Bull 423 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Makawi and Hadi 5Bull. Iraq nat. Hist. Mus. (2023) 17 (3): 423-434. https://doi.org/10.26842/binhm.7.2023.17.3.0423 ORIGINAL ARTICLE IDENTIFICATION OF HARD TICKS FROM BUFFALO BUBALUS BUBALIS (LINNAEUS, 1758) IN IRAQ Zainab A. Makawi* and Afkar M. Hadi Iraq Natural History Research Center and Museum, University of Baghdad, Baghdad, Iraq ⃰ Corresponding author: zainab@nhm.uobaghdad.edu.iq Recived Date: 14 Janaury 2023, Accepted Date 13 March 2023, Published Date:20 June 2023 This work is licensed under a Creative Commons Attribution 4.0 International License ABSTRACT Ticks (Acari: Ixodidae) are ectoparasites that infest livestock in every geographic region of the world and are vectors of several viral, bacterial, and protozoan pathogens to both animals and humans. There is little information is available is about tick presence in Buffalo Bubalus bubalis (Linnaeus, 1758) (Artiodactyla, Bovidae) in Iraq. The current study determined the species of ticks parasitizing Buffalo in some central and southern regions included: Baghdad (Al Fathelia), Karbala (Al-Hussainia), Wasit (Kut and Al-Suwairah), Al-Qadisia (Al- Diwaniyah, Al- Saniya, Al-Mihnawea, and Afak), Thi Qar (Al-Nasiriyah and Al-chibayish), Missan (Amara and Qalaat Salih) and Basrah (Al-Haretha, Al-Madena and Al-Deer). A total of 150 Buffalo were examined for ixodid ticks with an infestation rate 66.66%. A total of 172 Specimens of hard ticks were isolated including 104 (58.4%) males and 68 (39.53%) females. The current results revealed to eight species of ixodid ticks belong to the genus Hyalomma as follow: H. truncatum Koch,1844 (50.66%), H. excavatum Koch,1844 (24%), H. anatolicum Koch, 1844 (16%), H. marginatum Koch,1844 (8%), H. impeltatum Schulze & Schlottke, 1930 (8%), H. rufipes Koch,1844 (5.33%), H. scupense Schulze, 1919 (4%), H. dromedarii Koch,1844 (2.66%) respectively. The prevalence of these species in buffaloes was also discussed with previous studies in Iraq and the worldwide. As the current results suggested that buffaloes are considered a new host for three species of them in Iraq the following are: H. truncatum, H. impeltatum, and H. rufipes. Keywords: Al Diwaniyah, Buffalo, Hard Ticks, Hyalomma, Iraq. INTRODUCTION Ticks have considerable medicinal and veterinary significance since they are necessary hematophagous ectoparasites of birds, reptiles, and especially mammals (Mehlhorn and Armstrong, 2010). The bacterial, protozoal, spirochaetal, rickettsial, and viral species carried by ticks infect both humans and domestic animals and cause a number of diseases. Ticks are crucial for both livestock and people (Akhtar et al., 2011; Ullah et al., 2020). One of the most prevalent ectoparasites of livestock in the tropics and subtropics is called Hyalomma sp. This BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Iraq Natural History Research Center & Museum, University of Baghdad https://jnhm.uobaghdad.edu.iq/index.php/BINHM/Home Copyright © Bulletin of the Iraq Natural History Museum Online ISSN: 2311-9799-Print ISSN: 1017-8678 https://doi.org/10.26842/binhm.7.2023.17.3.0423 https://orcid.org/0000-0003-1136-9121 https://orcid.org/0000-0001-7928-8702 mailto:zainab@nhm.uobaghdad.edu.iq https://creativecommons.org/licenses/by/4.0/ https://jnhm.uobaghdad.edu.iq/index.php/BINHM/Home 424 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Identification of hard ticks from buffalo parasite reduces milk supply, results in weight loss, increases mortality, necessitates the use of acaricides, and physically harms the leather industry (Mulugeta et al., 2010). Ticks are obligate hematophagous ectoparasites that have negative effects on human and veterinary health; further promotes the spread of the virus that causes Crimean-Congo hemorrhagic fever in people and the deadly protozoa Theileria annulata in animals (Hurtado et al., 2018; Kumar et al., 2020). Ticks can be found worldwide and prefer humid and temperate climates; they typically attach to their host's legs, underarms, and abdomen (Nuttal, 1905). Hard Ticks (Ixodidae), the largest ticks’ family, contains 713 valid species (Barker and Murrell, 2004). There are two general types of Asian water buffalo, wild and domestic. Water buffalo are well adapted to swamps and areas subject to flooding, and number of buffalo is of great value due to their high economic importance (Abid and Fazaa, 2007). On the other hand, the life cycle of Ixodid ticks is influenced by a number of intrinsic and extrinsic factors (Shah-Fischer and Say, 1989). The aim of this study is to diagnose the species of hard ticks that infest buffalo in the areas of abundance of buffaloes in the Central, and the Southern of Iraq. MATERIALS AND METHODS Study area: The current study was conducted in some areas where buffalo breeding abounds in Iraq's central and southern regions belongs to their province as follow: Baghdad (Al Fathelia), Karbala (Al-Hussainia), Wasit (Kut and Al-Suwairah), Al-Qadisia (Al- Diwaniyah, Al- Saniya, Al-Mihnawea, and Afak), Thi Qar (Al-Nasiriyah and Al-chibayish), Missan (Amara and Qalaat Salih) and Basrah (Al-Haretha, Al-Madena and Al-Deer). Specimens' collection and processing: To make it easier to remove ticks from the skin at various body sites on each animal, including the ear, side of the neck, leg, foot, entire tail, including the tail brush, and half of the lower perineum and entire upper perineum, ticks were collected using cotton dipped in ethyl alcohol and tweezers. Collecting ticks were placed separately in small bottles containing 70% ethanol, labeled and transported to the laboratory in the "Iraq Natural History Research Center and Museum INHM" for diagnosis. The ticks were processed in the laboratory with a 10% potassium hydroxide solution (KOH) for transparent (Soulsby, 1982); specimens were diagnosed by taxonomic references (Mohammad, 1996; Walker et al., 2014); were photographed by digital camera (Samsung SM-N770F). RESULTS A total of 172 (68 females and 104 males) hard ticks specimens were isolated from 150 buffalo with infestation rate (66.66/100%), from total number (150) buffalo in Central and South regions of Iraq as: Baghdad (Al Fathelia), Karbala (Al-Hussainia), Wasit (Kut and Al- Suwairah), Al-Qadisia (Al- Diwaniyah, Al- Saniya, Al-Mihnawea, and Afak), Thi Qar (Al- Nasiriyah and Al-chibayish), Missan (Amara and Qalaat Salih) and Basrah (Al-Haretha, Al- Madena and Al-Deer). The current study revealed to eight species of hard ticks with infestation rates as follow: H. truncatum (50.66%), H. excavatum (24%), Hyalomma 425 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Makawi and Hadi anatolicum (16%), Hyalomma marginatum (8%), H. impeltatum (8%), Hyalomma rufipes (5.33%), H. scupense (4%), H. dromedarii (2.66%) respectively. (Tab. 1, Pls 1-8). A total of 178 specimens of Hard ticks were isolated including (104 males and 68 females) (Tab. 2). Some animals were infested with more than one species of hard ticks (mix infestations), as is the case in the Al- Diwaniyah region which shows Include infestation with three species of ticks (Hyalomma anatolicum, H. truncatum and H. marginatum) and Al-Nasiriyah City which shows include infestation with two species of ticks (Hyalomma dromedarii and H. rufipes). Table (1): Species of Hard ticks isolated from Buffalo in some areas of Iraq. Species of Hard ticks Isolate Total number of Buffalo Number of infested specimens % Hyalomma truncatum 150 76 50.66 H. excavatum 36 24 H. anatolicum 24 16 H. marginatum 12 8 H. impeltatum 12 8 H. rufipes 8 5.33 H. scupense 6 4 H. dromedarii 4 2.66 Table (2): The total number of isolated males and females according to the species of hard ticks. Species of Hard ticks Isolate No. of Males No. of females Total % Hyalomma truncatum 46 30 76 44.18 H. excavatum 16 20 36 20.93 H. anatolicum 18 6 24 13.95 H. marginatum 10 2 12 6.97 H. impeltatum 6 6 12 6.97 H. rufipes 8 0 8 4.65 H. scupense 2 4 6 3.48 H. dromedarii 4 0 4 2.23 Total 104 68 172 426 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Identification of hard ticks from buffalo Plate (1): (A) H. truncatum male, dorsal view [1. Cervical fields with unclear depression. 2. Conscutum with dark coloured (appears smooth and shiny), 3. Lateral grooves elongated, 4. Two posterior ridges; caudal depression (present and deep), 5. Central festoon with dark coloured. 6. Posteromedium groove absent. 7. Paramedian grooves absent); (B) H. truncatum male, ventral view (8. Spiracle areas have sparse setae. 9. Adanal plates shape has square ends. 10. Subanal plates are (distinct and small)]. Plate (2): (A) H. excavatum male, Dorsal view [1. Cervical fields with apparent depression, 2. Posteromedian with groove, 3. Lateral grooves (short), 4. Paracentral festoons with joined anteriorly, 6. Central festoon (pale)]; (B) H. excavatum male, Ventral view [7. Spiracle areas with sparse setae, 8. Adanal plates shape with square ends, 9. Subanal plates (distinct)]. 427 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Makawi and Hadi Plate (3): H. anatolicum male; (A), Dorsal view: 1. Cervical fields depression apparent, 2. Posteromedium groove present (long and narrow), 3. Central festoon dark, 4. Paracentral festoons separate anteriorly, (B) ventral View: 5. Spiracle areas have sparse setae, 6. Adanal plates shape has a round end. Plate (4): H. marginatum, male: (A) Dorsal view: 1. Cervical fields depression apparent, 2. Conscutum dark, 3. Lateral grooves long, 4. Two posterior ridges; caudal depression present (but shallow), 5. Central festoon dark, 6. Posteromedium groove present, 7. Paramedian grooves small, (B) Ventral view: 8. Spiracle areas have sparse setae, 9. Adanal plates shape has square ends, 10. Subanal plates distinct but small. 428 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Identification of hard ticks from buffalo Plate (5): (A). H. impeltatum male, (dorsal view), [1. Cervical fields depression apparent, 2. Conscutum dark, 3. Lateral grooves long, 4. Two posterior ridges, Coudal depression present, 5. Central festoon pale, 6. Posteromedium groove present, (B). H. impeltatum male, (Ventral), 7. Adanal plates shape has a square ends, 8. Subanal plates distinct]. Plate (6): H. rufipes male; (A) Dorsal view: 1. Cervical fields depression not apparent, 2. Conscutum dark, 3. Lateral grooves short, 4. Posterior ridges absent; caudal depression absent, 5.Posteromedium groove absent; paramedian grooves absent, (B) Ventral view: 6. Spiracle areas have dense setae, 7. Adanal plates shape has square ends, 8. Subanal plates distinct. 429 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Makawi and Hadi Plate (7): (A). H. scupense male, (Dorsal view), [1. Cervical fields depression apparent (but small), 2.Conscutum dark, 3. Lateral grooves long, 4. Four posterior ridges, 5. Posteromedium groove present, 6. Paramedian grooves large, (B). H. scupense male,(Ventral view), 7. Spiracle areas have sparse setae, 8. Adanal plates shape has square ends, 9. Subanal plates distinct]. Plate (8): H. dromedarii, male; (A) Dorsal view: 1. Cervical fields depression apparent, 2. Posteromedium groove present (long and narrow), 3. Central festoon dark, 4. Paracentral festoons separate anteriorly, (B) Ventral view: 1. Spiracle areas have sparse setae, 2. Adanal plates shape has a round end. 430 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Identification of hard ticks from buffalo DISCUSSION The current study recorded Buffalo infested rate with Hyalomma spp. (66.66% /100) from total number 150 buffaloes; these percentages are lower than those reported by Tarash (1982), who discovered 94.2% of the Hyalomma spp. in Basra's Al-Dehab Al-Abiad Village, higher than those reported by Al- Mawla (2001), who discovered 46% of Hyalomma species in Mosul, and lower than those reported by Abdul Hussein and Awad (2005) estimated of 73.6% of the Hyalomma in Basra. The results presented above are consistent with those obtained by Mustafa et al. (2019), when three different species of ticks were recorded parasitizing buffalos in Samarra, all of which belong to the genus Hyalomma include: H. anatolicum, H. scupense and H. turanicum. The reason for the genus Hyalomma dominance and spread is that it can survive in environments with low humidity and harsh climatic conditions due to its high tolerance (Kettle, 1995). The results of the current study showed that buffaloes were infested with eight species of ticks, all of which belongs to the genus Hyalomma, namely: H. truncatum (50.66%), H. excavatum (24%), H. anatolicum (16%), H. marginatum (8%), H. impeltatum (8%), H. rufipes (5.33%), H. scupense (4%), H. dromedarii (2.66%) respectively. The key clinical findings documented in this study included weight loss, mucous membrane pallor, lymph node enlargement, and a staring coat. The current study found that Hyalomma truncatum had the highest infestation rate 50.66% and Hyalomma dromedarii had the lowest infested rate 2.66%. While disagreed with Falih and Hamza (2022) who recorded four species of Hyalomma included: H. anatolicum 45.66% represented the highest percentage of collected ticks in buffaloes, H. marginatum 31.21%, H. dromedarii 16.76%, and H. scupense 6.35% represented the lowest percentage of collected ticks in buffaloes in Dhi-Qar and Al-Muthanna Province. Shubber (2014) recorded five species of Hyalomma include: H. anatolicum, H. dromedarii, H. excavatum, H. scupense, and H. turanicum in the Middle and South of Iraq. This study found mix infestation on a single host, which is consistent with Ahmad et al. (2021) who revealed to be infested by one or more species of ectoparasites. These differences could be due to the differences in a mount of samples, or the presence of suitable climates, or movement of animals from one area to another. According to the sex, the current study, recorded male population (104 specimens) more than females (68 specimens) in terms of infestation. Disagreed with Sayin et al. (2003) who revealed to female ticks to have a higher distribution than "male ticks". Aktas et al. (2004) also found that the female ticks’ population of Hylomma species was more than the male tick population. The current study revealed to mix infestation of two species of hard ticks in some regions, this result agrees with Ahmad et al. (2021) who cleared this important topic that decreased their level production, due to irritability, anemia, and raising the cattle and buffalo morbidity ratio. 431 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Makawi and Hadi CONCLUSION This comprehensive survey provides basic data on the infestation of buffalo by hard ticks species in the areas of abundance of buffaloes in many regions of Center and Southern Iraq as follow: Baghdad (Al Fathelia), Karbala (Al-Hussainia), Wasit (Kut and Al-Suwairah), Al- Qadisia (Al- Diwaniyah, Al- Saniya, Al-Mihnawea, and Afak), Thi Qar (Al-Nasiriyah and Al- chibayish), Missan (Amara and Qalaat Salih) and Basrah (Al-Haretha, Al-Madena and Al- Deer). The current study results revealed to eight species of hard ticks belong to genus Hyalomma as: H. truncatum, H. excavatum, H. anatolicum, H. marginatum, H. impeltatum, H. rufipes, H. scupense, H. dromedarii. As the current results showed that buffaloes are considered a new host for three species of them in Iraq; they are which include the following : H. truncatum, H. impeltatum, and H. rufipes. ACKNOWLEDGEMENTS The authors would like to thank the scientific team in the Vertebrates lab of Iraq Natural History Research Center and Museum, University of Baghdad for helping in collecting of specimens. CONFLICT OF INTEREST STATEMENT The authors declare that there are no conflicts of interest regarding the publication of this manuscript. LITERATURE CITED Abdul Hussain, M. A. and Awad, H. A. 2005. A taxonomic and epidemiological study of the hard ticks on domestic animals in Basrah Governorate. Ph.D. thesis, Collage of Science, University of Basrah. Basrah Journal of Science, 23(1): 93-108. Abid, H. S. and Fazaa, N. A. 2007. Water buffalo in the Iraqi Marshes Thi Qar and Missan Governorates . Status Report, 29 pp. Ahmad, M., Khan, R. A., Ullah, Z., Mahmood, S., Khan, M. S., Khan, M. 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Bubalus bubalis (Linnaeus, 1758) القراد الصلب من الجاموستشخيص في العراق زينب علوان مكاوي و أفكار مسلم هادي جامعة بغداد، بغداد، العراق /مركز بحوث و متحف التأريخ الطبيعي 20/6/2023، تأريخ النشر: 13/3/2023القبول: ، تأريخ 14/1/2023تأريخ االستالم: الخالصة ت خارجية تصيب املاشية في كل منطقة جغرافية في ( طفيلياAcari: Ixodidaeالقراد ) العالم وهي ناقالت للعديد من مسببات األمراض الفيروسية والبكتيرية واألولية لكل من الحيوانات والبشر. هناك القليل من املعلومات املتاحة حول انواع القراد التي تصيب ددت الدراسة الحالية في العراق. ح Bubalus bubalis (Linnaeus, 1758) الجاموس بعض املناطق الوسطى والجنوبية مثل: بغداد، أنواع القراد املتطفلة على الجاموس في جاموس 150كربالء، الكوت، الديوانية، الناصرية، العمارة والبصرة. تم فحص إجمالي عينة من 172٪، حيث تم عزل 66.66بحثا عن القراد الصلب وكانت نسبة اإلصابة ئج الحالية أن ٪( اناث. أظهرت النتا39.53) 68٪( ذكور و 58.4) 104القراد الصلب منها على Hyalommaثمانية أنواع من القراد الصلب تصيب الجاموس تنتمي إلى جنس ال H. truncatum (50.66%)، H. excavatum (24%) ،H. anatolicum : النحو التالي (16%) ،H. marginatum (8%) ،H. impeltatum (8%)،H. rufipes (5.33%) ، H. scupense (4%) وH. dromedarii (2.66 على التوالي. كما تمت مناقشة انتشار )% مع دراسات سابقة في العراق والعالم. حيث أن النتائج الحالية هذه األنواع في الجاموس .H. truncatum ،H: ضمت تعتبر الجاموس عائل جديد لثالثة أنواع منها في العراق impeltatum و ،H. rufipes.