Whilst the subject of ‘acid rain’ has received a great deal of attention from the mass media, focusing on dramatic toxic effects and the ensuing political arguments, the scientific studies have been slowly forging ahead. This book concentrates on one aspect of the problem, that of the effect of acid toxicity on the group of animals most severely affected - the aquatic animals living in fresh water.

The book results from a Symposium held at the University of Nottingham in March 1986 by the Society of Experimental Biology, when a number of scientists with expertise in this particular subject met to discuss the results of recent research into the problems. They also provided a series of articles on which this book is based. The conference was greatly helped by a financial contribution from SWAP (Surface Waters Acidification Project) – a research organisation jointly administered by the Royal Society of London, The Norwegian Academy of Science and Letters and the Royal Swedish Academy of Sciences.

The aim of the book is to cover a wide range of investigations taking place in both field and laboratory and to provide the necessary scientific background information for present and possible future approaches to the problems facing animals living in acidified fresh water. Starting initially with the environment in order to assess why problems have arisen in particular areas, the volume then deals with field and survival studies on invertebrates and vertebrates in order to examine the extent of the biological problem and the attempts which have been made to relate water quality and the susceptibility of animals.

Introduction

The devastating effects of acid precipitation (resulting from the conversion of atmospheric oxides of sulphur (SO2) and nitrogen (NOX) to sulphuric and nitric acid), on lake fauna and flora have been well documented (Likens & Borman, 1974; Leivestadt et al., 1976; Harvey & Lee, 1982). Losses of freshwater fish populations from such affected areas have been recorded (see, for example, Leivestadt & Muniz, 1976; Harvey, 1979, 1982) and possibly because of their great economic value many physiological studies have concentrated on the effects of acid exposure on fish (reviews by Wood & McDonald, 1982; McDonald, 1983; Wood, this volume). Decreases in invertebrate populations have also been reported (Abrahamsson, 1972; Aimer et al., 1974; France, 1983, 1985), but this has stimulated rather few studies on physiological disturbances resulting from acid exposure in invertebrate animals. Interestingly, the few studies which have been undertaken have shown invertebrates to be more tolerant to acid exposure than fish, or more accurately, than those few, mostly salmonid, fish on which physiological studies have concentrated.

A second common feature of the fish studies is that they have mostly used sulphuric acid (H2SO4) as the acid stressor. While H2SO4 precipitation still remains a most serious problem, in recent years emission of SO2 have declined while those of NOX have continued to rise. Despite this, few studies of the physiological effects of nitric acid (HNO3) pollution on aquatic animals have been carried out.

Introduction

The areas of North America and Northern Europe from which decline of fish populations in acid waters (pH ≤5.6) has been reported are usually characterised by high levels of precipitation and by weathering-resistant bedrock, resulting in poor soils and surface waters very low in dissolved substances ([Ca] ≤100 μmol l-1, 4 mg l-1; conductivity ≤60 μS cm-1) (reviews: Haines, 1981; Spry et al., 1981; Harvey, 1982; Harvey & Lee, 1982; Howells, 1983; see also papers in this volume by Brown & Sadler; Mason; Turnpenny).

The streams and lakes in these predominantly mountainous areas are, consequently, vulnerable to rapid and large changes in their chemistry. The soil may frequently be waterlogged or frozen, and may be thin or absent altogether (at bedrock outcrops and scree slopes). Episodes of heavy rainfall or snowmelt may therefore result in more or less direct runoff into the water bodies. The low concentration of dissolved substances in the water bodies ensures that the ability to buffer changes in acidity is poor, and concentration changes caused by runoff episodes are likely to be relatively large. The pH of the water may fall dramatically during such episodes (Tables 1, 2).

From time to time, fishkills (particularly of Salmonidae) are observed in such waters (Table 2), occurring over short periods (hours or days) and coinciding with increased water discharge associated with heavy rain, snowmelt or release of artificially impounded water.

Introduction

‘Acid Rain’ as a scientific and political issue has advanced since early claims of ecological damage were first formulated in the 1950s and 1960s from the initial, rather simplistic, assumptions and interpretations that could be formulated as a sequence of events initiated by the emission of SO2 from fossil fuel combustion, the formation of acidic radicles in the atmosphere which were then removed by rain and deposited; the rain falling in unbuffered waters rendering them acid by progressively consuming their alkalinity.

Following this early conceptualisation, the contributions of N gases and ammonia were later accepted, as well as the complexity of chemical reactions in the atmosphere and the alternate mechanisms of deposition. Hydrological and geological characteristics of catchments were also recognised as major influences determining the quality of surface waters which were thus distinguished from atmospheric deposition. The ‘susceptibility’ of a lake or stream was seen to be dependent not only on the rate of acidic deposition but also on the supply and/or depletion of alkaline materials leached from soil and weathered from rock. Where loss is not matched by supply from leaching and weathering, these materials become depleted in surface waters. It is recognised that this may eventually become intolerable for some aquatic species although others may be able to exploit the resultant loss of competition. Initial concern was expressed for fish, reported as lost from the affected lakes and rivers: other biological components of the aquatic ecosystem are reported to be similarly restricted.

Introduction

Stony streams normally contain a characteristic fauna of benthic macroinvertebrates, prominent among which are insects, especially Ephemeroptera, Plecoptera, Trichoptera and Diptera. Also present are flatworms, oligochaetes, a few malacostracan crustaceans and molluscs. In streams with moderate alkalinity and a pH of about 6 or more, the fauna is rich in total numbers of species (usually there are some 70–90 taxa) and many of these may be abundant. In acid streams where the mean pH is below 5.7–5.4, however, there is a distinct change in faunal composition. Some taxa disappear or become scarce, particularly mayflies, some caddisflies, crustaceans and molluscs. The fauna is thus impoverished in species and may contain only half the number of taxa found in less acid (soft water) streams.

For instance, in the upper River Tywi in west Wales a diverse fauna of 60–78 taxa occurs in streams containing mean concentrations of at least 85 μequiv l-1 calcium and magnesium, with mean pH 5.6 or above. At mean pH 5.3 or below, and slightly less calcium, only 46 taxa were found and these were generally sparse (Stoner, Gee & Wade, 1984). A similar reduction in numbers of taxa occurred at reduced pH in lowland streams of the Ashdown Forest in southern England (Townsend, Hildrew & Francis, 1983; Hildrew, Townsend & Francis, 1984).

Introduction

Adjustment of pH is one of the central tasks for homeostatic regulation. Deviations from certain set-point values may result in reduced metabolic performance, due to the enzyme activity of metabolic energy-producing processes having pronounced pH optima. Accordingly, any net endogenous production or exogenous induction of acid–base relevant ions has to be counteracted by equivalent removal from the body fluids in order to maintain steady state conditions.

The regulatory mechanisms available for this purpose are in principle the same in all classes of animals, but are (or can be) utilized to variable extents. The situation of fishes is characterized by their intimate contact with the aqueous environment, including utilization of water as a gas exchange medium. Immersion in water favours ion transfer mechanisms supporting acid–base regulation, but also entails severe restrictions for the regulation of Pco2 in the body fluids. This chapter will briefly delineate and discuss the basic principles of acid–base regulation in fishes with respect to their theoretical limitations, and to their relative importance for the regulation of acid–base homoiostasis in fishes. The selection of references was limited by space, and review articles have been cited wherever possible to provide greater access to the subject. This chapter leads directly into Chapter 6 by J.N. Cameron, which explores the exogenous and endogenous variables affecting acid–base regulation in fishes.

Buffering

Buffering is a mechanism for transient acid–base regulation. Surplus H+ are transferred into the non-dissociated state and masked by association with buffer bases.

Introduction: modules and architecture

The shape of the canopy influences many important aspects of the growth and development of plants and such effects are felt at many levels. Differences in canopy form may affect not only how much photosynthetically active radiation is intercepted by plants but may also regulate the spectral composition of radiation that filters to lower levels in the canopy and thus have photomorphogenetic consequences. The extent of shading both by and from close neighbours will also be affected by canopy shape, as will the degree of presentation to, or concealment from, consumers of nutritious foods such as fruits, leaves and buds. In a more agricultural context, canopy arrangement influences the extent to which disease spores or the droplets of a chemical designed to kill them (or prevent their development) can enter infectable zones.

The above ecological repertoire of plants is linked directly to their gross form and invites an obvious question concerning their evolution, namely: does the architectural ‘type’ of a plant have a rôle in the (Darwinian) fitness of an individual or, in other words, have certain whole plant forms been selected during evolution while others have been less successful?

This question forms the major theme of this chapter although Fisher (1984) has recently considered a similar topic. In addition, in order to better understand the mechanisms behind the magnificent variability in plant form that we see, some recent experimental data indicating the rôle of genomic changes in determining plant shape will be presented.

In most studies of crop canopies or of the foliage of single plants, all leaves are treated as if they have the same properties. This is done so that we may make generalisations about the ways in which plant or crop growth rates may be interpreted as a function of leaf area. There is no gainsaying that this approach with its underlying assumption has been profitable. Concepts such as leaf area index (LAI) and net assimilation rate (NAR) have contributed greatly to our understanding of how a photosynthetic surface contributes to determining the growth rate of plants. However, the assumption is false.

The leaves on a plant or in a crop form a population, an assemblage of things that can be counted, and they are manifestly not all the same. Their heterogeneity derives in part from the fact that they (like a population of rabbits in a field or of blue tits in a woodland) are not of the same age and change their properties as they age. They are also borne in different positions relative to each other and their positions determine which leaves shade which. The positions that they occupy in a canopy are also related to their age – in general, young leaves are found in the fringes of a canopy with older ones in their shade.

Population biologists have much experience of studying the behaviour of age-structured populations and the aim of this chapter is to explore how far the study of populations (demography) may contribute to the study of plant canopies.

Introduction

The term ‘acid water’ is variously defined in the literature, but it is usual to adopt an upper limit of pH 5.6, equivalent to the pH of pure water in equilibrium with atmospheric carbon dioxide. The UK Acid Waters Review Group (1986) thus defines three categories of water with respect to acidity:

1. (i) ‘permanently acid’: pH usually < 5.6, alkalinity zero or close to zero;

2. (ii) ‘occasionally acid’: pH occasionally < 5.6, low alkalinity;

3. (iii) ‘never acid’: pH never < 5.6, well buffered.

Although no survey of acid water distribution in the UK has ever been undertaken, the likely distribution can be inferred from the combination of solid and drift geology and soil type. Maps of these characteristics are given by the UK Acid Waters Review Group (1986), and a composite map is shown in Figure 1. This indicates a probable distribution of acid waters in the UK, predominantly to the west and north.

As far as fish are concerned, the definition of an acid water is arbitrary. Fish have been shown to exist in a wide range of pH levels, from 3.5 to 11; also, their response to acid conditions is determined by a complex of other factors such as related increases in toxic metal levels or indirect effects upon food organisms (Alabaster & Lloyd, 1980; Howells, 1983). The purpose of field studies is to establish the net effect of these combining or competing factors on fishery status.

Introduction

Plant canopy structure is the spatial arrangement of the above-ground organs of plants in a plant community. Leaves and other photosynthetic organs on a plant serve both as solar energy collectors and as exchangers for gases. Stems and branches support these exchange surfaces in such a way that radiative and convective exchange can occur in an efficient manner. Canopy structure affects radiative and convective exchange of the plant community, so information about canopy structure is necessary for modelling these processes.

In addition to considering how canopy structure and environment interact to affect the processes occurring in the plant community, the influence of the canopy on the environment should also be considered. The presence and structure of a canopy exert a major influence on the temperature, vapour concentration, and radiation regime in the plant environment. Interception and transmission of precipitation are also affected, as are soil temperature and soil heat flow. Canopy structure can therefore be important in determining the physical environment of other organisms within the plant community, and can strongly influence their success or failure. Plant canopy structure can indirectly affect such processes as photosynthesis, transpiration, cell enlargement, infection by pathogens, growth and multiplication of insects, photomorphogenesis, and competition between species in a plant community. The indirect influence on soil moisture and temperature can also affect root growth, evaporative water losses from the soil, residue decomposition and other soil microbial processes.

Growth analysis – old and new

When a canopy of leaves is sunlit, photosynthesis proceeds at a rate which depends on how photons are distributed over individual elements of the foliage and on the relationship between photosynthetic rate and irradiance for each foliage element. In principle, therefore, photosynthesis by a canopy, expressed per unit of ground area rather than per unit leaf area, can be estimated from a statistical description of irradiance as a function of leaf disposition. In many models of productivity, this is a central and complex component. In practice, however, modelling can often be greatly simplified with little sacrifice of precision by exploiting the observation that, at least during vegetative growth, uniform stands produce dry matter at a rate which is almost proportional to the amount of radiant energy intercepted by the canopy. In this chapter we consider the theoretical basis of this relationship, its experimental verification, and its usefulness for exploring the dependence of growth on environmental variables in general.

Traditional growth analysis is based on the observation that, when single plants are exposed to a more or less constant environment, their rate of growth is approximately proportional to their weight and to their leaf area until a significant fraction of older foliage is shaded by younger foliage. Consequently, relative growth rate (RGR) and net assimilation rate (NAR) are conservative indices of growth initially.

Introduction

The previous chapter (Heisler, this volume) describes the physiological mechanisms responsible for acid–base regulation in fishes. This chapter follows directly from Heisler's account and describes the physiological effects of and responses to exogenous variables (temperature, oxygen and carbon dioxide levels and pH) and endogenous variables (exercise, feeding and anaemia) which affect acid–base regulation and may limit the survival of fish.

Exogenous perturbations

Temperature

(i) Physico-chemical basis Temperature affects the acid–base status of fish because it affects the chemical equilibria both of water and of the principal buffer systems of the blood and intracellular fluids. A small part of pure water is normally dissociated into H+ and OH-; at 24 °C the quantity of each is 10-7M, and the pH is 7. At 0 °C, however, dissociation is reduced so that the pH of pure water is 7.47, and at 37 °C it is 6.81. Temperature also influences the important physiological buffers to an extent dependent upon the value of ΔH° (the latent heat of ionization) for each dissociation reaction. This value for water is about 7000 cal mol-1, but varies from only about 2200 for the bicarbonate system (which has a very flat temperature response) to more than 8000 for certain protein groups (Cameron, 1984; Reeves, 1976; Reeves & Malan, 1976). An important aspect of these temperature-induced changes in acid–base status is that they determine the net charge of proteins; the net charge in turn affects many biochemical properties, especially of enzymes (Somero, 1981).

Introduction

Over the past 15 years a number of studies have focused on characterising diurnal leaf movements that occur in a variety of plants in response to the sun's movement across the sky. It is now clear that these solar tracking leaf movements are triggered by a directional light stimulus and that these movements result in at least a partial regulation by the leaf of the intensity of the incident photon irradiance. The purpose of this chapter is to review what is known about the different kinds of leaf solar tracking movements, their impact on primary productivity, and the potential ecological roles of these phenomena.

Solar tracking is an expression applied to describe the heliotropic movements of both leaves and flowers; it denotes the ability of these structures to move in response to the diurnal change in the sun's position in the sky. Heliotropic movements are distinguishable from other directional types of growth by their rapidity, the reversibility and by the overnight resetting to face the morning sun (Yin, 1938). Two main kinds of diurnal movements are recognised: diaheliotropic movements in which the leaf lamina remain oriented perpendicular to the sun's direct rays and paraheliotropic movements in which the leaf lamina are oriented obliquely to the sun's direct rays (Ehleringer & Forseth, 1980). In the extreme cases of paraheliotropism, the leaf lamina may change from nearly perpendicular to the sun's rays to an orientation parallel to the sun's rays.

Introduction

An animal's food choice is constrained by its metabolic requirements and by the functional anatomy and physiology of its digestive tract. In this chapter I consider how these constraints operate, and how their effects vary with body size. For example, larger animals generally eat more food per day than smaller animals. However the more critical sorts of questions that I will ask are these:

1. Does a 5000 kg elephant bull eat 1000 times as much food per day as a 5 kg dikdik?

2. What allometric relation best predicts the trend in food intake with increasing body mass?

3. Do particular species deviate notably from the overall trend, in particular those of very large body size?

In this chapter and others of its kind I will introduce each section with a deductive proposition as to how the particular attribute being considered ought to vary in relation to body mass. I will then test whether the published data on large herbivores support or refute this starting hypothesis. The statistical technique to be used is that of least squares regression. The reader must first be forewarned of potential pitfalls in this method, as discussed by Peters (1983).

1. Standard regression techniques assume that the X-variate (i.e. body mass in our case) is measured without statistical error. Generally I will use the mean body mass for the age/sex category being considered (see Appendix I), except in those few cases where more precise figures are available for the particular animals observed. Some error may be introduced here, but it should be fairly minor on a log scale.

2. […]

In the preceding chapters of this book I have documented a variety of aspects of the ecology of those large mammalian herbivores that exceed 1000 kg in adult body mass. I have analyzed how these ecological features are related to the allometric trends evident among smaller species of large herbivore. I have pointed out a number of phenomena that appear to be characteristic of these so-called megaherbivores. I now want to draw together these threads to assess the degree to which megaherbivores share in common a distinct set of coadapted features, which can be referred to as the megaherbivore syndrome.

Faunal patterns

Only in parts of Africa and tropical Asia are the faunal communities of today representative of those that prevailed during the Pleistocene and earlier times in the geological record. In Africa the five extant species of megaherbivore make up only a small fraction of the total species diversity of large (> 5 kg) herbivores present continent-wide. The distribution of some 79 herbivore species in different ranges of body size suggests the existence of three modes in species richness: (1) at a body size of about 100–200 kg, made up largely of ruminant artiodactyls occupying savanna habitats; (2) at a body size of about 20 kg, consisting predominantly of forest duikers; (3) a small outlying blip in the megaherbivore size range, with most of these species being non-ruminants (Fig. 17.1).