Seasonal dynamic of the occurrence of the gregarines infection of Harpalus rufipes (Coleoptera, Carabidae) in agroecosystem

  • D. Y. Reshetnyak Oles Honchar Dnipropetrovsk National University
Keywords: extent of infestation, intensity of infection, gamonts, syzygies


Relationships in the “parasite-host” system are closely interrelated and occur at all levels from the molecular to behavioral and population ones. There are two models of realization of these relations. The first case is when the parasites are uniformly distributed in the host population. High extensiveness of invasion is accompanied by its low intensity. The second case is when a part of host population is infected with parasites, but the negative impact is manifested to the maximum extent. Invasion of the ground beetle Harpalus rufipes (De Geer, 1774), dwelling in sweet corn agroecosystems located in the vicinity of Dnipropetrovsk near Doslidnoe village, by several gregarines species is investigated in this study. H. rufipes is an abundant, ubiquitous species, living in extremely wide range of terrestrial ecosystems, with especially high populations inhabiting anthropogenically transformed environments. H. rufipes has a wide range of feeding. This species is distributed in the Central and Eastern Europe, and introduced to North America. Gregarines were found in the intestines of 20 individuals of H. rufipes from 190 (10.5%): Gregarina ovata Dufour, 1828, G. steini Berndt, 1902, G. amarae (Hammerschmidt, 1839) Frantzius, 1848, Clitellocephalus ophoni (Tuzet and Ormieres, 1956) Clopton, 2002, Torogregarina sphinx Clopton, 1998, Gigaductus macrospora Filipponi, 1948 and G. elongatus (Moriggi, 1943) Filipponi, 1948. There is high level of infestation of C. ophoni and G. steini. At the same time, not more than three species of the gregarines were localized in the beetle body. Seasonal dynamic of occurrence of the gregarines is as follows. Maximal indices of occurrence are found at the end of August (22.2%) and minimal ones at the end of June (4.8%). The highest total number of gregarines (383 ind.) is recorded at the end of August, the lowest one is fixed at the beginning of September (33 ind.). Indices of gregarine species dominance are as follows: C. ophoni – 34.0%, G. macrospora – 28.9%, G. steini – 20.6%, T. sphinx – 9.3%, G. amarae – 5.5%, G. ovata – 0.9% and G. elongatus – 0.4%. High temperatures in July and August helped to increase infection of H. rufipes by almost all gregarines compared to cool and wet conditions in June. The highest value of the index of abundance corresponds to the time of high average intensity of infestation by three common species of gregarines. Decline in abundance index by the end of summer and early fall may be due to the death of heavily infected individuals. High level of infection does not cause the pathogenic effect on the host organism.


Birthisel, S.K., Gallandt, E.R., Jabbour, R., 2014. Habitat effects on second-order predation of the seed predator Harpalus rufipes and implications for weed seedbank management. Biol. Control 70, 65–72. >>

Brygadyrenko, V.V., Reshetniak, D.Y., 2014a. 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. 41(2), 109–133.

Brygadyrenko, V.V., Reshetniak, D.Y., 2014b. Trophic preferences of Harpalus rufipes (Coleoptera, Carabidae) with regard to seeds of agricultural crops in conditions of laboratory experiment. Baltic Journal of Coleopterology 14(2), 179–190.

Brygadyrenko, V.V., Svyrydchenko, A.O., 2015. Influence of the gregarine Stenophora julipusilli (Eugregarinorida, Stenophoridae) on the trophic activity of Rossiulus kessleri (Diplopoda, Julidae). Folia Oecol. 42(1), 10–20.

Clopton, R.E., 2006. Two new species of Xiphocephalus in Eleodes tricostata and Eleodes fusiformis (Coleoptera: Tenebrionidae: Eleodini) from the Sandhills of Western Nebraska. J. Parasitol. 92(3), 569–577. >>

Clopton, R.E., 2009. Phylogenetic relationships, evolution, and systematic revision of the septate gregarines (Apicomplexa: Eugregarinorida: Septatorina). Comp. Parasitol. 76(2), 167–190. >>

Clopton, R.E., Cook, T.J., Cook, J.L., 2007. Revision of Geneiorhynchus (Apicomplexa: Eugregarinida: Actinocephalidae: Acanthosporinae) with recognition of four new species of Geneiorhynchus and description of Geneiorhynchus manifestus n. sp. parasitizing naiads of the Green Darner, Anax junius (Odonata: Aeshnidae) in the Texas Big Thicket. Comp. Parasitol. 74(2), 273–285.

Clopton, R.E., Cook, T.J., Cook, J.L., 2008. Trichurispora wellgundis n. g., n. sp. (Apicomplexa: Eugregarinida: Hirmocystidae) parasitizing adult water scavenger beetles, Tropisternus collaris (Coleoptera: Hydrophilidae) in the Texas Big Thicket. Comp. Parasitol. 75(1), 82–91. >>

Clopton, R.E., Nolte, C.M., 2002. 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. 88(4), 750–757.

Dunn, G.A., 1981. Distribution of Harpalus rufipes De Geer in Canada and United States (Coleoptera: Carabidae). Entomol. News 92(5), 186–188.

Dyakin, A.Y., 2004. Vzaimootnosheniya gregarinyi Urospora chiridotae i goloturii Chiridota laevis [The relationship of gregarines Urospora chiridotae and sea cucumbers Chiridota laevis]. V Nauchnaya Sessiya MBS SPbGU. Tezisyi Dokladov. SPb., 47–48 (in Russian).

Gaevskaya, A.V., Machkevsky, V.K., 2001. Problemyi morskoy parazitologii Azovo-Chernomorskogo basseyna. Kontseptualnyiy podhod [The problem of marine parasitology Azov-Black Sea Basin. The conceptual approach]. Ekologiya Morya 57, 36–43 (in Russian).

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

Holusa, J., Lukasova, K., Wegensteiner, R., Grodzki, W., Pernek, M., Weiser, J., 2012. Pathogens of the bark beetle Ips cembrae: microsporidia and gregarines also known from other Ips species. J. Appl. Entomol. 137(3), 181–187.

Hoshide, K, Janovy, J., 2002. The structure of the nucleus of Odonaticola polyhamatus (Gregarinea: Actinocephalidae), a parasite of Mnais strigata (Hagen) (Odonata: Calopterygidae). Acta Protozool. 41, 17–22.

Kim, J.I., Min, J.S., Kwon, M., Choi, J.-Y., Lee, S.H., 2014. Morphological and molecular characterizations of the Gregarina sp. (Apicomplexa: Protozoa) parasitizing on Phaedon brassicae (Coleoptera: Chrysomelidae). J. Asia Pac. Entomol. 17(1), 1–5. >>

Kryzhanovskij, O.L., Belousov, I.A., Kabak, I.I., Kataev, B.M., Makarov, K.V., Shilenkov, V.G., 1995. A checklist of the ground-beetles of Russia and adjacent lands (Insecta, Coleoptera, Carabidae). Pensoft Publishers, Sofia – Moscow. 271 p.

Lebedovskaya, M.V., 2013. Porazhenie dvustvorchatyih mollyuskov r. Chyornaya (Sevastopol) gregarinoy Nematopsis portunidarum (Frenzel, 1885) [The defeat of the bivalves of river Black (Sevastopol) by gregarines Nematopsis portunidarum (Frenzel, 1885)]. Scientific Notes of Vernadsky Taurida National University. Series Biology, chemistry 26(4), 85–93 (in Russian).

Luff, M.L., 1980. The biology of the ground beetle Harpalus rufipes in a strawberry field in Northumberland. Ann. Appl. Biol. 94(2), 153–164. >>

Rodriguez, Y., Omoto, C.K., Gomulkiewicz, R., 2007. Individual and population effects of Eugregarine, Gregarina niphandrodes (Eugregarinida: Gregarinidae), on Tenebrio molitor (Coleoptera: Tenebrionidae). Environ. Entomol. 36(4), 689–693. >>

Schreurs, J., Janovy Jr., J., 2008. Gregarines on a diet: The effects of host starvation on Gregarina confusa Janovy et al., 2007 (Apicomplexa: Eugregarinida) in Tribolium destructor Uyttenboogaart, 1933 (Coleoptera: Tenebrionidae) larvae. J. Parasitol. 94(3), 567–570.

Shearin, A.F., Reberg-Horton, S.C., Gallandt, E.R., 2008. Cover crop effects on the activity-density of the weed seed predator Harpalus rufipes (Coleoptera: Carabidae). Weed Sci. 56(3), 442–450.

Sienkiewicz, P., Lipa, J.J., 2009b. Prevalence of eugregarines (Apicomplexa: Eugregarinida) parasitizing in ground beetles (Coleoptera, Carabidae) in various habitats. Pol. Pismo Entomol. 78, 351–368.

Sienkiewicz, P., Lipa, J.J., 2009а. Clitellocephalus ophoni (Tuzet et Ormi`eres, 1956) (Apicomplexa: Eugregarinida: Gregarinidae) recorded in Poland on strawberry seed beetle Harpalus (Ophonus) rufipes (De Geer, 1774) (Coleoptera: Carabidae). Biol. Letters 46(1), 43–50.

Sienkiewicz, P., Lipa, J.J., 2010. Chrząszcze z rodziny biegaczowatych (Coleoptera: Carabidae) jako żywiciele pasożytniczych i komensalicznych eugregaryn (Apicomplexa: Eugregarinorida) – przegląd badań z terenu Polski. Wiad. Entomol. 29(4), 289–295.

Simdyanov, T.G., 2007. Gregarinea Dufour, 1828 – Gregarinyi [Gregarinea Dufour, 1828 – Gregarines]. In: Alimov, A.F. (Ed.). Protistyi. Rukovodstvo po zoologii [Protists. Guide to zoologists]. Science, SPb. 2, 20–140.

Thiele, H.U., 1977. Carabid beetles in their environments. Springer-Verlag, Berlin. >>

Zhang, J., Drummond, F.A., Liebman, M., Hartke, A., 1997. Phenology and dispersal of Harpalus rufipes De Geer (Coleoptera: Carabidae) in agroecosystems in Maine. J. Agr. Urban Entomol. 14(2), 171–186.

Zubareva, I.M., Bortsova, M.S., 2012. Epizooticheskiy protsess i ego otsenka pri toksokaroze domashnih plotoyadnyih [Epizootic process and its evaluation at toxocarosis of domestic carnivores]. Vestnik Veterinarii 4(63), 45–47.