Abstract
Morpho-functional group classifications have been widely used in studies concerning benthic macroalgal communities, due to their easy application and the reduced cost and workload compared with species-level identifications. However, their effectiveness in representing spatio-temporal patterns and describing the effect of disturbances has been disputed. We propose a new, expanded classification of morphological functional groups based on thallus structure, growth form, branching pattern, and taxonomic affinities. This approach was tested on subtidal macroalgal assemblages of the western Mediterranean. We examined the differences in composition of assemblages subjected to different types of stressors using species, traditional morphological groups, and new morphological groups. Results showed that the new morphological groups allowed to detect patterns highlighted through species analyses generally better than the use of traditional morpho-functional groups. The new morphological groups may represent a valid tool in monitoring programs and environmental impact assessments, where it is important to detect early stages of environmental changes using methods that allow to examine a large number of samples in a limited time.
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Airoldi L (1998) Roles of disturbance, sediment stress and substratum retention on spatial dominance in algal turf. Ecology 79:2759–2770
Airoldi L (2000a) Responses of algae with different life histories to temporal and spatial variability of disturbance in subtidal reefs. Mar Ecol Prog Ser 195:81–92
Airoldi L (2000b) Effects of disturbance, life-history and overgrowth on coexistence of algal crusts and turfs. Ecology 8:798–814
Airoldi L, Fabiano M, Cinelli F (1996) Sediment deposition and movement over a turf assemblage in a shallow rocky coastal area of the Ligurian Sea. Mar Ecol Prog Ser 133:241–251
Anderson MJ (2001) A new method for a non-parametric multivariate analysis of variance. Aust Ecol 26:32–46
Anderson MJ, Connell SD, Gillanders BM, Diebel CE, Blom WM, Saunders JE, Landers TJ (2005) Relationships between taxonomic resolution and spatial scales of multivariate variation. J An Ecol 74:636–646
Arevalo R, Pinedo S, Ballesteros E (2007) Changes in the composition and structure of Mediterranean rocky-shore communities following a gradient of nutrient enrichment: descriptive study and test proposed methods to asses water quality regarding macroalgae. Mar Pollut Bull 55:104–113
Balata D, Piazzi L (2008) Patterns of diversity in rocky subtidal macroalgal assemblages in relation to depth. Bot Mar 51:464–471
Balata D, Piazzi L, Cecchi E, Cinelli F (2005) Variability of Mediterranean coralligenous assemblages subject to local variation in sediment deposits. Mar Environ Res 60:403–421
Balata D, Piazzi L, Benedetti-Cecchi L (2007a) Sediment disturbance and loss of beta diversity on subtidal rocky reefs. Ecology 88:2455–2461
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
Balata D, Piazzi L, Nesti U, Bulleri F, Bertocci I (2010) Effects of enhanced loads of nutrients on epiphytes on leaves and rhizomes of Posidonia oceanica. J Sea Res 63:157–216
Ballesteros E (1986) Metodos de analisis estructural en comunidades naturales, en particular del fitobentos. Oecol Aquat 8:117–131
Ballesteros E, Torras X, Pinedo S, Garcia M, Mangialajo M, De Torres M (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
Benedetti-Cecchi L, Bulleri F, Cinelli F (2000) The interplay of physical and biological factors in maintaining mid-shore and low-shore assemblages on rocky coasts in the northwest Mediterranean. Oecologia 123:406–417
Benedetti-Cecchi L, Pannacciulli F, Bulleri F, Moschella PS, Airoldi L, Relini G, Cinelli F (2001) Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar Ecol Prog Ser 214:137–150
Brodie J, Andersen RA, Kawachi M, Millar AJK (2009) Endangered algal species and how to protect them. Phycologia 48:423–438
Chapman MG, Underwood AJ, Skilleter GA (1995) Variability at different spatial scales between a subtidal assemblage exposed to the discharge of sewage and two control assemblages. J Exp Mar Biol Ecol 189:103–122
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austr Ecol 18:117–143
Dethier M (1981) Heteromorphic algal life histories: the seasonal pattern and response to herbivory of the brown crust Ralfsia californica. Oecologia 49:333–339
Diaz P, Lopez JJ, Piriz ML (2002) Symptoms of eutrophication in intertidal macroalgal assemblages of Nuevo Gulf (Patagonia, Argentina). Bot Mar 45:267–273
Diaz-Pulido G, Villamil L, Almanza V (2007) Herbivory effects on the morphology of the brown alga Padina boergesenii. Phycologia 46:131–136
Diez I, Scilla A, Santolaria A, Gorostiaga JM (1999) Phytobenthic intertidal community structure along an environmental pollution gradient. Mar Pollut Bull 38:463–472
Domis LND, Famà P, Bartlett AJ, van Reine WFP, Espinosa CA, Trono GC (2003) Defining taxon boundaries in members of the morphologically and genetically plastic genus Caulerpa (Caulerpales, Chlorophyta). J Phycol 39:1019–1037
Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366
Eriksson BK, Johansson G, Snoeijs P (2002) Long-term changes in the macroalgal vegetation of the inner Gullmar Fjord, Swedish Skagerrak coast. J Phycol 38:284–296
Fowler-Walker MJ, Wernberg T, Connell SD (2006) Differences in kelp morphology between wave sheltered and exposed localities: morphologically plastic or fixed traits? Mar Biol 148:755–767
Fraschetti S, Gambi C, Giangrande A, Musco L, Terlizzi A, Danovaro R (2007) Structural and functional response of meiofauna rocky assemblages to sewage pollution. Mar Poll Bull 52:540–548
Gorgula SK, Connell SD (2004) Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Mar Biol 145:613–619
Gorostiaga JM, Diez L (1996) Changes in the sublittoral benthic marine macroalgae in the polluted area of Abra de Bilbao and proximal coast (northern Spain). Mar Ecol Progr Ser 130:157–167
Hay ME (1994) Species as “noise” in community ecology: do seaweeds block our view of the kelp forest? Trends Ecol Evol 9:414–416
Hirst AJ (2006) Influence of taxonomic resolution on multivariate analyses of arthropod and macroalgal reef assemblages. Mar Ecol Prog Ser 324:83–93
Hofmann LC, Nettleton JC, Neefus CD, Mathieson AC (2010) Cryptic diversity of Ulva (Ulvales, Chlorophyta) in the Great Bay Estuarine system (Atlantic USA): introduced and indigenous distromatic species. Eur J Phycol 45:230–239
Irving AD, Connell SD (2002) Interactive effects of sedimentation and microtopography on the abundance of subtidal turf-forming algae. Phycologia 41:517–522
Johansson G, Snoeijs P (2002) Macroalgal photosynthetic responses to light in relation to thallus morphology and depth zonation. Mar Ecol Prog Ser 244:63–72
Juanes JA, Guinda X, Puente A, Revilla JA (2008) Macroalgae, a suitable indicator of the ecological status of coastal rocky communities in the NE Atlantic. Ecol Indicators 8:351–359
Karez R, Engelbert S, Kraufvelin P, Pedersen MF, Sommer U (2004) Biomass response and change in composition of ephemeral macroalgal assemblages along an experimental gradient of nutrient enrichment. Aq Bot 78:103–117
Kendrick GA (1991) Recruitment of coralline crust and filamentous turf algae in the Galapagos archipelago: effect of simulated scour, erosion and accretion. J Exp Mar Biol Ecol 147:47–63
Konar B, Iken K (2009) Influence of taxonomic resolution and morphological functional groups in multivariate analyses of macroalgal assemblages. Phycologia 48:24–31
Kraufvelin P, Moy FE, Christie H, Bokn TL (2006) Nutrient addition to experimental rocky shore communities revisited: delayed responses, rapid recovery. Ecosystems 9:1076–1093
Kubler JE, Dudgeon SR (1996) Temperature dependent change in the complexity of form of Chondrus crispus fronds. J Exp Mar Biol Ecol 207:15–24
Leliaert F, Verbruggen H, Wysor B, Clerck De (2009) DNA taxonomy in morphologically plastic taxa: algorithmic species delimitation in the Boodlea complex (Chlorophyta: Cladophorales). Mol Phylogen Evol 53:122–133
Lindstrom SC (2008) Cryptic diversity, biogeography and genetic variation in Northeast Pacific species of Porphyra sensu lato (Bangiales, Rhodophyta). J Appl Phycol 20:951–962
Lirman D, Biber P (2000) Seasonal dynamics of macroalgal communities of the northern Florida Reef tract. Bot Mar 43:305–314
Littler MM, Arnold KE (1982) Primary productivity of marine macroalgal functional-form groups from southwestern North America. J Phycol 18:307–311
Littler MM, Littler DS (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am Nat 116:25–44
Littler MM, Littler DS (1984) Relationship between macroalgal functional form groups and substrate stability in a subtropical rocky intertidal system. J Exp Mar Biol Ecol 74:13–34
Loughnane CJ, McIvor LM, Rindi F, Stengel DB, Guiry MD (2008) Morphology, rbcL phylogeny and distribution of distromatic Ulva (Ulvophyceae, Chlorophyta) in Ireland and southern Britain. Phycologia 47:416–429
Mazzella L, Scipione MB, Buia MC (1989) Spatio-temporal distribution of algal and animal communities in a Posidonia oceanica (L.) Delile meadow. PSZNI Mar Ecol 10:107–131
Norton TA, Mathieson AC, Neushul M (1982) A review of some aspects of form and function in seaweeds. Bot Mar 25:501–510
Orfanidis S, Panayotidis P, Stamatis N (2003) An insight to the ecological evaluation index (EEI). Ecological Indicators 3:27–33
Paine RT (1990) Benthic macroalgal competition: complications and consequences. J Phycol 26:2–17
Panayotidis P, Montesanto B, Orfanidis S (2004) Use of low budget monitoring of macroalgae to implement the European Water Framework Directive. J Appl Phycol 16:49–59
Petrilli FL, De Renzi G, Palmerini P, Morelli R, De Flora S (1979) Survey of the pollution in a coastal area of the Thyrrenian Sea. Aerial photography, physic-chemical and microbiological investigations and mutagenic monitoring. Wat Res 13:895–904
Phillips JC, Kendrick GA, Lavery PS (1997) A test of a functional group approach to detecting shift of macroalgal communities along a disturbance gradient. Mar Ecol Prog Ser 153:125–138
Piazzi L, Balata D, Cecchi E, Cinelli F (2003) Co-occurrence of Caulerpa taxifolia and C. racemosa in the Mediterranean Sea: interspecific interactions and influence on native macroalgal assemblages. Cryptogamie Algol 24:233–243
Piazzi L, Balata D, Cinelli F (2004a) Species composition and morphological groups of macroalgal assemblages around Gorgona Island (north-western Mediterranean Sea). Cryptogamie Algol 25:19–38
Piazzi L, Balata D, Pertusati M, Cinelli F (2004b) Spatial and temporal variability of Mediterranean macroalgal coralligenous assemblages in relation to habitat and substrate inclination. Bot Mar 47:105–115
Piazzi L, Balata D, Cecchi E, Cinelli F, Sartoni G (2010) Species composition and patterns of diversity of macroalgal coralligenous assemblages of northwester Mediterranean Sea. J Nat Hist 44:1–22
Pinedo S, Garcia M, Satta MP, de Torres M, Ballesteros E (2007) Rocky-shore communities as indicators of water quality: a case study in the northwestern Mediterranean. Mar Pollut Bull 55:126–135
Roberts BK, Connell SD (2008) Detecting benthic responses to human-induced change: effectiveness of alternate taxonomic classification and indices. Mar Ecol Prog Ser 358:75–84
Sala E, Boudouresque CF (1997) The role of fishes in the organization of a Mediterranean sublittoral community. I: algal communities. J Exp Mar Biol Ecol 212:25–44
Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Phil Trans Royal Soc B 360:1879–1888
Saunders GW, Lehmkuhl KV (2005) Molecular divergence and morphological diversity among four cryptic species of Plocamium (Plocamiales, Florideophyceae) in northern Europe. Eur J Phycol 40:293–312
Soltan D, Verlaque M, Boudouresque CF, Francour P (2001) Changes in macroalgal communities in the vicinity of a Mediterranean sewage outfall after the setting up of a treatment plant. Mar Pollut Bull 42:59–70
Steneck RL, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498
Steneck RL, Watling L (1982) Feeding capabilities and limitation of herbivorous mollusks: a functional group approach. Mar Biol 68:299–319
Tronholm A, Steen F, Tyberghein L, Leliaert F, Verbruggen H, Siguan MAR, De Clerck O (2010) Species delimitation, taxonomy and biogeography of Dictyota in Europe. J Phycol 46:1301–1321
Underwood AJ, Chapman MG (1996) Scales of spatial patterns of distribution of intertidal invertebrates. Oecologia 107:212–224
Vadas RL, Steneck RL (1988) Zonation of deep water benthic algae in the Gulf of Maine. J Phycol 24:338–346
Vanderklift MA, Lavery PS (2000) Patchiness in assemblages of epiphytic macroalgae on Posidonia coriacea at a hierarchy of spatial scales. Mar Ecol Prog Ser 192:127–135
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Balata, D., Piazzi, L. & Rindi, F. Testing a new classification of morphological functional groups of marine macroalgae for the detection of responses to stress. Mar Biol 158, 2459–2469 (2011). https://doi.org/10.1007/s00227-011-1747-y
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DOI: https://doi.org/10.1007/s00227-011-1747-y