Foundation species' overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes

Although there is mounting evidence that biodiversity is an important and widespread driver of ecosystem multifunctionality, much of this research has focused on small-scale biodiversity manipulations. Hence, which mechanisms maintain patches of enhanced biodiversity in natural systems and if these patches elevate ecosystem multifunctionality at both local and landscape scales remain outstanding questions. In a 17 month experiment conducted within southeastern United States salt marshes, we found that patches of enhanced biodiversity and multifunctionality arise only where habitat-forming foundation species overlap—i.e. where aggregations of ribbed mussels (Geukensia demissa) form around cordgrass (Spartina alterniflora) stems. By empirically scaling up our experimental results to the marsh platform at 12 sites, we further show that mussels—despite covering only approximately 1% of the marsh surface—strongly enhance five distinct ecosystem functions, including decomposition, primary production and water infiltration rate, at the landscape scale. Thus, mussels create conditions that support the co-occurrence of high densities of functionally distinct organisms within cordgrass and, in doing so, elevate salt marsh multifunctionality from the patch to landscape scale. Collectively, these findings suggest that patterns in foundation species' overlap drive variation in biodiversity and ecosystem functioning within and across natural ecosystems. We therefore argue that foundation species should be integrated in our conceptual understanding of forces that moderate biodiversity–ecosystem functioning relationships, approaches for conserving species diversity and strategies to improve the multifunctionality of degraded ecosystems.

[1]  Chris J. Kennedy,et al.  The value of estuarine and coastal ecosystem services , 2011 .

[2]  C. Layman,et al.  Predation by the black-clawed mud crab,Panopeus herbstii, in Mid-Atlantic salt marshes: Further evidence for top-down control of marsh grass production , 2004 .

[3]  Elizabeth A. Canuel,et al.  Grazer diversity effects on ecosystem functioning in seagrass beds , 2003 .

[4]  Andrew Gonzalez,et al.  The functional role of producer diversity in ecosystems. , 2011, American journal of botany.

[5]  J. Zedler Algal mat productivity: Comparisons in a salt marsh , 1980 .

[6]  R. W. Frey,et al.  Biodeposition by the ribbed mussel Geukensia demissa in a salt marsh, Sapelo Island, Georgia , 1985 .

[7]  Mark D. Bertness,et al.  Population dynamics of the ribbed mussel, Geukensia demissa: The costs and benefits of an aggregated distribution , 1985, Oecologia.

[8]  E. Zavaleta,et al.  Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity , 2010, Proceedings of the National Academy of Sciences.

[9]  M. Bertness Fiddler Crab Regulation of Spartina alterniflora Production on a New England Salt Marsh , 1985 .

[10]  B. Silliman,et al.  Fungal farming in a snail , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[11]  R. Kneib Patterns of invertebrate distribution and abundance in the intertidal salt marsh: Causes and questions , 1984 .

[12]  Martin D. F. Ellwood,et al.  Doubling the estimate of invertebrate biomass in a rainforest canopy , 2004, Nature.

[13]  A. Hector,et al.  Biodiversity and ecosystem multifunctionality , 2007, Nature.

[14]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[15]  D. Watson,et al.  Mistletoe as a keystone resource: an experimental test , 2012, Proceedings of the Royal Society B: Biological Sciences.

[16]  M. Mazerolle,et al.  Title Model Selection and Multimodel Inference Based on (q)aic(c) , 2010 .

[17]  J. Bruno,et al.  Inclusion of facilitation into ecological theory , 2003 .

[18]  J. Teal DISTRIBUTION OF FIDDLER CRABS IN GEORGIA SALT MARSHES , 1958 .

[19]  B. Silliman,et al.  Secondary foundation species as drivers of trophic and functional diversity: evidence from a tree-epiphyte system. , 2014, Ecology.

[20]  M. B. Machmuller,et al.  Forecasting the effects of accelerated sea‐level rise on tidal marsh ecosystem services , 2009 .

[21]  Jake E. Simpson,et al.  Factors Affecting Soil Fauna Feeding Activity in a Fragmented Lowland Temperate Deciduous Woodland , 2012, PloS one.

[22]  H. Hemond,et al.  Surface Infiltration in Salt Marshes: Theory, Measurement, and Biogeochemical Implications , 1984 .

[23]  T. Jordan,et al.  A nitrogen budget of the ribbed mussel,Geukensia demissa, and its significance in nitrogen flow in a New England salt marsh1 , 1982 .

[24]  J. Webster,et al.  Loss of foundation species: consequences for the structure and dynamics of forested ecosystems , 2005 .

[25]  D. Franz,et al.  The influence of adult conspecifics and shore level on recruitment of the ribbed mussel Geukensia demissa (Dillwyn) , 1995 .

[26]  J. E. Byers,et al.  Density-dependent facilitation cascades determine epifaunal community structure in temperate Australian mangroves. , 2012, Ecology.

[27]  Peter Kareiva,et al.  Domesticated Nature: Shaping Landscapes and Ecosystems for Human Welfare , 2007, Science.

[28]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[29]  Garry D. Peterson,et al.  Response diversity, ecosystem change, and resilience , 2003 .

[30]  M. J. Hensel,et al.  Consumer diversity across kingdoms supports multiple functions in a coastal ecosystem , 2013, Proceedings of the National Academy of Sciences.

[31]  G. Daily,et al.  ECOSYSTEM SERVICES: Benefits Supplied to Human Societies by Natural Ecosystems , 2007 .

[32]  L. Jost Entropy and diversity , 2006 .

[33]  A. E. Stiven,et al.  Population processes in the ribbed mussel Geukensia demissa (Dillwyn) in a North Carolina salt marsh tidal gradient: spatial pattern, predation, growth and mortality , 1992 .

[34]  D. Tilman THE ECOLOGICAL CONSEQUENCES OF CHANGES IN BIODIVERSITY: A SEARCH FOR GENERAL PRINCIPLES101 , 1999 .

[35]  M. Bradford,et al.  Discontinuity in the responses of ecosystem processes and multifunctionality to altered soil community composition , 2014, Proceedings of the National Academy of Sciences.

[36]  B. Cardinale Biodiversity improves water quality through niche partitioning , 2011, Nature.

[37]  John F. Schalles,et al.  Landscape Estimates of Habitat Types, Plant Biomass, and Invertebrate Densities in a Georgia Salt Marsh , 2013 .

[38]  David Tilman,et al.  Several scales of biodiversity affect ecosystem multifunctionality , 2013, Proceedings of the National Academy of Sciences.

[39]  M. Dionne,et al.  Species‐specific mediation of temperature and community interactions by multiple foundation species , 2012 .

[40]  F. Tuya,et al.  Habitat cascades: the conceptual context and global relevance of facilitation cascades via habitat formation and modification. , 2010, Integrative and comparative biology.

[41]  J. Griffin,et al.  Top predators suppress rather than facilitate plants in a trait-mediated tri-trophic cascade , 2011, Biology Letters.

[42]  B. Silliman,et al.  Distribution and ecological role of the non-native macroalga Gracilaria vermiculophylla in Virginia salt marshes , 2009, Biological Invasions.

[43]  Peter M. Vitousek,et al.  Effects of plant composition and diversity on nutrient cycling , 1998 .

[44]  B. Helmuth,et al.  Morphological and Ecological Determinants of Body Temperature of Geukensia demissa, the Atlantic Ribbed Mussel, and Their Effects On Mussel Mortality , 2007, The Biological Bulletin.

[45]  M. Bertness,et al.  Interactions among Foundation Species and their Consequences for Community Organization, Biodiversity, and Conservation , 2011 .

[46]  J. E. Byers,et al.  Impacts of an abundant introduced ecosystem engineer within mudflats of the southeastern US coast , 2012, Biological Invasions.

[47]  J. Ludwig Issues and Perspectives in Landscape Ecology: Disturbances and landscapes: the little things count , 2005 .

[48]  M. Bertness,et al.  Hierarchical Organization via a Facilitation Cascade in Intertidal Cordgrass Bed Communities , 2007, The American Naturalist.

[49]  P. Reich,et al.  Impacts of Biodiversity Loss Escalate Through Time as Redundancy Fades , 2012, Science.

[50]  Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions , 2013, 1305.1985.

[51]  M. Bertness,et al.  Centuries of human-driven change in salt marsh ecosystems. , 2009, Annual review of marine science.

[52]  Helmut Hillebrand,et al.  Multiple functions increase the importance of biodiversity for overall ecosystem functioning. , 2008, Ecology.