Morphological diversity of the sensilla of the larval mouthparts among three species of Corydalidae (Insecta, Megaloptera) with reference to their possible functions

doi:10.21203/rs.3.rs-5231268/v1

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Morphological diversity of the sensilla of the larval mouthparts among three species of Corydalidae (Insecta, Megaloptera) with reference to their possible functions

https://doi.org/10.21203/rs.3.rs-5231268/v1

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Sensory structures on the mouthparts surface of three species of Corydalidae (Insecta, Megaloptera), Acanthacorydalis asiatica, Neoneuromus ignobilis and Protohermes similis, have been studied using Scanning Electron Microscopy. They were studied to morphologically characterize and compare the sensory structures present on the mouthparts. The identified sensilla types were sensilla basiconica (SB), fin-like sensilla (FLS), sensilla trichodea (ST), sensilla peg (SP), sensilla styloconica (SS), sensilla chaetica (SCh), and forficate sensilla (FS). The potential functions of these sensilla were discussed in relation to their morphology and location. Additionally, cuticular process (CP), small spine-shaped projections (sp) and cuticular pores (cp) were identified in the sensory regions of the studied species. Morphological comparisons revealed significant diversity in the sensilla of larval mouthparts among the three species, but there may be similarities in function.

mouthparts sensilla

Corydalidae

feeding process

scanning electron microscope

Insect mouthparts exhibit a remarkable diversity of form and function, playing a critical role in their evolutionary adaptation. The structure of mouthparts varies according to their dietary preferences, with significant structural differences observed particularly in the more derived orders, which can aid in their identification and classification (Cobben 1978; Faucheux 1975; Brożek 2014). Insect sensilla consist of an exocuticular outer structure through which stimuli are transmitted to sensory cell processes within the sensilla. The shape and size of these cuticular structures vary, but most sensilla appear as hairs or pegs, with the socket region distinguishable from the shaft (Altner & Prillinger 1980). During the feeding process, sensory organs on the surface of the mouthparts can identify and locate the host (Lewis 1970; Zacharuk 1980).

The order Megaloptera is traditionally considered an ancient holometabolous group, comprising about 397 species worldwide, and arguably includes the oldest known representatives of aquatic insects with complete metamorphosis (Rivera-Gasperín et al. 2019). Megaloptera larvae are predators and polyphagous, with significant differences in habitat and food preferences among families (Flint et al. 2008). Generally, larvae capture prey with their mandibles. They consume small prey without chewing, while larger prey are captured using mandibles and forelegs, then cut and swallowed using their mouthparts (New 1993; Azam 1969; Ardila-Camacho 2018). Mouthparts play crucial roles in the larval feeding process.

Megaloptera larvae are rich in proteins and polysaccharides, with an amino acid composition that meets the standards for high-quality proteins. They also exhibit significant antidiuretic effects, thus possessing high food value and potential for medicinal development (Shi et al. 2019). In certain regions, there is a high awareness about Megaloptera, and significant consumption of their larvae has been recorded (Cao et al. 2019). It can also contribute to rural revitalization, which can promote rural economic benefits and enhancing the economic status of rural residents (Cao et al. 2020). The present study investigates the sensory structures on the mouthparts of three Megaloptera species from the Corydalidae family: Acanthacorydalis asiatica, Neoneuromus ignobilis and Protohermes similis, which are important resource insects (Cao et al. 2014). The larvae of three species are large, medium and small in size. Size of the prey captured is positively correlated with the size of the mandibles, and consequently, with the size of the larvae (Hayashi 1998). This study describes the different types of mouthparts sensilla among three species of Corydalidae, discusses their probable functions, and their association with feeding habits. This research will lay a foundation for future studies on the evolution of mouthpart morphology and mechanisms for feeding.

Materials examined. The specimens for the study were collected from field collections in the river of the Emeishan City and Yuxi City, CHINA. The following are the details: Acanthacorydalis asiatica, 2023, Yuxi City, coll. YT. Li; Neoneuromus ignobilis, 2023, Emeishan City, coll. YT. Li; Protohermes similis, 2023, Emeishan City, coll. YT. Li. These specimens are deposited in the School of Life Science, Leshan Normal University, Leshan.

Sample for light microscopy. All specimens were first documented by light microscopy, employing a microscopic system of LY-WN.

Sample for Scanning electron microscopy. The specimens were washed with UP water to remove adherents, mucus, and impurities to obtain a clean observation surface and fixed with 3% glutaraldehyde overnight at 4°C. The fixed specimens were washed 3 times with UP water for 10 min each, fixed for 1 h after 1% osmium acid, and then washed 3 times with UP water for 10 min each. The specimens were then dehydrated in an ethanol series followed by drying in Critical Point Dryer. Stick all the specimens to the sample holder with conductive adhesive, and put the sample holder into the ion sputtering instrument for plating. Scanning electron microscope (SEM) studies were undertaken with a JSM-IT700HR scanning electron microscope.

Terminology of sensilla. Dentification and classification of sensilla and their terminology in the present study were based on McIver (1975), Zacharuk (1980), Altner & Prillinger (1980), Altner (1985), Shields (2010), Brożek & Chlond (2010) and Brożek & Bourgoin (2013).

Date analysis. The measurements for the mouthparts and sensilla were performed using Smart TIFF, V1.0.0.12, Carl Zeiss SMT along with processing of digital images using Adobe Photoshop CC2019.

The mouthparts of all the species studied A. asiatica, N. ignobilis and P. similis were four segments. Taking into account the external morphology and location, seven types of distinct sensilla were observed. The characters like the pore system, socket and shape of the sensilla were varying. The types of sensilla identified were included sensilla basiconica (SB), fin-like sensilla (FLS), sensilla trichodea (ST), sensilla peg (SP), sensilla styloconica (SS), sensilla chaetica (SCh), forficate sensilla (FS). Along with the identified sensilla, other cuticular process (CP), spine-shaped projections (sp) and cuticular pores (cp) were found to surround these sensilla. These sensory structures revealed several morphological differences among the three studied species.

Overall Morphology of the Mouthparts

The mouthparts of A. asiatica, N. ignobilis, and P. similis consisting of a labrum, a labium, a pair of separated mandibles and a pair of separated maxillas (Figs. 1–6).

The types of Sensilla of larval mouthparts

Sensilla basiconica (SB). Sensilla basiconica were observed on the large jaw surface. However, these sensory structures differed from one another in several details.

Sensilla basiconica had characteristic longitudinal grooves on their surface with acuminated apex and were inserted in flexible socket. They didn’t have any pore system and were located on all the species studied. Sensilla basiconica with longitudinal grooves were the ones which varied the most in their shape. In individual species different subtypes of these sensilla were observed.

The sensilla basiconica on the mandible varies in morphology. The smooth cuticle surface and flat undulating axis terminate at the top of the sensor, with the tip ranging from blunt to sharp (SB 1, SB 2, SB 3). The sensilla basiconica 1(SB 1) on the mandible of the A. asiatica. was a short rod, The morphology of the sensilla basiconica 2(SB 2) on the mandible of the N. ignobilis. was barb shaped, and the sensilla basiconica 3(SB 3) on the mandible of the P. similis. was sharp-tipped. There were three types according to the above differences.(Figs. 7–8, 20, 21–22, 35–36)

Fin-like sensilla (FLS). Fin-like sensilla typically possess a broad base and long stem, characterized by rough cuticle walls with lines, and an overall fin-like shape. These sensilla were closely arranged. Their length ranges from 76.27 ± 7.45 µm, and their width is 27.59 ± 1.64 µm. Based on their size, they are classified into two types: FB 1, which was wide, and FB 2, which was slender (Figs. 9, 12, 15, 17–19). These sensilla were found exclusively in A. asiatica.

Sensilla trichodea (ST). Sensilla trichodea were hair-like sensilla with pointed apices that vary greatly in length and were inserted into flexible sockets. The cuticular walls of these sensilla were smooth, but they possess a terminal pore that was usually difficult to observe directly, as it was frequently covered by a plug of viscous substance. These sensilla were arranged around the labial tip and the sensorial area of the labial apex. Sensilla trichodea were observed in all the species studied and were classified into two subtypes: sensilla trichodea1 (ST1) and sensilla trichodea2 (ST2). The length of ST1 ranged from ≥ 370.36 µm, ST2 ranged from 35.49–160.03 µm (Figs. 23, 28–30, 37, 40, 42–45).

Sensilla peg (SP). Sensilla peg (SP) has a finger-like appearance, maintaining the same thickness throughout with a slightly blunt apex. Their characteristic features include inflexible sockets and the presence of an apical pore. These sensilla were distributed around the sensilla trichodea and were numerous, arranged centrally on the sensory fields. In the present study, sensilla peg on the apical sensorial areas were categorized based on their sharpness into two types: SP1 (sharp: length = 9.73 ± 0.91) and SP2 (blunt: length = 10.8 ± 0.81 um) (Figs. 10–11). Sensilla peg were restricted to the A. asiatica.

Cuticular process (CP). In each sensory field, different sensilla were surrounded by different types of cuticular processes. Cuticular processes are denticles, with a wide base and a sharply pointed tip. They were slender and long, only slightly tapered from based to apex, and blunt tipped orslightly clavate. These cuticular elements were without sockets and pores system. The length of cuticular processes 1(CP1) from 12 ± 1.29 um, cuticular processes 2(CP2) ranged from 4.73 ± 0.94 um (Figs. 24–25, 27, 38–39, 41).

Forficate sensilla (FS). They were 8–11 µm long and cylindrical at the base. The tip was divided into two or three processes. They were nonporous, with a smooth cuticular wall, and found in the labrum tip sensory field (Figs. 25).

Sensilla styloconica (SS). Sensilla styloconica typically had a broad base and a long stem with smooth cuticular walls and blunt apex. These structures arise from elevated cylindrical projections with flexible sockets. These sensilla were located more marginally on the sensory fields. Based on their size, they were divided into two types, SS 1: slender. SS 2: blunt (Figs. 12–13, 26–27, 40–41).

Sensilla chaetica (SCh). Sensilla chaetica were hair-like structures with either a smooth or grooved surface and lack wall pores. They had a blunt apex, are inserted into flexible sockets with a stiff shaft, and were usually positioned perpendicular to the surface. These sensilla had different lengths (ranging from 52–533 um) so grouped as SCh1 (long sensilla ≥ 317 um), SCh2 (medium sensilla 134–317 um) and SCh3 (short 52–134 um) (Figs. 14–16, 20, 28–34, 42–48), located on the labrum, labium and maxilla segments of all the species studied.

Small spine-shaped projections (sp). Small spine-shaped projections were cuticular projections which elements were without sockets and pores system. They were observed in all the species studied (Figs. 46).

cuticular pore (cp). These were observed on the labial surfaces as small holes on epicuticle in all the species studied.

The mouthparts of the larvae of A. asiatica, N. ignobilis, and P. similis were morphologically compared for the first time using scanning electron microscopy. The morphological comparison revealed that the larval mouthparts sensilla exhibited significant diversity among the three species. The sensilla varied in number, shape, and size across the species. Their external morphology and ultrastructural characteristics suggest different functions, including chemosensory (gustatory and olfactory), thermos-hygrosensory, and mechanosensory roles (Backus 1988).

In this study, seven types of sensilla were observed on the mouthparts of the three species. They shared some common sensilla while also having unique types in the same mouthpart segments. The sensilla on mouthparts primarily function as contact chemoreceptors for tasting food, serving olfaction, gustation, and mechanosensation (Zacharuk 1985; Blaney & Chapman 1969; Chapman, 2003; Prakash et al. 1995; Spiegel et al. 2005). Various sensilla on the epipharynx were presumed to serve the taste function in insects (Faucheux 1975). The size of the prey captured was positively correlated with the size of the mandibles and, consequently, the size of the larvae (Hayashi 1998). This study first discussed the probable functions and associations of the different types of sensilla on the mouthparts with feeding process in these three species.

The putative function of sensilla on mandible and labrum. Mandibles of insects with biting mouthparts often had a dual function, cutting and grinding by the incisor and molar regions (Snodgrass 1994). In Megaloptera larvae, the mandible features an apical tooth and three preapical teeth (Martins, C & Contreras-Ramos, A. 2020). The preapical teeth were consistently worn down during feeding. sensilla basiconica (SB), inferred from their external morphology, primarily perform gustatory, olfactory, and mechanical functions (Zacharuk & Shields 1991; Chapman 2003; Shields 2008). These sensilla are typically involved in taste perception and food detection (Eilers et al. 2012; Yan et al. 1987). Although the sensilla basiconica (SB) on the larval mandible differ morphologically among the three species, they may be performing the same function. During feeding, larvae use their mandibles to capture, cut, and swallow larger prey (New 1993; Azam 1969; Ardila-Camacho 2018).

The labrum plays a crucial role in the feeding process. Sensilla on the tip of the labrum serve as the initial sensory organs to contact prey. In the three species, the apical part of the labrum was abundant with various sensilla, including fin-like sensilla (FLS), sensilla trichodea (ST), sensilla peg (SP), sensilla styloconica (SS). Sensilla trichodea on the region of the labrum among the three species probably represent mechano-chemosensilla. Their appearance and location are similar to those reported as having this dual function in other insects(Altner & Prillinger 1980; Backus 1985; Chapman 1998). In A. asiatica, location of fin-like sensilla in the same region of sensilla trichodea, making first contact with the substrate during feeding, likely representing mechano-chemosensilla.

Sensilla peg on the apical and subapical regions of the labrum were classified as chemosensilla with gustatory functions (uniporous sensilla). These correspond to thick-walled chemosensilla, functioning as taste hair contact chemoreceptors (Slifer 1970). The localization of sensilla peg shape, terminal pore, and inflexible sockets were nearly identical to peg, basiconic, or styloconic sensilla, which were gustatory sensilla (Zacharuk 1980; Altner & Prillinger 1980; Chapman 1998). The cuticular process in Eocanthecona furcellata was recognized as multilobed sensilla with a probable function as a humidity detector (Usha Rani 2009). Sensilla styloconica, similar to gustatory sensilla corresponding to sensilla basiconica type A described in Eocanthecona furcellata by Rani, which were gustatory sensilla (Rani, 2009; Wang et al. 2020). All these sensilla and cuticular process in the labrum of the three species play a mechanical and gustatory correlative role in the feeding process.

The putative function of sensilla on maxilla and labium. When the larvae are feeding, maxilla activity assists the mandible in swallowing and ingestion. Sensilla chaetica and trichodea with longitudinal grooves on shaft, flexible sockets and absence of pore are responsible for mechanical function(Zacharuk & Shields 1991; Shields 2008; Urbanek et al. 2016). Mechanosensilla of such characteristic appearance were pointed out by McIver (1975) however, author suggested they can be represented by a plenty of shapes. Comparison of the same position, the fin-like sensilla only found in the A. asiatica, it maybe represents mechanical function. These prominent sensilla may enhance the mechanical sensation among the three species larvae, aiding in sensing the shape and size of food resources.

Differences in the sensilla of three species and their role in feeding. Generally, the position and arrangement of different types of sensilla were similar among the studied Corydalidae species. Differences in the sensory morphology of labial sensilla among different trophic groups of Corydalidae were less known. The current results align with these observations, with some specific sensilla, such as the fin-like sensilla, restricted to A. asiatica. Sensilla chaetica and sensilla trichodea on the mouthparts, likely functioning as contact chemoreceptors with gustatory functions, were observed in both N. ignobilis and P. similis, but were less prevalent in A. asiatica. In A. asiatica, this function may be served by the fin-like sensilla.

The distribution pattern of labial mechanosensilla types, such as sensilla chaetica, and sensilla trichodea, in N. ignobilis and P. similis was quite similar to that of A. asiatica, which also has sensilla peg and fin-like sensilla. The functional significance of these sensilla on the mouthparts seems to be related to informing about the position of the mouthparts with respect to the prey, while facilitating the detection of food during feeding.

The species studied have a similar distribution of sensory locations, although they differ in body size, and these sensory locations play a crucial role in detecting food. Moreover, the types of sensory structures in the mouthparts of A. asiatica are more diverse compared to the other two species, but they may perform a similar function in the feeding process.

Author Contribution

CHENG QUAN CAO provided the funds. YU TONG LI prepared specimens and all the figures. YU TONG LI and YU MENG DAI wrote the main manuscript text. All authors reviewed the manuscript.

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Morphological diversity of the sensilla of the larval mouthparts among three species of Corydalidae (Insecta, Megaloptera) with reference to their possible functions

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Abstract

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Introduction

Materials and methods

Results

Overall Morphology of the Mouthparts

The types of Sensilla of larval mouthparts

Discussion

Conclusion

Declarations

Author Contribution

References

Additional Declarations

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