Abstract
Antennae and maxillary palps are the most important chemical reception organs of flies. So far, the morphology of antennae and maxillary palps of flies of most feeding habits have been well described, except for that of relatively rare aquatic predatory species. This study describes sensilla on antennae and maxillary palps of three aquatic predatory Lispe species: Lispe longicollis, L. orientalis and L. pygmaea. Types, distribution, and density of sensilla are characterised via light and scanning electron microscopy. One type of mechanoreceptors is found on antennal scape. Mechanoreceptors (two subtypes) and one single pedicellar button (in L. pygmaea) are located on antennal pedicel. Four types of sensilla are discovered on antennal postpedicel: trichoid sensilla, basiconic sensilla (three subtypes), coeloconic sensilla and clavate sensilla. A unique character of these Lispe species is that the coeloconic sensilla are distributed sparsely on antennal postpedicel. Mechanoreceptors and basiconic sensilla are observed on the surface of maxillary palps in all three species. We demonstrated clear sexual dimorphism of the maxillary palps in some of the Lispe species, unlike most other Muscidae species, are larger in males than females. This, along with their courtship dance behaviour, suggest their function as both chemical signal receiver and visual signal conveyer, which is among the few records of a chemical reception organ act as a signal conveyer in insects.
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Introduction
Antennae and maxillary palps are the main chemical reception organs of flies on which numerous sensilla of various types can be found1,2. These organs play indispensable roles in the lives of flies in searching for food sources, mates, oviposition sites as well as other key life history stages2,3,4,5,6,7,8,9,10,11. Flies are under high selection pressure for receiving sufficient chemical signals and/or cues that are associated with their life history, such as searching for mates12, foods13 or hosts14, and this could influence the morphology of the antennae15. Flies have a wide range of feeding habits including saprophagy, phytophagy, parasitism, hematophagy and predatory16,17, making them ideal models for studying the adaptation of insect olfactory organs according to different olfactory requirements. It is well documented that flies of different feeding habits have different antennal shape and sensillar types7,8,9,10,11. Structure of antennae and maxillary palps, especially the distribution and morphology of sensilla have been documented in detail in saprophagy, phytophagy and parasitismflies7,8,18,19, but few researches have focused on the predatory flies.
The species of genus Lispe Latreille (Diptera: Muscidae) are among the relatively rare predatory flies, closely associated to aquatic and subaquatic habitats20. Adult Lispe flies are commonly found around the margin of ponds, lakes, streams or seashore and prey on various insects including several mosquito species, such as anopheline and chironomid21,22. Visual perception is comparatively more important for these flies in hunting for their flying preys than chemical cues, yet they should still rely on their antennae and maxillary palps for olfactory cues and signals. Therefore, it is expected that the olfactory perception requirements of Lispe flies are largely different from that of saprophytic and parasitic flies, and this presumably results in specific antennal morphology adaptations. For example, Lispe neimongola Tian et Ma9 has two conspicuous distinctions: the absence of coeloconic sensilla (Co) and enlarged spoon-like maxillary palps. It is unclear whether these morphological characteristics are common among other Lispe flies.
In this study, we describe the morphology of antennae, maxillary palps and sensilla located on them among three common Lispe species: Lispe longicollis Meigen, L. orientalis Wiedemann, and L. pygmaea Fallén21,23,24. Combined with the data of L. neimongola9, we compare the morphology of antennal and maxillary palps of Lispe with other Muscoidea species, in order to reveal their morphological characteristics adapted to the aquatic predatory life style.
Results
General description of the antenna and maxillary palp
L. longicollis, L. orientalis and L. pygmaea all bear a pair of aristate antennae situated at the front of their heads, between two compound eyes. Antennal morphology is composed of three segments: a short proximal scape (Sc), a pedicel (Pd), and a distal flagellum possessing an elongated antennal postpedicel (Ppd) with a slender antennal arista (Ar). A pair of enlarged spoon-like maxillary palps arises at the distal part of the rostrum, a part of the proboscis (Fig. 1a,c,e, Supplementary Fig. S1).
Features on heads and antennae of adult Lispe longicollis, L. orientalis and L. pygmaea. Frontolateral view of (a) male L. longicollis, (c) L. orientalis, and (e) L. pygmaea heads by stereoscopic microscope. SEM micrograph of (b) male L. longicollis, (d) L. orientalis, and (f) L. pygmaea antenna, showing the posterior surface. Ar arista, Mp maxillary palp, Pd pedicel, Ppd postpedicel, Sc scape. Scale bars: (a,c,e) = 500 μm; (b,d,f) = 150 μm.
Scape and pedicel
The antennal scape is the most proximal and the shortest segment (Fig. 1b,d,f), with dense acuminate microtrichia and sporadic cylindrical mechanoreceptors (Mr) with longitudinally grooves (Fig. 2c).
SEM micrographs of features on the antennal scape and pedicel of adult Lispe longicollis, L. orientalis and L. pygmaea. (a) Anterior surface of antennal scape and pedicel of male L. longicollis, arrows showing mechanoreceptors. (b) Anterior surface of antennal scape and pedicel of male L. orientalis, arrows showing mechanoreceptors. (c) Mechanoreceptors on antennal scape of male L. pygmaea. (d) Pedicellar button of male L. pygmaea. Mr mechanoreceptors, Mr I subtype I mechanoreceptor, Mr II subtype II mechanoreceptor, Mt microtrichia, PB pedicellar button. Scale bars: (a,b) 50 μm; (c) 10 μm; (d) 5 μm.
The second segment of the antenna is the antennal pedicel, also covered with microtrichia. Two subtypes of mechanoreceptors can be distinguished by their shape and size on the antennal pedicel (Fig. 2a,b). Usually there are one or two longer mechanoreceptors (Mr I) located on the antennal pedicel. Shorter mechanoreceptors (Mr II) are morphologically like those found on antennal scape, but are straighter in shape and more variable in length.
One pedicellar button (PB) is found in pedicellar recess and near the pedicellar cleft after separated antennal pedicel from antennal postpedicel in L. pygmaea. Pedicellar button consists of a circular central dome and a slightly convex peripheral ring with a small bunch of peripheral microtrichia (Fig. 2d).
Postpedicel
The antennal postpedicel is the most prominent segment of the antenna on which several types of sensilla are found (Figs. 3a,b, 4a,b, 5a,b, Supplementary Fig. S2). It can be divided into two regions, anterior surface, and posterior surface. The surface of antennal postpedicel is covered with dense microtrichia, amongst which four types of sensilla can be found: trichoid sensilla (Tr) (Figs. 3c, 4c, 5c), basiconic sensilla (Ba, subtype I, II and III) (Figs. 3d–f, 4d,e, 5d–f), coeloconic sensilla (Co) (Figs. 3g, 4f, 5g), and clavate sensilla (Cl) (Figs. 3h, 4g, 5h).
SEM micrographs of features on antennal postpedicel of male Lispe longicollis. (a) Posterior surface of antennal postpedicel. (b) Distribution of different types of sensilla on antennal postpedicel. (c) Trichoid sensilla, box showing micropores on the surface. (d) Subtype I basiconic sensilla, box showing micropores on the surface. (e) Subtype II basiconic sensilla, box showing micropores on the surface. (f) Subtype III basiconic sensilla, box showing micropores on the surface. (g) Coeloconic sensilla. (h) Clavate sensilla, box showing micropores on the surface. Ba I subtype I basiconic sensilla, Ba II subtype II basiconic sensilla, Ba III subtype III basiconic sensilla, Co coeloconic sensilla, Cl clavate sensilla, Mt microtrichia, Tr trichoid sensilla. Scale bars: (a) 150 μm; (b) 10 μm; (c–f) 2.5 μm, 0.5 μm in box; (g) 2.5 μm.
SEM micrographs of features on antennal postpedicel of male Lispe orientalis. (a) Posterior surface of antennal postpedicel. (b) Distribution of different types of sensilla on antennal postpedicel. (c) Trichoid sensilla, box showing micropores on the surface. (d) Subtype I basiconic sensilla, box showing micropores on the surface. (e) Subtype II basiconic sensilla, box showing micropores on the surface. (f) Coeloconic sensilla. (g) Clavate sensilla, box showing micropores on the surface. Ba I subtype I basiconic sensilla, Ba II subtype II basiconic sensilla, Co coeloconic sensilla, Cl clavate sensilla, Mt microtrichia, Tr trichoid sensilla. Scale bars: (a) 150 μm; (b) 10 μm; (c–e,g) 2.5 μm, 0.5 μm in box; (f) 2.5 μm.
SEM micrographs of features on antennal postpedicel of male Lispe pygmaea. (a) Posterior surface of antennal postpedicel. (b) Distribution of different types of sensilla on antennal postpedicel. (c) Trichoid sensilla, box showing micropores on the surface. (d) Subtype I basiconic sensilla, box showing micropores on the surface. (e) Subtype II basiconic sensilla, box showing micropores on the surface. (f) Subtype III basiconic sensilla, box showing micropores on the surface. (g) Coeloconic sensilla. (h) Clavate sensilla, box showing micropores on the surface. Ba I subtype I basiconic sensilla, Ba II subtype II basiconic sensilla, Ba III subtype III basiconic sensilla, Co coeloconic sensilla, Cl clavate sensilla, Mt microtrichia, Tr trichoid sensilla. Scale bars: (a) 150 μm; (b) 10 μm; (c–f,h) 2.5 μm, 0.5 μm in box; (g) = 2.5 μm.
Maxillary palp
Maxillary palps of males are swollen in the three Lispe species, and can be regarded as a representative character of Lispe. The ladle-shaped maxillary palps of L. orientalis with near right-angled edge have the highest degree of swelling among the three species (Figs. 1c, 6a). Comparatively, spoon-shaped maxillary palps of L. longicollis with a nearly round edge have a lower degree of swelling (Fig. 1a), and that of L. pygmaea are slightly swollen (Figs. 1e, 6b). The swelling degree of the maxillary palp are significantly different among the three species and between sexes (Table 1, Fig. 7a, F5,24 = 39.99, P < 0.001; species: F2,24 = 77.05, P < 0.001; sex: F1,24 = 18.96, P < 0.001; species × sex: F2,24 = 13.44, P < 0.001), and much larger than typical Muscidae species such as Musca domestica and Fannia hirticeps (Table 1).
SEM micrographs of features on maxillary palps of Lispe orientalis and L. pygmaea. (a) Posterior surface on maxillary palp of male L. orientalis. (b) Posterior surface on maxillary palp of male L. pygmaea. (c) Different types of sensilla on maxillary palp of male L. orientalis. (d) Different types of sensilla on maxillary palp of male L. pygmaea. (e) Subtype IV basiconic sensilla of male L. orientalis. (f) Subtype IV basiconic sensilla of L. pygmaea. Mr III subtype III mechanoreceptor, Mt microtrichia, Ba IV subtype IV basiconic sensilla. Scale bars: (a,b) = 100 μm; (c,d) = 20 μm; (e,f) = 5 μm.
Two-way ANOVA results of characters of maxillary palps among three Lispe species and sexes. (a) Swelling degree of maxillary palps of the three species among three species and sexes. Male L. orientalis has significantly larger swelling than females (F5,24 = 39.99, P < 0.001; species: F2,24 = 77.05, P < 0.001; sex: F1,24 = 18.96, P < 0.001; species × sex: F2,24 = 13.44, P < 0.001). (b) The ratio of maxillary palp length to body length (LMP/BL) among three species and two sexes. Male L. orientalis has significantly longer maxillary palps than females (F5,24 = 3.98, P = 0.0090; species: F2,24 = 3.49, P = 0.05; sex: F1,24 = 1.41, P = 0.25; species × sex: F2,24 = 5.75, P = 0.0091). (c) The ratio of maxillary palp width to body length (WMP/BL) among three species and two sexes. Male L. orientalis has significantly wider maxillary palps than females (F5,24 = 63.58, P < 0.001; species: F2,24 = 111.78, P < 0.001; sex: F1,24 = 34.23, P < 0.001; species × sex: F2,24 = 1.26, P < 0.001). Different lower-case letters mean significant differences.
Our results show that compared to their body length, the relative maxillary palp length and the relative width are different between sex and among these Lispe species (Fig. 7b,c). There are significant differences in the ratio of maxillary palp length to body length (LMP/BL) (Fig. 7b, species: F2,24 = 3.49, P = 0.05; sex: F1,24 = 1.41, P = 0.25; species × sex: F2,24 = 5.75, P = 0.0091) and the ratio of maxillary palp width to body length (WMP/BL) among three species and between sex (Fig. 7c, species: F2,24 = 111.78, P < 0.001; sex: F1,24 = 34.23, P < 0.001; species × sex: F2,24 = 1.26, P < 0.001). These results showed strong sexual dimorphism of swelling degree (post hoc test, L. orientalis: P < 0.001, L. longicollis: P = 0.507, L. pygmaea: P = 0.103), LMP/BL (post hoc test, L. orientalis: P = 0.005, L. longicollis: P = 0.548, L. pygmaea: P = 0.108), and WMP/BL (post hoc test, L. orientalis: P < 0.001, L. longicollis: P = 1.000, L. pygmaea: P = 0.975) in L. orientalis but not in other species.
Two types of sensilla are found on the maxillary palps: mechanoreceptors and subtype IV basiconic sensilla (Ba IV). Mechanoreceptors (Mr III) are distributed around the distal rim of the maxillary palp (Fig. 6a–d), and Ba IV are blunt-tipped (Fig. 6e,f), distributed amongst dense microtrichia.
Sensilla on antennal postpedicel
Trichoid sensilla
Trichoid sensilla (Tr) are the most conspicuous and the most numerous sensilla in all three Lispe species. They gradually taper from relatively thick base to an acute apex, with micropores on the cuticle surface (Figs. 3c, 4c, 5c). Tr are the longest and with the largest basal diameter among all four types of sensilla on antennal postpedicel, about 20–25 μm in length (Table 2). Densities of Tr increase from the proximal region towards distal region on both anterior surface and posterior surface of antennal postpedicel (Table 3).
Basiconic sensilla
Three subtypes of basiconic sensilla (Ba) are identified on antennal postpedicel according to their shape and size. Subtype I basiconic sensilla (Ba I) are shorter than Tr, about 12–14 μm in length (Table 2). They appear as sturdy pegs that gradually taper to an acute tip (Figs. 3d, 4d, 5d). Subtype II basiconic sensilla (Ba II) are pegs with blunt-tip (Figs. 3e, 4e, 5e), about 10–12 μm in length, shorter than Ba I (Table 2). In L. longicollis and L. pygmaea, subtype III basiconic sensilla (Ba III) are also identified on the surface of antennal postpedicel (Figs. 3f, 5f). Compared with Ba I and Ba II, Ba III are the smallest both in length and basal diameter (Table 2). Ba are distributed relatively evenly on the surface of antennal postpedicel, less dense than Tr (Table 3).
Coeloconic sensilla
Coeloconic sensilla (Co) are characterised by longitudinally grooved walls, projecting from a shallow depression of integument. They are typically cone-shaped with sharp tips (Figs. 3g, 4f, 5g). Coeloconic sensilla are about 3–4 μm in length, much smaller compared to other types of sensilla (Table 2), and scattered sparsely on the surface of antennal postpedicel (Table 3).
The size and density of Co among different muscoid species of six genera (Hydrotaea armipes Fallén, Musca domestica L., Scathophaga stercoraria L., Delia radicum L., D. floralis Fallén, D. antiqua Meigen, D. platura Meigen, Fannia hirticeps Stein, F. scalaris Fabricius, F. canicularis L.) are compared in Tables 3 and 4. The sizes of Co on antennal postpedicel of these Lispe species are like other muscoid species, but the average densities of Co on their antennal postpedicel are lower.
Clavate sensilla
Clavate sensilla (Cl) can be distinguished by distal club-like swelling (Figs. 3h, 4g, 5h), about 12 μm in length, shorter than trichoid sensilla (Table 2). The distribution of Cl is relatively aggregated, most of them are discovered on the proximal and middle region of antennal postpedicel surface (Table 3).
Discussion
The present study describes the antennal sensilla of three aquatic predators, L. longicollis, L. orientalis and L. pygmaea using scanning electron microscopy. The morphology and distribution of mechanoreceptors, pedicellar button, trichoid sensilla, basiconic sensilla, and clavate sensilla of three Lispe species resemble to previous results on L. neimongola9 and other muscoid species, such as Delia radicum L.18, Musca domestica L.2, Fannia hirticeps Stein25, and Scathophaga stercoraria L.26. Mechanoreceptors are known to be sensitive to physical stimuli like gravity, air vibration, and tension caused by muscle activity27. Micropores were detected on the surface of Tr, Ba, and Cl (Figs. 3, 4, 5 boxes), which are characteristic in chemoreceptors. In addition, electrophysiological28,29 and neurological30,31 studies also identified odorant receptors (OR) and gustatory receptors (GR) in Tr30,32,33, Ba30,34,35, Co33,36, confirming their olfactory function.
The swollen maxillary palps in Lispe may increase their chemosensory functions. Different from the club-like maxillary palps in most of other fly species, maxillary palps of Lispe species are significantly swollen and flattened, and swelling degrees of maxillary palps in the three Lispe species are generally larger than typical muscoid species, such as Musca domestica L.2 and Fannia hirticeps Stein25 (Table 1). Maxillary palps mainly acted as gustatory sensory organ37 that react to molecules with low or zero vapor pressure, involved in contact or short-distance chemosensory functions38, compared to that of antennae, which typically perceive more volatile olfactory signals or chemical cues39. Shiraiwa40 pointed out that maxillary palps of fruit flies can improve their sensitivity to food odours, others suggested that maxillary palps perceive olfactory signals at shorter distance, and can be integrated with the signals perceived in antennae to allow better manoeuvring when approaching lures41. Larger maxillary palps of L. neimongola were suggested to provide larger surface area for basiconic sensilla and enhance the perception of gustatory odours or signals9. For predators flying rapidly to chase prey like Lispe22,42, more sensilla can increase their behavioural responsiveness43. The swollen maxillary palps of the three Lispe species may function similarly to improve their gustatory and/or olfactory sensitivity.
Maxillary palps could also be a signaller as well as a signal receiver. In respond to higher selection pressure of searching for food, hosts, or oviposition sites by chemosensory, female insects usually have larger antennae and maxillary palps or more sensilla attached to them9,44,45. In L. orientalis and L. neimongola9, maxillary palps are significantly more swollen in males than in females. Light microscopy photos (Figs. 1c, Supplementary Fig. S1c) and field observations show that maxillary palps of male L. orientalis are more conspicuous than other species when observed from a distance. Empiracle evidence shows that during courtship dance, some male Lispe flies circle around the female and flash their maxillary palps21,42. This could be important in correct species recognition and successful copulation, as many Lispe flies have highly overlapped habitats and ecological niches42,46. Thus, the maxillary palps could be dual-functional for male Lispe flies, and this is among some rare cases that an olfactory organ also plays a role as chemical signal receiver and as visual signal conveyer, which also indicates maxillary pales of L. orientalis are under different levels of sexual selection pressure.
Coeloconic sensilla are common on antennal postpedicel in most other fly species8,19,25,26,47,48, but are relatively sparse on antennal postpedicel of these three Lispe species, even completely missing in L. neimongola9. Beside chemosensory function, Coeloconic sensilla have been also proved to be sensitive to temperature and/or humidity signals49,50. Compared with olfactory, temperature or humidity, predators rely more on acute vision which enhance their ability of colour vision, movement awareness and depth perception, especially on fast moving preys19,51. Lower number of coeloconic sensilla on antennal postpedicel reflect the adaptation to predatory lifestyle and could be regarded as a character of the genus Lispe.
Methods
Adult L. longicollis, L. orientalis and L. pygmaea were captured from Kalamaili Ungulate Nature Reserve, Xinjiang, China, in August 2013. All specimens were pinned as museum samples and air dried on site. Morphology of antennae and maxillary palps were examined under Olympus SZX16 stereoscopic microscope (Olympus Corp., Tokyo, Japan), morphological photographs were taken by a Canon 500D digital camera (Canon, Inc., Tokyo, Japan) coupled with stereoscopic microscope. Continuous images on different focal lengths were composed by Helicon Focus for Windows (Helicon Soft Ltd., Kharkov, Ukraine). Five specimens for both sexes of each species were used for measuring body length as well as length and width of maxillary palp. Three male specimens for each species were used for scanning electron microscopy. Heads of all specimens were cut off, then surface debris was removed by rinsing in phosphate buffered saline buffer (pH 7.4). Subsequently, antennae and maxillary palps were dissected respectively, cleaned with detergent by ultrasonic cleaner. After dehydration in graded ethanol series (twice 15 min each with 60%, 70%, 80%, 90%, 95%, 100% ethanol), antennae and maxillary palps were mounted on aluminium stubs with double-sided adhesive tape, then left in a desiccator for 24 h to dry thoroughly. Samples were coated with gold and observed with a HITACHI S34Q scanning electron microscopy (Hitachi Corp., Tokyo, Japan) at the Microscopy Core Facility, Biological Technology Centre, Beijing Forestry University (Beijing, China).
Length, width of maxillary palps and body length of five specimens for each sex were measured. Then the swelling degree (width to length) of maxillary palps and the ratio of maxillary palp measures to body length (length of maxillary palp to body length and width of maxillary palp to body length) were calculated and compared by two-way ANOVA in SPSS 22.0 (IBM Corp., Armonk, New York) between different species and different sexes of each species. Results of two-way ANOVA were visualized by Sigmaplot 12.5 (Systat Software, Inc., Chicago, Illinois). Length, basal diameter, tip diameter (clavate sensilla only), density and distribution of sensilla were measured using micrographs taken under different magnifications. The length of each single sensillum was measured (ten repeats of each type of sensilla) from the proximal rim to the tip. Density and distribution of various types of sensilla were measured by measuring square areas (each representing 576 µm2) from proximal, median, and distal part (each consists one third of the antenna in length) of the antenna on both sides2, and ten quadrates were measured for each part. In this study, the terminology applied to describe antennal morphology and classification of types of sensilla followed those used by Cumming and Wood52.
Data availability
All data generated or analysed during this study are included in this published article.
Change history
06 January 2022
A Correction to this paper has been published: https://doi.org/10.1038/s41598-022-04882-z
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Acknowledgements
We are grateful to the invaluable help from the Microscopy Core Facility, Biological Technology Centre, Beijing Forestry University (Beijing, China). This study was supported by the National Natural Science Foundation of China (Grant number: 31872964) and Beijing Forestry University Outstanding Young Talent Cultivation Project (Grant number: 2019JQ03018).
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D.Z., X.Liu and X.Li conceived and designed the study. X.P. and G.L. took the LM and SEM photographs. Q.W. conducted the statistical analysis. D.Z., G.L., Q.W. and X.P. wrote the manuscript and made contributions to the discussion. D.Z., Q.W., X.Liu and X.Li revised the manuscript, and all authors approved the final version.
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Liu, G., Wang, Q., Liu, X. et al. Antennal and palpal sensilla of three predatory Lispe species (Diptera: Muscidae): an ultrastructural investigation. Sci Rep 11, 18357 (2021). https://doi.org/10.1038/s41598-021-97677-7
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DOI: https://doi.org/10.1038/s41598-021-97677-7
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