Justification and Merits of the Ecosystem Approach

Version 1 - 14/10/2010

Justification and merits of the ecosystem approach

Preliminary list of participants: F. Bréchignac, S. Carroll, S. Fuma, L. Håkanson,L. Kaputska, I. Kawagushi, L. Monte, T. Sazykina

1. Introduction: statement of the problem

The effects of ionising radiations on biological systems can occur at different levels of organisation: cells, organs, individuals, populations and communities. From an ecological point of view, populations and communities are of greater concerns. Nowadays, a significant interest is devoted to the protection of the environment from ionising radiation in an ecosystem-centred perspective (Bréchignac and Doi, 2009).

The expression “ecosystem approach to environmental protection” indicates that we are concerned with three main classes of effects:

a)The effects of radiation on biota

b)The effects of radiation on species populations as components of the ecosystem;

c)The systemic effects of radiation on the ecosystem as a whole.

Although the first kind of effects is of paramount importance for protecting the individuals of living species and for evaluating the consequences of radiation on the population dynamics, our analysis will focus on the systemic effects that are particularly important in an ecological perspective and that more strictly complies with commonly shared assumptions as those stated by the Convention on Biological Diversity ( asserting that :

“Ecosystem functioning and resilience depends on a dynamic relationship within species, among species and between species and their abiotic environment, as well as the physical and chemical interactions within the environment. The conservation and, where appropriate, restoration of these interactions and processes is of greater significance for the long-term maintenance of biological diversity than simply protection of species.”

In principle, the protection of the ecosystem from the ionising radiation, in an ecological perspective, requires that three main issues are addressed:

a)How to assess the effects of ionising radiation at level of the ecosystem;

b)How to identify and select suitable objectives for the protection of the ecosystem;

c)How to measure the level of achievement of these objectives (indicators).

The above listed issues are in agreement with traditional principles generally accepted within the frame of management theories based on the identification of effects, objectives and indicators.

As we have previously emphasised, “ecosystem” and “systemic level” are the keywords of the present analysis. We assume that the structure, the evolution, the functioning mechanisms of the ecosystem rather than the response of individuals are of significance within the perspective of the approach we are considering.

However, before we debate the subject of our concern, we should answer a basic question: does ionising radiation affect mechanisms that are eminently of ecological rather than merely of biological nature?

In the following sections we will try to give an affirmative answer to this question in order to justify the ecosystem approach to environmental protection.

1. The goal to protect populations

Many ecological risk assessments identify the population(s) as being the most relevant and pertinent object of protection. Nonetheless, the overwhelming majority of assessments of ecological risks of environmental chemicals (for example) are still based on an individual-level approach. It is of importance to note that the relative rarity of assessments that focus on population characteristics does not result from the absence of a scientific foundation or understanding, but rather from the lack of concerted effort to advance their use in a risk management context.

An operational definition of the population is essential to examine the biological and ecological context necessary for risk assessments. Roughgarden (1996)[L1] defined the population as a group of individuals that are genetically and reproductively connected so that the transfer of genetic information to the next generation is greater within the group that between groups. Although the individuals provide the means, reproduction for obligate sexual organisms is a population-level property. A ramification of this definition is that the individual organism is ecologically insignificant unless placed in the context of a population. The population provides the individual mates, a gene pool for genetic recombination, social structure, modified habitat, and all other information necessary for the survival and transmission of the genetic information of the individuals to the next generation.

There have been many published calls for ecological risk assessment that would consider risks to populations, no more simply to individuals. The main reason for that is that all individuals eventually die, whereas populations persist in the long run. This is why interest in population-level ecological risk assessment has dramatically increased within both, the scientific and regulatory communities. SETAC in particular is advancing the practice of population-level ecological risk assessment by establishing a framework for population-level assessment that includes definition of goals, identification of appropriate assessment methods, specification of data needs for different types of assessment applications, and development of a technical framework for integrating population-level consideration into risk management decisions. Such developments have been prompted by the consensus recognition that individual-based assessments are inadequate for the prediction of the ecological fate of a species-specific endpoint.

1. New ecological/ecosystem theories

As opposed to the classical approach to presenting the impacts of toxicants upon various aspects of biological and ecological systems, as depicted on Figure 1, a new framework is now proposed that incorporates complexity theory. Essentially, the basic format of this framework features two distinct different types of structures that concern risk assessment (Figure 4[L2]). Living organisms have a central core of information, subject to natural selection, that can impose homeostasis (body temperature) or diversity (immune system) upon the constituents of that system. The genome of an organism is highly redundant, a complete copy existing in virtually every cell, and directed communication and coordination between different segments of the organism is a common occurrence. Unless there are genetic changes in the structure of the germ line, impacts to the somatic cells and structure of the organism are erased upon the establishment of a new generation. Above this individual organism level, ecological structures (non-organismal) have fundamentally different properties. Here is no central and inheritable repository of information, analogous to the genome, which serves as the blueprint for an ecological system. Natural selection is furthermore selfish, working upon the phenotype characteristics of a genome and its close relatives and not upon a structure that exists beyond the confines of a genome.

Hence, the lack of a blueprint and the many interactions and non-linear relationships within an ecosystem mean that the history of past events is written into its structure and dynamics. The many non-linear dynamics and historical nature of ecosystems confer upon the system the property of complexity. Which feature specific properties to ecosystems that are critical to how they react to contaminants.

A few points can be summarized (Cambel, 1993[L3]):

- Complex structures are neither completely deterministic or stochastic, and they exhibit both characteristics.

- The causes and effects of the events which the system experiences are not proportional.

- The different parts of complex systems are linked and affect one another in a synergistic manner.

- Complex systems are dynamic and not in equilibrium; they are constantly moving targets.

Figure 1. Individual organism and ecological non-organism structures featuring the transition to complex systems. As information passes to the complex structure, it becomes part of the history of the ecosystem (after Landis and Ming-Ho, 2004[L4]).

New ecological/ecosystem theories (especially thermodynamical) are currently being developed that result in a better description and understanding of the behaviour of complex ecological systems (cf. In particular Jørgensen,2006a, 2006b; Müller et al., 2000; J. Kay[L5]).

1. Impact of ionising radiation on theecosystem: theoretical aspects

The exposure of individuals to ionising radiations can cause increases in lethality and morbidity, modifications of fertility, shortening of life span. These effects directly influence the size and the age structure of the species populations and can be modelled, in principle, by determining the values of some population parameters, such as the birth and death rates, as functions of the doses to individuals of different age classes (Woodhead, 2003). The effects,by altering the relative abundances of the different species in a given ecosystem,may influence the interaction among the species and, consequently, the structure of the communities and of the whole ecosystem.

It is well known that the inter-specific interaction can affects, favourably or adversely, both species in cases of competition, of mutualism/protocooperation and of predation/parasitism, or only one of the two interacting species in cases of commensalism and of amensalism. The induction of indirect effects on one species in consequences of the exposure to ionising radiation of the other species can occur as summarised in Table 1.

Table 1. Emergence of possible effects caused by altered sizes of populations exposed to ionising radiation (two interacting species).

Type of interaction / Induction of indirect effect
Competition
Mutualism and protocooperation
Parasitism and predation / Direct exposure of any of the two species can cause indirect effects on the other
Commensalism
Amensalism / Direct exposure of the neutral species can cause indirect effects on the benefited (or adversely affected) species
Neutralism / Direct exposure of any of the two species do not cause any indirect effect on the other species

However, in a complex ecosystem, the effects of exposure to radiation can “propagate” through several possible paths of the complicated web of interactions between the different species so that also neutral species can be indirectly affected.

The alteration of the characteristics of a species population is an effect of paramount importance from an ecological, systemic point of view.

Furthermore, ionising radiation can affects the mechanisms of interaction between species. For instance, the deterioration of the health status of predators and preys may alter the effectiveness of attack and of defence and, consequently, the predation rates.

The alteration of the abundances of the species populations and the modification of the interaction mechanisms are not the only possible changes in the ecosystem structure as they can initiate, following the reduction in size or the destruction of a population, further processes of ecological relevance such as the immigration from contiguous areas of individuals of the same species or the colonisation of the habitat by invasive species. The modification of the seral stage can be a dramatic manifestation of the impact of radiation on the ecosystem structure.

In conclusion, from the ecological point of view, the effects of ionising radiation can be grouped in three broad categories:

a)Alteration of the characteristics (f. i., size and structure) of each species population;

b)Alteration of the mechanisms of interaction between different species;

and, in consequence of a) and b),

c)Alteration of the ecosystem structure.

All the above mentioned effects depend on the intensity and the duration of the exposure and on the sensitivity to the radiation of the ecosystem.

Figure 2 depicts a generic ecosystem structure. Boxes and arrows represent species and possible interactions among species, respectively. Intuitively, our previous discussion can be summarised by the naive sentence that “the ecosystem approach considers the impact of ionising radiation on the boxes (species) and on the arrows (interactions)” in the complex system showed in the figure.

Figure 2. Complex web of interactions within an ecosystem.

For the sake of completeness, we should consider a further layer, beneath that showed in Figure 2, representing the physical or abiotic components of the habitat of the organisms. Indeed, at least in principle, the exploitation of these components can be affected by environmental noxious agents. An obvious example is the possible impairment of the photosynthetic processes in plants. Poor health status of animals can cause a less effective exploitation of the physical habitat with potential consequences for the survival and the reproduction. However, at our knowledge, the scientific literature do not report examples of such kinds of effects of ionising radiation for animals. On the other hand, in the case of vegetation, the effects are generically described in terms of impaired growth and development of species and destruction of biomass.

1. Impact of ionising radiation on the ecosystem: empirical studies

In the previous section we have tried to develop the rationale for motivating the ecosystem approach for the protection of the environment. The above considerations are of theoretical nature, however most of them are supported by the results of many investigations.

The effects of ionising radiation on populations of living organisms was the subject of a great deal of studies. According to Real et al. (2004), in the frame of the activities of the FASSET project, a comprehensive database relevant to plants and animals was created accounting for the information available for over 1000 references. This literature review listed effects such as the increase in mortality and morbidity, life shortening, reduced fertility and fecundity which, as we have previously emphasised, induce changes in the size and the age structure of the exposed populations and can initiate, in principle, modifications of the ecosystem structure. The reduction of populations of wild species is one of the most commonly described effects in highly contaminated areas from the most severe nuclear accidents (Sazykina and Kryshev, 2003; 2006). However, some effects that more directly concern the ecosystem features, such as the reduction of species diversity (reduced diversity of lichen communities, Brodo, 1964; Woodwell and Gannutz, 1967) were observed. Unluckily, the most catastrophic ecological effect, the destruction of the ecosystem (the lake Karachai in Southern Urals), was also reported in the literature (Kryshev and Sazykina, 1998). The interesting observations that mice in the Kyshtym heavily contaminated area become more frequently victims of predatory birds and that the resistance to parasites of some species can deteriorate are the most obvious examples of effects on the mechanisms of interaction between species (Sazykina and Kryshev, 2006). Fuma et al., 2010 performed laboratory experiments to investigate the response of a microbial community to  irradiation demonstrating the importance of interspecies interactions to explain the modification of the relative abundances of the different populations in the studied microcosm.

5.1Sensitivity to Toxic Agents

If there is no difference in sensitivity to toxic agents between ecosystems and single species, the single-species approach may be sufficient for ecotoxicity evaluation because of its simplicity. On the other hand, if there is difference in sensitivity between ecosystems and single species, the ecosystem approach is required for more precise ecotoxicity evaluation. It is likely appropriate to partially justify the ecosystem approach from sensitivity to toxic agents, because in some cases ecosystems have different sensitivity from single species while in the other cases they have similar sensitivity to single species as shown in the following examples:

<Example 1>- Polikarpov (1998) estimated “ecological masking zone” of ionising radiation, i.e., dose rate range at which no effects are observed at the ecosystem level, to be 0.1-0.4 Gy/y (10-40 μGy/h) by expert judgement based on various results including field data. On the other hand, Garnier-Laplace et al. (2010) derived a predicted no-effect dose rate (PNEDR) of 10 μGy/h by species sensitivity distribution (SSD) analysis based on single-species tests.

<Example 2>- Fuma et al. added five metals to the microcosm consisting of three species of microorganisms and the single-species culture of these constituent species, and observed effects on populations. No observed effect concentrations (NOECs) of manganese (Fuma et al. 2000), nickel (Fuma et al., 1998) and copper (Fuma et al., 2003) for the microcosm were equal to those for the single-species culture. On the other hand, NOECs of gadolinium (Fuma et al., 2001) and dysprosium (Fuma et al., 2005) for the microcosm were higher than those for the single-species culture.

<Example 3> -De Laender et al. (2009) showed by database survey that N/LOECmulti-species, i.e., NOEC or lowest observed effect concentration derived from freshwater multi-species (semi-)field testing, was higher than N/LOECsingle-species, i.e., NOEC or LOEC derived from freshwater single-species testing, in 90 % cases. On the other hand, ECx, multi-species, i.e., X % effect concentration derived from freshwater multi-species (semi-)field testing, was equivalent to ECx, single-species, i.e., X % effect concentration derived from freshwater single-species testing, when both ecotoxicity data were simultaneously obtained by same research group. They also demonstrated by theoretical ecosystem model simulations that ECx, single-species was higher than ECx, multi-species for phytoplankton but there was no difference between both ECx values for invertebrates when exposed to chemicals that directly target invertebrates. On the other hand, ECx, single-species was higher than ECx, multi-species for both phytoplankton and invertebrates when exposed to chemicals that directly target phytoplankton.

<Example 4>-Maltby et al. (2005) compared 5 % hazardous concentrations (HC5)*1 derived from SSD analysis of single-species acute toxicity data with NOECeco-LOECeco*2 ranges derived from (micro)mesocosm studies for 16 insecticides, and demonstrated that the lower HC5s (95 % confidence) of most insecticides were less than the NOECeco-LOECeco ranges in both single and multiple/continuous applications. They also showed that the median HC5s (50 % confidence) of most insecticides were lower than the NOECeco-LOECeco range in single applications. On the other hand, in multiple/continuous applications, the median HC5s of the half insecticides were in the NOECeco-LOECeco ranges while the median HC5s of the other half insecticides were higher or lower than the NOECeco-LOECeco ranges.