Introduction

Parasitism is a faunistic relationship shared throughout more than 50% of world biodiversity, between a parasite and a host, where the life of the parasite is dependent completely or partially on the host (Hannah and Lovejoy 2003). Bird lice are defined as obligated parasites, they need their host for survival and reproduction, and cannot live without the host for a long time. They feed primarily on feathers and dermal debris of birds (Tompkins and Clayton 1999). Chewing lice (Phthiraptera: Amblycera, Ischnocera) are wingless ectoparasites associated with wild and domestic birds in all regions around the world (Clayton et al. 2008). They are not significantly detrimental to birds by way of transmitting potential pathogens, but rather by heavy infestation causing health issues such as skin dermatitis, loss of body weight, irritability, as well as causing potential secondary infections (Clayton et al. 1999). This group of insects is still a neglected group due to the low number of recorded species (around 4000) compared to the expected potentially accountable species to the number of existing bird hosts (Price et al. 2003). There is, therefore, a lot of further studies needed to cover such important ectoparasites, especially in Africa and the Middle East.

Galliformes are a cosmopolitan order of birds that inhabit the whole world except the high Arctic (Burgin et al. 2018). Many species of these land fowl are widely domesticated by humans for many purposes: for their meat as food, kept as a hobby, and for biological control as predators of many species of ticks and fleas (Hassan et al. 1991; Duffy et al. 1992). Galliformes as birds are warm-blooded and therefore prone to high infestation of ectoparasites, such as chewing lice (Price et al. 2003: 329). Their heavy infestation leads to health threats including weight loss, dermatitis, and low reproduction (Clay 1941; Price and Graham 1997).

The domestic turkey, Meleagris gallopavo domesticus Linnaeus, 1758, is classified under the Phasianidae family of Galliformes birds. The turkey was an exotic bird to the Egyptian and Saudi Arabia avifauna for many years and then was selected to reproduce as a domesticated bird on farms in their countryside. According to Price et al. (2003), the turkey is known to host for many chewing lice species (Phthiraptera: Ischnocera and Amblycera). Unfortunately, in Egypt, there is little, and incomplete knowledge of the chewing lice infesting domestic turkeys (see Hafez and Madbouly 1966a, b, 1968a, b; Adly et al. 2019, 2020, 2021) the same case for the Saudi Arabia (Al-Ahmed et al. 2014; Nasser et al. 2015a; Shobrak et al. 2015; Alahmed et al. 2017; Al-Shammery 2021) Although the turkey is a common bird in Egypt and some parts of Saudi Arabia, and a very important bird in Egyptian menu, only two species of chewing lice associated with the turkey were recorded in Egypt by Hafez and Madbouly (1966a) and it never checked before for chewing lice in Saudi Arabia. Therefore, this work is aimed to review and update the knowledge about chewing lice infesting domestic turkey, Meleagris gallopavo domesticus in Egypt and Saudi Arabia, and includes an identification key to all the species infesting the turkey worldwide, providing new country records for Egypt and Saudi Arabia chewing louse fauna. Also, species of chewing lice recorded and expected to be associated with the turkey in Egypt and Saudi Arabia are summarized in Table 1.

Table 1 Summary of species of chewing lice (Phthiraptera) observed and expected to be associated with the domestic turkey, Meleagris gallopavo domesticus, in Egypt and Saudi Arabia
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Materials and methods

Nine domestic turkeys Meleagris gallopavo domesticus Linnaeus, 1758, were examined for chewing lice at two local farms outside Cairo, where turkeys are raised for their meat for food purposes only, in the period from March 2019 to June 2020. On the other hand, two domestic turkeys were examined for chewing lice and other parasites on the Riyadh bird market, Riyadh, Saudi Arabia in March 2017. The prevalence of chewing lice on these turkeys was 100%. The turkeys were identified according to Porter and Aspinall (2013). They were inspected visually and then the chewing lice were collected by using fine forceps. The chewing lice were taken from different body parts of the turkey, including the head, wings, abdomen, and near the cloaca. The captured turkeys were released safely after the examination. The collected chewing lice were placed in 70% ethyl alcohol, then cleared and mounted according to Adly et al. (2019).

Chewing lice were identified according to Kellogg and Paine (1914); Thompson (1948); Gustafsson et al. (2020). The following references were used in developing the identification key: Clay 1938, 1940; Emerson 1961; Price and Beer 1964; Eichler and Mey 1978. The host/parasite association patterns were also examined according to Price et al. 2003. Newly (to Egypt) identified specimens were photographed using a TOUPCAM LCMOS14000KPA camera, 14mp, fixed on a microscope, LABMED, Inc. USA. The PhotoScape program was used to prepare the final images. All specimens are deposited in ASUC (Adly et al. 2019).

Results

A total of 298 chewing lice specimens were collected from nine captured individuals from Egypt and 11 chewing lice samples were reported from the two examined individuals from Saudi Arabia ondomestic turkey, Meleagris gallopavo domesticus (Linnaeus) Table 2. Six species of chewing lice were identified. Two of these species, Menacanthus stramineus Nitzsch, 1818 (Amblycera: Menoponidae) and Goniodes gigas (Taschenberg, 1879) (Ischnocera: Philopteridae) are considered as new to Egypt while only the Goniodes gigas (Taschenberg, 1879) is considered as a new record to Saudi Arabia Species of chewing lice recorded and expected to be associated with the turkey in Egypt and Saudi Arabia are summarized in Table 1.

Table 2 Chewing lice species which associated with turkeys and collected through the current study in the period 2017 to 2020 in Egypt and Saudi Arabia
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Suborder Amblycera Kellogg, 1896

Family Menoponidae Mjöberg, 1910

Colpocephalum tausi (Ansari, 1951)

Galliferrisia tausi Ansari, 1951.

Type host

Indian peafowl Pavo cristatus Linnaeus, 1758.

Remarks:

This species of louse has not yet been recorded in Egypt or Saudi Arabia, perhaps due to the limitations of the survey process as well as the number of hosts examined.

Menacanthus stramineus Nitzsch, 1818 (Fig. 1).

Fig. 1
figure 1

Menacanthus stramineus Nitzsch, 1818 Male

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Eomenacanthus stramineus Nitzsch, 1818.

Material

Ex Host: Domestic Turkey, Meleagris gallopavo Linnaeus, 1758.

1♀, local farm, City: Cairo, country: Egypt, exact date: (1/March/2020), collector: Eslam Adly, deposition data (ASUC).

2♂ Riyadh bird market, Riyadh, Saudi Arabia in March 2017, collector: Areej A. Alkhalaf, deposition data: College of Science, Princess Nourah Bint Abdulrahman University.

Type host

Wild Turkey Meleagris gallopavo Linnaeus, 1758.

Remarks:

This is the first record of this species from Egypt, but it was recorded before from Saudi Arabia by Aldryhim (1991) from domestic chicken. This species is collected from feathers on the host’s body. It has a triangular head, weakly chitinized, slightly more broad than long, covered by lateral expansion of the head; ventral spinous process developed but not like that of Menacanthus pallidulus, post antennal region has medium-sized setae; temple has round end; gular plate with no chitinization; thorax narrower than head, prothorax wider than long, lateral angle acute; mesothorax highly chitinized; meta thorax with three long lateral setae on each side; legs short relative to the length of the body; hind femur with clear ctenidium; elongated abdomen, weakly chitinized, with characteristic hairy dorsum which separates this species from any other Menacanthus spp.; segment number IV has a cluster of thick spine-like setae; female without any clear genital plate; male faint chitinized characteristic genitalia.

Menopon gallinae (L., 1758)

Pedwulus gallinae Linnaeus, 1758.

Menopon brevipes Piaget, 1885.

Menopon longicephalum Kellogg, 1896.

Menopon lunanale Eichler, 1947.

Menopon major Piaget, 1880.

Liotheum pallidum Nitzsch, 1818.

Menopon productum Piaget, 1885.

Menopon productum Piaget, 1880.

Nirmus tngonocephalus Olfers, 1816.

Material

Ex Host: Domestic Turkey, Meleagris gallopavo Linnaeus, 1758.

26♀/21♂/6 Nymph, local farm, City: Cairo, country: Egypt, exact date: (1/March/2020), collector: Eslam Adly, deposition data (ASUC).

2♀ Riyadh bird market, Riyadh, Saudi Arabia in March 2017, collector: Areej A. Alkhalaf, deposition data: College of Science, Princess Nourah Bint Abdulrahman University.

Type host

Chicken Gallus gallus (Linnaeus, 1758).

Remarks:

This species has been recorded as associated with domestic chicken Gallus gallus domesticus Linnaeus by Hafez and Madbouly (1966a). Therefore, this record covers the first report of Menopon gallinae associated with domestic turkeys in Egypt. Also, it was recorded before from Saudi Arabia by Aldryhim (1991) from domestic chicken. It is a typical body louse found among the abdominal feathers and usually close to the feather shafts. Head is weakly chitinized, broad, reaching its widest point at the temporal region; shallow antennal fossa covered by lateral expansion of the head; post ocular fringe with characteristic small setae in comb-like rows; post antennal region with medium size setae; antenna has four segments, third segment has basal peduncle and is flattened anteriorly to fit with adjoining four; temple with round end; gular plate with faint chitinization; thorax narrow, prothorax wider than long, lateral angle acute; mesothorax highly chitinized; meta thorax with three long lateral setae on each side; legs short relative to the length of the body; hind femur with clear ctenidium; elliptical abdomen, weakly chitinized, with only posterior marginal row of setae (12–15), segment number IV has cluster of thick spine-like setae; female without any clear genital plate; male with fused segment VII-IX to form genitalia.

Suborder Ischnocera Kellogg, 1896

Family Philopteridae Burmeister, 1838

Chelopistes meleagridis (Linnaeus, 1758)

Pediculus meleagridis Linnaeus, 1758.

Philopterus stylifer Nitzsch, 1818.

Rhopaloceras styliferum Taschenberg, 1882.

Material

Ex Host: Domestic Turkey, Meleagris gallopavo Linnaeus, 1758.

9♀, 4 Nymph, local farm, City: Cairo, country: Egypt, exact date: (10/March/2019), collector: Eslam Adly, deposition data (ASUC).

Type host

Wild Turkey Meleagris gallopavo (Linnaeus, 1758).

Remarks:

Chelopistes meleagridis (large turkey louse) was previously recorded in Egypt by Hafez and Madbouly (1966a). This louse has a very characteristic body shape as well as distinctive pigmentation in body segments.

Goniocotes gallinae (De Geer, 1778)

Ricinus gallinae De Geer, 1778.

Philopterus hologaster Nitzsch, 1818.

Material

Ex Host: Wild Turkey, Meleagris gallopavo Linnaeus, 1758.

9♀/17♂, local farm, City: Cairo, country: Egypt, exact date: (10/March/2019), collector: Eslam Adly, deposition data (ASUC).

Type host

Chicken, Gallus gallus.

Remarks:

This species has been recorded as associated with domestic chicken, Gallus gallus domesticus by Hafez and Madbouly (1966a). Therefore, this record covers the first report of Goniocotes gallinae associated with domestic turkeys in Egypt. This species is usually found on the feathers of the whole domestic chicken, except for the head. Lice head is circular in shape; carina strongly sclerotized; pre-antennal area is small without dorsal pre-antennal sutures; antenna is exposed and filiform without clear sexual dimorphism; angulated temple, extended outward; occiput with two small connected occipital blotches; thorax rounded anteriorly; prothorax small with acute lateral angles; meso- and metathorax fused without clear separation, each with four marginal seta; abdomen weakly chitinized, oval with subequal segments, tergites clearly separated medially, pleurites well chitinized with single row of post spiracle setae, tip of abdomen of female is rounded, while of that of male is concave with a central rounded protrusion; male genitalia are weakly chitinized.

Goniodes gigas (Taschenberg, 1879) (Fig. 2).

Fig. 2
figure 2

Goniodes gigas (Taschenberg, 1879) adult. (a, Female; b, Male)

Full size image

Goniocotes gigas Taschenberg, 1879.

Goniocotes abdominalis Piaget, 1880.

Goniodes hologaster Denny, 1842.

Material

Ex Host: Domestic Turkey, Meleagris gallopavo Linnaeus, 1758.

47♀/36♂, local farm, City: Cairo, country: Egypt, exact date: (1/March/2020), collector: Eslam Adly, deposition data (ASUC).

3♀ Riyadh bird market, Riyadh, Saudi Arabia in March 2017, collector: Areej A. Alkhalaf, deposition data: College of Science, Princess Nourah Bint Abdulrahman University.

Type host

Chicken, Gallus gallus.

Remarks:

This report is the first for Goniodes gigas From Egypt and Saudi Arabia. This species is usually found on the neck and breast feathers of the domestic chicken. Head is slightly broad, robust, with marginal chestnut brown, anterior region broadly rounded, antenna are filiform with slight sexual dimorphism, temples project outward with acute angle tip, gula without setae; thorax trapezoidal, prothorax narrow with highly chitinized edges, mesothorax without clear separation from metathorax, metathorax projecting a little outward with clear chitinized edges just like the following abdominal segment; abdomen is oval in shape, gradually widening to segment IV and then tapering to segment VIII and ending with a concave tip, segments have characteristic chestnut brown colour, chitinization, and are arranged gradually over each other; male genitalia taper toward the end.

Lipeurus caponis (Linnaeus, 1758)

Pediculus caponis Linnaeus, 1758.

Lipeurus alpha Kellogg, 1908.

Lipeurus antennatus Piaget, 1885.

Lipeurus bakeri Carriker, 1956.

Lipeurus beta Kellogg, 1908.

Lipeurus borcherti Eichler, 1953.

Lipeurus dovei McGregor, 1918.

Lipeurus formosanus Sugimoto, 1929.

Lipeurus gamma Kellogg, 1908.

Lipeurus Iineatus McGregor, 1917.

Nirmus tesselatus Denny, 1842.

Lipeurus variabilis Burmeister, 1838.

Material

Ex Host: Domestic Turkey, Meleagris gallopavo Linnaeus, 1758.

73♀/31♂/18 Nymph, local farm, City: Cairo, country: Egypt, exact date: (10/March/2019), collector: Eslam Adly, deposition data (ASUC).

Nymph Riyadh bird market, Riyadh, Saudi Arabia in March 2017, collector: Areej A. Alkhalaf, deposition data: College of Science, Princess Nourah Bint Abdulrahman University.

Type host

Chicken, Gallus gallus.

Remarks:

Lipeurus caponis has already been recorded in Egypt by Hafez and Madbouly (1966a). and recorded by Aldryhim (1991) from domestic chicken.This species is cosmopolitan, associated with many Galliformes. It is usually found on the wing feathers, living between the barbules of the primary wing feathers of the chicken and some related species. Head is slightly elongated, longer than broad, rounded on the frontal region, eyes are conspicuous with characteristic large black spots behind them, conus is not well-developed; antenna have clear sexual dimorphism, in males looking like a leg of lice; temple is posteriorly rounded with a highly chitinized black edge, occipital region has characteristic comma shape; thorax has a black edge, prothorax is narrower than the head; fore legs are very small compared to the mid and hind legs; abdomen is elongated with decorated black edge; male genitalia highly chitinized tapering to the end of the body.

Valimia polytrapezia (Burmeister, 1838:343)

Lipeurus polytrapezius Burmeister, 1838.

Lipeurus gallipavonis Harrison, 1916.

Type host

Wild Turkey, Meleagris gallopavo.

Remarks:

This species has not yet been recorded on turkeys from Egypt and Saudi Arabia. This group of large, slender lice used to be known as Oxylipeurus-complex, but in 2020 Gustafsson and Zou revised this group and launched a new generic name Valimia-complex. Therefore, the species previously known as Oxylipeurus polytrapezius is now Valimia polytrapezia.

Key to species of chewing lice parasitized turkey

  1. 1.

    Antennae concealed under head, always club-shaped............... Amblycera 2

    Antennae projected from head, usually filiform in shape, dimorphic in some species............... Ischnocera 4

  2. 2.

    Ctenidia on abdominal sternite, no post palpal spines on head, subrectangular head temporal lobe............... Colpocephalum tausi

    No abdominal ctenidia on sternite............... 3

  3. 3.

    Ventral spines and pair of post palpal spines on head, mesosternum pointed medially with large number of setae............... Menacanthus stramineus

    No ventral spines on head, postnotum present at medio posterior pronotal margin, only one pair of abdominal sternal brushes............... Menopon gallinae

  4. 4.

    Abdomen long and slightly slim, the first antennal segment of male slightly thin............... 5

    Abdomen rounded to oval in shape, the first antennal segment of male large and stout............... 6

  5. 5.

    Male sub genital plate with medio-posterior process............... Valimia polytrapezia

    Male without this process, head much longer than wide, male abdomen lacking accessory tergal plates, distinctive male genitalia............... Lipeurus caponis

  6. 6.

    Antennal base is not annulated............... Chelopistes melegridis

    Antennal base is annulated............... 7

  7. 7.

    First antennal segment of male without appendage, but if present, not a sharp pointed one; pleurites of abdominal segment VIII of female with well-developed pulvilli-form setae............... Goniodes gigas

    First antennal segment of male with sharp pointed appendage; pleurites of abdominal segment VIII of female without setae............... Goniocotes gallinae

Discussion

Turkeys are one of the most common game and poultry birds globally. They are native to North America and have been introduced and domesticated around the world. Despite the wide range of distribution and their connection to humans which increases the possibility of transmitting parasites and diseases, very little studies have been done on their associated ectoparasites such as ticks, fleas, and lice (Lane et al. 2006). The recording of chewing lice of such popular and widespread birds such as turkey, is significant to evaluating the parasitic fauna of any country. Also, it’s role as a biological control agent critical within the food chain. On the other hand turkey is considered as one of the meat sources with some economic important out of all the poultry (FAO 2007). The recording of such ectoparasites (ticks, fleas, and lice) will also ultimately help in the prevention and control of disease transmission (Ansari 1944; Wall and Shearer 2001; Naz et al. 2011). Unfortunately, either for Egyptian or Saudi Arabia chewing lice fauna, there has been only very few studies on ectoparasites of wild and domestic birds including turkey. There is a gap in the study of the Middle East chewing lice fauna in many levels: species occurrence, host/parasite interaction and distributions,so many efforts were needed to be done to fill such gaps (Adly et al. 2021).

The chewing lice of turkey have been previously recorded through different parts of the world, including the native range as well as the introduced range, where Emerson in 1951 had recorded C. meleagridis on Eastern turkey and on Nelson-Merriam’s turkey while he recorded M. stramineus on Eastern turkey only (Emerson 1951). Malcomson in 1960 recorded C. meleagridis and M. stramineus on wild turkey in the USA (Malcomson 1960). Several publications discussed turkey/chewing lice interaction through different parts of the world (Hafez and Madbouly 1966a; Kellogg et al. 1969; Holt 2002; Lane et al. 2006; Atkinson et al. 2008, Gonzalez-Acuna et al. 2009; Rassouli et al. 2016).

The present study provides an update to chewing lice fauna of Egypt and Saudi Arabia and represents two new records of them for Egypt (Menacanthus stramineus and Goniodes gigas) and one new record from Saudi Arabia (Goniodes gigas). Also, the identification key provided through this work form a very good step in studying chewing lice of turkey and provide a tool for Vet. to identify the parasitic chewing lice through their farms around the world. Such impact was appeared with the publication of peacock chewing lice identification key as an example (Nasser et al. 2015a). Globally, eight species of chewing lice of two suborders of Phthiraptera were known to infest turkey, the first suborder is Amblycera with the following species: Colpocephalum tausi, Menacanthus stramineus, and Menopon gallinae. The second suborder is Ischnocera with the following species: Chelopistes meleagridis, Goniocotes gallinae, Goniodes gigas, Lipeurus caponis, and Valimia polytrapezia. Only two of all of this species, Chelopistes meleagridis and Lipeurus caponis, were recorded associated with domestic turkey in Egypt and Menopon gallinae and Goniocotes gallinae, have so far only been associated with Gallus gallus, but have not yet been recorded on turkeys in Egypt (Hafez and Madbouly 1966a) For Saudi Arabia, this work form the first examination of domestic turkey for chewing lice, but Goniocotes gallinae, Goniodes gigas, Menacanthus stramineus, Menopon gallinae, Lipeurus caponis were recorded by Aldryhim (1991). On the other hand, Colpocephalum tausi, and Valimia polytrapezia, have not yet been recorded either from Egypt or Saudi Arabia..

The present work forms a very small step in understanding a part of the large picture of chewing lice/host association in the Middle East. A lot of works were needed to cover the characteristic avifauna of the region either for migratory, native and resident birds.