Next Article in Journal
Wireless Wave Attenuation in Forests: An Overview of Models
Previous Article in Journal
Heavy Nitrogen Application Rate and Long-Term Duration Decrease the Soil Organic Carbon and Nitrogen Sequestration Rates in Forest Ecosystems
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 15
Issue 9
10.3390/f15091586
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

An Examination of the Antennal Sensilla of the Oligophagous Moth Species Dioryctria sylvestrella (Lepidoptera: Pyralidae)

by
Qi Wang
1,2,3,†,
Yujia Ma
2,3,†,
Dun Jiang
2,3 and
Shanchun Yan
2,3,*
1
Forest Protection Research Institute of Heilongjiang Province, Heilongjiang Academy of Forestry, Harbin 150040, China
2
School of Forestry, Northeast Forestry University, Harbin 150040, China
3
Key Laboratory of Sustainable Forest Ecosystem Management, Ministry of Education, Northeast Forestry University, Harbin 150040, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2024, 15(9), 1586; https://doi.org/10.3390/f15091586
Submission received: 12 July 2024 / Revised: 10 August 2024 / Accepted: 2 September 2024 / Published: 10 September 2024
(This article belongs to the Section Forest Health)
Browse Figures
Versions Notes

Abstract

:
Dioryctria sylvestrella (Lepidoptera: Pyralidae) is a destructive borer pest on Korean pine (Pinus koraiensis) indigenous to northeastern China. The antennal sensilla of D. sylvestrella were examined by scanning electron microscopy to understand the behavioral ecology of this insect pest. Both the male and female antennae are filiform, and each consists of a scape, a pedicel, and a flagellum. D. sylvestrella is characterized by sexual dimorphism. Only the male antennae present two deeply grooved thumblike protuberances on the crest surfaces of their fourth and fifth flagellomeres, respectively. These structures have never been reported for any other Pyralidae. Eight different types of sensilla with unique bioecological functions were detected on the antennae of both sexes. There may be structure–location–function relationships for these sensilla, and most of them are involved in communication between the insect and the host plant, mate detection, and oviposition site selection.

1. Introduction

The moth Dioryctria sylvestrella (Ratzeburg, 1840) (Lepidoptera; Pyralidae) occurs in Europe and parts of Asia [1,2,3,4,5,6,7,8]. It is restricted to infesting the genus Pinus koraiensis with occasional damage to Picea spp. (Table 1) [4]. In northeastern China, D. sylvestrella is the main pest species affecting P. koraiensis [9]. The adult moth spawns on the female pinecones, and the larvae bore into them until September and overwinter in the tender main shoots [9]. If larvae succeed in girdling the tips of branches, single cones or clusters of cones may suffer from withering, resulting in a decrease in the yield and quality of seeds or increasing the risk of windbreak. Recently, Korean pine infestation with D. sylvestrella larvae has increased and ~90% of all trees in plantation forests have been injured by this insect pest.
Early work demonstrated that the infestation rate of D. sylvestrella is closely related to the composition of volatile substances [10]. D. sylvestrella adults are attracted to their host plants by the volatile organic compounds (VOCs) they produce and release [11]. The present study aimed to investigate the chemical ecology of D. sylvestrella and especially the antennal sensilla that enable it to recognize host plant VOCs and moth pheromones. Antennal sensilla are sensors that detect and respond to various chemicals and mechanical stimuli in the surrounding environment [12,13,14] and perform crucial roles in mate and host detection, oviposition site selection, and foraging [15]. The ultrastructural characteristics, number, and distribution of different sensillum types in both sexes were studied to document differences between females and males. In addition, the possible structural function of each kind of sensillum was also discussed. These data are important for ongoing studies on host plant-seeking and mate-finding behavior in D. sylvestrella and provide a theoretical foundation for further studies of semiochemical control for this pest.
Table 1. Distribution and host plants of D. sylvestrella.
Table 1. Distribution and host plants of D. sylvestrella.
ContinentContryHosts
Asia [16,17]China, South Korea, ThailandP. koraiensis (S. et Z.), Pinus densata (Masters), Pinus densiflora (S. et Z.), Pinus thunbergii (P.), Pinus rigida (M.), Pinus parviflora (S. et Z.),
Europe [18,19]France, Germany, United Kingdom, Finland, Austria, Italy, Norway, Indonesia, Portugal, Russia, TurkeyPinus pinaster (Ait), Pinus sylvestris (L.), Pinus nigra (Laricio), Pinus caribaea (Morelet), Pinus halepensis (Mill.). Pinus kesiya (Royle ex Gord.), Pinus merkusii (Jungh et De Vriese), Pinus pinea (L.), Pinus brutia (Ten.), Pinus strobus (L.), Pinus excelsa (Wall.), Pinus canariensis (C. Smith), Pinus eldarica (Medw.)
Picea orientalis (L.)

2. Materials and Methods

2.1. Insects

In early May, mature D. sylvestrella larvae and pupae are encased in a cocoon composed of feces and resin. The branches of P. koraiensis bearing D. sylvestrella cocoons were collected from Diaoling forest in Linkou Town, Mudanjiang City, Heilongjiang Province, China. The red point indicates the location of the collection of material for research (Figure 1). The branches were excised from the trees, transferred to an insectary (Yinxi Instrument Co., Ltd., Shanghai, China), and incubated in a nylon net at 27 ± 3 °C. The net was misted with water daily. The emerging moths were fed sugar water once daily. The research team identified their COI genes and deposited the DNA barcode in the National Center for Biotechnology Institute (NCBI) database [20].

2.2. Specimen Preparation for Scanning Electron Microscopy (SEM)

Male and female antennae were rapidly excised and soaked in 2.5% (v/v) glutaraldehyde (Sigma-Aldrich, St. Louis, MO, USA) at 4 °C for 2 d to denature their proteins. The samples were first washed with alcohol in an ultrasonic bath (Jingbao Ultrasonic Technology Co., Ltd., Hangzhou, China) for 5 s. The antennae were progressively dehydrated using 50%, 70%, 80%, 90%, 95%, 100%, and 100% (v/v) ethanol for 5 min per step. After complete drying, the samples were glued onto the sample stages and plated with gold for 300 s using an ion sputtering coating instrument (Gressington 108 auto, Ted Pella, CA, USA). Subsequently, the antennae samples were examined under an FEI QUANTA 200 SEM (Thermo Fisher Scientific, Waltham, MA, USA) at 15 kV.

2.3. Nomenclature and Statistical Analysis

Micrographs of the antennae were taken, their shape and composition were examined, and the sensilla length, diameter, pattern, and distribution were measured for each flagellomere via Motic Images Advanced v. 3.2 (Motic Asia, Kowloon, Hong Kong, China). At least 30 of each type of sensillum from at least five moths of the same sex were measured to calculate the means. Differences between sexes were analyzed by t-test (p < 0.05) in SPSS v. 16.0 (IBM Corp., Armonk, NY, USA). Sensilla nomenclature was based on the methodology of Schneider (1964) [21]. The types of sensilla on the D. sylvestrella antennae were identified following the procedure of Callahan (1975) [22]. The antennal sensilla morphology of D. sylvestrella was compared against those of other pyralids [16,23,24].

3. Results

3.1. General Morphology and Types of Antennal Sensilla of D. sylvestrella

Both D. sylvestrella sexes have filiform (threadlike) antennae (Figure 2a). Each of these consists of a scape (S), a pedicel (P), and a flagellum (F). The pedicels are shorter and thinner than the scapes (Figure 2a). For the females and males, the mean lengths of the scapes and pedicels were 200.00 ± 18.60 µm and 140.00 ± 1.70 µm, respectively (N = 6), and 356.56 ± 22.20 µm and 153.65 ± 7.10 µm, respectively) (N = 6) (Table 2). There were 61 flagellar subsegments or flagellomeres in each long filiform flagellum of both sexes. However, females had significantly longer flagella (7834.16 ± 81.80 μm) compared to males (7027.31 ± 188.60 μm) (N = 6) (Table 2). Hence, some of the flagellomeres were longer in the female than in the male antennae. The mean female and male antenna lengths were 8174.16 ± 110.20 µm and 7536.52 ± 372.80 µm, respectively (N = 6) (Table 2).
The entire dorsal sides of the male and female antennae were covered with scales (Figure 2b–d), whereas the ventral side had sensilla trichodea (ST) and sensilla styloconica (SSt) at the end of each flagellomere (Figure 2c). Certain sensilla were localized to the scales on the dorsal surfaces of the flagella. Nevertheless, we focused on the ventral sensilla lacking scales as they were abundant and readily visible in the SEM images.
The male moths presented deeply grooved thumblike protuberances on the crest surfaces of their fourth and fifth flagellomeres (Figure 2e). On the fourth flagellomeres, these protuberances were 90.0 ± 3.2 µm long and 15.0 ± 1.9 µm wide (N = 5) wide. On the fifth flagellomeres, they were 150.0 ± 1.8 µm long and 25.0 ± 0.8 µm wide (N = 5). All protuberances had wrinkled cuticles and no observable sensilla (Figure 2e(e1,e2). The detection of these structures in the Pyralidae is unprecedented.

3.2. External Morphology of the Antennal Sensilla of D. sylvestrella

The major types of sensilla observed here were sensilla trichodea (ST), s. chaetica (SCh), s. coeloconica (SCo), s. styloconica (SSt), s. auricillica (SA), s. furcatea (SF), s. squamiformia (SSq), and Böhm bristles (BB). Figure 3 shows the distributions of all sensilla types on all flagellomeres except the Böhm bristles on the pedicels.

3.2.1. Sensilla Trichodea (ST)

Sensilla trichodea were the most abundant on the ventral surfaces of both the male and female D. sylvestrella antennal flagellomeres. ST occupied ~2/3 of the circumference of each flagellomere except for the scale-covered part. ST had two different sizes. The longer type was designated “ST-A” (Figure 4a). The lengths and basal widths were in the ranges of 69.59–92.15 ± 0.80 µm (N = 5) and 4.00–5.26 ± 0.20 µm (N = 5), respectively. The shorter type was designated “ST-B” and localized to the medial areas of the flagellomeres (Figure 4a). The bases were curved and the tips were directed towards those of the antennae. The main part of ST-B ran parallel to the flagellar cuticle. The lengths and basal widths were in the ranges of 32.22–47.59 ± 1.20 µm (N = 5) and 1.6–2.7 μm, respectively.
Trichoid ST-A and ST-B had transverse ridges on the entire lengths of their portions that were visible in most SEM images (Figure 4b). However, certain SEM views indicated that there were no ridges on the basal regions (Figure 4a). Preliminary TEM imaging showed three unbranched dendrites in certain STs, and these occurred more frequently on the flagellomeres of the female than the male moths (Figure 2c,d).

3.2.2. Sensilla Coeloconica (SCo)

Sensilla coeloconica were localized to the ventromedial areas of the flagellomeres and usually under the ST (Figure 5a). SCo sensilla had cuticular spines [25] that closed over the central double-walled sensillar “peg” (Figure 5a). One of the cuticular spines that had been cut open revealed that the double-walled peg is not a true terminal pore. The peg comprises solid, fingerlike cylindrical cuticular structures that fuse to form “slit-pores” along the length of the sensillum [25] (Figure 5b). The pegs were situated in cuticular pits or depressions with diameters in the range of 10–25 μm (N = 10) (Figure 5b). The mean length and basal width of the central peg were 6.0 ± 0.2 µm (N = 10) and 2.5 ± 0.2 µm (N = 10), respectively (Figure 5b). The basal diameters of the cuticular spines surrounding the pit were in the range of 4.5–5.1 μm (N = 10) (Figure 4b). The cuticular spines were open in one SCo (Figure 5c). The length and basal width of the peg in this sensillum were 4.8 μm and 2.4 μm, respectively (Figure 5c). The females had nearly twice as many SCo per flagellum (N = 10) as the males (N = 10).

3.2.3. Sensilla Auricillica (SA)

Sensilla auricillica were distributed on the ventromedial surface of each flagellomere (Figure 6a). They were elongated, rounded, and flattened and their shape resembled a shoehorn [26]. They tapered apically and had a slightly concave upper surface. The SA of D. sylvestrella had pointed apical tips (Figure 6a–c). Certain SA were broader and rounder than others (Figure 6b). However, none of them presented the entirely rounded-ended “rabbit-eared” shape characteristic of certain SA detected in the codling moth (Cydia pomonella) by Ebbinghaus et al. (1998) [26]. Each of the more rounded SA of D. sylvestrella tapered to a point at the apex. In both sexes, each flagellomere had 4–7 SA (N = 10). The lengths and mid-sensillar widths of the SA were in the ranges of 16.67–25.86 μm and 3.84–7.40 μm, respectively. The bases of most SA emerged from one of many honeycombed cuticular structures on the flagellar surface, and no sockets were visible. The bases of the SA were bent such that their main part lay nearly flat and parallel to the flagellar cuticle (Figure 6a,c). The broader SA projected almost vertically out of the flagellar surface (Figure 6b) and their surfaces had a ridged pattern (Figure 6b). Preliminary TEMs revealed numerous pores on the cuticles of certain SA.

3.2.4. Sensilla Furcatea (SF)

The shape of the sensilla furcatea resembled that of SA. SF had a wide concave upper surface (Figure 6c). Unlike SA, however, SF had a bifurcated apical tip (Figure 6d). The lengths and widths of SF were in the ranges of 18.08–19.47 μm (N = 6) and 3.15–3.78 μm (N = 6), respectively. SF were distributed on the ventromedial portion of each flagellomere and concomitantly with SA. SF occurred on the antennae of both male and female D. sylvestrella (Figure 6c).

3.2.5. Sensilla Styloconica (SSt)

Sensilla styloconica were robust in appearance and heavily reinforced with cuticular patterned ridges in their basal regions. They had pointed nipple-like tips projecting from their thicker cylindrical foundations (Figure 7a,b). A single SSt-like branch extended from the ventral end of each flagellomere and projected from a proximal flagellomere towards a distal one (Figure 2c). Groups of at least two SSt clustered at the tips of the terminal flagellomeres (Figure 7b). The basal cuticular ridge pattern of each SSt often had a honeycombed appearance (Figure 7a,b) that resembled the texture of the entire cuticular surface of each flagellum (Figure 7a,b). The surfaces of the distal parts of SSt were smooth (Figure 7a,b). The lengths and widths of SSt were in the ranges of 16.67–21.73 μm (N = 10) and 5.44–7.40 μm (N = 10), respectively. The honeycomb structures of certain SSt at the tips of the antennae had small holes. In contrast, the SSt on other flagellomeres lacked these perforations (Figure 7a,b). These holes might be dimpled cuticular substructures rather than true olfactory pores.

3.2.6. Sensilla Chaetica (SCh)

Sensilla chaetica were sparsely distributed across the ventral and dorsal flagellomeres of male and female antennae (Figure 8a). Removal of the dorsal scales of certain flagellomeres disclosed that SCh were also thinly spread across the dorsal surfaces (Figure 8a). Most specimens had six or fewer SCh per flagellomere. Nevertheless, the terminal male and female flagellomeres had ~12 SCh arranged in a circle (Figure 8b). A few other SCh sometimes occurred more proximally on these flagellomeres (Figure 8b).
The base of each SCh arose from one of thousands of hexagonal structures on the cuticular surfaces (Figure 8c). Each SCh had a robust basal part and tapered and curved toward the blunt apical tip (Figure 8a–c). SCh were corrugated along 2/3 of their length until their apices and their bases had corn-cobbed ridges. The heights and widths of the raised sockets were in the ranges of 1.80–2.81 μm and 4.15–5.92 μm (N = 10), respectively. The lengths and widths of the SCh “hairs” were in the ranges of 27.40–38.33 μm and 2.12–2.96 μm, respectively.

3.2.7. Sensilla Squamiformia (SSq)

Sensilla squamiformia exhibited surfaces resembling the leaves of certain Gramineae (Poaceae; grasses) and tapered apically. Their surface textures and shapes resembled very narrow scales (Figure 8a,d). These structures were readily observed both medially and laterally at the junctures of the dorsal scales and ventral areas. It was necessary to excise certain scales to view these structures. The lengths and widths of the SSq were in the range of 40.00–64.44 μm and maximum ~5 μm, respectively.

3.2.8. Böhm Bristles (BB)

Böhm bristles (BB) were short and spine-like. Their lengths and widths were in the ranges of 12.97–15.14 μm (N = 10) and 2.00–2.15 μm (N = 10), respectively (Figure 9a,b). About 20 BB were detected for every five or more moths. The BB were clustered in the ventral joints of the pedicel and their cusps were directed towards the scape sockets.

4. Discussion

D. sylvestrella is an insect of the genus Dioryctria in the Pyralidae family of Lepidoptera. The antennae of both male and female D. sylvestrella were filiform (threadlike), and their structure resembled those of the antennae of other adult pyralid borer moth species (Table 3) [16,23,24,27,28,29,30,31,32,33,34,35,36]. In both sexes, the entire dorsal sides of the flagella were covered by scales. Certain types of sensilla were either beside or below the scales. It was suggested that this configuration of sensilla and scales enabled the antennae to trap and concentrate odor molecules as they enter the sensilla pores [37]. The scales might also direct and orient the moths by sensing air currents in a manner resembling how scales help fish perceive water flow [38]. The scales ascended from a cavity structure. To facilitate sensilla analysis, we dehisced some of the scales and observed the cavity structure of D. sylvestrella antennae under SEM. Sun et al. (2011) reported “sensilla cavity” structures on Cnaphalocrocis medinalis (Guenee) antennae [31]. They proposed that the sensilla cavity traps water molecules, prevents desiccation, and perceives both humidity and temperature. Here, however, we observed that the cavity structures exposed when certain scales were removed from the D. sylvestrella antennae resembled the sensilla cavities of C. medinalis antennae. Similar cavity structures were reported for the antennae of other pyralids including Zamagiria dixolophella (Dyar) and Plodia Interpunctella (Hubner). Nevertheless, the authors never specified the types of sensilla they detected in these cavities [24,33]. We inferred that the sensory cavities were located below the antennal surfaces and enabled the information obtained by the scales to enter the antennae. Hence, this sensory perception mechanism could discern the suitability of any surface for the insect.
Castrejón-Gómez et al. (2003) observed a spikelike protuberance on each of the first seven flagellomeres under the hair scales of male Z. dixolophella antennae. This configuration was not detected on the antennae of any other Pyralidae and is considered a trait of sexual dimorphism [24]. Nevertheless, sexual dimorphism was detected in the antennae of D. sylvestrella. In the male (but not the female) antennae, thumblike protuberances with deep dorsal grooves extended from the hind portions of the fourth and fifth flagellomeres. These projections were larger than the spikelike protuberances on Z. dixolophella antennae and lacked scale tufts. The functions of both types of protuberances are unknown, and neither has been found on the antennae of any other Pyralidae. Castrejón-Gómez et al. (2003) also suggested that as these structures were unique to male moth antennae, and they might be implicated in male courtship behavior [24]. In addition, in Table 3, sexual dimorphism between females and males presented different numbers and types of sensilla observed in the antennae of adults of D. sylvestrella and other moths, such as Homoeosoma nebulella (Den. and Schiff.) [23], P. interpunctella [33], and Tirathaba rufivena (Walk.) [34]. Among them, the T. rufivena adult antennal sensilla SB was larger in size and number in females than in males, and SA was significantly more abundant in females [34]. Similar to ST-A and ST-B on the female antennae of D. sylvestrella, they were more abundant than on the male.
The sensilla of adult females and males of Pyralidae are generally 6–8 in number. Among these, the Pyralidae adult sensilla ST, SA, and SSt would have different subtypes (Table 3), and this phenomenon is quite common on Lepidoptera antennae. Here, we identified a longer “ST-A” and a shorter “ST-B” in both male and female D. sylvestrella antennae. The cuticles on the single walls of ST had numerous small pores and channels through which odor molecules could enter the lumens and thence the olfactory dendrites [39]. Maitani et al. (2010) used atomic force microscopy (AFM) to delineate ST topography in Helicoverpa zea (Boddie) and Utethesia ornatrix (L.). The authors proposed that the ridges on male ST were always associated with pores [40]. All of our SEM images except those of the short basal portion revealed transverse ridges along the entire lengths of both ST subtypes in male and female D. sylvestrella antennae. Hence, these structures had an olfactory function. Male moths use pheromones to locate females. Certain physiologically unique ST subtypes on male moth antennae contain a pheromone-sensitive olfactory complex. The antennae of male Ostrinia nubilalis (Hubner) displayed three different ST subtypes. The longest of these was type-A and it consisted of three cells. Two of these responded to different pheromone constituents while the third responded to a behavioral antagonist. Type-B contained two cells, of which, one detected pheromones while the other perceived a behavioral antagonist. Type-C comprised a single cell detecting both a pheromone and a behavioral antagonist [16]. Male Chilo partellus (Swinhoe) moths had three morphologically distinct ST subtypes innervated by one to three sensory cells. In type I, both pheromone components and pheromone-like compounds elicited strong responses in a single receptor neuron while other receptor neurons detected non-specific pheromones. Type II ST only responded to a single pheromone component. Female moth ST monitor VOCs at spawning sites [41]. Female O. nubilalis did not respond to pheromone components extracted from female glands. The aromatic and terpenoid odorant compounds released by host plants stimulated the shorter ST of Manduca sexta (L.) [25]. For D. sylvestrella, ST-A and ST-B were more abundant on the female than on the male antennae. Castrejón-Gómez et al. (2003) conjectured that the long ST on female antennae detect homogeneous pheromones [24]. By this mechanism, competition may be avoided among conspecific Helicoverpa zea females [42]. Female Choristoneura fumiferana (Clemens) detected pheromone components to determine whether the immediate environment was conducive to spawning [43]. Hansson et al. (1994) suggested that ST may also be classified using electrophysiological and electron microscopy techniques [44]. Sexual antenna dimorphism in D. rubella was the opposite of that in D. sylvestrella [27].
The unique external morphology of SCo readily distinguishes them from other sensilla. They have cuticular spines that form a “fence” enclosing the central double-walled sensillar “peg”. Most of the SCo on both male and female D. sylvestrella antennae consisted of pegs surrounded by fused cuticular fingers. However, the females presented a single open SCo lacking any “fence”. The antennae of several different moth species such as Synempora andese (Davis and Nielsen) have only a single SCo type exclusively with open pegs [45]. However, the antennae of other moth species have SCo with pegs surrounded by fused cuticular fingers [33]. The antennae of still other moth species bear two types of SCo [31,46]. The antennal flagella of female D. sylvestrella had more fingers surrounded by SCo than those of male D. sylvestrella. However, this configuration differed for the antennae of C. medinalis [31]. We speculated that in D. sylvestrella antennae, SCo enable females to find spawning grounds. An earlier study reported that SCo responded to plant VOCs [47]. However, as SCo pegs are located in pits and are far shorter than those of other single-walled wall-pore olfactory sensilla, the former have relatively lower odor molecule capture efficacy. Hunger and Steinbrecht (1998) proposed that SCo may respond to comparatively higher odorant concentrations because double-walled wall-pore sensilla have spike channels [47]. Guo et al. (2014) confirmed that the olfactory sensory neurons in the SCo of Schistocerca gregaria (Forskal) responded to different VOCs than those in sw-wp sensilla [48]. The SCo of Aedes aegypti (L.) have thermoreceptive cells while those of Periplaneta americana (L.) also bear cells that detect humidity. The latter have never been reported for moths. SCo may also be able to monitor carbon dioxide and prevent dehydration by detecting moisture [31,47,49,50,51,52].
SA are common in pyralids and were observed in both male and female D. sylvestrella antennae [16,23,32]. Several euryphagous lepidopteran moths such as Cydia pomonella (L.) and Spodoptera exigua (Hübner) also have SA [53]. These sensilla range in appearance from raisin-shaped to ear-shaped [54]. Unlike the antennae of D. sylvestrella, those of most other moth species do not possess multiple forms of SA. The antennae of D. sylvestrella harbor mainly elongated SA whereas other sensilla auricillica in D. sylvestrella antennae are broad and have rounded bases. Nevertheless, all SA in D. sylvestrella antennae have slightly concave upper surfaces and pointed apical tips. Our SEM images revealed slight vertical ridges on the surfaces of the SA in D. sylvestrella antennae. Maitani et al. (2010) stated that pores often accompanied these ridges. Hence, it is expected that the surfaces should be porous as well [40]. It was previously suggested that SA are involved in plant odor detection as their cuticles are perforated [55,56]. SA may also detect host plant odor molecules in Scoliopteryx libatrix (L.) [57]. C. Pomonella antennae possess two SA subtypes with three to four olfactory receptor neurons (ORNs) per sensillum. Single-cell recordings disclosed that SA responded to various plant VOCs that stimulated three excitatory responses in the SA neurons [58]. Van der Goes van Naters et al. (1998) postulated that SA may participate in sound wave and mechanical reception [59].
Sensilla furcatea were observed in the antennae of both D. sylvestrella sexes. Yang (2009) detected only two SF on the antennae of female Coleophora obducta (Meyrick) and they were sporadically distributed there [60]. We observed that SF and SA had similar external morphology, and they were separately distributed on the ventral surfaces of the flagella. TEM and electrophysiological recording analyses are required to determine whether they have similar functions.
We observed SSt in the antennae of both male and female D. sylvestrella. Each SSt protruded from the ventral edge of the antennal segment and had a smooth tubular body. In contrast, the terminal SSt on the apical antennal segments had overlapping curved and porous bodies. SSt may be bimodal gustatory and mechanical sensilla. Jefferson et al. (1970) proposed that the terminal pores on SSt might play a role in contact reception [61]. Here, we noticed that adult D. sylvestrella would touch the sugar water with their apical antennal segments as they contained terminal SSt. In this manner, the moths would taste the food before siphoning it. SSt may also enable insects to detect potential toxins in food sources [62]. The SSt at the ventral edges of the antennae can sense mechanical pressure during antenna curling. The SSt in Pyralidae may also be sensitive to heat and humidity [44]. Takács et al. (2008) indicated that adult borer moths can perceive infrared [63].
SCh were regularly arranged on both male and female D. sylvestrella antennae. Each antennal segment had SCh that were widely distributed across the dorsal surface, and ~12 SCh were arranged in a circular fashion on the terminal flagellomere. Similar SCh and SSt distribution patterns were reported for the antennae of P. interpunctella and Z. dixolopella [24,33]. Therefore, both SCh and SSt may have similar sensory functions. Altner et al. (1977) proposed that SCh detect taste and sense touch as they have pores on their tips and flexible sockets around their bristle bases [64]. SCh might be part of a gustatory system, enabling moths to identify their host plants, discriminate potential food sources, and find suitable oviposition sites [23,65]. We found that this circular sensilla configuration was common to the antennae of various moth species. Schneider (1964) suggested that SCh might be implicated in proprioception [16,21,22,23,24,30,65].
SSq resemble slender scales and are uniformly distributed among the scales on D. sylvestrella antennae. Yu (2004) proposed that SSq are involved in mechanoreception [66]. Yang (2009) mentioned that SSq may protect the antenna termini [60]. Here, we identified S. squamiformia on the antennae of both D. sylvestrella sexes. As SSq are widely dispersed along the antennal surfaces, they could detect changes in environmental and barometric pressure in addition to protecting the antenna termini.
Ma and Du (2000) observed Böhm bristles on the scapes and pedicels but never on the flagella of moth antennae [67]. Cuperus (1983) offered that BB are cuticular acceptors that perceive the mechanical pressure created by scape or pedicel rotation [68]. Li and Bai (2004) indicated that BB are gravity receptors that help spatially orient moths [69].

5. Conclusions

Our study revealed a sexual dimorphism with respect to the types, numbers, and distributions of sensilla of D. sylvestrella. Especially, the male antennae present two deeply grooved thumblike protuberances on the crest surfaces of their fourth and fifth flagellomeres. This knowledge will help us to confirm that the functions of antennae on male and female moths play different roles in mediating sexual and host-finding behavior. The foregoing analyses of the sensilla in D. sylvestrella antennae laid the foundation for elucidating the mechanisms of behavioral and electrophysiological communication between D. sylvestrella and the host plant. These structures in the sensory perception of borer moths are important for ongoing studies of semiochemical control for this pest.

Author Contributions

Conceptualization, S.Y.; methodology, Q.W. and Y.M.; validation, Q.W., D.J. and S.Y.; investigation, Q.W. and D.J.; data curation, Q.W. and Y.M.; writing—original draft preparation, Q.W. and Y.M.; writing—review and editing, S.Y.; visualization, D.J. and Y.M.; supervision, S.Y.; funding acquisition, Q.W. and S.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, grant number 32301605 and the Key Research and Development Projects in Heilongjiang, grant number 2023ZX02B05.

Data Availability Statement

All the data that support the findings of this study are available in the manuscript.

Acknowledgments

We thank Yong Zhi Cui (Northeast Forestry University, Harbin, Heilongjiang Province, China) for helping with SEM. We gratefully acknowledge Thomas C. Baker (Distinguished Professor of Entomology and Chemical Ecology Research, Department of Entomology The Pennsylvania State University 105 Chemical Ecology Laboratory University Park, PA 16802) for his effort in revision.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Piao, M.H.; Chen, X.X.; Lee, C.Y. The morphology of mature larvae of three species injurious to red pine cone from Korea (Lepidoptera). Acta Entomol. Sin. 2002, 45, 371–376. [Google Scholar]
  2. Jactel, H.; Goulard, M.; Menassieu, P.; Goujon, G. Habitat diversity in forest plantations reduces infestations of the pine stem borer Dioryctria sylvestrella. J. Appl. Ecol. 2002, 39, 618–628. [Google Scholar] [CrossRef]
  3. Jactel, H.; Kleinhentz, M.; Raffin, A.; Menassieu, P. Comparison of different selection methods for the resistance to Dioryctria sylvestrella Ratz. (Lepidoptera: Pyralidae) in Pinus pinaster Ait. Colloq. Linra. 1999, 90, 137–149. [Google Scholar]
  4. Jactel, H.; Menassieu, P.; Raise, G. Infestation dynamics of Dioryctria sylvestrella (Ratz.) (Lepidoptera: Pyralidae) in pruned maritime pine (Pinus pinaster Ait.). For. Ecol. Manag. 1994, 67, 11–22. [Google Scholar] [CrossRef]
  5. Kleinhentz, M.; Jactel, H.; Menassieu, P. Terpene attractant candidates of Dioryctria sylvestrella in maritime pine (Pinus pinaster) oleoresin, needles, liber, and headspace samples. J. Chem. Ecol. 1999, 25, 2741–2756. [Google Scholar] [CrossRef]
  6. Parsons, M.S.; Radford, J. Dioryctria sylvestrella (Ratzeburg, 1840) (Lepidoptera: Pyralidae) new to Britain. Entomol. Gazette. 2002, 53, 137–142. [Google Scholar]
  7. Öz, M.; Deniz, İ.; Okan, O.T.; Fidan, M.S. Chemical composition of oleoresin and larvae gallery resin of Pinus brutia attacked by Dioryctria sylvestrella Ratz. Drv. Ind. 2015, 66, 179–188. [Google Scholar] [CrossRef]
  8. Avci, M.; Bilener, M. Damage, biology and natural enemies of pine stem borer Dioryctria sylvestrella (Ratzeburg) (Lepidoptera: Pyralidae) in Lake’s District forests. Türk. Entomol. Bült. 2016, 6, 131–141. [Google Scholar] [CrossRef]
  9. Xu, B.; Yan, S.C.; Nie, W.L.; Wang, Y.L. A complementary study on biological characteristics of two species of Dioryctria (Lepidoptera: Pyralidae) and their damage to cones and twigs of Korean pine. Sci. Silvae Sin. 2010, 46, 79–85. [Google Scholar]
  10. Jactel, H.; Kleinhentz, M.; Marpeau-Bezard, A.; Marion-Poll, F.; Menassieu, P.; Burban, C. Terpene variations in maritime pine constitutive oleoresin related to host tree selection by Dioryctria sylvestrella RATZ. (Lepidoptera: Pyralidae). J. Chem. Ecol. 1996, 22, 1037–1050. [Google Scholar] [CrossRef]
  11. Wang, Q.; Yan, S.C.; Xu, B. Two Dioryctria species with different durvival strategies to adapt to chemical defense of host plant Pinus koraiensis. Sci. Silvae Sin. 2012, 48, 79–85. [Google Scholar]
  12. Steinbrecht, R.A. Zur morphometrie der antenne des seidenspinners, Bombyx mori L.: Zahl und verteilung der riechsensillen (Insecta, Lepidoptera). Z. Morphol. Tiere 1970, 68, 93–126. [Google Scholar] [CrossRef]
  13. Keil, T.A. Comparative morphogenesis of sensilla: A review. Int. J. Insect Morphol. Embryol. 1997, 26, 151–160. [Google Scholar] [CrossRef]
  14. Keil, T.A. Morphology and development of the peripheral olfactory organs. In Insect Olfaction; Hansson, B.S., Ed.; Springer: Berlin/Heidelberg, Germany, 1999; Volume 1, pp. 5–47. [Google Scholar]
  15. Derby, C.D.; Steullet, P. Why do animals have so many receptors? The role of multiple chemosensors in animal perception. Biol. Bull. 2001, 200, 211–215. [Google Scholar] [CrossRef] [PubMed]
  16. Hallberg, E.; Hansson, B.S.; Steinbrecht, R.A. Morphological characteristics of antennal sensilla in the European corn borer Ostrinia nubilalis (Lepidoptera: Pyralidae). Tissue Cell 1994, 26, 489–502. [Google Scholar] [CrossRef]
  17. Byun, C.S.; Kim, C.S.; Kim, J.K. Taxonomic Notes of Dioryctria abietella and D. sylvestrella (Lepidoptera: Pyralidae) in Korea. ResearchGate 1998, 59, 76–82. [Google Scholar]
  18. Menassieu, P.; Stockel, J.; Levieux, J. Données actuelles sur la biologie de Dioryctria sylvestrella (Ratz.) (Lep., Pyralidae) ravageur du Pin maritime (Pinuspinaster Ait) dans le Sud Ouest de la France. J. Appl. Entomol. 1989, 107, 238–247. [Google Scholar] [CrossRef]
  19. Oguzhan, S.; Yilmaz, C. Effects of Dioryctria sylvestrella (Ratzeburg, 1840) on Basal Area Increment Loss of the young Brutian pine (Pinus brutia Ten.) Trees in the south-western of Turkey. Res. J. Biotechnol. 2014, 9, 24–28. [Google Scholar]
  20. Lu, M.; Xie, D.; Song, X.; Chi, D. Identification of Dioryctria species boring Pinus koraiensis and P. sylvestris var. mongolica with COI gene dequences and morphological characteristics. J. Northeast. Agric. Univ. 2020, 48, 83–87. [Google Scholar]
  21. Schneider, D. Insect antennae. Annu. Rev. Entomol. 1964, 9, 103–122. [Google Scholar] [CrossRef]
  22. Callahan, P.S. Insect antennae with special reference to the mechanism of scent detection and the evolution of the sensilla. Int. J. Insect Morphol. Embryol. 1975, 4, 381–430. [Google Scholar] [CrossRef]
  23. Faucheux, M.J. Morphology and distribution of sensillaon the cephalic appendages, tarsi and ovipositor ofthe European sunßower moth, Homoeosoma nebulella Den. and Shiff. (Lepidoptera: Pyralidae). Int. J. Insect Morphol. Embryol. 1991, 20, 291–307. [Google Scholar] [CrossRef]
  24. Castrejón-Gómez, V.R.; Nieto, G.; Valdes, J.; Castrejón, F.; Rojas, J.C. The antennal sensilla of Zamagiria dixolophella Dyar (Lepidoptera: Pyralidae). Ann. Entomol. Soc. Am. 2003, 96, 672–678. [Google Scholar] [CrossRef]
  25. Shields, V.D.C.; Hildebr, J.G. Fine structure of antennal sensilla of the female sphinx moth, Manduca Sexta (Lepidoptera, Sphingidae) I. Auriculate, coeloconic, and styliform complex sensilla. Can. J. Zool. 1999, 77, 302–313. [Google Scholar] [CrossRef]
  26. Ebbinghaus, D.; Lösel, P.M.; Lindemann, M.; Scherkenbeck, J.; Zebitz, C.P. Detection of major and minor sex pheromone components by the male codling moth Cydia pomonella (Lepidoptera: Tortricidae). J. Insect Physiol. 1998, 44, 49–58. [Google Scholar] [CrossRef]
  27. Xu, J.; Deng, C.; Lu, W.; Wu, S. Ultrastructure Of Antennal Sensilla In Adults Of Dioryctria Rubella Hampson (Lepidoptera: Pyralidae). Insects 2021, 12, 821. [Google Scholar] [CrossRef]
  28. Jin, X.; Wang, H.Y.; Hu, Z.L.; Ma, M.R.; Li, J.Q.; Cui, J.Z. Observation on antenna of Dioryctria rubella Hampson (Lepidoptera: Pyralidae) with scanning electron microscopy. J. Environ. Entomol. 2021, 43, 40–47. [Google Scholar]
  29. Yang, L.J.; Li, X.G. Scanning Electron Microscopy Observation on Antennal Sensilla of Dioryctria pryeri Ragonot. J. Northwest For. Univ. 2007, 22, 132–135. [Google Scholar]
  30. Cornford, M.E.; Rowley, W.A.; Klun, J.A. Scanning Electron Microscopy of Antennal Sensilla of the European Corn Borer, Ostrinia nubilalis. Ann. Entomol. Soc. Am. 1973, 66, 1079–1088. [Google Scholar] [CrossRef]
  31. Sun, X.; Wang, M.Q.; Zhang, G. Ultrastructural observations on antennal sensilla of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). Microsc. Res. Tech. 2011, 74, 113–121. [Google Scholar] [CrossRef]
  32. Honda, H.; Hanyu, K. Scanning electron microscopy of antennal sensilla of the yellow peach moth, Conegethes punctiferalis (Guenèe) and Conegethes sp. (Lepidoptera: Pyralidae). Jpn. J. Appl. Entomol. Zool. 1989, 33, 238–246. [Google Scholar] [CrossRef]
  33. Ndomo-Moualeu, A.F.; Ulrichs, C.; Radek, R.; Adler, C. Structure and distribution of antennal sensilla in the Indian meal moth, Plodia interpunctella (Hübner, 1813) (Lepidoptera: Pyralidae). J. Stored Prod. Res. 2014, 59, 66–75. [Google Scholar] [CrossRef]
  34. Jixing, G.; Zimeng, D.; Guangchao, C.; Zheng, W.; Junfang, W.; Xiang, Z. Ultrastructure Characteristics and Sexual Dimorphism of Antennal Sensilla in Tirathaba rufivena (Lepidoptera: Pyralidae). Insects 2022, 13, 797. [Google Scholar] [CrossRef] [PubMed]
  35. Kasomhung, C.L.N.; Khirod, S.D.; Cynthia, B.M.; Joycy, M.K.; Sudipta, C. Scanning electron microscopy study of the antennal sensilla of cob borer, Stenachroia elongella (Lepidoptera: Pyralidae). Microsc. Res. Tech. 2023, 86, 556–564. [Google Scholar]
  36. Hansson, B.S.; Blackwell, A.; Hallberg, E.; Löfqvist, J. Physiological and morphological characteristics ofthe sex pheromone detecting system in male corn stemborers, Chilo partellus (Lepidoptera: Pyralidae). J. Insect Physiol. 1995, 41, 171–178. [Google Scholar] [CrossRef]
  37. Wall, C. Morphology and histology of the antenna of Cydia nigricana (F.) (Lepidoptera: Tortricidae). Int. J. Insect Morphol. Embryol. 1978, 7, 237–250. [Google Scholar] [CrossRef]
  38. Van der Pers, J.N.C.; Den Otter, C.J. Single cellresponses fromolfactory receptors of small ermine moths (Lepidoptera: Yponomeutidae) to sex attractants. J. Insect Physiol. 1978, 24, 337–343. [Google Scholar] [CrossRef]
  39. Liu, Z.; Hu, T.; Guo, H.W.; Liang, X.F.; Cheng, Y.Q. Ultrastructure of the olfactory sensilla across the antennae and maxillary palps of Bactrocera dorsalis (Diptera: Tephritidae). Insects 2021, 12, 289. [Google Scholar] [CrossRef]
  40. Maitani, M.M.; Allara, D.L.; Park, K.C.; Lee, S.G.; Baker, T.C. Moth olfactory trichoid sensilla exhibit nanoscale-level heterogeneity in surface lipid properties. Arthropod Struct. Dev. 2010, 39, 1–16. [Google Scholar] [CrossRef]
  41. Yu, J.; Yang, B.; Chang, Y.; Zhang, Y.; Wang, G. Identification of a general odorant receptor for repellents in the asian corn borer Ostrinia furnacalis. Front. Physiol. 2020, 11, 176–185. [Google Scholar] [CrossRef]
  42. Saad, A.D.; Scott, D.R. Repellency of pheromonesreleased by females of Heliothis armigera and H. zea to females of both species. Entomol. Exp. Appl. 1981, 30, 123–127. [Google Scholar] [CrossRef]
  43. Palanaswamy, P.; Seabrook, W.D. Behavioral responsesof the female eastern spruce budworm Choristoneura fumiferana (Lepidoptera: Tortricidae) to the sexpheromone of her own species. J. Chem. Ecol. 1978, 4, 649–655. [Google Scholar] [CrossRef]
  44. Hansson, B.S.; Hallberg, E.; Lofstedt, C.; Steinbrecht, R.A. Correlation between dendrite diameter and action potential amplitude in sex pheromone specific receptor neurons in male Ostrinia nubilalis (lepidoptera: Pyralidae). Tissue Cell 1994, 26, 503–512. [Google Scholar] [CrossRef] [PubMed]
  45. Faucheux, M.J.; Kristensen, N.P.; Shen-Horn, Y. The antennae of neopseustid moths: Morphology and phylogenetic implications with special reference to the sensilla (Insecta, Lepidoptera, Neopseustidae). Zool. Anzeiger. 2006, 245, 131–142. [Google Scholar] [CrossRef]
  46. Yin, J.; Cao, Y.Z.; Luo, L.Z.; Hu, Y. Ultra-structure of the antennal sensilla of the meadow moth, Loxostege sticticalis. Entomol. Knowl. 2004, 40, 56–59. [Google Scholar]
  47. Hunger, T.; Steinbrecht, R.A. Functional morphology of a double-walled multiporous olfactory sensillum: The sensillum coeloconicum of Bombyx mori (Insecta, Lepidoptera). Tissue Cell 1998, 30, 14–29. [Google Scholar] [CrossRef]
  48. Guo, M.; Krieger, J.; Große-Wilde, E.; Mißbach, C.; Zhang, L.; Breer, H. Variant ionotropic receptors are expressed in olfactory sensory neurons of coeloconic sensilla on the antenna of the desert locust (Schistocerca gregaria). Int. J. Biol. Sci. 2014, 10, 1–14. [Google Scholar] [CrossRef]
  49. Li, G.Q.; Tan, Z.H.; Lin, H.H.; Wen, Y.B.; Zhang, J.F.; Wu, H.X.; Xie, M.Q. SEM Observation on Sense Organs of Culicoides arakawae and Culicoides schultzei. South China Agric. Univ. 2000, 21, 72–75. [Google Scholar]
  50. McIver, S.B. Fine structure of antennal sensilla coeloconica of culicine mosquitoes. Tissue Cell 1973, 5, 105–112. [Google Scholar] [CrossRef]
  51. Davis, E.E.; Sokolove, P.G. Temperature responses of antennal receptors of the mosquito, Aedes aegypti. J. Comp. Physiol. 1975, 96, 223–236. [Google Scholar] [CrossRef]
  52. Annalisa, A.; Antonio, B.; Patrizia, S.; Roberto, R. Antennal morphology and fine structure of flagellar sensilla in hippoboscid flies with special reference to Lipoptena fortisetosa (Diptera: Hippoboscidae). Insects 2022, 13, 236. [Google Scholar] [CrossRef] [PubMed]
  53. Xu, J.; Li, Y.P.; Cheng, W.N.; Song, Y.Q.; Wu, J.X.; Sun, H.Z.; Jia, H. Morphological studies on the types and distribution of antennal sensilla in Spodeptera exigua (Hubner). Northwest AF Univ. 2008, 36, 189–193. [Google Scholar]
  54. Hansson, B.S. Olfaction in Lepidoptera. Experientia 1995, 51, 1003–1027. [Google Scholar] [CrossRef]
  55. Den Otter, C.J.; Schuil, H.A.; Oosten, S.V. Reception of host-plant odors and female sex pheromone in Adoxophyes orana (Lepidoptera: Tortricidae): Electrophysiology and morphology. Entomol. Exp. Appl. 1978, 244, 370–378. [Google Scholar]
  56. Mochizuki, F.; Sugi, N.; Shibuya, T. Pheromone sensillaof the beet armyworm, Spodoptera exigua (Hfibner) (Lepidoptera: Noctuidae). Appl. Entomol. Zool. 1992, 4, 547–556. [Google Scholar] [CrossRef]
  57. Anderson, P.; Hallberg, E.; Subchev, M. Morphology of antennal sensilla auricillica and their detection of plant volatiles in the Herald moth, Scoliopteryx libatrix L. (Lepidoptera: Noctuidae). Arthropod Struct. Dev. 2000, 29, 33–41. [Google Scholar] [CrossRef]
  58. Ansebo, L.; Ignell, R.; Lofqvist, J. Responsesto sex pheromone and plant odours by olfactory receptor neurons housed in sensillaauricillica of the codling moth, Cydia pomonella (Lepidoptera:Tortricidae). J. Insect Physiol. 2005, 51, 1066–1074. [Google Scholar] [CrossRef]
  59. Van der Goes van Naters, W.M.; Otter, C.J.D.; Maes, F.W. Olfactory sensitivity in tsetse flies: A Daily Rhythm. Chem. Senses 1998, 23, 351–357. [Google Scholar] [CrossRef]
  60. Yang, H.; Yan, S.C.; Li, J.; Gao, L.L. Ultrastructural observations on antennal sensilla of Coleophora obducta (Meyrick) (Lepidoptera: Coleophoridae). Micron 2009, 40, 231–238. [Google Scholar] [CrossRef]
  61. Jefferson, R.N.; Rubin, R.E.; Mcfarlands, S.U.; Shorey, H.H. Sex pheromones of noctuid moths, XXII. The external morphology of the antennae of Trichoplusia ni, Heliothis zea, Prodenia ornithogally, and Spodoptera exigua. Ann. Entomol. Soc. Am. 1970, 63, 1227–1238. [Google Scholar] [CrossRef]
  62. Kvello, P.; Almaas, T.J.; Mustaparta, H. A confined taste area in a lepidopteran brain. Arthropod Struct. Dev. 2006, 35, 35–45. [Google Scholar] [CrossRef] [PubMed]
  63. Takács, S.; Bottomley, H.; Andreller, I.; Zaradnik, T.; Schwarz, J.; Bennett, R.; Strong, W.; Gries, G. Infrared radiation from hot cones on cool conifers attracts seed-feeding insects. Proc. R. Soc. B Biol. Sci. 2009, 276, 649–655. [Google Scholar] [CrossRef] [PubMed]
  64. Altner, H.; Sass, H.; Altner, I. Relationship between structure and function of antennal chemo-, hygro-, and thermoreceptive sensilla in Periplaneta americana. Cell Tissue Res. 1977, 176, 389–405. [Google Scholar] [CrossRef] [PubMed]
  65. Jiang, X.; Ning, C.; Guo, H.; Jia, Y.; Huang, L.; Qu, M.; Wang, C. A gustatory receptor tuned to D-fructose in antennal sensilla chaetica of Helicoverpa armigera. Insect Biochem. Mol. Biol. 2015, 60, 39–46. [Google Scholar] [CrossRef] [PubMed]
  66. Yu, H.Z. Types of Antennal Sensilla and Partial Cloning and Sequence Analysis of the General Odorant Binding Proteins 2 Gene of the Stripe Stem Borer Chilo supprssalis (Walker). Master’s Thesis, Zhejiang University, Hangzhou, China, 2004. [Google Scholar]
  67. Ma, R.Y.; Du, J.W. Insect sensilla. Entomol. Knowl. 2000, 37, 179–183. [Google Scholar]
  68. Cuperus, P.L. Distribution of antennal sense organs in male and female ermine moth, Yponomeuta vigintipunctatus (Retzius) (Lepidoptera: Yponomeutidae). Int. J. Insect Morphol. Embryol. 1983, 12, 59–66. [Google Scholar] [CrossRef]
  69. Li, X.; Bai, S.f. Ultrastructural studies on the antennal sensilla of Diadegma semiclausum Hellen (Hyml., Ichneumonidae). J. Hunan Agric. Univ. 2004, 38, 45–48. [Google Scholar]
Forests 15 01586 g001
Figure 1. The location of collection of material for research.
Figure 1. The location of collection of material for research.
Forests 15 01586 g001
Forests 15 01586 g002
Figure 2. General morphology of the moth antennae. (a) Basal part of antenna shows prolonged scape (S), pedicel (P) and flagellum (F) of male moths (100×); (b) basal part of female antenna; (c) flagellum segment of female antenna; (d) flagellum segment of male antenna; (e) basal part of male antenna; (e1) frontal side of the thumb protuberances on fourth and fifth flagella of male antenna; (e2) back side of the thumb protuberances on fourth and fifth flagella of male antenna.
Figure 2. General morphology of the moth antennae. (a) Basal part of antenna shows prolonged scape (S), pedicel (P) and flagellum (F) of male moths (100×); (b) basal part of female antenna; (c) flagellum segment of female antenna; (d) flagellum segment of male antenna; (e) basal part of male antenna; (e1) frontal side of the thumb protuberances on fourth and fifth flagella of male antenna; (e2) back side of the thumb protuberances on fourth and fifth flagella of male antenna.
Forests 15 01586 g002
Forests 15 01586 g003
Figure 3. A schematic drawing of the 59th, 60th, and 61th flagellomere, illustrating the distribution and differences in density of the morphological types of sensilla. sc: scale covered region; no sc: scale-free region of the flagellomere.
Figure 3. A schematic drawing of the 59th, 60th, and 61th flagellomere, illustrating the distribution and differences in density of the morphological types of sensilla. sc: scale covered region; no sc: scale-free region of the flagellomere.
Forests 15 01586 g003
Forests 15 01586 g004
Figure 4. The ventral surface of one flagellomere. (a) The distribution of s. trichodea-A (white arrows) and the morphology of s. trichodea-B (white rings); (b) transverse ridges covering the entire lengths of ST-A and ST-B.
Figure 4. The ventral surface of one flagellomere. (a) The distribution of s. trichodea-A (white arrows) and the morphology of s. trichodea-B (white rings); (b) transverse ridges covering the entire lengths of ST-A and ST-B.
Forests 15 01586 g004
Forests 15 01586 g005
Figure 5. SEM photomicrographs of s. coeloconica. (a) SCo sensilla in which the cuticular spines were closed over the central double-walled central sensillar “peg”; (b) the cuticular spines had become cut on one of the SCo and here we could see that on the double-walled peg (white arrows); (c) one SCo in which the cuticular spines were open (white arrows).
Figure 5. SEM photomicrographs of s. coeloconica. (a) SCo sensilla in which the cuticular spines were closed over the central double-walled central sensillar “peg”; (b) the cuticular spines had become cut on one of the SCo and here we could see that on the double-walled peg (white arrows); (c) one SCo in which the cuticular spines were open (white arrows).
Forests 15 01586 g005
Forests 15 01586 g006
Figure 6. SEM photomicrographs of s. auricillica and s. furcatea. (a) The morphological features of a “shoehorn” type of shape s. auricillica, and the smooth surface of the basal part of s. trichodea (white arrows); (b) the morphological features of a “rabbit-eared” type of shape s. auricillica; (c) the distribution of SA (white rings), ST (white triangles) and SF (white arrows); (d) the morphological features of s. furcatea.
Figure 6. SEM photomicrographs of s. auricillica and s. furcatea. (a) The morphological features of a “shoehorn” type of shape s. auricillica, and the smooth surface of the basal part of s. trichodea (white arrows); (b) the morphological features of a “rabbit-eared” type of shape s. auricillica; (c) the distribution of SA (white rings), ST (white triangles) and SF (white arrows); (d) the morphological features of s. furcatea.
Forests 15 01586 g006
Forests 15 01586 g007
Figure 7. SEM photomicrographs of s. styloconica. (a) The morphological features of s. styloconica on the distal end of each flagellomere; (b) the morphological features of s. styloconica on the end of 61st flagellomere.
Figure 7. SEM photomicrographs of s. styloconica. (a) The morphological features of s. styloconica on the distal end of each flagellomere; (b) the morphological features of s. styloconica on the end of 61st flagellomere.
Forests 15 01586 g007
Forests 15 01586 g008
Figure 8. SEM photomicrographs of s. chaetica and s. squamiformia. (a) The distribution of s. chaetica (white arrows) and s. squamiformia (white rings) on each flagellomere. (b) The distribution of s. chaetica on the 61th flagellomere. (c) The morphological features of s. chaetica. (d) The morphological features of s. squamiformia.
Figure 8. SEM photomicrographs of s. chaetica and s. squamiformia. (a) The distribution of s. chaetica (white arrows) and s. squamiformia (white rings) on each flagellomere. (b) The distribution of s. chaetica on the 61th flagellomere. (c) The morphological features of s. chaetica. (d) The morphological features of s. squamiformia.
Forests 15 01586 g008
Forests 15 01586 g009
Figure 9. SEM photomicrographs of Böhm bristles. (a) The distribution of Böhm bristles; (b) the morphological features of Böhm bristles.
Figure 9. SEM photomicrographs of Böhm bristles. (a) The distribution of Böhm bristles; (b) the morphological features of Böhm bristles.
Forests 15 01586 g009
Table 2. Sizes of the antennal segment of D. sylvestrella.
Table 2. Sizes of the antennal segment of D. sylvestrella.
Antennal LocationGenderLength (μm)
Scape♀200.00 ± 18.64 a
♂355.56 ± 22.22 b
Pedicel♀140.00 ± 1.70 a
♂153.65 ± 7.06 b
Flagellum♀7834.16 ± 81.80 a
♂7027.31 ± 188.64 b
Total antenna♀8174.16 ± 110.17 a
♂7536.52 ± 372.8 b
Data are presented as mean ± S.E. (n = 6). In each section of the column, data followed by the same letter are not significantly different according to Mann–Whitney U-test (p = 0.05).
Table 3. Antennae shape and sensilla types of other adult pyralid moths compared with D. sylvestrella.
Table 3. Antennae shape and sensilla types of other adult pyralid moths compared with D. sylvestrella.
CategoryGenusFamilyAntennae ShapeTypes of Sensilla
♀♂
D. sylvestrellaDioryctriaPyralidaeFiliformST (I, II), SCh, SCo, SSt, SA, SF, SSq, BB
Dioryctria rubella (Hampson) [27,28]DioryctriaPyralidaeFiliformST, SCo, SA, SSt (I, II), BB, SSq, SB
D. pryeri (Ragonot) [29]DioryctriaPyralidaeFiliformST (I, II), SCo, SCh, SA, SSq, SB, SCam
Homoeosoma nebulella (Den. and Schiff.) [23]HomoeosomaPyralidaeFiliformST, SA, SCo, SCh, SSt, SB
Ostrinia nubilalis (Hübner) [16,30]OstriniaPyralidaeFiliformSSt, SCh, SCo, SA, ST, SB
Zamagiria dixolopella (Dyar) [24]ZamagiriaPyralidaeFiliform and segmentedST (I, II), SSq, SA, SCo, SCh, SSt
Cnaphalocrocis medinalis (Guenee) [31]CnaphalocrocisPyralidaeFiliformBB, SSt, ST, SSq, SA, SCo, SB, SCav
Conegethes punctiferalis (Guenee) [32]PiletoceraPyralidaeFiliformBB, SSt, ST, SCh, SSq, SA, SCo, SB
Plodia interpunctella (Hubner) [33]PlodiaPyralidaeFiliform and segmentedBB, SSt, ST, SCh, SSq, SA, SCo, SB
Tirathaba rufivena (Walk.) [34]TirathabaPyralidaeFiliformST, SCh, SA, SCo, SSt, BB, SSq, SB, SUp
Stenachroia elongella (Hampson) [35]StenachroiaPyralidaeFiliformST, SCh, SSt, SCo, SA(I, II), SSq, BB
SB: S. basiconica, SCam: S. campaniform, SCl: S. clavatea, SPo: smell pore, SP: S. placodea, SCav: S. cavity, SUp: S. uniporous peg.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Wang, Q.; Ma, Y.; Jiang, D.; Yan, S. An Examination of the Antennal Sensilla of the Oligophagous Moth Species Dioryctria sylvestrella (Lepidoptera: Pyralidae). Forests 2024, 15, 1586. https://doi.org/10.3390/f15091586

AMA Style

Wang Q, Ma Y, Jiang D, Yan S. An Examination of the Antennal Sensilla of the Oligophagous Moth Species Dioryctria sylvestrella (Lepidoptera: Pyralidae). Forests. 2024; 15(9):1586. https://doi.org/10.3390/f15091586

Chicago/Turabian Style

Wang, Qi, Yujia Ma, Dun Jiang, and Shanchun Yan. 2024. "An Examination of the Antennal Sensilla of the Oligophagous Moth Species Dioryctria sylvestrella (Lepidoptera: Pyralidae)" Forests 15, no. 9: 1586. https://doi.org/10.3390/f15091586

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop