How Ecosystems Respond to Stress

Abstract

Nearly all ecosystems are subject to periodic disturbances by natural events, such as flood, fire, drought, and insect infestation (Vogl 1980). When such perturbations are extreme, ecosystems of immense complexity undergo rapid transformation to systems of remarkable simplicity that are characterized by a scarcity of life forms and few or no symbiotic interactions. However, this transformation sets the stage for recovery, which allows the ecosystem to adapt to changing environments (Holling 1986). In healthy systems, therefore, these perturbations are seldom more than a temporary setback, and recovery is generally rapid (Odum 1969). By contrast to natural disturbances, anthropogenic stress is not a revitalizing agent, but a debilitating one. Stressed ecosystems do not recover; rather, further degradation may follow. Indeed, Odum et al. (1979) defined stress as a debilitating agent and perturbation (subsidy) as potentially beneficial. Anthropogenic stresses are of many specific types, but they can be classified into four main groups: physical restructuring (e.g., changes resulting from land use); the introduction of exotic species; discharge of toxic substances to air, land, and water; and overharvesting. Ecosystems lack the capacity to adapt to these stresses and maintain their normal functions and structure. Thus, stress results in a process of degradation, which is commonly marked by such signs as less biodiversity, reduced primary and secondary production, and lowered resilience (i.e., the capacity of an ecosystem to recover to its original state) to natural perturbations (Barrett and Rosenberg 1981, Odum 1985, Mageau et al. 1995). Given that regional ecosystems are unique and thus may differ considerably in their normal ranges of primary and secondary productivity, species composition, diversity, and nutrient cycling, and given that each system is exposed to unique combinations of stresses, it might be expected that patterns of response to stresses will be highly variable and unpredictable. Therefore, it is surprising to discover remarkable similarities in the response of ecosystems to stress (Odum 1985, Rapport et al. 1985, Rapport and Regier 1995). Stressed ecosystems are characterized by a “distress syndrome” (Rapport et al. 1985) that is indicated not only by reduced biodiversity and altered primary and secondary productivity but also by increased disease prevalence, reduced efficiency of nutrient cycling, increased dominance of exotic species, and increased dominance by smaller, shorter-lived opportunistic species. These signs have been well documented in a number of studies of both terrestrial and aquatic systems (Hilden and Rapport 1993, Rapport et al. 1995, Whitford 1995, Epstein and Rapport 1996, Wiehert and Rapport 1998). How might this distress syndrome pattern be explained? By what mechanisms do stressed ecosystems become degraded? Why has it proven so difficult to rehabilitate stressed ecosystems, even after the initial stresses have been reduced or removed altogether? In this article, we address these and related questions by an empirical examination of three very different regional ecosystems, each of which has had a long history of exposure to multiple anthropogenic and natural stresses. We selected study areas based on three main criteria: our familiarity with the history of these regions, the extensive documentation of both stress pressures and responses over a relatively long period of time, and the contrasting nature of the structure and function of these systems. Analysis of such case studies could be carried out at many levels of organization, ranging from communities to ecosystems, landscapes, and entire regions; our analysis covers this broad spectrum but focuses primarily on the ecosystem level. The Laurentian Great Lakes Basin. Before intensive European settlement in the early nineteenth century, the Laurentian Great Lakes Basin was characterized by extensive primary forests and by high abundance and diversity of mammals, fish, and waterfowl (Regier and Baskerville 1986). The fertile soils of the basin were ideal for agriculture. With rich soils, abundant supplies of wood, high-quality ore, and seemingly unlimited potential for power generation from many rivers and tributaries, the area was destined to become the industrial heartland of North America. By the mid-nineteenth century, the basin supported a thriving commercial fishery. Initially, the fishery used the abundant stocks of large nearshore benthic species, particularly sturgeon (Acipenser fulvescens) and whitefish (Coregonus sp.), both of which were overharvested and subsequently became locally extinct (Regier and Hartman 1973). Over the course of nearly two centuries of European settlement, most of the original forest cover in the southern portion of the basin (i.e., Lakes Erie and Ontario) has been replaced by extensive agricultural, urban, and industrial development. Many bays and harbors throughout the Great Lakes have been designated by the International Joint Commission on Boundary Waters (IJC) as “Areas of Concern.” These areas are characterized by heavy burdens of toxic substances, impoverished natural habitats, low biodiversity, and high nutrient loads (Harris et al. 1988, Hartig and Thomas 1988). There are 131 globally imperiled species and natural communities in the Great Lakes Basin (SOLEC 1996). Desert grasslands. The desert grasslands of North America have a long history of human occupancy (Bahre and Shelton 1993). However, degradation of these semi-arid grasslands was coincident with the development of commercial cattle ranching and the availability of well-drilling technology. The first records of major shrub and tree invasion appear after the drought of 1891-1893—a drought so severe that between 50 and 75% of the cattle in southeastern Arizona died of thirst and starvation (Bahre and Shelton 1993). By 1900, the devastating effects of overstocking were clearly recognized by government scientists (Griffiths 1901). At the present time, wind and water erosion due to overgrazing have changed vegetation patterns, erosion has led to the redistribution of soil to distant parts of the landscape, and soil compaction is common in the vicinity of livestock watering points (Figure 1). Recent evaluation of satellite imagery has documented the fragmentation of the grasslands that has followed shrub invasion and desertification (Eve and Peters 1996). Indigenous desert grasslands (Figure 2) in North America now persist only as remnant patches within a matrix of shrublands, coppice dunes, and shrub-grass mosaics (Whitford 1995). These shrub-dominated ecosystems represent alternate stable states compared to the original desert grasslands (Whitford et al. 1995). Increased degradation at cattle watering points in the Jornada Rangelands of the southwestern United States. Natural, undisturbed semi-arid grasslands in the Jornada Rangelands of the southwestern United States. The Kyrönjoki River and Estuary of southwestern Finland. The Kyrönjoki River flows into the Gulf of Bothnia (Baltic Sea), where it forms an estuary surrounded by an archipelago. Because it is a medium-sized river with a large catchment area (approximately 5000 km2), discharge shows a large seasonal fluctuation (between 4.8 and 329 m3/s; Hilden and Rapport 1993). As a result of more than four centuries of cultural stress, this system has become progressively degraded. A major factor contributing to ecological degradation is extensive physical restructuring in the catchment area, which includes loss of wetland habitat and nutrient enrichment (eutrophication) due to runoff from farming and human settlements (Hilden and Rapport 1993). The sulfide-bearing clay soils are one of the most distinctive features of the Kyrönjoki River and Estuary. These soils, which cover almost 10% of the total catchment area, generally lie no more than 50 m above sea level (Erviö 1975). Runoff from the sulfide-bearing clays is highly acidic (pH less than 5; Hartikainen and Ylihalla 1986). With increases in both soil disturbance and runoff, some areas in the lower reaches of the river and the estuary have become acidified, either seasonally or permanently. The increased frequency of acid and toxic discharges to the lower and middle reaches of the river since the early nineteenth century has resulted in many large-scale fish kills (Alasaarela and Heinonen 1984). of habitat as a result of physical restructuring of the river basin have also to the transformation of the fish (Hilden et al. four of stress that are in the degradation of one or more of the case study physical and introduction of exotic species. four were in the transformation of the Laurentian Great Lakes Basin and the desert grasslands of the southwestern United and and three of the four were in the transformation of the Kyrönjoki River and Estuary. and in stress pressures in the transformation and degradation of three different restructuring or and nutrient In the Laurentian Great Lakes physical restructuring has altered the nearshore the to the Great Lakes Basin was entire forest The result was erosion and severe runoff, which fish for both and human settlement increased and nutrient flows (Harris et al. 1988). The and of harbors to and the of to erosion process further reduced the of were to for fish in some southern were for resulting in the of and habitat (SOLEC 1996). In the nineteenth century, were a common of most in large such as the the Great Lakes to major in the is with large of or a total of the of fish into tributaries, the invasion of species, such as the sea into the Great where they have become major (Regier and Hartman 1973). the sea a heavy on the benthic fish whitefish (Coregonus and In the desert grasslands of North well-drilling and were the of human many of the desert were of water and could not be used for livestock were to water for In water were in and were on lower reaches of to of water for watering points were by as as These watering points as for the The of livestock at and watering points areas of high which in with from the restructuring also as three or more species of and from their habitat and cover to extensive areas of the desert and and Shelton 1993). to changes in and Whitford 1996). also to the of their effects on and by for soil water their extensive systems. In the Kyrönjoki River and extensive physical restructuring has human settlement for more than four In the century, the and of land rivers for followed the of changes have the of the of the of acidic and the of the of the of and in the reaches of the river (Hilden and Rapport 1993). these changes have altered the natural of both the river and the fish and waterfowl habitat and water of species are reduced as a result of in biodiversity and the invasion of opportunistic species. has had the most in the Laurentian Great Lakes Basin and the desert its effects in the Kyrönjoki River and Estuary appear to be of less In the Great Lakes has of highly nearshore and benthic and These effects have been by such as nutrient and by the sea (Regier and Baskerville Regier et al. 1988). In North desert overstocking cattle has led to of species (Figure by cattle has two major it soil soils so that they become more to wind and water and it the abundance of the the species by cattle over the been replaced by and species less to cattle (Bahre and Shelton to degradation of the A by an alternate stable over the grasslands in the Jornada Rangelands of the southwestern United States. from industrial and is a major of stress in aquatic ecosystems, but it has had a more in the transformation of terrestrial ecosystems such as desert grasslands. In the Laurentian Great from runoff, and industrial to and water have to of nearshore areas (Harris et al. and to the of toxic substances in of large fish in the Great Lakes of the human of the that have in the In waterfowl in the Great Lakes been by high levels of and its The has and in the Great Lakes Basin et al. In North desert from by in all of the cover from a with When a basin after is the for the et al. 1988). The abundance and of this is different in than it is in In the Kyrönjoki River and of and seasonal have resulted from human disturbance to soils, as discharge from human settlements and runoff from results in in the estuary and nearshore of exotic species. The of species has been particularly in changing the of the Great Lakes Basin and the desert grasslands of North America. In the Laurentian Great the introduction of and with the of natural such as the has led to a of the original fish by exotic species. In an to the and to a for the species, the was species a by the of (e.g., species; 1995). The of the sea and the introduction of the have led to further degradation of the Great Lakes Basin et al. The sea to the of the benthic fish by on and it the in the fish in the from a fish to an fish The by and has to the to a with low fish However, the to dominance by an benthic has been to such an that species from southern was to the desert grasslands of North America in in an to and was by to appear in of Arizona and et al. 1984). By this species was on of and in Arizona and et al. patches of have also been in the of southern this has to further thus the initial for which it was in many it has the (Whitford 1995). have been less of a in the Kyrönjoki River and Estuary. was into the Kyrönjoki the of the nineteenth century et al. 1984). The effects are not for but do not appear to have been after the of the has no of the ecosystem has been natural not in natural also as a stress, with anthropogenic of in the Laurentian Great Lakes for nutrient from runoff, and to the of habitat due to physical In the Kyrönjoki River and heavy runoff from soils, the of the In the desert grasslands of North periodic drought an stressed system by soil exposure and loss wind for the transformation of ecosystems and and responses (Holling and is the in which stress changes from one to that most the of the Laurentian Great Lakes and the desert grasslands of North America. In these two ecosystems, the of transformation (i.e., species and changes in species dominance and nutrient in a relatively a period of the mechanisms these changes were in in the Kyrönjoki River and by contrast to the two ecosystems in this article, have a history and appear to have more (Hilden and Rapport 1993). In all three ecosystems, were the result of multiple and stresses, in which anthropogenic stresses with natural perturbations (Regier and Hartman Hilden and Rapport 1993, Whitford et al. 1995). within the Laurentian Great Lakes Basin in in of the lower and some bays and harbors of the from one of to in which the species were replaced by exotic species. The transformation from a fish to a the or severe in (Coregonus and and the of an exotic fishery by and transformation of the Great Lakes Basin to be not to a stress, but to the of multiple stresses, habitat degradation, and the introduction of exotic (Regier and Baskerville Regier and 1996, and Regier in and that as of (i.e., of highly and habitat that and for the species that the now as of These areas have become of of and In the desert grasslands of North periodic drought, which is of the has to the of the at which grasslands have been to (Bahre and Shelton 1993, Whitford 1995). and both highly to drought, replaced the (Figure shrub and cover has some a degradation is followed in which the shrub over at even is (Whitford 1995). shrub has proven highly and to have been thus and 1995). such large areas of grasslands in the that supported are no to more than a of the cattle that were present ranching (Griffiths 1901). The more transformation of the River and its estuary from an system and to a system characterized by the increased dominance of fish has been less than the in the two systems. However, has been a marked and in the of a ecosystem that has for and has fish communities over the entire (Hilden and Rapport 1993). The main for ecosystem that the three case in are with the that Odum that are expected in stressed ecosystems, and with the signs of ecosystem distress by Rapport et al. in the of ecosystem The transformation of the three ecosystems from healthy to states three primary of nutrient cycling, by opportunistic or exotic species, and of These mechanisms are of nutrient results in a of the pattern of nutrient cycling, it from a (i.e., between and in healthy systems to a in stressed systems. In the Great for degradation of nearshore vegetation the of so that from the land were more of and used by nearshore In North desert stress nutrient by primary from and thus a of and In healthy desert nutrient of to the soil increases with the of and the of is relatively over the soil However, in stressed grasslands that have been to shrublands, nutrient is altered both and changes result from the of of to the soil seasonal and These result in temporary nutrient as soil increases in response to the of thus primary from (Whitford et al. changes in nutrient availability are of the of to of shrub in which is in a by the of and the by are in the of vegetation and the of soil erosion et al. In the Kyrönjoki River and the pattern of nutrient also In the loss of vegetation of from runoff to the and benthic of the by opportunistic or species. species that were present but become in stressed ecosystems, as do exotic species, their introduction was or Because between species have been (e.g., by natural or symbiotic ecosystem is to dominance by opportunistic and exotic species. These species are characterized by high relatively life and In the Laurentian Great Lakes for a fish species has become over the abundant and highly benthic fish (Rapport Regier et al. 1988, Regier and 1996). the initial of degradation in North desert grasslands are characterized by a in and an in The large of that are by wind and of degradation are characterized by the of such as the with that are drought such as drought, the loss of these large that are to wind and water of degradation are characterized by the invasion of and the loss of all livestock with large and exposed patches of the soil highly to further erosion and These changes have the of the the and the In the Kyrönjoki River and and are by the more In the the extensive vegetation has been replaced by or benthic of the transformation from highly to communities is the loss of In the Great and of vegetation has the original and their The loss of has been particularly such areas high species diversity and has in for nearshore fish species and of and and In the desert grasslands of North the loss of cover has to altered that the erosion thus further contributing to the loss of The loss of has an on the desert where loss of soils and cover increases to wind and water erosion to that can areas by for has also levels to to and of substances The acidic water is into the river or Because the of and toxic substances in the soils are the river water and the estuary will the of acidic for as long as the clay soils are used for (i.e., for the The and acidic the river and estuary has habitat for species, such as and (Hilden and Rapport 1993). the ecosystems in this will the mechanisms that have ecosystem However, the system has (i.e., it has become the very mechanisms that have to the transformation to In the Great for the of with the of that the communities in this ecosystem are not These changes to of and these in to the fish communities at the of the benthic fish in North desert overgrazing has resulted in the loss of of the these highly has proven difficult the loss of cover has exposed the soils, which have thus become more to erosion and even less for the of in the Kyrönjoki River and of clay soils to maintain an acidic that dominance by opportunistic species and the of the species. Indeed, for each of the case study areas in this article, have been to the degradation and ecosystem However, these by and not in a system to a healthy have been for ecosystems (e.g., in the semi-arid which to be to their et al. In the Great and have been for particularly in the of and Thomas the most highly and However, this highly ecosystem has to to healthy et al. is to that to rehabilitate the Laurentian Great Lakes have not been they have been very The in nutrient due to the of in is a has nutrient (i.e., reduced in some areas (e.g., the basin of Erie and the of in and fish stocks of more have to However, many stresses, particularly the of toxic substances of which are now by and the of habitats, and nearly the loss of the of the fish and communities that a major in the recovery of the Laurentian Great of in the of the Great Lakes is that where have been over the the of results have been to for of these not degraded. The the recovery of the fishery in the of was to the of Because wetland habitat was relatively and the primary of stress was nutrient has been a recovery of an of the original fish 1996). at in the desert grasslands of the have with less even in many areas the main been In have been some at shrub and of by of coppice dunes, and However, these have to for of lack of recovery of North desert grasslands that a process into as a of the initial invasion of the and 1995). With are the as that for further desertification by to areas the shrub in to patches that further erosion by wind and The are also well to natural further their In in which were to of for the not only but to that of within after a large the of the cover (Whitford et al. 1995). In the original desert grasslands were by the of the soils that to these soils and as a result of which were more to wind and soil for erosion now to have led to a system that desertification and in the Kyrönjoki River and Estuary are to the of However, as long as of and toxic substances in the soils and land it is that runoff from acidic clays will to the river and The from these with to rehabilitate ecosystems are to highly ecosystems do not stress loads are do not even with an from to the system and an These that has been in to the of the human that stress and the system (Rapport and Regier 1995, Rapport et al. are many for the lack of in ecosystems (Rapport and Regier 1995, Rapport et al. some common from the case studies in this systems become more to invasion from opportunistic species, which not the of the original disturbances to (i.e., soils and the for highly which on and on stable the of nutrient changes the entire of the its transformation to a system that the initial In all three mechanisms that were in the degradation of the case study areas are also in their to of mechanisms to the of to the of ecosystems, therefore, is the mechanisms that and these to the in nutrient cycling, one to and vegetation in the desert grasslands. nutrient in the Laurentian Great Lakes nutrient as well as habitat to nutrient a century the of to the of regional terrestrial ecosystems to by human to specific signs (e.g., loss of soil of species, of and in and forest by which this might be these signs not only the on which based but also the in ecosystems (Rapport et al. 1995, Rapport et al. The ecosystem distress syndrome (Rapport et al. which many features with signs of (Rapport and Regier points to as of in primary and secondary productivity, loss of biodiversity, and in nutrient cycling, and in dominance of from the life forms that are in their to smaller, shorter-lived forms that are These signs have also generally characterized the three case studies in this for in three The from an examination of these three is that the mechanisms that degradation after a in a system that further degradation even after the stresses that the transformation in are these of nutrient cycling, of opportunistic species, and of both a and a of degradation and at Ecosystems in alternate states may be highly to further to rehabilitate these altered ecosystems to into their original and the mechanisms for the this might the of the most to healthy ecosystems is to to stress pressures so that are not in was supported in by the in and a to both We are to and Wiehert for their in the history of changes in the Kyrönjoki and Great Lakes We and two for their highly We also and for their on and for in the The its of and and in the has been to the and has been as an