External morphology and developmental changes of tarsal tips and mouthparts of the invasive spotted lanternfly, Lycorma delicatula (Hemiptera: Fulgoridae)

Abstract

External structures of insects contribute to the ability of herbivores to select and feed on their host plants. The invasive spotted lanternfly, Lycorma delicatula (Hemiptera: Fulgoridae) is an economically important and polyphagous insect pest in the eastern US. The lanternfly causes substantial damage to many woody plants by sucking phloem sap, reducing photosynthesis, causing weeping wounds, and creating conditions for sooty mold. Lanternfly nymphs switch host plants during their development. However, little is known about relationship between the lanternfly and its plant hosts, and particularly about morphological adaptations of the lanternfly to host plant usage at each developmental stage of the pest. In this study, we focused on assessing changes in morphology of (a) the lanternfly mouthparts (stylets and labium), and (b) the lanternfly tarsal tips (arolia and tarsal claws) at each developmental stage. Our study revealed several developmental patterns among which the presence of the indentations on mandibular stylets in late instars and adults, as well as the exponential growth of the labium and stylet length, and the tarsal claw dispersal during the lanternfly development. Our findings are critical for investigating and predicting the lanternfly host range, and the lanternfly dispersal to new host trees at each developmental stage.

Fig 1. Morphometric characteristics measured for the labium, the stylet fascicle and the tarsal tip of Lycorma delicatula.

(A) Labium and stylets. Lb1, distance from the labial tip to the base of the first labial segment; Lb2, distance from the labial tip to the base of the last labial segment; Lb3, maximum width of the last labial segment; Sf, distance from the tip of the stylet fascicle to the base of the stylets; Sfe, distance from the apex of stylet fascicle extended from labial tip to the labial tip. (B) Tarsal tip, the dorsal view. Tc1, distance between tarsal claw tips; Tc2, distance between bending centers of the external arcs of the tarsal claws; Ptc1, distance between the lateral margin of the arolium and tarsal claw tips; Ptc2, distance between the lateral margin of the arolium and bending centers of the external arcs of the tarsal claws; A1, the maximum anterior width of the arolium; A2, length of the lateral margin of the arolium; ᶿ, the angle between the lateral margins of the arolium.

Fig 2. Labium and labial segments of Lycorma delicatula in nymphs and adults.

(A) 4^th instar nymph; (B) Adult male. LS1-LS5, labial segments; LS1, LS2, LS3, and LS4 in nymphs correspond respectively to LS1, LS2, LS4, and LS5 in adults; LS3 in adults (white) is the 5^th (extra) segment.

Fig 3. Labium and stylet length of Lycorma delicatula across developmental stages.

(A) Labium length changes. (B) Stylet length changes. Axis labels: 1–4, 1^st-4^th instar nymphs; a, adults.

Fig 4. Growth curves for the labium and stylet length during the lanternfly development.

(A) Labium length changes, exponential model (y = 1465.57e^0.02x, R² = 0.49). (B) Stylet length changes, exponential model (y = 1326.1e^0.01x, R² = 0.43). Axis labels: Day, days of the lanternfly development; day 0, hatching of the 1^st nymphal instar; day 74, appearance of the adults (based on dates reported in Dara et al. [8]).

Fig 5. SEM of the last segment of labium of Lycorma delicatula at each developmental stage.

(A) First instar nymph. (B) Second instar nymph. (C) Third instar nymph. (D) Fourth instar nymph. (E) Adult female. (F) Adult male. Bars: (A), (C), (D), and (F) = 500 μm; (B) = 400 μm; (E) = 1 mm.

Fig 6. Size changes in the last labial segment of Lycorma delicatula across developmental stages.

(A) Last segment length. (B) Last segment width. Axis labels: 1–4, 1^st-4^th instar nymphs; a, adults.

Fig 7. Growth curves for the last labial segment during the lanternfly development.

(A) Last segment length, exponential model (y = 572.49e^0.01x, R² = 0.21). (B) Last segment width, exponential model (y = 167.33e^0.007x, R² = 0.16). Axis labels: Day, days of the lanternfly development; day 0, hatching of the 1^st nymphal instar; day 74, appearance of the adults (based on dates reported in Dara et al. [8]).

Fig 8. SEM of the labial tip of Lycorma delicatula (Third instar nymph).

(A) Sensory fields. DSF, dorsal sensory field; VSF, ventral sensory field. (B) and (D) Dorsal sensory field. CS, clavate sensilla; FS, forticate sensilla, FLS, finger-like sensilla; CP, cuticular process; PGSM, multiporous peg sensilla; PGS, peg sensilla; P, pore. (labeled following Hao et al. [12]). Bars: (A) = 50 μm; (B) = 30 μm; (C) = 40 μm; (D) = 10 μm.

Fig 9. SEM of bristle-like sensilla on the labial tip of Lycorma delicatula nymphs and adults.

(A) Third instar nymph, dorsal sensory field. (B) Fourth instar nymph, ventral sensory field. (C) Adult female, ventral sensory field. (D) Adult male, ventral sensory field. BRS1, long bristle-like sensilla; BRS2, short bristle-like sensilla. Bars: (A), (B), (C), and (D) = 50 μm.

Fig 10. SEM of the mandibular stylets of Lycorma delicatula at each developmental stage.

(A) First instar nymph. (B) Second instar nymph. (C) Third instar nymph. (D) Fourth instar nymph. (E) Adult female. (F) Adult male. OP, oval prominences; LS, longitudinal striations. Bars: (A) and (B) = 10 μm; (C) and (D) = 30 μm, (E) and (F) = 50 μm.

Fig 11. SEM of the maxillary stylets of Lycorma delicatula (second instar nymph).

FC, food canal; SC, salivary canal; ICs, interlocking canals (labeled following Hao et al. [12]). Bar: 40 μm.

Fig 12. SEM of the tarsal tips of the forelegs of Lycorma delicatula at each developmental stage.

(A) First instar nymph. (B) Second instar nymph. (C) Third instar nymph. (D) Fourth instar nymph. (E) Adult female. (F) Adult male. Ar, arolium; Tc, tarsal claw; Tsl, terminal sticky lip. Bars: (A) and (B) = 100 μm; (C) = 200 μm; (D) = 300 μm, (E) and (F) = 400 μm.

Fig 13. Distance between the tarsal claws of the forelegs of Lycorma delicatula across developmental stages.

(A) Distance between tarsal claw tips. (B) Distance between bending centers of the external arcs of the tarsal claws. Axis labels: 1–4, 1^st-4^th instar nymphs; a, adults.

Fig 14. Growth curves for the distance between the tarsal claws of the forelegs during the lanternfly development.

(A) Distance between tarsal claw tips, exponential model (y = 219.2e^0.02x, R² = 0.72). (B) Distance between bending centers of the external arcs of the tarsal claws, exponential model (y = 235.09e^0.02x, R² = 0.69). Axis labels: Day, days of the lanternfly development; day 0, hatching of the 1^st nymphal instar; day 74, appearance of the adults (based on dates reported in Dara et al. [8]).

Fig 15. SEM of the arolium surface of the forelegs of Lycorma delicatula at each nymphal stage.

(A) First instar nymph. (B) Second instar nymph. (C) Third instar nymph. (D) Fourth instar nymph. Bars: (A), (B), and (C) = 50 μm; (D) = 100 μm.

Fig 16. Distance between tarsal claws and arolium, and the angle of the arolium growth.

(A) Distance between tarsal claws and arolium. (B) Angle of the arolium growth. Axis labels: 1–4, 1^st-4^th instar nymphs; a, adults.

Fig 17. Growth curves for distance between tarsal claws and arolium, and the angle of the arolium growth during the lanternfly development.

(A) Distance between tarsal claws and arolium, exponential model (y = 17.11e^0.03x, R² = 0.76). (B) Angle of the arolium growth, quadratic model (y = 47.67–0.51x + 0.007 x², R² = 0.16). Axis labels: Day, days of the lanternfly development; day 0, hatching of the 1^st nymphal instar; day 74, appearance of the adults (based on dates reported in Dara et al. [8]).

Fig 18. The allometric relationship between the labium length and the distance between the tarsal claws relative to the lanternfly developmental stages.

(A) Original growth curves for the labium length (Lb1) and the distance between the tarsal claw tips (Tc1) (Lb1: y = 1465.57e^0.02x; Tc1: y = 219.2e^0.02x). (B) Growth curves for the labium length (Lb1) and the distance between the tarsal claw tips (Tc1) plotted on a log-log scale (Lb1: ln(y) = 7.46+0.29ln(x); Tc1: ln(y) = 5.34+0.34ln(x)). Axis labels: Day, days of the lanternfly development which correspond to the developmental stages; day 0, hatching of the 1^st nymphal instar; day 74, appearance of the adults (based on dates reported in Dara et al. [8]).