Environmental metabolomics as an ecological indicator: Metabolite profiles in juvenile fish discriminate sites with different nursery habitat qualities

Abstract Estuarine habitats contribute disproportionately as nursery habitats for marine fish, yet are amongst the most anthropogenically degraded ecosystems on Earth. Juvenile fish growing in urbanised estuarine habitats are subject to a mosaic of stressors, thus development of higher resolution methods to gain a more complete assessment of fish responses is vital. Accordingly, this study provides the first assessment of metabolomic profiling as a new bioindicator of habitat quality for juvenile fish. We matched traditional bioindicator methods (fish growth rates) with metabolomic profiles in juvenile snapper (Chrysophrys auratus), a culturally and commercially important species across Australia and New Zealand. Juvenile snapper were collected from, and within, harbour sites occupying a gradient in turbidity, a significant stressor for this species that is known to result in reduced weight, mortality and deleterious physiological responses. We found that fish growth assessed using otolith increments was not reflective of the turbidity gradient with little discrimination among sites. However, metabolomic profiling was highly sensitive and reproducible, with 100% accuracy in discriminating fish from harbours with differing turbidity. These differences in metabolic profiles were largely driven by metabolites and pathways involved in energy production, processes of growth, or the immune response. In particular, the amino acids Cysteine and 4-aminobutyric acid (GABA), linked to growth and development in snapper, were elevated in juveniles from more pristine harbours, and offer promising candidates for use as a biomarker of habitat quality in this species. Thus, we show that metabolomic approaches can uncover site differences that traditional and more coarse methods were unable to detect. This work provides a novel baseline for the use of metabolomic profiling on wild-caught snapper to inform management and conservation decisions, with the potential to identify biomarkers reflective of habitat quality.