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1 September 2011 Morphological Characterization and Distribution of Sensilla on Maxillary Palpi of Six Bactrocera Fruit Flies (Diptera: Tephritidae)
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Abstract

Several members of the Tephritidae (Diptera) are destructive pests of fruits and vegetables. This study used scanning electron microscopy to analyze the external morphology, typology, size, and distribution of maxillary palpus sensilla of both female and male adults of 6 fruit fly species, Bactrocera cucurbitae (Coquillett), B. diaphora (Hendel), B. dorsalis (Hendel), B. minax (Enderlein), B. scutellata (Hendel), and B. tau (Walker). The palpus is equipped with sensilla chaetica, sensilla basiconica, and microtrichia. In addition, the possible functions of the sensillum types are discussed. Probable functions include the mechanoreception of sensilla chaetica and microtrichia, and olfaction of sensilla basiconica. Future functional morphology and electrophysiological studies are needed to confirm these proposed functions.

Fruit flies (Diptera: Tephritidae) are among the most important insect pests worldwide with the larval stages attacking a wide variety of fruits and vegetables (Clarke et al. 2005). Bactrocera is one of the largest genera in the Tephritidae with over 500 described species belonging in 28 subgenera (Smith et al. 2003). These species are widely distributed in the Asia-Pacific region. In China, Bactrocera cucurbitae (Coquillett), Bactrocera diaphora (Hendel), Bactrocera dorsalis (Hendel), Bactrocera minax (Enderlein), Bactrocera scutellata (Hendel), and Bactrocera tau (Walker) are commonly found in the field (Hu et al. 2010). Among these 6 species, the oriental fruit fly, B. dorsalis, can be the most economically serious insect pest in tropical and subtropical regions (Li et al. 2007). The oriental fruit fly is highly polyphagous and is able to infest the fruits of more than 250 species of host plants, including commercial crops such as mango, citrus, coffee, and chili pepper, as well as non-cultivated wild hosts (Clarke et al. 2005).

Fruit flies, like other insects, acquire information about their environment through sensory systems. Furthermore, many monitoring and control techniques for tephritid flies use olfactory-based behavioral manipulation (Hull & Cribb 1997). In insects, olfactory receptor neurons are located in cuticular sensilla which exist on the antennae and other head-associated body parts (Anton et al. 2003). Maxillary palpi, which are in direct contact with a feeding substrate, perceive odors more directly than antennae, which often perceive diffused odors rather than concentrated ones through direct contact (Wasserman & Itagaki 2003). As part of our ongoing research on olfactory mechanisms used for mate and host location by tephritid species, the characterization and determination of the abundance and distribution of sensilla of different fruit flies using scanning electron microscopy (SEM) techniques became imperative. Recently, the antennal sensilla of 6 Bactrocera species have been described (Hu et al. 2010). Yet little work has been published describing the abundance and distribution of sensilla on the maxillary palpi. Thus, the aim of our study was to examine, describe, quantify and compare the sensilla present on the maxillary palpi of both females and males of 6 fruit fly species, i.e., B. cucurbitae, B. diaphora, B. dorsalis, B. minax, B. scutellata, and B. tau, as a prerequisite for future electrophysiological studies of the antennal sensory system involved in chemical communication.

MATERIALS AND METHODS

Adult B. cucurbitae, B. diaphora, B. dorsalis, B. minax, B. scutellata, and B. tau were collected using glass McPhail traps with proteinaceous baits placed in navel orange (Citrus reticulata L.) orchards in Yunnan Province and Chongqing Municipality, China, in 2009. After identification, specimens were kept in 70% alcohol before being prepared for Scanning Electron Microscopy (SEM). Voucher specimens were deposited in the insect collection of Southwest University, Chongqing, People's Republic of China.

Scanning Electron Microscopy (SEM)

Approximately 20 adults of each species were decapitated under a stereomicroscope (SZX12; Olympus, Tokyo, Japan) using a sharp blade. The maxillary palpi of females and males were removed separately and fixed in 2.5% glutaraldehyde mixed with phosphate buffer solution, pH 7.4, at 4°C for 24h. Maxillary palpi were subjected to post-fixation in 1% osmium tetroxide for 2h. After having been washed 3 times for 15 min each time in double-distilled H2O, the specimens were dehydrated in a graded alcohol series of 30, 50, 70, 80, and 90% and absolute ethanol for 15 min at each concentration. This dehydration process was followed by criticalpoint drying. Subsequently, either the ventral or dorsal sides of maxillary palpi were mounted on sticky tape. Immediately before observation, the maxillary palpi were sputter coated with gold in an E-1010 high-resolution sputter coater (Hitachi, Tokyo, Japan). The specimens were examined in an S-3000N SEM scanning electron microscope (Hitachi) operated at 15kV.

Statistical Analysis

The morphological terminology used here followed that of Schneider (1964), Zacharuk (1985), and Dickens et al. (1988). Three to 5 maxillary palpi were observed for each fruit fly species and sex. Sensilla on the dorsal and ventral surfaces of the maxillary palpi were identified, counted, and measured. Measurements (micrometers) obtained from photomicrographs of 3 to 5 samples for each sex and species were used to calculate means. The number of various types of sensillum per unit area was used to estimate the number of sensilla on the whole maxillary palpus. A sampling quadrant on the surface of maxillary palpus was randomly chosen and the number of each type of sensillum within that quadrant was counted. The area of each sampling photograph quadrant was 2,958 µm2 with magnification at 1800x. The values were converted to density, i.e., number per one unit area of 10,000 µm2. Two-way analysis of variance (ANOVA) with interaction was used to examine the effects of species and sex on the abundance, length, and diameter of each sensillum type, and the length and diam of the maxillary palpus structure. Data were analyzed using JMP 8.0.2 software (SAS Institute 2009).

RESULTS

General Maxillary Palpus Morphology

The maxillary palpi were attached to the proximal part of the proboscis (Fig. 1A). The proboscis covered the palpi except for their tips, and they were extended during probing and feeding. The complete surface of the maxillary palpus was exposed to the environment. There was a significant species × sex interaction for palpus length. This interaction was driven by B. minax females, which had the longest maxillary palpi (1266.3 ± 117.7 µm) of the 6 species (F5,36 = 3.94, P = 0.006) (Table 1). There were no significant differences in the diam of palpi among the 6 species or the sexual genders (F5,36 = 0.54, P = 0.74).

Fig. 1.

Scanning electron micrographs of head and sensilla of B. cucurbitae, B. diaphora, and B. tau. A. Head of B. cucurbitae ♀ bearing large compound eyes (C), antennae (A) and maxillary palpi (P). Heads of the other 5 species are similar. B. B. cucurbitae ♀ : sensilla chaetica (SC) on middle of palpus. C. B. cucurbitae ♂: sensilla chaetica (SC) on distal part of palpus. D. B. diaphora ♀: sensilla chaetica on maxillary palpus. E. B. diaphorasensilla chaetica (SC) and microtrichia (MI) on promixal part of palpus. F B. tau ♀: sensilla chaetica (SC) on distal part of palpus. Pr: promixal part; Di: distal part. A. 1mm; B. 50 µm; C. 30 µm. D. 500 µm; E. 20 µm; F. 20 µm.

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TABLE 1.

MEAN LENGTH AND DIAMETER (±SE) (UM) OF MAXILLARY PALPI OF THE SIX BACTROCERA SPECIES (N = 4).

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Types of Maxillary Palpus Sensilla

Sensilla chaetica (SC), microtrichia (MI) and sensilla basiconica (SB) were observed on the maxillary palpi of females and males of all 6 species. There were significant species × sexual gender interactions for length and diam, but only significant differences between the sexes for microtrichia length, microtrichia diam and sensilla basiconica length (Table 2). The sensilla chaetica (SC) occurred on the maxillary palpi of both sexes of the 6 fruit fly species, but were distributed sparsely at the distal ends of the palpi (Fig. 1-D). The SC were characterized by a grooved surface and straight hairs with sharp tips, each of which was located in a wide socket (Fig. 1-B, C, E and F). The SC were longest (>103 µm) for B. minax males and females, and B. scutellata males (Table 3). The B. minax male SC had the widest diam (7.8 ± 1.3 µm) followed by B. tau females (6.3 ± 0.9 urn) (Table 3)

The microtrichia were densely distributed on the maxillary palpi (Fig. 2-A-D). The microtrichia have longitudinal grooves along the shaft of the sensillum and crests with slightly sharp tips. Microtrichia on palpi of females tended to be longer than those on the palpi of males with the notable exception of B. scutellata in which they were 18.6 ± 0.8 µm and 20.5 ± 2.0 µm long in females and males, respectively. In B. minax the lengths of palpus microtrichia were as follows: females -24.3 ± 0.2 µm; the longest of all 6 species, and males -22.8 ± 1.0 µm; and the corresponding widths were 4.5 ± 0.3 µm and 6.2 ± 0.9 µm, i.e., the widest of all 6 species (Table 3). B. dorsalis males had the shortest maxillary palpus microtrichia (12.6 ± 0.7 µm) and the narrowest diam (1.5 ± 0.0 µm).

The sensilla basiconica were numerous toward the tip of the maxillary palpus and had slightly pointed tips (Fig. 2-A, B and D). They were each set into a tight socket (Fig. 3 -A and F). The lengths of sensilla basiconica differed significantly between some species, and sexes, and there was a significant species × sex interaction; however the diam of sensilla basiconica differed significantly between species but not between sexes and there was a significant species × sex interaction (Table 2). The sensilla basiconica length was longest for B. minax females and shortest for B. dorsalis and B. scutellata females (Table 3). Sensilla basiconica diam were greater for B. minax females and narrower for both B. diaphora and B. dorsalis males (Table 3).

Abundance and Distribution of Maxillary Palpus Sensilla

The distribution patterns of sensilla on the maxillary palpi of females and males of 6 fruit fly species were very similar (Figs. 1, 2, 3). The abundance of sensilla differed significantly between species, and there were significant species × sex interactions; however only the distally distributed SC had significant differences between sexes (Table 4).

Overall, B. cucurbitae and B. diaphora form a homogenous subset (Table 5) with a significantly greater abundance of total sensilla than the other 4 fruit fly species. B. cucurbitae males have more MI than the other species (Table 5). SC occur both distally and proximally on the maxillary palpus. B. cucurbitae and B. diaphora females had significantly more SC than the other species.

Microtrichia (MI) were the most abundant of all sensilla on the maxillary palpus. The mean MI abundance for B. cucurbitae males was 56% greater than for B. dorsalis females, which had the lowest mean MI abundance (Table 5). Sensilla basiconica (SB) were found distally on the palpus also. SB abundance was greater in males than females for 3 of the 6 species, i.e., B. cucurbitae, B. dorsalis, and B. tau. Mean SB abundance was 31% greater in B. cucurbitae males than in B. minax males (Table 5).

TABLE 2.

ANOVA TABLE FOR SENSILLA LENGTH AND DIAMETER OF SIX BACTROCERA SPECIES (N = 4).

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TABLE 3.

MEAN (±SE) LENGTH AND DIAMETER (MM) OF THE SENSILLA PRESENT ON THE MAXILLARY PALP OF SIX BACTROCERA SPECIES (N = 4).

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Fig. 2.

Microtrichia and sensilla basiconica on maxillary palpi of B. dorsalis, B. minax, and B. scutellata. A. B. dorsalis ♀: microtrichia (MI) and sensilla basiconica (SB) on middle of palpus. B. B. minax ♂: microtrichia (MI) interspersed with sensilla basiconica (SB) covering the palpus surface. C. B. minax ♂: microtrichia (MI) on proximal part palpus. D. B. scutellata ♀: microtrichia (MI) extending beyond and interspersed with sensilla basiconica (SB) on palpus surface. A. 20 µ; B. 20 µm; C. 20 µm; D. 10 µm.

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DISCUSSION

This study describes the morphology and abundance of various sensilla located on the maxillary palpi of adult females and males of 6 fruit fly species, i.e., B. cucurbitae, B. diaphora, B. dorsalis, B. minax, B. scutellata, and B. tau. The results in this study generally conform to those previously reported for other dipteran species (Sukontason et al. 2003; Wasserman & Itagaki 2003; Spiegel et al. 2005; Ngern-Klun et al. 2007; Sukontason et al. 2007; Chen & Fadamiro 2008; Smallegange et al. 2008).

Microtrichia described in this study are similar to those on the maxillary palpi of several Diptera families such as Chrysomya nigripes [Calliphoridae] (Ngern-Klun et al. 2007), Neobelliera bullata (Wasserman & Itagaki 2003), Hydrotaea chalcogaster [Muscidae] (Sukontason et al. 2007), Lutzomyia longipalpis [Psychodidae] (Spiegel et al. 2005), Musca domestica [Muscidae] (Smallegange et al. 2008). The MI are the most abundant on the maxillary palpi of both sexes of the 6 species. They were classified as non-innervated structures in some insect species (Fernandes et al. 2002, 2004; Sukontason et al. 2007; Smallegange et al. 2008). The microtrichia are most often described as mechanoreceptors associated with antennal structures (Hull & Cribb 1997; Siddiqui et al. 2010), and specifically associated with dipteran antennae (Castrejon-Gomez & Rojas 2009; Arzuffi et al. 2008; Chen & Fadamiro 2008; Fernandes et al. 2002; Sukontason et al. 2004, 2007). Recently, Hu et al. (2010) described MI on the antennae of Bactrocera species, which they considered to have a mechanosensory function. MI on the surface of the maxillary palpi of the 6 fruit flies may also be mechanoreceptors.

Fig. 3.

Detailed views of sensilla basiconica and microtrichia on the ventral sides of the maxillary palpi of the 6 Bactrocera species. A. B. cucurbitae ♂: ventral view details of sensilla basiconica (SB) and microtrichia (MI). B. B. diaphore ♂: microtrichia (MI) interspersed with sensilla basiconica (SB) covering the palpus surface. C. B. dorsalis ♂: ventral view detail of sensilla basiconica (SB) and microtrichia (MI). D. B. minax ♀: distal end of palpus of showing sensilla basiconica (SB). E. B. scutellata ♂: sensilla basiconica (SB) covering the palpus surface. F. B. tau ♀: sensilla basiconica (SB) and microtrichia (MI) on distal end of palpus. A. 5 µm; B. 10 µm; C. 10 µm; D. 10 µm: E. 5 µm; F. 10 µm.

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TABLE 4.

ANOVA TABLE FOR NUMBER OF SENSILLA (MICROTRICHIA [MI], SENSILLA BASICONICA [SB] AND SENSILLA CHAETICA [SC]) PER UNIT AREA (10,000 µM2) ON MAXILLARY PALPI OF BACTROCERA FEMALES AND MALES (N = 4).

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TABLE 5.

MEAN (±SE) NUMBER OF SENSILLA (MICROTRICHIA [MI], SENSILLA BASICONICA [SB] AND SENSILLA CHAETICA [SC]) PER UNIT AREA (10,000 µM2) ON MAXILLARY PALPI OF BACTROCERA FEMALES AND MALES (N = 4).

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The mechanosensory function of bristles of the sensilla chaetica have previously been described on the palpi of various species as follows: de Bruyne et al. (1999) (Drosophila), Wasserman & Itagaki (2003) (Neobellieria bullata), and Sukontason (2007) (Hydrotaea chalcogaster). The morphological structure of sensilla chaetica observed in this study is in concordance with those characterized on the palpi of the Dipteran, Neobellieria bullata (Wasserman & Itagaki 2003); therefore, it is likely that this type of sensilla is also involved with mechanosensory function.

The sensilla basiconica seen in this study are similar to SB on the palpi of other Diptera (de Bruyne et al. 1999; Ngern-Klun et al. 2007; Wasserman & Itagaki 2003). SB have also been reported in the antennae of other non-Dipteran insects such as the eucalyptus woodborer, Phoracantha semipunctata [Coleoptera: Cerambycidae] (Lopes et al. 2002); although the exact number of SB on the palpi was undetermined. Kelling et al. (2002) found 75–90 SB on the palpi of the housefly, Musca domestica, and ∼60 SB have been recorded from Drosophila (de Bruyne et al. 1999), similar to the range (55–117) found in the 6 species of Bactrocera. The presence of wall pores suggest that SB have an olfactory role (Zacharuk 1985; Lopes et al. 2002). The presence of SB with dendritic branches also suggests an olfactory function, which has been verified by the use of electrophysiological recordings in Phoracantha semipunctata (F) [Coleoptera: Cerambycidae] (Lopes et al. 2002). However, this type of sensilla is similar to the sensilla in the palpi of other Diptera (de Bruyne et al. 1999; Ngern-Klun et al. 2007; Wasserman & Itagaki 2003). With the exception of B. cucurbitae, the sensilla occurred in nearly equal numbers on both sexes, which suggests that SB may have host discrimination olfactory functions.

In conclusion, the maxillary palpi of B. cucurbitae, B. diaphora, B. dorsalis, B. minax, B. scutellata, and B. tau are equipped with morphologically similar sensilla. Sensilla chaetica and microtrichia on the palpi of females and males suggest the importance of mechanoreception. The distally distributed sensilla basiconica are not as numerous as the microtrichia, but the presence of cuticular pores suggests an olfactory function. Those results will provide information needed for ongoing studies of behavioral responses of fruit flies to environmental stimuli.

ACKNOWLEDGMENTS

This study was funded in part by the National Basic Research Program of China (2009CB125903, 2009CB119200), Natural Science Foundation of Chongqing (CSTC, 2009BA1042), the Program for Changjiang Scholars and Innovative Research Team in University (IRT0976), and the earmarked fund for Modern Agro-Industry (Citrus) Technology Research System of China to Jin-Jun Wang. We thank Mr. Stephen Sanders for his time to critically read the revised manuscript.

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Guo-Na Zhang, Helen Hull-Sanders, Fei Hu, Wei Dou, Jin-Zhi Niu, and Jin-Jun Wang "Morphological Characterization and Distribution of Sensilla on Maxillary Palpi of Six Bactrocera Fruit Flies (Diptera: Tephritidae)," Florida Entomologist 94(3), 379-388, (1 September 2011). https://doi.org/10.1653/024.094.0301
Published: 1 September 2011
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