Revista Cienﬁca, FCV-LUZ / Vol. XXXV Received: 05/11/2025 Accepted: 23/02/2026 Published: 19/03/2026 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico 1 of 6 Revista Cienﬁca, FCV-LUZ / Vol. XXXVI UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico First comprehensive survey of Ixodid ck populaons on Arabian-Barb horses in Northeastern Algeria: Species inventory and abioc factors inﬂuence Primer estudio integral de las poblaciones de garrapatas Ixodidae en caballos Árabe-Berbé del noreste de Argelia: Inventario de especies e inﬂuencia de factores abiócos Nesrine Mellouk¹* , Karina Bachtarzi² , Faycal Zeroual³ , Narimene Mansouri⁴ , Assia Allaoui² , Idir Bitam⁵ ¹ Chadli Bendjedid University, Department of Veterinary Sciences, Faculty of Nature and Life Sciences, Laboratory of Funconal and Evoluonary Ecology Research, El Taref, Algeria. ² Gestion de la Santé et Productions Animales Research Laboratory, Institut des Sciences Vétérinaires El-Khroub, Université de Constantine 1 Frères Mentouri, Constantine, Algeria. ³ Chadli Bendjedid University, Faculty of Nature and Life Sciences, Department of Veterinary Sciences, Laboratory of Biodiversity and Ecosystems Polluon, El Taref, Algeria. ⁴ Chadli Bendjedid University, Faculty of Nature and Life Sciences, Department of Veterinary Sciences, Laboratory of Epidemiological surveillance, health, producon and reproducon, experimentaon and cell therapy of domesc and wild animals , El Taref, Algeria. ⁵ ESSAIA, École Supérieure des Sciences de l'Aliment et des Industries Agroalimentaires, Alger, Algérie. *Corresponding author: mellouk.nesrine@univ-eltarf.dz ABSTRACT Ticks infestaon has been shown to be a real health threat to horses in the Mediterranean basin. To idenfy the environmental factors underlying this risk, a prospecve study was carried out from April to September 2024 on 67 Arabian-Barb horses distributed over six diﬀerent climac and geographic sites, ranging from the humid coastal plains of the province El Tarf (4 sites, n = 46, altude 50-300 m) to the semi- arid interior highlands of the province of Tébessa (2 sites, n = 21, altude 400-700 m). A total of 825 cks were manually collected, according to a standardized ﬁve-minute inspecon protocol, and diﬀerenated microscopically through a detailed morphological analysis of speciﬁc characteriscs.The results showed that slightly more than the third of the horses were infested (overall: 34.3 %), with an average parasite burden of 36 cks per animal. More signiﬁcantly, the distribuon of ck species revealed a clear ecological structure (P < 0.001). Species of the genus Rhipicephalus dominated largely in humid, low altude areas, accounng for 86.2 % of the total number of collected cks. In drier, higher-altude zones, however, Hyalomma anatolicum was the predominant species, represenng 54.0 % of all cks collected. This diﬀerence was strongly linked to altude, as evidenced by stascal correlaons: a negave relaonship was observed for R. annulatus (ρ = -0.79, P = 0.002) and R. bursa (ρ = -0.83, P = 0.001), while a posive correlaon was found for H. anatolicum (ρ = 0.67, P = 0.015). The stascal model integrang altude and bioclimac zone alone accounted for 69 % of the observed variance, thereby demonstrang the decisive role of these abioc factors. However, the sex of the horse (male vs. female) did not show any Signiﬁant link to infestaon risk (p= 0.741). Key words: Ticks; horses; bioclimate; altude; Algeria; Mediterranean regions. RESUMEN La infestación por garrapatas ha demostrado ser una amenaza real para la salud de los caballos en la cuenca mediterránea. Para idenﬁcar los factores ambientales subyacentes a este riesgo, se llevó a cabo un estudio prospecvo de abril a sepembre de 2024 en 67 caballo árabe-bereber distribuidos en seis emplazamientos climácos y geográﬁcos diferentes, que abarcaban desde las húmedas llanuras costeras de la provincia de El Tarf (4 emplazamientos, n = 46, altud 50-300 m) hasta las alplanicies interiores semiáridas de la provincia de Tébessa (2 emplazamientos, n = 21, altud 400-700 m). Se recolectaron manualmente un total de 825 garrapatas, según un protocolo estandarizado de inspección de cinco minutos, y se diferenciaron microscópicamente mediante un análisis morfológico detallado de caracteríscas especíﬁcas.Los resultados mostraron que algo más de un tercio de los caballos estaban infestados (frecuencia porcentual global: 34.3 %), con una carga parasitaria media de 36 garrapatas por animal. De manera más signiﬁcava, la distribución de especies de garrapatas reveló una clara estructura ecológica (P < 0.001). Las especies del género Rhipicephalus dominaban ampliamente en las áreas húmedas y de baja altud, representando el 86.2 % del total de garrapatas recolectadas. Sin embargo, en las zonas más secas y de mayor altud, Hyalomma anatolicum fue la especie predominante, representando el 54,0 % de todas las garrapatas recolectadas. Esta diferencia estuvo fuertemente ligada a la altud, como lo evidenciaron las correlaciones estadíscas: se observó una relación negava para R. annulatus (ρ = -0.79, P = 0 .002) y R. bursa (ρ = -0.83, P = 0.001), mientras que se encontró una correlación posiva para H. anatolicum (ρ = 0.67, P = 0.015). El modelo estadísco que integraba únicamente la altud y la zona bioclimáca explicó el 69 % de la varianza observada, demostrando así el papel decisivo de estos factores abiócos. Sin embargo, el sexo del caballo (yegua vs. macho) no mostró ninguna relación signiﬁcava con el riesgo de infestación (p = 0.741). Palabras clave: Garrapatas; caballos; bioclima; altud; Argelia; regiones mediterráneas. https://doi.org/10.52973/rcfcv-e362852

First comprehensive survey of Ixodid ck populaons on Arabian-Barb horses / Mellouk et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico INTRODUCTION Ticks (Acari: Ixodida) is a signiﬁcant animal health and economic issue for equine breeders around the Mediterranean basin. They impact not only equine welfare but also the ﬁnancial proﬁtability, primarily through a sensive decrease in producvity [1]. The harm these cks cause is due to the inoculaon of bioacve saliva loaded with molecules that inhibit coagulaon and modulate the immune system, disrupts hemostasis and oﬅen causes localized inﬂammatory reacons on the skin [2]. Furthermore, these molecules play a central role as vectors for various pathogens such as bacteria, viruses, and protozoa, which signiﬁcantly expand their epidemiological scope [3 , 4]. The Arab-Barb horse (Equus caballus) stands out among diﬀerent equine breeds. Renowned as a genec symbol of the Maghreb and also valued for its resilience and adaptability, it nevertheless shows a notable suscepbility to ck infestaons. Ticks do not only aﬀect the horse’s physical capabilies but also reduce its commercial value, thereby compromising the economic stability of equine breeding sectors, whether convenonal or undergoing modernizaon [5]. In the North African context cks represent a major health concern in equine medicine as they are vectors for pathogens responsible for signiﬁcant infecous diseases such as piroplasmosis, anaplasmosis, and various theilerioses. The genera Hyalomma and Rhipicephalus are among the primary vectors implicated in the transmission of these diseases. These condions have a considerable clinical and economic impact, represenng a major obstacle to the sustainability of breeding in the region [6]. Several studies highlight the crucial impact of the environment on the distribuon and abundance of cks. The distribuon and populaon dynamics of cks are closely linked to environmental factors such as climate, humidity, vegetaon, and altude [7 , 8]. Understanding these bioc interacons is essenal. This knowledge is of increasing importance in an era of climate change, which could radically alter the range of these arthropods and, consequently, the geographical spread of the pathogens they transmit [9]. Research conducted in the Maghreb has contributed to a beer understanding of these parameters. Indeed, in Tunisia, Gharbi et al. [10] demonstrated the inﬂuence of seasonal and climac variaons on infestaon levels in horses. Similarly, an Algerian study on livestock revealed that the composion of parasic communies is impacted by environmental gradients [11]. The importance of quantave studies for understanding ck ecology, demonstrated in North Africa, proves equally crucial in other climac contexts. Recent work conﬁrms this; In France, under a Mediterranean climate, Nadal and al quanﬁed the precise inﬂuence of environmental parameters such as temperature and altude on parasic risk [1]. Meanwhile, in ecologically diﬀerent areas such as Iran, where connental and semi-arid climates predominate, the work of Gholmohammadi et al. [12] and al established the seasonal dynamics of infestaons in horses. Recent connental analyses have shown that human- induced land-use changes, combined with climate change, are driving the expansion of cks and consequently increasing the risk of disease transmission [13 , 14]. However, despite the knowledge already gained, signiﬁcant gaps persist, parcularly concerning the Arab-Barb horse in Algeria. Although this breed constutes the majority of the naonal equine herd [15] no study has yet integrated all the abioc (climate, altude) and bioc (host, age, sex) factors that could inﬂuence ck infestaons [16] .This mulfactorial approach is nevertheless important for understanding parasite dynamics, as suggested by the results of work on other equine species [17]. The absence of a detailed characterizaon of ck populaons associated with the Arab-Barb horse in the diﬀerent agro-ecological zones of northeastern Algeria is parcularly concerning given that this breed is oﬅen raised in resource- limited systems, where it is necessary to implement economical and eﬀecve control plans [4] Under such condions, targeted control methods, based on precise knowledge of local epidemiology, are essenal to ensure their sustainability and cost-eﬀecveness [18]. For an opmal control strategy, it is necessary to idenfy the ck community; this has proven eﬀecve in work concerning livestock in a Mediterranean environment [11]. This work aims to establish the ﬁrst quantave inventory of ixodid ck species parasizing the Arabian-Barb horse in northeastern Algeria and to understand how bioc and abioc factors inﬂuence the level of infestaon. MATERIALS AND METHODS Ethical approval The study was approved by the Ethics Commiee of Department of Veterinary Sciences, Chadli Bendjedid University, El Tarf, Algeria, in accordance with internaonal animal welfare standards (14/2024). Study period and area The study was conducted from April to September 2024 across six sites distributed in two Contrasng bioclimac provinces of northeastern Algeria. The humid region (province of El Tarf, 36°46’N, 8°19’E) is characterized by a humid Mediterranean climate, with an annual rainfall of 600-800 mm and an average temperature of 18.5 °C. Sampling followed a geographical gradient across four localies: the coastal site of Lac des Oiseaux (50-100 m), the intermediate zones of Sidi Kassi (100-150 m), and the inland sectors of Ain El Karma (150-200 m) and El Kala (200-300 m). The semi-arid region (Province of Tébessa, 35°24’N, 8°07’E) features a semi-arid climate, with an annual rainfall ranging from 300 to 400 mm and a mean temperature of 20.5 °C. Two representative localities were sampled: Ogla Malha (400-550 m), a traditional horse-breeding area in a steppe environment, and Bir El Ater (550-700 m), a border region characterized by resilient horse breeding practices. These two provinces, covering the six study sites, reﬂect a signiﬁcant ecological gradient—from humid coastal environments to drier connental interiors—and accurately represent the diverse bioclimac condions found across North Africa. 2 of 6

Revista Cienﬁca, FCV-LUZ / Vol. XXXVI UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico Animals and rearing condions The studied cks were collected from sixty-seven adult Arabian-Barb horses. The laer breed, historically rooted in North African landscapes, is has usually been used for agricultural work, transport, and recreaonal equestrian acvies. Forty- three females and twenty-four males, aged four to ﬁﬅeen years, distributed across two disnct bioclimac zones originated from a humid region (n = 46) and a semi-arid region (n = 21). Within an extensive farming system, horses were subjected to similar management pracces, which involved the separate handling of males and females. An exclusive methodological condion was to ensure that no acaricide treatments had been administered to the animals during the six months prior to and throughout the study period, to avoid distorng the observaon of natural ck-related epidemiological parameters. Tick collecon and idenﬁcaon The collecon protocol was based on a standardized ﬁve- minute monthly examinaon per horse. Visible cks were collected and preserved in 70 % ethanol. The taxonomic keys by Estrada-Peña et al. [19] and Apanaskevich and Horak [20] were used for morphological idenﬁcaon. This standard regional approach ensures consistency with established acarological pracces. Epidemiological parameters and stascal analyses The main indicators of parasic infestaon—namely percentage frequency, mean intensity, and mean abundance— were calculated using the methodology established by Bush et al. [21]. For each of these esmates, we determined the 95 % conﬁdence interval to specify their stascal reliability [21]. • percentage frequency = (Number of infested horses/Total number examined) × 100 • Mean Intensity = Total number of cks/Number of infested horses • Mean Abundance = Total number of cks/Total number of horses examined Stascal analyses were conducted using R soﬅware (version 4.3.2), ulizing the lme4, car, and performance packages for modeling and result validaon. Data normality was veriﬁed by Shapiro-Wilk test, indicang non-normal distribuons (W = 0.82, P < 0.001). Spearman correlaons therefore quanﬁed relaonships between altude and species abundance. A generalized linear mixed model (GLMM) analyzed the combined inﬂuence of environmental factors with total ck abundance as dependent variable, altude and bioclimac zone as ﬁxed eﬀects, and sampling site as random eﬀect. Collinearity was assessed by variance inﬂaon factor. The signiﬁcance threshold was set at P < 0.05. Data are presented as mean ± standard deviaon. RESULTS AND DISCUSSION The results of this study reveal a complex epidemiological dynamic, inﬂuenced by environmental factors that modulate parasite distribuon. The examinaon of 67 horses showed that 23 were infested, corresponding to an overall percentage frequency of 34.33 %. Although this ﬁgure falls at the lower end of data reported for the Mediterranean basin, it contrasts with higher rates observed in Tunisian equids [10]. Diﬀerences in management pracces and climate between the two regions could explain this discrepancy. Analysis of parasite loads showed a mean infestaon intensity of 35.87 cks per infested animal and a mean abundance of 12.31 cks per horse across the enre herd. This combinaon of moderate percentage frequency with high individual loads reveals a parcular epidemiological proﬁle [22], which suggests that the risk of infestaon is not uniformly distributed but rather concentrated within speciﬁc ecological foci or on certain individuals. The analysis of the distribuon of the 825 collected cks conﬁrms the key role of the humidity/aridity gradient. Nearly 70 % of the cks (67.9 %) came from the humid zone. A Chi-square test conﬁrmed that this diﬀerence in total abundance between the zones was highly signiﬁcant (χ² = 105.5, df = 1, P < 0.001). The detailed breakdown by species, presented in TABLE I, highlights contrasng ecological preferences. The Rhipicephalus (R. annulatus and R. bursa) show a very clear ecological aﬃnity for humidity, with over 80 % of their numbers located in the humid zone. This strong dependence conﬁrms their known physiology [23] and corroborates similar observaons on cale in the region [24]. In contrast, the Hyalomma genus shows greater tolerance. Notably, H. anatolicum is slightly more abundant in the semi-arid zone (54 % of its numbers), a behavior also observed in Tunisia [25] and likely linked to adaptaon to higher temperatures [26]. Finally, the species D. marginatus and I. ricinus, strictly conﬁned to humid sites, act as true bio-indicators of these forest habitats. TABLE I ECOLOGICAL DISTRIBUTION OF TICK SPECIES IN HUMID AND SEMI ARID ZONES Species Humid Zone Semi-Arid Zone Total Hyalomma marginatum 208 (65,2 %) 111 (34,8 %) 319 Hyalomma anatolicum 58 (46,0 %) 68 (54,0 %) 126 Hyalomma scupense 47 (51,6 %) 44 (48,4 %) 91 Rhipicephalus annulatus 123 (80,4 %) 30 (19,6 %) 153 Rhipicephalus bursa 65 (84,4 %) 12 (15,6 %) 77 Dermacentor marginatus 20 (100 %) 0 (0 %) 20 Ixodes ricinus 39 (100 %) 0 (0 %) 39 Total 560 (67,9 %) 265 (32,1 %) 825 For each species represent its distribuon between zones, calculated as (number of individuals in the zone / total individuals of the species) × 100 3 of 6

First comprehensive survey of Ixodid ck populaons on Arabian-Barb horses / Mellouk et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico The relaonship between altude and the abundance of each species was calculated. The results of Spearman correlaons, illustrated in TABLE II, revealed signiﬁcant relaonships. Correlaon analyses revealed a strong aﬃnity for low altudes in the Rhipicephalus genera (R. annulatus: ρ = -0.79, P = 0.002; R. bursa: ρ = -0.83, P = 0.001) and typical forest species (Ixodes ricinus: ρ = -0.85, P < 0.001; Dermacentor marginatus: ρ = -0.81, P = 0.001). In contrast, Hyalomma anatolicum showed a moderate positive correlation with altitude (ρ = 0.67, P = 0.015). This distribuon suggests that the highest slopes in the semi-arid zone provide, along the studied bioclimac gradient, a more favorable microclimate for this species, thereby demonstrang the complexity of the interacons between cks and local environmental factors through this parcular ecological niche [27]. To synthesize the combined inﬂuence of these factors, a GLMM was constructed. Its results, presented in TABLE III, aribute major explanatory power to abioc factors. The bioclimac zone and altude explain approximately 70 % of the observed variance. This result fully validates our environmental approach and makes it a reliable predicve tool for idenfying at-risk zones [28]. TABLE II RELATIONSHIPS BETWEEN ALTITUDE AND ABUNDANCE OF MAIN TICK SPECIES: SPEARMAN’S RANK CORRELATION COEFFICIENTS. Species Correlaon coeﬃcient (ρ) P-value 95% Conﬁdence Interval Rhipicephalus annulatus -0, 79 0, 002 [-0, 92 to -0, 52] Rhipicephalus bursa -0, 83 0, 001 [-0, 94 to -0, 58] Hyalomma anatolicum 0, 67 0, 015 [0, 38 to 0, 84] Ixodes ricinus -0, 85 < 0, 001 [-0, 95 to -0, 62] Dermacentor marginatus -0, 81 0, 001 [-0, 93 to -0, 55] ρ, Spearman’s rank correlaon coeﬃcient ; CI, Conﬁdence Interval. The Spearman’s ρ coeﬃcient was calculated by ranking the altude and ck abundance values independently and then measuring the strength and direcon of the monotonic relaonship between these ranks. TABLE III. RESULTS OF A GENERALIZED LINEAR MIXED MODEL ANALYZING THE EFFECTS OF ABIOTIC FACTORS ON TOTAL TICK ABUNDANCE Parameter Coeﬃcient Standard Error z-value P-value VIF Fixed Eﬀects Intercept 15,32 3,45 4,44 < 0,001 - Altude (m) -0,018 0,006 -3,00 0,003 1,8 Bioclimac Zone 8,45 2,87 2,94 0,003 2,1 Random Eﬀect Site (Variance) 2,34 1,21 - - - Model Fit Marginal R² 0,58 - - - - Condional R² 0,69 - - - - GLMM: Generalized Linear Mixed Model; SE: Standard Error; VIF: Variance Inﬂaon Factor: R², coefficient of determination. The model esmates were calculated using a GLMM with a negave binomial distribuon and a log-link funcon. The coeﬃcients represent the expected change in the log-count of total cks for a one-unit increase in the predictor, while controlling for random variaon between sampling sites. Contrary to some studies that reported a sex-biased infestaon in certain species [29], we did not detect a signiﬁcant diﬀerence in percentage frequency between mares (32.56 %) and males (37.50 %, P = 0.741). It should be noted that these variaons can depend on several factors: the ck species involved, the speciﬁc pathogen, or the rearing condions. For example, recent studies conducted on Dermacentor cks in comparable management systems have not shown a signiﬁcant link between the risk of infestaon and the sex of the host animal [30]. This homogeneity could be linked to the extensive rearing condions of the studied herd, which may standardize exposure to the parasite. Alternavely, it might suggest a homogeneous response of the Arab-Barb breed to infestaon, a hypothesis that warrants further study. The predominant role of these abioc factors idenﬁed in this model is consistent with recent ﬁndings from other geographical contexts. Zhang et al. [31] recently demonstrated, in cks of the genus Hyalomma in China, that combining climatic variables with occurrence data offers excellent reliability — an approach consistent with the one validated in the present study. This finding is further supported by recent analyses conducted in Xinjiang, where the integration of vector distribution data with climatic and ecological parameters proved equally critical in elucidating the dynamics of tick-borne pathogens [32]. Furthermore, Modeling of Ixodes ricinus vector dynamics in Europe has identified land use and precipitation as the main determinants of ck abundance [33]. Lansdell et al. [33] demonstrated that humidity-related variables consistently outperform other abioc parameters in explaining the distribuon of this species across European ecosystems. These ﬁndings corroborate those of the present study, in which the humidity/aridity gradient also emerges as the major ecological 4 of 6

Revista Cienﬁca, FCV-LUZ / Vol. XXXVI UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico factor structuring ck communies in the Mediterranean basin. This convergence thus validates the robustness of the environmental approach adopted and its applicability beyond the Algerian context. Contrary to some older studies that reported a host sexbiased infestaon paern, the present study detected no signiﬁcant diﬀerence in percentage frequency between mares (32.56 %) and males (37.50 %; p = 0.741). This absence of sexrelated bias is consistent with recent molecular observaons in Dermacentor albipictus [34]. This ﬁnding is also in agreement with epidemiological surveys conducted on asymptomac horses in France [35]. This homogeneity may be related to the extensive rearing condions of the studied herd, which standardize exposure to the parasite by migang potenal sexlinked behavioral biases. It might also suggest a homogeneous response of the ArabBarb breed to infestaon—a hypothesis that warrants further invesgaon through controlled studies combining parasite burden measurements with analysis of humoral and cellular immune proﬁles. CONCLUSION This ﬁrst characterizaon of ck infestaon in the Arab-Barb horse in Algeria reveals an epidemiological proﬁle structured by key environmental factors. This ecological understanding provides a robust foundaon for the development of targeted, raonal, and economically sustainable management techniques, speciﬁcally designed for the region’s agricultural systems. It lays the groundwork for integrated and sustainable health management, which is essenal for animal welfare and the economic proﬁtability of local agricultural operaons. Conﬂict of interest The authors declare no conﬂict of interest. BIBLIOGRAPHIC REFERENCES [1] Nadal C, Chanet C, Delaunay C, Pitel PH, Marsot M, Bonnet SI. 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