Relationships between invertebrate benthos, environmental drivers and pollutants at a subcontinental scale

Highlights

• Natural factors chiefly drive small invertebrates at regional biogeographic scales.

• Pollutants have differing impacts on epifaunal and infaunal invertebrates.

• Highly resolved taxonomy is important for detecting pollutant impacts on richness.

• Biomonitoring of pollutants is more efficient if pollutant and fauna specific.

Abstract

Marine ecosystems are structured by an array of natural and anthropogenic drivers, their diverse influences varying between different community types and across space. We assessed consistency in variation in composition and richness for three communities (macro- and meio-faunal communities associated with macroalgae, and soft-sediment infaunal communities) across natural and pollution gradients at the subcontinental scale of southeastern Australia. Community structure varied with natural environmental factors (temperature, wave exposure) and, to a lesser extent, pollutant loads (catchment effects, heavy metals, hydrocarbons and nutrients) across 43 sites spanning 2700 km. The community types showed differing sensitivities to pollutants: algal macrofauna was most strongly associated with hydrocarbon pollution and nutrient loading; algal meiofauna with heavy metals and nutrients; and infauna with catchment effects and nutrients. Different taxonomic resolutions were needed to detect significant pollution relationships for the three community types, indicating that monitoring programmes are most effective if pollutant- and fauna-specific.

Introduction

Multiple local-scale studies describe relationships between abiotic covariates (including pollutants) and temperate reef macrofauna and meiofauna (e.g. Edgar and Barrett, 2000; Pinedo et al., 2007; Yamada et al., 2007). Regional-scale studies are less common, but notably include an investigation of the Adriatic Sea (Balsamo et al., 2010). An important next step is to assess the generality and magnitude of impacts of stressors across broad geographic scales that include multiple coastal environments where pollutants are accumulating in sediments (Chen et al., 2007; Dachs and Méjanelle, 2010; Olsen et al., 1982), and also reef habitats with diverse macroalgal beds (Moy and Walday, 1996; Davis et al., 2003; Ling et al., 2018). A particular challenge in this broad-scale context is to differentiate the strong natural gradients in environmental conditions from influences of the interacting suite of local pollutants that are also present. An understanding of variability in impacts of pollutants in different habitat types is additionally needed.

The Great Southern Reef, the mosaic of temperate rocky reefs spanning five Australian states and their capitals, possesses immense economic and social importance (Bennett et al., 2016). A key characteristic is a high richness of endemic biodiversity that is poorly known relative to tropical reefs (Poore, 1995). As elsewhere, pollution poses a threat to the persistence of this temperate reef biodiversity (Islam and Tanaka, 2004; Ling et al., 2018), including to the habitat-forming macroalgae on which many associated species depend (Airoldi and Beck, 2007). Particularly near large cities, the biogenic habitat-formers and associated reef biota are exposed to a patchy array of pollutants, including heavy metals, toxic organic chemicals, sewage inputs, agricultural runoff, and plastics (Crain et al., 2009; Ling et al., 2018).

Local impacts of pollutants on reefs adjacent to southern Australian capital cities have been investigated in several related studies, including urban impacts on fishes, mobile invertebrates, sessile invertebrates and macroalgae (Fowles et al., 2018a, Fowles et al., 2018b; Stuart-Smith et al., 2015). The presence of microplastic in this region has also been investigated with plastic particles found to be ubiquitous on the seafloor adjacent to rocky reefs (Ling et al., 2017). Overall, the reef communities studied are impacted to different degrees by the wide variety of pollutants present, but show a general transition towards “short and simplified” structural configurations, whereby taxa and habitats become dominated by fewer, smaller species (Ling et al., 2018). Much improved predictive models on pollutant impacts on reef and adjacent soft-sediment depositional zones are nevertheless needed if management is to efficiently respond to the diverse array of threats (Crain et al., 2009).

Macrofaunal and meiofaunal invertebrates comprise poorly studied but abundant and critically important components of benthic ecosystems. These animals range from ~0.125 mm to ~16 mm in body size, and live in association with macroalgae and other habitats on hard surfaces, and in sediments (Edgar, 1983). Although their small size precludes broad public and scientific interest, macrofauna and meiofauna provide an essential link in marine food webs (Edgar and Moore, 1986; Taylor, 1998), and play a crucial role in nutrient cycling (Hutchings, 1998).

Invertebrates in soft sediment (infauna) tend to be more widely investigated than surface-dwelling invertebrates on reefs (epifauna). They have been used as indicator taxa to monitor local environmental impacts on marine systems because standardised samples are relatively easy to collect using remotely deployed sediment grabs, as opposed to requirements for diver-based sampling of reef epifauna. Moreover, many pollutants settle out on the soft-sediment depositional zones, and thereby come into direct contact with infauna (Bryan and Langston, 1992; Ellis et al., 2006; Ling et al., 2018; Wildsmith et al., 2017).

Furthermore, taxonomic resolution is an important element that can influence detection of impacts of environmental and pollutants factors on benthic communities. Although species-level identification might seem ideal, it is costly and time-consuming (Ellis, 1985; Warwick, 1988). Thus, identifying the highest taxonomic rank that can be used to detect community patterns is key to efficiently mapping impacts over large areas (Terlizzi et al., 2003).

Here we examine the distribution of reef epifauna (in macro- and meio-faunal size classes) and nearby infauna in relation to natural environmental and pollution gradients along 2700 km coastal distance around south-eastern mainland Australia and Tasmania. We investigate variability in structure and richness for three different community types (reef macroalgal macrofauna >1 mm; reef macroalgal meiofauna 0.125–1 mm; and adjacent sediment infauna >1 mm) against seventeen different environmental and pollutant covariates grouped into five categories: environmental, catchment effects, heavy metals, hydrocarbons and nutrients. Our investigation thus comprises a natural experiment, where strong associations between covariates and communities are distinguished. Once identified, associations represent priorities for subsequent experimental study to attribute causation.

Specifically, we assess relative effect sizes associated with three hypotheses: (1) To what extent do different natural environmental and pollutant stressors affect faunal communities relative to each other (when assessed using a consistent methodology for the same set of sites across a subcontinental scale)? (2) Are the effects of different pollutants consistent between macrofaunal and meiofaunal communities, and between epifaunal and infaunal communities? (3) How does sorting of samples to different taxonomic resolution affect detection of impacts of pollutants?