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Nematicidal effects of some plant-extracts

to Aphelenchoides composticola (Nematoda)


infesting mushroom, Agaricus bisporus
Panvinder S. GREWAL*
Nenzatology Sectiopt, National Centre for Mushroonl Research and Training,
Solan - 173 213, India.

SUMMARY

Leaf, flower or seed-extracts 29 of dominant plant species found in northern India were screened against adult and juvenile stages
of Aphelenchoides conzposticola infesting white button mushroom, Agancus bisporus. Leaf-extracts of Bougainvillea spectabilis,
Calotropis procera, Cedrella tootza, Jacaranda acutifolia, Melia azadirach, Ricinus conmunis and Tagetes patula and seed-extracts
of M. azadirach and R. conzlnunis were highly toxic to this nematode. Nematicidal activity in leaf-extracts of most plant species
varied withthe method of extract preparation. Two statistical models,viz., analysis of variance and probit analysis, were compared
to test the effectiveness of the extracts. The role of incorporating dried leaves of pre-tested plants in mushroom compost for
management of A. composticola populations is also discussed.

RÉSUME

Action nématicide de quelques extraits végétaux envers Aphelenchoides composticola (Nenzatoda)


infestant le champignon de couche, Agaricus bisporus

Des extraits provenant de feuilles, de fleursou de graines de plantes dominantes dans le nord de l’Indeont été testés envers les
adultes et les stades juvéniles d‘Aphelenchoides composticola, infestant le champignon de couche, Agaricus bisporus. Les extraits
foliaires de Bougainvillea spectabilis, Calotropis procera, Cedrella toona, Jacaranda acutifolia, Melia azadirach, Ricinus conznzunis
et Tagetes patula, et les extraits provenant de semences de M. azadirach et de R. comlnunis sont très toxiques pour le nématode.
L’action nématicide des extraits foliaires de la plupart des espèces végétales varie suivant la méthode de préparation. Deux modèles
statistiques (analyse de variance et analyse ‘‘ probit ”) ont été comparés pour les tests d’activité des extraits. L’incorporation de
feuilles séchées de plantes pré-testées au compost des champignonnières pour contrôler les populations d’A. conzposticola est
également discutée.

Mycophagousnematodes Aphelenchoidescomposti- compost at the timeof spawning can lead to significant


cola, A. sacchan’ and Ditylenchus mnyceliophagous are loss in yield (Arnold & Blake, 1968; Grewal, 1987).
reported to cause heavy losses in yields of mushroom, Although nematicides including aldicarband phorate
Agaricus bisporus in commercial farms in India (Chha- (Cayrol & Ritter, 1972; Chhabra & Kaul, 198l), beno-
bra & Kaul, 1982; Sharma, Thapa & Nath, 1981). myl, fenamiphos, oxamyl and thiabendazole (McLeod
Because of the lack of bulk pasteurization facilities and & Khair, 1978), carbofuran,diazinon and dichlorvos
the endemic and acute nature of the nematode problem (Grewal & Sohi, 1987a) have been shown to control A.
in some potential and traditional mushroom growing composticola in mushrooms, recent reports have illus-
areas (including Himachal Pradesh, Jammu and Kash- trated toxic effects of pesticides on mushroom mycelium
mir, Punjab and Haryana),some growers areclosing and losses in yield (Grewal & Sohi, 1987b; Grewal,
d o m their mushroom farms (Thapa, Sharma & Nath, Upadhyay & Sohi, 1988; White, 1986). Furthermore, the
1981; Grewal & Sohi, 1987~).Both A. composticola and use of systemic nematicidesin mushroom culture results
A. sacchari cause u p to 100 OO/ loss in mushroom yield in toxic residues in the produce(Bahl & Agnihotri,
depending upon theinitial inoculum and time of intro- 1987).
duction into the compost (Grewal, 187; Sharma,Thapa Plant-extractsnematicidalagainst A. composticola
& Kaur, 1985). Damage thresholds of A. composticola (Seth et al., 1986; Grewal & Sohi, 1988) wouldbe a
are so low that even a single nematode per 200 g of cheaper and effective alternative. Grewal (1988) dem-

* Present address :Entonzology and Insect Pathology Section, AFRC Institute of Horticultural Research, Littlehampton, West Sussex,
BN17 6Lc Great Britain.

atol. Revue (3) :31 7-322 (1989) 317


P. S. Grewal

onstrated that the incorporation of dried leaves of four were run by adding 1 ml distilled waterto the nematode
different plants to mushroom compost resulted in the suspension. There were seventreatmentsreplicated
suppression of A. composticola populations below econ- threetimes in afactorialdesign : cold orhotwater
omicinjury level and in an increase in the nitrogen extract,
three
concentrations and a distilled water
content of the compost and the yield of the mushroom, control. The cavity blocks were covered and incubated
Agaricus bisporus. The present paper reports the results at 250 for 48 hours.Leaf-extracts(bothCWE and
of further trials wherein most of the dominant plant HWE)of only one plant species were tested at a time.
species(with abundant foliage) fromnorthern India Nematicidaleffects of seed or flower-extracts (only
were screened to test the leaf, seed or flower-extract HWE) were tested similarly (three concentrations and
toxicity against A. composticola. one control).
While recording the data on nematode mortality, the
active lethaleffects(nematicidal) were distinguished
Materials and methods from the nematostatic effects (suppressionof nematode
movement). The extract solution in cavity block was
PREPARATION
OF EXTRACTS diluted (1:128) with distilled water, and the numbers of
Leaf-extracts of29 plant species viz., Allium cepa, deadIlive nematodes were recorded after 24 h.
Althea rosea, Azadirachta indica, Araucaria sp., Bauhi-
nia variegata, Bougainvillea spectabilis, Brassica campes- ANALYSISOF DATA
tris, Callistemon lanceolata, Calotropis procera, Cannabis Data foreach specieswere analysed by probit analysis
sativa, Cedrella toona, Cedrus deodara, Chenopodium and analysis of variance (after arcsin transformations).
album, Chrysanthemum cinerarifolium, Clerodendron The hot andcold water assays were tested for differences
infortunatum, Curcuma longa, Dahlia variabilis, Ficus using parallel probit regression analysis (Ross, 1980).
hispida,Jacaranda acutifolia, Lantana camara, Melia Estimates of LC,, (as percentages) and theslope of each
azadirach, Morus alba, Nerium indicum, Pinus roxbur- assay are presented in Tables 1 & 2.
gii, Populus ciliata, Ricinus communis, Tagetes patula, Tests of significance are based on the chi-squared
Thuja sp. and Zingiber officinale were prepared both in statistic :
cold and hot water. (a) heterogeneity : tests for consistency of repliCates
Coldwaterleaf-extracts (CWE) were prepared by and fit of the model;
blendingthe leaves of testplants in distilledwater (b) parallelism : tests for parallelism of probit re-
(100 g/500 ml) in a mixer at 250 for 2 min. The extracts gression line;
were then filtered through aWhatman filter paper No.1 (c) position : tests for differences in LC50 assuming
and stored at 50 until needed. Hot water leaf-extracts a parallel response.
(HWE) were prepared by boiling the leaves of test plants
in distilledwater (100 g/500 ml) for 20 min.After Results
cooling, the extracts were filtered as described above, the
volume adjusted to 500 ml and stored at 50. LEAF-EXTRACTS
Hot water extracts were also prepared from the seeds
of A. indica, C. lanceolata, M. azadirach and R. comrnu- The leaf-extracts of seventeen plant species, out of 29
nis and also from the flowers of B. spectabilis, C. cine- tested, showed nematicidal effects against A. composti-
rarifolium, D. variabilis and T. patula. cola. The data on per cent nematode mortality caused
by the cold or hot water formulationsof the leaf-extracts
NEMATODE
CULTURE of these plants are presented in Fig. 1.
Cold water preparations of the leaf-extracts of C.
Aphelenchoides composticola Franklin was cultured in procera and J. acutifolia caused 100 O/O nematode mor-
glass bottles on grain spawnof the mushroom, Agaricus tality at 5 O/o concentration. Furthermore, 100 O/O mor-
bisporus (Lange)Singer(Strain S l l ) as describedby tality wasalso produced by cold water extracts of B.
Grewal(1988). The nematodes were extracted from the spectabilis, C. toona, M. azadirach, R. communis and T.
infested spawn using Baermann funnel (Hooper, 1986). patula at 10 O/o concentration. Hot water leaf-extracts of
The nematode suspension with al1 life stages was then only C. procera, J. acutifolia and R. communis caused
calibrated. 100 O/o nematode kill at 10 O/O concentration.
Results from the probitanalysis and of the analysis of
SCREENING FOR NEMATICIDAL EFFECTS variance of thedataare presented inTable 1. T h e
efficacy of the leaf-extracts and of their formulations
Extracts were used at 2, 5 or10 O/O concentration were compared at two levels : mean overall effect at
(dilutions in distilled water). One ml of thediluted 2-10 O/o concentration by the analysis of variance and at
extract was added to a cavity blockcontaining110 the levelof 50 O/o nematode kill (LC,, values) by the
( k 12) nematodes in one ml of distilled water. Controls probit analysis.

318 Revue Nématol. 12 (3) :31 7-322 (1989)


Effects of plant-extracts to Aphelenchoides composticola

Table 1
Effects of leaf-extracts on A. conzposticola :probit analysis and analysis of variance

varianceofAnalysis
analysis
Probit

Plant species water Cold Extract


Significance
Hot water TxC
int.x
LC50
Slope
LC50
Slope
Position
Parallel-
Hetero-
Type
Conc.
(O/d geneityS ism

Althea rosea 19.2' 1.92 4.6 3.72 *** *** ns ***C *** ***
Azadirachta indica 3.1 2.36 4.2 2.69 *** ns
ns ns *** ns
Bougainvillea spectabilis 2.6 3.24 75.9' 1.22 *** *** ns *** *** ***
2.49
Callistemon lanceolata 7.4 1.77 11.1' *** * * ns *** ns
Calotropis procera < 2.0* nd2.50 1.4' * *** ns *** *** ***
3.44
Cannabis sativa 3.2 2.45 9.1 *** *** * *** *** **Y

Cedrella toona 1.41 43.4' 4.64 2.8 *** *** ns *** *** ***
Chenopodium 4.56albunz 4.0 2.41 3.6 *** *** *** ns *** ***
2.61 5.7 2.13 5.4
Chysanthenlum cinerarifoliunt ns ns * ns *** ns
variabilisDahlia 0.86 0.4 > 10.0' nd *** ns * *** ** ns
acutifolia
Jacaranda 2.0 nd 0.7' 1.37 *** *** *** ns *** ***
Lantana canzara 3.18 4.4
1.9+ 2.00 *** *** *** *** *** ***
Melia azadirach 3.86 2.8 0.58 0.1' *** *** ns *** *** ***
roxburgii
Pinus 3.92 3.4 1.45 1.0' *** * *** *** *** ***
1.95
Populus ciliata 12.4' 1.26 9.1 *** ns* ns *** ns
Ricinus comnzunis 2.07 1.0' 0.8' 2.13 * ns *** ns *** ns
Tagetes patula 2.2922.4'4.41 3.5 *** * ns *** *** ***
ns : not significant (P > 0.05); * P < 0.05; ** P < 0.01; *** P < 0.001
nd :not determined-failure of probit analysisto converge
' : LC50 outside the range 2-10 Y O
: heterogeneity~-significance was in al1 cases due to lack of fit of the model and not variation between replicates
: Type x Concentration interaction

Table 2 Leaf-extracts (both cold or hot water preparations) of


the twelve plant species viz., A. cepa, Araucaria sp., B.
Effects of seed- or flower-extracts on A. conzposticola :
variegata, B. campestris, C. deodara, C. infortunatum, C.
Probit analysis and analysis of variance
longa, E hispida, M. alba, N.indicunl, Thuja spp. and
analysis
Probit
Analysis Z. officinale showed noorlittle (< 40 "O) nematode
of mortality even at 10 O/O concentration.
LC50 (%) Slope
Hetero-
variance
geneity SEEDOR FLOWER-EXTRACTS
SEEDEXTRACTS Hot water preparations of the seed-extracts of three
Azadirachta indica 3.7 3.82 ***' *** out of the four plant species testedwere highly toxic to
Melia azadirach < 2.0' nd nd *** the target nematode(Fig. 2). Seed-extracts of M . azadi-
Ricinus conmunis < 2.0' nd nd *** rach (at 10 O/o concentration) and R. c o n m u n i s (at 5 and
FLOWER EXTRACTS 10 O/o concentration) caused 100 O/O nematode mortality.
Bougainvillea specta- Seed-extracts of A. indica causedmore than 80 Oo/
ns bilis 3.68 8.6 *** nematode kill at andabove 5 O/O concentration. However,
Chrysanthentunz ci- C. lancedata showed little effect (maximum mortality,
ns
nerarifolium 3.62 8.7 *** 44 .)O"
ns 1.95 9.1
Tagetes patula *** Flower-extracts (only hot water formulations tested)
of three plant species out of the four species screened,
ns : not significant (P > 0.05); *** P < 0.001
showed nematicidal effects on the testnematode (Fig. 2).
nd : not determined-failure of probit analysis to converge
+ : LC50outside the range 2-10 O/o Although none of the plant species caused complete
S : Heterogeneity significancewas due tolack of fit of the model and mortality at the concentrations tested (2-10 ,)O" more
not variation between replicates than 50 O/O nematode kill resulted from the flower-ex-

Revue Nérnatol. 12 (3) :31 7-322 (1989) 3 19


P. S. Grewal

tracts of B. spectabilis, C. cinerarifolium and T. patula from the leaves. Both of these possibilities have been
at 10 O/O concentration. D. variabilis showed little effect supported by EgunjobiandAfolami (1976) Who
on the target nematode (maximum mortality, 26 "0). observed an increase in the toxicity of neem leaf-
Results of the probit analysis and of the analysis of extracts to Pratylenchus brachyurus after boiling.
varianceforbothseed- and flower-extracts of these Present findings revealed that the seed-extracts of A.
plants are summarised in Table 2. indica, M. azadirach and of R. cornmunis are highly
toxic to A. composticola. Recently, Devakumer, Gos-
Discussion wami and Mukerjee (1985) observed that limonoids
(compounds belonging to B-furano-triterpenoids) pre-
Nemato-toxic compounds in the leaf extracts of the sent in the kernels of neem (A. indica) are the main
Seventeen plant species out of 29 tested listed in Table nematotoxic principles. However, no such active nema-
1 were water-soluble and could be filtered, in contrasr ticidal compounds have yet been identified from the
to that of garlic (Alliaun sativumn) in which the toxins are seeds of M. azadirach and R. cornmunis.
water insoluble and cannot be filtered through m a t - The use of two different statistical models foranalysis
man filter paper No. 1 (Nath et al., 1982).However, of the data helpedtoelucidatesome of the relative
differential effects of leaf extracts of the plants tested advantages and disadvantages of the two models. Al-
and of their formulations (cold or hot water extracts) on though LC,, values are generally used to compare the
nematode mortality suggest that the active nematicidal
principles in various plants could be different. On the
basisof the effects of cold or hot water extracts on
nematode mortality (when the data were processed for
anabsis of variance, Tab. l), the plant species tested
codd be grouped into four distinct categories as fol-
lows :
(i) Wherehotand cold waterextracts were equally
effective, indicating the thermostable nature of their
active principles, e.g. Azadirachta indica, Callistemon
lanceolata, Chenopodiurnalbum, Chrysanthemum ci-
nerarifoliurn, Jacaranda acutifolia, Populus ciliata and
Ricinus cornmunis. However, the probit analysis re-
vealed that the LC,, values for cold of hot water assays
variedsignificantly for al1 plant species except c. m
2 100
cinerarifolium (Tab. 1). This showed that although
the two formulations of a leaf-extract do not differ à? 50
significantly, the concentrations at which 50 O/' of the
O
individuals die (LC,o values) may be variable.
(ii)Where nematicidal activity was observed in cold 100
water extract but was less (i.e. max. 25.6 %O nematode 50
mortality) in the hotwater extracts showing the ther-
molabile nature of the nemato-toxic principles, e.g. O
Bougainvillea spectabilis, Cedrella toona, Dahlia va- 100
riabilis and Tagetes patula. Grewal and Sohi (1988)
observed thatthe nematicidalcompounds inthe 50
leaves of Tectona grandis were also heat-labile. O
(iii)Where hot waterextracts, possessed nematicidal 2 5 10 2 5 10 2 5 10
activity but were signifitantly (p < 0.001) less toxic % Concentration
than cold waterextracts, e.g. Calotropis Procera,
Lantana camara, Melia azadirach and Pinus roxbur- Fig. 1. Mean O/o mortality (corrected accordingto Abbot, 1925)
gii. The reason for such an effect is not known, but of A. composticola at 2,5 and 10 O/o concentration of cold water
rnay be due toa minor change broughtby heat in the (CWE) and hot water(HWE) prepared leaf-extractsof various
plant species after 48 h : A : Altkea rosea; B : Azadirackta
chemical nature of active principle.
indica; C : Bougainvillea spectabilis; D : Callistemon lanceo-
(iv) Where hot water
extracts were significantly lata; E : Calotropis procera; F : Cannabis sativa; G : Cedrella
(p < 0.001) more toxic than cold water extracts, e.g. toona; H : Chenopodium album; 1 : Ck ysantkemumcinerari-
Althea rosea and Cannabis sativa.Such aneffect may folium; J : Dahlia variabilis; K : Jacaranda acutifolia; L :
be due either to a favourable chemical change orthat Lantana camara; M : Melia azadirack; N : Pinus roxburgii;
the heat enhanced the extraction of active ingredients O : Populus ciliata; P : Ricinus cornmunis; Q : Tagetes patula.

3 20 Revue Nématol. 12 (3) :31 7-322 (1989)


Effects of plant-extracts to Aphelenchoides composticola

relative toxicities of leaf-extracts and of their formu- increased yield of A. bisporus. Sohi, Grewal and Seth
lations but it does not depict or take into consideration (1987) and Grewal (1988) also observed that the leaf-
the response of the nematode exposed to higher doses matter incorporation in compost increased the popu-
of the extract. The latter typeof effect is better depicted lations of nematode-trapping/antibiotic-producing
by the analysis of variance. As is evident from the data, fungiand suppressed that of competitor/pathogenic
that in some cases e.g. cold water leaf-extracts of D. moulds. It was thereforesuggested that arange of
variabilis (Tab. 1), 50 ,/O killof the nematode was interrelated factors including leaf-extract toxicity, leaf
producedataconcentration of 0.4 O/, but complete decomposition products (supported by Sayre, Patrick
mortality was not achieved even at 10 ,/O concentration. and Thorpe, 1965), activities of nematode-trapping fungi
Whereas in others, e.g. cold water leaf-extracts of J. andfungal-antibiosis were responsiblefor thesup-
acutifolia, the LC,, value was much higher (2 ,/O) but pression of A. composticola populations below economic
complete mortality was observed at 5 ,/O concentration. injury levels.
In other words, the straight line probit model does not It is therefore concluded that the incorporation of
fit in well where the quantal response is truly sigmoid. dried leaves of pre-selected plants (screened for their
In suchcases, the significance of heterogeneity resulted nematicidal effects) could provide a suitable and cheap-
from the lack of fit of the model, i.e. due to thefailure eralternative to biologically manage A. composticola
of the probit analysis to converge(Tab. 1 & 2). infesting the Indian mushroom industry. Although the
Conversely, when thequantalresponse is linear, the active nematicidal principles from the leaf-extracts of
probit model is the best which also predicts the LC,, the plant species screened in the present study are yet
values even outside the range of the concentrations to be characterized, these findings will enable us to test
tested. the above theories in different geographical regions of
Apart from the nematicidal activity, the leaf extracts the country using locally available leaf-matter.
of some of the above plants were shown to possess other
beneficialeffectsincludingincrease inthe mycelial ACKNOWLEDGEMENTS
growth of A. bisporus (Sohi, Grewal & Seth, 1987) and
The authorisgrateful to Mr RodneyEdrnondsonand
fungi-suppressive effects to common mushroom weed
Mr JohnFenlonforhelpinstatisticalanalysis, Mr Paul
moulds (Grewal & Grewal, 1988). Furthermore, Grewal Richardson for correcting the English and Mrs Sue Bewsey for
(1988) demonstrated thatthe incorporation of dried typing the manuscript.
leaves of A. indica, C. sativa, Eucalyptus hybrid (E.
tereticornis) and R. comrnunis to the mushroomcompost
significantly reduced A. composticola populations, im-
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Accepté pourpublication le 22 novembre 1988.

322 Revue Nématol. 12 (3) :317-322 (1989)