Integration of ESCA index through the use of sessile invertebrates

Authors

DOI:

https://doi.org/10.3989/scimar.04565.01B

Keywords:

coralligenous assemblages, ESCA and ESCA-TA indices, ecological quality, macroalgae, macro-invertebrates, Mediterranean Sea

Abstract


The ESCA (Ecological Status of Coralligenous Assemblages) index was developed to assess the ecological quality of coralligenous habitat using macroalgae as a biological indicator. The aim of this study was to evaluate the response to human-induced pressures of macroalgae and sessile macro-invertebrates shaping the coralligenous habitat and to integrate their sensitivity into the ESCA index. Coralligenous assemblages were sampled at 15 locations of the NW Mediterranean Sea classified into three groups: i) marine protected areas; ii) low urbanized locations; and iii) highly urbanized locations. A sensitivity level value was assigned to each taxon/group on the basis of its abundance in each environmental condition, the data available in the literature and the results of an expert judgement survey. The index that includes the totality of the assemblages (named ESCA-TA), calculated using both macroalgae and sessile macro-invertebrates, detected the levels of human pressure more precisely than the index calculated with only macroalgae or with only invertebrates. The potential for assessing the ecological quality of marine coastal areas was thus increased with the ESCA-TA index thanks to the use of a higher variety of descriptors.

Downloads

Download data is not yet available.

References

Airoldi L. 2003. The effects of sedimentation on rocky coastal assemblages. Oceanogr. Mar. Biol. Annu. Rev. 41: 161-203.

Anderson M.J. 2001. A new method for a non-parametric multivariate analysis of variance. Aust. Ecol. 26: 32-46.

Anderson M.J. 2006. Distance-based test for homogeneity of multivariate dispersions. Biometrics 62: 245-253. https://doi.org/10.1111/j.1541-0420.2005.00440.x PMid:16542252

Anderson M.J., Robinson J. 2003. Generalised discriminant analysis based on distances. Aust. N. Z. J. Statistics 45: 301-318. https://doi.org/10.1111/1467-842X.00285

Anderson M.J., Willis T.J. 2003. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84: 511-524. https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2

Anderson M.J., Ellingsen K.E., McArdle B.H. 2006. Multivariate dispersion as a measure of beta diversity. Ecol. Lett. 9: 683-693. https://doi.org/10.1111/j.1461-0248.2006.00926.x PMid:16706913

Anderson M.J., Gorley R.N., Clarke K.R. 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods.

Balata D., Piazzi L., Cecchi E., et al. 2005. Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposits. Mar. Environ. Res. 60: 403-421. https://doi.org/10.1016/j.marenvres.2004.12.005 PMid:15924991

Balata D., Piazzi L., Benedetti-Cecchi L. 2007a. Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology 8: 2455-2461. https://doi.org/10.1890/07-0053.1

Balata D., Piazzi L., Cinelli F. 2007b. Increase of sedimentation in a subtidal system: effects on the structure and diversity of macroalgal assemblages. J. Exp. Mar. Biol. Ecol. 351: 73-82. https://doi.org/10.1016/j.jembe.2007.06.019

Balata D., Piazzi L., Rindi F. 2011. Testing a new classification of morphological functional groups of marine macroalgae for the detection or responses to disturbance. Mar. Biol. 158: 2459-2469. https://doi.org/10.1007/s00227-011-1747-y

Ballesteros E. 2006. Mediterranean coralligenous assemblages: a synthesis of present knowledge. Oceanogr. Mar. Biol. Annu. Rev. 44: 123-195. https://doi.org/10.1201/9781420006391.ch4

Ballesteros E., Torras X., Pinedo S., et al. 2007. A new methodology based on littoral community cartography dominated by macroalgae for the implementation of European Water Framework Directive. Mar. Pollut. Bull. 55: 172-180. https://doi.org/10.1016/j.marpolbul.2006.08.038 PMid:17045303

Bavestrello G., Cerrano C., Zanzi D., et al. 1997. Damage by fishing activities in the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aq. Conserv. Mar. Freshwater Ecosyst. 7: 253-262. https://doi.org/10.1002/(SICI)1099-0755(199709)7:3<253::AID-AQC243>3.0.CO;2-1

Bermejio R., Fuente G., Vergara J.J., et al. 2013. Application of the CARLIT index along a biogeographical gradient in the Alboran Sea (European Coast). Mar. Pollut. Bull. 72: 107-118. https://doi.org/10.1016/j.marpolbul.2013.04.011 PMid:23673205

Bertolino M., Cerrano C., Bavestrello G., et al. 2013. Diversity of Porifera in the Mediterranean coralligenous accretions, with description of a new species. ZooKeys 336: 1-37. https://doi.org/10.3897/zookeys.336.5139 PMid:24146570 PMCid:PMC3800777

Birk S., Bonne W., Borja A., et al. 2012. Three hundred ways to assess Europe's surface waters: an almost complete overview of biological methods to implement the Water Framework Directive. Ecol. Ind. 18: 31-41. https://doi.org/10.1016/j.ecolind.2011.10.009

Cánovas Molina A., Montefalcone M., Vassallo P., et al. 2016. Combining literature review, acoustic mapping and in situ observations: an overview of coralligenous assemblages in Liguria (NW Mediterranean Sea). Sci. Mar. 80: 7-16.

Casas-Guell E., Teixidó N., Garrabou J., et al. 2015. Structure and biodiversity of coralligenous assemblages over broad spatial and temporal scales. Mar. Biol. 162: 901-912. https://doi.org/10.1007/s00227-015-2635-7

Cecchi E., Gennaro P., Piazzi L., et al. 2014. Development of a new biotic index for ecological status assessment of Italian coastal waters based on coralligenous macroalgal assemblages. Eur. J. Phycol. 16: 1709-1717. https://doi.org/10.1080/09670262.2014.918657

Cerrano C., Bavestrello G., Bianchi C.N., et al. 2000. A catastrophic mass-mortality episode of gorgonians and other organisms in the Ligurian Sea (North-western Mediterranean), summer 1999. Ecol. Lett. 3: 284-293. https://doi.org/10.1046/j.1461-0248.2000.00152.x

Clarke K.R. 1993. Non-parametric multivariate analyses of changes in community structure. Aust. Ecol. 18: 117-143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x

Clarke K.R., Gorley R.N. 2006. Primer v6: user manual/tutorial. PRIMER-E, Plymouth.

Coma R., Linares C., Ribes M., et al. 2006. Consequences of a mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Menorca (NW Mediterranean). Mar. Ecol. Progr. Ser. 327: 51-60. https://doi.org/10.3354/meps327051

Darling E.S., Alvarez-Filip L., Oliver T.A., et al. 2012. Evaluating life-history strategies of reef corals from species traits. Ecol. Lett. 15: 1378-1386. https://doi.org/10.1111/j.1461-0248.2012.01861.x PMid:22938190

de la Nuez-Hernández D., Valle C., Forcada A., et al. 2014. Assessing the erect bryozoan Myriapora truncata (Pallas, 1766) as indicator of recreational diving impact on coralligenous reef communities. Ecol. Ind. 46: 193-200. https://doi.org/10.1016/j.ecolind.2014.05.035

Deter J., Descamp P., Ballista L., et al. 2012. A preliminary study toward an index based on coralligenous assemblages for the ecological status assessment of Mediterranean French coastal waters. Ecol. Ind. 20: 345-352. https://doi.org/10.1016/j.ecolind.2012.03.001

EC. 2008. DIRECTIVE 2008/56/EC of the European Parliament and of the Council, of 17 June 2008, establishing a framework for Community action in the field of marine environmental policy (Marine Strategy Framework Directive). Official Journal of the European Commission, G.U.C.E. 25/6/2008, L 164/19.

Falace A., Kaleb S., Curiel D., et al. 2015. Calcareous bio-concretions in the northern Adriatic Sea: habitat types, environmental factors that influence habitat distributions, and predictive modeling. PLoS ONE 10: e0140931. https://doi.org/10.1371/journal.pone.0140931 PMid:26560891 PMCid:PMC4641629

Garrabou J., Sala E., Arcas A., et al. 1998. The impact of diving on rocky sub-littoral communities: a case study of a bryozoan population. Conserv. Biol. 12: 302-312. https://doi.org/10.1046/j.1523-1739.1998.96417.x

Garrabou J., Coma R., Bensoussan N., et al. 2009. Mass mortality in Northwestern Mediterranean rocky benthic communities: effects of the 2003 heat wave. Global Change Biol. 15: 1090-1103. https://doi.org/10.1111/j.1365-2486.2008.01823.x

Gatti G., Montefalcone M., Rovere A., et al. 2012. Seafloor integrity down the harbor waterfront: the coralligenous shoals off Vado Ligure (NW Mediterranean). Adv. Limnol. 3: 51-67. https://doi.org/10.4081/aiol.2012.5326

Gatti G., Bianchi C.N., Morri C., et al. 2015a. Coralligenous reefs state along anthropized coasts: application and validation of the COARSE index, based on a rapid visual assessment (RVA) approach. Ecol. Ind. 52: 567-576. https://doi.org/10.1016/j.ecolind.2014.12.026

Gatti G., Bianchi C.N., Parravicini V., et al. 2015b. Ecological change, sliding baselines and the importance of historical data: lessons from combining observational and quantitative data on a temperate reef over 70 years. PLoS ONE 10: e0118581. https://doi.org/10.1371/journal.pone.0118581 PMid:25714413 PMCid:PMC4340909

Grime J.P. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am. Nat. 111: 1169-1194. https://doi.org/10.1086/283244

Harmelin J.G., Capo S. 2001. Effects of sewage on bryozoan diversity in Mediterranean rocky bottoms. In: Wyse J., Spencer J. (eds), Bryozoan, Studies 2001. Swets and Zeitlinger, pp. 151-156.

Hong J.S. 1983. Impact of pollution on the benthic community. Environmental impact of the pollution on the benthic coralligenous community in the Gulf of Fos, north-western Mediterranean. Bull. Korean Fish. Soc. 16: 273-290.

Huete-Stauffer C., Vielmini I., Palma M., et al. 2011. Paramuricea clavata (Anthozoa, Octocorallia) loss in the Marine Protected Area of Tavolara (Sardinia, Italy) due to a mass mortality event. Mar. Ecol. 32: 107-116. https://doi.org/10.1111/j.1439-0485.2011.00429.x

Jackson J.B., Sala E. 2001. Unnatural oceans. Sci. Mar. 65: 273-281. https://doi.org/10.3989/scimar.2001.65s2273

Kipson S., Fourt M., Teixidó N., et al. 2011. Rapid biodiversity assessment and monitoring method for highly diverse benthic communities: a case study of Mediterranean coralligenous outcrops. PLoS ONE 6: e27103. https://doi.org/10.1371/journal.pone.0027103 PMid:22073264 PMCid:PMC3206946

Linares C., Coma R., Garrabou J., et al. 2008. Size distribution, density and disturbance in two Mediterranean gorgonians: Paramuricea clavata and Eunicella singularis. J. Appl. Ecol. 45: 688-699. https://doi.org/10.1111/j.1365-2664.2007.01419.x

Lopez y Royo C., Silvestri C., Pergent G., et al. 2009. Assessment of human-induced pressures on the coastal zone, using publicly available data. J. Environ. Manag. 90: 1494-1501. https://doi.org/10.1016/j.jenvman.2008.10.007 PMid:19054603

Martin C.S., Giannoulaki M., De Leo F., et al. 2014. Coralligenous and maërl habitats: predictive modelling to identify their spatial distributions across the Mediterranean Sea. Sci. Rep. 4: 5073. https://doi.org/10.1038/srep05073

Mateos-Molina D., Palma M., Ruiz-Valentín I., et al. 2015. Assessing consequences of land cover changes on sediment deliveries to coastal waters at regional level over the last two decades in the northwestern Mediterranean Sea. Ocean Coast. Manage. 116: 435-442. https://doi.org/10.1016/j.ocecoaman.2015.09.003

Montefalcone M., Albertelli G., Morri C., et al. 2009. Legal protection is not enough: Posidonia oceanica meadows in marine protected areas are not healthier than those in unprotected areas of the northwest Mediterranean Sea. Mar. Pollut. Bull. 58: 515-519. https://doi.org/10.1016/j.marpolbul.2008.12.001 PMid:19150722

Montefalcone M., Morri C., Bianchi C.N., et al. 2017. The two facets of species sensitivity: stress and disturbance on coralligenous assemblages in space and time. Mar. Pollut. Bull. 117: 229-238. https://doi.org/10.1016/j.marpolbul.2017.01.072 PMid:28185652

Nikolic V., Zuljevic A., Mangialajo L., et al. 2013. Cartography of littoral rocky-shore communities (CARLIT) as a tool for ecological quality assessment of coastal waters in the Eastern Adriatic Sea. Ecol. Ind. 34: 87-93. https://doi.org/10.1016/j.ecolind.2013.04.021

Parravicini V., Micheli F., Montefalcone M., et al. 2010. Rapid assessment of benthic communities: a comparison between two visual sampling techniques. J. Exp. Mar. Biol. Ecol. 395: 21-29. https://doi.org/10.1016/j.jembe.2010.08.005

Parravicini V., Micheli F., Montefalcone M., et al. 2013. Conserving biodiversity in a human-dominated world: degradation of marine sessile communities within a protected area with conflicting human uses. PLoS ONE 8: e75767. https://doi.org/10.1371/journal.pone.0075767 PMid:24143173 PMCid:PMC3797118

Piazzi L., Gennaro P., Balata D. 2011. Effects of nutrient enrichment on macroalgal coralligenous assemblages. Mar. Pollut. Bull. 62: 1830-1835. https://doi.org/10.1016/j.marpolbul.2011.05.004 PMid:21620421

Piazzi L., Gennaro P., Balata D. 2012. Threats to macroalgal coralligenous assemblages in the Mediterranean Sea. Mar. Pollut. Bull. 64: 2623-2629. https://doi.org/10.1016/j.marpolbul.2012.07.027 PMid:22863350

Piazzi L., Balata D., Cecchi E., et al. 2014. Effectiveness of different investigation procedures in detecting anthropogenic impacts on coralligenous assemblages. Sci. Mar. 78: 319-328. https://doi.org/10.3989/scimar.03989.28A

Piazzi L., Gennaro P., Cecchi E., et al. 2015. Improvement of the ESCA index for the evaluation of ecological quality of coralligenous habitat under the European Framework Directives. Medit. Mar. Sci. 16: 419-426. https://doi.org/10.12681/mms.1029

Piazzi L., La Manna G., Cecchi E., et al. 2016. Protection changes the relevancy of scales of variability in coralligenous assemblages. Estuar. Coast. Shelf Sci. 175: 62-69. https://doi.org/10.1016/j.ecss.2016.03.026

Ponti M., Fava F., Abbiati M. 2011. Spatial-temporal variability of epibenthic assemblages on subtidal biogenic reefs in the northern Adriatic Sea. Mar. Biol. 158: 1447-1459. https://doi.org/10.1007/s00227-011-1661-3

Sala E., Garrabou J., Zabala M. 1996. Effects of diver frequentation on marine sub-littoral population of the bryozoan Pentapora fascialis. Mar. Biol. 126: 451-459. https://doi.org/10.1007/BF00354627

Sartoretto S., David R., Aurelle D., et al. 2014. An integrated approach to evaluate and monitor the conservation state of coralligenous bottoms: the INDEX-COR method. In: Bouafif C., Langar H., Ouerghi A. (eds), Proceedings of the second Mediterranean Symposium on the conservation of Coralligenous and other Calcareous Bio-Concretions (Portoro?, Slovenia, 29-30 October 2014). UNEP/MAP – RAC/SPA, RAC/SPA publ., Tunis: pp. 159-165.

Stachowitsch M. 2003. Research on intact marine ecosystems: a lost era. Mar. Pollut. Bull. 46: 801-805. https://doi.org/10.1016/S0025-326X(03)00109-7

Taylor R.B., Peek J.T.A., Rees T.A.V. 1998. Scaling of ammonium uptake by seaweeds to surface area: volume ratio: geographical variation and the role of uptake by passive diffusion. Mar. Ecol. Progr. Ser. 169: 143-148. https://doi.org/10.3354/meps169143

Teixidó N., Garrabou J., Harmelin J.-G. 2011. Low dynamics, high longevity and persistence of sessile structural species dwelling on Mediterranean coralligenous outcrops. PLoS ONE 6: e23744. https://doi.org/10.1371/journal.pone.0023744 PMid:21887308 PMCid:PMC3161055

Teixidó N., Casas E., Cebrian E., et al. 2013. Impacts on coralligenous outcrop biodiversity of a dramatic coastal storm. PLoS ONE 8: e53742. https://doi.org/10.1371/journal.pone.0053742 PMid:23326496 PMCid:PMC3542355

Published

2017-06-30

How to Cite

1.
Piazzi L, Gennaro P, Cecchi E, Serena F, Nike Bianchi C, Morri C, Montefalcone M. Integration of ESCA index through the use of sessile invertebrates. Sci. mar. [Internet]. 2017Jun.30 [cited 2024Mar.28];81(2):283-90. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1708

Issue

Section

Articles

Most read articles by the same author(s)