Skip to main content

Advertisement

Log in

Depth-related distribution patterns of subtidal macrobenthos in a well-established marine protected area

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Effective marine resource management requires knowledge of the distribution of critical habitats that support resource populations and the processes that maintain them. Reefs that host diverse macrobenthic communities are important habitats for fish. However, detailed information on macrobenthic communities is rarely available and is usually limited to SCUBA diving depths. To establish depth-related distribution patterns and drivers that structure reef communities, the macrobenthos situated in a warm-temperate marine protected area (MPA; 34°01′24S; 23°54′09E) was sampled between 2009 and 2012. Comparison of shallow (11–25 m) and deep (45–75 m) sites revealed significantly different communities, sharing only 27.9 % of species. LINKTREE analysis revealed a changeover of species along the depth gradient, resulting in four significantly different assemblage clusters, each associated with particular environmental variables. High light intensity supported benthic algae at shallow depths, and as light availability decreased with depth, algal cover diminished and was eventually absent from the deep reef. Upright growth forms and settled particulate matter were positively related to depth and dominated the deep reef. Reduced wave action and currents on the deep reef can explain the increased settling of suspended particles. Under such conditions, clogging of feeding parts of the encrusting species is expected, and upright growth would be favoured. Considering that most MPAs are restricted to shallow coastal habitats and that macrobenthic communities change significantly with depth, it is probable that many unique deep reef habitats are currently afforded no protection.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Barange M, Gili JM (1988) Feeding cycles and prey capture in Eudendrium racemosum (Cavolini, 1785). J Exp Mar Biol Ecol 115:281–293. doi:10.1016/0022-0981(88)90160-8

    Article  Google Scholar 

  • Bell J, Barnes D (2000a) The distribution and prevalence of sponges in relation to environmental gradients within a temperate sea lough: vertical cliff surfaces. Divers Distrib 6:283–303

    Article  Google Scholar 

  • Bell J, Barnes DKA (2000b) The influences of bathymetry and flow regime upon the morphology of sublittoral sponge communities. J Mar Biol Assoc UK 80:707–718

    Article  Google Scholar 

  • Bell J, Smith D (2004) Ecology of sponge assemblages (Porifera) in the Wakatobi region, south-east Sulawesi, Indonesia: richness and abundance. J Mar Biol Assoc UK 84:581–591. doi:10.1017/S0025315404009580h

    Article  Google Scholar 

  • Blondel J (2003) Guilds or functional groups: does it matter? Oikos 2:223–231

    Article  Google Scholar 

  • Bo M, Tazioli S, Spanò N, Bavestrello G (2008) Antipathella subpinnata (Antipatharia, Myriopathidae) in Italian seas. Ital J Zool 75:185–195. doi:10.1080/11250000701882908

    Article  Google Scholar 

  • Bo M, Bavestrello G, Canese S, Giusti M, Salvati E, Angiolillo M, Greco S (2009) Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea. Mar Ecol Prog Ser 397:53–61. doi:10.3354/meps08185

    Article  Google Scholar 

  • Bo M, Bertolino M, Borghini M, Castellano M, Covazzi Harriague A, Di CamilloCG, Gasparini G, Misic C, Povero P, Pusceddu A, Schroeder K, Bavestrello G (2011) Characteristics of the mesophotic megabenthic assemblages of the Vercelli Seamount (north Tyrrhenian Sea). PLoS ONE 6:e16357

    Article  CAS  Google Scholar 

  • Bongaerts P, Ridgway T, Sampayo EM, Hoegh-Guldberg O (2010) Assessing the “deep reef refugia” hypothesis: focus on Caribbean reefs. Coral Reefs 29:309–327. doi:10.1007/s00338-009-0581-x

    Article  Google Scholar 

  • Booth DJ, Murray BR (2008) Coexistence. In: Jorgensen S (ed) Encycl. Elsevier, Ecol, pp 664–668

    Google Scholar 

  • Boyd AJ, Taunton-Clark J, Oberholster GPJ (1992) Spatial features of the near-surface and midwater circulation patterns off western and southern South Africa and their role in the life histories of various commercially fished species. S Afr J Mar Sci 12:189–206

    Article  Google Scholar 

  • Branch G, Griffiths CL, Branch M, Beckley L (2010) Two oceans: a guide to the marine life of southern Africa. Struik, Cape Town

    Google Scholar 

  • Brouwer S (2002) Movement patterns of red steenbras Petrus rupestris tagged and released in the Tsitsikamma National Park, South Africa. S Afr J Mar Sci 24:375–378

    Article  Google Scholar 

  • Brouwer SL, Griffiths MH (2004) Age and growth of Argyrozona argyrozona (Pisces: Sparidae) in a marine protected area: an evaluation of methods based on whole otoliths, sectioned otoliths and mark-recapture. Fish Res 67:1–12. doi:10.1016/j.fishres.2003.08.007

    Article  Google Scholar 

  • Buxton CD (1987) Life history changes of two reef fish species in exploited and unexploited marine environment in South Africa. Dissertation, Rhodes University, Grahamstown

  • Buxton C, Smale M (1984) A preliminary investigation of the marine ichthyofauna in the Tsitsikamma Coastal National Park. Koedoe 27:13–24

    Article  Google Scholar 

  • Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429. doi:10.1038/415426a

    Article  CAS  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  • Clarke K, Warwick R (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth

    Google Scholar 

  • Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69. doi:10.1016/j.jembe.2008.07.009

    Article  Google Scholar 

  • Coma R, Gili J, Zabala M, Riera T (1994) Feeding and prey capture cycles in the aposymbiotic gorgonian Paramuricea clavata. Mar Ecol Prog Ser 115:257–270

    Article  Google Scholar 

  • Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 80(199):1302–1310. doi:10.1126/science.199.4335.1302

    Article  Google Scholar 

  • Cowley P, Brouwer S, Tilney R (2002) The role of the Tsitsikamma National Park in the management of four shore-angling fish along the south-eastern Cape coast of South Africa. S Afr J Mar Sci 24:37–41

    Article  Google Scholar 

  • De Cáceres M, Jansen F (2013) Package ‘indicspecies’. [Documentation files] http://cran.r-project.org/web/packages/indicspecies/index.html

  • De Cáceres M, Legendre P, Wiser SK, Brotons L (2012) Using species combinations in indicator value analyses. Methods Ecol Evol 3:973–982. doi:10.1111/j.2041-210X.2012.00246.x

    Article  Google Scholar 

  • Deter J, Descamp P, Boissery P, Ballesta L, Holon F (2012) A rapid photographic method detects depth gradient in coralligenous assemblages. J Exp Mar Biol Ecol 418–419:75–82. doi:10.1016/j.jembe.2012.03.006

    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. doi:10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2

    Google Scholar 

  • Eckman JE, Duggins DO (1993) Effects of flow speed on growth of benthic suspension feeders. Biol Bull 185:28–41

    Article  Google Scholar 

  • Fitzpatrick BM, Harvey ES, Heyward AJ, et al. (2012) Habitat specialization in tropical continental shelf demersal fish assemblages. PLoS One 7:e39634. doi:10.1371/journal.pone.0039634

  • Garrabou J, Ballesteros E, Zabala M (2002) Structure and dynamics of north-western Mediterranean rocky benthic communities along a depth gradient. Estuar Coast Shelf S 55:493–508. doi:10.1006/ecss.2001.0920

    Article  Google Scholar 

  • Gili J, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food webs. Trends Ecol Evol 13:316–321. doi:10.1016/S0169-5347(98)01365-2

    Article  CAS  Google Scholar 

  • Gori A, Rossi S, Berganzo E, Pretus JL, Dale MRT, Gili J (2011a) Spatial distribution patterns of the gorgonians Eunicella singularis, Paramuricea clavata, and Leptogorgia sarmentosa (Cape of Creus, northwestern Mediterranean Sea). Mar Biol 158:143–158. doi:10.1007/s00227-010-1548-8

    Article  Google Scholar 

  • Gori A, Rossi S, Linares C, Berganzo E, Orejas C, Dale MR, Gili J (2011b) Size and spatial structure in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Mar Biol 158:1721–1732. doi:10.1007/s00227-011-1686-7

    Article  Google Scholar 

  • Gori A, Viladrich N, Gili J, Kotta M, Cucio C, Magni L, Bramanti L, Rossi S (2012) Reproductive cycle and trophic ecology in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Coral Reefs 31:823–837. doi:10.1007/s00338-012-0904-1

    Article  Google Scholar 

  • Griffiths M, Wilke C (2002) Long-term movement patterns of five temperate-reef fishes (Pisces: Sparidae): implications for marine reserves. Mar Freshw Res 53:233–244. doi:10.1071/MF01148

    Article  Google Scholar 

  • Hancke L (2010) Dynamics of the Tsitsikamma current, with implications for larval transport of chokka squid (Loligo reynaudii) on the eastern Agulhas Bank. Dissertation, Cape Peninsula University of Technology

  • Hanekom N, Randall R, Bower D, Riley A, Kruger N (2012) Garden Route National Park: The Tsitsikamma SANParks section—state of knowledge. South African National Parks

  • Hentschel B, Shimeta J (2008) Suspension feeders. In: Jorgensen S (ed) Encyclopedia of Ecology. Elsevier, Amsterdam, pp 3437–3442

    Chapter  Google Scholar 

  • Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo M, Puglise KA, Pyle RL, Zawada DG, Appeldoorn R (2010) Theme section on “Mesophotic Coral Ecosystems: characterization, ecology, and management”. Coral Reefs 29:247–251. doi:10.1007/s00338-010-0614-5

    Article  Google Scholar 

  • Huston M (1985a) Patterns of species diversity on coral reefs. Annu Rev Ecol Syst 16:149–177

    Article  Google Scholar 

  • Huston M (1985b) Patterns of species diversity in relation to depth at Discovery Bay, Jamaica. Bull Mar Sci 37:928–935

    Google Scholar 

  • Jackson J (1977) Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am Nat 111:743–767

    Article  Google Scholar 

  • Jackson J, Winston J (1982) Ecology of cryptic coral reef communities. I. Distribution and abundance of major groups of encrusting organisms. J Exp Mar Biol Ecol 57:135–147. doi:10.1016/0022-0981(82)90188-5

    Article  Google Scholar 

  • Jones G (2008) Marine animals of the Cape Peninsula. Southern Underwater Research Group Press, Cape Town

    Google Scholar 

  • Kaandorp JA (1999) Morphological analysis of growth forms of branching marine sessile organisms along environmental gradients. Mar Biol 134:295–306. doi:10.1007/s002270050547

    Article  Google Scholar 

  • Kahng SE, Garcia-Sais JR, Spalding HL, Brokovich E, Wagner D, Weil E, Hinderstein L, Toonen RJ (2010) Community ecology of mesophotic coral reef ecosystems. Coral Reefs 29:255–275. doi:10.1007/s00338-010-0593-6

    Article  Google Scholar 

  • Kohler KE, Gill SM (2006) Coral point count with excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269. doi:10.1016/j.cageo.2005.11.009

    Article  Google Scholar 

  • Kowalke J (1999) Filtration in antarctic ascidians–striking a balance. J Exp Mar Biol Ecol 242:233–244. doi:10.1016/S0022-0981(99)00108-2

    Article  Google Scholar 

  • Legendre P (2013) Indicator species: computation. In: Levin Simon (ed) Encyclopedia of biodiversity, 2nd edn. Academic Press, Waltham, MA, pp 264–268

    Chapter  Google Scholar 

  • Lesser MP, Slattery M, Leichter JJ (2009) Ecology of mesophotic coral reefs. J Exp Mar Biol Ecol 375:1–8. doi:10.1016/j.jembe.2009.05.009

    Article  Google Scholar 

  • Locker SD, Armstrong RA, Battista TA, Rooney JJ, Sherman C, Zawada DG (2010) Geomorphology of mesophotic coral ecosystems: current perspectives on morphology, distribution, and mapping strategies. Coral Reefs 29:329–345. doi:10.1007/s00338-010-0613-6

    Article  Google Scholar 

  • Loya Y (1972) Community structure and species diversity of hermatypic corals at Eilat, Red Sea. Mar Biol 13:100–123. doi:10.1007/BF00366561

    Article  Google Scholar 

  • Macarthur R, Levins R (1967) The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101:377–385

    Article  Google Scholar 

  • Okamura B, Partridge JC (1999) Suspension feeding adaptations to extreme environments in a marine bryozoan. Biol Bull 196:205–215

    Article  Google Scholar 

  • Palardy JE, Witman JD (2011) Water flow drives biodiversity by mediating rarity in marine benthic communities. Ecol Lett 14:63–68. doi:10.1111/j.1461-0248.2010.01555.x

    Article  Google Scholar 

  • Palumbi S (1984) Tactics of acclimation: morphological changes of sponges in an unpredictable environment. Science 225:1478–1480

    Article  CAS  Google Scholar 

  • Petersen JK (2007) Ascidian suspension feeding. J Exp Mar Biol Ecol 342:127–137. doi:10.1016/j.jembe.2006.10.023

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core team (2014) Nlme: linear and nonlinear mixed effects models. R package version 3.1-202. http://cran.r-project.org/package=nlme.pdf

  • Porter JW (1972) Patterns of species diversity in Caribbean reef corals. Ecology 53:745–748

    Article  Google Scholar 

  • R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • RStudio Team (2015) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. http://rstudio.com/

  • Riisgård HU, Manríquez P (1997) Filter-feeding in fifteen marine ectoprocts (Bryozoa): particle capture and water pumping. Mar Ecol Prog Ser 154:223–239. doi:10.3354/meps154223

    Article  Google Scholar 

  • Roberts MJ, van den Berg M (2005) Currents along the Tsitsikamma coast, South Africa, and potential transport of squid paralarvae and ichthyoplankton. Afr J Mar Sci 27:375–388. doi:10.2989/18142320509504096

    Article  Google Scholar 

  • Roberts M, Ribbink A, Morris T, van den Berg M, Engelbrecht D, Harding R (2006) Oceanographic environment of the Sodwana Bay coelacanths (Latimeria chalumnae), South Africa. S Afr J Sci 102:435–444

    Google Scholar 

  • Root R (1967) The niche exploitation pattern of the blue-gray gnatcatcher. Ecol Monogr 37:317–350

    Article  Google Scholar 

  • Rossi S, Tsounis G, Orejas C, Padrón T, Gili J, Bramanti L, Teixidó N, Gutt J (2008) Survey of deep-dwelling red coral (Corallium rubrum) populations at Cap de Creus (NW Mediterranean). Mar Biol 154:533–545. doi:10.1007/s00227-008-0947-6

    Article  Google Scholar 

  • Russ GR (1982) Overgrowth in a marine epifaunal community: competitive hierarchies and competitive networks. Oecologia 53:12–19

    Article  Google Scholar 

  • Samaai T, Gibbons MJ (2005) Demospongiae taxonomy and biodiversity of the Benguela region on the west coast of South Africa. Afr Nat Hist 1:1–96

    Google Scholar 

  • Sarkar D (2008) Lattice: multivariate data visualization with R. Springer, New York

    Book  Google Scholar 

  • Seitz RD, Wennhage H, Bergstro U, Lipcius RN, Ysebaert T (2014) Ecological value of coastal habitats for commercially and ecologically important species. ICES J Mar Sci 71:648–665. doi:10.1093/icesjms/fst152

    Article  Google Scholar 

  • Sheppard C (1980) Coral cover, zonation and diversity on reef slopes of Chagos atolls, and population structures of the major species. Mar Ecol Prog Ser 2:193–205. doi:10.3354/meps002193

    Article  Google Scholar 

  • Shears N, Babcock R (2002) Marine reserves demonstrate top-down control on temperate reefs. Oecologia 132:131–142

  • Sherman C, Nemeth M, Ruíz H, Bejarano I, Appeldoorn R, Pagán F, Schärer M, Weil E (2010) Geomorphology and benthic cover of mesophotic coral ecosystems of the upper insular slope of southwest Puerto Rico. Coral Reefs 29:347–360. doi:10.1007/s00338-010-0607-4

    Article  Google Scholar 

  • Sink KJ, Boshoff W, Samaai T, Timm PG, Kerwath S (2006) Observations of the habitats and biodiversity of the submarine canyons at Sodwana Bay. S Afr J Sci 102:466–474

    Google Scholar 

  • Sundborg Å (1956) The River Klarälven: a study of fluvial processes. Geogr Ann 38:125–237

    Google Scholar 

  • Tilney R, Nelson G, Radloff S, Buxton C (1996) Ichthyoplankton distribution and dispersal in the Tsitsikamma National Park Marine Reserve, South Africa. S Afr J Mar Sci 17:1–14

    Article  Google Scholar 

  • Torre L, Servetto N, Leonel Eory M, Momo F, Titian M, Abele D, Sahade R (2012) Respiratory responses of three Antarctic ascidians and a sea pen to increased sediment concentrations. Polar Biol. doi:10.1007/s00300-012-1208-1

    Google Scholar 

  • Virgilio M, Airoldi L, Abbiati M (2006) Spatial and temporal variations of assemblages in a Mediterranean coralligenous reef and relationships with surface orientation. Coral Reefs 25:265–272. doi:10.1007/s00338-006-0100-2

    Article  Google Scholar 

  • Wildish D, Kristmanson D (1997) Benthic suspension feeders and flow. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Wing S, Jack L (2012) Resource specialisation among suspension-feeding invertebrates on rock walls in Fiordland, New Zealand, is driven by water column structure and feeding mode. Mar Ecol Prog Ser 452:109–118. doi:10.3354/meps09588

    Article  Google Scholar 

  • Woodin S, Jackson J (1979) Interphyletic competition among marine benthos. Am Zool 19:1029–1043. doi:10.1093/icb/19.4.1029

    Article  Google Scholar 

  • Zuur A, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14. doi:10.1111/j.2041-210X.2009.00001.x

    Article  Google Scholar 

  • Zuur A, Hilbe J, Ieno E (2013) A beginner’s guide to GLM and GLMM with R. A frequentist and bayesian perspective for ecologists. Highland Statistics Ltd., Newburgh

    Google Scholar 

Download references

Acknowledgments

Funding for this project was provided by the National Research Foundation of South Africa, the Elwandle Node of the South African Environmental Observation Network, the South African Institute for Aquatic Biodiversity, the African Coelacanth Ecosystem Programme and the British Ecological Society. We thank SANParks, in particular Kyle Smith  and CapeNature for their assistance in the field, Toufiek Samaai, Kerry Sink, Shirley Parker-Nance, Lara Atkinson and Wayne Florence for assistance in identification of invertebrates and Angus Paterson and Clinton Veale for their constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. R. Heyns.

Additional information

Responsible Editor: J.-M. Gili.

Reviewed by G. Gonzalez-Mirelis and undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 414 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Heyns, E.R., Bernard, A.T.F., Richoux, N.B. et al. Depth-related distribution patterns of subtidal macrobenthos in a well-established marine protected area. Mar Biol 163, 39 (2016). https://doi.org/10.1007/s00227-016-2816-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2816-z

Keywords

Navigation