Metabolic responses of the Nereid polychaete, Alitta succinea, to hypoxia at two different temperatures
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]
References (83)
Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms
Aquat. Toxicol.
(1992)Oxygen consumption by three species of lamellimbranch mollusc in declining ambient oxygen tension
Comp. Biochem. Physiol.
(1971)- et al.
Studies on the respiration of the polychaete Ophelia bicornis
Comp. Biochem. Physiol.
(1980) - et al.
Economies of scaling: more evidence that allometry of metabolism is linked to activity, metabolic rate and habitat
J. Exp. Mar. Biol. Ecol.
(2013) - et al.
Influence of bioturbation by the polychaete Nereis diversicolor on the structure of bacterial communities in oil contaminated coastal sediments
Mar. Pollut. Bull.
(2007) - et al.
Pyruvate oxidoreductases involved in glycolytic anaerobic metabolism of polychaetes from the continental shelf off central-south Chile
Estuar. Coast. Shelf Sci.
(2000) - et al.
Behavioral effects of low dissolved oxygen on the bivalve Macoma balthica
J. Exp. Mar. Biol. Ecol.
(2008) Between the devil and the deep blue sea: the coastal zone in an era of globalisation
Estuar. Coast. Shelf Sci.
(2012)- et al.
Bioturbation: a fresh look at Darwin's last idea
Trends Ecol. Evol.
(2006) - et al.
Pollutant-particle associations and dynamics in coastal marine environments: a review
Mar. Chem.
(1982)
The influence of infaunal (Nereis diversicolor) abundance on degradation of organic matter in sandy sediments
J. Exp. Mar. Biol. Ecol.
Evaluating macrobenthic process indicators in relation to organic enrichment and hypoxia
Ecol. Ind.
Effects of periodic hypoxia on mortality, feeding, and predation in an estuarine epifaunal community
J. Exp. Mar. Biol. Ecol.
A comparattve study of respiration in two tropical marine polychaetes
Comp. Biochem. Physiol.
Broad-scale effects of hypoxia on benthic community structure in Chesapeake Bay, USA
J. Exp. Mar. Biol. Ecol.
Prediction of the fate of DDT in sediments on the Palos Verdes margin
Cont. Shelf Res.
The effects of body size, oxygen tension and mode of life on the oxygen uptake of polychaetes
Comp. Biochem. Physiol.
Toward a greater understanding of pattern, scale and process in marine benthic systems: a picture is worth a thousand worms
J. Exp. Mar. Biol. Ecol.
Contaminant dispersal on the Palos Verdes continental margin: I. Sediments and biota near a major California wastewater discharge
Sci. Total Environ.
Multiple stressor effects identified from species abundance distributions: interactions between urban contaminants and species habitat relationships
J. Exp. Mar. Biol. Ecol.
Physiological and biochemical effects of acute exposure of fish to hydrogen sulfide
Comp. Biochem. Physiol. C.
Predicting summer hypoxia in the northern Gulf of Mexico: redux
Mar. Pollut. Bull.
Long-term divergent tidal flat benthic community recovery following hypoxia-induced mortality
Mar. Pollut. Bull.
Effects of hypoxia on movements and behavior of selected estuarine organisms from the southeastern United States
J. Exp. Mar. Biol. Ecol.
Respiratory adaptation to temporary hypoxia by the polychaete Cirriformia tentaculata
Comp. Biochem. Physiol.
Oxygen uptake, the circulatory system, and haemoglobin function in the intertidal polychaete Terebella haplochaeta (Ehlers)
J. Exp. Mar. Biol. Ecol.
Uber die Reaktionsgeschwindigkeit bei der Inversion von Rohrzucker durcj sauren
Z. Phys. Chem.
Adult body mass and annual production/biomass relationships of field populations
Ecol. Monogr.
Weitere Studien u ̈ber das Wa ̈rmegleich- gewicht unter Gasmoleku ̈len
Toward a metabolic theory of ecology
Ecology
Life at stable low oxygen levels: adaptations of animals to oceanic oxygen minimum layers
J. Exp. Biol.
Effects of low dissolved oxygen events on the macrobenthos of the lower Chesapeake Bay
Estuaries
Principles of Comparative Respiratory Physiology
Marine benthic hypoxia: a review of its ecological effects and the behavioral responses of benthic macrofauna
Oceanogr. Mar. Biol.
Spreading dead zones and consequences for marine ecosystems
Science
The functional role of estuarine benthos
Effects of size and temperature on metabolic rate
Science
A unifying explanation for diverse metabolic scaling in animals and plants
Biol. Rev.
Benthic-pelagic coupling: a benthic review
Oceanogr. Mar. Biol.
Energy metabolism as related to body size and respiratory surfaces, and its evolution
Comparative metabolic rates of common western North Atlantic Ocean sciaenid fishes
J. Fish Biol.
Cited by (10)
Two-year survey of Alitta succinea (Annelida: Nereididae) in fouling communities with notes on morphology and reproduction
2024, Ocean and Coastal ResearchAnimal Response to Hypoxia in Estuaries and Effects of Climate Change
2023, Climate Change and EstuariesOxygen consumption during and post-hypoxia exposure in bearded fireworms (Annelida: Amphinomidae)
2020, Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental PhysiologyEffect of high temperature and hypoxia on median lethal time and physiological function in sea cucumber Apostichopus japonicus of two sizes
2018, Journal of Fishery Sciences of China