Final Comments: Implications of Hormesis to Ecotoxicology and Ecological Risk Assessment (ERA)

Peter M. Chapman, Ph.D.

EVS Environment Consultants

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I thank the seven individuals who commented on my original white paper (Chapman, 2001). As expected they have not endorsed all of my thoughts. Also as expected, they have both built on my original white paper and raised some very important additional issues that need to be considered.

There appears to be general agreement that hormesis has a role in ecotoxicology and ecological risk assessment (ERA). However, there is disagreement as to the extent of that role, particularly in ERA. Giesy (2001) does not believe accommodating hormesis in ERA would be particularly useful as "hormesis is not the major cause of uncertainties". While I agree that there are other processes that create greater uncertainties in ERA, I continue to believe that we should not simply ignore the reality of hormesis. My view is supported by Menzie (2001) who notes that hormetic phenomena are currently incorporated into ERA "where such responses are known as in the case of essential nutrients." He also notes that presently there is acceptance of some level of stress by environmental managers (e.g., fire, flood), thus the idea that less exposure is better is not universally held. Similarly, Suter (2001) notes that ecological risk assessors and managers would be open to the phenomenon of hormesis, provided it was suitably demonstrated.

Giesy (2001) and Menzie (2001) suggest that incorporating hormesis into ecotoxicology and ERA does not need to involve a paradigm shift. I believe this is an issue of semantics, not disagreement. For instance, Menzie (2001) suggests that instead of a paradigm shift we need "a more complete understanding of the relationships between exposure and effects at various organizational scales."

Four key issues are raised in the commentaries. The first key issue is the importance of focusing on exposure-response relationships in general, rather than on the specific issue of hormesis. Menzie (2001) and Suter (2001) both suggest that hormesis is an example of an unusual exposure-response relationship at low doses and concentrations, not an umbrella term for such relationships. This is a particularly valuable concept, in my opinion, and I agree with this assessment. Giesy (2001) expands on this theme and further suggests that the concept of "subsidy-stress" developed by Odum (1971) may be a more appropriate term than hormesis. He also notes that we should not assume low-level effects are mediated by the same mechanism as higher-level effects, another very important point. Coincidentally, shortly after getting Giesy's (2001) comments, I received a letter from a former student of Odum's providing me with copies of pertinent portions of his Dissertation (Knight, 1980) and two subsequent papers (Knight, 1981, 1983). Knight's work builds on Odum (1971) and deals with the concept of subsidy-stress in terms of ecosystem responses and energy flow within ecosystems. Knight's letter pointed out the relevance of the concept of subsidy-stress to hormesis. His publications referenced earlier studies that had shown hormetic/subsidy-stress responses in field populations not in relation to contaminants, but in relation to biotic interactions (Hargrave, 1970; Cooper, 1973; Flint and Goldman, 1975). Knight's comments and publications reinforce my contention that hormesis cannot be ignored in detailed level ERAs involving natural systems. I agree with Menzie (2001) that using the term "hormesis" for all potentially hormetic phenomena "might confuse the idea with a common mechanistic process and could detract from addressing the varied and important underlying processes." Gentile (2001) comments similarly. As for the possibility of using the term "subsidy-stress" rather than hormesis, this may be useful in certain cases (Suter, 2001) but, as noted above, there is a need for an umbrella term for unusual exposure-response relationship at low doses and concentrations. Because of their present specific connotations, it is unlikely that either "subsidy-stress" or "hormesis" would provide a suitable umbrella term.

The second key issue is whether hormetic responses can be applied above the level of the individual (Giesy, 2001) and the difficulty in translating individual-level responses to community-level responses in ERA (Elnabarawy, 2001; Gentile, 2001). Giesy (2001) comments that individuals can evolve whereas ecosystems "represent the abiotic and biotic result of such adaptations", thus "the concept of hormesis is not directly applicable to ecosystems and the term hormesis should be reserved for adaptive responses of individual organisms." I am unclear whether these comments exclude subsidy-stress responses at the ecosystem level, however clearly ecosystems can and do exhibit hormetic responses, and these responses should not be ignored. However, the suggestion of reserving the term "hormesis" for adaptive responses of individual organisms has merit.

The third key issue is whether ERA should consider hormetic responses as positive or not. Giesy (2001) argues that "any response that moves an organism out of its normal homeostatic range or requires expenditure of energy or mobilization of stored resources be viewed as a negative response". In my opinion this is too simplistic an approach, though I agree that it will be protective (probably overly protective). This approach is appropriate, as I noted (Chapman, 2001) for a screening level ERA, but not for a detailed level ERA. Menzie (2001) notes that the difficulty of incorporating potential positive effects into environmental policy can only be resolved by better understanding of organism responses to low levels of stress.

The fourth key issue is "the general question of how should one set a regulatory exposure limit for a stressor that exhibits a hormetic concentration-response pattern" (Bailer, 2001). Some good thoughts are provided but no clear solution to what I agree is a "non-trivial question". Clearly this question is a major limitation to the future use of hormesis in regulatory ecotoxicology and ERA.

Elnabarawy (2001) and Giesy (2001) also note the importance of societal expectations. Such are, of course, part of risk management, not risk assessment. However, they also frame the ERA ­ if there is no concern regarding low doses, there will be no focus on low doses. Menzie (2001) correctly stresses the importance of educating policy makers (and some scientists) in the diversity of exposure-response relationships.

Additional issues raised in the commentaries and that need to be considered include:

· What are the key research needs that will allow successful competition for precious research dollars (Elnabarawy, 2001).

· Could there be sufficient replication of conditions in community-level exposure experiments (e.g., pond-level, mesocosms) to detect hormetic responses? Mechanistic or population modeling might be necessary (Bailer, 2001; Gentile, 2001).

· Are hormetic results always direct responses or are they indirect (secondary) effects resulting from a direct effect (Rand, 2001; Giesy, 2001)? And what does this mean?

· Hormesis for non-essential substances may be best framed within the concept of assimilative capacity (Menzie, 2001).

· Whether or not hormesis is an adaptive response remains to be clearly established (Rand, 2001).

· The roles of response variability and statistical power are important in interpreting the significance of hormetic responses (Gentile, 2001).

· Whether the identification of hormetic thresholds can effectively replace uncertainty factors is uncertain at best (Gentile, 2001).

· Until ecotoxicology and ERA are routinely based on exposure-response relationships, hormesis will neither be noticed nor deemed an important issue by scientists or managers in general (Suter, 2001).

It is clear from the comments that there is a role for hormesis in both ecotoxicology and ERA, though there presently is not agreement as to the extent of that role. Defining that role will require, as noted by five of the seven commentaries (Gentile, 2001; Giesy, 2001; Menzie, 2001; Suter, 2001; Rand, 2001), an underlying mechanistic theory that will allow " being able to a priori forecast which stressor-response relationships are the most likely to result in a hormetic response". Stebbing (1998) has proposed a mechanism for growth hormesis, however it is likely that this is not the only mechanism of hormesis. The lack of underlying mechanisms for hormesis/subsidy-stress is perhaps the single greatest impediment to greater acceptance of the phenomenon/phenomena in ecotoxicology and ERA.

References

Bailer AJ. Experiments, analyses and decisions: Hormesis in ecotoxicology. BELLE Newsletter 2001; 10(1):this issue.

Chapman PM. The implications of hormesis to ecotoxicology and ecological risk assessment (ERA). BELLE Newsletter 2001; 10(1):this issue.

Cooper DC. Enhancement of net primary productivity by herbivore grazing in aquatic laboratory microcosms. Limnology and Oceanography 1973; 18: 31-37.

Elnabarawy M. Commentary: Role of Hormesis in Ecological Risk Assessment. BELLE Newsletter 2001; 10(1):this issue.

Flint RW, Goldman CR. The effects of a benthic grazer on the primary productivity of the littoral zone of Lake Tahoe. Limnology and Oceanography 1975; 20: 935-944.

Gentile JH. The implications of hormesis to ecotoxicology and ecological risk assessment (ERA). BELLE Newsletter 2001; 10(1):this issue.

Giesy JP. Hormesis ­ Does it have relevance at population-, community-, or ecosystem-levels of organization? BELLE Newsletter 2001; 10(1):this issue.

Hargrave BT. The effect of a deposit-feeding amphipod on the metabolism of benthic microflora. Limnology and Oceanography 1970; 15: 21-30.

Knight RL. Energy Basis of Control in Aquatic Ecosystems. Ph.D. Dissertation, University of Florida, 1980.

Knight RL. A control hypothesis for ecosystems - energetics and quantification with the toxic metal cadmium. pp. 601-615 In: Mitsch WJ, Bosserman RW, Klopatek JM (eds), Energy and Ecological Modeling. Developments in Environmental Modelling. Elsevier Scientific Publishing Co., Amsterdam, 1981.

Knight RL. Energy basis of ecosystem control at Silver Springs, Florida. pp. 161-179. In: Fontaine TD, Bartell SM (eds), Dynamics of Lotic Ecosystems. Ann Arbor Science, Ann Arbor, MI, 1983.

Menzie CA. Hormesis in ecological risk assessment: A useful concept, a confusing term, and/or a distraction? BELLE Newsletter 2001; 10(1):this issue.

Odum EP. Fundamentals of Ecology. W. B. Saunders Co., Philadelphia, PA, 1971.

Rand GM. Commentary: Role of Hormesis in Ecological Risk Assessment. BELLE Newsletter 2001; 10(1):this issue.

Stebbing ARD. A theory for growth hormesis. Mutation Research 1998; 403: 249-258.

Suter GWII. Focus on exposure-response relationships, and complex forms will come naturally. BELLE Newsletter 2001; 10(1):this issue.