Vol. 508: 129–138, 2014 MARINE ECOLOGY PROGRESS SERIES Published August 4 doi: 10.3354/meps10867 Mar Ecol Prog Ser Additive and site-specific effects of two foundation species on invertebrate community structure A. Randall Hughes1,*, Paul E. Gribben2,4, David L. Kimbro1, Melanie J. Bishop3 1Northeastern University Marine Science Center, 430 Nahant Rd., Nahant, MA 01908, USA 2Plant Functional Biology and Climate Change Cluster, School of the Environment, University of Technology, Sydney, NSW 2007, Australia 3Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia 4Present address: Institute of Natural and Mathematical Sciences, Massey University, Auckland 0745, New Zealand ABSTRACT: Many aquatic and terrestrial ecosystems are comprised of assemblages of multiple foundation species. Despite the common occurrence of multiple foundation species, relatively few studies have examined the independent and combined effects of multiple co-occurring foundation species or investigated whether they facilitate similar or distinct associated communities. At 2 sites in a temperate Australian mangrove forest, we examined the independent and interactive effects of co-occurring intermediate foundation species (the macroalga Hormosira banksii and the oyster Saccostrea glomerata —each of which is facilitated by mangrove pneumatophores) on associated community structure. Because the identity of the associated species facilitated by these 2 founda- tion species can differ, we hypothesized that their combined effects on species richness would be independent and additive. We found that despite their mutual facilitation by mangrove pneu- matophores, the 2 intermediate foundation species exhibited independent and positive effects on associated species abundance, richness, and composition. Associated species abundance and richness increased consistently with S. glomerata biomass. In contrast, associated species abun- dance and richness only responded to H. banksii presence (not biomass), and this response dif- fered across sites. Our finding that functionally different species produce additive effects on biodiversity is consistent with predictions from other recent studies of facilitation cascades. Fur- thermore, the site-specific effects of foundation species in this study add to growing evidence that while foundation species can set the potential abundance and richness of associated communities, realized community structure is determined by processes operating at larger spatial and temporal scales. KEY WORDS: Algae · Context dependency · Facilitation cascade · Foundation species · Mangrove · Oyster Resale or republication not permitted without written consent of the publisher INTRODUCTION assemblages of multiple foundation species, yet they are rarely examined as such (Thomsen et al. 2010, Foundation species provide habitat and/or refuge Angelini et al. 2011). In some cases, multiple foun - from abiotic or biotic stress, facilitating diverse com- dation species overlap with one another and are munities (Dayton 1972, Bruno et al. 2003). Many hier archically organized into a facilitation cascade aquatic and terrestrial ecosystems are comprised of whereby a basal foundation species facilitates an *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 130 Mar Ecol Prog Ser 508: 129–138, 2014 intermediate foundation species, and this interme - ever, relatively few manipulations of foundation spe- diate (often in combination with the basal species) cies have included multiple levels of biomass or been in turn facilitates a community of associated orga - replicated across different sites, limiting our under- nisms (Gribben et al. 2009, Hughes et al. 2009, Altieri standing of context dependency in the strength of et al. 2010, Thomsen et al. 2010, Angelini et al. 2011, facilitation by foundation species. Bishop et al. 2012). In other instances, multiple foun- Here, we examine the independent and interactive dation species can overlap, without cascading effects of 2 co-occurring intermediate foundation effects, or co-exist in spatial mosaics of discrete species of temperate Australian mangrove forests, patches (Angelini et al. 2011, Bishop et al. 2012). the macroalga Hormosira banksii and the oyster Sac- Despite the common occurrence of multiple founda- costrea glomerata, on the richness and abundance tion species, relatively few studies have examined of their associated communities. These intermediate the independent and combined effects of multiple foundation species are independently facilitated by co-occurring foundation species or investigated pneumatophores of Avicennia marina mangroves, whether they facilitate similar or distinct ecological the alga responding to pneumatophore density, and communities (but see Gribben et al. 2009, Altieri et the oyster responding to pneumatophore presence or al. 2010, Bishop et al. 2012, Dijkstra et al. 2012). absence (Bishop et al. 2012). Both intermediate spe- Facilitation of biotic communities is highly de- cies are found at different abundances across a range pendent on the functional identity of the foundation of microhabitats; when on their own, the density of species involved (Bruno & Bertness 2001, Ellison et each has been shown to influence the richness and al. 2005, Irving & Bertness 2009, Bishop et al. 2013, abundance of the associated community they support Gribben et al. 2013). Within habitats, co-occurring (Bishop et al. 2012). In previous studies, we found foundation species may modify different biotic or that some invertebrate species are facilitated by each abiotic factors and, hence, support different eco - of these foundation species, but others are facilitated logical communities (Dijkstra et al. 2012). Thus, just only by oysters (Bishop et al. 2012). Hence, it is possi- as the number and functional identity of species in a ble that the effect of the 2 foundation species on community determine ecosystem processes (Cardinale invertebrate richness is independent and additive et al. 2012, Hooper et al. 2012, Naeem et al. 2012), but that one foundation species alters the density- the number and functional identity of co-occurring dependent effects of the other on the abundance of foundation species may determine the richness, com- invertebrates. We conducted a factorial manipulation position, and abundance of the facilitated community of foundation species presence-absence and density (Angelini & Silliman 2014). If multiple foundation to examine how variation within each species influ- species vary substantially in functional traits, then ences the facilitative effects of the other. In addition, there may be little overlap in the composition of spe- we tested the consistency of their effects on the asso- cies that associate with each foundation species ciated community at 2 sites. (Thomsen et al. 2010), leading to additive effects on the diversity and abundance of the associated com- munity. Alternatively, co-occurrence of foundation MATERIALS AND METHODS species may conceivably increase or decrease com- munity richness and/ or abundance because of non- Study system additive synergisms or antagonisms among the foun- dation species or their associates. Within temperate Australian mangrove forests, the The community-level effects of foundation species macroalga Hormosira banksii and the oyster Sac- can also depend on the relative abundance and func- costrea glomerata co-exist at mid-intertidal eleva- tional variation of a given foundation species and not tions among the pneumatophores of the mangrove simply on its presence or absence (Hughes & Sta- Avicennia marina (Bishop et al. 2012). In mangroves, chowicz 2004, Kimbro & Grosholz 2006, Bishop et al. the alga is free living, retained in place by the entan- 2012, 2013, Gribben et al. 2013). In particular, foun- glement of its long thalli of branched chains of vesi- dation species density and/or biomass can have cles among the pneumatophores (Bishop et al. 2012, strong effects on the abundance and richness of asso- 2013). Consequently, its density displays a positive ciated species. Because these same traits are often relationship with the density and height of pneu- highly variable across space and time, it is likely that matophores (Bishop et al. 2012, 2013). Despite this foundation species effects on the community vary reliance of the alga on the pneumatophores, previous across different contexts (Agrawal et al. 2007). How- studies independently manipulating the density of Hughes et al.: Context-dependent effects of foundation species 131 the alga and the pneumatophores have shown that biomass, no H. banksii; (5) low S. glomerata biomass, the effect of the alga on invertebrates overwhelms low H. banksii biomass; (6) low S. glomerata biomass, the direct effects of the pneumatophores on inverte- high H. banksii biomass; (7) high S. glomerata bio- brates (Bishop et al. 2012). The oyster, although also mass, no H. banksii; (8) high S. glomerata biomass, ex hibiting some dependency on pneumatophores as low H. banksii biomass; and (9) high S. glomerata a substrate for attachment (Bishop et al. 2012), also biomass, high H. banksii biomass. The range of bio- forms small aggregations, typically 15 to 25 cm in mass treatments for each of the foundation species diameter, around shell fragments found on the se - was based on the range of variation in their abun- diment surface (M. J. Bishop pers. obs.). Thus, in dance observed in this system (Bishop et al. 2012). contrast to the alga, the small-scale distribution