1. Introduction
Vector-borne diseases are complex systems that require the interactions between arthropod vectors hosts and pathogens, constrained by a set of environmental variables [
1]. Particularly, vector reproduction, dispersal, and survival are strongly influenced by environmental conditions [
2]. Ecological niche models (ENMs) have become powerful tools in the study of vector ecology. These are mainly used to determine their current and/or future potential distribution, to identify risk areas prone to the emergence of infectious outbreaks, or to distinguish environmental variables that regulate the dynamics of infectious diseases at a landscape level [
3]. When applied to the estimation of potential geographic distribution, ecological niche models identify nonrandom patterns that usually emerge from the superposition analysis of a collection of presence-only or presence/absence data with a set of environmental variables [
4,
5] using different machine learning techniques [
6,
7].
An important arthropod disease carrier is ticks, which, in addition to being hematophagous ectoparasites of wild and domesticated animals and humans, are also known to be key vectors of a great variety of pathogens, such as protozoa, rickettsia, spirochaetes, and viruses [
8,
9,
10]. Human-induced environmental changes appear to be important drivers that enhance tick distribution and survival. These vectors have triggered important human outbreaks such as tick-borne encephalitis (TBE) in Europe, Kyasanur forest disease (KFD) in India, Crimean-Congo hemorrhagic fever (CCHF) in Turkey and Russia, Q fever in the Netherlands, and Rocky Mountain spotted fever (RMSF) in the southern United States and in northern Mexico [
11,
12,
13]. Overall, these events have supported the recognition of tick and tick-borne diseases as important emerging threats to humans and animals [
14,
15,
16].
Hard ticks’ survival off hosts relies heavily on their ability to resist desiccation either by physiological or behavioral adaptations or by the environmental characteristics of the ecosystem in which they are found. For example, Illoldi-Rangel et al. [
17] determined that the ecological suitability determined by climatic and environmental variables of ticks related to the transmission of Lyme disease of the genus
Ixodes and
Amblyomma cajennense can be used to assess the risk of vector-borne diseases even in poorly studied sites such as Mexico. Feria-Arrollo et al. [
18] describe how the distribution of
Ixodes scapularis responds positively to climate change, expanding its geographical distribution and therefore increasing the risk of contact between this important vector with humans and livestock.
Many vector-borne pathogens such as Lyme disease, malaria, Chagas disease, or Leishmaniosis simultaneously use several arthropod species to reach their ultimate hosts [
19,
20,
21,
22]. The assessment of ecological niche models at a genus level can be a useful tool to identify areas of importance for the dynamics of vector-borne diseases, for the identification of areas of higher risk of contact, or for the delimitation of sanitary control fences to prevent the emergence of a potential infectious outbreak. Strategies intended to contain outbreak episodes are usually expensive and difficult to implement [
23], and modeling techniques can be very useful in the design of more efficient sentinel strategies.
In this study, we estimated the potential distribution of four genera of ticks of medical and veterinary importance in Mexico using nine modeling algorithms in order to identify areas of greater suitability for their presence.
3. Results
We found 85 total records for
Amblyomma spp., 44 for
Dermacentor spp., 71 for
Ixodes spp., and 72 for
Rhipicephalus spp. (
Figure 1) (
Table S1). We selected only the ticks recorded from native hosts because our main concern was the natural distribution of the four genera of ticks in Mexico. This criterion reduced the final number of occurrences because of numerous reports on livestock of uncertain geographic origin. The accuracy for ENM estimated that the models for the tick genera varied from very good (AUC values ≥ 0.8) to regular (AUC values between 0.7 and 0.8) for the nine algorithms used (
Table 2). We removed Bioclim from the final model because of its low accuracy for all genera.
The models of distribution estimated for the genera
Amblyomma and
Rhipicephalus had the highest AUC values (
Table 2). Overall, the algorithms used to estimate the potential distribution of
Amblyomma spp. suggested that the areas with greater suitability in Mexico corresponded with the neotropical region of the country (
Figure 2). The most important environmental variables for the genus
Amblyomma were, in order of importance, land use and vegetation, minimum temperature of the coldest month, and precipitation of the warmest quarter (
Table S1), which together accounted for about 85% of the registered presences. In contrast, the distribution models for
Rhipicephalus spp. suggested that the areas of greatest suitability are found in the northeastern portion of the country, in the Yucatan peninsula, and in some areas around the sea of Cortez (
Figure 2). The environmental variables that were strongly associated with the presence of the records of
Rhipicephalus spp. were land use and vegetation, and annual precipitation (
Table S2).
The models generated for the
Ixodes and
Dermacentor genera had a lower predictive precision. The areas of greatest suitability for the
Ixodes genus in Mexico are mainly associated with forested areas in the central and southern mountain ranges (Neovolcanic axis and the Sierra Madre Oriental and Sur) and the coastal areas of the Yucatan peninsula (
Figure 2). The environmental variables that were associated with the presence of almost 90% of the records are land use, annual rainfall, and average daytime range (
Table S2). Finally, the areas suitable for the genus
Dermacentor in Mexico are more widely distributed than the other three genera (
Figure 2). However, the areas of greatest suitability for this genus were mainly located in the Nearctic portion of the country.
4. Discussion
The ecological niche models indicated that the four tick genera have different distribution patterns in Mexico (
Figure 2). The genus
Amblyomma in Mexico is represented by 26 species, seven having a Neotropical distribution (
A. nodosum,
A. oblongoguttatum,
A. longirostre,
A. pacar,
A. pecarium,
A. rotundatum, and
A. sabanerae) and three with a Nearctic distribution (
A. americanum,
A. coelebs, and
A. (=
Robertsicus)
elaphense) [
61]. Eleven have presence in both biogeographic realms (
A. auricularium,
A. cajennense,
A. calcaratum,
A. dissimile,
A. imitator,
A. inornatum,
A. maculatum,
A. ovale,
A. parvum,
A. triste, and
A. scutatum). Five species (
A. humerale,
A. multipuntum,
A. tigrinum,
A. tuberculatum, and
A. varium) were not considered in this study because no reliable information was found about their specific location [
25].
Amblyomma cajennense has the most extensive distribution in the country [
25], and according to the literature, this species is also one of the most widely distributed in the Americas, ranging from the southern United States to northern Argentina [
62]. Ticks from the genus
Amblyomma are aggressive and are generalist species that participate as vectors of pathogens of medical and veterinary importance. Their presence in the northern hemisphere is associated with warm and humid localities that range in elevation up to 1000 m above sea level and with high ecosystem productivity (NDVI values < 0.56) [
63,
64,
65]. The genus
Amblyomma has been recorded in 30 of the 32 states of Mexico [
25]. The states with the highest number of records are Chiapas, Tamaulipas, and Veracruz, followed by Tabasco, Yucatan, Sinaloa, Nayarit, Colima, and Oaxaca [
25,
62]. The ecological characteristics described above were consistent with our model, including the prediction being favorable, and the areas associated with the states bordering the Gulf of Mexico and the Pacific Ocean within the Neotropical biogeographical region were predicted as favorable (
Figure 2).
The geographical distribution of
Amblyomma tends to expand in response to climate change, shifts in land-use, the movement of humans and domestic animals, and the introduction of alien species [
66]. Importantly, individuals that have been collected in localities that range between the 1000 and 1500 m above sea levels or in semi-dessert habitats are not documented as reproductive populations [
62]. These group of species have a low resistance to desiccation [
67] and poor tolerance to temperature variations [
62,
68,
69,
70].
The genus
Ixodes is the most diverse of the family Ixodidae [
71]. In Mexico, there are 26 species of the 243 recognized worldwide. However, most of these species are poorly represented in Mexico, represented by only one record within the country, and many of the immature stages of these species remain unknown [
24].
Ixodes ricinus is recognized as a complex of several species of ticks that together have an almost cosmopolitan distribution (
I. ricinus, I. scapularis, I. pacificus, I. affinis, I. pavloski, I. persulcatus, I. nipponensis, I. gibbosus, I. jellisoni, I. pararicinus, and
I. nuttallianus) [
72]. Subsequent phylogenetic studies determined that
I. muris, I. minor, and
I. granulatus should also be included in the
I. ricinus complex [
73,
74]. The most widely distributed species from the complex in Europe are
I. ricinus and
I. persulcatus, while in North America, they are
I. scapularis and
I. pacificus. These species occupy similar niches in their respective distribution areas [
75].
In North America, many of the immature stages of
Ixodes species can parasitize a large number of hosts that include reptiles, birds, and mammals, whereas
Ixodes adults tend to be restricted to large mammals (e.g., cervids and carnivores) [
76,
77,
78]. Most
Ixodes ticks perform vertical movements on the vegetation to reach their host. However, within the genus, it has also been observed that some species search for their hosts in relatively open environments. Regardless of their behavior, our results are consistent with the associations found previously of these ticks to ecosystems with a relatively high percentage of vegetation covering the ground since they have shown to be sensitive to extreme temperatures and dry conditions (
Figure 2). For example, it was determined that unfed nymphs reached a 50% mortality at an exposure of −11.6 °C during eight consecutive hours under laboratory conditions [
79]. Vegetation was found to generate microenvironmental conditions that prevent the temperature from falling below 0 °C, even during the intensely cold winter periods of the forested environments where these ticks are regularly found. Furthermore, it has been shown that
Ixodes members are particularly sensitive to high temperatures (~30 °C) and water loss [
80], with higher temperatures associated with increased mortality, reduced oviposition success, and host-seeking activity.
Globally, 36 species of
Dermacentor are recognized [
81], 11 of which are documented in Mexico. In general,
Dermacentor ticks are found in all biogeographic regions [
82], but they are better represented in the Holarctic region. However,
D. albipictus, D. dissimilis, D. halli, D. nitens, and
D. variabilis occur in both the Nearctic and Neotropical realms, and
D. imitans is a Neotropical species. Native artiodactyl and perissodactyl mammals are common hosts of this species. However,
D. albipictus and
D. variabilis, which are the most common species in Mexico, are also associated with native carnivora and lagomorpha that inhabit many states of the country [
26,
83].
As with other tick genera, the distribution of
Dermacentor is the result of a complex interaction between climate variables, and host and habitat availability [
83,
84]. Nonetheless, climate constraints seem not to be a limiting factor for
Dermacentor spp. Dispersal because they have an efficient water balance, which enables them to colonize new environments [
80,
85]. This resistance to desiccation combined with the association of adult
Dermacentor ticks with wide distributed hosts [
26] could explain the board distribution in Mexico (
Figure 2).
Rhipicephalus is present in all biogeographic realms. However, there are no endemic species of this genus in the Nearctic and the Neotropical regions [
82], which suggests that this genus was probably introduced to the Americas with livestock or other animals from Eurasia and Africa. The genus
Rhipicephalus contains what are probably the most generalist species, parasitizing amphibians, reptiles, birds, and mammals. Besides high diversity of hosts, it has been suggested that
Rhipicephalus genus in the Americas also has species that have adapted well to both tropical and temperate ecosystems [
86]. Within Mexico, there is a greater proportion of species adapted to tropical ecosystems, with the more suitable areas for this genus in costal ecosystems (
Figure 2).
Overall, ticks have physiological requirements which require certain environmental characteristics that are optimal for their development and survival [
87]. The localities where these characteristics converge can potentially be part of their geographical distribution [
88], and due to their ability to maintain and transmit pathogens of veterinary and medical importance, these localities can be considered as important risk areas [
89]. Although potential distribution models are extensively used, it is important to consider that different algorithm can estimate different outcomes [
90]. However, the generation of an assembly of the predicted models can help identify areas of agreed suitability for ticks and for the establishment of surveillance and control programs.
Management recommendations should consider that the main limitation of ecological niche models when used to estimate the potential distribution of tick species is the taxonomic inconsistencies widely discussed by different authors [
91,
92,
93]. The geographic distribution of a species is determined by a set of complex ecological, geological, and evolutionary processes of each taxon, so the correct geographic location of a record to a species is crucial for the generation of successful models [
18,
88,
94,
95]. We strongly believe that the estimation of genus-based ecological niche models can be useful in approaching the identification of suitable areas for these vectors of medical and veterinary importance.
The knowledge about tick diversity and the ecological features that determine their distribution in Mexico is far from completion. We are currently at a decisive moment for humanity, in which we must not only be able to deal the consequences of the changes we have exerted directly on biodiversity, land use, and climate but also must understand how these modifications influence complex processes such as vector dynamics and the diseases they transmit. The technical improvements to ecological niche modeling and the generation of quality databases may assist the decision-making processes during this period of uncertainty to prevent the emergence of infectious outbreaks that threaten human wellbeing and animal health.