Nematode Parasites on Agricultural Crops and Their

JIRCASJournal No.4: 29-39 (1997)

Nematode Parasites on Agricultural Crops and Their

Distribution in Sri Lanka

a)

H. M. Rohini EKANAYAKE al and Yukio TO IDA bl

Entomology Division, Horticultural Crops Research and Development Institute (HORD!) (Gannoruwa, Peradeniya, Sri Lanka)

bl Crop Production and Postharvest Technology Division, Japan

International Research Center for Agricultural Sciences(]IRCAS) (Tsukuba, Ibaraki, 305 Japan)

Received September 2, 1996

Abstract

Plant-parasitic nematodes associated with 54 kinds of crops and their distribution

were investigated in Sri Lanka. Forty eight species in 24 genera were detected in this

survey, of which 41 were identified at the species level. Their distribution was classified into the following four types, 1) widespread type; Meloidogyne arenaria, M. incognita

and Rotylenchulus reniformis 2) semi widespread type; Hirschmanniella oryzae, M. javanica and Radopholus simils 3) highland type; Globodera rostochiensis and M. hapla, and 4) area specific type ; M. brevicauda and M. graminicola. The nematodes important

for agriculture in Sri Lanka were as follows ; M. arenaria, M. incognita, M. javanica, G. rostochiensis, M. hapla, M. brevicauda, M. graminicola, R. reniformis, R. similis, T. semipenetrans, Pratylenchus loosi, P. brachyurus, Aphelenchoides besseyi and H. oryzae

Additional key words: nematode pests, detection frequency, crop damage,

distribution types

29

Introduction

Plant-parasitic nematodes are important pests

in agriculture all over the world. In Sri Lanka,

along with continuous land development, the

implementation of agricultural intensification

projects, and the introduction of various plant

materials and agricultural products from other

countries to the island, nematode damage is

becoming increasingly conspicuous in many crops

and districts.

Investigations on plant-parasitic nematodes of

this country were initiated in 1940 by G. A Loos,

who reported the occurrence of several plant

parasitic nematodes including Aphelenchoides fragariae on foliage plants

15). He also reported four

30 JIRCAS]. No.4, 1997

species of the genus Criconemoides including three

new species, as well as five species of the genus

X . h. . 1 d . 16. 17) I h zp mema me u ing two new species . n t e

early stage of nematological studies, most of the

information dealt with nematodes parasitic to tea5

' 7•

8, 9, 10, 11, 14, 17, 20) Investigation of root-knot

nematodes in Sri Lanka began in 1953 when Loos

described a new species, Meloidogyne brevicauda 18

) Th ft M . M . . on tea . ere a er, . arenarza, . mcognzta

d M . . "d "f" d 12'

13) d h an . ;avanzca were 1 enti 1e an t e

following nematodes were recorded up to 1978 ;

Boleodorus sp., Helicotylenchus multicinctus,

Hoplolaimus pararobustus, M. arenaria, M. hap/a,

Pratylenchus curvitatus, P. loosi, Radopholus similis,

S ll 8, 10, 20, 21)

cute onema brachyurum . Lamberti and 11)

Ekanayake conducted a survey on plant-parasitic

nematodes in some parts of the island, and they

reported the presence of 18 genera, such as A.

besseyi, Criconemoides (=Criconemella),

Ditylenchus, Hirschmanniella , Longidorus, M.

brevicauda, Paratrichodorus, Rotylenchus,

Trichodorus, Tylenchulus, Xiphinema and others.

Ekanayake first reported the presence of Globodera

rostochiensis on potato in the highlands of Sri

Lanka in 19901) and she identified the pathotype of

this species as Ro 12). In 1992, Toida and

Ekanayake 22

) described the restricted distribution

of this nematode.

In this paper we present the results of

nematological investigations conducted in Sri

Lanka. We investigated nematode species and

their distribution in most of the agro-ecological

areas in Sri Lanka from 1991 to 1995 under the

collaborative research program between the

Central Agricultural Research Institute (presently

· Horticultural Crops Research and Development

Institute), Sri Lanka and the Tropical Agriculture

Research Center (presently Japan International

Research Center for Agricultural Sciences), Japan.

Some of the studies carried out by H.M.R.

Ekanayake were supported financially by the

Swedish Agency for Research Cooperation with

Developing Countries (SAREC) in Sri Lanka.

Materials and Methods

Sampling sites : The island consists of 22 sub

agro-ecological regions with 25 districts. Sampling

sites were selected from 10 km2

grids from each

district. Sixteen districts were sampled, during the

survey, namely, Anuradhapura, Puttalam, Matale,

Amparai, Badulla, Kandy, Kegalle, Gampaha,

Moneragala, Nuwara Eliya, Colombo, Ratnapura,

Kalutara, Galle, Matara and Hambantota(Fig.l).

Attempts were made to cover as many districts as

possible. However due to the situation prevailing

in the country only limited areas were explored

and of these 16 districts, Anuradhapura, Puttalam

Manna/ ..... \ .· .-·········· Vavuniya .. ···:···· : .. : ... ... : ..

... .

Anuradhapura .. ··, . .... ·

..-:· ... :

./ Polonnaruwa· .• ~· 'j .:

./ Kurunagala \ ·· ·· · ·· .. ·. . .. : : Matale ( ·-,_ .. = ····.~.atticaloa ·• : :·· . .. ···. :

Gampa·h·~·::.:····j····.::.; ·· ~-~~~·~·-.") \ ..

'······ ........ ../..Kega;.'.r· ............ ··········/Bad~·I;;·: ( _~mparai

Colombe;> : \ ": Nuwara Eliya \··· ····· · .. \ ···· · .............. ...-.. ./ Moneragala

Kalutara \ < .. \ Ratnapura ...-· \:

. : . · ........ .. .:··.

.··. ··::·········· .....

:·,

. ... .. · Hambantota

Fig. 1 Districts of Sri Lanka Dark shading indicates the 16 districts surveyed for nematode fauna.

H.M.Rohini EKANAYAKE et al. : Nematode Parasites on Agricultural Crops 31

and Moneragala were not sampled completely.

Sampling method : Ten sub-samples were

collected from each field in a selected site from

each grid. Fifty four kinds of crops were surveyed,

such as vegetables, pulses, paddy rice, fruit trees,

sugarcane, pepper, tea, coffee, tobacco, cotton,

rubber, etc. In total more than 23,000 samples were

collected during the investigation. Each sample

consisted of roots, soil around the root system, and

stems and leaves if necessary. The amount of soil

per sample varied from 1-2 kg.

Extract and fixation of nematodes: Nematodes

were extracted from soil by sieving and the

Baermann funnel technique. They were decanted

in water, concentrated and fixed in 5% formalin

solution after heat treatment. These specimens

were stored in plastic vials until examination.

Aliquots of 2 to 5g of roots were stained by acid

fuchsin in boiling lacto-glycerol and cleared for 24

hours in plain lacto-glycerol to detect the

nematodes invading root tissues. Fragments of

roots (10g), stems (10g) or leaves (3-5g) cut into

small pieces were incubated in petri dishes for 24

hours to extract the nematodes, which were killed

in 5 % hot formalin and stored in plastic vials.

Nematodes fixed in 5 % formalin were mounted on

glass slides using the rapid glycerol methoct19).

The stained nematodes in plant tissues were

directly mounted in glycerol for identification.

Results and Discussion

1) Nematode species and their detection frequencies

The nematodes detected in this survey and

identified at the species level, and their host crops

are listed in Table 1. Of these the most common

nematode genera and their detection frequencies

in selected crops are listed in Table 2. We detected

48 species in 22 genera of plant-parasitic

nematodes, of which 41 species were identified at

the species level (Table 1). Based on the results,

Xiphinema, Meloidogyne and Helicotylenchus,

consisted of comparatively many species.

Xiphinema consisted of nine species, of which

three species, X basiri, X insigne and X dijfusum,

had already been recorded in coconut by

Ekanayake and Lamberti4). Six species of

Meloidogyne and five species of Helicotylenchus

were detected and identified, respectively.

These three genera were found to occur on

more than 80% of the major crops, though crop

damage caused by Xiphinema and Helicotylenchus

was not significant. Genera Hoplolaimus and

Pratylenchus were also detected on many crops but

in a rather low frequency. Boleodorus sp. and P.

l lZ) d d • h. neg ectus were not etecte m t 1s survey.

Rotylenchulus reniformis and Longidorus spp. were

observed in several crops. Trichodorus spp. and

Radopholus similis were found on a few crops.

Globodera rostochiensis (Plate 3-F) was detected

only on potato and Hirschmanniella oryzae only on

rice in a comparatively high frequency.

Meloidogyne was detected on most of the important

crops in a fairly high frequency, especially on

tomato in which the detection frequency (60%) was

the highest in this survey (Table 2).

Four most common species of Meloidogyne, i.

e. M. arenaria (Plate 1-A, B), M. incognita (Plate 1-

Table 1. Plant-parasitic nematodes detected in Sri Lanka (1991-1995)

Species

Aphelenchoides besseyi A. fragariae Aphelenchus avenae

Criconemel la curvata C. ornata Ditylenchus sp. Dolichodorus hetercephalus Globodera rostochiensis

Hosts*

Rice (01yza sativa) Cabbage (Brassica oleracea), Strawberry (Fragaria spp.) Banana (Musa spp.), Sugarcane (Saccharum officinarum), Sweet potato (Jpomoea batatas) Cacao (Theobroma cacao), Sugarcane Eggplant (Solanum melongena), Maize (Zea mays). Sugarcane Onion (Allium cepa), Tobacco (Nicotiana tabacum) Sugarcane Potato (Solanum tuberosum)

32

(Continued from Table 1)

Species

Helicoty/enchus crenacauda H. dihystera

H. multicinctus

H. pseudorobustus H. willmottae Hemicriconemoides cocophil/us Hirschmanniella myzae Hoplolaimus seinhorsti

H. pararobustus Longidorus afzali

L. /aevicapitatus Meloiodogyne arenaria

M. brevicauda M. graminicola M. hap/a M. incognita

M.javanica

Paralongidorus sp. Paratrichodorus sp. Paratylenchus sp.

Pratylenchus brachyurus

P. loosi P. zeae

Radopholus similis Rotylenchulus reniformis

Rotylenchus sp. Scutellonema brachyurum S. conicaudatum Triclzodorus sp. Tylenclzulus semipenetrans Tylenchus sp. Xiphinema americanum sensu Jato

X. basiri X. diffusum X. elongatum X. enciculiferum X. ifacolum X. inaequale X. insigne

X. krugi

JIRCAS J. No.4, 1997

Hosts*

Coconut (Cocos nucifera), Coffee (Coffea arabica), Rice, Sugarcane Banana, Citrus (Citrus spp.), Cacao, Coffee, Cowpea (Vigna sinensis), Grape (Vitis vinifera), Maize, Onion, Papaya (Carica papaya), Sugarcane, Tea (Camellia sinensis) Apple (Mulus pumila), Banana, Cacao, Cassava (Manihot esculenta), Citrus, Mango (Mangifera indica), Sugarcane, Tea Citrus, Sugarcane Banana, Sugarcane Banana, Coconut Rice Banana, Beet (Beta vulgaris), Blackgram (Phaseolus mungo), Chili (Capsicum annuus), Cardamom (Ellettaria cardamomum), Coconut, Coffee, Cotton (Aosgipum hirstum), Grape, Ground nut (Arachis hypogaea), lnnala (Coleus rotunfo/ius), Maize, Onion, Soybean (Glycine max), Tea, Yampee (Dioscorea trifida) Alternanthera (Altlzerantlzera sessilis), Cassava, Rice Cardamom, Cotton, Grape, Pineapple (Anans comosus), Tomato (Lycopersicon esculentum) Carrot (Dacus carota), Cucumber (Cucumis sativus), Sugarcane Bean (Phaseplus vulgaris), Beet, Bitter gourd (Monordica Charantia), Faba bean (Vicia faba), Indian pennywort (Cente/la asiatica), Snake gourd (Trichosanthes anguina), Tobacco, Tomato Tea Rice Beet, Carrot, Chili, Potato Carrot, Cassava, Eggplant, Papaya, Pepper (Piper nigrum), Pumpkin (Cucurbita moschata), Snake gourd. Soybean, Spinach (Spinacia oleracea), Sweet popato, Tobacco, Tomato Banana, Bean, Carrot, Chili, Cucumber, Okura (Hybiscus esculentus), Soybean, Tobacco, Tomato Grape Cassava, Tea Banana, Cacao, Citrus, Coffee, Grape, Green gram (Phaseolus aureus), Ground nut, Okra, Onion, Sesame (Sesamum indicum), Sugarcane, Tea, Tobacco Cassava, Cotton, Grape, Ground nut, Leek (Allium porrum), Maize, Pineapple, Sugarcane, Sweet potato Apple, Tea Cabbage, Cucumber, Eggplant, Maize, Papaya, Pineapple, Rice, Sugarcane, Tobacco Banana, Cacao, Cardamom, Pepper, Spinach, Sugarcane Bean, Blackgram, Carrot, Chili, Hindu Cowpea (Vigna cylindrica), Indian pennywort, Loofah (Luffa cylindrica), Spinach, Soybean Grape Citrus, Greater yam (Dioscorea alata) Chili, Cotton, Papaya, Pineapple Pineapple, Rice, Tea. Tomato Citrus, Pepper Celery (Apium graveolens), Chili, Papaya, Pineapple, Snake gourd Banana, Citrus. Coffee, Cucurbit (Cucurbita spp.), Guava (Psidiwn guajava), Papaya, Sweet potato Coconut, Citrus, Rubber (Hevea brasilensis), Sugarcane Cardamom, Pineapple, Sugarcane Cacao, Citrus (Citrus grandis), Coconut, Coffee, Maize, Mango, Rubber Abocado (Persea americana), Citrus. Cucumber, Tomato Citrus, Coconut Banana, Sugarcane Banana, Beta! nut plam (Arecc1 cathechu), Cacao, Citrus, Cotton, Leek, Papaya, Sugarcane Bean, Coconut, Papaya, Sugarcane

* Aphe/enchus, Criconemel/a, Dolichodorus, Hemicriconemoides, Longidorus, Paralongidorus, Paratylenchus Rotylenchus Scutellonema, Tylenchus and Xiphinema were detected in soil surrounding roots of the crops.

** Citrus excluding C.grandis means Citrus spp.


Table 2. Percentage frequency of detection of common nematodes from each crop in Sri Lanka

Nematodes Crops

Rice Potato Citrus Pineapple Sugarcane Tomato Cucurbits Banana Bean Capsicum

Globodera rostochiensis 13.4 Hirschmanniella oryzae 39.4 Radopholus similis Rotylenchulus ren.ifonnis Tylenchulus semipenetrans 8. 1 Helicotylenchus spp. 1.4 2.6 39.8 Hoplolaimus spp. 3.1 0.7 2.3 Longidorus spp. 11.8 Meloidogyne spp . 0.4 3.7 Pratylenchus spp. 1.1 0.5 3.1 Trichodorus spp. 0.4 Xiphinema spp. 2.2 1.3 30.1

Plate 1. Photomicrographs of female perinea! patterns of Meloidogyne arenaria (A, B) and M. incognita (C, D) in Sri Lanka

8.7

9.4

11.9 3. 1

10.9

7.8 12.0 2.1 0.5 1.2 3.6 0.8

15 .1 10.3 7.1 22.5 11.7 5.1 10.9 2.4 2.2 2.2 10.6 2.2 10.6 I. I 6.5 8.3 59.3 29.9 11.2 10.9 4.1 9.9 2.1 3. 1 0.4 0.4

IS . I 6.3 8.5 9.6 8.3 2.8

Plate 2. Photomicrographs of female perinea! patterns of Meloidogyne javanica (A, B) and M. brevicauda (C, D) in Sri Lanka

34 JIRCAS ]. No.4, 1997

C, D), M. javanica (Plate 2-A, B) and M. hapla were detected mainly on vegetable crops. In

addition, species indigenous to Sri Lanka, M.

brevicauda (Plate 2-C,D) and M. graminicola, one

of the common root-knot nematode in the tropics,

were identified. Meloidogyne species found in this

survey and their typical host crops in Sri Lanka are

listed in Table 3. It was reconfirmed that M.

graminicola occurred only on rice and a few

gramineous plants, and M. brevicauda only on mature tea bushes, whereas the other four species

were detected on various crops. Although

Helicotylenchus spp. were detected on many crops

in a fairly high frequency, they were not regarded

yet as important pests in agriculture. Detection frequency of six species of Meloidogyne is shown in

Table 4. Detection frequency of M. arenaria was

the highest (64%), and that of M. incognita, the

most harmful species of root-knot nematodes, was

also high (54%). These detection rates differed from those recorded in Thailana2

3l, where M.

incognita was detected in the highest frequency

Table 3. Main crops attacked seriously by Meloidogyne species in Sri Lanka

Nematode species

M. arenaria

M. incognita M.javanica M.hapla M. grami11icola M. brevicauda

crops

Beet, Bitter gourd, Faba bean, Innala (Kaffir potato), Snake gourd, Tomato Carrot, Eggplant, Spinach, Tomato Carrot, Chili, Spinach, Tomato Beet, Carrot, Chili Rice Tea

Table 4. Percentage frequency of detection of Meloidogyne species in some areas in Sri Lanka

Nematode species

M. arenaria M. incognita M. javanica M. hap/a M. grami11icola M. brevicaucla

Frequency of detection(%)*

64.3 53.6 32.1 25.0

7.0 3.6

*No. of each species x 100/No. of sampling sites

while M. arenaria was hardly found. M. javanica was found at a moderate rate, and M. hapla, M. graminicola and M. brevicauda were detected in a low frequency in Sri Lanka. However, M. exigua, M. microcephala and M. naasi which had been reported in Thailana2

3l, were not detected in the

current survey in Sri Lanka.

2) Distribution of nematodes Distribution of the major nematodes attacking

crops is depicted in Figs. 2-7. M. incognita (Fig. 2),

M. arenaria (Fig. 4) and R. reniformis (Fig. 3)

were the most widespread species in Sri Lanka. H.

oryzae (Fig. 5), M. javanica (Fig. 6) and R. similis (Fig. 7) were fairly widespread and H. oryzae showed a similar type of distribution to that

reported previousl/l. Tylenchulus semipenetrans (Fig. 5) was detected from four sites and Globodera rostochiensis (Fig. 3) from three sites only in the

highlands of the midcountry. M. graminicola (Fig. 6) was found in paddy fields at two sites in the

southern part of the country and M. brevicauda

• .. -••

. }

Fig. 2. Distribution of Meloidogyne incognita in Sri Lanka


• R. reniformis

~ G. rostochiensis

• ••

\ / 1

~ .. ~- • ! t,.\ •• • j

~ Fig. 3. Distribution of Rotylenchulus reniformis and

Globodera rostochiensis in Sri Lanka

••• •• • •

'7.· • .,. • j •. 5

~ • I

Fig. 4. Distribution of Meloidogyne arenaria in Sri Lanka

• H. oryzae

El;:! T. semipenetrans

• Fig. 5. Distribution of Hirschmanniella oryzae and

Tylenchulus semipenetrans in Sri Lanka

• M. javanica

~ M. graminicola

.. •

• ) • • ,,. . la )

• • / • s

I

Fig. 6. Distribution of Meloidogyne javanica and M. graminicola in Sri Lanka

36 JIRCAS ]. No.4, 1997

• R. simi/is

~ M. hap/a

D M. brevicauda

•

~ .J·. 1-.·· ~ ..

•

\ .. )

Fig. 7. Distribution of Radopholus similis, Meloidogyne hapla and M. brevicauda in Sri Lanka

(Fig. 7) only in tea gardens at one site in the

highlands of the midcountry. M. hap/a is adapted

to a cooler climate and it was detected in a limited

area. As C. rostochiensis depends only on potato

plants, due to quarantine regulations, its habitat in

Sri Lanka is restricted only to areas around Nuwara

Eliya in the highlands at an elevation of nearly

2000m above the sea level. On the other hand, the

distribution of monophagous or oligophagous

nematodes such as M. brevicauda and M.

graminicola is influenced by host plant distribution.

Distribution of T. semipenetrans seemed to be

associated with the expansion of citrus cultivation

areas because it was detected mostly in citrus

gardens.

The distribution of these nematodes was classified into the following four types ; 1)

nematodes distributed most widely in Sri Lanka such as M. arenaria, M. incognita and R. reniformis

which were also distributed widely in the tropics,

and sub-tropics, and showed a wide host range, 2)

nematodes distributed in slightly restricted areas

such as H. oryzae, M. javanica and R. similis,

which were distributed widely in the tropics but exhibited a less wide host range, 3) nematodes

found only in the highlands in this country such as

G. rostochiensis and M. hap/a which were

distributed chiefly in the temperate area (high

altitude areas) of the island, and 4) nematodes

detected in extremely limited areas, such as M.

brevicauda and M. graminicola, which were indigenous to Sri Lanka and/ or monophagous .

3) Crop injury by nematodes

G. rostochiensis, M. arenaria (Plate 3-A), M.

incognita (Plate 3-B), M. javanica (Plate 3-C), M.

hap la (Plate 3-D), M. graminicola, and R.

reniformis were important pests in agriculture in

Sri Lanka just as in other countries. M. brevicauda

(Plate 3-E) which was described in this country18

J

caused severe damage to mature tea plants in the

highlands. M. graminicola and H. oryzae induced

poor growth and yields or yellowing in paddy rice

in some cultivated areas. Some of the migratory

ecto- and/ or endoparasitic nematodes also caused

obvious damage to crops in this country.

Aphelenchoides besseyi and A. fragariae damaged foliage plants. Pratylenchus brachyurus injured

strawberry and some other plants. R. similis

injured banana and T. semipenetrans citrus trees,

respectively. It was reported that P. loosi which

was first described as a new species on this island

14J caused the most serious damage to tea

plants in the highlands, while R. similis attacked 6)

pepper as well as banana . Although

Helicotylenchus spp. were considered to be

injurious to crops due to their high frequency of

detection in various crop fields, economic damage

of crops caused by these nematodes was not

significant. Xiphinema spp. and Longidorus spp.

were also considered to be harmful to crops

because they were the largest nematodes with a spear big enough to injure crops, among plant

parasitic nematodes. However, symptoms of crop

damage were not observed in this investigation.

Deleterious effect of other nematodes including

Criconemella spp., Hoplolaimus spp.

Paratrichodorus sp., Scutellonema spp., etc., on


Plate 3. Crop roots or tubers infested with root-knot nematodes and cysts of the potato cyst ne matode in Sri Lanka A: Bitter gourd damage by Meloidogyne arenaria . B: Spinach damage by M. incognito. C: Tomato dam age by M. javanica. D: Potato damage by M. hapla. E: Tea damage by M. brevicauda. F: Cysts of Globodera rostochiensis.

crops could not be observed.

Based on the crop injury and geographical

distribution described above, important nematode

pests attacking crops of economic importance in

Sri Lanka at present were considered to be M.

incognita, M. arenaria, M. javanica, M. hapla, G.

rostochiensis, M . brevicauda, M. graminicola, R.

reniformis, R . similis, T. semipenetrans, P.

brachyurus, P. loosi, A. besseyi and H. oryzae.

Acknowledgements

We thank Mr. V. H. Janis, Mss. C.

Bulugahapitiya and I. Hettiarrachchi , CARI

(HORDI), Sri Lanka, for their assistance in the

collection and processing of the samples. We also

thank Dr. T. Yaegashi, Meiji University, Japan, for

his help in taking micrographs of perinea! patterns

of Meloidogyne spp.

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20) Sivapalan, P. (1968). Association of Radopholus

similis with declining young tea fields. Pl. Dis.

Reptr. 52:528.

21) Sivapalan, P. (1978). Investigation on root-knot

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22) Toida, Y. and Ekanayake, H.M.R.K. (1992)

Occurrence and distribution of the potato cyst

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48.

23) Toida Y., Keereewan, S., Sano, Z., Mizukubo,

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Documents

Nematode Parasites on Agricultural Crops and Their