Acid Rain Impacts on Calcium Nutrition and Forest Health

Abstract

Forest ecosystems throughout the world are exposed to acid rain, a complex solution consisting largely of H+, SO42−, NH4+, and NO3− pollutant ions derived from sulfur and nitrogen oxides. Although the public in the United States may view acid deposition as a localized pollution issue specific to certain regions of North America and northern Europe, recent evidence of acidic deposition throughout much of Asia, including tropical forest regions, has demonstrated that acid deposition is actually a global phenomenon (Abate 1995). Furthermore, despite downward trends in sulfate concentrations associated with reductions in sulfur dioxide emissions mandated by the 1990 Clean Air Act Amendments, the acidity of precipitation in eastern North America does not seem to be decreasing (Scherbatskoy et al. in press). For example, over the course of 10 fog events on the summit of Mt. Mansfield, Vermont (elevation 1237 m), during summer 1998, the cloud water had an average pH of 2.8, with several events of pH 2.1–2.5 (Sean Lawson and Timothy Scherbatskoy, personal communication, data on file at the School of Natural Resources, The University of Vermont). The median and minimum cloud water pH values from Mt. Mansfield are more acidic than comparable summer measurements made on nearby Whiteface Mountain, New York (elevation 1483 m), from 1982 to 1987 (pH 3.4–3.8; Mohnen 1992). These findings collectively highlight the severity of cloud water acidity engulfing montane forests in the eastern United States and the ongoing nature of acid deposition. The prevalence and persistence of acid deposition has fueled public concern about the widespread impact of acid rain on forest health. It is now well documented that anthropogenic changes in precipitation chemistry and acidity have occurred over the past several decades in North America. In addition, acid deposition-induced leaching, depletion, and cycling disruption of calcium in forest soils has recently been demonstrated (Lawrence et al. 1995, Likens et al. 1996, 1998). Cumulative estimates show that, as a result of acid deposition, the pool of calcium in the soil complex may have shrunk by as much as 50% during the past 45 years (Likens et al. 1996), a reduction that may have long-term implications even if the acidity of precipitation begins to ameliorate over time. Despite these well-documented and substantial physical changes, the extent and nature of the impact of these belowground changes on forest ecosystem health has been uncertain or only speculative. The National Acid Precipitation Assessment Program (NAPAP), in its 1992 Report to Congress (NAPAP 1992), declared that “there remains no evidence of a general, widespread decline of forest tree species caused by acidic deposition.” However, the report did conclude that “acidic deposition has been firmly implicated as a causal factor in northeastern high-elevation red spruce decline” (NAPAP 1992). Indeed, numerous field and laboratory studies have demonstrated that red spruce (Picea rubens) has suffered widespread freezing injury (Peart et al. 1991, DeHayes 1992), growth reductions (Cook and Zedaker 1992), and mortality (Johnson et al. 1986, 1992, 1996) over the past 40 years. The cause(s) of enhanced freezing injury and decline of red spruce, including the possible influence of air pollution, were a major focus of NAPAP's Forest Response Program and have been studied intensively in both North America and Europe. Red spruce decline has, in fact, become synonymous with acid rain throughout much of the Northern Hemisphere. Despite this general association, an empirically based physiological understanding of and explanation for red spruce decline have not been established. Several potential broad-based explanations have been proposed. For instance, perturbation of calcium nutrition has been identified as a potential stress factor contributing to red spruce decline (Shortle and Smith 1988, McLaughlin et al. 1993, Lawrence et al. 1995). Specifically, it has been proposed that aluminum that is mobilized in mineral soil by acid deposition reduces soil storage of calcium and its availability for root uptake (Shortle and Smith 1988, Bondietti et al. 1990, Lawrence et al. 1995). The resulting calcium deficiencies might be expected to lead to the reductions in Ca: Al ratios, sap-wood area, and live crown volumes that are evident in some red spruce trees (Shortle and Smith 1988), leaving trees more vulnerable to secondary stresses, such as diseases, insect pests, and freezing stress. Acid-induced reductions in foliar calcium concentrations of red spruce in the southern Appalachians have also been linked to increases in dark respiration and reductions in net photosynthesis, which could also contribute to decline symptoms (McLaughlin et al. 1991, 1993). An alternative explanation for the effects of acid rain on red spruce (Sheppard 1994) holds that exposure of trees to elevated SO42- in acid rain may alter carbon metabolism of trees by consuming energy associated with sequestering SO42- ions and repairing injury that a buildup of these ions might cause to membrane proteins. The “cost” of such carbon allocation is expected to be physiological impairment and increased vulnerability to secondary stresses, including freezing stress. Whatever the mechanism for red spruce decline, a strong direct link between freezing injury and red spruce decline has been established in northern montane regions of the red spruce geographic range (DeHayes et al. 1990, DeHayes 1992, Johnson et al. 1996). The link is so strong that red spruce decline is actually attributed to freezing injury in northern regions (Wilkinson 1990, Tobi et al. 1995). Freezing injury results in a loss of foliage critical for photosynthate production and storage, and it leads to the reduced basal area, height growth, and live crown volume typical of the red spruce decline syndrome (Wilkinson 1990, DeHayes 1992, Tobi et al. 1995). Historical evidence and analysis indicate that the frequency of freezing injury episodes in red spruce forests has increased over the past 40 years (Friedland et al. 1984, DeHayes 1992, Johnson et al. 1992, 1996), a period that coincides with increased emissions of sulfur and nitrogen oxides and acid deposition. Although much has been learned about the ecology and decline of red spruce (e.g., Barnard et al. 1990, Eagar and Adams 1992, NAPAP 1992, Johnson et al. 1996), including freezing injury symptomology and pathology, a clear understanding of the physiological and environmental causes of freezing injury in red spruce has not emerged. In particular, an empirically supported mechanism that explains how acid rain might enhance freezing injury susceptibility and lead to the deterioration of forest health has been lacking. In this article, we synthesize existing and new information that demonstrates acid rain alteration of the foliar calcium pool specifically associated with the plasma membrane-cell wall compartment in red spruce mesophyll cells. In addition, we provide direct evidence that links this physiological disruption to red spruce freezing injury and decline throughout eastern North America. Finally, we consider the acid-induced alteration of this particular physiologically important pool of calcium in the context of other hypotheses for red spruce decline and discuss the broad implications of alteration of the foliar calcium pool to forest health and well-documented soil calcium depletion. Despite early reports of “winter drying” or “desiccation” as causes of the foliar dieback referred to as “winter injury” in red spruce (Curry and Church 1952, Pomerleau 1962, Morgenstern 1969), it is now well established that red spruce winter injury is caused by subfreezing temperatures (Strimbeck et al. 1991, Perkins et al. 1991, DeHayes 1992). Red spruce has been subjected to repeated, severe, regionwide freezing injury for many decades. In recent years, major regionwide freezing injury events have occurred at approximately 4-year intervals on average, with moderate, more localized injury occurring in intervening years. Numerous cold tolerance assessments of red spruce have been conducted over the past decade. Despite varying procedures and sampling of different northern montane populations, a remarkably consistent pattern of midwinter maximum cold tolerance for red spruce has emerged. Laboratory studies indicate that the average temperature at which current-year needles of red spruce in northern New England and New York undergo freezing injury is in the range of-37 °C to −47 °C (Table 1). Because controlled freezing environments are thought to be less stressful than natural conditions (Hadley et al. 1996, Schaberg and DeHayes in press), these laboratory freezing studies probably overestimate the cold tolerance of red spruce. Estimates of midwinter cold tolerance for current-year foliage of red spruce from northern US populations. Estimates of midwinter cold tolerance for current-year foliage of red spruce from northern US populations. The most comprehensive assessment of cold tolerance in red spruce, which examined the January cold tolerance of 60 red spruce trees an range on Mt. Mansfield, an average injury temperature of °C and a range °C to °C Schaberg et al. in of the trees were at temperatures than °C et al. in of from Mt. Mansfield over the past years that temperatures as as °C that to as as °C and °C in approximately and of 1). during most in northern montane temperatures the maximum cold tolerance of at some red spruce the susceptibility of red spruce to freezing northern by have winter cold tolerance well minimum temperatures (DeHayes 1992). Freezing injury susceptibility is for red spruce than such as temperatures and cold tolerance on Mt. Cumulative of minimum winter temperatures at over a cold tolerance of 60 red spruce trees et al. in Freezing injury susceptibility of red spruce is to current-year which is approximately 10 °C less of freezing in winter than foliage (DeHayes et al. 1990, DeHayes 1992). The in freezing tolerance between and needles that red spruce has the physiological to cold In fact, if current-year needles of red spruce were in cold tolerance to the species freezing injury in the most the cold tolerance of current-year environmental such as acid rain, that might the cold tolerance of foliage by a be expected to result in a in the frequency of freezing has, in fact, established that exposure of red spruce foliage to both et al. et al. 1992, et al. 1994) and (DeHayes et al. 1991, et al. acidic cloud water reduces the cold tolerance of current-year that we have conducted over several years both laboratory and field conditions and trees as well as have documented that exposure to acidic reduces the midwinter freezing tolerance of red spruce trees by °C and DeHayes in press). tolerance reductions of this are to the widespread freezing injury to red spruce in northern montane forests over the past 40 years (DeHayes 1992, Johnson et al. 1996). if of acid deposition reduced red spruce cold tolerance by an average of the reduction in average cold °C to approximately be expected to lead to freezing injury conditions approximately years on Mt. Mansfield 1). Acid deposition in the pH range be for northern montane red spruce trees on the of the cold tolerance range of the red spruce trees on Mt. how pollution has to enhanced freezing injury and the decline of red spruce we have studied the of red to acid deposition. In particular, we have examined acid in calcium as a potential mechanism for injury in red spruce is an in trees and a major in soil and Acid deposition has a substantial and influence on leaching, depletion, and cycling of calcium in forest soils (Shortle and Smith 1988, Lawrence et al. 1995, Likens et al. 1996). findings highlight the belowground and implications of and also the that acid deposition might have effects on calcium of trees and forest health. The potential effects of a reduction in calcium are for red spruce, the North tree species decline has been firmly linked to of acid deposition (NAPAP 1992). information has demonstrated that red spruce trees with foliar calcium concentrations are less cold than trees foliar calcium in the range Schaberg and DeHayes in press). In fact, is a strong and between cold tolerance and foliar calcium for trees foliar calcium these to be at calcium concentrations red spruce trees in a soil in northern New trees that were to freezing injury had foliar calcium concentrations in not foliage than trees Furthermore, has documented that acid foliar calcium et al. 1988, DeHayes et al. 1991, McLaughlin et al. 1996, Schaberg et al. in Acid-induced calcium has also been proposed to cause dark respiration increases and carbon metabolism associated with red spruce decline in the southern freezing injury is not a (McLaughlin et al. 1990, 1991, 1993). between foliar calcium and midwinter cold tolerance for red spruce trees in New that foliar calcium than or are the range of foliar calcium and DeHayes in press). between foliar calcium and freezing injury for current-year and foliage of red spruce trees in New with of susceptibility or (Wilkinson to freezing injury Acid-induced foliar and cold tolerance red spruce trees to acid that of a solution with an cloud chemistry and acidic pH and DeHayes in demonstrated that calcium from current-year needles during in to pH than to pH concentrations were in of foliage exposed to the more acidic An in to the of calcium that most of the calcium derived from needles than and that 50% more calcium from current-year foliage than from foliage Schaberg and DeHayes in press). of also that pH foliage 60 more than pH Furthermore, acid calcium were by membrane disruption and a °C reduction in freezing tolerance at pH than at pH during and winter to acid exposure result that acid has a direct impact on membrane of and it to the plasma membrane as the potential of acid-induced calcium of acid on physiological of red spruce. pH pH In calcium leaching, foliar as by tolerance from red spruce foliage and DeHayes in press). are not different or are different at based on of of pH and pH on in calcium of needles of red spruce current-year needles needles and DeHayes in press). of Although were to in foliar calcium between pH we have not a reduction in calcium in foliage with acid that pH and However, calcium and is and this is critical to its physiological in The of the calcium in needles is calcium and which are of In the calcium ions in the plasma membrane some calcium from the are of major physiological pool of a of foliar the of to environmental conditions and et al. 1993, et al. 1993, 1996). Because foliar calcium estimates the and calcium these estimates may in the and Indeed, recent have demonstrated the of foliar calcium with and the of between and foliar calcium DeHayes et al. In fact, foliar calcium concentrations are not an of of for trees calcium concentrations the range between calcium and calcium concentrations for current-year foliage of red spruce (DeHayes et al. are not The plasma membrane of a critical in cold and injury and solution and the of to freezing during cold and 1986, 1988, calcium plasma membrane and and by and of membrane and and et al. and cold at in its effects on membrane of a mesophyll plasma membrane physiological of calcium and possible physiological of acid-induced The pool et al. also an important as a in the and of environmental including temperature and et al. 1993, et al. 1993, 1996). temperatures may the plasma membrane the calcium with that physiological to freezing stress. changes in In to the of general in cold data specifically in the cold tolerance of red spruce. foliar calcium in not needles are and to environmental changes that changes in membrane to cold For example, increases of in current-year needles DeHayes et al. may an in calcium associated with increases in membrane reductions in are most associated with changes in the acid of membrane (DeHayes et al. and with a for in the and of the cold and 1986, 1988, of calcium in current-year and needles of red spruce The in during a midwinter is for not needles (DeHayes et al. have also documented reductions in DeHayes et al. and freezing tolerance (Strimbeck et al. in red spruce not needles in to a midwinter the both and freezing tolerance to changes in and cold tolerance with the well-documented changes in membrane in of during cold and and the that is important to cold if acid reduces calcium leaching, an alteration in membrane and freezing injury susceptibility to other to foliar calcium to the physiological of calcium in the reduced cold tolerance of acid red spruce were by the of of the critical compartment of the foliar calcium have now and a for in et al. and have it to the impact of acid and soil solution chemistry on red spruce and nutrition et al. in examined freezing foliar and foliar calcium of red spruce trees in a soil for its calcium Schaberg et al. in were exposed in a to expected to result in calcium soil solution calcium or soil solution aluminum or which with and calcium uptake by (Shortle and Smith and pH or pH which causes calcium et al. in calcium enhanced foliar calcium concentrations and increased of respiration during the early et al. in soil aluminum the of calcium and other foliar throughout the and reduced increased foliar calcium did not alter aluminum the changes in to be direct and of foliar calcium calcium aluminum soil had impact on foliar calcium leaching, or freezing which that of soil and foliar calcium may not have important physiological for red spruce In to the soil acid had physiological to the pH pH to the including in summer and early in foliar calcium and in and reductions in and winter freezing tolerance and of current-year needles (Table Acid reductions in mesophyll were in summer a maximum of between by midwinter (Table even acid had been pattern evident for the acid influence on cold tolerance (Table of soil soil and acid on current-year foliar calcium and calcium and cold tolerance in red of soil soil and acid on current-year foliar calcium and calcium and cold tolerance in red Although soil calcium and aluminum calcium nutrition and these did not enhance foliar calcium leaching, alter or freezing which to be critical to red spruce decline in northern montane in foliar calcium from soil probably in calcium (e.g., the of calcium in that have physiological in from direct acid to by enhanced calcium leaching, to membrane to disruption of in environmental The in cold tolerance and susceptibility to freezing injury in red spruce needles of different (DeHayes is consistent with the pattern of in in current-year needles as well as in foliar calcium acidic or no is in current-year needles of red spruce during early summer in current-year needles are than in needles throughout summer and early acid-induced calcium is expected to be The substantial in foliar calcium the and cold tolerance between and current-year red spruce to the of red spruce current-year The and persistence of the acid influence on and cold tolerance throughout winter and the to acid in are most a of the of calcium the of of calcium in the and the on to In mesophyll the of and the net of foliar calcium calcium loss the physiological implications of acid deposition may be in summer and is and ongoing loss is not the the different the influence of pH aluminum on foliar nutrition et al. in The the for in associated with aluminum were for pH than for pH acid aluminum on were also for the of acid-induced reduction in for trees 1994) and trees January 1995). of pH and aluminum did not acid-induced reductions of In fact, of the most physiologically findings the of other The of between acid and soil calcium is it that acid-induced foliar calcium leaching, depletion, and cold tolerance reductions were not by soil of calcium and cold tolerance The pool of other calcium is for leaching, resulting in membrane of a potential pool of and reductions in the freezing tolerance of current-year red spruce Acid may result from of H+, SO42−, or both et al. 1995). Specifically, calcium could of on or the and of by at the be to red spruce foliage of freezing stress et al. and it has been implicated as a critical pollutant in cold tolerance reductions in this species et al. 1991, However, we have demonstrated cold tolerance reductions in to acid that no were with Schaberg and DeHayes in or had concentrations et al. in These with reduced not concentrations in foliar et al. 1988, McLaughlin et al. 1996), indicate that acid calcium and cold tolerance reductions are not are most the result of by results that direct acid deposition on needles a environmental stress in that it which is not in resulting in a that may not be by of foliar calcium of plasma and a loss of freezing tolerance in current-year needles the depletion. These findings a direct impairment of from acid deposition of well-documented belowground and provide a explanation for cold tolerance reductions in trees specifically associated with deposition of acid on foliage et al. 1992). In to which or in carbon the mechanism the direct of acid deposition on specific foliar calcium and cold findings also the of the physiologically and pool in and that in this pool may not be by typical analysis of foliar In fact, of in this mechanism for acid deposition perturbation of cold that direct acidic deposition on red spruce foliage calcium ions specifically associated with plasma of mesophyll cells. a is plasma are and calcium is physiological impairment leads to the more secondary symptoms of freezing injury in northern regions, elevated respiration (McLaughlin et al. and enhanced susceptibility to other that forest health. mechanism a direct link between acid deposition and increases in red spruce freezing injury in northern montane forests over the past 40 years, a period that coincides with increased pollution Acid deposition-induced alteration of and membrane documented in northern forests also be expected in to acidic deposition in the southern Although did not the pool McLaughlin et al. that acid deposition-induced calcium and changes in membrane may cause respiration to The acid alteration explanation for red spruce decline that we have proposed may a explanation for red spruce decline throughout the montane red spruce forests of eastern North acid deposition is mechanism specifically for the of the red spruce freezing injury such as the freezing tolerance between and the of the cold tolerance to and the persistence of the acid-induced reduction in cold tolerance throughout winter the of acidity is Furthermore, the of the cold tolerance to acid of the in the pH or its is consistent with the that on not with the that or some other pollutant freezing injury Finally, the than the direct influence of acid deposition in the proposed mechanism is with assessments of red spruce decline growth impairment be expected if direct sulfate or carbon metabolism disruption were in red spruce decline (e.g., et al. 1991, changes in most have a even in the of freezing However, most studies have documented or even growth in red spruce exposed to acid in the of such as subfreezing temperatures et al. 1986, et al. et al. 1990, et al. Indeed, growth reductions associated with red spruce decline in northern montane forests to be the direct result of the freezing injury (Wilkinson 1990, Tobi et al. than exposure to the acidic Although it is well established that acid deposition has to forest soil calcium (Lawrence et al. 1995, Likens et al. 1996), findings have that acid deposition influence foliar of belowground In fact, direct acid-induced disruption of to soil calcium as by the that acid even in in soils with we that soil calcium have an on in more calcium soil For example, red spruce trees with foliar concentrations of calcium in soils show a reduced cold tolerance The physiological impairment of trees foliar calcium reduced resulting from soil calcium The substantial acid-induced soil calcium that has recently been documented (Lawrence et al. 1995, Likens et al. 1996) be expected to deficiencies and forest health and ecosystem The of acid deposition on ecosystem calcium and are by and potential are by indicate for the Lawrence et al. Likens et al. Schaberg and DeHayes press), al. et al. et al. The results in this also the strong that acid rain alteration of membrane is not to red spruce is in this species of its to freezing In fact, acid-induced foliar calcium has been demonstrated in many other forest tree including and spruce (Picea and red eastern and and of membrane cold and other secondary stress have not been made for these However, we have recently demonstrated an acid reduction in membrane in that is comparable to that of red spruce exposed to the acidic (Table Schaberg et al. in However, so that cold tolerance if could not be these data show that acid-induced membrane is not specific to red spruce and that acid-induced foliar disruption may be a more general phenomenon than the freezing injury syndrome evident in red spruce. of in the current-year foliage of red spruce and of pH or pH cloud water of in the current-year foliage of red spruce and of pH or pH cloud water Although it is well that calcium a critical in to numerous (e.g., and and et al. 1993, et al. 1993, 1996), the implications of soil calcium its impact on the physiologically important uncertain at this time. Because most calcium in is and it is the and pool that to a critical and in stress acid-induced soil calcium also and membrane the potential for to injury could have an influence on forest health In this the stress and health of montane forest ecosystems may be by a acid-induced alteration of and to physiological impairment and a to be by an of environmental Because the pool in now be the potential for or alteration as a factor in other recent regionwide forest in eastern North America supported by the National the US Forest Northern and the and for on an of this and and for are also to and for