Metabolic responses of the Nereid polychaete, Alitta succinea, to hypoxia at two different temperatures

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Highlights

  • We assess physiological tolerance to hypoxia of A. succinea, a key bioturbator.

  • succinea is an efficient oxyregulator with critical O2 saturations as low as 10%.

  • Hypoxia mutes the temperature–metabolism relationship.

  • Significant effect of hypoxia on the mass–metabolism relationship of A. succinea.

Abstract

Coastal hypoxia has detrimental effects to community ecology, degrading community structure and diminishing benthic function. Benthic function is largely driven by infauna bioturbation, which facilitates life-supporting processes by increasing the quality of marine sediments for nearly all biota. These infauna-mediated processes are diminished by coastal hypoxia. However, some infauna have been documented to exhibit metabolic plasticity to low oxygen allowing them to maintain some form of benthic function. Of particular interest to this study is the Nereid polychaete Alitta succinea. Stopflow respirometry was used to assess the hypoxic tolerance of A. succinea, by quantifying resting metabolic rate (VO2 ), critical oxygen saturation (i.e. the oxygen level below which worms could not maintain aerobic metabolism), and the oxyregulation ability at an acclimation temperature (25 °C) and after an acute temperature increase (to 30 °C). The acute Q10 during normoxia was 4.6, though this effect of temperature on VO2 was completely muted during hypoxia with a Q10 of 1. Compared among other polychaetes, A. succinea was the most efficient at oxyregulation, resulting in low critical oxygen saturation levels of 16% and 10% at 25 and 30 °C, respectively. Finally, there was a significant effect of hypoxia on the mass metabolism relationship of A. succinea. Oxygen consumption rates were significantly higher during hypoxia only for smaller A. succinea, suggesting a physiological size selection for hypoxia response. These findings demonstrate the significant effect of hypoxia on A. succinea metabolism, but also provide the metabolic justification for survival of this infaunal worm during severe hypoxia.

Introduction

High human densities in coastal areas have adverse effects for marine systems (Mee, 2012, Vitousek et al., 1997); urbanization and agricultural activity along coastal river drainages results in fertilization of the marine environment, causing eutrophication (Nixon, 1995). The visible response to eutrophication is a greening of the water, as phytoplankton and aquatic vegetation directly respond to nutrient input (Rabalais, 2002); a more serious concern is the unseen decline in bottom-water dissolved oxygen (DO). Excess production from phytoplankton settles to the bottom and is heterotrophically consumed, primarily by microbes, adding to DO consumption in bottom-waters (Rabalais et al., 2010, Turner et al., 2012). This depletion is exacerbated in stratified water bodies where surface DO does not reach the bottom and hypoxia can develop (Levin et al., 2009).

Hypoxia affects marine systems globally (Diaz and Rosenberg, 2008), degrading benthic community structure and quality, and diminishing benthic function and services (Steckbauer et al., 2011). Coastal hypoxia, a shortage in DO concentrations, is difficult to define, as different taxonomic groups, body sizes, and skeletal types have varying oxygen tolerances and thresholds (Diaz and Rosenberg, 1995, Vaquer-Sunyer and Duarte, 2008). A meta-analysis found that sublethal effects were elicited in benthic invertebrates at a median DO concentration of 2.13 mg O2 l 1 (Vaquer-Sunyer and Duarte, 2008). Coastal hypoxia is often defined as DO concentrations ≤ 2 mg O2 l 1 or ~ 24% O2 saturation at 25 °C (Diaz and Rosenberg, 2008, Murphy et al., 2011, Turner et al., 2012), and this is the classification used in this study.

Benthic systems exhibit a predictable and graded series of responses to hypoxia (Rabalais et al., 2010). At the initial onset organisms increase respiration (Wannamaker and Rice, 2000), and mobile fauna migrates from the area (Ludsin et al., 2009, Seitz et al., 2009). As DO further declines, sessile fauna ceases feeding and decreases activities not related to respiration (Diaz and Rosenberg, 1995). Infauna migrate closer to the sediment surface as reduced compounds accumulate (Vaquer-Sunyer and Duarte, 2010), and have been observed on or extending above the sediment surface in a moribund condition (Long et al., 2008, Sturdivant et al., 2012). Finally, if the duration of hypoxia is sustained, mass mortality occurs in all but the most tolerant of species (Diaz and Rosenberg, 1995, Levin et al., 2009). This succession is largely dependent on the persistence of hypoxia, which can last from a few hours to a few months (Diaz and Rosenberg, 1995).

The degradation in benthic community structure is of particular concern regarding infauna. Infauna are relatively sessile, and therefore susceptible to changes in the surrounding environment. They hold ecological importance as a major energetic link between primary producers and higher consumers (Diaz and Schaffner, 1990), such as epibenthic predators including demersal fish (Nilsen et al., 2006). However, an important function infauna serve in marine systems is through bioturbation (Rhoads and Boyer, 1982), the biological displacement or mixing of sediments (Solan et al., 2003). Infauna bioturbation facilitates life-supporting processes by increasing the quality of marine sediments for nearly all biota (Meysman et al., 2006). Sediment permeability, chemical gradients in pore water, remineralization, and inorganic nutrient efflux are a few of the sediment properties and functions regulated by infauna bioturbation (Lohrer et al., 2004). Additionally, given that most pollutants that enter estuaries and coastal bays are particle reactive and bind to sediment particles (Olsen et al., 1982), the level of bioturbation plays a key role in distributing and sequestering pollutants within the sediment (e.g. McMurtry et al., 1985, Sherwood et al., 2002, Stull et al., 1996).

Most studies assessing the effect of hypoxia on the benthic environment show that hypoxia retards benthic community structure and function (Rakocinski, 2012, Sturdivant et al., 2013, van Colen et al., 2010), and predict a cessation in infauna activity during severe hypoxia (Vaquer-Sunyer and Duarte, 2008), which stymies bioturbation. This is largely due to the relationship between DO concentration and infauna metabolic rate (Shumway, 1979), where infauna decrease activity and depress their metabolism in a low DO environment (Diaz and Rosenberg, 1995). However, recent observations by Sturdivant et al. (2012) documented some infauna to be surprisingly active during severe hypoxia, indicating physiological adaptations for some species to not just survive hypoxic events, but maintain some benthic function through bioturbaton. It has been suggested that some marine infauna may exhibit metabolic plasticity to hypoxia (Gonzalez and Quiñones, 2000, Schӧttler, 1979). Of particular interest to this study is the Nereid polychaete, Alitta succinea.

A. succinea is a cosmopolitan species that inhabits littoral and sublittoral sediments in temperate and tropical regions globally (Zenkevich, 1951). Nereids typically live in relatively permanent U-shaped or branching burrows in mud or sand, and often reach very high densities in intertidal areas (Kristensen, 1981). Previous work has documented the importance that Nereids have on sediment processes (Cuny et al., 2007, Papaspyrou et al., 2010, Pischedda et al., 2008), and described Nereid physiology in relation to O2 uptake, O2–CO2 exchange, O2–NO3 exchange, PH4 regeneration, and oxygen heterogeneity in burrows (Kristensen, 1981, Kristensen, 1985, Kristensen, 1989, Pischedda et al., 2012, Swan et al., 2007). Some members of the family Nereidae are known to be facultative anaerobes (Schӧttler, 1979), and in Chesapeake Bay A. succinea populations are characterized by their population level resiliency to hypoxia (Sagasti et al., 2001). With the exception of Kristensen (1983), little to no information is available regarding metabolic or respiratory responses of A. succinea to hypoxia, but previous physiology studies on polychaetes in the family Nereidae suggest a pattern of oxygen-conformity (Kristensen, 1983, Shumway, 1979). Given the observation of A. succinea activity in an area of Chesapeake Bay experiencing DO < 0.5 mg O2 l 1 over a multi-week period (Sturdivant et al., 2012), assessments of basic metabolic requirements, critical oxygen levels, and concomitant oxyregulation are necessary for understanding the hypoxia tolerance of A. succinea. This study investigated changes in metabolic rate, critical oxygen levels, and oxyregulation of A. succinea exposed to acute hypoxia (~ 24 h) at two temperatures. More specifically, the effects of hypoxia on resting metabolic rate (VO2 ), critical oxygen saturation (Scrit), and oxyregulation (K1/K2) were measured at the worm's acclimation temperature (25 °C) and after an acute temperature increase (to 30 °C).

Section snippets

Study organism

A. succinea (25–350 mg wet-weight) were collected from the upper Haulover, near the Virginia Institute of Marine Science Eastern Shore Laboratory (ESL), Wachapreague Virginia, USA. At low tide, A. succinea were collected near adjacent oyster reefs via sediment grabs and careful sieving, and held in buckets with ambient sediment and water for transport back to the lab. Once back at the lab the worms were kept for the duration of the experiment in a 1 m2 aquarium fed by filtered seawater. Because

Response to acute temperature change at normoxia

The values of VO2 increased significantly at the higher temperature during normoxia (df = 21, p = 0.009, T =  2.86). The acute Q10 value for VO2 at normoxia was 4.6.

Response to hypoxia at two temperatures

The relationship between mass and metabolism was represented on a log–log scale. There was a significant effect of mass (F = 35.26, p < 0.0005), oxygen condition (F = 71.93, p < 0.0005), and temperature (F = 40.93, p < 0.0005) on O2 uptake rate (Fig. 3). There was no significant oxygen condition by temperature interaction. O2 uptake rate was higher at

Response to acute temperature change

Temperature is an important physical property of the environment that measures the motion and kinetic energy of molecules (Gillooly et al., 2001). The effect of temperature on metabolism has been documented for more than a century (Boltzmann, 1872, Arrhenius, 1889), and in our study an acute increase in temperature during normoxia resulted in significant changes in VO2 similar to those observed in other polychaetes (Shumway, 1979). The temperature related increase in VO2 (acute Q10 during

Acknowledgments

Supported in part by NSF funded OCE-PRF and Duke University Marine Lab funded Joseph S. Ramus Endowment to S.K.S. We also thank D. Forward for a helpful critique and critical discussions. [SS]

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