5
Egypt. J. Agronematol., Vol. 17, No.1, PP. 51-64 (2018)
Description and Identification of Four Species of
Plant-parasitic Nematodes Associated with
Forage Legumes
*
*
Mahfouz M. M. Abd-Elgawad ; Mohamed F.M. Eissa ; Abd-Elmoneim Y.
**
El-Gindi ; Grover C. Smart
***
****
; and Ahmed El-bahrawy
.
*
Plant Pathology Department, National Research Centre.
**
Department of Agricultural Zoology and Nematology, Faculty of Agriculture, University of
Cairo, Giza, Egypt.
*** Department of Entomology and Nematology, IFAS, University of Florida, USA.
**** Institute for Sustainable Plant Protection, National Council of Research, Bari, Italy.
Abstract
Four species of plant parasitic nematodes were present in soil samples
planted with forage legumes at Alachua County, Florida, USA. The detected
species Belonolaimus longicaudatus, Criconemella ornate, Hoplolaimus galeatus,
and Paratrichodorus minor were described in the present study. They belong to
orders Rhabditida (Belonolaimus longicaudatus, Criconemella ornate, and
Hoplolaimus galeatus) and Triplonchida (Paratrichodorus minor) and to taxonomical
families Dolichodoridae (Belonolaimus longicaudatus), Hoplolaimidae (Hoplolaimus
galeatus)
Criconematidae
(Criconemella
ornate),
and
Trichodoridae
(Paratrichodorus minor). The identification of the present specimens was based on
the classical taxonomy, following morphological and morphometrical characters in
the species specific identification keys.
Keywords:
Belonolaimus longicaudatus, Criconemella ornate, Hoplolaimus
galeatus, Paratrichodorus minor, morphology, species description.
Introduction
As is widely and rightly held nematodes (round worms) are diversified
multicellular animals comprising free living to plant, animal and even humanparasitic species. They represent a group of the most numerous metazoans in soil
and aquatic sediments. From an environmental point of view, nematodes are part of
nearly all ecosystems in their roles as bacterivores, herbivores, parasites of
animals and plants, and consumers of dissolved as well as particulate organic
matter (Mekete et al., 2012). Among them, plant-parasitic nematodes (PPNs) form
prominent and distinguished group. These latter are mostly hidden enemy of the
growers as the nematodes are generally subterranean in habitats and farmers are
52
Mahfouz M. M. Abd-Elgawad, et al.,….
unaware of losses caused by them. A great loss to crops has been reported in
quantitative, qualitative and monetary terms. Considering their impact on crops,
Abd-Elgawad and Askary (2015) reported an average worldwide crop loss of
12.6% which equaled $215.77 billion due to these nematodes for only the top 20
life-sustaining crops based on the 2010-2013 production figures and prices.
Moreover, 14.45% or $142.47 billion was an average annual yield loss in the
subsequent group of food or export crops. These figures are staggering, and the
authentic figure, when more crops are counted, certainly exceeds such estimations.
Nevertheless, it is noteworthy that PPNs are among the least studied, with
close to only 26,000 (estimated < 3%) species described to date (Hugot et al.,
2001; Mekete et al., 2012). Accuracy of identification is, therefore, fundamental to
our understanding and communication of the ecological role of any organism. It
goes without saying that PPN identification has its strength in agricultural
applications because of its economic participation in nematode management
implications. Consequently, PPN species delimitation methods in the context of
agricultural and health-related applications are more refined at the species and
below species level than methods employed in nematode biodiversity studies. Yet,
both groups of studies help in better understanding of nematology and its interaction
with relevant disciplines. In fact, specimen identification are imperative not only for
choosing adequate management control strategies for PPNs but also for avoiding
spreading of such exotic nematodes in quarantine materials. Yet, PPNs are one of
the hardest groups to be identified due to their microscopic sizes as well as the
difficulties in observing key diagnostic characters/features under conventional light
microscope (Carneiro et al., 2017).
On the other hand, legumes represent some of the best quality forages for
livestock since they are palatable, help maintain proper functioning of the ruminant
digestive processes and stimulate high production of both meat and milk. Since they
possess an excellent attribute of biological nitrogen fixation in association with
rhizobia, which helps in sustaining soil fertility, legumes are used as green manure
by ploughing them into the soil. Considering their impact on crops, PPNs associated
with common forage legumes were studied for morphometric identification in this
work.
Materials and Methods
Soil of three experimental areas with established stands of fifteen adapted
clover cultivars were sampled for PPNs. The experimental areas, properties of the
University of Florida, were located in Alachua County near Gainesville, Florida, USA
at altitude of 30 degrees north and a longitude of 82 degrees west. The three
experiments, set up initially to test forage cultivars, had been established in a
randomized block design with clover cultivars and controls as treatments. The
sampled clover cultivars comprised Trifolium repens (white clover) cvs 'FL-XP1',
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
Description and Identification of Four Species of Plant-parasitic Nematodes Associated ……
53
'Regal', 'FL-XP2', 'LA-SI', and 'Tillman'; T. pretense (red clover) cv. 'Kenstar'; T.
vesiculosum (arrowleaf clover) cvs 'Amclo', 'REPS-5' and 'Yuchi'; T. incarnatum
(crimson clover) 'Dixie'; T. subterraneum (subterranean clover) cvs 'Mt. Barker' and
'Woogenellup'; T. alexandrinum (Egyptian clover) cv. 'Bigbee'; Medicago sativa
(alfalfa) cv. 'FL-77'; and Melilotus alba var annua (sweet clover) cv. 'Hubam'.
Phytonematodes associated with the forage legumes of these experiments were
reported to the generic level (Abd-Elgawad et al., 2017). About five 2.5-cm
diameter cores were taken randomly within the root zone (upper 15-20 cm) from
each plot and then mixed thoroughly to form one sample representing the plot. Each
sample was placed in a plastic bag, stored in an ice chest, and transported to the
nematology laboratory. Samples not processed immediately were stored at 10 ± 1
0
3
C until processed. Nematodes were extracted from 100 cm soil from each sample
using a centrifugal-flotation technique (Caveness and Jensen, 1955), placed in
vials, and stored in a refrigerator at 4C for no more than three days until identified
to genera and counted. Thereafter, some of the nematodes extracted from the study
(Abd-Elgawad et al., 2017) were taken and processed for identification to the
species level as originally described by Goodey (1963). Three percent formalin was
used for making temporary mounts of nematodes. One percent water agar was
®
used (for en face mounts) and Zut slide-ringing compound was used to seal the
slides. Drawings were made with the camera lucida technique equipped to the
microscope. All measurements except ratios are expressed in μm as means ±
standard deviation. Key references of Rau (1963), Luc and Raski (1981),
Jairajpuri and Baqri (1973), and Decraemer (1980) were consulted to identify
species of Belonolaimus, Criconernella, Hoplolaimus, and Paratrichodorus. A
magnification of 1000 x was used to identify all nematodes. Throughout these
identifications, we adopted the systematic scheme of De Ley and Blaxter (2002)
for the higher classification which has been updated where appropriate by
Decraemer and Hunt (2013) to reflect new taxa proposals.
Results and Discussions
Species of four genera of plant-parasitic nematodes associated with all the
above-mentioned clover cultivars were identified as Belonolaimus longicaudatus,
Criconemella ornate, Hoplolaimus galeatus, and Paratrichodorus minor (Tables 1-4;
Figs. 1-4). Measurements and drawings of nematode species are presented in
Tables 1 through 4 and Figures 1 through 4; respectively. Golden (1971) classified
the genera and higher categories of the order Tylenchida in which all of these
nematodes are placed except Paratrichodorus minor which is in the order
Dorylamida and published by Siddiqi (1973). Nevertheless, family Trichodoridae is
no longer part of Dorylaimida and Tylenchida doesn't exist (now it is Rhabditida). In
fact, recent molecular phylogenetic analyses recognize 12 clades within the
Nematoda, with plant-parasitic taxa located in the basic clade I (Trichodoridae) and
clade II (Longidoridae) and in the more advanced clade 12 with the
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
54
Mahfouz M. M. Abd-Elgawad, et al.,….
Tylenchomorpha (Holterman et al., 2006; Decraemer and Hunt, 2013).
Accordingly, the species identified herein belong to orders Rhabditida
(Belonolaimus longicaudatus, Criconemella ornate, and Hoplolaimus galeatus) and
Triplonchida (Paratrichodorus minor) and to taxonomical families Dolichodoridae
(Belonolaimus
longicaudatus),
Hoplolaimidae
(Hoplolaimus
galeatus)
Criconematidae (Criconemella ornate), and Trichodoridae (Paratrichodorus minor).
The morphometric identification carried out herein neither negates the need for
molecular tools for its documentation nor declines the presence of other PPN
species associated with such forages (Abd-Elgawad et al., 2018). In fact, PPNs
have been receiving sufficient attention regarding their taxonomy and evolution and
therefore they are currently undergoing continuous modifications in their
classification, phylogeny and taxonomy (e.g. Sun et al., 2014; Guesmi-Mzoughi et
al., 2016).
Belonolaimus longicaudatus (Table1; Fig.1) was identified using the
dichotomous key of Rau (1963). He stated that this species is different from B.
euthychilus, B. gracilis, and B. maritimus to which it is related in ratio of stylet length
to tail length. Sixty to 100% of B. longicaudatus populations have stylets shorter
than tails while the opposite is true with the other species. B. longicaudatus differs
from B. nortoni in that B. longicaudatus has a relatively longer stylet and lips of
vulva are not protruding.
Table (1): Measurements and ratios of females and males of Belonolaimus
longicaudatus associated with forage legumes.
Body regions and
organs
Body length
Dimensions (μm) and ratios
Females (n= 10)
Males (n= 10)
Minimum Maximum Average±S.D. Minimum Maximum Average±S.D.
2085
2871
2395 ± 121
1987
2193
2031 ± 136
Body diameter
36
44
41
38
43
41
Tail length
120
172
150 ± 14.8
110
169
141 ±16
Anal body diameter
32
38
34
29
34
31
Stylet length
118
129
123 ± 11.3
112
119
115 ± 11
Esophagus length
268
290
276
314
335
325
Distance from head to vulva
1028
1520
1278
--
-
-
-
-
-
39
47
43
Spicule length
A ratio
62
67
-
61
65
-
B ratio
7.8
8.3
-
6.6
7.3
-
C ratio
14
19
-
13
15
-
Ć ratio
3.8
4.5
-
3.8
3.9
-
V%
49%
55%
—
-
-
-
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
Description and Identification of Four Species of Plant-parasitic Nematodes Associated ……
55
The image cannot be displayed. Your computer may not hav e enough memory to open the image, or the image may hav e been corrupted. Restart your computer, and then open the file again. If the red x still appears, y ou may hav e to delete the image and then insert it again.
Fig. (1): Belonolaimus longicaudatus (Rau, 1958).
(A) Anterior body region, (B) Head region, (C) Vulval region, (D) Female tail, E - Male tail.
Criconemella ornate (Table 2; Fig. 2) is related to C. curvatum but differs from
the latter by the absence of labial plates and by the pointed outline of the anterior
vulvar flap (Raski, 1952). Additional important features of C. ornate is the presence
of the sub-lateral lobes and the relatively few annules, i.e., 87 to 92 annules (Raski,
1958).
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
56
Mahfouz M. M. Abd-Elgawad, et al.,….
Table (2): Measurements and ratios of females of Criconemella ornate associated
with forage legumes.
Dimensions (μm) and ratios(n= 13)
Body regions and organs
Body length
Body diameter
Tail length
Anal body diameter
Stylet length
Esophagus length
Distance from head to vulva
Spicule length
A ratio
B ratio
C ratio
Ć ratio
V%
Minimum
Maximum
Average ± S.D.
340
28
14
13
44
85
310
9
3
16
1.1
86%
460
46
27
24
61
127
395
-16
4
27
1.1
96%
404 ± 34
37
21 ± 5.4
19
52 ± 4.5
103
366
-----91%
Jairajpuri and Baqri (1973) presented a key for Hoplolaimus spp. They
differentiated between H. Tylenchiformis, having three annules in the lip region and
female tails usually bluntly rounded, and H. galeatus (Table 3; Fig. 3), having four or
more annules and female tails rounded. Also, they used the following characteristics
of H. galeatus to differentiate it from other Hoplolaimus spp.: four incisures on the
body, excretory pore located below the hemizonid, one phasmid in anterior part of
the body and one phasmid in the posterior part of it, and spicules 40 - 50 μm long.
Table (3): Measurements and ratios of females and males of Hoplolaimus galeatus
associated with forage legumes.
Dimensions (μm) and ratios
Females (n= 10)
Body regions and organs
Minimum Maximum
Body length
Body diameter
Tail length
Anal body diameter
Stylet length
Esophagus length
Distance from head to vulva
Spicule length
A ratio
B ratio
C ratio
Ć ratio
V%
1283
40
15
31
48
178
736
-25.8
6.7
38.4
0.5
52%
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
1643
55
37
39
60
220
853
-37.8
8.4
97.6
1.0
58%
Average ±
S.D.
1464 ± 119
47
26 ± 8
35
5.2 ± 4.6
200
807
-------
Males (n= 4)
Minimum Maximum
983
35
20
25
42
165
-51
28.1
6
37.3
0.8
--
1195
42
32
33
50
190
-59
28.5
6.3
49.2
1.0
--
Average ±
S.D.
1072 ± 99
39
26 ± 5
28
45 ± 3.6
180
-55
------
Description and Identification of Four Species of Plant-parasitic Nematodes Associated ……
57
Fig. (2): Criconemella ornate (Raaki, 1958, Luc & Raski, 1981).
(A) Adult female, (B) Head en face view, (C) Female tail, (D) Anterior body region.
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
58
Mahfouz M. M. Abd-Elgawad, et al.,….
Fig. (3): Hoplolabnus galeatus (Cobb, 1913, Thorne, 1935).
(A) Vulval region, (B) Female tail, (C) Anterior body region, (D) Male, head region, (E) Male, tail region.
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
59
Description and Identification of Four Species of Plant-parasitic Nematodes Associated ……
After Siddiqi's division (1973) of the genus Trichodorus into Paratrichodorus
and Trichodorus, there had been considerable confusion in the literature because
some authors apparently had not recognized Paratrichodorus spp. as a valid genus,
whereas others had (Perry and Rhoades, 1982). Now, both genera are well
established (e.g., Decraemer and Hunt, 2013). In our specimens (Table 4; Fig. 4)
the two characters used for separating the genus, i.e. male with bursa and female
with weak and indistinct sclerotization between the vulva and vagina were
recognizable and it keys to P. christiei. Yet, our specimens agreed with the
synonomy of P. christiei and P. minor since the lengths of the onchiostyle and
spicules of our specimens overlap those of both species (Loof, 1975; Decraemer,
1980).
Table (4): Measurements and ratios of females and males of Paratrichodorus minor
associated with forage legumes.
Dimensions (μm) and ratios
Females (n= 10)
Body regions and organs
Average±
Minimum Maximum
S.D.
Males (n= 4)
Minimum
Maximum
Average ±
S.D.
Body length
462
735
610 ±117
589
692
633 ± 4
Body diameter
30
49
35
34
38
37
Tail length
--
--
--
19
23
20 ± 2
Anal body diameter
--
--
--
9
12
10
Stylet length
30
48
41 ± 8
32
40
36 ± 4
Esophagus length
96
122
106
85
90
87
Distance from head to vulva
240
370
310
--
--
--
Spicule length
--
--
--
58
66
61
A ratio
15
15.4
15.2
17.3
18.2
--
B ratio
4.8
6
5.4
6.9
7.7
--
C ratio
--
--
--
30
31
--
Ć ratio
--
--
--
1.9
2.1
--
50%
52%
51%
--
--
=
V%
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
60
Mahfouz M. M. Abd-Elgawad, et al.,….
Fig. (4) Paratrichodorus minor (Allen,1957, Siddiqi, 1973).
(A) Adult female, (B) Female, anterior body region, (C) Male tail, (D) Vulval region, E- Female tail.
Egypt. J. Agronematol., Vol. 17, No. 1, (2018)
Description and Identification of Four Species of Plant-parasitic Nematodes Associated ……
61
Acknowledgement
This study was supported in part by the NRC In-house project entitled
'Pesticide alternatives against soilborne pathogens attacking legume cultivation in
Egypt'.
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64
وﺻﻒ وﺗﻌﺮﻳﻒ أرﺑﻌﺔ أﻧﻮاع ﻣﻦ اﻟﻨﻴﻤﺎﺗﻮدا اﻟﻤﺘﻄﻔﻠﺔ ﻧﺒﺎﺗﻴﺎ اﻟﻤﺮﺗﺒﻄﺔ ﺑﺎﻟﺒﻘﻮﻟﻴﺎت اﻟﻌﻠﻔﻴﺔ
ﻣﺤﻔﻮظ ﻣﺤﻤﺪ ﻣﺼﻄﻔﻰ ﻋﺒﺪ اﻟﺠﻮاد* ،ﻣﺤﻤﺪ ﻓﻬﻤﻲ ﻣﺤﻤﺪ ﻋﻴﺴﻲ* ،ﻋﺒﺪ اﻟﻤﻨﻌﻢ ﻳﺎﺳﻴﻦ اﻟﺠﻨﺪي**،
ﺟﺮوﻓﺮ ﺳﻤﺎرت*** ،وأﺣﻤﺪ اﻟﺒﺤﺮاوي
*
****
ﻗﺴﻢ أﻣﺮاض اﻟﻨﺒﺎت ،اﻟﻤﺮﻛﺰ اﻟﻘﻮﻣﻲ ﻟﻠﺒﺤﻮث ،اﻟﺪﻗﻲ ،١٢٦٢٢اﻟﻘﺎﻫﺮة ،ﻣﺼﺮ.
** ﻗﺴﻢ اﻟﺤﻴﻮان واﻟﻨﻴﻤﺎﺗﻮﻟﻮﺟﻴﺎ اﻟﺰراﻋﻴﺔ ،ﻛﻠﻴﺔ اﻟﺰراﻋﺔ ،ﺟﺎﻣﻌﺔ اﻟﻘﺎﻫﺮة ،اﻟﻘﺎﻫﺮة ،ﻣﺼﺮ.
*** ﻗﺴﻢ اﻟﺤﺸﺮات واﻟﻨﻴﻤﺎﺗﻮﻟﻮﺟﻲ ،ﻣﻌﻬﺪ ﻋﻠﻮم اﻟﻐﺬاء واﻟﺰراﻋﺔ ،ﺟﺎﻣﻌﺔ ﻓﻠﻮرﻳﺪا ،اﻟﻮﻻﻳﺎت اﻟﻤﺘﺤﺪة اﻷﻣﺮﻳﻜﻴﺔ.
**** ﻣﻌﻬﺪ اﻟﻮﻗﺎﻳﺔ اﻟﻤﺴﺘﺪاﻣﺔ ﻟﻠﻨﺒﺎت ،اﻟﻤﺠﻠﺲ اﻟﻘﻮﻣﻲ ﻟﻠﺒﺤﻮث ،ﻣﺪﻳﻨﺔ ﺑﺎري ،إﻳﻄﺎﻟﻴﺎ.
اﻟﻤﻠﺨﺺ اﻟﻌﺮﺑﻲ
ﺗﻢ وﺻﻒ وﺗﻌﺮﻳﻒ أرﺑﻌﺔ أﻧﻮاع ﻣﻦ اﻟﻨﻴﻤﺎﺗﻮدا اﻟﻤﺘﻄﻔﻠﺔ ﻧﺒﺎﺗﻴﺎ اﻟﻤﺮﺗﺒﻄﺔ ﺑﺎﻟﺒﻘﻮﻟﻴﺎت اﻟﻌﻠﻔﻴﺔ ﻓﻲ ﻣﻘﺎﻃﻌﺔ
اﻻﺷﻮا ﻓﻲ وﻻﻳﺔ ﻓﻠﻮرﻳﺪا ﺑﺎﻟﻮﻻﻳﺎت اﻟﻤﺘﺤﺪة اﻷﻣﺮﻳﻜﻴﺔ .اﻷﻧﻮاع اﻟﻤﻜﺘﺸﻔﺔ ﻓﻲ ﻫﺬﻩ اﻟﺪراﺳﺔ ﻫﻲ
ﺑﻴﻠﻮﻧﻮﻻﻳﻤﻮس ﻟﻮﻧﺠﻴﻜﻮداﺗﻮس ،ﻛﺮﻳﻜﻮﻧﻴﻤﻴﻼ أورﻧﺎت ،ﻫﻮﺑﻠﻮﻻﻳﻤﻮس ﺟﺎﻟﻴﺎﺗﻮس ،وﺑﺎراﺗﺮﻳﻜﻮدوروس
ﻣﻴﻨﻮر ،وﻫﻲ ﺗﻨﺘﻤﻲ إﻟﻲ اﻟﺮﺗﺐ رﺑﺪﻳﺘﻴﺪا )ﺑﻴﻠﻮﻧﻮﻻﻳﻤﻮس ﻟﻮﻧﺠﻴﻜﻮداﺗﻮس ،ﻛﺮﻳﻜﻮﻧﻴﻤﻴﻼ اورﻧﺎت،
وﻫﻮﺑﻠﻮﻟﻴﻤﻮس ﺟﺎﻟﻴﺎﺗﻮس( وﺗﺮﻳﺒﻠﻮﻧﺸﻴﺪا )ﺑﺎراﺗﺮاﻳﻜﻮدوروس ﻣﻴﻨﻮر( واﻟﻌﺎﺋﻼت اﻟﺘﺼﻨﻴﻔﻴﺔ
دوﻟﻴﻜﻮدورﻳﺪاي )ﺑﻴﻠﻮﻧﻮﻻﻳﻤﻮس ﻟﻮﻧﺠﻴﻜﻮداﺗﻮس( ،ﻫﻮﺑﻮﻟﻮﻻﻳﻤﻴﺪاي )ﻫﻮﺑﻠﻮﻻﻳﻤﻮس ﺟﺎﻟﻴﺘﻮس(
ﻛﺮﻳﻜﻮﻧﻤﺎﺗﻴﺪا )ﻛﺮﻳﻜﻮﻧﻴﻤﻴﻼ اورﻧﺎت( ،وﺗﺮﻳﻜﻮدورﻳﺪاي )ﺑﺎراﺗﺮﻳﻜﻮدوروس ﻣﻴﻨﻮر( .اﺳﺘﻨﺪ اﻟﺘﻌﺮﻳﻒ
اﻟﺤﺎﻟﻲ ﻟﻬﺬﻩ اﻷﻧﻮاع إﻟﻰ اﻟﺘﺼﻨﻴﻒ اﻟﻜﻼﺳﻴﻜﻲ ﺑﺎﺳﺘﺨﺪام ﻣﻔﺎﺗﻴﺢ ﺗﺤﺪﻳﺪ اﻷﻧﻮاع اﻟﻤﺤﺪدة ﺑﻨﺎء ﻋﻠﻰ
اﻟﺼﻔﺎت واﻟﻘﻴﺎﺳﺎت اﻟﻤﻮرﻓﻮﻟﻮﺟﻴﺔ )اﻟﺨﺎﺻﺔ ﺑﺎﻟﺸﻜﻞ اﻟﻈﺎﻫﺮي(.
اﻟﻜﻠﻤﺎت اﻟﺪاﻟﺔ :ﺑﻴﻠﻮﻧﻮﻻﻳﻤﻮس ﻟﻮﻧﺠﻴﻜﻮداﺗﻮس -ﻛﺮﻳﻜﻮﻧﻴﻤﻴﻼ اورﻧﺎت -ﻫﻮﺑﻠﻮﻻﻳﻤﻮس ﺟﺎﻟﻴﺎﺗﻮس-
ﺑﺎراﺗﺮﻳﻜﻮدوروس ﻣﻴﻨﻮر -اﻟﺸﻜﻞ اﻟﻈﺎﻫﺮي -وﺻﻒ اﻷﻧﻮاع.
)Egypt. J. Agronematol., Vol. 17, No. 1, (2018