Article bibliographique

MIGRATION OF, PLANT-PARASITIC NEMATODES TOWARDS PLANT ROOTS

Jean-Claude PROT Laboratoire de Nématologie, ORSTOM, B.P. 1386, Dakar, Sénégal.

The controversy regarding the movement of Riding & Smith, 1972 ; Siddiqui & Viglierchio, plant-parasitic nematodes in soi1 and their abil- 1970), are lacking in plant-parasitic nematodes. ity to find host roots has continued since 1925 Mechanoreceptors such as setae, bristles, papil- (Steiner)., The first hypotheses were proposed lae or free nerve endings occur in plant-parasitic by Steiner when he reviewed the subject. His nematode and they may aid in root penetration hypotheses were : (Doncaster & Seymour, 1973). Phytoparasitic

nematodes also possess potential chemo-recep- That had the ability to 'Ocate , tors which could allow them to locate their hosts host roots over considerable distances. a t a distance. Baldwin (1977) indicated tha t That plant roots produced secretions which for such a receptor to function, it would be were carried bY the Soi1 water and acted expected t o have at least one neuron in contact as selective stimuli upon the nema. with the environment. On the basis of that That amphids were the sense organs criterium, nematodes possess several organs through which nematodes responded to which may function as possible chemore,ceptors. the stimuli. Setae are present among nem'atodes and

The purpose of this review was t o study and analyze the data that have accumulated in the intervening 55 years that may modify or verify Steiner's original hypothesis. The main subject requirements for verification can be categorized in three main areas, possession of sense organs, movement over great distances and root stimuli.

Sense organs

Many organs with possible sensory function have been described among the nematodes based primarily on morphological character- istics. Ocelli, which are known to have a photo- receptive function in aquatic nematodes (Croll,

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Maggenti (1964), Croll and Maggenti (1968) have shown that they are connected with a peripheral nervous system but there is no evidence that the neurons contained in the setae are in contact with the exterior. In nematodes, they appear to be primarily mechanoreceptors while setae are known to be chemoreceptors among insects.

Certain papillae of Meloidogyne incognita (Baldwin & Hirschmann, 1973), Capillaria hepatica (Wright, 1974), IIeterodera glycines (Baldwin & Hirschmann, 1975) and Trichinel la spirallis (McLaren, 1976), which have pore-like openings to the exterior, may be chemorecep- tors.

Ultrastructural studies show that the phas- mids of filariae and Necafor arnericanus were open to the exterior and appear to be structur-

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ally ,identical t o the amphids but are smaller and less well developed (Kozek, 1968 ; McLaren, 1972, 1976). Even though phasmids may be chemoreceptors among the filariae, the paycity of information about these organs among plant- parasitic nematodes precludes assigning a defi- nite chemosensory function to those organs among the latter group.

Amphids have attracted the most attention % among the sensory organs of phytoparasitic

nematodes. The cytological studies of Baldwin and Hirschmann (1973, 1975), Endo and Wergin (1977) have shown that the neurons of the amphids terminate in a cavity open t o the exterior. Circumstantial evidence about the function of the amphids in chemo-reception was described by Lewis and Hodgkin (1977). They showed that a chemosensory mutation among Caenorhabditis elegans was frequently acc,om- panied by sonle neuroanatomical changes in the amphidial neurons.

I t appears therefore that nematodes possess a t least one type of chemoreceptor, the amphids and possibly two others, the phasmids and a variety of papillae. It is also possible that some others will be discovered ; for example, Wright and Chan (1974) described a possible chemo- receptor which consists of a cuticle-lined cham- ber, open t o the exterior and containing four nerve endings, located posterior to the nerve ring of ‘Capillaria hepatica.

Moreover, the sensitivity of ‘this organ(s) is very high. Dusenbery (1975) demonstrated that solutions of D-tryptophan a t a concentration of 10-4 and 10-3 M/1 acted as a repellent for Caenorhabditis elegans, while pyridine, a t the same concentrations attracted this nematode (Dusenbery, 1976) ; Prot (1979) showed that juveniles of ikfeloidogyne jauanica and M. inco- g n i f a were repelled by mineral salts solutions at the same conc,entrations. Another evidence of the high sensitivity of chemoreception in nematodes is indicated by the fact that some nematodes, induding Panagrellus rediuivus (Ba- lakanich & Samoiloff, 1974), Nippostrongylus brasiliensis (Bone & Shorey, 1977 ; Roberts & Thorson, 1977), Heferodera schachtii and Globo- dera rostochiensis (Greet, Green & Poulton, 1968 ; Green & Greet, 1972) and Rotylenchulus reni- formis (Nakasono, 1977), produce pheromones

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. ..

which attract the mating partner, sometimes over great distances (Evans, 1970).

Additional evidence for ehemosensory percep- tion in nematodes can be derived from the fact that low concentrations of nerve poisons suc,h as the oxidation or hydrolysis products of temik affect the behaviour of nematodes (Nel- mes, 1970), their migrations (McLeod &, Khair, 1975) and the attraction, of males towards females (Hough & Thomason, 1975).

Movement over great distances

In the field, ‘nematode dissemination is mostly due to passive dispersal. Phytoparasitic nema- todes are disseminated by wind, irrigation, flooding and activities of man and animals. Likewise, a high populat4ion density may cause a spread on the borders of an initial population (Stein, 1965). Nematodes could also follow the growth of the roots on which they are feeding, as O’Bannon and Tommerlin (1969) observed to be the manner by which Radopholus s imil is spread up to 15 m per year in a citrus grove.

Because passive dissemination of phyto- parasitic nematodes has been widely accepted as the major means by which nematodes move in fields there has developed a general concept that these parasites do not move over any great distance by their own locomotion. “Evidence indicates, that , unless carried passively, plant- parasitic nematodes usually spend most of their life in the vicinity of their birth, moving perhaps only a few centimeters a year. Unless this is proven to be untrue, we should be conservative in Our estimates of nematodes’ long distanc,e active migration.” (Norton, 1978). However, active rnovement of individuals over consider- able distance has been observed. Wallace (1961) showed that Ditylenchus dipsaci migrated 10 cm within 5 h in a temperature gradient. Blake (1962) observed a similar displacement towards oat seedlings with the same nematode. Evans (1969-1970) showed that the males of Globodera rostochiensis migrated 15 cm in 72 h t o reach females ; some juveniles of the same nematode were able to migrate successfully 45 cm t o reach the host plant roots (Rode, 1962) and 40 cm in a temperature gradient (Rode, 1969). In the

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Migrat ions of plant parasitic nematodes

field, A n g u i n a t r i f i c i could travel upwards in the soil o f 30 cm in order to parasitize’ wheat plants (Leulcel, 1962).

More recently, Santos (1973) observed that males of Meloidogyne spp. were capable of mov- ing 15 cm in the absence of any stimulus. Harri- son and Smart (1975) found that 50% of popu- lations of Trichodorus christiei and Trichodorus prozirnus moved horizontally 20 cm in 72 11 to reach the roots of a tomato plant. With Tylen- chorhynchus claytoni, DiSanzo (1973) observed a movement of 10 cm in 10 days. During studies using five different populations of Meloidogyne, Prot (1978, 1979) and Prot and Netscher (1978) found that at least 50% of the juveniles of al1 the populations were able to migrate 25 cm vertically in 10 days ; 50% of the juveniles of two of the populations migrated 50 cm.

These observations, under a variety of exper- imental conditions, with nematodes of different genera, bring out the fact that some plant- parasitic nematodes are able to migrate greater distances than has generally been accepted for these nematodes, a t least, when they are influenced by a stimulus. These migrations can: have economical significance. It has been shown that in very sandy West African soil ( > 80%) only 0.9% of the Meloidogyne survived the dry season in the 20-40 cm soil horizon and none in the top 20 cm of the soil (Demeure, ‘1978). It is also a frequent observation that even though sampling does not reveal the presence of Meloidogyne, susceptible crops grown in fields apparently nematode-free are often heav- ily and quiclcly parasitized (de Guiran, 1966). This capability of vertical migration may also explain the rapid reinfestation of this horizon which is sometimes observed following a nema- ticide treatment of sandy top soil. Indeed, Johnson and McKeen (1973) showed tha t a Meloidogyne incogni ta population, placed a t a depth of 125 cm, reduced a tomato harvest by 10%. These authors observed galls on roots in the top 15 cm of the soil.

The attraction of plants

ATTRACTION BY ROOTS

Table 1 summarizes the principal ob’serva- tions carried out in t.his field. Although these

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studies have been undertalcen in varied condi- tions and with different nematodes, the majority of the authors accept the hypot,hesis that host roots are attractive t o phytoparasitic nematodes. Some authors have observed attraction, repul- sion or a total absence of effect of roots on the nematodes within the same experiment. Weser (1956) interpreted this variability as the result of an interplay between a repellent and an attractive agent, both produced by the plant ; the observed effect is determined by the respect- ive quantities of these two agents at the moment .of the experiment. In the same manner, Viglier- Chio (1961), Who observed a roots’ attraction in a natural soil and a repellent effect in pure silica Sand, proposed that the stimuli of repul- sion, masking weaker stimuli of attraction in the all-Sand systems, were adsorbed on the soil colloids,. the attractions’ stimuli becoming domi- nant in this case.

According to some authors, the congregation of ‘the nematodes near host roots is due t o a modification of their rate of movement (Kühn, 1959) or a trapping in the water film existing on the roots’ surface (Sandstedt & Schuster, 1962) following initial random movements. Rohde (1960) suggested that the high CO, con- centrations, existing in the immediate vicinity of the roots, inhibited nematode movement, thus preventing them from leaving the rhizo- sphere. This last hypothesis seems difflcult to defend, particularly for the endoparasites which could not penetrate roots when their movements were inhibited.

It is generally accepted that attraction to roots occurs but the consensus is that the attrac- tion is nonspecific. However, Viglierchio (1961) observed that, in the case of IIeterodera schachtii, the plant’s attractiveness was correlated with its ,efflciency as a host. Lee and Evans (1973) showed that there was a strong correlation between the degree of attraction of rice seedling extract of an individual variety and its suscepti- bility t o Aphelenchoides besseyi. Grifin (1969) reported that a resistant and a susceptible cultivar. of alfalfa attracted Meloidogyne kapla juveniles equally when they were tested separ- ately ; during a simultaneous comparison how- ever, 71% of the juveniles migrated towards the susceptible plant and only 29% towards

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J . C. Prot

Table 1

Effects of host or nonhost plants or roots on phytoparasit,ic nemat*odes deplacement + = attraction, - = repellent, O = no effect

Plan t or roots Nematode Genera Tomato Vege- Cereales Sugar- Grasses, Tissues

tables beet orna- culture mentals

and weeds

Meloidogyne + + -!-

+ + + + t + + O

+ + + - + O -

Heterodera Glo bodèra O

O + ' . O + + + + + +

+ O

- +

Hemicriconemoides

Pratylenchus f 8 '

Ditylenchus + +

Aphelenchoides

Hoplolaimus + Tylenchorhynchus

Helicotylenchus

Rotylenehulus

308

. . . . +.

+

+

+ +

+ + + +

+ + O

+ + + +

Records

Bird, 1960 Bird, 1962 Di Sanzo, 1969 Griffin, 1969 Haynes & Jones, 1976 Linford, 1939 Lownsbery & Viglierchio, 1960 Lownsbery & Viglierchio, 1961 Peacock, 1959 Prot, 1975 Sandstedt, Sullivan & Schuster, 1961

Viglierchio, 1961 Wieser, 1955 Wieser, 1956

Bergmann &Van Duuren, 1959 Davis & Fisher, 1976 Hann & Lee, 1975 Kühn, 1959 Rode, 1962 Viglierchio, 1961 Wallace, 1958 Wallace, 1960 Weischer, 1959

Azmi & Jairajpuri, 1977

Di Sanzo, 1969 Edmunds & Mai, 1967 El-Sheriff & Mai, 1969 Lavallee & Rohde, 1962

O Schuster & Sandstedt, 1962

+ Linford, 1939

Blake, 1962 Griffin, 1969 Klingler, 1963

Barraclough & French, 1965 Lee & Evans, 1973

Azmi & Jairajpuri, 1976 Azmi & Jairajpuri, 1977

Azmi & Jairajpuri, 1977 Di Sanzo,' 1973

Alby & Russell, 1975 Azmi & Jairajpuri, 1977

+ Linford, 1939

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Migrat ions of plant parasit ic nematodes

the resistant cultivar. Are these results due to fortuitdus selections of plant and nematodes ? Possibly but it may also be possible that al1 nematodes are not sensitive to the same stimu- lus (i) and that al1 plants do not produce similar attractant(s) and repellent(s).

ATTRACTION OF ROOT TIPS AND GALLS

Nematodes are generally found clustered preferentially around specificf root zones and Table 2 summarizes the principal observations. Most plant-parasitic nematodes choose the zone of cellular elongation. Peacock (1959) demon- strated that if a piece of cellophane was placed between the roots and the nematodes, the juve- niles of Meloidogyne followed the root-tip as it grew on the other side of the cellophane. The areas of previous penetration, the galls and the injured parts of the roots are also particularly attractive to these juveniles (see Table 2).

The ’ juveniles of Heterodera rostochiensis aggregate at the points of production of new rootlets ; Widdowson, Doncaster and Fenwick (1958) observed that when concentrations of

these juveniles were found a t isolated points dong the main roots, almost invariably lateral rootlets appeared a t these points.

ATTRACTION I N RELATION T O THE PHYSIOLOGICAZ, CONDITION OF THE ROOTS

Another demonstration of the active attract- ’

iveness of roots is the fact that attraction vanishes when the root’s growth is stopped or limited (Lownsbery & Viglierchio, 1961). The attractiveness is proportional to the rate of growth of the roots (Wieser, 1955 ; Lavallee & Rohde, 1962). Moreover, roots killed by heating lost their attractiveness (Linford, 1939 ; Bird, 1962).

MODIFICATIONS OF ROOT ATTRACTIVENESS INDUCED BY NATURAL O R SYNTHETIC PRODUCTS

Some natural and synthetic chemicals prevent root invasion by phytoparasitic nematodes. Christie (1959) described an experiment, made by van Weërdt, in which Radopholus s imi l i s moved towards the roots of a corn plant located several inches away but if a rutabaga plant had

Table 2 Preferential root zones of penetration and aggregation of plant-parasitic nematodes

Zone of roots Nematode genera region primordia root punctured area of pilifer-

of ce11 of galls roots previous ous elon- second- pen- region, gation ary roots etration

Meloidogyne + Bird, 1960 + + Bird, 1962 + + Linford, 1939 + Linford, 1942 + + + Peacock, 1959 + Wieser, 1955

Heterodera + Kampfe, 1960

Glo bodera + + Pratylenchus + +

Widdowson, Doncaster & Fenwick, 1958

Gadd & Loos, 1941 Lavallee & Rodhe, 1962

+ Linford, 1939

Trichodorus 4- Pitcher, 1967

Rotylenchus + Linford, 1939

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J . C. Pro€

been grown previously in the soil, the corn roots were not invaded. Peacock (1961) has shown that c,harcoal inhibited the penetration of Meloidogyne juveniles into tomato roots. Char- coal stopped the invasion of roots of tomato and tobacco by Pratylenchus penetrans and Heterodera tabacum (Miller & McIntyre, 1976). Some other compounds such as aldicarb (Abdel- Rahman & Eissa, 1974 ; De Grisse & Moussa, 1971 ; Hough & Thomason, 1975) or carbo- furan (Di Sanzo, 1973) have been shown t o have the same activity. Rossner (1974) reported tha t the foliar applications of some substances

' influenced the invasion of the rhizosphere of the hast plants. These substances are known t o be nerve poisons.

The modifications of the rhizosphere by the roots, and their action on phytoparasitic nematode migrations

Roots alter the soil's physical characteristics and the chemical composition of the soil solu- tion. They induce some m'echanical and minera- logical modification of the soil (Sarkar, Jenkin & Wyn Jones, 1979) ; moreover, the soil par- ticles adjoining roots are slightly compressed. The roots are also able t o produce temperature gradients (Tanner, 1963 ; El-Sherif C% Mai, 1969) and redoxpotentialgradients (Lundegardh,l942).

Plants alter the chemical c.omposition and the pH of the soil solution by adsorbing .sorne compounds and by releasing some others. Thus, concentration gradients of minera1 salts can be created consecut,ively by root uptake (Bay- Shaw, Vaidyanathan & Nye, 1972 ; Barber, 1974 ; Dunham & Nye, 1976). The roots are also able to elicit gradients of organic compounds that they release as exudates, secretions, muci- lages, mucigels, lysates. The quantities of or- ganic materials released by the roots are not negligible since they can represent up t o 10420% of the total plant dry matter (Barber & Martin, 1976 ; Martin, 1977 ; Rovira, 1979). These or- ganic materials not only change the soil physi- cally, they also change il; biologically by altering the rhizophere microorganisms both quantitatively and qualitatively from those pre- sent in soil lacking roots.

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SOIL COMPRESSION, SIZE OF. SOIL PARTICLES

Wallace (19583, c ) suggested that each nema- tode attains its maximum speed of displacement for a determined pore diameter and that there exists a simple relation between the body length, the particle size and the speed of displacement. He also showed (1961) that in a particle size gradient Ditylenchus dipsaci aggregated at the end of a gradient where the particles are the finest.. If the nematodes appear t o be sensitive t o the physic-al properties of the soil, i t is diffl- cult. t o conceive that a root changes the soi1 structure suficiently in order to influence the migration of nematodes, at least, for more than a few mm.

TEMPERATURE GRADIENT

Temperature has a strong influeme on the activity of nematodes. Wallace (1963) analyzed available data and concluded that most plant- parasitic nematodes become inactive between 5 and 150 and between 30 and 400. The optai- mum range for ac,tivit,y was about 15 to 300. Temperature under 5 O and over 400 are often lethal.

El-Sherif and Mai (1969) expressed the hypo- thesis that roots could create a temperature gradient. able to orient phytoparasitic. nema- todes. In fact, they have shown that germinating alfalfa seeds establish a temperature gradient of 0.0330/cm in agar and that Pratylenchus penetrans, Difylenclzus dipsaci and Tylenchorhyn- chus claytoni responded positively t o such a gradient. ; Trichodorus chi.istiei and X i p h i n e m a americanunz showed no response.

lCIany animal-parasit>ic nemataodes exhibit a positive thermotactic response. These thermo- taxes may even be suicicial ; for example, N i p p o - strongylrrs brasiliensis moves towards the hottest end of a temperature gradient until it dies (McCue 6: Thorson, 1964).

Relatively few studies have been carried out concerning the behaviour of phytoparasitic nematodes in a, temperature gradient. In addi- tion t o the examples cited previously, Wallace (1961) showed that in a temperature gradient of 2-300, Ditylenchus dipsaci aggregates a t 100, Klinger (1972) found that Pratylenchus penetrans and D. dipsaci had positive thermo-taxes when

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Migrat ions of plant parasitic nematodes

the ambient temperature was 8.60 whereas only B. dipsaci was attracted towards the heat source a t 27.30. Rode (1969 ; 1970) observed t,hat the juveniles of Heterodern rostochiensis placed in a temperature gradient at a superoptimal temperature moved down the heat gradient until they reached their eccritic temperature.

Besicles some contradictions between the results of Wallace (1961) and Klingler (1972), Croll (1967) observed that acclimatization in- fluenced the eccritic thermal response of D. dip- saci ; this nematode accumulated a t the tempe- rature in which it had been previously stored. This was also demonstrated by Hedgecock and Russel (1975) with Caenorhabditis elegans.

It appears from these results that plant- parasitic nematodes are able t o migrate along a thermal gradient towards their thermal pref- erendum or their previous storage tempera- tures. But, if y e consider the thermal gradients existing in the soil and their daily variations it seems diRcult that the temperature gradients created by the roots is useful for the nematodes t o locate their llosts over large distances.

ELECTRO-CHEMICAL POTENTIAL, REDOX POTENTIAL

Experinlents conducted by Bird (1959) indi- catecl tha t juveniles of Meloidogyne javanica and M . Aapla'were strongly attracted t o some reduc- ing agents, particularly sodium dithionite. He put forward the hypothesis that attraction t o roots could primarily be explained as a move- ment oriented along a potential gradient created by a lower redox potential at the roots' surface. Especially, the accumulation of Meloidogyne juveniIes in the region of ce11 elongation may be due to a potential difierence of 10/20/mV between this part and the contiguous areas of the root.

In an electric field Panagrellus redivivus and nemas of the genera Tylenchus and Pratylenchus migrated towards the cathode (Caveness & Panzer, 1960), Heterodera schachtii displayed a tactic movement towards the cathode (Jones, 1960). Croll (1967) confirmed the observations of Caveness and Panzer (1960) and Sukul, Das and Ghosh (1975) demonstrated that A n g u i n a tritici migrated towards the anode and Di ty - lenchus dipsaci towards the cathode. In the

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latter case, the oriented movement was sup- pressed when a magnetic field was applied in a direction perpendicular to the electrical field and when the Salt solutions used during the experiment had high magnetic susceptibilities. These authors suggested that the nematodes may sense the change in potential of their ionic atnlosphere through the medium of negatively charged organic molecules contained in the amphids. On the other hand, Klingler (1965) considered that the redox potential had no action on Ditylenchus dipsaci. He observed that sodium dithionite woulcl attract, but another reducing agent, hydrogen, had no efiect ; whereas the oxidizing agent, potassium per- manganate, was also an attractant. Moreover, he did not find a constant attraction t o the 'anode or the cathode. 1

Most authors who have studied this pheno- menon have concluded that the redos potential or an elec,tric field can orient nematode migra- tions and it seems possible that the gradient of electrical potential created by the roots could contribute t o their attraction for nematodes.

MOISTURE GRADIENTS

Humidity gradients can be established in the soil by addition of water or by evapotranspira- tion. When they were placed in a moisture gradient, the infestant stages of Globodera rostochiensis (Wallace, 1960), Ditylenchus dipsaci (Wallace, 1961.) and Meloidogyne javanica (Prot, 1979) migrated towards the wet end. The moist- ure gradients affected nematode migrations in the soil, however, Wallace (1960) reported tha t the host roots counteracted the response t o a moisture gradient.

CONCENTRATION GRADIENTS OF MINERAL SALTS

Dropkin, Martin and Johnson (1958) demon- strated Lhat high Salt concentration inhibited movement of juveniles of Heterodera. and Meloi- dogyne within the eggs. Ibrahim and Hollis (1967) and Evans (1969) indicated that minera1 salts influenced the movement of Tylencho- rhynchus martini and Globodera rostochiensis. Warcl (1973) and Dusenbery (1974) have shown that Caenorhabditis elegans was' attracted to different anions and cations while Stringfellow

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J . C. Prot

(1974) observed that the hydroxyl ion was an attractant t o the male of Pelodera strongyloides.

Prot (1978u) indicated tthat eleven of twelve mineral salts tested exhibited a significant repul- sion t o juveniles of Meloidogyne javanica ; exami- nation of tracks of these juveniles in a Salt gradient showed that the repulsion was the result of an orientation of their movement (Prot, 1978~). This capacity t o migrate toward the region having the Iower Salt concentration was common within one population of M. javanica and two populations of M . incogni fa , while with Heferodera oryzae, only NaCl acted as a repellent among four salts tested, and none were repellent to Scufellonema cavenessi (Prot, 1979~). The sensitivity of the juveniles of Meloidogyne is very great (Prot, 1979a) and it is possible that their orientation along the mineral salts gradient created by the roots, partly explains the attrac- tion of roots for. these nematodes.

PH Little information is available on the influence

of pH on the migration of phytoparasitic nema- todes. Jairajpuri and Azmi (1978) observed that in general nematodes aggregated in a p H range from 5.5 to 8, when they were placed in a pH gradient. Bird (1959), on the other hand, found that the juveniles of Meloidogyne were not attracted to any particular pH. Since there is a paucity of data available, it is dificult to speculate on the influences of pH gradient on the migration of' phytoparasitic nematodes toward their hosts.

ROOT DIFFUSATES

Weischer (1959) observed that the juveniles of Globodera rosfochiensis and Heterodera schach- tii moved faster and farther when they were in contact with root diffusates of potato or sugar- beet. A factor(s) emanating from the roots and stimulating the movement of Hemicycliophora paradoza was left in the soil after a culture of millet (Luc, 1961 ; Luc, Lespinat & Souchaud, 1969). The same observation was made with Meloidogyne in soils that had supported tomato growth (Prot, 1975). Moreover, Azmi and Jairaj- puri (1976) demonstrated that Hoplolaimus indicus and Helicotylenchus indicus increased their rate of movement as they approached the

312

host. From al1 these experiments it appears tha t root diffusates released into the soil increase the velocity of plant,-parasit.ic nematodes. How- ever, this is not the only action of root diffusates, they also attract nematodes.

The attractants of roots remain in the soil after the plants have been removed (Wallace, 1958 ; Luc, 1962 ; Prot, 1975) and the degree of orientation toward the root area increased with the time the roots were in the soil (Wallace, 1960). Wieser (1955) using tomato, and Lee and Evans (1973) wit,h rice observed that root diffusates obtained in water attracted Meloido- gyne hapla and Aphelench.oides besseyi respect- ively . Viglierchio (1960), Lownsbery and Viglier- Chio (1960, 1961) demonstrated that this attrac- tion was in part due t o a dialyzable agent ema- nating from the roots. Analysing the root diffusates of tomato and testing their different components, Bird (1959, 1962) found that the juveniles of Meloidogyne javanica and M : hapla responded positively t o ascorbic acid, giberellic acid and glutamic acid.

There is considerable evidence tha t some plant-parasitic nematodes, mainly Heterôdera and Meloidogyne, have their velocity increased and are attracted by the root diffusates reIeased by their hosts.

CARBON DIOXIDE AND OSYGEN

Carbon dioxide has a particular place among root diffusates, because it is produced by every root and is quantit>atively the most important product. Consequently, many studies have been devoted to the behaviour of plant-parasitic nematodes dong a gradient of this chemical.

Klinger (1959) observed that Ditylenchus dipsaci moved towards carbon dioxide intro- duced in the soil with a capillary tube ; the attraction took place in the absence of a redox potential and pH gradient (Klingler, 1961). Some other phytoparasitic nematodes also have their movement oriented dong a CO, gradient. Johnson and Viglierchio (1961) showed that the juveniles of M . hapla, 144. j avan ica and H . schachtii accumulated around a source of CO,. Pratylenchus penetrans was also attracted towards this gas (Klingler, 1972 ; Edmunds & Mai, 1967). Analysing the behaviour of D. dip- saci along a CO, gradient, Klingler (1963)

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Migra€ ions of plant purasitic nematodes

determined that the minimum concentration difference necessary for a directed movement

' to occur was between 0.08% and 0.15% per cm. These authors suggested that in a natural soi1 such a gradient could be created by the roots over some millimeters and perhaps as much as 1-2 cm. Other authors believe that CO, may not be the root attracting factor, or at.least may not be the main factor. Peacock (1961) found that charcoal prevented the invasion of the roots by Meloidogyne incognita and that strongly basic ion eschange resins failed to prevent the infestation ; he suggested that, if the CO, was the attracting factor, the resins must have the same effect as charcoal. Bird (1960) stated that if the juveniles of M . javanica , H . sclzachtii and Pratylenchus minyus were grouped around a CO, source this would 'not explain why the most attractive portion of a plant root for Meloidogyne is the region of ce11 elongation ; this he believed was because in this area the redox potential is lowest. If CO, was present in greater concentra- tion in this region, i t would tend t o raise the redox potential. Moreover, he reported that a living root attracted M . javanica juveniles away from a CO, source. He also found that galls attracted juveniles more strongly than adjacent healthy tissues but he did not find a significant difference of CO, production between galls and adjacent healthy areas (Bird, 1962). El-Sherif and Mai (1969) observed that the CO, released from germinating alfalfa seeds failed to attract Pratylenchus penetrans in the absence of the heat gradient created by these seedlings.

Reproducing the experiments of Rogers (1966 a ; 1966 b ) , Croll and Viglierchio (1 969) found that the positive response of the infective stages of Ditylenchus dipsaci to a gradient of CO, was inhibited after a treatment with KI3. This response was restored when the juveniles were subsequently treated with H,S. They proposed a pattern of a chemoreceptor in which two free sulphydryl groups reacted with CO,.

Despite some contradictions between the foregoing, it seems that CO, may be one of the attracting factors for plant-parasitic nematodes toward host roots, even if it is not the main and only factor. But it is difficult to conceive that it could influence their movements over more than 1 or 2 cm from the roots.

Revue Nkmatol. 3 (2): 305-318 (1980)

If roots release CO, and absorb oxygen they create a negative gradient of O,. Klingler (1965) did not find an oriented movement of Di ty - lenchus dipsaci in a descending gradient of oxygen. While Johnson and Viglierchio (1961) observed the aggregation of the infective stages of H . schachtii and D. dipsaci around an oxygen source, Bird (1959) concluded that 0, did not attract the juveniles of M . javnnica and M . hapla and Klingler (1961) even found that O, has a repellent effect on D. dipsaci. Oxygen therefore seems to have no effect on the directional migra- tion of phytoparasitic nematodes.

MICROORGANISMS Free living nematodes are attracted toward

fungal and bacterial colonies on which they feed (Klink, Dropkin & Mitchell, 1970 ; Andrew & Nicholas, 1976 ; Pollock & Samoiloff, 1976). The nematophagous fungi appear t o be able to attract their prey (Balan & Gerber, 1972) ; Monoson, Galsky, Griffin & McGrath, 1973 ; Field & Webster, 1977 ; Jansson & Nordbing- Hertz, 1979). Rhizospheric microorganisms and those associated with the roots can influence the movements of the plant-parasitic nematodes. Edmunds and Mai (1967) observed that alfalfa seedlings infested with Fusar ium oxysporum were more attractive t o Pratylenchus penetra.ns than healthy seedlings. The juveniles of Meloi- dogyne aggregated around Escherichia Coli colo- nies (Bird, 1959) and those of Heierodera sclzach- tii were attracted towards some bacteria isolated from the rhizosphere of sugar-beet (Bergman & Van Duuren, 1959). Linford (1939) found that bacterial colonies incited the grouping of juve- niles of Meloidogyne only when anaerobic condi- tions were created which stopped their move- ment and prevented them from escaping.

It appears that microorganisms may influence the migrations of phytoparasitic nematodes and those living in the rhizosphere could be part of the root's attraction. This appears to be possible even though root attraction has been observed under sterile conditions (Blake, 1962 ; Lavallee & Rohde, 1962).

Conclusions How can one integrate al1 the observations

and information on plant-parasitic nematode

313

J . C . Prot

migrations collected over more than five dec- ades ?

It appears that Steiner (1925) was correct about several aspects. Phytoparasitic nematodes possess sense organs which allow them t o orient their movements over gradient,s of chemicals, temperature, redox-potential, etc. It appears certain that the amphid is one of these organs. Moreover, the sensitivity of this organ(s) is very high. Nematodes are capable of orientation in chemical gradients in which the highest concen- tration is only 10-3 M/1, in CO, gradients with a cpncentration difference of 0.08% per cm and in temperature gradients of 0.0330 per cm.

Plant-parasitic nematodes are attracted tow- ards host plant roots. This is widely accepted. The attraction does not appear to be seleclive' generally, althon,gh some results do show a select,ivity.

The roots produced some information which allowed the .nematodes t o orient their move- ments. This concept is accepted by a majority of authors. Differences in opinion concern only the identity of the stimulus (i). On review of al1 the observations, disagreements appear to be groundless ; the essential point seems t o be that almost every stimulus tested is able to influence nematode migration (a t least for those nema- todes belonging to the genera Heterodera, Globo- dera, Meloidogyne, and Ditylenchus) . Moreover, al1 of these stimuli seem to participate in the orientation of the invasive stages t>owards the host roots ; a t least over short distances (1-2 cm) from the roots.

A more controversial point is the ability of phytoparasitic nematodes to migrate over large distances. It has been generally accepted that these nematodes are not capable of such migra- tions. However, many exceptions ta this general view have been observed with nematodes belong- ing t o various genera (Angu ina , D i t y l enchus , Globodera, Heterodera, Meloidogyne, Trichodorus and Tylenchorhynchus). It is probable that not. al1 nematodes are able t o migrate over large distances in the soil ;. but, before concluding whether such migrations are exceptional or not, i t seems necessary to perform experiments with many types of nematodes under various condi-

. tions, especially within different soil types. When migrations over more than 10 cm occur,

- are . . they due to a random movement followed ,~

314

by an attraction wit4hin the last 1 or 2 cm around the roots, or can the nematodes locate the host roots a t distances of 10 or 20 cm ? In considering the last suggestion, it is dificult to conceive that the gradients of temperature, redox potential or CO, creat>ed by the roots, have an action over such distances. In this case only the secretions of roots (or their bacterial by-products) could be thought capable of establishing a gradient, over such distances if they are carried by water percolation.

The more important fact appears to be that phytoparasitic nematodes are attracted by the host roots and that the the sensitivity of the perception is very high. This concept is impor- tant because it could open a new possible method of control using products stopping the action of the nematodes' neuroreceptors and thereby preventing or decreasing the invasion of the roots.

ACKNOWLEDGMENTS

The author i s grateful to Drs. S. D. Van Gundy and R. Mankau for their suggestions and revision of the English text.

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Revue Nématol. '3 (2) : 305-318 (1980)