The ionic regulatory role of the salivary secretion of the cattle tick, Boophilus microplus

doi:10.1016/0022-1910(69)90201-7

Journal of Insect Physiology

Volume 15, Issue 8, August 1969, Pages 1421-1430

https://doi.org/10.1016/0022-1910(69)90201-7 Get rights and content

Abstract

The ionic concentrations of sodium, potassium, magnesium, calcium, and chloride in the haemolymph and saliva of Boophilus microplus have been determined together with the osmotic pressures. The elimination of electrolytes along with excess water in the saliva prevents osmotic and electrolytic imbalance in the tick. The difference between the sodium and chloride ion intake and that retained by the tick is accounted for by the calculated content of the saliva. The salivary secretory mechanism is able to exercise some regulatory control over the haemolymph osmotic pressure and the ionic concentrations in the engorged tick. The amino acid composition of the haemolymph is stated.

References (20)

D.W. Sutcliffe
The chemical composition of haemolymph in insects and some other arthropods in relation to their phylogeny
Comp. Biochem. Physiol.
(1963)
L. Barton Browne et al.
Some changes resulting from water deprivation in the blowfly Lucilia cuprina
J. Insect Physiol.
(1968)
R.J. Best
A rapid electrometric method for determining chloride content of soils
J. agric. Sci.
(1929)
G.J. Boné
Récherches sur les glandes coxales et la régulation du milieu interne chez l'Ornithodorus moubata Murray
Annls Soc. r. zool. Belg.
(1943)
J.P.T. Boorman
Observations on the feeding habits of the mosquito Aedes (Stegomyia) aegypti (Linnaeus): The loss of fluid after a blood-meal and the amount of blood taken during feeding
Ann. trop. Med. Parasit.
(1960)
D.S. Dittmer
J.D. Gregson
Electrical observations of tick feeding in relation to disease transmission
L.L. Jones
Osmotic regulation in several crabs of the Pacific coast of North America
J. cell. comp. Physiol.
(1941)
A.D. Lees
Chloride regulation and the function of the coxal glands in ticks
Parasitology
(1946)
H.M.O. Lester et al.
Notes on the process of digestion in tsetse-flies
Bull. ent. Res.
(1928)

There are more references available in the full text version of this article.

Cited by (45)

Role of Rhipicephalus microplus cheliceral receptors in gustation and host differentiation
2015, Ticks and Tick-borne Diseases
Citation Excerpt :
R. microplus is able to tolerate large amounts of salt, since it performs the osmotic and ionic balance by removing excess electrolytes ingested during feeding through salivation. The amount of sodium ions in the bovine blood is six times higher than the amount of potassium ions (Tatchell, 1969). Although salts can be phagostimulants for many insects (Smedley and Eisner, 1995) it is believed that the ability to perceive salts in animals is more implicated in warnings against hypersalinity than in a mechanism responsive to sodium needs, thus triggering a deterrent response (Dethier, 1977).
Rhipicephalus microplus is considered the most economically important ectoparasite of cattle worldwide. It is known that zebuine breeds of cattle are less susceptible to tick infestation than taurine breeds. Contact chemoreceptors in the cheliceral pit sensilla of ticks respond selectively to phagostimulant compounds, however their role in blood feeding relative to host susceptibility to infestation remains to be fully understood. We addressed this topic by conducting taste electrophysiology experiments with cheliceral pit sensilla preparations of R. microplus females. Solutions of five known ixodid tick phagostimulants were tested at different concentrations: sodium (NaCl), and potassium chloride (KCl) (10⁻³–10⁻¹ M); glucose (10⁻⁴–10⁻¹ M); adenosine triphosphate (ATP) (10⁻⁶–10⁻² M); and reduced l-glutathione (GSH) (10⁻⁶–10⁻² M). Serum samples from six susceptible animals of the Girolando breed (5/8 Bos indicus × 3/8 B. taurus) and six resistant Nelore bovines (pure B. indicus) were also tested. A dose-dependent response of gustatory neurons associated with the chelicerae sensillum to NaCl, glucose, GSH, and ATP were observed. Responses by the cheliceral inner digit pit sensilla of R. microplus to KCl and glucose were also observed and they are reported here for the first time. In addition to an electrophysiological response to known phagostimulants, chemoreceptors in the chelicera of R. microplus responded differently to serum from cattle susceptible and resistant to infestation. The cheliceral pit neurons were more responsive to serum of R. microplus resistant bovines with a higher mean spike frequency (53.5 ± 2 spikes s⁻¹) than to serum samples from susceptible cattle (40.3 ± 2 spikes s⁻¹). The implications of chemosensation during tick blood feeding are discussed.
Ticks: Physiological aspects with implications for pathogen transmission
2010, Ticks and Tick-borne Diseases
Ticks have attracted a great deal of scientific attention primarily because of their role as vectors of numerous pathogens. The majority of tick researchers worldwide focus primarily on microbiological and clinical issues relating to these pathogens, and on methods (pesticidal and biological) for controlling tick populations. Unfortunately, it is often forgotten that ticks are also interesting in their own right to the general biologist because of their unusual physiological (and other) adaptations. Here I review some of these adaptations relating primarily to osmoregulation. (i) I outline their ability to take up water vapour directly from the atmosphere, an adaptation that enables them to withstand desiccation for extended periods while unfed and, in the case of larvae and nymphs, following engorgement. (ii) I present the remarkable filtration–resorption mechanism of the argasid tick coxal organ, analogous to that of the vertebrate glomerular kidney, that enables them to regulate haemolymph fluid volume and composition following the blood meal. (iii) I then turn attention to the salivary glands of female ixodid ticks, which serve the on-host osmoregulatory function in this family of ticks, (iv) and I discuss the pharmacological control of salivary fluid secretion. (v) Finally, I link the latter to the mechanism of pathogen transmission by the salivary glands, using the tick-borne Thogoto virus as a specific example.
Morphological, histological, and ultrastructural characterization of degenerating salivary glands in females of the cattle-tick Rhipicephalus (Boophilus) microplus (CANESTRINI, 1887) (Acari: Ixodidae)
2005, Micron
The present study describes the morphology and ultrastructure of the salivary glands of semi-engorged females of the southern cattle-tick Rhipicephalus (Boophilus) microplus. The acini that compose these glands, at that specific feeding stage, show cells featuring degenerative process of the salivary glands, such as: vacuolated cytoplasm, condensed chromatin, fragmented nuclei, and presence of apoptotic bodies. In addition, the presence of microorganisms was detected, with morphology typical of protozoa, inside these organs.
Morphological evidence that salivary gland degeneration in the American dog tick, Dermacentor variabilis (Say), involves programmed cell death
2003, Tissue and Cell
During the preoviposition and oviposition periods of ixodid ticks, the salivary glands degenerate. It is unclear whether this is a necrotic or a programmed cell death event. We used an in situ TUNEL technique to determine if salivary gland degeneration involves apoptosis. Salivary glands were dissected from replete females at days 3, 5, 8, 11, 13, and 33 post-detachment. There were no differences in tick weight at detachment, suggesting that changes were not due to engorgement abnormalities. The onset of apoptosis began at day 5 and continued through oviposition at day 33. The greatest amount of nuclei containing fragmented DNA was observed on day 8 post-detachment, suggesting this was the peak occurrence of programmed cell death. Further, the temporal organization of programmed cell death suggests that the granule-secreting acini undergo apoptosis first, and that during the first week of oviposition the type I acini do not exhibit programmed cell death. These data suggest that the type I acini may still function in maintaining off-host hydration state of ovipositing females. These data provide morphological evidence that salivary gland degeneration involves a temporal programmed cell death event.
Salivary glands and saliva of Amblyomma variegatum ticks: comparison of immatures and adults in relation to the pathogenesis of dermatophilosis
1995, Veterinary Parasitology
Salivary glands from immature and adult Amblyomma variegatum were compared for differences in potential components responsible for the systemic aggravation by adult ticks of the skin disease dermatophilosis. Whole salivary glands from adult, nymphal and larval A. variegatum ticks were compared for structural differences by light microscopy and for protein content by gel electrophoresis. Type-2 salivary gland acini from adult ticks at the second stage of feeding contained significantly greater (P<0.01) proportions of c1 secretory granules than those from either of the immature instars. There was also significantly more area occupied with e secretory granules in the type-3 salivary gland acini from adult ticks compared with larval ticks. Electrophoresis of whole salivary glands showed seven bands present only in the adult material; of these, three were dense bands at 37, 35 and 31 kDA. Electrophoresis of saliva from adult and nymphal. A. variegatum obtained by artificial stimulation showed that nine bands were unique to the saliva produced by adults; of these nine bands one was a dense band at 67 kDa. It was concluded that adult salivary material was different from that of immature ticks and that further studies on the relationship between the feeding of adult A. variegatum and dermatophilosis should investigate these components unique to the adults.
Evidence of a myoepithelial cell in tick salivary glands
1994, International Journal for Parasitology
Type III acini from feeding female Dermacentor variabilis varied in size during in vitro and in vivo fluid production. As the type III acinus enlarged, its lumen enlarged and the adlumenal cell became thinner. As the acinus contracted, its lumen became smaller while the adlumenal cell became wider. Actin was demonstrated in salivary glands using an immunoblot technique. Actin was localized in the adlumenal cells of type III acini with fluorescent microscopy using rhodamine-phalloidin and with electron microscopy using heavy meromyosin to decorate actin filaments. Pre-treatment of salivary glands with cytochalasin D abolished fluorescence in adlumenal cells subsequently treated with rhodamine-phalloidin. These results support the hypothesis that the adlumenal cell in type III acini functions as a myoepithelial cell.

View all citing articles on Scopus

View full text

Article preview

Journal of Insect Physiology

Abstract

References (20)

The chemical composition of haemolymph in insects and some other arthropods in relation to their phylogeny

Comp. Biochem. Physiol.

Some changes resulting from water deprivation in the blowfly Lucilia cuprina

J. Insect Physiol.

A rapid electrometric method for determining chloride content of soils

J. agric. Sci.

Récherches sur les glandes coxales et la régulation du milieu interne chez l'Ornithodorus moubata Murray

Annls Soc. r. zool. Belg.

Observations on the feeding habits of the mosquito Aedes (Stegomyia) aegypti (Linnaeus): The loss of fluid after a blood-meal and the amount of blood taken during feeding

Ann. trop. Med. Parasit.

Electrical observations of tick feeding in relation to disease transmission

Osmotic regulation in several crabs of the Pacific coast of North America

J. cell. comp. Physiol.

Chloride regulation and the function of the coxal glands in ticks

Parasitology

Notes on the process of digestion in tsetse-flies

Bull. ent. Res.

Cited by (45)

Role of Rhipicephalus microplus cheliceral receptors in gustation and host differentiation

Ticks: Physiological aspects with implications for pathogen transmission

Morphological, histological, and ultrastructural characterization of degenerating salivary glands in females of the cattle-tick Rhipicephalus (Boophilus) microplus (CANESTRINI, 1887) (Acari: Ixodidae)

Morphological evidence that salivary gland degeneration in the American dog tick, Dermacentor variabilis (Say), involves programmed cell death

Salivary glands and saliva of Amblyomma variegatum ticks: comparison of immatures and adults in relation to the pathogenesis of dermatophilosis

Evidence of a myoepithelial cell in tick salivary glands