ПАРАЗИТОЛОГИЯ, 2020, том 54, № 2, с. 126-136.
УДК 576.895
PHEROMONES OF IXODID TICKS IN TICK CONTROL:
FIFTY YEARS OF STUDIES, HOPES, AND FRUSTRATIONS
© 2020 S. A. Leonovich⁕
Zoological Institute RAS,
University emb. 1, St. Petersburg, 199034, Russia
⁕e-mail: leonssa@mail.ru
Received: 30.11.2019
Received after revision: 25.12.2019
Accepted: 25.12.2019
In the present review, the data on studies of pheromones of hard ticks (family Ixodidae) accumu-
lated since the discovery of tick pheromones is briefly analyzed from the point of view of usage of
these semiochemicals in tick control. Some disadvantages of the use of pheromones in tick control can
be explained by peculiarities of their role in tick sexual behavior in the wild and also by complicated
character of their life cycle. Perspective new methods of tick control are also mentioned.
Keywords: ixodid ticks, tick control, pheromones
DOI: 10.31857/S1234567806020030
STUDIES OF PHEROMONES IN METASTRIATE HARD TICKS
(SUBFAMILY AMBLYOMMINAE)
The term pheromone is used for biologically active substances (or a group of substances)
that are secreted by an animal specimen into the environment and affect other specimens of
this species, providing the latter with the information necessary for inevitable changes in their
behavior (definition by Leonovich, 2005). Copulation needs preliminary finding and identifica-
tion of sexual partner; information on the safety of a shelter helps other representatives of the
species to survive, etc. All these activities are regulated by pheromones (Sonenshine, 2005,
2006). Chemical substances that influence behavior between individuals of different species,
e. g., chemical signals that repel predators are designated as allomones, and that attract them
are called kairomones (Sonenshine, 2006).
In the present review, the author does not analyze pheromones revealed in other tick groups
(e.g. Argasidae), pointing attention only to hard ticks (fam. Ixodidae), and mainly to ticks,
important from the medical and veterinary points of view.
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The first evidence on the presence of pheromones in ixodid ticks Dermacentor variabilis
(Say), Amblyomma americanum (Linneaus), and A. maculatum Koch was obtained by Berger
(Berger et al., 1971; Berger, 1972). During feeding of ticks on rabbits, after reaching some
degree of engorgement, males had detached, searched for females, and copulated. When females
were covered with cages penetrable for odors, males gathered near the border line, trying to
penetrate into the cage. Applying of methylenchloryde extract of virgin females fed for 7-8
days, on males, resulted in the reaction of detachment of males and attempts of male-to-male
copulation. The necessary condition of appearance of this reaction included feeding for no
less than 7 days. At the same time, extract of males that had fed for no less than 7 days, did
not result in any reactions of males and females, in spite of the degree of their engorgement.
Hungry specimens of both sexes did not react to female extracts. Species specificity of extract
was absent (Berger et al., 1971).
Similar data were obtained in ticks Dermacentor andersoni Stiles and D. variabilis (So-
nenshine et al., 1974, 1977). The reaction of males included reattachment from the place of
the primary attachment, orientation to the source of the pheromone (feeding female), active
search for this site, and subsequent copulation. Active males, i. e., males that had fed for
7 days, copulated with females killed and covered with lacquer and not attractive before, after
covering with extract of homogenates of engorged females in hexane. Species specificity of
extract was absent.
Later, by methods of chromatography in combination with biological tests, this pheromone
was identified as 2,6-dichlorophenol (С6Н3ОНCl2) (Berger, 1972; Sonenshine et al., 1976;
Leahy, Booth, 1978). At present, the presence of sex pheromones of this type was demonstrated
in about 20 species of hard metastriate ticks, comprising representatives of the genera
Amblyomma, Dermacentor, Hyalomma, Rhipicephalus (for more detail, see Leonovich, 2005).
The author of the present review also paid a lot of attention to tick pheromones, even
discovering the presence of the sex pheromone, 2,6-dichlorophenol, in the Desert tick
Hyalomma asiaticum Schulze, dweller of sand deserts of Central Asia (Leonovich, 1981).
Independent of discovery and identification of sex pheromones in metastriate ticks, quite
different pheromone reactions were revealed (Gladney, 1971; Gladney et al., 1974; Rechav
et al., 1976, 1977; Rechav, Whitehead, 1977; Norval, Rechav, 1979).
It was found that males of some tick species during feeding start producing some volatile
substance attracting hungry specimens of both species and even nymphs (Rechav et al., 1976).
The reaction included orientation toward the source of the pheromone and the subsequent
attachment of percipients near this source. Hungry males were not attractive at all (Rechav,
Whitehead, 1977). Engorged specimens of both sexes were not attractive to fed males (source
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of the pheromone) (Berger et al., 1971). By the analogy with earlier described type of reaction
in insects, this class of pheromones was designated as “aggregation-attachment pheromones”
(Sonenshine et al., 2003; Sonenshine, 2006).
The attraction-aggregation-attachment pheromone is actually a mixture of three or more
specific compounds that mediate different behaviors leading to the formation of species-specific
feeding clusters on a host. As mentioned, the attraction-aggregation-attachment pheromone
is produced exclusively by males, but is attractive to both unfed males and females of the
same species. It is secreted by unusually large glands, the Type 2 dermal glands located on
the ventral surfaces of the feeding males. Two components, namely, o-nitrophenol and methyl
salicylate were identified by high-pressure liquid chromatography (HPLC) in extracts of these
glands dissected from fed male ticks (Diehl et al., 1991). In the tick Amblyomma variegatum
Fabricius, aggregation-attachment pheromone was represented by a mixture of two substituted
phenols, methyl salicylate and o-nitrophenol and nonanoic acid (Shoni et al., 1984; Pheromone
biochemistry, 2014).
In the present case, the pheromone provides feeding of parasite females only on the host
where ready for insemination males are already present.
Thus, within metastriate ticks (Abmlyomminae) two types of volatile distant pheromones
were revealed: non species-specific sex pheromone and species-specific (at least in known
cases) attraction-aggregation-attachment pheromone. These pheromones also differ in their
chemical structure (Sonenshine, 2004).
The analysis of the available data demonstrates the existence of two types of the involve-
ment of pheromones in metastriate tick sexual behavior, based on the existence of two types
of pheromones (Leonovich, 1981, 1981a). In the first case, hungry males and females are
able to feed independently on a host, and selection of attachment place depends only on reac-
tions on different stimuli of the host itself. Females, after attachment to the host, stay in the
attachment site till the end of engorgement. Copulation strongly depends on the degree of
engorgement, because spermatogenesis and ovogenesis in metastriate hard ticks finishes only
after engorgement i.e., copulation is possible only in really “mature” males and females (for
more details, see Leonovich, 2005). It is evident that some factors signaling on the readiness
(or potential readiness) of a female for copulation in conditions where successful fertilization
and egg development must exist. This signal is mostly successfully performed by a chemical
volatile substance produced in special glands after completion of ovogenesis (in other words,
the sex pheromone). Being percept by males, this factor results in detachment of males that
move towards the source of the pheromone and reattach near this source (in reality, near the
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half-engorged female). The probability of successful copulation is provided by delayed devel-
opment of non-fertilized females and their long stay in this state (Balashov, 1967). Production
of the pheromone in this case is not blocked, providing finding of such half-engorged females
by males ready for copulation
The second type of pheromone-dependent behavior is typical of ixodid species where
attraction-aggregation-attachment (AAA) pheromones were revealed (Rechav et al., 1976,
1977; Rechav, 1978; Rechav, Whitehead, 1977; Gladney et al., 1974, etc.). These pheromones,
as mentioned above, are produced only by males during feeding on host blood.
In the latter case, females are unable to feed on hosts in the absence of feeding males (Re-
chav, 1978b). Thus, the AAA pheromone, produced by males and species-specific serves as
such a signal. Later, pheromone reactions are realized in the way described above for the first
type of pheromone involvement in tick behavior. Some advantage of the latter case is explained
by the fact that fertilization is guaranteed for virtually all the females. In this case, the sex
pheromone serves only as a signal informing male on the readiness of a female for copulation.
Genital pheromones provide mounting of males, and thus are designated as mounting
pheromones (Hamilton et al., 1989; Sonenshine, 2005). These pheromones are cholesteryl
ethers, in particular, cholesteryl oleate (Sonenshine et al., 1992; Sonenshine, 2005; Phero-
mone biochemistry. 2014). These pheromones are contact ones, but they were also used in
tick control (see below).
Quite another type of pheromones was also found in ixodid ticks. These pheromones are
named arrestment (or assembly) pheromones. Arrestment pheromones decrease locomotor
activity. When ticks come in contact with other conspecific individuals, or waste material
deposited by such individuals, they cease activity and remain quiescent. Often, clusters of
arrested individuals occur in vegetation or, in the case of nidicolous species, in the duff on the
floor of caves or burrows (Sonenshine, 2006).
STUDIES OF PHEROMONES IN PROSTRIATE HARD TICKS
(SUBFAMILY IXODINAE)
An assumption on the existence of pheromones in ticks of the subfamily Ixodinae, rep-
resented in the world fauna by a single genus Ixodes, was based on the existence of hungry
fertilized females (for more details, see Leonovich, 2005). Many publications where phero-
mones of tick of the genus Ixodes are mentioned are based on works by Graf (1975, 1978),
who proposed the existence of sex pheromones in the tick Ixodes ricinus. The detailed ac-
quaintance with these works, however, results in many doubts on the reliability of these data,
because no any quantitative data of his experiments are given. Later, his data were disproved
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by several authors (e.g., behavior experiments on Ixodes holocyclus Neumann (Treverrow
et al., 1977), and also on I. ricinus L. and I. persulcatus P. Sch. (Uspensky, Emeljanova,
1980). According to the cited authors, ticks of the genus Ixodes produce a pheromone, but
not the sex pheromone, but the aggregation pheromone. The author of the present review did
not find any evidence on the existence of volatile (distant) sex pheromones or other phero-
mones (aggregation pheromones), providing formation of aggregations in ticks I. ricinus and
I. persulcatus from natural populations. A propos, Uspensky and Emeljanova (1980) rightfully
mention that the assembly pheromone found in the examined species is most likely a relic,
that had survived in the evolution of Ixodinae, and play no significant role at present. In my
opinion, their data (mean number of ticks forming aggregations in a small Petri dish (10 cm
in diameter) constituting 2-3 tick out of 10 (!), being statistically significant, are doubtful in
relation to existence of the pheromone.
According to the private opinion of the author (together with his experience in field and
laboratory experiments with the dog tick and the Taiga tick), no assembly pheromones are
present in the mentioned species of the genus Ixodes (I. ricinus and I. persulcatus), and find-
ing of hungry fertilized females in the wild can be quite correctly explained without applying
the pheromone hypothesis (for more details, see Leonovich, 2005). Besides, contradictory
opinions also exist in available literature (Romanenko, 1991).
It should be mentioned that the sex pheromone of metastriate ticks (namely, 2,6-dichloro-
phenol) affects some receptor cells in the Haller’s organ of Ixodes ricinus (Leonovich, 2014).
In electrophysiological experiments with intracellular recording of action potentials, a specific
sensory cell in the distal knoll olfactory sensillum of the Haller’s organ responded to very
low concentrations of 2,6-dichlorophenol (Leonovich, 2004). This sensillum also responded
to phenol compounds (ortho-chlorophenol, ortho-methylphenol (also named ortho-cresol).
In spite of electrophysiological response, adults of both sexes, nymphs, and larvae of Ixodes
ricinus were not attracted to 2,6-dichlorophnol. They also were not repelled by the odor of
this chemical substance; in other words, their behavioral reaction to 2,6-dichlorophenol was
neutral (Leonovich, 2005).
Attraction of ticks of the mentioned species to components of ticks excreta (such as gua-
nine) were observed (e.g. Benoit et al., 2008), but are they really pheromones (substances
specially produced in special glands for providing another specimen of the same species with
information changing the behavior?) In my opinion, not every attractant is the pheromone.
We do not analyze other types of pheromones, best of all described in a review by Sonen-
shine (2006), because they were not used in attempts of tick control with the use of pheromones.
130
The use of pheromones in tick control
The first thing that is rather evident is the use of pheromone-acaricide mixtures in order
to kill ticks attracted by a pheromone. Attempts to apply this method in practice are used in
some countries even nowadays (Bhoopathy, Ravi, 2017). But what kind of pheromones (and,
hence, what tick species can be affected by this method?)
Arrestment pheromones seem to be most useful for tick control. In some cases, combin-
ing the components of the arrestment pheromone with an acaricide (i.e., toxicants used to kill
ticks) in a slow-release delivery system, a substantial increase in tick control was achieved
(Sonenshine et al., 2003).
Some US patents on the use of arrestment pheromones in combination with acaricides
exist, e.g., patent US5296227A (Allan et al., 2001): A patent for controlling of the bont tick
Amblyomma hebraeum Koch with the use of pheromones, which includes a pheromone
composition having 1% by weight each of said decoy of O-nitrophenol and methyl salicy-
late; 0.2% by weight in volume of said decoy of 2,6-dichlorophenol; and 0.1% by weight of
phenylacetaldehyde; an acaricide selected from the group consisting of organophosphorous
compounds and pyrethroid compounds; and a matrix material selected from the group consist-
ing of polyvinylchloride, nylons and waxes, said matrix material being impregnated with said
pheromone composition (Alan et al., 2001).
In vitro experiments also demonstrated effectiveness of the use of pheromone-acaricide
mixtures, e. g. against larvae of Rhipicephalus sanguineus (Latreille), R. (Boophilus) microplus
(Canestrini), R. haemaphysaloides Supino, Hyalomma marginatum Koch and Haemaphysalis
bispinosa Neumann, and adults of R. sanguineus and R. microplus (Ranju et al., 2018). The
problem with such experimental works is the transition of laboratory methods into natural
conditions (see below) - the basic circumstance hampering the use of these method in practice.
Mounting sex pheromones mixed with acaricides were also used in tick control, at least,
a patent on this method also exists (Sonenshine et al., 1992).
Methods of strengthening the effectiveness of commonly used tail or ear tags impregnated
with acaricides by admixture of pheromones, turning them into decoys, were used for the
control of the bont tick, Amblyomma hebraeum (Acari: Ixodidae), on cattle in Zimbabwe
(Norval et al., 1991, 1996).
In spite of the mentioned attempts to use pheromones for tick control in nature, the method
in general did not succeed. The most difficult problem of all remains: the translation of labo-
ratory research into the extremely diverse parasite control requirements of farming systems
in a way that is practically useful (Willadsen, 2006). The methods can be widely used only
if it is not expensive.
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But more important thing is that actually the use of pheromones very poorly affects the life
cycle of the tick in nature. Adults ticks can be killed with acaricides mixed with pheromones
in higher degree than killed by acaricides only. But, nevertheless, if only some females will
survive (and it is inevitable), they will produce such number of eggs that will restore tick
population. Larvae and nymphs, in the majority of cases (except for one-host ticks), feed on
small mammals; the latter cannot be eliminated in natural biotopes. Hence, pathogens will
exist in natural foci, surviving in host-parasite systems, involving larvae - small mammals -
nymphs - medium-size mammals - adults - large mammals.
Attachment of ticks precedes production of pheromones - hence, the tick will be killed,
but after infecting of a host with pathogens.
The same story is true when we concern the use of acaricides themselves (without admixture
of pheromones). This method is still widely used in tick control practice (Jensenius et al., 2005).
Satisfactory tick control is often difficult due to unrealistic expectations and because of constant
re-infestation pressure. Some of the most important factors are changes in tick distributions,
our inability to control wildlife tick hosts and differences in tick control approaches. These
factors probably cause most real and perceived product failures (Dryden, 2009).
The use of acaricides, nevertheless, being mixed with pheromones or not, also have very
important disadvantages. The main of the latter includes growing resistance of ticks against
acaricides. For example, an increase of multi-acaricide resistant Rhipicephalus ticks in Uganda
was observed (Vudrico et al., 2016).
The use of repellents seems more reliable: in this case we do not kill ticks but prevent tick
bites, which is very important for protecting humans, preventing transmission of pathogens
from ticks to humans. The use of tick repellents in cattle seems to be rather expensive and,
thus, useless (Ginsberg, 2014). But it can be expedient for pets.
Finding natural repellents of the plant origin seems useful because they do not pollute the
wild. Some data on plants that are (and can be) used as tick repellents can be found in a review
by Benelli et al. (2016). Repellent effect against tick vectors of public health importance (Ixodes
ricinus, Ixodes persulcatus, Amblyomma cajennense (Fabricius), Haemaphysalis bispinosa,
Haemaphysalis longicornis Neumann, Hyalomma anatolicum Koch, Hyalomma marginatum
rufipes Koch, Rhipicephalus appendiculatus Neumann, Rhipicephalus (Boophilus) microplus,
Rhipicephalus pulchellus Gerstaker, Rhipicephalus sanguineus and Rhipicephalus turanicus
Pomerantzev). The most frequent botanical families exploited as sources of acaricides and
repellents against ticks were Asteraceae (15 % of the selected studies), Fabaceae (9 %), La-
miaceae (10 %), Meliaceae (5 %), Solanaceae (6 %) and Verbenaceae (5 %).
Genetic control methods become more and more popular, trying to decrease environmental
pollution and selection of drug resistant ticks. E.g., preventing (silencing) the expression of
132
a single RNA gene (subolesin) with the use of RNA interference resulted in appearance of ticks
with diminished reproductive performance that prevented successful mating and production
of viable offspring of Rhipicephalus (Boophilus) microplus (Fuente de la et al., 2006; Merino
et al., 2011). But now, these methods develop only in laboratory and are pointed mainly to
the detailed analysis of tick genetics associated with reproduction (Nijhof et al., 2006). In the
future, however, genetic studies seem rather perspective.
In order to decrease losses in cattle population caused by ticks and cattle diseases transmit-
ted by the latter, some authors point to the necessity of affecting the cattle rather than ticks
(Shyma et al., 2013). The authors point to the fact that chemical control of diseases has been
found to be ineffective and also involving large cost. To reduce our reliance on these chemi-
cal products, it is necessary to embark on programs that include habitat management, genetic
selection of hosts, and development of a strain capable of inducing host resistance to ticks.
Selection for disease resistance provides alternate method for sustainable control of tick-borne
diseases. Domestic livestock manifests tick-resistance by skin thickness, coat type, coat color,
hair density, skin secretions, etc (Shyma et al., 2013).
AKNOWLEDGEMENTS
The author is grateful to Mrs. J. Trott (Warminster, UK) for checking of English. The
work was performed within the frames of the project “Elaboration of the modern basis
for the taxonomy and phylogeny of parasitic and bloodsucking arthropods” (State Reg.
No. АААА-А19-119020790133-6).
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ФЕРОМОНЫ ИКСОДОВЫХ КЛЕЩЕЙ И ИХ ИСПОЛЬЗОВАНИЕ
В БОРЬБЕ С КЛЕЩАМИ: ПЯТЬДЕСЯТ ЛЕТ ИССЛЕДОВАНИЙ,
НАДЕЖД И РАЗОЧАРОВАНИЙ
С. А. Леонович⁕
Зоологический институт РАН,
Санкт-Петербург, Университетская наб., 1, 199034, Россия
⁕e-mail: leonssa@mail.ru
Ключевые слова: иксодовые клещи, борьба с клещами, феромоны
РЕЗЮМЕ
В обзоре кратко проанализированы данные по феромонам иксодовых клещей (cемейство
Ixodidae) накопленные за пятьдесят лет их исследований, начиная с работы первооткрывателей,
с точки зрения возможностей и результатов использования феромонов в практике борьбы с опас-
ными видами клещей. Принципиальные ограничения использования феромонов для сокращения
численности опасных видов клещей объясняются особенностями феромонных реакций клещей
в реальной природе, а также сложным жизненным циклом клещей. Кратко анализируются новые
перспективные методы ограничения вреда, наносимого клещами.
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