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Trampling on coral reefs: tourism effects on harpacticoid copepods

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Abstract

Human trampling is a common type of disturbance associated with outdoor recreational activities in coastal ecosystems. In this study, the effect of trampling on the meiofaunal harpacticoid copepod assemblage inhabiting turfs on a coral reef was investigated. In Porto de Galinhas, northeastern Brazil, reef formations near the beach are one of the main touristic destinations in the country. To assess trampling impact, two areas were compared: a protected area and an area subject to intensive tourism. Densities of total Harpacticoida and of the most abundant harpacticoid species showed strong reductions in the trampled area. An analysis of covariance revealed that the loss of phytal habitat was not the main source of density reductions, showing that trampling affected the animals directly. In addition, multivariate analysis demonstrated differences in the structure of harpacticoid assemblages between areas. Of the 43 species identified, 12 were detected by the Indicator Species Analyses as being indicators of the protected or trampled areas. Moreover, species richness was reduced in the area open to tourism. At least 25 harpacticoids are new species for science, of these, 20 were more abundant or occurred only in the protected area, while five were more abundant or occurred only in the trampled area; thus, our results highlight the possibility of local extinction of still-unknown species as one of the potential consequences of trampling on coral reefs.

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References

  • Alcantara R, Ferreira BP, Travassos P (2004) A pesca artesanal e o turismo em Porto de Galinhas, Pernambuco. Bol Téc Cient CEPENE 12:195–207

    Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Armstrong E, Rogerson A, Leftley JW (2000) The abundance of heterotrophic protists associated with intertidal seaweeds. Estuar Coast Shelf Sci 50:415–424

    Article  Google Scholar 

  • Arroyo NL, Aarnio K, Ólafsson E (2007) Interactions between two closely related phytal harpacticoid copepods, asymmetric positive and negative effects. J Exp Mar Biol Ecol 341:219–227

    Article  Google Scholar 

  • Asencio G, Clasing E, Herrera C, Stead R, Navarro J (1993) Copépodos Harpacticoídeos de las comunidades de Venus antiqua y Mulinia sp en la planicie mareal de Yaldad, Quéllon, Chiloé, Chile. Rev Chil Hist Nat 66:455–465

    Google Scholar 

  • Azovsky AI, Saburova MA, Chertoprud ES, Polikarpov IG (2005) Selective feeding of littoral harpacticoids on diatom algae: hungry gourmands? Mar Biol 148:327–337

    Article  Google Scholar 

  • Brown PJ, Taylor RB (1999) Effects of trampling by humans on animals inhabiting coralline algal turf in the rocky intertidal. J Exp Mar Biol Ecol 235:45–53

    Article  Google Scholar 

  • Carman KR, Thistle D (1985) Microbial food partitioning by three species of benthic copepods. Mar Biol 88:143–148

    Article  Google Scholar 

  • Casu D, Ceccherelli G, Castelli A (2006a) Immediate effects of experimental human trampling on mid-upper intertidal benthic invertebrates at the Asinara Island MPA (NW Mediterranean). Hydrobiologia 555:271–279

    Article  Google Scholar 

  • Casu D, Ceccherelli G, Curini-Galletti M, Castelli A (2006b) Human exclusion from rocky shores in a Mediterranean marine protected area (MPA): An opportunity to investigate the effects of trampling. Mar Environ Res 62:15–32

    Article  PubMed  CAS  Google Scholar 

  • Contessa L, Bird FL (2004) The impact of bait-pumping on populations of the ghost shrimp Trypaea australiensis Dana (Decapoda: Callianassidae) and the sediment environment. J Exp Mar Biol Ecol 304:75–97

    Article  Google Scholar 

  • Costa OS Jr, Nimmo M, Attrill ML (2008) Coastal nutrification in Brazil: A review of the role of nutrient excess on coral reef demise. J South Am Earth Sci 25:257–270

    Article  Google Scholar 

  • Coull BC (1988) Ecology of the marine meiofauna. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, pp 18–38

    Google Scholar 

  • Coull BC (1999) Role of meiofauna in estuarine soft-bottom habitats. Aust J Ecol 24:327–343

    Article  Google Scholar 

  • Coull BC, Creed EL, Eskin RA, Montagna PA, Palmer MA, Wells JBJ (1983) Phytal meiofauna from the rocky intertidal at Murrels Inlet, South Carolina. Trans Am Microsc Soc 102:380–389

    Article  Google Scholar 

  • Danovaro R, Scopa M, Gambi C, Franschetti S (2007) Trophic importance of subtidal metazoan meiofauna: evidence from in situ exclusion experiments on soft and rocky substrates. Mar Biol 152:339–350

    Article  Google Scholar 

  • De Troch M, Steinarsdóttir MB, Chepurnov V, Ólafsson E (2005) Grazing on diatoms by harpacticoid copepods: species-specific density-dependent uptake and microbial gardening. Aquat Microb Ecol 39:135–144

    Article  Google Scholar 

  • Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Ferreira MN, Rosso S (2009) Effects of human trampling on a rocky shore fauna on the São Paulo coast, southeastern Brazil. Braz J Biol 69:993–999

    Article  PubMed  CAS  Google Scholar 

  • Gerber RP (1981) Species composition and abundance of lagoon zooplankton at Eniwetak Atoll, Marshall islands. Atoll Res Bull 247:1–22

    Google Scholar 

  • Gheskiere T, Vincx M, Weslawski JM, Scapini F, Degraer S (2005) Meiofauna as descriptor of tourism-induced changes at sandy beaches. Mar Environ Res 60:245–265

    Article  PubMed  CAS  Google Scholar 

  • Gibbons MJ, Griffiths CL (1986) A comparison of macrofaunal and meiofaunal distribution and standing stock across a rocky shore, with an estimate of their productivities. Mar Biol 93:181–188

    Article  Google Scholar 

  • Giere O (2009) Meiobenthology: The microscopic motile fauna of aquatic sediments, 2nd edn. Springer-Verlag, Berlin

    Google Scholar 

  • Hall MO, Bell SS (1993) Meiofauna on the seagrass Thalassia testudinum: population characteristics of harpacticoid copepods and associations with algal epiphytes. Mar Biol 116:137–146

    Article  Google Scholar 

  • Hardiman N, Burgin S (2010) Recreational impacts on the fauna of Australian coastal marine ecosystems. J Environ Manage 91:2096–2108

    Article  PubMed  Google Scholar 

  • Hicks GRF (1971) Some littoral harpacticoid copepods, including five new species, from Wellington, New Zealand. NZ J Mar Freshw Res 5:86–119

    Article  Google Scholar 

  • Hicks GRF (1977) Species composition and zoogeography of marine phytal harpacticoid copepods from Cook Strait, and their contribution to total phytal meiofauna. NZ J Mar Freshw Res 11:441–469

    Google Scholar 

  • Hicks GRF (1985) Meiofauna associated with rock shore algae. In: Moore PG, Seed R (eds) The ecology of rocky coasts. Columbia University Press, New York, pp 36–56

    Google Scholar 

  • Hicks GRF (1986) Distribution and behaviour of meiofaunal copepods inside and outside seagrass beds. Mar Ecol Prog Ser 31:159–170

    Article  Google Scholar 

  • Hsu CB, Chen CP, Hsieh HL (2009) Effects of sediment compaction on macroinfauna in a protected coastal wetland in Taiwan. Mar Ecol Prog Ser 375:73–83

    Article  Google Scholar 

  • Huys R, Gee JM, More CG, Hamond R (1996) Marine and brackish water harpacticoid copepods. Part 1. Keys and notes for identification of the species. In: Barnes RSK, Crothers JH (eds) Synopses of the British Fauna (New Series), vol 51. Field Studies Council, Shrewsbury, p 352

    Google Scholar 

  • Johnson GEL, Attrill MJ, Sheehan EV, Somerfield PJ (2007) Recovery of meiofauna communities following mudflat disturbance by trampling associated with crab-tiling. Mar Environ Res 64:409–416

    Article  PubMed  CAS  Google Scholar 

  • Kubosova K, Brabec K, Jarkovsky J, Syrovatka V (2010) Selection of indicative taxa for river habitats: a case study on benthic macroinvertebrates using indicator species analysis and the random forest methods. Hydrobiologia 651:101–114

    Article  Google Scholar 

  • Lang K (1948) Monographie der Harpacticiden: I: 1–896; II: 897–1682. Håkan Ohlsson Booksellers, Lund; Nordiska Bökhandeln, Stockholm

  • Lang K (1965) Copepoda Harpacticoidea from the Californian Pacific coast. Kungliga Svenska Vetenskapsakademiens Handlingar, Fjärde Serien 10(2):1–560, pls. 1–6

    Google Scholar 

  • Laycock RA (1974) The detrital food chain based on seaweeds. I. Bacteria associated with the surface of Laminaria fronds. Mar Biol 25:223–231

    Article  Google Scholar 

  • Leão ZMAN, Dominguez JML (2000) Tropical coast of Brazil. Mar Pollut Bull 41:112–122

    Article  Google Scholar 

  • Magurran AE (2004) Measuring biological diversity. Blackwell Science, Oxford

    Google Scholar 

  • Maida M, Ferreira BP (1997) Coral reefs of Brazil: an overview. Proc 8th Int Coral Reef Symp 1:263–274

    Google Scholar 

  • Matias-Peralta H, Yusoff FM, Shariff M, Arshad A (2005) Effects of some environmental parameters on the reproduction and development of a tropical marine harpacticoid copepod Nitocra affinis f. californica Lang. Mar Pollut Bull 51:722–728

    Article  PubMed  CAS  Google Scholar 

  • McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance based redundancy analysis. Ecology 82:290–297

    Article  Google Scholar 

  • Milazzo M, Badalamenti F, Riggio S, Chemello R (2004) Patterns of algal recovery and small-scale effects of canopy removal as a result of human trampling on a Mediterranean rocky shallow assemblage. Biol Conserv 117:191–202

    Article  Google Scholar 

  • Mouillot D, Culioli J-M, Chi TD (2002) Indicator species analysis as a test of non-random distribution of species in the context of marine protected areas. Environ Conserv 29:385–390

    Article  Google Scholar 

  • Netto SA, Valgas I (2010) The response of nematode assemblages to intensive mussel farming in coastal sediments (Southern Brazil). Environ Monit Assess 162:81–93

    Article  PubMed  Google Scholar 

  • Noodt W (1964) Copepoda Harpacticoidea aus dem Litoral des Roten Meeres. Kieler Meeresforsch 20:128–154

    Google Scholar 

  • Ohtsuka S, Iwasaki N (1998) Redescription of two diosaccid harpacticoid copepods from the Northern Mariana Islands. Nat Hist Res 5:17–29

    Google Scholar 

  • Pinn EH, Rodgers M (2005) The influence of visitors on intertidal biodiversity. J Mar Biol Ass U.K. 85:263–268

    Article  Google Scholar 

  • Punti T, Rieradevall M, Prat N (2009) Environmental factors, spatial variation, and specific requirements of Chironomidae in Mediterranean reference streams. J N Am Benthol Soc 28:247–265

    Article  Google Scholar 

  • Rogerson A (1991) On the abundance of marine naked amoebae on the surface of five species of macroalgae. FEMS Microbiol Lett 85:301–312

    Article  Google Scholar 

  • Rossi F, Forster RM, Montserrat F, Ponti M, Terlizzi A, Ysebaert T, Middelburg JJ (2007) Human trampling as short-term disturbance on intertidal mudflats: effects on macrofauna biodiversity and population dynamics of bivalves. Mar Biol 151:2077–2090

    Article  Google Scholar 

  • Santos PJP, Castel J, Souza-Santos LP (1999) Development time of harpacticoid copepods: some empirical models and implications. J Mar Biol Ass U.K. 79:1123–1124

    Article  Google Scholar 

  • Santos PJP, Souza-Santos LP, Castel J (2003) Population dynamics of Nannopus palustris (Copepoda, Harpacticoida) in the oligo-mesohaline area of the Gironde estuary (France). Cah Biol Mar 44:329–338

    Google Scholar 

  • Sarmento VC, Barreto AFS, Santos PJP (2011) Meiofauna response to human trampling on coral reefs. Scient Mar 75:559–570

    Article  Google Scholar 

  • Schiel DR, Taylor DI (1999) Effects of trampling on a rocky intertidal algal assemblage in southern New Zealand. J Exp Mar Biol Ecol 235:213–235

    Article  Google Scholar 

  • Schratzberger M, Lampadariou N, Somerfield PJ, Vandepitte L, Vanden Berghe E (2009) The impact of seabed disturbance on nematode communities: linking field and laboratory observations. Mar Biol 156:709–724

    Article  Google Scholar 

  • Sheehan EV, Coleman RA, Thompson RC, Attrill MJ (2010) Crab-tiling reduces the diversity of estuarine infauna. Mar Ecol Prog Ser 411:137–148

    Article  Google Scholar 

  • Smith JR, Murray SN (2005) The effects of experimental bait collection and trampling on a Mytilus californianus mussel bed in southern California. Mar Biol 147:699–706

    Article  Google Scholar 

  • Smith JR, Fong P, Ambrose RF (2008) The impacts of human visitation on mussel bed communities along the California coast: are regulatory marine reserves effective in protecting these communities? Environ Manage 41:599–612

    Article  PubMed  Google Scholar 

  • Song SJ, Ryu J, Khim JS, Kim W, Yun SG (2010) Seasonal variability of community structure and breeding activity in marine phytal harpacticoid copepods on Ulva pertusa from Pohang, east coast of Korea. J Sea Res 63:1–10

    Article  Google Scholar 

  • Steinarsdóttir MB, Ingólfsson A, Ólafsson E (2010) Field evidence of differential food utilization of phytal harpacticoids collected from Fucus serratus indicated by δ13C and δ15N stable isotopes. Estuar Coast Shelf Sci 88:160–164

    Article  Google Scholar 

  • Van De Werfhorst LC, Pearse JS (2007) Trampling in the rocky intertidal of central California: a follow-up study. Bull Mar Sci 81:245–254

    Google Scholar 

  • Veiga P, Besteiro C, Rubal M (2010) Meiofauna communities in exposed sandy beaches on the Galician coast (NW Spain), six months after the Prestige oil spill: the role of polycyclic aromatic hydrocarbons (PAHs). Scient Mar 72:385–394

    Google Scholar 

  • Vervoort W (1964) Free-living Copepoda from Ifaluk Atoll in the Caroline Islands. US Natl Mus Bulletin 236, US National Museum, Washington, DC, p 431

  • Wells JBJ (2007) An annotated checklist and keys to the species of Copepoda Harpacticoida (Crustacea). Zootaxa 1568:1–872

    Google Scholar 

  • White AT, Vogt HP, Arin T (2000) Philippine coral reefs under threat: the economic losses caused by reef destruction. Mar Pollut Bull 40:598–605

    Article  CAS  Google Scholar 

  • Wynberg RP, Branch GM (1997) Trampling associated with bait-collection for sandprawns Callianassa kraussi Stebbing: effects on the biota of an intertidal sandflat. Environ Conserv 24:139–148

    Article  Google Scholar 

  • Yeatman HC (1970) Copepods from Chesapeake Bay sponges including Asterocheres jeanyeatmanae n. sp. Trans Amer Microsc Soc 89:27–38

    Article  Google Scholar 

  • Zar JH (1996) Biostatistical Analysis, 3rd edn. Prentice-Hall, New Jersey

    Google Scholar 

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Acknowledgments

V. C. Sarmento acknowledges a MSc scholarship and P. J. P. Santos acknowledges a research fellowship (305609/2004-1) from CNPq. Thanks are due to Dr. Janet W. Reid for English language revision, to Aliny F. S. Barreto for help with field sampling and harpacticoid sorting, and to Dr. Adilma M. Cocentino for algae identifications.

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  1. Department of Zoologia, Centro de Ciências Biológicas, Universidade Federal de Pernambuco, Av. Prof. Morais Rêgo s/n, Recife, Pernambuco, 50670-420, Brazil

    V. C. Sarmento & P. J. P. Santos

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  1. V. C. Sarmento
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Correspondence to V. C. Sarmento.

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Sarmento, V.C., Santos, P.J.P. Trampling on coral reefs: tourism effects on harpacticoid copepods. Coral Reefs 31, 135–146 (2012). https://doi.org/10.1007/s00338-011-0827-2

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