Online first
Current issue
Archive
Special Issues
About the Journal
Publication Ethics
Anti-Plagiarism system
Instructions for Authors
Instructions for Reviewers
Editorial Board
Editorial Office
Contact
Reviewers
All Reviewers
2024
2023
2022
2021
2020
2019
2018
2017
2016
General Data Protection Regulation (RODO)
RESEARCH PAPER
Conspecific hyperparasitism in the Hyalomma excavatum tick and considerations on the
biological and epidemiological implications of this phenomenon
1
Chair and Department of Biology and Parasitology, Medical University, Lublin, Poland
2
Institute of Parasitology, Slovak Academy of Sciences, Slovak Republic
3
Institute of Zoology, Slovak Academy of Sciences, Slovak Republic
Corresponding author
Alicja Buczek
Medical University, Chair and Department of Biology and Parasitology, ul. Radziwiłłowska 11, 20-080, Lublin, Poland
Medical University, Chair and Department of Biology and Parasitology, ul. Radziwiłłowska 11, 20-080, Lublin, Poland
Ann Agric Environ Med. 2019;26(4):548-554
KEYWORDS
TOPICS
ABSTRACT
Introduction:
This study presents for the first time a case of Hyalomma excavatum hyperparasitism and an analysis of this phenomenon in terms of its potential role in the biology of ticks and epidemiology of tick-borne diseases.
Material and methods:
Two partially engorged H. excavatum females, one fully engorged female, and 5 males were collected from a naïve rabbit and placed together in a rearing chamber at a temperature of 25°C and 75% humidity.
Results:
3–4 days after tick detachment from the host’s skin, one partially engorged H. excavatum female was observed attached to the idiosoma of the fully engorged conspecific female.
Conclusions:
This study and observations of other authors confirm that partially engorged ixodid ticks can re-infest the host, and even co-feeding fully engorged ticks in order to collect the blood meal that is indispensable for important physiological processes. However, inefficient feeding of a partially engorged female on another conspecific female may reduce its reproductive performance and disturb the development of eggs and larvae. It seems that parasitism of a tick on another conspecific specimen, when at least one of them is infected by a microorganism, may be a yet poorly explored route of transmission of pathogens or symbionts between the ticks. Initiation of feeding by a hungry or partially engorged tick on a fully engorged specimen is an attempt to obtain food in the drastic conditions of the absence of a target host. Tick hyperparasitism with concurrent pathogen transmission can contribute to the genospecific diversity of pathogens in vectors and hosts.
This study presents for the first time a case of Hyalomma excavatum hyperparasitism and an analysis of this phenomenon in terms of its potential role in the biology of ticks and epidemiology of tick-borne diseases.
Material and methods:
Two partially engorged H. excavatum females, one fully engorged female, and 5 males were collected from a naïve rabbit and placed together in a rearing chamber at a temperature of 25°C and 75% humidity.
Results:
3–4 days after tick detachment from the host’s skin, one partially engorged H. excavatum female was observed attached to the idiosoma of the fully engorged conspecific female.
Conclusions:
This study and observations of other authors confirm that partially engorged ixodid ticks can re-infest the host, and even co-feeding fully engorged ticks in order to collect the blood meal that is indispensable for important physiological processes. However, inefficient feeding of a partially engorged female on another conspecific female may reduce its reproductive performance and disturb the development of eggs and larvae. It seems that parasitism of a tick on another conspecific specimen, when at least one of them is infected by a microorganism, may be a yet poorly explored route of transmission of pathogens or symbionts between the ticks. Initiation of feeding by a hungry or partially engorged tick on a fully engorged specimen is an attempt to obtain food in the drastic conditions of the absence of a target host. Tick hyperparasitism with concurrent pathogen transmission can contribute to the genospecific diversity of pathogens in vectors and hosts.
REFERENCES (73)
1.
de la Fuente J, Estrada-Peña A, Venzal JM, Kocan KM, Sonenshine DE. Overview: Ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci. 2008; 13: 6938–6946.
2.
Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004; 129: S3–14.
3.
Dantas-Torres F, Chomel BB, Otranto D. Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol. 2012; 28(10): 437–446.
4.
Ghosh S, Nagar G. Problem of ticks and tick-borne diseases in India with special emphasis on progress in tick control research: A review. J Vector Borne Dis. 2014; 51: 259–270.
5.
Kemp D, Stone B, Binnington K. Tick attachment and feeding: Role of the mouthparts, feeding apparatus, salivary gland secretions and the host response. In: Obenchain F, Galun R, editors, Physiology of Ticks. Pergamon Press, Oxford; 1982. p. 119–168.
6.
Šimo L, Kazmirova M, Richardson J, Bonnet SI. The essential role of tick salivary glands and saliva in tick feeding and pathogen transmission. Front Cell Infect Microbiol. 2017; 7: 281.
8.
Londoňo IM. Transmission of microfilariae and infective larvae of Dipetalonema viteae (Filarioidea) among vector ticks, Ornithodoros tartakowskyi (Argasidae), and loss of microfilariae in coxal fluid. J Parasitol. 1976; 62(5): 786–788.
9.
Moorhouse DE, Heath AC. Parasitism of female ticks by males of the genus Ixodes. J Med Entomol. 1975; 12: 571–572.
10.
Camicas JL, Hervy JP, Adam F, Morel PC. The ticks of the world: nomenclature, described stages, hosts, distribution (Acaridida, Ixodida). Orstom, Paris, 1998.
11.
Estrada-Peña A, Venzal JM. Climate niches of tick species in the Mediterranean region: modeling of occurrence data, distributional constraints, and impact of climate change. J Med Entomol. 2007; 44(6): 1130–1138.
12.
Riabi HRA, Atarodi A. Faunistic study of hard ticks (Ixodidae) of domestic ruminants in the Southern Khorasan-e-Razavi in comparing with other regions of the Province in 2012 Iran. J Vet Adv. 2014; 4(5): 508–515.
13.
Chhillar S, Chhilar JS, Kaur H. Investigations on some hard ticks (Acari: Ixodidae) infesting domestic buffalo and cattle from Haryana, India. J Entomol Zool Stud. 2014; 2(4): 99–104.
14.
Kar S, Dervis E, Akın A, Ergonul O, Gargili A. Preferences of different tick species for human hosts in Turkey. Exp Appl Acarol. 2013; 61(3): 349–355.
15.
Keskin A, Bulut YE, Keskin A, Bursali A. Tick attachment sites in humans living in the Tokat province of Turkey. Turk Hij Den Biyol Derg. 2017; 74: 121–128.
16.
Aktas M, Altay K, Ozubek S, Dumanli N. A survey of ixodid ticks feeding on cattle and prevalence of tick-borne pathogens in the Black Sea region of Turkey. Vet Parasitol. 2012; 187(3–4): 567–571.
17.
Psaroulaki A, Ragiadakou D, Kouris G, Papadopoulos B, Chaniotis B, Tselentis Y. Ticks, tick-borne rickettsiae, and Coxiella burnetii in the Greek Island of Cephalonia. Ann N Y Acad Sci. 2006; 1078: 389–399.
18.
Ghashghaei O, Nourollahi-Fard SR, Khalili M, Sharifi H. A survey of ixodid ticks feeding on cattle and molecular detection of Coxiella burnetii from ticks in Southeast Iran. Turk J Vet Anim Sci. 2017; 41(1): 46–50.
19.
Chochlakis D, Ioannou I, Sandalakis V, Dimitriou T, Kassinis N, Papadopoulos B, Tselentis Y, Psaroulaki A. Spotted Fever Group Rickettsiae in Ticks in Cyprus. Microb Ecol. 2012; 63(2): 314–323.
20.
Leulmi H, Aouadi A, Bitam I, Bessas A, Benakhla A, Raoult D, Parola P. Detection of Bartonella tamiae, Coxiella burnetii and rickettsiae in arthropods and tissues from wild and domestic animals in northeastern Algeria. Parasit Vectors. 2016; 9: 27.
21.
Akuffo R, Brandful JAM, Zayed A, Adjei A, Watany N, Fahmy NT, Hughes R, Doman B, Voegborlo SV, Aziati D, Pratt D, Awuni JA, Adams N, Dueger E. Crimean-Congo hemorrhagic fever virus in livestock ticks and animal handler seroprevalence at an abattoir in Ghana. BMC Infect Dis. 2016; 16: 324.
22.
Zavitsanou A, Babatsikou F, Koutis C. Crimean Congo hemorrhagic fever: an emerging tick-borne disease. Health Sci J. 2009; 3(1): 10–18.
23.
Orkun Ö, Karaer Z, Çakmak A, Nalbantoğlu S. Identification of TickBorne Pathogens in Ticks Feeding on Humans in Turkey. PLoS Negl Trop Dis. 2014; 8: e3067.
24.
Sergent A. Presentation d’une nymphe de tique parasitant une autre nymphe de la meˆme espe`ce. Bull Soc Hist Nat Afr N. 1930; 21: 195 (in French).
25.
Usakov UY. Homoparasitism in the Ixodic ticks. Zool Zh. 1961; 40: 608 (in Russian).
26.
Winston PW, Bates DH. Saturated Solutions for the Control of Humidity in Biological Research. Ecology. 1960; 41: 232–237.
27.
Labruna MB, Ahid SMM, Soares HS, Suassuna ACD. Hyperparasitism in Amblyomma rotundatum (Acari: Ixodidae). J Parasitol. 2007; 93: 1531–1532.
28.
Anastos G. Accidental Parasitism of a tick by a tick. Psyche. 1948; 55: 36–37.
29.
Moorhouse DE. Observations on copulation in Ixodes holocyclus Neumann and the feeding of the male. J Med Entomol. 1966; 3(2): 168–171.
30.
Norval RAI. Copulation and feeding in males of Ixodes pilosus Koch 1844 (Acarina: Ixodidae). J Ent Soc Sth Africa. 1974; 37: 129–133.
31.
Nilsson A. Parasitism of female Ixodes trianguliceps by the males. Oikos. 1975; 26: 295–298.
32.
Ntiamoa-Baidu Y. Parasitism of female Ixodes (Afrixodes) moreli (Acari: Ixodidae) by males. J Med Entomol. 1986; 23(5): 484–488.
33.
Alekseev AN, Dubinina HV. Exchange of Borrelia burgdorferi between Ixodes persulcatus (Ixodidae: Acarina) sexual partners. J Med Entomol. 1996; 33(3): 351–354.
34.
Alekseev AN, Dubinina HV. Some aspects of mite (Oppiidae) and tick (Ixodidae) pathology as a result of anthropogenic pressure. In: Mitchell R, HornDJ, Needham GR and Welbourn WC, editors, Acarology IX. vol. 1. Ohio Biological Survey, Columbus; 1996. p. 117–20.
35.
Alekseev AN, Dubinina HV. Enhancement of risk of tick-borne infection: environmental and parasitological aspects of the problem. J Med Entomol. 2008; 45(4): 812–815.
36.
Žygutienė M, Alekseev A, Dubinina H, Kazlauskienė R. Evidence for a risk of tick-borne infection in the city parks of Vilnius, Lithuania. Ekologija. 2008; 54(1): 40–43.
37.
Nikitin AY, Morozov IM. Exoskeleton anomalies among taiga tick males from populations of the Asiatic part of Russia. Parazitologiia, 2017; 51: 38–44 (in Russian).
38.
Boxler B, Odermat P, Haag-Wackernagel D. Host finding of the pigeon tick Argas reflexus. Med Vet Entomol. 2016; 30(2): 193–199.
39.
Buczek A, Zając Z, Woźniak A, Kulina D, Bartosik K. Locomotor activity of adult Dermacentor reticulatus ticks (Ixodida: Ixodidae) in natural conditions. Ann Agric Environ Med. 2017; 24(2): 271–275.
40.
Carroll JF, Schmidtmann ET. Dispersal of blacklegged tick (Acari: Ixodidae) nymphs and adults at the woods-pasture interface. J Med Entomol. 1996; 33: 554–558.
41.
Černý V. Horizontal migration at the tick (Ixodes ricinus L.). Folia Zool. 1959; 8: 208–212.
43.
Bartosik K, Buczek A. The impact of intensity of invasion of Ixodes ricinus and Dermacentor reticulatus on the course of the parasitic phase. Ann Agric Environ Med. 2012; 19(4): 651–655.
44.
Buczek A, Bartosik K, Zając Z, Stanko M. Host-feeding behaviour of Dermacentor reticulatus and Dermacentor marginatus in mono-specific and inter-specific infestations. Parasit Vectors. 2015; 8: 470.
45.
Rechav Y, Hay L. The effects of nutritional status of rabbits and sheep on their resistance to the ticks Rhipicephalus evertsi evertsi and R. appendiculatus. Exp Appl Acarol. 1992; 15(3): 171–179.
46.
Heinze DM, Carmical JR, Aronson JF, Alarcon-Chaidez F, Wikel S, Thangamani S. Murine cutaneous responses to the rocky mountain spotted fever vector, Dermacentor andersoni, feeding. Front Microbiol. 2014; 5: 198.
47.
Buczek A, Lachowska-Kotowska P, Bartosik K. The effect of synthetic pyrethroids on the attachment and host-feeding behaviour in Dermacentor reticulatus females (Ixodida: Amblyommidae). Parasit Vectors. 2015; 8: 366.
48.
Tsunoda T. Detachment of hard ticks (Acari: Ixodidae) from hunted sika deer (Cervus nippon). Exp Appl Acarol. 2014; 63(4): 545–550.
49.
Sonenshine DE, Roe RM. Biology of Ticks 2nd Edition. Vol. 1 Oxford University Press, New York, 2014.
50.
Řeháček J. Rickettsia slovaca – the organism and its ecology. Academia, Prague, 1984.
51.
Votava CL, Rabalais FC, Ashley DC. Transmission of Dipetalonema viteae by hyperparasitism in Ornithodorus tartakovskyi. J Parasitol. 1974; 60: 479.
52.
Helmy N, Khalil GM, Hoogstraal H. Hyperparasitism in Ornithodoros erraticus. J Parasitol. 1983; 69(1): 229–233.
53.
Samsinakova A, Kalalova S, Daniel M, Dusbabek F, Honzakova E, Černý V. Entomogenous fungi associated with the tick Ixodes ricinus (L.). Folia Parasitol. 1974; 21(1): 39–48.
54.
Yoder JA, Hanson PE, Zettler LW, Benoit JB, Ghisays F, Piskin K. Internal and external mycoflora of the American dog tick, Dermacentor variabilis (Acari: Ixodidae), and its ecological implications. Appl Environ Microbiol. 2003; 69(8): 4994–4996.
55.
Greengarten PJ, Tuininga AR, Morath SU, Falco RC, Norelus H, Daniels TJ. Occurrence of soil- and tick-borne fungi and related virulence tests for pathogenicity to Ixodes scapularis (Acari: Ixodidae). J Med Entomol. 2011; 48(2): 337–344.
56.
Noda H, Munderloh UG, Kurtti TJ. Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl Environ Microbiol. 1997; 63(10): 3926–3932.
57.
Crowder CD, Matthews HE, Schutzer S, Rounds MA, Luft BJ, Nolte O, Campbell SR, Phillipson CA, Li F, Sampath R, Ecker DJ, Eshoo MW. Genotypic variation and mixtures of Lyme Borrelia in Ixodes ticks from North America and Europe. PLoS One. 2010; 5: e10650.
58.
Yashina L, Petrova I, Seregin S, Vyshemirskii O, Lvov D, Aristova V, Kuhn J, Morzunov S, Gutorov V, Kuzina I, Tyunnikov G, Netesov S, Petrov V. Genetic variability of Crimean-Congo haemorrhagic fever virus in Russia and Central Asia. J Gen Virol. 2003; 84: 1199–1206.
59.
Alekseev AN, Semenov AV, Dubinina HV. Evidence of Babesia microti infection in multi-infected Ixodes persulcatus ticks in Russia. Exp Appl Acarol. 2003; 29(3–4): 345–353.
60.
Stańczak J, Gabre RM, Kruminis-Łozowska W, Racewicz M, KubicaBiernat B. Ixodes ricinus as a vector of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in urban and suburban forests. Ann Agric Environ Med. 2004; 11(1): 109–114.
61.
Otranto D, Dantas-Torres F, Giannelli A, Latrofa M.S, Cascio A, Cazzin S, Ravagnan S, Montarsi F, Zanzani SA, Manfredi MT, Capelli G. Ticks infesting humans in Italy and associated pathogens. Parasit Vectors. 2014; 7: 328.
62.
Asman M, Nowak-Chmura M, Solarz K, Szilman E, Semla M, Zyśk B. Anaplasma phagocytophilum, Babesia microti, Borrelia burgdorferi sensu lato, and Toxoplasma gondii in Ixodes ricinus (Acari, Ixodida) ticks collected from Slowinski National Park (Northern Poland). J Vector Ecol. 2017; 42(1): 200–202.
63.
Raileanu C, Moutailler S, Pavel I, Porea D, Mihalca AD, Savuta G, Vayssier-Taussat M. Borrelia diversity and co-infection with other tick borne pathogens in ticks. Front Cell Infect Microbiol. 2017; 7: 36.
64.
Zając V, Wójcik-Fatla A, Sawczyn A, Cisak E, Sroka J, Kloc A, Zając Z, Buczek A, Dutkiewicz J, Bartosik K. Prevalence of infections and coinfections with 6 pathogens in Dermacentor reticulatus ticks collected in eastern Poland. Ann Agric Environ Med. 2017; 24(1): 26–32.
65.
Moniuszko A, Dunaj J, Święcicka I, Zambrowski G, ChmielewskaBadora J, Żukiewicz-Sobczak W, Zajkowska J, Czupryna P, Kondrusik M, Grygorczuk S, Swierzbinska R, Pancewicz S. Co-infections with Borrelia species, Anaplasma phagocytophilum and Babesia spp. in patients with tick-borne encephalitis. Eur J Clin Microbiol Infect Dis. 2014; 33(10): 1835–1841.
66.
Jahfari S, Hofhuis A, Fonville M, van der Giessen J, van Pelt W, Sprong H. Molecular Detection of Tick-Borne Pathogens in Humans with Tick Bites and Erythema Migrans, in the Netherlands. PLoS Negl Trop Dis. 2016; 10(10): e0005042.
67.
Vascellari M, Ravagnan S, Carminato A, Cazzin S, Carli E, Da Rold G, Lucchese L, Natale A, Otranto D, Capelli G. Exposure to vector-borne pathogens in candidate blood donor and free-roaming dogs of northeast Italy. Parasit Vectors. 2016; 9: 369.
68.
Beck AF, Holscher KH, Butler JF. Life cycle of Ornithodoros turicata americanus (Acari: Argasidae) in the laboratory. J Med Entomol. 1986; 23(3): 313–319.
69.
Davis GE. Ornithodoros parkeri Cooley: Observations on the Biology of This Tick. J Parasitol. 1941; 27(5): 425–433.
70.
Endris RG, Haslett TM, Monahan MJ, Phillips JG. Laboratory biology of Ornithodoros (Alectorobius) puertoricensis (Acari: Argasidae). J Med Entomol. 1991; 28(1): 49–62.
71.
Oliver JH Jr, McKeever S, Pound JM. Parasitism of larval Ixodes ticks by chigger mites and fed female Ornithodoros ticks by Ornithodoros males. J Parasitol. 1986; 72(5): 811–812.
72.
Alekseev AN, Dubinina HV. Venereal and cannibalistic ways of Borrelia burgdorferi sensu lato exchange between males and females of Ixodes persulcatus. Rocz Akad Med Bialymst. 1996; 41: 103–110.
73.
Durden LA, Gerlach RF, Beckmen KB, Greiman SE. Hyperparasitism and non-nidicolous mating by male Ixodes angustus ticks (Acari: Ixodidae). J Med Entomol. 2018; 55(3): 766–768.
| eISSN: | 1898-2263 |
| ISSN: | 1232-1966 |
Generation of the DOI (Digital Object Identifier) - task financed under the agreement No NrRCN/SP/0532/2021/1 by the Minister of Science and Higher
© 2006-2025 Journal hosting platform by Bentus
We process personal data collected when visiting the website. The function of obtaining information about users and their behavior is carried out by voluntarily entered information in forms and saving cookies in end devices. Data, including cookies, are used to provide services, improve the user experience and to analyze the traffic in accordance with the Privacy policy. Data are also collected and processed by Google Analytics tool (more).
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
You can change cookies settings in your browser. Restricted use of cookies in the browser configuration may affect some functionalities of the website.
