Serotonin-like immunoreactivity in the central nervous system of two ixodid tick species

Article
First Online:
Received:
Accepted:

Abstract

Immunocytochemistry was used to describe the distribution of serotonin-like immunoreactive (5HT-IR) neurons and neuronal processes in the central nervous system (CNS), the synganglion, of two ixodid tick species; the winter tick, Dermacentor albipictus and the lone star tick, Amblyomma americanum. 5HT-IR neurons were identified in the synganglion of both tick species. D. albipictus had a significantly higher number of 5HT-IR neurons than A. americanum. The labeling pattern and number of 5HT-IR neurons were significantly different between sexes in D. albipictus, but were not significantly different between sexes in A. americanum. 5HT-IR neurons that were located in the cortex of the synganglion projected processes into the neuropils, invading neuromeres in the supraesophageal ganglion including the protocerebrum, postero-dorsal, antero-dorsal and cheliceral neuromeres. In the subesophageal ganglion, dense 5HT-IR neuronal processes were found in the olfactory lobes, pedal, and opisthosomal neuromeres. Double-labeling with neurobiotin backfilled from the first leg damaged at the Haller’s organ revealed serotoninergic neuronal processes surrounding the glomeruli in the olfactory lobes. The high number of the 5HT-IR neurons and the extensive neuronal processes present in various regions of the synganglion suggest that serotonin plays a significant role in tick physiology.

Keywords

5-Hydroxytryptamine 5-HT Acari Amblyomma americanum Dermacentor albipictus Synganglion 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

We thank K. M. Collins, J. B. Welch, Z. Syed and two anonymous reviewers for critically reviewing this manuscript. We thank N. Davis for generously training N. A. H. in immunocytochemical methods; the RCMI Advanced Imaging Core Facility at University of Texas, San Antonio for use of the Zeiss LSM 510; and J. M. Pound for thoughtful discussion. We also thank D. Burchers for rearing ticks and technical support. N. A. H. is supported by a USDA, ARS, Postdoctoral Research Associate Program award to A. Y. L.

References

  1. Binnington KC (1983) Ultrastructural identification of neurohemal sites in a tick: evidence that the dorsal complex may be a true endocrine gland. Tiss Cell 15:317–327CrossRefGoogle Scholar
  2. Binnington KC, Tatchell RJ (1973) The nervous system and neurosecretory cells of Boophilus microplus (Acarina, Ixodidae). Z Wiss Zool 185:193–206Google Scholar
  3. Bowman AS, Sauer JR (2004) Tick salivary glands: function, physiology and future. Parasitology 129(Suppl):S67–S81PubMedGoogle Scholar
  4. Chen A, Holmes SP, Pietrantonio PV (2004) Molecular cloning and functional expression of a serotonin receptor from the southern cattle tick, Boophilus microplus (Acari: Ixodidae). Insect Mol Biol 13:45–54PubMedCrossRefGoogle Scholar
  5. Chow YS, Wang CH (1974) Neurosecretory cells and their ultrastructures of Rhipicephalus sanguineus (Latreille) (Acarina: Ixodidae). Acta Arachnol 25:53–67Google Scholar
  6. Coast GM, Orchard I, Phillips JE, Schooley DA (2002) Insect diuretic antidiuretic hormones. Adv Insect Physiol 29:273–280Google Scholar
  7. Dacks AM, Nickel T, Mitchell BK (2003) An examination of serotonin and feeding in the flesh fly Neobellieria bullata (Sarcophagidae: Diptera). J Insect Behav 16:1–21CrossRefGoogle Scholar
  8. Dacks AM, Christensen TA, Hildebrand JG (2006) Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498:727–746PubMedCrossRefGoogle Scholar
  9. Davis NT, Hildebrand JG, Homberg U, Agricola H-J, Teal PEA, Altstein M (1996) Neuroanatomy and immunocytochemistry of the median neuroendocrine cells of the subesophageal ganglion of the tobacco hawkmoth, Manduca sexta: immunoreactivities to PBAN and other neuropeptides. Microsc Res Tech 35:201–229PubMedCrossRefGoogle Scholar
  10. Dekeyser MA (2005) Acaricide mode of action. Pest Manag Sci 61:103–110PubMedCrossRefGoogle Scholar
  11. Dhanda V (1967) Changes in neurosecretory activity at different stages in the adult Hyalomma dromedarii Koch, 1844. Nature 214:508–509PubMedCrossRefGoogle Scholar
  12. Drummond RO (2004) Ticks and what you can do about them. Wilderness Press, Berkeley, CaliforniaGoogle Scholar
  13. Eichenberger G (1970) Das zentralnervensystem won Ornithodorus moubata (Murray), Ixodidae: Argasidae, und seine postembryonale Entwicklung. Acta Trop XXVII:15–53Google Scholar
  14. Eisen Y, Warburg MR, Galun R (1973) Neurosecretory activity as related to feeding and oogenesis in the fowl-tick Argas persicus (Oken). Gen Comp Endocrinol 21:331–340PubMedCrossRefGoogle Scholar
  15. Fain JM, Berridge MJ (1979) Relationship between hormonal activation of phosphatidylinositol hydrolysis, fluid secretion and calcium flux in the blowfly salivary gland. Biochem J 178:45–58PubMedGoogle Scholar
  16. Gabbay S, Warburg MR (1977) The diversity of neurosecretory cell types in the cave tick Ornithodoros tholozani. J Morphol 153:371–386CrossRefGoogle Scholar
  17. Gabe M (1955) Histological data on neurosecretion in arachnids. Arch Anat Microsc Morphol Exp 44:351–383Google Scholar
  18. George JE, Davey RB, Pound JM (2002) Introduced ticks and tick-borne disease: the threat and approaches to eradication. Vet Clin Food Anim 18:401–416CrossRefGoogle Scholar
  19. Harrewijn P, Kayser H (1997) Pymetrozine, a fast-acting and selective inhibitor of aphid feeding. In-situ studies with electronic monitoring of feeding behaviour. Pestic Sci 49:130–140CrossRefGoogle Scholar
  20. Ioffe ID (1964) Distribution of neurosecretory cells in the central nervous system of Dermacentor pictus Herm. (Acarina, Chelicerata). Dokl Akad Nauk SSSR S Evoluts Morfol 154:229–232Google Scholar
  21. Kloppenburg P, Hildebrand JG (1995) Neuromodulation by 5-hydroxytryptamine in the antennal lobe of the sphinx moth Manduca sexta. J Exp Biol 198:603–611PubMedGoogle Scholar
  22. Kloppenburg P, Ferns D, Mercer AR (1999) Serotonin enhances central olfactory neuron responses to female sex pheromone in the male sphinx moth Manduca sexta. J Neurosci 19:8172–8181PubMedGoogle Scholar
  23. Lange AB (2004) A neurohormonal role for serotonin in the control of locust oviducts. Arch Insect Biochem Physiol 56:179–190PubMedCrossRefGoogle Scholar
  24. Lange AB, Orchard I, Barrett FM (1989) Changes in haemolymph serotonin levels associated with feeding in the blood-sucking bug, Rhodnius prolixus. J Insect Phys 35:393–399CrossRefGoogle Scholar
  25. Li AY, Davey RB, Miller RJ, George JE (2003) Resistance to coumaphos and diazinon in Boophilus microplus (Acari: Ixodidae) and evidence for the involvement of an oxidative detoxification mechanism. J Med Entomol 40:482–490PubMedGoogle Scholar
  26. Li AY, Davey RB, Miller RJ, George JE (2004) Detection and characterization of amitraz resistance in the Southern Cattle Tick, Boophilus microplus (Acari: Ixodidae). J Med Entomol 41:193–200PubMedCrossRefGoogle Scholar
  27. Li AY, Davey RB, Miller RJ, George JE (2005) Mode of inheritance of amitraz resistance in a Brazilian strain of the southern cattle tick, Boophilus microplus (Acari: Ixodidae). Exp Appl Acarol 37:183–198PubMedCrossRefGoogle Scholar
  28. McSwain JL, Tucker JS, Essenberg RC, Sauer JR (1989) Brain factor induced formation of inositol phosphates in tick salivary glands. Insect Biochem 19:343–350CrossRefGoogle Scholar
  29. Meola S (1970) Sensitive paraldehyde-fuschin technique for neurosecretory system of mosquitoes. Trans Am Microsc Soc 89:66–71CrossRefGoogle Scholar
  30. Mercer A, Hayashi J, Hildebrand JG (1995) Modulatory effects of 5-hydroxytryptamine on voltage-gated currents in cultured antennal lobe neurons of the sphinx moth Manduca sexta. J Exp Biol 198:613–627PubMedGoogle Scholar
  31. Mercer A, Kloppenburg P, Hildebrand J (1996) Serotonin-induced changes in the excitability of cultured antennal-lobe neurons of the sphinx moth Manduca sexta. J Comp Physiol A178:21–31Google Scholar
  32. Nässel DR (1988) Serotonin and serotonin-immunoreactive neurons in the nervous system of insects. Prog Neurobiol 30:1–85PubMedCrossRefGoogle Scholar
  33. Obenchain FD (1974a) Structure and anatomical relationships of the synganglion in the American dog tick, Dermacentor variabilis (Acari: Ixodidae). J Morphol 142:205–224CrossRefGoogle Scholar
  34. Obenchain FD (1974b) Neurosecretory system of the American dog tick, Dermacentor variabilis (Acari: Ixodidae). I. Diversity of cell types. J Morphol 142:433–446CrossRefGoogle Scholar
  35. Obenchain FD, Oliver Jr JH (1975) Neurosecretory system of the American dog tick, Dermacentor variabilis (Acari: Ixodidae). II. Distribution of secretory cell types, axonal pathways and putative neurohemal-neuroendocrine associations; comparative histological and anatomical implications. J Morphol 145:269–294PubMedCrossRefGoogle Scholar
  36. Paine SH, Kemp DH, Allen JR (1983) In vitro feeding of Dermacentor andersoni (Stiles): effects of histamine and other mediators. Parasitology 86:419–428PubMedCrossRefGoogle Scholar
  37. Pound JM, Oliver Jr JH (1982) Synganglial and neurosecretory morphology of female Ornithodoros parkeri (Cooley) (Acari: Argasidae). J Med Entomol 173:159–177Google Scholar
  38. Prullage JB, Pound JM, Meola SM (1992) Synganglial morphology and neurosecretory centers of adults Amblyomma americanum (L.) (Acari: Ixodidae). J Med Entomol 29:1023–1034PubMedGoogle Scholar
  39. Roshdy MA, Shourkey NM, Coons LB (1973) The subgenus Persicargas (Ixodoidea: Argasidae: Argas). 17. A neurohemal organ in A. (P.) arboreus Kaiser, Hoogstraal, and Kohls. J Parasitol 59:540–544CrossRefGoogle Scholar
  40. SAS Institute (1998) SAS/STAT user’s guide, release 6.03 edition. SAS Institute, CaryGoogle Scholar
  41. Seyfarth E-A, Hammer K, Grünert U (1990a) Serotonin-like immunoreactivity in the CNS of spiders. Verh Dtsch Zool Ges 83:640 (text in German)Google Scholar
  42. Seyfarth E-A, Hammer K, Grünert U (1990b) Serotonin—like immunoreactivity in the CNS of spiders. In: Elsner N, Roth G (eds) Brain—perception, cognition. Proceedings of the 18th Göttingen neurobiology conference. Thieme Verlag Stuttgart, New York, p 321Google Scholar
  43. Schachtner J, Bräunig P (1993) The activity pattern of identified neurosecretory cells during feeding behavior in the locust. J Exp Biol 185:287–303PubMedGoogle Scholar
  44. Sonenshine DE (1991) Biology of ticks, vol 1. Oxford University Press, New York, p 447Google Scholar
  45. Steullet P, Guerin PM (1994) Identification of vertebrate volatiles stimulating olfactory receptors on tarsus I of the tick Amblyomma variegatum Fabricius (Ixodidae). I. Receptors within the Haller’s organ capsule. J Comp Physiol A 174:27–38PubMedGoogle Scholar
  46. Szlendak E, Oliver Jr JH (1992) Anatomy of synganglia, including their neurosecretory regions, in unfed, virgin female Ixodes scapularis Say (Acari: Ixodidae). J Morphol 213:349–364PubMedCrossRefGoogle Scholar
  47. van Wijk M, Wadman WJ, Sabelis MW (2006) Morphology of the olfactory system in the predatory mite Phytoseiulus persimilis. Exp Appl Acarol 40:217–229PubMedCrossRefGoogle Scholar
  48. Zhu XX, Oliver Jr JH (1991) Immunocytochemical localization of an insulin-like substance in the synganglion of the tick Ornithodoros parkeri (Acari: Argasidae). Exp Appl Acarol 13:153–160PubMedCrossRefGoogle Scholar
  49. Zhu XX, Oliver Jr JH (2001) Cockroach allatostatin-like immunoreactivity in the synganglion of the American dog tick Dermacentor variabilis (Acari: Ixodidae). Exp Appl Acarol 25:1005–1013PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.ARS, Knipling-Bushland U.S. Livestock Insects Research LaboratoryUSDAKerrvilleUSA
  2. 2.Department of EntomologyLouisiana State UniversityBaton RougeUSA
  3. 3.Department of Biology, RCMI Advanced Imaging CoreUniversity of Texas at San AntonioSan AntonioUSA

Personalised recommendations