Haller's Organ Research Articles

Regeneration of Haller's sensory organ in two species of hard ticks of the genus Haemaphysalis (Acari: Ixodidae).

A study of Haller's organ regeneration in nymphs and adults of Haemaphysalis turturis and parthenogenetic females of H. longicornis, from which the forelegs had been amputated during the previous instar, revealed structural changes in regenerated organs. The adult regenerates reestablished atavistic structural features, while the nymphal regenerates retained larval features, which is typical of regenerates of two other genera examined previously (Ixodes and Hyalomma). Data on regeneration of Haller's sensory organ testify to an ancient character of the genus, standing closely to the base of the phylogenetic tree of hard ticks.

Phenol and lactone receptors in the distal sensilla of the Haller's organ in Ixodes ricinus ticks and their possible role in host perception.

Extract of steer wool odor was found to excite olfactory receptor(s) in a wall-pore olfactory sensillum on the distal knoll of the Haller's organ. Three active volatile compounds were revealed in this odor by gas chromatography. Electrophysiological experiments revealed two types of receptors (sensory neurons) within the sensilla examined. One type of receptor responded only to phenolic derivatives, such as o-chlorophenol, o-bromophenol, o-methylphenol, 2,6-dichlorophenol, 2,6-dibromophenol, 2,4,6-trichlorophenol, but not to o-nithrophenol, p-methylphenol, 2,5-dichlorophenol, 3,5-dichlorophenol, 2,6-dinithrophenol, 2,6-dimethylphenol, and pentachlorophenol. The other type of receptor responded only to gamma-valerolactone. It is assumed that these cells play an important role in perception of a host from long distances (10-15 m), which is typical of Ixodes ricinus ticks.

Effect of juvenoids and retinoic acid on the development or larva and nymphs of the tick Ixodes ricinus L. (Acari: Ixodidae) and regeneration of Haller's organ during metamorphosis

Larvae and nymphae of the tick Ixodes ricinus L. display similar reactions to analogs of the insect juvenile hormones (methopren and pyriproxyfen), which induce at both stages juvenalization of the Haller's sense organ regenerates. Similar effects were also described for retinoic acid. Unlike juvenoids, retinoic acid can affect not only regeneration, but also normal development of the Haller's organ and cause changes corresponding to so-called regenerative induction. Amputation of the leg and treatment with retinoic acid do not affect the duration of larval or nymphal development, while juvenoids somewhat accelerate their development.

Regeneration of limbs and sensory organs in Ixodid ticks (Acari, Ixodeidea, Ixodidae and Argasidae)

We present a review of our own and literature data on reparative regeneration in ixodid ticks (chelicerate arthropods). Ticks have a high potential for reparative regeneration and a close relationship between regeneration and development determined by similar hormonal regulatory mechanisms. These mechanisms depend on ecdysteroid hormones, which participate in the initiation of both processes, and juvenile hormones, which direct these processes either to the maintenance of larval features or to the development of nymphal and adult features. We present a detailed analysis of the regeneration of Haller's sensory organs in ixodid ticks and propose an hypothesis about the role of juvenile hormones in the modification of morphogenetic processes in this group. Furthermore, we present data on the effects of insect juvenile hormone analogs (methoprene and fenoxycarb) on the regeneration of Haller's organ, which support this hypothesis. Studies on reparative regeneration in arthropods provide a broader view of the problem of repair morphogenesis in animals.

Regeneration of Haller's sensory organ in the tick, Ixodes rubicundus (Acari: Ixodidae)

A study of regeneration in nymphs and adults of the South African tick Ixodes (Afrixodes) rubicundus, from which the forelegs had been amputated during the previous instar, revealed that the structural changes in regenerated Haller's sensory organs resemble those observed in other ixodid ticks, in particular in another prostriate tick, Ixodes (Ixodes) ricinus. The adult regenerates re-establish their atavistic features in terms of the increased number of different sensilla on the distal knoll, in the anterior pit and the capsule. The nymphal regenerates, in contrast, re-establish the features of the previous instar through a reduction in the number of some sensilla on the distal knoll and in the post-capsular area. The structural changes in different compartments of the organ appear independent. The phenomenon of regenerative induction through the appearance of specific changes in Haller's organ of the contralateral non-treated foreleg is probably characteristic only of prostriate ticks. A unique modification in the regenerated Haller's organ as revealed by duplication of the Haller's organ capsule was discovered in both I. rubicundus nymphs and adult ticks.

Pathways of regeneration of Haller's sensory organ during the life cycle of the tick Hyalomma asiaticum.

A study of regeneration in nymphs and adults of the Asiatic desert tick, Hyalomma asiaticum, from which forelegs had been amputated during the previous instar, revealed that regenerated Haller's sensory organs exhibited significant changes in structure. Adult regenerates possessed atavistic features in terms of the number and topography of different sensillar types. Regularity in these changes was similar to that demonstrated in regenerates of Ixodes ricinus (Leonovich and Belozerov [1992] Exp. Appl. Acarol., 15:59-79). Nymphal regenerates, by contrast, had larval features of the parent species. An hypothesis is presented about the ontogenesis of the complete, peripheral, polymodal sensory organ as a process in which the initial cell differentiation of cells begins at different starting points.

Identification of vertebrate volatiles stimulating olfactory receptors on tarsus I of the tick Amblyomma variegatum Fabricius (Ixodidae)

Gas chromatography-coupled electrophysiological recordings (GC-EL) from olfactory sensilla within the capsule of Haller's organ of the tick Amblyomma variegatum indicate the presence of a number of stimulants in rabbit and bovine odours, and in steer skin wash. Some of these stimulants were fully identified by gas chromatography-mass spectrometry analysis and by matching electrophysiological activity of synthetic analogues as: 1) hexanal, 2-heptenal, nonanal, furfural, benzaldehyde, and 2-hydroxybenzaldehyde (in all extracts); 2) heptanal, 2-, 3-, and 4-methylbenzaldehyde, and gamma-valerolactone (only in bovine and rabbit odour). Careful examination of the electrophysiological responses permit characterization of 6 receptor types: 1) a benzaldehyde receptor, 2) a 2-hydroxybenzaldehyde receptor, 3) three types of receptors responding differently to aliphatic aldehydes, and 4) a lactone receptor.

Systematic relationships in the soft ticks (Acari: Ixodida: Argasidae)

Abstract. A phylogenetic analysis of relationships at the generic to subgeneric level is carried out for the family Argasidae. The analysis is based on a total of eighty‐three characters drawn from larval and adult body and leg morphology, Haller's organ morphology, development and behaviour. These characters are polarized by comparison with representatives of the families Ixodidae and Nuttalliellidae (both suborder Ixodida), and the suborders Holothyrida and Mesostigmata. A total of two equally most parsimonious trees was generated after successive approximations character weighting. Although the support for some lineages in these trees is not very strong, they provide a substantially better overall fit to the data than any of the hypotheses derived from existing classifications of the family.The classification of the Argasidae is revised to reflect the results of the phylogenetic analysis, and compared to existing classifications employed by Eastern European (‘Soviet’) and American authors. The subfamily Argasinae sens.n. contains one genus, Argas sens.n., with five subgenera, A.(Argas) sens.n. [including A.(Persicargas)syn.n.], A.(Secretargas), A.(Ogadenus), A.(Proknekalia)comb.n. and A.(Alveonasus)comb.n. The latter two subgenera (latter three in the Soviet classification) are transferred from the Ornithodorinae, where they were classified as subgenera of Ornithodoros (American school) or Alveonasus (Soviet school). The Ornithodorinae sens.n. consists of three genera, Ornithodoros sens.n., Otobius sens.n. and Carios stat.n. [raised from Argas (Carios)]. The genus Ornithodoros includes the previously recognized subgenera Ornithodoros (Pavlovskyella), O.(Ornamentum) and Argas (Microargas), all syn.n., while Otobius is expanded to include Ornithodoros sparnuscomb.n. The genus Carios contains nearly all bat‐associated argasids, including the previously recognized genera Antricola and Nothoaspis, and subgenera Argas (Chiropterargas), Ornithodoros (Alectorobius), O.(Reticulinasus) and O.(Subparmatus), all syn.n. The available evidence does not allow recognition of subgenera in the genera Ornithodoros, Otobius or Carios.SummaryA phylogenetic analysis of relationships in the Argasidae based on a wide variety of characters drawn from all life stages generated two highly similar and relatively well corroborated hypotheses of relationships. These hypotheses provide a much better fit to the data than phylogenies derived from existing, traditional classifications, and are used as the basis for a revision of the classification within the Argasidae. Although this classification has its weaknesses, e.g. the relatively poor support for Ornithodoros, Carios and Argas (Secretargas), it is considered superior to traditional classifications not only because of the superior fit to the data, but also because it recognizes only monophyletic taxa. In addition, by abandoning the more or less typological approach traditional in argasid systematics in favour of a lineage approach, it allows the explicit recognition of affinities for all taxa, including unusual forms such as Argas (Alveonasus) cooleyi, Ornithodoros transversus, O.elongatus, Otobius megnini, O.lagophilus, O.sparnus, Carios rudis and C.reddelli.

An application of scanned focused ion beam milling to studies on the internal morphology of small arthropods

SummaryFor the first time a scanned focused ion beam of approximately 50 nm diameter has been used to prepare biological material. Small defined areas of the surface were removed by ion etching to allow examination of the underlying structures with a scanning electron microscope. Different milling procedures were carried out on two anatomical features in mites of the genus Halarachne (Halarachnidae: Mesostigmata). In the first, square holes were milled into the surface of the peritrematal plate to reveal the structure of the underlying respiratory peritrematal groove. In the second, transverse cuts were made across the shafts of the sensory sensilli which make up the sensory Haller's organ on tarsus I. This latter procedure revealed detail both within the core and walls of sensilli. Details of specimen preparation and milling procedures, as well as suitability and interpretation of results, are presented.

Haller's Organ in the Tick Family Argasidae (Acari: Parasitiformes: Ixodida)

The structure of Haller's organ in all major groups of soft ticks, family Argasidae, is reexamined, and hypotheses of setal homology are proposed based on a comparative study of developmental patterns. The larvae of most taxa have 7 setae in the anterior pit (1 serrate, 1 conical, 2 fine, 2 porose, 1 grooved) and 4 porose setae in the capsule. The postlarval stages add up to 3 setae to the anterior pit (1 serrate, 1 porose, 1 grooved) and up to 3 porose setae to the capsule. Preliminary hypotheses of polarity, distinguishing ancestral from derived character states, are generated for most characters examined by comparisons with results obtained for the other major family of ticks, Ixodidae, and (where possible) other members of Parasitiformes. Most of the variability in the setal complement of the anterior pit and capsule results from paedomorphosis, and nearly all the observed changes in the setal complement (both modifications of addition patterns and changes in fundamental numbers) are restricted to single species or small species groups. A correlation between changes in Haller's organ structure and changes in life history patterns is suggested but cannot be confirmed based on presently available data.

Regeneration of Haller's sensory organ in the tick Ixodes ricinus L.

Amputation of legs in nymphs of ticks, obtained from the first laboratory generation, resulted in regeneration of the legs after moulting to adults. Haller's sensory organ on the upper surface of each foreleg tarsus was significantly modified following regeneration. Haller's organ in non-amputated legs of the experimental ticks remained unchanged, being comparable to controls. Pored olfactory sensilla in the anterior pit, in a capsule and on a distal knoll usually increased in number, as well as grooved, thin and conical sensilla. Bordering gustatory and double-walled postcapsular sensilla either decreased or increased in number. All additional sensilla were consistent in their location. Form of the anterior pit and capsule's aperture also deeply changed after the regeneration. The authors distinguish this changes as atavistic. No correlation between changes in different parts of the organ were found. A phenomenon of induction was discovered in our study: if a distal part of tick's gnathosoma was amputated together with the left foreleg, Haller's organ in the right, untreated leg possessed the same changes after moulting as the regenerated organ in the previously amputated left foreleg.

Perception of breath components by the tropical bont tick, Amblyomma variegatum Fabricius (Ixodidae). II. Sulfide-receptors.

Wall-pore sensilla in the capsule of Haller's organ on foreleg tarsi of the tick, Amblyomma variegatum, show multicellular responses upon stimulation with human and bovine breath. Filtering breath through charcoal removes the stimulant for some of these receptors. Analysis by gas chromatography coupled with olfactory sensillum electrophysiological recordings indicates that an ethanol extract of the breath components trapped on charcoal contains a major stimulant eluting at the same retention time as H2S. Two types of H2S-sensitive receptors have been identified. They are housed in separate sensilla, and are called sulfide-receptor 1 and 2. Although, both receptor types are characterized by a high sensitivity to H2S with an estimated threshold of ca. 0.1 ppb and a response range covering 5-6 log orders of magnitude, their overall response to sulfides and mercaptans is nevertheless dissimilar. The type 1 receptor fires slightly more upon stimulations with H2S than type 2, whereas ethylmercaptan induces a stronger response from type 2, and dimethyl sulfide activates only receptor 2. In a bioassay, H2S tested at concentrations of ca. 0.02 ppm and 1 ppm equally arouses 60% of resting ticks. Two-thirds of these ticks quest the air with their first pair of legs, and the remainder start active search. By contrast, H2S at ca. 1 ppm in a mixture with CO2 severely diminishes the locomotor stimulating effect of CO2.

Perception of breath components by the tropical bont tick, Amblyomma variegatum Fabricius (Ixodidae). I. CO2-excited and CO2-inhibited receptors.

Wall-pore olfactory sensilla located in the capsule of Haller's organ on the tarsus of Amblyomma variegatum ticks bear cells responding to vertebrate breath: one of these sensilla contains a CO2-excited receptor and a second sensillum has a CO2-inhibited receptor. Each of these antagonistic CO2-receptors, which display typical phasic-tonic responses, monitors a different CO2-concentration range. The CO2-inhibited receptor is very sensitive to small concentration changes between 0 and ca. 0.2%, but variations of 0.01% around ambient (ca. 0.04%) induce the strongest frequency modulation of this receptor. An increase of just 0.001-0.002% (10-20 ppm) above a zero CO2-level already inhibits this receptor. By contrast, the CO2-excited receptor is not so sensitive to small CO2 shifts around ambient, but best monitors changes in CO2 concentrations above 0.1%. This receptor is characterized by a steep dose-response curve and a fast inactivation even at high CO2-concentrations (greater than 2%). In a wind-tunnel, Amblyomma variegatum is activated from the resting state and attracted by CO2 concentrations of 0.04 to ca. 1%, which corresponds to the sensitivity range of its CO2-receptors. The task of perceiving the whole concentration range to which this tick is attracted would thus appear to be divided between two receptors, one sensitive to small changes around ambient and the other sensitive to the higher concentrations normally encountered when approaching a vertebrate host.

Argas (Argas) monolakensis, new species (Acari: Ixodoidea: Argasidae), a parasite of California gulls on islands in Mono Lake, California: description, biology, and life cycle.

Argas (Argas) monolakensis, n. sp., is described from adults, nymphs, and larvae collected from under and around nests of California gulls, Larus californicus Lawrence, on islands in Mono Lake, Mono County, Calif., and from specimens reared in the laboratory. This species is closely related to A. cooleyi Kohls & Hoogstraal, a parasite of cliff swallows, Hirundo pyrrhonota Vieillot, but is easily distinguished by hypostome dentition and roof of Haller's organ in all stages and chaetotaxy of the larvae. This tick was successfully reared and maintained in the laboratory by feeding them on domestic chickens. Larvae require 5-8 d to feed, whereas all postlarval stages feed rapidly within 9-62 min. At Mono Lake, ticks are above ground and seek hosts only at night. The number of nymphal stages varies from 2 to 5 depending on the developmental temperature and sex of the tick. Ticks over winter at Mono Lake as second- to fifth-stage nymphs and adults. Ovarian diapause is common with preoviposition periods in extreme cases lasting up to 20 mo. This tick will readily feed on humans and has the potential to transmit Mono Lake virus, which has been isolated from an estimated 2-8% of ticks on various islands. To date, A. monolakensis is known only from islands in Mono Lake, Calif.

Morphology and structural organization of Haller's organ during postembryonic development ofArgas (Persicargas) walkerae (Ixodoidea: Argasidae)

Scanning-electron-microscopic investigations of Haller's organ in larvae, nymphs I, II, III and IV, and male and female adult Argas (Persicargas) walkerae ticks showed that morphology and structural organization change during postembryonic development. Stage-dependent differences existed regarding setal numbers of the anterior pit as well as formation and reticulation of cuticular projections in the capsule cavity. The anterior pit increased in size in the course of postembryonic development. It contained only seven setae in larvae, one conical, setiform and grooved seta each as well as two porose and fine setae. Nymphs I, II, III and IV adult ticks had equal numbers of setae; however, one additional unilaterally serrate and grooved seta each were present. Setal length increased continuously during postembryonic development and attained maximum values in adult ticks. The capsule consisted of roof and cavity and was located distinctly lateral in larvae, slightly lateral in nymphs I and II, and in all other stages directly on the longitudinal axis of tarsus. The capsule roof showed a reticular structure. The slit-like main aperture was located peripherally and arranged transversally to the longitudinal axis of tarsus I in larvae. Nymphs and adult ticks had a central, circular main aperture. Stage-dependent cuticular projections of varying form protruded into the capsule cavity. Larvae had only single, free-standing projections which ramified slightly and communicated with each other. Projections were more heavily reticulated in nymphs I and II. In nymphs III and IV as well as male and female adult ticks, a long centrally situated tube of reticular appearance was seen, which was supported by a large number of radially organized and interlocking pillars and communicated with the capsule roof. In all tick stages there were always four porose setae present, arranged on the capsule floor.

Scanning electron microscopy of ticks for systematic studies: structure of Haller's organ in eight species of the subgenus Sternalixodes of the genus Ixodes (Acari: Ixodidae).

Haller's organs of eight of nine known species of the subgenus Sternalixodes of the genus Ixodes were studied with scanning electron microscopy. The morphology of the organ is remarkably uniform throughout the subgenus. The major differences are in the prominence of the tarsal hump and the steepness of the tarsal hump walls. Comparisons are made with a similar study done previously on the subgenus Multidentatus . Results of this study support the validity of the subgenus Sternalixodes .

Pneumonyssus africanus Fain, 1959 (Acari, Mesostigmata). Comparison of larva and adults with P. simicola Banks, 1901

The lung mite P. africanus Fain, 1959 and its larva from a new host (Mandrillus leucophaeus) is described and compared to the most frequently found species, P. simicola Banks, 1901. The chaetotaxy of the legs is essentially identical, but leg IV of P. simicola bears 5 spines and 10 setae, while in P. africanus one of the spines is replaced by a seta. Also, very fragile small setae were discovered at the base of the ambulacra on legs II, III and IV in P. africanus and only on leg IV in P. simicola. The chaetae of the ‘Haller's organ’ on leg I are described in detail, and formulae for the chaetotaxy of all legs and measurements of both species are given. ac]19860213

Chemically mediated behavior in Acari: Adapations for finding hosts and mates

Ticks and mites respond to a limited spectrum of stimuli in their search for hosts and mates. Airborne chemical signals include carbon dioxide, ammonia, organic acids, terpenoids, 2,6-dichlorophenol, and other phenolic compounds. These are detected primarily by sensilla in and adjacent to Haller's organ. Most ixodid species examined have one or more multiporose sensilla that detect such volatiles. These olfactoreceptors enable the ticks to respond to remote volatile chemicals from hosts and from the other ticks, e.g., sex pheromones. Other sensilla, probably mechanogustatory in function, also occur on the tarsi. Gustatory sensilla on the palps detect assembly pheromones that enable ticks and mites to respond to conspecific or heterospecific chemical stimuli in their environment. Responses to those stimuli in ticks result in clustering, i.e., arrestant behavior. Arrestant behavior also occurs in certain mites. Finally, cheliceral chemosensilla enable ticks to recognize specific phagostimulants in host blood, e.g., ATP and glutathione, that stimulate feeding. InDennacentor variabilis andD. andersoni, these same cheliceral chemosensilla recognize species-specific genital sex pheromones in the vulvae of conspecific mates, without which they do not copulate.

The Haller's Organ Roof and Anterior Pit Setae of Argas Ticks (Ixodoidea: Argasidae). Subgenera Secretargas and Ogadenus

Adults of the Argas subgenera Secretargas (3 species) and Ogadenus (1 species) were studied by scanning electron microscopy. In each species, the anterior pit and Haller's organ are situated in a large dorsal hump of Tarsus I and the 9 setae of the anterior pit are characteristic of the genus Argas in structure and numbers. In A. (S.) transgariepinus, an Ethiopian-Palearctic crevice-dwelling parasite of bats, the Haller's organ capsule roof is solid with a slitlike transverse aperture. In A. (S.) hoogstraali and A. (S.) echinops, Malagasy soil-dwelling parasites of Oplurus (Varanidae) lizards and the hedgehog-tenrec (Insectivora: Tenrecidae), respectively, the Haller's organ is virtually unroofed but partially screened by arborescent dorsal projections from the posterior wall of the capsule, and the open capsule contains numerous fine pleomorphs. In A. (O.) brumpti, a soil-dwelling parasite of the hyrax (Procavia), other terrestrial mammals, and lizards in the Ethiopian Region, the capsule is also virtually unroofed and contains numerous fine pleomorphs. The unroofed capsule is probably phylogenetically primitive and occurs only in these 3 and 2 other Argas species. The soil microhabitat (in Argas confined to 3 of the 4 species recorded here), and the reptile or ancient mammal hosts of these 3 species, as well as the zoogeographical isolation of 2 of the species in the Malagasy Region, are distinctive in this genus of 56 species. The interrelationships between an unroofed Haller's organ capsule and unusual biological properties remain to be determined.

Bat Ticks of the Genus Argas (Ixodoidea: Argasidae). 13. Haller's Organ Roof and Anterior Pit Setae in Carios and Chiropterargas

Adults of 4 of the 6 species constituting the subgenus Carios and of 3 of the 4 species constituting the subgenus Chiropterargas were studied by scanning electron microscopy. All species parasitize Old World cave-dwelling insectivorous bats (Microchiroptera). The anterior pit setae number 10 in Carios and 10 or 11 in Chiropterargas. In most Carios, the setiform seta is replaced by a second serrate seta. In 2 of the 3 studied Chiropterargas species, 1 of the 2 grooved setae is exceptionally long. Porose setae number 3 in Carios and 3 or 4 in Chiropterargas. The Haller's organ roof in both subgenera is solid, lacking perforations; the aperture is narrowly transverse in Carios, irregularly wide or wide and transverse in Chiropterargas; uniquely, 1 or 2 sensilla protrude from the aperture of Chiropterargas species. The protruding sensilla and long grooved seta of Chiropterargas suggest a probably distinctive sensory-behavior pattern common to these ticks. Other morphological characters are discussed and compared to show relationships between these 2 subgenera and the subgenera Argas and Persicargas and distinctive characters present only in adult and/or larval Carios and Chiropterargas.