Cuticular plasticization in the tick, Amblyomma hebraeum (Acari: Ixodidae): possible roles of monoamines and cuticular pH

W R Kaufman, P C Flynn, Stuart E Reynolds

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

The degree of plasticization of the alloscutal cuticle of a 'hard' (ixodid) tick, Amblyomma hebraeum, and a 'soft' (argasid) tick, Ornithodoros moubata, was assessed throughout the blood-feeding period. Cuticle viscosity was calculated from rate of creep of cuticle under constant load using a Maxwell model. Feeding-related plasticization (i.e. increased rate of extension under a constant load) occurred in A. hebraeum but not in O. moubata. Maxwell viscosity of unfed A. hebraeum cuticle was relatively high (similar to 720. GPa. s) but was significantly lower in feeding ticks. Small partially fed ticks displayed a viscosity of similar to 108 GPa. s. Still lower values (42 GPa. s) were observed in the largest of the engorged ticks. Following cessation of feeding, there was a significant but limited reversal in viscosity back to similar to 100. GPas. The water content of cuticle of unfed A. hebraeum (23.4% of wet mass) rose sharply after the onset of feeding and reached a plateau value of 34.0% at a fed/unfed weight ratio of 3 and beyond. Ixodid ticks lay down new endocuticle during the feeding period. The observed increase in cuticle hydration suggests that both old and new cuticles are hydrated during feeding. Monoamines may play an important role in controlling cuticle viscosity. Dopamine (DA) injected into partially fed A. hebraeum caused plasticization. 5-Hydroxytryptamine (serotonin, 5-HT), which induces plasticization in the blood-sucking insect Rhodnius prolixus, had no statistically significant effect on tick cuticle. Octopamine (OA) and tyramine both caused cuticle stiffening (i.e. opposed plasticization). This suggests a possible inhibitory effect but co-injection of OA with DA did not reduce DA-induced plasticization. The mechanism leading to plasticization of tick cuticle may involve a change in cuticular pH. The viscosity of tick cuticle loops was highest at pH. 8.0 (389 GPa. s) and fell precipitously in the acidic range to a low value of 2.2. GPa. s at pH 5.5-5.7. A cuticular pH of similar to 6.5 would account for the lowest viscosity observed under physiological conditions (42.4 GPa. s for large, day 0, engorged ticks). The V-ATPase inhibitor, concanamycin A, was a potent inhibitor of DA-induced plasticization. These results are consistent with a model in which DA acts to cause plasticization through transport of H+ ions into the cuticle. Measurement of cuticular ion (Na+, K+, Ca2+, Mg2+) content did not suggest that plasticization is caused by any of these ions. Taken together, our results suggest that the mechanism of cuticular plasticization in feeding A. hebraeum is related to hydration, and involves the transport of H+ ions into the sub-cuticular space by cells in the hypodermis. Feeding-induced plasticization was not observed in the rapid feeding tick, O. moubata.
Original languageEnglish
Pages (from-to)2820-2831
Number of pages12
JournalThe Journal of Experimental Biology
Volume213
Issue number16
DOIs
Publication statusPublished - 15 Aug 2010

Fingerprint

Amblyomma hebraeum
Ixodidae
monoamines
tick
Ticks
cuticle
ticks
Acari
Viscosity
viscosity
dopamine
Ornithodoros moubata
Dopamine
serotonin
Octopamine
ions
octopamine
Serotonin
Ion Transport
ion

Keywords

  • 5-hydroxytryptamine
  • dopamine
  • Amblyomma hebraeum
  • ticks
  • concanamycin A
  • tyramine
  • octopamine
  • Ornithodoros moubata
  • cuticular plasticization

Cite this

Cuticular plasticization in the tick, Amblyomma hebraeum (Acari: Ixodidae): possible roles of monoamines and cuticular pH. / Kaufman, W R; Flynn, P C; Reynolds, Stuart E.

In: The Journal of Experimental Biology, Vol. 213, No. 16, 15.08.2010, p. 2820-2831.

Research output: Contribution to journalArticle

@article{1bb21094ad99409b92a167362fb50da5,
title = "Cuticular plasticization in the tick, Amblyomma hebraeum (Acari: Ixodidae): possible roles of monoamines and cuticular pH",
abstract = "The degree of plasticization of the alloscutal cuticle of a 'hard' (ixodid) tick, Amblyomma hebraeum, and a 'soft' (argasid) tick, Ornithodoros moubata, was assessed throughout the blood-feeding period. Cuticle viscosity was calculated from rate of creep of cuticle under constant load using a Maxwell model. Feeding-related plasticization (i.e. increased rate of extension under a constant load) occurred in A. hebraeum but not in O. moubata. Maxwell viscosity of unfed A. hebraeum cuticle was relatively high (similar to 720. GPa. s) but was significantly lower in feeding ticks. Small partially fed ticks displayed a viscosity of similar to 108 GPa. s. Still lower values (42 GPa. s) were observed in the largest of the engorged ticks. Following cessation of feeding, there was a significant but limited reversal in viscosity back to similar to 100. GPas. The water content of cuticle of unfed A. hebraeum (23.4{\%} of wet mass) rose sharply after the onset of feeding and reached a plateau value of 34.0{\%} at a fed/unfed weight ratio of 3 and beyond. Ixodid ticks lay down new endocuticle during the feeding period. The observed increase in cuticle hydration suggests that both old and new cuticles are hydrated during feeding. Monoamines may play an important role in controlling cuticle viscosity. Dopamine (DA) injected into partially fed A. hebraeum caused plasticization. 5-Hydroxytryptamine (serotonin, 5-HT), which induces plasticization in the blood-sucking insect Rhodnius prolixus, had no statistically significant effect on tick cuticle. Octopamine (OA) and tyramine both caused cuticle stiffening (i.e. opposed plasticization). This suggests a possible inhibitory effect but co-injection of OA with DA did not reduce DA-induced plasticization. The mechanism leading to plasticization of tick cuticle may involve a change in cuticular pH. The viscosity of tick cuticle loops was highest at pH. 8.0 (389 GPa. s) and fell precipitously in the acidic range to a low value of 2.2. GPa. s at pH 5.5-5.7. A cuticular pH of similar to 6.5 would account for the lowest viscosity observed under physiological conditions (42.4 GPa. s for large, day 0, engorged ticks). The V-ATPase inhibitor, concanamycin A, was a potent inhibitor of DA-induced plasticization. These results are consistent with a model in which DA acts to cause plasticization through transport of H+ ions into the cuticle. Measurement of cuticular ion (Na+, K+, Ca2+, Mg2+) content did not suggest that plasticization is caused by any of these ions. Taken together, our results suggest that the mechanism of cuticular plasticization in feeding A. hebraeum is related to hydration, and involves the transport of H+ ions into the sub-cuticular space by cells in the hypodermis. Feeding-induced plasticization was not observed in the rapid feeding tick, O. moubata.",
keywords = "5-hydroxytryptamine, dopamine, Amblyomma hebraeum, ticks, concanamycin A, tyramine, octopamine, Ornithodoros moubata, cuticular plasticization",
author = "Kaufman, {W R} and Flynn, {P C} and Reynolds, {Stuart E}",
year = "2010",
month = "8",
day = "15",
doi = "10.1242/jeb.044412",
language = "English",
volume = "213",
pages = "2820--2831",
journal = "The Journal of Experimental Biology",
issn = "0022-0949",
publisher = "Company of Biologists Ltd",
number = "16",

}

TY - JOUR

T1 - Cuticular plasticization in the tick, Amblyomma hebraeum (Acari: Ixodidae): possible roles of monoamines and cuticular pH

AU - Kaufman, W R

AU - Flynn, P C

AU - Reynolds, Stuart E

PY - 2010/8/15

Y1 - 2010/8/15

N2 - The degree of plasticization of the alloscutal cuticle of a 'hard' (ixodid) tick, Amblyomma hebraeum, and a 'soft' (argasid) tick, Ornithodoros moubata, was assessed throughout the blood-feeding period. Cuticle viscosity was calculated from rate of creep of cuticle under constant load using a Maxwell model. Feeding-related plasticization (i.e. increased rate of extension under a constant load) occurred in A. hebraeum but not in O. moubata. Maxwell viscosity of unfed A. hebraeum cuticle was relatively high (similar to 720. GPa. s) but was significantly lower in feeding ticks. Small partially fed ticks displayed a viscosity of similar to 108 GPa. s. Still lower values (42 GPa. s) were observed in the largest of the engorged ticks. Following cessation of feeding, there was a significant but limited reversal in viscosity back to similar to 100. GPas. The water content of cuticle of unfed A. hebraeum (23.4% of wet mass) rose sharply after the onset of feeding and reached a plateau value of 34.0% at a fed/unfed weight ratio of 3 and beyond. Ixodid ticks lay down new endocuticle during the feeding period. The observed increase in cuticle hydration suggests that both old and new cuticles are hydrated during feeding. Monoamines may play an important role in controlling cuticle viscosity. Dopamine (DA) injected into partially fed A. hebraeum caused plasticization. 5-Hydroxytryptamine (serotonin, 5-HT), which induces plasticization in the blood-sucking insect Rhodnius prolixus, had no statistically significant effect on tick cuticle. Octopamine (OA) and tyramine both caused cuticle stiffening (i.e. opposed plasticization). This suggests a possible inhibitory effect but co-injection of OA with DA did not reduce DA-induced plasticization. The mechanism leading to plasticization of tick cuticle may involve a change in cuticular pH. The viscosity of tick cuticle loops was highest at pH. 8.0 (389 GPa. s) and fell precipitously in the acidic range to a low value of 2.2. GPa. s at pH 5.5-5.7. A cuticular pH of similar to 6.5 would account for the lowest viscosity observed under physiological conditions (42.4 GPa. s for large, day 0, engorged ticks). The V-ATPase inhibitor, concanamycin A, was a potent inhibitor of DA-induced plasticization. These results are consistent with a model in which DA acts to cause plasticization through transport of H+ ions into the cuticle. Measurement of cuticular ion (Na+, K+, Ca2+, Mg2+) content did not suggest that plasticization is caused by any of these ions. Taken together, our results suggest that the mechanism of cuticular plasticization in feeding A. hebraeum is related to hydration, and involves the transport of H+ ions into the sub-cuticular space by cells in the hypodermis. Feeding-induced plasticization was not observed in the rapid feeding tick, O. moubata.

AB - The degree of plasticization of the alloscutal cuticle of a 'hard' (ixodid) tick, Amblyomma hebraeum, and a 'soft' (argasid) tick, Ornithodoros moubata, was assessed throughout the blood-feeding period. Cuticle viscosity was calculated from rate of creep of cuticle under constant load using a Maxwell model. Feeding-related plasticization (i.e. increased rate of extension under a constant load) occurred in A. hebraeum but not in O. moubata. Maxwell viscosity of unfed A. hebraeum cuticle was relatively high (similar to 720. GPa. s) but was significantly lower in feeding ticks. Small partially fed ticks displayed a viscosity of similar to 108 GPa. s. Still lower values (42 GPa. s) were observed in the largest of the engorged ticks. Following cessation of feeding, there was a significant but limited reversal in viscosity back to similar to 100. GPas. The water content of cuticle of unfed A. hebraeum (23.4% of wet mass) rose sharply after the onset of feeding and reached a plateau value of 34.0% at a fed/unfed weight ratio of 3 and beyond. Ixodid ticks lay down new endocuticle during the feeding period. The observed increase in cuticle hydration suggests that both old and new cuticles are hydrated during feeding. Monoamines may play an important role in controlling cuticle viscosity. Dopamine (DA) injected into partially fed A. hebraeum caused plasticization. 5-Hydroxytryptamine (serotonin, 5-HT), which induces plasticization in the blood-sucking insect Rhodnius prolixus, had no statistically significant effect on tick cuticle. Octopamine (OA) and tyramine both caused cuticle stiffening (i.e. opposed plasticization). This suggests a possible inhibitory effect but co-injection of OA with DA did not reduce DA-induced plasticization. The mechanism leading to plasticization of tick cuticle may involve a change in cuticular pH. The viscosity of tick cuticle loops was highest at pH. 8.0 (389 GPa. s) and fell precipitously in the acidic range to a low value of 2.2. GPa. s at pH 5.5-5.7. A cuticular pH of similar to 6.5 would account for the lowest viscosity observed under physiological conditions (42.4 GPa. s for large, day 0, engorged ticks). The V-ATPase inhibitor, concanamycin A, was a potent inhibitor of DA-induced plasticization. These results are consistent with a model in which DA acts to cause plasticization through transport of H+ ions into the cuticle. Measurement of cuticular ion (Na+, K+, Ca2+, Mg2+) content did not suggest that plasticization is caused by any of these ions. Taken together, our results suggest that the mechanism of cuticular plasticization in feeding A. hebraeum is related to hydration, and involves the transport of H+ ions into the sub-cuticular space by cells in the hypodermis. Feeding-induced plasticization was not observed in the rapid feeding tick, O. moubata.

KW - 5-hydroxytryptamine

KW - dopamine

KW - Amblyomma hebraeum

KW - ticks

KW - concanamycin A

KW - tyramine

KW - octopamine

KW - Ornithodoros moubata

KW - cuticular plasticization

UR - http://www.scopus.com/inward/record.url?scp=77955651326&partnerID=8YFLogxK

UR - http://dx.doi.org/10.1242/jeb.044412

U2 - 10.1242/jeb.044412

DO - 10.1242/jeb.044412

M3 - Article

VL - 213

SP - 2820

EP - 2831

JO - The Journal of Experimental Biology

JF - The Journal of Experimental Biology

SN - 0022-0949

IS - 16

ER -