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Cuticular structures on antennae of the bot , Portschinskia magnifica (Diptera: Oestridae)

ARTICLE in PARASITOLOGY RESEARCH · JULY 2012 Impact Factor: 2.1 · DOI: 10.1007/s00436-012-3004-9 · Source: PubMed

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ORIGINAL PAPER

Cuticular structures on antennae of the bot fly, Portschinskia magnifica (Diptera: Oestridae)

Dong Zhang & Qi-Ke Wang & De-Fu Hu & Kai Li

Received: 9 April 2012 /Accepted: 8 June 2012 /Published online: 10 July 2012 # Springer-Verlag 2012

Abstract Portschinskia magnifica Pleske, 1926, is an en- described in the oestrid funiculus. Interestingly, these dangered subcutaneous parasitic fly of voles that mimics bristles can appear as multi-tipped short structures in bumblebees in appearance. Although the importance of some individuals. P. magnifica lacks sensory pits that antennae in Diptera has been repeatedly stressed, there is are usually abundant in other oestrid . The size, still a lack of morphology information of this group, let number, and distribution of sensilla on the male and alone this species. Antennae of adult P. magnifica were female antennal funiculus are provided here, armed with studied with a stereoscopic microscope and scanning elec- a discussion of their presumable sensilla functions and tron microscope. Six subtypes of antennal sensilla were evolutionary trends. observed on the funiculus and arista (one subtype of trichoid sensilla, one subtype of basiconic sensilla, and four subtypes of coeloconic sensilla). Sensilla on the antennal funiculus Introduction from one sample of both male and female flies were also mapped. Female P. magnifica bear a larger number of sen- Portschinskia magnifica Pleske, 1926, is one of the largest silla than males, and more sensilla were discovered on the parasitic flies that belong to the subfamily Hypodermatinae, posterior surface than on the anterior surface. However, Oestridae. Adult Portschinskia flies strikingly resemble bum- what make this species special are the distinct structures blebees in size and shape (Fig. 1b), which suggests mimicry. and new morphological characteristics discovered in the The larvae of this genus are subcutaneous parasites which antenna. The antennal funiculus of P. magnifica is complete- typically spend their larval stages in the skin or soft tissues ly enveloped by an antennal pedicel. A large number of of rodents and lagomorphs. P. magnifica mainly infests the branched or unbranched trichoid and basiconic sensilla are field vole, Apodemus speciosus (Rodentia: Muridae). Gener- identified on the antennal funiculus. These two make the ally, only one larva can be found on the ventral surface near most numerous types of sensilla distributed all over the the tail of voles (Colwell et al. 2006). Larval development funicular surface. P. magnifica has the most coeloconic requires approximately 2 months, and there is a distinct pupal sensilla subtypes in previously studied oestrid flies. A total diapause for overwintering. Zumpt (1965) indicated that of four subtypes of coeloconic sensilla are found, with infested mice are sluggish and easily approached, thus making subtype I and subtype II on the proximal and middle part them susceptible to predation; he also pointed out that “large” of the antennal funiculus and subtype III and subtype IV on numbers of larvae often cause death among mice. the antennal arista. Two large bristles that resemble mecha- P. magnifica that has been studied in this paper was listed noreceptors on the proximal two antennal segments located by Colwell et al. (2009) as a rare and endangered bot close to the arista are a unique feature. This has never been species. It is endemic to Asia and recorded for the first time in Beijing. Currently, there is a paucity of information on : : : oestrid fly sensory organs (Hunter and Adserballe 1996; D. Zhang Q.-K. Wang D.-F. Hu K. Li (*) Fernandes et al. 2002; Ngern-klun et al. 2007; Poddighe et Department of Zoology, College of Biological Sciences al. 2010). This situation prevents a deeper understanding of and Biotechnology, Beijing Forestry University, – Qinghua East Road No. 35, Mailbox 162, Beijing 100083, China the biology, host parasite interactions, and morphology of e-mail: [email protected] this group. Since the antennal sensory organs are one of the 1652 Parasitol Res (2012) 111:1651–1659

Fig. 1 Light micrographs of the body, heads, and antennae of adult P. magnifica. a Head of male P. magnifica. b Lateral view of male adult P. magnifica. c Head of female P. magnifica. d Magnification of the male antenna. e Magnification of the female antenna. f Magnification of the female antenna, showing the position of the funiculus inside the scape. g The opening of the female scape, showing the position of the arista. Ar arista, Fn funiculus, Pd pedicel, Sc scape. Scale bar02mmina and c, 5 mm in b, 0.5 mm in d, f, and g, and 1 mm in e

main sources for Diptera to pick up outside information (Canon, Inc., Tokyo, Japan) coupled with the stereoscopic (Boo 1980; Amer and Mehlhorn 2006; Guha et al. 2012; microscope for further analysis. Wang et al. 2012), this study looks at the fine antennal To prepare for observation with the scanning electron structure of adult P. magnifica. Descriptions of cuticular microscope (SEM), the heads of ten pinned flies (males05, structures and, in particular, sensilla with presumed olfacto- females05) were first cut off and rinsed in phosphate-buffered ry function, are reported herein. saline (PBS) buffer (pH 7.4) to remove surface debris. There- after, for further cleaning, the funiculus was dissected from the head and cleaned with detergent. Specimens were then Materials and methods rinsed with PBS and dehydrated in a graded ethanol series (30, 50, 70, 80, 90, 95, and 100 %, in each case for 2 h), Both male and female adult bot flies (P. magnifica) were mounted on stubs with double-sided adhesive tape, left in captured during June of 2006, 2009, and 2011 in Songshan a desiccator overnight to dry thoroughly, and then coated Mountain or Xiaolongmen, Beijing, China. The specimens with gold (Ngern-klun et al. 2007). Samples were ob- were pinned as museum samples and air-dried on site. served using a HITACHI S34Q scanning electron micro- The morphology of the antenna was studied by using an scope (Hitachi Corp., Tokyo, Japan) at the Microscopy Core Olympus SZX16 stereoscopic microscope (Olympus Corp., Facility, Biological Technology Center, Beijing Forestry Uni- Tokyo, Japan). A series of photographs of continuous versity (Beijing, China). Micrographs of antennae were taken; sequences was taken by a Cannon 500D digital camera the dimensions of the sensilla were measured. Abundant Parasitol Res (2012) 111:1651–1659 1653 distribution and measurements of the antennal sensilla types structures (Fig. 5a), a characteristic to distinguish microtri- were compared between males and females. chiae from basiconic sensilla and trichoid sensilla. Different All the micrographs and ultra-micrograph files were an- from any sensilla, the microtrichiae gradually tapers into a alyzed on a standard Windows XP platform by Adobe sharply pointed tip. An observation of the antennal funiculus Photoshop CS2 (Adobe Systems, Inc., San Jose, CA, reveals that a total of four morphological types of sensilla are USA) and Helicon Focus (Helicon Soft Ltd., Kharkov, scattered on the entire funicular surface, including trichoid Ukraine) for Windows. The sequence series of light photo- sensilla, basiconic sensilla, and two kinds of coeloconic graphs was fed to Helicon Focus to compose images with sensilla. more field depth. The types, original distribution, and num- The arista (Ar) consists of two short basal segments and ber of sensilla from a single specimen of both sexes were one long distal segment that twisted towards the tip marked and presented in Fig. 6. (Fig. 2d). The surface of the aristal segment is also covered The terminology and nomenclatures used to describe with microtrichiae. Two subtypes of cone-shaped coelo- antennal morphology and classification of sensilla types in conic sensilla are found at the base. this study follow the ones used by Hunter and Adserballe Trichoid sensilla and basiconic sensilla are located random- (1996), Shanbhag et al. (1999), and Setzu et al. (2011). ly all over the funicular surface (Fig. 6), while the two types of coeloconic sensilla are only distributed on the proximal and middle part. The ventral surface in both sexes has more Results sensilla than the dorsal surface. The number of sensilla on the funicular surface of P. magnifica shows sexual dimor- General description of the antenna of P. magnifica phism. All four types of funicular sensilla were found on both sexes, but females have a significantly larger number than One of the largest species in Calyptratae, P. magnifica,is males. However, Fig. 6 was made according to antennal SEM equipped with a pair of antennae located on the frontal images of two individuals, the images could not cover the region of the head between the compound eyes (Fig. 1a, c, whole surface area, and inaccuracy could not be avoided. d, and e). Each antenna consists of three well-developed Two bristles are found on the antennal funiculus near the segments, a proximal scape (Sc), a pedicel (Pd), and a arista in some specimens. The larger one is about 152.4± flagellum; the latter is further divided into a funiculus (Fn) 11.2 μm in length and 9.4±3.2 μm in width, and the smaller and an arista (Ar) (Fig. 2d). one is about 75.4±8.6 μm in length and 4.9±1.8 μmin The scape is the shortest segment with two clusters of long width (Fig. 2f, g). bristles, about 200 μm in length and situated on the anterior side (Fig. 1d, e). The pedicel of P. ma gn if ic a envelopes the Trichoid sensilla funiculus completely and thus is easily mistaken as the third segment of the antenna (Fig. 1f, g). The pedicel bears micro- Trichoid sensilla (Tr) are the largest cuticular apparatus of all trichiae while two kinds of bristles are also found on this the types of sensilla found on the antennal funiculus of P. segment; the shorter ones with a smooth surface (Fig. 2a,c) magnifica. Most of the Tr on the P. magnifica funiculus are are usually found on the posterior surface, whereas the longer, straight, elongated, hair-like structures that arise from con- grooved ones are identified on the anterior surface (Fig. 2a,b). spicuous wide bases (Fig. 3a, b, c), while some of the Tr are The structure at the base of these bristles is similar to with short branches. Tr display no significant sexual dimor- the tactical hairs in other dipteran families, such as phism in size (18.83±2.63 μm long, with a 3.21±0.32 μm Muscidae (Sukontason et al. 2004), Calliphoridae basal diameter in females; 19.04±3.88 μm long, with a 3.86± (Sukontason et al. 2007), and Cuterebridae (Fernandes 0.46 μm basal diameter in males). Tr are the commonest et al. 2002), implying that they are capable of receiving sensilla type followed by basiconic sensilla; we counted 102 mechanical stimulations. Tr per antenna in males (36 in the anterior surface, 66 in the Even though the antennal funiculus is surrounded by a posterior surface) and 160 in females (68 in the anterior pedicel, numerous sensilla still can be found on this segment. surface, 92 in the posterior surface) on Fig. 6. These sensilla The antennal funiculus is roughly subspherical but can be are mainly distributed over the middle and distal part of the divided into two aspects: anterior surface (An) (Fig. 2d)and funiculus on both male and female flies (marked by stars in posterior surface (Po) (Fig. 2d). The antennal funiculus meas- Fig. 6a, b, c, and d). ures about 335–362 μm in length, 584–597 μminwidth,and 220–233 μm in thickness, and the arista is 1,025–1,045 μm Basiconic sensilla long. The funicular surface is densely covered with microtrichiae Unlike Tr, basiconic sensilla (Ba) found on the P. magnifica (27.15±7.34 μm in length) that arise from scale-like surface funiculus are shorter, curved, and sharp-tipped digitiforms, 1654 Parasitol Res (2012) 111:1651–1659

Fig. 2 SEM micrograph of features on the pedicel, funiculus, and arista of P. magnifica. a Anterior and posterior view of the pedicle. b Basal section of a bristle on the anterior surface; the distal section of the bristle is shown in the box. c Bristle on the posterior surface. d Anterior and posterior view of the funiculus and arista; the distal end of the arista is shown in the box. e Magnification of the anterior side of the funiculus; notice the position of two large bristles and arista. f Magnification of the two bristles showing the longitudinal grooves. g Multi- tipped shortened bristle on the funiculus. An anterior surface, Ar arista, Br bristle, Fn funicu- lus, Po posterior surface. Scale bar00.5 mm in a;10μminb, 5 μminthebox;6μminc; 300 μmind and 10 μm in the box; 100 μmine,50μminf, and 10 μming

usually with one long branch or several small branches diameter of 2.45±0.16 μm near its base, 2.71±0.17 μm (Fig. 4b, c, d). A larger magnification displays densely popu- at the tip in females; 3.90±1.06 μm long, with a diam- lated pores on the surface (Fig. 4c, d). The length and basal eter of 1.98±0.13 μm near its base, 2.53±0.43 μm at the diameter of Ba vary between sexes (10.92±2.44 μmlong, tip in males) are easily recognizable by the irregularly with a diameter of 2.72±0.16 μm near its base in females; patented apical dilatations (Fig. 5b). Co II (6.65± 11.85±1.35 μm long, with a diameter of 3.28±0.16 μmnear 2.61 μm long, with a diameter of 2.56±0.62 μm near its base in males). Statistics show sexual dimorphism in these its base in females; 5.06±1.02 μm long, with a diameter sensilla; a total of 187 were found in females (79 in the of 2.33±0.35 μm near its base in males) are character- anterior surface, 108 in the posterior surface) and 62 in males ized by deep, irregular, longitudinal grooves in their (23 in the anterior surface, 39 in the posterior surface). Similar walls over the distal one third to one half of the sensilla to Tr, they are also distributed in the middle and distal part of (Fig. 5c). Co I and Co II are found intermixed with each the antennal funiculus but are most concentrated around the other in the proximal and middle part of the antennal arista, close to the antennal pedicel opening, where no other funiculus located in shallow depressions 9.70–15.31 μm type of sensilla exists (Fig. 4a). in diameter (Fig. 5a). There are 11 Co I in males and 16 in females, and 10 Co II in males and 16 in females, Coeloconic sensilla making them the least sensilla subtypes on the funiculus. Co III are located on both male and female aristae while Four subtypes of coeloconic sensilla (Co I, Co II, Co III, Co IV are only found on female aristae. Co III (2.77± and Co IV) can be distinguished according to the shape 0.51 μm long, 2.25±0.15 μm in basal diameter in and size (Fig. 4b, c, e, and g), with two on the funiculus females; 2.83±0.21 μm long, 2.27±0.36 μm in basal diameter and two on the arista. Co I (4.39±0.59 μm long, with a in males) are small blunt-tipped cones situated in conspicuous Parasitol Res (2012) 111:1651–1659 1655

Fig. 3 SEM micrograph of Tr on P. magnifica funiculus. a The distribution of Tr in microtrichiae. b Tr without branches. c Tr with a few branches. d Tr with multiple branches. Mt microtrichia, Tr trichoid sensilla. Scale bar0 6 μmina and 5 μminb–d

depressions at the base of the arista (Fig. 5d, e), while Co IV females) are triangular in shape that sit on the proximal– (4.51±1.33 μm long, 2.58±0.91 μm in basal diameter in middle part of the arista (Fig. 5f,g).

Fig. 4 SEM micrograph of Ba on P. magnifica funiculus. a Distribution of Ba in the area close to the arista. b Ba without branches. c Ba with short branches. d Ba with one long branch. Ba basiconic sensilla, Mt microtrichia. Scale bar0 20 μm a,5μminb and c,2μm in d 1656 Parasitol Res (2012) 111:1651–1659

Fig. 5 SEM micrograph of four subtypes of Co on P. magnifica funiculus. a Distribution of Co on the funicular surface. b Magnification of Co I. c Magnification of Co II. d An overview of the aristal base showing Co III. e Magnification of Co III. f An overview of the arista showing Co IV. g Magnification of Co IV. Co I–Co IV coeloconic sensilla subtype I–IV. Scale bar015 μm in a,3μminb, 1.5 μminc, 20 μmind and f,2μmine, and 5 μming

Discussion Most oestrids have relatively minute antennae, especially in comparison with other muscoid flies whose antennal Sensory organs on the antennae of are responsible for scape and pedicel are usually short, inconspicuous, and the recognition and acceptance of stimuli involved in feed- haired. But the enlarged antennal pedicel completely envel- ing, aggregation, copulation, parasitism, and phoresy. These oping the antennal funiculus in P. magnifica is a genus- stimuli include odors, humidity, temperature, mechanical specific characteristic that has rarely been discovered in stimuli, and infrared radiation (Schmitz and Bleckmann oestrid species. Only a few similar cases have been reported 1997; Hallberg and Hansson 1999). This study shows that a so far. In Gasterophilus nigricornis (Gasterophilinae) variety of sensillar types exist on the antenna of P. magnifica, (Zhang et al. 2012) and Oestrus ovis (Oestrinae) (Poddighe which is distinct in many ways compared to other muscoid or et al. 2010), antennal pedicels are slightly flattened and tend even oestrid species. An unusual aspect of P. ma gn if ic a is the to cover the base of the antennal funiculus. In Hypoderma enlarged antennal pedicel almost encapsulating the funiculus, bovis, the proximal part of the globular antennal funiculus is so that only the arista is visible in profile. The lack of pits on hidden within the cup-shaped antennal pedicel (Hunter and the antennal funiculus and the four subtypes of funicular and Adserballe 1996). The function of this structure might be aristal Co also contribute to its specialty. Another characteris- similar to funicular depressions (pits or sacculus) which tic is the two long, stout bristles located at the base of the were suggested to trap odor molecules, facilitate odor de- arista. By current literature, P. magnifica is the only species in tection (Hunter and Adserballe 1996), and protect the fragile Oestridae with branched sensilla; both Tr and Ba may bear sensilla from mechanical irritation or damage (Shanbhag et one to a few long or short branches. al. 1995). Parasitol Res (2012) 111:1651–1659 1657

No sensory pits are discovered on the antennae of P. D. hominis (Fernandes et al. 2002: Fig. 2d). Co IV, on both magnifica (Fig. 6); however, the elevated pit number on the male and female arista with near-triangular profile, are anal- antennal funiculus is considered to be a synapomorphic trait of ogous to those found in the slot of the arista of G. nigricor- the (Hunter and Adserballe 1996). In H. bovis nis (Zhang et al. 2012), while the grooved Co II and cone- females, the anterodorsal funicular surface is estimated to shaped Co IV are only identified on P. magnifica. Even have 300 pits (Hunter and Adserballe 1996). About 60–78 though the arista usually bears no sensilla (Foelix et al. pits are identified on G. nigricornis funiculus (Zhang et al. 1989), a variety of sensilla are discovered on the arista of 2012). In contrast, few pits (mostly 2–14) are recorded on the D. hominis (Diptera: Oestridae) (Fernandes et al. 2002). A antennal funiculus of female flies in superfamily Muscoidea meticulous study of the sensory neuron structure in the arista (Ross and Anderson 1987; Ross 1992;Lewis1971; Bay and shaft of Drosophila melanogaster provides the physiological Pitts 1976;Beenetal.1988; Kaib 1974; Dethier et al. 1963). evidence for potential chemoreceptive or thermo/hygrorecep- The lack of pits on the antennal funiculus of P. magnifica and tive function in the arista (Foelix et al. 1989). Co on antennal

Dermatobia hominis (Fernandes et al. 2002) may indicate a funiculus are generally believed to be chemo- (CO2), thermo-, special case. However, other species of Oestridae, as well as or hygroreceptive (Zacharuk 1985; Blackwell et al. 1992; representative species of other families in Calyptratae (e.g., Cribb 1997; Keil 1999). As a result, on the P. magnifica arista, Calliphoridae, Mystacinobiidae, Rhinophoridae, Sarcophagi- coeloconic sensilla are likely to have the same functions. dae, and Tachinidae) need to be studied in order to test this The bristles (Fig. 2f, g) have never been discovered at the hypothesis. base of the arista in oestrid species (Hunter and Adserballe P. magnifica has the most subtypes of Co in the currently 1996; Poddighe et al. 2010; Zhang et al. 2012), because reported oestroid species. Co I with enlarged irregularly bristles are usually located in the antennal scape and antennal patented heads resemble the Co with bulbous extremity in pedicel as mechanoceptors (Shanbhag et al. 1999;Hunterand

Fig. 6 Types, number, and distribution of four types of sensilla on the anterior and posterior surfaces of male and female adult P. magnifica. a Anterior surfaces of male. b Posterior surfaces of male. c Anterior surfaces of female. d Posterior surfaces of female 1658 Parasitol Res (2012) 111:1651–1659

Adserballe 1996;Schneider1964;Hallemetal.2006). On the Bay DE, Pitts CW (1976) Antennal olfactory sensilla of the face fly antennal funiculus of five male and five female P. magnifica Musca autumnalis De Geer (Diptera: Muscidae). Int J Morphol Embryol 5:1–16 studied, all the females and two males bear long bristles. Been TH, Schomaker CH, Thomas G (1988) Olfactory sensilla on the Interestingly, the bristles on the other males are short and antenna and maxillary palp of the sheep head fly, Hydrotaea multi-tipped, almost completely concealed by microtrichiae. irritans (Fallen) (Diptera: Muscidae). Int J Insect Morphol – Both bristles are significantly smaller than the bristles on the Embryol 17:121 33 Blackwell A, Mordue AJ, Mordue W (1992) Morphology of the first two antennal segments, while the longitudinal grooves on antennae of two species of biting midge: Culicoides impunctatus the surface may suggest their homology. Mechanoreceptors (Goetghebuer) and Culicoides nubeculosus (Meigen) (Diptera: are suggested to control the movement and direction of certain Ceratopogonidae). J Morphol 213:85–103 segments of the antenna in aphids (Hemiptera: Aphididae) Boo KS (1980) Antennal sensory receptors of the male mosquito, Anopheles stephensi. Z Parasitenkd 61:249–264 (Zhang and Zhang 2000; Bromely et al. 1980). Although no Bromely AK, Dunn JA, Anderson M (1980) Ultrastructure of the muscles are found in the antennal funiculus, it is still possible antennal sensilla of aphids. II. Trichoid, chordotonal and campa- to observe some movements in the antennal flagellum, which niform sensilla. Cell Tissue Res 205:493–551 is brought about by the flow of hemolymph (Schneider 1964). Colwell DD, Hall MJR, Scholl PJ (2006) A synopsis of the biology, hosts, distribution, disease significance and management of the These bristles could have similar function in the antennal genera. In: Colwell DD, Hall MJR, Scholl PJ (eds) The oestrid flagellum. flies: biology, host-parasite relationships, impact and manage- The unbranched sensilla Tr and Ba on the P. magnifica ment. CABI Publishing, Oxfordshire, pp 220–305 funiculus resemble those found in O. ovis (Poddighe et al. Colwell DD, Otranto D, Stevens JR (2009) Oestrid flies: eradication and extinction versus biodiversity. Trends Parasitol 25:500–504 2010), H. bovis (Hunter and Adserballe 1996), and G. nigri- Cribb BW (1997) Antennal sensilla of the female biting midge: For- cornis (Zhang et al. 2012). But the presence of branched Tr cipomyia (Lasiohelea) townsvillensis (Taylor) (Diptera: Ceratopo- and Ba is for the first time shown in oestrid species. However, gonidae). Int J Insect Morphol Embryol 25:405–425 branched Tr are reported by Ross and Anderson (1987)onthe Dethier VG, Larsen JR, Adams JR (1963) The fine structure of the olfactory receptors of the blowfly. In: Zotterman Y (ed) Olfaction antennal funiculus of Delia radicum. Also, during later devel- and Taste. Pergamon Press, Oxford, pp 105–114 opmental stages of mosquito larvae, many trichoid sensilla Fernandes FF, Linardi PM, Chiarini-Garcia H (2002) Morphology of develop multiple branched shafts (McIver and Beech 1986; the antenna of Dermatobia hominis (Diptera: Cuterebridae) based – Green and Hartenstein 1997). The number of branched Tr is on scanning electron microscopy. J Med Entomol 39:36 43 Foelix RF, Stocker RF, Steinbrecht RA (1989) Fine structure of a relatively small, while most of the Ba are with short or long sensory organ in the arista of Drosophila melanogaster and some branches (Fig. 4c, d). It is tempting to suggest that the other dipterans. 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