New Zealand Aquatic Environment and Biodiversity Report No. 44 2010 ISSN 1176-9440 Isolated and interactive effects of two key species on ecosystem function and trophic linkages in New Zealand soft-sediment habitats A. M. Lohrer L. D. Chiaroni S. F. Thrush J. E. Hewitt Isolated and interactive effects of two key species on ecosystem function and trophic linkages in New Zealand soft-sediment habitats A. M. Lohrer L.D. Chiaroni S. F. Thrush J. E. Hewitt NIWA P O Box 11115 Hillcrest Hamilton 3251 New Zealand Aquatic Environment and Biodiversity Report No. 44 2010 Published by Ministry of Fisheries Wellington 2010 ISSN 1176-9440 © Ministry of Fisheries 2010 Lohrer, A.M.; Chiaroni, L.D.; Thrush, S.F.; Hewitt, J.E.(2010). Isolated and interactive effects of two key species on ecosystem function and trophic linkages in New Zealand soft-sediment habitats. New Zealand Aquatic Environment and Biodiversity Report No. 44. 69 p. This series continues the Marine Biodiversity Biosecurity Report series which ceased with No. 7 in February 2005. EXECUTIVE SUMMARY Lohrer, A.M.; Chiaroni, L.D.; Thrush, S.F.; Hewitt, J.E. (2010) Isolated and interactive effects of two key species on ecosystem function and trophic linkages in New Zealand soft-sediment habitats. New Zealand Aquatic Environment and Biodiversity Report 44. 69 p. The objective of this project was to better characterise and quantify marine ecosystem functioning in New Zealand soft-sediment habitats. Experiments involved manipulations of ―ecosystem engineers‖, key species that are known to influence a variety of sedimentary rates and processes. Manipulations of two key species (horse mussels, Atrina zelandica, and burrowing urchins, Echinocardium cordatum) were used to shift functioning in localised areas of soft-sediment habitat. Changes in local benthic biodiversity and trophic relationships were then quantified. Three experimental sites in Mahurangi Harbour, where the densities of Atrina and Echinocardium were inversely correlated, were examined during a 2.5 year period. The chief finding was the drastic shift in soft-sediment habitat characteristics associated with gradients in the density of the burrowing urchins. Using density manipulations in well replicated experiments at multiple sites, we found consistent and sharp changes in sediment characteristics that occurred at densities of about 10 urchins m-2. Sediment characteristics often differed significantly in magnitude and variability across this critical density threshold. Atrina shells tended to facilitate rare taxa and small sedentary species, increasing total macrofaunal abundance and richness. Echinocardium had negative effects on macrofauna abundance and richness, and only large mobile species seemed to survive well in its presence. Theora lubrica, the most common individual macrofaunal species in our experiments, was positively associated with Atrina at the site and experimental plot level. Theora thrives in organically enriched sediments, and Atrina is known to enhance sediment organic content via biodeposition. However, Theora was negatively correlated with Echinocardium in three separate experiments. The constant reworking of sediment by Echinocardium reduced Theora’s success, as the small surface-oriented bivalve apparently requires stable sediments in order to keep its short feeding siphon above the sediment-water interface. Internal dynamics within the sediment column appeared to be important in Echinocardium-dominated habitats, where fresh food particles were locally produced by microphytes living at the sediment water interface. Echinocardium affects microphyte production via two competing density-dependent processes: Echinocardium grazes microphytes, but also stimulates microphyte growth by excreting nutrients and bioturbating the sediment (releasing nutrients from sediment pore-waters). Thus, organic matter is turned over rapidly in the Echinocardium dominated sediments. Water column dynamics appear to be important in Atrina dominated habitats. Analysis of sediment pigment ratios indicated a greater presence of detrital particles in Atrina beds, probably derived from settling or bio-deposited phytoplankton. Sediment chlorophyll a content and total pigments increased at Atrina sites during the summer, the season when water column phytoplankton stocks (and inputs of phytodetritus) are typically highest. In summary, we documented important interactive effects two key species in New Zealand soft- sediment habitats. The two species appear to have very different functional roles, and their interactions were generally antagonistic; Atrina tended to have negative effects on chlorophyll a content and positive effects on macrofauna, whereas Echinocardium tended to inhibit macrofauna and promote benthic primary producers. Although Atrina and Echinocardium can co-occur, their densities are often non-overlapping. Protection of these two key species to maintain a more diverse set of ecological functions must involve conservation at the habitat, estuary and coastal ecosystem level. 3 1. INTRODUCTION Marine soft-sediment habitats interact with overlying seawater through benthic-pelagic linkages, and figure prominently in biogeochemical cycles and global elemental budgets (Snelgrove 1999, Austen et al. 2002, Thrush & Dayton 2002). Although the role of biota in the functioning of soft-sediment ecosystems is recognised in a general sense—we know that bioturbators and other structure-forming ―ecosystem engineers‖ (Jones et al. 1994) are important components of the system—ecosystem function is a complex concept, and there is no single type of measurement that can be used to capture and quantify all aspects of ecosystem performance. The goal of this project was to complete a set of integrated experiments where up to 10 parameters corresponding to ecosystem functioning in subtidal soft-sediment habitats could be measured. We manipulated the densities of key benthic species to produce significant changes in functioning in localised areas and measured responses in well replicated experimental treatments. The first year (Specific Objective 1) was focused on key bioturbators in New Zealand’s subtidal soft- sediment systems. Infaunal urchins of the genus Echinocardium constantly rework surface sediment by burrowing through it (Lohrer et al. 2005). In previous experiments, we demonstrated how bioturbation by Echinocardium releases nutrients from the sediment, enhancing primary production by microphytes such as benthic diatoms (Lohrer et al. 2004). Although the positive effects of Echinocardium on food resources and oxygen concentrations in the sediment column may benefit some co-occurring macroinvertebrates, the constant destabilisation of sediment may harm other species that must maintain contact with the sediment-water interface. These longer-term impacts— changes in sediment characteristics, microalgal biomass, and concomitant changes in macroinvertebrate abundance and diversity—are the principal focus of this project. The second and third years (Specific Objectives 2 and 3) were focused on interactions between two key species, Echinocardium and Atrina zelandica. Atrina is a large suspension-feeding bivalve that remains stationary in soft-sediment habitats, protruding 5-15 cm into the overlying bottom water. Atrina creates biogenic structure (i.e., hard substrate and vertical relief) in soft-sediment habitats, and can influence bottom water flow and turbulence (Green et al. 1998). The faeces and pseudofaeces produced by Atrina, known as biodeposits, tend to enrich surrounding sediments with organic matter, providing food for macrofauna and increasing macrofaunal abundance and diversity (Norkko et al. 2001, Hewitt et al. 2006). Thus the roles of Atrina and Echinocardium appear to be starkly contrasting. The effect of the two species in combination was not known and was investigated here. We chose to examine intact soft-sediment habitats in the field to encompass a variety of natural environmental drivers, but used manipulative experimental approaches to more clearly distinguish cause and effect. The response variables we measured were not necessarily independent, as direct and indirect feedbacks are common in sediment systems. However, each variable related to ecosystem functioning either directly or indirectly. For example, we measured sediment chlorophyll a content— a metric of microalgal standing stock—because of its relationship with a commonly used index of ecosystem functioning, primary production (Tilman et al. 1996, 2001, Hector et al. 1999). However, the concept of ―multi-functionality‖ is increasingly recognised, with the understanding that no single index of functioning can adequately capture the varied contributions of biodiversity (Hector & Bagchi 2007, Stachowicz et al. 2007). It is for this reason that we chose to measure multiple interrelated parameters. Finally, by manipulating the densities of key engineering species, we were better positioned to understand the drivers of significant shifts in functioning and could compare the influences of the two key species using common currencies. The two key species that we investigated are each widely distributed in estuarine, coastal, and shelf ecosystems throughout New Zealand (Ellis et al. 2000, Lohrer et al. 2005). Atrina is found across a range of muddy to sandy sediments, from the shallow subtidal to a depth of about 40 m. These bivalves have been reported from Stewart Island to Northland, with remnants of extensive beds known 4 to exist in the Nelson-Marlborough region