Physiological, Developmental and Behavioral Effects of Marine Pollution

The ocean plays a key role in cycles of carbon, nitrogen, phosphorus and a variety of other important chemicals. Ocean chemistry has been changing due to human activities, both regionally in coastal waters and in the open ocean. Some of the greatest impacts are on carbon, nitrogen, and dissolved oxygen, which affect biological productivity. The rate of primary production is determined primarily by light and nutrients. Decades of pollution of marine waters, along with coastal habitat destruction, overfishing and bottom trawling have had devastating impacts on biodiversity and habitats. The increasing demand for seafood worldwide has depleted fish populations and devastated the economic well-being of coastal communities. At the same time, climate change is altering the oceans in major ways that we are only beginning to understand.

Obtaining food for energy is essential for all living things that don’t photosynthesize. Reduced feeding and digestion are commonly observed after exposure to a variety of pollutants. Alterations in feeding, nutrient assimilation, and energetics in many species could not only impact their own population dynamics, but also could have community-wide repercussions. Decreased feeding is not only a general response to contaminants, but also can result in a “positive feedback” situation, since poor nutrition resulting from decreased feeding can in turn make animals more susceptible to contaminants (Dissanayake et al. Aquat Toxicol 89:40–46,2008). These authors advised that “ecotoxicological studies need to take into account the nutritional state of the test organism to achieve the full assessment of contaminant impact.” On the other hand, it is also likely that decreased feeding will reduce further uptake of contaminants. This is particularly true for animals at higher trophic levels, which acquire much of their body burden of contaminants from their food. Additional discussion of pollution effects on feeding is covered in Chap. 9, Behavior.

Respiration includes the transport of oxygen from the outside of the organism into the cells and the transport of carbon dioxide in the opposite direction. Cellular respiration, which takes place within cells, consists of the metabolic processes by which energy is obtained by breaking down glucose through enzymatic pathways (glycolysis and the Krebs cycle), creating water, carbon dioxide and ATP. Respiration responds directly to metabolic needs. Most toxicants studied have been found to reduce the metabolic rate and thus, the respiration of many organisms. Many studies have relied primarily on a single metric, oxygen consumption, to determine changes in metabolic rates. In some cases, however, lowered oxygen consumption can be attributed to reduced ventilation of the gills or to gill damage, and in other cases the toxic mechanism is disruption of the enzymes of cellular respiration. Relatively few studies have related effects on respiration to carbon assimilation through measures of feeding and excretion or have examined total effects on the carbon, nitrogen, or energy budget.

Maintaining a constant internal chemical environment (homeostasis) is a critical physiological activity that is particularly important in certain taxa living in fluctuating environments such as estuaries and in those that migrate between fresh- and salt water. Stress, such as exposure to contaminants, typically causes a disruption of this activity, which involves primarily the gills. The ability to ionoregulate or to osmoregulate (mostly Na and Cl regulation) following exposure to stress decreased in most of the species studied with most of the contaminants. Concomitant with osmoregulation is the necessity to excrete ammonia, a waste product of protein metabolism; this activity may be either enhanced or depressed by contaminants and is affected by salinity and whether the animals are fed or not. Increased excretion rates reflect increased reliance on protein metabolism.

Reproduction is obviously a very important endpoint, since impaired reproduction can have rapid repercussions at the population level. Life-cycle characteristics of different organisms are a major factor in determining their vulnerability to particular contaminants. There are many ways in which reproduction can be affected, but one of particular concern is by very low levels of some environmental chemicals that can interfere with the endocrine system, termed endocrine disruption. Contaminants can also directly affect gametogenesis, mating, and fertilization. These various stages of the reproductive process are clearly connected to one another.

Embryonic stages of marine animals have been used extensively in explorations of effects of contaminants and toxicity testing. This chapter provides a review and summary of the nature of observed adverse effects and toxic levels on embryonic development for important classes of chemical pollutants. Early life stages are generally more susceptible to environmental contaminants than later stages, so many studies focus on embryos or larvae. Embryos can be exposed to developmental toxicants during oogenesis in exposed females, during the brief period between shedding of gametes and fertilization, and after fertilization. Studies have shown that chemicals incorporated into the egg during oogenesis can produce malformations in the embryos that subsequently develop from these eggs. In most experimental studies, however, embryos are exposed to chemicals after fertilization. Exposures can be throughout embryonic development or during shorter time periods. Although many toxicity tests still use hatching success as the endpoint of interest, common responses include delayed development and formation of abnormalities. Chemicals can affect morphogenetic movements such as gastrulation, tissue interactions such as induction, growth, and degeneration or cell death, which is an inherent part of embryonic development. Some responses do not become apparent until larval or juvenile stages.

After hatching, an organism leaves a relatively closed and protected system for life in a larger environment. Many studies have been performed exposing larval stages directly to contaminants or examining larvae after embryonic exposure. Larvae may be more sensitive than embryonic stages of the same organism, since embryos are protected by an outer membrane that may reduce contaminant uptake (e.g. chorion) that is no longer present in larvae. Larvae also must usually swim and obtain food. Most benthic invertebrates have planktonic larvae, which at a certain stage of development settle to the bottom to metamorphose into a juvenile stage in an appropriate habitat. Larval exposures to contaminants can lead to impaired settlement in the benthic environment and/or to delayed physiological disturbances as juveniles or adults.

Growth is an obvious and easily measured response, and is included in many standard toxicity tests as well as in research projects. Reduced growth is frequently traced back to reduced food intake, but even without reduced feeding, it is a logical outcome since organisms must expend energy to defend themselves against and detoxify contaminants. The more energy needed to detoxify pollutants, the less will be available for growth. In addition to overall body growth, molting, regeneration, development of calcified structures (shell and bone), carcinogenesis, and smoltification are other developmental processes that take place after larval stages. These processes are all sensitive to environmental contaminants.

Behavior is a particularly sensitive measure of an organism’s response to stresses, including environmental contaminants. Noticeable changes in behavior can be found at low concentrations of chemicals, often lower than concentrations affecting biochemical biomarkers. Since behavior is a link between physiological and ecological processes, it is a particularly important type of response. In addition to being sensitive, behavioral changes are likely to occur in nature and can have ecological effects at the population and community level. While much early research focused on avoidance, tremors, or coughs, complex behaviors such as predator/prey interactions, burrowing, reproductive, and social behaviors are much more relevant to ecological impacts.

Bioavailability refers to the fraction of the total chemical in the environment that is available for absorption into biota. This depends on the chemical, the organism, and environmental conditions, such as temperature, DO, and pH. Uptake of contaminants generally is via the skin, respiratory system, or food, with food being a major route of uptake for species that are higher on the food web such as large carnivorous fishes or mammals. Hydrophobic compounds that have low water solubility (log octanol/water partition coefficient – log K_ow >6) are absorbed primarily from food, while compounds with low hydrophobicity (log K_ow <4) are more water-soluble, and are absorbed directly from the water, primarily by the gills. Hydrophobic chemicals including halogenated organics and metals that have low water solubility tend to be adsorbed to sediments, which are the main sink and source for uptake into biota (via pore water). They also partition onto particulates and small planktonic organisms. Once absorbed, only a portion of the chemical actually reaches the circulation for distribution around an animal’s body. This amount is affected by processes including absorption, transport, biotransformation, and excretion via gills or kidneys. Within cells, metals can become associated with metallothioneins or metal rich granules, which make them unavailable, while metals associated with enzymes can cause toxicity. The subcellular distribution also affects the degree of trophic transfer. Persistent organic chemicals tend to accumulate in fatty tissue and to biomagnify up food webs. Organic chemicals are metabolized with the cytochrome P450 (CYP) enzyme system. Both metals and organic chemicals tend to accumulate in the liver or hepatopancreas; lipophilic chemicals accumulate in the blubber of large animals such as marine mammals.

While previous chapters have focused on what pollutants do to marine organisms, this chapter deals with what marine organisms do to pollutants – taking them up from the environment and doing something with them such as storage or metabolism. Uptake can be through the skin, gills, or gut and may involve adsorption, passive diffusion, active transport, or endocytosis. The specific kinetics of uptake relate to the concentration and nature of the contaminant. The term bioaccumulation is generally used to describe uptake, but there are specific terms and acronyms that refer to variations in processes but are not always used correctly. Bioaccumulation refers to uptake from all sources in the environment. The bioaccumulation factor (BAF or BSAF) refers to the concentration in the organism relative to that of the sediment, when that is the major source of accumulation. If the concentration is normalized to the amount of lipid in the organism and the amount of organic carbon in sediments, the ratio may be referred to as the accumulation factor (AF). Bioconcentration is a more specific term that refers to accumulation from water. The bioconcentration factor (BCF) is the concentration of a chemical in the organism relative to that in the water. Biomagnification refers to increasing concentrations of a persistent contaminant from one trophic level to the next in a food chain, due to accumulation from food. The biomagnification factor (BMF) is the concentration at one trophic level divided by that at the trophic level below.

Tolerance is the ability of organisms to cope with stress, in this case to environmental pollutants. It appears to be a widespread phenomenon, and can be achieved by physiological acclimation or genetic adaptation. It can be assessed by comparing responses (lethal or sublethal) of individuals from different populations to the same degree of stress, e.g. the same concentration of a toxicant would produce less of an effect in a tolerant population. The phenomenon is well documented for metals and organic contaminants (for example, resistance of insect populations to insecticides is well-known). There are also cases in which tolerance has been looked for but not found in chronically exposed populations; probably more cases than have been reported in the literature, as this can be viewed as “negative data” and not reported. When enhanced tolerance does not occur in polluted populations, the reasons may be difficult to ascertain; it may be because detoxification mechanisms are adequate to cope with elevated exposures, or that dispersal and mixing between contaminated and reference populations obscures any observation of tolerance, or that the fitness costs counteract the selective advantage of the tolerance, or other reasons.

Compensatory responses to pollutants at the physiological level are referred to as “acclimation.” Pre-exposure to chemicals can induce or enhance detoxification processes, discussed in the previous chapter, which reduces toxicity in pre-exposed organisms, either in the lab or at field sites. These responses (e.g. synthesis of MTs, CYPs) can mitigate effects on individuals experiencing moderate stress. Developing tolerance is energetically expensive, however, and may have deleterious effects on energy allocation. Thus exposure over extended periods may reduce fitness and increase selection pressure for genetically resistant individuals in populations that have variation and heritability for the response. The development of these populations that have adapted and become more resistant to pollution can be considered an evolutionary compensatory mechanism.