challenges of living in hypoxic and hypercapnic aquatic environments, The

The Challenges of Living in Hypoxic and Hypercapnic Aquatic Environments1,2

LOUIS E. BURNETT3

SYNOPSIS. Organisms living in coastal waters, and especially estuaries, have long been known to have behavioral or physiological mechanisms that enable them to exist in water containing low amounts of oxygen. However, the respiratory consumption of oxygen that generates hypoxia is also responsible for producing significant amounts of carbon dioxide. An elevation of carbon dioxide pressure in water will cause a significant acidosis in most aquatic organisms. Thus, the combination of low oxygen and elevated carbon dioxide that occurs in estuaries represents a significant environmental challenge to organisms living in this habitat. Organisms may maintain oxygen uptake in declining oxygen conditions by using a respiratory pigment and/or by making adjustments in the convective flow of water and blood past respiratory surfaces (ie., increase cardiac output and ventilation rate). Severe hypoxia may result in an organism switching partially or completely to anaerobic biochemical pathways to sustain metabolic rate. There is also evidence to suggest that organisms lower their metabolism during hypoxic stress. Elevated water CO, (hypercapnia) produces an acidosis in the tissues of organisms that breathe it. This acidosis may be wholly or partially compensated (Le., mechanisms return pH to pre-exposure levels), or may be uncompensated. Some studies have examined the effects on organisms of exposure simultaneously to hypoxia and hypercapnia. This article reviews some of the specific adaptations and responses of organisms to low oxygen, to high carbon dioxide, and to the cooccurrence of low oxygen and high carbon dioxide.

INTRODUCTION

A significant factor in limiting the distribution of macroorganisms in aquatic environments is the availability of oxygen. This is true because nearly all animals require oxygen in the process of producing energy. Estuaries are particularly noted for the development of low environmental oxygen levels (hypoxia), although they are not unique in this respect (Diaz and Rosenburg, 1995). Water-breathing animals that live in estuaries may experience extremes in oxygen availability (e.g., Renaud, 1985; Atkinson et al., 1987; Rabalais et al., 1994). This appears to be a part of a cycle that is seasonal and tidal in the estuaries associated with salt marshes along the southeastern United States (Cochran and Burnett, 1996).

An estuary is defined as a semi-enclosed body of water with freshwater input and tidal flushing by the ocean (Cameron and Pritchard, 1963). Because of the water runoff from the land, estuaries are rich in nutrients and are typically considered highly productive environments. Thus, as a fisheries resource, estuaries are important. However, because coastal areas sustain large human populations, the impacts of human activity on estuarine ecosystems can be quite profound. Diaz and Rosenburg (1995), in a review of the ecological effects of hypoxia, conclude that human activities have enhanced the occurrence of hypoxia and anoxia in a number of important ecosystems around the world, including estuaries. These authors suggest that many ecosystems are now severely stressed by hypoxia.

In this article I will review the effects of hypoxia and hypercapnia (high CO^sub 2^) on selected estuarine organisms. I will focus on estuarine organisms because much work on organisms has centered on estuaries. However, the information presented here is applicable to any organism encountering hypoxia and/or hypercapnia. There is a large literature on organismal adaptations to hypoxia and I will not attempt to summarize that literature here. Rather, I will provide an overview of the strategies different organisms have used to live in hypoxic environments. Much less has been done on adaptations to hypercapnia and to combinations of hypoxia and hypercapnia.

It is well-known that many organisms are able to resist and/or compensate for low levels of environmental oxygen (Mangum and Van Winkle, 1973; Grieshaber et al., 1994; Mangum, 1997 this symposium). However, it is not well appreciated that environmental hypoxia is nearly always accompanied by an elevation of water carbon dioxide (and thus a decrease in water pH). The biological oxygen demand responsible for lowering oxygen levels produces carbon dioxide as the main product of metabolism. The same processes occur in aerial environments. As it does in aerial environments, photosynthesis in water fixes carbon dioxide, removing it from the water. However, gases are roughly 7,000 times less diffusible in water than air (Dejours, 1975). Because gases are not very mobile in water, bodies of water are rarely homogeneous with respect to dissolved oxygen or carbon dioxide. In addition, the capacity of water to hold molecules of oxygen is significantly lower than that of air (53.8 (mu)mol Liter ' torr^sup -1^ in air at 25degC as compared to 1.4 l,mol liter^sup -1^ torr^sup -1^ in sea water or 1.7 (mu)mol liter ^sup -1^ torr^sup -1^ in fresh water). Water is able to hold more carbon dioxide than oxygen because of the hydration reactions of carbon dioxide that produce bicarbonate and carbonate ions.