Effects of Intertidal Position on Metabolism and Behavior in the Acorn Barnacle,Balanus glandula

Abstract

The intertidal zone is characterized by persistent, tidally-driven fluctuations in both abiotic (e.g., temperature, [O2], salinity) and biotic (e.g., food availability, predation) factors, which make this a physiologically challenging habitat for resident organisms. The relative magnitude and degree of variability of environmental stress differs between intertidal zones, with the most extreme physiological stress often being experienced by organisms in the high intertidal. Given that so many of the constantly shifting parameters in this habitat are primary drivers of metabolic rate (e.g., temperature, [O2], food availability), we hypothesized that sessile conspecifics residing in different tidal zones would exhibit distinct ‘metabolic phenotypes,’ a term we use to collectively describe the organisms’ baseline metabolic performance and capacity. To investigate this hypothesis, we collected acorn barnacles (Balanus glandula) from low, mid, and high intertidal positions in San Luis Obispo Bay, CA and measured a suite of biochemical (whole-animal citrate synthase (CS) and lactate dehydrogenase (LDH) activity, aerial [D-lactate]), physiological (O2 consumption rates), morphological (body size) and behavioral (e.g., cirri beat frequency, % time operculum open) indices of metabolism. We found tidal zone-dependent differences in B. glandula metabolism that primarily related to anaerobic capacity, cirral activity patterns and body size. Barnacles from the low intertidal tended to have a greater capacity for anaerobic metabolism (i.e., increased LDH activity, increased baseline [D-lactate]), have reduced cirral beating activity—and presumably reduced feeding—when submerged, and be smaller in size compared to conspecifics in the high intertidal. We did not, however, see any D-lactate accumulation in barnacles from any tidal height throughout the 96 h of air exposure. This trend indicates that the enhanced capacity of low intertidal barnacles for anaerobic metabolism may have evolved to support metabolism during more prolonged episodes of emersion or during events other than emersion (e.g., coastal hypoxia, predation). There were also no significant differences in CS activity or baseline oxygen consumption rates (in air or seawater at 14˚C) across tidal heights, which implies that aerobic metabolic capacity may not be as sensitive to tidal position as anaerobic processes. Understanding how individuals occupying different shore heights differ in their metabolic capacity becomes increasingly interesting in the context of global climate change, given that the intertidal zone is predicted to experience even greater extremes in abiotic stress.

Geographic variation in vulnerability to warming temperatures in an intertidal barnacle species

“…The concentration of oxygen in air is roughly 20-fold higher than in seawater, so oxygen may be more accessible during emersion at moderate temperatures then during immersion [61]. By staying closed barnacles may also reduce to vulnerability predation during immersion [62]. At warmer temperatures, barnacles began immersion with higher initial respiration rates that declined gradually over the 6-hr immersion period.…”

“…The concentration of oxygen in air is roughly 20-fold higher than in seawater, so oxygen may be more accessible during emersion at moderate temperatures then during immersion [61]. By staying closed barnacles may also reduce to vulnerability predation during immersion [62].…”

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation

“…During these periods of aerial exposure, oxygen uptake can be inhibited as a result of a need for water conservation or because animals have aquatic-adapted gas exchange mechanisms that function poorly in air (Barnes et al, 1963;Newell, 1973;Davenport and Irwin, 2003). Many intertidal organisms have evolved behavioral, physiological, and biochemical mechanisms that confer high tolerance to internal hypoxia during these times (Falfushynska et al, 2020), but warming temperatures are likely to increase the cost of deploying these mechanisms and to exacerbate associated oxygen deficits through increased metabolic rates (Horn et al, 2021).…”