Coexisting lacertid lizard species Podarcis siculus and Podarcis melisellensis differ in dopamine brain concentrations

  • Barbara Nikolic
  • Paula Josic
  • Davorka Buric
  • Mirta Tkalec
  • Duje Lisicic
  • Sofia A. BlazevicEmail author
  • Dubravka Hranilovic
Original Paper


In the eastern Adriatic, Podarcis siculus, an invasive species, competitively excludes the native Podarcis melisellensis. Monoamine neurotransmitters—serotonin (5HT), dopamine (DA), and noradrenaline (NA)—are implicated in social behavior, and could lie at the basis of the direct behavioral interference of P. siculus with P. melisellensis. To understand the relationship between social behavior and monoamines, as well as the differences in behavior between P. siculus and P. melisellensis, we developed a high-performance liquid chromatography (UV/VIS detection) method with which we were able to reliably measure concentrations of 5HT, DA, and NA in 32 brains of the two lizard species. We observed no statistically significant influence of species, sex, or their interaction on brain NA and 5HT concentrations. Statistically significant influence of species on dopamine levels were recorded, with P. siculus having twice as much dopamine in their brains. Taking into account that a significant aggressive relationship, with P. siculus dominating over P. melisellensis, has been previously observed, and that dopamine directly influences this behavior, the observed differences in dopamine levels could represent a trait in these species and may contribute to the competitive exclusion of P. melisellensis by P. siculus in the eastern Adriatic.


Monoamines Competitive exclusion Aggressive behavior HPLC Eastern Adriatic 



The authors wish to thank MSc Dora Persic for her help during the adaptation of the method for HPLC separation, MSc Marko Glogoski for his assistance in the retrieval of the animals from the wild, and Marija Potocic for her assistance in caring for the animals during captivity.


This study was funded by the Support from the University of Zagreb (UniZg PP0031 to DH). The funding source had no involvement in any stage of the research and publication of the results.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.


  1. Breed MD, Moore J (2016) Homeostasis and time budgets. In: Breed MD, Moore J (eds) Animal behavior, 2nd edn. Academic Press, New York, pp 109–144CrossRefGoogle Scholar
  2. Capaldo A, Laforgia V, Sciarrillo R et al (2004) Effects of dopamine on the adrenal gland of Podarcis sicula (Reptilia, Lacertidae). Gen Comp Endocrinol 135:17–24. CrossRefGoogle Scholar
  3. Capula M (1992) Competitive exclusion between Podarcis lizards from Thyrrenian islands: inference from comparative species distributions. In: Korsos Z, Kiss I (eds) Proceedings of the 6th Ordinary General Meeting Societas Europaea Herpetologica. Hungarian Natural History Museum, Budapest, Hungary, pp 89–93Google Scholar
  4. Capula M (2002) Genetic evidence of natural hybridization between Podarcis sicula and Podarcis tiliguerta (Reptilia: Lacertidae). Amphib Reptil 23:313–321. CrossRefGoogle Scholar
  5. Capula M, Luiselli L, Bologna MA, Ceccarelli A (2002) The decline of the Aeolian wall lizard, Podarcis raffonei: causes and conservation proposals. Oryx 36:66–72. CrossRefGoogle Scholar
  6. Carretero MA (2008) An integrated Assessment of a group with complex systematics: the Iberomaghrebian lizard genus Podarcis (Squamata, Lacertidae). Integr Zool 3:247–266. CrossRefGoogle Scholar
  7. Cox NA, Temple HJ (2009) European red list of reptiles. Office for Official Publications of the European Communities, LuxembourgGoogle Scholar
  8. De Almeida RMM, Ferrari PF, Parmigiani S, Miczek KA (2005) Escalated aggressive behavior: dopamine, serotonin and GABA. Eur J Pharmacol 526:51–64. CrossRefGoogle Scholar
  9. De Falco M, Sellitti A, Sciarrillo R et al (2014) Nonylphenol effects on the HPA axis of the bioindicator vertebrate, Podarcis sicula lizard. Chemosphere 104:190–196. CrossRefGoogle Scholar
  10. Downes S, Bauwens D (2002) An experimental demonstration of direct behavioural interference in two Mediterranean lacertid lizard species. Anim Behav 63:1037–1046. CrossRefGoogle Scholar
  11. Downes S, Bauwens D (2004) Associations between first encounters and ensuing social relations within dyads of two species of lacertid lizards. Behav Ecol 15:938–945. CrossRefGoogle Scholar
  12. Font E, Barbosa D, Sampedro C, Carazo P (2012) Social behavior, chemical communication, and adult neurogenesis: studies of scent mark function in Podarcis wall lizards. Gen Comp Endocrinol 177:9–17. CrossRefGoogle Scholar
  13. Gorman GC, Soulé M, Yang SY, Nevo E (1975) Evolutionary genetics of insular adriatic lizards. Evolution 29:52–71. CrossRefGoogle Scholar
  14. Grillner S, Robertson B (2016) The Basal Ganglia over 500 million years. Curr Biol 26:R1088–R1100. CrossRefGoogle Scholar
  15. Herrel A, Huyghe K, Vanhooydonck B et al (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proc Natl Acad Sci USA 105:4792–4795. CrossRefGoogle Scholar
  16. Hranilovic D, Blazevic S, Ivica N et al (2011) The effects of the perinatal treatment with 5-hydroxytryptophan or tranylcypromine on the peripheral and central serotonin homeostasis in adult rats. Neurochem Int 59:202–207. CrossRefGoogle Scholar
  17. Huyghe K, Husak JF, Herrel A et al (2009) Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis. Horm Behav 55:488–494. CrossRefGoogle Scholar
  18. Jelić D, Kuljerić M, Koren T et al (2012) Red book of amphibians and reptiles of Croatia. Ministry of Environmental and Nature Protection State, State Institute for Nature Protection, ZagrebGoogle Scholar
  19. Kabelik D, Alix VC, Singh LJ et al (2014) Neural activity in catecholaminergic populations following sexual and aggressive interactions in the brown anole, Anolis sagrei. Brain Res 1553:41–58. CrossRefGoogle Scholar
  20. Kaliontzopoulou A, Carretero MA, Llorente GA (2007) Multivariate and geometric morphometrics in the analysis of sexual dimorphism variation in Podarcis lizards. J Morphol 268:152–165. CrossRefGoogle Scholar
  21. Korzan WJ, Forster GL, Watt MJ, Summers CH (2006) Dopaminergic activity modulation via aggression, status, and a visual social signal. Behav Neurosci 120:93–102. CrossRefGoogle Scholar
  22. Leonard BE (2002) Stress, norepinephrine and depression. Acta Neuropsychiatr 14:173–180. CrossRefGoogle Scholar
  23. Libersat F, Pflueger H-J (2004) Monoamines and the orchestration of behavior. Bioscience 54:17.;2 CrossRefGoogle Scholar
  24. Ling TJ, Summers CH, Renner KJ, Watt MJ (2010) Opponent recognition and social status differentiate rapid neuroendocrine responses to social challenge. Physiol Behav 99:571–578. CrossRefGoogle Scholar
  25. Mamou R, Marniche F, Amroun M, Herrel A (2016) Trophic ecology of two sympatric lizard species: the Algerian sand lizard and the wall lizard in Djurdjura, northern Algeria. Zool Ecol 8005:1–9. Google Scholar
  26. McCarthy MM, De Vries GJ, Forger NG (2016) Sexual differentiation of the brain: a fresh look at mode, mechanisms, and meaning, 3rd edn. Elsevier, AmsterdamGoogle Scholar
  27. Michelangeli M, Smith CR, Wong BBM, Chapple DG (2017) Aggression mediates dispersal tendency in an invasive lizard. Anim Behav 133:29–34. CrossRefGoogle Scholar
  28. Miczek KA, Fish EW, De Bold JF, De Almeida RMM (2002) Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and γ-aminobutyric acid systems. Psychopharmacology 163:434–458. CrossRefGoogle Scholar
  29. Nevo E, Gorman GC, Soulé M et al (1972) Competitive exclusion between insular Lacerta species (Sauria, Lacertidae)—notes on experimental introductions. Oecologia 10:183–190. CrossRefGoogle Scholar
  30. Nikolic B, Persic D, Blazevic SA, Hranilovic D (2018) Development of HPLC method for serotonin, dopamine and noradrenaline determination in rat brain tissue samples. In: Jukic CI, Borcic E, Despotovic M (eds) NeuRi2018. Rijeka, Croatia, p 66Google Scholar
  31. Olivier B (2015) Serotonin: a never-ending story. Eur J Pharmacol 753:2–18. CrossRefGoogle Scholar
  32. Raynor RG (1989) Ecological segregation between Podarcis sicula and Podarcis melisellensis in Yugoslavia. Herpetol J 1:418–420Google Scholar
  33. Rhodes ME, Creel TJ, Nord AN (2010) Sex differences in CNS neurotransmitter influences on behavior. In: Pfaff DW, Arnold AP, Etgen AM et al (eds) Hormones, Brain and behavior, 2nd edn. Academic Press, New York, pp 2747–2787Google Scholar
  34. Robinson GE, Fernald RD, Clayton DF (2008) Genes and social behavior. Science 322(80):896–900. CrossRefGoogle Scholar
  35. Sagonas K, Kapsalas G, Valakos E, Pafilis P (2017) Living in sympatry: the effect of habitat partitioning on the thermoregulation of three Mediterranean lizards. J Therm Biol 65:130–137. CrossRefGoogle Scholar
  36. Sawin EA, Murali SG, Ney DM (2014) Differential effects of low-phenylalanine protein sources on brain neurotransmitters and behavior in C57Bl/6-Pahenu2 mice. Mol Genet Metab 111:452–461. CrossRefGoogle Scholar
  37. Stoof JC, Russchen FT, Verheijden PFHM, Hoogland PVJM (1987) A comparative study of the dopamine-acetylcholine interaction in telencephalic structures of the rat and of a reptile, the lizard Gekko gecko. Brain Res 404:273–281. CrossRefGoogle Scholar
  38. Tank AW, Wong DL (2015) Peripheral and central effects of circulating catecholamines. Compr Physiol 5:1–15. Google Scholar
  39. Thomas J, Khanam R, Vohora D (2015) A validated HPLC-UV method and optimization of sample preparation technique for norepinephrine and serotonin in mouse brain. Pharm Biol 53:1539–1544. CrossRefGoogle Scholar
  40. van Erp AMM, Miczek KA (2000) Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J Neurosci 20:9320–9325. CrossRefGoogle Scholar
  41. Watt MJ, Forster GL, Korzan WJ et al (2007) Rapid neuroendocrine responses evoked at the onset of social challenge. Physiol Behav 90:567–575. CrossRefGoogle Scholar
  42. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483–494. CrossRefGoogle Scholar
  43. Wu X, Wang R, Jiang Q et al (2014) Determination of amino acid neurotransmitters in rat hippocampi by HPLC-UV using NBD-F as a derivative. Biomed Chromatogr 28:459–462. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Division of Animal Physiology, Department of BiologyFaculty of Science, University of ZagrebZagrebCroatia
  2. 2.Division of Botany, Department of BiologyFaculty of Science, University of ZagrebZagrebCroatia

Personalised recommendations