2006. 14 (1)



Belozerov V. N.

About author:

Belozerov V. N., Biological Research Institute, St. Petersburg State University, Stary Peterhof, St. Petersburg, 198504, Russia


The problem of juvenile hormones (JHs) in ixodoid ticks is quite controversial and disputable due to contradictions in data on effects of JHs, juvenoids and their antagonists in these chelicerate arthropods. It remains unsolved until now even after recent studies by R.M. Roe’s group (USA), whose conclusion that JHs are absent in ticks and do not control their metamorphosis and reproduction (Roe et al. 1999b, 2001; Neese et al. 2000), was supported by some insect physiologists (Gilbert et al. 2000; Wilson 2004). However my investigations on limb regeneration in ticks have demonstrated specific morphogenetic effects of JH-agonists and antagonists upon sensillar sets in Haller’s organ regenerates (Belozerov 1999a, 2001 a,b,c, 2003a,b, 2004). They provided evidence of similarity between ticks (as chelicerate arthropods) and insects (as mandibulate arthropods) in regard to JHs and their function as “status quo” factors in the control of developmental processes. This is confirmed also by the retinoic acid (RA) juvenilizing effects known in insects (Nemec et al. 1993), and discovered recently in ixodid ticks (Belozerov 2003a, 2004a). Action of RA in morphogenetic processes in ticks is revealed also by its specific teratogenic effect through axial duplication of some compartments in Haller’s organ regenerates. The study of Haller’s organ regeneration in ticks provides positive perspectives for investigations in tick endocrinology and developmental biology, particularly in bioassaying of compounds with JH-activity for chelicerate arthropods.


Abdelmonem, A.E., Khalil, G.M., Sonenshine, D.E. and
Sallam, O.A. 1986. Effect of two insect growth
regulators on the camel tick, Hyalomma (H.) drom-
edarii (Ixodidae). Journal of Medical Entomology,
23: 156–162.

Bassal, T.T.M. 1974. Activity of juvenile hormone ana-
logues during embryogenesis in Hyalomma drom-
edarii (Ixodidae). Zeitschrift für Parasitenkunde,
45: 85–89.

Bassal, T.T.M. and Roshdy, M.A. 1974. Argas (Persi-
cargas) arboreus: juvenile hormone analog termi-
nation of diapause and oviposition control. Exper-
imental Parasitology, 36: 34–39.

Belozerov, V.N. 1999a. Juvenilization of Haller’s organ
regenerates in ixodid ticks (Acarina: Ixodidae) un-
der the effect of insect juvenile hormone mimics.
Entomological Review, 79 (1): 70–80 [in Russian:
Entomologicheskoe obozrenie, 78 (1): 211–223].

Belozerov, V.N. 1999b. Regenerative modifications in
the external structure of Haller’s organ in nymphs
of Ixodes ricinus L. (Acari: Ixodidae). Acarina, 7
(1): 29–33.

Belozerov, V.N. 1999c. Morphogenetic effect of insect
juvenile hormone analogs in ixodid ticks. In: Sev-
enth International Conference on the Juvenile Hor-
mones (Jerusalem, August 29 – September 3, 1999),
Abstracts. Session 8–1.

Belozerov, V.N. 2000. Reparative regeneration in ticks
(Acari: Ixodoidea) and its hormonal control. In: A.
Buczek and C. Blaszak (Eds.) Stawonogi paso¿yt-
nuicze i alergogenne, Publisher KGM, Lublin, pp.

Belozerov, V.N. 2001a. Regeneration of limbs and sen-
sory organs in ixodoid ticks (Acari: Ixodoidea:
Ixodidae, Argasidae). Russian Journal of Develop-
mental Biology, 32 (3): 129–142 [in Russian: On-
togenez, 32 (3): 163–179].

Belozerov, V.N. 2001b. Effect of precocene on larval
development and regeneration of Haller’s organ
during larval-nymphal metamorphosis of Ixodes
ricinus (Acari: Ixodidae). Entomological Review,
81 (4): 200–210 [in Russian: Entomologicheskoe
obozrenie, 80 (2): 244–254].

Belozerov, V.N. 2001c. Some problems concerning the
role of juvenile hormones in the control of develop-
ment in ticks (Acari: Ixodoidea). In: A. Buczek and
C. Blaszak (Eds.) Stawonogi paso¿yty i nosiciele,
Publisher KGM, Lublin, pp. 45–57.

Belozerov, V.N. 2002a. New cases of the capsule dupli-
cation in Haller’s organ of immature Ixodes ticks
(Acari: Ixodidae). Acarina, 10 (1): 75–79.

Belozerov, V.N. 2002b. Haller’s organ regeneration as
a model for studying tick endocrinology and devel-
opmental biology. In: 4th International Conference
on Ticks and Tick-Borne Pathogens (Banff, Cana-
da, 21–26 July 2002), Program and Abstracts, p. 72.

Belozerov, V.N. 2002c [About the role of juvenile
hormones in the control of development in ixodid
ticks]. In: 7th Congress of Russian Entomol. Soci-
ety (St. Petersburg, August 19–24, 2002), Ab-
stracts. St. Petersburg, p. 33–34. [in Russian]

Belozerov, V.N. 2003a. Effects of juvenoids and retin-
oic acid on development of larvae and nymphs in
the tick Ixodes ricinus L. (Acari: Ixodidae) and
regeneration of Haller’s organ in them during met-
amorphosis. Russian Journal of Developmental
Biology, 34 (1): 42–50 [in Russian: Ontogenez, 34
(1): 50–60].

Belozerov, V.N. 2003b. Duplication of the Anterior-pit
compartment in adult regenerates of Haller’s organ
of the tick Hyalomma anatolicum (Acari: Ixodidae)
under influence of retinoic acid. Acarina, 11 (1):

Belozerov, V.N. 2004a. Specific features of Haller’s
organ regeneration in the tick Haemaphysalis long-
icornis (Acari, Ixodidae) in the presence of metho-
prene and retinoic acid. Russian Journal of Devel-
opmental Biology, 35 (3): 168–173 [in Russian:
Ontogenez, 35 (3): 213–219].

Belozerov, V.N. 2004b. Juvenile hormones in develop-
ment of ixodid ticks: pro et contra? In: Fifth Sym-
posium of the European Association of Acarolo-
gists (EURAAC) (26–30 July 2004, Berlin), Pro-
gramme, Abstracts. Freie Universität Berlin, p.27.

Belozerov, V.N. 2004c. [Participation of juvenoids and
retinoic acid in processes of reparative regeneration
and development in ixodid ticks (Acari: Ixodidae)].
In: Yu.S. Balashov (Ed.). VIII Russian Acarologi-
cal Congress (St. Petersburg, 30 November – 2
December, 2004). St. Petersburg, p. 22–24. [in

Belozerov, V.N., Kok, D.J. and Fourie, L.J. 1997. Re-
generation of Haller’s organ in the tick, Ixodes
rubicundus (Acari: Ixodidae). Experimental and
Applied Acarology, 21 (9): 629–648.

Belozerov, V.N. and Leonovich, S.A. 1995. Pathways of
regeneration of Haller’s sensory organ during the
life cycle of the tick Hyalomma asiaticum. Journal
of Experimental Zoology, 271 (3): 196–204.

Chinzei, Y., Taylor, D. and Ando, K. 1991. Effects of
juvenile hormone and its analogs on vitellogenin
synthesis and ovarian development in the soft tick,
Ornithodoros moubata. Journal of Medical Ento-
mology, 28: 506–513.

Chinzei, Y. and Taylor, D. 1994. Hormonal regulation of
vitellogenin biosynthesis in ticks. Advances in Dis-
ease Vector Research, 10: 1–22.

Conna,t J.L., Ducommon, J. and Diehl, P.A. 1983.
Juvenile hormone-like substances can induce vitel-
logenesis in the tick Ornithodoros moubata. Inter-
national Journal of Invertebrate Reproduction and
Development, 6: 285–294.

Diehl, P.A, Connat, L.L. and Dotson, E. 1986. Chemis-
try, function and metabolism of tick ecdysteroids.
In: J.R. Sauer and J.A. Hair (Eds.). Morphology,
physiology and behavioural biology of ticks. Ellis
Horwood, Chichester, pp. 165–193.

Donahue, W.A., Teel, P.D., Strey, O.F. and Meola, R.W.
1997. Pyriproxyfen effect on newly engorged lar-
vae and nymphs of the lone star tick. Journal of
Medical Entomology, 34: 206–211.

Friesen, K.J. and Kaufman, W.R. 2004. Effects of 20-
hydroecdysone and other hormones on egg devel-
opment, and identification of a vitellin-binding
protein in the ovary of the tick, Amblyomma he-
braeum. Journal of Insect Physiology, 50: 519–

Gilbert, L.I., Granger, N.A. and Roe, R.M. 2000. The
juvenile hormones: historical facts and specula-
tions on future research directions. Insect Biochem-
istry and Molecular Biology, 30 (4): 617–644.

Ioffe, I.D., Uspensky, I.V., Bessmertnaya, I.K. and Kach-
anko, N.I. 1977. [Effect of synthetic juvenile hor-
mone analogues on Ixodoidea]. Zhurnal obshchey
biologii, 38: 885–892. [in Russian]

Ioffe, I.D. and Uspensky, I.V. 1979. [An action of insect
juvenile hormone analogs on nymphs of ixodid
ticks]. Meditsinskaya parasitologia i parasitarnye
bolezni, 48: 39–46. [in Russian]

Khalil, G.M., Sonenshine, D.E., Hanafy, H.A. and Ab-
delmonem, A.E. 1984. Juvenile hormone effects on
the camel tick, Hyalomma dromedarii. Journal of
Medical Entomology, 21: 561–566.

Laufer, H. 1988. Comparisons of terpenoids in verte-
brates and invertebrates. In: F. Sehnal, A. Zabza
and D.I. Denlinger (Eds.). Endocrinological Fron-
tiers in Physiological Insect Ecology. Wroclaw
Technical University, pp. 907–918.

Leahy, M.G. and Booth, K.S. 1980. Precocene: induc-
tion of tick sterility and ecdysis failure. Journal of
Medical Entomology, 17: 18–21.

Leonovich, S.A. and Belozerov, V.N. 1992. Regenera-
tion of Haller’s sensory organ in the tick, Ixodes
ricinus (Acari: Ixodidae). Experimental and Ap-
plied Acarology, 15 (1): 59–79.

Leonovich, S.A. and Belozerov, V.N. 2004. Regenera-
tion of Haller’s sensory organ in two species of hard
ticks of the genus Haemaphysalis (Acari: Ixodi-
dae). Experimental and Applied Acarology, 33 (4):

Li, Y. and Jiang, Z. 1995. Effects of exogenous ecdyster-
oids and juvenile hormone analogue on reproduc-
tion of Haemaphysalis longicornis Neumann. Acta
Parasitol. and Medical Entomol. Sinica, 2: 235–

Liu, J., Jiang, Z., Yin, C.H., Zou, B., Sun, R. and Guan,
X. 1997. Evidence for the existence of juvenile
hormone synthesized by the synganglion of Haem-
aphysalis longicornis (Acari: Ixodidae). Systemat-
ic and Applied Acarology, 2: 51–56.

Liu, J., Zhao, X., Liu, Sh. and Jiang, Z. 1999. Effects of
juvenile hormone III on Haemaphysalis longicornis
(Acari: Ixodidae). Systematic and Applied Acarol-
ogy, 4: 3–7.

Liu, J., Liu, L., Zhang, Y., Wei, Zh. and Liu, J. 2002.
Preliminary studies on the juvenile hormone of
Haemaphysalis longicornis. In: 11th International
Congress of Acarology, Program and Abstracts
Book. Merida, Mexico, p.110.

Lomas, L.O., Black, J.C. and Rees, H.H. 1996. Evi-
dence for the existence of juvenile hormones in
ticks. Transactions of Biochemical Society, 24:

Lomas, L.O. and Rees, H.H. 1998. Endocrine regulation
of development and reproduction in Acarines. In:
G.M. Coast and S.G. Webster (Eds.). Recent Ad-
vances in Arthropod Endocrinology. Academic
Press, New York, pp. 91–124.

Lunke, M.D. and Kaufman, W.R. 1993. Hormonal con-
trol of ovarian development in the tick Amblyomma
hebraeum. Invertebrate Reproduction and Deve-
lopment, 23 (1): 25–38.

McDaniel, R.S. and Oliver, J.H. 1978. Effect of two
juvenile hormone analogs and α-ecdysone on nym-
phal development, spermatogenesis and embryo-
genesis in Dermacentor variabilis. Journal of Pa-
rasitology, 64: 571–573.

Neese, P.A., Kallapur, V.L., Apperson, C.S., Sonen-
shine, D.E. and Roe, R.M. 1998. Do ticks have JH?
A new perspective. In: 10th International Congress
of Acarology, Program and Abstracts Book. Sym-
posium 1A.

Neese, P.A., Sonenshine, D.E., Kallapur, V.L., Apper-
son, C.S. and Roe, R.M. 2000. Absence of insect
juvenile hormones in the American dog tick Der-
macentor variabilis (Say) (Acari: Ixodidae) and in
Ornithodoros parkeri Cooley (Acari: Argasidae).
Journal of Insect Physiology, 46 (4): 477–490.

Neese, P.A., Kallapur, V.L., Apperson, C.S., Sonen-
shine, D.E. and Roe, R.M. 2001. Bioassay, Radi-
obiosynthesis, and GC/MS analysis of juvenile
hormone in ticks: a new perspective. In: R.B.
Halliday at al. (Eds.). Proceedings of the 10th
International Congress of Acarology. CSIRO Pub-
lisher, Melbourne, pp. 612–617.

Nemec, V., Kodrik, D., Matolin, S. and Laufer, H. 1993.
Juvenile hormone-like effects of retinoic acid in
insect metamorphosis, embryogenesis and repro-
duction. Journal of Insect Physiology, 39 (12):

Obenchain, F.D. 1979. Non-acaricidal chemicals for
management of Acari of medical and veterinary
importance. In: J.G. Rodriguez (Ed.). Recent ad-
vances in Acarology, vol. 2. Academic Press, New
York, pp. 35–43.

Obenchain, F.D. and Mango, C.K.A. 1980. Effects of
exogenous ecdysteroids and juvenile hormones on
reproductive development in female Ornithodoros
porcinus porcinus. American Zoologist, 20 (3):
Abstract No 1192.

Palmer, M.J., Harmon, M.A. and Laudet, V. 1999.
Characterization of EcR and RXR homologues in
the ixodid tick, Amblyomma americanum (L.).
American Zoologist, 39: 747–757.

Pound, J.M. and Oliver, J.H. 1979. Juvenile hormone:
evidence of its role in the reproduction of ticks.
Science, 206: 355–357.

Riddiford, L.M. 1996. Juvenile hormone: the status of its
“status quo” action. Archives of Insect Biochemis-
try and Physiology, 32 (3): 271–286.

Roe, R.M., Apperson, C.S. and Sonenshine, D.E. 1992.
Evidence of a juvenoid in ticks. In: Proceedings of
19th International Congress of Entomology, Ab-
stracts. Bejing, p. 669.

Roe, R.M., Kallapur, V., Majumder, C., Lassiter, M.T.,
Apperson, C.S., Sonenshine, D.E. and Windeer,
B.S. 1993. Biochemical evidence for the presence
of a juvenoid in ticks. In: D. Borovsky and A.
Spielman (Eds.). Host-regulated developmental
mechanisms in vector arthropods. IFAS, Vero
Beach, pp. 110–120.

Roe, R.M., Kallapur, V., Linderman, R.J. and Sonen-
shine, D.E. 1999a. Hydrolysis of juvenile hormone
in the American dog tick, Dermacentor variabilis.
In: Acarology IX, vol. 2 (Symposia). Ohio Biol.
Survey, Columbus, pp. 493–496.

Roe, R.M., Neese, P.A.,Kallapur, V., Apperson, C.S.
and Sonenshine, D.E. 1999b. Role of juvenile hor-
mone in the regulation of metamorphosis and re-
production in ticks: a new perspective. In: Seventh
International Conference on the Juvenile Hormones
(Jerusalem, August 29 – September 3, 1999). Ab-
stracts, session 7–7.

Roe, R.M., Kallapur, V., Neese, P.A., Apperson, C.S.
and Sonenshine, D.E. 2001. Juvenile hormone reg-
ulation of metamorphosis and reproduction in ticks:
A critical re-examination of the evidence and a new
perspective. In: R.B. Halliday at al. (Eds.). Pro-
ceedings of 10th International Congress of Acarol-
ogy. CSIRO Publisher, Melbourne, pp. 604–611.

Slusser, J.H. and Sonenshine, D.E. 1996. The absence of
ovicidal effects of fenoxycarb in the deer tick
Ixodes dammini as observed by light, scanning and
transmission electron microscopy. Journal of Med-
ical Entomology, 29 (1): 115–117.

Solomon, K.R. and Evans, A.A. 1978. Activity of juve-
nile hormone mimics in egg-laying ticks. Journal
of Medical Entomology, 14: 433–436.

Solomon, K.R., Mango, C.K.A. and Obenchain, F.D.
1982. Endocrine mechanisms in ticks: effect of
insect hormones and their mimics on development
and reproduction. In: F.D. Obenchain and R. Galun
(Eds.). Physiology of Ticks. Pergamon Press, Ox-
ford, pp. 399–438.

Sonenshine, D.E., Roe, R.M., Venkatesh, K., Apperson,
C.S., Winder, B.S., Schriefer, M.E. and Baehr, J.C.
1989. Biochemical evidence of the occurrence of a
juvenoid in ixodid ticks. In: D. Borovsky and A.
Spielman (Eds.). Host Regulated Developmental
Mechanisms in Vector Arthropods. IFAS, Vero
Beach, pp. 9–17.

Stauffer, A. and Connat, J.L. 1990. Anteroposterior
gradient during nymphal-adult molting cycle of the
tropical bont tick, Amblyomma variegatum. Roux’s
Archiv of Developmental Biology, 198 (2): 309–

Teel, P.D., Donahue, W.A., Strey, O.F. and Meola, R.W.
1996. Effects of pyriproxyfen on engorged females
and newly oviposited eggs of the lone star tick.
Journal of Medical Entomology, 33: 721–725.

Venkatesh, K., Roe, R.M., Apperson, C.S., Sonenshine,
D.E., Schriefer, M.E. and Boland, L.M. 1990. Me-
tabolism of juvenile hormone during adult devel-
opment of Dermacentor variabilis. Journal of Med-
ical Entomology, 27 (1): 36–42.

Wilson, T.G. 2004. The molecular site of action of
juvenile hormone and juvenile hormone insecti-
cides during metamorphosis: how these compounds
kill insects. Journal of Insect Physiology, 50 (2–3):

Wyatt, G.R. 1997. Juvenile hormone in insect reproduc-
tion — a paradox? European Journal of Entomol-
ogy, 94 (3): 323–333.