Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T16:45:08.532Z Has data issue: false hasContentIssue false
  • English
  • Français

Shared haemogregarine infections in competing lacertids

Published online by Cambridge University Press:  28 September 2021

Urban Dajčman Open the ORCID record for Urban Dajčman [Opens in a new window] ,
Miguel A. Carretero ,
Rodrigo Megía-Palma ,
Ana Perera ,
Rok Kostanjšek  and
Anamarija Žagar
Urban Dajčman
Affiliation:
Biotechnical Faculty of the University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia
Miguel A. Carretero
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre, 4169-007 Porto, Portugal
Rodrigo Megía-Palma
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal Department of Biomedicine and Biotechnology, Universidad de Alcalá, Parasitology Area, School of Pharmacy, 28805, Alcalá de Henares, Spain
Ana Perera
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal
Rok Kostanjšek
Affiliation:
Biotechnical Faculty of the University of Ljubljana, Jamnikarjeva 101, 1000 Ljubljana, Slovenia
Anamarija Žagar*
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal Department of Organisms and Ecosystem Research, National Institute of Biology, Večna pot 111, SI-1000 Ljubljana, Slovenia
*
Author for correspondence: Anamarija Žagar, E-mail: anamarija.zagar@nib.si
Get access Rights & Permissions [Opens in a new window]

Abstract

In parasite–host interactions host species may differ in their ability to fight parasitic infections, while other ecological interactions, including competition, may differentially alter their physiological state, making them even more susceptible to parasites. In this study, we analyse the haemogregarine blood parasites infecting two competing lizard species, Iberolacerta horvathi and Podarcis muralis, and explore host–parasite relationships under different host competition scenarios. Both species were infected with haemogregarine parasites belonging to the genus Karyolysus. Using the 18S rRNA gene, six new Karyolysus haplotypes were identified clustering with other Central and Eastern European samples, and widely shared between both lizard hosts. Haemogregarine infections were detected at all sampled sites with over 50% of individuals parasitized. Overall, I. horvathi was more frequently and also more intensely parasitized than P. muralis, with higher infection rates observed in syntopy. Males of both species tended to be more frequently infected and showed a higher infection intensity than conspecific females. The results suggest that parasitisation by haemogregarines may be relevant in the dynamics of the competitive relationship between these lizard species. More studies, including immunological response analysis, and the identification of the vectors are needed to better understand host–parasite relationships and competition.

Keywords

CompetitionhaemogregarinesKaryolysuslacertidaesyntopy
Type
Research Article
Information
Parasitology , Volume 149 , Issue 2 , February 2022 , pp. 193 - 202
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alizon, S, de Roode, JC and Michalakis, Y (2013) Multiple infections and the evolution of virulence. Ecology Letters 16, 556–567.10.1111/ele.12076CrossRefGoogle ScholarPubMed
Álvarez-Calvo, J (1975) Nuevas especies de hemococcidios en lacértidos españoles. Cuadernos de Ciencias Biológicas 4, 207–222.Google Scholar
Álvarez-Ruiz, L, Megía-Palma, R, Reguera, S, Ruiz, S, Zamora-Camacho, F, Figuerola, J and Moreno-Rueda, G (2018) Opposed elevational variation in prevalence and intensity of endoparasites and their vectors in a lizard. Current Zoology 64, 197–204.10.1093/cz/zoy002CrossRefGoogle Scholar
Amo, L, López, P and Martín, J (2004) Prevalence and intensity of haemogregarinid blood parasites in a population of the Iberian rock lizard, Lacerta monticola. Parasitology Research 94, 290–293.10.1007/s00436-004-1212-7CrossRefGoogle Scholar
Arakelyan, M, Harutyunyan, T, Aghayan, S and Carretero, M (2019) Infection of parthenogenetic lizards by blood parasites does not support the “red queen hypothesis” but reveals the costs of sex. Zoology 136, 125709.10.1016/j.zool.2019.125709CrossRefGoogle Scholar
Arneberg, P, Skorping, A, Grenfell, B and Read, A (1998) Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society of London. Series B: Biological Sciences 265, 1283–1289.10.1098/rspb.1998.0431CrossRefGoogle Scholar
Barnard, S and Upton, S (1994) A Veterinary Guide to the Parasites of Reptiles. Protozoa: Krieger Publishing Company.Google Scholar
Barrientos, R and Megía-Palma, R (2021) Associated costs of mitigation-driven translocation in small lizards. Amphibia-Reptilia 1, 1–8.Google Scholar
Barthel, A, Kopka, I, Vogel, H, Zipfel, P, Heckel, D and Groot, A (2014) Immune defence strategies of generalist and specialist insect herbivores. Proceedings of the Royal Society B: Biological Sciences 281, 20140897.10.1098/rspb.2014.0897CrossRefGoogle ScholarPubMed
Barton, K (2020) MuMIn: Multi-Model Inference. R package version 1.43.17. https://CRAN.R-project.org/package=MuMIn.Google Scholar
Belliure, J, Smith, L and Sorci, G (2004) Effect of testosterone on T cell-mediated immunity in two species of Mediterranean lacertid lizards. Journal of Experimental Zoology 301A, 411–418.10.1002/jez.a.20068CrossRefGoogle Scholar
Beyer, T and Sidorenko, N (1984) Karyolysus sp. (Haemogregarinidae, Adeleida, Apicomplexa): host-parasite relationships of persisting stages. The Journal of Protozoology 31, 513–517.10.1111/j.1550-7408.1984.tb05493.xCrossRefGoogle Scholar
Breg, A, Janota, B, Peganc, M, Petrovič, I, Tome, S and Vamberger, M (2010) Slikovni določevalni ključ za plazilce Slovenije. Ljubljana: Societas Herpetologica Slovenica.Google Scholar
Carbayo, J, Martín, J and Civantos, E (2019) Habitat type influences parasite load in Algerian Psammodromus (Psammodromus algirus) lizards. Canadian Journal of Zoology 97, 172–180.10.1139/cjz-2018-0145CrossRefGoogle Scholar
Cocca, W, Žagar, A, Sillero, N, Jowers, M, Krofel, M, Lužnik, M, Podnar, M, Tvrtković, N, Carretero, MA and Crottini, A (2021) Genetic diversity of Horvath's Rock Lizard meets current environmental restrictions. Conservation Genetics 22, 483–498.10.1007/s10592-021-01351-4CrossRefGoogle Scholar
Damas-Moreira, I, Harris, D, Rosado, D, Tavares, I, Maia, J, Salvi, D and Perera, A (2014) Consequences of haemogregarine infection on the escape distance in the lacertid lizard, Podarcis vaucheri. Acta Herpetologica 9, 119–123.Google Scholar
Dormann, C, Calabrese, J, Guillera-Arroita, G, Matechou, E, Bahn, V, Barton, K, Beale, C, Ciuti, S, Elith, J and Gerstner, K and others (2018) Model averaging in ecology: a review of Bayesian, information-theoretic, and tactical approaches for predictive inference. Ecological Monographs, 88, 485–504.10.1002/ecm.1309CrossRefGoogle Scholar
Drechsler, RM, Belliure, J and Megía-Palma, R (2021) Phenological and intrinsic predictors of mite and haemacoccidian infection dynamics in a Mediterranean community of lizards. Parasitology 148, 1328–1338.10.1017/S0031182021000858CrossRefGoogle Scholar
Ebert, D, Lipsitch, M and Mangin, K (2000) The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. The American Naturalist 156, 459–477.10.1086/303404CrossRefGoogle ScholarPubMed
Ekner-Grzyb, A, Sajkowska, Z, Dudek, K, Gawałek, M, Skórka, P and Tryjanowski, P (2013) Locomotor performance of sand lizards (Lacerta agilis): effects of predatory pressure and parasite load. Acta Ethologica 16, 173–179.10.1007/s10211-013-0148-2CrossRefGoogle ScholarPubMed
Engelstädter, J and Hurst, G (2009) The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology, Evolution, and Systematics 40, 127–149.10.1146/annurev.ecolsys.110308.120206CrossRefGoogle Scholar
Garcia-Porta, J, Irisarri, I, Kirchner, M, Rodríguez, A, Kirchhof, S, Brown, J, MacLeod, A, Turner, A, Ahmadzadeh, F and Albaladejo, G and others (2019) Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nature Communications, 10, 1–12.10.1038/s41467-019-11943-xCrossRefGoogle ScholarPubMed
Garrido, M and Pérez-Mellado, V (2013) Patterns of parasitism in insular lizards: effects of body size, condition and resource availability. Zoology 116, 106–112.10.1016/j.zool.2012.09.003CrossRefGoogle ScholarPubMed
Goater, C and Ward, P (1992) Negative effects of Rhabdias bufonis (Nematoda) on the growth and survival of toads (Bufo bufo). Oecologia 89, 161–165.10.1007/BF00317213CrossRefGoogle Scholar
Godfrey, S, Bull, C, Murray, K and Gardner, M (2006) Transmission mode and distribution of parasites among groups of the social lizard Egernia stokesii. Parasitology Research 99, 223–230.10.1007/s00436-005-0120-9CrossRefGoogle ScholarPubMed
Haklová-Kočíková, B, Hižňanová, A, Majláth, I, Račka, K, Harris, D, Földvári, G, Tryjanowski, P, Kokošová, N, Malčeková, B and Majláthová, V (2014) Morphological and molecular characterization of Karyolysus – a neglected but common parasite infecting some European lizards. Parasites & Vectors 7, 1–12.10.1186/s13071-014-0555-xCrossRefGoogle ScholarPubMed
Hartig, F (2020) DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed) Regression Models. R package version 0.3.2.0. https://CRAN.R-project.org/package=DHARMa.Google Scholar
Hassl, AR (2012) Blood parasitism by hemogregarines in Central European lizards. Herpetozoa 25, 83–86.Google Scholar
Hatcher, MJ, Dick, JT and Dunn, AM (2006) How parasites affect interactions between competitors and predators. Ecology Letters 9, 1253–1271.10.1111/j.1461-0248.2006.00964.xCrossRefGoogle ScholarPubMed
Hrazdilová, K, Červená, B, Blanvillain, C, Foronda, P and Modrý, D (2021) Quest for the type species of the genus Hepatozoon – phylogenetic position of hemogregarines of rats and consequences for taxonomy. Systematics and Biodiversity 19, 622–631.10.1080/14772000.2021.1903616CrossRefGoogle Scholar
Huelsenbeck, J, Ronquist, F, Nielsen, R and Bollback, J (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.10.1126/science.1065889CrossRefGoogle ScholarPubMed
Jong-Brink, M, Bergamin-Sassen, M and Soto, M (2001) Multiple strategies of schistosomes to meet their requirements in the intermediate snail host. Parasitology 123, 129–141.10.1017/S0031182001008149CrossRefGoogle ScholarPubMed
Karadjian, G, Chavatte, JM and Landau, I (2015) Systematic revision of the adeleid haemogregarines, with creation of Bartazoon ng, reassignment of Hepatozoon argantis Garnham, 1954 to Hemolivia, and molecular data on Hemolivia stellata. Parasite 22, 31.10.1051/parasite/2015031CrossRefGoogle Scholar
Katoh, K, Misawa, K, Kuma, KI and Miyata, T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.10.1093/nar/gkf436CrossRefGoogle ScholarPubMed
Kozjek, K, Dolinar, M and Skok, G (2017) Objective climate classification of Slovenia. International Journal of Climatology 37, 848–860.10.1002/joc.5042CrossRefGoogle Scholar
Krofel, M, Cafuta, V, Planinc, G, Sopotnik, M, Šalamun, A, Tome, S, Vamberger, M and Žagar, A (2009) Razširjenost plazilcev v Sloveniji: pregled podatkov, zbranih do leta 2009. Natura Sloveniae 11, 61–99.Google Scholar
Kryštufek, B. and Janžekovič, F (1999) Ključ za Določanje Vretenčarjev Slovenije. Ljubljana: DZS.Google Scholar
Lanfear, R, Frandsen, P, Wright, A, Senfeld, T. and Calcott, B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34, 772–773.Google ScholarPubMed
Lazić, M, Carretero, M, Živković, U and Crnobrnja-Isailović, J (2017) City life has fitness costs: reduced body condition and increased parasite load in urban common wall lizards, Podarcis muralis. Salamandra 53, 10–17.Google Scholar
Maia, J, Harris, D, Carranza, S and Gómez-Díaz, E (2014) A comparison of multiple methods for estimating parasitemia of hemogregarine hemoparasites (Apicomplexa: Adeleorina) and its application for studying infection in natural populations. PloS One 9, e95010.10.1371/journal.pone.0095010CrossRefGoogle ScholarPubMed
Maia, J, Carranza, S and Harris, D (2016) Comments on the systematic revision of adeleid haemogregarines: are more data needed? Journal of Parasitology 102, 549–552.10.1645/15-930CrossRefGoogle ScholarPubMed
Megía-Palma, R, Martínez, J and Merino, S (2016) A structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. The Science of Nature 103, 1–10.10.1007/s00114-016-1378-8CrossRefGoogle Scholar
Megía-Palma, R, Martínez, J and Merino, S (2018a) Manipulation of parasite load induces significant changes in the structural-based throat color of male Iberian green lizards. Current Zoology 64, 293–302.10.1093/cz/zox036CrossRefGoogle Scholar
Megía-Palma, R, Martínez, J, Cuervo, JJ, Belliure, J, Jiménez-Robles, O, Gomes, V and Merino, S (2018b) Molecular evidence for host–parasite co-speciation between lizards and Schellackia parasites. International Journal for Parasitology, 48, 709–718.10.1016/j.ijpara.2018.03.003CrossRefGoogle Scholar
Megía-Palma, R, Jiménez-Robles, O, Hernández-Agüero, J and Riva, I (2020a) Plasticity of haemoglobin concentration and thermoregulation in a mountain lizard. Journal of Thermal Biology 92, 102656.10.1016/j.jtherbio.2020.102656CrossRefGoogle Scholar
Megía-Palma, R, Arregui, L, Pozo, I, Žagar, A, Serén, N, Carretero, MA and Merino, S (2020b) Geographic patterns of stress in insular lizards reveal anthropogenic and climatic signatures. Science of the Total Environment 749, 141655.10.1016/j.scitotenv.2020.141655CrossRefGoogle Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE) (pp 1–8). New Orleans, LA.10.1109/GCE.2010.5676129CrossRefGoogle Scholar
Netherlands, E, Cook, C, Du Preez, L, Vanhove, M, Brendonck, L and Smit, N (2018) Monophyly of the species of Hepatozoon (Adeleorina: Hepatozoidae) parasitizing (African) anurans, with the description of three new species from hyperoliid frogs in South Africa. Parasitology 145, 1039–1050.10.1017/S003118201700213XCrossRefGoogle ScholarPubMed
O'Donoghue, P (2017) Haemoprotozoa: making biological sense of molecular phylogenies. International Journal for Parasitology: Parasites and Wildlife 6, 241–256.Google ScholarPubMed
Oppliger, A and Clobert, J (1997) Reduced tail regeneration in the common lizard, Lacerta vivipara, parasitized by blood parasites. Functional Ecology 11, 652–655.10.1046/j.1365-2435.1997.00134.xCrossRefGoogle Scholar
Oppliger, A, Celerier, M and Clobert, J (1996) Physiological and behaviour changes in common lizards parasitized by haemogregarines. Parasitology 113, 433–438.10.1017/S003118200008149XCrossRefGoogle Scholar
Oppliger, A, Clobert, J, Lecomte, J, Lorenzon, P, Boudjemadi, K and John-Alder, H (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecology Letters 1, 129–138.10.1046/j.1461-0248.1998.00028.xCrossRefGoogle Scholar
Osojnik, N, Žagar, A, Carretero, M, García-Muñoz, E and Vrezec, A (2013) Ecophysiological dissimilarities of two sympatric lizards. Herpetologica 69, 445–454.10.1655/HERPETOLOGICA-D-13-00014CrossRefGoogle Scholar
Perko, D and Orožen Adamič, M (1998) Slovenija: pokrajine in ljudje; atlas Slovenije v sliki in besedi. Ljubljana: Založba Mladinska Knjiga.Google Scholar
Poulin, R (1999) The functional importance of parasites in animal communities: many roles at many levels? International Journal for Parasitology 29, 903–914.10.1016/S0020-7519(99)00045-4CrossRefGoogle ScholarPubMed
Presnell, J, Schreibman, M. and Humason, G (1997) Humason's Animal Tissue Techniques. Baltimore: Johns Hopkins University Press.Google Scholar
Puente, J, Martinez, J, Rivero-de Aguilar, J, Herrero, J and Merino, S (2011) On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges. Molecular Ecology 20, 3275–3287.10.1111/j.1365-294X.2011.05136.xCrossRefGoogle Scholar
Pulgarìn-R, P, Gómez, J, Robinson, S, Ricklefs, R and Cadena, C (2018) Host species, and not environment, predicts variation in blood parasite prevalence, distribution, and diversity along a humidity gradient in Northern South America. Ecology and Evolution 8, 3800–3814.10.1002/ece3.3785CrossRefGoogle Scholar
R Core Team (2020) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Rambaut, A, Drummond, A, Xie, D, Baele, G and Suchard, M (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901.10.1093/sysbio/syy032CrossRefGoogle ScholarPubMed
Reichenow, E (1913) Karyolysus lacertae, ein wirtswechselndes Coccidium an der Eidechse Lacerta muralis und der Milbe Liponyssus saurarum. Arb Kaiserlichen Gesundheitsamte 45, 317–363.Google Scholar
Reichenow, E (1919) Der Entwicklungsgang der Hämococcidien Karyolysus und Schellackia nov. gen. Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 10, 440–447.Google Scholar
Richard, J and Lapini, L (1993) Trophic niche overlap in syntopic populations of Lacerta horvathi and Podarcis muralis (Reptilia, Lacertidae). Atti del museo civico di storia naturale di Trieste 45, 151–157.Google Scholar
Robar, N, Murray, D and Burness, G (2011) Effects of parasites on host energy expenditure: the resting metabolic rate stalemate. Canadian Journal of Zoology 89, 1146–1155.10.1139/z11-084CrossRefGoogle Scholar
Roberts, ML, Buchanan, KL and Evans, MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal behaviour 68, 227–239.10.1016/j.anbehav.2004.05.001CrossRefGoogle Scholar
Ronquist, F and Huelsenbeck, J (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.10.1093/bioinformatics/btg180CrossRefGoogle ScholarPubMed
RStudio Team (2021) RStudio: Integrated Development for R. Boston, MA: RStudio, PBC.Google Scholar
Rutschmann, A, Dupoué, A, Miles, DB, Megía-Palma, R, Lauden, C, Richard, M, Badiane, A, Rozen-Rechels, D, Brevet, M, Blaimont, P, Meylan, S, Clobert, J, Le Galliard, J (2021) Intense nocturnal warming alters growth strategies, colouration and parasite load in a diurnal lizard. J Anim Ecol , 90, 1864–1877.10.1111/1365-2656.13502CrossRefGoogle Scholar
Salvador, A, Veiga, J, Martin, J, Lopez, P, Abelenda, M and Puertac, M (1996) The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation. Behavioral Ecology 7, 145–150.10.1093/beheco/7.2.145CrossRefGoogle Scholar
Salvi, D, Harris, D, Kaliontzopoulou, A, Carretero, M and Pinho, C (2013) Persistence across Pleistocene ice ages in Mediterranean and extra-Mediterranean refugia: phylogeographic insights from the common wall lizard. BMC Evolutionary Biology 13, 1–18.10.1186/1471-2148-13-147CrossRefGoogle ScholarPubMed
Sambrook, J, Fritsch, E and Maniatis, T (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory PressGoogle Scholar
Schall, J (1992) Parasite-mediated competition in Anolis lizards. Oecologia 92, 58–64.10.1007/BF00317262CrossRefGoogle ScholarPubMed
Scott, M and Dobson, A (1989) The role of parasites in regulating host abundance. Parasitology Today 5, 176–183.10.1016/0169-4758(89)90140-3CrossRefGoogle ScholarPubMed
Sillero, N, Dos Santos, R, Teodoro, A and Carretero, M (2021) Ecological niche models improve home range estimations. Journal of Zoology 313, 145–157.10.1111/jzo.12844CrossRefGoogle Scholar
Smallridge, C and Bull, C (2000) Prevalence and intensity of the blood parasite Hemolivia mariae in a field population of the skink Tiliqua rugosa. Parasitology Research 86, 655–660.10.1007/PL00008547CrossRefGoogle Scholar
Sorci, G, Clobert, J and Michalakis, Y (1996) Cost of reproduction and cost of parasitism in the common lizard, Lacerta vivipara. Oikos, 121–130.10.2307/3545754CrossRefGoogle Scholar
Speybroeck, J, Beukema, W, Bok, B, Voort, J and Velikov, I (2016) Field Guide to the Amphibians & Reptiles of Britain and Europe. London: Bloomsbury Publishing.Google Scholar
Svahn, K (1974) Incidence of blood parasites of the genus Karyolysus (Coccidia) in Scandinavian lizards. Oikos, 43–53.10.2307/3543544CrossRefGoogle Scholar
Svahn, K (1975) Blood parasites of the genus Karyolysus (Coccidia, Adeleidae) in Scandinavian lizards. Description and life cycle. Norwegian Journal of Zoology 23, 277–295.Google Scholar
Telford, S (2009) Hemoparasites of the Reptilia. Boca Raton: CRC Press.Google Scholar
Tomé, B, Pereira, A, Harris, D, Carretero, M and Perera, A (2019) A paradise for parasites? Seven new haemogregarine species infecting lizards from the Canary Islands. Parasitology 146, 728–739.10.1017/S0031182018002160CrossRefGoogle ScholarPubMed
Tomé, B, Harris, DJ, Perera, A and Damas-Moreira, I (2021) Invasive lizard has fewer parasites than native congener. Parasitology Research 120, 2953–2957.10.1007/s00436-021-07233-5CrossRefGoogle ScholarPubMed
Toth, LG, Szabo, M and Webb, D (1995) Adaptation of the tetrazolium reduction test for the measurement of the electron transport system (ETS) activity during embryonic development of medaka. Journal of Fish Biology 46, 835–844.10.1111/j.1095-8649.1995.tb01606.xCrossRefGoogle Scholar
Veiga, J, Salvador, A, Merino, S and Puerta, M (1998) Reproductive effort affects immune response and parasite infection in a lizard: a phenotypic manipulation using testosterone. Oikos 313–318.10.2307/3546971CrossRefGoogle Scholar
Wieczorek, M, Rektor, R, Najbar, B and Morelli, F (2020) Tick parasitism is associated with home range area in the sand lizard, Lacerta agilis. Amphibia-Reptilia 1, 1–10.Google Scholar
Wu, Q, Richard, M, Rutschmann, A, Miles, DB and Clobert, J (2019) Environmental variation mediates the prevalence and co-occurrence of parasites in the common lizard, Zootoca vivipara. BMC Ecology 19, 1–11.10.1186/s12898-019-0259-3CrossRefGoogle ScholarPubMed
Žagar, A (2008) The lowest altitudinal record of Horvath's rock lizard (Iberolacerta horvathi) in Slovenia. Natura Sloveniae 10, 59–61.Google Scholar
Žagar, A (2016) Altitudinal distribution and habitat use of the common wall lizard Podarcis muralis (Linnaeus, 1768) and the Horvath's rock lizard Iberolacerta horvathi (Méhely, 1904) in the Kočevsko region (S Slovenia)/Višinska razširjenost in raba prostora pozidne kušč. Natura Sloveniae 18, 47.Google Scholar
Žagar, A, Osojnik, N, Carretero, M and Vrezec, A (2012) Quantifying the intersexual and interspecific morphometric variation in two resembling sympatric lacertids: Iberolacerta horvathi and Podarcis muralis. Acta Herpetologica 7, 29–39.Google Scholar
Žagar, A, Kos, I and Vrezec, A (2013) Habitat segregation patterns of reptiles in Northern Dinaric Mountains (Slovenia). Amphibia-Reptilia 34, 263–268.10.1163/15685381-00002889CrossRefGoogle Scholar
Žagar, A, Carretero, M, Krofel, M, Lužnik, M, Podnar, M and Tvrtković, N (2014) Reptile survey in Dinara Mountain (Croatia) revealed the southernmost known population of Horvath's rock lizard (Iberolacerta horvathi). Natura Croatica 23, 235.Google Scholar
Žagar, A, Bitenc, K, Vrezec, A and Carretero, M (2015a) Predators as mediators: differential antipredator behavior in competitive lizard species in a multi-predator environment. Zoologischer Anzeiger-A Journal of Comparative Zoology 259, 31–40.10.1016/j.jcz.2015.10.002CrossRefGoogle Scholar
Žagar, A, Carretero, M, Osojnik, N, Sillero, N and Vrezec, A (2015b) A place in the sun: interspecific interference affects thermoregulation in coexisting lizards. Behavioral Ecology and Sociobiology 69, 1127–1137.10.1007/s00265-015-1927-8CrossRefGoogle Scholar
Žagar, A, Simčič, T, Carretero, M and Vrezec, A (2015c) The role of metabolism in understanding the altitudinal segregation pattern of two potentially interacting lizards. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 179, 1–6.10.1016/j.cbpa.2014.08.018CrossRefGoogle Scholar
Žagar, A, Carretero, M, Vrezec, A, Drašler, K and Kaliontzopoulou, A (2017) Towards a functional understanding of species coexistence: ecomorphological variation in relation to whole-organism performance in two sympatric lizards. Functional Ecology 31, 1780–1791.10.1111/1365-2435.12878CrossRefGoogle Scholar
Zechmeisterová, K, De Bellocq, J and Široky, P (2019) Diversity of Karyolysus and Schellackia from the Iberian lizard Lacerta schreiberi with sequence data from engorged ticks. Parasitology 146, 1690–1698.10.1017/S0031182019001112CrossRefGoogle ScholarPubMed
Zuk, M and McKean, K (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.10.1016/S0020-7519(96)80001-4CrossRefGoogle ScholarPubMed
Supplementary material: File

Dajčman et al. supplementary material

Dajčman et al. supplementary material 1

Download Dajčman et al. supplementary material(File)
File 22.7 KB
Supplementary material: Image

Dajčman et al. supplementary material

Dajčman et al. supplementary material 2

Download Dajčman et al. supplementary material(Image)
Image 1.2 MB