Viktor Brygadyrenko, Daria Reshetniak


Clitellocephalus ophoni (Tuzet and Ormieres, 1956) Clopton, 2002, is one of the parasites of a common ground beetle species, Harpalus rufipes (De Geer, 1774), inhabiting practically the entire temperate zone of Eurasia. Photographs of 177 gamonts and 74 syzygies of C. ophoni from specimens of three populations of H. rufipes collected from the countryside near Dnipropetrovsk (Ukraine), were analyzed according to 15 linear characteristics and 18 indices for gamonts and 6 indices for syzygies. The coefficient of variation (CV) for the majority of linear parameters for gamonts ranged between 28.2-71.3%. Out of 15 linear parameters, only 6 showed a normal distribution; the others showed a statistically significant asymmetry (the maximum indicators on the histogram of distribution were inclined to the area of minimum value). The distribution of all 18 morphological indices diverged from the norm. Two maximum indicators were registered in the disposition of the widest point of the protomerite and deutomerite. The minimum CV was registered for the ratio of gamont length to the length of its deutomerite. The size ratios of the primite and satellite in the syzygies were more constant than the morphological indices for the gamonts. The sex of the host does not affect the length of the protomerite and deutomerite, but does affect their width, the disposition of the nucleus and the widest point of the deutomerite. The length of the protomerite and deutomerite relative to the length of the gamont is better described through linear functions, while their width has a nonlinear dynamic and is better described through parabolic function. The ratio of morphometric indices to total length of C. ophoni gamonts is also better described through nonlinear functions. The data obtained on the morphological variability of C. ophoni needs to be compared with the results for artificially infected individuals of other Harpalus species.


Key words: Clitellocephalus; Harpalus rufipes; gregarine; morphometric characteristics; ratio of morphometric indices


Received: September 23, 2015; Revised: November 30, 2015; Accepted: December 3, 2015; Published online: May 10, 2016

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Kryzhanovskij OL, Belousov IA, Kabak II, Kataev BM, Makarov KV, Shilenkov VG. A checklist of the ground-beetles of Russia and adjacent lands (Insecta, Coleoptera, Carabidae). Sofia, Moscow: Pensoft Publishers; 1995.

Harrison S, Gallant ER. Behavioural studies of Harpalus rufipes De Geer: An important weed seed predator in northeastern US agroecosystems. Int J Ecol. 2012;2012:846546.

Zhang J, Drummond FA, Liebman M, Hartke A. Phenology and dispersal of Harpalus rufipes De Geer (Coleoptera: Carabidae) in agroecosystems in Maine. J Agric Urban Ent. 1997;14(2):171-86.

Hartke A, Drummond FA, Liebman M. Seed feeding, seed caching, and burrowing behaviors of Harpalus rufipes De Geer larvae (Coleoptera: Carabidae) in the Maine potato agroecosystem. Biol Control. 1998;13(2):91-100.

Midtgaard F. Is dispersal density-dependent in carabid beetles? A field experiment with Harpalus rufipes (De Geer) and Pterostichus niger (Schaller) (Col., Carabidae). J Appl Ent. 1999;123(1):9-12.

Matalin AV. Typology of the life cycles of ground beetles (Coleoptera, Carabidae) of the Western Palearctic. Zool Zh. 2007;86(10):1196-210.

Luff ML. The biology of the ground beetle Harpalus rufipes in a strawberry field in Northumberland. Ann Appl Biol. 1980;94:153-64.

Shearin AF., Reberg-Horton SC, Gallandt ER. Cover crop effects on the activity-density of the weed seed predator Harpalus rufipes (Coleoptera: Carabidae). Weed Sci. 2008;56(3):442-50.

Reshetniak DY, Brygadyrenko VV. Optimizing of Harpalus rufipes (Coleoptera, Carabidae) diet under laboratory conditions. Visn Dnipropetr Univ Ser Biol Ekol. 2013;21(1):38-42.

Brygadyrenko VV, Reshetniak DY. Morphological variability among populations of Harpalus rufipes (Coleoptera, Carabidae): What is more important – the mean values or statistical peculiarities of distribution in the population? Folia Oecol. 2014;41(2):109-33.

Brygadyrenko VV, Reshetniak DY. Trophic preferences of Harpalus rufipes (Coleoptera, Carabidae) with regard to fruits and seeds of agricultural crops in conditions of laboratory experiment. Baltic J Coleopterol. 2014;14(2):179-90.

Petrusenko AA, Petrusenko SV. The family of ground beetles (Carabidae). In: Vasil'ev VP, editor. Pests of Agricultural Crops and Forest Plantations. Kiev: Urozhaj; 1973. p. 363-87.

Birthisel SK, Gallandt ER, Jabbour R. Habitat effects on second-order predation of the seed predator Harpalus rufipes and implications for weed seedbank management. Biol Control. 2014;70:65-72.

Thiele HU. Carabid beetles in their environments. Berlin: Springer-Verlag; 1977.

Korolev ОV, Brygadyrenko VV. Influence of individual variation in the trophic spectra of Pterostichus melanarius (Coleoptera, Carabidae) on the adaptation possibilities of its population. Folia Oecol. 2014;41(1):34-43.

Geus A. Sporentierchen Sporoza, Die Gregarinida: Die Tierwelt Deutschlands. Teil 57. Jena: VEB Gustav Fischer; 1969.

Sienkiewicz P, Lipa JJ. Prevalence of eugregarines (Apicomplexa: Eugregarinida) parasitizing in ground beetles (Coleoptera, Carabidae) in various habitats. Polish J Entomol. 2009;78:351-68.

Sienkiewicz P, Lipa JJ. Chrząszcze z rodziny biegaczowatych (Coleoptera: Carabidae) jako żywiciele pasożytniczych i komensalicznych eugregaryn (Apicomplexa: Eugregarinorida) – przegląd badań z terenu Polski. Wiad Entomol. 2010;29(4):289-95.

Clopton RE, Nolte CM. Clitellocephalus americanus n. gen., n. sp. (Apicomplexa: Eugregarinida: Gregarinidae) from Cratacanthus dubius (Coleoptera: Carabidae: Harpalinae) in the Nebraska Sandhills and Clitellocephalus ophoni n. comb. (Apicomplexa: Eugregarinida: Gregarinidae) from Ophonus pubescens (Coleoptera: Carabidae: Harpalinae) in Sète, France. J Parasitol. 2002;88:750-57.

Sienkiewicz P, Lipa JJ. Clitellocephalus ophoni (Tuzet et Ormieres, 1956) (Apicomplexa: Eugregarinida: Gregarinidae) recorded in Poland on strawberry seed beetle Harpalus (Ophonus) rufipes (De Geer, 1774) (Coleoptera: Carabidae). Biol Letters. 2009;46(1):43-50.

Tuzet O, Ormieres R. Sur quelques Gregarines de le region de Sete. Ann Parasit Hum Comp. 1956;31:317-30.

Desportes I, Jolivet P, Mateu J, Theodorides J. Présence de Gregarina ophoni Tuzet et Ormieres 1956 (Eugregarina Gregarinidae) chez Notobia bradytoides (Bates) (Coléoptère Carabidae) en Equateur. Ann Parasit Hum Comp. 1980;55:145-6.

Desportes I, Schrével J, editors. Treatise on Zoology - Anatomy, Taxonomy, Biology. The Gregarines (2 vols). Paris: Brill; 2013. 781 p.

Korolev OV, Shendrik LI, Bojko ОО, Brygadyrenko VV. Gregarinida and Mermithida parasitism in Pterostichus melanarius (Coleoptera, Carabidae) in Dnipropetrovs’k region. Vìsn Dnìpropetr Unìv Ser Bìol Ekol. 2009;17(2):50-4.

Clopton RE. Synoptic revision of Blabericola (Apicomplexa: Eugregarinida: Blabericolidae) parasitizing blaberid cockroaches (Dictyoptera: Blaberidae), with comments on delineating gregarine species boundaries. J Parasitol. 2012;98(3):572-83.

Clopton RE. Revision of the genus Xiphocephalus and description of Xiphocephalus ellisi n. sp. (Apicomplexa: Eugregarinida: Stylocephalidae) from Eleodes opacus (Coleoptera: Tenebrionidae) in the western Nebraska Sandhills. J Parasitol. 1999;85:84-9.

Clopton RE, Hays JJ. Revision of the genus Protomagalhaensia and description of Protomagalhaensia wolfi n. comb. (Apicomplexa: Eugregarinida: Hirmocystidae) and Leidyana haasi n. comb. (Apicomplexa: Eugregarinida: Leidyanidae) parasitizing the lobster cockroach, Nauphoeta cinerea (Dictyoptera: Blaberidae). Comp Parasitol. 2006;73(2):137-56.

Brygadyrenko VV, Svyrydchenko AO. Influence of the gregarine Stenophora julipusilli (Eugregarinorida, Stenophoridae) on the trophic activity of Rossiulus kessleri (Diplopoda, Julidae). Folia Oecol. 2015;42(1):10-20.

Abro A. Gregarines: Their effects on damselflies (Odonata: Zygoptera). Ent Scand 1971;2:294-300.

Siva-Jothy MT, Plaistow SJ. Fitness cost of eugregarine parasitism in a damselfly. Ecol Entomol. 1999;24:465-70.

Canales-Lazcano J, Contreras-Garduño J, Córdoba-Aguilar A. Fitness-related attributes and gregarine burden in a non-territorial damselfly Enallagma praevarum Hagen (Zygoptera: Coenagrionidae). Odonatologica. 2005;34(2):123-30.

Locklin JL, Vodopich DS. Patterns of gregarine parasitism in dragonflies: Host, habitat, and seasonality. Parasitol Res. 2010;107:75-87.

Zuk M. The effects of gregarine parasites, body size, and time of day on spermatophore production and sexual selection in field crickets. Behav Ecol Sociobiol. 1987;21:65-72.

Zuk M. The effects of gregarine parasites on longevity, weight loss, fecundity and developmental time in the field crickets Gryllus veletis and G. pennsylvanicus. Ecol Entomol. 1987;12:349-54.

Harry OG. Gregarines: Their effect on the growth of the desert locust (Schizogregaria). Nature 1970;225:964-6.

Lord JC, Omoto CK. Eugregarines reduce susceptibility of the hide beetle, Dermestes maculatus, to apicomplexan pathogens and retard larval development. J Invertebr Pathol. 2012;111:186-8.

Rodriguez Y, Omoto CK, Gomulkiewicz R. Individual and population effects of Eugregarine, Gregarina niphandrodes (Eugregarinida: Gregarinidae), on Tenebrio molitor (Coleoptera: Tenebrionidae). Environ Entomol. 2007;36:689-93.

Bouwma AM, Howard KJ, Jeanne RL. Parasitism in a social wasp: Effect of gregarines on foraging behavior, colony productivity, and adult mortality. Behav Ecol Sociobiol. 2005;59:222-33.

Bollatti F, Ceballos A. Effect of gregarines (Apicomplexa: Sporozoa) on survival and weight loss of Victorwithius similis Beier, 1959 (Arachnida: Pseudoscorpiones). J Invertebr Pathol. 2014;117:13-8.

Rueckert S, Leander BS. Morphology and phylogenetic position of two novel marine gregarines (Apicomplexa, Eugregarinorida) from the intestines of North-Eastern Pacific ascidians. Zool Scr. 2015;37(6):637-45.

Diakin AI, Paskerova GG. Morphology of Urospora chiridotae (Sporozoa: Gregarinomorpha: Eugregarinida) from sea cucumber Chiridota laevis (Echinodermata: Holothuroidea: Apoda). Parazitologiia. 2004;38(3):225-38.

Rueckert S, Villette PMAH, Leander BS. Species boundaries in gregarine apicomplexan parasites: A case study – comparison of morphometric and molecular variability in Lecudina cf. tuzetae (Eugregarinorida, Lecudinidae). J Eukaryot Microbiol. 2011;58(4):275-83.

Hussain KJ, Krishnan SM, Johny S, Whitman DW. Phenotypic plasticity in a gregarine parasite (Apicomplexa: Eugregarinordia) infecting grasshoppers. Comp Parasitol. 2013;80(2):233-9.

Giglio A, Giulianini PG, Zetto T, Talarico F. Effects of the pesticide dimethoate on a non-target generalist carabid, Pterostichus melas italicus (Dejean, 1828) (Coleoptera: Carabidae). Ital J Zool. 2011;78(4):471-7.

Schluter D. The ecology of adaptive radiation. Oxford: Oxford University Press; 2000.


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