The prevalence and intensity of external parasites in domestic pigeons (Columba livia domestica) in Egypt with special reference to the role of deltamethrin as insecticidal agent.

This study aimed to investigate the prevalence and intensity of external parasites in domestic pigeons in Giza, Egypt, from January 2020 to December 2020. A total of 300 domestic pigeons (25 pigeons per month) were examined. The birds were divided into groups based on their age. The oxidative stress parameters; serum zinc concentration, serum malondialdehyde (MDA), and serum Nitric oxide were evaluated in single and mixed external parasitic infestations. The prevalence of external parasites in examined pigeons was 80.3%. The detected parasites were Pseudolynchia canariensis (P. canariensis), Hippobosca equina (H. equina), Columbicola columbae (C. columbae), Menopon gallinae (M. gallinae), Knemidocoptes species (spp.) and Dermanyssus gallinae (D. gallinae); their incidences were 41.6, 26, 7, 5,0.33 and 0.33%, respectively. The highest infestation was recorded in both spring and summer. . The incidence of disease was higher in squabs and young birds than in adults. The mixed external parasitic infestation was recorded in this study. The infected birds showed decreased serum zinc concentration and elevated MDA and serum Nitric oxide levels. In conclusion, regular monthly treatment with deltamethrin is recommended as an effective drug in the treatment of the infested birds and succeeded in reducing the incidence of externalparasites in the treated birds; in addition, pigeon management measures must be implemented to reduce the risk of external parasites.

Introduction

Pigeons coexist with different animal and poultry species as well as humans all over the world (Alkharigy et al., 2018). In Egypt, domestic pigeons are a valuable source of essential protein for people as they gain more weight quickly than other birds, its meat is palatable, easy to breed, and require slight management (El-Dakhly et al., 2016). Pigeons can be infected with a wide range of pathogens and serve as a reservoir for parasitic diseases. The proximity of pigeons to other domestic birds heightens the risk of parasitic infestation in poultry (Alkharigy et al., 2018). Pigeons harbor both external and/or internal parasites (Attia and Salem 2021).

Poultry ectoparasites are abundant in the tropics, where poor husbandry practices and favorable climatic circumstances allow them to thrive (Imura et al., 2012, Badparva et al., 2015, Salem and Attia, 2021). These parasites induce several direct and indirect effects on the pigeon, including weight loss, irritability, decreased productivity, malnutrition, low growth, decreased egg production and the development of a variety of clinical symptoms as; ruffled broken feathers, feathers loss, itching, pruritis, dermatitis, emaciation, inconvenience, death especially in squabs as well as indirect harm by transmitting other diseases (Radfar et al., 2012, Attia and Salem, 2021). The most common external parasites infesting pigeons are P. canariensis, Argas persicus, D. gallinae, M. gallinae, C. columbae, and Menocanthus stramineus (Atkinson et al.,2008).

Insects can harbor a lot of pathogens and convey them to the host from these pathogens “blood parasites” as Haemoproteus columbae which transmitted by the bite of ectoparasitic hippoboscid flies (Hussein and Abdelrahim, 2016); Plasmodium relictum, which is one of the most common species of avian malaria (Beadell et al., 2006) and Leucocytozoon marchouxi (Swinnerton et al., 2005, Martinsen et al., 2006, Hussein and Abdelrahim, 2016). Deltamethrin (a pyrethroid derivative) has become a popular pesticide in many nations due to its low toxicity and wide safety margin for poultry (Eladl et al., 2018). Deltamethrin affects the nervous system of insects that touch or ingest them, which leads to the rapid paralysis and death of these insects (Elyazar et al., 2011). In the same way, deltamethrin considered as an effective insecticide for the control of insects on pigeons and the surrounding environment (Attia and Salem, 2021). Accordingly, the aim of this study is to understand the biodiversity and determine the prevalence of pigeon external parasitic infestation with evaluation of oxidative stress markers and zinc levels which will aid in the planning of actions to improve the health of these birds in Egypt.

Material and methods

Ethical approval

This study was designed according to the Ethical Committee, Faculty of Veterinary Medicine regulations. Birds were humanly handled and safely released after clinical investigations.

Pigeon sampling

During the observation period from January to December 2020, 300 pigeons (25 bird per month) were investigated. Three hundred Birds were collected from different poultry clinics, poultry market and pigeon rearing houses from Giza, Egypt which lies in 29.9870°N 31.2118°E with a hot desert climate. The average ambient temperature in Giza in winter ranged from 21.1 °C (70.0)°F: 24.2 °C (75.6)°F with relative humidity 46:57%, in spring, 28.4 °C (83.1)°F : 34.9 °C (94.8)°F with relative humidity 37:44%, in summer 34.5 °C (94.1)°F : 41 °C (1 0 6)°F with relative humidity 39:53% and in autumn 25 °C (77.7)°F : 32.4 °C (90.3)°F with relative humidity 47: 57%. The examined birds were divided according to age as 80 squabs (day old to one month), 100 young (form one month to 7 months old) and 120 adults (above 7 months of age). Every bird was physically examined to detect the age and presence of external parasites (data were retrieved from the owners).

History and clinical examination of pigeons

External parasites

The feathers and skin were carefully examined for the presence of any macroscopic external parasites by naked eye then parasites were picked up and/ or skin scraping was adopted to identify the parasites using an Olympus Stereoscopic microscope (SZX16; Japan (Soulsby, 1986, Attia and Salem, 2021).

Identification of the parasites

All the collected parasites from the birds and their premises were preserved in 70% ethyl alcohol. Then, these parasites were identified using the keys recorded by Soulsby, 1986, Attia and Salem, 2021.

Blood samples

Blood was collected from jugular vein of externally parasitized birds on plain tubes for sera separation. Sera were kept on −20 °C for further investigations according to Attia et al., (2020).

Biochemical analysis

Serum zinc concentration were analysed using ionized coupled plasma by mass spectrometry method as described by Page et al., 2018, Attia et al., 2020.

Evaluation of oxidative stress markers

The level of serum malondialdehyde (MDA) using the reaction of thiobarbituric acid and then separation occurred on HPLC. The detection was performed using UV at 532 nm. Serum Nitric oxide (NO) level were analysed as mentioned by Khazaei and Nematbakhsh, 2012; briefly; colorimetric NO assay kit was used (Calbiochem-Novabiochem Corporation, San Diego, Calif), that measures the total nitrate and nitrite on serum based on Griess reaction and measured using wavelength 450 nm as mentioned by Aktas et al., 2017, Aytekin and Unubol Aypak, 2011.

Recommendation for external parasites control

Deltamethrin (Butox, 12.5 % solution, 1 mL / 4 L of water for birds & 1 mL /L for surrounding environment), is recommended for monthly spraying. Precautions have been taken during deltamethrin spraying, and the remains have been disposed of in a sanitary manner.

Statistical analysis

Data were statistically analyzed by using SPSS Version 18.0 software (Inc., Chicago, IL, USA). Blood parameters in infested and control non infested group were compared by independent T-test following the normality of data. A p- value consider significant when (p < 0.05).

Results

History and clinical investigations

Investigated pigeons were exhibited indications of illness such as general weakness, decreased egg production in layers, un-thriftiness, ruffled feathers, decreased weight gain, emaciation with protrusion of keel bone (Fig. 1A) and in some cases; pigeon flies were observed on birds’ body, under/or on the wings or on tail (Fig. 1B) and Fig. 2.

Fig. 1

A: Pigeon showing emaciation with ruffled feather; B: Pigeon showing ruffled feather with presence of Pseudolynchia flies on its body; C: Pigeon showing unilateral arthritis with presence of raised grayish color scales with grayish exudates in between scales on pigeon’s shank.

Fig. 2

A, B & C: Pigeon feathers showing attachment of C. columbae. D: Pigeon feathers showing attachment of M. gallinae.

Most of the examined pigeons were positive with at least with one of external parasitic species. The overall prevalence rate was 80.3%.

External parasites

External parasites usually observed on living birds. In case of lice infestation, eggs were attached with feathers roots, while in red mite; the red spots were observed surround the bird vent, unilateral arthritis was observed in birds mange with presence of dull raised scales tinged with grayish to brown color exudate on shank of pigeon leg (Fig. 1C).

Two hundred and forty-one; out of 300 examined pigeons, were positive for external parasites infestations. Six different types of external parasites were detected as follow: P. canariensis, H. equina, C. columbae, M. gallinae, Knemidocoptes spp. and D. gallinae with prevalence 41.6, 26, 7, 5, 0.33 and 0.33%, respectively. The intensity of external parasites on pigeon’s body were ranged from (1–6), (1–4), (8–25) and (5–20) in case of P. canariensis, H. equina, C. columbae, and M. gallinae, respectively.

The prevalence and intensity of ectoparasites in domestic pigeons based on their age were summarized in (Fig. 3 & Table 1) and Fig. 4.

Fig. 3

A: Adult P. canariensis. B: Microscopic appearance of D. gallinae.

Table.1

Prevalence and intensity of ectoparasites in domestic pigeons in Giza, Egypt from January 2020 to December 2020.

Parasites	Positive cases (%)	Parasite’s intensity	Age
			Squabs(80)	Young(1 0 0)	Adults(1 2 0)
P. canariensis	125 (41.6)	1–6	50 (62.5%)	65 (65%)	10 (8.33%)
H. equina	78 (26)	1–4	12 (15%)	22 (28%)	44 (36.6%)
C. columbae	21 (7)	8–25	10 (12.5%)	8 (8%)	3 (2.5%)
M. gallinae	15 (5)	5–20	6 (0.75%)	4 (4%)	5 (4.16%)
D. gallinae	1 (0.33)	–	0	0	1 (0.33%)
Knemidocoptes spp.	1(0.33)	–	0	0	1 (0.33%)
Total	241 (80.3%)	–	78/80(97.5%)	99/100 (99%)	63/120 (52.5%)

Fig. 4

A summarized diagram showing the prevalence of different external parasites of pigeons in Giza, Egypt from January 2020 to December 2020.

Single infestation of pigeons with P. canariensis, H. equina, C. columbae, M. gallinae, Knemidocoptes spp. and D. gallinae were recorded also; mixed external parasites infestation between (P. canariensis and H. equina); (P. canariensis and C. columbae); (C. columbae and M. gallinae) and (P. canariensis; C. columbae and M. gallinae) were observed and summarized in; Table 2.

Table.2

Prevalence of single and mixed infestation of external parasites in domestic pigeons.

Parasite	Type of infestation	Prevalence(Positive cases/300 total examined birds)
		No.	%
P. canariensis	Single	90	30
H. equina		66	22
C. columbae		9	3
M. gallinae		3	1
D. gallinae		1	0.33
Knemidocoptes spp.		1	0.33
P. canariensis + H. equina	mixed	22	7.33
P. canariensis + C. columbae		31	10.33
C. columbae + M. gallinae		12	4
P. canariensis + C. columbae + M. gallinae		6	2
Total No. of positive pigeons		241	80.3

The highest prevalence of external parasites was detected in spring and summer seasons as seen in (Table 3).

Table.3

Seasonal prevalence of external and internal parasites in domestic pigeons.

External	Parasite	Spring		Summer		Autumn		Winter
		No.	%	No.	%	No.	%	No.	%
	Pseudolynchia canariensis	57	76	60	80	5	6.66	3	4
	Hippobosca equina	18	24	48	66.6	12	16	0	0
	Columbicola columbae	8	10.66	10	13.33	2	2.66	1	1.33
	Menopon gallinae	6	8	9	12	0	0	0	0
	Dermanyssus gallinae	0	0	1	1.33	0	0	0	0
	Knemidocoptes spp.	0	0	1	1.33	0	0	0	0

No. = number of positive cases.

%= prevalence (No. of positive birds/ total [75 examined bird in each season]).

Infested pigeon with H. equina showed significantly higher in Nitric oxide (120.56 ± 4.56, ±95% C.I.) while in mixed infestation with P. canariensis it reaches to 145.89 ± 9.43; the Nitric oxide levels was low in M. gallinae reach to 56.89 ± 3.76. Serum MDA reach to 100.30 ± 6.48, 95% C.I.; in mixed infestation with P. canariensis, H. equina, while it was low in C. columbae infestation. zinc levels were decreased with parasitic infestation as it reaches to low levels in P. canariensis, H. equina mixed infestation; all data were compared to control levels of oxidative stress markers and zinc levels (Table 4).

Table.4

Oxidative stress markers in relation to single and mixed infection of external parasites.

Parasite	Oxidative stress markers
	Nitric oxide	MDA serum	Zinc
P. canariensis	95.57 ± 3.67	78.38 ± 5.17	54.04 ± 2.85
H. equina	120.56 ± 4.56	88.38 ± 4.49	36.77 ± 1.32
C. columbae	67.98 ± 7.00	30.33 ± 3.35	100.24 ± 1.00
M. gallinae	56.89 ± 3.76	33.56 ± 3.46	110.52 ± 2.96
D. gallinae	79.89 ± 5.99	50.33 ± 1.03	33.57 ± 2.82
Knemidocoptes spp.	80.14 ± 6.33	52.35 ± 1.67	34.66 ± 3.62
P. canariensis + H. equina	145.89 ± 9.43	100.30 ± 6.48	28.89 ± 1.52
P. canariensis + C. columbae	110.00 ± 3.59	98.33 ± 2.45	59.97 ± 3.95
C. columbae + M. gallinae	74.49 ± 9.32	60.38 ± 2.98	100.67 ± 2.96
P. canariensis + C. columbae + M. gallinae	160.84 ± 3.57	98.89 ± 2.78	34.56 ± 2.96
Control	49.78 ± 0.95	27.89 ± 0.69	118.00 ± 0.94

Periodical, monthly usage of deltamethrin in the infested flocks revealed a marked decrease in external parasites numbers after two days of treatment with relieve of the clinical signs.

Discussion

Pigeons are a point of anxiety since they can spread zoonoses to humans and are a reservoir for numerous parasite diseases affecting poultry (Sari et al., 2008). Most of examined pigeons showed signs of ruffled feathers, severe emaciation. Similar signs were observed in case of parasitic infestation as recorded by Abd El-Rahman et al., 2008, Mohamed et al., 2009, Abdel Rahman et al., 2019.

Ectoparasites live on feathers and skin of the host, using as a shelter and food provider, they also have a considerable negative influence on host health and productivity. From our results, the overall prevalence of external parasites was 80.3% (241/300) either single or mixed infestations, six different arthropods species were identified as follow: P. canariensis (41.6%), H. equina (26%), C. columbae (7%), M. gallinae (5%), D. gallinae (0.33 %), and Knemidocoptes spp (0.33%). Higher prevalence 89% (89/100) was recorded in Tripoli, Libya by Alkharigy et al., (2018) as they found the prevalence of C. columbae (82%), Goniodes gallinae (18%), M. gallinae (3%) and P. canariensis (1%). Also, Radfar et al., (2011) recorded higher prevalence of external parasites in pigeon, C. columbae (79.41%), M. gallinae (44.11%) and P. canariensis (63.72%) in south khorasan; Iran while, in Colombia, Pérez-García et al., (2015) found that the prevalence of C. columbae (64%), P. canariensis (52%), M. gallinae (24%). Borji et al., (2012) reported that the prevalence of C. columbae (42.8%), P. canariensis (16.1%) and M. gallinae (7.1%) in Mashhad city Iran. Also, Ali et al., (2020) recorded two external parasites on (Harami) pigeons, including the shaft louse M. gallinae and P. canariensis with 100 and 88.90% prevalence, respectively in Medina, Saudi Arabia.

In another study, the incidence of H. equina was 26% while Sokół and Michalski, (2015) noticed the low host specificity of H. equina which could attack cattle, dogs, hares, birds, and humans.

The prevalence of C. columbae was 21% however, Jahantigh et al., 2016, Dranzoa et al., 1999, Foronda et al., 2004 recorded higher prevalence of C. columbae 78.40%, 94.1 and 100% in Iran, Uganda, and Tenerife, respectively.

From our findings, Knemidocoptes spp. was observed in one case only with incidence of 0.33% during summer season and its lesion was found as unilateral arthritis and presence of severe dermatitis that appeared as raised dull color scales with presence of grayish color exudate between scales. Similar findings were observed in a parallel study conducted by Abou-Alsoud and Karrouf, (2016) who detected Knemidocoptes Pilae with prevalence of (11.5 %) in Budgerigars in Mansoura public park, Egypt.

The mixed infestation was reported as follow: P. canariensis + H. equina with prevalence 7.33%. P. canariensis + C. columbae with 10.33 % prevalence; C. columbae + M. gallinae (4%) and P. canariensis + C. columbae + M. gallinae (2%). Also, Alkharigy et al., (2018) recorded mixed infestation with external parasites in Libya. The mixed infestation of pigeon with external parasites could be contributed to that ectoparasites can live together without causing any hurtful effects on each other (Radfar et al., 2011).

The occurrence of ectoparasitic infestations in squabs (82.5%) was higher than young (77%) and lowest prevalence was recorded in adults (18%). Same observations were recorded by da Cunha Amaral et al., (2013) in case of P. canariensis infestation but, Msoffe et al., 2010, Radfar et al., 2012 noticed that the prevalence of P. canariensis were higher in adult pigeons than squabs. Adult pigeons are predicted to have a lower incidence of ectoparasites since they have a higher level of parasite immunity (Merila et al.,1995) and adult birds use their claws and the bill to get rid of ectoparasites (Clayton et al., 2010, Waite et al., 2012).

From our results, the intensity (number of external parasites that are found per bird) of external parasites on pigeon’s boy ranged from (1:6), (1:4), (8:25) and (5:20) in case of P. canariensis, H. equina, C. columbae and M. gallinae, respectively. This result is agreed with Attia and Salem (2021) as they noticed that the intensity of P. canariensis flies was 1: 6 (2.00 ± 1.0) on pigeons' body in El- Gharbia, Egypt.

The ambient temperature is the key determinant of the frequency, quantity, and diversity of external parasites allover year (Al-Barwari and Saeed, 2012, Attia et al., 2017). In our study the highest prevalence of external parasites infestations was recorded in both spring and summer. The prevalence of P. canariensis was 76% and 80%, C. columbae was 10.66% and 13.33%, M. gallinae was 8 % and 12% in spring and summer, respectively. D. gallinae only detected in summer season only 1.33%. The lowest prevalence of external parasites infestation in our study was recorded in autumn and winter season, P. canariensis was 6.66% and 4%, C. columbae was 2.66% and 1.33% in autumn and winter, respectively. on the other hand, no positive cases of M. gallinae and D. gallinae were recorded in autumn and winter. The differences in the seasonal prevalence may be contributed to the ambient temperature in Egypt exceed 25 Co in both spring and summer which considered a favorable condition for insects’ population.

Continuous exposure of poultry to ectoparasites that act as intermediate hosts for different parasitic worms increases the potential for the spread of parasitic diseases among birds (Ashenafi and Eshetu, 2004). So, monthly spray of deltamethrin is recommended and provoke acceptable result and succeeded in limitation of external parasites load. This result is agreed with (Attia and Salem, 2021) as they found deltamethrin is effective in P. canariensis control. Deltamethrin has proven its efficiency in controlling insects and we recommend in the future to load the active substance on biological nanoparticles to increase its efficiency. Also, recommend the use of some additives on pigeon food and drink as prebiotics (Abd El-Hack et al., 2021b, Yaqoob et al., 2021) probiotics (Abd El-Hack et al., 2021, Alagawany et al., 2021a, El-Saadony et al., 2021a), bioactive plants compounds (El-Saadony et al., 2021b), bioactive peptides (El-Saadony et al., 2021c, El-Saadony et al., 2021e), green synthesized nanoparticles (El-Saadony et al., 2021d, El-Saadony et al., 2021f), herbal extracts (Reda et al., 2021, Abou-Kassem et al., 2021), phytogenic compounds (Abd El-Hack et al., 2021c, Ashour et al., 2020), and essential oils (Alagawany et al., 2021b, El-Tarabily et al., 2021, Abd El-Hack et al., 2020) to strengthen their immune system and increase disease resistance.

The oxidative stress markers as (Nitric oxide and MDA levels) were raised in parasitic infestation either in single parasites or in mixed infestation due to rapid erythrocyte destruction and secretion of oxygen radicles (Mousa and Soliman, 2016); as recorded by Nazifi et al., 2011, Razavi et al., 2011 found that the antioxidant enzyme activity of superoxide dismutase (SOD), glutathione peroxidase (GPX), and catalase, were raised during parasitic infestation.

Conclusion

When we spoke with pigeon owners, we discovered that most of them were unaware of dealing with a parasitic infestation in domestic pigeons, and some of them do not remedy them at all. From our findings, pigeons have a significant prevalence of external parasites, with single or mixed infestation. Oxidative stress markers were significantly elevated during either single or mixed external parasites infestations. Pathogenicity studies, regular monitoring, treatment, and control strategies must be put in place to reduce pigeon parasitic infestation considering that these birds are in close contact with other poultry and human. Deltamethrin could be considered as an effective insecticide for controlling of external parasites in the pigeon and would be recommended for regular use hand by hand with biosecurity measures.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.