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Redescription and phylogenetic analysis of the type species of the genus Panagrellus Thorne, 1938 (Rhabditida, Panagrolaimidae), P. pycnus Thorne, 1938, including the first SEM study

Joaquín Abolafia
Joaquín Abolafia
 y 
Matteo Vecchi
Matteo Vecchi
   | 01 oct 2021
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Publicado en línea: 01 oct 2021
Páginas: 1 - 20
DOI: https://doi.org/10.21307/jofnem-2021-080
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© 2021 Joaquín Abolafia et al., published by Sciendo.
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Figure 1:

Panagrellus pycnus Thorne, 1938 (line drawing). (A) Neck; (B) Anterior end; (C) Female reproductive system; (D) Entire female; (E) Female posterior end; (F) Lateral field; (G) Male posterior end; (H) Entire male.
Panagrellus pycnus Thorne, 1938 (line drawing). (A) Neck; (B) Anterior end; (C) Female reproductive system; (D) Entire female; (E) Female posterior end; (F) Lateral field; (G) Male posterior end; (H) Entire male.

Figure 2:

Panagrellus pycnus Thorne, 1938 (light microscopy). (A) Neck (anterior white arrow pointing the excretory pore, posterior white arrow pointing the hemizonid, black arrow pointing the deirid); (B) Anterior end; (C) Vagina; (D) Female reproductive system; (E) Female posterior end (arrow pointing the phasmid); (F) Lateral field; (G) Entire female; (H) Male posterior end (black arrows pointing genital papillae, GP; mid-ventral papillae, MP; white arrow pointing the phasmid, ph); (I) Entire male.
Panagrellus pycnus Thorne, 1938 (light microscopy). (A) Neck (anterior white arrow pointing the excretory pore, posterior white arrow pointing the hemizonid, black arrow pointing the deirid); (B) Anterior end; (C) Vagina; (D) Female reproductive system; (E) Female posterior end (arrow pointing the phasmid); (F) Lateral field; (G) Entire female; (H) Male posterior end (black arrows pointing genital papillae, GP; mid-ventral papillae, MP; white arrow pointing the phasmid, ph); (I) Entire male.

Figure 3:

Panagrellus pycnus Thorne, 1938 (light microscopy). (A–E) Morphological variability of spicules and gubernaculum.
Panagrellus pycnus Thorne, 1938 (light microscopy). (A–E) Morphological variability of spicules and gubernaculum.

Figure 4:

Panagrellus pycnus Thorne, 1938 (scanning electron microscopy). A–C: Lip region in lateral, ventral and frontal views, respectively (arrows pointing the amphids); D–F: Stomatal denticles; G: Lateral field; H: Excretory pore; I: Deirid; J: Vagina; K, Q: Spicules tip in lateral and dorsal views, respectively; L, M: Female posterior end in lateral and ventral views, respectively; N: Male phasmid; O, P: Male posterior end in lateral and ventral views, respectively (black arrows pointing the genital papillae, white arrow pointing the phasmid); R: Mid-ventral papillae (arrow).
Panagrellus pycnus Thorne, 1938 (scanning electron microscopy). A–C: Lip region in lateral, ventral and frontal views, respectively (arrows pointing the amphids); D–F: Stomatal denticles; G: Lateral field; H: Excretory pore; I: Deirid; J: Vagina; K, Q: Spicules tip in lateral and dorsal views, respectively; L, M: Female posterior end in lateral and ventral views, respectively; N: Male phasmid; O, P: Male posterior end in lateral and ventral views, respectively (black arrows pointing the genital papillae, white arrow pointing the phasmid); R: Mid-ventral papillae (arrow).

Figure 5:

Morphology of the spicules and gubernacula of the species of the genera Baujardia Bert, Tandingan De Ley, Van Driessche, Segers and De Ley, 2003 and Panagrellus Thorne, 1938. (A) Baujardia; (B–D) Panagrellus species with truncated manubrium; (E–I) Panagrellus species with rounded or conoid manubrium; (E–P) Panagrellus species with curved or hook-shaped manubrium (c = calamus, dh = dorsal hump, l = lamina, m = manubrium, v = velum, t = tip).
Morphology of the spicules and gubernacula of the species of the genera Baujardia Bert, Tandingan De Ley, Van Driessche, Segers and De Ley, 2003 and Panagrellus Thorne, 1938. (A) Baujardia; (B–D) Panagrellus species with truncated manubrium; (E–I) Panagrellus species with rounded or conoid manubrium; (E–P) Panagrellus species with curved or hook-shaped manubrium (c = calamus, dh = dorsal hump, l = lamina, m = manubrium, v = velum, t = tip).

Figure 6:

Bayesian Inference tree showing the phylogenetic position of Panagrellus pycnus and its related taxa based on a concatenated 18S and 28S rDNA regions. Bayesian posterior probabilities (pp) are given for each clade. Nodes with pp < 0.70 were collapsed. When pp = 1, its value is not shown. Scale bar shows the number of substitutions per site.
Bayesian Inference tree showing the phylogenetic position of Panagrellus pycnus and its related taxa based on a concatenated 18S and 28S rDNA regions. Bayesian posterior probabilities (pp) are given for each clade. Nodes with pp < 0.70 were collapsed. When pp = 1, its value is not shown. Scale bar shows the number of substitutions per site.

Comparative morphometrics of Panagrellus pycnus Thorne, 1938.

Reference Present paper Thorne (1938) Hechler (1971a) Andrássy (2005)**
Country Italy USA USA Hungary
Sex Female Male Female Male Female Male Female Male
n 10 10 ? ? 12 15 ? ?
Body length (L) 993–1,258 931–1,322 1,000–1,400 800–1,200 1,170–1,410 900–1,222 1,170–1,410 800–1,200
a 23.6–29.6 24.6–29.9 18.0 21.0 16.0–21.5 20.6–26.9 16.0–22.0 21.0–27.0
b 5.3–16.5 4.6–6.5 8.0 6.8 6.1–8.0 5.7–7.4 6.1–8.0 5.7–7.4
c 6.8–8.1 7.8–10.9 8.5 9.0 7.6–10.4 7.9–10.4 8.0–10.0 8.0–10.0
c' 4.9–7.0 3.6–5.1 4.7* 4.2* 5.8* 4.7* 6.0 3.5–4.0
V 63–69 – 73 – 71–77 – 71–77 –
Stoma length 12–16 10–14 ? ? 11–14 10–13 12–14 12–14
Spicules length (arc) – 70–81 – ? – 71–81* – ?
Spicules length (chord) – 56–61 – ? – 54–70 – 50–70
Gubernaculum length – 28–29 – ? – 25–27 – 25–27

Length of the spicules (measured in arc) of the Panagrellus species with hooked manubrium.

References Ceylonensis Dubius Filiformis Leperisini Pycnus Redivivus Redivivus as leucocephalus Redivivus as parasiticus Silusioides
Present paper – – – – 70–81 – – – –
Goodey (1922) – – – – – 70* – – –
Steiner (1936) – – – – – – ? – –
Thorne (1938) – – – – 74*** – – – –
Sandground (1939) – – – – – – – 65–68* –
Rühm (1956) – – – – – 70–90* ceylonensis? – – –
Tsalolikhin (1965) – – – – – – – – 75–90**
Sanwal (1960) – 60–62* – – – – – – –
Hechler (1970) – – – – – 77* – – –
Hechler (1971a) – 56–60* – – 71–81* 64–74* 45* – –
Hechler (1971b) 81–89* – – – 77–83* – – – –
Sukul (1971) – – 27* – – – – – –
Massey (1974) – – – 60* – – – – –
Stock and Nadler (2006) 83* redivivus? silusioides? 64* dubius? leperisini? – – – 65* ceylonensis? parasiticus? – – –

GenBank accession numbers of the species used in the phylogenetic tree.

Species 18S rDNA 28S rDNA
Ablechroiulus lacustris EU196013 EU195976
Acrobeles complexus KU180671 DQ145620
Acrobeloides nanus DQ102707 DQ903076
Acrostichus halicti HQ130163 HQ130212
Aglenchus agricola KJ869356 KP835679
Alloionema appendiculatum FJ665982 KP204846
Alloionema californicum KX017492 NA
Alloionema similis KX185606 NA
Anguina tritici AY593913 KC818620
Baujardia mirabilis AF547385 NA
Brevibucca punctata NA DQ077787
Brevibucca saprophaga EU196018 KU180677
Bunonema reticulatum EU196017 EU195989
Bunonema richtersi FJ040451 NA
Buonema franzi AJ966477 NA
Butlerius butleri KP453998 NA
Caenorhabditis angaria JN636068 JN636068
Cephalobus persegnis AY284663 AF143368
Cervidellus alutus AF202152 KU180683
Cuticonema vivipara EU196019 EU195991
Diplogaster rivalis KJ636326 NA
Diplogastrellus gracilis KJ877216 KJ877249
Diploscapter coronatus AY593921 NA
Ditylenchus destructor KJ636422 MN307126
Eucephalobus oxyurioides AY284665 HM439768
Fictor stercorarius KJ877235 KJ877282
Halicephalobus gingivalis 1 JX674039 JX194163
Halicephalobus gingivalis 2 NA KU180686
Heterodera koreana MZ027493 MZ027488
Koerneria luziae AB597232 KJ877284
Macrolaimus sp. LC382049 NA
Merlinius brevidens KX789708 NA
Mesorhabditis anisomorpha AF083013 NA
Micoletzkya buetschlii JX163973 NA
Mononchoides composticola KP067833 NA
Myolaimus byersi KU180665 KU180676
Myolaimus sp. NA DQ145643
Neoalloionema tricaudatum KR817916 KR817917
Oscheius insectivorus AF083019 EU195968
Panagrellus ceylonensis NA DQ408251
Panagrellus dubius 1 NA DQ145648
Panagrellus dubius 2 NA DQ408252
Panagrellus levitatus KY126845 NA
Panagrellus pycnus MZ656001 MZ656000
Panagrellus redivivoides 1 MH608262 MH608297
Panagrellus redivivoides 2 MH608263 MH608298
Panagrellus redivivus 1 AF083007 DQ408250
Panagrellus redivivus 2 MK541674 MK541658
Panagrellus redivivus 3 NA AF331910
Panagrellus sp. 1 MN082326 NA
Panagrellus sp. 2 MH608264 MH608299
Panagrellus sp. 3 KP876562 KM489128
Panagrobelus sp. LC382079 NA
Panagrobelus stammeri 1 FJ969134 NA
Panagrolaimus davidi AJ567385 AY878385
Panagrolaimus detritophagus EU543176 GU014547
Panagrolaimus subelongatus KY119431 NA
Panagrolaimus trilabiatus KF011487 NA
Parasitorhabdis obtusa EU003189 EF990724
Plectonchus sp. AY593920 NA
Plectonchus wyganti KJ636307 NA
Plectus aquatilis AY284700 EF417147
Pristionchus fissidentatus KJ877237 KJ877273
Procephalobus sp. EU543179 NA
Propanagrolaimus filiformis KJ636392 NA
Propanagrolaimus sp. KJ434175 NA
Protorhabditis sp. AF083001 AY602168
Pseudacrobeles variabilis AF202150 NA
Psilenchus ilarus MK639403 MW716284
Rhabditella axei NA AY602177
Rhabditophanes sp. 1 JX674037 JX674036
Rhabditophanes sp. 2 AF202151 AY294185
Rotylenchus urmiaensis KP718970 KP718967
Shahnema ardabilense KM454872 KM454873
Shahnema golestanense KM454874 KM454875
Shahnema ilamense KM454870 KM454871
Steinermena feltiae FJ040419 NA
Steinernema scarabaei FJ040424 AY172023
Strongyloides callosciureus AB272231 AB272231
Strongyloides robustus AB272232 NA
Sudhausia crassa KJ877232 KJ877279
Tarantobelus arachnicida 1 MG669658 MF177710
Tarantobelus arachnicida 2 MZ655998 MZ656002
Tarantobelus arachnicida 3 MZ655999 MZ656003
Teratorhabdis mariannae EF990716 EF990721
Turbatrix aceti 1 AF202165 AY294184
Turbatrix aceti 2 KU180673 KU180690
Zeldia punctata NA DQ145662

Morphometrics of Panagrellus pycnus Thorne, 1938 obtained from culture.

Sex Female Male
n 10 10
Body length (L) 1,114.2 ± 103.5 (993–1258) 1,022.0 ± 117.5 (931–1,322)
a 26 ± 2.0 (23.6–29.6) 27 ± 1.6 (24.6–29.9)
b 6.9 ± 3.4 (5.3–16.5) 5.4 ± 0.5 (4.6–6.5)
c 7.5 ± 0.4 (6.8–8.1) 8.6 ± 0.9 (7.8–10.9)
c' 6.0 ± 0.6 (4.9–7.0) 4.4 ± 0.5 (3.6–5.1)
V 66.5 ± 1.8 (63–69) –
Lip region width 14.8 ± 1.2 (12–16) 14.1 ± 0.7 (13–15)
Stoma length 13.8 ± 1.4 (12–16) 12.7 ± 1.2 (10–14)
Pharyngeal corpus length 109.4 ± 4.9 (104–120) 107.4 ± 6.8 (93–114)
Isthmus length 39.6 ± 5.7 (30–50) 40.0 ± 5.7 (32–53)
Bulbus length 27.9 ± 2.0 (24–31) 27.8 ± 2.5 (24–33)
Pharynx length 176.1 ± 6.6 (167–190) 175.2 ± 11.8 (151–189)
Nerve ring – anterior end 148.3 ± 8.8 (137–160) 139.7 ± 11.0 (122–161)
Excretory pore – anterior end 128.9 ± 7.5 (120–139) 115.8 ± 11.0 (104–139)
Deirid-anterior end 153.3 ± 9.9 (142–160) 163.0 ± 6.1 (156–167)
Neck length 189.9 ± 6.8 (181–203) 187.9 ± 12.5 (161–202)
Body diameter at neck base 37.9 ± 3.1 (34–44) 35.1 ± 2.7 (33–42)
Body diameter at midbody 42.4 ± 4.6 (37–52) 37.6 ± 4.1 (32–47)
Lateral field width 5.7 ± 2.1 (4–8) 6.3 ± 1.0 (5–8)
Anterior ovary or testis length 551.4 ± 49.5 (463–650) 233.0 ± 41.7 (188–289)
Anterior oviduct length 56.1 ± 15.8 (40–91) –
Anterior uterus length 377.4 ± 63.8 (287–496) –
Post-vulval uterine sac length 133.4 ± 22.2 (99–162) –
Vagina length 42.0 ± 8.5 (36–48) –
Vulva – anterior end 740.9 ± 74.0 (668–863) –
Rectum or cloaca length 28.2 ± 3.8 (20–32) 9.8 ± 0.7 (9–11)
Anal body diameter 25.1 ± 2.8 (22–30) 27.2 ± 3.4 (23–34)
Tail length 148.9 ± 11.9 (133–170) 119.6 ± 10.1 (104–137)
Phasmid - anus distance 55.6 ± 6.1 (46–67) 47.7 ± 6.7 (36–57)
Spicules length (arc) – 77.4 ± 3.3 (70–81)
Gubernaculum length – 30.0 ± 1.2 (29–32)
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