The Relationships Between Plant Parasitic Nematodes of Sugarbeet And Other Soil Fauna

INTRODUCTION ------------------------------------------------------------- 
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densities with crop yields and on the average prices reported in 
certain period.  
 Reduction of crop losses due to nematodes is one way of 
increasing crop yields. Therefore, chemical control methods 
could be tested and optimized to improve growth. At the same 
time, some additives, such as fertilizers or soil amendments may 
be tested in order to decrease the rate of nematicides to minimize 
the environmental pollution and keep the control process more 
economical.  
 Importance of biological control depends on 
microorganisms themselves or natural products extracted from 
plants, fungi, bacteria, marine organisms including algae and 
others as potential chemicals for the use as nematicides, 
pesticides, antibiotic and some pharmacological compounds have 
been considered (Cardellina et al., 1993; Chang et al. 1993; 
Chitwood, 1993; Mayer et al, 1993; Khan and Saxena, 1996; 
Kerry and Bourne, 1996;Youssef et al. 1998; Mostafa, 1998; 
Mostafa et al. 1998; Abdel-Rahman, 1999 (a & b); Maareg and 
Badr,2000 and Badr, 2001. 
The purpose of the present study is to investigate the 
relationship among plant parasitic nematode and different groups 
of soil fauna (microorganisms and animals) in sugarbeet fields, 
therefore, the present investigation was initiated by discussing 
the following studies: 
1) Surveying of the soil arthropod and nematode fauna and 
microorganisms groups associated with sugarbeet fields at the 
Ten-thousand faddan, West Nubaryia. 
INTRODUCTION ------------------------------------------------------------- 
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2) Field population dynamics of root-knot nematode, 
Meloidogyne incognita throughout growing stages of 
sugarbeet plant. 
3) Relationship between M. incognita and soil microorganisms 
(soil bacteria and fungi). 
4) Relationship between M. incognita and predacious soil 
mites. 
5) Interrelationship among plant parasitic nematode, M. 
incognita, nematophagous fungus and predator nematode in 
the rhizosphere of sugarbeet plants. 
6) Evaluation of some animal manures for mass production and 
as substrate carrier for nematophagous fungi. 
7) Susceptibility of sugarbeet varieties to root-knot nematode, 
M. incognita. 
8) Relationship between initial population density of M. 
incognita and sugarbeet yields. 
  Generally, our investigation suggest the use of nematode 
antagonistic organisms which gave best results in the integrated 
root-knot nematodes management programs to protect the 
environment, human and animal health from the chemical 
compounds dangerous reaching to safety and high agriculture 
production according to GAP recommendations. 
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REVIEW  OF  LITERATURE 
 
1. Plant parasitic nematodes associated with sugar beet 
plants: 
 The intensive cultivation of sugarbeet begun in Germany 
in the first half of the last century soon led to a decline in the 
harvested yield due to unknown causes. This decline in yield was 
generally attributed to " beet fatigue " .  In 1882 Kühn studied the 
problem and conclusively proved that the harvest drop was 
caused by the nematode Heterodera schachtii . In 1889 , under 
Kühn's leadership, an experimental station for nematode control 
was organized at Halle which later recognized as the first plant-
protection institute in the world . ( Decker, 1981 ) . 
 In Egypt , root – knot nematode , Meloidogyne incognita 
and M. javanica  were reported as major nematode pests of 
sugarbeet ( Ibrahim, 1982 and Oteifa and El-Gindi, 1982 ) . Also, 
in Egypt, Koura ( 1983 ) carried out a survey work in sugarbeet 
producing areas and recorded the presence of seven nematode 
genera, viz. Helicotylenchus, Hirschmanniella, Tylenchorhynchus, 
Hoplolaimus, Criconemoides and Pratylenchus in decreasing 
order .  
 Of some 50 described and species of Meloidogyne, only 
few parasitize sugarbeet, viz. M. arenarea, M. incognita, M. 
javanica, M. hapla and M. naasi , are economically important to 
sugarbeet production (Arnold , 1984). 
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 Keller (1984) mentioned that nematodes Heterodera 
schachtii, Meloidogyne spp. and Trichodrus spp. attack sugarbeet 
roots and described their symotoms and biology . 
 Caubel (1984) stated that the Heterodera schachtii 
nematode is the most important of the sugarbeet nematodes and 
gave an account of its distribution . The other nematodes found 
on sugarbeet are H. trifolii , Meloidogyne naasi, Ditylenchus 
dipsaci , D. destructor , Trichodorus spp. and Longidorus spp. 
In studies of relationship between  Heterodera schachtii and , 
Meloidogyne hapla and Nacobbus aberrans  on sugarbeet, 
Inserra et al. (1984) showed that the nematode of  H. schachtii 
and .M hapla  were the most serious pests of sugarbeet in almost 
every country that has a long tradition of beet cultivation . 
 In Spain, Tobar et al. (1984) showed that Heterodera 
schachtii (sugarbeet), H. avenae (cereals), H. goettingiona (peas 
and beans), Meloidogyne incognita (tobacco ana beet), M. 
artiellia (cereals and legumes) and Pratylenchus sp. (cereals and 
other crops), were the most wide spread and significant nematode 
pests. M. artiellia in particular was associated with newly 
irrigated soil  
 Ashoub (1984) studied the pathogenicity of Rotylenchulus 
reniforms to sugarbeet, Beta vulgaris L. in association with some 
physical and chemical soil properties. She found that 
Rotylenchulus multiplied better in sandy clay loam soil of 
Maryiout than in sandy loam soil in Sinai. Rotylenchulus build-
up was higher at sugarbeet fields in calcareous soil and males 
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were abundant, but their percentage was higher in non-
calcareous soil. 
Tacconi (1985) found that the most common nematode in 
Italy are Heterodera schachtii on sugarbeet plantations. 
 Abd El-Massih (1985) noticed that eight important 
nematodes namely, Ditylenchus myceliophagous, 
Helicotylenchus dihystera, Heterodera zeae, Hoplolaimus sp., 
Meloidogyne incognita and M. javanica, Pratylenchus sp., 
Rotylenchulus reniformis and Tylenchorhynchus spp. associated 
with sugarbeet plants at different localities (El-Hamoul Barary 
and West Nubaria regions). Nematode genera, Meliodogyne and 
Rotylenchulus were dominantly found in all the examined fields 
with high population densities. 
 El-Kazzaz et al. (1987) surveyed plant parasitic nematode 
species at sugarbeet fields in Egypt, Pratylenchus penetrans, 
Tylenchorhynchus dubius, Meloidogyne spp. and Heterodera sp., 
they were dominant in all soil samples collected from sugarbeet 
fields and were recorded in high populations in the sugarbeet 
rhizosphere. Large numbers of giant cells were observed 9-14 
days following inoculation of roots with M. incognita. Nematode 
population initially increased and then decreased or fluctuated. 
 In Egypt, Maareg et al. (1988 a) noticed that ten plant 
parasitic genera were associated with sugarbeet cultivars. These 
genera were Criconemoides, Ditylenchus, Helicotylenchus, 
Heterodera, Hoplolaimus, Meloidogyne, Pratylenchus, 
Rotylenchulus, Trichodorus and Tylenchorhynchus. Root-knot 
nematode, Meloidogyne spp. reniform nematodes, Rotylenchulus 
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reniformis and stunt nematode species, Tylenchorhynchus spp. 
were the most prevalent in all beet fields at west Nubaria and 
Kafr El-Sheikh regions. They were found in (100, 70 and 63%) 
and 68, 82 and 76%) of all the collected samples from west 
Nubaria and Kafr El-Sheikh, respectively. 
 Maareg et al. (1988 b) reported that the plant parasitic 
nematodes, especially root-knot nematodes, Meloidogyne 
javanica and M. incognita are known among the most serious 
pests of sugarbeet crop in Egypt. 
Glaba (1990 b) reported that the nematode, Ditylenchus 
dipsaci was found on 24% of sugarbeet fields. Occurrence of the 
nematode according to the natural and economic conditions of 
the area, soil type and other factors are analyzed. D. dipsaci on 
sugarbeet is of no economic importance. 
In the distribution of root-knot nematodes, Meloidogyne 
spp., Glaba (1990 a) collected 567 root samples of fodder beet 
from fields in Gdansk district of Poland. Who reported that M. 
hapla was found in 8% of samples. Other species of Meloidogyne 
were not present in all samples of this area. 
Redondo and Villarias (1991) reported that Heterodera 
schachtii nematode is probably the most serious pest of sugar 
beet in Spain. This nematode is widely distributed in the Duero 
valley (80.000 – 100.000 ha.). About 26.000 soil samples from 
this area have been analyzed and H. schachtii has been found in 
75% of them.  
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Robb et al. (1992) stated that Heterodera schachtii is a 
major pest on sugar beet in Western Nebraska sugar beet (Beta 
vulgaris L.) farms and is costly to control. 
Cooke et al. (1993) recorded that the nematode species of 
Heterodera, Meliodogyne, Ditylenchus, Nacobbus, Trichodorus, 
Paratrichodorus and Longidorus genera on sugar beet roots. 
Caswell Chen and Thomason (1993) investigated the root 
length, diameter and calculated corresponding root volumes 
occupied by nematode life stages of Heterodera schachtii in 
sugar beet. They found that a mean root volume of 0.04 mm³ was 
occupied by second stage juveniles, 0.27 mm³ by 3
rd
 stage 
juveniles, 0.5 mm³ by 4
th
 stage juveniles, 0.5 mm³ by adduct 
females and 0.04 mm³ by 4
th
 stage males. 
Surveys initiated at a sugar beet collection by Schlang 
(1993) who showed that soil adhering to beet originating from an 
area where Heterodera schachtii was prevalent contained an 
average of 9360 eggs and larvae /100 ml soil, the contamination 
ranging from 12 to 60.000 eggs and larvae / 100 ml soil. Also, 
results revealed that at one site, the adhering soil to the beet after 
lifting contained 8.7 times more cyst nematode and 6.8 times 
more eggs and larvae than did soil core samples taken from the 
infected field immediately after harvest. 
Parvizi et al. (1993) studied the distribution of nematode 
infecting of sugar beet fields (about 1002.3 ha.) at the regions, 
Oroumieh, Maindoab, Khoy and Pyranshahr, in west Azerbaijan. 
The results indicated that the percentages of infested soil samples 
were collected from different field were 19.81, 22.35, 3.75 and 
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0.0, respectively for the four localities. They found that 
Heterodera schachtii was dominant in the examined soil samples 
than other species. 
Kyrou (1993) noticed that the root-knot nematodes, 
Meloidogyne incognita, M. javanica and cyst nematode, 
Heterodera schachtii infested sugar beet roots in Greece. On the 
other hand, who gave some morphological observations and 
measurements of H. schachtii, which is recorded for the first time 
in Greece. 
In Iran, Moghaddan and Kheiri (1995) extracted and 
identified 23 nematode species collected from sugar beet fields 
belonging to 15 genera of Tylenchida. Amplimerlinius globigerus 
and Heterodera mani nematodes are reported for the first time in 
Iran. Heterodera schachtii and Meloidogyne javanica were found 
in the soil as well as in root samples. 
Cooke (1995) reviewed and listed the nematode pests 
which can attack sugar beet plants, viz. Ditylenchus dipsaci, 
Nacobbus aberrans, Heterodera schachtii, Meloidogyne 
incognita, M. javanica, M. arenarea, M. hapla, M. naasi, 
Trichodorus spp., Paratrichodorus spp. and Longidorus spp . 
The cyst nematode, H. schachtii and root-knot nematodes, 
Meloidogyne spp. are the most important pests of sugar beet.  
Maareg et al. (1998) revealed that five nematode genera 
namely, Helicotylenchus, Meloidogyne, Pratylenchus 
Rotylenchulus and Tylenchorhynchus were common in the soil 
and root samples collected from newly reclaimed sandy soils of 
sugar beet fields in Al-Bostan region. The genus Meloidogyne 
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was observed in high frequency of occurrence (100%) and 
population density (2896 / 200 ml soil). While Pratylenchus was 
found in low occurrence and population density (61% and 439 / 
200 ml soil, respectively). Helicotylenchus, Rotylenchus and 
Tylenchorhynchus were recorded in moderate frequency (83, 71 
and 75% , respectively). Identified species of genus Meloidogyne 
were M. javanica and M. incognita. M. javanica sp. was 
dominant in this area. 
Maareg and Hassanein (1999) surveyed plant parasitic 
nematode associated with sugarbeet plants at the West of Nubaria 
region. They recorded that nine nematode genera, 
Criconemoides, Ditylenchus, Helicotylenchus, Pratylenchus, 
Rotylenchulus, Trichodorus, Tylenchorhynchus, Hoplolaimus and 
Meloidogyne. The nematodes of Meloidogyne (M. javanica and 
M. incognita), Rotylenchulus (R. reniformis) and 
Tylenchorhynchus spp. were dominant in the investigated region.  
 
Plant parasitic nematodes-agrometrological factors 
relations: 
 The main climatic factors to exert an influence on the 
development of nematodes are temperature and humidity. These 
factors are indirectly primary act. Through the soil or through the 
plant. Furthermore, these conditions are themselves interrelated 
and hence any ecological action is perforce heterogeneous. 
 In the first study for thermal-time relationships of 
nematode development, Tylor (1933) revealed that the duration 
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of the gall of nematode (Meloidogyne sp.) was 25 days at a 
temperature of 27°C and 87 days at a temperature of 16.5°C. 
 Oteifa and El-Gindi (1957) found that M. javanica 
hatched at 30°C and developed at undisclosed temperatures from 
invasion to egg production on early planted tomato in 42 days, 
invasion by second generation juveniles occurred 68 days after 
the initial invasition. Also, Ahmed and Khan (1964) confirmed 
these findings. 
 Seshadri (1965) studied the severity effect of soil 
humidity on population density of Criconemoides xenoplex 
nematode. Who found that the humidity in the soil in the 
experimental vessel was 7.8%, the number of nematodes found 
was 960 + 368; at the humidity of 11.6 – 6.15% + 1,337; and at 
15.5-18.09% + 2,101. Nematodes which have penetrated a plant 
were affected indirectly through the plant by a moisture 
deficiency. 
 Philis (1984) studied the development and reproduction of 
M. javanica on tomato plants in Cyprus at four nematode infested 
sites, two (S1,S2) outdoors and two (S3,S4) in greenhouses. Who 
found that root invasion occurred 17, 7, 16 and 19 days after 
planting at S1, S2, S3 and S4, respectively. Earlier invasion at S2 
was due to favourable temperature soon after planting. Soil 
temperature at the time of invasion at S1, S2 and S4 were 23, 29 
and 18°C, respectively and the accumulated day degrees above 
10°C from planting to invasion were 168, 145 and 161°C days, 
respectively. Invasion by juveniles of generation at S1,S2,S3 and 
S4 occurred at 7, 13, 31 and 21 days after egg laying when soil 
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temperature were 25.5, 26.5 and 20.0°C at S1, S2 and S4, 
respectively. 
 Lahtinen et al. (1988) studied the threshold temperature 
and minimum thermal time on life cycle of Meloidogyne hapla in 
a greenhouse in Finland. They found that the threshold 
temperature was 8.25°C and thermal time above this base for 
development for juvenile to the first juvenile of the second 
generation was about 553°C days. The results revealed that the 
rate of egg hatch had showed at the lowest temperature used 
(17°C), possibly because of a slight diapause. 
 Influence of temperature on population of Meloidogyne 
javanica was evaluated by Madulu and Trudgill (1994). They 
found that the rate of development increased linearly between 
18°C and 27°C. On a thermal time basis, the threshold or base 
temperature fordevelopment was estimated by extrapolation to be 
12.9°C and requirement for development 350°C days above the 
base. These values were compared with those for M. hapla, a 
temperate species, and their effects on development time in 
relation to temperature were also discussed. 
 Trudgill (1995) showed that the rate of development of M. 
javanica remained nearly constant between 27 and 31°C, it is 
unlikely that the life cycle and the rate of development of M. 
javanica are shorter than these of M. incognita at any 
temperature. 
 Hassan (1998) studied response of the nematodes, 
Meloidogyne javanica, Pratylenchus sp., Helicotylenchus sp. and 
Longidorus sp. associated with date palm trees and the 
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nematodes, M. javanica, Tylenchulus semipenetrans, 
Helicotylenchus sp. and Pratylenchus sp. associated with orange 
trees to soil moisture, soil temperature and subsoil water during 
two years in Minia Governorate, Egypt. Variation of soil 
moisture, soil temperature and subsoil water level throughout the 
different seasons was followed by the fluctuation of nematode 
population. Significant positive correlation  among all these 
factors and nematode numbers had been observed. 
 Ploeg and Maris (1999) studied the effects of temperature 
degrees on the duration of the life cycle of Meloidogyne 
incognita population. The life cycle was completed on tomato 
plants between soil temperature of 16.2 and 30° C, but not at 
35.4° C. On the other hand, on the marigold plant (Tagetes 
hybrid) variety Polynema, the life cycle was completed only at 
30° C. Estimates for the base temperature and required heat sun 
were 10.1° C and 400° C days, respectively. 
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2. Arthropode fauna associated with cultivated soil: 
 Soil fauna investigations began in Egypt in the early 
twentieth. Priesher (1929-1937; 1938-1950) investigated some 
individuals of Thysanura that pass one or more of its stages in 
soil. Certain biological aspects of Gryllotalpa gryllotalpa (L.) 
and its distribution in Egypt were recorded by Kassab (1938). 
The insect fauna of the dung was investigated by Hafez (1938, 
1947 and 1948). His investigation covered fauna occurring in 
either fresh or old farmyard manure, and also in the dung of 
working and grazing animals. Later on, El-Kifl (1957 and 1958) 
evaluated soil arthropods in a farm at Giza, Egypt. Who also 
recorded the magnitude of Myriapods in a cultivated land. El Kifl 
et al. (1974) investigated soil arthropods, other than insects in a 
new reclaimed area. Popp (1960) described some new oribated 
species and new genera extracted by Tadros from the previous 
farm at Giza region. Wafa et al. (1965) studied most probable 
factors responsible for soil fauna fluctuations in Giza region. 
Tadros (1975) studied some important factors responsible for soil 
oribatid fluctuations, in Kafr El-Sheikh region, Egypt. 
 The correlation between percentage of both organic matter 
and micro-flora, with the horizontal distribution of soil oribatids 
in Shoubra El-Kheima, Qualubia Governorate, Egypt was also 
investigated by Tadros et al. (1977). Tadros and Saad (1979) in 
special investigation compared soil fauna existing in an ordinary 
vegetable farm and some vegetables grown under plastic tunnels. 
Abo-Korah (1979) recorded fauna from new reclaimed area. 
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Maareg (1979) surveyed soil animals of three different soils, clay 
(rain-fed olive), clay loam (irrigated olive soil) and sandy clay 
loam (vine farm) in the Egyptian Western Desert. 
 Abo-Korah et al. (1980) investigated soil fauna especially 
tarsonomid mites under certain field crops in Menoufyia 
Governorate, Egypt and under truck crops. While, Moustafa 
(1980) investigated the soil mites in cotton fields. Maareg (1984) 
studied the monthly variation of arthropod fauna populations 
associated with some selected cattle manure amendment. In a 
survey and ecological studies on predaceous and non-
phytophagous mites in Egypt carried out by Zaher (1986) Who 
showed that 400 mites species belonging to 58 families, the 
magnitude of the collected mites (253 species) belonging to 
Prostigmata. Maareg et al. (1986 b) studied the seasonal 
fluctuation of the fauna inhabiting the chicken manure especially 
the predaceous fauna. Also, Maareg et al. (1986 a) studied 
seasonal fluctuation and vertical distribution of soil acari groups 
under sugar cane plants. Sharshir (1986) studied most ecological 
factors responsible for the population density and dynamics of 
soil fauna especially acari population, acari density of soil mites 
under different orchards in Kafr El-Sheikh Governorate, Egypt. 
 Sevastianov and Rady (1989) reviwed mite genera of 
family Saproglyphidae (Sarcoptiforms) in the world fauna, with 
description of Procaluolia hamadi mite as a new species from 
Egypt. 
 In Nigeria in two contrasting environments, Badejo (1990) 
found that changes in abundance of soil mites within and 
between seasons on the forest under cassava plots, but