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Characterization of Juvenile Stages of Bursaphelenchus crenati Rühm, 1956 (Nematoda: Aphelenchoidoidea)

Alexander Y. Ryss
Alexander Y. Ryss
 und 
Kristina S. Polyanina
Kristina S. Polyanina
   | 03. Dez. 2018
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Online veröffentlicht: 03. Dez. 2018
Seitenbereich: 459 - 472
DOI: https://doi.org/10.21307/jofnem-2018-042
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© 2018 Alexander Y et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Figure 1

Bursaphelenchus crenati. Development in egg. A. Cleavage; B. Gastrula; C,D. First stage juvenile (J1) within egg shell, at different focal planes; E,F,G. Second stage juvenile (J2) molting with shed cuticle, at different focal planes; H. Hatching J2, preparing to leave the egg shell. Scale 20 µm.
Bursaphelenchus crenati. Development in egg. A. Cleavage; B. Gastrula; C,D. First stage juvenile (J1) within egg shell, at different focal planes; E,F,G. Second stage juvenile (J2) molting with shed cuticle, at different focal planes; H. Hatching J2, preparing to leave the egg shell. Scale 20 µm.

Figure 2

Bursaphelenchus crenati. Methylene blue staining. Junior juveniles. A,B. Second stage juvenile (J2): A. Genital primordium; B. Tail; C,D. Genital primordium of J3 female juveniles (arrows: anterior germinal zone); E,F. Tails of female J3; G, H. Genital primordium of J3 male juveniles (arrows: posterior germinal zone); I,J. Tails of male J3 (arrows: cloaca primordium). Scale 20 µm.
Bursaphelenchus crenati. Methylene blue staining. Junior juveniles. A,B. Second stage juvenile (J2): A. Genital primordium; B. Tail; C,D. Genital primordium of J3 female juveniles (arrows: anterior germinal zone); E,F. Tails of female J3; G, H. Genital primordium of J3 male juveniles (arrows: posterior germinal zone); I,J. Tails of male J3 (arrows: cloaca primordium). Scale 20 µm.

Figure 3

Bursaphelenchus crenati. Methylene blue staining. Genital primordium and tails of the fourth stage juveniles and adults. A. Genital primordium of the fourth stage female juvenile (J4); B,C. Molting female juvenile J4-adult; B. Genital primordium; C. Tail; D. Genital system of adult female; E, F. Fourth stage male juvenile; E. Genital primordium; F. Tail and cloacal primordium; G. Genital system of adult male. Scale 50 µm.
Bursaphelenchus crenati. Methylene blue staining. Genital primordium and tails of the fourth stage juveniles and adults. A. Genital primordium of the fourth stage female juvenile (J4); B,C. Molting female juvenile J4-adult; B. Genital primordium; C. Tail; D. Genital system of adult female; E, F. Fourth stage male juvenile; E. Genital primordium; F. Tail and cloacal primordium; G. Genital system of adult male. Scale 50 µm.

Figure 4

Position of genital primordia in bodies of male juveniles and adults. Scale 50 µm.
Position of genital primordia in bodies of male juveniles and adults. Scale 50 µm.

Figure 5

Position of genital primordia in bodies of female juveniles and adults. Scale 50 µm.
Position of genital primordia in bodies of female juveniles and adults. Scale 50 µm.

Figure 6

Bursaphelenchus crenati. Molting juveniles (shedding cuticle in tail). A,B. Molting male juvenile from J2 to J3; A. Genital primordium (gp); B. Tail and cloacal primordium (cp); C-H. Molting male juvenile from J3 to J4; C. Genital primordium of molting J3-J4 (aac – anterior apical cell, sz – somatic zone, gerz -germinal zone); D, E, H. Tail and cloacal primordium (cp) of J3-J4 male juvenile; F. Genital primordium of molting male J3-J4 juvenile at “loop stage”; G. Drawing of F with explanation of the reversion of the somatic zone (sz) with anterior apical cell (aac) flexed to the germinal zone (gerz); gc – germinal cells; pac – posterior apical cell, sn – somatic nuclei, vc – ventral cord nuclei; I,J – molting female J3-J4 juvenile; I. Genital primordium with anterior germinal zone (gerz); J. Tail. Scale 50 µm.
Bursaphelenchus crenati. Molting juveniles (shedding cuticle in tail). A,B. Molting male juvenile from J2 to J3; A. Genital primordium (gp); B. Tail and cloacal primordium (cp); C-H. Molting male juvenile from J3 to J4; C. Genital primordium of molting J3-J4 (aac – anterior apical cell, sz – somatic zone, gerz -germinal zone); D, E, H. Tail and cloacal primordium (cp) of J3-J4 male juvenile; F. Genital primordium of molting male J3-J4 juvenile at “loop stage”; G. Drawing of F with explanation of the reversion of the somatic zone (sz) with anterior apical cell (aac) flexed to the germinal zone (gerz); gc – germinal cells; pac – posterior apical cell, sn – somatic nuclei, vc – ventral cord nuclei; I,J – molting female J3-J4 juvenile; I. Genital primordium with anterior germinal zone (gerz); J. Tail. Scale 50 µm.

Figure 7

Diagrams of juvenile growth. A. Body length; B. Ratio of genital primordium length to body length (GP/L, %). Standard deviation (STD) levels are marked for mean values.
Diagrams of juvenile growth. A. Body length; B. Ratio of genital primordium length to body length (GP/L, %). Standard deviation (STD) levels are marked for mean values.

Figure 8

Dauer juveniles. Methylene blue staining. A. Male juvenile J3D; B. Female juvenile J3D; C. Genital primordium of male dauer juvenile; D. Tail of male dauer juvenile. Scale 50 µm for A,B and 20 µm for C,D.
Dauer juveniles. Methylene blue staining. A. Male juvenile J3D; B. Female juvenile J3D; C. Genital primordium of male dauer juvenile; D. Tail of male dauer juvenile. Scale 50 µm for A,B and 20 µm for C,D.

Figure 9

Dauer juveniles molted to J4D after 3 hr in 0.9% NaCl solution. A. Male juvenile; B. Female juvenile.
Dauer juveniles molted to J4D after 3 hr in 0.9% NaCl solution. A. Male juvenile; B. Female juvenile.

Measurements (in µm) and ratios of the development stages of Bursaphelenchus crenati.

Stage/Character J2→J3 male J2→J3 female J3→J4 male J3→J4 female J4→male J4→female Dauer J3D
n 16 5 10 20 5 17 20
L 347 ± 7 323 ± 86 370 ± 3 377 ± 10 596 ± 91 544 ± 69 413 ± 20
(338–354) (181–410) (366–374) (364–398) (532–660) (433–614) (392–463)
Body width 9 ± 1 10 ± 2 11 ± 2 12 ± 1 16 ± 0.3 13 ± 3 8 ± 1
(8–10) (8–14) (9–13) (11–13) (14–17) (9–17) (6–9)
Pharynx 107 ± 4 103 ± 21 110 ± 5 110 ± 5 112 ± 9 117 ± 6 119 ± 9
(104–112) (65–116) (105–115) (102–117) (105–118) (109–123) (101–128)
Pharyngeal gland 49 ± 5 51 ± 1 49 ± 4 48 ± 4 46 ± 1 48 ± 6 43 ± 7
(44–56) (49–53) (44–55) (41–54) (45–47) (40–55) (35–55)
Stylet 7 ± 1.2 8 ± 1 7 ± 1 9 ± 0.7 9 ± 0.4 9 ± 1.4 9.4 ± 0.4
(6–9) (6–9) (6–8) (8–10) (9–10) (8–11) (9–10)
Lip region width 5.0 ± 0.3 5 ± 0.6 5.6 ± 0.5 5 ± 0.6 5 ± 0.4 5.4 ± 0.4 4.8 ± 1.0
(4–5) (4–6) (4.8–6.0) (4–6) (5–6) (5–6) (4–7)
Lip region height 3 ± 0.3 2.4 ± 0.2 2.4 ± 0.1 3 ± 0.3 3 ± 1 2.9 ± 0.4 2.9 ± 0.3
(2–3) (2–3) (2.3–2.5) (2–3) (2–3)– (2–3) (2.5–4)
Median bulb from 46 ± 1 45 ± 8 47 ± 0.1 47 ± 3 46 ± 12 53 ± 3 49 ± 2
Anterior (45–47) (31–50) (46–48) (40–50) (38–54) (51–58) (45–51)
Median bulb length 11 ± 1.2 11 ± 0.9 12 ± 1 12 ± 1 13 ± 1 13 ± 0.2 11 ± 2
(10–13) (10–12) (11–13) (10–13) (12–14) (12.5–13.5) (9–15)
Median bulb width 9 ± 1.1 8 ± 1.5 10 ± 1 10 ± 1 9.9 ± 0.2 10 ± 1 8 ± 2
(8–10) (6–10) (9–11) (7–10) (9.5–10.0) (9–11) (6–10)
Excretory pore 51 ± 1 50 ± 8 53 ± 2 54 ± 4 52 ± 12 58 ± 3 40 ± 3
from anterior (50–52) (37–56) (51–54) (45–59) (44–61) (54–62) (37–44)
Tail 22 ± 4 21 ± 6 22 ± 1 26 ± 1.5 28 ± 5 28 ± 3 37 ± 3
(20–28) (11–27) (21–24) (24–28) (25–32) (23–31) (30–41)
Anal body width 8 ± 0.4 8 ± 3 11 ± 2 11 ± 1.1 11 ±3 10.1 ±0.9 8 ± 1
(7–8) (5–12) (8–13) (10–13) (9–13) (9–11) (5–9)
Genital primordium 18 ± 4 10 ± 3 20 ± 2 18 ± 5 158 ± 138 197 ± 105 14.8 ± 2.1
Length (GPL) (14–23) (6–14) (17–22) (13–28) (60–255) (122–369) (11–18)
Genital primordium 5 ± 1 5 ± 1 4.8 ± 05 5 ± 1 10 ±5 9 ± 3 3.9 ± 0.4
Width (GPW) (4–5) (3–7) (4.0–5.3) (3–6) (6–13) (7–14) (3–5)
Spicule length – – – – – – –
Along arc
a 40 ± 5 34 ± 8 34.8 ± 5.2 32 ± 2 39 ± 12 41.5 ± 4.6 54 ± 8.3
(34–46) (22–41) (28.4–41.8) (29–35) (31–48) (36.8–48.9) (44.6–69.6)
b 6.0 ± 0.3 5.6 ± 0.6 6.1 ± 0.2 6.1–0.2 9.1 ± 0.3 7.8 ± 0.6 5.5 ± 0.4
(5.7–6.4) (4.8–6.4) (5.9–6.3) (5.8–6.5) (8.9–9.2) (6.7–8.3) (5.1–6.4)
b’ 3.2 ± 0.1 3.1 ± 0.3 3.4 ± 0.2 3.4 ± 0.2 5.3 ± 0.4 4.6 ±0.5 3.5 ±0.3
(3.1–3.3) (2.8–3.6) (3.2–3.6) (3.1–3.7) (5.1–5.6) (4.0–5.2) (3.0–4.1)
c 16.0 ± 2.5 15.6 ± 0.6 16.6 ± 0.9 14.8 ± 0.8 21.1 ± 0.9 19.7 ± 1.7 11.2 ± 0.9
(12.4–17.9) (14.7–16.2) (15.1–17.3) (13.8–1.58) (20.5–21.7) (18.0–22.3) (9.9–13.2)
c’ 2.8 ± 0.4 2.8 ± 0.5 2.1 ± 0.3 2.3 ± 0.2 2.6 ±0.1 2.8 ± 0.3 4.7 ± 0.5
(2.4–3.4) (2.2–3.4) (1.7–2.5) (2.0–2.8) (2.6–2.7) (2.3–3.2) (4.3–5.5)
V % or (V): genital primordium center from anterior, to body length, in % 61 ± 2 64 ± 3 62 ± 1 66 ± 2 52 ± 3 73.2 ± 1.6 62 ± 5
(59–64) (59–68) (60–64) (63–68) (49–54) (70.5–74.3) (56–72)
GPL/GPW 4.0 ± 1.1 2.3 ± 0.6 4.2 ± 0.2 3.9 ±1 15 ± 6 20 ± 4 3.8 ± 0.5
(3.0–5.4) (1.5–2.9) (3.9–4.5) (2.7–6.1) (10–19) (16–27) (3–4.5)
GPL/L, % 5.2 ± 1.2 3.3 ± 1.0 5.5 ± 0.6 5 ± 1 25 ± 19 35.3 ±15.2 4 ± 1
(4.2–6.6) (1.8–4.3) (4.5–5.9) (4–7) (11–39) (24.3–60.0) (3–5)
Lip region length to its 1.8 ± 0.3 2.0 ± 0.3 2.3 ± 0.2 1.9 ± 0.2 2.1 ± 0.6 1.9 ± 0.1 1.6 ± 0.3
Width (1.6–2.3) (1.6–2.4) (2.0–2.6) (1.6–2.4) (1.7–2.5) (1.8–2.0) (1.4–2.4)
Median bulb length to 1.4 ± 0.2 1.4 ± 0.2 1.2 ± 0.1 1.2 ± 0.1 1.3 ± 0.2 1.3 ± 0.1 1.4 ± 0.2
Its width (1.1–1.6) (1.3–1.7) (1.2–1.3) (1.0–1.4) (1.2–1.4) (1.2 ± 1.4) (1.1–1.7)

Tabular key to juvenile stages of Bursaphelenchus crenati.

C1 C2 C3 C4 C5 C6
Stage/Character Copulative structures Average body size, in µm Ratio: genital primordium to body length, in % Genital primordium cellular structure Cloaca primordium or cloaca around rectum Genital primordium somatic part: a division to sections
J2 Absent 170 (150–180) 4 Small with two large germinal cells in center Absent Absent
J3 male Absent 370 (340–400) 5 (4–7) 2–5 large germinal cells in the posterior part of primordium, 12 small somatic nuclei in anterior part Present Absent
J3 female Absent 380 (340–400) 4 (3–4) 2–5 large germinal cells in the anterior part of primordium, 12 small somatic nuclei in posterior part Absent Absent
J4 male Absent 460 (380–530) 18 (11–25) 20–60 large germinal cells in anterior part of primordium and 30–60 somatic cells in posterior part Present Absent
J4 female Absent 490 (480–510) 27 (16–33) 20–60 large germinal cells in anterior part of primordium and 30–60 somatic cells in posterior part Absent Absent
Male, adult Paired spicules in cloaca, at tail end 700 (610–800) 67 (58–72) More than 60 germinal cells in anterior part Present Absent
Female, adult Vulva at 75% body length from anterior end 840 (750–1100) 62 (55–71) More than 60 germinal cells in anterior part Absent Present
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