Abstract
As global change alters multiple environmental conditions, predicting species’ responses can be challenging without understanding how each environmental factor influences organismal performance. Approaches quantifying mechanistic relationships can greatly complement correlative field data, strengthening our abilities to forecast global change impacts. Substantial salinity increases are projected in the San Francisco Estuary, California, due to anthropogenic water diversion and climatic changes, where the critically endangered delta smelt (Hypomesus transpacificus) largely occurs in a low‐salinity zone (LSZ), despite their ability to tolerate a much broader salinity range. In this study, we combined molecular and organismal measures to quantify the physiological mechanisms and sublethal responses involved in coping with salinity changes. Delta smelt utilize a suite of conserved molecular mechanisms to rapidly adjust their osmoregulatory physiology in response to salinity changes in estuarine environments. However, these responses can be energetically expensive, and delta smelt body condition was reduced at high salinities. Thus, acclimating to salinities outside the LSZ could impose energetic costs that constrain delta smelt's ability to exploit these habitats. By integrating data across biological levels, we provide key insight into the mechanistic relationships contributing to phenotypic plasticity and distribution limitations and advance the understanding of the molecular osmoregulatory responses in nonmodel estuarine fishes.
Highlights
Current and forecasted shifts in environmental conditions due to human activities are changing the sources, strengths and directions of selective pressures for organisms globally (Rice and Emery 2003)
Our data demonstrate that delta smelt have the capacity for coordinated molecular responses to effectively osmoregulate and regain homeostasis across a broad range of salinities
At the highest salinity (34.0 ppt), fish displayed reduced body condition even with unlimited food resources, and functional analyses identified that lipid, protein, and carbohydrate metabolism played major roles in delta smelt’s compensatory responses to salinity stress outside the low-salinity zone (LSZ) conditions. These findings align with theoretical models and empirical evidence in other species showing that osmoregulatory processes are energetically expensive (Morgan and Iwama 1991; Boeuf and Payan 2001; Ku€ltz 2015), and that such environmental stress can impose sublethal costs due to the additional energy needed to recover and maintain homeostasis (Calow and Forbes 1998; Sokolova et al 2012)
Summary
Current and forecasted shifts in environmental conditions due to human activities are changing the sources, strengths and directions of selective pressures for organisms globally (Rice and Emery 2003). In the San Francisco Estuary ecosystem (SFE; California, USA), in addition to strong natural tidal influences, salinity gradients are affected by both direct (e.g., freshwater diversion and flow regulation; Lund et al 2010) and indirect anthropogenic activities (e.g., climate change induced heightened saltwater intrusion from sea-level rise and reduced snowpack leading to diminished freshwater flows; Cloern et al 2011; Cloern and Jassby 2012) Despite these complexities, salinity is a key abiotic factor limiting aquatic organisms (Nicol 1967), and it is critical to examine species’ responses to salinity changes to understand biological impacts under different global change scenarios
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