Meeting Report
Towards an Effective, Rational and Sustainable
Approach for the Control of Cattle Ticks in
the Neotropics
Agustín Estrada-Peña 1,2, *, Matías Szabó 3 , Marcelo Labruna 4 , Juan Mosqueda 5 ,
Octavio Merino 6 , Evelina Tarragona 7 , José M. Venzal 8 and José de la Fuente 9,10
1
2
3
4
5
6
7
8
9
10
*
Department of Animal Pathology, Faculty of Veterinary Medicine, 50013 Zaragoza, Spain
Research Group in Emerging Zoonoses, IA2, 50013 Zaragoza, Spain
Federal University of Überlandia, Überlandia 38408-100, Brazil; szabo@famev.ufu.br
University of Sao Paulo, Sao Paulo 05508-220, Brazil; labruna@usp.br
Faculty of Veterinary Medicine, Autonomus University of Querétaro, Santiago de Querétaro 76010, Mexico;
joel.mosqueda@uaq.mx
Faculty of Veterinary Medicine, University of Tamaulipas, Tamaulipas 87000, Mexico;
mero840125@hotmail.com
INTA Rafaela, Santa Fe RN34 227, Argentina; tarragona.evelina@inta.gob.ar
Faculty of Veterinary Medicine, University of the Republic, Salto 11200, Uruguay; dpvuru@hotmail.com
SaBio, Instituto de Investigación en Recursos Cinegéticos (IREC-CSIC-UCLM-JCCM), Ronda de Toledo s/n,
13005 Ciudad Real, Spain; jose_delafuente@yahoo.com
Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University,
Stillwater, OK 74078, USA
Correspondence: aestrada@unizar.es
Received: 1 December 2019; Accepted: 24 December 2019; Published: 30 December 2019
Abstract: Ticks and transmitted pathogens constitute a major burden for cattle industry in the
Neotropics. To address this limitation, the Spanish Ibero-American Program of Science and Technology
in Development office (CYTED) supported from 2018 a network of scientists named “LaGar” (CYTED
code 118RT0542) aimed at optimizing the control strategies of cattle ticks in the neotropical region.
As part of network activities, a meeting and course were organized on 4–8 November 2019 in Querétaro,
Mexico to address the objective of developing the infrastructure necessary for an effective, sustainable
(i.e., combination of efficacious acaricides with anti-tick vaccines) and rational (i.e., considering tick
ecology, seasonal dynamics and cattle-wildlife interactions) control of cattle tick infestations and
transmitted pathogens. The course was focused on scientists, students, cattle holders and producers
and pharmaceutical/industry representatives. In this way the course addressed the different views
presented by participants with the conclusion of producing a research-driven combination of different
interventions for the control of tick tick-borne diseases.
Keywords: tick; vaccine; ecology; neotropics; cattle; wildlife; pathogen
1. Introduction: The Need to Optimize Control Strategies of Ticks and Tick-Borne Pathogens
Affecting Cattle in the Neotropics
Ticks and tick-borne pathogens, like protozoans of the genus Babesia, and bacteria of the genus
Anaplasma are among the most important pests of cattle in Central and South America, as well as
in many other parts of the world. Most of the estimated world’s population of 1.2 billion cattle are
at risk of exposure to tick and tick-transmitted pathogens, producing significant losses derived of
decreased meat and milk production, or fatalities [1,2]. The bovine babesiosis (also known as cattle
Vaccines 2020, 8, 9; doi:10.3390/vaccines8010009
www.mdpi.com/journal/vaccines
Vaccines 2020, 8, 9
2 of 9
fever and transmitted by ticks of the subgenus Boophilus) is still seriously affecting cattle production
in wide regions of the world. The disease is produced by several species of protozoans, of which
most important are Babesia bovis and B. bigemina, which are transmitted by Rhipicephalus (Boophilus)
microplus and R. annulatus among cattle and other wild ungulates. The disease is difficult to detect in
chronically infected animals that serve as reservoirs: ticks ingest the parasite with blood meals and
efficiently transmit to naïve cattle [3]. Rhipicephalus ticks and the pathogens they transmit present
significant threats to cattle populations worldwide. While R. annulatus is restricted to some parts
of Mexico and USA, R. microplus is a successful species that extend from the USA-Mexico border to
northern Argentina. To these two species, it is necessary to add the species in the group Amblyomma
cajennense, which have in most cases a great interest in human health, but that also have an impact on
animal production.
Control measures for tick-borne pathogens have commonly focused on the tick vectors, ignoring
the large interactions of the ticks and the environment. The holistic view of tick-host-environment is
capital to continued efficacy of control measures [4–7]. Pioneering studies addressed the investigation
of tick population dynamics, interactions with livestock and wild hosts, and tick’s seasonal activity
that is driven by climate factors [6–14]. The development of models explaining all these traits
helped to understand both the spatial dynamics and the climate suitability of pathogen-transmitting
ticks, [11,12,15]. However, the control of tick-transmitted pathogens still needs a detailed regional-scale
spatial modelling framework identifying environmental conditions and landscape patterns driving to
the establishment and spread of permanent cycles of transmission.
The control of cattle ticks infestations in the neotropics is still dependent on the generalized use
of classic acaricides without strategies considered as tick ecology, the possible endemic stability of
tick-borne pathogens, its economic impact, or the importance of other vertebrates in the spread of
these pathogens. This is causing the emergence of multiacaricide-resistant ticks with a large impact on
cattle production [7–10]. The resistance of ticks to acaricides is widespread. The Food and Agriculture
Organization of the United Nations (FAO), recently proposed an agenda to activate a coordinated
program of tick control in Central and South America. The FAO working group on tick resistance
to ixodicides, together with the coordinated inputs by major pharmaceutical companies proposed
measures to address that effort, including: (i) the correct application of the acaricides, including
considerations of efficacy and efficiency; (ii) the development of nationwide community and farmer
sensitization programs on ticks; (iii) the continuous monitoring of tick populations, the inter-year
changes of pathogens prevalence, and the emergence of resistance to acaricides; (iv) the monitoring of
wildlife-tick-livestock interactions; and (v) the development of new anti-tick vaccines.
In this context, the Spanish CYTED office approved in 2018 and continues supporting a network
of scientists named “LaGar” (CYTED code 118RT0542) aimed to optimize the control strategies of ticks
in the neotropical region. The objectives of the network are to elaborate on a solid framework aimed to
optimize the methods for ticks control, pivoting over three basic strategies, namely (i) the ecology of
the ticks; (ii) the interface of the tick-cattle-wild animals interface and the ecological studies aimed to
disentangle this complex system; and (iii) the optimization of the use of classic acaricides and novel
vaccine interventions.
2. The Course: Building Scientific Capacity in Mexico
As part of the activities of the network, a course was organized in 4–8 November 2019 to address
the objective of developing the infrastructure necessary to understand how the climate may alter
the finely tuned patterns of tick activity, the changing patterns of infections by tick-borne pathogens,
the importance of the wildlife as super-spreaders of ticks vectors and pathogens, and the role of
vaccines in the control of ticks.
The course was intended to disseminate the scientific knowledge in Mexico at both theoretical and
laboratory and field practical levels and to implement a multidisciplinary approach for the control of
cattle tick infestations and tick-borne infectious diseases affecting humans and animals in Central and
Vaccines 2020, 8, 9
3 of 9
Vaccines 2019, 7, x FOR PEER REVIEW
3 of 9
South America (Figure 1). A special emphasis was given to the importance of wildlife in the support of
the
supportpopulations
of permanent
ticks affecting
cattle,
the ecology
of factors
ticks, and
other human
factors
permanent
of populations
ticks affectingofcattle,
the ecology
of ticks,
and other
affecting
affecting
human
and
animal
health
and
livestock
production
and
trade.
and animal health and livestock production and trade.
Figure
Figure 1.
1. Some
Someevents
eventsin
inthe
themeeting
meetingof
ofthe
thenetwork
network “LaGar”
“LaGar” in
in Querétaro,
Querétaro, México.
México. (A)
(A) The
The members
members
of
of the
the network
network who attended the meeting. From
From left
left to
to right,
right, top
top row,
row, Juan Mosqueda, Octavio
Octavio
Merino,
Merino, and
and Matias
Matias Szabó;
Szabó; mid
mid row,
row, Marcelo
Marcelo Labruna
Labruna and
and Evelina
Evelina Tarragona;
Tarragona; bottom
bottom row,
row, Agustín
Agustín
Estrada-Peña,
Estrada-Peña, José
José M.
M. Venzal,
Venzal, and José de la Fuente. (B)
(B) The
The main
main session
session of
of lectures
lectures on
on tick
tick ecology
ecology
and control.
control. (C,D)
(C,D) Two
Two aspects
aspects of
of the
the seminar
seminar and
and working
working sessions
sessions on
on “update
“update of
of identification
identification of
of
and
ticks in
in the
the Neotropics”
Neotropics” lead by J. M. Venzal and E. Tarragona.
ticks
Tarragona.
The program
programincluded
included(i)(i)anan
introduction
to the
ecology
of ticks
the neotropics
in the
The
introduction
to the
ecology
of ticks
in theinneotropics
in the cattlecattle-wildlife
interface
by M. Labruna
M. (ii)
Szabó;
(ii) an overview
of the distribution
and
wildlife
interface
by M. Labruna
and M. and
Szabó;
an overview
of the distribution
and seasonal
seasonal
dynamics
of
the
tick
subgenus
Boophilus,
by
A.
Estrada-Peña;
(iii)
the
current
concepts
of
dynamics of the tick subgenus Boophilus, by A. Estrada-Peña; (iii) the current concepts of vaccinomics
vaccinomics
by
J.
de
la
Fuente;
(iv)
a
view
to
the
world
of
ticks
by
J.M.
Venzal,
which
was
completed
by
by J. de la Fuente; (iv) a view to the world of ticks by J.M. Venzal, which was completed by a one-day
a one-day
course capacitation
on morphological
determination
of importance
ticks of importance
in the Neotropics,
course
capacitation
on morphological
determination
of ticks of
in the Neotropics,
by E.
by
E.
Tarragona
and
J.M.
Venzal.
The
course
was
developed
in
the
Faculty
of
Veterinary
Medicine
in
Tarragona and J.M. Venzal. The course was developed in the Faculty of Veterinary Medicine
in the
the
University
of
Querétaro
(México)
with
the
joint
participation
of
the
National
Council
of
Science
of
University of Querétaro (México) with the joint participation of the National Council of Science of
Mexico (CONACYT),
thethe
World
Organisation
for
Mexico
(CONACYT), The
TheMexican
MexicanService
ServiceofofAnimal
AnimalHealth
Health(SENASICA),
(SENASICA),
World
Organisation
Animal
Health
(OIE)
and
the
Council
of
Science
and
Technology
of
Querétaro,
México
(CONCYTEQ).
for Animal Health (OIE) and the Council of Science and Technology of Querétaro, México
(CONCYTEQ).
3. The Ecology of Ticks as a Framework for Successful and Sustainable Tick Control
3. The
Ecology
of Ticks
as a and
Framework
forare
Successful
and Sustainable
TickisControl
The
protozoans
B. bovis
B. bigemina
the etiological
agents of what
considered “the most
economically significant diseases of cattle in tropical and subtropical areas” [15]. All species of the
The protozoans B. bovis and B. bigemina are the etiological agents of what is considered “the most
genus Babesia are transmitted by ticks that feed on a limited range of hosts. The main vectors of these
economically significant diseases of cattle in tropical and subtropical areas” [15]. All species of the
pathogens are one-host ticks of the genus Rhipicephalus spp. ticks, which are widespread in tropical and
genus Babesia are transmitted by ticks that feed on a limited range of hosts. The main vectors of these
subtropical countries [1,16]. The exploit of the highly efficient one-host cycle by the ticks allows the
pathogens are one-host ticks of the genus Rhipicephalus spp. ticks, which are widespread in tropical
quick spread of foci of diseases. These two tick species, once primarily parasites of wild ungulates are
and subtropical countries [1,16]. The exploit of the highly efficient one-host cycle by the ticks allows
the only vectors involved in the biological transmission of babesiosis. The most common incubation
the quick spread of foci of diseases. These two tick species, once primarily parasites of wild ungulates
period is about 2–3 weeks after tick infestation. The experimental inoculation of Babesia commonly
are the only vectors involved in the biological transmission of babesiosis. The most common
produces shorter incubation periods [17]. The clinical manifestations of babesiosis are typical of a
incubation period is about 2–3 weeks after tick infestation. The experimental inoculation of Babesia
commonly produces shorter incubation periods [17]. The clinical manifestations of babesiosis are
typical of a haemolytic anemia but vary according to agent and host factors, like age and immune
Vaccines 2020, 8, 9
4 of 9
haemolytic anemia but vary according to agent and host factors, like age and immune status [17].
After a prepatent period following the onset of feeding by Babesia-infected tick larvae, peak parasitemia
and the manifestation of clinical signs occur. Babesia bigemina matures approximately 9 days after larval
attachment, and it is only transmitted by nymphs and adults of the tick [16,18–22].
Anaplasma marginale is the most prevalent tick-borne pathogen of cattle worldwide, with endemic
regions in North, Central, and South America, as well as Africa, Asia and Australia [23]. Ixodid ticks
are the biological vectors of A. marginale, while mechanical transmission can occur through fly bites
and reuse of needles [5]. The one-host tick R. microplus is estimated to be the main vector of A. marginale
in Brazil [24,25]. Once an animal is exposed to this pathogen, acute infection develops, which is
characterized by fever, high levels of bacteremia, anemia, weakness, reduced growth and milk
production, miscarriage, and in some cases death [26].
It is well known that any successful tick control framework must to be built over a solid knowledge
of the biology of the targeted tick species. This includes not only a reliable knowledge of its distribution,
but also the factors behind the realized range of the species, which are dependent on abiotic traits
(i.e., temperature and relative humidity) and biotic ones (i.e., hosts). The finely tuned combination of
these traits determines the probability a tick can survive in the environment. Human actions on the
environment, like populating large areas with livestock, increment the suitability of a habitat for ticks
because the high density of hosts.
The increase in development and application of modelling exercises for understanding tick
population dynamics had led to the capture of the actions of climate on the basic traits of the
performance of tick’s life cycle [12–14]. It is widely accepted that vertebrates move through a matrix of
suitable habitat, being these movements governed by simple rules depending on the behaviour of the
vertebrate species and the habitat/non-habitat geographical patterns [27–29]. Studies exist about the
importance of the landscape composition on the movement of animals through “corridors” that connect
patches of suitable habitat, therefore impacting the abundance of ticks [12]. These movements affect the
availability of hosts for ticks at specific points of the habitat [30], thus impacting also tick abundance.
The simulation of animal movements, and their preferences towards some types of vegetation, together
with the response of ticks to climate has surfaced as a suitable way to capture basic parameters of the
phenology and abundance of ticks [19,31].
Further on the spatial scale of tick distribution, there is also a temporal pattern, which draws
what is known as “seasonality” or the moments of the year in which ticks are active and questing for
hosts. The root of the tick control using classic ixodicides is to know the onset of such period of activity,
to match the application of the chemical with the activity of the tick. In some cases, like the ticks of the
complex A. cajennense, this is further complicated because the immature stages are commonly parasites
of small mammals, adults feeding on livestock. The feeding on rodents introduces a potential “noise”
because the natural variability of the populations of rodents, and how the different stages of ticks
feed on them. To date, efforts to model the seasonality of ticks have been reduced to one host species,
like R. microplus and R. annulatus, the former being most important tick in the region. Efforts have been
made using process-driven models [7,14] but a new approach that use direct recordings by satellite
imagery is being introduced. The technique is based on the annual variation of both the ground surface
temperature and the vegetal vigour to capture the pattern of larval seasonality. Preliminary results
support the hypothesis that this method, supported by previous empirical data on tick activation by
prevailing weather conditions, will provide an adequate information for predictive mapping of larval
R. microplus activity.
4. The Wild Animals and the Cattle-Tick Interface
Basic to host tick parasitism at the cattle-wildlife interface is the knowledge that much of the
existing tick-host association patterns are driven by biogeography and ecological specificity of the
parasite [32]. This pattern was reaffirmed for neotropical ticks [33,34] who observed on a meta-analysis
Vaccines 2020, 8, 9
5 of 9
that strict host specificity is not common among Neotropical hard ticks and that tick distribution is
rather driven by tick ecology and evolution of habitat specificity.
It is important to highlight that cattle raising is necessarily related to a radical environmental
alteration: the replacement of native vegetation by pastures. This non-indigenous and artificial
environment coupled with high animal density supports high infestations levels of another exotic
being, Rhipicephalus microplus, a tick species introduced from tropical and subtropical Asia [35] and
that became the main cattle tick in the region. Wildlife hosts that regularly or occasionally use pastures
may be exposed to exotic R. microplus and associated pathogens such as Babesia and Anaplasma but
also other less known as the Mogiana tick virus [36]. Indeed, fully engorged R. microplus female
ticks are frequently found on hosts such as Puma concolor (cougar), Cerdocyon thous (crab-eating fox),
Odocoileus virginianus (White-tailed deer), Blastocerus dichotomus (marsh deer) Ozotoceros bezoarticus
(Pampas deer), Myrmecophaga tridactyla (giant anteater) and others [37–41]. The proximity to native
fauna and its environment, exposes bovines to indigenous ticks and several were already registered
on this host. Albeit in different geographical and ecological settings throughout the Neotropics,
species such as Amblyomma mixtum, Amblyomma neumanni, Amblyomma parvum, Amblyomma sculptum,
Amblyomma tonelliae, Amblyomma triste, Ixodes aragaoi and Ixodes pararicinus are frequent parasites of cattle.
Other species are found on bovines more rarely as is the case of Amblyomma aureolatum, Amblyomma
dissimile, Amblyomma dubitatum, Amblyomma hadanii, Amblyomma pseudoconcolor, Amblyomma tigrinum,
Dermacentor nitens, Ixodes longiscutatus, Haemaphysalis juxtakochi [42–45]. It would be of great importance
to distinguish among occasional cattle infestations with indigenous ticks from those more frequent and
relevant for bovines. For example, it was already noted that, within their geographical distribution,
species such as A. neumanii and A. mixtum can maintain their life cycle on bovines [42,46]. Other tick
species, however, rely on wild hosts to maintain their life cycle and parasitize bovines fortuitously.
Exposure of cattle to wildlife ticks could be better understood if infestations of natural environment
and indigenous hosts were also known. It is necessary to consider that environmental changing is an
ongoing but uneven process throughout the Neotropics and tick ecology at the cattle-wildlife interface
will necessarily acquire new features.
5. Anti-Tick Vaccines: An Efficacious and Sustainable Intervention for the Control of Cattle
Tick Infestations
Anti-tick vaccines point to a completely different strategy to control tick infestations and pathogen
transmission. It is based on the vaccination of cattle using different antigens with different roles in
the physiology of ticks. The vaccines do not kill the ticks in the same way the acaricides do, and it
is necessary to instruct the producer about how to observe a basic set of rules in the protection of
cattle against ticks and the correct use of the different available methods for this control. Anti-tick
vaccines became available in the early 1990s for the control of R. microplus cattle tick infestations in a
cost-effective manner to reduce the use of acaricides and the selection of acaricide-resistant ticks and
contamination of the environment and animal products with pesticide residues [47–50]. Vaccines using
tick BM86 and SUB antigens were also used in pen trials to reduce R. microplus tick infestations in
wildlife hosts [51]. Field trials have not been conducted with wildlife in the Neotropics, but the efficacy
of the vaccine was demonstrated in red deer under field conditions in Spain [51].
Despite recent advances in the identification and characterization of tick protective antigens [52–54],
the major challenges faced to further advance the implementation of effective vaccination strategies
for the control of cattle tick infestations and tick-borne diseases include: (a) rational and
effective combination of anti-tick vaccines with acaricides and other traditional control measures;
(b) development and implementation of cost-effective and safe vaccines reducing infestations by
multiple tick species in different hosts; (c) vaccine formulations to reduce tick infestations and pathogen
infection and/or transmission; and (d) funding and fulfilling regulatory requirements for vaccine
registration. To address these challenges we propose (a) to use information on tick life cycle and
the effect of biotic and abiotic factors for the effective combination of multiple control measures
Vaccines 2020, 8, 9
6 of 9
including vaccines for the control of tick infestations and pathogen infection and transmission [55];
(b) modeling the vaccination strategies against ticks and transmitted pathogens to guide the selection
of appropriate antigen combinations, target hosts and vaccination time schedule [53]; (c) to use latest
omics technologies in a vaccinomics approach combined with systems biology and big data machine
learning algorithms to identify new protective antigens and advance quantum immunology [56,57];
(d) to combine tick-derived and pathogen derived antigens in effective vaccine delivery formulations
to target multiple tick species in domestic and both domestic and wild hosts [55–58]; (e) to develop
country and host/tick species driven strategies to increase the efficacy of vaccination and other control
strategies for cattle ticks and transmitted pathogens [59]. Finally, it is important to advance research
on areas such as sequencing and assembly of tick genomes, vector competence, functionality of tick
microbiota, functional analysis of tick-host-pathogen interactions, and pathogen control of tick/host
epigenetics to develop vaccines and methods to manipulate tick genetics and microbiota for new
effective interventions to control tick infestations and transmitted pathogens affecting both human and
animal health [60,61].
6. Conclusions and Future Actions
The multi-disciplinary approaches for tick control addressed in the meeting identified several
points for action, envisaged to be developed in the near future. These points were identified as in need
of urgent development and include: (i) an adequate understanding of the effects of regional climate
patterns on the parasitic load by ticks; (ii) the contribution of the local wild fauna to the spread of the
ticks and its contribution to the support of foci of pathogens; (iii) the impact of human actions on the
changing landscape patterns, configuring the availability of hosts for ticks; (iv) the development of new
anti-tick vaccines effective against multiple ticks species; and (v) the development of guidelines about
the importance of the correct use of acaricides and the improvements in tick control derived from the
combined use of vaccination strategies and classic acaricides aimed to distribute the information to
national animal health authorities. The discussions of the group also addressed the need of building
a suitable modelling environment aimed at developing adequate control strategies according to the
regional parameters of tick loads, the elasticity of the tick ecology adapted to the governing weather
features, the prevalence of pathogens, landscape patterns, and a complete analysis of costs and benefits.
These points will be addressed and reinforced in future meetings and actions within the CYTED
“LaGar” project.
Author Contributions: Leading the network, A.E.-P.; organizing the meeting J.M.; conception the paper focus
and outline, J.d.l.F. and A.E.-P.; contribution to the course, paper and pictures, A.E.-P., M.S., M.L., J.M., O.M., E.T.,
J.M.V. and J.d.l.F. All authors have read and agreed to the published version of the manuscript.
Funding: The meeting and course were supported by CYTED (Grant number 118RT0542, Spain) and the Faculty
of Veterinary Medicine of the University of Querétaro (México).
Acknowledgments: We thank members of our laboratories for their contributions to and support of this initiative.
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
2.
3.
4.
5.
6.
Bock, R.; Jackson, L.; Vos, A.D.; Jorgensen, W. Babesiosis of cattle. Parasitology 2004, 129, 247–269. [CrossRef]
McCosker, P.J. The Global Importance of Ticks; Academic Press: Cambridge, MA, USA, 1981.
Howell, J.M.; Ueti, M.W.; Palmer, G.H.; Scoles, G.A.; Knowles, D.P. Persistently infected calves as
reservoirs for acquisition and transovarial transmission of Babesia bovis by Rhipicephalus (Boophilus) microplus.
J. Clin. Microbiol. 2007, 45, 3155–3159. [CrossRef]
Pegram, R.G.; Wilson, D.D.; Hansen, J.W. Past and present national tick control programs: Why they succeed
or fail. Ann. N. Y. Acad. Sci. 2000, 916, 546–554. [CrossRef]
Sonenshine, D.E. Biology of Ticks; Oxford University Press: Oxford, UK, 1991; Volume 2.
Wang, H.H.; Grant, W.E.; Teel, P.D. Simulation of climate-host-parasite-landscape interactions: A spatially
explicit model for ticks (Acari: Ixodidae). Ecol. Model. 2012, 243, 42–62. [CrossRef]
Vaccines 2020, 8, 9
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
7 of 9
Corson, M.S.; Teel, P.D.; Grant, W.E. Microclimate influence in a physiological model of cattle-fever tick
(Boophilus spp.) population dynamics. Ecol. Model. 2004, 180, 487–514. [CrossRef]
Estrada-Peña, A. Geostatistics and remote sensing using NOAA-AVHRR satellite imagery as predictive
tools in tick distribution and habitat suitability estimations for Boophilus microplus (Acari: Ixodidae) in South
America. Vet. Parasitol. 1999, 81, 73–82. [CrossRef]
Estrada-Peña, A.; Bouattour, A.; Camicas, J.L.; Guglielmone, A.; Horak, I.; Jongejan, F.; Latif, A.; Pegram, R.;
Walker, A.R. The known distribution and ecological preferences of the tick subgenus Boophilus (Acari: Ixodidae)
in Africa and Latin America. Exp. Appl. Acarol. 2006, 38, 219–235. [CrossRef] [PubMed]
Estrada-Peña, A.; García, Z.; Fragoso, H. The distribution and ecological preferences of Boophilus microplus
(Acari: Ixodidae) in Mexico. Exp. Appl. Acarol. 2006, 38, 307–316. [CrossRef] [PubMed]
Estrada-Peña, A.; Venzal, J.M. High-resolution predictive mapping for Boophilus annulatus and B. microplus
(Acari: Ixodidae) in Mexico and Southern Texas. Vet. Parasitol. 2006, 142, 350–358. [CrossRef] [PubMed]
Mount, G.A.; Haile, D.G.; Daniels, E. Simulation of blacklegged tick (Acari: Ixodidae) population dynamics
and transmission of Borrelia burgdorferi. J. Med. Entomol. 1997, 34, 461–484. [CrossRef] [PubMed]
Mount, G.A.; Haile, D.G.; Davey, R.B.; Cooksey, L.M. Computer simulation of Boophilus cattle tick
(Acari: Ixodidae) population dynamics. J. Med. Entomol. 1991, 28, 223–240. [CrossRef] [PubMed]
Teel, P.D. Effect of saturation deficit on eggs of Boophilus annulatus and B. microplus (Acari: Ixodidae).
Ann. Entomol. Soc. Am. 1984, 77, 65–68. [CrossRef]
Callow, L.L. Strain immunity in babesiosis. Nature 1964, 204, 1213–1214. [CrossRef] [PubMed]
Uilenberg, G. Babesia—A historical overview. Vet. Parasitol. 2006, 138, 3–10. [CrossRef] [PubMed]
Suarez, C.E.; Noh, S. Emerging perspectives in the research of bovine babesiosis and anaplasmosis.
Vet. Parasitol. 2011, 180, 109–125. [CrossRef]
Callow, L.L.; Hoyte, H.M.D. Transmission experiments using Babesia bigemina, Theileria mutans, and the cattle
tick, Boophilus microplus. Aust. Vet. J. 1961, 37, 10. [CrossRef]
Riek, R.F. The life cycle of Babesia bigemina (Smith and Kilborne, 1893) in the tick vector Boophilus microplus
(Canestrini). Aust. J. Agric. Res. 1964, 15, 802–821. [CrossRef]
Riek, R.F. Life cycle of Babesia argentina (Lignières, 1903) (Sporozoa: Piroplasmidea) in the tick vector Boophilus
microplus (Canestrini). Aust. J. Agric. Res. 1966, 17, 247–254. [CrossRef]
Dalgleish, R.J.; Stewart, N.P.; Callow, L.L. Transmission of Babesia bigemina by transfer of adult male Boophilus
microplus [cattle tick]. Letter to the editor. Aust. Vet. J. 1978, 54, 205–206.
Mahoney, D.F.; Mirre, G.B. A note on the transmission of Babesia bovis (syn B argentina) by the one-host tick,
Boophilus microplus. Res. Vet. Sci. 1979, 26, 253–254. [CrossRef]
Battilani, M.; De Arcangeli, S.; Balboni, A.; Dondi, F. Genetic diversity and molecular epidemiology of
Anaplasma. Infect. Genet. Evol. 2017, 49, 195–211. [CrossRef]
Kessler, R.H.; Schenk, M.A.M. Carrapato, tristeza parasitária e tripanossomose dos bovinos. In Embrapa Gado
de Corte-Livro Técnico (INFOTECA-E); Campo Grande: Mato Grosso do Sul, Brasil, 2002.
Ribeiro, M.F.B.; Facury-Filho, E.J.; Passos, L.M.F.; Saturnino, H.M.; Malacco, M.A.F. Use of standardized
inoculum of Anaplasma marginale and chemoprophylaxis to control bovine anaplasmosis. Arq. Bras. Med.
Vet. Zootec. 2003, 55, 21–26. [CrossRef]
Kocan, K.M.; de la Fuente, J.; Blouin, E.F.; Coetzee, J.F.; Ewing, S.A. The natural history of Anaplasma marginale.
Vet. Parasitol. 2010, 167, 95–107. [CrossRef] [PubMed]
Estrada-Peña, A. The relationships between habitat topology, critical scales of connectivity and tick abundance
Ixodes ricinus in a heterogeneous landscape in northern Spain. Ecography 2003, 26, 661–671. [CrossRef]
Tack, W.; Madder, M.; Baeten, L.; Vanhellemont, M.; Gruwez, R. Local habitat and landscape affect Ixodes
ricinus tick abundances in forests on poor, sandy soils. For. Ecol. Manag. 2012, 265, 30–36. [CrossRef]
Vuilleumier, S.; Metzger, R. Animal dispersal modelling: Handling landscape features and related animal
choices. Ecol. Modell. 2006, 190, 159–170. [CrossRef]
Urban, D.; Keitt, T. Landscape connectivity: A graph-theoretic perspective. Ecology 2011, 82, 1205–1218.
[CrossRef]
Macal, C.M.; North, M.J. Tutorial on agent-based modelling and simulation. J. Simul. 2010, 16, 151–162.
[CrossRef]
Klompen, J.S.H.; Black IV, W.C.; Keirans, J.E.; Oliver, J.H., Jr. Evolution of ticks. Ann. Rev. Entomol. 1996, 41,
141–161. [CrossRef] [PubMed]
Vaccines 2020, 8, 9
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
50.
51.
8 of 9
Nava, S.; Guglielmone, A.A. A meta-analysis of host specificity in Neotropical hard ticks (Acari: Ixodidae).
Bull. Entomol. Res. 2012, 103, 216–224. [CrossRef]
Estrada-Peña, A.; Nava, S.; Tarragona, E.; Bermúdez, S.; de la Fuente, J.; Domingos, A.; Labruna, M.;
Mosqueda, J.; Merino, O.; Szabó, M.; et al. Species occurrence of ticks in South America, and interactions
with biotic and abiotic traits. Sci. Data 2019, 6, 1–5. [CrossRef]
Barré, N.; Uilenberg, G. Spread of parasites transported with their hosts: Case study of species of cattle tick.
Rev. Sci. Tech. 2010, 29, 149–160.
De Oliveira Pascoal, J.; de Siqueira, S.M.; da Costa Maia, R.; Szabó, M.P.J.; Yokosawa, J. Detection and
molecular characterization of Mogiana tick virus (MGTV) in Rhipicephalus microplus collected from cattle in a
savannah area, Uberlândia, Brazil. Ticks Tick Borne Dis. 2019, 10, 162–165. [CrossRef] [PubMed]
Cançado, P.H.D.; Zucco, C.A.; Piranda, E.M.; Faccini, J.L.H.; Mourão, G.M. Rhipicephalus (Boophilus) microplus
(Acari: Ixodidae) as a parasite of pampas deer (Ozotoceros bezoarticus) and cattle tick in Brazil’s Central
Pantanal. Rev. Bras. Parasitol. Vet. 2008, 18, 49–53.
Labruna, M.B.; Jorge, R.S.P.; Sana, D.A.; Jácomo, A.T.A.; Kashivakura, C.K.; Furtado, M.M.; Ferro, C.;
Perez, S.A.; Silveira, L.; Santos, T.S., Jr.; et al. Ticks (Acari: Ixodidae) on wild carnivores in Brazil.
Exp. Appl. Acarol. 2005, 36, 149–163. [CrossRef]
Pound, J.M.; George, J.E.; Kammlah, D.M.; Lohmeyer, K.H.; Dave, R.B. Evidence for role of white-tailed
deer (Artiodactyla: Cervidae) in epizootiology of cattle ticks and southern cattle ticks (Acari: Ixodidae) in
reinfestations along the Texas/Mexico border in South Texas: A Review and Update. J. Econ. Entomol. 2010,
103, 211–218. [CrossRef]
Szabó, M.P.J.; Labruna, M.B.; Pereira Campos, M.; Duarte, J.M.B. Ticks (Acari: Ixodidae) on wild marsh-deer
(Blastocerus dichotomus) from Southeast of Brazil: Infestations prior and after habitat loss. J. Med. Entomol.
2003, 40, 268–274. [CrossRef]
Szabó, M.P.J.; Pascoal, J.O.; Martins, M.M.; Ramos, V.D.N.; Osava, C.F.; Santos, A.L.Q.; Yokosawa, J.;
Rezende, L.M.; Tolesano-Pascoli, G.V.; Torga, K.; et al. Ticks and Rickettsia on anteaters from Southeast and
Central-West Brazil. Ticks Tick Borne Dis. 2019, 10, 540–545. [CrossRef]
Almazán, C.; Torres-Torres, A.; Torres-Rodríguez, L.; Soberanes-Céspedes, N.; Ortiz-Estrada, M. Biological
aspects of Amblyomma mixtum (Koch, 1844) in northeastern Mexico. Quehacer Científico Chiapas 2016, 11,
10–19.
Barbieri, A.M.; Venzal, J.M.; Marcili, A.; Almeida, A.P.; Gomzález, E.M.; Labruna, M.B. Borrelia burgdorferi
sensu lato infecting ticks of the Ixodes ricinus Complex in Uruguay: First Report for the Southern Hemisphere.
Vector Borne Zoon Dis. 2013, 13, 147–153. [CrossRef]
Ramos, V.N.; Piovezan, U.; Franco, A.H.A.; Rodrigues, V.S.; Nava, S.; Szabó, M.P.J. Nellore cattle (Bos indicus)
and ticks within the Brazilian Pantanal: Ecological relationships. Exp. Appl. Acarol. 2016, 68, 227–240.
[CrossRef] [PubMed]
Nava, S.; Venzal, J.M.; González-Acuña, D.; Martins, T.F.; Guglielmone, A. Ticks of the Southern Cone of America:
Diagnosis, Distribution, and Hosts with Taxonomy, Ecology and Sanitary Importance; Elsevier: Amsterdam,
The Netherlands; Academic Press: Cambridge, MA, USA, 2017; p. 348.
Guglielmone, A.A.; Mangold, A.J.; Aguirre, D.H.; Gaido, A.B. Ecological aspects of four species of ticks
found on cattle in Salta, Northwest Argentina. Vet. Parasitol. 1990, 35, 93–101. [CrossRef]
De la Fuente, J.; Kocan, K.M. Strategies for development of vaccines for control of ixodid tick species.
Parasite Immunol. 2006, 28, 275–283. [CrossRef] [PubMed]
De la Fuente, J.; Almazán, C.; Canales, M.; Pérez de la Lastra, J.M.; Kocan, K.M. A ten-year review of
commercial vaccine performance for control of tick infestations on cattle. Anim. Health Res. Rev. 2007, 8,
23–28. [CrossRef]
De la Fuente, J.; Moreno-Cid, J.A.; Canales, M.; Villar, M.; Pérez de la Lastra, J.M. Targeting arthropod
subolesin/akirin for the development of a universal vaccine for control of vector infestations and pathogen
transmission. Vet. Parasitol. 2011, 181, 17–22. [CrossRef]
Willadsen, P. Tick control: Thoughts on a research agenda. Vet. Parasitol. 2006, 138, 161–168. [CrossRef]
Carreón, D.; Pérez de la Lastra, J.M.; Almazán, C.; Canales, M.; Reglero, M. Vaccination with BM86, subolesin
and akirin protective antigens for the control of tick infestations in white tailed deer and red deer. Vaccine
2012, 30, 273–279. [CrossRef]
Vaccines 2020, 8, 9
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
9 of 9
De la Fuente, J.; Estrada-Peña, A. Why new vaccines for the control of ectoparasite vectors have not been
registered and commercialized? Vaccines 2019, 7, 75. [CrossRef]
De la Fuente, J.; Contreras, M. Tick vaccines: Current status and future directions. Expert Rev. Vaccines 2015,
14, 1367–1376. [CrossRef]
García-García, J.C.; Montero, C.; Redondo, M.; Vargas, M.; Canales, M.; Boué, O.; Rodríguez, M.; Joglar, M.;
Machado, H.; González, I.L.; et al. Control of ticks resistant to immunization with Bm86 in cattle vaccinated
with the recombinant antigen Bm95 isolated from the cattle tick, Boophilus microplus. Vaccine 2000, 18,
2275–2287.
Estrada-Peña, A.; Carreón, D.; Almazán, C.; de la Fuente, J. Modeling the impact of climate and landscape
on the efficacy of white-tailed deer vaccination for cattle tick control in northeastern Mexico. PLoS ONE 2014,
9, e102905. [CrossRef] [PubMed]
De la Fuente, J.; Villar, M.; Estrada-Peña, A.; Olivas, J.A. High throughput discovery and characterization of
tick and pathogen vaccine protective antigens using vaccinomics with intelligent Big Data analytic techniques.
Expert Rev. Vaccines 2018, 17, 569–576. [CrossRef] [PubMed]
Contreras, M.; Villar, M.; de la Fuente, J. A vaccinomics approach to the identification of tick protective
antigens for the control of Ixodes ricinus and Dermacentor reticulatus infestations in companion animals.
Front. Physiol. 2019, 10, 977. [CrossRef] [PubMed]
Contreras, M.; Kasaija, P.D.; Merino, O.; de la Cruz-Hernandez, N.I.; Gortazar, C.; de la Fuente, J.
Oral vaccination with a formulation combining Rhipicephalus microplus Subolesin with heat inactivated
Mycobacterium bovis reduces tick infestations in cattle. Front. Cell Infect. Microbiol. 2019, 9, 45. [CrossRef]
[PubMed]
De la Fuente, J.; Contreras, M.; Estrada-Peña, A.; Cabezas-Cruz, A. Targeting a global health problem: Vaccine
design and challenges for the control of tick-borne diseases. Vaccine 2017, 35, 5089–5094. [CrossRef]
De la Fuente, J.; Contreras, M.; Kasaija, P.D.; Gortazar, C.; Ruiz-Fons, J.F.; Mateo, R.; Kabi, F. Towards
a multidisciplinary approach to improve cattle health and production in Uganda. Vaccines 2019, 7, 165.
[CrossRef]
De la Fuente, J. Controlling ticks and tick-borne diseases . . . looking forward. Ticks Tick Borne Dis. 2018, 9,
1354–1357. [CrossRef]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).