Article

Article name MORPHOMETRIC VARIABILITY OF GROUND BEETLES BEMBIDION MINIMUM (COLEOPTERA, CARABIDAE): WHO SHOULD CHANGE MORE, MALES OR FEMALES?
Authors

Olexandr Parhomenko, PhD, Department of Biology, Faculty of Natural and Geographical Education and Ecology, National Pedagogical Dragomanov University (Pirogov st., 9, Kyiv, 01601, Ukraine); iD ORCID: https://orcid.org/0000-0002-4608-7813; e-mail: o.v.parhomenko@npu.edu.ua
Vladimír Langraf, PhD, Department of Zoology and Anthropology, Faculty of Natural Sciences, Constantine the Philosopher University in Nitra (Tr. A. Hlinku 1, Nitra, 94901, Slovakia); iD ORCID: https://orcid.org/0000-0002-3839-3036; e-mail: langrafvladimir@gmail.com
Kornélia Petrovičová, PhD, Institute of Plant and Environmental Sciences, Faculty of Agrobiology and Food Resources, Slovak, University of Agriculture in Nitra (Tr. A. Hlinku 2, Nitra, 94901, Slovakia); iD ORCID: https://orcid.org/0000-0002-1581-2517; e-mail: kornelia.petrovicova@gmail.com
Viktoriia Komlyk, PhD, Department of Zoology and Ecology, Faculty of Biology and Ecology, Oles Honchar Dnipro National University (Gagarin av. 72, Dnipro, 49010, Ukraine); iD ORCID: https://orcid.org/0000-0002-3727-5847; e-mail: slinko@ua.fm
Viktor Brygadyrenko, PhD, Department of Zoology and Ecology, Faculty of Biology and Ecology, Oles Honchar Dnipro National University (Gagarin av. 72, Dnipro, 49010, Ukraine); iD ORCID: https://orcid.org/0000-0002-9448-8232; e-mail: brigad@ua.fm

Reference to article

Parhomenko O., Langraf V., Petrovičová K., Komlyk V., Brygadyrenko V. 2022. Morphometric variability of ground beetles Bembidion minimum (Coleoptera, Carabidae): who should change more, males or females?. Nature Conservation Research 7(1): 42–69. https://dx.doi.org/10.24189/ncr.2022.008

Section Research articles
DOI https://dx.doi.org/10.24189/ncr.2022.008
Abstract

Morphological variability can be used as an indicator of the state of invertebrate populations. Microevolutionary processes can show up in the morphological differentiation of populations. This includes differences between morphometric characters in the two sexes. The variability of 12 populations of Bembidion minimum (Coleoptera, Carabidae) was assessed by 24 morphometric characteristics and indices in this article. Bembidion minimum is a halophile that lives in ecosystems of Protected Areas in Ukraine (Black Sea Biosphere Reserve, Dniprovsko-Orilskyi Nature Reserve, Ornithological Sanctuary «Bulakhovsky Liman», Regional Landscape Park «Dniprovi Porogy», Samara Forest). The coefficients of variation for males, females, and combined populations of males and females were estimated in the article. The studied populations inhabited different soil and plant conditions and were under the influence of anthropogenic factors of varying intensity. The redundancy analysis shows three clusters. In the first cluster, morphometric characteristics and indices in both males and females were linked to environmental variables (herb layer, salt, composition of soil). The second cluster had morphometric characteristics and indices in both males and females with a link to environmental variables (pH, litter, recreational load, cattle grazing). The third cluster formed morphometric characteristics and indices in both males and females that are not affected by any environmental variables. The coefficient of variation for most of the linear morphometric characteristics of B. minimum (width of head, length of prothorax, width of prothorax, length of elytra and distance between setae on the elytra) for males was significantly lower than for the combined sample of males and females. The variability of width of elytra and length of body was significantly higher for females than for males. The degree of variability of males, females and their combined sample did not significantly differ for nonlinear morphometric characteristics, as well as for the six morphometric indices (body proportions) studied by us. In general, in the 12 studied populations of B. minimum, the coefficient of variation for most of the studied measurements was insignificantly lower in males (CV = 5.59%) than in females (6.10%) or in the combined sample of males and females (6.75%). The lowest variability in populations of B. minimum was found for morphometric indices: CV = 3.89% for males, CV = 3.76% for females, and CV = 3.86% for the combined population (males + females). The absence of differences in the mean values of the coefficient of variation between males, females and the combined sample of males and females for each individual population suggests that both males and females make a relatively equal contribution to the polymorphism of B. minimum populations. An assessment of the morphological variability of invertebrates, and especially the variation of coefficients of linear parameters and morphometric indices, can be used to indicate the state of ecosystems in Protected Areas in Ukraine and other countries.

Keywords

body length, carabids, coefficient of variation, litter invertebrates, population, sexual dimorphism, morphometrics, zoophagous

Artice information

Received: 27.01.2022. Revised: 04.02.2022. Accepted: 10.02.2022.

The full text of the article
References

Abdel-Dayem M.S. 1998. The Egyptian species of Bembidion Latreille, 1802 (Coleoptera, Carabidae). Bulletin of the Entomological Society of Egypt 76: 181–198.
Andersen I. 1985. Ecomorphological adaptations of riparian Bembidiini species (Coleoptera: Carabidae). Entomologia Generalis 11(1–2): 41–46. DOI: 10.1127/entom.gen/11/1985/41
Avtaeva T.A., Sukhodolskaya R.A., Brygadyrenko V.V. 2021. Modeling the bioclimatic range of Pterostichus melanarius (Coleoptera, Carabidae) in conditions of global climate change. Biosystems Diversity 29(2): 140–150. DOI: 10.15421/012119
Baranovski B.A., Ivanko I.A., Gasso V.J., Ponomarenko O.L., Dubyna D.V., Roshchyna N.O., Karmyzova L.O., Polevа J.L., Nikolaieva V.V. 2021. Biodiversity of the Regional Landscape Park Samara Plavni within the first large reservoir in Europe. Biosystems Diversity 29(2): 160–179. DOI: 10.15421/012121
Baranovski B.А., Karmyzova L.А., Roshchyna N.O., Ivanko I.A., Karas O.G. 2020. Ecological-climatic characteristics of the flora of a floodplain landscape in Southeastern Europe. Biosystems Diversity 28(1): 98–112. DOI: 10.15421/012014
Barton P.S., Gibbk H., Manningk A., Lindenmayer D.B., Cunningham S.A. 2011. Morphological traits as predictors of diet and microhabitat use in a diverse beetle assemblage. Biological Journal of the Linnean Society 102(2): 301–310. DOI: 10.1111/j.1095-8312.2010.01580.x
Belaoussoff S., Kevan P.G., Murphy S., Swanton C. 2003. Assessing tillage disturbance on assemblages of ground beetles (Coleoptera: Carabidae) by using a range of ecological indices. Biodiversity and Conservation 12(5): 851–882. DOI: 10.1023/A:1022811010951
Benítez H.A. 2013. Assessment of patterns of fluctuating asymmetry and sexual dimorphism in carabid body shape. Neotropical Entomology 42(2): 164–169. DOI: 10.1007/s13744-012-0107-z
Benítez H., Briones R., Jerez V. 2011. Intra and Inter-population morphological variation of shape and size of the Chilean magnificent beetle, Ceroglossus chilensis in the Baker River Basin, Chilean Patagonia. Journal of Insect Science 11(1): 94. DOI: 10.1673/031.011.9401
Benítez H.A., Lemic D., Puschel T.A., Gasparic H.V., Kos T., Baric B., Bazok R., Zivkovic I.P. 2018. Fluctuating asymmetry indicates levels of disturbance between agricultural productions: An example in Croatian population of Pterostichus melas melas (Coleptera: Carabidae). Zoologischer Anzeiger 276: 42–49. DOI: 10.1016/J.JCZ.2018.07.003
Boyko O.O., Gugosyan Y.A., Shendrik L.I., Brygadyrenko V.V. 2019. Intraspecific morphological variation in free-living stages of Strongyloides papillosus (Nematoda, Strongyloididae) parasitizing various mammal species. Vestnik Zoologii 53(4): 313–324. DOI: 10.2478/vzoo-2019-0030
Braun S.D., Jones T.H., Perner J. 2004. Shifting average body size during regeneration after pollution – a case study using ground beetle assemblages. Ecological Entomology 29(5): 543–554. DOI: 10.1111/j.0307-6946.2004.00643.x
Brygadyrenko V.V. 2015. Parameters of ecological niches of Badister, Licinus and Panagaeus (Coleoptera, Carabidae) species measured against eight ecological factors. Baltic Journal of Coleopterology 15(2): 137–154.
Brygadyrenko V.V., Korolev О.V. 2015. Morphological polymorphism in an urban population of Pterostichus melanarius (Illiger, 1798) (Coleoptera, Carabidae). Graellsia 71(1): e025. DOI: 10.3989/graellsia.2015.v71.126
Brygadyrenko V.V., Reshetniak D.Y. 2014. 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 Oecologica 41(2): 109–133.
Desender K., Verdyck P. 2001. Geographic scaling and genetic differentiation in two highly mobile European saltmarsh beetles. Belgian Journal of Zoology 131(1): 31–42.
Di Grumo D., Lovei G. 2016. Body size inequality in ground beetle (Coleoptera: Carabidae) assemblages as a potential method to monitor environmental impacts of transgenic crops. Periodicum Biologorum 118(3): 223–230. DOI: 10.18054/pb.2016.118.3.3921
Emlen D. 2008. The evolution of animal weapons. Annual Review of Ecology, Evolution, and Systematics 39: 387–413. DOI: 10.1146/annurev.ecolsys.39.110707.173502
Ernsting G., Isaaks J. 1997. Effects of temperature and season on egg size, hatchling size and adult size in Notiophilus biguttatus. Ecological Entomology 22(1): 32–40. DOI: 10.1046/j.1365-2311.1997.00040.x
Eyre M.D., Luff M.L. 2004. Ground beetle species (Coleoptera, Carabidae) associations with land cover variables in northern England and southern Scotland. Ecography 27(4): 417–426. DOI: 10.1111/j.0906-7590.2004.03757.x
Fairbairn D., Blankenhorn W., Székely T. 2007. Sex, size and gender roles: Evolutionary studies of sexual size dimorphism. Oxford: Oxford University Press. 266 p.
Fincke O., Waage J., Koenig W. 1997. Natural and sexual selection components of odonate mating patterns. In: J.C. Choe, B.J. Crespi (Eds.): Mating Systems in Insects and Arachnids. Cambridge: Cambridge University Press. P. 58–74. DOI: 10.1017/CBO9780511721946.004
Geodakjan V.A. 1982. Sexual dimorphism and the evolution of duration of ontogenesis and its stages. In: V.J.A. Novak, J. Mlikovsky (Eds.): Evolution and Environment. Praha: ČSAV. P. 229–237.
Giglio A., Giulianini P.G., Zetto T., Talarico F. 2011. Effects of the pesticide dimethoate on a non-target generalist carabid, Pterostichus melas italicus (Dejean, 1828) (Coleoptera: Carabidae). Italian Journal of Zoology 78(4): 471–477. DOI: 10.1080/11250003.2011.571222
Gobbi M., Fontaneto D. 2008. Biodiversity of ground beetles (Coleoptera: Carabidae) in different habitats of the Italian Po lowland. Agriculture, Ecosystems and Environment 127(3–4): 273–276. DOI: 10.1016/j.agee.2008.04.011
Gorban V., Huslystyi A., Espejo J.M.R., Bilova N. 2021. Prediction of SOC in calcic chernozem in the steppe zone of Ukraine using brightness and colour indicators. Ekológia (Bratislava) 40(4): 325–336. DOI: 10.2478/eko-2021-0034
Gritsan Y.I., Sytnyk S.A., Lovynska V.M., Tkalich I.I. 2019. Climatogenic reaction of Robinia pseudoacacia and Pinus sylvestris within Northern Steppe of Ukraine. Biosystems Diversity 27(1): 16–20. DOI: 10.15421/011902
Gugosyan Y.A., Boyko O.O., Brygadyrenko V.V. 2019. Morphological variation of four species of Strongyloides (Nematoda, Rhabditida) parasitising various mammal species. Biosystems Diversity 27(1): 85–98. DOI: 10.15421/011913
Hurka K. 1996. Carabidae of the Czech and Slovak Republics. Zlin: Kabourek. 565 p.
Iablokov-Khnzorian S.M. 1976. Fauna of the Armenian Republic of the USSR. Ground beetles (Carabidae). Yerevan: Publishing house of the Academy of Sciences of the Armenian SSR. 295 p. [In Russian]
Jensen L.B. 1990. Effect of temperature on the development of the immature stages of Bembidion lampros (Coleoptera: Carabidae). Entomophaga 35: 277–281. DOI: 10.1007/BF02374803
Kawano K. 2016. Comparative quantification of intralocalityal, interlocalityal, and interspecific variability in stag beetles (Coleoptera: Lucanidae) and the questions of phenotypic plasticity and species selection. Annals of the Entomological Society of America 109: 555–566. DOI: 10.1093/aesa/saw011
Knapp M., Saska P. 2012. The effects of habitat, density, gender and duration on overwintering success in Bembidion lampros (Coleoptera: Carabidae). Journal of Applied Entomology 136(3): 225–233. DOI: 10.1111/j.1439-0418.2011.01643.x
Komlyk V.O., Brygadyrenko V.V. 2019a. Morphological variability of Bembidion aspericolle (Coleoptera, Carabidae) populations in conditions of anthropogenic impact. Biosystems Diversity 27(1): 21–25. DOI: 10.15421/011903
Komlyk V.O., Brygadyrenko V.V. 2019b. Morphological variability of Bembidion minimum (Coleoptera, Carabidae) populations under the influence of natural and anthropogenic factors. Biosystems Diversity 27(3): 250–269. DOI: 10.15421/011935
Komlyk V., Brygadyrenko V. 2020. Morphological variability of Bembidion varium (Coleoptera, Carabidae) in gradient of soil salinity. Folia Oecologica 47(1): 23–33. DOI: 10.2478/foecol-2020-0004
Kostova R., Guéorguiev B. 2016. The ground beetles (Coleoptera: Carabidae) of the Strandzha Mountain and adjacent coastal territories (Bulgaria and Turkey). Biodiversity Data Journal 4: e8135. DOI: 10.3897/BDJ.4.e8135
Kozak V.M., Romanenko E.R., Brygadyrenko V.V. 2020. Influence of herbicides, insecticides and fungicides on food consumption and body weight of Rossiulus kessleri (Diplopoda, Julidae). Biosystems Diversity 28(3): 272–280. DOI: 10.15421/012036
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. Sofia-Moscow: Pensoft. 271 p.
Kunakh O.M., Lisovets O.I., Yorkina N.V., Zhukova Y.O. 2021. Phytoindication assessment of the effect of reconstruction on the light regime of an urban park. Biosystems Diversity 29(3): 276–285. DOI: 10.15421/012135
Lagarde F., Corbin J., Goujon C., Poisbleau M. 2005. Polymorphisme et performances au combat chez les mâles de Lucane cerf-volant (Lucanus cervus). Revue d'Écologie 60(2): 127–137.
Lagisz M. 2008. Changes in morphology of the ground beetle Pterostichus oblongopunctatus F. (Coleoptera; Carabidae) from vicinities of a zinc and lead smelter. Environmental Toxicology and Chemistry 27(8): 1744–1747. DOI: 10.1897/07-661.1
Langraf V., David S., Babosová R., Petrovičová K., Schlarmannová J. 2020. Change of ellipsoid biovolume (EV) of ground beetles (Coleoptera, Carabidae) along an urban–suburban–rural gradient of Central Slovakia. Diversity 12: 475. DOI: 10.3390/d12120475
Langraf V., Petrovičová K., David S., Kanská M., Nozdrovická J., Schlarmannová J. 2018. Change phenotypic traits in ground beetles (Carabidae) reflects biotope disturbance in Central Europe. Journal of the Entomological Research Society 20(2): 119–129.
Langraf V., Petrovičová K., David S., Nozdrovická J., Petrovič F., Schlarmannová J. 2019. The bioindication evaluation of ground beetles (Coleoptera: Carabidae) in three forest biotopes in the southern part of Central Slovakia. Ekológia (Bratislava) 38(1): 25–36. DOI: 10.2478/eko-2019-0003
Lindroth C.H. 1974. Coleoptera, Carabidae. Handbooks for the identification of British insects. London: Royal Entomological Society of London. 148 p.
Lindroth C.H. 1985. The Carabidae (Coleoptera) of Fennoscandia and Denmark. Vol. 1. 226 p.
McGeoch M.A. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73(2): 181–201. DOI: 10.1111/j.1469-185X.1997.tb00029.x
Nitzu E. 2003. Contributions to the knowledge of the tribus Bembidiini (Coleoptera: Carabidae) from Romania. Travaux du Museum National d'Histoire Naturelle Grigore Antipa 45(1): 179–185.
Okuzaki Y., Sota T. 2018. Predator size divergence depends on community context. Ecology Letters 21(7): 1097–1107. DOI: 10.1111/ele.12976
Osman W., El-Samad L.M., Mokhamer E.H., El-Touhamy A., Shonouda M. 2015. Ecological, morphological, and histological studies on Blaps polycresta (Coleoptera: Tenebrionidae) as biomonitors of cadmium soil pollution. Environmental Science and Pollution Research 22(18): 14104–14115. DOI: 10.1007/s11356-015-4606-4
Pakhomov O.Y., Kunakh O.M., Babchenko A.V., Fedushko M.P., Demchuk N.I., Bezuhla L.S., Tkachenko O.S. 2019. Temperature effect on the temporal dynamic of terrestrial invertebrates in technosols formed after reclamation at a post-mining site in Ukrainian steppe drylands. Biosystems Diversity 27(4): 322–328. DOI: 10.15421/011942
Pokhylenko A.P., Didur O.O., Kulbachko Y.L., Bandura L.P., Chernykh S.A. 2020. Influence of saprophages (Isopoda, Diplopoda) on leaf litter decomposition under different levels of humidification and chemical loading. Biosystems Diversity 28(4): 384–389. DOI: 10.15421/012049
Putchkov A.V., Brygadyrenko V.V., Nikolenko N.Y. 2020. Ecological-faunistic analysis of ground beetles and tiger beetles (Coleoptera: Carabidae, Cicindelidae) of metropolises of Ukraine. Biosystems Diversity 28(2): 163–174. DOI: 10.15421/012022
Puchkov A.V., Brygadyrenko V.V., Faly L.I., Komaromi N.A. 2020. Staphylinids (Coleoptera, Staphylinidae) of Ukrainian metropolises. Biosystems Diversity 28(1): 41–47. DOI: 10.15421/012007
Pеtillon J., Georges A., Canard A., Ysnel F. 2007. Impact of cutting and sheep grazing on ground-active spiders and carabids in intertidal salt marshes (Western France). Animal Biodiversity and Conservation 30(2): 201–209.
Rouabah A., Villerd J., Amiaud B., Plantureux S., Lasserre F. 2015. Response of carabid beetles diversity and size distribution to the vegetation structure within differently managed field margins. Agriculture, Ecosystems and Environment 200: 21–32. DOI: 10.1016/j.agee.2014.10.011
Rueffler C., Van Dooren T.J.M., Leimar O., Abrams P.A. 2006. Disruptive selection and then what? Trends in Ecology and Evolution 21(5): 238–245. DOI: 10.1139/g11-052
Rusynov V.I., Brygadyrenko V.V. 2017. Morphological variability of a population of Anatolica eremita (Coleoptera, Tenebrionidae): Constancy of morphometric indices with variation of linear parameters of the body. Baltic Journal of Coleopterology 17(2): 205–217.
Serrano J. 2013. New catalogue of the family Carabidae of the Iberian Peninsula (Coleoptera). Murcia: Universidad de Murcia. 192 p.
Shreeves G., Field J. 2008. Parental care and sexual size dimorphism in wasps and bees. Behavioral Ecology and Sociobiology 62(5): 843–852. DOI: 10.1007/s00265-007-0510-3
Shulman M.V., Pakhomov O.Y., Brygadyrenko V.V. 2017. Effect of lead and cadmium ions upon the pupariation and morphological changes in Calliphora vicina (Diptera, Calliphoridae). Folia Oecologica 44(1): 28–37. DOI: 10.1515/foecol-2017-0004
Sowa G., Skalski T. 2019. Effects of chronic metal exposure on the morphology of beetles species representing different ecological niches. Bulletin of Environmental Contamination and Toxicology 102(2): 191–197. DOI: 10.1007/s00128-018-02532-7
Sukhodolskaya R.A., Eremeeva N.I. 2013. Body size and shape variation in ground beetle Carabus aeruginosus F.-W., 1822 (Coleoptera, Carabidae). Contemporary Problems of Ecology 6(6): 609–615. DOI: 10.1134/S1995425513060127
Talarico F., Brandmayr P., Giglio A., Massolo A., Brandmayr T.Z. 2011. Morphometry of eyes, antennae and wings in three species of Siagona (Coleoptera, Carabidae). ZooKeys 100: 203–214. DOI: 10.3897/zookeys.100.1528
Ter Braak C.J.F., Šmilauer P. 2012. Canoco reference manual and user′s guide: Software for ordination, version 5.0. Ithaca, USA: Microcomputer Power. 496 p.
Theiss S., Heimbach U. 1994. Laborzuchtverfahren für laufkäfer der art Bembidion tetracolum (Coleoptera: Carabidae). Entomologia Generalis 19(1/2): 61–64. DOI: 10.1127/entom.gen/19/1994/061
Thiele H.U. 1977. Carabid beetles in their environments. A study on habitat selection by adaptation in physiology and behaviour. Berlin: Springer-Verlag. 369 p. DOI: 10.1007/978-3-642-81154-8
Thornhill R., Alcock J. 1983. The evolution of insect mating systems. London: Harvard University Press. 535 p.
Tyler G. 2010. Variability in colour, metallic lustre, and body size of Carabus arvensis Herbst, 1784 (Coleoptera: Carabidae) in relation to habitat properties. Entomologica Fennica 21(2): 90–96. DOI: 10.33338/ef.84514
Vittum P.J., Morzuchi B.J. 1990. Effect of soil pH on Japanese beetle (Coleoptera: Scarabaeidae) oviposition in potted turfgrass. Journal of Economic Entomology 83(5): 2036–2039. DOI: 10.1093/jee/83.5.2036
Zhuk V.V. 2019. Biology of reproduction and development. Part 1. Perm: Publishing Center of Perm State National Research University. 232 p. [In Russian]