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Plant-parasitic nematodes associatedwith semi-temperate vegetables inthe highlands of Benguet Province,PhilippinesNordalyn B. Pedroche a , Luciana M. Villaneuva a & Dirk De Waeleb ca Semi-temperate Vegetable Research and Development Center ,Benguet State University , La Trinidad , Benguet , 2601 ,Philippinesb Laboratory of Tropical Crop Improvement, Department ofBiosystems , Faculty of Bioscience Engineering, University ofLeuven (KU Leuven) , Kasteelpark Arenberg , 13, 3001 , Leuven ,Belgiumc School of Environmental Sciences and Development, North-WestUniversity Private Bag X6001 , Potchefstroom , 2520 , South AfricaPublished online: 08 Nov 2012.

To cite this article: Nordalyn B. Pedroche , Luciana M. Villaneuva & Dirk De Waele (2013) Plant-parasitic nematodes associated with semi-temperate vegetables in the highlands of BenguetProvince, Philippines, Archives Of Phytopathology And Plant Protection, 46:3, 278-294, DOI:10.1080/03235408.2012.739928

To link to this article: http://dx.doi.org/10.1080/03235408.2012.739928

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Plant-parasitic nematodes associated with semi-temperate vegetables in

the highlands of Benguet Province, Philippines

Nordalyn B. Pedrochea, Luciana M. Villaneuvaa and Dirk De Waeleb,c*

aSemi-temperate Vegetable Research and Development Center, Benguet State University, LaTrinidad, Benguet 2601, Philippines; bLaboratory of Tropical Crop Improvement, Department ofBiosystems, Faculty of Bioscience Engineering, University of Leuven (KU Leuven), KasteelparkArenberg 13, 3001 Leuven, Belgium; cSchool of Environmental Sciences and Development,North-West University Private Bag X6001, 2520 Potchefstroom, South Africa

(Received 10 October 2012; final version received 11 October 2012)

Thirteen genera (Aphelenchoides, Criconemella, Ditylenchus, Globodera, Helico-tylenchus, Hoplolaimus, Meloidogyne, Longidorus, Paratrichodorus, Pratylenchus,Trichodorus, Tylenchus and Xiphinema) of plant-parasitic nematodes were foundassociated with 15 semi-temperate vegetable crops in Benguet Province,Philippines. Among these taxa, Helicotylenchus, Meloidogyne and Pratylenchuswere the most predominant. Four taxa that can vector plant viruses were alsofound: Trichodorus, Paratrichodorus, Longidorus and Xiphinema. The taxaParatrichodorus, Longidorus and Xiphinema have not been reported previouslyon semi-temperate vegetable crops in the Philippines. The most predominantnematode species were H. dihystera, P. penetrans and Meloidogyne spp. Thesenematodes were found abundantly in five out of the nine municipalities surveyed:Atok, Bakun, Buguias, Kibungan and Mankayan. The incidence of Criconemellasp., G. rostochiensis, Hoplolaimus sp., Longidorus sp., Trichodorus sp. andTylenchus sp. was also recorded in at least one municipality. The predominantnematode species were also found on every vegetable crop examined. Moreparticularly, H. dihystera was highly abundant on cucumber, cauliflower, Chinesecabbage, sweet pepper, snap bean and onion; P. penetrans was highly abundanton carrot, celery, garden pea, broccoli, cabbage, Chinese cabbage, Chinesemustard, onion, potato, radish and lettuce; Meloidogyne spp. were highlyabundant on celery, cucumber, Chinese mustard, carrot, sweet pepper and potato.According to the formula by Fortuner and Merny (1973) for identifying thepotential plant pathogens, these predominant nematode species were classified aspotential pathogens with the ability to cause economic loss which shows that theyare probably important active pathogens of these semi-temperate vegetables. Theincidence of other nematode species in the rhizosphere included G. rostochiensison sweet pepper, garden pea and potato; D. dipsaci on onion; Tylenchus sp. onlettuce, onion and broccoli; A. fragariae on carrot, lettuce, broccoli and onion;Criconemella sp. on cucumber and cauliflower; Longidorus sp. on carrot, celery,cucumber, broccoli, cabbage, cauliflower, Chinese mustard, snap beans, onion,potato and radish; X. americanum on lettuce, broccoli and onion; Paratrichodorussp. on carrot, lettuce, onion and potato; and Trichodorus sp. on snap bean, potatoand radish.

Keywords: frequency of occurrence; highlands; Philippines; plant-parasiticnematodes; population density; survey; vegetables

*Corresponding author. Email: [email protected]

� 201 Taylor & Francis

http://dx.doi.org/10.1080/03235408.2012.739928Vol. 46, No. 3, 278–294,

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Introduction

Benguet Province is the major semi-temperate vegetables producing region in thePhilippines owing to its favourable climate. The semi-temperate vegetables cultivatedin this province include broccoli (Brassica oleraceae var. italica), cabbage (B.oleraceae var. capitata), carrot (Daucus carota), cauliflower (B. oleraceae var.botrytis), celery (Apium graveolens), cucumber (Cucumis sativus), garden pea (Pisumsativum), lettuce (Lactuca sativa), snap bean (Phaseolus vulgaris) and sweet pepper(Capsicum annuum).

Because the production of semi-temperate vegetables is the major source ofincome for thousands of small-holder farmers in the highlands (Cordillera) in thenorthern part of Luzon, the semi-temperate vegetables industry in the highlands iscontinuously being developed to improve its productivity in order to meet theincreasing demands for these high value crops by the expanding human populationof the Philippines. To increase the productivity, newly improved cultivars, such ashigh-yielding hybrids, were imported from other countries and are now beingcultivated extensively. This practice might have led to the introduction of newdisease and pest problems caused by a variety of pathogens including plant-parasiticnematodes, such as foliar diseases caused by Aphelenchoides fragariae, a foliarnematode (Villanueva et al. 2006).

Surveys conducted more than 30 years ago to determine the incidence of plant-parasitic nematodes in Benguet Province reported the association of the followingnematode genera with some of the above-mentioned vegetables: Meloidogyne(Valdez 1968), Pratylenchus, Tylenchorhynchus, Helicotylenchus and Hemicyclio-phora (Dela Rosa and Davide 1969). Studies carried out later on plant-parasiticnematodes in the Philippines concentrated mostly on their occurrence and damage tocommon (sub)tropical crops, such as maize (Zea mays), soybean (Glycine max),string bean (Vigna unguiculata ssp. sesquipedalis), etc., cultivated in other, mostlylowland, regions of the Philippines (Toledo and Davide 1969; Davide 1988). As aresult, little is known about the incidence of plant-parasitic nematodes on semi-temperate vegetables in the country.

In temperate regions, a relatively large number of plant-parasitic nematodespecies have been found on vegetables. Several of these can cause substantialdamage to vegetables by reducing their growth and yield. Meloidogyne spp. cancause substantial damage to carrot (Vrain 1981; Hay and Pethybridge 2005),cucumber (Walters et al. 1999), lettuce (Wong and Mai 1973) and tomato(Solanum lycopersicum) (Van Der Beek et al. 1998). On carrot, the quality of thetap roots is affected: infected roots are usually forked and galled whereasuninfected roots are long and smooth (Vrain 1981). Cucumber plants showchlorosis and stunting throughout the growing season when infected severely withMeloidogyne spp. while tomato plants infected with the same nematodes can havelower yields compared to the uninfected plants (Colyer et al. 1998). Lettuce plantsinfected with Meloidogyne spp. failed to produce marketable heads in the field(Wong and Mai 1973).

A number of Pratylenchus spp., such as P. barkati, P. brachyurus, P. coffeae, P.dasi, P. loosi, P. zeae, was reported to occur in the rhizosphere or roots of vegetables(Sikora and Fernandez 2005). Pratylenchus penetrans caused economic losses oncabbage, cauliflower, lettuce and onion (Olthof and Potter 1973). In carrots, thisnematode species can reduce the size of the tap roots by feeding on the roots during

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the early stages of their development (Hay and Pethybridge 2005). Crop loss causedby Pratylenchus spp. can exceed 50% in both carrot and onion and was substantialin organic farms in Germany (Hallmann et al. 2007). Other host plants ofPratylenchus spp. include cabbage (Waceke 2007), garden pea and snap bean (Greenand Verdejo 1985).

Tylenchorhynchus spp. were reported to cause moderate stunting in someplants in the Netherlands (Sharma 1968). Cauliflower, garden pea and radish(Raphanus sativus) were listed as suitable host plans, while carrot and cucumberwere listed as poor host plants. Tomato was also mentioned as a poor host forTylenchorhynchus spp. by Khan et al. (1986). The species of Helicotylenchus areoften found in vegetable fields. According to Sikora and Fernandez (2005), thesenematodes, however, cause no serious damage to vegetables. They have long beenknown to parasitise garden pea (Green and Dennis 1981) and soybean in the USbut no significant damage was reported (Niblack 1992). The species ofHemicycliophora were able to infect tomato (Cooper et al. 1970), lettuce(Klinkenberg 1963) and varieties of B. oleracea, such as broccoli, cabbage andcauliflower (Khera and Zuckerman 1963), but no significant damage wasobserved. Recently, however, Walker (2004) reported in South Australia forkingof tap roots caused by H. saueri which resulted in unmarketable yield of infectedcarrots.

The objectives of our study were to update the incidence of plant-parasiticnematodes associated with semi-temperate vegetables in Benguet Province and toidentify the predominant plant-parasitic nematode species associated with semi-temperate vegetables in this province which is the major semi-temperate vegetableproducing region of the Philippines.

Materials and methods

Sampling

In Benguet Province, samples were taken from nine municipalities: Atok, Bakun,Bokod, Buguias, Kabayan, Kapangan, Kibungan, La Trinidad and Mankayan(Figure 1).

The first sampling was carried out between the dry seasons of 2004 and 2005(December 2004 to March 2005) (Table 1). This was followed by a second samplingduring the rainy season of 2005 (June–July). The third and last sampling was carriedout during the dry season of 2006 (February–May). Spreading of the sampling wasnecessary because different vegetables are cultivated at different times of the year.For example, in the highlands, carrot and potato are planted during the dry seasonwhereas snap beans, cucumber, garden pea and sweet pepper are planted eitherduring the dry or wet season. Celery and crucifers are planted throughout the year.

In each municipality surveyed, at least five semi-temperate vegetable farms wereselected at random. The number of samples collected per farm varied from one areato another and depended on the size of the field under cultivation. The size of thefields under cultivation ranged from 200 m2 to over 5000 m2.

Soil and/or root samples were collected from the following 15 vegetables:broccoli, cabbage, carrot, cauliflower, celery, Chinese cabbage (B. oleraceae ssp.pekinensis), cucumber, garden pea, lettuce, onion (Allium cepa), Chinese mustard (B.oleraceae ssp. chinensis), radish, snap bean, sweet pepper and potato (Solanumtuberosum).

280 N.B. Pedroche et al.

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Sampling depth was 30 cm. The soil samples were stored in plastic bags while theroot samples were stored in brown paper bags in a cool box and transported to thelaboratory for the nematode extraction and identification.

Nematode extraction and identification

Nematode extraction and identification were carried out at the Biological ControlLaboratory and the Central Service Laboratory of the Semi-temperate VegetableResearch and Development Center (STVRDC) at the Benguet State University(BSU), La Trinidad, Benguet.

Nematodes were extracted from two sets of 200 ml soil subsamples using amodified Baermann tray method for vermiform nematodes and a flotation methodfor cyst nematodes (Shurtleff and Averre 2000). The first set of soil was placed on asieve in a dish with water and left at room temperature (+258C) for 48 h. The waterfrom the dish was collected and placed in test tubes (175 ml capacity) and left for3 h. This allowed the nematodes to settle at the bottom of the test tubes. Then thesupernatant was sucked of using a 50 ml pipette. One ml of the nematode suspensionwas transferred to a counting dish for observation under the stereomicroscope. Thesecond set of soil was placed on a large ceramic dish, and then 300–500 ml of tapwater was added and left at room temperature (+258C) for 48 h. Each of thefloating cysts was picked out using a bamboo splinter and placed on a counting dishand observed under the stereomicroscope.

Nematodes were also extracted from 1 g root subsamples. The roots werewashed, cut into pieces of 1 cm length and macerated in a kitchen blender. Themacerated roots were then placed on a sieve in a dish with water and left at roomtemperature (+258C) for 48 h (Shurtleff and Averre 2000). Other 1 g rootsubsamples were set aside and stained using the acid-fuchsin staining method(Shurtleff and Averre 2000).

Figure 1. Municipalities surveyed in Benguet Province (enlarged), Philippines.


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Table1.

Samplingperiods,cropscultivatedandsoiltypein

thedifferentdistrictsbelongingto

themunicipalities

sampled,Benguet

Province,Philippines.

Samplingperiod

District

Municipality

Cropscultivated

Soiltype

Decem

ber

2004

Englandad,Paoay

Atok

Cabbage,

Chinesecabbage,

carrot,

potato,radish

Loamysand

Decem

ber

2004

CentralBuguias,Loo,Natubleng,Bangao

Buguias

Cabbage,

Chinesecabbage,

carrot,

potato,radish,garden

pea

Loam

toloamysand

Decem

ber

2004

Balakbak,Datakan,Cuba,Paykek

Kapangan

Snapbean,cucumber

Clayey

toloamy

February

2005

Sipitan

Bakun

Cabbage

Clayey

toloamy

February

2005

Madaymen

Kibungan

Cabbage,

garden

pea

Siltloam

March2005

Adaoay

Kabayan

Cabbage,

garden

pea

Loam

toloamysand

March2005

Acnal

Bokod

Garden

pea

Loam

July

2005

Balakbak,Datakan,Paykek

Kapangan

Cucumber,snapbean

Clayey

toloamy

July

2005

Englandad,Paoay

Atok

Cabbage,

broccoli,carrot,potato,snap

bean,celery

Loamyto

loamysand

July

2005

Loo,Natubleng,Bangao

Buguias

Carrot,lettuce,onion

Loamyto

loamysand

Novem

ber

2005

Acnal

Bokod

Cauliflower,snapbean,sw

eetpepper

Loam

Novem

ber

2005

Adaoay

Kabayan

Cauliflower

Clayey

toloamy

Decem

ber

2005

Madaymen

Kibungan

Garden

pea,potato,cabbage,

radish,

lettuce

Siltloam

Decem

ber

2005

Sipitan,Bagtangan

Bakun

Garden

pea,potato,cabbage,

radish,

lettuce

Clayey

toloamy

Decem

ber

2005

Nangayangan,Bulalacao

Mankayan

Garden

pea,potato,cabbage,

radish,

lettuce,sw

eetpepper

Clayloam

toloamy

February

andMay2006

Swamp,Balili,Bekkel

LaTrinidad

Broccoli,lettuce

Siltloam

toloamy

sand


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Selected nematode specimens extracted from the soil and roots werekilled and fixed with hot 4% formaldehyde and mounted on glass slides (Shurtleffand Averre 2000) for the identification using a light microscope. Nematodetaxa present in the soil and root samples were counted under a stereoscopicmicroscope.

Assessment of nematode population densities

The number of extracted plant-parasitic nematodes was counted and recorded foreach crop and each farm. The numbers counted in the 200 ml soil subsamples wereconverted to 1 l of soil.

The frequency of occurrence, population density and abundance index (AI) werecalculated for each nematode taxon for each crop to estimate their incidence. Thefrequency of occurrence is the percentage of farms in which the taxon was foundwhile population density is the mean of the number of nematodes expressed per soilor root unit. The AI was calculated as the logarithm of the average observednematode population density in the farms in which the taxon was found(log10x þ 1). Based on the criteria proposed by Fortuner and Merny (1973), anematode taxa is frequent when detected in more than 30% of the fields. It can beconsidered abundant when 200 individuals are recovered per dm3 soil (AI ¼ 2.3) or20 individuals per g roots (AI ¼ 1.3) (Fargette and Queneherve 1988).

The different nematode species and genera were also classified in four groupsaccording to their potential pathogenic ability (Fortuner and Merny 1973): (1)potential pathogens with the ability to cause economic loss because the nematodesare both frequent and highly abundant; (2) potential pathogens due to their highabundance but limited in distribution due to their low frequency of occurrence; (3)omnipresent pathogens due to their high frequency of occurrence but not potentialpathogens because they are very low in abundance; (4) fortuitous parasites withoutthe ability to cause economic loss due to both a low frequency and low abundance.

Results

In total, 463 soil and 142 root samples were collected from 86 farms in BenguetProvince in the Philippines (Table 2).

Thirteen genera of plant-parasitic nematodes were found associated with the 15vegetables surveyed: Aphelenchoides, Criconemella, Ditylenchus, Globodera, Helico-tylenchus, Hoplolaimus, Meloidogyne, Longidorus, Paratrichodorus, Pratylenchus,Trichodorus, Tylenchus and Xiphinema (Table 3).

Based on a limited random sampling study, the following nematode species wereidentified: Aphelenchoides fragariae, Ditylenchus dipsaci, Globodera rostochiensis,Helicotylenchus dihystera, Pratylenchus penetrans and Xiphinema americanum. Thesecond-stage juveniles (J2) ofMeloidogyne species can hardly be identified. However,the examination of mature females isolated from the roots revealed the presence ofthree species: M. incognita, M. javanica and M. hapla.

Nematode incidence in the municipalities

In general, H. dihystera, P. penetrans and Meloidogyne spp. were found to occurfrequently and abundantly in the rhizosphere and roots of the vegetables examined


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compared to the other nematode taxa found during the survey (Table 3). Based ontheir potential pathogenic ability, they belong to the first group as defined byFortuner and Merny (1973) and can be considered as potential pathogens with theability to cause economic loss. They were also found on every vegetable examined.

In the soil samples, H. dihystera, a spiral nematode, was found frequently in thenine municipalities surveyed with frequencies ranging from 79 to 100% (Table 4). Itwas found abundantly in Atok, Bokod, Buguias, Kabayan and Kapanganmunicipalities. Similarly, P. penetrans, a lesion nematode, was found in highfrequencies in all nine municipalities with frequencies ranging from 58 to 100%. Itwas also found abundantly in five out of the nine municipalities: Atok, Bakun,Buguias, Kibungan and Mankayan. Meloidogyne spp., root-knot nematodes,occurred frequently in eight out of the nine municipalities with frequencies rangingfrom 43 to 95%. These nematodes were found abundantly in three municipalities:Atok, Buguias and Kapangan. Other nematodes found during the survey such asCriconemella sp., G. rostochiensis, Hoplolaimus sp., Longidorus sp., Trichodorus sp.and Tylenchus sp. were frequent in at least one municipality but were not abundant(Table 4).

In the root samples, P. penetrans was found frequently in six out of the ninemunicipalities but was only abundant in Buguias, Kibungan and La Trinidad (Table5). Meloidogyne spp. occurred frequently in three municipalities (Atok, Buguias andMankayan) but were not abundant. Helicotylenchus dihystera and G. rostochiensisappeared frequent in at least one municipality but were not abundant. The othernematodes had a low incidence (Table 5).

Nematode incidence on the vegetables

In the soil samples, H. dihystera was found associated with every vegetable surveyedbut it is highly frequent and abundant on cucumber, cauliflower, Chinese cabbage,sweet pepper, snap bean and onion, with frequencies ranging from 79 to 100%

Table 2. Number of soil and root samples collected of semi-temperate vegetables in BenguetProvince, Philippines.

Soil Roots

Carrot 63 8Celery 15 11Cucumber 20Garden pea 8Lettuce 94 61Broccoli 24 12Cabbage 66 7Cauliflower 23 24Chinese cabbage 14Chinese mustard 1Sweet pepper 6 6Snap bean 5Onion 22 8Potato 93 5Radish 9Total 463 142


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Table

3.

Incidence

ofplant-parasiticnem

atodes

associatedwithsemi-temperate

vegetablesin

Benguet


Nem

atodespecies

FAI

Ca

Ce

Cu

GP

Le

Br

Cab

Cau

CC

CM

SP

SB

On

Po

Ra

Aphelenchoides

fragariae

2.4

0.1

Criconem

ella

sp.

7.6

0.2

Ditylenchusdipsaci

2.3

0.1

Globoderarostochiensis

16.7

0.3

þþ

þHelicotylenchusdihystera

93.9

2.2

þþ

þþþ

þþ

þþ

þþþ

þþþ

þþþþ

þþþ

þþþ

þþ

Hoplolaim

ussp.

6.4

0.1

þMeloidogynespp.

74.4

1.7

þþþþ

þþþ

þþ

þþ

þþ

þþþ

þþ

þþ

þLongidorussp.

48.2

0.9

þ*

þ*

þ*

þ*

þ*

þ*

þ*

*þ*

þ*

þ*

þ*

Paratrichodorussp.

1.4

0.1

**

*Pratylenchuspenetrans

87.7

2.4

þþþ

þþþ

þþþþ

þþþþ

þþþ

þþþþ

þþþ

þþ

þþþ

þþþ

þþþ

Trichodorussp.

18.3

0.5

þþþ

þþ

þTylenchussp.

11.7

0.2

þþ

Xiphinem

aamericanum

2.3

0.1

**

*

F,frequency

ofoccurrence

(%);AI,abundance

index;þfrequent(presentin

more

than30%

ofthefieldssurveyed);þþabundant(A

I�

2.3/dm

3soilorAI�

1.3/g

roots);þþþfrequentandabundant(F

430%

andAI�

2.3/dm

3soil

orAI�

1.3/g

roots);*foundforthefirsttimein

Benguet

Province

onthisvegetable.Ca,carrot;Ce,celery;Cu,cucumber;GP,garden

pea;Le,lettuce;Br,broccoli;Cab,cabbage;Cau,cauliflower;CC,Chinesecabbage;CM,Chinese

mustard;SP,sw

eetpepper;SB,snapbean;On,onion;Po,potato;Ra,radish.


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Table

4.

Frequency

ofoccurrence

(F,%)andabundance

index

(AI)

per

lsoilofplant-parasiticnem

atodes

foundin

therhizosphereofsemi-temperate

vegetablesin

Benguet


Atok

Bakun

Bokod

Buguias

Kabayan

Kapangan

Kibungan

La

Trinidad

Mankayan

FAI

FAI

FAI

FAI

FAI

FAI

FAI

FAI

FAI

Aphelenchoides

fragariae

00

00

00

10.04

00

00

00

13

0.2

00

Criconem

ella

sp.

70.2

00

42

0.6

30.1

20

0.3

16

0.5

00

70.2

00

Ditylenchusdipsaci

00

00

80.1

30.3

19

0.6

00

00

10.01

00


37

0.8

00

00

19

0.4

00

29

0.7

18

0.4

20.03

29

0.5

Helicotylenchusdihystera

95

2.4

79

1.7

100

2.7

99

2.4

100

2.9

100

2.6

84

1.5

96

2.1

88

1.8

Hoplolaim

ussp.

20.1

00

00

00

00

00

00

32

0.6

00

Meloidogynespp.

95

2.7

72

0.9

17

0.6

83

2.3

51

1.4

99

2.4

60

1.2

83

1.7

43

0.9

Longidorussp.

88

1.6

30.04

78

1.6

67

1.4

72

1.4

72

1.6

10

0.1

59

1.1

40.1

Paratrichodorussp.

20.1

00

00

40.2

00

00

00

30.1

00.0

Pratylenchuspenetrans

100

2.7

97

2.8

58

1100

3.1

61

1.4

68

1.6

97

2.7

99

2.2

76

2.5

Trichodorussp.

54

1.2

00

58

141

1.5

41

110

0.3

00

12

0.2

20

Tylenchussp.

00

00

00

20.1

00

00

00

61

1.1

60.1

Xiphinem

aamericanum

10.03

00

00

00

00

00

00

12

0.2

00


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Table

5.

Frequency

ofoccurrence

(F,%)andabundance

index

(AI)

per

groots

ofplant-parasiticnem

atodes

foundin

theroots

ofsemi-temperate

vegetablesin

Benguet


Atok

Bakun

Bokod

Buguias

Kabayan

Kapangan

Kibungan

La

Trinidad

Mankayan

FAI

FAI

FAI

FAI

FAI

FAI

FAI

FAI

FAI

Aphelenchoides

fragariae

00

00

00

00

00

00

00

00

00

Criconem

ella

sp.

00

00

00

00

00

00

00

00

00

Ditylenchusdipsaci

00

00

00

00

00

00

00

90.2

00


33

0.8

00

00

00

00

00

00

00

00

Helicotylenchusdihystera

00

25

0.2

42

0.4

00

80.4

00

00

27

0.3

33

0.2

Hoplolaim

ussp.

00

00

00

00

00

00

00

00

00

Meloidogynespp.

67

0.6

00

00

75

1.1

00

00

17

0.2

20

0.3

50

0.8

Longidorussp.

00

00

30.02

00

70.2

00

00

00

00

Paratrichodorussp.

00

00

00

00

00

00

00

00

00

Pratylenchuspenetrans

33

0.2

75

1.2

55

0.7

94

1.3

22

0.5

00

100

2.3

100

1.8

50

0.4

Trichodorussp.

00

00

17

0.2

00

00

00

00

00

00

Tylenchussp.

00

00

00

00

00

00

00

00

00

Xiphinem

aamericanum

00

00

00

00

00

00

00

10.01

00


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(Table 3). Based on its potential pathogenic ability in the rhizosphere, H. dihysterabelongs to the first group as defined by Fortuner and Merny (1973) on these crops.In the root samples, H. dihystera was found highly frequent but less abundant inlettuce, cabbage, cauliflower, sweet pepper and onion. Based on its potentialpathogenic ability in the roots, H. dihystera belongs to the third group as defined byFortuner and Merny (1973) on these crops.

Pratylenchus penetrans was found in every vegetable surveyed and was highlyfrequent and abundant on carrot, celery, garden pea, broccoli, cabbage, Chinesecabbage, Chinese mustard, onion, potato and radish in the soil samples withfrequencies ranging from 77 to 100% (Table 3). Based on its potential pathogenicability in the rhizosphere, P. penetrans belongs to the first group as defined byFortuner and Merny (1973) on these crops. In the root samples, P. penetrans wasfound highly abundant and frequent on carrot, celery, lettuce, broccoli, cabbage,onion and potato with frequencies ranging from 33 to 100%. Based on its potentialpathogenic ability in the roots, H. dihystera belongs to the first group as defined byFortuner and Merny (1973) on these crops.

Meloidogyne spp. were found highly frequent and abundant in the soil samples ofcelery, cucumber and Chinese mustard with frequencies ranging from 98 to 100%(Table 3). Based on their potential pathogenic ability in the rhizosphere,Meloidogyne spp. belong to the first group as defined by Fortuner and Merny(1973) on these crops. These nematodes were also found highly frequent but lessabundant in the soil samples of other crops, such as carrot, lettuce, sweet pepper,onion, garden pea, snap bean, broccoli, cabbage, cauliflower, Chinese cabbage,radish and potato. Based on their potential pathogenic ability in the rhizosphere,Meloidogyne spp. belong to the third group as defined by Fortuner and Merny (1973)on these crops. Meloidogyne spp. were found highly frequent and abundant in theroots of carrot, celery, sweet pepper and potato with frequencies ranging from 83 to100%. Based on their potential pathogenic ability in the roots, Meloidogyne spp.belong to the first group as defined by Fortuner and Merny (1973) on these crops.

Globodera rostochiensis was detected in high frequency but low abundance in therhizosphere of sweet pepper, garden pea and potato (Table 3). Based on its potentialpathogenic ability, G. rostochiensis belongs to the third group as defined by Fortunerand Merny (1973) on these crops. Globodera rostochiensis was also found in soilsamples of carrot, cucumber, snap bean, broccoli, cabbage and Chinese cabbage butwith both low frequency and abundance. In the root samples, G. rostochiensisoccurred only with high frequency and abundance in potato.

Ditylenchus dipsaci was found less frequent but highly abundant only in therhizosphere of onion with a frequency of 25% (Table 3). Based on its potentialpathogenic ability, D. dipsaci belongs to the second group as defined by Fortunerand Merny (1973) on this crop. This nematode species was also found in the roots oflettuce and onion in very low frequency and abundance. Tylenchus sp. was foundhighly frequent but less abundant in the rhizosphere of lettuce, onion and broccoliwith frequencies ranging from 41 to 78% (Table 4). Based on its potential pathogenicability, Tylenchus sp. belongs to the third group as defined by Fortuner and Merny(1973) on these crops. It was also found in the rhizosphere of carrot and potato butin very low frequency and abundance. Tylenchus sp. was not found in the roots ofany vegetable surveyed. Similarly, Criconemella sp. was found frequent but lessabundant in the rhizosphere of cucumber and cauliflower with frequencies of about40% (Table 4). It was also found in very low frequency and abundance in the


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rhizosphere of carrot, lettuce, onion, snap bean, cabbage and potato. Criconemellasp. was not found in the roots of any vegetable surveyed. Hoplolaimus sp. was foundfrequent (61%) but less abundant in the rhizosphere of broccoli (Table 3). It was alsofound in the rhizosphere of lettuce, cabbage and onion but in both low frequenciesand abundances. Hoplolaimus sp. was not found in the roots of any vegetablesurveyed. Aphelenchoides fragariae was detected in the rhizosphere of carrot, lettuce,broccoli and onion in very low frequencies (2–17%) and abundances (Table 3). Itwas found only in the municipalities of Buguias and La Trinidad. In La Trinidad,however, it was detected in more than 30% of the soil samples collected.Aphelenchoides fragariae was not found in the roots of any vegetable surveyed.Longidorus sp. was found frequent but less abundant in the rhizosphere of carrot,celery, cucumber, broccoli, cabbage, cauliflower, Chinese mustard, snap bean, onion,potato and radish with frequencies ranging from 33 to 100% (Table 3). In the roots,Longidorus sp. was only found in cauliflower in very low frequency and abundance.Xiphinema americanum was found in the rhizosphere of lettuce, broccoli and onion inlow frequencies (1%, 20% and 13%, respectively) and low abundances (Table 3). Itwas also detected in very low frequency and abundance in the roots of cauliflower.Paratrichodorus sp. was found in the rhizosphere of carrot, lettuce, onion and potatobut in low frequencies (ranging from 1 to 18%) and low abundances (Table 3).Paratrichodorus sp. was not found in the roots of any vegetable surveyed.Trichodorus sp. was found frequent but less abundant in the rhizosphere of snapbean, potato and radish with frequencies ranging from 27 to 33% (Table 3). It alsooccurred less frequent and abundant in the rhizosphere of carrot, celery, cucumber,lettuce, broccoli, cabbage, cauliflower, Chinese cabbage and onion with frequenciesranging from 7 to 24%. In the roots, Trichodorus sp. was found frequent but lessabundant in cauliflower and sweet pepper.

Discussion

The spiral nematode H. dihystera was found highly frequent and abundant on sixcrops, viz. cucumber, cauliflower, Chinese cabbage, sweet pepper, snap bean andonion. In some fields, it also occurred frequently and abundantly on carrot, cabbage,potato and lettuce. In all these fields, H. dihystera can be considered an activepathogen of these vegetables. In the Philippines,Helicotylenchus was reported to be apathogen on cabbage, carrot, cucumber, lettuce, onion, potato and sweet pepper(Dela Rosa and Davide 1969; Alberto 1999; Infante and Castro 1999; Madamba1999). Our results, therefore, confirm these earlier reports of the association ofHelicotylenchus with the above-mentioned vegetables but with the addition of threecrops, viz. cauliflower, snap bean and Chinese cabbage. Despite the importance ofH.dihystera, there are no reports as to the extent of its pathogenicity to vegetables in thecountry. Helicotylenchus dihystera was reported to parasitise a number of crops andis a serious parasite of bluegrass and turf in Australia (O’Bannon and Inserra 1989).It was also found to parasitise garden pea and soybean in the US but no damage wasobserved (Green and Dennis 1981; Niblack 1992). The nematode was also found in anumber of vegetable crops but was not able to cause serious damage in the field(Sikora and Fernandez 2005).

The relatively high frequencies and abundances of P. penetrans in most of thesemi-temperate vegetable crops surveyed, both in the soil and the roots, identify thisnematode species as an active pathogen of these semi-temperate vegetables. A light


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to extensive root discolouration was observed in samples infected with this nematodespecies which indicates that this nematode species can cause damage to these crops.In the Philippines, Pratylenchus was first reported in cabbage (Davide and Comedis1972), celery (Reyes and Villanueva 1981), lettuce, onion, Chinese mustard, potatoand sweet pepper (Dela Rosa and Davide 1969). The results of our study corroboratefindings published in the Philippines several decades ago with additional newassociations with carrot, cucumber, garden pea, broccoli, Chinese cabbage, snapbean and radish. Similar to the other nematodes found, there is a scarcity ofinformation on the impact of P. penetrans on vegetable crops specifically crop lossstudies in sub-tropical and tropical regions (Sikora and Fernandez 2005). In othercountries, such as Australia and Tasmania, species of Pratylenchus, specifically P.crenatus, were frequently detected on carrot but no significant relationship withdamage was observed (Hay and Pethybridge 2005).

The frequency and abundance of root-knot nematodes, Meloidogyne spp., variedacross vegetables and municipalities in the soil samples collected. They wereconsidered active pathogens of celery, cucumber and Chinese mustard based on theirhigh frequency and abundance on these crops. In some areas, they were also observedwith both high frequency and abundance and as such were also considered aspathogens of carrot, cabbage, potato, sweet pepper, onion, snap bean and Chinesecabbage. Although they were less abundant on other crops, they occurred veryfrequently in the municipalities surveyed. In Benguet Province, crops are usuallyrotated or planted at the same time in a mixed cropping system. This might haveinfluenced the observed variation across crops and localities. Moreover, plantingmaterials and farming tools are widely shared by farmers in the same area and thismight have contributed to the increasing problem caused by root-knot nematodes inthe area.

Infection by Meloidogyne spp. is characterised by yellowing, wilting of the plantand galling of the roots but these symptoms were not apparent during the time ofsampling. Various semi-temperate vegetable crops were reported to be infected byroot-knot nematodes in the country, such as cabbage, carrot, cauliflower, celery,cucumber, garden pea, lettuce, onion, Chinese mustard, potato, radish, snap beanand sweet pepper among others (Castillo 1968; Valdez 1968; Dela Rosa and Davide1969; Toledo and Davide 1969; Davide 1972; Fajardo and Palo 1999; Infante andCastro 1999; Orillo et al. 1999; Reinking 1999). Meloidogyne spp. are widelydistributed and considered worldwide the most economically important pathogens onagricultural crops (Sasser 1977). According to Sikora and Fernandez (2005), the damagecaused by these nematodes has been demonstrated clearly in intensive agriculturalproduction systems but they can also cause severe damage in subsistence farming. Theseauthors state that there is still a need to assess crop losses caused by this group ofnematodes in less intensive production systems. As a result, knowledge on theimportance of root-knot nematodes varies greatly between developed and developingcountries (Coyne et al. 2009). Sikora and Fernandez (2005) also stated that among thepathogenic threats to agricultural production worldwide, including resource-poorfarmers, root-knot nematodes might single-handedly pose the utmost risk.

The stem and bulb nematode, D. dipsaci, was only abundant in onion soilsamples collected from Buguias municipality but occurred in low frequency.Symptoms of infection by this nematode species were not evident at the time ofsampling. Infection by this nematode species can lead to distortion of abovegroundand necrosis of belowground plant parts in severe cases. This nematode was first


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reported in the country on onion several decades ago (Lopez 1999) but until now thedamage it can cause to crops currently planted is still unknown. The nematode wasreported as one of the most devastating nematodes of crops such as garlic, onion,legumes, cereals, strawberries and bulb-producing ornamental plants mostly intemperate regions. The presence of 10 or more nematodes in 400 cm3 soil is said tobe the economic threshold level (Sikora and Fernandez 2005).

Tylenchus sp. was associated with carrot, potato, lettuce, onion and broccoli. Itwas, however, detected in low abundance and therefore cannot be considered as apotential pathogen of these crops. In addition, its occurrence is somewhat limited tothe municipality of La Trinidad. In the past, Infante and Castro (1999) reported it tobe a pathogen of cabbage and onion but damage by this nematode in the country hasnot been reported so far.

Globodera rostochiensis or the potato cyst nematode was found in the rhizosphereof carrot, cabbage, potato, sweet pepper, broccoli, snap bean, cucumber, Chinesecabbage and garden pea. However, it was recorded in moderate frequency and verylow abundance in the soil samples. It was only encountered in high frequency andabundance in the root samples of potato. Hence, it was considered as a potentialpathogen with the ability to cause economic loss to potato particularly in themunicipality of Atok. Those that were found in the rhizosphere of other crops hadprobably infected previously grown susceptible crops, such as potato. The potatocyst nematode can stay dormant and survive in the soil for years without its hostplant, i.e. potato, or in between crops as viable second-stage juveniles in an enclosedhardened sheath (Robertson et al. 1999). They can hatch and infect plants at oncewhen they detect host root diffusates (Robinson et al. 1985). The presence of thisnematode species on potato in the Philippines has been reported previously (Davide1988). The nematode was reported to cause poor growth, chlorosis and stunting inpotato and tomato but yield losses are often unknown in (sub)tropical countries(Sikora and Fernandez 2005).

Aphelenchoides fragariae, a foliar nematode, was detected at very low populationdensities in soil planted with carrot, celery, broccoli and onion. Hence, this nematodespecies was not considered as a potential pathogen to these crops. Its detection mightbe related to the previous crop grown. The crops from which A. fragariae wasrecovered commonly rotated with strawberry. Aphelenchoides fragariae has beenreported earlier associated with strawberry in the same area (Villanueva et al. 2006)but was not detected during a survey in 1989–1990 (Villanueva 1992). In recentyears, the local government of Benguet Province imported new strawberry cultivarsin an effort to improve the farmers’ productivity. This might have been the reasonfor the unintentional introduction of this nematode in the area. There are existingpolicies for importation or introduction of planting materials in the Philippines suchas the Plant Quarantine Law which was enacted as early as 1922. Evaluation andPest Risk Analysis (PRA) are being done by the Bureau of Plant Industry to regulateor restrict the movement of these living organisms in the country. The detection of A.fragariae brings us to question the rigidity of the plant quarantine services forincoming planting materials in the Philippines. However, it is also possible that theextraction methods used by researchers in the last two decades, i.e. Cobb’s sievingmethod, were not appropriate to extract this type of nematode.

Criconemella sp. and Hoplolaimus sp. were associated with some crops but werenot considered as potential pathogens of these crops. The association of thesenematodes with semi-temperate vegetables in the Philippines has not been reported


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so far. However, according to Sikora and Fernandez (2005), they are often found insubtropical soils and could be important pathogens of vegetables

Longidorus sp., X. americanum, Paratrichodorus sp. and Trichodorus sp. wereassociated with some crops but, overall, were not considered potential pathogens.Trichodorus sp. was first reported on cabbage by Davide and Comedis (1972).Species of the genera Longidorus, Xiphinema and Paratrichodorus were previouslynot found in the Cordillera but were reported on other crops, such as sugarcane, inthe lowlands (Gargantiel and Davide 1973). However, though detected in lownumbers, these nematodes can be important as virus vectors. This way, they candamage their hosts both directly and indirectly. Damage caused by these nematodesis often more pronounced in the seedling stage which may result in swollen lateralroots.

It is likely that the potential nematode problems mentioned above can beaggravated if left unmanaged. The risk of nematode population build-up is high andcould result in crop damage and yield loss. Therefore, in the future, it is critical todetermine the virulence/aggressiveness of the nematode populations present andtheir reproductive and damage potential on each semi-temperate crop grown. Itwould also give greater accuracy to these findings if all the nematodes could beidentified to species level.

More effort should also be done to monitor these plant-parasitic nematodes on aregular basis despite of the, more often than not, rough terrains, isolated vegetablefarms and limited agricultural resources and infrastructure. Increasing farmer’sawareness on the potential damage to crops by plant-parasitic nematodes would alsocontribute in their restriction and movement from one field to another by simplystarting from basic cultural practices such as sanitation.

The results we are presenting can also be used as baseline information for policy-makers in updating regulations for these pathogens, on the one hand, and preventionof their spreading or further monitoring of their population build-up on the otherhand. One should also look closely into the existing quarantine procedures whichwould probably need to be updated with the careful inclusion on how to deal withnematological problems in the country. Unless these potential problems can beaddressed properly or collectively, in a more integrated approach, there will alwaysbe the risk of important yield loss caused by these plant-parasitic nematodes.

Acknowledgements

This research was made possible by a Flemish Interuniversity Council (VLIR-UOS)scholarship to N. Pedroche. The authors thank the local farmers of the surveyed farms fortheir permission to take samples from their fields and their help during the survey.

References

Alberto RT. 1999. Survey, identification, and pathogenicity test of plant-parasitic nematodesassociated with onion (Allium cepa L.) and varietal reaction. In: Tangonan NG, editor.Host index of plant diseases in the Philippines. Philippines: Nueva Ecija. p. 137–138.

Castillo MB. 1968. Survey and taxonomy of nematodes attacking ginger, black pepper, beans,peas, cowpea, eggplant and celery in the Philippines (Phase II: Biological Studies). NRCPRes Bull. 31:83–96.

Colyer PD, Kirkpatrick TL, Vernon PR, Barham JD, Bateman RJ. 1998. ReducingMeloidogyne incognita injury to cucumber in a tomato-cucumber double-cropping system.J Nematol. 30:226–231.


Dow

nloa

ded

by [

Eas

tern

Mic

higa

n U

nive

rsity

] at

18:

12 1

0 O

ctob

er 2

014

Cooper AF, Van Gundy SD, Stolzy LH. 1970. Nematode reproduction in environments offluctuating aeration. J Nematol. 2:182–188.

Coyne DL, Fourie H, Moens M. 2009. Current and future management strategies in resource-poor farming. In: Perry RN, Moens M, Starr JL, editors. Root-knot nematodes.Wallingford, UK: CAB International. p. 444–466.

Davide RG. 1972. Nematodes of Philippine crops and their control. Philipp Phytopathol SocBull. 2:34 p.

Davide RG. 1988. Nematode problems affecting agriculture in the Philippines. J Nematol.20:214–218.

Davide RG, Comedis A. 1972. Chemical control of nematodes on cabbage in Atok, Benguet.Philipp Agric. 55:282–288.

Dela Rosa AG, Davide RG. 1969. Pathogenicity test of four genera of plant parasiticnematodes on vegetable crops. Philipp Phytopathol. 5:29–38.

Fajardo TG, Palo MA. 1999. The root-knot nematode Heterodera radicicola (Greef) Muller oftomato and other plants in the Philippine islands. In: Tangonan NG, editors. Host indexof plant diseases in the Philippines. Philippines: Nueva Ecija. p. 47.

Fargette M, Queneherve P. 1988. Populations of nematodes in soil under banana, cv. Poyo, inthe Ivory Coast. 1. The nematofauna occurring in the banana producing areas. RevueNematol. 11:239–244.

Fortuner R, Merny G. 1973. Les nematodes parasites des racines associes au riz en BasseCasamance (Senegal) et en Gambie, Cahiers de l’Orstom. Serie Biologique. 21:3–20.

Gargantiel FT, Davide RG. 1973. Survey and pathogenicity tests of plant-parasiticnematodes associated with sugarcane in Negros Occidental. Philipp Phytopathol. 9:59–66.

Green CD, Dennis EB. 1981. An analysis of the variability in yield of pea crops attacked byHeterodera goettingiana, Helicotylenchus vulgaris, and Pratylenchus thornei. Plant Pathol.30:65–71.

Green CD, Verdejo S. 1985. Colonisation of Pisum sativum and Phaseolus vulgaris byPratylenchus penetrans in sterile media. Nematologica. 31:452–456.

Hallmann J, Frankenberg A, Paffrath A, Schmidt H. 2007. Occurrence and importance ofplant-parasitic nematodes in organic farming in Germany. Nematology. 9:869–879.

Hay FS, Pethybridge SJ. 2005. Nematodes associated with carrot production in Tasmania,Australia, and the effect of Pratylenchus crenatus on yield and quality of Kuroda-typecarrot. Plant Dis. 89:1175–1180.

Infante CS, Castro F. 1999. Nematodes associated with vegetable crops in Region XI:PCARRD highlights 1999. In: Tangonan NG, editors. Host index of plant diseases in thePhilippines. Philippines: Nueva Ecija. p. 34, 42, 139.

Khan RM, Khan AM, Khan MW. 1986. Interaction between Meloidogyne incognita,Rotylenchulus reniformis and Tylenchorhynchus brassicae on tomato. Revue Nematol.9:245–250.

Khera S, Zuckerman BM. 1963. In vitro studies of host-parasite relationships of some plant-parasitic nematodes. Nematologica. 9:1–6.

Klinkenberg CH. 1963. Observations on the feeding habits of Rotylenchus uniformis,Pratylenchus crenatus, P. penetrans, Tylenchorhynchus dubius and Hemicycliophora similis.Nematologica. 9:502–506.

Lopez, ME. 1999. Philippine plant diseases. In: Tangonan NG, editors. Host index of plantdiseases in the Philippines. Philippines: Nueva Ecija. p. 48.

Madamba CP. 1999. The biology of the root-knot nematodes in ramie, with a consideration ofdisinfesting rootstocks for the transplanting. In: Tangonan NG, editor. Host index ofplant diseases in the Philippines. Philippines: Nueva Ecija. p. 17–18.

Niblack TL. 1992. Pratylenchus, Paratylenchus, Helicotylenchus and other nematodes onsoybean in Missouri. J Nematol. 24:738–744.

O’Bannon JH, Inserra RN. 1989. Helicotylenchus species as crop damaging parasiticnematodes. Nematology Circular No. 165. Tallahassee (FL): Florida Department ofAgriculture and Consumer Service.

Olthof THA, Potter JW. 1973. The relationship between population densities of Pratylenchuspenetrans and crop losses in summer-maturing vegetables in Ontario. Phytopathology.63:577–582.


Dow

nloa

ded

by [

Eas

tern

Mic

higa

n U

nive

rsity

] at

18:

12 1

0 O

ctob

er 2

014

Orillo FT, Schafer LA, Revilla BA. 1999. Common diseases of vegetable crops and theircontrol in the Philippines. In: Tangonan NG, editor. Host index of plant diseases in thePhilippines. Philippines: Nueva Ecija. p. 77, 138, 149, 156.

Reinking OA. 1999. Philippine plant diseases. In: Tangonan NG, editor. Host index of plantdiseases in the Philippines. Philippines: Nueva Ecija. p. 48.

Reyes TT, Villanueva LM. 1981. Screening of crops for resistance to Meloidogyne incognita.Research and planning conference on root-knot nematodes, Meloidogyne spp. Raleigh,NC: North Carolina State University. p. 76–81.

Robertson L, Robertson WM, Jones, JT. 1999. Direct analysis of the secretions of the potatocyst nematode Globodera rostochiensis. Parasitology. 119:167–176.

Robinson MP, Atkinson, HJ, Perry, RN. 1985. The effect of delayed emergence on infectivityof juveniles of the potato cyst nematode Globodera rostochiensis. Nematologica. 31:171–178.

Sasser JN. 1977. Worldwide dissemination and importance of the root-knot nematodes,Meloidogyne spp. J Nematol. 9:26–29.

Sharma RD. 1968. Host suitability of a number of plants for the nematode Tylenchorhynchusdubius. Netherlands J Plant Pathol. 74:97–100.

Shurtleff MC, Averre CW. 2000. Diagnosing plant diseases caused by nematodes. St. Paul,MN: APS Press. 189 p.

Sikora RA, Fernandez E. 2005. Nematode parasites of vegetables. In: Luc M, Sikora RA,Bridge J, editors. Plant parasitic nematodes in subtropical and tropical agriculture.Wallingford, UK: CAB International. p. 329–330.

Toledo RR, Davide RG. 1969. Reactions of different vegetable and field crops to infection byMeloidogyne javanica. Philipp Phytopathol. 5:45–51.

Valdez RB. 1968. Survey, identification and host-parasite relationships of root-knotnematodes occurring in some parts of the Philippines. Philipp Agric. 51:802–824.

Van Der Beek JG, Poleij LM, Zijlstra C, Janssen R, Janssen GJW. 1998. Variation invirulence within Meloidogyne chitwoodi, M. fallax, and M. hapla in Solanum spp.Phytopathology. 88:658–665.

Villanueva LM. 1992. Plant parasitic nematodes associated with strawberry in the Philippines.In: Proceedings of the 2nd International Workshop on Plant Nematology, Karachi,Pakistan. Pakistan: University of Karachi. p. 13–17.

Villanueva LM, Kiat-Ong BE, Pedroche NB. 2006. Foliar nematode and Verticillium wilt:Emerging problems in strawberry production in Benguet. In: Proceedings of the AnnualScientific Meeting of the Pest Management Council of the Philippines, Davao, Philippines.Philippines: University of the Philippines, Los Banos. 85 p.

Vrain TC. 1981. Relationship between Meloidogyne hapla density and damage to carrots inorganic soils. J Nematol. 14:50–57.

Waceke JW. 2007. Plant-parasitic nematodes associated with cabbages in Kenya. AfricanCrop Science Conference, El-Minia, Egypt. p. 1071–1074.

Walker GE. 2004. Associations between carrot defects and nematodes in South Australia.Australasian Plant Pathol. 33:579–584.

Walters SA, Wehner TC, Barker KR. 1999. Greenhouse and field resistance in cucumber toroot-knot nematodes. Nematology. 1:279–284.

Wong TK, Mai WF. 1973. Pathogenicity of Meloidogyne hapla to lettuce as affected byinoculum level, plant age at inoculation and temperature. J Nematol. 5:126–129.


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plant-parasitic nematodes associated with semi-temperate vegetables in the highlands of benguet...

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