Published data revealed that Tagetes
spp. suppress polyphagous endoparasitic root nematodes, that the effect varies, perhaps between Tagetes
spp. and cultivars, certainly between nematode genera and perhaps between species and strains. The effect is sometimes striking but the picture in general is far from complete and not clear. This situation determined the three objectives of our investigation: occurrence and significance of Tagetes
effect, interpretation, and possibilities of application in agriculture.
For most of the trials plants were cultivated under controlled and field conditions, and their growth evaluated; nematode populations were collected, cultivated, maintained and transferred; nematodes in soil and plant tissues were counted and results were analysed statistically. Several special techniques were used occasionally as indicated in the relevant sections.
The occurrence and significance of special Tagetes
effects on plant nematode population were determined with species of Pratylenchus, Meloidogyne, Tylenchorhynchus, Rotylenchus
other ectoparasitic nematodes, Ditylenchus
spp. were markedly suppressed by Tagetes
in tube cultures (Tables 1-5) and in field trials (Tables 6 and 7, Figs 1 and 2). This was true for P. penetrans, P. crenatus, P. neglectus
and probably P. thornei.
Soil type may be of influence on the result. There were great differences in effectiveness between Tagetes
spp. and cultivars. The effectiveness against Pratylenchus
spp. decreases in the order T. patula, T. erecta, T. minuta,
with T. patula
markedly better. T. patula
Harmony suppresses field populations of Pratylenchus
spp. in a few months and fallow requires a few years to reach a comparable low final density of these nematodes. Density never fell to zero, probably because of limited reproduction on weeds and limited reproduction on Tagetes
itself if it is grown for a full season. There was no evidence that resistance of Tagetes
was broken or that nematode strains resistant to Tagetes
effects arose even after 7-10 successive crops of T. patula.
Biennial rotations of T. patula
and good hosts kept Pratylenchus
spp. at a low density, except the population of P. thornei
on heavy soil which fluctuated at a rather high level (Fig. 2).Tagetes
spp. were generally as effective or better than fallow in suppressing Meloidogyne
spp. in tube cultures (Tables 8-12), although with some notable exceptions. Meloidogyne
larvae were less persistent than Pratylenchus
larvae in fallow soil. T.patula
severely suppressed M. hapla, M. incognita, M. arenaria
and M.javanica. T. erecta
was also suppressive but slightly more syncytia formed in all four Meloidogyne spp.; M. hapla
reproduced and maintained a small population on T. erecta. T. minuta
differed markedly from the earlier species in that it suppressed M. hapla
and M. incognita
completely and M.javanica
almost completely, whereas M. arenaria
could breed on this plant and reach considerable densities in both roots and soil. Any general effect by Tagetes
on Meloidogyne is
therefore complicated by certain exceptions which may account for conflicting published results.
Tube and field trials showed that Tylenchorhynchus
spp. were suppressed by T. patula
in different soils (Table 7), that Tyl. dubius
was suppressed better and more rapidly by T. patula
than by fallow (Fig. 3A, B; literature), and that T. erecta
and T. minuta
were about as effective as T. patula
against Tyl. dubius
(Table 6). Tyl. dubius
was suppressed slightly less effectively and less rapidly than Pratylenchus
spp. in the same soil by T. patula
The data on R.robustus
supports the view that Tagetes spp.,
at any rate T. patula
Golden Harmony and Harmony, maintains a rather high density. Unexplained peaks of the density under Tagetes
and fallow make it difficult to indicate any Tagetes
effect at all; factors other than the presence of higher plants may govern the population dynamics of this species.
The genera Hemicycliophora, Paratylenchus
are not generally suppressed by Tagetes
cultivars. Specific host-nematode relationships may vary as widely as is the case with these nematodes on other plants, and no special Tagetes
effect can be demonstrated against these ectoparasites. Some species breed profusely on certain Tagetes
spp. but are not affected by other Tagetes
The stem nematode D. dipsaci
may reproduce to a limited extent and cause typical symptoms in T. patula
and T. erecta,
but not in T. minuta.
The same is true for the foliar nematode A. ritzemabosi
(Plate 1A and B).
The data leave no doubt that certain Tagetes
spp. suppress certain species of plant nematodes unusually strongly. The Tagetes
effect manifested itself most clearly with Pratylenchus
spp. and Tyl. dubius,
but was evidently not present or not marked against R. robustus
and several other ectoparasitic genera, nor against D. dipsaci
and A. ritzemabosi.
The results alone or combined with published data do not fully explain the mechanism. For a further analysis the exoradicular effects, the effects on the surface of the plant or during penetration, and the endoradicular effects were subsequently studied.
Exoradicular effects may contribute to, but not explain the larger part of the Tagetes
effect. As with the good host red clover, P. penetrans is
not particularly attracted nor deterred by growing roots of T. patula
on agar plates, but there was some aggregation around the roots in soil (Table 14), though it concerned only part of the soil population (Fig. 5). Percolates from pots of T. patula,
red clover, apple or without a plant did not differ in effect on activity or mortality of P. penetrans in vitro.
Survival of P. penetrans
in water cultures of T. patula
and T. minuta
was only slightly less than in water culture of apple, control solution or distilled water, and the effect was at any rate slight and unspecific (Table 15). Tagetes
soil was distinctly nematicidal for some days after the roots have been removed. This effect, however, was not very strong and was not specific for Tagetes
, because red clover was equally and apple even more effective than T. patula
and T. minuta
(Table 16). Damage or kill of nematodes outside the root may therefore play a role, but it is apparently not the essential part of the Tagetes
Root systems of three different Tagetes
spp. were penetrated by M. hapla
larvae as much as root systems of a suitable host. The same holds for penetration by P. penetrans
, except perhaps for T. patula
which fewer nematodes entered than other Tagetes
spp. or good hosts in most trials (Table 17). As a rule only a few of the larvae around the roots succeed in penetrating.
Endoradicular influences comprise nematode survival and development, nematicidal effects and histological reactions in Tagetes
tissues. M. hapla
larvae enter Tagetes
spp. to the same amount as tomato within a week. Only a few of the larvae around the roots succeed, although potential sites for penetration are present in excess. The unsuccessful nematodes outside the root decrease rapidly in number, more rapidly in the presence of growing plants than in fallow soil, which may be important for the population dynamics of nematodes in general. M. hapla
survives for at least 4 weeks within roots of Tagetes
spp., but development beyond the infective second larval stage is hardly noticeable in T. patula
and T. minuta
, whereas only a few larvae develop and reach adulthood in T. erecta
The picture is similar with P. penetrans
. The percentage penetration is generally low in all plants, but significantly lower in T. patula
than in T. erecta
, T. minuta
or red clover (Table 19, Fig. 6). T. patula
may resist penetration by this nematode The main difference between a suitable host such as red clover, and T. patula
is that nematodes reproduce in the first plant and decline or remain few in T. patula.
In T. minuta
the nematodes survive and may even develop and multiply, though at slower rate than in red clover (Figs. 6, 7 and 8). T. patula
, T. minuta
and red clover represent degrees of host suitability from almost zero through low to very high (Fig. 7, Table 20). The equilibrium density under T. patula
is very low but not zero because some reproduction occurs when the plants have grown a long while. The percentage males among the sexually differentiated nematodes is not higher in the very resistant T. patula
and does not increase with ageing of host plants, as has often been published. T. patula
allows very little escape or survival of P. penetrans
once the nematodes have entered the roots, whereas the population in T. minuta
roots does escape and may be infective as in suitable hosts (Tables 21 and 22).
Root extracts of Tagetes
spp., contrary to root exudates, contain a nematicidal principle which manifests itself against P. penetrans in vitro
from the third day on (Fig. 9A, B, C). Extract of T. patula
is more effective than extract of T. minuta
and the latter is more effective than extract of potato or control solutions. Fractioning of root extracts of T. patula
over a column of Sephadex G-75 indicate high mortality in a later fraction. No attempt was made to identify the active principle(s) in this fraction. This effect in vitro may be related to the Tagetes
effect on nematodes in soil. It may be caused by the nematicides such as the thiophenes isolated from Tagetes
roots by Uhlenbroek & Bijloo (1958, 1959). There was some nematode kill in potato root extract too, distinctly less than in Tagetes
extract but distinctly higher than in the control solutions. This indicates the presence of a weak nematicidal effect in potato root extract and may support the indication recorded earlier that plants establish or induce in general an "antinemic potential" by means of their exudates or other substances in water or soil. The Tagetes
effects are much stronger and evidently differ from it.
Histological reactions as part of the endoradicular influences of Tagetes
on penetrated nematodes are not conspicuous. Tagetes
cultures, unlike most other plants, normally grow well and have well-developed root systems without discoloration in soils with dense populations of Meloidogyne
spp. Despite this healthy appearance Tagetes
roots may show barely visible histological reactions after such nematode infestations.M. hapla
larvae penetrate the root apex of T. patula
in much the same way as that of tomato. They do not normally develop nor cause marked necrosis or swelling in the roots of T. patula
. Occasionally, however, small syncytia or sometimes even small galls occur associated with a developing larva. Unlike tomato, T.patula
develops few and very small syncytia and galls and only slowly, and the nematode often dies and syncytia often abort in T. patula
penetrates young roots of T. patula
, T. minuta
and red clover at random sites on their surface except at the apex and causes cortical lesions in all three plants. The lesions in T. patula
are small, dark and necrotic but do not abort from surrounding cortex tissue; they normally harbour only 1-3 nematodes, often dead, dying or twisted. In T. minuta
the lesions appear slower, are larger and less dark than in T. patula
; the number of nematodes per lesion may be up to 38 and often occur outside lesions. Red clover lesions appear still slower, are usually larger and contain a large breeding population. Histological reactions, therefore, largely coincide with nematode development.
The endoradicular effects are apparently instrumental in the nematode suppression by Tagetes
spp. They are incorporated in or super-imposed upon the common plant-nematode relationships which are different for each association and may therefore influence the result. It is suggested that the special nematicidal principle in Tagetes
is made up of more components, of which thiophenes recorded up to now from T. erecta
, and that the components or their relative weights vary between Tagetes
spp. Some other Compositae
related closely to Tagetes
spp. were also found to be effective against P. penetrans
and also contained the same thiophenes as found in Tagetes
or hitherto unidentified active principles. T. patula
is probably superior to other Tagetes
spp. in its effect against P. penetrans
because necrosis appears earlier and more acutely. This may be a consequence of more rapid intoxication of the nematodes, as in root extracts.
Ectoparasitic cortex feeders of the genus Tylenchorynchus
are affected less and root-vessel feeders are evidently not influenced by the nematicidal principles in Tagetes
roots, probably because they do not undergo the same type or degree of contact with the Tagetes
tissue. The Tagetes
effect, therefore, seems to be generally strong for endoparasitic root nematodes or cortical feeders, but varies even within this group with the different plant-nematode associations.
The agricultural value of Tagetes
as a source of organic matter, stains, therapeutics, or other chemicals, and as ornamentals is limited and has up to now supported only small-scale cultivation. The use of Tagetes
crops for suppression of plant nematodes and the marked growth improvement obtained in main crops, is handicapped by the lack of value of the crop. Furthermore Tagetes
spp. and cultivars are limited in their agricultural applicability. Nematode suppression is the primary determinant of their practical value so that T. patula
particularly the cultivars Golden Harmony or Harmony are recommended. They are more effective against Pratylenchus
and at least as effective against Meloidogyne populations, and appear to be as good or better than other Tagetes
cultivars for growing and handling as a crop. Seed characteristics, rapid development as an autumn crop and winter-hardiness could all be improved, whereas a search for profitable use of the crop is desirable. Breeding of Tagetes
spp. have resulted in a great assortment of ornamentals, and prospects seem good for the plant breeder of combining strong nematicidal effect with useful agricultural properties.
The desired characters will depend on the type of agriculture. Tagetes
grown as a full-season crop has been found effective by several workers and may cause striking growth and yield increments, it may find use in areas where valuable main crops are grown and where land rent is low, as in some tropical and subtropical countries. Tagetes
as a spring crop does not seem promising in temperate climates due to its slow seedling growth. Even when sown densely, 10 cm apart on 15 May, minimum densities of Pratylenchus
could be achieved only after about 2 months; these densities appear later when greater plant distances are taken (Fig. 10). Tagetes
grown as an autumn crop has better possibilities. The degree of development of autumn Tagetes
is evidently critical for its effect, and this varies strongly from year to year. Autumn Tagetes
may be very effective in nematode suppression as well as in yield increase of main plants in certain years (Tables 23, 24 and 25), but the earliest sowing dates after an early pea crop varied in the period 1961-1968 from 6 July to 14 August, and a good development was obtained in only 4 out of 8 years (Table 6). Continuous autumn Tagetes
, however, may be effective despite failure in certain years. Autumn Tagetes
should be sown not later than the end of July and 10 rather than 25 cm apart is advisable.
Simultaneous culture of Tagetes
with a main crop appeared to be effective around and between trees and woody ornamentals and may be promising in more cases, especially since sowing at 60 cm apart completely suppressed nematodes, though slower than when closer sown. Sowing between rows is practized incidentally (Plate IIC and D). Sowing under cereals and other high crops to give the crop a quicker start after harvesting the main crop has not so far been promising, because only few weak plants survived.
Autumn application after a main crop and application between rows of a main crop may be promising under certain conditions. The technical possibilities increase when climatic conditions allow a better growth in the autumn or when agricultural systems allow a full-season crop.
Yield of main crops after Tagetes
may be increased by nematological or other growth factors or both. Tagetes
promoted growth of apple seedlings in soil with P. penetrans
to 167 % of fallow infested soil, though Tagetes
decreased growth in uninfested soil; allowance for the nitrogen used by Tagetes
would lead to a higher growth promotion in infested soil (Table 27). The decline in nematode population continued markedly after the growth of Tagetes
had been disrupted by removal of the tops. Direct mulch with a natural dosage of Tagetes
roots suppresses P. penetrans
much better than other mulches or fallow. It is probable that there is a significant aftereffect also under field conditions. Leaf mulches were also effective in suppressing P. penetrans
, but Tagetes
leaves were less effective than apple and no specific nematicidal effect of Tagetes
leaves could be demonstrated. The results in uninfested soil show that cultivation of Tagetes
and removal of tops decreases soil fertility in unfertilized soil (Table 27). The addition of root or leaf mulch generally increases soil fertility and therefore growth of test plants (Tables 30, 31, 32). These effects, however, are unspecific, and would have been smaller in fertilized soils, uninfested or infested. The dominance of nematicidal over non- nematicidal effects of Tagetes
is clear for the growth of apple seedlings in soil infested with P. penetrans
. The relative weight of these factors may of course be different in other plant nematode relationships.
Our results, therefore, confirm or substantiate the marked Tagetes
effect, but also the variation between plant-nematode relationships. The Tagetes
effect is exceptional in nature, though not completely restricted to the genus Tagetes
because it does occur in some genera ofthe Heleniae
. The effect appears to be centred inside the roots and is evidently correlated with the presence in these plants of strongly nematicidal thiophenes, which are rare elsewhere in nature. The fact that it is conspicuous against endoparasitic polyphagous root nematodes and not against epidermal and vessel feeders is understandable from the difference in parasitic way of life.
Histopathological reactions to nematode invasion vary between Tagetes
spp. This may explain the stronger effect of T. patula
on P. penetrans
than of other Tagetes
spp. The concept of nematode intoxication by nematicidal thiophenes and histopathological resistance phenomena may be interrelated and are not necessarily contradictory.
Use of Tagetes
spp. often markedly increases yield of main crops, but is limited by type of agriculture. In temperate regions Tagetes
grown simultaneously with the main crop or grown in the autumn after the main crop is considered promising. Slow seedling growth, high light requirement and frost susceptibility of available cultivars are disadvantages. Tagetes
has better prospects in tropical and subtropical agriculture.