MARINE ECOLOGY PROGRESS SERIES Vol. 311: 233–250, 2006 Published April 13 Mar Ecol Prog Ser OPENPEN ACCESSCCESS Biodiversity and the functioning of seagrass ecosystems J. Emmett Duffy* School of Marine Science and Virginia Institute of Marine Science, The College of William and Mary, Gloucester Point, Virginia 23062-1346, USA ABSTRACT: Biodiversity at multiple levels — genotypes within species, species within functional groups, habitats within a landscape — enhances productivity, resource use, and stability of seagrass ecosystems. Several themes emerge from a review of the mostly indirect evidence and the few exper- iments that explicitly manipulated diversity in seagrass systems. First, because many seagrass com- munities are dominated by 1 or a few plant species, genetic and phenotypic diversity within such foundation species has important influences on ecosystem productivity and stability. Second, in sea- grass beds and many other aquatic systems, consumer control is strong, extinction is biased toward large body size and high trophic levels, and thus human impacts are often mediated by interactions of changing ‘vertical diversity’ (food chain length) with changing ‘horizontal diversity’ (heterogene- ity within trophic levels). Third, the openness of marine systems means that ecosystem structure and processes often depend on interactions among habitats within a landscape (landscape diversity). There is clear evidence from seagrass systems that advection of resources and active movement of consumers among adjacent habitats influence nutrient fluxes, trophic transfer, fishery production, and species diversity. Future investigations of biodiversity effects on processes within seagrass and other aquatic ecosystems would benefit from broadening the concept of biodiversity to encompass the hierarchy of genetic through landscape diversity, focusing on links between diversity and trophic interactions, and on links between regional diversity, local diversity, and ecosystem processes. Maintaining biodiversity and biocomplexity of seagrass and other coastal ecosystems has important conservation and management implications. KEY WORDS: Food web · Habitat structure · Landscape · Production · Stability · Trophic transfer Resale or republication not permitted without written consent of the publisher INTRODUCTION areas for juvenile stages of commercially important species (Heck et al. 2003) contributes significantly to Seagrass beds are among the most widespread and the economic importance of estuarine fisheries (Ander- productive coastal ecosystem types worldwide, and son 1989, Costanza et al. 1997). Moreover, because range from the tropics to boreal margins of every much seagrass production ends up in below-ground ocean (Hemminga & Duarte 2000). Seagrasses provide tissues and ungrazed detritus, seagrass beds are an physical structure on otherwise largely featureless important global sink for carbon, accounting for an sediment bottoms, enhancing community diversity, estimated 15% of net CO2 uptake by marine organisms biomass, and primary and secondary production. The on a global scale, despite contributing only 1% of leaves provide a substratum for growth of epiphytic marine primary production (Duarte & Chiscano 1999). microalgae that fuel food webs and a shelter for inver- Unfortunately, seagrass beds are also among the tebrates and fishes that reach substantially greater most threatened of marine habitats (Short & Wyllie- densities than in unvegetated benthic habitats (Heck & Echevarria 1996, Duarte 2002). As in most other Orth 1980, Orth et al. 1984). This combined productiv- shallow marine ecosystems, 3 threats stand out as ity of seagrasses and associated algae ranks seagrass being especially pervasive. These are eutrophication beds among the most productive ecosystems on earth (Howarth et al. 2000, Cloern 2001), overfishing (Jack- (Duarte & Cebrián 1996), and their provision of nursery son et al. 2001), and the destruction of physical and *Email: [email protected] © Inter-Research 2006 · www.int-res.com 234 Mar Ecol Prog Ser 311: 233–250, 2006 biogenic habitat (Watling & Norse 1998, Thrush & Day- ties. It has long been recognized that the identities of ton 2002). These impacts, along with pollution, have species in a system strongly influence its functioning. caused major changes in abundance, species composi- Particular keystone species, dominant species, and tion, and structure of marine communities, including ecosystem engineers have pervasive impacts on struc- regional and even global extinctions (Carlton et al. ture and functioning of a wide range of ecosystems 1999, Jackson et al. 2001). Of the several types of (Jones et al. 1994, Power et al. 1996, Grime 1998). In human insults that the natural world faces, however, seagrass systems, specifically, identity of the dominant species extinction is arguably unique in being the only seagrass and macroalgal species strongly influences one that is irreversible. Thus, there are compelling sediment biogeochemistry, nutrient cycling, water-col- reasons for understanding how declining biodiversity umn oxygen profiles, water filtration capacity, primary mediates ecosystem functional processes such as pro- and secondary production, carbon storage, support of ductivity, trophic transfer, and carbon storage. higher trophic levels including commercially impor- Recognizing these links, the potential influence of tant species, and response to disturbance (Heck & Orth changing biodiversity on ecosystem functioning (BEF) 1980, Duarte 1991, Lemmens et al. 1996, Cebrián et al. has become a central topic in ecology and conservation 1997, Duarte et al. 1997, Valiela et al. 1997, Wigand et biology (Tilman 1999, Loreau et al. 2001, Naeem 2002, al. 1997, Lipcius et al. 1998, Hemminga & Duarte 2000, Srivastava & Vellend 2005) and a controversial one Deegan et al. 2002). For example, shallow eutrophic (Huston 1994, Huston et al. 2000, Schwartz et al. 2000, estuaries are often dominated by macroalgae (Valiela Wardle et al. 2000). By ecosystem functioning, I mean et al. 1997), which support much sparser animal popu- aggregate processes of whole ecosystems, such as pri- lations than seagrass beds (Deegan 2002). Experimen- mary and secondary production, trophic transfer, bio- tal removal of macroalgae in a eutrophic estuary geochemical fluxes, and resistance and resilience shifted dominance back to eelgrass Zostera marina, of ecosystem-level properties to disturbance. In this substantially enhancing abundances of fishes and review, I consider whether and how changing biodi- decapod crustaceans, and reducing water-column versity, across a hierarchy of taxonomic and ecological hypoxia (Deegan et al. 2002). At a finer taxonomic scales, may influence the functioning of seagrass eco- scale, 4 Mediterranean seagrass species spanned an systems, based on the few explicit experimental tests order of magnitude in the proportion of their produc- of such relationships and on inferences from other lines tion stored as refractory detritus (Cebrián et al. 1997), of evidence. I close with thoughts on how this research and a suite of Philippine seagrass species responded might inform our response to mitigating worldwide quite differently to experimental sediment loading, seagrass decline and its consequences for ecosystem with some species declining rapidly, but others show- services important to human society. ing an opportunistic growth increase (Duarte et al. 1997). Similarly, the identity of herbivore taxa is important FUNCTIONAL ASPECTS OF BIODIVERSITY to ecosystem processes; fishes and sea urchins often injure seagrasses by feeding on them, whereas most Living organisms vary at every level of the phyloge- gastropods and crustaceans facilitate seagrasses by netic hierarchy from individual genes through higher grazing their competitors (Hughes et al. 2004, Valen- taxa, and ecological assemblages vary in composition tine & Duffy 2005). Even superficially similar grazer from guilds or functional groups, through communi- taxa can have widely different impacts on the structure ties, to landscapes. This variation is of interest in and functioning of seagrass systems (Duffy et al. 2003, understanding ecosystem functioning insofar as it pro- 2005). In short, the ecosystem consequences of vides a proxy for variation in traits important to pro- variation in species identity are well documented and cesses such as growth, production, and resource use uncontroversial for seagrass beds and other eco- (e.g. Norberg et al. 2001). Historically, most research systems. exploring biodiversity effects on ecosystem function- The more challenging question is whether and how ing has equated ‘biodiversity’ with the number of the richness or variety of elements (genotypes, species, species (Tilman 1999, Loreau et al. 2001). In principal, habitat types) in a system influence its functioning. however, diversity at any level might influence eco- That is, are there general relationships between spe- system processes, and there is evidence that variation cies richness and ecosystem processes, or are species at several levels does so, as reviewed below. effects entirely idiosyncratic? Under what circum- Conceptually, diversity can be partitioned into varia- stances might we expect diversity effects or idiosyn- tion in identity (often called composition in the BEF lit- crasy? These and related questions have been a pri- erature) and number (or richness) of elements, whether mary focus of recent research in ecology (reviewed by those elements are