Introduction

Lice (Phthiraptera) are hemimetabolous insects taxonomically divided into two main morphologically distinct groups: blood-sucking lice (Anoplura) and skin-chewing lice (Mallophaga) (Marcondes 2017; Durden 2019). The bodies of these insects are bilaterally symmetric and dorsoventrally flattened, facilitating their movement through the host’s fur or feathers (Meyer and Madon 2002; Marcondes 2017). Their host and nutrition specificity make them challenging to keep alive once separated from the host (Jassem et al. 2023; Springer et al. 2023). The impact of a lice infestation depends on the species’ aggressivity and the host’s overall health (Ahmed et al. 2009; Gharbi et al. 2013). Light infestations may cause mild discomfort, itching, and irritation. In contrast, heavy infestations can significantly induce anemia, dermatitis, secondary bacterial infections, weight loss, and decreased animal productivity (Al-Saffar and Al-Mawla 2008; Da Silva et al. 2013; Mirzaei et al. 2016; Gharbi et al. 2020; Eren et al. 2022). All these consequences could lead to economic losses for breeders who depend on animal products for sustenance and income (Benelli et al. 2018; Meguini et al. 2018; Muhammad et al. 2021).

In Algeria, animal lice infestations were considered benign entomological epizootic for a long time (Meguini et al. 2018; Ouarti et al. 2020b). This is why there were few surveys on these ectoparasites. The first entomological investigations, dated 2013 and 2014, focused on free-range chicken lice (Medjouel et al. 2013; Medjouel et al. 2014). Since then, lice have aroused very little interest in the Algerian scientific community, and only two studies on nesting birds’ lice were published (Baziz-Neffah et al. 2015; Touati et al. 2015). In early 2018, animal lice started increasing gradually in scope, moving from a sporadic topic to a highly discussed research axe. Studies that followed assessed the diversity of lice species in domestic mammals and farmyard chickens (Meguini et al. 2018), wild boars (Sus scrofa) (Zeroual et al. 2018), and cattle egrets (Bubulcus ibis) (Amina et al. 2018). Later various works investigated lice infestation in wildlife birds such as Miropidae (Torki et al. 2020), the Eurasian coot (Fulica atra) (Ziani et al. 2020), the Common Moorhen (Gallinula chloropus) (Ziani et al. 2021), Passeriformes (Ouarab et al. 2021), migratory and sedentary doves (Absi et al. 2021) and the white stork (Ciconia Ciconia) (Touati et al. 2022). Other works on wild mammal lice have also been published, including those on the common gundi (Ctenodactylus gundi) (Meddour et al. 2022) and the black rats (Rattus rattus) (Randa et al. 2022). Overall, the Algerian studies cited above focused on the lice diversity in wild animals. In contrast, few were interested in domestic ruminants and birds (Saidi et al. 2020; Nahal et al. 2021). Consequently, lit is known about the role of these pests as potential vectors of infectious diseases. Only two Algerian molecular studies have highlighted proof of this possibility (Zeroual et al. 2018; Ouarti et al. 2021). Therefore, it can be assumed that since several sucking or chewing lice species feed on blood, they could serve as reservoirs and vectors of infectious diseases (Aleksandravičienė et al. 2021; Ouarti et al. 2021; Kazim et al. 2022). Indeed, many examples of Anatidae or mammals’ lice species (Ansari 1955) and Amblycera were reported as potential vectors of cestodes and some filaria to swans and geese (Clayton et al. 2008; Hugon 2015; Benelli et al. 2018). Animal lice present a complex challenge for managing livestock and wildlife in Algeria and beyond (Ouarti et al. 2020b). To effectively address this issue, it is crucial, from a cognitive science perspective, to understand the intricacies of how animal lice acquire and probably transmit these pathogenic agents (Promrangsee et al. 2019; Ouarti et al. 2020a).

It will also be necessary to delve into these pests’ morphology, mechanisms to locate and infest the hosts, and how the host’s immune system responds to infestation. Overall, drawing up a checklist of all parasitic animal lice and their associated hosts can provide valuable insights into the evolution of lice parasitic behavior and host-parasite interactions and contribute to stopping the spread and persistence of lice infestations. Nevertheless, developing and implementing sustainable control measures will require a multifaceted approach considering the unique challenges of different host species and their environments.

The current study aimed to assess ruminant and domestic bird lice diversity in northern Algeria and debate their veterinary importance.

Materials and methods

Study areas and period of sampling

During two years, field collections were carried out on domestic birds and ruminants in six regions of northeastern Algeria: El Tarf (36°51’21.5"N, 8°19’34.5"E), Sétif (36°9′0″N, 5°26′0″E), Oum El Bouaghi (35°52′39″N, 7°06′49″E), Guelma (36°28′0″N, 7°26′0″E), Mila (36°27′0″N, 6°16′0″E) and Bordj Bou Arreridj (36°04′00″N, 4°46′00″E) (Fig. 1).

Fig. 1
figure 1

Geographical distribution of ruminants and domestic fowl lice species collected in six regions of northeastern Algeria

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These cattle-breeding zones belong to similar bioclimatic stages: El Tarf and Guelma have a Mediterranean climate with very hot summers, whereas the rest of the regions have a cold, semi-arid environment with warm summer days (Peel et al. 2007). For our study, we looked for ruminant and bird farms in each study region and adapted the fieldwork according to their disponibility.

Animals

Various animal species, including ruminants and domestic fowl, were involved in this study. One cattle farm (Sétif), four sheep farms (El Tarf n = 3 and Sétif n = 1), and eight goat farms (El Tarf n = 5, Guelma n = 1, Sétif n = 1, Oum El Bouaghi n = 1) were randomly chosen and regularly visited. The study was conducted for backyard chickens in three traditional El Tarf region farms, nine from Bordj Bou Arreridj and one from Mila. In addition, one turkey breeding and two groups of pigeons located in El Tarf (Ain El Kerma) were also checked for the presence of lice. The number of animals on each farm is detailed in Tables 1 and 2.

Table 1 Ruminants lice species, sampling regions, hosts, and specimens collected
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Table 2 Domestic birds’ lice species, sampling regions, hosts, and specimens collected
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Lice collection and identification

For birds, the collections were made manually or using entomological grippers by inspecting the entire body of the birds, paying specific attention to the head and feathers of the neck, wings, belly, and tail. When the birds were overly infested, a bioinsecticide powder (based on lavender and geranium essential oils) with no side effects was sprinkled on their bodies. After that, they were placed in a carton box for 30 min (Clayton and Walther 1997). In the case of ruminants, the parasitized sheep’s fleeces were separated or, in some cases, cut with scissors, and the lice were then retrieved from the deepest parts of the wool. The skin was brushed using a stainless-steel lice comb for cattle and goats. All the lice found on each examined animal were collected and directly stored in individual prelabelled Eppendorfs containing 70% ethanol.

The morphological identification of sampled lice was realized at the species level under a Leica® binocular lens with LED light. The dichotomous keys and criteria provided by Tuff (Tuff 1977), Wall (Wall and Shearer 2001), Pajot (Pajot 2000), and Hugon (Hugon 2015) were used for the morphological identification of adult specimens, while nymphal stages were excluded. The nomenclature of the lice species used in this study was chosen based on names provided by earlier investigations and for which there is a scientific consortium (Hopkins and Clay 1953; Barnard 2011; Dik and Halajian 2013; Meguini et al. 2018; Ouarti et al. 2020a). A microscope (Zeiss Axio Zoom.V16, Zeiss, Marly le Roi, France) was used to acquire dorsal and ventral photos of each species at a magnification of x56 (Fig. 2a and Fig. 2b).

Fig. 2
figure 2

Dorsal and ventral photographs of some of the collected lice species x56. a: Bovicola caprae[♀:A, B; ♂ C, D; Nymphe: E]; Bovicola bovis[♀:F, G]; Haematopinus eurysternus[♀:H, I; ♂ J, K; Nymphe: L, M]; Linognathus africanus[♀:N, O; ♂ P, Q]; Lipeurus caponis[♀:R, S]; Columbicola columbae[♀:T, U; ♂ V, W]; Chelopistes meleagridis[♀:X, Y; ♂ Z, Z’]. b: Goniodes dissimilis[♀:1, 2; ♂ 3, 4]; Goniocotes gallinae[♀:5, 6; ♂ 7, 8]; Menacanthus stramineus[♀:9, 10; ♂ 11, 12]; Menopon gallinae[♀:13, 14; ♂ 15, 16]; Campanulotes bidentatus[♀:17, 18; ♂ 19, 20]

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Results

Ruminants and domestic bird’s lice diversity

A total of 4488 lice (1355 from ruminants and 3133 from birds) were collected from more than 184 infested hosts belonging to various animal species. The outcome of the morphological identification summarized in Tables 1 and 2 confirmed the presence of five lice species belonging to three different genera in ruminants and ten species affiliated with nine genera in birds.

Among all infested ruminants, the most common lice were from goats, more particularly, Bovicola caprae (Gurlt, 1843) with 474/1355 (34.98%) collected specimens, followed by Linognathus africanus (Kellogg & Paine, 1911) with 393/1355 (29%) samples. Haematopinus eurysternus (Nitzsch, 1818) was more common in cattle with 314/1355 (23.17%) lice. However, the infestation rates of Bovicola ovis (Schrank, 1781) and Bovicola bovis (Linnaeus, 1758) were only 10.84% and 1.99%, respectively.

In backyard chickens, seven species were sampled. The amblyceran chewing lice Menacanthus stramineus (Nitzsch, 1818) lice were the most frequently collected with 1704/2667 (63.89%) specimens. They were followed by another chewing louses Menopon gallinae (Linnaeus, 1758), with 751/2667 (28.15%) samples. Three other ischnoceran species, including Goniocotes gallinae (de Geer, 1778), Goniodes dissimilis (Denny, 1842), and Goniodes gigas (Taschenberg, 1879), were collected with low abundances of 3.78%, 2.58%, and 1.01%, respectively. We also identified 14 specimens of Lipeurus caponis (Linnaeus, 1758) and only one Cuclotogaster heterographus female (Nitzsch, 1866).

All the examined turkeys were infested with one or two genera. Chelopistes meleagridis (Linnaeus, 1758) was the most common species (66.27%), while Me. stramineus (Nitzsch, 1818) was the second most common (33.72%). Lice infested all the pigeons in both groups. Two species were identified on them: 105/128 (82.03%) Columbicola columbae (Linnaeus, 1758) and 23/128 (17.96%) Campanulotes bidentatus s.l. (Scopoli, 1763).

3.2. Geographical distribution of lice species

During our investigation in El Tarf localities, farms from this region were the most infested with 2365/4488 (52.70%) collected lice belonging to 13 species, followed by those from Mila (three species), Sétif (five species) and Bordj Bou Arreridj (four species). On the other hand, only two goat species (B. caprae and L. Africanus) were identified in Oum EL Bouaghi and Guelma (Fig. 1). The relative abundance of each species according to the sampled region is detailed in Figs. 3 and 4.

Fig. 3
figure 3

Ruminant lice species and infestation rates according to sampling regions

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Fig. 4
figure 4

Domestic fowl lice species and infestation rates according to sampling regions

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Discussion

Lice species have probably always been associated with humans, animals, and their ancestors (Light et al. 2010; Durden 2019; Patel et al. 2021). They have been scattered worldwide through the migrations humans have made during their existence. (Reed et al. 2004; Duvallet et al. 2017). Because of this intimate association between lice and their hosts, these insects showed strong co-speciation and coevolution (Boyd et al. 2017; Sweet et al. 2022). Their origin is still unknown. However, phylogenetic studies suggested that Anoplura and Mallophaga are monophyletic and that all lice derive from a non-hematophagous ancestor that developed its mouthparts to adapt to a hematophagous feeding behavior (Reed et al. 2007; Johnson et al. 2022).

Due to this nutrition mode, the vectorial competence of these arthropods has been highlighted throughout human evolution (Houhamdi et al. 2005; Amanzougaghene et al. 2020). However, this ability to transmit pathogens has often been restricted to some Anoplurans blood-sucking lice species of public health importance, such as Pediculus humanus humanus (Linnaeus, 1758) and P. humanus capitis (Linnaeus, 1758) (Amanzougaghene et al. 2017; Mana et al. 2017; Louni et al. 2018; Boumbanda Koyo et al. 2019).

Although domestic and wild animals have specific lice species, they are seldom considered a significant problem in Algeria. As a result, breeders often ignore them and consider them harmless to their animals. Furthermore, according to previous studies, relatively few of these animal lice species are potential vectors of pathogens (Kumsa et al. 2012; Zeroual et al. 2018; Promrangsee et al. 2019; Ouarti et al. 2021). Instead, the frequently highlighted pathogens in literature were the swinepox virus and the murine Mycoplasma associated with Haematopinus suis (Linnaeus, 1758) and Polyplax spinulosa (Burmeister, 1839) (Hornok et al. 2015; Ramakrishnan and Ashokkumar 2019; Delhon 2022).

In Algeria, less is known about the diversity of sucking and chewing lice and their part in vector-borne disease epidemiology. Several studies were conducted on human lice’s phylogeny and vector competence (Mana et al. 2017; Louni et al. 2018; Ouarti et al. 2022), while few were interested in animal lice (Medjouel et al. 2013; Medjouel et al. 2014; Meguini et al. 2018; Nahal et al. 2021; Ouarab et al. 2021). Therefore, a survey of ruminants’ most prevalent lice species and domestic fowl is imperative to understand host-lice interaction. Furthermore, the detailed findings could update any outdated information regarding the diversity of lice and host records in northeastern Algeria.

During our survey and among 4488 collected specimens, five ruminant and ten fowl lice species were identified. Our results regarding the identified lice species on ruminants and poultry are consistent with those described in previous Algerian studies (Meguini et al. 2018; Nahal et al. 2021; Ouarab et al. 2021). The goat lice B. caprae and the poultry body louse Me. stramineus were the most common lice species. For a long time, the goat-biting louse, B. caprae, was morphologically confused with its close parent, B. limbatus (syn. B. limbata). Ancient studies have even suggested convergent evolution between both species (Der Breite 1985; Benitez Rodriguez et al. 1986). However, they can be differentiated by examining the male genitalia and the female’s size, where B. limbatus specimens are more robust (Der Breite 1985; Price and Graham 1997).

Interestingly, B. caprae can only be hosted by goats (Benelli et al. 2018). In our survey, the goats were often co-infested by B. caprae and L. africanus. Previous studies confirmed these findings, where chewing and sucking lice were present on the same host (Rashmi and Saxena 2017; Corke and Matthews 2018; Mansur et al. 2019; González-Álvarez 2020).

The African blue-sucking louse L. africanus can be hosted by sheep and goats (Aimee and Patrick 2019). It can be distinguished from L. stenopsis by observing the head’s posterolateral margins bulging in L. africanus(O’callaghan et al. 1989; Nizamov and Prelezov 2021). Unlike Bovicols, which are limited to a direct pathogenic role by damaging the host skin and reducing its resistance to other diseases (White et al. 2022), L. africanus can carry various pathogenic agents such as Anaplasma ovis, Coxiella burnetti, and Rickettsia spp. (Ehlers et al. 2020; Ouarti et al. 2021). The hematophagous short-nosed cattle louse H. eurysternus identified in our study alongside B. bovis can be responsible for severe anemia and mortalities (Lasisi et al. 2010). It may also be involved in transmitting pathogens such as Theileria orientalis, Rickettsia spp., and C. burnetti(Reeves et al. 2006; Hornok et al. 2010; Lakew et al. 2021). However, the vectorial competence of these lice cannot be confirmed as the pathogenic agents could mechanically be acquired during a blood meal on an infected host.

The chicken body louse Me. stramineus was reported in several studies in Europe and other countries as the most common bird lice species (Paliy et al. 2018; Adly et al. 2022; Chambless et al. 2022; Kouam et al. 2022; Shaikh et al. 2023). Domestic poultry can be infested by this species via lice transfer after direct contact with wild turkeys and birds (Hugon 2015). In addition, this amblyceran louse can parasitize a wide range of hosts and is often localized in areas with a low density of feathers (Smith 2004; Martinů et al. 2015; Paliy et al. 2018; Adly et al. 2022; Chambless et al. 2022; Kouam et al. 2022). Heavily-infested chickens were reported to have skin with scabs, dried blood, dander, serous oozing, and areas carrying lice aggregates. Minor punctiform wounds in the bleeding area of young feathers were also noticed. This is in agreement with all symptoms reported in previous studies (Devaney 1976; Pavlovic et al. 1989; Shanta et al. 2006).

Over fieldwork, the shaft lice M. gallinae were more frequently collected on young birds than adults. They can be morphologically differentiated from Menacanthus sp. by the absence of a spine-like sclerotinized ventral process on the head (Yevstafieva 2015; Saikia et al. 2017). Organized in a single file along the feathers shaft, they usually feed on feather particles (Price and Graham 1997; Saxena et al. 1997; Sudiana et al. 2020). Although it is generally admitted that chicken body louse damages are more severe than those induced by shaft louse, several studies have emphasized that M. gallinae-infested chickens are less egg productive than uninfested (Ikpeze et al. 2008; Abdullah and Mohammed 2013; Mohammed and Mohammad 2021).

Despite their classification among chewing lice, Me. stramineus and M. gallinae can adopt a hematophagous behavior by grinding fledgling feathers under the skin and absorbing thus tiny blood droplets visible through their digestive tract inducing thus, in some cases, severe anemia (Sychra et al. 2008; Kumar et al. 2017; Abdullah et al. 2018). Due to this behavior, these lice species have been suspected as potential vectors of bacteria, virus, and protozoa. Pathogens such as Borrelia sp, Wolbachia, the equine encephalomyelitis virus, and Toxoplasma gondii were isolated from Me. stramineus(Covacin and Barker 2007; Al-Lebawi and Hadi 2015; Ahmed et al. 2020; Corrin et al. 2021; Ouarab et al. 2021), while Chlamydia psittaci the psittacosis agent in birds was detected in M. gallinae(Mirzaei et al. 2016; Kaboudi et al. 2019).

Three ischnoceran species were also identified in backyard chickens: Go. gallinae (chicken fluff louse), G. dissimilis (brown chicken louse), and G. gigas (large chicken louse); these low pathogenic species are often confused because of their close general morphology (Sychra et al. 2008; Hugon 2015). Nevertheless, the study of their phylogenetic relationship shows that they belong to the same cluster and form a monophyletic group (Nasser et al. 2020; Mohammed Adnan and Shamal Abdullah 2021).

Our survey identified C. meleagridis alongside M. stramineus as the most frequent turkeys lice. This species is usually localized on wild and domesticated turkeys’ neck and breast feathers (Reeves et al. 2007; Sanchez-Montes et al. 2018; Adly et al. 2022). C. meleagridis lice feed on their host’s feathers, causing significant skin damage, irritation, and discomfort in severe infestations (Camacho-Escobar et al. 2014; Maturano and Daemon 2014; Rabana et al. 2019; Shaikh et al. 2021). To the best of our knowledge, there is no molecular evidence of the vector potential of C. meleagridis(Ouarti et al. 2021). However, as noticed for other chewing lice species, it is theoretically possible for the large turkey louse to act as a vector of specific diseases or pathogens.

All the examined pigeons of the study were infested with Co. columbae (slender pigeon louse) and Ca. bidentatus s.l. (small pigeon louse). These two species are recognized worldwide as the most common pigeon lice (Alajmi et al. 2021; Olejkov et al. 2021; Al-Badrani and Al-Muffti 2023; Jassem et al. 2023). Co. columbae lice live between the barbs of the primary and secondary tail feathers, deposit their eggs under the wings and feed on the chest feathers (Price and Graham 1997; Hugon 2015; Soliman et al. 2022). Ca. bidentatus s.l. adults are more versatile; they can be found in all body regions or mainly on fluffy parts of body feathers (Hugon 2015; Marcondes 2017). Studies have shown that the combined infestations of these two lice species interfere negatively with male sexual parades and induce female pigeons to choose uninfested males for mating (Clayton 1990,1991; Price and Graham 1997).

Overall, the high prevalence of some lice species in our study could be attributed to poor management practices in ectoparasite control, poor hygiene, and inadequate use of insecticides that favor the lice species’ reproduction (Mulugeta et al. 2010; Meguini et al. 2018; Durden 2019). A conducive environment in terms of weather and climate could also be incriminated (Mansur et al. 2019). Indeed, climatic conditions, including temperature and humidity, are essential in the lice’ life cycle (Chen and Mullens 2014; Durden 2019). As it was noticed for the El Tarf region, where we collected 2365 lice, favorable and optimum climatic conditions, host availability, and abiotic factors would potentiate the increase in abundance, thus increasing the lice infestation rate.

In order to preserve animal productivity, lice infestation control should typically involve using insecticides (pyrethroid). However, reasonable insecticide use should be mandatory to avoid overuse that can lead to environmental pollution and resistance among lice species. Alternatively to these chemical control methods, good sanitation practices and breeding conditions can also help to prevent and control lice infestations. This includes regularly cleaning and disinfecting breeding locals, coops, and equipment and removing and destroying dead-infested animals’ bodies. Overall, combining chemical and non-chemical control methods can effectively manage lice infestations in birds and ruminants. Further research will be needed to expand the Algerian list of chewing and sucking lice -by including wild mammalian species- and to access their ability to transmit pathogenic agents.