Secondary Rhinaria Research Articles

Preference of Pentalonia nigronervosa for infected banana plants tends to reverse after Banana bunchy top virus acquisition

Pentalonia nigronervosa Coquerel (Hemiptera: Aphididae) is the vector of the Banana Bunchy Top Virus (BBTV), the most serious viral disease of banana (Musa spp.) in the world. Before acquiring the virus, the vector is more attracted to infected banana plants in response to the increased emissions of volatile organic compounds (VOCs). Here, we test the hypothesis that BBTV acquisition directly modifies the preference of P. nigronervosa for infected banana plants, and that the change in preference results from the alteration of the organs linked to the VOC detection or to the behaviour of the vector. We found that the preference of P. nigronervosa for infected banana plants reverses after virus acquisition in dessert banana, while it remains similar between healthy and infected banana plants before and after the acquisition of BBTV. At the same time, aphids reared on infected bananas had smaller forewing areas and hind tibia length than aphids reared on healthy bananas, although the number of secondary rhinaria on the antennae was lower on dessert banana-reared aphids than plantain-reared aphids, this was not affected by the infection status of the aphid. These results support the "vector manipulation hypothesis—VMH" of pathogens to promote their spread. They have implications for the BBTV management.

Secondary Rhinaria Contribute to Major Sexual Dimorphism of Antennae in the Aphid Semiaphis heraclei (Takahashi)

Sexual generation is an important generation in the life cycle of host-alternating aphids, and its population size determines the intensity of the peak in the next spring. Although male trapping techniques based on olfactory stimuli have been successfully established in the field, the biological basis of olfactory perception in males is unclear. In this study, we compared the morphology of antennae and the types, sizes, numbers, and distribution of sensilla between males and sexual females in the host-alternating aphid Semiaphis heraclei (Hemiptera: Aphididae). We found that flagellum length differentiation contributed to the majority of the sexual dimorphism of antennae. Most sensillum types or subtypes, including trichoid sensilla subtype I, campaniform sensilla, and primary rhinaria subtypes I and II, were enlarged in males. In addition, males bore more trichoid sensilla subtype I than sexual females. In particular, secondary rhinaria were present in males only and could not be detected in sexual females. These results revealed the structural basis of male olfactory perception. Our findings provide insight into the mechanism underlying chemical communication between sexual aphids and could thus be useful for pest control.

Two new species of the genus Macrosiphoniella Del Guercio, 1911 (Hemiptera, Aphidomorpha: Aphididae) inhabits yarrow in Kazakhstan

Two new aphid species of the nominotypical subgenus of the genus Macrosiphoniella (Aphidinae) are described from Kazakhstan. Both species inhabits yarrow (Achillea millefolium L.). Macrosiphoniella kazakhstanica sp. n. most similar to M. silvestrii Roberti, 1954 but differs latter in the number of secondary rhinaria in apterous and alate viviparous females (5–10 and 24–26 vs 14–25 and 48–68), proportion of the processus terminalis to the base of the VI antennal segment (3.7–4.9 vs 2.8–3.6), proportion of antennal segment III to processus terminalis (0.82–0.98 vs 1.11–1.36), as well as the absence of dorsal sclerites at base of setae and color of all tibiae (brown in M. silvestrii and pale in the middle in new species). Macrosiphoniella sarmatica sp. n. is similar to M. terraealbae Kadyrbekov, 2000 but differs from latter in the ratios of the length of the processus terminalis to the length of the base of the 7th antennal segment (3.15–3.75 vs 2.7–3.1), length of the frontal setae to diameter of third antennal segment (1.6–1.7 vs 2.2–2.6), the number of accessory setae on the ultimate rostral segment (6 vs 7–8) and the number of setae on the cauda (10–13 vs 12–19).

New Lipaphis species (Hemiptera, Aphididae, Macrosiphini) from central Trkiye living on Sisymbrium sp. (Brassicaceae).

Lipaphis (Lipaphis) erdemi sp. nov. is described from apterous and alatae viviparous females collected in Central Anatolia (Trkiye) on Sisymbrium sp. (Brassicaceae). The new species is markedly different from the other species of the subgenus Lipaphis by having secondary rhinaria on the antennal segments III, IV and frequently V in apterous viviparous females, and always having secondary rhinaria on the antennal segments III, IV and V in alate viviparae. Other features that allow to separate the new species from the other species of the subgenus are presented. The new species is morphologically most similar to L. erysimi and L. pseudobrassicae. An identification key based on apterous viviparous females of the genus Lipaphis known from Trkiye is provided.

Polyphenism in Antennal Sensilla Among Different Adult Morphs of Nonhost-Alternating, Holocyclic Sitobion avenae (Hemiptera: Aphididae).

Aphids, mainly distributed in temperate zones, exhibit seasonal generation-alternating phenomena. Across the life cycle, different morphs are produced. Sitobion avenae (Fabricius 1775) is a major pest of wheat worldwide. To elucidate olfactory perception of morph-specific behavior across their life cycle, we investigated antennal sensilla among seven morphs using scanning electron microscopy. Trichoid, placoid, coeloconic, and campaniform sensilla were identified. Trichoid sensilla, big multiporous placoid sensilla (primary rhinarium), a group of sensilla (primary rhinaria), and campaniform sensilla showed similar distribution and resemblance among morphs, whereas small multiporous placoid sensilla (secondary rhinaria) exhibited obvious differences. Compared to apterous morphs, alate morphs possessed a greater abundance of secondary rhinaria, with the greatest found in males on antennal segments III–V. Alate virginoparae and alate sexuparae ranged from six to fourteen rhinaria on antennal segment III. Fundatrices, apterous virginoparae and apterous sexuparae only had one or two secondary rhinaria on antennal segment III while they disappeared in oviparae. Secondary rhinaria, lying in a cuticle cavity, are convex or concave in their central part. In males, both forms were present, with a greater proportion of convex form than that of the concave form. Fundatrices and virginoparae had the convex form while sexuparae had the concave form. Polyphenism of secondary rhinaria might suggest their association with the olfactory functions of morph-specific behavior. These results have improved our understanding of the adaptive evolution of the antennal sensilla in nonhost-alternating, holocyclic aphids.

Characterization of Antennal Sensilla and Immunolocalization of Odorant-Binding Proteins on Spotted Alfalfa Aphid, Therioaphis trifolii (Monell).

The spotted alfalfa aphid [Therioaphis trifolii (Monell), Homoptera, Drepanosiphidae] is a well-known destructive pest that can significantly reduce alfalfa yields. Herein, the morphology of antennal sensilla of T. trifolii has been examined by using scanning electron microscopy and the ultrastructure of sensilla stellate and placoidea was described by transmission electron microscopy. Stellate sensilla, placoid sensilla, and coeloconic sensilla were found on the 6th segment, and a single sensillum placoidea was located on the 5th segment. Placoid sensilla were also present on the 3rd antennal segment of alate and apterous aphids, and the number was similar between two morphs. Two types of trichoid sensilla and coeloconic sensilla were found on the antennae, respectively. The results of ultrastructure showed that stellate sensilla are innervated by three neurons, while placoid sensilla present three groups of neurons, equipped with 2–3 dendrites in each neuron group. Immunocytochemical localization of odorant-binding proteins (OBPs) was performed on ultrathin sections of sensilla stellate and placoidea, and we observed that the antiserum against OBP6 intensively labeled all placoid sensilla from both primary and secondary rhinaria. OBP7 and OBP8 could also be detected in placoid sensilla, but less strongly than OBP6. In addition, OBP6, OBP7, and OBP8 were densely labeled in stellate sensilla, suggesting OBP6, OBP7, and OBP8 may sense alarm pheromone germacrene A in T. trifolii.

A new genus of gall-forming aphids of tribe Fordini Baker, 1920 (Hemiptera: Aphididae: Eriosomatinae) from Near East

SummaryInbaria n. gen. is proposed based on type species Geoica swirskii Remaudière & Inbar, 2004, resulting in a new combination, Inbaria swirskii (Remaudière & Inbar, 2004) n. comb. Inbaria easily differs from all Pistacia gall-producing aphids of the tribe Fordini by the size of the primary and secondary rhinaria in fall migrants. Inbaria n. gen. is differentiated morphologically from the similar genera Geoica Hart, 1894 and Slavum Mordvilko, 1927. Genetically (COI), the two genera Geoica and Inbaria show a large divergence of more than 9% of the sequence. Notes on some morphological characters in apterous fundatrigeniae and descriptions of the embryo of the apterous exule, within alate viviparous females of I. swirskii, are provided.

Rhinariaphis – A remarkable new aphid genus from Afghanistan (Hemiptera: Aphididae: Aphidinae)

In this paper, we describe a new aphid genus, Rhinariaphisgen. nov., from the tribe Macrosiphini (Aphididae: Aphidinae) with the type species Rhinariaphis tuberculatasp. nov., from specimens that have been collected in Afghanistan, where it is associated with Lophanthus pinetorum (=Nepeta cabulica) (Lamiaceae). Rhinariaphis is superficially similar to the Hyperomyzus subgenus Neonasonovia due to its characteristically shaped siphunculi, but it is also similar to the genera Eucarazzia and Klimaszewskia because of some of the characters of the ultimate rostral segment. Representatives of this genus can easily be distinguished from other Macrosiphini genera due to the presence of numerous secondary rhinaria on antennal segments III, IV and V as well as by the thick setae on their large tuberculate bases. In addition to the taxonomy of the genus, a scanning electron microscopy (SEM) study was performed and the main morphological characters are presented with detailed descriptions of the antennal and body sensilla.

New species of the aphid tribe Macrosiphini (Homoptera, Aphididae, Aphidinae) from Kazakhstan

Two new species of the genera Uroleucon Mordvilko, 1914 and Pleotrichophorus Borner, 1930 are described from Kazakhstan. Uroleucon dzhungaricum sp. n. feeding on Senecio nemorensis L. (Asteraceae) in the Dzhungar Ala Tau is closely related to U. minor (Borner, 1940). Both these species differ from the closely related U. solidaginis (Fabricius, 1794) in a smaller length ratio between the processus terminalis and the 3rd antennal segment (0.8–1.0 versus 1.0–1.5). The new species differs from U. minor (Born.) in a greater number of the secondary rhinaria on the 3rd antennal segment of the apterous viviparous females (21–37 versus 15–21), in a fewer number of hairs on the cauda (10–16 and 15–23), and in the host plant. Pleotrichophorus ugamicus Kadyrbekov, sp. n. feeding on Artemisia santolinifolia Turcz. is described from the Sairam-Ugam Natural Park (Southern Kazakhstan). The new species is similar to P. glandulosus (Kaltenbach, 1846) and P. achilleae Holman, 1965. Pleotrichophorus ugamicus sp. n. differs from these species in the length ratio of the processus terminalis to the base of the 6th antennal segment (4.1–5.0 versus 5.0–9.0 and 5.1–6.2), in that of the ultimate rostral segment to the 2nd segment of the hind tarsus (0.68–0.76 versus 0.80–0.97 and 0.80–0.90), and in the host plant. This species differs from P. glandulosus in the ratio of the length of dorsal hairs on tergites I–V to the basal diameter of the 3rd antennal segment (1.0–1.2 and 1.4–1.7). In addition, the new species differs from P. achilleae in the length ratio of the 3rd antennal segment to the 6th segment (0.56–0.66 versus 0.70–0.87) and to the processus terminalis (0.67-0.82 versus 1.39–1.80), as well as in the shape of the dorsal hairs. A key to the Palaearctic species of the genus Pleotrichophorus is presented.

New species of the genus Klimaszewskia Szelegiewicz, 1979 (Homoptera, Aphididae) from Kazakhstan

Two new species of the genus Klimaszewskia were described from aphid collections made in 2010–2011 in the “Katon-Karagaiskii” State National Natural Park (the Kazakhstan part of the Altai Mountains). Klimaszewskia altaica Kadyrbekov, sp. n. inhabiting Nepeta sibirica and K. katonica Kadyrbekov, sp. n. inhabiting Dracocephalum grandiflorum differ from the other known species of this genus in a smaller number of hairs on the ultimate rostral segment and on the 2nd segment of the hind tarsus and also in the presence of indistinct, strongly flattened marginal protuberances. They differ in the length ratio between the processus terminalis and the base of the 6th antennal segment (3.6–4.6 in the former, and 4.2–5.2 in the latter species), the siphunculi and the body (0.17–0.24 versus 0.25–0.27), and the cauda and the 2nd segment of the hind tarsus (1.7–2.2 and 2.25–2.35), as well as in the length of hairs on the frons, antennae, and tergites, in the number of hairs on tergite VIII (8–10 and 2–3), and in the number of secondary rhinaria on the 3rd antennal segment (3–12 compared to 0–2). The holotypes and some paratypes of the new species are deposited in the collection of the Institute of Zoology (Almaty, Kazakhstan). Some part of the paratypes is kept in the Zoological Institute of the Russian Academy of Sciences (St. Petersburg, Russia).

Immunolocalization of Odorant-Binding Proteins on Antennal Chemosensilla of the Peach Aphid Myzus persicae (Sulzer)

The antennal sensilla of Myzus persicae were mapped using scanning and transmission electron microscopy. Placoid sensilla and coeloconic sensilla were found on the 6th segments, whereas 2 types of trichoid sensilla were present all through the length of the antenna. A single sensillum placoideum was located on the 5th segment, whereas alate aphids also presented placoid sensilla on the 3rd antennal segment. Immunocytochemical localization of odorant-binding proteins (OBPs) was performed on ultrathin sections of antennal chemosensilla. The antiserum against OBP7 intensively labeled all placoid sensilla from both primary and secondary rhinaria, with gold granules concentrated in the lymph surrounding the dendrite. OBP6 and OBP3 could also be detected in placoid sensilla, but less strongly than OBP7. Barely significant reaction or no reaction was observed with antibodies against OBP8.

A new species of Hyperomyzus (Neonasonovia) (Hemiptera: Aphididae) from Jamaica

Hyperomyzus (Neonasonovia) pullatus Hall & Garraway sp. n (Hemiptera: Aphididae) is described based on apterous specimens collected from Eupatorium sp., (Asteraceae) in Jamaica. Photos and illustrations are provided. It is compared with an undescribed species from Costa Rica. It is distinguished from Hyperomyzus (Neonasonovia) nigra (Baker) by having narrower siphunculi, less secondary rhinaria and a longer rostrum.

Two New Species ofAulacorthum(Hemiptera: Aphididae) from Korea

ABSTRACT Two new species of the genus Aulacorthum, Aulacorthum asteriphagum sp. nov. and Aulacorthum corydalicola sp. nov., are recognized from Korea on Aster scaber Thunb. and Corydalis spp. (C. pallida Pers. and C. speciosa Maxim.), respectively. They are described and illustrated in comparison with the closely related species Aulacorthum solani Kaltenbach 1843. Aulacorthum asteriphagum is mainly characterized by many secondary rhinaria (4–12) on Antenna III, and A. corydalicola is distinguished by short antennae (2.30–2.75 mm) including dark Antenna III. A revised key to the identification of the Korean species of Aulacorthum is presented.

Electrophysiological characterisation of olfactory sensilla in the black bean aphid, Aphis fabae

Electrophysiological responses of three different olfactory sensilla (proximal primary rhinaria (PPR), distal primary rhinaria (DPR) and secondary rhinaria (SR)) to the sex pheromone components, nepetalactol, nepetalactone, and a plant volatile, ( E)-2-hexenal, were investigated in four different morphs of the black bean aphid, Aphis fabae Scopoli. The DC responses recorded directly from the antennal sensilla and termed electrosensillograms (ESGs) were generally much larger (up to 14 mV) than electroantennogram (EAG) responses (up to 2.5 mV). Characteristic morph-specific response profiles to these compounds were observed in each type of rhinarium and response waveforms were different between ( E)-2-hexenal and the sex pheromone components. ( E)-2-Hexenal elicited the largest responses at PPR, while nepetalactol and nepetalactone elicited the largest responses at SR in gynoparae and males. Nepetalactol and nepetalactone also showed significant activities on DPR and PPR in all morphs. In contrast, ( E)-2-hexenal had almost no activity on SR. However, almost all of the SR investigated in males and gynoparae were sensitive to both nepetalactol and nepetalactone. A small sub-set of male SR responded mainly to nepetalactol. SR of winged virginoparae did not respond to the sex pheromone compounds. Paraffin oil (the solvent control) also elicited significant responses at PPR in virginoparae but not in other morphs. In a further experiment, SR of winged virginoparae showed no response to 30 other plant volatile compounds or the alarm pheromone component, ( E)- β-farnesene. Nepetalactol and nepetalactone had similar dose-response profiles in the SR of gynoparae. The results indicate that SR in males and gynoparae are highly specialised to detect sex pheromone compounds, while the DPR and PPR are relatively broadly tuned to both plant volatiles and sex pheromone components. The presence of SR in winged virginoparae that are not responsive to sex pheromone components, alarm pheromone, or any of the plant volatile compounds tested may indicate a possible role of these sensilla to detect, as yet, unknown compound(s) with a high specificity. The present study also suggests that PPR may play a role in detecting paraffin-related compounds such as cuticular hydrocarbons of plants.

Responses of the aphids Phorodon humuli and Rhopalosiphum padi to sex pheromone stereochemistry in the field.

Gynoparous female and male damson-hop aphids, Phorodon humuli (Schrank), were caught in the field by water traps that were releasing the sex pheromone of this species, (1RS,4aR,7S,7aS)-nepetalactol. No behavioral activity was elicited by (4aS,7S,7aR)-nepetalactone, the major sex pheromone component of other aphid species such as Megoura viciae Buckton, even though olfactory cells were found in the secondary rhinaria on the third antennal segment of P. humuli that responded strongly to this compound. Gynoparous female P. humuli in the field responded less strongly to (1R,4aS,7S,7aR)-nepetalactol, the sex pheromone of the bird cherry-oat aphid, Rhopalosiphum padi (L.), than they did to the (4aR,7S,7aS)-nepetalactols, but males responded only to the latter. The (4aR,7S,7aS)-nepetalactone showed no electrophysiological activity so was not used in field trials. Releasing either the (4aS,7S,7aR)-nepetalactone or the (1R,4aS,7S,7aR)-nepetalactol with the (4aR,7S,7aS)-nepetalactols did not inhibit the response of P. humuli gynoparous females and males to the latter. Males of R. padi responded as strongly to the (4aR,7S,7aS)-nepetalactols as they did to (1R,4aS,7S,7aR)-nepetalactol. Males of P. humuli and R. padi responded positively to an increased concentration of the (4aR,7S,7aS)-nepetalactols released from two vials compared with that from a single vial, as did P. humuli (in one of two experiments) and R. padi to the (1RS,4aR,7S,7aS)- and (1R,4aS,7S,7aR)-nepetalactols when released together.

Functional specialisation and polyphenism in aphid olfactory sensilla

Electroantennogram (EAG) responses to the aphid sex pheromone components, (1 R,4a S,7 S,7a R)-nepetalactol and (4a S,7 S,7a R)-nepetalactone, and a plant volatile, (E)-2-hexenal, were investigated at three different positions (5/6th, 4/5th and 3/4th inter-segmental regions) along the antennae of four different morphs in two host-alternating aphid species, Aphis fabae Scopoli and Rhopalosiphum padi (L.). Position-dependent and morph-specific EAG responses were elicited in both species. The nepetalactol and nepetalactone isomers elicited large EAG responses at all three recording positions in males of both species, such that primary rhinaria as well as secondary rhinaria appeared to respond. Asexual female morphs showed relatively smaller EAG responses to these compounds. The secondary rhinaria, which have been reported as sex pheromone receptors in males, were not very different in their number and distribution between gynoparae and alate virginoparae, but the gynoparae showed significantly larger EAG responses to nepetalactol and nepetalactone. The alate virginoparae showed EAG responses that were similar to those of apterous virginoparae, which lack secondary rhinaria. Taking the EAG response profiles together with the distribution of the secondary rhinaria, it is suggested that the function of secondary rhinaria differs between the morphs. Secondary rhinaria appear to detect sex pheromone components in males and gynoparae but not in the alate virginoparae. If they are functional in the latter morph, they are likely to play a role in detecting specific, but as yet unknown, volatile compounds. Some 30 plant volatiles were tested but none evoked an EAG response that could be allocated to the secondary rhinaria. In contrast to the very different EAG response profiles to the pheromone compounds between morphs, EAG responses to (E)-2-hexenal were similar in all forms and both species. These findings suggest that this plant volatile was detected only by the two primary rhinaria, which are common to all morphs. The present study showed that EAG responses were not a simple summation of receptor potentials between recording and reference electrodes in aphids. The localised distribution pattern of olfactory receptor neurones around the recording electrode was also likely to contribute to the EAG responses.

The influence of parasitism on wing development in male and female pea aphids

Wing formation in presumptive alate morphs (virginoparae and males) was observed for the pea aphid, Acyrthosiphon pisum, exposed to attack by the parasitoid, Aphidius ervi, at different stages of host development. Morphological abnormalities in parasitized aphids such as complete apterization (development of a wingless form), formation of rudimentary wing buds, and deformed wings indicate a possible disruption of the endocrine system. Changes in the body shape and the number of olfactory secondary rhinaria on the antennae could indicate an influence of juvenile hormone in parasitized A. pisum but the development of fifth-stadium supernumerary larvae (indicated by an extra moult and which can be induced by exogenous juvenile hormone treatments) was not found in parasitized aphids. In addition, while apterization of virginoparae can also be induced by the pro-allatocidal compound Precocene III, this was not possible in the male. Males which survived parasitoid attack without forming aphid mummies (indicating that oviposition had not occurred) developed as wingless individuals suggesting that the reproductive-tract-fluids from the female parasitoid were important in the wing inhibition process. Teratocytes from the parasitoid appeared to promote developmental arrest in parasitized aphids.

NOTES ON A NEW GENUS AND SPECIES OF MACROSIPHINAE (HOMOPTERA: APHIDIDAE)FROM CHINA*

Abstract In this paper, a new genus, Chusiphuncula Zhang and new species, Chusiphuncula sorbarisucta Zhang, is recognized according to its unique morphological character combinations. The new genus is closely related to Rhopalosiphoninus Baker, but differs from the latter in: 1)head with lateral frontal tubercles smooth (rough in Rhopalosiphoninus); 2)siphunculus 0. 36× as long as body (0. 20–0. 33 in Rhopalosiphoninus); 3)cauda pentagonal (triangular in Rhopalosiphoninus) and 4)alate viviparous female with 7 secondary rhinaria on antennal segment (more than 10 in Rhopalosiphoninus). The type specimens are deposited in Institute of Zoology, Academia Sinica.

The GenusUroleuconMordvilko (Insecta, Aphidoidea) in South America, with a key and descriptions of four new species

Uroleuconis one of only two genera of Aphidinae to have undergone significant speciation in South America, with a group of about 14 endemic, morphologically similar species feeding on native Compositae, especiallyBaccharis.Multivariate morphometrics (canonical variates analysis, CVA) was used to discriminate between these species and compare them with the North American subgenusLambersius, in which most of them have hitherto been placed. It is concluded that they probably form a separate monophyletic group. Four new species are described in this group —brevisiphon,essigi,petrohuenseandpseudomuermosum— and five names are placed in synonymy. Of the other species ofUroleuconin South America,U. lizerianumis widespread and feeds on many species of native and introduced Compositae; it is morphometrically inseparable from the North American speciesU. ambrosiaeand is probably an introduced form of that species, but has consistently fewer secondary rhinaria. A key is provided to the 19 available species ofUroleuconrecorded from South America.

The Genus Uroleucon Mordvilko (Insecta, Aphidoidea) in South America, with a key and descriptions of four new species

Abstract Uroleucon is one of only two genera of Aphidinae to have undergone significant speciation in South America, with a group of about 14 endemic, morphologically similar species feeding on native Compositae, especially Baccharis. Multivariate morphometrics (canonical variates analysis, CVA) was used to discriminate between these species and compare them with the North American subgenus Lambersius , in which most of them have hitherto been placed. It is concluded that they probably form a separate monophyletic group. Four new species are described in this group — brevisiphon , essigi , petrohuense and pseudomuermosum — and five names are placed in synonymy. Of the other species of Uroleucon in South America, U. lizerianum is widespread and feeds on many species of native and introduced Compositae; it is morphometrically inseparable from the North American species U. ambrosiae and is probably an introduced form of that species, but has consistently fewer secondary rhinaria. A key is provided to the 19 available species of Uroleucon recorded from South America.