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FIGURE 4.7 A typical dose-response curve from ecotoxicology.

Log Dose of Poison

Log Dose of Poison

Levin, 1985; Levin et al., 1989), by Taub in relation to her work on the standardized aquatic microcosm (Taub, 1997), and most strenuously, by John Cairns over three decades of writing (Cairns, 1974, 1983, 1985, 1986a, 1995a, 2000). The main argument against reliance on single-species tests in risk assessment is that they provide no information on indirect and higher order effects in multispecies systems, which many ecologists believe are important. Taub (1997) has summarized the situation as follows:

Single-species toxicity tests are inadequate to predict the effects of chemicals in ecological communities although they provide data on the relative toxicity of different chemicals, and on the relative sensitivity of different organisms. Only multispecies studies can provide demonstrations of: (1) indirect trophic-level effects, including increased abundances of species via increased food supply through reduced competition or reduced predation; (2) compensatory shifts within a trophic level; (3) responses to chemicals within the context of seasonal patterns that modify water chemistry and birth and death rates of populations; (4) chemical transformations by some organisms having effects on other organisms; and (5) persistence of parent and transformation products.

Thus, two categories of the effect of a pollutant are included in ecotoxicology:

(1) direct impact on a species, derivable from single-species toxicity tests, and

(2) indirect impacts due to interactions between species, best derivable from multi-species toxicity tests. The study of indirect effects is an important topic in ecology (Abrams et al., 1996; Carpenter et al., 1985; Miller and Kerfoot, 1987; Strauss, 1991 and; Wootton, 1994), and some researchers believe that the indirect effects are quantitatively more significant than the direct effects. For example, Patten's theoretical work (Higashi and Patten, 1989; Patten, 1983) indicates a dominance of indirect effects in ecosystems. Based on matrix mathematics and information on direct trophic linkages, Patten and his co-workers have developed a number of concepts and indices of network structure and function that quantify indirect effects and that challenge conventional thinking about ecological energetics (Fath and Patten, 2000; Higashi et al., 1993; Patten, 1985, 1991; Patten et al., 1976). This is a unique theory, termed network environs analysis, that represents a fascinating, though controversial, view of ecology (Loehle, 1990; Pilette, 1989; Weigert and Kozlowski, 1984). An example of an indirect effect caused by trophic interactions would be the increase in a prey population, which occurs when a predator population is eliminated by a toxin. In this case the direct effect is the impact of the toxin on the predator, which in turn causes the indirect effect of the release of the prey from control by the predator. Nontrophic interactions such as facilitation may also be involved in indirect effects (Stachowicz, 2001).

Ecologists, as indicated above, have criticized regulators for relying on single-species tests. Cairns and Orvos (1989) were particularly outspoken. They said "The development of predictive tests has been driven more by regulatory convenience than by sound ecological principles." And, "In an era where systems management is a sine qua non in every industrial society on earth, it is curious that the archaic fragmented approach of quality control is still in practice for the environment. Probably the reason for this is that the heads of most regulatory agencies are lawyers and sanitary engineers rather than scientists accustomed to ecosystem studies."

Regulators, on the other hand, find that multispecies toxicity tests (microcosms and mesocosms) have problems that limit their utility in risk assessment, including issues of standardization, replication, cost, and clarity of end points. Furthermore, regulators point to the existence of at least some comparisons between single-species tests and tests with microcosms and mesocosms which suggest that results from single-species tests can be extrapolated to higher levels of organization (Giddings and Franco, 1985; Larson et al., 1986). An example of the interplay between ecologists and regulators is provided in a special issue of the journal Ecological Applications (Vol. 7, pp. 1083-1132) which provides discussion about EPA's decision to formally drop the use of mesocosms as the high tier in testing of pesticides. Apparently, there is a fundamental lack of agreement between ecologists and regulators about the need for multispecies toxicity tests (Dickson et al., 1985).

This situation presents an ecological engineering design challenge to create multispecies toxicity tests in the form of microcosms and mesocosms that will satisfy both ecologists and regulators. A large volume of literature has developed on various systems design and testing protocols (Hammons, 1981; Hill et al., 1994; Kennedy et al., 1995a; Pritchard and Bourquin, 1984; Sheppard, 1997; Voshell, 1989). Much of this work is funded by the EPA and the chemical production industries. For example, starting in the 1980s, the EPA funded center-scale research first at Cornell University, then at the Microcosm Estuarine Research Laboratory (MERL) facility on Narragansett Bay, RI, and presently at the Multiscale Experimental Ecosystem Research Center (MEERC) at the University of Maryland. Earlier work by the University of Georgia scientists on end points for microcosm testing of chemicals is a good example of efforts by ecologists to develop simple designs and appropriate end points (Hendrix et al., 1982; Leffler, 1978, 1980, 1984). They used small aquatic microcosms and tested for the influence of chemical inputs on a variety of system parameters listed below:

Biomass

Chlorophyll a

Net daytime production

Nighttime respiration

Gross production

Net community production

From this work Leffler (1978) derived a formal definition of stress with several metrics that could be useful as end points (Figure 4.8). Stress is evident and quantified by the difference between the experiment and control microcosms in Leffler's definition. Unfortunately, this approach is relatively complicated compared with the simple LD50 toxicity test on single species, which regulators prefer. However, the University of Georgia research described above represents the kind of efforts ecol-ogists are taking to meet the needs of regulators for multispecies toxicity tests.

Some of the most valuable progress at bridging the gap between regulators and ecologists has been in the development of standardized microcosms. Regulators value precision (low variance) and reproducibility (Soares and Calow, 1993), and these preferences have led some ecologists to design, build, and operate small, simple e

Day of Exposure

FIGURE 4.8 Definition of stress as a deviation in system response in a microcosm experiment. (From Leffler, J. W. 1978. Energy and Environmental Stress in Aquatic Systems. J. H. Thorp and J. W. Gibbons (eds.). U.S. Dept. of Energy, Washington, DC. With permission.)

FIGURE 4.8 Definition of stress as a deviation in system response in a microcosm experiment. (From Leffler, J. W. 1978. Energy and Environmental Stress in Aquatic Systems. J. H. Thorp and J. W. Gibbons (eds.). U.S. Dept. of Energy, Washington, DC. With permission.)

microcosms as test systems. Precision and reproducibility in a test system provide the confidence in results that regulators appreciate for decision making. Beyers and H. T. Odum (1993) called these "white mouse" microcosms, drawing on the analogy of standard experimental animals used in medical research. The first example of a standardized microcosm in ecotoxicology was developed by Robert Metcalf (Met-calf, 1977a, b; Metcalf et al., 1971), who was an entomologist with an interest in

FIGURE 4.10 Energy circuit diagram of the food chains in Metcalf's microcosm.

the environmental effects of pesticides. Metcalf tried several different designs, but most of his work was done with glass aquariums containing an aquatic-terrestrial interface representative of an agricultural field and a farm pond (Figure 4.9). The aquarium was seeded in a standardized schedule with the following organisms which formed three food chains (Figure 4.10):

Aquatic Habitat

200 Culex pipiens quinquefasciatus (mosquito larvae)

3 Gambusia affinis (mosquito fish)

10 Physa sp. (snails)

30 Daphnia magna (water fleas)

A few strands of Oedogonium cardiacum (a green alga)

A few milliliters of plankton culture

Terrestrial Habitat

50 Sorghum halpense seeds (a flowering plant) 10 larvae of Estigmeme acrea (caterpillar)

Radio-labelled test chemicals were added to the system and their biomagnification and biodegradation were studied routinely. Experiments were run for a standard 33 days and the timing of additions of different organisms was designed for the sorghum, Daphnia, and mosquito larvae to be completely eaten by the end of the experiment! Thus, Metcalf's microcosm was not intended to be self-sustaining, but rather it was designed to collapse ecologically and be a short-term model, especially of food chain biomagnification. Metcalf and his students studied more than 100 pesticides and other chemicals with this system mostly in the 1970s, and the microcosm was modified and used by other researchers (Gillett and Gile, 1976).

Frieda Taub developed a standardized aquatic microcosm (SAM) which continues to be used (Taub, 1989, 1993). This system was reviewed by Beyers and H. T. Odum (1993), including an energy circuit diagram of the system. Taub's microcosm consists of a nearly gnotobiotic, 3-l flask culture with 10 algal species (blue-greens, greens, diatoms), five animal species (protozoa, Daphnia, amphipods, ostracods, and rotifers), and a mix of bacteria which cover a range of biogeochemical niches and feeding types. The system is run with a standard protocol for 63 days, and has been studied and verified to such a degree that it has been registered with the American Society for Testing and Materials as a standard method (ASTM E1366-90). The system is especially significant in ecological engineering because it represents the culmination of several decades of research design by Taub and her co-workers. The system is widely known and the chemically defined media and the microcosm itself are named after Taub, which is a reflection of her long record of work on its development and use. The development of the SAM can be traced back to the 1960s with early work on gnotobiotic microcosms (Taub, 1969a, 1969b, 1969c; Taub and Dollar, 1964, 1968).

The design research required to develop the SAM is an example of the kind of trial-and-error study required in ecological engineering to create ecosystems which perform specific functions, in this case to serve as a model test system for ecotoxicology. Here the engineering is in the design/choice of growth chamber, container, media, and organisms that make up the ecosystem, rather than in the "pumps and pipes" type design characteristic of conventional engineering. Living organisms are not completely understood and are not easy to combine into working systems, unlike the case for well understood engineering systems such as hydraulics or electronics. Thus, ecological engineering design differs from conventional engineering design because of the unknown factors associated with biological species. If organisms were completely understood, as perhaps approximated with Thomas Park's flour beetles, then the ecological system becomes a "machine" with a level of design equivalent to conventional engineering. Perhaps Park's flour beetle microcosm, in its elegant simplicity, is like the pencil or the screw, both equally elegant and simple machines whose engineering histories are described in book length treatments by Petroski (1989) and Ryeczynski (2000), respectively.

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