Geographic Distribution of the Scorpion Fauna in the Central Moroccan Region of Souss-Massa with Potential Implications for Public Health

Despite the medical importance of North African scorpions, many aspects of their ecology which may be important to understand envenoming patterns throughout their range, remain understudied. The region of Souss-Massa in central Morocco exhibits a high incidence of scorpion envenomings, with 29 437 cases reported between 2005 and 2010, resulting in 32 deaths. In the present study, we provide an updated inventory of scorpions occurring throughout the Souss-Massa region, with additional information about their distribution and notes on preferred habitats for each species observed. Sampling was carried out at 39 stations over a three-year period: June and August 2020, April and June 2022, and July and August 2023. Twelve species belonging to two families were recovered over the course of the study. The families Buthidae and Scorpionidae were represented by eleven and a single species respectively. Overall, this represents 71% of all species reported to occur in the Souss-Massa region. Apart from Androctonus mauritanicus, A. bourdoni, A. sergenti and Hottentotta gentili which are present in and around human dwellings, all other species were found in uninhabited areas. Apart from Scorpio mogadorensis, all the species of scorpions we recovered can cause severe envenomation with potentially fatal outcomes. Field-based ecological investigations should be encouraged to gain a more accurate and comprehensive understanding of scorpion distribution patterns and habitat preference. In turn, this will inform the health-science community of the etiological factors responsible for scorpion envenoming.

Each year across the world, 1.2 million scorpion stings are recorded, resulting in the deaths of 3 250 individuals (Chippaux and Goyffon 2008).Ninety percent of these victims are children under the age of 15, mainly from poor rural communities (Semlali et al. 2009;Chippaux 2020).In Morocco, scorpion envenoming represents a medical emergency and is considered a major public health concern, with a high rate of endemism.According to El Oufir (2019), the Poison Control and Pharmacovigilance Center of Morocco reported 26 819 cases of scorpion stings and envenomations, registered in 41 Moroccan provinces in 2019 alone.Stings are especially common during spells of high temperatures, and rank first (30−50% of the total) among all emergencies reported to the Poison Control and Pharmacovigilance Center of Morocco (El Oufir 2016).
The high incidence of scorpion stings can be explained in part by the richness and diversity of the Moroccan scorpion fauna.Located on the Northwestern littoral zone of Africa, Morocco has one of the most diverse assemblages of scorpions in the world with over 60 species recorded, the majority of which belong to the medically significant family Buthidae.In Morocco, at least nine species belonging to either the genera Androctonus or Hottentotta, are known to be potentially lethal (El Hidan et al. 2016;Touloun 2019).
Most cases occur in the central mountainous provinces and the southern valleys of the Massa and Draa rivers.Within these areas, most fatalities occur in a few localised hotspots and are highest in the province of Kelâa Es-Sraghna.According to the Poison Control and Pharmacovigilance Center of Morocco, 29 437 cases were recorded in the Souss-Massa region between 2005 and 2010, resulting in 32 fatalities (El Hidan et al. 2016).
The aim of this study was to highlight the diversity of scorpions, their distribution and their preferred habitats across the Souss-Massa region, and to gain a better understanding of the etiological factors responsible for scorpion stings and envenomations.We present herein an updated inventory of scorpion populations at 39 sampling stations located across the region, and provide Introduction units, from the plains of Souss, Chtouka and Massa on the one hand to the High Atlas and Anti-Atlas Mountains on the other.According to the Higher Planning Commission of Morocco (HCP 2021), the Souss-Massa region consists of two prefectures (Agadir Ida-Outanane and Inzegane Ait Melloul) and four provinces (Chtouka Ait Baha, Taroudant, Tata and Tiznit) (Figure 1), and includes 175 communes (21 urban and 154 rural).According to estimates by the HCP (2021), the population of Souss-Massa comprises 1 881 050 urban and 1 105 380 rural dwellers.

Collection and identification of scorpions
Scorpions were collected in situ using 16 cm stainless steel forceps.Suitable areas were searched by lifting stones, rocks, tree bark and litter.Burrows suspected of being occupied by scorpions were dug with a shovel to try and dislodge them.We included both synanthropic and undisturbed habitats in our searches.Nocturnal searches were conducted using ultraviolet lamps.

Results
A total of 391 scorpions were identified from 39 sampling stations distributed across the two prefectures and four provinces of the Souss-Massa region (Table 2).The family Buthidae was represented by 11 species across four genera (Androctonus, Buthus, Hottentotta and Orthochirus) (Figure 2).The family Scorpionidae was represented by a single species (Scorpio mogadorensis) (Figure 2).

Ecological and biogeographical characteristics of the recovered scorpion fauna Androctonus Ehrenberg, 1828
Androctonus bourdoni Vachon, 1948 We found this species in a single station in the province of Ait Baha (S7; n = 3) (Figure 1).Throughout our investigation,   we noticed the preference of this species for sandy soils with scattered stones, close to human habitations.
Androctonus sergenti Vachon, 1948 Specimens of this species were found at two sampling stations in Tiznit province (S16; n = 4, S17; n = 5) (Figure 1).All specimens were either sheltering under large rocks on clay soils close to human dwellings or inside houses.
In our field investigations we only discovered B. atlantis under rocks and never in deep burrows.

Discussion
The abundance and variety of scorpion species in Morocco can be attributed to the geographic position of Morocco in the Palearctic region, its distinctive geological history, and the country's diverse topography which includes mountain ranges, deserts and coastal areas.These factors have led to the presence of elements from both the Palearctic and Afrotropical fauna, enhancing the richness and diversity of scorpion species in the region.
Our observations showed that A. mauritanicus cohabits with B. atlantis at Rwaiss (S1) in a rock-strewn sandy substrate (Figure 3a).Androctonus mauritanicus was collected in an argan grove at Almaasar (S20), sheltered under the stones below the argan trees and next to traditional adobe houses on a cactus steppe.Androctonus bourdoni was initially described as a subspecies of A. mauritanicus by Vachon (1948) but was recently elevated to species status by Ythier and Lourenço (2022).
It was inventoried at a single station in the study area, Sidi Ouassay (S7), south of Agadir, where it cohabited with B. atlantis on a sandy substrate with scattered stones.Androctonus sergenti, easily recognisable by the punctation on the metasomal tegument, is a mountain species that represents the genus Androctonus and found on the slopes of the Anti-Atlas overlooking the Souss valley (Vachon 1952).We collected it south of Tiznit (S16, S17) in rocky clay soils, in cohabitation with H. gentili and S. mogadorensis.Hottentotta gentili cohabited with B. elmoutaouakili in Sidi Abdellah El Bouchouari (S4) and Bounaamane (S9) in rocky substrates associated with dense vegetation composed of Argania spinosa and Euphorbia echinus (Figure 3c).At Tiwrar (S18) and Amskroud (S19), H. gentili occupied rugged, rocky terrain covered with A. spinosa.Finally, at the Cap Ghir station (S23), H. gentili occupied a coastal habitat composed of rocky substrate and dense vegetation.Androctonus mauritanicus, A. bourdoni, A. sergenti and H. gentili have been found in and around human habitations.Their synanthropic affinities, active nocturnal foraging habits and defensive behaviour, combined with the extreme potency of their venom, make them ideal candidates for severe scorpion envenomation with potentially fatal outcomes.
Buthus elmoutaouakili was found in argan groves, hiding under rocks, in shallow burrows or in deep burrows made by S. mogadorensis (Figure 2e) in areas shared by both species.While this is an interesting observation, it is not clear if it is an example of commensalism or competition.The two species were recorded sympatrically at Tlata Uoanass (S5) and Oued Adoudou (S13).Buthus mardochei is commonly encountered within the argan groves of the Souss plain, where it hides under stones and rarely digs shallow burrows.Buthus parroti was first described as a subspecies of B. atlantis (Pocock, 1889), but was elevated to species status by Sousa et al. (2017).The two species are known to occupy different habitats in western Morocco; B. parroti is a forest species, while B. atlantis prefers sand dunes (Vachon 1952).Our findings corroborate this; we found B. parroti in the argan groves of the Souss-Massa plain hidden in very deep burrows (Figure 2h) and found B. atlantis in coastal regions on sandy or rocky substrate.In addition to stations S1 and S7, we found B. atlantis at Aglou (S10), which extends the species' known range to the southern region of Agadir.Buthus draa was described by Lourenço and Slimani (2004).It can be distinguished from other Buthus scorpions in the region by its dark vesicle and fifth metasomal segment.We observed B. draa cohabiting with H. gentili in the Tata province (S36, S37 and S38) in different types of substrates and just outside human habitations.During our study, Orthochirus innesi was only found in the palm oases of Tata province, hiding among the leaf litter or under stones, and never in areas occupied by B. draa or H. gentili.This could be due to its small size (<3 cm), making it an easy target for these aggressive predators.Scorpio mogadorensis is the only representative of the Scorpio genus in the Souss-Massa region.In this study, this particular species mostly inhabited deep burrows on a soft substrate, generally composed of a mixture of clay and limestone in relatively moist environments such as the banks of wadis, near dams or in coastal areas often associated with clumps of vegetation, especially those of jujube and euphorbia (Figure 2l).
The severity of scorpionism in Morocco is the result of the diversity of Buthidae representatives, mainly from the genera Androctonus, Buthus and Hottentota, all of which possess highly potent neurotoxic venoms (Aboumaâd et al. 2014).These three genera are well represented in the region of Souss-Massa.Androctonus mauritanicus, A. bourdoni, A. sergenti and H. gentili were the scorpions most frequently found in and around human dwellings.This brings them into close contact with humans, and as a result may represent a higher risk of envenoming for local populations, whereas B. elmoutaouakili, B. mardochei, B. parroti, B. atlantis, B. lienhardi, B. draa, O. innesi and S. mogadorensis were most likely to be encountered in wild habitats and isolated agricultural settings.Agricultural workers are most at risk of being stung by these species, all of which but one, S. mogadorensis, can cause severe envenomation.Scorpio mogadorensis is characterised and easily recognised by its robust pincers, indicating its lower venom potency (Forde et al. 2022).While its venom can induce some mild pain, the species is typically regarded as harmless.

Conclusion
This work is a contribution to the study of scorpions present in the Souss-Massa region, and deals with different ecological and biogeographical aspects with potential implications for public health.We recovered twelve species of scorpions over the course of this study: A. mauritanicus, A. bourdoni, A. sergenti, H. gentili, B. elmoutaouakili, B. mardochei, B. parroti, B. atlantis, B. lienhardi, B. draa, O. innesi and S. mogadorensis, and established a distribution map of all of these species.This map has important medical implications, in order to plan an effective strategy for the control of scorpionism in the region.

Figure 1 :
Figure 1: Map of Souss-Massa region showing the localities where scorpions have been collected; insert showing location within Morocco and Africa

Table 2 :
List of scorpion species inventoried in the study area