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Wariness of reef fish to passive diver presence with varying dive gear type across a coral reef depth gradient

Published online by Cambridge University Press:  19 July 2017

Dominic A. Andradi-Brown Open the ORCID record for Dominic A. Andradi-Brown [Opens in a new window] ,
Erika Gress ,
Jack H. Laverick Open the ORCID record for Jack H. Laverick [Opens in a new window] ,
Margaux A. A. Monfared ,
Alex David Rogers  and
Dan A. Exton
Dominic A. Andradi-Brown*
Affiliation:
Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK Operation Wallacea, Wallace House, Old Bolingbroke, Spilsby PE23 4EX, UK
Erika Gress
Affiliation:
Operation Wallacea, Wallace House, Old Bolingbroke, Spilsby PE23 4EX, UK
Jack H. Laverick
Affiliation:
Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK Operation Wallacea, Wallace House, Old Bolingbroke, Spilsby PE23 4EX, UK
Margaux A. A. Monfared
Affiliation:
Operation Wallacea, Wallace House, Old Bolingbroke, Spilsby PE23 4EX, UK School of Biological Sciences, University of Portsmouth, University House, Winston Churchill Avenue, Portsmouth PO1 2UP, UK
Alex David Rogers
Affiliation:
Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK
Dan A. Exton
Affiliation:
Operation Wallacea, Wallace House, Old Bolingbroke, Spilsby PE23 4EX, UK
*
Correspondence should be addressed to: D. A. Andradi-Brown, Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK email: dominic.andradi-brown@zoo.ox.ac.uk
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Abstract

Both active and passive human interactions with reef fish communities are increasingly recognized to cause fish behavioural changes. However, few studies have considered how these behavioural adaptations impact standard reef survey techniques, particularly across natural gradients of interest to ecologists and reef managers. Here we measure fish abundance, biomass and minimum approach distance using stereo-video surveys to compare the effects of bubble-producing open-circuit scuba vs near-silent closed-circuit rebreathers. Surveys extended across a shallow to upper-mesophotic gradient on the fringing reefs of Utila, Honduras, to explore how the effects of diver gear choice vary with depth. For most fish families we recorded similar abundances and biomass with the two diving techniques, suggesting that open-circuit transects are generally appropriate for surveying western Atlantic reefs similar to Utila with regular tourist diving but no spearfishing. Despite no overall significant difference in fish abundance or biomass, we identified several fish families (Labridae, Pomacentridae, Scaridae) that allowed closed-circuit rebreather divers to approach more closely than open-circuit divers. In addition, smaller fish generally allowed divers to approach more closely than larger fish, and in most cases divers could approach fish more closely on mesophotic than shallow reefs. Despite these significant differences in approach distances, their magnitude suggest they are unlikely to affect reef fish detectability during normal fish surveys for most families. Our findings highlight the importance of considering variation in fish behavioural adaptations along natural gradients such as depth, which otherwise has the potential to cause biases when surveying by traditional monitoring programmes.

Keywords

Fish warinessmesophotic coral ecosystemclosed-circuit rebreatherflight initiation distancepassive diver presenceDOVstereo-video systemminimum approach distanceHonduras

Information

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 98 , Issue 7 , November 2018 , pp. 1733 - 1743
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

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Footnotes

†

These authors have contributed equally and are joint last authors.

References

REFERENCES

Anderson, M.J., Gorley, R.N. and Clarke, K.R. (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: PRIMER-E.Google Scholar
Andradi-Brown, D., Laverick, J., Bejarano, I., Bridge, T., Colin, P.L., Eyal, G., Jones, R., Kahng, S., Reed, J., Smith, T., Spalding, H., Weil, E. and Wood, E. (2016a) Threats to mesophotic coral ecosystems and management options. In Baker, E.K., Puglise, K.A. and Harris, P.T. (eds) Mesophotic coral ecosystems – a lifeboat for coral reefs? Nairobi and Arendal: The United Nations Environment Programme and GRID-Arendal, pp. 67–82.Google Scholar
Andradi-Brown, D.A., Gress, E., Wright, G., Exton, D.A. and Rogers, A.D. (2016b) Reef fish community biomass and trophic structure changes across shallow to upper-mesophotic reefs in the Mesoamerican Barrier Reef, Caribbean. PLoS ONE 11, e0156641.Google Scholar
Andradi-Brown, D.A., Grey, R., Hendrix, A., Hitchner, D., Hunt, C.L., Gress, E., Madej, K., Parry, R.L., Régnier-McKellar, C., Jones, O.P., Arteaga, M., Izaguirre, A.P., Rogers, A.D. and Exton, D.A. (2017) Depth-dependent effects of culling – do mesophotic lionfish populations undermine current management? Royal Society Open Science 4, 170027.Google Scholar
Andradi-Brown, D.A., Macaya-Solis, C., Exton, D.A., Gress, E., Wright, G. and Rogers, A.D. (2016c) Assessing Caribbean shallow and mesophotic reef fish communities using baited-remote underwater video (BRUV) and diver-operated video (DOV) survey techniques. PLoS ONE 11, e0168235.Google Scholar
Bejarano, I., Appeldoorn, R.S. and Nemeth, M. (2014) Fishes associated with mesophotic coral ecosystems in La Parguera, Puerto Rico. Coral Reefs 33, 313–328.Google Scholar
Box, S.J. and Canty, S.W.J. (2011) The long and short term economic drivers of overexploitation in Honduran coral reef fisheries due to their dependence on export markets. Proceedings of the 63rd Gulf and Caribbean Fisheries Institute November 1–5, 2010 San Juan, Puerto Rico 63, 43–51.Google Scholar
Brokovich, E., Ben-Ari, T., Kark, S., Kiflawi, M., Dishon, G., Iluz, D. and Shashar, N. (2010) Functional changes of the visual system of the damselfish Dascyllus marginatus along its bathymetric range. Physiology and Behavior 101, 413–421.Google Scholar
Brown, B.L. and Hendrix, S.B. (2014) Partial correlation coefficients. Encyclopedia of statistics in behavioural science. Chichester: Wiley.Google Scholar
Chapman, C.J., Johnstone, A.D.F., Dunn, J.R. and Creasey, D.J. (1974) Reactions of fish to sound generated by divers’ open-circuit underwater breathing apparatus. Marine Biology 27, 357–366.Google Scholar
Clark, C.W. (1994) Antipredator behavior and the asset-protection principle. Behavioral Ecology 5, 159–170.Google Scholar
Clarke, K.R., Somerfield, P.J. and Chapman, M.G. (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. Journal of Experimental Marine Biology and Ecology 330, 55–80.Google Scholar
Cole, R.G. (1994) Abundance, size structure, and diver-oriented behaviour of three large benthic carnivorous fishes in a marine reserve in Northeastern New Zealand. Biological Conservation 70, 93–99.Google Scholar
Cole, R.G., Syms, C., Davey, N.K., Gust, N., Notman, P., Stewart, R., Radford, C.A., Carbines, G., Carr, M.H. and Jevs, A.G. (2007) Does breathing apparatus affect fish counts and observations? A comparison at three New Zealand fished and protected areas. Marine Biology 150, 1379–1395.Google Scholar
Cronk, L. and Steadman, S. (2002) Tourists as a common-pool resource: a study of dive shops on Utila, Honduras. In Cohen, J. and Dannhaeuser, N. (eds) Economic development: an anthropological approach. Walnut Creek, CA: Altamira Press, pp. 51–68.Google Scholar
Dickens, L.C., Goatley, C.H.R., Tanner, J.K. and Bellwood, D.R. (2011) Quantifying relative diver effects in underwater visual censuses. PLoS ONE 6, e18965.Google Scholar
Doiron, S. and Weissenberger, S. (2014) Sustainable dive tourism: social and environmental impacts – the case of Roatan, Honduras. Tourism Management Perspectives 10, 19–26.Google Scholar
English, S., Wilkinson, C. and Baker, V. (1997) Survey manual for tropical marine resources. Townsville: Australian Institute of Marine Sciences.Google Scholar
Feary, D.A., Cinner, J.E., Graham, N.J. and Januchowski-Hartley, F.A. (2011) Effects of customary marine closures on fish behavior, spear-fishing success, and underwater visual surveys. Conservation Biology 25, 341–349.Google Scholar
Fernald, R.D. (1985) Growth of the teleost eye: novel solutions to complex constraints. Environmental Biology of Fishes 13, 113–123.Google Scholar
Gobert, B., Berthou, P., Lopez, E., Lespagnol, P., Turcios, M.D.O., Macabiau, C. and Portillo, P. (2005) Early stages of snapper–grouper exploitation in the Caribbean (Bay Islands, Honduras). Fisheries Research 73, 159–169.Google Scholar
Gotanda, K.M., Turgeon, K. and Kramer, D.L. (2009) Body size and reserve protection affect flight initiation distance in parrotfishes. Behavioral Ecology and Sociobiology 63, 1563–1572.Google Scholar
Gray, A.E., Williams, I.D., Stamoulis, K.A., Boland, R.C., Lino, K.C., Hauk, B.B., Leonard, J.C., Rooney, J.R., Asher, J.M., Lopes, K.H. and Kosaki, R.K. (2016) Comparison of reef fish survey data gathered by open and closed circuit scuba divers reveals differences in areas with higher fishing pressure. PLoS ONE 11, e0167724.Google Scholar
Grol, M.G.G., Rypel, A.L. and Nagelkerken, I. (2014) Growth potential and predation risk drive ontogenetic shifts among nursery habitats in a coral reef fish. Marine Ecology Progress Series 502, 229–244.Google Scholar
Harborne, A.R., Afzal, D.C. and Andrews, M.J. (2001) Honduras: Caribbean coast. Marine Pollution Bulletin 42, 1221–1235.Google Scholar
Harvey, E., Fletcher, D. and Shortis, M. (2001) A comparison of the precision and accuracy of estimates of reef-fish lengths determined visually by divers with estimates produced by a stereo-video system. Fishery Bulletin 99, 63–71.Google Scholar
Harvey, E., Fletcher, D., Shortis, M. and Kendrick, G.A. (2004) A comparison of underwater visual distance estimates made by scuba divers and a stereo-video system: implications for underwater visual census of reef fish abundance. Marine and Freshwater Research 55, 573–580.Google Scholar
Januchowski-Hartley, F.A., Cinner, J.E. and Graham, N.A.J. (2014) Fishery benefits from behavioural modification of fishes in periodically harvested fisheries closures. Aquatic Conservation: Marine and Freshwater Ecosystems 24, 777–790.Google Scholar
Januchowski-Hartley, F.A., Graham, N.A.J., Cinner, J.E. and Russ, G.R. (2015) Local fishing influences coral reef fish behavior inside protected areas of the Indo-Pacific. Biological Conservation 182, 8–12.Google Scholar
Januchowski-Hartley, F.A., Graham, N.A.J., Feary, D.A., Morove, T. and Cinner, J.E. (2011) Fear of fishers: human predation explains behavioral changes in coral reef fishes. PLoS ONE 6, e22761.Google Scholar
Kramer, P.McField, M., Filip, L., Drysdale, I., Flores, M., Giró, A. and Pott, R. (2015) 2015 report card for the Mesoamerican Reef, http://www.healthyreefs.org: Healthy Reefs Initiative.Google Scholar
Kulbicki, M. (1998) How the acquired behaviour of commercial reef fishes may influence the results obtained from visual censuses. Journal of Experimental Marine Biology and Ecology 222, 11–30.Google Scholar
Lindfield, S.J., Harvey, E.S., Halford, A.R. and McIlwain, J.L. (2016) Mesophotic depths as refuge areas for fishery-targeted species on coral reefs. Coral Reefs 35, 125–137.Google Scholar
Lindfield, S.J., Harvey, E.S., McIlwain, J.L. and Halford, A.R. (2014a) Silent fish surveys: bubble-free diving highlights inaccuracies associated with SCUBA-based surveys in heavily fished areas. Methods in Ecology and Evolution 5, 1061–1069.Google Scholar
Lindfield, S.J., McIlwain, J.L. and Harvey, E.S. (2014b) Depth refuge and the impacts of scuba spearfishing on coral reef fishes. PLoS ONE 9, e92628.Google Scholar
Mallet, D. and Pelletier, D. (2014) Underwater video techniques for observing coastal marine biodiversity: a review of sixty years of publications (1952–2012). Fisheries Research 154, 44–62.Google Scholar
Mapstone, B.D. and Ayling, A.M. (1998) An investigation of optimum methods and unit sizes for the visual estimation of abundances of some coral reef organisms. Townsville: Great Barrier Reef Marine Park Authority, Research Publication Series 47.Google Scholar
Oksanen, J., Guillaume Blanchet, F., Kindt, R., Legendre, P., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solums, P., Stevens, M.H.H., Wagner, H. (2015) vegan: community ecology package. R package version 2.2-1. http://CRAN.R-project.org/package=veganGoogle Scholar
Pinheiro, H.T., Goodbody-Gringley, G., Jessup, M.E., Shepherd, B., Chequer, A.D. and Rocha, L.A. (2016) Upper and lower mesophotic coral reef fish communities evaluated by underwater visual censuses in two Caribbean locations. Coral Reefs 35, 139–151.Google Scholar
Radford, C.A., Jeffs, A.G., Tindle, C.T., Cole, R.G. and Montgomery, J.C. (2005) Bubbled waters: the noise generated by underwater breathing apparatus. Marine and Freshwater Behaviour and Physiology 38, 259–267.Google Scholar
R Core Team (2013) R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. http://www.R-project.org/Google Scholar
Sale, P.F. (1997) Visual census of fishes: how well do we see what is there? Proceedings of the 8th International Coral Reef Symposium 2, 1435–1439.Google Scholar
Sciberras, M., Jenkins, S.R., Kaiser, M.J., Hawkins, S.J. and Pullin, A.S. (2013) Evaluating the biological effectiveness of fully and partially protected marine areas. Environmental Evidence 2, 4.Google Scholar
Sieber, A. and Pyle, R. (2010) A review of the use of closed-circuit rebreathers for scientific diving. Underwater Technology 29, 73–78.Google Scholar
Sogard, S.M. (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bulletin of Marine Science 60, 1129–1157.Google Scholar
Thompson, A.A. and Mapstone, B.D. (1997) Observer effects and training in underwater visual surveys of reef fishes. Marine Ecology Progress Series 154, 53–63.Google Scholar
Titus, B.M., Daly, M. and Exton, D.A. (2015) Do reef fish habituate to diver presence? Evidence from two reef sites with contrasting historical levels of scuba intensity in the Bay Islands, Honduras. PLoS ONE 10, e0119645.Google Scholar
Watson, D.L. and Harvey, E.S. (2007) Behaviour of temperate and sub-tropical reef fishes towards a stationary scuba diver. Marine and Freshwater Behaviour and Physiology 40, 85–103.Google Scholar