Morphological characterization of the antennal sensilla of t he earwig Anisolabis maritima (Dermaptera: Carcinophoridae) with reference to their probable functions

Abstract

The earwig, Anisolabis maritima (Dermaptera: Carcinophoridae), is one of the most significant insects in KSA because, it was recorded in Saudi Arabia as a beneficial predator on eggs and newly hatched larvae of the red palm weevil, Rhyncophorus ferrugineus. We examined the external morphology of the antennal sensilla of males and females of A. maritima using scanning electron microscopy (SEM). The filiform antennae of A. maritima were of the conventional type comprising a basal scape, pedicle and a long, thread-like flagellum, which was composed of 12 flagellomeres of males and 16 flagellomeres of females. Six morphologically unique sensillar types were found and described on the antennae of males and females of A. maritima. Of those identified, there were three types of porous trichoid sensilla (long, curved and arcuate), and two types of basiconic sensilla (short and curved), and one type of aporous trichoid sensilla. The shape, external morphology and array of sensilla on the antennae of males and females of A. maritima were similar.

1. Introduction

Anisolabis maritima is a cosmopolitan insect worldwide in distribution (Arnett, 1993). Most stages have been found throughout the year, males seemed more prevalent from late spring through autumn. Eggs were found during the warmer months, and were guarded by the females (Nishida, 2002). Zimmerman (2001) stated that A. maritima is found only along the seashore. It is an endemic species in order Dermaptera and represents an adaptive radiation from a marine littoral ancestor which is indigenous to Hawaii. It is frequent in winter beneath the piles of seaweed, boards, and debris just above high tide make, and is also recorded from Jacksonville for key west on east coast (Brindle, 1981). The earwigs are not considered as pests, although they are elsewhere in the world. These can be found in a variety of habitats including caves, coastal and marine littoral areas, mesic and sometimes wet forests, and possibly in the recent lava flows (Nishida, 2002). Earwigs are significant generalist predators of a range of orchard pests (Suckling, 2006). The A. maritima earwig was recorded in KSA as a predator for the eggs of the red palm weevil Rhynchophorus ferrugineus (2002, ).

The aim of the present work is to identify and investigate the different sensilla that are distributed on the legs and anal cerci of A. maritima adults with discussion of their possible function in the behavior of host location and oviposition of the insect, which could facilitate future studies on neurobiology of olfaction and gestation. A. maritima may be used as a beneficial predator for the eggs of R. ferrugineus in future and as a tool in integrated pest management program (IPM).

2. Materials and methods

2.1. Scanning electron microscopy

Experimental adult individuals, males and females, of A. maritima were obtained from the Ministry of Agriculture and Water in El-Kharj, Riyadh, KSA. The morphological characters and location of different sensilla distributed on the antennae of the earwig A. maritima were examined using scanning electron microscopy. The insects were soaked in 70% ethanolic alchohol for 24 h, then the antennae were separated from the bodies of the insects. The specimens were rinsed thoroughly in distilled water and were fixed in 4% glutaraldehyde for 24 h at 5 °C, these were then dehydrated in conceding series concentration of acetone, individually for 1 h, and air dried. The specimens were mounted individually on stubs, then coated with gold and were examined using scanning electron microscopy (SEM) (JEOL-JSM b36 OLV); the observations were obtained and recorded from 10 males and 10 females.

3. Results

3.1. General description of A. maritima antennae

The filiform antennae of both sexes were of the conventional type comprising basal scape, pedicel and flagellum, which was composed of 12 flagellomeres of males and 16 flagellomeres of females. The long antenna of males was 1812.5 μm, and that of females was 2078.12 μm. The scape, pedicel and flagellum of males constituted 156.2, 78.1 and 1437.5 μm, and that of females constituted 1906.2 μm of the entire antennal length, respectively (Fig. 1A). On the surface of the entire antennae numerous sensilla were distributed (Fig. 1B and C), which were equal in both sexes but were different in the number of hair: females had 855 hair and males had 635 hair. The flagellomeres of females consisted 811 hair and those of males consisted 590 hair (Table 1).

Figure 1.

(A) Scanning electron micrograph (SEM) of an antenna of a male A. maritima showing the scape (Sc), pedicel (Pd) and flagellum (Fl). The antenna of a female A. maritima is similar in shape and morphology, but is slightly longer. (B) Magnified part of the antenna showing many hair surface cover. (C) Lateral flagellomeres showing numerous cover with sensilla.

Table 1.

Abundance and distribution of sensilla on the antennae of A. maritima.

Sex	Antennal segments
	Sc	Pd	Flagellum
			F1	F2	F3	F4	F5	F6	F7	F8	F9	F10	F11	F12	F13	F14	F15	F16	T.F1	T.S
Male	25	20	32	30	38	41	39	46	49	50	56	64	73	72	–	–	–	–	590	635
Female	26	18	36	30	38	42	45	46	53	50	50	62	60	76	75	52	44	52	811	855

Number and location of the various sensilla observed on the antennae of males and females of A. maritima. Sc: scape, Pd: pedicle, Fl: flagellum, T.Fl: total number seta of flagellomeres, T.S: total number sensilla of antenna.

4. Terminology

Antennal sensilla have been named differently by various authors despite similarity in their external morphology and positions on the antennae (Moran and Brown, 1973; Singleton-Smith et al., 1978; Ossiannilsson, 1992; van Baaren et al., 1996; Sorker et al., 2004; Kristoffersen et al., 2006; Onagbola and Fadamiro, in press). To avoid this inconsistency in terminology, we classified and named the various sensilla observed on the antennae of A. maritima based on their morphological details as revealed by SEM and followed the nomenclature of Ossiannilsson (1992), Shanbhag et al. (1999), Chapman (1998), Bleeker et al. (2004), Kristoffersen et al. (2006) and Onagbola and Fadamiro (in press). The description of the types of sensilla is based largely on our inference from the published photomicrographs, using morphological characters such as presence and positions of pores as bases identification.

5. Types of sensilla

5.1. Porous sensilla

Fig. 2 shows the types of sensilla observed on the antennae of A. maritima. Five morphologically different types of hair-like olfactory sensilla were identified on the antennae of A. maritima. These included three types of trichoid sensilla: (1) the long (ST1) type I (Fig. 2A, length = 112.5 μm), (2) curved (ST2, Fig. 2C, L = 43.93 μm), and (3) arcuate (ST3, Fig. 2D, L = 100 μm), and two types basiconic sensilla: (1) short (BS1, Fig. 2E, L = 1500 μm) and (2) curved (BS2, Fig. 2F, L = 9.80 μm). The surface of the ST1 and ST3 sensilla was longitudinally grooved (Fig. 2A, B and D), whereas the surface of the ST2 sensilla appeared smooth (Fig. 2C), and the BS1 and BS2 sensilla were thick (Fig. 2E and F). The shafts of the long sensilla (ST1) were straight, those of the ST2 were curved, of the ST3 arcuate, of the BS1 short and of the BS2 curved and the basal insertions into sockets were characterized by fluted surface (Fig. 2). The tip of the apical seta is morphologically the same in both sexes of A. maritima whereas the ST1 and ST2 are tapering, ST3, BS1 and BS2 are blunt. We found them on the scape segment antennal except for ST3 which was found on the pedicle, and BS2 was found on the first flagellomeres. The SEM showed (Fig. 2B–F) that these porous sensilla had wall pores, suggesting a plausible role in the perception of olfactory stimuli.

Figure 2.

Micrographs of the porous sensilla on the antennae of A. maritima: (A) ST1 long; (B) magnified part of ST1; (C) ST2 curved; (D) ST3 arcuate. (E) BS1.

5.2. Aporous sensilla

One type of aporous trichoid sensilla, ST1, was found on the antennae of both sexes of A. maritima (Fig. 3A). The ST1 sensilla (L = 107.5 μm) were long, tapering tip and was found on the antennal scape. Generally, the sensilla (porous and aporous) are found on the all antennae both sexes but they have concentrated terminal portions of each antennal flagellomere, and the sensilla revealed aporous walls, suggesting a non-olfaction for these sensilla.

Figure 3.

Micrographs of the aporous trichoid sensilla (ST1) on the antennae of A. maritima.

6. Discussion

The various sensilla and their distribution on the antennae of males and females of A. maritima, as revealed in this study, were consistent with those reported for other insects (van Baaren et al., 1996; Ochieng et al., 2000; Sorker et al., 2004; Kristoffersen et al., 2006). However, some of these sensilla have been characterized differently by the various authors cited above. Six types of sensilla were observed on the antennae of males and females of A. maritima with no difference in their abundance and distribution between the sexes. Among these sensilla, more attention was focused on the identified mechano- and olfactory sensilla owing to their probable importance in mate and host finding by A. maritima. Typically, porous sensillar walls suggest olfactory function (Steinbrecht, 1984; Hallberg et al., 2003; Kristoffersen et al., 2006; Onagbola and Fadamiro, in press; Onagbola et al., in press). Odorant substances including sex pheromones and host plant volatiles diffuse through the wall pores of antennal sensilla into the sensillar lymph and are transferred to olfactory receptors on the dendrites of olfactory neurons by odorant binding proteins (Leal, 2005).

According to Onagbola et al. (in press) the photo micrographs of the cross-section of the apical seta did reveal porous walls, suggesting an olfactory function. Sensilla with a similar morphological conformation were also reported on the antennae of other insects (Petterson et al., 2001; Ryan, 2002; Chen and Fadamiro, 2007; Sharaby and Al-Dossary, 2007). These sensilla vary in size, depending on their location on the antennal flagellum; they appear to be morphologically similar otherwise. Our SEM study revealed porous walls on the ST1, ST2, ST3, BS1 and BS2 sensilla, suggesting an olfactory function. The sensilla that are found on the antennae of both sexes of A. maritima are likely olfactory in function, perhaps involved in the perception of host-related stimuli.

One type of aporous trichoid sensilla with smooth surface shafts and tapering tip was found on the antennae of both males and females of A. maritima. The presence of aporous trichoid sensilla has also been reported on the antennae of other insect (Ossiannilsson, 1992; Kristoffersen et al., 2006). The external morphology of the aporous trichoid sensilla on the antennae of A. maritima resembles that of the type III (St3-AP) aporous trichoid sensilla reported on the antennae of Diaphorian citri (Onagbola et al., in press). Also, in this study we observed one aporous basiconic sensilla on the antennae of A. maritime, the surface of which appeared thick. Because the shafts of these sensilla are connected to conical basal sockets by cuticular membranes, Chapman (1998) suggested that they might have mechanosensory functions. Similar mechanosensory sensilla were also characterized by Kristoffersen et al. (2006) on the antennae of the psyllid Trioza apicalis. Our SEM revealed that these types of sensilla are devoid of wall pores, suggesting a non-olfactory role. Sensilla with a similar morphology and location have been described on the antennae of other insect and termed chaetica sensilla with suggested mechanosensory or proprioceptive functions based on their characteristic morphology and location on the proximal region of the scape (Ochieng et al., 2000).

To our knowledge, this is the first study to describe the detailed morphology of the antennal sensilla of A. maritima. Five olfactory sensilla and one mechanosensory sensillium were characterized supporting the plausible use of olfactory (Wenninger and Hall, in press) and vibratory (Yang et al., 1986; Tishechkin, 1989, 2005) cues for host and/or mate finding in this species. These results obtained provide direct morphological evidence that the antennae of A. maritima possess structures that can play a role in both chemo- and mechanosensory modalities for mate finding and host plant location. These results substantiate the possibility that synthetic repellents and/or attractants may be developed for practical pest control applications., which should exploit chemically mediated host plant finding mechanism in this species.