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All issues Volume 31 (2024) Parasite, 31 (2024) 57 Full HTML
Open Access
Issue
Parasite
Volume 31, 2024
Article Number 57
Number of page(s) 13
DOI https://doi.org/10.1051/parasite/2024057
Published online 27 September 2024

© A. Zahri et al., published by EDP Sciences, 2024

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Blood-sucking arthropods, such as ticks, fleas, mosquitoes and phlebotomine sand flies, are responsible for the transmission of a large number of pathogens including bacteria, viruses, protozoa, and helminths, which can have a significant impact on human and animal health, and on the global economy through considerable economic losses [61, 84]. The global spread of these vectors and their transmitted pathogens is driven by many factors, mainly related to climatic and environmental changes, the evolution of international trade, the movement of human and animal populations, or resistance developed to insecticidal compounds used for insect control [62, 84]. As a consequence, several human outbreaks of vector-borne diseases have recently been reported on different continents. In Africa, the last confirmed outbreak of dengue fever, a mosquito-borne flavivirus, was described in Tanzania in 2019 [48]. Furthermore, the largest epidemics ever seen of West Nile fever, caused by a virus transmitted by the bites of Culex mosquitoes, was observed in the United States of America between 2002 and 2003 [79], whereas outbreaks regularly occurred in several central European countries in 2018, demonstrating intense transmission [23]. Moreover, two major outbreaks of visceral leishmaniasis due to Leishmania donovani transmitted by Phlebotomus argentipes sand flies were documented in the Indian sub-continent in 2014 and 2018 [64, 83]. The south of Venezuela and north of Brazil experienced massive outbreaks of Amazonian onchocerciasis (river blindness), which is a neglected tropical disease transmitted by simuliid black flies [31]. So far, the impact of biting midges (Diptera: Ceratopogonidae) on public health is limited to the transmission of Oropouche Fever Virus (ORFV), which causes a febrile illness in humans in Central and South America [26, 96], and leading currently to health impacts in French Guiana [75]. However, they are competent vectors for other viruses of veterinary interest, such as Schmallenberg Virus (SBV), Bluetongue Virus (BTV) affecting livestock [9, 63], African Horse Sickness Virus (AHSV), which causes a fatal disease in the equine population [27], and Epizootic Hemorrhagic Disease Virus (EHDV), which is booming in Europe [93].

Dogs are reservoir hosts of many vector-borne zoonotic pathogens (e.g., Anaplasma phagocytophilum and A. platys, Borrelia burgdorferi sensu lato complex, Ehrlichia canis and E. ewingii, Dirofilaria immitis and D. repens, Leishmania infantum, Rickettsia conorii and R. rickettsii, Dipylidium caninum, Babesia canis vogeli and B. canis rossi) [84], most of which has previously been reported in Morocco [12, 39, 40, 88, 94, 95]. Dog populations have increased remarkably in developed and developing countries, with dogs playing a major role in supporting people with mental illnesses and physical disabilities [81]. At the same time, the number of stray dogs has increased in developing countries due to ineffective control programs [57]. They are often confined to shelters which are located in rural and peri-urban areas and are exposed to the risk of infection by various vector-borne pathogens [57]. In addition, they are suffering from a lack of the necessary veterinary care and adequate preventive measures [57]. Therefore, they represent high-risk foci for workers and visitors, who may be exposed to zoonotic pathogens [51]. Although the diversity of sand flies, mosquitoes, and Culicoides has been studied in Morocco [3, 15, 101, 104], knowledge of arthropod fauna in shelters, which is essential for assessing the risk of transmission of vector-borne zoonotic pathogens, remains undescribed.

Thus, the aim of this work was to (a) describe the populations of biting midges, mosquitoes, and sand flies in four dog shelters located in central Morocco, (b) discuss their potential involvement as vectors in the transmission of various pathogens, and (c) assess the risk of these shelters as foci for zoonotic diseases.

Material and methods

Study area

This study was carried out in four dog shelters (DS) located in four different regions (DS1, Rabat-Salé-Kénitra region; DS2, Casablanca-Settat region; DS3, Fez-Meknès region and DS4, Béni Mellal-Khénifra region) of central Morocco. These regions are characterized by a Mediterranean climate with mild, wet winters and hot, dry summers. DS1 (33.806538, −6.902472) is located in the rural district of Sidi Yahya Zaër, while the others are in peri-urban areas at the city edges of Bouskoura (DS2, 33.507278, −7.631269), Fez (DS3, 34.004291, −5.106422), and Khouribga (DS4, 32.845631, −6.938536). DS1, DS2, and DS4 are constituted by large, multiple and open dog kennels (3–5 dogs per kennel), whereas DS3 is characterized by several uncovered rooms, where dogs can roam freely. Additionally, there is a special room for abandoned cats in DS2 and DS3, and stalls for donkeys and mules without owners in DS2. All these shelters are well fenced. DS1 and DS2 are surrounded by forests and field crops, and DS3 and DS4 by a few green spaces.

Insect collections and identification

A single Onderstepoort Veterinary Institute (OVI) black light suction trap was placed at each DS to collect adult Culicoides. This 220 V trap was equipped with a 30 cm fluorescent UV neon tube (8 W) attracting insects and with a fan propelling them to a collection pot, filled with a buffer solution, which is used to limit nucleic acid degradation and consequently increase the probability of viral genome detection (RNAlater-like solution was prepared as described by Camacho-Sanchez et al. [22] using the following stock solutions and reagents: 0.5 M ethylenediaminetetraacetic acid (EDTA) disodium salt dihydrate (18.61 g/100 mL, pH to 8.0 with NaOH through stirring), 1 M sodium citrate salt dihydrate (29.4 g/100 mL, stirring used for dissolving), ammonium sulfate (powdered) and sterile water (see Appendix for the protocol used to prepare this solution). Two drops of commercial detergent (manufactured by Ecolab Maroc, Casablanca, Morocco) were added to the collection pot to help the drowning of Culicoides, avoiding their drying which complicates morphological identification.

Adult mosquitoes were collected using a BG-Pro mosquito trap (BGP), baited only with CO2 (without BG-Lure), installed at each DS, and hung at a tree branch where there is no access for dogs. The trap is powered by an external 6 V battery and equipped with white light bulbs, a fan, and a collector net. CO2 was produced with a fire extinguisher at a flow rate of 0.5 kg/day. The collected mosquitoes were transported live to the laboratory and then killed by freezing at −20 °C.

Sand flies were sampled using castor oil on sticky papers (20 × 20 cm) disposed on walls inside the different DS. 30 sticky papers were used on each trapping night in the DS concerned.

Trapping was carried out from April 1 to November 30, 2022 with two successive sampling nights per month and DS. The traps and sticky papers were functional from 6 pm to 10 am. The collected insects were sent directly to the Parasitology and parasitic diseases laboratory of the Institut Agronomique et Vétérinaire (IAV) Hassan II for morphological identification to the species level using relevant keys [7, 8, 35, 73]. These blood-feeding arthropods were stored at −80 °C.

Data analysis

To explore the diversity of the collected insects, different parameters and ecological indexes were calculated using Microsoft Office Excel 2019 (Microsoft Corporation, Redmond, WA, USA): (i) the absolute abundance (N) (total number of specimens collected by the various traps used); (ii) the relative abundance (RA) [(the number of specimens of each species/the total number of specimens of the family) × 100]; (iii) the sex ratio (SR) [(the result of dividing the number of females by the number of males belonging to the same species collected for each family)]; (iv) the frequency of occurrence per DS (C (%)/DS) [(number of collections containing the species under consideration / total number of surveys carried out) × 100]; (v) the species richness (S) (number of all species collected for each family in each study area); and (vi) the Shannon and Wiener diversity index (H’)[(H’ = Σ Pi log2 Pi) and Pi is the proportion of all samples belonging to the “i-th” species]. Graphs were created using R version 4.2.0 with the ggplot2 R package [89].

Results

Species composition

During the 64 collection nights, a total of 2,321 Culicoides biting midges (Diptera: Ceratopogonidae) were collected, representing fourteen species with the dominance of Culicoides imicola (55.96%), followed by C. paolae (16.07%), C. circumscriptus (10.29%), and C. newsteadi (5.77%). The number of collected females was higher compared to males (1,723♀/598♂). The sex ratio differs depending on the species. Thirty-four engorged females were identified, dominated by Culicoides imicola (27/34) (Table 1).

Table 1

Total number, global abundance, rank, sex ratio, and occurrence per dog shelter (C (%)/DS) of collected biting midges (Ceratopogonidae: Culicoides) by UV-light/suction trap (OVI type), from April to November 2022, at four dog shelters (DS) in central Morocco.

A total of 570 mosquito specimens (Diptera: Culicidae) were caught, belonging to two genera: Culex (97.20%) and Culiseta (2.80%) (Table 2). Culex pipiens s.l. was the most frequent species (96.84%) followed by Culiseta longiareolata (2.80%) and Cx. perexiguus (0.36%). Females were predominant versus males (525♀/45♂), which means they were favored in the sex ratio. Five of the 525 females were engorged.

Table 2

Total number, global abundance, rank, sex ratio, and occurrence per dog shelter (C (%)/DS) of caught mosquitoes (Culicidae) by BG-Pro mosquito trap (BGP), from April to November 2022, at four dog shelters (DS) in central Morocco.

A total of 475 sand flies (Diptera: Psychodidae) were recorded, belonging to two genera (Table 3). Seven Phlebotomus species (62.70%) and three Sergentomyia species (37.30%) were collected. Sergentomyia minuta was the most prevalent species (34.31%), followed by Phlebotomus sergenti (32.42%), typical Ph. perniciosus (PN) (8.63%), Ph. alexandri (6.94%), and Ph. riouxi (6.52%). The males outnumbered the females (133♀/342♂) and therefore, the sex ratio was favorable towards all male species except for Sergentomyia fallax. Twelve engorged females were found, with the dominance of Phlebotomus sergenti (10/12).

Table 3

Total number, global abundance, rank, sex ratio, and occurrence per dog shelter (C (%)/DS) of trapped sand flies (Psychodidae) by sticky traps, from April to November 2022, at four dog shelters (DS) in central Morocco. Ph: Phlebotomus, Se: Sergentomyia.

Seasonal occurrence, diversity, and species richness of collected arthropods

The abundance of Culicoides populations, already active in April, grew progressively to reach a first peak in June in DS1 and in July at DS3. Then, the second peak occurred in September followed by a rapid population decrease in October/November (Fig. 1). Very few Culicoides were collected in DS2 and DS4. Culicoides imicola was the dominant species, with an abundance peak in September (Fig. 2) at both sites (42.90% of the total collection at DS1 and 71.0% at DS3), whereas the rank of other species variated between sites. Culicoides paolae was abundant at DS1 (29.00%), with an abundance peak in June and August, but rare at DS3 (< 0.50%). Culicoides circumscriptus was the third most abundant species at DS1 (12.20%), peaking in August, with a similar abundance to C. newsteadi (9.40 and 8.10%) at DS3, where the latter peaked in September (Fig. 2). The richness and diversity were maximum at DS1 (H’ = 1.57; S = 13) and the DS3 (H’ = 1.09; S = 13), while observed biodiversity was lowest at DS2 (H’ = 0.56; S = 2) and DS4 (H’ = 0.00; S = 1) (Table 4).

thumbnail Figure 1

Monthly abundance of blood-sucking arthropods collected at the four dog shelters (DS).

thumbnail Figure 2

Seasonal variations of the most abundant Culicoides species trapped at DS1 and DS3.

Table 4

Total number and species richness of Culicoides biting midges (Diptera: Ceratopogonidae) at the four dog shelters (DS) studied.

For mosquitoes, the activity season extended from April to November (8 months) with a marked peak observed in May (Fig. 1). Except in DS1, where the majority of specimens were collected (82.40%), the mosquito fauna in the other DS remained very limited (17.60%). Culex pipiens s.l. was the most abundant species (96.84%), collected mainly at DS1, and presented a unimodal pattern (Fig. 3). The highest number of specimens was observed in May. In contrast, due to the scarcity of species in the other DS, the study of seasonality remains impossible, which explains the low values of the biodiversity parameters (Table 5).

thumbnail Figure 3

Seasonal variations of the most collected mosquito species caught at DS1.

Table 5

Total number and species diversity of mosquitoes (Diptera: Culicidae) at the four dog shelters (DS) studied.

For the sand flies, the populations were active from June to October (Fig. 1) (5 months) at DS1, DS3, and DS4 with two peaks in July and September. On the contrary, no sand fly was collected in DS2. Sergentomyia minuta was the most abundant species (68.30%) followed by typical Phlebotomus perniciosus (PN) (14.80%), and typical Ph. longicuspis (LC) (11.80%) in DS1 (Fig. 4). The first two species displayed a bimodal trend with a first peak observed in July and the second most remarkable in September, while the third species showed a unimodal pattern of temporal distribution with a peak in September. Phlebotomus sergenti was the most abundant species at DS3 and DS4 (53.70% and 77.10%, respectively) with a peak in July followed by Ph. riouxi (17.30%) (abundance peak in June), and Ph. alexandri (14.80%) (abundance peak in June and August) at DS3 (Fig. 4). The abundance of other species remains very low at DS4 (Fig. 4). The biodiversity was greater at DS3 (H’ = 1.41; S = 8) than at the other DS (DS1 (H’ = 0.99; S = 7) and DS4 (H’ = 0.81; S = 6)) (Table 6).

thumbnail Figure 4

Seasonal variations of the most prevalent sand fly species collected at DS1, DS3, and DS4.

Table 6

Total number and species diversity of phlebotomine sand flies (Diptera: Psychodidae) at the four dog shelters (DS) studied.

Discussion

The entomological survey highlighted the composition, abundance, and diversity of blood-sucking arthropods collected at four dog shelters (DS) in central Morocco over an eight-month period from the beginning of April to the end of November 2022. The monitoring of these blood-sucking arthropods during 64 catch nights, allowed us to identify a total of 2,321 Culicoides biting midges (Diptera: Ceratopogonidae), 570 mosquitoes (Diptera: Culicidae), and 475 sand flies (Diptera: Psychodidae).

Species composition

This study demonstrated the presence of at least fourteen Culicoides species at DS1 and DS3. The observations of González et al. [51] showed the same number of species collected in three dog and cat shelters located in northern Spain. Culicoides were absent in DS2 and DS4. This lack of observed specimens can be explained by the absence of the humid organic matter necessary for the breeding of biting midges in the vicinity of the traps. Furthermore, the regular use of volatile insecticides at DS2 could explain the general absence of arthropods in this shelter. Regarding DS4, the fact that it is located in a windy area limits the population of blood-sucking arthropods observed throughout the study period. Culicoides imicola was the most collected species in the present study, and is the most common species in Morocco and frequently collected in countries with a Mediterranean climate, especially on livestock farms [5, 15, 45, 55]. This abundance indicates the presence of moist clayey muds, which provide the specific larval sites required for the development of this species larvae [18]. Generally, Culicoides imicola is considered to be a heliophilous species resistant to desiccation, which explains its abundance in warmer regions [32]. The second most abundant species at DS1 was Culicoides paolae (29.0%), whereas at DS3, it was C. newsteadi (9.4%). The differences in abundance noted in these two study areas may be related to ecological parameters. The high abundance of Culicoides paolae at DS1 is associated with the presence of decaying prickly pear trees requiring clay-rich soil and high salinity, which provides a suitable environment for egg-laying by females [13, 74]. The first record of Culicoides paolae in Morocco was in 2019 [14]. This species remains among the most frequently encountered Culicoides species in several studies carried out in Tunisia [97], Italy [46], and Malta [50]. The observed abundance of Culicoides newsteadi in DS3 is connected to the presence of water-saturated organic matter, which constitutes the optimal breeding site for this species [4, 18]. Culicoides circumscriptus remained the third most frequently collected species in DS1 (12.2%) and DS3 (8.1%). The capacity of Culicoides circumscriptus to adapt to different habitats may explain its similar presence at DS1 and DS3 [102].

Regarding mosquitoes, Culex pipiens s.l. (96.84%) was the most dominant species in the current study, which corroborates the results of Filali Mouatassem et al. [44] and González et al. [51], where Cx. pipiens s.l. was the most abundant species in Morocco (89.92%) and Spain (76.80%). DS1 had the highest number of specimens collected compared to DS2, DS3, and DS4, which may be associated with the availability of an aquatic environment required for larval development [44, 72]. In the present study, low biodiversity was observed in terms of mosquito species compared to that observed in Spain (eight species; González et al. [51]), which is perhaps correlated to the presence of anthropogenic larval habitats (water containers, waste water) at the studied sites, where Culex pipiens s.l. is mainly found alone [2]. This species prefers water rich in organic matter, and its abundance is positively correlated to urbanization and agriculture optimizing its nuisance [2]. It should be noted that a few specimens of Culiseta longiareolata were collected during this study. These findings are consistent with what is found in dog and cat shelters in northern Spain [51]. It is known that these two species share the same breeding sites, and consequently the differences in their observed abundance seem more likely to be linked to competition in the same larval habitats [71].

Unlike the results of González et al. [51], which indicated a total absence of sand flies in dog and cat shelters in northern Spain, our study highlighted substantial diversity of these blood-sucking arthropods, which varied between DS1, DS3, and DS4 depending on biotic and abiotic factors [99]. The lack of sand fly species in DS2 is probably related to the regular treatment of all dogs in this shelter with collars containing 10% imidacloprid and 4.5% flumethrin. This is consistent with the results of a study carried out in a dog shelter in Italy, where the use of these collars had a reducing effect on the composition of the sand fly fauna [85]. Ten sand fly species were identified in the current study. In southern Italy, five species of sand fly were collected at a dog shelter [100]. In contrast, only two species were reported in another study carried out at a dog shelter in Lecce, Italy [76]. Sergentomyia minuta was the dominant species in our study, accounting for 34.31% of total catches in the three DS. Its greatest abundance (68.30%) was observed at DS1. This finding matches three previous studies in dog shelters in Italy [67, 76, 100], in which this species represented 92.70%, 46.46%, and 45.10% of all sand flies collected. This species is more frequently collected in dry, open areas and sandy soils in rural and urban settings [16, 34], similar to the conditions described at DS1 [59]. On the other hand, Phlebotomus sergenti was the most abundant species at DS3 (53.70%) and DS4 (77.10%), representing 32.42% of all specimens collected in the present study. These observations are in contrast with those of Latrofa et al. [67], Mendoza-Roldan et al. [76], and Tarallo et al. [100] who reported the absence of this species from dog shelters in southern Italy. This high abundance indicates their preference for the sandy-loam soils observed at these two DS [59]. Typical form of Phlebotomus perniciosus (PN) and Ph. longicuspis (LC) remain the second (14.80%) and third (11.80%) most collected species at DS1, respectively. Phlebotomus perniciosus is characterized by endo-exophilic behavior and is widely distributed in northern and south-western Morocco [52, 104], whereas Ph. longicuspis has an exophilic character with preference for sandy-loam soils [59, 104]. On the contrary, Phlebotomus riouxi, which remains a rare species in the Maghreb region and Ph. alexandri, which is very common in urban areas, were the most encountered species at DS3 [8, 30].

Seasonal activity

Our findings are in line with those of González et al. [51], in northern Spain, who observed a marked peak of Culicoides in early summer and a decrease in their activity in autumn. These observations disagree with those of previous entomological studies in Morocco [13, 69], in which the most remarkable peaks occurred in spring and autumn.

Regarding the Culicoides species, Culicoides imicola showed a peak of activity in September in Rabat, which is in agreement with Bourquia et al. [15]. It is worth noting that there was a sudden decrease in abundance in July at DS1 and in August at DS3; this could be explained by the decrease of vegetation and forest cover during this period, which is unfavorable to Culicoides imicola [6, 37]. The population of this Afrotropical species is known to be affected by wind speed, which impacts their flight activity [6]. Culicoides paolae presented two peaks observed in June and August. This finding is in discordance with that documented in Andalusia (southern Spain) by Estrada et al. [42], who reported that September and October were the most abundant months for Culicoides paolae, which prefers the Mediterranean climate. Our study survey highlighted the abundance of Culicoides newsteadi during summer, which is contradictory with other reports in Morocco and Italy where C. newsteadi was more abundant in spring [15, 47]. Thus, this species is characterized by its ability to tolerate the highest minimum temperatures [4]. The higher number of Culicoides circumscriptus was observed in summer. This result is supported by Ortega et al. [82] during their study in southern Spain, indicating that this species reaches its peak of activity in summer, marked by highest maximum temperatures. Previous observations have reported this species on cattle farms close to coastal plains, and it has regularly been described in humid and sub-humid zones of Morocco [13, 46].

Regarding the seasonal pattern of mosquito populations, this study demonstrated a peak in abundance in late spring, which is in accordance with the findings of Marc et al. [72], where the peak of Culex pipiens s.l. activity in the province of Kénitra (Morocco) occurred in June. In contrast, the activity of mosquitoes studied in Spain showed a sinusoidal dynamic with a peak in abundance in early summer [51]. This can be explained by the impact of weather on mosquito population habitats in the study areas concerned. Several studies have found that high temperatures accompanied by a lack of precipitation in summer reduce aquatic breeding sites for Culex pipiens s.l., confirming that this species is affected by drought [20, 92]. In addition, early precipitation conditions contribute to their increased abundance, while the extension of their season is a consequence of late rainfall conditions [36].

Regarding the seasonal activity of sand flies, our findings align with those of Talbi et al. [99] in Aichoun (central Morocco) and Zarrouk et al. [104] in Tétouan city and Oued Laou village (northern Morocco), who reported the bimodal seasonal trends of sand fly populations with two remarkable peaks occurring in July and September. However, in contrast to these findings, other entomological investigations carried out in Morocco have shown that sand flies exhibit two significant peaks of abundance in June and August in Zlililgh (central Morocco), and in August and October in Taza (central-north Morocco) [53, 65]. These seasonal fluctuations could be associated with the climatic conditions that influence their life cycle [49, 104]. Their activity duration remains short, extending from June to October in the present study. This finding is in line with what is reported in other studies in northern and central Morocco indicating that the seasonal activity of sand flies begins in summer and ends in autumn [99, 104]. The activity of Sergentomyia minuta showed a bimodal cycle, as reported in Marrakech city (central Morocco) by Boussaa et al. [17] and it is well distributed in a semiarid climate [59]. On the other hand, Phlebotomus sergenti peaked in July in this study and another in Marrakech [17]. While in northern Morocco, this species experienced two peaks in abundance: the first in July and the second in September [104]. According to Kahim et al. [59], this species is distributed in several bioclimatic stages and its abundance is favored by a semiarid climate. In this study, Phlebotomus perniciosus (PN) displayed two peaks recorded in July and in September as stated in previous studies conducted in Spain and Morocco, which is abundant in humid to semi-arid climates [49, 52, 104]. Phlebotomus longicuspis (LC) which was sympatric with Ph. perniciosus (PN) in DS1 presented a unimodal seasonal distribution with peak activity in September. These results are in agreement with those of Guernaoui et al. [54] in southwest Morocco and it is well described in Saharan areas [59]. Phlebotomus riouxi is frequently collected in arid and hyper arid climates, while the abundance of Ph. alexandri increases in subhumid to arid zones [8, 30].

Vector role

Regarding their role in disease transmission, Culicoides are potential vectors of Bluetongue Virus (BTV) in livestock, which is endemic in Morocco [33]. The peak abundance of Culicoides observed in our study coincides with very high BTV infection rates [70]. Interestingly, of the 1,723 females collected in the current study, 34 (2.00%) were blood fed (27 Culicoides imicola, 3 C. newsteadi, 2 C. saevus/langeroni, 1 C. circumscriptus, and 1 C. longipennis). In contrast, blood fed females were absent in the collections of Culicoides found by González et al. [51] in northern Spain. Slama et al. [97] confirmed the canine origin of the blood meal in a female Culicoides imicola, which can feed on livestock, birds, and humans. Furthermore, many Culicoides species including Culicoides obsoletus, C. punctatus, and C. pulicaris are known to feed on dogs in Siberia [78]. In contrast, analysis of blood meals from 400 females collected in Israel and Zimbabwe did not suspect the dog as the host species. Oura and El Harrak [87] reported the BTV infection of 21% of dogs in Morocco infected by the bites of Culicoides. According to Hanekom et al. [56], an infected dog suffers from anorexia, lethargy, dyspnea, and hypoxia, but remains unable to replicate the virus [86], which can be transmitted by direct contact or ingestion of infected meats from infected sheep [55]. With regard to African Horse Sickness Virus (AHSV), this is another Orbivirus that has been the subject of a few studies in dogs worldwide. Van Sittert et al. [103] reported the death of a dog in South Africa due to this virus, which never had access to horse meat, although Braverman and Chizov-Ginzburg [19] concluded that vector transmission in the case of AHSV in dogs remains accidental, as it cannot be a reservoir and its role in epidemiology is neglected. Of note, a recent study in Italy showed the presence of Dirofilaria immitis and D. repens DNA in Culicoides paolae, which are mosquito-borne nematodes [80].

Culex pipiens is the main vector of West Nile Virus (WNV), that has caused several epizootics in horses in Morocco [43]. According to El Rhaffouli et al. [41] and Assaid et al. [3], this emerging arbovirus (arthropod-borne virus) affecting humans is still circulating in Morocco. A few studies have demonstrated that dogs are highly exposed to WNV: the seroprevalence rate found in Morocco was 62% [38], whereas it was 30.2% and 8.1% in Libya [11] and France [66], respectively. The dog population remains an effective means of measuring the circulation and spread of the virus in a given area [11, 38, 66]. Consequently, it seems highly appropriate to set up a sentinel surveillance system at dog shelters in various parts of the kingdom, located in rural and peri-urban areas close to the human population, in order to obtain data on viral exposure and intervene at the appropriate time to overcome the damage associated with WNV on animal and human health, which is still endemic in North and West Africa [10]. Culex pipiens is also a vector of Dirofilaria immitis and D. repens, whose reservoir is the dog, and can be transmitted to humans [21, 24, 91]. In addition, human exposure to these filarial infections is favored by an endemic context, as is the case in the Mediterranean basin [77]. Dirofilaria immitis was more prevalent (14.5%) than D. repens (3%) in dogs tested in central and northern Tunisia [91]. However, Dirofilaria repens infection was more predominant in dogs from shelters located in southeastern Spain [25] and southern Romania [29]. As for Morocco, the status of these mosquito-borne nematodes is unclear, so regular screening of mosquitoes and dogs for Dirofilaria sp. is still highly recommended to update data and implement an appropriate control plan.

It is well known that Sergentomyia minuta is implicated in the transmission of Leishmania tarentolae (Subgenus: Sauroleishmania), which mainly infects geckoes but can also affect other reptiles, such as lizards [76]. The dog is exposed to Leishmania tarentolae without being a competent reservoir of the infection [76]. The fact that this species feeds on humans highlights its opportunistic behavior, well-illustrated in another study carried out in Italy, in which human DNA was found in 16 blood engorged Sergentomyia minuta [1]. In addition, Leishmania major has been detected in Sergentomyia minuta collected in southern Tunisia, where cutaneous leishmaniasis is endemic [58], as well as being involved in the transmission of Toscana virus in France [28]. Its vectorial capacity is optimized by its abundance in a leishmaniosis endemic area, which corresponds to the location of DS1 in central Morocco, where there are foci of human visceral and cutaneous leishmaniasis [34]. In Morocco, Leishmania tropica is transmitted exclusively by Phlebotomus sergenti, which is responsible for human cutaneous leishmaniasis and is also involved in the canine visceral form [68, 104]. Therefore, it seems that DS3 and DS4 are suitable environments for the emergence of new zymodemes and the spread of the disease on a large scale [90]. On the other hand, Phlebotomus perniciosus and Ph. longicuspis are potential vectors of Leishmania infantum infection, which causes zoonotic visceral leishmaniasis and zoonotic cutaneous leishmaniasis in several Mediterranean countries, including Morocco [104]. At DS1, the simultaneous presence of dogs, which play an epidemiological role as reservoirs of this protozoan, and the plant litter necessary for the development of the larvae of these species maintains the life cycle of the parasite and increases the risk of transmission of the disease, which is a major public health problem [60]. Phlebotomus riouxi can be incriminated as a vector of Leishmania tropica, as reported by Tabbabi et al. [98] in southeast Tunisia. The anthropophilic behavior of Phlebotomus alexandri, which prefers the peri-urban environment to feed on humans, may explain its abundance at DS3, and it has been suspected that it is involved in the life cycle of Leishmania infantum [30], suggesting its coexistence with L. tropica, which may contribute to the spread of infections and the appearance of new foci.

In summary, this descriptive study focused on entomological investigations of the arthropod fauna at four dog shelters in central Morocco, which determined the diversity, abundance, and composition of Culicoides (Diptera: Ceratopogonidae), mosquitoes (Diptera: Culicidae), and sand flies (Diptera: Psychodidae), with the aim of discussing their vectorial roles and assessing the risk of these shelters as zoonotic diseases foci. The high abundance of several potential vector species increases the risk of the circulation of many vector-borne pathogens, including those of zoonotic interest in Morocco, namely West Nile virus, Dirofilaria immitis, and D. repens transmitted by Culex pipiens, Leishmania infantum transmitted by the bites of infected Phlebotomus perniciosus and Ph. longicuspis, and L. tropica spread by infected Ph. sergenti. As a result, regular monitoring of vector-borne pathogens in dog shelters as well as arthropod fauna is strongly needed, to obtain sufficient data to set up surveillance and control systems for the risks assessed.

Acknowledgments

The authors sincerely thank the staff of the four dog shelters (Mehdi, Noureddine, Brahim, Hamid, Issam, and Azzedine) for their valuable help and collaboration in carrying out this study.

Conflicts of interest

No competing interests to be declared by the authors of this work.

Appendix

Protocol used for the preparation of RNAlater-like solution (1.5 Litres)

  1. In a beaker, combine: 935 mL MilliQ H2O, 40 mL of 0.5M EDTA, 25 mL of 1M sodium citrate trisodium salt dihydrate, and 700 g of ammonium sulfate.

  2. Stir on a hot plate stirrer on low heat until the ammonium sulfate is completely dissolved.

  3. Allow to cool, adjust the pH of the solution to pH 5.2 using 1M H2SO4.

  4. Transfer to a screw top bottle and store at room temperature.

Final concentrations:

  • 25 mM sodium citrate trisodium salt dihydrate

  • 10 mM EDTA

  • 70% (w/v) ammonium sulfate

  • pH 5.2

References

  1. Abbate JM, Maia C, Pereira A, Arfuso F, Gaglio G, Rizzo M, Caracappa G, Morino G, Pollmeier M, Gianetto S, Brianti E. 2020. Identification of trypanosomatids and blood feeding preferences of phlebotomine sand fly species common in Sicily, Southern Italy. PLoS One, 15(3), e0229536. [CrossRef] [PubMed] [Google Scholar]
  2. Arich S, Assaid N, Weill M, Tmimi FZ, Taki H, Sarih M, Labbé P. 2024. Human activities and densities shape insecticide resistance distribution and dynamics in the virus-vector Culex pipiens mosquitoes from Morocco. Parasites & Vectors, 17(1), 72. [CrossRef] [PubMed] [Google Scholar]
  3. Assaid N, Mousson L, Moutailler S, Arich S, Akarid K, Monier M, Beck C, Lecollinet S, Failloux AB, Sarih M. 2020. Evidence of circulation of West Nile virus in Culex pipiens mosquitoes and horses in Morocco. Acta Tropica, 205, 105414. [CrossRef] [PubMed] [Google Scholar]
  4. Barceló C, Purse BV, Estrada R, Lucientes J, Miranda MÁ, Searle KR. 2021. Environmental drivers of adult seasonality and abundance of biting midges Culicoides (Diptera: Ceratopogonidae), bluetongue vector species in Spain. Journal of Medical Entomology, 58(1), 350–364. [PubMed] [Google Scholar]
  5. Baylis M, El Hasnaoui H, Bouayoune H, Touti J, Mellor PS. 1997. The spatial and seasonal distribution of African horse sickness and its potential Culicoides vectors in Morocco. Medical and Veterinary Entomology, 11(3), 203–212. [CrossRef] [PubMed] [Google Scholar]
  6. Baylis M, Bouayoune H, Touti J, El Hasnaoui H. 1998. Use of climatic data and satellite imagery to model the abundance of Culicoides imicola, the vector of African horse sickness virus in Morocco. Medical and Veterinary Entomology, 12(3), 255–266. [CrossRef] [PubMed] [Google Scholar]
  7. Becker N, Petric D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A. 2010. Mosquitoes and their control, 2nd edn. Springer: Heidelberg. [CrossRef] [Google Scholar]
  8. Benallal KE, Garni R, Harrat Z, Volf P, Dvorak V. 2022. Phlebotomine sand flies (Diptera: Psychodidae) of the Maghreb region: A systematic review of distribution, morphology, and role in the transmission of the pathogens. PLoS Neglected Tropical Diseases, 16(1), e0009952. [CrossRef] [PubMed] [Google Scholar]
  9. Benelli G, Buttazzoni L, Canale A, D’Andrea A, Del Serrone P, Delrio G, Foxi C, Mariani S, Savini G, Vadivalagan C, Murugan K, Toniolo C, Nicoletti M, Serafini M. 2017. Bluetongue outbreaks: looking for effective control strategies against Culicoides vectors. Research in Veterinary Science, 115, 263–270. [CrossRef] [PubMed] [Google Scholar]
  10. Benjelloun A, El Harrak M, Belkadi B. 2016. West Nile disease epidemiology in North-West Africa: Bibliographical review. Transboundary and Emerging Diseases, 63(6), 153–159. [Google Scholar]
  11. Ben-Mostafa KK, Savini G, Di Gennaro A, Teodori L, Leone A, Monaco F, Alaoqib MMA, Rayes AA, Dayhum A, Eldaghayes I. 2023. Evidence of West Nile virus circulation in horses and dogs in Libya. Pathogens, 13(1), 1–13. [CrossRef] [PubMed] [Google Scholar]
  12. Boudebouch N, Sarih M, Socolovschi C, Amarouch H, Hassar M, Raoult D, Parola P. 2009. Molecular survey for spotted fever group rickettsiae in ticks from Morocco. Clinical Microbiology and Infection, 15, 259–260. [CrossRef] [PubMed] [Google Scholar]
  13. Bourquia M. 2019. Déterminants environnementaux de la distribution des Culicoides (Diptera : Ceratopogonidae), moucherons vecteurs de virus d’animaux d’intérêt économique, au Maroc. Ph.D. thesis. IAV Hassan II, Morocco and Montpellier Sup Agro: France. [Google Scholar]
  14. Bourquia M, Garros C, Rakotoarivony I, Gardès L, Huber K, Boukhari I, Delécolle JC, Baldet T, Mignotte A, Lhor Y, Khallaayoune K, Balenghien T. 2019. Update of the species checklist of Culicoides Latreille, 1809 biting midges (Diptera: Ceratopogonidae) of Morocco. Parasites & Vectors, 12(1), 459. [CrossRef] [PubMed] [Google Scholar]
  15. Bourquia M, Garros G, Rakotoarivony I, Boukhari I, Chakrani M, Huber K, Gardes L, Wint W, Baldet T, Khallaayoune K, Balenghien T. 2020. Composition and seasonality of Culicoides in three host environments in Rabat region (Morocco). Revue d’Élevage et de Médecine Vétérinaire des Pays Tropicaux, 73(1), 37–46. [Google Scholar]
  16. Boussaa S, Boumezzough A, Sibold B, Alves-Pires C, Marquez FM, Glasser N, Pesson B. 2009. Phlebotomine sandflies (Diptera: Psychodidae) of the genus Sergentomyia in Marrakech region, Morocco. Parasitology Research, 104(5), 1027–1033. [CrossRef] [PubMed] [Google Scholar]
  17. Boussaa S, Guernaoui S, Pesson B, Boumezzough A. 2005. Seasonal fluctuations of phlebotomine sand fly populations (Diptera: Psychodidae) in the urban area of Marrakech, Morocco. Acta Tropica, 95(2), 86–91. [CrossRef] [PubMed] [Google Scholar]
  18. Braverman Y. 1974. Breeding sites of some Culicoides species (Diptera, Ceratopogonidae) in Israel. Mosquito News, 34(3), 303–308. [Google Scholar]
  19. Braverman Y, Chizov-Ginzburg A. 1996. Role of dogs (Canis domesticus) as hosts for African horse sickness virus. Veterinary Microbiology, 51(1–2), 19–25. [CrossRef] [PubMed] [Google Scholar]
  20. Bravo-Barriga D, Gomes B, Almeida APG, Serrano-Aguilera FJ, Pérez-Martín JE, Calero-Bernal R, Reina D, Frontera E, Pinto J. 2017. The mosquito fauna of the western region of Spain with emphasis on ecological factors and the characterization of Culex pipiens forms. Journal of Vector Ecology, 42(1), 136–147. [CrossRef] [PubMed] [Google Scholar]
  21. Bravo-Barriga D, Parreira R, Almeida APG, Calado M, Blanco-Ciudad J, Serrano-Aguilera FJ, Pérez-Martín JE, Sánchez-Peinado J, Pinto J, Reina D, Frontera E. 2016. Culex pipiens as a potential vector for transmission of Dirofilaria immitis and other unclassified Filarioidea in Southwest Spain. Veterinary Parasitology, 223, 173–180. [CrossRef] [PubMed] [Google Scholar]
  22. Camacho-Sanchez M, Burraco P, Gomez-Mestre I, Leonard JA. 2013. Preservation of RNA and DNA from mammal samples under field conditions. Molecular Ecology Resources, 13(4), 663–673. [CrossRef] [PubMed] [Google Scholar]
  23. Camp JV, Nowotny N. 2020. The knowns and unknowns of West Nile virus in Europe: what did we learn from the 2018 outbreak? Expert Review of Anti-Infective Therapy, 18(2), 145–154. [CrossRef] [PubMed] [Google Scholar]
  24. Cancrini G, Scaramozzino P, Gabrielli S, Di Paolo M, Toma L, Romi R. 2007. Aedes albopictus and Culex pipiens implicated as natural vectors of Dirofilaria repens in central Italy. Journal of Medical Entomology, 44(6), 1064–1066. [PubMed] [Google Scholar]
  25. Cancrini G, Allende E, Favia G, Bornay F, Antón F, Simón F. 2000. Canine dirofilariosis in two cities of southeastern Spain. Veterinary Parasitology, 92(1), 81–86. [CrossRef] [PubMed] [Google Scholar]
  26. Carpenter S, Groschup MH, Garros C, Felippe-Bauer ML, Purse BV. 2013. Culicoides biting midges, arboviruses and public health in Europe. Antiviral Research, 100(1), 102–113. [Google Scholar]
  27. Castillo-Olivares J. 2021. African horse sickness in Thailand: Challenges of controlling an outbreak by vaccination. Equine Veterinary Journal, 53(1), 9–14. [CrossRef] [PubMed] [Google Scholar]
  28. Charrel RN, Izri A, Temmam S, De Lamballerie X, Parola P. 2006. Toscana virus RNA in Sergentomyia minuta flies. Emerging Infectious Diseases, 12(8), 1299–1300. [CrossRef] [PubMed] [Google Scholar]
  29. Cimpan AA, Baneth G, Nachum-Biala Y, Miron L, Rojas A. 2022. Dirofilaria repens predominates in shelter dogs from South Romania. Comparative Immunology, Microbiology and Infectious Diseases, 84, 101793. [CrossRef] [PubMed] [Google Scholar]
  30. Colacicco-Mayhugh MG, Masuoka PM, Grieco JP. 2010. Ecological niche model of Phlebotomus alexandri and P. papatasi (Diptera: Psychodidae) in the Middle East. International Journal of Health Geographics, 9, 2. [CrossRef] [PubMed] [Google Scholar]
  31. Conceição PA, Crainey JL, Almeida TP, Shelley AJ, Luz SLB. 2013. New molecular identifiers for Simulium limbatum and Simulium incrustatum s.l. and the detection of genetic substructure with potential implications for onchocerciasis epidemiology in the Amazonia focus of Brazil. Acta Tropica, 127(2), 118–125. [CrossRef] [PubMed] [Google Scholar]
  32. Conte A, Goffredo M, Ippoliti C, Meiswinkel R. 2007. Influence of biotic and abiotic factors on the distribution and abundance of Culicoides imicola and the Obsoletus complex in Italy. Veterinary Parasitology, 150(4), 333–344. [CrossRef] [PubMed] [Google Scholar]
  33. Daif S, El Berbri I, Lhor Y, Fassi Fihri O. 2022. Serological and molecular prevalence study of bluetongue virus in small domestic ruminants in Morocco. Scientific Reports, 12(1), 19448. [CrossRef] [PubMed] [Google Scholar]
  34. Daoudi MM, Boussaa S, Boumezzough A. 2020. Modeling spatial distribution of Sergentomyia minuta (Diptera: Psychodidae) and its potential implication in leishmaniasis transmission in Morocco. Journal of Arthropod-Borne Diseases, 14(1), 17–28. [PubMed] [Google Scholar]
  35. Delécolle JC. 1985. Nouvelle contribution à l’étude systématique et iconographique des espèces du genre Culicoides (Diptera: Ceratopogonidae) du Nord-Est de la France, Ph.D. Thesis, Université Louis Pasteur de Strasbourg, UFR sciences de la vie et de la terre: France. [Google Scholar]
  36. Degaetano AT. 2005. Meteorological effects on adult mosquito (Culex) populations in metropolitan New Jersey. International Journal of Biometeorology, 49(5), 345–353. [CrossRef] [PubMed] [Google Scholar]
  37. Diarra M, Fall M, Lancelot R, Diop A, Fall AG, Dicko A, Seck MT, Garros C, Allène X, Rakotoarivony I, Bakhoum MT, Bouyer J, Guis H. 2015. Modelling the abundances of two major Culicoides (Diptera: Ceratopogonidae) species in the Niayes area of Senegal. PloS One, 10(6), e0131021. [CrossRef] [PubMed] [Google Scholar]
  38. Durand B, Haskouri H, Lowenski S, Vachiery N, Beck C, Lecollinet S. 2016. Seroprevalence of West Nile and Usutu viruses in military working horses and dogs, Morocco, 2012: dog as an alternative WNV sentinel species? Epidemiology and Infection, 144(9), 1857–1864. [CrossRef] [PubMed] [Google Scholar]
  39. El Hamiani Khatat S, Daminet S, Kachani M, Leutenegger CM, Duchateau L, El Amri H, Hing M, Azrib R, Sahibi H. 2017. Anaplasma spp. in dogs and owners in north-western Morocco. Parasites & Vectors, 10(1), 202. [CrossRef] [PubMed] [Google Scholar]
  40. El-Mouhdi K, Boussaa S, Chahlaoui A, Fekhaoui M. 2022. Prevalence and risk factors of canine leishmaniasis in Morocco: a systematic review and meta-analysis. Journal of Parasitic Diseases, 46(4), 967–987. [CrossRef] [PubMed] [Google Scholar]
  41. El Rhaffouli H, Lahlou-Amine I, Loutfi C, Laraqui A, Bajjou T, Fassi-Fihri O, El Harrak M. 2013. Serological evidence of West Nile virus infection among humans in the Southern Provinces of Morocco. Journal of Infection in Developing Countries, 7(12), 999–1002. [CrossRef] [PubMed] [Google Scholar]
  42. Estrada R, Carmona VJ, Alarcón-Élbal PM, Miranda MA, Borrás D, Roche ML, Tamarit A, Navarro J, Lucientes J. 2011. Primera cita de Culicoides paolae Boorman, 1996 (Diptera, Ceratopogonidae) para la península Ibérica y aportaciones sobre su distribución. Boletín de la Sociedad Entomológica Aragonesa, 49, 217–221. [Google Scholar]
  43. Failloux AB, Bouattour A, Faraj C, Gunay F, Haddad N, Harrat Z, Jancheska E, Kanani K, Kenawy MA, Kota M, Pajovic I, Paronyan L, Petric D, Sarih M, Sawalha S, Shaibi T, Sherifi K, Sulesco T, Velo E, Gaayeb L, Victoir K, Robert V. 2017. Surveillance of arthropod-borne viruses and their vectors in the Mediterranean and Black Sea regions within the MediLabSecure Network. Current Tropical Medicine Reports, 4(1), 27–39. [CrossRef] [PubMed] [Google Scholar]
  44. Filali Mouatassem T, Faraj C, Guemmouh R, Rais N, El Ouali Lalami A. 2019. Quantitative inventory of mosquito larvae (Diptera: Culicidae) and physicochemical analysis of aquatic habitats in the region of Fez, Morocco. Bulletin de la Société de Pathologie Exotique, 112(2), 105–113. [Google Scholar]
  45. Foxi C, Meloni G, Puggioni G, Manunta D, Rocchigiani A, Vento L, Cabras P, Satta G. 2019. Bluetongue virus detection in new Culicoides species in Sardinia, Italy. Veterinary Record, 184(20), 621. [CrossRef] [PubMed] [Google Scholar]
  46. Foxi C, Pinna M, Monteys VS, Delrio G. 2011. An updated checklist of the Culicoides Latreille (Diptera: Ceratopogonidae) of Sardinia (Italy), and seasonality in proven and potential vectors for bluetongue virus (BTV). Proceedings of the Entomological Society of Washington, 113(4), 403–416. [CrossRef] [Google Scholar]
  47. Foxi C, Delrio G, Falchi G, Marche MG, Satta G, Ruiu L. 2016. Role of different Culicoides vectors (Diptera: Ceratopogonidae) in bluetongue virus transmission and overwintering in Sardinia (Italy). Parasites & Vectors, 9(1), 440. [Google Scholar]
  48. Gainor EM, Harris E, LaBeaud AD. 2022. Uncovering the burden of dengue in Africa: considerations on magnitude, misdiagnosis, and ancestry. Viruses, 14(2), 233. [CrossRef] [PubMed] [Google Scholar]
  49. Gálvez R, Descalzo MA, Miró G, Jiménez MI, Martín O, Dos Santos-Brandao F, Guerrero I, Cubero E, Molina R. 2010. Seasonal trends and spatial relations between environmental/meteorological factors and leishmaniasis sand fly vector abundances in Central Spain. Acta Tropica, 115(1–2), 95–102. [CrossRef] [PubMed] [Google Scholar]
  50. Goffredo M, Buttigieg M, Meiswinkel R, Delécolle JC, Chircop S. 2004. Entomological surveillance for bluetongue on Malta: first report of Culicoides imicola Kieffer. Veterinaria Italiana, 40(3), 278–281. [PubMed] [Google Scholar]
  51. González MA, Goiri F, Barandika JF, García-Pérez AL. 2021. Culicoides biting midges and mosquito fauna at three dog and cat shelters in rural and periurban areas in Northern Spain. Medical and Veterinary Entomology, 35(1), 79–87. [CrossRef] [PubMed] [Google Scholar]
  52. Guernaoui S, Pesson B, Boumezzough A, Pichon G. 2005. Distribution of phlebotomine sand flies, of the subgenus Larroussius, Morocco. Medical and Veterinary Entomology, 19(1), 111–115. [CrossRef] [PubMed] [Google Scholar]
  53. Guessous-Idrissi N, Chiheb S, Hamdani A, Riyad M, Bichichi M, Hamdani S, Krimech A. 1997. Cutaneous leishmaniasis: an emerging epidemic focus of Leishmania tropica in north Morocco. Transactions of the Royal Society of Tropical Medicine and Hygiene, 91(6), 660–663. [CrossRef] [PubMed] [Google Scholar]
  54. Guernaoui S, Boumezzough A, Pesson B, Pichon G. 2005. Entomological investigations in Chichaoua: an emerging epidemic focus of cutaneous leishmaniasis in Morocco. Journal of Medical Entomology, 42(4), 697–701. [CrossRef] [PubMed] [Google Scholar]
  55. Hammami S, Bouzid M, Hammou F, Fakhfakh E, Delécolle JC. 2008. Occurrence of Culicoides spp. (Diptera: Ceratopogonidae) in Tunisia, with emphasis on the bluetongue vector Culicoides imicola. Parasite, 15(2), 179–181. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  56. Hanekom J, Hoepner SN, Du Preez K, Leisewitz A. 2022. The clinical presentation and management of a naturally occurring bluetongue virus infection in a pregnant Rottweiler dog. Journal of the South African Veterinary Association, 93(2), 151–155. [CrossRef] [PubMed] [Google Scholar]
  57. Hazelrig CM, Gettings JR, Cleveland CA, Varela-Stokes A, Majewska AA, Hubbard K, Burton KW, Yabsley MJ. 2023. Spatial and risk factor analyses of vector-borne pathogens among shelter dogs in the Eastern United States. Parasites & Vectors, 16(1), 197. [CrossRef] [PubMed] [Google Scholar]
  58. Jaouadi K, Ghawar W, Salem S, Gharbi M, Bettaieb J, Yazidi R, Harrabi M, Hamarsheh O, Ben Saleh A. 2015. First report of naturally infected Sergentomyia minuta with Leishmania major in Tunisia. Parasites & Vectors, 8, 649. [CrossRef] [PubMed] [Google Scholar]
  59. Kahime K, Boussaa S, El Mzabi A, Boumezzough A. 2015. Spatial relations among environmental factors and phlebotomine sand fly populations (Diptera: Psychodidae) in central and southern Morocco. Journal of Vector Ecology, 40(2), 342–354. [CrossRef] [PubMed] [Google Scholar]
  60. Kahime K, Boussaa S, Ouanaimi F, Boumezzough A. 2015. Species composition of phlebotomine sand fly fauna in an area with sporadic cases of Leishmania infantum human visceral leishmaniasis, Morocco. Acta Tropica, 148, 58–65. [CrossRef] [PubMed] [Google Scholar]
  61. Kalluri S, Gilruth P, Rogers D, Szczur M. 2007. Surveillance of arthropod vector-borne infectious diseases using remote sensing techniques: A review. PLoS Pathogens, 3(10), 1361–1371. [Google Scholar]
  62. Knols BG, Takken W. 2007. Alarm bells ringing: more of the same, and new and novel diseases and pests, in Emerging Pests and Vector-Borne Diseases in Europe. Takken W, Knols BGJ, Editors. Wageningen Academic Publishers: The Netherlands. p. 13–19. [CrossRef] [Google Scholar]
  63. Koenraadt CJ, Balenghien T, Carpenter S, Ducheyne E, Elbers AR, Fife M, Garros C, Ibáñez-Justicia A, Kampen H, Kormelink RJ, Losson B, Van der Poel WH, De Regge N, Van Rijn PA, Sanders C, Schaffner F, Van Oldruitenborgh-Oosterbaan MMS, Takken W, Werner D, Seelig F. 2014. Bluetongue, Schmallenberg – what is next? Culicoides-borne viral diseases in the 21st century. BMC Veterinary Research, 10, 77. [CrossRef] [PubMed] [Google Scholar]
  64. Kumar A, Saurabh S, Jamil S, Kumar V. 2020. Intensely clustered outbreak of visceral leishmaniasis (kala-azar) in a setting of seasonal migration in a village of Bihar, India. BMC Infectious Diseases, 20, 10. [CrossRef] [PubMed] [Google Scholar]
  65. Lahouiti K, El Ouali Lalami A, Maniar S, Bekhti K. 2013. Seasonal fluctuations of phlebotomines sand fly populations (Diptera: Psychodidae) in the Moulay Yacoub province, centre Morocco: Effect of ecological factors. African Journal of Environmental Science and Technology, 7(11), 1028–1036. [Google Scholar]
  66. Laidoudi Y, Durand G, Watier-Grillot S, Dessimoulie AS, Labarde C, Normand T, Andréo V, Guérin P, Grard G, Davoust B. 2023. Evidence of antibodies against the West Nile virus and the Usutu virus in dogs and horses from the Southeast of France. Transboundary and Emerging Diseases, 2023, 1–8. [CrossRef] [Google Scholar]
  67. Latrofa MS, Iatta R, Dantas-Torres F, Annoscia G, Gabrielli S, Pombi M, Gradoni L, Otranto D. 2018. Detection of Leishmania infantum DNA in phlebotomine sand flies from an area where canine leishmaniosis is endemic in southern Italy. Veterinary Parasitology, 253, 39–42. [CrossRef] [PubMed] [Google Scholar]
  68. Lemrani M, Nejjar R, Pratlong F. 2002. A new Leishmania tropica zymodeme – causative agent of canine visceral leishmaniasis in northern Morocco. Annals of Tropical Medicine and Parasitology, 96(6), 637–638. [CrossRef] [PubMed] [Google Scholar]
  69. Lhor Y, Khayli M, Bouslikhane M, El Harrak M, Fassi-Fihri O. 2015. Spatial and seasonal distribution of Culicoides species in Morocco in relation to the transmission of bluetongue viruses. British Journal of Virology, 2(6), 88–95. [CrossRef] [Google Scholar]
  70. Lhor Y, Kyriaki N, Khayli M, Bouslikhane M, Fassi Fihri O, El Harrak M. 2017. Bluetongue in Morocco 2004 to 2015: An overview. Journal of Infectious Diseases and Epidemiology, 3(1), 23. [Google Scholar]
  71. Madeira S, Bernardino R, Osório HC, Boinas F. 2024. Mosquito (Diptera: Culicidae) fauna of a zoological park in an urban setting: Analysis of Culex pipiens s.l. and their biotypes. Insects, 15(1), 45. [CrossRef] [PubMed] [Google Scholar]
  72. Mark I, Chibani A, Al Emad A, Alkhali AA, Belala A, Hadji M, Belghyti D, El Kharrim K. 2016. Étude écologique et entomologique des Culicides larvaires des gites de la province de Kenitra (Maroc). European Journal of Scientific Research, 12(32), 1857–7881. [Google Scholar]
  73. Mathieu B, Cêtre-Sossah C, Garros C, Chavernac D, Balenghien T, Carpenter S, Setier-Rio ML, Vignes-Lebbe R, Ung V, Candolfi E, Delécolle JC. 2012. Development and validation of IIKC: an interactive identification key for Culicoides (Diptera: Ceratopogonidae) females from the Western Palaearctic region. Parasites & Vectors, 5, 137. [CrossRef] [PubMed] [Google Scholar]
  74. Meiswinkel R, Gomulski LM, Delécolle JC, Goffredo M, Gasperi G. 2004. The taxonomy of Culicoides vector complexes – unfinished business. Veterinaria Italiana, 40(3), 151–159. [PubMed] [Google Scholar]
  75. Mélanie G, Pichard C, Restrepo J, Lavergne A, Perez L, Enfissi A, Abboud P, Lambert Y, Ma L, Manot M, Demar M, Djossou F, Servas V, Nacher M, Andrieu A, Prudhomme J, Michaud C, Rousseau C, Jeanne I, Duchemin JB, Epelboin L, Rousset D. 2021. Outbreak of Oropouche virus in French Guiana. Emerging Infectious Diseases, 27(10), 2711–2714. [CrossRef] [PubMed] [Google Scholar]
  76. Mendoza-Roldan JA, Latrofa MS, Iatta R, Manoj RS, Panarese R, Annoscia G, Pombi M, Zatelli A, Beugnet F, Otranto D. 2021. Detection of Leishmania tarentolae in lizards, sand flies and dogs in southern Italy, where Leishmania infantum is endemic: hindrances and opportunities. Parasites & Vectors, 14(1), 461. [CrossRef] [PubMed] [Google Scholar]
  77. Mendoza-Roldan JA, Gabrielli S, Cascio A, Manoj RRS, Bezerra-Santos MA, Benelli G, Brianti E, Latrofa MS, Otranto D. 2021. Zoonotic Dirofilaria immitis and Dirofilaria repens infection in humans and an integrative approach to the diagnosis. Acta Tropica, 223, 106083. [CrossRef] [PubMed] [Google Scholar]
  78. Mezenev NP. 1990. Blood-sucking punkies (Ceratopogonidae) in north central Siberia. Parazitologiia, 24(1), 28–36 (in Russian). [PubMed] [Google Scholar]
  79. Murray KO, Mertens E, Despres P. 2010. West Nile virus and its emergence in the United States of America. Veterinary Research, 41(6), 67. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  80. Napoli E, Panarese R, La Russa F, Cambera I, Mendoza-Roldan JA, Otranto D, Brianti E. 2022. Detection of Dirofilaria DNA and host blood - meal identification in Culicoides paolae biting – midges. Parasitology, 31, 1–17. [Google Scholar]
  81. Ormerod EJ, Edney ATB, Foster SJ, Whyham MC. 2005. Therapeutic applications of the human-companion animal bond. Veterinary Record, 157(22), 689–691. [CrossRef] [PubMed] [Google Scholar]
  82. Ortega MD, Holbrook FR, Lloyd JE. 1999. Seasonal distribution and relationship to temperature and precipitation of the most abundant species of Culicoides in five provinces of Andalusia, Spain. Journal of the American Mosquito Control Association, 15(3), 391–399. [PubMed] [Google Scholar]
  83. Ostyn B, Uranw S, Bhattarai NR, Das ML, Rai K, Tersago K, Pokhrel Y, Durnez L, Marasini B, Van der Auwera G, Dujardin JC, Coosemans M, Argaw D, Boelaert M, Rijal S. 2015. Transmission of Leishmania donovani in the hills of Eastern Nepal, an outbreak investigation in Okhaldhunga and Bhojpur districts. PLoS Neglected Tropical Diseases, 9(8), e0003966. [CrossRef] [PubMed] [Google Scholar]
  84. Otranto D, Dantas-Torres F, Breitschwerdt EB. 2009. Managing canine vector-borne diseases of zoonotic concern: part one. Trends in Parasitology, 25(4), 157–163. [CrossRef] [PubMed] [Google Scholar]
  85. Otranto D, Dantas-Torres F, De Caprariis D, Di Paola G, Tarallo VD, Latrofa MS, Lia RP, Annoscia G, Breitshwerdt EB, Cantacessi C, Capelli G, Stanneck D. 2013. Prevention of canine leishmaniosis in a hyper-endemic area using a combination of 10% imidacloprid/4.5% flumethrin. PLoS One, 8(2), e56374. [CrossRef] [PubMed] [Google Scholar]
  86. Oura CAL, Sebbar G, Loutfi C, Fassi-Fehri O, Touil N, El Harrak M. 2014. No evidence for replication of a field strain of bluetongue virus serotype 1 in the blood of domestic dogs. Research in Veterinary Science, 96(1), 217–219. [CrossRef] [PubMed] [Google Scholar]
  87. Oura CAL, El Harrak M. 2011. Midge – transmitted bluetongue in domestic dogs. Epidemiology and Infection, 139(9), 1396–1400. [CrossRef] [PubMed] [Google Scholar]
  88. Pandey VS, Dakkak A, Elmamoune M. 1987. Parasites of stray dogs in the Rabat region, Morocco. Annals of Tropical Medicine and Parasitology, 81(1), 53–55. [CrossRef] [PubMed] [Google Scholar]
  89. R Core Team. 2022. R: a language and environment for statistical computing [Internet]. R Foundation for Statistical Computing: Vienna, Austria. Available from: https://www.R-project.org/. [Google Scholar]
  90. Rhajaoui M, Fellah H, Pratlong F, Dedet JP, Lyagoubi M. 2004. Leishmaniasis due to Leishmania tropica Mon – 102 in a new Moroccan focus. Transactions of the Royal Society of Tropical Medicine and Hygiene, 98(5), 299–301. [CrossRef] [PubMed] [Google Scholar]
  91. Rjeibi M, Rouatbi M, Mabrouk M, Tabib I, Rekik M, Gharbi M. 2017. Molecular study of Dirofilaria immitis and Dirofilaria repens in dogs from Tunisia. Transboundary and Emerging Diseases, 64(5), 1505–1509. [CrossRef] [PubMed] [Google Scholar]
  92. Rosà R, Marini G, Bolzoni L, Neteler M, Metz M, Delucchi L, Chadwick EA, Balbo L, Mosca A, Giacobini M, Bertolotti L, Rizzoli A. 2014. Early warning of West Nile virus mosquito vector: climate and land use models successfully explain phenology and abundance of Culex pipiens mosquitoes in north-western Italy. Parasites & Vectors, 7, 269. [CrossRef] [PubMed] [Google Scholar]
  93. Savini G, Afonso A, Mellor P, Aradaib I, Yadin H, Sanaa M, Wilson W, Monaco F, Domingo M. 2011. Epizootic Heamorragic Disease. Research in Veterinary Science, 91(1), 1–17. [CrossRef] [PubMed] [Google Scholar]
  94. Sarih M, Jouda F, Gern L, Postic D. 2003. First isolation of Borrelia burgdorferi sensu lato from Ixodes ricinus ticks in Morocco. Vector Borne and Zoonotic Diseases, 3(3), 133–139. [CrossRef] [PubMed] [Google Scholar]
  95. Seng P, Sarih M, Socolovschi C, Boudebouch N, Hassar M, Parola P, Raoult D, Brouqui P. 2009. Detection of Anaplasmataceae in ticks collected in Morocco. Clinical Microbiology and Infection, 15, 86–87. [CrossRef] [PubMed] [Google Scholar]
  96. Sick F, Beer M, Kampen H, Wernike K. 2019. Culicoides biting midges – underestimated vectors for arboviruses of public health and veterinary importance. Viruses, 11(4), 376. [CrossRef] [PubMed] [Google Scholar]
  97. Slama D, Haouas N, Mezhoud H, Babba H, Chaker E. 2015. Blood meal analysis of Culicoides (Diptera: Ceratopogonidae) in central Tunisia. PLoS One, 10(3), e0120528. [CrossRef] [PubMed] [Google Scholar]
  98. Tabbabi A, Ghrab J, Aoun K, Ready PD, Bouratbine A. 2011. Habitats of the sand fly vectors of Leishmania tropica and L. major in a mixed focus of cutaneous leishmaniasis in southeast Tunisia. Acta Tropica, 119(2–3), 131–137. [CrossRef] [PubMed] [Google Scholar]
  99. Talbi FZ, El Ouali Lalami A, Fadil M, Najy M, Ech-Chafay H, Lachhab M, Lotfi S, Nouayti N, Lahouiti K, Faraj C, Idrissi AJ. 2020. Entomological investigations, seasonal fluctuations and impact of bioclimate factors of phlebotomines sand flies (Diptera: Psychodidae) of an emerging focus of cutaneous leishmaniasis in Aichoun Central Morocco. Journal of Parasitology Research, 2020, 6495108. [CrossRef] [Google Scholar]
  100. Tarallo VD, Dantas-Torres F, Lia RP, Otranto D. 2010. Phlebotomine sand fly population dynamics in a leishmaniasis endemic peri-urban area in southern Italy. Acta Tropica, 116(3), 227–234. [CrossRef] [PubMed] [Google Scholar]
  101. Trari B, Dakki M. 2017. Atlas des moustiques (Diptera : Culicidae) du Maroc, distribution, bioécologie et rôle vecteur. Travaux de l’Institut Scientifique, Rabat, Série Zoologie, 51, 128. [Google Scholar]
  102. Uslu U, Dik B. 2007. Description of breeding sites of Culicoides species (Diptera: Ceratopogonidae) in Turkey. Parasite, 14(2), 173–177. [CrossRef] [EDP Sciences] [PubMed] [Google Scholar]
  103. Van Sittert S, Drew TM, Kotze JL, Strydom T, Weyer CT, Guthrie AJ. 2013. Occurrence of African horse sickness in a domestic dog without apparent ingestion of horse meat. Journal of the South African Veterinary Association, 84(1), 1–5. [CrossRef] [Google Scholar]
  104. Zarrouk A, Boussaa S, Belqat B. 2022. Distribution and ecology of phlebotomine sand flies (Diptera: Psychodidae) in endemic and nonendemic area of leishmaniasis in Northern Morocco. Journal of Medical Entomology, 59(6), 2120–2129. [CrossRef] [PubMed] [Google Scholar]

Cite this article as: Zahri A, Ahlamine M, Abou-Elaaz F-Z, Talimi H, El Berbri I, Balenghien T & Bourquia M. 2024. Diversity of biting midges, mosquitoes and sand flies at four dog shelters in rural and peri-urban areas of Central Morocco. Parasite 31, 57.

All Tables

Table 1

Total number, global abundance, rank, sex ratio, and occurrence per dog shelter (C (%)/DS) of collected biting midges (Ceratopogonidae: Culicoides) by UV-light/suction trap (OVI type), from April to November 2022, at four dog shelters (DS) in central Morocco.

In the text
Table 2

Total number, global abundance, rank, sex ratio, and occurrence per dog shelter (C (%)/DS) of caught mosquitoes (Culicidae) by BG-Pro mosquito trap (BGP), from April to November 2022, at four dog shelters (DS) in central Morocco.

In the text
Table 3

Total number, global abundance, rank, sex ratio, and occurrence per dog shelter (C (%)/DS) of trapped sand flies (Psychodidae) by sticky traps, from April to November 2022, at four dog shelters (DS) in central Morocco. Ph: Phlebotomus, Se: Sergentomyia.

In the text
Table 4

Total number and species richness of Culicoides biting midges (Diptera: Ceratopogonidae) at the four dog shelters (DS) studied.

In the text
Table 5

Total number and species diversity of mosquitoes (Diptera: Culicidae) at the four dog shelters (DS) studied.

In the text
Table 6

Total number and species diversity of phlebotomine sand flies (Diptera: Psychodidae) at the four dog shelters (DS) studied.

In the text

All Figures

thumbnail Figure 1

Monthly abundance of blood-sucking arthropods collected at the four dog shelters (DS).
In the text
thumbnail Figure 2

Seasonal variations of the most abundant Culicoides species trapped at DS1 and DS3.
In the text
thumbnail Figure 3

Seasonal variations of the most collected mosquito species caught at DS1.
In the text
thumbnail Figure 4

Seasonal variations of the most prevalent sand fly species collected at DS1, DS3, and DS4.
In the text

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