery . I 975. Separa te a nd combined effects of Paratylenchus neoamblyceplwlus and Criconemoides xenoplax o n ' Myrohalan ' plum. Phytopathology 65: 328-3 30. 4. Brewer, R. 197 8. Pri nciples of ecology. Philadelphia: W. B. Sa unders Co. 5. Bridge, J ohn , and N. G. M. H ague. 1974. The feeding beh avior of Tylenchorhynchus and Merlinius species and their effect on growth of perennial r yegrass. Ne matologica 20 :11 9- 130. 6. Chapman , R. A. I 959. Development of Pratylenchus penetrans and Tylenchorhynchus martini on red clover and alfalfa. Phytopathology 49: 357- 359. 7. Cha pman , R. A. 1965. Infect.ion of sin gle root systems by larvae of two coincident species of root-knot nematodes. Nematologica 12: 89 (Abstr.). 8. Chapman , R. A., and D. R. Turner. 1975. Effect o f M eloidogyne incognita o n reprod uction of Pratylenchu.
