Endangered species’ trait responses to environmental variability in agricultural settings

Authors

Keywords:

normalized difference vegetation index (NDVI), automated water extraction index (AWEI), demographic traits, Spermophilus citellus, habitat

Abstract

Paper description:

  • Understanding interactions between species traits and changing environmental conditions can contribute to better conservation planning and management of threatened open grassland ecosystems.
  • Grassland specialist species, such as the European ground squirrel Spermophilus citellus L. 1766, are currently facing severe population decline.
  • Human-induced conditions and abiotic factors are the main drivers of the species’ responses at individual and population levels to the environmental conditions in the Central Banat area (Serbia)
  • Strategies aimed at stopping population decline should focus on both species traits and behavioral flexibility, ongoing changes in spatial heterogeneity, weather conditions and climate predictions.


Abstract: Understanding the spatial and temporal effects of variable environmental conditions on demographic characteristics is important in order to stop the decline of endangered-species populations. To capture interactions between a species and its environment, in this work the demographic traits of the European ground squirrel (EGS), Spermophilus citellus, were modeled as a function of agricultural landscape structure. The habitat suitability index was determined for 20 localities within the study area based on habitat use, management and type. After mapping the habitat patch occupancy in the field, crop cover maps, the average normalized difference vegetation index (NDVI) and automated water extraction index (AWEI) were obtained from satellite images covering the period 2013-2015. This data was used to develop population-level generalized linear models (GLMs) and individual-level conditional mixed-effects models (GLMMs) in R package Ime4, focusing on the key demographic traits of the EGS. The land composition and patch carrying capacity (PCC) are the key determinants of the endangered EGS population size, while system productivity is the main factor influencing individuals’ body condition after monitoring for variations across sampling years and age classes. The proposed landscape structural models show that human activities and abiotic factors shape the demographic rates of the EGS. Thus, to conserve threatened species, an appropriate focus on the spatial adaptation strategies should be employed.

https://doi.org/10.2298/ABS190715061N

Received: July 15, 2019; Revised: September 2, 2019; Accepted: September 9, 2019; Published online: September 13, 2019

How to cite this article: Nikolić T, Arok M, Radišić D, Mirč M, Velaja L, Milić D, Ćirović D.Endangered species’ trait responses to environmental variability in agricultural settings. Arch Biol Sci. 2020;72(1):13-21.

Downloads

Download data is not yet available.

References

Wolff S, Schrammeijer EA, Schulp CJ, Verburg PH. Meeting global land restoration and protection targets: What would the world look like in 2050? Glob Environ Change. 2018;52:259-72.

Puzović S, Panjković B, Tucakov M, Stojnić N, Sabadoš K, Stojanović T, Vig L, Marić B, Tešić O, Kiš A, Galamboš L, Pil N, Kicošev V, Stojšić V, Timotić D, Perić R, Bošnjak T, Delić J, Dobretić V, Stanišić J. Upravljanje prirodnom baštinom u Vojvodini. Novi Sad: Sekretarijat za urbanizam, graditeljstvo i zaštitu životne sredine, Pokrajinski zavod za zaštitu prirode. 2015. 156 p. Serbian.

Benton TG, Plaistow SJ, Coulson TN. Complex population dynamics and complex causation: devils, details and demography. Proc Biol Sci. 2006;273(1591):1173-81.

Brooks ME, Mugabo M, Rodgers GM, Benton TG, Ozgul A. How well can body size represent effects of the environment on demographic rates? Disentangling correlated explanatory variables. J Anim Ecol. 2016;85(2):318-28.

Coroiu C, Kryštufek B, Vohralík, V, Zagorodnyuk, I. Spermophilus citellus. In: The IUCN Red List of Threatened Species [Internet]. IUCN; 2008 Jun 30. [cited 2019 Feb 10] Available from: http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T20472A9204055.en

Janderková J, Matějů J, Schnitzerová P, Petruš J, Sedláček J, Uhlíková J. Soil charatcteristics at Spermophilus citellus localities in the Czech Republic (Rodentia: Sciuridae). Lynx. 2011;42:99-111.

Janák M, Marhoul P, Matějů J. Action Plan for the Conservation of the European Ground Squirrel Spermophilus citellus in the European Union [Internet]. European Commission; 2013 [cited 2019 Feb 11]. Available from: https://ec.europa.eu/environment/nature/conservation/species/action_plans/pdf/EUSAP_EuropeanGround%20Squirrel_Final.pdf

Ružić A. Contribution to the knowledge of ecology of the ground squirrel Citellus citellus L. Proc Inst Ecol Biogeogr. 1950;1:97-140. Serbian.

Petrov MB. Mammals of Yugoslavia, insectivores and rodents. Belgrade: Natural history museum of Belgrade. 1992. 186 p.

Uredba o ekološkoj mreži. Offic Gazzete Rep Serb. 2010;102/2010p. Serbian.

Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T. Coupled dynamics of body mass and population growth in response to environmental change. Nature. 2010;466(7305):482-7.

Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, Fromentin JM, Hoegh-Guldberg O, Bairlein F. Ecological responses to recent climate change. Nature. 2006;416(6879):389-95.

Parmesan C. Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst. 2006;37:637-69.

Toïgo C, Gaillard JM, Van Laere G, Hewison M, Morellet N. How does environmental variation influence body mass, body size, and body condition? Roe deer as a case study. Ecography. 2006;29(3):301-8.

Callaghan D, Heath M, O'Sullivan J, Pritchard D. Important Bird Areas and potential Ramsar Sites in Europe. Wageningen: BirdLife International; 2011. 126 p.

Anderson S, Darbyshire I, Halski B. Important Plant Areas. In: Willis KJ, Bachman S, editors. RBG Kew, state of the world’s plants report-2016. London: Royal Botanical Garden, Kew; 2016. p. 24-7.

Sekulić N, Šinžar-Sekulić J, editors. [Emerald Ecological Network in Serbia]. Beograd: Republika Srbija: Ministarstvo životne sredine i prostornog planiranja, Zavod za zaštitu prirode Srbije; 2010. 100 p. Serbian.

Ramsar Convention Secretariat. The Ramsar Convention Manual: a guide to the Convention on Wetlands (Ramsar, Iran, 1971). 6th ed. Gland, Switzerland: Ramsar Convention Secretariat; 2013. 109 p.

Katona K, Váczi O, Altbäcker V. Topographic distribution and daily activity of the European ground squirrel population in Bugacpuszta, Hungary. Acta Theriologica, 2002;47(1):45-54.

Ružić A. Određivanje uzrasnih kategorija u populaciji tekunice Citellus citellus L. Arhiv Biol Nauka. 1966;18:65-70. Serbian.

Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ. Restitution of mass–size residuals: validating body condition indices. Ecology. 2005;86(1):155-63.

Ramos-Lara N, Koprowski JL, Kryštufek B, Hoffmann IE. Spermophilus citellus (Rodentia: Sciuridae). Mammalian Species. 2014;46(913):71-87.

Crnojević V, Lugonja P, Brkljač BN, Brunet B. Classification of small agricultural fields using combined Landsat-8 and RapidEye imagery: case study of northern Serbia. J Appl Remote Sens. 2014;8(1):083512.

Verboom J, Pouwels R. Ecological functioning of ecological networks: a species perspective. In: Jongman RHG, Pungetti G, editors. Ecological networks and greenways; concept, design, implementation. Cambridge: Cambridge University Press; 2004. p. 4-72.

Merrick MJ, Koprowski JL. Circuit theory to estimate natal dispersal routes and functional landscape connectivity for an endangered small mammal. Landscape Ecol. 2017; 32:1163-79.

Bates D, Maechler M, Bolker B, Walker S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.7. J Stat Softw. 2014;1(7):1-23.

Burnham KP, Anderson DR. Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res. 2004;33(2):261-304.

Fisher JT, Anholt B, Bradbury S, Wheatley M, Volpe JP. Spatial segregation of sympatric marten and fishers: the influence of landscape and species-scapes. Ecography. 2013;36(2):240-8.

Sozio G, Mortelliti A. Empirical evaluation of the strength of interspecific competition in shaping small mammal communities in fragmented landscapes. Landscape Ecol. 2016;31(4):775-89.

Hodgson JA, Moilanen A, Wintle BA, Thomas CD. Habitat area, quality and connectivity: striking the balance for efficient conservation. J Appl Ecol. 2011;48:148-52.

Guo Q, Taper M, Schoenberger M, Brandle J. Spatial-temporal population dynamics across species range: from centre to margin. Oikos. 2005;108(1):47-57.

Stirnemann I, Mortelliti A, Gibbons P, Lindenmayer DB. Correction: Fine-Scale Habitat Heterogeneity Influences Occupancy in Terrestrial Mammals in a Temperate Region of Australia. PLoS One. 2015;10(10):e0140802.

Fischer C, Flohre A, Clement LW, Batáry P, Weisser WW, Tscharntke T, Thies C. Mixed effects of landscape structure and farming practice on bird diversity. Agr Ecosyst Environ. 2011;141(1):119-25.

Schooley RL, Branch, LC. Habitat quality of source patches and connectivity in fragmented landscapes. Biodivers Conserv. 2011;20(8):1611-23.

Dickson BG, Roemer GW, McRae BH, Rundall JM. Models of regional habitat quality and connectivity for pumas (Puma concolor) in the southwestern United States. PLoS One. 2011;8(12):e81898.

Tews J, Brose U, Grimm V, Tielbörger K, Wichmann MC, Schwager M, Jeltsch F. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. J Biogeogr. 2004;31(1):79-92.

Ye X, Skidmore AK, Wang T. Within-patch habitat quality determines the resilience of specialist species in fragmented landscapes. Landsc Ecol. 2013;28(1):135-47.

Pavkov G, editor. Specijalni rezervat prirode “Slano Kopovo” – predlog za stavljanje pod zaštitu kao prirodnog dobra od izuzetnog značaja. 1999. Novi Sad: Zavod za zaštitu prirode Srbije, Beograd, Odeljenje Novi Sad. 80 p. Serbian.

Panjković B, Kovačev N, editors. Specijalni rezervat prirode “Okanj bara” –predlog za stavljanje pod zaštitu kao zaštićenog područja I kategorije. Novi Sad: Pokrajinski Zavod za zaštitu prirode. 2011. 373p. Serbian.

Kicošev V, Tucakov M, Kovačev M. Park prirode “Rusanda” - predlog za stavljanje pod zaštitu kao zaštićenog područja II kategorije. Novi Sad: Pokrajinski Zavod za zaštitu prirode. 2011. 254p. Serbian.

Mérő TO, Bocz R, Polyák L, Horváth G, Lengyel S. Local habitat management and landscape‐scale restoration influence small‐mammal communities in grasslands. Anim Conserv. 2015;18(5):442-50.

Seabloom EW, Bjørnstad ON, Bolker BM, Reichman OJ. Spatial signature of environmental heterogeneity, dispersal, and competition in successional grasslands. Ecol Monogr. 2005;75(2):199-214.

Barker OE, Derocher AE. Habitat selection by arctic ground squirrels (Spermophilus parryii). J Mammal. 2010;91(5):1251-60.

Bylo LN, Koper N, Molloy KA. Grazing intensity influences ground squirrel and American badger habitat use in mixed-grass prairies. Rangel Ecol Manag. 2014;67(3):247-54.

Győri-Koósz B, Katona K, Altbäcker V. Diet composition of European Ground Squirrel in grazed or mowed grasslands. Hung Small Game Bull. 2013;11:215-25. Hungarian.

Győri-Koósz B. Diet preference of the European ground squirrel [Spermophilus citellus (Linnaeus, 1766)] in Hungarian natural and seminatural grassland habitats investigation by floristic composition and microhistological faeces analysis [dissertation], [Sopron]: Institute of Wildlife Management and Vertebral Zoology, Faculty of Forestry, University of West Hungary; 2015. 16 p.

Čavlović D, Beloica J, Obratov-Petković D, Đurđević V, Košanin O. Simulation of long-term changes in environmental factors and grassland composition in three protected areas of Serbia. Tuexenia. 2017;37:431-46.

Váczi O. The effects of abiotic environmental factors on spatio-temporal activity pattern of the European ground squirrel (Spermophilus citellus) [dissertation]. [Budapest]: Eötvös Loránd University. 2005. 131 p. Hungarian.

Váczi O, Koósz B, Altbäcker V. Modified ambient temperature perception affects daily activity patterns in the European ground squirrel (Spermophilus citellus). J Mammal. 2006;87(1):54-9.

Vuković A, Vujadinović M, Rendulić S, Djurdjević V, Ruml M, Babić V, Popović, D. Global warming impact on climate change in Serbia for the period 1961-2100. Thermal Science. 2018;22(6):2267-80.

McCain CM, King SR. Body size and activity times mediate mammalian responses to climate change. Glob Chang Biol. 2014;20(6):1760-9.

Nikolić T, Radišić D, Ćosić N, Díaz-Delgado R, Milić D, Vujić A, Ćirović D. Landscape heterogeneity effects on keystone rodent species: agro-ecological zoning for conservation of open grasslands. Biodivers Conserv. 2019;28(12): 3139-58.

Boutin, S, Lane, JE. Climate change and mammals: evolutionary versus plastic responses. Evol Appl. 2014;7(1):29-41.

Downloads

Published

2020-03-24

How to Cite

1.
Nikolić T, Arok M, Radišić D, Mirč M, Velaja L, Milić D, Ćirović D. Endangered species’ trait responses to environmental variability in agricultural settings. Arch Biol Sci [Internet]. 2020Mar.24 [cited 2024Mar.29];72(1):13-21. Available from: https://www.serbiosoc.org.rs/arch/index.php/abs/article/view/4485

Issue

Section

Articles

Most read articles by the same author(s)