Cmp. Biochem. Fh~s~#~. Vol. iOilC, No. l/Z, PP. 3-6, 1991 Printed in Great Britain

~~9219i s3.00 + 0.00 0 1991 Pergamon Press pIc

MINI-REVIEW

PHYSIOLOGICAL COSTS OF COMBATING CHEMICAL TOXICANTS: ECOLOGICAL IMPLICATIONS

P. CALOW Department of Animal and Plant Sciences, University of Sheffield, Sheffield, SlO 2TN, U.K.

(Telephone: 0742-768555; FAX: 0742-760159)

(Receioed 1 October 1990)

Abstmct-1. Evidence is presented that combating the poisoning effects of toxic chemicals is metaboIically costly.

2. This has implications for relating physiological stress responses observed at the level of individual organisms to population effects, and needs to be incorporated explicitly into models making this link.

3. The cost hypothesis also has implication for the evolution of stress resistance either as a fixed or facultative (inducible) response. Optimi~tion models incorpomting these ideas are reviewed and discussed.

INTRODUCFION

Chemical toxicants challenge biological systems. Their effects can be resisted by organisms in a number of possible ways: avoidance or escape reactions; exclusion (for example, many aquatic animals ex- posed to toxic chemicals secrete more mucus on to exposed surfaces); removal (in-coming toxicants might be actively pumped out); neutralization (by complexation with protective proteins) and/or ex- cretion; repair of damage caused by toxicants. If all these responses fail, there will be irreversible damage, pathological effects, leading ultimately to death. Selye (1950, 1973), Hatch (1962) and several others (Hellawell, 1986) have proposed a graded series of these responses to increasing concentrations of, or times of exposure to, toxicants.

A priori it is likely that all these responses are costly for the organism in terms of metabolic resources and especially energy (Calow, 1989). Here, I review evi- dence for these costs, and then consider their impli- cation for understanding the proximate and ultimate (see Mayr, 1961) responses of populations, and to some extent ecosystems, to chemical stress.

EVIDENCE FOR COSTS

In very general terms, there are bound to be metabolic costs, subsumed in basal (maintenance) metabolism, of keeping organisms organised in a thermodynamically “unfriendly” world (Prigogine et al., 1972). There are three kinds of evidence indicat- ing that these costs are enhanced with toxic stress:

1. A priori evidence

Many of the response processes listed in the Intro- duction are energy-d~anding. Increased activity is clearly so. The energetic cost of active transport is calculable but seemingly low relative to total metab- olism (Potts and Parry, 1964). Many observations of

3

increased Oz consumption of aquatic animals due to salinity stress were probably largely attributable to increased activity, but similar increases in isolated tissues may in part be due to enhanced active trans- port (reviewed by Newell, 1979). The energy costs of secreting mucous defences could be considerable (Calow, 1979). There are appreciable net energy costs to the processes of protein synthesis and possibly catabolism (Hawkins, 1991) that are the basis for the induction of neutralization (see above), excretion and repair processes (Calow, 1989). It remains doubtful, however, if in isolation the induction of specific protective proteins has an appreciable effect on en- ergy budgets relative to the overall throughput of energy within organisms. For example, we estimate metallothionein synthesis to represent < 5% total metabolism in metal-challenged daphnids (Barber et al., 1990). It is possible, nevertheless, that accumu- lated losses from this source over a lifetime are important for both individual and Darwinian fitness.

2. Direct metabolic measures

A general prediction that arises from models in- volving graded physiological responses that are metabolically costly is that metabolic rate should increase with increasing levels of toxicant (exposure and/or concentration) until irreversible pathological effects impair metabolism itself (Calow, 1989). There are some reports of this from observations on Oz consumption (Basha et al., 1984; Le Bras, 1987) and direct calorimetry (Gnaiger, 1981). However, several reviews suggest that these kinds of results can take all possible forms, e.g. with metabolic rate increasing or decreasing continuously with the level of toxicant (e.g. Calabrese et al., 1977; McKim et al., 1987). There are, however, many problems in obtaining and inte~reting these kinds of data: (a) O2 consumption is sensitive to a wide range environmental conditions, apart from toxicants, and not all these have been properly controlled in the experimental work; (b) it is

4 P. CALOW

usual to recognise various components of total metabolism-basal, standard, active, etc-and not all these need respond in the same way or synchronously to environmental stresses (Newell, 1979). For example, in some recent experiments on ~a~~n~ we (Baird et al., 1990; Barber et al., 1990) demonstrated that though there was circumstantial evidence for the deployment of stress-resisting mechanisms under chronic exposure to toxic chemicals, there was no significant increase in O2 consumption. However, under these circumstances, there was a reduction in food intake and hence in the metabolic costs associ- ated with this. Therefore, an unchanged metabolic rate here indicated that a greater proportion of total respiratory metabolism was concerned with mainten- ance; (c) the resistance/repair processes might be more-or-less protracted relative to the level of toxi- cant, with the former giving the impression of a continuously reducing and the latter a continuously increasing response with toxicant (Calow, 1989); (d) toxicants might uncouple oxygen consumption from phosphorylation (Slater, 1963), and so increasing oxygen consumption might not be indicative of the rising costs predicted by the model. In some recent unpublished work we have measured oxygen con- sumption in chironomid larvae after increasing levels of whole-body gamma irradiation. Here there is unlikely to have been uncoupling of phosphorylation, but we did observe first an increase and then a decrease in O2 consumption with increasing dose- confirming the model (Aly and Calow, unpublished).

being applied (but see below). Certainly, heavy-metal tolerant strains of several species of flowering plant have lower production rates than non-tolerant eco- types when grown in “clean” soil (Cook et al., 1972; Wilson, 1988). The trade-offs between individual growth rate and survival rate for a variety of species of fishes (Beverton and Holt, 1959) and sea urchins (Ebert, 1982, 1985) could be because some species invest more in survival at the expense of growth. Finally, field data comparing resistant and suscep- tible genetic strains of animals in stressed and un- stressed environments, indicate that whereas resistant strains are fitter under the appropriate stress, they are less fit in unstressed environments (review Sibly and Calow, 1989-their Table 1).

To summarise, there is some good, but not decisive, evidence for appreciable costs of stress resistance. This needs further research on the costs of particular processes, the careful measurement and partition of metabolic rate under stress, bearing in mind the complications likely from the uncoupling of phos- phorylation, and the effects on production in tolerant and non-tolerant strains under stressed and non- stressed conditions.

IMPLICATIONS FOR PROXIMATE RESPONSES

A further prediction is that more resistant geno- types within species should incur higher metabolic costs associated with resistance. Observations that more resistant genotypes often have lower rates of metabolism (Koehn and Bayne, 1989; Hoffman and Parsons, 1989) are therefore disconcerting, but do not necessarily refute the cost hypothesis-in that the lower total metabolism may be due to reductions in those components not directly associated with stress resistance (see 2b above). The partitioning of metab- olism needs more careful consideration. Moreover, the costs of stress resistance may only be apparent under stress once the resistance processes are induced (this is an assumption of the graded response and will be discussed further below).

By “proximate responses” I mean those that occur immediately upon application of the chemical toxi- cant and over the short (ecological) time-span there- after (Mayr, 1961). These are often measured in terms of “physiological” responses, since they can be as- sessed relatively easily and quickly, but it is usually understood, implicitly if not explicitly, that they can be related to population and ecosystem level effects.

3. Direct measures of production

It follows that if metabolic costs are increased in response to toxicants (and energy income is un- affected), production processes must be reduced. That is, there should be a trade-off between capacity to survive toxic stress and growth rate and reproduc- tive output (Sibly and Calow, 1989).

Scope for growth (difference between energy in- come and expenditure = production in energy bud- get) has been observed to reduce under conditions of toxic stress for a variety of aquatic animals in both field and laboratory situations (e.g. Bayne et al., 1979; Naylor et al., 1989). However, care needs to be exercised here in that toxicants often impair energy intake (“supply side” effects-see Baird et al., 1990) and this can dominate the metabolic response (“de- mand side” effects-see Baird et al., 1990).

There are models that make explicit links between energy budget descriptions of individual physiology and the dynamics (i.e. change in abundance) of their pop~ations (Kooijman et al., 1989; Nisbet et al., 1989; Hallam et al., 1990). These presume functional relationships between the energy allocation to repro- duction (from the fraction of energy committed to producing propagules and their individual sizes) and the time between life-history events (from the fraction of energy committed to somatic growth and the form of growth curves) but have largely ignored the conse- quences for survival of investing in increased main- tenance. The potential problems that arise from the latter are illustrated in the interpretation of scope for growth (above). This has frequently been used as a population-relevant index of stress, because re- ductions in it signal reductions in production and hence fecundity and growth (and from the latter, time between birth and breeding and breeding periods). However, a reduction in scope for growth might be a consequence of increases in maintenance metab- olism, due to the deployment of stress-resisting mech- anisms. The consequent enhanced survival of individu~s might compensate for reduced recruit- ment in terms of changes in abundance. The precise outcome depends upon the exact form of all the functional relationships involved (Calow and Sibly, 1990) and these, therefore, deserve more thorough investigation.

These trade-offs will be particularly obvious if the At the community/ecosystem level there are also extra costs are incurred even when there is no stress obvious consequences for costs associated with stress

Costs of combating chemicals 5

resistance. If these kinds of costs are incurred gener- ally, then there will be an increase in observed R/B ratio, and a reduction in P]R and P/B ratios (where P = production; B = biomass; R = respiratory heat loss-all usually intended to apply to whole trophic levels). A further consequence of this is that the imbalance may make the ecosystem more dependent upon energy sources from outside (Margalef, 1975). Odum (1985) has already predicted these metabolic trends in ecosystems under stress, but on the basis of rather general the~odynami~ arguments.

IMPLICATIONS FOR ULTIMATE RESPONSES

Not all genotypes are likely to respond in the same way to toxic stresses. There are at least two possibil- ities: (1) different genotypes might occupy different positions on the trade-off curves between investment in resistance (i.e. due to differential ability to deploy stress-resisting mechanisms defined under Introduc- tion) and production and (2) different genotypes might vary in their ability to shift to different points on the trade-off curve depending upon conditions (i.e. due to differential ability to induce stress-resisting m~hanisms).

Long-term exposure to chemical toxicants might favour either one of these kinds of evolutionary (ultimate) responses; the former (1) would lead to a fixed adaptation-i.e. increased resistance at the ex- pense of reduced production; the latter (2) would lead to a facultative (inducible) adaptation-i.e. a capacity to “switch on” energy~x~nsive stress-resisting pro- cesses at appropriate times. Which will evolve will depend upon the frequency of occurrence of the stress, and the genetic variance from which selection can be effected. Fixed responses have been docu- mented in flowering plants (see under Evidence for Costs-3), but appear to be less obvious in animals where inducible responses have been doc~ented (e.g. our work on Duphniu; Baird et al., 1990; Barber et al., 1990). It seems possible that this might be related to mobility; terrestrial plants are stuck with relatively fixed conditions whereas animals can move into and out of polluted patches. This difference deserves further consideration.

The word “might” was used to qualify the predic- tion that chemical stresses will favour resistant geno- types, i.e. investment in the mechanisms that ameliorate the toxic effect of these chemicals. There are two other alternatives: (1) it might pay to take the risk of being poisoned for the sake of growing rapidly; (i.e. invest less, not more, in defence) so that the time between breeding events is reduced and hence the mortality rate over this period will, by definition, be reduced. Whether this will be favoured depends, importantly, on the form of the trade-off curve and the way that that itself responds to stress (Sibly and Calow, 1989). Interestingly, it follows from this that we should expect more to be invested in general defence structures in more benign environ- ments with high potential production than in more stringent environments with low production. This “defence release hypothesis” could explain the latitu- dinal increase in predator-defences towards the equator in certain molluscs documented by Vetmeij (1978) but not explained by him in this way (cf. Sibly

and Calow, 1989); (2) as well as, or possibly in place of, these direct evolutionary responses to stress there can also be indirect ones (Maltby et al., 1987); i.e. impai~ent of one component of fitness by a toxic stress (e.g. growth rate) might favour genotypes that start bigger. Such indirect, life-cycle responses have been documented in one population of aquatic invert- ebrates (Maltby et al., 1987).

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