Limited resilience in hotspots of functional richness: the Mediterranean riparian shrublands
Abstract
Functional diversity indices are increasingly being used to describe plant community assembly processes and ecosystem functioning. However, their relevance for predicting alterations in ecosystem functioning of riparian plant communities is still largely unknown. We investigated the functional patterns of riparian forests along environmental gradients, using biological and environmental data from 189 well-preserved riverine locations in mainland Portugal. We calculated functional diversity indices (e.g. Richness, Redundancy, Divergence) for four riparian forest types, namely the Alder woodlands, Ash woodlands, Tree-heath shrublands and Mediterranean shrublands, using their plant species composition and 25 plant functional traits. We used multiple linear regression to predict the effect of the environment in the functional structure of riparian forests and ultimately evaluate the resilience of the riparian forests to environmental fluctuations. We found that Mediterranean shrublands have a significantly higher Functional Richness and a lower Functional Redundancy in comparison to the other riparian forest types. Both regional and habitat variables were important for predicting the functional diversity of riparian forests, with varying patterns according to forest types. In particular, we found that the redundancy of Mediterranean shrublands is mostly affected by precipitation, suggesting their potential vulnerability to climate change in the study area. Our results suggest the usefulness of functional diversity measures for conservation and monitoring the ecological functioning of riparian forests.
Keywords
Functional diversity indices Functional richness Functional redundancy Riparian forests Resilience PortugalNotes
Acknowledgements
We acknowledge the Fundação para a Ciência e a Tecnologia I.P. (Portugal), FCT for financial support to Centro de Estudos Florestais (Project UID/AGR/00239/2013), Ph.D. Grant (I Lozanovska; PD/BD/114442/2016) and Post-doc Grant, (FC Aguiar; SFRH/BPD/112417/2015). We are in debt to APA I.P. (formerly the Water Institute, INAG IP) that provided access to biological and environmental data. The authors are thankful to the two anonymous Reviewers for the valuable help in improvement of the manuscript.
Supplementary material
References
- Aguiar FC, Ferreira MT, Albuquerque A, Moreira I (2007) Alien and endemic flora on reference and non-reference sites from Mediterranean type-streams of Portugal. Aquat Conserv Mar Freshw Ecosyst 17:335–347CrossRefGoogle Scholar
- Aguiar FC, Ferreira MT, Albuquerque A, Rodríguez-González P, Segurado P (2009) Structural and functional responses of riparian vegetation to human disturbance: performance and spatial-scale dependence. Fundam Appl Limnol 175:249–267CrossRefGoogle Scholar
- Aguiar FC, Cerdeira JO, Martins MJ, Ferreira MT (2013a) Riparian forests of Southwest Europe: are functional trait and species composition assemblages constrained by environment? J Veg Sci 24:628–638CrossRefGoogle Scholar
- Aguiar FC, Fabiao AM, Bejarano MD, Merritt D, Nilsson C, Martins MJ (2013b) FLOWBASE - a riparian plant traitbase. http://www.isa.ulisboa.pt/proj/flowbase/. Accessed Aug 2017
- Alados CL, Pueyo Y, Barrantes O, Escós J, Giner L, Robles AB (2004) Variations in landscape patterns and vegetation cover between 1957 and 1994 in a semiarid Mediterranean ecosystem. Landsc Ecol 19:545–561CrossRefGoogle Scholar
- Amigo J, Rodríguez-Guitián MA, Honrado JJP, Alves P (2017) The lowlands and midlands of Northwestern Atlantic Iberia. In: Loidi J (ed) The vegetation of the iberian peninsula, plant and vegetation. Springer International Publishing, Basel, pp 191–250CrossRefGoogle Scholar
- Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62:245–253CrossRefPubMedGoogle Scholar
- Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156CrossRefPubMedGoogle Scholar
- Barton K (2016) MuMin: multi-model interfereence. R Package Version 1.15.6. https://cran.rproject.org/web/package/MuMin/index.html. Accessed June 2016
- Bendix J (1994) Scale, direction, and pattern in riparian vegetation-environment relationships. Ann Asoc Am Geogr 84:652–665CrossRefGoogle Scholar
- Bernard-Verdier M, Navas ML, Vellend M, Violle C, Fayolle A, Garnier E (2012) Community assembly along a soil depth gradient: contrasting patterns of plant trait convergence and divergence in a Mediterranean rangeland. J Ecol 100:1422–1433CrossRefGoogle Scholar
- Biggs BJF, Nikora VI, Snelder TH (2005) Linking scales of flow variablity to lotic ecosystem structure and function. River Res Manag 21:283–298CrossRefGoogle Scholar
- Borcard D, Legendre P, Avoic-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Stat Rep 85:1826–1832Google Scholar
- Botta-Dukat Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540CrossRefGoogle Scholar
- Bruno D, Gutierrez-Canovas C, Sanchez-Ferndndez D, Velasco J, Nilsson C (2016) Impacts of environmental filters on functional redundancy in riparian vegetation. J Appl Ecol 53:846–855CrossRefGoogle Scholar
- Burnham KP, Anderson DR (2002) Model selection, and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
- Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087CrossRefGoogle Scholar
- Camporeale C, Ridolfi L (2006) Riparian vegetation distribution induced by river flow variability: a stochastic approach. Water Resour Res 42:1–13CrossRefGoogle Scholar
- Cooper DJ, Andersen DC, Chimner R (2003) Multiple pathways for woody plant establishment on floodplains at local to regional scales. J Ecol 91:182–196CrossRefGoogle Scholar
- Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecol Monogr 79:109–126CrossRefGoogle Scholar
- Cornwell WK, Schwilk DW, Ackerly DD (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87:1465–1471CrossRefPubMedGoogle Scholar
- Dai A (2011) Drought under global warming: a review. WIREs Clim Change 2:45–65CrossRefGoogle Scholar
- de Bello F, Leps J, Lavorel S, Moretti M (2007) Importance of species abundance for assessment of trait composition: an example based on pollinator communities. Community Ecol 8:163–170CrossRefGoogle Scholar
- de Frutos A, Navarro T, Pueyo Y, Alados CL (2015) Inferring resilience to fragmentation-induced changes in plant communities in a semi-arid Mediterranean ecosystem. PLoS One 10:1–18CrossRefGoogle Scholar
- de la Riva EG, Lloret F, Pérez-Ramos IM, Marañón T, Saura-Mas S, Díaz-Delgado R, Villar R (2016a) The importance of functional diversity in the stability of Mediterranean shrubland communities after the impact of extreme climatic events. J Plant Ecol 10:281–293Google Scholar
- de la Riva EG, Tosto A, Pérez-Ramos IM, Villar R, Olmo M, Anten NP, Marañón T (2016b) A plant economics spectrum in Mediterranean forests along environmental gradients: is there coordination among leaf, stem and root traits? J Veg Sci 27:187–199CrossRefGoogle Scholar
- Diaz S, Cabido M (1997) Plant functional types and ecosystem function in relation to global change. J Veg Sci 8:463–474CrossRefGoogle Scholar
- Diaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655CrossRefGoogle Scholar
- Donoghue MJ (2008) Colloquium paper: a phylogenetic perspective on the distribution of plant diversity. Proc Natl Acad Sci USA 105:11549–11555CrossRefPubMedPubMedCentralGoogle Scholar
- Elmqvist T, Folke C, Nystrom M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488–494CrossRefGoogle Scholar
- Espírito-Santo D, Capelo J, Neto C, Pinto-Gomes C, Ribeiro S, Canas RQ, Costa JC (2017) Lusitania. In: Loidi J (ed) The vegetation of the Iberian Peninsula, plant and vegetation. Springer International Publishing, Basel, pp 35–82CrossRefGoogle Scholar
- Flanagan NE, Richardson CJ, Ho M (2015) Connecting differential responses of native and invasive riparian plants to climate change and environmental alteration. Ecol Appl 25:753–767CrossRefPubMedGoogle Scholar
- Florsheim JL, Mount JF, Chin A (2008) Bank erosion as a desirable attribute of rivers. Bioscience 58:519–529CrossRefGoogle Scholar
- Freschet GT, Dias ATC, Ackerly DD, Aerts R, van Bodegom PM, Cornwell WK, Dong M, Kurokawa H, Liu G, Onipchenko VG, Ordonez JC, Peltzer DA, Richardson SJ, Shidakov II, Soudzilovskaia NA, Tao J, Cornelissen JHC (2011) Global to community scale differences in the prevalence of convergent over divergent leaf trait distributions in plant assemblages. Glob Ecol Biogeogr 20:755–765CrossRefGoogle Scholar
- Futuyma DJ, Moreno G (1998) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233CrossRefGoogle Scholar
- Gurnell AM, Bertoldi W, Corenblit D (2012) Changing river channels: the roles of hydrological processes, plants and pioneer fluvial landforms in humid temperate, mixed load, gravel bed rivers. Earth Sci Rev 111:129–141CrossRefGoogle Scholar
- Hooper DU, Chapin FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setala H, Symstad AJ, Vandemeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
- IPCC (2014) Summary for Policymakers. Climate Change 2014: Synthesis Report. In: Team CW, Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, p 151Google Scholar
- Jasmin JM, Kassen R (2007) On the experimental evolution of specialization and diversity in heterogeneous environments. Ecol Lett 10:272–281CrossRefPubMedGoogle Scholar
- Johansson ME, Keddy PA (1991) Intensity and asymmetry of competition between plant pairs of different degrees of similarity: an experimental study on two guilds of wetland plants. Oikos 60:27–34CrossRefGoogle Scholar
- Kilsby CG, Tellier SS, Fowler HJ, Howels TR (2007) Hydrological impacts of climate change on the Tejo and Guadiana Rivers. Hydrol Earth Syst Sci 11:1175–1189CrossRefGoogle Scholar
- Kominoski JS, Shah JJF, Canhoto C, Fischer DG, Giling DP, Gonzalez E, Griffiths NA, Larranaga A, LeRoy CJ, Mineau MM, McElarney YR, Shirley SM, Swan CM, Tiegs SD (2013) Forecasting functional implications of global changes in riparian plant communities. Front Ecol Environ 11:423‒432CrossRefGoogle Scholar
- Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305CrossRefPubMedGoogle Scholar
- Laliberte E, Wells JA, DeClerck F, Metcalfe DJ, Catterall CP, Queiroz C, Aubin I, Bonser SP, Ding Y, Fraterrigo J, McNamara S, Morgan JW, Sanches Merlos D, Vesk PA, Mayfield MM (2010) Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecol Lett 13:76–86CrossRefPubMedGoogle Scholar
- Laughlin DC, Joshi C, Richardson SJ, Peltzer DA, Mason NWH, Wardle DA (2015) Quantifying multimodal trait distributions improves trait-based predictions of species abundances and functional diversity. J Veg Sci 26:46–57CrossRefGoogle Scholar
- Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits. Funct Ecol 16:545–556CrossRefGoogle Scholar
- Lawson JR, Fryirs KA, Lenz T, Leishman MR (2015) Heterogenous flows foster heterogenous assemblages: relationships between functional diversity and hydrological heterogenity in riparian plant communities. Freshw Biol 60:2208–2225CrossRefGoogle Scholar
- Maire V, Gross N, Börger L, Proulx R, Wirth C, Pontes L, da Silveira Pontes L, Soussana JF, Louault F (2012) Habitat filtering and niche differentiation jointly explain species relative abundance within grassland communities along fertility and disturbance gradients. New Phytol 196:497–509CrossRefPubMedGoogle Scholar
- Mason NWH, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118CrossRefGoogle Scholar
- Mason NWH, Irz P, Lanoiselée C, Mouillot D, Argillier C (2008b) Evidence that niche specialization explains species–energy relationships in lake fish communities. J Anim Ecol 77:285–296CrossRefPubMedGoogle Scholar
- Mason NWH, de Bello F, Doležal J, Lepš J (2011) Niche overlap reveals the effects of competition, disturbance and contrasting assembly processes in experimental grassland communities. J Ecol 99:788–796CrossRefGoogle Scholar
- Mason NWH, de Bello F, Mouillot D, Pavoine S, Dray S (2012) A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients. J Veg Sci 24:794–806CrossRefGoogle Scholar
- McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185CrossRefPubMedGoogle Scholar
- Micheli F, Halpern BS (2005) Low functional redundancy in coastal marine assemblages. Ecol Lett 8:391–400CrossRefGoogle Scholar
- Moles AT, Perkins SE, Laffan SW, Flores-Moreno H, Awasthy M, Tindall ML, Sack L, Pitman A, Kattge J, Aarssen LW, Anand M, Bahn M, Blonder B, Cavender-Bares J, Cornelissen JHC, Cornwell WK, Diaz S, Dickie JB, Freschet GT, Griffiths JG, Gutierrez AG, Hemmings FA, Hickler T, Hitchcock TD, Keighery M, Kleyer M, Kurokawa H, Leishman MR, Liu K, Ulo N, Onipchenko V, Onoda Y, Penuelas J, Pillar VD, Reich PB, Shiodera S, Siefert A, Sosinski EE Jr, Soudzilovskaia NA, Swaine EK, Swenson NG, van Bodegom PM, Warman L, Weiher E, Wright IJ, Zhang H, Zobel M, Bonser SP (2014) Which is a better predictor of plant traits: temperature or precipitation? J Veg Sci 25:1167–1180CrossRefGoogle Scholar
- Mouchet MA, Villeger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876CrossRefGoogle Scholar
- Mouillot D, Graham NAJ, Villeger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177CrossRefPubMedGoogle Scholar
- Naeem S (1998) Species redundancy and ecosystem reliability. Conserv Biol 12:39–45CrossRefGoogle Scholar
- Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579CrossRefGoogle Scholar
- Naiman RJ, Décamps H (1997) The ecology of interfaces: riparian zones. Annu Rev Ecol Syst 28:621–658CrossRefGoogle Scholar
- Naiman RJ, Décamps H (2005) Riparia: ecology, conservation, and management of streamside communities. Elsevier Academic Press, San DiegoGoogle Scholar
- Naiman RJ, Bunn SE, Nilsson C, Petts GE, Pinay G, Thompson LC (2002) Legitimizing fluvial ecosystems as users of water: an overview. Environ Manag 30:455–467CrossRefGoogle Scholar
- Navarro T, Pascual V, Alados CL, Cabezudo B (2009) Growth forms, dispersal strategies and taxonomic spectrum in a semi-arid shrubland in SE Spain. J Arid Environ 73:103–112CrossRefGoogle Scholar
- Pakeman RJ (2011) Functional diversity indices reveal the impacts of land use intensification on plant community assembly. J Ecol 99:1143–1151CrossRefGoogle Scholar
- Pavoine S, Gasc A, Bonsall MB, Mason NWH (2013) Correlations between phylogenetic and functional diversity: mathematical artefacts or true ecological and evolutionary processes? J Veg Sci 24:781–793CrossRefGoogle Scholar
- Petchey OL, Evans KL, Fishburn IS, Gaston KJ (2007) Low functional diversity and no redundancy in British avian assemblages. J Anim Ecol 76:977–985CrossRefPubMedGoogle Scholar
- Pillar VD, Blanco CC, Müller SC, Sosinski EE, Joner F, Duarte LDS (2013) Functional redundancy and stability in plant communities. J Veg Sci 24:963–974CrossRefGoogle Scholar
- Poff NL (1997) Landscape filters and species traits: towards mechanistic understanding and prediction in stream ecology. J N Am Benthol Soc 16:391–409CrossRefGoogle Scholar
- Poff NL, Olden JD, Vieira NKM, Finn DS, Simmons MP, Kondratieff BC (2006) Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J N Am Benthol Soc 25:730–755CrossRefGoogle Scholar
- Rao RC (1982) Diversity and dissimilarity coefficients: a unified approach. Theor Popul Biol 43:24–43CrossRefGoogle Scholar
- Renöfält BM, Nilsson C, Jansson R (2005) Spatial and temporal patterns of species richness in a riparian landscape. J Biogeogr 32:2025–2037CrossRefGoogle Scholar
- Ricklefs RE, Travis J (1980) A morphological approach to the study of avian community organization. Auk 97:321–338Google Scholar
- Roscher C, Schumacher J, Gerighausen U, Schmid B (2014) Different assembly processes drive shifts in species and functional composition in experimental grasslands varying in sown diversity and community history. PLoS One 9:e101928CrossRefPubMedPubMedCentralGoogle Scholar
- Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162CrossRefGoogle Scholar
- Salinas MJ, Blanca G, Romero AT (2000) Evaluating riparian vegetation in semi-arid Mediterranean watercourses in the south-eastern Iberian Peninsula. Environ Conserv 27:24–35CrossRefGoogle Scholar
- Sasaki T, Katabuchi M, Kamiyama C, Shimazaki M, Nakashizuka T, Hikosaka K (2014) Vulnerability of moorland plant communities to environmental change: consequences of realistic species loss on functional diversity. J Appl Ecol 51:299–308CrossRefGoogle Scholar
- Schleuter DS, Aufresne MD, Assol FM (2010) A user’s guide to functional diversity indices. Ecol Monogr 80:469–484CrossRefGoogle Scholar
- Spasojevic MJ, Suding KN (2012) Inferring community assembly mechanisms from functional diversity patterns: the importance of multiple assembly processes. J Ecol 100:652–661CrossRefGoogle Scholar
- Stella JC, Riddle J, Piégay H, Gagnage M, Trémélo ML (2013) Climate and local geomorphic interactions drive patterns of riparian forest decline along a Mediterranean Basin river. Geomorphology 202:101–114CrossRefGoogle Scholar
- Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69:476–498CrossRefGoogle Scholar
- Stromberg JC, Lite SJ, Marler R, Paradzick C, Patrick B, Shorrock D, White MJ, White MS (2007) Altered stream-flow regimes and invasive plant species: the Tamarix Case. Glob Ecol Biogeogr 16:381–393CrossRefGoogle Scholar
- Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302CrossRefGoogle Scholar
- Vandewalle M, de Bello F, Berg MP, Bolger T, Dolédec S, Dubs F, Feld CK, Harrington R, Harrison PA, Lavorel S, da Silva PM, Moretti M, Niemela J, Santos P, Satter T, Sousa JP, Sykes MT, Vanbergen AJ, Woodcock BA (2010) Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiv Conserv 19:2921–2947CrossRefGoogle Scholar
- Villeger S, Mouillot D (2008) Additive partitioning of diversity including species differences: a comment on Hardy and Senterre (2007). J Ecol 96:845–848CrossRefGoogle Scholar
- Villeger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301CrossRefPubMedGoogle Scholar
- Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892CrossRefGoogle Scholar
- Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23CrossRefGoogle Scholar
- Walker BH (1995) Conserving biological diversity through ecosystem resilience. Conserv Biol 9:747–752CrossRefGoogle Scholar