Nicole A. Hill

Integrating abundance and functional traits reveals new global hotspots of fish diversity

Species richness has dominated our view of global biodiversity patterns for centuries. The dominance of this paradigm is reflected in the focus by ecologists and conservation managers on richness and associated occurrence-based measures for understanding drivers of broad-scale diversity patterns and as a biological basis for management. However, this is changing rapidly, as it is now recognized that not only the number of species but the species present, their phenotypes and the number of individuals of each species are critical in determining the nature and strength of the relationships between species diversity and a range of ecological functions (such as biomass production and nutrient cycling). Integrating these measures should provide a more relevant representation of global biodiversity patterns in terms of ecological functions than that provided by simple species counts. Here we provide comparisons of a traditional global biodiversity distribution measure based on richness with metrics that incorporate species abundances and functional traits. We use data from standardized quantitative surveys of 2,473 marine reef fish species at 1,844 sites, spanning 133 degrees of latitude from all ocean basins, to identify new diversity hotspots in some temperate regions and the tropical eastern Pacific Ocean. These relate to high diversity of functional traits amongst individuals in the community (calculated using Rao’s Q), and differ from previously reported patterns in functional diversity and richness for terrestrial animals, which emphasize species-rich tropical regions only. There is a global trend for greater evenness in the number of individuals of each species, across the reef fish species observed at sites (‘community evenness’), at higher latitudes. This contributes to the distribution of functional diversity hotspots and contrasts with well-known latitudinal gradients in richness. Our findings suggest that the contribution of species diversity to a range of ecosystem functions varies over large scales, and imply that in tropical regions, which have higher numbers of species, each species contributes proportionally less to community-level ecological processes on average than species in temperate regions. Metrics of ecological function usefully complement metrics of species diversity in conservation management, including when identifying planning priorities and when tracking changes to biodiversity values.

PHYLOGENETIC AND GEOGRAPHIC VARIATION IN HOST BREADTH AND COMPOSITION BY HERBIVOROUS AMPHIPODS IN THE FAMILY AMPITHOIDAE

Abstract Predicting the host range for herbivores has been a major aim of research into plant–herbivore interactions and an important model system for understanding the evolution of feeding specialization. Among many terrestrial insects, host range is strongly affected by herbivore phylogeny and long historical associations between particular herbivore and plant taxa. For small herbivores in marine environments, it is known that the evolution of host use is sculpted by several ecological factors (e.g., food quality, value as a refuge from predators, and abiotic forces), but the potential for phylogenetic constraints on host use remains largely unexplored. Here, we analyze reports of host use of herbivorous amphipods from the family Ampithoidae (102 amphipod species from 12 genera) to test the hypotheses that host breadth and composition vary among herbivore lineages, and to quantify the extent to which nonpolar secondary metabolites mediate these patterns. The family as a whole, and most individual species, are found on a wide variety of macroalgae and seagrasses. Despite this polyphagous host use, amphipod genera consistently differed in host range and composition. As an example, the genus Peramphithoe rarely use available macrophytes in the order Dictyotales (e.g., Dictyota) and as a consequence, display a more restricted host range than do other genera (e.g., Ampithoe, Cymadusa, or Exampithoe). The strong phylogenetic effect on host use was independent of the uneven distribution of host taxa among geographic regions. Algae that produced nonpolar secondary metabolites were colonized by higher numbers of amphipod species relative to chemically poor genera, consistent with the notion that secondary metabolites do not provide algae an escape from amphipod herbivory. In contrast to patterns described for some groups of phytophagous insects, marine amphipods that use chemically rich algae tended to have broader, not narrower, host ranges. This result suggests that an evolutionary advantage to metabolite tolerance in marine amphipods may be that it increases the availability of appropriate algal hosts (i.e., enlarges the resource base).

A Standardised Vocabulary for Identifying Benthic Biota and Substrata from Underwater Imagery: The CATAMI Classification Scheme

Imagery collected by still and video cameras is an increasingly important tool for minimal impact, repeatable observations in the marine environment. Data generated from imagery includes identification, annotation and quantification of biological subjects and environmental features within an image. To be long-lived and useful beyond their project-specific initial purpose, and to maximize their utility across studies and disciplines, marine imagery data should use a standardised vocabulary of defined terms. This would enable the compilation of regional, national and/or global data sets from multiple sources, contributing to broad-scale management studies and development of automated annotation algorithms. The classification scheme developed under the Collaborative and Automated Tools for Analysis of Marine Imagery (CATAMI) project provides such a vocabulary. The CATAMI classification scheme introduces Australian-wide acknowledged, standardised terminology for annotating benthic substrates and biota in marine imagery. It combines coarse-level taxonomy and morphology, and is a flexible, hierarchical classification that bridges the gap between habitat/biotope characterisation and taxonomy, acknowledging limitations when describing biological taxa through imagery. It is fully described, documented, and maintained through curated online databases, and can be applied across benthic image collection methods, annotation platforms and scoring methods. Following release in 2013, the CATAMI classification scheme was taken up by a wide variety of users, including government, academia and industry. This rapid acceptance highlights the scheme’s utility and the potential to facilitate broad-scale multidisciplinary studies of marine ecosystems when applied globally. Here we present the CATAMI classification scheme, describe its conception and features, and discuss its utility and the opportunities as well as challenges arising from its use.

Beyond the bed: Effects of metal contamination on recruitment to bedded sediments and overlying substrata

Metal-contaminated sediments pose a recognised threat to sediment-dwelling fauna. Re-mobilisation of contaminated sediments however, may impact more broadly on benthic ecosystems, including on diverse assemblages living on hard substrata patches immediately above sediments. We used manipulative field experiments to simultaneously test for the effects of metal contamination on recruitment to marine sediments and overlying hard substrata. Recruitment to sediments was strongly and negatively affected by metal contamination. However, while assemblage-level effects on hard-substratum fauna and flora were observed, most functional groups were unaffected or slightly enhanced by exposure to contaminated sediments. Diversity of hard-substratum fauna was also enhanced by metal contamination at one site. Metal-contaminated sediments appear to pose less of a hazard to hard-substratum than sediment-dwelling assemblages, perhaps due to a lower direct contaminant exposure or to indirect effects mediated by contaminant impacts on sediment fauna. Our results indicate that current sediment quality guidelines are protective of hard-substrata organisms.

Contaminated suspended sediments toxic to an Antarctic filter feeder: Aqueous‐ and particulate‐phase effects

Disturbances such as dredging, storms, and bioturbation result in the resuspension of sediments. This may affect sessile organisms that live on hard substrates directly above the sediment. Localized sediment contamination exists around many Antarctic research stations, often resulting in elevated contamination loads in marine sediments. To our knowledge, the potential impact of resuspended contaminated sediments on sessile fauna has not been considered, so in the present study, we assessed the sensitivity of Antarctic spirorbid polychaetes to aqueous metals and to metal-contaminated sediments that had been experimentally resuspended. Worms were first exposed to aqueous metals, both singly and in combination, over 10 d. Spirorbid mortality was tolerant to copper (median lethal concentration [LC50], 570 microg/L), zinc (LC50, > 4,910 microg/L), and lead (LC50, > 2,905 microg/L); however, spirorbid behavior responded to copper concentrations as low as 20 microg/L. When in combination, zinc significantly reduced mortality caused by copper. A novel technique was used to resuspend sediments spiked with four concentrations of three metals (up to 450 microg/g dry wt of copper, 525 micro/g dry wt of lead, and 2,035 microg/g dry wt of zinc). The response of spirorbids to unfiltered suspended sediment solutions and filtered solutions (aqueous metal exposure) was measured. Suspended sediments were toxic to filter-feeding spirorbids at concentrations approximating those found in contaminated Antarctica areas. Toxicity resulted both from aqueous metals and from metals associated with the suspended sediments, although suspended clean sediments had no impact. To our knowledge, the present study is the first to show that resuspension of contaminated sediments can be an important pathway for toxicity to Antarctic hard substrate organisms. Based on the present results, current sediment-quality guidelines used in the evaluation of Australian sediments may be applicable to Antarctic ecosystems.

Quantifying Fish Assemblages in Large, Offshore Marine Protected Areas: An Australian Case Study

As the number of marine protected areas (MPAs) increases globally, so does the need to assess if MPAs are meeting their management goals. Integral to this assessment is usually a long-term biological monitoring program, which can be difficult to develop for large and remote areas that have little available fine-scale habitat and biological data. This is the situation for many MPAs within the newly declared Australian Commonwealth Marine Reserve (CMR) network which covers approximately 3.1 million km2 of continental shelf, slope, and abyssal habitat, much of which is remote and difficult to access. A detailed inventory of the species, types of assemblages present and their spatial distribution within individual MPAs is required prior to developing monitoring programs to measure the impact of management strategies. Here we use a spatially-balanced survey design and non-extractive baited video observations to quantitatively document the fish assemblages within the continental shelf area (a multiple use zone, IUCN VI) of the Flinders Marine Reserve, within the Southeast marine region. We identified distinct demersal fish assemblages, quantified assemblage relationships with environmental gradients (primarily depth and habitat type), and described their spatial distribution across a variety of reef and sediment habitats. Baited videos recorded a range of species from multiple trophic levels, including species of commercial and recreational interest. The majority of species, whilst found commonly along the southern or south-eastern coasts of Australia, are endemic to Australia, highlighting the global significance of this region. Species richness was greater on habitats containing some reef and declined with increasing depth. The trophic breath of species in assemblages was also greater in shallow waters. We discuss the utility of our approach for establishing inventories when little prior knowledge is available and how such an approach may inform future monitoring efforts within the CMR network.

Predictions of beta diversity for reef macroalgae across southeastern Australia

We analyzed and predicted spatial patterns of turnover in macroalgal community composition (beta diversity) that accounted for broad-scale environmental gradients using two contrasting community modelling methods, Generalised Dissimilarity Modelling (GDM) and Gradient Forest Modelling (GFM). Percentage cover data from underwater macroalgal surveys of subtidal rocky reefs along the southeastern coastline of continental Australia and northern coastline of Tasmania were combined with 0.018-resolution gridded environmental variables, to develop statistical models of beta diversity. GDM, a statistical approach based on a matrix regression, and GFM, a machine learning approach based on ensemble tree based methods, were used to fit models and generate predictions of beta diversity within unsurveyed areas across the region of interest. Patterns of macroalgal beta diversity predicted by both methods were remarkably congruent and showed a similar and striking change in community composition from eastern South Australia to western Victoria and northern Tasmania. Macroalgal communities differed markedly in predicted composition between the open coast and inshore locations. A distinct algal community was predicted for the enclosed Port Philip Bay in Victoria. Sea surface temperature standard deviation and average contributed most to changes in beta diversity for both the GDM and GFM models; changes in wave exposure and oxygen also influenced beta diversity in the GDM model, while salinity and exposure contributed substantially to the GFM model. The GDM and GFM analyses allowed us to model and predict spatial patterns of beta diversity in macroalgal communities comprising .180 species over 6600 km of coastline. These outputs advance regional-scale conservation management by allowing planners to interpolate from point source ecological data to assess the distribution of biodiversity across their full domain of interest. The congruence betweenmethods suggests that strong environmental gradients related to temperature and exposure are the common drivers of community change in this region.

Loss of native rocky reef biodiversity in Australian metropolitan embayments.

Urbanisation of the coastal zone represents a key threat to marine biodiversity, including rocky reef communities which often possess disproportionate ecological, recreational and commercial importance. The nature and magnitude of local urban impacts on reef biodiversity near three Australian capital cities were quantified using visual census methods. The most impacted reefs in urbanised embayments were consistently characterised by smaller, faster growing species, reduced fish biomass and richness, and reduced mobile invertebrate abundance and richness. Reef faunal distribution varied significantly with heavy metals, local population density, and proximity to city ports, while native fish and invertebrate communities were most depauperate in locations where invasive species were abundant. Our study adds impetus for improved urban planning and pollution management practises, while also highlighting the potential for skilled volunteers to improve the tracking of changes in marine biodiversity values and the effectiveness of management intervention.

Choosing between strategies for designing surveys: autonomous underwater vehicles

Autonomous underwater vehicles (AUV), which collect images of marine habitats, are now an established sampling tool. The use of AUVs is becoming more widespread as they offer a non-destructive method to survey substantial spatial areas. The design of AUV surveys has historically been based on expert knowledge andAUVspecific considerations, such as reducing geolocation error. The expert knowledge encompasses intuition, previous surveying experiences and holistic knowledge of the study region. 2. We investigate the statistical aspects to AUV survey design for estimation of percentage cover of key benthic biota. We investigate the presence of spatial autocorrelation in AUV data using model-based geostatistics and examine the effect of autocorrelation on survey design by examining different design strategies – methods for placing AUV transects. The design strategies are assessed by inspecting the expected bias and the expected standard deviation ofmodel predictions, where the model depends on the choice of design. 3. The AUV data exhibited a wide range of autocorrelation, from non-existent to substantial. The design strategies varied in their statistical performance and nearly all strategies had shortcomings. Design strategies that were consistently poor performers had (i) transects placed in parallel in a single spatial dimension and (ii) made no attempt to spread out the transects in space. The superior design types had more transect-to-transect separation (but not toomuch) and effectively spanned important covariates. 4. The results give guidelines to researchers designing AUV surveys for biological mapping and for monitoring. In particular, we demonstrate that any spatial design should seek spatial balance, such as would be introduced by a systematic or stratified component within a randomized design. Knowledge of the system under study should be incorporated and, if possible, should be done so in a formalmanner that is objective and repeatable.

Physico-chemical changes in metal-spiked sediments deployed in the field: Implications for the interpretation of in situ studies

Manipulative field studies are useful for investigating cause-effect relationships between contamination and benthic community health. However, there are many challenges for creating environmentally relevant exposures and determining what measurements are necessary to correctly interpret the results. This study describes the physical and chemical changes in the properties of metal-spiked marine sediments deployed in four different locations for up to 11 months. The test sediments lost between 20% and 75% of their volume during the deployment period, with the greatest losses occurring at sites affected by strong hydrodynamic activity. More sediment was lost from clean treatments than those spiked with high metal concentrations and corresponded with differential recruitment of infauna to these treatments. In general, a greater proportion of spiked-metals remained at lower energy sites (48-85%) than at higher energy sites (15-48%). The decreased metal concentrations were attributed mostly to the loss of the metal-spiked sediments (through resuspension) and their dilution with sediments depositing from the surrounding environment. A range of recommendations are made for optimising the information gained from field-based studies using metal-spiked sediments. These include the careful documentation of physico-chemical sediment properties pre- and post-deployment, the use of co-located sediment traps and knowledge of site-specific hydrodynamic processes.