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. 2018 Jun 3;50(2):183–206. doi: 10.21307/jofnem-2018-010

Description and Distribution of Three Criconematid Nematodes from Hangzhou, Zhejiang Province, China

Maria Munawar 1, Thomas O Powers 2, Zhongling Tian 1, Timothy Harris 2, Rebecca Higgins 2, Jingwu Zheng 1,3,*
PMCID: PMC6909330  PMID: 30451437

Abstract

Populations of Criconemoides parvus, Discocriconemella hengsungica, and Discocriconemella limitanea, isolated in Hangzhou, China from the rhizosphere soil of woody perennials were characterized morphologically and molecularly. The morphometric data of the Chinese populations were compared with populations from other regions of the world. DNA barcoding with the mitochondrial COI gene confirmed conspecificity of Chinese and Costa Rican populations of D. limitanea. Phylogenetic assessment using a near full-length 18S ribosomal DNA sequence provided weak support for a grouping of Criconemoides parvus from China and C. annulatus from western North America. The phylogenetic position of D. hengsungica from China and an unknown species of Discocriconemella from Thailand relative to D. limitanea suggests that the genus Discocriconemella is not monophyletic. The study provides the first record of D. hengsungica in China and confirms the presence of C. parvus previously reported from China. Biogeographic implications of these nematode distributions are discussed.

Keywords: Criconemoides parvus, Discocriconemella hengsungica, D. limitanea, DNA barcoding, Nematode morphology, Phylogeny, Scanning electron microscopy

Species of genera Criconemoides (Taylor, 1936) and Discocriconemella (De Grisse & Loof, 1965) have global distributions (Geraert, 2010, Eskandari et al., 2010) and are known to be associated with agricultural crops, grasslands and woody perennials (Siddiqi, 2000). At present, the genus Criconemoides contains 42 valid species (Geraert, 2010) with only three species (C. informis (Micoletzky, 1922) Taylor, 1936; C. parvus Raski, 1952, and C. zavadskii (Taulaganov, 1941) Raski, 1958) reported from China. Discocriconemella, after the transfer of D. inarata Hoffman, 1974 to Mesocriconema (Powers et al., 2010; 2014) contains 27 valid species. Only D. limitanea (Luc, 1959) De Grisse and Loof, 1965 was formerly known to be reported from China (Yin et al., 1994; Ye et al., 1997; Zhang et al., 1997; Li et al., 2006).

During a routine nematological survey of Hangzhou city, Zhejiang province, China, large populations of three criconematids were recovered from the rhizosphere of woody perennials. Morphological studies revealed the identity of these nematodes as C. parvus, D. hengsungica (Choi & Geraert, 1975) and D. limitanea. Previously, C. parvus was reported from Shandong (Liu et al., 2004) and Liaoning provinces (Tan and Ye, 2009) in Pisum sativum and Pinus sp. rhizosphere, respectively. However, no morphological descriptions or photo documentations were presented in the Chinese literature to confirm the actual identity of C. parvus. Similarly, D. limitanea was reported from Guangzhou (Yin et al., 1994), Guangdong (Ye et al., 1997), Fujian (Zhang et al., 1997) and Yunan (Li et al., 2006) provinces, in the rhizosphere of fruits and Rosaceae plants. Most of the descriptions are in Chinese and without photo documentation or molecular data.

Discocriconemella hengsungica was originally described from Korea, and is the only record of its occurrence (Choi and Geraert, 1975), but there is no molecular information available for this species.

Thus, the objectives of the study were to: (1) establish the identity of these three species by morphological and molecular characterization, (2) integrate the morphometric characterization of Chinese populations of D. limitanea and C. parvus with measurements reported from different countries, (3) evaluate the phylogenetic and biogeographic relationships of these species within Criconematidae using 18S and COI DNA sequence.

Materials and methods

Nematode detection and morphological observations: Soil samples were collected from undisturbed natural locations in the Hangzhou Botanical Garden. Nematodes were extracted from soil using a modified Cobb sieving and flotation–centrifugation method (Jenkins, 1964). Nematodes were killed and fixed in hot 4% formaldehyde, infiltrated with glycerin following the method of Seinhorst (1959), and mounted on slides for observation and preservation. The measurements and light micrographs of nematodes were accomplished using an ocular micrometer and a Zeiss Stemi 2000-C compound microscope.

Nematodes were also examined using a Hitachi TM-1000 scanning electron microscope (SEM). For the SEM examination, the nematodes were fixed in a mixture of 2.5% paraformaldehyde and 2.5% glutaraldehyde, washed three times in 0.1 M cocodylate buffer, post-fixed in 1% osmium tetroxide, dehydrated in a series of ethanol solutions and critical point-dried with CO2. After mounting on stubs, the samples were coated with gold. Specimens from Costa Rica were processed for SEM using the methods described in Powers et al. (2010).

Molecular analyses

DNA samples from China were prepared according to Zheng et al. (2003). Individual nematodes were transferred into an Eppendorf tube containing 16 µL ddH2O. Two microliters PCR buffer solution was added to each tube. Nematodes were crushed using a sterilized pipette tip, briefly spun and immediately frozen at −68oC for at least 30 min. The tubes were heated to 85oC for 2 min, briefly spun, followed by the addition of 2 µL proteinase K. The tubes were incubated at 56oC for 1 to 2 hrs, followed by 10 min at 95oC. After incubation, these tubes were cooled at 4oC and used for PCR (Zheng et al., 2003). Several sets of primers (synthesized by Invitrogen, Shanghai, China) were used in the PCR analyses to amplify the near full-length18S region of rDNA and COI region. Two sets of primers: the forward 18S39F (5′-AAA GAT TAA GCC ATG CAT G-3′) and the reverse 18S977R (5′-TTT ACG GTT AGA ACT AGG GCG G-3′), the forward 18S900F (5′-AAG ACG GAC TAC AGC GAA AG-3′) and the reverse 18S1713R (5′-TCA CCT ACA GCT ACC TTG TTA CG-3′) for amplification of the nearly full-length 18S rRNA (Olson et al., 2017). For the amplification of COI the primers used were COI-F5-(5′-AATWTWGGTGTTGGAACTTCTTGAAC-3′) and COI-R9-(5′ CTTAAAACATAATGRAAATGWGCWACWACATAATAAGTATC-3) (Powers et al., 2014). The 25-µl PCR was performed using 2x-TsingKe Master Mix DNA polymerase (Beijing TsingKe Biotech Co., Ltd) according to the manufacturer’s protocol in a BIOER-XP thermocycler. The thermal cycler program for 18S and COI was as follows: denaturation at 95°C for 5 min, followed by 40 cycles (18S) or 50 cycles (COI) of denaturation at 94°C for 30 s, annealing at 50°C (18S) or 48°C (COI) for 30 s, and extension at 72°C for 90 s. A final extension was performed at 72°C for 5 min as described by Powers et al. (2014) and Olson et al. (2017). PCR products were separated and visualized on 1% agarose gels and stained with ethidium bromide. PCR products of sufficiently high quality were sent for sequencing by Invitrogen (Shanghai, China).

Phylogenetic analysis

Phylogenetic trees were constructed by maximum likelihood (ML) in MEGA version 6. Sequences were edited using CodonCode Aligner version 4.2 (http://www.codoncode.com/) and aligned using Muscle within MEGA version 6 (Tamura et al., 2013). Gap opening penalty was set at −400 with a gap extension penalty of 0. The general time reversible model with Gamma-distributed rates plus invariant sites (GTR+G+I) was determined to be the best substitution model by Bayesian Information Criterion using the Best Fit Substitution Model tool in MEGA 6.0. The ML trees used the all sites option for gaps and 200 bootstrap replications to assess clade support. The 18S tree used all the taxa previously presented in Powers et al. (2017) plus the eight new sequences from China. The COI tree includes the same taxa as the 18S tree, adding 79 new COI sequences to GenBank, plus 11 new sequences from China. GenBank accession numbers and associated metadata are presented in supplementary Table 1.

Table 1.

Morphometric data and distribution of Criconemoides parvus. All measurements in µm.

Authors This study Raski (1952) a Loof (1991) Eskandari et al. (2010) Mirghasemi et al. (2014) Rashid et al. (1986) Popovivi and Ciobanu (2000) Liskova et al. (2004)
Origin Chinese population Berkeley, California, USA Iran Iran Iran Brazil Romania Slovak Republic
Host Pomegranate Artemesia sp. Populus sp. - Tea Theobroma cacao - Robinia pseudoacacia
n 15 - 33 23 8 29 1 1
L 270.4-324.5 259-295 240-330 252-313 260-346 210-270 299 280
a 12.8-15.0 11.7-14.5 16-Oct 8.8-13.5 11.3-14.4 12-Aug 12.4 11.6
b 3.7-4.2 3.0-3.4 3.2-4.2 3.2-4.1 3.1-4 3.0-3.6 3.9 3.3
c 20.7-32.1 - 21-55 21.7-45.4 47.9-65 18-47 33.2 23.3
V 93.6-95.6 92.5-95.9 94-97 93.6-96.7 95.9-96.5 91-94 95 94.3
VL/VB 0.7-1.2 - 0.6-0.9 0.6-0.9 0.7-0.80 0.4-1.1 0.7 0.7
Stylet 26.5-30.3 38-41 26-32 30-43 30.2-36.1 34.5-43 35 41
Stylet %L 8.7-10.6 - 11-Sep 10.4-15.9 - 14-18 12 14.6
R 140.0-168 142-156 142-172 144-167 148-160 124-141 173 178
Rex 43.0-48 46-49 41-53 45-53 - 39-52 50 -
RV 9.0-13.0 11-12 8-12 9-13 8-10 8-11 12 16
RVan 2.0-3 - 0-4 0-2 3-5 1-3 2 6
Ran 6.0-10 - 6-11 7-11 5-7 6-9 9 10
Tail length 9.1-15.6 - - 6-14 - 6-11 - -
Male Unknown Unknown - - - Known - -
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aOriginal description.

Results

Systematics

Criconemoides parvus (Raski, 1952) (Figs. 1, 2; Table 1)

Figure 1.

Figure 1

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Light photomicrographs of Criconemoides parvus: A: entire female; B, C: head region; D: mid-body (arrows showing anastomosis); E, F: pharyngeal region (arrows showing position of the excretory pore); G, posterior region showing the reproductive system; H: posterior region showing crenation on annuli; I-K: female tail (arrows showing position of vulva and anus; scale bars = A =50 µm, all others 10 µm).

Figure 2.

Figure 2

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Scanning electron microscopy of Criconemoides parvus: A-C: lip region; D: mid-body showing crenations; E-H: posterior region of the female showing vulva and anus (arrows showing position of anus; scale bars = A, B = 5 µm; C, F, G, H = 10 µm; D= 20 µm).

Description

Female: Body cylindrical, ventrally arcuate after heat relaxation. The cephalic region is flat, continuous with the body contour. En face view, an oral disc with slightly elevated lateral pseudolips, oral aperture slit-like, with submedian lobes absent. Surrounding and apparently fused with the oral disc is a single labial annulus with dorsal and ventral indentations. Body annuli retrorse with posterior margins finely crenate, more prominent on the posterior body, anastomoses common in the middle of the body. Stylet is short with rounded basal knobs, DGO indistinct, and oesophagus criconematoid. Excretory pore at the base of the oesophageal bulb. Gonad monodelphic, outstretched, spermatheca oblong, filled with rod-shaped sperm, vagina straight, vulva closed, anterior and posterior annuli around the vulva larger than the preceding body annuli; discontinuous annuli are more common near the region of the vulva. Tail conoid ending in a rounded terminus and the anus is indistinct.

Male: Not found.

Locality and habitat: The population was found in the rhizosphere of Punica granatum L. from Xixi wetland, Hangzhou, Zhejiang Province, China on May 5, 2017. The geographical location of the sampling site is 30°16'23″N; 120°3'33″E.

Differential diagnosis: Males were not described in the original description by Raski (1952). The type locality was near Winnemucca, Nevada in the mountains of western North America around the roots of Artemisia sp. Subsequent reports mention females with spermatheca filled with sperm but it was not until 34 years later that Rashid et al., (1986) described a male from an earlier Netherlands collection that included males, but did not describe them (De Grisse and Loof, 1965). Another character not mentioned in the original description is the presence of anastomoses. An Iranian population reported by Loof & Barooti (1991) and a Romanian population by Liskova et al. (2004) described anastomoses as either absent or occasional. Specimens of the Chinese population had numerous anastomoses. Most other morphological characters of the Chinese populations match the original description.

Morphometrically, the three Iranian populations described by Loof and Barooti, (1991) have bodies that are slightly longer than the original description (240-346 µm vs. 259-295 µm) and stylets that are shorter (26-32 µm vs. 38-41 µm). A Brazilian population reported by Rashid et al. (1986) had fewer body annuli (R = 124-141 vs. 142-156) as compared with the original description. Two New Zealand populations reported by Loof et al. (1997) and Wouts (2006) recorded slightly longer stylets (42-46 µm vs. 44-49 µm vs. 38-41 µm, respectively) and relatively fewer body annuli (R = 126-169 vs. 128-147 vs. 142-156, respectively) as compared with the original description. The Romanian and Slovak Republic populations reported by Popovici and Ciobanu (2000) and Liskova et al. (2004) correspond well to the original description except for a higher number of body annuli (R = 173 vs. 178 vs 142-156, respectively). When compared with the original description, the Chinese population has a slightly longer body (270-324.5 µm vs. 259-295 µm) and a shorter stylet (26.5-30.3 µm vs. 38-41 µm).

Discocriconemella hengsungica (Choi and Geraert, 1975) (Figs. 3, 4; Table 2)

Figure 3.

Figure 3

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Light photomicrographs of Discocriconemella hengsungica: A: entire female; B: mid-body (arrow showing annuli without anastomosis); C-D: head region (arrows showing flexible stylet and basal knobs); E: pharyngeal region (arrow showing position of the excretory pore); F, posterior region showing the reproductive system (arrows showing reflexed ovary, spermatheca, position of vulva and anus); G: female tail ; scale bars = A =50 µm, all others 10 µm).

Figure 4.

Figure 4

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Scanning electron microscopy of Discocriconemella hengsungica: A: entire female; B-D: labial disc in different angles; E: mid-body annuli without anastomosis; F: posterior region of the female showing vulva and anus (arrows showing the position of anus; scale bars = A =50 µm; B-D= 10 µm; E, F=20 µm).

Table 2.

Morphometric data of Discocriconemella hengsungica. All measurements in µm.

Authors This study Choi & Geraert, 1975 a
Origin China Korea
Host Castanopsis sclerophylla Zea mays
n 15 females 5 females
L 333.1±19.0(307.9-382.6) 285-315
a 9.4±1.0(8.2-11.5) 8.2-9.8
b 2.5±0.1(2.3-2.8) 2.5-2.6
c 19.6±3.0(15.2-25.7) -
c' 0.7±0.1(0.5-0.8) -
V 89.2±0.8(87.8-90.4) 87-90
VL/VB 1.1±0.1(1.0-1.3) -
Stylet 107.4±3.4(100.3-113.5) 104-108
Stylet % L 32.3±1.7(28.6-34.6) -
R 91.3±2.2(88.0-94.0) 82-90
Rex 33.5±1.6(30.0-36.0) 31
RV 9.8±0.4(9.0-10.0) 13-14
RVan 5.2±0.8(4.0-6.0) 7
Ran 4.7±0.7(4.0-6.0) 7
Lip height 5.0±0.5(4.0-5.7) -
Pharynx 131.5±3.3(126.4-137.5) 121
Max. body diam. 35.7±2.7(30.1-39.3) 28
Vulva body diam. 31.9±1.9(28.0-34.4) -
Dis. from vulva to tail term. 35.9±3.2(31.3-43.3) -
Anal body diam. 26.5±2.1(22.5-29.4) -
Tail length 17.4±2.8(12.0-21.8) 13
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Note: aOriginal Description.

Description

Female: Body cylindrical, ventrally curved after heat relaxation. Labial region a disc-like appearance in profile. En face view, does not show a discrete oral disc, instead the stylet appears to be located centrally in an inner rectangular area surrounded by a continuous, broad labial annulus with deep ventral and dorsal indentations forming two pairs of dorsal and ventral lobes combined with distinct lateral bulges. The oral disc and amphid apertures are indistinct due to amphidal excretions in SEM images. The labial annulus is separated from the body annulus by a high neck or collar. Body annuli retrorse to angular, without anastomosis or interruptions. Stylet long and flexible with anchor-shaped knobs, DGO indistinct; oesophagus criconematoid. Excretory pore located near the middle of the oesophageal bulb. Gonad monodelphic, outstretched, some individuals with reflexed ovary, spermatheca rounded filled with spherical sperm, vagina straight, and vulva closed. Tail conoid broadly rounded, and terminal annuli displaced dorsally and the anus is indistinct.

Male: Not found.

Locality and habitat: The population was found in the rhizosphere of Castanopsis sclerophylla (Lindl.) Schott from a Botanical garden in Hangzhou, Zhejiang Province, China on March 28, 2017. The geographical location of the sampling site is ″30°15'17″N; 120°07'01″E.

Differential diagnosis: In the original description of D. hengsungica six specimens were studied. Only one female was observed with a few anastomoses. No anastomoses were observed on the Chinese specimens. The spermatheca was described as filled with sperm but no males were found. Similarly, the Chinese population had specimens with sperm-filled spermatheca, but no males were found. The original description lacks information on the morphology of the labial disc, position of excretory pore and anus, shape of vagina and vulva. Morphology of the Chinese population fits well with the characters included in the original description except for the complete absence of anastomoses. Morphometrically, the Chinese population is slightly longer (307-382 µm vs. 285-315 µm) with relatively longer stylets (100.3-113.5 µm vs. 104-108 µm) and less annuli from vulva to tail terminus (RV = 9-10 vs. 13-14). The slight morphometric differences could be attributed to fewer specimens studied in the original description and geographical variability.

Discocriconemella limitanea (Figs. 5–8; Tables 3–4)

Figure 5.

Figure 5

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Light photomicrographs of Discocriconemella limitanea: A: entire female; B: mid-body (arrow showing anastomosis); C-E: pharyngeal region (arrow showing position of the excretory pore); F: posterior region showing the reproductive system; G-I, female tail (arrows showing position of vulva and anus; scale bars = A =50 µm, all others 10 µm).

Figure 8.

Figure 8

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Scanning electron microscopy of Discocriconemella limitanea female from La Selva and Las Cruces, Costa Rica: A,B) entire female; C-H) head profiles in different angles; I-K) female posterior region showing vulva and anus.

Table 3.

Morphometric data and distribution of Discocriconemella limitanea. All measurements in µm.

Authors This study Luc (1959) a Coomans (1966) Luc (1970) Sauer and Winoto (1975) Rashid et al. (1986) Van den Berg and Cadet (1992) Rahaman and Ahmed (1994) Talavera and Hunt, 1997 Crozzoli and Lamberti (2003) Syn. (D. repleta) Pinochet and Raski 1976 Syn. (D. repleta) Loof and Sharma (1980) Syn. (D. repleta) Vovlas et al. (1990)
origin China Costa Rica French Guinea Congo Ivory Cost Malaysia Brazil South Africa India Eucador Venezuela Brazil Brazil Peru
Host Magnolia grandiflora Forest soil Cinchona succirubra - Coffea sp. Forest Soil Theobroma cacao Forest Soil Bambusa sp. Forest Soil Forest Soil Theobroma cacao - Forest Soil
n 15 5 3 8 20 11 36 11 20 18 - 10 - 8
L 223.9- 270.1 225-270 207-228 260-280 180- 250 200-250 190-280 220-260 180-240 190-270 191-202 250-290 187-271 219-245
a 5.9-7.5 6.8-8.7 5.8-7.6 8-11 7-8 5-8 7.5-9.5 5.9-7.4 6.2-6.7 7.6-12 5.6-6.4 7-8 6.8-8.8 8.3-9.5
b 2.6-3.2 1.9-3.3 2.5-2.6 2.8-2.9 2.5-3 2.7-3.2 2.6-3.2 2.4-2.6 2.5-2.7 2.7-3.5 2.5-2.8 2.6-3.1 - 2.8-3.1
c 15.7-24.7 - 16 17-25 - 20-33 20.4-46 17.8-22.3 14-21 15.5-20.5 15-20 20-26 - 27-39
V 90.2-92.5 89-93 87-89 88-92 84-90 90-93 89-94 88-91 87-91 89.1-94.3 88-90 92-95 - 92-93
VL/VB 0.8-1.2 - - - - 0.6-1.1 - 0.87-1.1 0.8-1.4 - - 0.8-0.9
Stylet 53.1-59.6 45-57 52-53 53-55 38-50 45-53 43-52 52.5-59.2 48-51 35-51 48-54 59-66 43-56 44-47
Stylet %L 20.2-25.3 18-25.3 - - - - 17-23 22.3-25.2 23.5-26.6 16.6-19.7 - - - 18-20
R 96.0-114 98-121 90-110 102-110 84-113 95-120 99-111 107-113 104-120 103-138 96-110 117-116 98-118 107-114
Rex 33.0-37 33-41 34 32-36 - 35-38 34-44 28-33 34-39 37-47 - 37-42 - 30-34
RV 11.0-13.0 10-11 11-12 12-15 - 11-15 8-14 12-15 14-16 9-12 12-14 10-11 9-13 11-13
RVan 4.0-5.0 - 4 4-6 - 4-5 2-7 5-7 6-7 2-3 4-5 3-4 0-4
Ran 6.0-8.0 - 7 7-9 - 6-9 5-10 5-8 7-9 6-8 7-8 7-8 6-10 5-7
Tail 9.8-16.4 - - - - - 4.5-13 10.3-14 - 10.5-16.5 - - - 5.6-8.9
Male Unknown Known - - - Known - - Unknown - - Known - -
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aOriginal description.

Table 4.

Morphometric data and distribution of Discocriconemella limitanea in Chinese provinces. All measurements in µm.

Authors This study Yin et al. (1994) Ye et al. (1997) Zhang et al. (1997) Zhang et al. (1997) Li et al. (2006)
Origin (Province, City) Zhejiang Hangzhou Guangzhou Guangdong Fujian, Xiamen Fujian, Zhang pu Yunan, Kunming
Host Magnolia grandiflora Lychee — Fruit trees Fruit trees Rosaceae plants
n 15 6 6 20 19 -
L 223.9-270.1 225-260 217-280 180-230 210-260 183-257
a 5.9-7.5 — 6.2-8.2 5.6-8.2 7-12 —
b 2.6-3.2 — 2.3-3.4 2.3-3.3 206-301 —
c 15.7-24.7 — 16.2-28.6 11-15 16-20
V 90.2-92.5 89-91 89-91 90-93 87-91 —
VL/VB 0.8-1.2 — 094-1.06 — — —
Stylet 53.1-59.6 51-53 46-56 51-57 45-50 —
Stylet % L 20.2-25.3 — — — —
R 96.0-114 110-122 90-98 92-104 94-110 96-103
Rex 33.0-37 — 30-34 30-37 30-36 34-37
RV 11.0-13.0 10-12 11-13 8-10 10-13 12-14
RVan 4.0-5.0 — 4-8 1-2 4-5 —
Ran 6.0-8.0 — 5-8 5-8 6-9 —
Tail 9.8-16.4 — — — — —
Male Unknown — — — Known —
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Figure 7.

Figure 7

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Scanning electron microscopy of Discocriconemella limitanea: A) entire female; B-E: oral disc in different angles; F-H: posterior region of the female showing vulva and anus (arrows showing position of the anus; scale bars = A =50 µm; B-G = 10 µm; H = 20 µm).

Description

Female: Body stout, ventrally arcuate after heat relaxation, lip region with disc-like appearance. En face view, a labial annulus with deep dorsal and ventral indentations, the oral opening appearing as a slit on a rounded oral disc flanked by two lateral amphidial apertures. The lateral edges of the labial annulus straight, lacking a central bulge. Body annuli retrorse, finely crenate edges, frequent anastomoses or discontinuous annuli that demarcate lateral lines. Stylet robust, anchor-shaped knobs, DGO indistinct. Oesophagus criconematoid. Excretory pore at the base of the oesophageal bulb. Gonad monodelphic, prodelphic, outstretched, spermatheca oblong rounded, filled with spherical sperm, vagina straight, vulva closed. Ventral post-vulval region straight, narrowing immediately posterior to the vulva, elongate-conoid. The terminal annulus is simple or lobed. Anus indistinct in light microscopy.

Male: Not found in Chinese population.

Locality and habitat: The population was found in the rhizosphere of Magnolia grandiflora Linn from a Botanical garden, Hangzhou, Zhejiang Province, China on April 13, 2017. The geographical position of the sampling site is ″30°15'09″N; 120°07'01″E.

Differential diagnosis: In the original description males were not described; however, most populations of D. limitanea are reported to have spermatheca filled with sperm. Several reports include the description of a male. Powers et al. (2011) listed a single male (GB #FJ489535) still within the cuticle of the previous molt (Fig. 6C). The specimen had a body length of 258 µm, spicule of 19 µm, and gubernaculum of 5 µm. In the female, the relatively abrupt constriction of the post-vulval body was not described or illustrated in the original description, but the populations from Malaysia (Sauer and Winoto, 1975), Brazil (Rashid et al., 1986), India (Rahaman and Ahmed, 1994) and Ecuador (Talavera and Hunt, 1997) reported the narrowing of the post-vulval body profile. The South African population (Van den berg and Cadet, 1992) was reported to have distinct tooth-like projections on the margins of the ventral body annuli. The Brazilian population (Loof and Sharma, 1980) was reported to have a conspicuous break between the fourth and fifth annuli.

Figure 6.

Figure 6

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Light photomicrographs of Discocriconemella limitanea from La Selva, Costa Rica; A) entire female, PNID-184030; B) entire female, PNID-184026; C) entire male PNID-151041; D) female tail, PNID-184031; E) female anterior, PNID-184031.

Morphometrically, the Congo population (Coomans, 1966) is slightly longer than the original description (260-280 µm vs. 207-228 µm. The Ivory Coast population (Luc, 1970) was reported to have the shortest body length (180 µm) and smallest stylet (38 µm) in the population compared with the original description. The Malaysian and Ecuadorean populations were reported to have larger V values (90-93 vs. 89.1-94.3 vs. 87-89, respectively) and smaller stylets (45-53 µm vs. 35-51 µm vs. 52-53 µm, respectively) in relation to the original description. The two Brazilian populations reported by Loof and Sharma (1980) and Rashid et al. (1986) are a mixture of small and large specimens. These two populations also differ from each other morphometrically; the notable difference of these two populations from the original description is the variable body length (167-306 µm vs. 190-280 µm vs. 207-228 µm, respectively) and stylet lengths (50-77 µm vs. 43-52 µm vs. 52-53 µm respectively). The South African, Indian and Venezuelan populations are morphologically close to the original description, except that the South African population has a longer body length (260-280 µm vs. 207-228 µm) while the body length of the Venezuelan population is shorter (191-280 µm vs. 207-228 µm), and the Indian population was reported to have smaller stylets (48-51 µm vs. 52-53 µm). The Chinese population in this study matches well with the original description except for a slightly longer body length (220-260 µm vs. 207-228 µm) and longer stylet length (53-60 µm vs. 52-53 µm). Overall, the morphometrics are within the range of variation of the species according to the populations described by various authors.

Five additional populations of D. limitanea from China have been reported from Guangzhou, Guangdong, Fujian and Yunan provinces. Nematodes from all of these populations have overlapping morphometric ranges, fit well within with the original description and Confirm to the species as described by multiple authors (Luc, 1970; Rashid et al., 1986; Rahaman and Ahmed, 1994; Talavera and Hunt, 1997).

Molecular profiles and phylogenetic status

Several key systematic features of criconematid nematodes are revealed by the 18S and COI phylogenetic trees. First, in the 18S tree (Fig. 9) which provides better resolution at the deeper nodes in the tree, there is strong bootstrap support (99%) for a clade that combines Discocriconemella limitanea from China with conspecific specimens from Costa Rica. This clade confirms the species identification and provides evidence of an amphi-Pacific disjunction, the first molecular data from a nematode to support this distribution pattern. Studies of many plant species suggest this is one of several intercontinental distribution patterns that link Asia and North America (Li and Wen, 2013; 2014; Fritsch et al., 2015). COI (Fig. 10) also supports this grouping at a lower support value (82%). Similarly, Criconemoides parvus groups with C. annulatus Cobb in Taylor, 1936 from western U.S. in the 18S tree, albeit at a relatively low support value (58%). There are no molecular data of C. parvus from North America, although the type locality is in the western state of Nevada. The placement of Discocriconemella hengsungica and an unknown Discocriconemella specimen from Thailand, in both 18S and COI trees, provides strong evidence that the genus Discocriconemella is not a monophyletic group. Discocriconemella hengsungica is a member of a larger criconematid clade that predominantly includes nematodes that possess scales or projections on the cuticle in at least one life stage. Xenocriconemella (De Grisse and Loof, 1965) is also a member of this group which adds evidence that cuticle projections are not reliable taxonomic characters in establishing the genera (Powers et al., 2017).

Figure 9.

Figure 9

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Maximum likelihood tree of 232 18 S criconematid sequences. Substitution model GTR+G+I and 200 bootstrap replications. Each specimen is identified by a Nematode Identification number or GenBank Accession number (for taxa not sequenced by the authors), species name, and location as supplied by the author. Brackets are provided to indicate genera or specific species. Bootstrap values over 50 are applied by nodes in red. Specimens from China are highlighted in yellow.

Figure 10.

Figure 10

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Maximum likelihood COI tree of 175 criconematid sequences. Substitution model GTR+G+I and 200 bootstrap replications. Each specimen is identified by a Nematode Identification number, species name and location. Bootstrap values of more than 50 are applied by nodes in red. Specimens from China are highlighted in yellow.

Overall, the addition of these species from China to a reference dataset of criconematid nematodes provides insight into the biogeography of nematodes in general. It is likely that additional collections of plant parasitic nematodes from Asia will also contribute to fundamental questions of angiosperm biogeography (Raven and Axelrod, 1974; Fritsch et al., 2015; Wen et al., 2016).

Table AI.

Table of location data and GenBank accession numbers for specimens appearing on the COI maximum likelihood tree, in tree order.

NID Species Stage Locality** Ecoregion GenBank Accession #
1057 Mesocriconema sp. J Spring Creek Prairie, NE Central Tall Grasslands KJ788024
1129 Mesocriconema sp. F Avoca Prairie and Savanna State Natural Area, WI Upper Midwest Forest-Savanna Transition Zone KJ788031
2973 Mesocriconema sp. F Red Rock Prairie Preserve, MN Central Tall Grasslands KY574752
1054 Mesocriconema sp. F Spring Creek Prairie, NE Central Tall Grasslands KJ788021
1388 Mesocriconema sp. F Nine-Mile Prairie, NE Central Tall Grasslands KJ788053
1051 Mesocriconema sp. F Stafford County, KS Central and Southern Mixed Grasslands KJ788019
5515 Mesocriconema sp. F Downs Prairie Natural Area, AR Mississippi Lowland Forests KY574764
5501 Mesocriconema sp. J Clymer Meadows, TX Texas Blackland Prairies KY574813
956 Mesocriconema sp. F Schluckebier Prairie State Natural Area, WI Upper Midwest Forest-Savanna Transition Zone KJ788015
5502 Mesocriconema sp. F Roth Prairie Natural Area, AR Mississippi Lowland Forests KY574731
1300 Mesocriconema sp. F Lowndes County, MS Southeastern Mixed Forests KJ787926
5540 Mesocriconema sp. J Chihuahuan Desert Research Institute, TX Chihuahan Desert MF770954
3660 Mesocriconema sp. F Lance Rosier Unit, BITH, TX Piney Woods Forests KY574795
3086 Mesocriconema nebraskense F Hayden Prairie Preserve, IA Central Tall Grasslands KY574679
5506 Mesocriconema nebraskense J Roth Prairie Natural Area, AR Mississippi Lowland Forests KY574695
5505 Mesocriconema sp. F Roth Prairie Natural Area, AR Mississippi Lowland Forests KY574724
5527 Mesocriconema sp. F Warren Prairie Natural Area, AR Piney Woods Forests KY574807
1346 Mesocriconema xenoplax F Great Falls Park, GWMP, VA Southeastern Mixed Forests KY574831
1375 Mesocriconema xenoplax F Nine-Mile Prairie, NE Central Tall Grasslands KJ787916
2557 Mesocriconema xenoplax F Autauga County, AL Southeastern Mixed Forests KY574633
3320 Mesocriconema xenoplax J Twin Creeks, GRSM, TN Appalachian-Blue Ridge Forests KY574832
728 Mesocriconema xenoplax F Pickens County, SC Southeastern Mixed Forests KJ787873
5587 Mesocriconema xenoplax F Tuskegee National Forest, AL Southeastern Mixed Forests KY574626
5603 Mesocriconema xenoplax J Big Sandy Creek Unit, BITH, TX Piney Woods Forests MF770959
2694 Mesocriconema xenoplax F Albright Grove, GRSM, TN Appalachian-Blue Ridge Forests MF770909
3078 Mesocriconema xenoplax F Gifford Woods State Park, VT New England Acadian Forests KY574639
3491 Mesocriconema xenoplax F West Point, GRSM, TN Appalachian-Blue Ridge Forests MF770951
1135 Mesocriconema inaratum F Nine-Mile Prairie, NE Central Tall Grasslands KJ787935
7003 Mesocriconema inaratum F Prairie Pines, NE Central Tall Grasslands MF770967
2919 Mesocriconema inaratum F Aurora Prairie Preserve, SD Central Tall Grasslands KY574657
2920 Mesocriconema inaratum J Aurora Prairie Preserve, SD Central Tall Grasslands MF770921
3187 Mesocriconema sp. F Roth Prairie Natural Area, AR Mississippi Lowland Forests KY574833
570 Mesocriconema sp. J Jonathan Dickinson State Park, FL Florida Sand Pine Scrub KJ788061
3280 Mesocriconema sp. F Apalachicola Bluffs and Ravines Preserve, FL Southeastern Conifer Forests KY574834
3646 Mesocriconema sp. F Neches Bottom and Jack Gore Unit, BITH, TX Piney Woods Forests KY574817
2905 Mesocriconema sp. F Barta Brothers Ranch, NE Nebraska Sandhills Mixed Grasslands KY574825
3175 Mesocriconema sp. F Kellogg-Weaver Dunes SNA, MN Central Tall Grasslands KY574826
443 Mesocriconema discus J Brookings County, SD Central Tall Grasslands KJ787868
2627 Mesocriconema ericaceum F Brushy Mtn., GRSM, TN Appalachian-Blue Ridge Forests KX290522
5976 Mesocriconema ericaceum J Brushy Mtn., GRSM, TN Appalachian-Blue Ridge Forests KX290542
5990 Mesocriconema ericaceum F Brushy Mtn., GRSM, TN Appalachian-Blue Ridge Forests KX290548
2900 Mesocriconema sp. F Barta Brothers Ranch, NE Nebraska Sandhills Mixed Grasslands MF770919
2902 Mesocriconema sp. F Barta Brothers Ranch, NE Nebraska Sandhills Mixed Grasslands MF770920
3966 Mesocriconema sp. F Turkey Creek Unit, BITH, TX Piney Woods Forests MF770953
3085 Mesocriconema rusticum F Hayden Prairie Preserve, IA Central Tall Grasslands MF770940
5572 Mesocriconema rusticum F Akershus County, Norway Scandinavian and Russian Taiga KY574621
3050 Mesocriconema rusticum F Hayden Prairie Preserve, IA Central Tall Grasslands MF770936
3059 Mesocriconema sp. J Hayden Prairie Preserve, IA Central Tall Grasslands MF770937
362 Mesocriconema curvatum F Treasure Co, MT Northern Short Grasslands KJ787847
3172 Mesocriconema sp. J Kellogg-Weaver Dunes SNA, MN Central Tall Grasslands MF770942
3174 Mesocriconema sp. F Kellogg-Weaver Dunes SNA, MN Central Tall Grasslands MF770943
3169 Mesocriconema sp. F Kellogg-Weaver Dunes SNA, MN Central Tall Grasslands KY574821
3431 Mesocriconema sp. F Oaky Woods Wildlife Management Area, GA Southeastern Mixed Forests KY574822
3457 Mesocriconema sp. F Oaky Woods Wildlife Management Area, GA Southeastern Mixed Forests KY574823
3460 Mesocriconema sp. F Oaky Woods Wildlife Management Area, GA Southeastern Mixed Forests MF770949
1242 Mesocriconema onoense F Auburn University, Auburn, AL Southeastern Mixed Forests KJ787834
502 Mesocriconema ornatum F USDA Southeastern Fruit and Nut Tree Reseach Station, GA Southeastern Mixed Forests KJ787824
P184030 Discocriconemella limitanea F Las Cruces Biological Station, Costa Rica Isthmian-Pacific Moist forests KJ788069
ZB17051005279 Discocriconemella limitanea F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770975
ZB17042605146 Discocriconemella limitanea F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770973
ZB17051005280 Discocriconemella limitanea F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770976
ZB17042605147 Discocriconemella limitanea F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770974
ZB17051005282 Discocriconemella limitanea F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770978
ZB17051005281 Discocriconemella limitanea F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770977
1231 Bakernema inaequale F Pauchaug State Forest, WI Northeastern Coastal Forests MF770896
1460 Bakernema inaequale F Purchase Knob, GRSM, NC Appalachian-Blue Ridge Forests MF770902
1484 Bakernema inaequale F Arlington Woods, GWMP, VA Southeastern Mixed Forests MF770903
1157 Lobocriconema thornei F Tippecanoe County, IN Central Forest-Grassland Transition Zone KU236522
3368 Lobocriconema thornei F Crane Hollow Preserve, OH Appalachian Mixed Mesophytic Forests KU236539
2525 Lobocriconema thornei F Michigan State University, East Lansing, MI Southern Great Lakes Forests KU236534
3382 Lobocriconema thornei F Porcupine Mountains Wilderness State Park, MI Western Great Lakes Forest KU236626
3414 Lobocriconema thornei F Parfrey's Glen State Natural Area, WI Upper Midwest Forest-Savanna Transition Zone KU236627
3317 Lobocriconema sp. F Twin Creeks, GRSM, TN Appalachian-Blue Ridge Forests KU236521
3229 Lobocriconema sp. F Ozark National Forest, AR Central US Hardwood Forests KU236631
5563 Lobocriconema incrassatum F Emigration Canyon, UT Wasatch and Uinta Montane Forests KU236508
5576 Lobocriconema incrassatum J Providence Canyon, Cache County, UT Wasatch and Uinta Montane Forests KU236620
5577 Lobocriconema incrassatum F Providence Canyon, Cache County, UT Wasatch and Uinta Montane Forests KU236621
3675 Lobocriconema sp. F Canyonlands, BITH, TX Piney Woods Forests KU236623
3677 Lobocriconema sp. F Canyonlands, BITH, TX Piney Woods Forests KU236624
894 Lobocriconema sp. F Chimney Creek, GRSM, TN Appalachian-Blue Ridge Forests KU236496
1206 Lobocriconema sp. F Pine Cliff State Natural Area, WI Upper Midwest Forest-Savanna Transition Zone KU236491
3267 Lobocriconema sp. F Ozark National Forest, AR Central US Hardwood Forests KU236495
3203 Lobocriconema sp. F Ichetucknee Springs State Park, FL Southeastern Conifer Forests KU236554
577 Lobocriconema sp. F Ichetucknee Springs State Park, FL Southeastern Conifer Forests KU236548
3195 Lobocriconema sp. F Ichetucknee Springs State Park, FL Southeastern Conifer Forests KU236552
5583 Lobocriconema warrenense F St. Francis National Forest, AR Mississippi Lowland Forests MF770958
3645 Lobocriconema warrenense F Big Sandy Creek Unit, BITH, TX Piney Woods Forests KU236546
3668 Lobocriconema warrenense F Big Sandy Creek Unit, BITH, TX Piney Woods Forests KU236547
2914 Lobocriconema sp. F Aurora Prairie Preserve, SD Central Tall Grasslands KU236570
1382 Lobocriconema sp. J Spring Creek Prairie, NE Central Tall Grasslands KU236568
1 Lobocriconema sp. F Timmas Farm State Ecological Preserve, NE Central Tall Grasslands KU236629
2273 Lobocriconema sp. F Roy E. Larsen Sandyland Sanctuary, TX Piney Woods Forests KU236555
2862 Lobocriconema sp. F Konza Prairie Biological Station, KS Flint Hills Tall Grasslands KU236557
3068 Lobocriconema sp. F Cataloochee, GRSM, NC Appalachian-Blue Ridge Forests KU236601
3196 Lobocriconema sp. F Ichetucknee Springs State Park, FL Southeastern Conifer Forests KU236613
3249 Lobocriconema sp. F Oconaluftee, GRSM, NC Appalachian-Blue Ridge Forests KU236571
3257 Lobocriconema sp. F Ozark National Forest, AR Central US Hardwood Forests KU236572
3057 Lobocriconema sp. F Tunica Hills State Wildlife Refuge, LA Mississippi Lowland Forests KU236597
1395 Lobocriconema sp. F Leiter Manxion & Turkey Run, GWMP, VA Southeastern Mixed Forests KU236630
3297 Lobocriconema sp. F Torreya State Park, FL Southeastern Conifer Forests KU236608
3615 Lobocriconema sp. F Big Sandy Creek Unit, BITH, TX Piney Woods Forests KU236588
3663 Lobocriconema sp. F Lance Rosier Unit, BITH, TX Piney Woods Forests KU236590
1288 Pakcriconemoides sphaerocephalum F Spring Creek Prairie, NE Central Tall Grasslands MF770898
1455 Pakcriconemoides sphaerocephalum F Juan Diaz County, Puerto Rico Puerto Rican Moist Forests MF770901
ZB17051104893 Criconemoides parvus F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770968
1099 Criconemoides annulatus F Custer Gallatin National Forest, MT South Central Rockies Forests MF77089
3669 Criconemoides annulatus F Canyonlands Unit, BITH, TX Piney Woods Forests MF770952
5765 Criconemoides annulatus F Roosevelt National Forest, CO Colorado Rockies Forests MF770961
5565 Criconemoides annulatus F Emigration Canyon, UT Wasatch and Uinta Montane Forests MF770956
5566 Criconemoides annulatus F Emigration Canyon, UT Wasatch and Uinta Montane Forests MF770957
1101 Criconemoides informis F Gallatin National Forest, MT South Central Rockies Forests KJ787842
5788 Criconemoides informis J Uncompahgre National Forest, CO Colorado Rockies Forests MF770962
2962 Hemicycliophora cf. sphagni F Hobe Sound National Wildlife Refuge, FL Florida Sand Pine Scrub MF770923
1261 Hemicycliophora cf. macristhmus F Great Falls Park, GWMP, VA Southeastern Mixed Forests KJ788066
3040 Hemicycliophora sp. J Uinta-Wasatch-Cache National Forest, UT Wasatch and Uinta Montane Forests MF770934
3041 Hemicycliophora sp. J Uinta-Wasatch-Cache National Forest, UT Wasatch and Uinta Montane Forests MF770935
5921 Gracilacus wuae J Ontario, Canada Eastern Great Lakes lowland forests MF770965
5922 Gracilacus wuae J Ontario, Canada Eastern Great Lakes lowland forests MF770966
5748 Gracilacus sp. F Santa Fe National Forest, NM Colorado Rockies Forests MF770960
2508 Paratylenchus sp. F Jepson Prairie Preserve, CA California Central Valley Grasslands MF770905
281 Paratylenchus projectus F Hitchcock County, NE Central and Southern Mixed Grasslands MF770889
878 Paratylenchus projectus F Steele County, ND Northern Mixed Grasslands MF770890
1328 Criconema mutabile F Fresno County, CA California Central Valley Grasslands KU236637
3432 Criconema mutabile F Oaky Woods Wildlife Management Area, GA Southeastern Mixed Forests MF770948
2460 Criconema sp. F Beaumont Unit, BITH, TX Piney Woods Forests MF770904
2686 Criconema sp. F Auburn University, Auburn, AL Southeastern Mixed Forests MF770908
1404 Criconema permistum F Leiter Mansion & Turkey Run, GWMP, VA Southeastern Mixed Forests MF770900
923 Criconema permistum F Laurel Falls Trail, GRSM, TN Appalachian-Blue Ridge Forests MF770891
927 Criconema permistum F Laurel Falls Trail, GRSM, TN Appalachian-Blue Ridge Forests MF770892
2766 Hemicriconemoides chitwoodi F Anderson County, SC Southeastern Mixed Forests MF770916
5545 Hemicriconemoides sp. F Noh Bo Forest, Thailand Kayah-Karen Montane Rain Forests MF770955
ZB17042605150 Discocriconemella hengsungica F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770969
ZB17051005283 Discocriconemella hengsungica F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770970
ZB17051005284 Discocriconemella hengsungica F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770971
ZB17051005285 Discocriconemella hengsungica F Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF770972
3270 Discocriconemella sp. F Noh Bo Forest, Thailand Kayah-Karen Montane Rain Forests MF770946
1212 Xenocriconemella macrodora F Accotink Watershed, VA Southeastern Mixed Forests MF770894
1213 Xenocriconemella macrodora F Accotink Watershed, VA Southeastern Mixed Forests MF770895
3141 Xenocriconemella macrodora F Ponce de Leon State Park, FL Southeastern Conifer Forests MF770941
3483 Xenocriconemella macrodora F Wakulla Springs State Park, FL Southeastern Conifer Forests MF770950
2991 Ogma octangularis F Gifford Woods State Park, VT New England Acadian Forests MF770928
3356 Ogma octangularis F Raspberry Island, APIS, WI Western Great Lakes Forest MF770947
2985 Ogma octangularis F Gifford Woods State Park, VT New England Acadian Forests MF770926
3004 Ogma octangularis F Goshen Prong, GRSM, TN Appalachian-Blue Ridge Forests MF770932
3005 Ogma octangularis F Goshen Prong, GRSM, TN Appalachian-Blue Ridge Forests MF770933
1247 Criconema sp. F Nine-Mile Prairie, NE Central Tall Grasslands MF770897
1399 Criconema sp. F Nine-Mile Prairie, NE Central Tall Grasslands MF770899
2975 Ogma decalineatus F Red Rock Prairie Preserve, MN Central Tall Grasslands MF770924
2976 Ogma decalineatus F Red Rock Prairie Preserve, MN Central Tall Grasslands MF770925
2635 Criconema loofi F Brushy Mtn., GRSM, TN Appalachian-Blue Ridge Forests KX290563
2758 Criconema sphagni F Trillium Gap, GRSM, TN Appalachian-Blue Ridge Forests MF770912
2759 Criconema sphagni F Trillium Gap, GRSM, TN Appalachian-Blue Ridge Forests MF770913
2808 Criconema sphagni F Twin Creeks, GRSM, TN Appalachian-Blue Ridge Forests MF770918
2807 Criconema sphagni J Twin Creeks, GRSM, TN Appalachian-Blue Ridge Forests MF770917
3067 Criconema sphagni F Cataloochee, GRSM, NC Appalachian-Blue Ridge Forests MF770938
3069 Criconema sphagni F Cataloochee, GRSM, NC Appalachian-Blue Ridge Forests MF770939
3220 Criconema sphagni F Purchase Knob, GRSM, NC Appalachian-Blue Ridge Forests MF770944
2724 Criconema longulum J Gregory Bald, GRSM, NC Appalachian-Blue Ridge Forests MF770910
2522 Criconema petasum F Michigan State University, East Lansing, MI Southern Great Lakes Forests MF770906
2993 Criconema petasum F Gifford Woods State Park, VT New England Acadian Forests KU236641
2994 Criconema petasum F Gifford Woods State Park, VT New England Acadian Forests MF770930
5842 Crossonema fimbriatum F Simes Tract, Harvard Forest LTER, MA New England Acadian Forests MF770963
5843 Crossonema fimbriatum F Simes Tract, Harvard Forest LTER, MA New England Acadian Forests MF770964
2995 Crossonema fimbriatum F Gifford Woods State Park, VT New England Acadian Forests MF770931
2755 Crossonema menzeli F Trillium Gap, GRSM, TN Appalachian-Blue Ridge Forests MF770911
2948 Crossonema menzeli F West Point, GRSM, TN Appalachian-Blue Ridge Forests MF770922
2761 Crossonema menzeli F Tongass National Forest, AK Northern Pacific Coastal Forests MF770914
2762 Crossonema menzeli F Tongass National Forest, AK Northern Pacific Coastal Forests MF770915
2989 Crossonema sp. F Gifford Woods State Park, VT New England Acadian Forests MF770927
2992 Crossonema sp. F Gifford Woods State Park, VT New England Acadian Forests MF770929
2573 Ogma murrayi F Santa Cruz Island Reserve, CA California Coastal Sage and Chaparral MF770907
3262 Ogma murrayi F Ozark National Forest, AR Central US Hardwood Forests MF770945
2636 Ogma seymouri F Brushy Mtn., GRSM, TN Appalachian-Blue Ridge Forests KX290587
2753 Ogma seymouri F Tongass National Forest, AK Northern Pacific Coastal Forests KX290594
2779 Ogma seymouri F Tongass National Forest, AK Northern Pacific Coastal Forests KX290599
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Table AII.

Table of location data and GenBank accession numbers for new Discocriconemella limitanea, Criconemoides parvus and Discocriconemella hengsungica specimens appearing on the 18S maximum likelihood tree, in tree order.

ZB17052504993 Discocriconemella limitanea Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795592
ZB17052504991 Discocriconemella limitanea Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795591
ZB17052504983 Criconemoides parvus Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795587
ZB17052504981 Criconemoides parvus Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795586
ZB17052504979 Criconemoides parvus Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795585
ZB17052504987 Discocriconemella hengsungica Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795589
ZB17052504985 Discocriconemella hengsungica Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795588
ZB17052504989 Discocriconemella hengsungica Hangzhou, Zhejiang Province, China Eastern coast of China, flooded grasslands and savannas MF795590
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Acknowledgments

This research was supported by the National Natural Science Foundation of China (Project no. 31371921) and by U.S. National Science Foundation Proposal DEB-1145440. The authors acknowledge Dr. N. H. Rong and X. Li, for providing assistance in the preparation of SEM and R. Cai and N. Qu for helping with the samplings.

Appendix

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