Profiling soil free-living nematodes in the Namib Desert, Namibia
Eugene MARAIS1, Gillian MAGGS-KÖLLING1, Chen SHERMAN2, Tirza DONIGER2, LIU Rentao3, Binu M TRIPATHI4, Yosef STEINBERGER2,*()
1 Gobabeb Research and Training Centre, Walvis Bay, Gobabeb 953, Namibia 2 The Mina & Everard Goodman Faculty of Life Sciences Bar-Ilan University, Ramat-Gan 5290002, Israel; 3 Key Laboratory for Restoration and Reconstruction of Degraded Ecosystem in Northwestern China of Ministry of Education, Ningxia University, Yinchuan 750021, China 4 Korea Polar Research Institute, Incheon 21990, Korea
Functional structure and diversity of soil free-living nematodes in a desert environment depend on plant gender and sampling site. The objective of this study was to compare the composition, abundance and tropic group of soil free-living nematodes in the upper 0-10 cm soil layer under the male and female Acanthosicyos horridus Welw. ex Hook. f. plants and in the inter-shrub open areas (control) in the Namib Desert, Namibia in April 2015. Soil moisture, organic matter (OM) and pH was also analyzed. Free-living nematodes were extracted from 100 g soil using the Baermann funnel procedure, and total number of nematodes was counted under a microscope. Community composition and diversity of soil free-living nematodes were analyzed using 18S rDNA sequences. Results indicated that a total of 67 groups, including 64 species, 2 genera and 1 family were identified. Feeding behavior of 58 species were identified as follows: 15 bacteria-feeding species, 12 fungi-feeding species, 10 plant-parasite species, 5 omnivorous-predator species, 8 animal-parasite species, 5 invertebrate-parasite species and 3 non-free-living nematodes, known as marine species. Moreover, soil free-living nematodes were found to be affected by sampling locations and plant gender, and community composition and density of these nematodes were strongly influenced by soil OM content. Result confirmed that spatial location and plant cover were main factors influencing the diversity of soil free-living nematodes. Moreover, molecular tools were found to be very useful in defining the richness of soil non-free-living nematodes. In conclusion, the results elucidated the importance of biotic variables in determining the composition and abundance of soil free-living nematodes in the Namib Desert, Namibia.
Table 1 ANOVA results for soil physical-chemical characteristics at different sites and locations
Fig. 1 Density of soil free-living nematodes at different sites (Delta, Gobabeb and Far East (FE) sand dunes) and locations. Fem., female A. horridus plants; Cont., control (inter-shrub open areas). Different lowercase letters indicate significant differences among three locations at P<0.05 level.
Fig. 2 Relative abundances of metazoa, fungi, algae and protista groups at different sites and locations based on 18S rDNA sequences. Fem., female A. horridus plants; Cont., control (inter-shrub open areas).
Location
Delta (%)
Gobabeb (%)
Far East sand dunes (%)
Male
17
50
0
Female
33
0
13
Control
33
0
37
Male and female
0
0
37
Male and control
0
25
0
Female and control
0
13
13
Male, female and control
17
13
0
Table 2 Percentages of soil free-living nematodes at different sites and locations, and overlap percentage among plant gender and control locations
Nematode species
Delta
Gobabeb
Far East sand dunes
Trophic group
Cont.
Fem.
Male
Cont.
Fem.
Male
Cont.
Fem.
Male
Ditylenchus destructor
_
_
+
FF
Number of species
_
_
1
Acrobeles ciliatus
+
_
+
BF
Amblydorylaimus isokaryon
_
_
+
OP
Anisakis simplex
_
_
+++
AP
Aphelenchoides (genus)
_
_
+
FF
Aphelenchoides sp. US02
_
+
+
FF
Brugia timori
_
_
+++
TM
Bursaphelenchus abruptus
_
_
+
FF
Caenorhabditis elegans
_
_
+
BF
Cephalobus cubaensis
_
_
+
BF
Cooperia oncophora
_
_
+
AP
Echinocephalus overstreeti
_
_
++
Enchodelus longispiculus
_
_
+
PF
Enterobius vermicularis
_
_
+
AP
Fergusobia sp. 281
_
_
+
FF
Fergusobia sp. 469
_
_
+
FF
Halalaimus sp. TCR26
_
_
+
MS
Halalaimus sp. TCR93
_
_
+
MS
Isolaimium multistriatum
_
_
+
MS
Krefftascaris sharpiloi
_
_
+
AP
Longidorus jonesi
_
+
+++
PP
Meloidogyne javanica
_
_
+
PP
Meloidogyne sp. Pak.P.R.m2
_
_
+
PP
Meloidogyne sp. VO-2014
_
_
+
PP
Panagrolaimidae sp. NK-2011b
_
_
+
BF
Parastrongyloides trichosuri
_
+
+++
OP, AP
Passalurus ambiguus
_
_
+++
OP
Pseudhalenchus minutus
_
_
+
Rhyssocolpus paradoxus
_
+
OP
Rhyssocolpus vinciguerrae
_
_
+
OP
Robustodorus megadorus
_
_
+
Romanomermis culicivorax
+
+
+
Schistonchus caprifici
_
_
+
PP
Steinernema feltiae
_
_
+
PI
Steinernema sp. T51
_
_
+
PI
Syphacia muris
_
_
+
Tricoma sp. 2 CYC-2009
_
_
+
Trophotylenchulus sp. TSH-2009
_
_
+
Xiphinema krugi
_
_
++
Xiphinema setariae
_
_
+++
PP
Number of species
2
5
39
PP
Ditylenchus sp. 5 JH-2014
_
+
_
FF
Number of species
0
1
0
Acrobeles sp.
_
+
+
+
_
+
_
+
+
BF
To be continued
Continued
Nematode species
Delta
Gobabeb
Far East sand dunes
Trophic group
Cont.
Fem.
Male
Cont.
Fem.
Male
Cont.
Fem.
Male
Acrobeles sp. MA-2012
+
+
+
+
+
+
+
_
+
BF
Acrobeloides cf. buetschlii 1 JH-2012
+++
+++
-
+
-
++
+
+
+
BF
Acrobeloides maximus
+++
+++
+
+++
_
+++
_
+
++
BF
Aphelenchus avenae
_
+
_
_
_
+
_
+
++
FF
Aporcelaimellus sp. JH-2004
+
+
+
++
+++
+
+
+
+
Bursaphelenchus anatolius
_
+
_
_
+
++
_
+
+
FF
Bursaphelenchus penai
+
+
_
+
+
+
_
+
+
FF
Cephalobidae (family)
+
++
_
+++
+++
+++
+
+++
+++
BF
Cylicostephanus goldi
+
_
_
+
+
+
+++
_
+
AP
Deladenus proximus
_
+
_
+
+
+++
_
+
+
PW
Haemonchus placei
++
+
+
+++
+++
+++
+++
+
+
PPR
Hexamermis albicans
+
+
+
+
+
+
+
_
_
EA
Hexatylus sp. 1 JH-2014
_
+
_
+
+
+
_
+
+
FF
Malenchus pressulus
_
+
+
_
+
+
_
+
+
PPR
Meloidogyne incognita
_
_
+
_
_
+
_
+
+
PP
Panagrolaimus paetzoldi
_
_
+
_
_
++
_
+
+
BF
Panagrolaimus sp. AS01
+
+++
+++
++
+++
+++
+
+++
+++
BF
Panagrolaimus sp. AS03
+
+++
+++
_
_
+
_
+
+
BF
Panagrolaimus sp. SN103
_
+
++
+
+
+
_
+
+
BF
Paratylenchus goldeni PP
+++
+++
+
+++
+
+++
+
++
++
PP
Paratylenchus labiosus
_
+
_
_
_
+
_
+
+
PP
Turbatrix aceti
_
_
+
+
+
+
_
+
+
AP
Tylenchulus semipenetrans
+
++
+
+
+
+
_
+
+
FF
Uncultured Rhabdolaimus (genus)
+
_
+
++
+
+++
+++
+
+
BF
Number of species
14
20
16
20
18
25
10
22
24
Total number of species
14
20
17
22
23
64
10
23
24
Table 3 Taxa and trophic groups of soil free-living nematodes using 18S rDNA sequences and BLAST similarity analysis at different sites and locations
Species/genus
Family
Habitat
Reference
Alaninema
Aphrophridae
Intestinal parasites in slugs
Ivanova et al. (2013)
Amblydorylamus
Dorylaimidae
Nematode from Antarctica
Elshishka et al. (2015)
Brugia-B. malayi
Filariidae
Present only in Southeast Asia
Triteeraprapab et al. (2001)
Bursaphelenchus
Parasitaphelenchidae
Obligate mycrophages
Ryss et al. (2005)
Cooperia
Cooperiidae
Intestinal parasites in cattle
Dorny et al. (1997)
Cylicostephanus-C. goldi
Strongylidae
Intestinal parasites of horses
Bucknell et al. (1995)
Deladnus
Neotylenchidae
Parasitic nematodes
Bedding (2009)
Deladenus siricidicola
Neotylenchidae
Biological control agent of woodwasp
Bedding (2009)
Dicelis
Drilonematoidea
Parasitic earthworm
Spiridonov (1992)
Drasico nemoralis
Endemic earthworm from far East Russia
Ivanova et al. (2014)
Enerobius
Oxyuridae
Intestinal parasite in humans
Brown (2006)
Epsilonema
Epsilonematidae
Marine species
Gourbault and Decraemer (1994)
Eubosrichus
Desmodoridae
Marine species
Polz et al. (1999)
Gongylongema
Gongylonematidae
Bird and mammal parasites
Soulsby (1982)
Greeffiella
Desmoscolecoidea
Free-living marine nematode
Abolafia and Pena-Santiago (2016)
Haemonchus
Trichostronylidae
Pathogenic nematodes of ruminants
Fleming et al. (2006)
Halalaimus
Oxystominidae
Marine species
Turpeenniemi (1998)
Halomonhystera
Monhysteridae
Marine species
Tchesunov et al. (2015)
Table 4 Family and habitat of these species of soil free-living nematodes in this study
Fig. 3 Relative abundance of genera of soil free-living nematodes using 18S rDNA sequences and BLAST similarity analysis at three sites and locations
Fig. 4 Venn diagram showing similarity and dissimilarity of soil free-living nematodes at each locations and possible relationship in plant gender. Number of 0-4 means groups of soil free-living nematodes at the phylum level.
Type
Variable
Initial conditional effect
MCR (%)
F
P
Sampling site
OM
0.09
9
2.78
0.034*
WHC
0.08
8
2.23
0.086
Cond
0.08
8
2.23
0.078
pH
0.07
7
2.20
0.114
SM
0.01
1
0.35
0.824
Total
33
Plant gender
OM
0.09
9
2.78
0.028*
WHC
0.08
8
2.23
0.092
Cond
0.08
8
2.23
0.092
pH
0.07
7
2.20
0.104
SM
0.01
1
0.35
0.770
Total
33
Table 5 Redundancy analysis (RDA) of environmental variables based on sampling site and plant gender
Fig. 5 Redundancy analysis (RDA) elucidating effects of sampling sites (D, Delta; E, Far East sand dunes; G, Gobabeb) on soil free-living nematodes. The number 1-23 means the replicates for sampling sites.
Fig. 6 Redundancy analysis (RDA) elucidating effects of plant gender and control (F, female; M, male; C, control) on soil free-living nematodes. The number 1-23 means the replicates for plant gender and control.
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