Skip to main content
SpringerLink
Log in

Environmental enrichment increases the number of telencephalic but not tectal cells of angelfish (Pterophyllum scalare): an exploratory investigation using optical fractionator

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

Based on previous evidence that environmental enrichment is associated with telencephalic cellular proliferation and that stable visuotopic tectal circuits are essential for discrimination of placement and identity of stationary or moving objects in the visual field, differential plasticity is expected in these areas. Here we tested this hypothesis in the Angelfish (Pterophyllum scalare), a species of ornamental fish with great value in the aquarist trade. We hypothesized that total telencephalic cell number would increase under the influence of an enriched environment whereas the tectal cell number would not change. To test this hypothesis, 12 aquaria of 80 l each were used, with six fish in each. The aquaria had either an enriched environment (EE) including stones, plants, sand and the presence of another fish from the Loricariidae family for interspecific social interaction, or an impoverished environment (IE), in which stimuli were limited to intraspecific interactions in a barren aquarium. After 62 days, six fish from each treatment were euthanized, and their brains were fixed and sectioned for Nissl staining. Then, stereological estimates of the total number of cells were performed. The fish showed no differences in weight gain, feed conversion ratio, condition factor, specific growth rate or survival. Animals kept in the enriched environment had a higher number of total telencephalic cells than animals kept in the impoverished environment (1,038,555 ± 65,357 vs. 758,331 ± 51,587, bilateral t-test, p = 0.008), but a similar number of tectal optical cells (EE 424,097 ± 29,914 vs. IE 471,409 ± 50,850, bilateral t-test, p = 0.445752). We concluded that cell proliferation in response to stimulation by the enriched environment is differentially expressed in the telencephalon and tectal areas of Pterophyllum scalare.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abreu CC, Fernandes TN, Henrique EP, Pereira PDC, Marques SB, Herdeiro SLS, Guerreiro-Diniz C (2019) Small-scale environmental enrichment and exercise enhance learning and spatial memory of Carassius auratus, and increase cell proliferation in the telencephalon: an exploratory study. Braz J Med Bio Res 52:5

    Google Scholar 

  • Abrous DN, Wojtowicz JM (2008) Neurogenesis and hippocampal memory system. Cold Spring Harb Monogr Ser 52:445

    Google Scholar 

  • Agrillo C, Miletto Petrazzini ME, Tagliapietra C, Bisazza A (2012) Inter-specific differences in numerical abilities among teleost fish. Front Psychol 3:483

    PubMed  PubMed Central  Google Scholar 

  • Angelucci F, De Bartolo P, Gelfo F, Foti F, Cutuli D, Bossu P, Caltagirone C, Petrosini L (2009) Increased concentrations of nerve growth factor and brain-derived neurotrophic factor in the rat cerebellum after exposure to environmental enrichment. Cerebellum 8:499–506

    Article  CAS  PubMed  Google Scholar 

  • Barreto RE, Rodrigues P, Luchiari AC, Delicio HC (2006) Time-place learning in individually reared angelfish, but not in pearl cichlid. Behav Process 73:367–372

    Article  Google Scholar 

  • Birse SC, Leonard RB, Coggeshall RE (1980) Neuronal increase in various areas of the nervous system of the guppy, Lebistes. J Comp Neurol 194:291–301

    Article  CAS  PubMed  Google Scholar 

  • Branchi I, D’Andrea I, Fiore M, Di Fausto V, Aloe L, Alleva E (2006) Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol Psych 60:690–696

    Article  CAS  Google Scholar 

  • Cacho MS, Yamamoto ME, Chellappa S (2007) Mating system of the Amazonian cichlid angelfish Pterophyllum scalare. Braz J Biol 67:161–165

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KD (2016) Fish neurogenesis in context: assessing environmental influences on brain plasticity within a highly labile physiology and morphology. Brain Behav Evol 87:156–166

    Article  PubMed  Google Scholar 

  • Dunlap KD, Silva AC, Chung M (2011) Environmental complexity, seasonality and brain cell proliferation in a weakly electric fish, Brachyhypopomus gauderio. J Exp Biol 214:794–805

    Article  PubMed  PubMed Central  Google Scholar 

  • Eadie BD, Redila VA, Christie BR (2005) Voluntary exercise alters the cytoarchitecture of the adult dentate gyrus by increasing cellular proliferation, dendritic complexity, and spine density. J Comp Neurol 486:39–47

    Article  PubMed  Google Scholar 

  • Furuya WW, de Souza SR, Furuya VRB, Hayashi C, Ribeiro RP, (1998) Dietas peletizada e extrusada para machos revertidos de tilápias do Nilo (Oreochromis niloticus L.), na fase de terminação. Ciência Rural 28(3):483–487

  • Ge S, Sailor KA, Ming GL, Song H (2008) Synaptic integration and plasticity of new neurons in the adult hippocampus. J Physiol 586:3759–3765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glaser E, Wilson P (1998) The coefficient of error of optical fractionator population size estimates: a computer simulation comparing three estimators. J Microscop 192:163–171

    Article  CAS  Google Scholar 

  • Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492–2498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gundersen H, Jensen E (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Laplaza LM (2009) Recent social environment affects colour-assortative shoaling in juvenile angelfish (Pterophyllum scalare). Behav Process 82:39–44

    Article  Google Scholar 

  • Gómez-Laplaza LM, Gerlai R (2015) Angelfish (Pterophyllum scalare) discriminate between small quantities: a role of memory. J Comp Psychol 129:78–83

    Article  PubMed  Google Scholar 

  • Gómez-Laplaza LM, Morgan E (2003) The influence of social rank in the angelfish, Pterophyllum scalare, on locomotor and feeding activities in a novel environment. Lab Anim 37:108–120

    Article  PubMed  Google Scholar 

  • Gómez-Laplaza LM, Morgan E (2005) Time-place learning in the cichlid angelfish, Pterophyllum scalare. Behav Process 70:177–181

    Article  Google Scholar 

  • Ilieş I, Sîrbulescu RF, Zupanc GK (2014) Indeterminate body growth and lack of gonadal decline in the brown ghost knifefish (Apteronotus leptorhynchus), an organism exhibiting negligible brain senescence. Can J Zool 92:947–953

    Article  Google Scholar 

  • Kacperczyk A, Jędrzejowska I, Daczewska M (2011) Differentiation and growth of myotomal muscles in a non-model tropical fish Pterophyllum scalare (Teleostei: Cichlidae). Anat Histol Embryol 40:411–418

    Article  CAS  PubMed  Google Scholar 

  • Kasiri M, Farahi A, Sudagar M (2012) Growth and reproductive performance by different feed types in fresh water angelfish (Pterophyllum scalare Schultze, 1823). Vet Res Forum 3:175–179

    PubMed  PubMed Central  Google Scholar 

  • Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493–495

    Article  CAS  PubMed  Google Scholar 

  • Le Cren ED, (1951) The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol 20 (2):201

  • Lema SC, Hodges MJ, Marchetti MP, Nevitt GA (2005) Proliferation zones in the salmon telencephalon and evidence for environmental influence on proliferation rate. Comp Biochem Physiol A Mol Integr Physiol 141:327–335

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Chen Z, Gao J, Wang L, Chen X, Zhao Y (2016) The complete mitochondrial genome of the altum angelfish Pterophyllum altum (Pellegrin, 1903). Mitochondrial DNA A DNA Mapp Seq Anal 27:3705–3706

    CAS  PubMed  Google Scholar 

  • Martins CI, Galhardo L, Noble C, Damsgård B, Spedicato MT, Zupa W, Beauchaud M, Kulczykowska E, Massabuau JC, Carter T, Planellas SR, Kristiansen T (2012) Behavioural indicators of welfare in farmed fish. Fish Physiology and Biochemistry 38(1):17–41

  • Meek J (1983) Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum. Brain Res 287:247–297

    Article  CAS  PubMed  Google Scholar 

  • Mirescu C, Gould E (2006) Stress and adult neurogenesis. Hippocampus 16:233–238

    Article  CAS  PubMed  Google Scholar 

  • Mora F, Segovia G, del Arco A (2007) Aging, plasticity and environmental enrichment: structural changes and neurotransmitter dynamics in several areas of the brain. Brain Res Rev 55:78–88

    Article  CAS  PubMed  Google Scholar 

  • Ortega-Salas AA, Cortés GI, Reyes-Bustamante H (2009) Fecundity, growth, and survival of the angelfish Pterophyllum scalare (Perciformes: Cichlidae) under laboratory conditions. Rev Biol Trop 57:741–747

    PubMed  Google Scholar 

  • Perera TD, Park S, Nemirovskaya Y (2008) Cognitive role of neurogenesis in depression and antidepressant treatment. Neuroscientist 14:326–338

    Article  PubMed  Google Scholar 

  • Perry AN, Grober MS (2003) A model for social control of sex change: interactions of behavior, neuropeptides, glucocorticoids, and sex steroids. Horm Behav 43:31–38

    Article  CAS  PubMed  Google Scholar 

  • Pham TM, Winblad B, Granholm AC, Mohammed AH (2002) Environmental influences on brain neurotrophins in rats. Pharmacol Biochem Behav 73:167–175

    Article  CAS  PubMed  Google Scholar 

  • Radmilovich M, Fernández A, Trujillo-Cenóz O (2003) Environment temperature affects cell proliferation in the spinal cord and brain of juvenile turtles. J Exp Biol 206:3085–3093

    Article  PubMed  Google Scholar 

  • Rieder CL, Cole RW (2002) Cold-shock and the mammalian cell cycle. Cell Cycle 1:169–175

    Article  CAS  PubMed  Google Scholar 

  • Rosenzweig MR, Bennett EL, Hebert M, & Morimoto H (1978) Social grouping cannot account for cerebral effects of enriched environments. Brain Res 153:563–576

  • Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N, Caleo M (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24:1850–1856

    Article  PubMed  Google Scholar 

  • Sakamoto H, Yoshida M, Uematsu K (1999) Naturally occurring somatic motoneuron death in a teleost angelfish, Pterophyllum scalare. Neurosci Lett 267:145–148

    Article  CAS  PubMed  Google Scholar 

  • Salvanes AG, Moberg O, Ebbesson LO, Nilsen TO, Jensen KH, Braithwaite VA (2013) Environmental enrichment promotes neural plasticity and cognitive ability in fish. Proc Biol Sci 280:20131331

    Article  PubMed  PubMed Central  Google Scholar 

  • Schloesser RJ, Lehmann M, Martinowich K, Manji HK, Herkenham M (2010) Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol Psychiatry 15:1152–1163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider CH, Gross MC, Terencio ML, de Tavares É, Martins C, Feldberg E (2015) Chromosomal distribution of microsatellite repeats in Amazon cichlids genome (Pisces, Cichlidae). Comp Cytogenet 9:595–605

    Article  PubMed  PubMed Central  Google Scholar 

  • Slomianka L, West MJ (2005) Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 136:757–767

    Article  CAS  PubMed  Google Scholar 

  • Traniello IM, Sîrbulescu RF, Ilieş I, Zupanc GK (2014) Age-related changes in stem cell dynamics, neurogenesis, apoptosis, and gliosis in the adult brain: a novel teleost fish model of negligible senescence. Dev Neurobiol 74:514–530

    Article  PubMed  Google Scholar 

  • Van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci 96:13427–13431

    Article  PubMed  PubMed Central  Google Scholar 

  • von Krogh K, Sorensen C, Nilsson GE, Overli O (2010) Forebrain cell proliferation, behavior, and physiology of zebrafish, Danio rerio, kept in enriched or barren environments. Physiol Behav 101:32–39

    Article  CAS  Google Scholar 

  • West MJ (2002) Design-based stereological methods for counting neurons. Prog Brain Res 135:43–51

    Article  PubMed  Google Scholar 

  • West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482–497

    Article  CAS  PubMed  Google Scholar 

  • Zhu SW, Yee BK, Nyffeler M, Winblad B, Feldon J, Mohammed AH (2006) Influence of differential housing on emotional behaviour and neurotrophin levels in mice. Behav Brain Res 169:10–20

    Article  CAS  PubMed  Google Scholar 

  • Zikopoulos B, Kentouri M, Dermon CR (2000) Proliferation zones in the adult brain of a sequential hermaphrodite teleost species (Sparus aurata). Brain Behav Evol 56:310–322

    Article  CAS  PubMed  Google Scholar 

  • Zupanc G (2006) Neurogenesis and neuronal regeneration in the adult fish brain. J Comparat Physiol A 192:649–670

    Article  CAS  Google Scholar 

  • Zupanc GK (2008) Adult neurogenesis and neuronal regeneration in the brain of teleost fish. J Physiol-Paris 102:357–373

    Article  PubMed  Google Scholar 

  • Zupanc GK, Horschke I (1995) Proliferation zones in the brain of adult gymnotiform fish: a quantitative mapping study. J Comp Neurol 353:213–233

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are in debt with EMBRAPA (Aracaju-SE), National Council of Scientific and Technological Development (CNPq) for financial support to R.Y. Fujimoto (CNPq 304533/2019-0), and to UFPA/HUJBB, LNI (UFPA/Belém) and LBN (IFPA/Bragança). All procedures in this study were previously approved by the ethics committee of UFPA/CEUA, n°1875240419.

Availability of data and material

The data that supports the findings of this study are available from the corresponding author upon reasonable request.

Funding

There is no financial support to this study.

Author information

Authors and Affiliations

  1. Universidade Federal do Pará, Hospital Universitário João de Barros Barreto, Laboratório de Neurodegeneração e Infecção, Rua dos Mundurucus, n°4487, Guamá, Belém, Pará, CEP: 66.073-005, Brazil

    Daniel Guerreiro Diniz, Nara Gysely de Morais Magalhães, Gabrielly Lisboa da Silva Soares & Cristovam Wanderley Picanço Diniz

  2. Instituto Federal de Educação Ciência e Tecnologia do Pará, Campus Bragança, Laboratório de Biologia Molecular e Ambiental, Rua da Escola Agrícola, S/N, Vila Sinhá, CEP: 68.600-000, Bragança, Pará, Brasil

    Lucas Silva de Siqueira, Ediely Pereira Henrique, Patrick Douglas Correa Pereira, Cristovam Guerreiro Diniz & Cintya Castro de Abreu

  3. Universidade Tiradentes, Avenida Murilo Dantas, nº300, Farolândia, CEP: 49.032-490, Aracaju, Sergipe, Brasil

    Peterson Emmanuel Guimarães Paixão & Juliana Oliveira Meneses

  4. Universidade Federal do Pará, Rua Augusto Corrêa, nº01, Guamá, CEP: 66.075-110, Belém, Pará, Brasil

    Márcia Valéria Silva do Couto & Natalino da Costa Sousa

  5. Embrapa Tabuleiros Costeiros, Avenida Beira mar, nº3250, CEP: 49.025-040, Aracaju, Sergipe, Brasil

    Rodrigo Yudi Fujimoto

  6. Universidade Federal de Alagoas, Campus Arapiraca, Pólo Penedo, CEP: 57.200-000, Penedo, Alagoas, Brasil

    Fernanda dos Santos Cunha

  7. Instituto Evandro Chagas, Laboratório de Microscopia Eletrônica, Avenida Almirante Barroso, nº492, Marco, CEP: 66.093-020, Belém, Pará, Brasil

    Daniel Guerreiro Diniz

Authors
  1. Daniel Guerreiro Diniz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lucas Silva de Siqueira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ediely Pereira Henrique
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrick Douglas Correa Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cristovam Guerreiro Diniz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cintya Castro de Abreu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nara Gysely de Morais Magalhães
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gabrielly Lisboa da Silva Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Peterson Emmanuel Guimarães Paixão
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Juliana Oliveira Meneses
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Márcia Valéria Silva do Couto
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Natalino da Costa Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Fernanda dos Santos Cunha
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Cristovam Wanderley Picanço Diniz
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Rodrigo Yudi Fujimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors listed executed substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data for the work; and drafting the work or revising it critically for important intellectual content; and final approval of the version to be published; agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Cristovam Wanderley Picanço Diniz.

Ethics declarations

Conflict of interest

The authors have no any conflict of interest to declare.

Ethics approval

Approved by the ethics committee of UFPA/CEUA, n°1,875,240,419.

Consent to participate

Not applicable.

Consent for publication

The authors agree with this publication.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Diniz, D.G., de Siqueira, L.S., Henrique, E.P. et al. Environmental enrichment increases the number of telencephalic but not tectal cells of angelfish (Pterophyllum scalare): an exploratory investigation using optical fractionator. Environ Biol Fish 103, 847–857 (2020). https://doi.org/10.1007/s10641-020-00986-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-020-00986-5

Keywords

Search

Navigation