N. Voulvoulis and M.D. Scrimshaw
6.2 ENDOCRINE DISRUPTERS IN THE RECEIVING AQUATIC ENVIRONMENTAQUATIC ENVIRONMENT
6.2.2 E FFECTS TO B IOTA IN R ECEIVING S URFACE W ATERS
During the 1980s, anglers observed that several wild roaches exhibited a range of deformities in certain stretches of some U.K. rivers. When hermaphrodite and inter- sex fish were discovered near sewage outfalls in the early 1990s, concern arose over the presence of environmental estrogens entering the aquatic environment. A link between the production of VTG in male fish normally detected only in fertile females, and sewage effluent was established.7,28
182 Endocrine Disrupters in Wastewater and Sludge Treatment Processes
The majority of data on EDCs are related to the aqueous environment from observations of abnormalities in biota, predominantly fish, present in surface waters.
Adverse effects have included VTG induction in male fish, which is normally identified only in fertile females,29 intersex where the organism possesses both male and female characteristics, various physical deformities,30 and behavioral effects.31 Any behavioral change while not necessarily affecting the individual may adversely influence a population from the reproductive implications.32 Many effects have also been demonstrated under laboratory conditions for a wide range of organisms, both aquatic and terrestrial. Selected examples of abnormalities observed in aquatic organ- isms are shown in Table 6.1.
Though an EDC can be present in the aquatic system, it may not necessarily assert an estrogenic response to any organisms present within. The response observed in biota attributed to EDCs depends on numerous factors. Bioavailability plays an important role (Section 6.2.2.1), as does the EDC, environmental parameters, and the target organism. Examples of these factors and how they may influence the effect of EDCs to a target organism are given in Table 6.2.
6.2.2.1 Bioavailability
In order to have an endocrine disrupting effect to biota in surface waters, EDCs must first become bioavailable to the aquatic organism. Bioavailability is the response that a compound elicits from an organism over a range of concentrations and is synonymous with toxicity.60 The degree of bioavailability is dependent on:
1. Chemical structure and properties (sorption capability, persistence) 2. Route of exposure (biomagnification, bioconcentration)
3. Aquatic life form of interest (benthic, demersal, pelagic organisms) The physicochemical properties of the organic contaminant determine whether the EDC will favor the solid or aqueous phase and its persistence in the environment.
Many EDCs have high Koc and therefore will sorb to the sediment. This allows lower concentrations of EDCs to be abstracted for drinking water treatment or water reuse practices. However, this has an adverse effect on bottom dwelling biota that have demonstrated increased levels of VTG as a result.29 Water currents or bioturbation allows for resuspension of the sediment and resultant bioavailability to biota present in water column.
The classic picture of pollutant transfer from sediments to organisms involves an intermediate stage in the water column. However, it is now believed that direct transfer from sediments to organisms occurs to a large extent.61 The bioavailability of many organic compounds in natural solids decline with increasing time. This process is known as sequestration, and EDCs such as polyaromatic hydrocarbons (PAHs), PCBs, and pesticides undergo this, decreasing the availability of the com- pound to biota.62 The importance of lifestyle and feeding habits of biota and their interaction between the dissolved and solid (suspended/whole sediment) phase is illustrated in Figure 6.2.
Endocrine Disrupters in Receiving Waters183 TABLE 6.1
Selected Examples of Abnormalities Observed in Aquatic Organisms as a Result of EDCs
Organism Type Effect Cause Observation
Rainbow trout (Oncorhynchus mykiss)
Fish Reproductive Sewage effluent Downstream of effluent discharge has induced the production of VTG in the male14,20,24
Roach (Rutilus rutilus)
Fish Reproductive Sewage effluent Downstream of effluent discharge, intersex has been induced (in some cases 100% of the male fish contained oocytes in their testes)4
Flounder (Platichthys flesus)
Fish Reproductive Sewage effluent Downstream of effluent discharge has induced the production of VTG in the male33
Japanese medaka (Oryzias latipes)
Fish Behavioral Estradiol Decreased fecundity in the female resulting in altered sexual activity34
Reproductive Nonylphenol Abnormal gonad and anal fin (female-like) observed in male35
White sucker Fish Reproductive Pulp mill effluent Reduced gonadal size in the female exposed to less than 1% effluent (pulp mill), though at other sites, similar concentrations have not induced endocrine effects36
Fathead minnows (Pimephales promelas)
Fish Reproductive Methylmercury Reduced gonadal development and spawning success of adult female37
Barnacle
(Elminius modestus)
Invertebrate Developmental Nonylphenol Estradiol
The timing of larval development to the cypris stage was disrupted (accelerated) 38
Physiological Nonylphenol Estradiol
Long-term (12 months) exposure led to significant reduction in adult barnacle size38
Dogwhelk Invertebrate Developmental Tributyltin Severely retarded larval development39
(Nucella lapillus) Reproductive Tributyltin Masculinization of the female (imposex)39
Water flea (Daphnia magna)
Invertebrate Reproductive Nonylphenol and ethoxylate Induction of metabolic androgenization in the female40 (continued)
184Endocrine Disrupters in Wastewater and Sludge Treatment Processes TABLE 6.2
Factors Affecting Toxic Responses in Organisms from EDCs
Factors Effects to Organisms from EDC Exposure
EDC Type of EDC/
Metabolite
The different groups of EDCs or metabolites in the same group require different concentrations in order to cause a response in organisms assuming bioavailability.
For fish (Oryzias latipes), the LC50 (48 hours) of the surfactant nonylphenol-16-ethoxylate (NP16EO) and metabolites nonylphenol-9-ethoxylate (NP9EO) and nonylphenol (NP) are 110, 11.2, and 1.4 mg l–1, respectively, illustrating that increasing toxicity occurs with decreasing ethoxylate units.41
The lowest observed effective concentration (LOEC) for VTG synthesis in primary fish cells for estradiol (E2), NP and bisphenol A was 1, 14, and 25 µg l–1, respectively.42
Physicochemical properties
Factors such as the Kow, Koc, and water solubility greatly impact on the effects an EDC may induce because of the bioavailability of the EDC. EDCs with low water solubility will favor partitioning to suspended/whole sediment and so will be in contact with benthic organisms more than pelagic.43
In blue mussels (Mytilus edulis), PBDEs and PCBs of similar hydrophobicity can have very different bioaccumulation factors (BAF), with preference to PBDE bioaccumulation.44
Individual/mixtures EDCs are able to act together to produce significant effects even when they are present at concentrations below their individual effect threshold.45,46
The effect of a mixture of substances can be additive, synergistic, and even antagonistic.47
In soil-water systems, pesticide behavior in the presence of surfactants is dependent on the degree of hydrophobicity of the pesticide, surfactant type, and concentration.48
VTG induction occurred at lowest mixtures concentrations (E2 and NP, E2 and methoxychlor, NP and methoxychlor) even when concentrations were below individual LOECs.49
Environmental concentration
The concentrations required for EDCs to induce endocrine disrupting effects to biota may not always be present in watercourses.
For NP and bisphenol A, there is a safety margin of 100 and 3000 between concentration in effluent and effects monitored by receptor and indicator assays. However, for E2 there is no safety margin due to a much smaller LOEC.42