Health Risks of Simulium ( Boophthora ) erythrocephalum (De Geer, 1776) in the Valencian Autonomous Region, Eastern Spain

The presence and distribution of Simulium erythrocephalum 1776) in the Valencian Autonomous Region is analyzed, an arthropod of medical-sanitary importance due to the marked anthropophilic characteristics exhibited and the tendency to carry out massive attacks. The increasing incidence registered in certain areas as a consequence of their hematophagy, and the meager availability of epidemiological, fauna, bioecological, and distribution data, have led to this study. A field study of 137 samplings was carried out from 2013 to the present in the 14 hydrographic basins of the Valencian Autonomous Region. The study variables were the presence or absence of preimaginal states, environmental and physical-chemical parameters of the water, bite data from the Generalitat Valenciana, population density and incidence of bites by municipality, and geographic location of the population areas. A scarce and reduced presence of the aforementioned species is revealed in the study area. Risk maps of human populations near the detected breeding areas are provided, and the epidemiological interest is discussed due to its vector capacity to transmit pathogens that cause disease. The number of bites registered between 2015, 2016, 2017, and 2018 in the seven health departments involved is provided. The general trend toward an increase in the number of cases is observed year after year, where the highest peaks in the number of cases coincide with the months of June, July, and August, and eventually, September and October. Surveillance and control programs to minimize the problem in the Spanish health system are needed.


Introduction
Black flies (Diptera: Simuliidae) constitute a harmful group of arthropods due to their bites, allergic reactions, and parasitic diseases. In some places, such as Spain, they do not act as disease transmitters, though it is important not to forget their vector role in the transmission of the parasitic agent triggering human onchocerciasis. Climate change and global warming can contribute to the displacement of Simuliidae from their endemic places (Central Africa, South America, Central America, and Yemen) to the European continent. Simulium erythrocephalum (De Geer, 1776) is significant because of its possible action as a vector vehicle and transmitter of disease-causing agents, and because it is a telmophagus insect that lacerates the skin and blood capillaries. from perceiving the pain of the bite, prevent blood clotting and contribute to increased blood flow in the area, facilitating its intake [1][2][3]. These components can cause allergic reactions such as dermatitis (which can persist for several days), poisoning such as simuliotoxicosis [4,5], and even asphyxia due to airway obstruction [6]. This species can cause "Black Fly Fever", a medically recognized syndrome consisting of headache, feverish sweating, chills, swollen lymph glands, joint pain, nausea, lack of energy, laziness, feeling tired and psychological depression [7]. These symptoms are due to the reaction to compounds secreted by the salivary glands [8]. This syndrome can have a significant economic impact due to sick leave, disability compensation, prolonged treatment, hospitalization, and even job loss [7]. The bites of this species can cause intoxication of the blood flow, the symptoms of which consist of accelerated circulation, dyspnea, hyperthermia, hypothermia, nervous disorders and, in extreme cases, death [9].
However, they not only affect man directly but also indirectly, negatively impacting tourist and recreational activities located in rivers and nearby areas, creating economic losses in the tourism sector [1,5]. Therefore, suffering the bites of these Diptera is a brake on the well-being of people and their sources of economic livelihood. Historically, the study of these nematocerous dipterans in Spain was not approached from a health perspective, due to the low significance of their bites in the past. However, from 1995 to the present, the situation has changed considerably. This dipteran is acquiring great relevance in certain regions of the national territory, among which the Valencian Autonomous Region stands out [10,11] where they are colonizing river basins and water channels due to the improvement of the water quality of the rivers, the expansion of the distribution area of plant species used by larvae and pupae as adhesion support, and by the effects on local climatology due to climate change and global warming. All these causes are favoring the increase in simuliid populations, their dispersal, settlement, and colonization in areas where their presence was not perceived in the past. These factors are leading to an exponential increase in the nuisance to human populations close to the breeding, growth, and development areas of the flies. Females of S. erythrocephalum cause discomfort to humans both in Spain [3,[12][13][14][15] and European countries [16][17][18]. The simultaneous hatching of adults raises the population level to the status of a plague, causing outbreaks such as those that occurred in the Danube [7] and Ebro [19,20] rivers.
Indeed, evidence shows that on certain occasions, administrations have had to resort to the mechanical removal of hydrophytes and helophytes from riverbeds manually or with the aid of an amphibious vehicle to reduce the populations of S. erythrocephalum and other hematophagous species. Land and air treatments with formulations based on the use of Bacillus thuringiensis variety israeliensis have been used in areas that required it, such as La Ribera (Figure 1). Of this species, its anthropophilic preference is recognized [18,21], as well as the tendency of females to form swarms and attack in masse [18]. For these reasons, S. erythrocephalum can act as a potential transmitter of Onchocerca volvulus in Europe. In fact, laboratory studies have already shown that it is a competent vector for the transmission of this filaria [22].  processed. Subsequently, taxonomics were identified and classified using dichotomous keys [23,24] and a Leica brand MZ APO stereoscopic microscope assisted with a Leica brand model CLS 100 X cold light source as described in [14,25]. Ultimately, the classified specimens were deposited in the Entomology Collection of the University of Valencia (General Study). Finally, a geographic information system (GIS) was used to prepare the risk map. In addition, note that the bite data provided by the Conselleria de

Results
Of the 137 samplings carried out in the study area, the presence of S. erythrocephalum was verified in four sampling stations. Two were located in the middle (SER1) and upper (SER2) section of the Serpis river, and the other two were in the lower section of the Júcar river basin, one in its tributary the Albaida river (JUR1) and another in the insertion from another of its tributaries, the Magro River (JUR2) (Figure 2). From these breeding areas, and knowing that the flight range of the adults of this species is between 20 and 30 km [7,8,17], three zones of influence were configured around each of the points where the identified species were found.In the maps, a maximum distance of 15 km was considered as the furthest dispersion range. This decision was made considering that some authors confirmed females of the species traveling up to 5 km in search of hosts from which to obtain blood [19]. At greater distances, it is assumed that the females tend to reduce their movements and therefore their bites, although they are capable of traveling greater distances if required (Figure 2). In this manner, three risk zones were delimited around each of the points where the presence of the species was corroborated. The first zone, with a radius of 5 km, is represented in maroon and indicative of high risk; the second, with a 10-km radius, is represented in orange and indicative of medium risk. The third zone, with a 15-km radius, is represented in yellow and indicative of low risk.   Lastly, it is found that the months in which the highest number of cases have been registered coincide with the annual seasons with favorable physicochemical characteristics for the reproduction, development, and growth of this species. The highest peaks are in the months of June, July, and August and, eventually, in September and October (Table 1). However, analyzing the sum of the data for each year, the months in which the most cases were registered were August 2015 and 2016, and July in 2017 and 2018. Although it is still necessary to deepen the study of the bioecology of this species of sanitary importance, the results of this work reveal the need to consider the ethology of this dipteran when implementing surveillance and control plans to reduce its effects on citizen health.

Discussion
The presence of S. erythrocephalum in the studied areas, together with the proximity of urban centers along the indicated river channels, entails an incidence on humans. The incidence of bites has increased in recent years in the Valencian Autonomous Region, which has taken measures to reduce its repercussions [10,11,14]. This same effect is reflected in other areas of Spain, such as the Aragonese Autonomous Region [26]. In this work, the risk areas to which the municipalities are subjected are identified, establishing different ranges based on distances and population densities. In this regard, it is not possible to correlate these data with other data from Spain given the lack of knowledge of it.
In conclusion, and in clear harmony with other authors [16,17,19], it is stated that S. erythrocephalum is one of the simuliid species with the greatest impact on the human population.
Fortunately, its current vector potential in Spain is zero. As a result of all the above, it is necessary to acquire a global and integrative perspective to understand the phenological, ethological, and bioecological dynamics of this species. This knowledge facilitates implementation of both the necessary surveillance strategies and the most effective and appropriate control actions in each case as quickly as possible. In addition, the growing and numerous citizen complaints, as well as the innumerable medical treatments shown in this article and other regions of the national territory [26], should encourage health professionals to develop a greater knowledge of the characteristics of the pathologies due to this dipteran. This awareness correctly prepares health practitioners to face this type of clinical picture when manifested in citizens and helps predict expected areas of higher incidence resulting from living near the aforementioned hematophagus. Increased knowledge allows for discerning between types of bites of various arthropodsmore specifically, insects-identifying whether they are due to mosquitoes, simuliids, or others. In this way, the data collected in the health consultations of citizens due to these hematophagous and anthropophilic organisms would be of higher quality and reliability, thus being able to infer and analyze these data with greater scientific rigor. Finally, it is necessary to inform and educate the population of how this dipteran can impact their daily life.
Finally, simuliid species with obligate hematophagy of biomedical and veterinary importance [27] such as S. erythrocephalum are generalist species regarding the type of habitat in which they develop, Therefore, these species are capable of tolerating a wide range of ecological conditions. Under this premise and given the current climate change scenario in which certain authors and institutions predict a decrease in coldwater river habitats and greater environmental variability [28], it would be expected that the resulting conditions would favor the distribution and colonization of S. erythrocephalum to new geographic areas, increasing its harm to the well-being of citizens. Therefore, it is recommended to deepen the study of the ecological requirements of the breeding places of black fly species that, like S. erythrocephalum, can be considered a plague negatively affecting public health as a consequence of increased temperatures from climate change [29]. In this way, the knowledge of the bioecology of the species will play a crucial role when it comes to implementing treatment plans for preimaginal states, minimizing the sizes of their populations and reducing their incidences in public health. In the case of S. erythrocephalum, it is important to know that it is a species whose preimaginal development optimum is 20°C, tolerates values higher than 25°C, shows a narrow range of altitudinal tolerance with its optimum around 75 meters above sea level (masl), so that its distribution in the Valencian Autonomous Region is restricted to elevations between 5 and 240 masl [27]. Likewise, some authors ecologically described this species as preferring lentic and warm waters typical of the middle and lower sections of rivers [30].
In addition, the results provided offer useful information on the location of S. erythrocephalum, which will help in the development and execution of surveillance and control programs.

Conclusions
Simulium erythrocephalum is one of the main black fly species that threatens public health in Spain. In recent years, there have been frequent events of massive hatchings of this simuliid, whose nutritional habits have serious repercussions on health care systems. For this reason, it has been pertinent to carry out the present study. This work provides relevant information on the distribution of the species, risk areas, population density, and incidence of bites per municipality according to the flight range of adult specimens, which is useful. The results obtained can be implemented by researchers, public health practitioners, and policy makers as well as companies specializing in the control of noxious species to minimize the magnitude of the problem of black fly bites in the Spanish health system.