Phytoindication approach to assessing factors determining the habitat preferences of red deer (Cervus elaphus)

  • V. I. Domnich Zaporizhzhia National University
  • A. V. Domnich Zaporizhzhia National University
  • O. V. Zhukov Bogdan Khmelnitsky Melitopol State Pedagogical University
Keywords: Cervidae; ecological niche; nitrogen content in soil; population management; Mantel test; species response


The study examined the possibility of using the phytoindication technique to describe habitat preferences of red deer in a relatively homogeneous area. Two alternative hypotheses were tested. Hypothesis 1 suggests that the relationship between red deer and vegetation is due to a trophic factor, so preferences for individual plant species cause vegetation to influence the distribution of animal numbers. Hypothesis 2 suggests that environmental factors influence vegetation, structuring and determining the productive level of the community as a whole. Therefore, environmental factors, rather than individual plant species, cause vegetation-animal interactions. The research was conducted on Biryuchiy Island Spit, where the Azov-Sivash National Nature Park is located. The geobotanical surveys were performed in three types of ecosystems: sandy steppe (vegetation class Festucetea vaginatae), saline meadows (vegetation class Festuco–Puccinellietea), and artificial forest plantation (vegetation class Robinietea). 250 releves were recorded according to the Brown-Blanquet approach. The number of fecal pellets and the number of groups of pellets of red deer was recorded together with geobotanical surveys in the same sample plots. The pellet groups counted in the field were converted to deer densities in specific vegetation classes taking into account the number of pellet groups on the site and the decay rate of the fecal pellets. The vegetation types were distinguished by the number of deer fecal pellets per unit area. The highest number of fecal pellets was found for the plant class Festucetea vaginatae, somewhat fewer fecal pellets were in the plant class Robinietea, and the lowest number was in the plant class Festuco-Puccinellietea. A geometric distribution model is adequate for explaining the experimental data on the number of fecal pellets. A total of 59 species of flowering plants were found. Based on the species composition and projective cover of species, the ecological regimes of ecotopes were identified by phytoindication. The correspondence analysis of the vegetation revealed two ordination axes. The ordination axis 1 (CA1) was able to explain 11.3% of community inertia, and the ordination axis 2 (CA2) was able to explain 5.2% of community inertia. The maximum excretory activity of animals was recorded for the central part of the ordination space, indicating the presence of an optimum zone in the gradient of environmental factors that structure plant communities. The forward selection procedure allowed the Nutrients Availability variable to be selected as the most important variable to explain variation in the plant community structure. The number of deer fecal pellets exhibited different patterns of response in the Nutrients Availability gradient. The response within the plant class Festucetea vaginatae could best be explained by Model III from the list of HOF-models. The response of the excretory activity of deer within the class Festuco-Puccinellietea could best be fitted by the model IV, which represents a symmetric Gaussian curve. The response of excretory activity in the Robinietea vegetation class was asymmetrical bimodal. The ecological properties of the red deer ecological niche in both the drier and less mineralized part of the range of ecological conditions and the wetter and more mineralized part should be assessed in the context of the prospects for future studies.


Acevedo, P., & Cassinello, J. (2009). Human-induced range expansion of wild ungulates causes niche overlap between previously allopatric species: Red deer and Iberian ibex in mountainous regions of Southern Spain. Annales Zoologici Fennici, 46(1), 39–50.

Alves, J., Alves da Silva, A., Soares, A. M. V. M., & Fonseca, C. (2013). Pellet group count methods to estimate red deer densities: Precision, potential accuracy and efficiency. Mammalian Biology, 78(2), 134–141.

Austin, M. P. (2002). Spatial prediction of species distribution: An interface between ecological theory and statistical modelling. Ecological Modelling, 157, 101–118.

Bagherirad, E., Abdullah, M., & Amirkhani, M. (2013). Using pellet group counts to estimate the population size of the Persian gazelle in the steppe area of Golestan National Park, Iran. Malaysian Applied Biology, 42(2), 51–57.

Ball, M. E. (1974). Floristic changes on grasslands and heaths on the Isle of Rhum after a reduction or exclusion of grazing. Journal of Environmental Manage-ment, 2, 299–318.

Barrios-Garcia, M. N., & Ballari, S. A. (2012). Impact of wild boar (Sus scrofa) in its introduced and native range: A review. Biological Invasions, 14(11), 2283–2300.

Bartelheimer, M., & Poschlod, P. (2016). Functional characterizations of Ellenberg indicator values – a review on ecophysiological determinants. Functional Eco-logy, 30(4), 506–516.

Bennett, L. J., English, P. F., & McCain, R. (1940). A study of deer populations by use of pellet-group counts. The Journal of Wildlife Management, 4(4), 398.

Bobrowski, M., Gillich, B., & Stolter, C. (2015). Modelling browsing of deer on beech and birch in Northern Germany. Forest Ecology and Management, 358, 212–221.

Bodmer, R. E. (1990). Ungulate frugivores and the browser-grazer continuum. Oi-kos, 57(3), 319.

Braun-Blanquet, J. (1964). Pflanzensoziologie, Grundzüge der Vegetationskunde. 3rd ed. Springer Vienna, Vienna.

Britton, A., & Pakeman, R. (2009). Vegetation monitoring of Rum Natura habitats. Scottish Natural Heritage Commissioned Report, F05LC06, 1–90.

Buechner, M. (1987). A geometric model of vertebrate dispersal: Tests and implica-tions. Ecology, 68(2), 310–318.

Chytry, M., Tichy, L., Drevojan, P., Sádlo, J., & Zeleny, D. (2018). Ellenberg-type indicator values for the Czech flora. Preslia, 90(2), 83–103.

Cochran, G. A., & Stains, H. J. (1961). Deposition and decomposition of fecal pellets by Cottontails. The Journal of Wildlife Management, 25(4), 432.

Côté, S. D., Rooney, T. P., Tremblay, J.-P., Dussault, C., & Waller, D. M. (2004). Ecological impacts of deer overabundance. Annual Review of Ecology, Evolution, and Systematics, 35(1), 113–147.

Debeljak, M., Džeroski, S., Jerina, K., Kobler, A., & Adamič, M. (2001). Habitat suitability modelling for red deer (Cervus elaphus L.) in South-Central Slovenia with classification trees. Ecological Modelling, 138, 321–330.

Didukh, Y. P. (2011). The ecological scales for the species of Ukrainian flora and their use in synphytoindication. Phytosociocenter, Kyiv.

Domnich, A. V. (2015). Ratychni yak strukturno-funktsionalnyi element ostrivnykh zapovidno-okhoronnykh terytorii Pivdennoho Skhodu Ukrainy [Ungulates as a structural-functional element of island and steppe ecosystems in conservation areas of south-east of Ukraine]. Dnipro National University Press, Dnipro (in Ukranian).

Dubyna, D. V., Neuhäuslová, Z., & Shelyag-Sosonco, J. R. (1994). Coastal vegeta-tion of the “Birjucij Island” Spit in the Azov Sea, Ukraine. Preslia, 66, 193–216.

Dubyna, D. V., Neuhäuslová, Z., & Shelyag-Sosonco, J. R. (1995). Vegetation of the “Birjucij Island” Spit in the Azov Sea. Sand steppe vegetation. Folia Geobotanica and Phytotaxonomica, 3(1), 1–31.

Dufresne, M., Bradley, R. L., Tremblay, J.-P., Poulin, M., & Pellerin, S. (2009). Cle-arcutting and deer browsing intensity interact in controlling nitrification rates in forest floor. Écoscience, 16(3), 361–368.

Eberhardt, L., & Van Etten, R. C. (1956). Evaluation of the pellet group count as a deer census method. The Journal of Wildlife Management, 20(1), 70.

Ellenberg, H., Weber, H. E., Dull, R., Wirth, V., Werner, W., & Paulissen, D. (1991). Zeigerwerte von Pflanzen in Mitteleuropa. Scripta Geobotanica, 18, 1–248.

Feest, A., Van Swaay, C., & Van Hinsberg, A. (2014). Nitrogen deposition and the reduction of butterfly biodiversity quality in the Netherlands. Ecological Indica-tors, 39, 115–119.

Forsyth, D. M. (2005). Protocol for estimating changes in the relative abundance of deer in New Zealand forests using the Faecal Pellet Index (FPI). Landcare Re-search contract report LC0506/027 to the Department of Conservation, Lincoln, New Zealand.

Gebert, C., & Verheyden-Tixier, H. (2008). Variations of diet composition of Red deer (Cervus elaphus L.) in Europe. Mammal Review, 31, 189–201.

Gonzalez-Hernandez, M. P., & Silva-Pando, F. J. (1999). Nutritional attributes of understory plants known as components of deer diets. Journal of Range Mana¬gement, 52(2), 132.

Goslee, S. C., & Urban, D. L. (2007). The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software, 22(7), 1–19.

Hanley, T. A. (1997). A nutritional view of understanding and complexity in the pro¬blem of diet selection by deer (Cervidae). Oikos, 79(2), 209.

Harestad, A. S., & Bunnell, F. L. (1987). Persistence of black-tailed deer fecal pellets in coastal habitats. The Journal of Wildlife Management, 51(1), 33.

Harrison, K. (2004). Browsing by red deer negatively impacts on soil nitrogen availa¬bility in regenerating native forest. Soil Biology and Biochemistry, 36(1), 115–126.

Heckel, C. D., Bourg, N. A., McShea, W. J., & Kalisz, S. (2010). Nonconsumptive effects of a generalist ungulate herbivore drive decline of unpalatable forest herbs. Ecology, 91(2), 319–326.

Heinken, T., & Raudnitschka, D. (2002). Do wild ungulates contribute to the disper-sal of vascular plants in central European forests by epizoochory? A case study in NE Germany. Forstwissenschaftliches Centralblatt, 121(4), 179–194.

Hierl, L. A., Franklin, J., Deutschman, D. H., Regan, H. M., & Johnson, B. S. (2008). Assessing and prioritizing ecological communities for monitoring in a regional habitat conservation plan. Environmental Management, 42(1), 165–179.

Hirzel, A. H., & Le Lay, G. (2008). Habitat suitability modelling and niche theory. Journal of Applied Ecology, 45(5), 1372–1381.

Hirzel, A. H., Hausser, J., Chessel, D., & Perrin, N. (2002). Ecological-niche factor analysis: How to compute habitat-suitability maps without absence data? Ecolo¬gy, 83(7), 2027–2036.

Hobbs, N. T. (1996). Modification of ecosystems by ungulates. The Journal of Wildlife Management, 60(4), 695.

Hofmann, R. R. (1989). Evolutionary steps of ecophysiological adaptation and diver¬sification of ruminants: A comparative view of their digestive system. Oecologia, 78(4), 443–457.

Holmes, S. A., & Webster, C. R. (2011). Herbivore-induced expansion of generalist species as a driver of homogenization in post-disturbance plant communities. Plant Ecology, 212(5), 753–768.

Horsák, M., Hájek, M., Tichý, L., & Juřičková, L. (2007). Plant indicator values as a tool for land mollusc autecology assessment. Acta Oecologica, 32(2), 161–171.

Huisman, J., Olff, H., & Fresco, L. F. M. (1993). A hierarchical set of models for species response analysis. Journal of Vegetation Science, 4(1), 37–46.

Jansen, F., & Oksanen, J. (2013). How to model species responses along ecological gradients – Huisman-Olff-Fresco models revisited. Journal of Vegetation Scien¬ce, 24(6), 1108–1117.

Kappes, H., Kopeć, D., & Sulikowska-Drozd, A. (2014). Influence of habitat structure and conditions in floodplain forests on mollusc assemblages. Polish Journal of Ecology, 62(4), 739–750.

Kay, R. N. B., & Staines, B. W. (1981). The nutrition of the Red deer (Cervus elaphus). Nutrition Abstracts and Reviews, Series B, 51, 601–622.

Knapp, A. K., Blair, J. M., Briggs, J. M., Collins, S. L., Hartnett, D. C., Johnson, L. C., & Towne, G. (1999). The keystone role of bison in North American tallgrass prairie. BioScience, 49, 39–50.

Knight, T. M., Dunn, J. L., Smith, L. A., Davis, J., & Kalisz, S. (2009). Deer facilitate invasive plant success in a Pennsylvania forest understory. Natural Areas Jour-nal, 29(2), 110–116.

Kolomiychuk, V. P., & Bezkorovajnyj, O. S. (2011). Vegetation dynamics of Biryu¬chy Island Spit (Kherson region). Gruntoznavstvo, 12, 95–100.

Konvicka, M., Hula, V., & Fric, Z. (2003). Habitat of pre-hibernating larvae of the endangered butterfly Euphydryas aurinia (Lepidoptera: Nymphalidae): What can be learned from vegetation composition and architecture? European Journal of Entomology, 100(3), 313–322.

Kuijper, D. P. J. (2011). Lack of natural control mechanisms increases wildlife-fo-restry conflict in managed temperate European forest systems. European Jour-nal of Forest Research, 130(6), 895–909.

Kuijper, Dries P.J., Jędrzejewska, B., Brzeziecki, B., Churski, M., Jędrzejewski, W., & Żybura, H. (2010). Fluctuating ungulate density shapes tree recruitment in natural stands of the Białowieża Primeval Forest, Poland. Journal of Vegetation Science, 21(6), 1082–1098.

Kumbasli, M., Makineci, E., & Cakir, M. (2010). Long-term effects of Red deer (Cervus elaphus) grazing on soil in a breeding area. Journal of Environmental Biology, 31, 185–188.

Kunakh, O. N., Kramarenko, S. S., Zhukov, A. V., Zadorozhnaya, G. A., & Kramarenko, A. S. (2018). Intra-population spatial structure of the land snail Vallonia pulchella (Müller, 1774) (Gastropoda; Pulmonata; Valloniidae). Ruthenica, 28(3), 91–99.

Laing, S. E., Buckland, S. T., Burn, R. W., Lambie, D., & Amphlett, A. (2003). Dung and nest surveys: Estimating decay rates. Journal of Applied Ecology, 40(6), 1102–1111.

Long, Z. T., Pendergast, T. H., & Carson, W. P. (2007). The impact of deer on relationships between tree growth and mortality in an old-growth beech-maple fo¬rest. Forest Ecology and Management, 252, 230–238.

Massé, A., & Côté, S. D. (2012). Linking habitat heterogeneity to space use by large herbivores at multiple scales: From habitat mosaics to forest canopy openings. Forest Ecology and Management, 285, 67–76.

Melis, C., Buset, A., Aarrestad, P. A., Hanssen, O., Meisingset, E. L., Andersen, R., Moksnes, A., & Røskaft, E. (2006). Impact of red deer Cervus elaphus grazing on bilberry Vaccinium myrtillus and composition of ground beetle (Coleoptera, Carabidae) assemblage. Biodiversity and Conservation, 15(6), 2049–2059.

Mirzoeva, A., & Zhukov, O. (2021). Conchological variability of Anadara kagoshimensis (Bivalvia: Arcidae) in the northern part of the Black-Azov Sea basin. Biologia.

Mitchell, B., & McCowan, D. (1984). The defecation frequencies of Red deer in different habitats. In: Institute of Terrestrial Ecology. Annual Report 1983. Henry Ling Limited, The Dorset Press, Dorchester, Dorset. Pp. 15–17.

Moore, E. K., Britton, A. J., Iason, G., Pemberton, J., & Pakeman, R. J. (2015). Land¬scape-scale vegetation patterns influence small-scale grazing impacts. Biological Conservation, 192, 218–225.

Müller, A., Dahm, M., Bøcher, P. K., Root-Bernstein, M., & Svenning, J.-C. (2017). Large herbivores in novel ecosystems – Habitat selection by Red deer (Cervus elaphus) in a former brown-coal mining area. PLoS One, 12(5), e0177431.

Mysterud, A., Langvatn, R., Yoccoz, N. G., & Stenseth, N. C. (2001). Plant phenol-logy, migration and geographical variation in body weight of a large herbivore: The effect of a variable topography. Journal of Animal Ecology, 70(6), 915–923.

Nugent, G., Fraser, K. W., & Sweetapple, P. J. (1997). Comparison of Red deer and possum diets and impacts in podocarp-hardwood forests, Waihaha catchment, Pureora Conservation Park. Science for Conservation , 50. Dept. of Conservation, Wellington.

Nuttle, T., Ristau, T. E., & Royo, A. A. (2014). Long-term biological legacies of her-bivore density in a landscape-scale experiment: Forest understoreys reflect past deer density treatments for at least 20 years. Journal of Ecology, 102(1), 221–228.

Oksanen, J., & Minchin, P. R. (2002). Continuum theory revisited: What shape are spe¬cies responses along ecological gradients? Ecological Modelling, 157, 119–129.

Oostermeijer, J. G. B., & van Swaay, C. A. M. (1998). The relationship between but¬terflies and environmental indicator values: A tool for conservation in a chan¬ging landscape. Biological Conservation, 86(3), 271–280.

Pendergast, T. H., Hanlon, S. M., Long, Z. M., Royo, A. A., & Carson, W. P. (2016). The legacy of deer overabundance: Long-term delays in herbaceous understory recovery. Canadian Journal of Forest Research, 46(3), 362–369.

Pérez-Barbería, F. J., Hooper, R. J., & Gordon, I. J. (2013). Long-term density-de-pendent changes in habitat selection in Red deer (Cervus elaphus). Oecologia, 173(3), 837–847.

Pielech, R., Zając, K., Kadej, M., Malicki, M., Malkiewicz, A., & Tarnawski, D. (2017). Ellenberg’s indicator values support prediction of suitable habitat for pre-diapause larvae of endangered butterfly Euphydryas aurinia. PLoS One, 12(6), e0179026.

Ponomarenko, O., Banik, M., & Zhukov, O. (2021). Assessing habitat suitability for the Common Pochard, Aythya ferina (Anseriformes, Anatidae) at different spatial scales in Orel’ River valley, Ukraine. Ekológia (Bratislava), 40(2), 154–162.

Prokudin, Y. N. (Ed.). (1987). Opredelitel’ vysshykh rastenij Ukrainy [Identification key to higher plants of Ukraine]. Naukova Dumka, Kyiv (in Russian).

Rogers, G., Julander, O., & Robinette, W. L. (1958). Pellet-group counts for deer census and range-use index. The Journal of Wildlife Management, 22(2), 193.

Rooney, T. P., & Waller, D. M. (2003). Direct and indirect effects of white-tailed deer in forest ecosystems. Forest Ecology and Management, 181, 165–176.

Sabo, A. E., Frerker, K. L., Waller, D. M., & Kruger, E. L. (2017). Deer-mediated changes in environment compound the direct impacts of herbivory on understorey plant communities. Journal of Ecology, 105(5), 1386–1398.

Semiadil, G., Barry, T. N., Muir, P. D., & Hodgson, J. (1995). Dietary preferences of sambar (Cervus unicolor) and red deer (Cervus elaphus) offered browse, forage legume and grass species. The Journal of Agricultural Science, 125(1), 99–107.

Sokal, R. R., & Rohlf, F. J. (1995). Biometry: The principles and practice of statistics in biological research. W. H. Freeman and Co., New York.

Sokolov, S. G., & Zhukov, A. V. (2017). Functional diversity of a parasite assem-blages of the Chinese sleeper Perccottus glenii Dybowski, 1877 (Actinopterygii: Odontobutidae) and habitat structure of the host. Biology Bulletin, 44(3), 331–336.

Staines, B. W. (2009). The use of natural shelter by Red deer (Cervus elaphus) in relation to weather in North-East Scotland. Journal of Zoology, 180(1), 1–8.

Suter, W., Suter, U., Kriisi, B., & Schütz, M. (2004). Spatial variation of summer diet of red deer Cervus elaphus in the Eastern Swiss Alps. Wildlife Biology, 10(1), 43–50.

Szymura, T. H., Szymura, M., & Macioł, A. (2014). Bioindication with Ellenberg’s indicator values: A comparison with measured parameters in Central European oak forests. Ecological Indicators, 46, 495–503.

Tahtinen, B., Murray, B. D., Webster, C. R., Tarasoff, C. S., & Burton, A. J. (2014). Does ungulate foraging behavior in forest canopy gaps produce a spatial subsi-dy with cascading effects on vegetation? Forest Science, 60(5), 819–829.

Ter Braak, C. J. F. (1986). Canonical correspondence analysis: A new eigenvector technique for multivariate direct gradient analysis. Ecology, 67(5), 1167–1179.

Tiitsaar, A., Kaasik, A., Lindman, L., Stanevitš, T., & Tammaru, T. (2016). Host associations of Coenonympha hero (Lepidoptera: Nymphalidae) in Northern Europe: Microhabitat rather than plant species. Journal of Insect Conservation, 20(2), 265–275.

Tschöpe, O., Wallschläger, D., Burkart, M., & Tielbörger, K. (2011). Managing open habitats by wild ungulate browsing and grazing: A case-study in North-Eastern Germany. Applied Vegetation Science, 14(2), 200–209.

Waller, D. M., & Alverson, W. S. (1997). The white-tailed deer: A keystone herbi-vore. Wildlife Society Bulletin, 25, 217–226.

Webster, C. R., Jenkins, M. A., & Rock, J. H. (2005). Long-term response of spring flora to chronic herbivory and deer exclusion in Great Smoky Mountains Na-tional Park, USA. Biological Conservation, 125(3), 297–307.

Williams, C. D., Moran, J., Doherty, O., Mc Donnell, R. J., Gormally, M. J., Knut-son, L. V., & Vala, J.-C. (2009). Factors affecting Sciomyzidae (Diptera) across a transect at Skealoghan Turlough (Co. Mayo, Ireland). Aquatic Ecology, 43(1), 117–133.

Wilmshurst, J. F., Fryxell, J. M., & Hudsonb, R. J. (1995). Forage quality and patch choice by wapiti (Cervus elaphus). Behavioral Ecology, 6(2), 209–217.

Yorkina, N., Maslikova, K., Kunah, O., & Zhukov, O. (2018). Analysis of the spatial organization of Vallonia pulchella (Muller, 1774) ecological niche in technosols (Nikopol Manganese Ore Basin, Ukraine). Ecologica Montenegrina, 17(1), 29–45.

Zhukov, O., Kunah, O., Dubinina, Y., & Novikova, V. (2018). The role of edaphic, vegetational and spatial factors in structuring soil animal communities in a floodplain forest of the Dnipro River. Folia Oecologica, 45, 8–23.

Zhukov, O., Kunah, O., Dubinina, Y., Zhukova, Y., & Ganzha, D. (2019). The effect of soil on spatial variation of the herbaceous layer modulated by overstorey in an Eastern European poplar-willow forest. Ekologia (Bratislava), 38(3), 253–272.

Zhukov, O., Kunah, O., Fedushko, M., Babchenko, A., & Umerova, A. (2021). Temporal aspect of the terrestrial invertebrate response to moisture dynamic in technosols formed after reclamation at a post-mining site in Ukrainian steppe drylands. Ekológia (Bratislava), 40(2), 178–188.

Zimaroeva, А. A., Zhukov, O. V., & Ponomarenko, O. L. (2016). Determining spa¬tial parameters of the ecological niche of Parus major (Passeriformes, Paridae) on the base of remote sensing data. Vestnik Zoologii, 50(3), 251–258.

Zonneveld, I. S. (1983). Principles of bio-indication. Environmental Monitoring and Assessment, 3, 207–217.

Zverev, A. A. (2020). Methodological aspects of using indicator values in biodiversity analysis. Contemporary Problems of Ecology, 13(4), 321–332.

Zymaroieva, A., Zhukov, O., Fedoniuk, T., Pinkina, T., & Hurelia, V. (2021). The relationship between landscape diversity and crops productivity: Landscape scale study. Journal of Landscape Ecology, 14(1), 39–58.