The nature of scale and the use of hierarchy theory in understanding the ecology of aquatic macrophytes

Aquatic Botany, 41 ( 1991 ) 253-261

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The nature of scale and the use of hierarchy theory in understanding the ecology of aquatic macrophytes A n d r e w M. F a r m e r ~ a n d M i c h a e l S. A d a m s b aNature Conservancy Council for England, Northminster House, Peterborough, PE I 1 UA, UK bDepartment of Botany, University of Wisconsin, Birge Hall 430 Lincoln Drive, Madison, W153706, USA (Accepted for publication 19 December 1990)

ABSTRACT Farmer, A.M. and Adams, M.S., 1991. The nature of scale and the use of hierarchy theory in understanding the ecology of aquatic macrophytes. Aquat. Bot., 41: 253-261. This paper discusses the importance of undertaking studies at the appropriate scale to generate correct answers to the problems posed by an investigator. An account is given of how it is easy to infer more from small-scale physiological work than is appropriate. However, we also show how such work may be usefully extended to provide answers at larger scales. Particular attention is paid to the importance of disturbance in aquatic ecosystems. This includes two case studies, the first concerning a particular experiment relating to eutrophication and the second to the general phenomenon of lake acidification due to wet acidic deposition. In both cases, observations made at different scales are found to be appropriate for understanding the response of different species. As a result, a multi-scale and multi-disciplinary approach is advocated for major research studies whenever possible.

INTRODUCTION

Those who undertake research into macrophyte ecology have asked questions at many levels of organisation. What we have to consider from a hierarchical viewpoint is whether the right questions are being asked for a particular problem and whether the right conclusions are being drawn. It is important to note that in both of these contexts we cannot divorce the nature of the investigator from the way in which science is undertaken. Each of us will approach a given problem from a standpoint coloured by our past research experience. When presented with the problems of a disappearing macrophyte from a eutrophicating lake, some will ask questions about nutrient cycling and others about the biochemistry of photosynthetic shade adaptation and competition for light with epiphytes. Of course, neither approach is right or wrong, they just provide different answers at different levels. In generating 0304-3770/91/$03.50

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conclusions we must also not forget the pressures that are associated with the presentation of science. In this context there is a great tendency to make one's work seem to be the definitive answer to as many questions as possible. This obviously facilitates publication and it is not unknown for editors and reviewers to suggest that some piece of work be "discussed in a broader context". In practice this can mean unwarranted extrapolation from small-scale physiological studies to processes in lakes themselves. In this paper we discuss the nature of scale and hierarchy theory in an aquatic macrophyte context. Much of this will be a development from our previous discussion of this subject (Farmer and Adams, 1989), though some of the basic ideas will have to be restated here. As one result of stressing the importance of larger scale processes is to cast doubt on the relevance of smaller scale investigations, we follow with a discussion of the importance of physiological work and the ways in which it can be made more relevant to lake ecology. As the role of disturbance and the interpretation of change is of considerable interest to many workers, we will also devote a section to change in macrophyte communities. Much of this discussion has to be set in a general context, so we conclude with two case studies. The first describes the importance of scale for a specific experimental study. The second shows how a correct interpretation of scale can aid in the understanding of one of the major concerns of macrophyte ecologists today. LEVELS OF STUDY

Particular approaches are relevant to particular scales. Interpretation from one scale to another is not a simple matter. The properties of, for example, a larger scale are not a simple accumulation of its components. This has long been recognised by ecologists (e.g. Odum, 1959), but its practical implications are not always followed. The confusion is often the result of h u m a n perspectives. Thus in one sense a plant community is observed as a collection of individual plants, but it is the processes that pertain to the community which shape it. These processes cannot be understood by a consideration of the individual plants alone. They can be better understood by considering that the larger scale levels provide the framework in which the smaller scales operate. These higher levels define what is or is not allowed (Allen and Starr, 1982; O'Neill et al., 1986). Pattee ( 1978 ) distinguished the terms "rules" and "laws" in defining the nature of constraints on components of a system. The rules indicate constraints imposed by the system and the laws are constraints that result from the nature of a component itself. Farmer and Adams ( 1989 ) described a series of rules and laws that pertain to macrophyte productivity at a number of hierarchical levels. Thus for an individual plant, an internal constraint on productivity may be its levels of carboxylating enzymes, while the

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external constraint may be competition for light with other macrophytes. However, at a c o m m u n i t y level this competition becomes an internal constraint. As macrophyte ecologists, we must be aware of the problem of the artificial removal of external constraints on a component of the system that we are studying, if we wish to make predictions at a higher level. It is all too easy, for instance, to remove any external constraints on photosynthesis when plants are studied in the laboratory, which makes interpretation of in situ assimilation rates very difficult. Initially, therefore, it is necessary to fix both the scale and boundaries of the study being undertaken. These must be determined not by the ways in which the data are collected, but by the patterns that are seen in the behaviour of the system (Allen and Hoekstra, 1986). Identifying scale boundaries requires detailed analysis of pattern, which may be best achieved by multivariate analysis (Allen and Starr, 1982 ). Once this is achieved then the scales at which a study should be undertaken will be more obvious. In many cases there should be an interaction of holist and reductionist approaches. Such a dialectical approach will allow a continuing redefinition and focusing of the questions being asked. THE APPROACH OF THE PHYSIOLOGIST

Some may suggest from the discussion above that there is little ecological relevance to the results of the physiologist. Does the photosynthetic rate of a carefully chosen, healthy terminal shoot of Myriophyllum have any meaning in a study of an eutrophicated lake? We believe that it does. Carefully controlled and detailed studies of the physiological ecology of aquatic macrophytes are vital to an understanding of the ecology of lakes and streams. Physiological ecology is concerned with the way in which a plant varies with alterations in the external environment and the way in which changes in the environment are accommodated by reactions in the plant (Larcher, 1980). However, a simple study of the response of a plant to a single environmental variable may be of limited value in terms of understanding its role in a lake, unless it is known to be of overriding importance. Increasingly, studies are being made of responses to multiple environmental factors (e.g. Maberly, 1986 ). This is an important avenue down which future research must go to make physiological studies more ecologically relevant. Farmer and Adams ( 1989 ) discussed how the scale of physiological investigations can be increased to provide data that are more easily interpreted in the context of the ecology of a lake. They pinpointed three ways in which past researchers have achieved this. One way is to increase the temporal scale of a study, e.g. by studies across one or more seasons. Alternatively, one may attempt to increase the spatial scale, e.g. by studying physiological responses along transects of environmental gradients or within canopies of monospecific stands of macrophytes. All of these approaches have to be combined with

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basic demographic and distributional data. In interpreting the physiological data at a higher level, we can see that it provides the internal constraints to population and community structures. In other words, photosynthetic research will show where a plant cannot grow (e.g. in water too deep for adequate light levels for net carbon assimilation). However, they cannot predict abundance within those boundaries. Abundance is often determined by interactions between species. This is a community level process, i.e. one at a higher hierarchical level to physiological measurements. C H A N G E IN M A C R O P H Y T E C O M M U N I T I E S - - SUCCESSION, D E V E L O P M E N T A N D PERTURBATION

For many lake ecologists and managers it is change in the macrophyte communities that is of most interest. Farmer and Adams (1989) discussed the limited nature of many studies of aquatic macrophyte communities in this context. It is usual that in such studies particular attention is paid to the correct spatial scale to provide adequate description of that community. However, rarely is there the possibility to study detailed changes over a long period of time. This type of information is still strikingly lacking in aquatic macrophyte ecology and yet it is vital for a complete understanding of the nature of change and development in the plant communities. We may distinguish two types of change that are perceived by most researchers. First, there is what is interpreted as succession within a lake community. Second, there are perceived perturbations. That succession occurs in mesotrophic and eutrophic lakes is well established and the process is rapid enough to be directly studied on a h u m a n scale. Some oligotrophic lakes may show almost no perceived change. It is possible, for example, that deep-water bryophyte communities may have existed with little change in the same lakes over thousands of years (Farmer, 1988 ). It is with the effects of perturbation that we wish to concentrate. This is very often seen to be of most immediate importance and particularly so when man is causing the perturbation (e.g. by the introduction of exotic species or pollution). Allen and Starr( 1982 ) distinguished the terms "disturbance" and "perturbation". A disturbance is considered to operate on a scale that is very different to the organism or system being observed. A disturbance may be so short-lived that a plant will remain unaffected, or it may be so long-lived that its entire life cycle is completed without being affected. However, if the disturbance and the plant/system in question are operating on similar scales, then the plant will react. The disturbance will act as a perturbation to the system. If these disturbances are regular (e.g. the regular drying of vernal pools, wave action, etc.) then they will become integral to the functioning of the system, i.e. they will become 'incorporated'. If the disturbance does not nor-

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mally operate at the scale in question then the system may be disrupted, it will act as a perturbation and will not become incorporated. Let us illustrate some of these points by reference to lake macrophytes. It must be remembered that the aquatic environment is often less stressful than the terrestrial. Many terrestrial disturbances are dampened or lost in water (e.g. temperature fluctuations ). However, some new disturbances may occur. Thus although a macrophyte may not experience such wide diurnal temperature fluctuations, it may experience considerable changes in diurnal carbon supply as rapid photosynthesis in dense macrophyte stands uses up free carbon dioxide during the day. Such a disturbance is regular and has become 'incorporated', e.g. by adaptations to bicarbonate use or C4-1ike metabolism. An obvious disturbance for littoral macrophytes is wave disturbance. Again this is regular and incorporation may have occurred by the evolution of morphological adaptations such as the isoetid growth form (Boston, 1986 ). Perturbations within the natural lake community are often less easy to distinguish. Obviously the removal of plants by wave action is a perturbation for those individuals, but not for the population. Even the removal of a population of plants from one part of the lake is often reversed by the invasion of propagules from other sites. The system is able to maintain an equilibrium. It is with influence of man that the most striking perturbations on a lake-wide level has been seen to occur. We can distinguish a number of different types of perturbation ranging from a few extreme cases of the complete poisoning of lakes by excessive pollution to eutrophication, acidification and the introduction of alien species. CASE STUDY 1 - - GROWTH RESPONSE TO INCREASING NUTRIENTS

The responses of macrophytes to increasing nutrient availability are of primary importance in, for example, estimating limitations of productivity and for managers investigating the effects of eutrophication. We shall consider one of the simplest studies, i.e. that of culturing plants under a range of nutrient levels. The question being addressed is: what is the response of the plant to increasing nutrient availability? However, this is not precise enough. Are we concerned with the physiological response of the plant (as measured by growth rate) or the response of the plant within a system subjected to increasing nutrients? As we shall see, the two questions are very different. Roelofs et al. (1984) cultured Littorella uniflora (L.) Aschers. under a range of increasing water column phosphorus concentrations. They found that between 0.1 and 1.0/zmol P O 4 1 - l the plants showed a positive growth response to increasing phosphorus availability, but between 1.0 and 5.0/~mol P O 4 1-1 a negative response was shown. How is this to be interpreted? The positive response can be described as a directly physiological one; however, the negative response cannot. This is because the latter was found to be due to in-

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creased epiphyte growth. In other words, the plants were not responding to phosphorus availability at all, but to competition for light. The unit being measured (growth rate) is constrained by many factors, including tissue nutrient availability. However, the culture conditions do represent a microcosm. The structure of the community (macrophyte and epiphytes) is also constrained by nutrient availability. The release of this constraint allowed an increase in competition and thus the imposition of a further constraint on macrophyte growth. Interpreting this in terms of a hierarchical structure, the highest level is that of the nutrient status of the system, which constrains levels beneath it. However, these lower levels are not on the same hierarchical level and impose further constraints on each other. Littorella uniflora is lost from lakes undergoing eutrophication and the loss may be due to increased epiphyte shading (Sand-Jensen and Sondergaard, 1981; Farmer and Spence, 1986). The results of Roelofs et al. (1984) are, therefore, useful in understanding the effects of eutrophication, although we do not know what constraints present in a lake are not present in the microcosm. The results do not tell us about the complete response of the plant itself to increasing phosphorus availability. To do this would require removing the epiphytes. To decide on such action, therefore, depends on whether one requires information about the ecology or strict physiology of Littorella uniflora. CASE S T U D Y 2 - - T H E A C I D I F I C A T I O N O F L A K E S

One of the most pressing concerns for macrophyte ecologists in Europe and North America is the acidification of poorly buffered lakes by the transport of air pollutants over long distances and the subsequent changes in lake biota, including macrophytes (Farmer, 1990). In considering the lake as the system in which all of the actions of acidification can take place, we can describe a number of processes and interpretations that are scale dependent. However, we must again define the questions that we are asking. We consider that it is the concern of most macrophyte biologists to seek an explanation for the observed changes in the lake flora. In other words, why do the populations of some species decrease and those of others increase? Let us take a particular case. Grahn ( 1986 ) summarised vegetation changes in the lakes in southern Sweden. The most striking effect of acidification is the increase in abundance of Sphagnum spp. and benthic algae and the reduction in (or even loss) ofisoetid species such as Littorella uniflora and Lobelia dortmanna L. Why does this happen? We could look for the answer at any scale that we wish. The input of acidifying substances affects the whole lake and so ecosystem level responses might be changed. However, the increase in hydrogen ion concentrations might have their effect at the cellular level. In fact, various workers have sought explanations at many different levels. Some of the most interesting work on the physiological effects of acidification has been carried out by Roelofs et al. (1984). They studied both photo-

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synthesis and nutrient uptake. The effect of acidification is to cause a reduction in sediment carbon dioxide levels and cause a shift in the available nitrogen supply from nitrate to ammonium. Both of these changes favour Juncus bulbosus L. over Littorella uniflora. The effect of the acidification is seen in terms of changes in the abiotic processes that supply the physiological needs of the plant. The increase in the growth of Sphagnum spp. can also be understood in physiological terms, in that a low pH is necessary to maintain the physiological integrity of the plant (e.g. Kilham, 1982) and that it promotes the acidification of its local environment, possibly causing a self-acceleration of the acidifying process (Grahn et al., 1974). A number of processes have been studied at the population and community level. Studies have found that the productivity of Lobelia dortmanna is decreased by acidification. Although this is an indication of physiological activity, its measurement has been undertaken within the community, either in microcosms (Leivestad et al., 1976) or in the field (e.g. Grahn, 1986). The decline in productivity may be the cause of a decline in its numbers. The reduction in productivity is usually thought to be due to overgrowth by benthic algae or periphyton, which are promoted by acidification. This causes increased competition for light and is a community level effect. Lazarek ( 1987 ) studied a possible population level response. One possible cause for the reduction in Lobelia dortmanna numbers may be through decreased recruitment. Lazarek (1987) found that germination of the seeds was not affected by the low pH or the algal mats, but that subsequent seedling survival was markedly reduced. Again this may be due to competition for light. By looking at the entire system, further factors become important. It is here that explanations are sought for the increase in benthic algal production. One of the most striking aspects of acidified lakes is their clarity. It has been suggested that the increase in available light on the lake floor allows an increase in algal abundance (e.g. Hultberg, 1983 ). However, Lazarek ( 1985 ) suggests that there is in fact no increase in production rates, but the increased biomass is due to reduced grazing and decomposition rates. To seek an understanding of the problems of lake acidification at one level would provide a very incomplete explanation. It is probable that for a given component of the system an explanation is best sought at one particular level. This may be at the physiological level for Sphagnum spp., the population/ community levels for Lobelia dortmanna and the ecosystem level for the benthic algae. As Klein ( 1984 ) has advocated, the acid rain problem for lakes must be studied using both laboratory and field work to provide an ecosystems approach. CONCLUSIONS

We have tried here to show the importance of maintaining a hierarchical perspective in the design, undertaking and interpretation of studies concern-

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ing the ecology of aquatic macrophytes. It seems evident that there is much to be learned from studying macrophytes at many levels of organisation. In fact, a complete picture is very often achieved only when studies are undertaken at more than one scale at the same time. In many cases this may be best achieved by collaboration between workers with expertise at various levels (Redfield, 1988 ). A good example of this is shown by the Long-Term Ecological Research sites in the United States and, in particular, our own experience at the Northern Lakes site in Wisconsin. It is our opinion that there needs to be much greater interaction between macrophyte ecologists of different perspectives if the increasingly complex questions of aquatic ecology are to be answered in a meaningful way. REFERENCES Allen, T.F.H. and Hoekstra, T.W., 1986. Description of complex prairies through hierarchy theory. Proceedings of the 9th North American Prairie Conference, pp. 71-73. Allen, T.F.H. and Starr, T.B., 1982. Hierarchy. Chicago University Press, Chicago. 206 pp. Boston, H.L., 1986. A discussion of the adaptations for carbon acquisition in relation to the growth strategy of aquatic isoetids. Aquat. Bot., 26: 259-270. Farmer, A.M., 1988. Biomass, tissue nutrient and heavy metal content of deep-water mosses from two ponds in the Cape Cod National Seashore, USA. Lindbergia, 14:133-137. Farmer, A.M., 1990. The effects of lake acidification on aquatic m a c r o p h y t e s - a review. Environ. Pollut., 65:219-240. Farmer, A.M. and Adams, M.S., 1989. A consideration of the problems of scale in the study of the ecology of submersed aquatic macrophytes. Aquat. Bot., 26: 247-258. Farmer, A.M. and Spence, D.H.N., 1986. The growth strategy and distribution of isoetids in Scottish freshwater lochs. Aquat. Bot., 26: 247-258. Grahn, O., 1986. Vegetation structure and primary production in acidified lakes in southwestern Sweden. Experientia, 42: 465-470. Grahn, O., Hultberg, H. and Landner, L., 1974. Oligotrophication - - a self-accelerating process in lakes subjected to excessive supply of acid substances. Ambio, 3: 93-94. Hultberg, H., 1983. Liming of acid-stressed ecosystems: induced chemical and biological effects. VDI Ber. (Ver. Dtsch. Ing.), 500: 409-414. Kilham, P., 1982. The biogeochemistry of bog ecosystems and the chemical ecology of Sphagnum. Mich. Bot., 21: 159-168. Klein, R.M., 1984. Ecosystems approach to the acid rain problem. In: R.A. Lindhurst (Editor), Direct and Indirect Effects of Acid Deposition on Vegetation. Ann Arbor Science, Ann Arbor, MI, pp. 1-11. Larcher, W., 1980. Physiological Plant Ecology. Springer, Berlin, 303 pp. Lazarek, S., 1985. Epiphytic algal production in the acidified Lake Ghrdsj6n, SW Sweden, Ecol. Bull., 37: 213-218. Lazarek, S., 1987. Germination ecology and deterioration of Lobelia dortmanna L. seeds and seedlings in acidified lakes. In: H. Witters and O. Vanderborght (Editors), Ecophysiology of Acid Stress in Aquatic Organisms, Belgian Royal Zoological Society, Brussels, pp. 449-457. Leivestad, H., Hendrey, G., Muniz, I.P. and Snevik, E., 1976. Effects of acid precipitation on freshwater organisms. In: F. Braekke (Editor), Impact of Acid Precipitation on Forest and Freshwater Ecosystems in Norway. Res. Rep. FR 6/76, SNSF-Project, As, Norway, pp. 87111.

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