Skip to main content
SpringerLink
Log in

Environmental enrichment effects on the reproductive behavior of captive nurse sharks Ginglymostoma cirratum

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

Abstract

Nurse sharks (Ginglymostoma cirratum, Ginglymostomatidae) are one of the most exhibited shark species in aquariums worldwide. However, in these locations, their reproductive success rate is frequently low. Considering that there is probably an olfactory mediation for nurse shark reproduction, and that environmental enrichment has a potentially positive effect on reproduction of captive animals, the present study aimed to evaluate whether the use of olfactory enrichment would stimulate olfactory-driven behaviors and consequently generate effects in the exhibition of reproductive behaviors by the species both in the short and long term. The study was divided into three phases (control, short-term enrichment and long-term enrichment), was conducted at two institutions with distinct husbandry and used aqueous extracts of basil leaves as olfactory enrichment. Eleven individuals were selected through focal sampling for behavioral observations with instantaneous recording, the total of 120 h of observation were divided into active and inactive periods. Results showed that basil-based olfactory enrichment was effective in increasing the occurrence of reproductive behaviors in both female and male nurse sharks. Additionally, the long-term results showed higher effects in males, which strengthen the theory of olfactory mediation of reproductive behavior in the species as individuals became aware of the sensory cues in the environment and performed more olfactory-driven reproductive behaviors. It is important to note that enrichment effects are different between sexes and therefore close monitoring and scheduling are essential to avoid over-stimulation or habituation to the enrichment.

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

Similar content being viewed by others

Notes

  1. Projeto Tamar, personal communication

References

  • AES (2008) The 2008 AES international captive elasmobranch census

  • Ahlbeck Bergendahl I, Salvanes AGV, Braithwaite VA (2016) Determining the effects of duration and recency of exposure to environmental enrichment. Appl Anim Behav Sci 176:163–169. https://doi.org/10.1016/j.applanim.2015.11.002

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  CAS  PubMed  Google Scholar 

  • Amo L (2017) The role of olfaction in mate selection and reproductive behaviour. In: Olfaction in animal behaviour and welfare. CABI, Wallingford, pp 85–101. https://doi.org/10.1079/9781786391599.0085

    Chapter  Google Scholar 

  • Anderson C, Arun AS, Jensen P (2010) Habituation to environmental enrichment in captive sloth bears-effect on stereotypies. Zoo Biol 29:705–714. https://doi.org/10.1002/zoo.20301

    Article  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J stat Softw 67. https://doi.org/10.18637/jss.v067.i01

  • Beach FA (1976) Sexual attractivity, proceptivity, and receptivity in female mammals. Horm Behav 7:105–138. https://doi.org/10.1016/0018-506X(76)90008-8

    Article  CAS  PubMed  Google Scholar 

  • Carlstead K, Shepherdson D (1994) Effects of environmental enrichment on reproduction. Zoo Biol 13:447–458. https://doi.org/10.1002/zoo.1430130507

    Article  Google Scholar 

  • Carrier JC, Murru FL, Walsh MT, Pratt HL (2003) Assessing reproductive potential and gestation in nurse sharks (Ginglymostoma cirratum) using ultrasonography and endoscopy: an example of bridging the gap between field research and captive studies. Zoo Biol 22:179–187. https://doi.org/10.1002/zoo.10088

    Article  Google Scholar 

  • Carrier JC, Pratt HL, Martin LK (1994) Group reproductive behaviors in free-living nurse sharks, Ginglymostoma cirratum. Copeia 1994:646. https://doi.org/10.2307/1447180

    Article  Google Scholar 

  • Castro ALF, Rosa RS (2005) Use of natural marks on population estimates of the nurse shark, Ginglymostoma cirratum, at Atol das Rocas biological reserve, Brazil. Environ Biol Fish 72:213–221. https://doi.org/10.1007/s10641-004-1479-7

    Article  Google Scholar 

  • Ceballos G, Ehrlich PR, Barnosky AD, García A, Pringle RM, Palmer TM (2015) Accelerated modern human–induced species losses: entering the sixth mass extinction. Sci Adv 1:e1400253. https://doi.org/10.1126/sciadv.1400253

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark F, King AJ (2008) A critical review of zoo-based olfactory enrichment. In: Hurst JL, Beynon RJ, Roberts SC, Wyatt TD (eds) Chemical signals in vertebrates 11. Springer New York, New York, NY, pp 391–398. https://doi.org/10.1007/978-0-387-73945-8_37

    Chapter  Google Scholar 

  • Colbachini H, Pizzutto CS, Jorge-Neto PN, Gutierrez RC, Gadig OBF (2020) Body movement as an indicator of proceptive behavior in nurse sharks (Ginglymostoma cirratum). Environ Biol Fish 103:1257–1263. https://doi.org/10.1007/s10641-020-01018-y

    Article  Google Scholar 

  • Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Volume 2. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes), FAO species catalogue for fishery purposes. FAO, Rome

  • Conway WG (2011) Buying time for wild animals with zoos. Zoo Biol 30:1–8. https://doi.org/10.1002/zoo.20352

    Article  PubMed  Google Scholar 

  • Crawley MJ (2013) The R book, 2nd ed. John Wiley & Sons, Ltd, Chichester, UK https://doi.org/10.1002/9781118448908

  • Crofton EJ, Zhang Y, Green TA (2015) Inoculation stress hypothesis of environmental enrichment. Neurosci Biobehav Rev 49:19–31. https://doi.org/10.1016/j.neubiorev.2014.11.017

    Article  PubMed  Google Scholar 

  • Crooks N, Waring CP (2013) A study into the sexual dimorphisms of the Ampullae of Lorenzini in the lesser-spotted catshark, Scyliorhinus canicula (Linnaeus, 1758). Environ Biol Fish 96:585–590. https://doi.org/10.1007/s10641-012-0048-8

    Article  Google Scholar 

  • da Silva R, Pearce-Kelly P, Zimmerman B, Knott M, Foden W, Conde DA (2019) Assessing the conservation potential of fish and corals in aquariums globally. J Nat Conserv 48:1–11. https://doi.org/10.1016/j.jnc.2018.12.001

    Article  Google Scholar 

  • de Azevedo CS, Cipreste CF, Young RJ (2007) Environmental enrichment: A GAP analysis. Appl Anim Behav Sci 102:329–343. https://doi.org/10.1016/j.applanim.2006.05.034

    Article  Google Scholar 

  • Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM, Harrison LR, Carlson JK, Davidson LN, Fordham SV, Francis MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE, Compagno LJ, Ebert DA, Gibson C, Heupel MR, Livingstone SR, Sanciangco JC, Stevens JD, Valenti S, White WT (2014) Extinction risk and conservation of the world’s sharks and rays. Elife 3. https://doi.org/10.7554/eLife.00590

  • Gardiner JM, Hueter RE, Maruska KP, Sisneros JA, Casper BM, Mann DA, Demski LS (2012) Sensory physiology and behavior of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 365–418. https://doi.org/10.1201/b11867-20

    Chapter  Google Scholar 

  • Garla RC, Garcia J, Veras LB, Lopes NP (2009) Fernando de Noronha as an insular nursery area for lemon sharks, Negaprion brevirostris, and nurse sharks, Ginglymostoma cirratum, in the equatorial western Atlantic Ocean. Mar Biodivers Rec 2:e109. https://doi.org/10.1017/S1755267209000670

    Article  Google Scholar 

  • Greenway E, Jones KS, Cooke GM (2016) Environmental enrichment in captive juvenile thornback rays, Raja clavata (Linnaeus 1758). Appl Anim Behav Sci 182:86–93. https://doi.org/10.1016/j.applanim.2016.06.008

    Article  Google Scholar 

  • Henningsen AD, Smale M, Garner R, Kinnunen N (2004a) Reproduction, embryonic development, and reproductive physiology of elasmobranchs, in: Smith M, Warmolts D, Thoney D, Hueter R (Eds.) The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and Their Relatives. Ohio Biological Survey, Inc. 2004, Columbus, Ohio, pp 227–236

  • Henningsen AD, Smale MJ, Gordon I, Garner R, Marin-Osorno R, Kinnunen N (2004b) Captive breeding and sexual conflict in elasmobranchs, in: Smith M, Warmolts D, Thoney D, Hueter R (Eds.) The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and Their Relatives. Ohio Biological Survey, Inc. 2004, Columbus, Ohio, pp. 237–248

  • ICMBio (2018) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume VI - Peixes. ICMBio/MMA, Brasília

    Google Scholar 

  • Janse M, Zimmerman B, Geerlings L, Brown C (2017) Sustainable species management of the elasmobranch populations within European aquariums: a conservation challenge. J Zoo Aquarium Res 5:172–181. https://doi.org/10.19227/jzar.v5i4.313

    Article  Google Scholar 

  • Janssen JD, Kidd A, Ferreira A, Snowden S (2017) Training and conditioning of elasmobranchs in aquaria, in: Smith M, Warmolts D, Thoney D, Hueter R, Murray M, Ezcurra J (Eds.) The elasmobranch husbandry manual II: recent advances in the Care of Sharks, Rays and Their Relatives. Ohio Biological Survey, Inc., Columbus, pp. 209–221

  • Johnson RH, Nelson DR (1978) Copulation and possible olfaction-mediated pair formation in two species of Carcharhinid sharks. Copeia 1978:539. https://doi.org/10.2307/1443626

    Article  Google Scholar 

  • Khaki A, Azad FF, Nouri M, Khaki AA (2011) Effects of basil, ocimum basilicum on spermatogenesis in rats. J Med Plant Res 5:4601–4604. https://doi.org/10.5897/JMPR.9000511

    Article  Google Scholar 

  • Khaki A, Khaki AA, Ezzatzadeh A, A-Ashteani H (2013) Effect of Ocimum basilicum on ovary tissue histopathology after exposure to electromagnetic fields (EMF) in rats. African J Pharm Pharmacol 7:1703–1706. https://doi.org/10.5897/AJPP12.1073

    Article  Google Scholar 

  • Klimley AP (1980) Observations of courtship and copulation in the nurse shark, Ginglymostoma cirratum. Copeia 1980:878. https://doi.org/10.2307/1444471

    Article  Google Scholar 

  • Koop JH (2005) Reproduction of captive Raja spp. in the Dolfinarium Harderwijk. J Mar Biol Assoc United Kingdom 85:1201–1202. https://doi.org/10.1017/S0025315405012312

    Article  Google Scholar 

  • Kuczaj S, Lacinak T, Fad O, Trone M, Solangi M, Ramos J (2002) Keeping environmental enrichment enriching. Int J Comp Psychol 15:127–137

    Google Scholar 

  • Kuenen M (2000) A log of captive births by an Atlantic nurse shark, “Sarah”. Drum Croak 31:22–24

    Google Scholar 

  • Lee KA, Huveneers C, Peddemors V, Boomer A, Harcourt RG (2015) Born to be free? Assessing the viability of releasing captive-bred wobbegongs to restock depleted populations. Front Mar Sci 2:1–14. https://doi.org/10.3389/fmars.2015.00018

    Article  Google Scholar 

  • Lehner PN (1998) Handbook of ethological methods, 2nd edn. Cambridge University Press, New York

    Google Scholar 

  • Luer CA, Gilbert PW (1985) Mating behavior, egg deposition, incubation period, and hatching in the clearnose skate, Raja eglanteria. Environ Biol Fish 13:161–171. https://doi.org/10.1007/BF00000926

    Article  Google Scholar 

  • Marin-Osorno R, Ezcurra JM, O’Sullivan JB (2017) Husbandry of the Tiger shark, Galeocerdo cuvier, at the Acuario de Veracruz, México, in: Smith M, Warmolts D, Thoney D, Hueter R, Murray M, Ezcurra J (Eds.) The elasmobranch husbandry manual II: recent advances in the Care of Sharks, Rays and Their Relatives. Ohio Biological Survey, Inc., Columbus, pp. 23–32

  • McFarlane GA, Wydoski RS, Prince ED (1990) External tags and marks. Am Fish Soc Symp 7:9–29

    Google Scholar 

  • Meagher RK, Ahloy Dallaire J, Campbell DLM, Ross M, Møller SH, Hansen SW, Díez-León M, Palme R, Mason GJ (2014) Benefits of a ball and chain: simple environmental enrichments improve welfare and reproductive success in farmed american mink (Neovison vison). PLoS One 9:e110589. https://doi.org/10.1371/journal.pone.0110589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreira N, Brown JL, Moraes W, Swanson WF, Monteiro-Filho ELA (2007) Effect of housing and environmental enrichment on adrenocortical activity, behavior and reproductive cyclicity in the female tigrina (Leopardus tigrinus) and margay (Leopardus wiedii). Zoo Biol 26:441–460. https://doi.org/10.1002/zoo.20139

    Article  PubMed  Google Scholar 

  • Näslund J, Johnsson JI (2016) Environmental enrichment for fish in captive environments: effects of physical structures and substrates. Fish Fish 17:1–30. https://doi.org/10.1111/faf.12088

    Article  Google Scholar 

  • Newberry RC (1995) Environmental enrichment: increasing the biological relevance of captive environments. Appl Anim Behav Sci 44:229–243

    Article  Google Scholar 

  • Nielsen BL, Jezierski T, Bolhuis JE, Amo L, Rosell F, Oostindjer M, Christensen JW, McKeegan D, Wells DL, Hepper P (2015) Olfaction: an overlooked sensory modality in applied ethology and animal welfare Front Vet Sci 2. https://doi.org/10.3389/fvets.2015.00069

  • Penning M, Reid GM, Koldewey H, Dick G, Andrews B, Arai K, Garratt P, Gendron S, Lange J, Tanner K, Tonge S, Van den Sande P, Warmolts D, Gibson C (2009). Turning the tide: A global aquarium strategy for conservation and sustainability. World Association of Zoos and Aquariums (WAZA), Bern

  • Pine W, Hightower J, Coggins L, Lauretta M, Pollock K (2012) Design and analysis of tagging studies. In: Zale AV, Parrish DL, Sutton TM (eds) Fisheries Techniques. American Fisheries Society, Bethesda, pp 521–572

    Google Scholar 

  • Pratt HL Jr, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 60:157–188. https://doi.org/10.1023/A:1007656126281

    Article  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. the R Foundation for Statistical Computing., Viena

  • Rosa RS, Castro ALF, Furtado M, Monzini J, Grubbs RD (2006) Ginglymostoma cirratum(Western Atlantic subpopulation). The IUCN red list of threatened species 2006: e.T60224A12327471 [WWW document]. https://doi.org/10.2305/IUCN.UK.2006.RLTS.T60224A12327471.en

  • Samuelson MM, Lauderdale LK, Pulis K, Solangi M, Hoffland T, Lyn H (2017) Olfactory enrichment in California Sea lions (Zalophus californianus): an effective tool for captive welfare? J Appl Anim Welf Sci 20:75–85. https://doi.org/10.1080/10888705.2016.1246362

    Article  CAS  PubMed  Google Scholar 

  • Shepherdson D (1994) The role of environmental enrichment in the captive breeding and reintroduction of endangered species. In: Olney PJS, Mace GM, Feistner ATC (eds) Creative conservation: interactive management of wild and captive animals. Chapman & Hall, London, pp 167–177

    Chapter  Google Scholar 

  • Tarou LR, Bashaw MJ (2007) Maximizing the effectiveness of environmental enrichment: suggestions from the experimental analysis of behavior. Appl Anim Behav Sci 102:189–204. https://doi.org/10.1016/j.applanim.2006.05.026

    Article  Google Scholar 

  • Wafer LN, Jensen VB, Whitney JC, Gomez TH, Flores R, Goodwin BS (2016) Effects of environmental enrichment on the fertility and fecundity of zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 55:291–294

    PubMed  PubMed Central  Google Scholar 

  • Waghray S (1985) Olfactory organ and its sexual dimorphism in the electric ray, Narcine timlei (day). Indian J Fish 32:148–151

    Google Scholar 

  • Wells DL (2009) Sensory stimulation as environmental enrichment for captive animals: a review. Appl Anim Behav Sci 118:1–11. https://doi.org/10.1016/j.applanim.2009.01.002

    Article  Google Scholar 

  • Wells DL, Egli JM (2004) The influence of olfactory enrichment on the behaviour of captive black-footed cats, Felis nigripes. Appl Anim Behav Sci 85:107–119. https://doi.org/10.1016/j.applanim.2003.08.013

    Article  Google Scholar 

  • Whitney NM, Lear KO, Gaskins LC, Gleiss AC (2016) The effects of temperature and swimming speed on the metabolic rate of the nurse shark (Ginglymostoma cirratum, Bonaterre). J Exp Mar Bio Ecol 477:40–46. https://doi.org/10.1016/j.jembe.2015.12.009

    Article  Google Scholar 

  • Yano K, Sato F, Takahashi T (1999) Observations of mating behavior of the manta ray,Manta birostris, at the ogasawara islands. Japan Ichthyol Res 46:289–296. https://doi.org/10.1007/BF02678515

    Article  Google Scholar 

  • Young RJ (2003) Environmental enrichment for captive animals, 1st edition. Ed. Blackwell science ltd, Universities Federation for Animal Welfare (UFAW), Oxford, UK. https://doi.org/10.1002/9780470751046

  • Zar JH (2010) Biostatistical analysis, 5th Editio. ed. Pearson Prentice Hall, Upper Saddle River

  • Brasil (2018) Acordo de Cooperação Técnica n° 3202386. Processo n° 02070.003869/2018-45 from June 05, 2018. Diário Oficial da União, Brasília, DF, ed 106, sec 3, pp. 108

Download references

Acknowledgments

The authors thank the São Paulo Aquarium and the TAMAR Project staff for maintaining the sharks used in the present study and allowing observations out of working hours. They also thank all the contributors to the work, especially M. Miranda, B. Ogata, C. S. de Azevedo, C. Colbachini and W. Vilegas.

Availability of data and material

Not applicable.

Code availability

Not applicable.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.

Author information

Authors and Affiliations

  1. Elasmobranch Research Lab, Coastal Campus of São Vicente, São Paulo State University, Praça Infante Dom Henrique, s/n, São Vicente, SP, 11330-900, Brazil

    Helen Colbachini & Otto Bismarck Fazzano Gadig

  2. Aquário de São Paulo, R. Huet Bacelar, 407, São Paulo, SP, 04275-000, Brazil

    Helen Colbachini

  3. Department of Animal Reproduction, Faculty of Veterinary Medicine and Husbandry, University of Sao Paulo, Av. Prof. Orlando Marques de Paiva, 87, São Paulo, SP, 05508-010, Brazil

    Cristiane Schilbach Pizzutto

  4. Laboratory of Bioprospection of Natural Products – Biosciences Institute, Coastal Campus of São Vicente, São Paulo State University, Praça Infante Dom Henrique, s/n, São Vicente, SP, 11330-900, Brazil

    Leonardo Mendes de Souza Mesquita

Authors
  1. Helen Colbachini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristiane Schilbach Pizzutto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leonardo Mendes de Souza Mesquita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Otto Bismarck Fazzano Gadig
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

H Colbachini, LM de Souza Mesquita and OBF Gadig performed the experiments. H Colbachini, CS Pizzutto, LM de Souza Mesquita and OBF Gadig analyzed and interpreted the data. H Colbachini and CS Pizzutto wrote the manuscript. H Colbachini, CS Pizzutto, LM de Souza Mesquita and OBF Gadig critically revised the manuscript. All authors approved the manuscript for publication.

Corresponding author

Correspondence to Helen Colbachini.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

The use and care of experimental animals obeyed the Brazilian laws, guidelines and policies on animal welfare, according to IBAMA (IN 07/2015) and by the institutions technical staff. As no invasive method was applied, no further ethical approval was required.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

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

Colbachini, H., Pizzutto, C.S., de Souza Mesquita, L.M. et al. Environmental enrichment effects on the reproductive behavior of captive nurse sharks Ginglymostoma cirratum. Environ Biol Fish 104, 471–488 (2021). https://doi.org/10.1007/s10641-021-01087-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-021-01087-7

Keywords

Search

Navigation