Contributions to Zoology 89 (2020) 412-433 CTOZ brill.com/ctoz

Insect toward aquatic ; reassessment of antennal sensilla in the water bug families , and (: : )

Agnieszka Nowińska University of Silesia in Katowice, Faculty of Natural Science, Institute of Biology, ­Biotechnology and Environmental Protection, 40-007 Katowice, Bankowa 9, Poland [email protected] Jolanta Brożek University of Silesia in Katowice, Faculty of Natural Science, Institute of Biology, ­Biotechnology and Environmental Protection, 40-007 Katowice, Bankowa 9, Poland

Abstract

The first comparative morphology study on antennal sensilla of Ochteridae, Gelastocoridae and Aphelo- cheiridae, carried out with the use of a scanning electron microscope, is provided. Our research hypoth- esis was: the antennal sensilla of the studied families reflect their different adaptations for use in aquatic habitats, while maintaining a common set of sensilla similar to other water bugs (Nepomorpha). There- fore, the number and placement of antennal sensilla of several in the mentioned families were studied using scanning electron microscopy. Nine main types of mechano- chemo- and thermo- hygroreceptive sensilla were confirmed on their surface, including sensilla trichodea, chaetica, club-like, campaniformia, basiconica, coeloconica, plate-like, ampullacea and sensilla placodea multilobated. While seven of these were already documented in other species, two of them (sensilla plate-like and placodea multilobated) were yet to be documented on the antennae of Nepomorpha. All families display differences in the shape and length of antennae as well as among sensilla types. These findings support our hypothesis regarding differences in sensillar structures among families adapted differently to suitable niches. Differences between these families and previously studied nepomorphan taxa (Nepoidea) were also documented. However, the general set of sensilla observed on the antennae of the studied species is very similar to the one documented in Nepoidea. Therefore, we confirmed our assumptions regarding similarities in antennal sensilla between the studied families and other nepomorphan .

© Nowińska & Brożek, 2020 | doi:10.1163/18759866-bja10008 This is an open access article distributed under the terms of the cc by 4.0 license. Downloaded from Brill.com10/07/2021 01:22:58PM via free access

REASSESSMENT OF ANTENNAL SENSILLA in TRUE WATER BUGS 413

Keywords antennal sensilla – morphology – nepomorpha – Ochteridae – Gelastocoridae – Aphelocheiridae

Introduction by some family groups: Ochteridae, Gelasto- coridae, which are terrestrial/hydrophiine Members of the true water bugs, or Nepomor- bugs, which comprise water margin inhabit- pha have long attracted the attention of re- ants (China, 1955; Popov, 1971; Schuh & Slater, searchers due to the possession of diverse 1995; Papáček, 2001; Kment & Jindra, 2008), as body structures and lifestyles. These nepo- well as Aphelocheiridae and the other re- morphan insects, being predaceous (except maining families (, Belostomatiade, most corixids, that may also be scavengers or Corixiidae, , Notomectidae, Plei- consume algae), are one of the most special- dae and ) which live submerged ized groups among heteropterans. The Nepo- in water (Polhemus & Polhemus, 1988). morpha are recognized as a group of second- Popov (1971) hypothesized that a proto-­ arily aquatic bugs among the suborder of heteropteran terrestrial lineage gave rise, Heteroptera (Popov, 1971). Most remaining among others, to protoochterids that resulted taxa in this infraorder are terrestrial, except in three main branches of aquatic bugs in the the , or semi-aquatic bugs (Pol- mid- period: The first branch was hemus et al., 1995; Schuh & Slater, 1995). Nepoidea (Nepidae and ), the The water bugs currently classified as the second was Corixoidea () and the Nepomorpha, include about 2000 species third branch at first led to Ochteroidea and worldwide (Polhemus et al., 1995), with 13 fam- next to Naucoroidea, Notonectoidae and Ple- ilies recognized in this infraorder (Nieser, oidea. The present study focuses on the sensil- 2002). By contrast, 11 families were distin- lar system of the antennae in three particular guished by Chen et al. (2005) and were grouped families (Ochteridae, Gelastocoridae and differently in seven superfamilies (Hebsgaard Aphelocheiridae) which are considered suit- et al., 2004; Brożek, 2014; Ye et al., 2020). able targets for studying the evolution of or- Evolutionary transitions of insects from ganismal traits resulting from multiple transi- terrestrial to aquatic habitats provide impor- tions between land and water. tant insights into how their organismal traits The family Ochteridae consists of 80 spe- have responded to major adaptive shifts (Cre- cies, and displays its highest diversity in tropi- spo, 2011). Opportunities for documentation cal regions. The four-segmented antennae are such inferences are limited, because many easily visible because they extend over the secondarily aquatic taxa are still lack- head (Chen et al., 2005). In contrast with ing detailed morphological data. nepomorphan groups which are fully aquatic, The beginning of diversification of the Ochteridae are considered to be semi-aquatic whole nepomorphan group is estimated to (hydrophiine), or even riparian (Chen et al., have occurred in the late (about 263 2005). They inhabit mossy rocks along Ma) (Ye et al., 2020). It is certain, on the basis streams, walls of waterfalls, sand banks and of , that they existed during the mid- other edges of water reservoirs (Zettel & Lane, Triassic and are a divergence from the terres- 2010). They are zoophagous and are believed trial group (Grimaldi & Engel, 2005). Impor- to prey on small such as dipter- tant examples of Nepomorpha are represented an larvae (ChenDownloaded et al., 2005 from Brill.com10/07/2021). Many members 01:22:58PM via free access

414 NOWIŃSKA & BROŻEK of the Ochteridae are terrestrial and are often ­Naucoridae, but later was elevated to family found at long distances from aquatic habitats position (Štys & Jansson, 1988). Aphelocheiroi- (Ye et al., 2020). dea, a new superfamily, was formed after- Gelastocoridae consists of two subfamilies, wards, consisting of two families, Aphelochei- Gelastocorinae and Nerthrinae (Todd, 1955). ridae and Potamocoridae (Hebsgaard, 2004), They all have four-segmented antennae con- after which they were collapsed into a single cealed in groves beneath the eyes (Todd, 1955; family in the aforementioned superfamily Chen et al., 2005), not visible from the dorsal (Brożek, 2014). A recent study gave conflicting perspective. The Gelastocoridae are consid- results and Aphelocheiridae returned to Nau- ered riparian or even terrestrial bugs (similar coroidea (Ye et al., 2020). Therefore, in this to Ochteridae), which distinguishes them study we consider the morphology of sensilla from most Nepomorphan families in terms of on the family level and do not exclude Aphelo- . Several species of have even cheiridae from belonging to any superfamily been collected far from water. At least three (Aphelocheiroidea or Naucoroidea). species have been found under water (La Riv- Among sensory organs, the antennae usu- ers, 1953). However given the gelastocorids’ ally have the highest concentration and diver- habitat, this particularity is rather the excep- sity. External sensilla possess an external cu- tion. There is no documentation regarding ticular shaft of various sizes and shapes, and a their ability to fly. Some species even have socket or joint that anchors the process in the fused hemelytra which makes them unable to surrounding epidermis, so they present many fly (Chen et al., 2005). They are predatory bugs different morphologies adapted to their mo- (Schuh & Slater, 1995) and have the ability to dality. They play a mechanical, chemosensory jump while hunting prey. and thermo-hygroreceptive function (Slifer, Aphelocheiridae, similar to the other taxa 1970; Altner & Prillinger, 1980; Hallberg & previously discussed, have four-segmented Hansson, 1999; Zacharuk, 1980; Shields, 2010). antennae. In contrast to Gelastocoridae, the Sensillar systems are especially important antennae in Aphelocheiridae are easily visi- for aquatic insects which live in dense, dark, ble, since they are not concealed. Species of highly complex habitat conditions or species Aphelocheirus are known for their ability to with poor vision capabilities (Brönmark & stay submerged underwater (Andersen & Hanssons, 2000; Wisenden, 2000). Moreover, Weir, 2004), which is possible due to their plas- in aquatic insects, the distinction between tron respiration system that also allows them taste and olfaction is vague, but is still used to complete their entire life cycle underwater based on the structure and particular location (Polhemus & Polhemus, 1988). They feed on of the sensilla, or behavioral response (Zacha- immature forms of various aquatic insects ruk, 1980; Crespo, 2011). such as Ephemeroptera and Trichoptera. Until now, several types of labial sensilla While there are no doubts about the classifi- (sensilla trichodea, chaetica, squamiformia, cation of Gelastocoridae and Ochteridae – basiconica, club-like, paddle-like, cupola- they both belong to the superfamily Ochteroi- shaped, and peg sensilla) have been described dea (Štys & Jansson, 1988; Hebsgaard, 2004; in numerous species of Nepomorpha (Brożek, Brożek, 2014; Ye et al., 2020) the systemat- 2013, 2014). More general research has also ic ­position of Aphelocheiridae in Nepomor- been done on the basal shapes of the anten- pha isunclear. In previous classifications the nae and distributions of some sensilla in rep- was a subfamily of Aphelocheirinae resentatives of nepomorphan families (Popov,

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Moreover, a small amount of data about the Materials and methods morphology and distribution of more visible sensilla (trichodea or basiconica) on the sur- The material was obtained from the collec- face of antennae of glauca, Plea tions of the Natural History Museum in Vien- leachi, , Ranatra linearis and Sig- na, Zoological Museum of the State Moscow ara striata has been presented by Chaika & University and Hungarian Natural History Sinitsina (1999), although the possible func- Museum in Budapest. Additional species of tions of the sensilla have not been indicated. Nerthra and have been donated However, newer morphological studies of an- by Ping-ping Chen. All specimens have been tennal sensilla from species of Nepoidea, per- cleaned in an ultrasound cleaner, the anten- formed by Nowińska & Brożek (2019), have nae have been dissected, dried in ethanol, shown some inconsistencies in comparison to mounted, sputtered with gold or chromium data from Chaika & Sinitsina (1999). and observed with the use of the scanning Although some papers (mentioned above) electron microscopes Phenom XL and Hitachi have shed light on the antennal structures and UHR FE-SEM SU 8010 in the scanning micros- reception of environmental stimuli in some copy laboratory of the Faculty of Natural Sci- nepomorphan species, the understanding of ence, Institute of Biology, Biotechnology and the olfactory system in water bugs is still poor. Environmental Protection of Silesian Univer- Limited information on morphology and sity in Katowice. We follow the terminology physiology is available, for a small number of and classification reported in other papers on species. The identification and description antennal sensilla of insects (Altner & Prill- of antennal sensilla, through the use of scan- inger, 1980; Nowińska & Brożek, 2019). ning electron microscopy (SEM), for a com- The antennae of eight species from three prehensive understanding of the sensory sys- families have been studied: tems of the antennae, was performed only for Aphelocheiridae: a few Nepoidea species (Nowińska & Brożek, (Fabricius,1803) 2019). Obtained from Hungarian We expect that the antennal sensilla of Natural History Museum studied species from these families differ, be- Label data: Seine bei Rouen, cause of their various adaptations to the water Gallia, coll. Horvath habitat. No studies of fine morphology and Ochteridae: marginatus ultrastructure have been performed so far on (Latreille,1804) these representatives of the families. Obtained from Hungarian The research hypothesis is: the antennal Natural History Museum sensilla of the studied families reflect their dif- Label data: Japan, Okayama ferent adaptations for use in aquatic habitats, H. Sauter, det. P. Chen while maintaining a common set of sensilla Gelastocoridae: Gelastocorinae: similar to other water bugs (Nepomorpha). Gelastocoris sp. Therefore, the aim of this study is to exam- Obtained from Zoological ine the morphological diversity and distribu- Museum of the State tion of sensilla on the antennae, assign prob- Moscow University able functions and compare them with Species identified in the homologous structures observed in other Museum, the place of nepomorphan groups, as well as other terres- collection cannot be trial and semi-aquatic heteropteran groups. Downloadedconfirmed from Brill.com10/07/2021 01:22:58PM via free access

416 NOWIŃSKA & BROŻEK

Gelastocoris flavus flavus shorter (130 and 120 μm) and wider than the (Guérin-Méneville,1835) other two (230 and 270 μm). Whole antennae Obtained thanks to dona- are visibly covered with hair-like sensilla (fig. tion from Dr Ping-ping Chen 1a). The antennae of Gelastocoris and Nerthra Label data: Bronopondo, are visibly thicker. In both, the last antenno- road to Brownsweg, ponds, mer remains the longest (around 300 μm in leg. N. NieserSN229/30, det. Gelastocoris and around 400/500 μm in Ner- P. Chen thra) but there is a difference in the length of Nerthrinae: the third antennomer. In Gelastocoris it is Nerthra femoralis much shorter (170 μm) than in Nerthra (Montandon,1899) (around 200-300 μm), but in both cases the Obtained from Natural third antennomer is the shortest (figs 2a, 4b). History Museum in Vienna In Aphelocheirus we observe around 1 mm Species identified in the long and thin four-segmented antennae. The Museum, the place of first two antennomers (scapus and pedicel) collection cannot be are shorter (around 150 and 170 μm), while the confirmed other two (antennomers of flagellum) are vis- Nerthra fuscipes ibly longer (300 and 490 μm). The antennae (Guérin-Méneville,1843) are rather smooth, with only some groups of Obtained from Hungarian thick sensilla visible on the surface (fig. 5a). Natural History Museum Label data: Mexico, Procopp Antennal sensilla Nerthra ampliata In this study, based on morphological charac- (Montandon,1899) teristics, nine main types of sensilla have been Obtained from Hungarian found (sensilla trichodea, chaetica, club-like, Natural History Museum campaniformia, basiconica, coeloconica, am- Label data: N. Guinea, Biro pullacea, plate-like and multilobated) (fig. 6). 1900, Stephansort, Astro- Some of these types have been described in labe Bay other insects (McIver, 1975; Zacharuk, 1980), as Nerthra ranina well as in some heteropteran insects (Brożek, (Herrich-Schäffer,1853) 2013, 2014; Nowińska & Brożek, 2019). Sensilla Obtained thanks to dona- trichodea, club-like, campaniformia and basi- tion from Dr Ping-ping Chen conica (subtype 1), because of their flexible Label data: Argentina, det. sockets, are believed to play a mechanorecep- Nieser & Chen tive function. Sensilla basiconica (subtype 2, 3 and 4) function as chemoreceptive sensilla given their porous surface and inflexible sock- Results et. Pores on the surface of these sensilla indi- cate an olfactory function. Another function is Gross morphology of the antennae thermo-hygroreception and it is performed by Differences in the shapes of the species’ an- sensilla ampullacea and sensilla coeloconica. tennae have been observed. The length of the Taking into account the external morphologi- thin antennae of Ochterus is approximate- cal features (shape and build) of sensilla plate- ly 750 μm. The first two antennomeres are like and multilobated, we assume that they

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Figure 1 Ochterus marginatus; SCh, sensilla chaetica; SB, sensilla basiconica; ST, sensilla trichodea; SCo, sensilla coeloconica.

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Figure 2 A, B, Gelastocoris flavus flavus; C, D, Gelastocoris sp.; SClL, sensilla club-like; SA, sensilla ampullacea; ST, sensilla trichodea; SPM, sensilla placodea multilobated; SB, sensilla basiconica. perform a chemoreceptive function. Morpho- into flexible sockets. According to the surface logical features and distribution of antennal shape and length, two subtypes have been sensilla are summarized in table 1 and the dis- distinguished: tribution of sensilla on the antennae is report- 1. Sensilla trichodea (ST1) – these are long ed in specific figures (figs 1a, 2a, 4b, 5a). sensilla trichodea, blunt-tipped straight Sensilla trichodea – these are usually long hairs with a smooth surface. They are sensilla resembling hair, tapered from the usually numerous on the surface of the base to the tip and curved towards the anten- antennae and have been found in all of nal shaft or they are nearly straight hairs. Fre- the studied species (figs 1b, 2c, 4f). quently, they occur in large numbers, less 2. Sensilla trichodea (ST2) – these are ­often as a single hair. They are embedded long sensilla trichodea, blunt-tipped and

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Figure 3 Gelastocoris flavus flavus; ST, sensilla trichodea; SCo, sensilla coeloconica; SCa, sensilla campaniformia; SClL, sensilla club-like.

curved towards the antennal shaft, with Ochterus on all antennomeres, where they oc- a ribbed surface. They are slightly wider cur singularly and in Nerthra ampliata as a than ST1. They have been found in single sensillum on the first antennomere Ochterus, Gelastocoris and Nerthra on all (figs 1a, 4d). of the antennomeres (figs 1c, 2c, 3a). Sensilla club-like (SClL) – these sensilla are Sensilla chaetica (SCh) – these sensilla are more pronounced and thicker than sensilla more pronounced than sensilla trichodea, trichodea. They are ribbed, flattened and rise mainly in length and width. They are ribbed from flexible sockets. They occurred in and inserted in flexible sockets, rising much Ochteridae. In G. flavus and Gelastocoris sp. on higher than sensilla trichodea, which makes the 1st and 2nd antennomeres, these sensilla them well visible. They have been found in occur in groups and in Nerthra femoralis on

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Figure 4 A, B, C, E, Nerthra femoralis; D, Nerthra ampliata; F, Nerthra fuscipes; SPM, sensilla placodea multilo- bated; SClL, sensilla club-like; SCh, sensilla chaetica; SCo, sensilla coeloconica; ST, sensilla trichodea; SB, sensilla basiconica. Downloaded from Brill.com10/07/2021 01:22:58PM via free access REASSESSMENT OF ANTENNAL SENSILLA in TRUE WATER BUGS 421

Figure 5 Aphelocheirus aestivalis; SPl, sensilla plate-like; SB, sensilla basiconica; SCa, sensilla campaniformia; SA, sensilla ampullacea.

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Figure 6 Shapes of sensilla; ST, sensilla trichodea; SCh, sensilla chaetica; SCa, sensilla campaniformia; SClL, sensilla club-like; SB, sensilla basiconia; SPl, sensilla plate-like; SPM, sensilla placodea multilobated; SA, sensilla ampullacea; SCo, sensilla coeloconica.

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Table 1 The presence of sensilla types on the antennae, according to their function and their arrangement Species MS CHS THS UNF sensilla on Sensilla quantity (olfactory?) antennomeres (anm)

Ochterus ST1 SB2 SA ST all anm ST numerous marginatus ST2 SB3 SCo SCh all anm SCh singularily SCh SB4 SB2 4th anm SB2 few SB1 SB3 the 3rd and 4th anm SB3 numerous SB4 2nd and 4th anm SB4 singularily or few SCo 3rd and 4th anm SCo singularily or few Gelastocoris ST1 SB2 SA SPM ST all anm ST numerous sp. ST2 SB3 SClL 1st and 2nd SClL occur in groups SClL SB4 anm SB2 2nd-4th anm SB2 singularily SB1 SB3 last anm SB3 numerous SB4 2nd-4th anm SB4 singularily SPM 3rd and 4th anm SPM numerous Gelastocoris ST1 SB2 SA SPM ST all anm ST numerous flavus flavus ST2 SB4 SCo SClL 1st and 2nd anm SClL occur in groups SCa SB2 2nd-4th anm SB2 singularily SClL SB4 2nd-4th anm SB4 occur in groups / line SB1 SCo 2nd anm SCo few SPM 3rd and 4th anm SPM numerous Nerthra ST1 SB2 SA SPM ST all anm ST numerous femoralis ST2 SCo SClL 1st anm SClL single SCa SB2 2nd-4th anm SB2 singularily SClL SCo 4th anm SCo in groups /singularily SB1 SPM 3rd and 4th anm SPM numerous Nerthra ST1 SB2 SA SPM ST all anm ST numerous fuscipes ST2 SB2 2nd-4th anm SB2 singularily SB1 SPM 3rd and 4th anm SPM numerous Nerthra ST1 SB2 SA SPM ST all anm ST numerous ampliata ST2 SCh 1st anm SCh single SCh SB2 2nd-4th anm SB2 singularily SB1 SPM 3rd and 4th anm SPM numerous Nerthra ST1 SB2 SA SPM ST all anm ST numerous ranina ST2 SB4 SCo SB2 2nd-4th anm SB2 singularily SB1 SB4 2nd and 4th anm SB4 singularily SCo 4th anm SCo few SPM 3rd and 4th anm SPM numerous Aphelocheirus ST2 SB2 SA SPl ST 3rd anm ST singularily aestivalis SCa SB3 SB2 3rd and 4th anm SB2 in groups SB3 tip of the 4th anm SB3 single SPl 4th anm SPl numerous

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424 NOWIŃSKA & BROŻEK the 1st antennomere, single sensillum club- of the surface is ribbed and porous. They like have been found figs. 2a, 3d, 4b). are wider at the base and tapered along Sensilla campaniformia (SCa) – these are their length. These sensilla have been round plates with a single pore, embedded in found in Ochterus marginatus on the flexible sockets. They have been documented 2nd-4th antennomere, where sensilla oc- only in a few species. However, this type is cur singularly or a few of them are spread common for all insects so we believe it is also on the surface. In Gelastocoris sp. on the present in other species studied (figs 3b, 5d). 2nd-4th antennomere, sensilla occur sin- Sensilla basiconica – these are long struc- gularly and in Gelastocoris flavus flavus tures, thick and curved or tapered at the tip. they occur in groups or a few sensilla are They are inserted in inflexible sockets. We arranged in line along the antennomere. have distinguished four subtypes of these These sensilla have also occurred singu- sensilla: larly in Nerthra ranina on the 2nd and 1. Sensilla basiconica (SB1) – this kind of 4th antennomere. They are straight or sensilla is responsible for mechanore- bent towards the surface of the antenna ception. It is present between the anten- (figs 1b, 2b). nomeres and is being stimulated by the Sensilla coeloconica (SCo) – these are peg in movement of each antennomere. It is a pit sensilla, embedded in shallow open cavi- common type of sensilla on insects’ an- ties of the cuticle. They are embedded in in- tennae (fig. 4f). flexible sockets. They are nonporous and oc- 2. Sensilla basiconica (SB2) – these are cur among sensilla trichodea. These sensilla sensilla basiconica with the same width have been found in Ochterus on the 3rd and 4th along the whole surface and slightly antennomere, where sensilla occur singularly, rounded tip. They bear pores along the in groups or in a line of a few sensilla, Gelasto- whole surface. SB2 have been found in coris flavus flavus where few sensilla have all of the studied species. In Aphelochei- been observed on the 2nd antennomere, Ner- rus on the 3rd and 4th antennomere, sen- thra femoralis on the base and near the tip of silla occur in groups. In Gelastocoris and the 4th antennomere, where sensilla occur in Nerthra on the 2nd-4th antennomere, groups or singularly and in Nerthra ranina sensilla occur singularly. In Ochterus the where few sensilla have been found on the 4th most visible and significant are sensilla antennomere (figs 1c, f, 3a, c, 4e). at the tip of the 4th antennomere – one Sensilla plate-like (SPl) – these are round sensillum at the tip is surrounded by a sensilla, with uneven edges. They occur only few other SB2 (figs 1e, 5c, e). on the distant half of the 4th antennomere of 3. Sensilla basiconica (SB3) – these are po- Aphelocheirus and are more or less evenly dis- rous sensilla basiconica, long and flat- tributed (fig. 5b). tened along the whole length. They have Sensilla ampullacea (SA) – these are peg in been found in Ochterus on the third and pit sensilla with an external opening, which is fourth antennomere, in Gelastocoris on cuticular and round, and in which no peg the last antennomere and in Aphelochei- is visible because it is set internally at the rus as a single sensillum at the tip of the ­bottom of a tube. Sensilla ampullacea rise antenna (figs 1b, 5b). from inflexible sockets. Single structures have 4. Sensilla basiconica (SB4) – these are been found in all of the studied species, in dif- sensilla basiconica that are smooth at ferent locations throughout the antennae

the base and tapered at the tip. The rest (figs 2d, 5f). Downloaded from Brill.com10/07/2021 01:22:58PM via free access

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Sensilla placodea multilobated (SPM) – olfactory, tactile (mechanoreception) and these are round cavities with small oval protu- thermo-hygroreceptive systems. The first sys- berances, that do not extend beyond the cu- tem is composed by sensilla with wall pores ticular surface. They have been observed in (sensilla basiconica, plate-like sensilla and Nerthra species and Gelastocoris on the 3rd probably sensilla placodea multilobated). The and 4th antennomere, distributed on the second system – mechanoreception – includes whole surface of the antennomere (figs 2c, different sensilla trichodea and chaetica as 4a, c). well as campaniformia and cone-shaped pro- prioceptive sensilla, all placed in flexible sock- ets and bearing characteristic nonporous sur- Discussion faces. The hygro-thermoreceptive sensory system is represented by nonporous peg in This paper summarizes our morphological pit sensilla (ampulacea) and sensilla coelocon- studies of the external antennal sensilla in ica. All such sensilla are common in most in- three families of Nepomorpha, performed sects (Chapman, 1998) as well as in nepomor- with the use of a scanning electron micro- phan nepid taxa (Nowińska & Brożek, 2019) scope. This study is important for the continu- and in the currently studied families. However, ation of other morphological studies on the their different polymorphic shapes constitute nepomorphan taxa and suggests possible different subtypes, which may be assigned to functions of sensilla based on their morphol- different functions depending on their mor- ogy and distribution on the antennae. Simi- phology and receptor’s structures. lar studies have already been done in two other families – Belostomatidae and Nepidae Olfactory sensilla (Nowińska & Brożek, 2019). More general re- In Ochteridae (Ochterus marginatus) the ol- search concerning the shapes of antennae factory system includes three subtypes of sen- and general occurrence of sensilla on the sur- silla basiconica (SB2, SB3 and SB4) which are face has been carried out by Popov (1971), similar in both genera of Gelastocoridae Schuh & Slater (1995) and Chen et al. (2005). (Gelastocorinae; Gelastocoris sp., G. flavus) During these studies, nine morphological and Nethra (Gelastocoridae: Nethrinae). All types of sensilla have been observed and their examined species of Gelastocoridae were probable functions have been indicated. Sets found to share numerous sensilla placodea of sensilla were compared within the studied multilobated (SPM). A slight difference in the families, as well as with other nepomorphan aforementioned taxa was observed in the ol- families, semi-aquatic bugs (Gerromorpha) factory system of Aphelocheiridae (Aphelo- and other heteropteran species. cheirus aestivalis), in which only two types of sensilla basiconica (SB2 and SB3) were ob- Sensilla types served, albeit in fewer numbers, as well as sev- The antennae of insects include many elemen- eral plate-like sensillum (SP1). In the present tary sensilla, and they are treated as a complex study, all sensilla categorized as belonging to multimodal insect organ (Chapman, 1998). the olfactory system meet the standards re- The morphological analysis of antennal garding olfactory sensilla previously morpho- sensory organs of the studied families (Ochteri- logically documented in other insects by dae, Gelastocoridae and Aphelocheiridae) many authors (Altner & Prillinger, 1980; Chap- shows the presence of different sets of sen­ man, 1998; Shields, 2010; Nowińska & Brożek, silla, forming three basal sensory systems: 2017, 2019). Downloaded from Brill.com10/07/2021 01:22:58PM via free access

426 NOWIŃSKA & BROŻEK

At this stage of research, it is difficult to caveat does not exclude the sensilla’s chemo- clearly indicate the extent of olfactory percep- receptive function. These taxa, especially tion in these bugs, as they are mainly associ- Aphelocheiridea, prefer stable water habitats ated with the aquatic environment. The cur- (Andersen & Weir, 2004). Particular features, rent data shows evident differences between such as the cuticle without pores in chemo- relevant taxa, because sensilla SB3 or SB4 are sensory sensilla, were found in other water- present only in some of the studied species living , thus reflecting a possible (table 1). SB3 is thin walled with many pores in adaptation to the aquatic habitat (Gaino & contrast to the thick, grooved and porous sen- Rebora, 1999). Probably, these sensilla are silla SB4. Both types (SB3 and SB4) of olfacto- highly specific for the mentioned taxa and re- ry sensilla were recognized in many insect sponsible for specific behavior. groups (Zacharuk, 1980; Brézot et al., 1997; Ah- Structures similar to sensilla placodea mul- mad et al., 2016). It is significant that SB4 was tilobated have been discovered on heteropter- recognized in taxa related to Ochteridae and ans’ bodies and described as sieve-pores (Cob- Gelastocoridae. SB4 is only documented in ben, 1978) or cuticular peg-plates (Andersen, one Nertha species. In turn, SB3 is pointed in 1982; Andersen & Weir, 2004). However, the Ochterus, Gelastocoris and Aphelocheirus, but aforementioned authors did not identify any probably absent in Nethra species. Such dif- pores. Essentially, there is no clear informa- ferences in sensilla sets may imply the specific tion on whether these structures are glandu- reception of chemical compounds. Analyzing lar or sensorial. In the present study, the struc- the distribution and number of olfactory sen- tures “sensilla placodea multilobated” are silla on antennae in the particular taxa exam- numerous and present on the antennae only ined, several SB2, SB3 and SB4 were found on in gelastocorid species. According to Slifer the penultimate and last antennomers (table (1970), such grouped pegs in caves can be as- 1) with the exception of Aphelocheirus, in sociated with an olfactory role, perceiving which several SB2 occurred in groups on the long distance stimuli. We observe significant penultimate and last antennomere, while SB3 discrepancies in chemical information detec- was singularly located at the end of the last tion sensilla, which are highly sensitive, due to antennomere. In contrast, the presence of SB2 aquatic insects’s various adaptations to help (thin walled multiporous) in all tested species in foraging, mating, reproduction, and assess- can point to a monofunctional sensillum, ment of predatory risk (Yee, 2014). probably responsible for the diagnosis of wa- A fundamental prerequisite for nepomor- ter chemistry. phans and other aquatic insects is to be able Sensilla placodea multilobated (SPM) are to receive sensory cues in two very different found only in Gelastocoridae species and an- biotopes during the immature and the adult other type – plate like (SPl) – only in Aphche- stage, repectively. Olfactory systems consist- locheiridae. The latter type is distributed on ing of different shaped sensilla basiconica the last antennomere along its length and is (subtypes 2, 3) and coeloconica (subtypes 1, 2, believed to be a chemoreceptive sensillum. 3) were also distinguished in other nepomor- Moreover, this shape of sensillum has not phan taxa (Nepidae and Belostomatidae) been observed in Ochteridae. The expected (Nowińska & Brożek, 2019). However, the characteristic pores are impossible to observe placoid-shaped olfactory sensilla did not oc- on the multilobated sensilla of gelastocorids cur. An important feature is the presence of a and plate-like in aphelocheirid species, due to common type of olfactory sensillum basiconi- the pores’ probable small size. However, this cum SB2 in all previouslyDownloaded fromstudied Brill.com10/07/2021 Nepoidea 01:22:58PM via free access

REASSESSMENT OF ANTENNAL SENSILLA in TRUE WATER BUGS 427

(Nowińska & Brożek, 2019), as well as in all of and that the curiously modified setiform sen- the presently studied species. The occurrence silla of Nepa served as static organs under wa- of other different types of olfactory sensilla in ter (Chapman, 1998). The mechanoreception Nepoidea is more characteristic for particular system of the antennae in the studied aquatic genera and species. bug species is represented by trichoid sensilla Generally, chemoreception in aquatic in- of different shapes. Many trichoid sensilla are sects is the perception, via gustatory sensilla, fine enough to detect air vibrations (Shields, of chemicals in an aqueous solution. If the in- 2010). Thus, these sensilla are numerous in sects are airborne, the chemicals are per- terrestrial and semi-aquatic bugs (Gonzaga- ceived by olfactory sensilla. Behavioral studies Segura et al., 2013; Nowińska & Brożek, 2018). on the diving beetle Laccophilus maculosus Also, aquatic taxa can detect vibrations by us- showed that in the air, these beetles respond- ing hair sensilla on the surface of water or ed to about 10% of the concentration required while submerged. Hair sensilla (trichoid sen- to produce a similar response in water. A simi- silla) are considered to be the structure from lar study pointed out that multiporous sensil- which all other types of sensilla are derived la on the antennae of the diving beetle (McIver, 1970). They may appear as thick, hair- Graphoderus occidentalis are probably olfac- like or flattened structures (chaetica, club- tory, but may also be sensitive to lower con- like) or very fine hairs. Some of such hairs centrations of chemicals in both air and wa- have peg-like or cone-like shapes. The present ter. It might indicate that the sensing of odors data shows mechanoreceptive sensilla in the on both media is based on similar molecular three studied families as being composed of and physiological processes (Jensen & Zacha- trichoid sensilla thin and smooth (ST1), slight- ruk, 1992). It has also been reported that the ly thick and ribbed (ST2) and thick and ribbed great diving beetle Dytiscus marginalis (Lin- (chaetica, club-like) (SCh, SClL). All of these naeus, 1758) has a very well developed chemo- types of sensilla are numerous in representa- receptive sensilla located on the antennae tives of Ochteridae and Gelastocoridae and (odor) or maxillary and labial palpi (taste), less numerous in Aphelocheiridae and repre- which are critical for detecting potential food sent similar patterns of distribution. In Aph- (Yee, 2014). elocheirus, however, they were observed sin- gularly and the types of mechanoreceptive Mechanoreceptive sensilla sensilla were very limited on the antenom- The study of insect’s mechanoreceptive sen- meres in comparison with the other nepo- silla has a long history. The most obvious morphans (Nepidae and Belostomatidae), ­peripheral sense organs are the numerous cu- which also prefer the underwater life-style. ticular hairs on the insects’ bodies and ap- Probably, the absence of long mechanorecep- pendages, called setae, which are a type of tive sensilla on the antennal surface in Aph- mechanoreceptive sensilla. McIver (1975) and elocheirus might be an adaptation to the type others classified a variety of sensilla and in- of environment. The antennae are situated on ferred their functions from general observa- the head without any physical protection tions on the insects’ behaviours and on the from environmental stressors, therefore not structure and topography of the sensilla. In concealed in grooves beneath the eyes as ob- this way, it was determined that setiform/ served in Gelastocoridae or Nepoidea (Popov, hairform sensilla could monitor touch and in- 1971; Nowińska & Brożek, 2019). In Nepoidea, dicate the flexion of joints; that campaniform there is a great morphological diversity when sensilla could register bending of the cuticle, it comes to mechanoreceptiveDownloaded from Brill.com10/07/2021 sensilla, where 01:22:58PM via free access

428 NOWIŃSKA & BROŻEK nine types were recognized, five of which sockets and few in number. According to Alt- were new for this group (Nowińska & Brożek, ner (1983), such morphological characters of 2019). the sensilla represent one fundamental sensil- lum type and their structural features can be Hygro-thermoreceptive sensilla regarded as adaptations to hygro- and ther- Various kinds of sensilla are described and de- moreception. The bimodal hygro-thermore- fined in the hygro-thermosensitive sensillar ceptive sensilla exhibited the strongest re- system (Altner & Prillinger, 1980). Usually, sponses to changes in humidity as well as sensilla hygro-thermosensitive appear as temperature changes, because the moist cells’ small aporous cuticular pegs (i.e., sensilla coe- and the dry cells’ discharge rates increase with loconica) originating from the antennal sur- high temperatures. This phenomenon was ob- face or set in pits (sensilla ampulacea) (Tichy served i.e., in Periplaneta americana (Tichy & & Kallina, 2013). Generally, water bugs fly from Kallina, 2013). one body of water to another during mating season or to find new water habitats. They can Comparison to the other heteropteran also disperse in other ways (Wróblewski, groups 1980). Temperature and humidity are major It is significant that within Nepomorpha there determinants of distribution patterns for spe- are two types of antennae. In Ochteridae and cies. In Gelastocoridae, some species are not Aphelocheiridae the antennae are long and able to fly (due to fused hemielytra) and in extend over the head, making them very simi- others flight has not been observed, but none- lar to the long and thin antennae in Gerro- theless these species are frequently found morpha and other heteropterans (Andersen, away from water. It seems like this kind of hy- 1982; Shuch & Slather, 1995), while in Nepoi- gro-thermosensitive sensilla is essential for dea, the antennae are short and concealed be- finding other water reservoirs (Chen et al., neath the head, as in Gelastocoridae (La Riv- 2005). This might explain the presence of sev- ers, 1953; Menke, 1979; Zettel & Lane, 2010). eral sensilla ampullacea and sensilla coelo- Nonetheless, both types of antennae involve conica in the studied species. In Aphelochei- complex sensilla of different modalities and rus, which happens to be the only species living appearance, despite a common underlying submerged, numerous sensilla ampullacea architecture. occur. These have been found along with sen- Generally, a sensillar system is conserved silla SPl, on the last antennomere. However, throughout the different insect orders, mak- several sensilla coeloconica (SCo) have also ing it improbable that these different types of been found in species of Gelastocoridae and sensilla have evolved independently several Ochteridae, localized mainly on the 3rd and times (Steinbrecht, 1997). That is probably 4th antennomeres. Moreover, sensilla ampul- why a similar set of functional sensilla is ob- lacea were in different ­locations throughout served in terrestrial and aquatic heteropteran the antennae in these taxa. In Nepoidea, sen- insects. silla coeloconica (three subtypes) with the However, the adaptive value of conserving same structure also ­occurred (Nowińska & both types of olfactory sensilla (‘single-walled Brożek, 2019). Therefore, we cannot exclude wall-pore’, ‘double-walled wall-pore’) through- the potential hygro-­thermoreceptive function out almost all insect taxa to date requires of sensilla ampulacea and coeloconica. More- ­further verification (Steinbrecht, 1997). The over, these sensilla, especially sensilla coleo- ­sensory peg of the double-walled sensilla is conica, are aporous sensilla­ with inflexible smooth at the base Downloadedand has afrom grooved Brill.com10/07/2021 ­cuticular 01:22:58PM via free access

REASSESSMENT OF ANTENNAL SENSILLA in TRUE WATER BUGS 429 surface distally, with pores organized in spoke et al., 1997; Sinitsina & Chaika, 1998; Ahmad channels between each ridge, in contrast to et al., 2016), coreids (Akent’eva, 2008) and in the single-walled sensilla with a porous thin Gerromorpha (Nowińska & Brożek, 2017). The cuticular wall. Also, sensilla basiconica distin- thermo-hygroreceptive sensilla found in the guished in the presently studied water taxa, studied families (ampulacea or aporous sen- belong to both ‘single-walled wall pore’ (SB2, silla coeloconica) are mostly the same types SB3) and ‘double-walled wall pore’ classes and functions, although their size and how (SB4). Olfactory sensilla basiconica (SB2) are they are embedded is different. Aporous sen- present in all studied taxa and the remaining silla coeloconica on the flagellum can also be sensillar types (SB3, SB4) have different con- regarded as playing a thermo-hygroreceptive figurations according to subfamilies/species. role, in other insects/heteropteran species: In the studied taxa, sensilla ampulacea (SA), Nezara viridula (), Odontopus campaniformia (SCa) and trichoidea (ST2) be- nigricornis (), Cyclopelta siccifo- long to a standard set of sensilla, just like SB2. lia (),Chrysocoris purpureus (Scu- Probably, these sensilla (SB2, ST2, SA, SCa) telleridae), Piezodorus guildinii (Pentatomi- originated from the protoheteropteran line dae), Leptoglossus zonatus () as well and retain plesiomorphic sensillar features. as in some gerromorphan species (Usha Rani Hence, we observe some common features of & Madhavendra, 1995, 2005; Brézot et al., 1997; Ocheroidea and Aphelocheiridae with Nepoi- Chapman, 1998; Silvaet al., 2010 Ruchty, 2009; dea. Among the other types of sensilla, signifi- Gonzaga-Segura et al., 2013 Nowińska & cant changes in their shape, size and distribu- Brożek, 2017; Schneider, 2018). For terrestrial tion were demonstrated in the studied taxa. heteropteran insects, another common type Sensilla placodea (usually olfactory) are not of mechanoreceptive sensilla is sensilla trich- common in nepomorphan taxa (except Aph- odea, but usually in different lengths and even elocheiridae), as sensilla placodea multilobat- distributions on all antennomeres, similar to ed are characteristic of one family (Gelasto- mechanoreceptive sensilla basiconica. Sensil- coridae). In Nepoidea, however, sensilla la chaetica are less numerous than sensilla coeloconica (subtypes 1, 2, 3) were recog- trichodea and are sparsely distributed or only nized as multiporous chemoreceptive sensilla occur as single structures in different terres- (Nowińska & Brożek, 2019), whereas in the trial heteropteran taxa. Sensilla campanifor- presented taxa, sensilla coeloconica are recog- mia show a uniform structure in all mentioned nized as hygro-thermoreceptive sensilla. Oth- taxa (Chinta et al., 1997; Slu, 1980; Akent’eva, er heteropteran taxa/species display a pres- 2008; Ahmad et al., 2016; Nowińska & Brożek, ence of multiporous sensilla basiconica or 2017). trichodea (‘single-walled wall-pore’, ‘double- Ochteridae is more connected with terres- walled wall-pore’) on the antennae, while sen- trial environments (Andersen & Weir, 2004), silla placodea are rarely present. However, of- therefore similarities with the antennal sen- ten their shape, size and number are slightly silla of terrestrial Heteroptera could have varied, like in reduviids (Catalá, 1997; Gracco been expected, which is different from what is & Catalá, 2000; Guerenstein & Guerin, 2001; observed in Gelastocoridae and Aphelocheiri- Carbajal de la Fuente & Catalá, 2002; Slu, 1980), dae. Present studies have shown that the main miriids (Chinta et al., 1997), (Rani & sets of antennal sensilla in these three fami- Madhavendra, 2005; Ventura & Panizzi, 2005), lies (table 1, fig. 6) are generally similar to lygaeids (Rani & Madhavendra, 2005), pen- those in Nepoidea – insects submerged in tatomids (Rani & Madhavendra, 1995; Brézot ­water. Multiple Downloadedtypes of from mechanoreceptive Brill.com10/07/2021 01:22:58PM via free access

430 NOWIŃSKA & BROŻEK and chemoreceptive sensilla were docu­ plate-like (SPl) only in Aphelocheiridae, on mented in all of them. Sensillum club-like, the other hand, indicates an autapomorphy. which was new for Nepoidea, was also ob- Currently and according to expectations, served during­ the presented studies and sen- we have not found any signs indicating a rela- silla ­ampullacea works as the main thermo-­ tionship between Ochteroidea and Aphelo­ hygroreceptive sensillum for all the families in cheiridae, because the taxon is quite distant Nepoidea as well as within the presently stud- from the family. Future study of antennal ied species. ­sensilla in naucoroid species may be of im­ The main difference between nepoid portance when it comes to phylogenetic con­ groups (six types of mechanoreceptive sensil- siderations. la in Belostomatidae and seven types in Nepi- dae) (Nowińska & Brożek, 2019) and the fami- lies mentioned above, is the fewer amount of Conclusions mechnoreceptive sensilla types (three: tricho- dea, chaetica and campaniformia). These dif- The studied families show variations in their ferences in structure/types of sensilla in par- adaptation to aquatic habitats, as well as in an- ticular taxa show how sensory systems have tennae’s shapes. The basal set of sensilla (ST2, adapted to new lifestyles, and future studies SCa, SB2, SA) is similar in all of them and is not on other nepomorphan families may show different from the sensilla present in Nepoidea further new features. (ST2, SCa, SB2, SA). They share the same type of sensillum (SClL) which is new to Nepomor- Short phylogenetic remarks for studied pha, and all of the studied families, as well as groups Nepoidea, use mainly sensilla ampullacea for In the present study, the antennal sensilla thermo-hygroreception. On the other hand, (ST1, ST2, SCh, SB1 SB2, SCa, SCo) are presum- the shapes of antennae and sets of sensilla in ably plesiomorphic, due to having the same the studied families of Nepomorpha are differ- shapes and similar distributions of the sensil- ent compared to semi-aquatic bugs (Gerro- la as reported in Nepoidea (Nowińska & morpha). There are more sensilla subtypes in Brożek, 2019) – the superfamily considered to Gerromorpha (18) and their antennae are very be the primary taxon of Nepomorpha (Popov long and thin, while the antennae of the stud- 1971, Hebsgaard et al., 2004, Brożek, 2014). ied species bear fewer types of sensilla, are On the other hand, sensilla placodea multi- much shorter and, in some species (Gelasto- lobated (SPM) have been reported only in the coridae), concealed beneath the eyes. The an- species of Gelastocorinae and Nerthrinae and tennae of Aphelocheiridae bear sparsely dis- probably represent an evolutionary novelty tributed sensilla, which are mostly sensilla for them, therefore being synapomorphic. basiconica. It is possible that the number of Sensillum basiconicum (SB4) has been ob- sensilla has been reduced because of their served only in ochterid and gelastocorid spe- preference for running water habitats. The an- cies and is a synapomorphic feature of Gelas- tennae of Ochteridae and Gelastocoride are tocoridae and Ochteridae, and therefore, a mostly covered by sensilla trichodea, with confirmation of their close relationship. There lone sensilla basiconica and coeloconica is more evidence to suggest a close relation- sparsely distributed on the surface. There were ship between Gelastocoridae and Ochteridae, two types of thermo-hygroreceptive sensil- which together compose Ochteroidea (Heb- la present in the families – sensillum ampul- sgaard, et al., 2004). The presence of sensilla laceum and sensillumDownloaded coeloconicum. from Brill.com10/07/2021 New 01:22:58PM via free access

REASSESSMENT OF ANTENNAL SENSILLA in TRUE WATER BUGS 431 types of sensilla, characteristic of the anten- species in the course of their postembryonic de- nae of Aphelocheiridae (SPl) and Ochteroidea velopment. Entomol. Rev., 88, 381–390. (SPM), have also been found. This supports Altner, H. & Prillinger, L. (1980) Ultrastructure of our hypothesis that the antennal sensilla of chemo- thermo- and hygrorecep- the studied families reflect their different ad- tors and its functional significance. Int. Rev. Cy- aptations for use in aquatic habitats, while tol., 67, 69–139. maintaining a common set of sensilla similar Altner, H., Schaller-Selzer, L., Stetter, H. & Wohlrab, to other nepomorphan insects. The study also I. (1983) Poreless sensilla with inflexible sockets. confirms the systematic position of Ochteri- Cell Tissue Res., 234, 279–307. dae as closely related to Gelastocoridae. An- Andersen, N.M. (1982) The Semiaquatic Bugs (He- tennal sensilla of Naucoroidea will be studied miptera, Gerromorpha) Phylogeny, Adaptations, in the future. Therefore, we expect to compare Biogeography and Classification. Scandinavian present results of Aphelocheiridae with other Science Press Ltd, Klampenborg. species of Naucoroidea and apply a cladistic Andersen, N.M. & Weir, T.A. (2004) Australian method for a more thorough assessment of Water Bugs. Their biology and identifica- their phylogenetic significance. tion ­(Hemiptera-Heteroptera, Gerromorpha & Nepomorpha). Entomonograph, 14, 1–344. Brézot, P., Tauban, D. & Renou, M. (1997) Sense organs Acknowledgements on the antennal flagellum of the green stink bug, Nezara viridula (L.) (Heteroptera: Pentatomi- The authors would like to thank H. Zettel from dae): sensillum types and numerical growth dur- the Natural History Museum in Vienna, Yu. A. ing the post-embryonic development. Int. J. Insect Popov from the Zoological Museum of the Morphol. Embryol., 25, 427–441. State Moscow University and P. Kobor from Brönmark, C. & Hansson, L.A. (2000) Chemical the Hungarian National History Museum for communication in aquatic systems: an intro- the access to their respective nepomorphan duction. Oikos, 88, 103–109. collections, Ping-ping Chen for donating ad- Brożek, J. (2013) Comparative analysis and system- ditional species of Nerthra and Gelastocoris, atic mapping of the labial sensilla in the Nepo- and J. Karcz from the University of Silesia in morpha (Heteroptera: Insecta). Sci. World J., Poland for help in SEM documentation in the 2013, 1–44. Laboratory of Scanning Microscopy. We also Brożek, J. (2014) Phylogenetic signals from ne­ thank Dan Polhemus and an anonymous re- pomorpha (Insecta: Hemiptera:Heteroptera) viewer for their useful comments that helped mouthparts: stylets bundle, sense organs, and improving the paper. labial segments. Sci, World J, 2014, 1–30. Carbajal de la Fuente, A.L. & Catalá, S.S. (2002) Re- lationship between antennal sensilla pattern References habitat in six species of Triatominae. Mem. Inst. Oswaldo Cruz, 97, 1121–1125. Ahmad, A., Parveena, Sh., Brożek, J. & Dey, D. Catalá, S.S. (1997) Antennal sensilla of Triatominae (2016) Antennal sensilla of phytophagous and (Hemiptera, ): a comparative study predatory pentatomids (Hemiptera: Pentatomi- of five genera. Int. J. Insect. Morphol. Embryol., dae): a comparative study of four genera. Zool. 26, 67–73. Anz., 261, 48–55. Chaika, S.Y. & Sinitsina, E.E. (1999) Sensory organs Akent’eva, N.A. (2008) The formation of the anten- of the labium and antennae in water bugs (Het-

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