In situ effects of human disturbances on coral reef-fish assemblage structure: temporary and persisting changes are reflected as a result of intensive tourism
Tiago Albuquerque A B C , Miguel Loiola B C D , José de Anchieta C. C. Nunes C D E , José Amorim Reis-Filho C D E , Cláudio L. S. Sampaio F and Antoine O. H. C. Leduc D G
+ Author Affiliations
- Author Affiliations
A Universidade Federal da Bahia, Instituto de Geociências, Programa de Pós Graduação em Geologia Costeira e Sedimentar, Salvador, Bahia, 40170-115, Brasil.
B Universidade Federal da Bahia, Instituto de Geociências, Laboratório de Estudos em Recifes de Corais e Mudanças Globais (RECOR), Salvador, Bahia, 40170-115, Brasil.
C Instituto de Educação e Ciências de Utilidades Sócio-Ambientais (ECUS), Salvador, Bahia, 41940-250, Brasil.
D Universidade Federal da Bahia, Instituto de Biologia, Programa de Pós Graduação em Ecologia e Biomonitoramento, Salvador, Bahia, 40170-115, Brasil.
E Universidade Federal da Bahia, Instituto de Biologia, Laboratório de Ecologia Bentônica (LEB), Salvador, Bahia, 40170-115, Brasil.
F Universidade Federal de Alagoas, Departamento de Engenharia de Pesca, Penedo, Alagoas, 57200-000, Brasil.
G Corresponding author. Email: mirabiles@hotmail.com
Marine and Freshwater Research 66(1) 23-32 https://doi.org/10.1071/MF13185
Submitted: 12 July 2013 Accepted: 21 March 2014 Published: 29 October 2014
Abstract
Non-lethal human disturbances are often drivers of change in animal population and community structure. To gauge their severity, short-term behaviour (e.g. avoidance and habituation) has been argued to be a sensitive measure. However, many of these behavioural changes may occur only if disturbance-free habitat is readily accessible. In coral-reef fish, we tested whether human disturbances from intensive (i.e. loud music, swimming, snorkelling, splashing and fish feeding by numerous visitors) tourist visitations resulted in assemblage structure shifts led by short-term behaviour. We monitored fish assemblage before, during and after tourist visitations to monitor changes associated with behaviour. Additionally, we monitored two adjacent reefs not visited by tourists because of difficult approach by boat. We posited that if short-term benefits of relocating to disturbance-free habitat outweigh the costs of tolerating disturbances, fish assemblage structure should shift along with tourist visitation levels. By contrast, if sensitive species are unable or unwilling to relocate, we predicted greater levels of assemblage heterogeneity between the visited and control reefs. Our results showed that in situ human visitations led to significant shifts in assemblage structure, resulting from short-term behavioural changes. Additionally, we showed significant between-reefs differences, whereby control reefs were characterised by higher species richness, larger fish sizes and variations in relative trophic guild prevalence. Our results suggest that short-term relocations to adjacent disturbance-free reefs may not mitigate the effects of human disturbances.
Additional keywords: Bahia, behaviour, Boipeba island, Brazil, conservation, snorkelling.
References
Alencar, C. M. M. (2011). Tensões entre pesca, turismo e exploração de gás reconfigurando ruralidade na ilha de Boipeba. Desenvolvimento e Meio Ambiente 23, 148–166.Amo, L., López, P., and Martin, J. (2006). Nature-based tourism as a form of predation risk affects body condition and health state of Podarcis muralis lizards. Biological Conservation 131, 402–409.
| Nature-based tourism as a form of predation risk affects body condition and health state of Podarcis muralis lizards.Crossref | GoogleScholarGoogle Scholar |
Azevedo, G. (2009). Atividade alimentar e uso do habitat por diferentes fases ontogenéticas de Halichoeres poeyi (Pisces: Labridae) em Arraial do Cabo, Rio de Janeiro. M.Sc. Thesis, Universidade Federal de Fluminense, Niterói, Brasil.
Bannerot, S. P., and Bohnsack, J. A. (1986). A stationary visual census technique for quantitatively assessing community structure of coral reef fishes. NOAA Technical Report NMFS 41, 1–15.
Beale, C. M., and Monaghan, P. (2004a). Behavioural responses to human disturbance: a matter of choice? Animal Behaviour 68, 1065–1069.
| Behavioural responses to human disturbance: a matter of choice?Crossref | GoogleScholarGoogle Scholar |
Beale, C. M., and Monaghan, P. (2004b). Human disturbance: people as predation‐free predators? Journal of Applied Ecology 41, 335–343.
| Human disturbance: people as predation‐free predators?Crossref | GoogleScholarGoogle Scholar |
Bellan, G. L., and Bellan-Santini, D. R. (2001). A review of littoral tourism, sport and leisure activities: consequences on marine flora and fauna. Aquatic Conservation: Marine and Freshwater Ecosystems 11, 325–333.
| A review of littoral tourism, sport and leisure activities: consequences on marine flora and fauna.Crossref | GoogleScholarGoogle Scholar |
Bray, J. R., and Curtis, J. T. (1957). An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27, 325–349.
| An ordination of the upland forest communities of southern Wisconsin.Crossref | GoogleScholarGoogle Scholar |
Carney, K. M., and Sydeman, W. J. (1999). A review of human disturbance effects on nesting colonial waterbirds. Waterbirds 22, 68–79.
| A review of human disturbance effects on nesting colonial waterbirds.Crossref | GoogleScholarGoogle Scholar |
Carr, M. R. (1999). ‘Plymouth Routines in Multivariate Analysis. Primer User Manual.’ (Natural Environment Research Council: Swindon, UK.)
Castro, C. B., and Pires, D. O. (2001). Brazilian coral reefs: what we already know and what is still missing. Bulletin of Marine Science 69, 357–371.
Chapman, M. R., and Kramer, D. L. (2000). Movements of fishes within and among fringing coral reefs in Barbados. Environmental Biology of Fishes 57, 11–24.
| Movements of fishes within and among fringing coral reefs in Barbados.Crossref | GoogleScholarGoogle Scholar |
Christ, C., Hillel, O., Matus, S., and Sweeting, J. (2003). ‘Tourism and Biodiversity. Mapping Tourism’s Global Footprint.’ (Conservation International: Washington, DC.)
Clarke, K. R., and Warwick, R. M. (1994). ‘Change in Marine Communities: an Approach to Statistical Analysis and Integration.’ (Natural Environment Research Council: Swindon, UK.)
Davenport, J., and Davenport, J. L. (2006). The impact of tourism and personal leisure transport on coastal environments: a review. Estuarine, Coastal and Shelf Science 67, 280–292.
| The impact of tourism and personal leisure transport on coastal environments: a review.Crossref | GoogleScholarGoogle Scholar |
Day, R. W., and Quinn, G. P. (1989). Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59, 433–463.
| Comparisons of treatments after an analysis of variance in ecology.Crossref | GoogleScholarGoogle Scholar |
Di Franco, A., Milazzo, M., Baiata, P., Tomasello, A., and Chemello, R. (2009). Scuba diver behaviour and its effects on the biota of a Mediterranean marine protected area. Environmental Conservation 36, 32–40.
| Scuba diver behaviour and its effects on the biota of a Mediterranean marine protected area.Crossref | GoogleScholarGoogle Scholar |
Dudley, N. (2008). ‘Guidelines for Applying Protected Area Management Categories.’ (International Union for Conservation of Nature: Gland, Switzerland.)
Ferreira, C., Floeter, S. R., Gasparini, J. L., Ferreira, B. P., and Joyeux, J. C. (2004). Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison. Journal of Biogeography 31, 1093–1106.
| Trophic structure patterns of Brazilian reef fishes: a latitudinal comparison.Crossref | GoogleScholarGoogle Scholar |
Floeter, S. R., Krohling, W., Gasparini, J. L., Ferreira, C. E. L., and Zalmon, I. R. (2007). Reef fish community structure on coastal islands of the southeastern Brazil: the influence of exposure and benthic cover. Environmental Biology of Fishes 78, 147–160.
| Reef fish community structure on coastal islands of the southeastern Brazil: the influence of exposure and benthic cover.Crossref | GoogleScholarGoogle Scholar |
Francini-Filho, R. B., Coni, E. O. C., Meirelles, P. M., Amado-Filho, G. M., Thompson, F. L., Pereira-Filho, G. H., Bastos, A. C., Abrantes, D. P., Ferreira, C. M., Gibran, F. Z., Güth, A. Z., Sumida, P. Y. G., Oliveira, N. L., Kaufman, L., Minte-Vera, C. V., and Moura, R. L. (2013). Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers. PLoS ONE 8, e54260.
| Dynamics of coral reef benthic assemblages of the Abrolhos Bank, eastern Brazil: inferences on natural and anthropogenic drivers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXit1Ciu7Y%3D&md5=c4b328e53f04b5f4502fb72936f2b738CAS | 23365655PubMed |
Frid, A., and Dill, L. M. (2002). Human-caused disturbance stimuli as a form of predation risk. Conservation Ecology 6, 1–16.
Froese, R., and Pauly, D. (2000). ‘FishBase 2000: Concept, Design and Data Sources.’ ICLARM, Los Baños, Philippines. Available at www.fishbase.org [accessed 24 April 2013]
Gauch, H. G. (1982). ‘Multivariate Analysis in Community Ecology.’ (Cambridge University Press: Cambridge, UK.)
Gill, J. A., Norris, K., and Sutherland, W. J. (2001). Why behavioural responses may not reflect the population consequences of human disturbance. Biological Conservation 97, 265–268.
| Why behavioural responses may not reflect the population consequences of human disturbance.Crossref | GoogleScholarGoogle Scholar |
Gössling, S. (1999). Ecotourism: a means to safeguard biodiversity and ecosystem functions? Ecological Economics 29, 303–320.
| Ecotourism: a means to safeguard biodiversity and ecosystem functions?Crossref | GoogleScholarGoogle Scholar |
Hair, J. F., Anderson, R. E., Tatham, R. L., and Black, W. C. (1998). ‘Multivariate Data Analysis.’ 5th edn. (Prentice Hall: Englewood Cliffs, NJ.)
Heil, L., Fernández-Juricic, E., Renison, D., Cingolani, A. M., and Blumstein, D. T. (2007). Avian responses to tourism in the biogeographically isolated high Córdoba Mountains, Argentina. Biodiversity and Conservation 16, 1009–1026.
| Avian responses to tourism in the biogeographically isolated high Córdoba Mountains, Argentina.Crossref | GoogleScholarGoogle Scholar |
Honey, M. (1999). ‘Ecotourism and Sustainable Development: Who Owns Paradise?’ (Island Press: Washington, DC.)
Humann, P., and DeLoach, N. (2002). ‘Reef Fish Identification: Florida, Caribbean and Bahamas.’ 3rd edn. (New World Publications: Jacksonville, FL.)
Ilarri, M. D. I., de Souza, A. T., Medeiros, P. R., Grempel, R. G., and de Rosa, I. M. L. (2008). Effects of tourist visitation and supplementary feeding on fish assemblage composition on a tropical reef in the southwestern Atlantic. Neotropical Ichthyology 6, 651–656.
| Effects of tourist visitation and supplementary feeding on fish assemblage composition on a tropical reef in the southwestern Atlantic.Crossref | GoogleScholarGoogle Scholar |
Johns, B. G. (1996). Responses of chimpanzees to habituation and tourism in the Kibale Forest, Uganda. Biological Conservation 78, 257–262.
| Responses of chimpanzees to habituation and tourism in the Kibale Forest, Uganda.Crossref | GoogleScholarGoogle Scholar |
Kramer, D. L., and Chapman, M. R. (1999). Implications of fish home range size and relocation for marine reserve function. Environmental Biology of Fishes 55, 65–79.
| Implications of fish home range size and relocation for marine reserve function.Crossref | GoogleScholarGoogle Scholar |
Laborel, J. L. (1969). Madreporaires et hydrocoralliaires recifaux des cotes bresiliennes. Systematique, ecologie, repartition verticale et geographie. Annales de l’Institut Oceanographique de Paris 47, 171–229.
Leão, Z., and Dominguez, J. (2000). Tropical coast of Brazil. Marine Pollution Bulletin 41, 112–122.
| Tropical coast of Brazil.Crossref | GoogleScholarGoogle Scholar |
Lessa, R., and Nóbrega, M. F. (2000). Guia de identificação de peixes marinhos da Região Nordeste. DIMAR, In Programa REVIZEE, Score-NE. Recife, PE, Brazil.
Madsen, J. (1995). Impacts of disturbance on migratory waterfowl. The Ibis 137, S67–S74.
| Impacts of disturbance on migratory waterfowl.Crossref | GoogleScholarGoogle Scholar |
Mayhew, P. W. (1988). The daily energy intake of European wigeon in winter. Ornis Scandinavica 19, 217–223.
| The daily energy intake of European wigeon in winter.Crossref | GoogleScholarGoogle Scholar |
Milazzo, M., Badalamenti, F., Vega Fernandez, T., and Chemello, R. (2005). Effects of fish feeding by snorkellers on the density and size distribution of fishes in a Mediterranean marine protected area. Marine Biology 146, 1213–1222.
| Effects of fish feeding by snorkellers on the density and size distribution of fishes in a Mediterranean marine protected area.Crossref | GoogleScholarGoogle Scholar |
Milazzo, M., Anastasi, I., and Willis, T. J. (2006). Recreational fish feeding affects coastal fish behavior and increases frequency of predation on damselfish Chromis chromis nests. Marine Ecology Progress Series 310, 165–172.
| Recreational fish feeding affects coastal fish behavior and increases frequency of predation on damselfish Chromis chromis nests.Crossref | GoogleScholarGoogle Scholar |
Miller, S. G., Knight, R. L., and Miller, C. K. (1998). Influence of recreational trails on breeding bird communities. Ecological Applications 8, 162–169.
| Influence of recreational trails on breeding bird communities.Crossref | GoogleScholarGoogle Scholar |
Moura, R. L., and Francini-Filho, R. B. (2005). ‘A Rapid Marine Biodiversity Assessment of the Abrolhos Bank, Bahia, Brazil.’ (Conservation International, Center for Applied Biodiversity Science: Washington DC.)
Nunes, de A. C. C. J., Sampaio, C. L. S., and Barros, F. (2013). How wave exposure, group size and habitat complexity influence foraging and population densities in fishes of the genus Halichoeres (Perciformes: Labridae) on tropical rocky shores. Marine Biology 160, 2383–2394.
| How wave exposure, group size and habitat complexity influence foraging and population densities in fishes of the genus Halichoeres (Perciformes: Labridae) on tropical rocky shores.Crossref | GoogleScholarGoogle Scholar |
Oliveira, E. S. (2007). Impactos socioambientais e econômicos do turismo e as suas repercussões no desenvolvimento local: o caso do Município de Itacaré-Bahia. Interações. Revista Internacional de Desenvolvimento Local 8, 193–202.
Parsons, D. M., and Eggleston, D. B. (2006). Human and natural predators combine to alter behavior and reduce survival of Caribbean spiny lobster. Journal of Experimental Marine Biology and Ecology 334, 196–205.
| Human and natural predators combine to alter behavior and reduce survival of Caribbean spiny lobster.Crossref | GoogleScholarGoogle Scholar |
Rodriguez-Prieto, I., and Fernandez-Juricic, E. (2005). Effects of direct human disturbance on the endemic Iberian frog at individual and population levels. Biological Conservation 123, 1–9.
| Effects of direct human disturbance on the endemic Iberian frog at individual and population levels.Crossref | GoogleScholarGoogle Scholar |
Rodriguez-Prieto, I., Fernandez-Juricic, E., Martin, J., and Regis, Y. (2009). Antipredator behavior in blackbirds: habituation complements risk allocation. Behavioral Ecology 20, 371–377.
| Antipredator behavior in blackbirds: habituation complements risk allocation.Crossref | GoogleScholarGoogle Scholar |
Segal, B., and Castro, C. B. (2001). A proposed method for coral cover assessment: a case study in Abrolhos, Brazil. Bulletin of Marine Science 69, 487–496.
Silva, I. R., Nascimento, H. M., and Rebouca, R. C. (2009). Avaliação da sensibilidade ambiental das praias localizadas no arquipélago Tinharé/Boipeba, litoral sul do Estado da Bahia. Geociências 28, 193–201.
Skagen, S. K., Knight, R. L., and Orians, G. H. (1991). Human disturbance of an avian scavenging guild. Ecological Applications 1, 215–225.
| Human disturbance of an avian scavenging guild.Crossref | GoogleScholarGoogle Scholar |
Sokal, R. R., and Rohlf, F. J. (1995). ‘The Principles and Practice of Statistics in Biological Research.’ 3rd edn. (W. H. Freeman and Co.: New York.)
Sutherland, W. J., and Crockford, N. J. (1993). Factors affecting the feeding distribution of red-breasted geese Branta ruficollis wintering in Romania. Biological Conservation 63, 61–65.
| Factors affecting the feeding distribution of red-breasted geese Branta ruficollis wintering in Romania.Crossref | GoogleScholarGoogle Scholar |
Tuite, C. H., Hanson, P. R., and Owen, M. (1984). Some ecological factors affecting winter wildfowl distribution on inland waters in England and Wales, and the influence of water-based recreation. Journal of Applied Ecology 21, 41–61.
| Some ecological factors affecting winter wildfowl distribution on inland waters in England and Wales, and the influence of water-based recreation.Crossref | GoogleScholarGoogle Scholar |
Underwood, A. J. (1994). On beyond BACI: sampling designs that might reliably detect environmental disturbances. Ecological Applications 4, 3–15.
| On beyond BACI: sampling designs that might reliably detect environmental disturbances.Crossref | GoogleScholarGoogle Scholar |
Verhulst, S., Oosterbeek, K., and Ens, B. J. (2001). Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers. Biological Conservation 101, 375–380.
| Experimental evidence for effects of human disturbance on foraging and parental care in oystercatchers.Crossref | GoogleScholarGoogle Scholar |
Warwick, R. M., and Clarke, K. R. (1991). A comparison of some methods for analysing changes in benthic community structure. Journal of the Marine Biological Association of the United Kingdom 71, 225–244.
| A comparison of some methods for analysing changes in benthic community structure.Crossref | GoogleScholarGoogle Scholar |
Webb, N. V., and Blumstein, D. T. (2005). Variation in human disturbance differentially affects predation risk assessment in western gulls. The Condor 107, 178–181.
| Variation in human disturbance differentially affects predation risk assessment in western gulls.Crossref | GoogleScholarGoogle Scholar |
West, A. D., Goss-Custard, J. D., Stillman, R. A., Caldow, R. W., le V dit Durell, S. E., and McGrorty, S. (2002). Predicting the impacts of disturbance on shorebird mortality using a behaviour-based model. Biological Conservation 106, 319–328.
| Predicting the impacts of disturbance on shorebird mortality using a behaviour-based model.Crossref | GoogleScholarGoogle Scholar |
Zakai, D., and Chadwick-Furman, N. E. (2002). Impacts of intensive recreational diving on reef corals at Eilat, northern Red Sea. Biological Conservation 105, 179–187.
| Impacts of intensive recreational diving on reef corals at Eilat, northern Red Sea.Crossref | GoogleScholarGoogle Scholar |
