biogeochemistry: some opportunities and challenges for the future

BIOGEOCHEMISTRY: SOME OPPORTUNITIES AND CHALLENGESFOR THE FUTURE

GENE E. LIKENSInstitute of Ecosystem Studies, Millbrook, New York 12545, U.S.A.(∗ author for correspondence, e-mail: [email protected])

(Received 20 August 2002; accepted 6 April 2003)

Abstract. There are major opportunities for big, important questions to drive biogeochemical re-search in the future. Some suggestions are presented, such as: what are the controls on N lossand retention in watershed-ecosystems; what are the rates and controls on biological N fixation anddenitrification in diverse ecosystems; how does scale (temporal and spatial) control biogeochemicalflux and cycling; what controls the apparent and actual weathering rates in terrestrial ecosystems andwhat is the fate of the weathered products; how can biogeochemical function best be integrated onregional to global scales; and what are the quantitative interrelationships between hydrologic cyclesand biogeochemical cycles? Some brief examples and approaches to address such questions, forexample, the value of multidisciplinary teams for addressing complicated questions, and the use ofsophisticated tools (e.g., stable isotopes, spatial statistics, remote sensing), are presented.

Keywords: acid rain, antibiotics, biogeochemistry, eutrophication, hydrology, legacies, N and Cacycling, scale, weathering

1. Introduction

Upon learning that the Desdemona he had just murdered in a jealous rage wasindeed without guilt, Othello calls down extreme torments upon himself – devils,winds, hot sulphur, liquid fire (Othello, the Moor of Venice, Act V – Scene II,Shakespeare, 1564–1616). While the windborne sulfur deposited on land and waterof eastern North America and western and central Europe over the past century orso may be less dramatic than is called to mind by this Shakespearean prose, itscontinuing addition to these ecosystems is neither trivial nor without ecological‘torment’.

Indeed, the atmospheric deposition of ‘hot sulphur’ in acid deposition has neverkilled anyone directly, and thus its guilt is subtle (difficult to detect), and its ser-ious, long-term effects on terrestrial and aquatic ecosystems have been difficultto monitor and ultimately control. Despite governmental attempts to reduce aciddeposition by reducing the precursor emissions of NOx and particularly SO2, aciddeposition continues and its impacts persist at the ecological and biogeochemicallevel. Now, however, data are accumulating that show major direct human healtheffects of the particulate matter emitted as part of the overall air pollution problemassociated with acid deposition (e.g., Pyn, 2002; Kaiser, 2000). Ironically, some

Water, Air, and Soil Pollution: Focus 4: 5–24, 2004.© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

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TABLE I

Some major questions and challenges for biogeochemistry

1. What are the specific effects and relationships of the increasing size of the human popu-lation on flux and cycling of elements, and what are the biogeochemical effects of forcingfunctions often incongruent in space and time associated with these changes?

2. What controls fluxes of N and P to and from natural and human-dominated (cities,agricultural) ecosystems?

– effect of disturbance/nutrient saturation/instream-watershed retention/denitrification/

interactions with other element cycles;

– effects of atmospheric deposition, and flows of fertilizer, food, waste.

3. What is and what controls C sequestration in diverse ecosystems (e.g., forest, ocean,lakes, wetlands) on variable temporal and spatial scales?

4. What controls weathering rates, and what are the fates of the weathered products,including nutrient loss in terrestrial ecosystems?

5. What is the qualitative and quantitative role of non-human animals in the flux and cyclingof nutrients, and what are the long-term effects of these fluxes (e.g., guano and otherwaste products)?

6. How do the flux and cycling of antibiotics, steroids, hormones and pharmaceuticals affectelement flux and cycling?

7. What is the quantitative linkage between biogeochemistry and species richness, speciesextinction and invasion of alien species?

8. What are the effects of lags and legacies on current and future biogeochemical fluxes andcycles?

9. What are the quantitative interrelationships between hydrology and biogeochemistry?

10. How can a better synoptic understanding of the biogeochemical flux, cycling andinteraction of elements among air, land and water (including ocean) systems be achieved?

11. What are the critical linkages and feedbacks among major nutrient and toxic elementfluxes and cycles?

12. What are the potential impacts of bioterrorism on biogeochemical fluxes and cycles, andhuman welfare that depends on these cycles?

estimates of the death toll related to such air pollution particles are controversialbecause of a glitch in the statistical software; nevertheless, morbidity estimates inthe U.S. appear to be large (Kaiser, 2002).

My objective here is to identify some of the current major challenges for biogeo-chemistry where intensive research and creative thinking could be especially re-warding (Table I). I expand briefly on four of these: two (flux and cycling of N, andweathering release of Ca) that have been studied extensively for long periods andtwo (impacts of legacies, and the flux, cycling and effects of antibiotics, steroids,hormones, etc.) that have been studied less well from a biogeochemical point ofview. My focus will be on biogeochemical flux and cycling. Flux is defined as a

BIOGEOCHEMISTRY: OPPORTUNITIES AND CHALLENGES 7

flow or movement across a boundary, real or specified, and cycling is movementand interchange within a boundary.

2. Challenges and Opportunities

Biogeochemistry is a vibrant, robust and growing field. From the early writings ofVernadsky (1944, 1945) and Hutchinson (1944, 1950) to in-depth analyses of lake(Schindler, 1980) and forest ecosystems (Likens et al., 1977) the field now hasmatured and become more focused on problems at regional to global scales andthose directly relevant to humans (e.g., Schlesinger, 1997; Burke et al., 1998).

What are the ‘big’, important questions driving inquiry in biogeochemistry?I have no special crystal ball in this regard, but will offer some observations. Iwon’t describe here current progress and discoveries. That has been done well inBiogeomon 2002 and in this special issue.

Clearly our field, and others, is being pushed toward questions and programsrequiring large, multidisciplinary teams (Likens, 1998, 2001a, b). This trend isfostered by the scope and complexity of the questions posed and addressed, aswell as by the requirements of various funding agencies. This approach to bigand relevant questions provides an important opportunity to make quantum leapsin our understanding as questions are tackled at large scales, by combining thetalents of diverse disciplines, with powerful, new tools of analysis, statistics andcommunication, and by addressing directly the complexities involved.

Nevertheless, there often is a mismatch between the need for teamwork and thedifficulties and insufficient training to organize a multidisciplinary research teamand to make it work. We have opportunities for major advances in this area. Basedon my experience as part of a team effort over several decades, I have emphasizedthe importance of trust in structuring efficient and productive teams (Likens, 1998,2001a, b). Edmondson, in analyzing the effectiveness of hospital, medical teamsand manufacturing work teams has found that psychological safety (PS), ‘... ashared belief held by members of a team that the team is safe for interpersonalrisk taking...’ strongly influences learning and performance of teams (Edmondson,1999). Because most of us care about what other people think of us, Edmondsonfinds that PS is fundamental to leadership and thus characterizes the effectivenessand performance of group or team effort (e.g., Edmondson, 1999; Edmondson etal., 2001).

At a somewhat less lofty level, but possibly more important, is the value ofindividual intelligent inquiry, combined with serendipity, and often referred toas investigator-initiated research. Prior giants in our field, C. Darwin and G. E.Hutchinson, combined an extremely inquisitive approach with brilliant observa-tional skills, characterized by keeping their eyes, ears and mind open to newthoughts and ideas (Likens, 2002). As a result they made seminal contributions tothe field of biogeochemistry. Darwin isn’t usually thought of as a biogeochemist,

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but many of his contributions were biogeochemical in nature (e.g., Darwin, 1881).A recent account of his valuing what probably was the first ecological experiment,including the chemical analysis of plants and soil in the development of his ideas,is especially noteworthy (Hector and Hooper, 2002).

I would argue that the truly major challenges for biogeochemistry in the futurerelate to aspects of human-accelerated environmental change, particularly theirlinkages and feedbacks (Likens, 1991, 1998), namely, global climate change, stra-tospheric ozone depletion, toxification of the biosphere (pollution of air, land andwater), loss of biodiversity, and the all-pervasive effects of land-use changes. But,what are the specific effects and relationships of the increasing size of the humanpopulation on the flux and cycling of elements?

The effect of climate change on biogeochemical flux and cycling is poorlystudied and in many cases is largely characterized by speculation, at least at theglobal scale. Some major questions related to climate change include: What con-trols carbon sequestration in different systems and on variable spatial and timescales, from stomates to ocean sediments?; What controls the fluxes of N to andfrom natural and human-dominated ecosystems? The effects of climate change(particularly from changes in atmospheric CO2 concentration, regional changesin temperature, moisture and quality of precipitation) on biogeochemical flux andcycling, provide particularly important challenges and opportunities for research.Large-scale (plot/macrocosms) studies with elevated CO2 (e.g., the Free-Air CO2

Enrichment [FACE] network in the U.S.; Hendrey et al., 1999; DeLucia et al.,1999), and combining soil warming with experimental manipulations of moistureand nitrogen availability in subhectare- to hectare-sized plots (e.g., Rustad et al.,2001) have great potential, but are expensive, difficult to maintain for long periodsand require team efforts.

How can a better synoptic understanding of the biogeochemical flux, cyclingand interaction of elements among air, land and water (including ocean) systemsbe obtained? Satellite-borne sensors and other types of remote sensing have beeninstrumental in the exciting development of synoptic approaches over a broad rangeof spatial and temporal scales (e.g., Matson and Ustin, 1991; Aber et al., 1993;Martin and Aber, 1997; Burke et al., 1998; Martin et al., 1998; see Wessman andAsner, 1998). For example, the Airborne Visible InfraRed Imaging Spectrometer(AVIRIS) is making significant progress in assessing the N content of foliage ona regional scale (Ollinger et al., 2002). Chlorophyll concentration maps are nowavailable for entire areas of the ocean leading to better estimates of phytoplanktonbiomass and calculations of NPP for the entire ocean (Morel and Antoine, 2002).We are becoming much more skilled at addressing large-scale, biogeochemicalquestions with these new and developing technologies.

Nevertheless, much more attention needs to be given to integrating spatial andtemporal patterns of global change to predict better the anthropogenic influenceon ecosystem and biogeochemical processes. Generally, patterns of disturbanceare not uniform (spatially or temporally) as area (scale) increases and processes


become more incongruent in space and time. Recently, however, biogeochemistryhas evolved from examining the flux and cycling of single elements to a greaterfocus on element interactions (e.g., Likens, 1981; Sterner et al., 1992; Caraco etal., 1993; Burke et al., 1998). But, what are the critical linkages and feedbacksamong major nutrient and toxic element cycles?

What is the linkage between biogeochemistry and species richness, speciesextinction and invasion of alien species? The effects of species richness, loss ofspecies and invasion of alien species on biogeochemical flux and cycling are poorlyknown. An interesting example is the invasion of zebra mussels (Dreissena poly-morpha) into the Hudson River (Strayer et al., 1996, 1999; Caraco et al., 1997).These alien species invaded the River in 1991 and by 1993 were the dominantfilter feeder in the system, having reduced the native mussel population by 60%.There have been many ecological effects of this invasion, but the biogeochemicalresponses have included a decrease in dissolved oxygen by about 15% and in-creases in dissolved inorganic N and soluble reactive P in the River (Caraco et al.,1997, 2000; Strayer et al., 1999).

Most studies of community and population dynamics in ecosystems have notbeen integrated with biogeochemical analyses, but some recent studies have demon-strated the importance and value of such integration (e.g., Wedin and Tilman, 1990;Cronan and Grigal, 1995; Schimel et al., 1996; Finzi et al., 1998; Hooper andVitousek, 1998; Tilman, 1998; Lovett et al., 2002).

Better integration of chemistry, geology, biology and hydrology is needed inbiogeochemical studies of watersheds and regions. For example, what are the quant-itative interrelationships between hydrology and biogeochemistry; and what havebeen and will be the biogeochemical effects of extreme human impacts on hy-drology, for example dams (less flashy runoff and sedimentation/sink for chemic-als), paving (more flashy runoff), wetland drainage (more flashy runoff), reducinggroundwater levels?

What will be the quantitative effect of El Niño – Southern Oscillations (ENSO)on biogeochemical flux and cycling, as influenced by global warming, on regionalto global scales via the impact on flood-drought cycles and the resulting effectson biological and chemical cycles? There are strong spatial and temporal charac-teristics and responses to these climate anomalies (e.g., Molles and Dahm, 1990;www.cdc.noaa.gov/ENSO).

Moreover, understanding hydrological pathways can be very important for eval-uating the biogeochemical response of soil, and groundwater, and surface waters tovarious environmental changes, including climate change, land-use disturbances,etc. (e.g., Hooper and Shoemaker, 1986; Church, 1997; Cirmo and McDonnell,1997; Creed and Band, 1998; Kendall and McDonnell, 1998; Hill et al., 2000;Mitchell, 2001).

Now, for a brief look at four major problems:

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3. The Flux and Cycling of Nitrogen

Humans have disrupted the flux and cycling of N for a very long time (e.g., Vit-ousek et al., 1997), by the transfer of N from long-term storage pools: for example,by the release of N in fossil fuels to the atmosphere by combustion; and the transferof N in guano deposits to agricultural fields. Through the Haber-Bosch process,huge amounts of N2 in the atmosphere have been converted to biologically-reactiveN (fertilizer) and applied to soils and waters worldwide (e.g., Vitousek et al., 1997;Galloway and Cowling, 2002b). Vitousek et al. (1997) estimated that human activ-ity has approximately doubled the rate of nitrogen input to the global, terrestrialnitrogen cycle. Howarth et al. (2002) estimated that anthropogenic N inputs (e.g.,inorganic fertilizer, atmospheric emissions of NOx) to the U.S. doubled between1961 and 1997.

Notwithstanding the importance of N to human societies, e.g., for food pro-duction, and the vast amount of research on the biogeochemistry of N, there stillremain major uncertainties about the magnitude and controls on fluxes of N to andfrom natural and human-dominated ecosystems, especially at large scales (Table I).For example, ecological controls on N-fixation are poorly understood yet this is acritical biogeochemical flux, affecting primary production in both aquatic and ter-restrial ecosystems (e.g., Howarth et al., 1999; Vitousek and Field, 1999; Marino etal., 2002; Vitousek et al., 2002). Even the potential role of N limitation for primaryproduction, which has been studied extensively, is poorly understood in temperateforest ecosystems. The factors affecting the onset, magnitude and continuation ofN-saturation in forests are variable spatially and temporally (e.g., Stoddard, 1994;Aber et al., 1998, 2002). Yet these factors may control retention and output of Nfrom watersheds. A current ‘hot topic’ in N biogeochemistry is watershed retentionand specifically the role of stream ecosystems and riparian areas in this retention(e.g., Fisher et al., 1998; Alexander et al., 2000; Peterson et al., 2001; Bernhardt etal., 2002). Likewise, our limited understanding of denitrification – where it occurs,how much occurs and what controls rates – is critical to understanding N retentionin watersheds.

Caraco et al. (2003) found that relatively simple models, based on human-population density only, predicted variations of NO−

3 export for large rivers (wa-tersheds >10 000 km2), but these models lost predictive power at smaller scalesand explained only 8% of the 1000-fold variation in NO−

3 export for watersheds<100 km2. A somewhat more complex model using various loading factors, ex-plained about 60 to 80% of the variance of this watershed export. Consideration ofN retention and gaseous loss would increase the predictive power of these models,especially for small watersheds.

Based on volume-weighted concentrations and fluxes of dissolved inorganic N(DIN: NH+

4 + NO−3 ) in precipitation at the Hubbard Brook Experimental Forest

(HBEF) in New Hampshire, atmospheric inputs increased from about 200 molha−1 yr−1 in 1964–1965 to ∼700 mol ha−1 yr−1 in 1973–1974, and then fluc-


Figure 1. Monthly, volume-weighted concentrations of NO−3 in stream water for Watershed 6 of the

HBEF.

tuated around 500–600 mol N ha−1 yr−1 to the present. Streamwater fluxes ofDIN, mostly NO−

3 , were relatively low (100–200 mol ha−1 yr−1) during 1964–1965 to 1968–1969, increased to highest values (300–500 mol ha−1 yr−1) during1969–1976, and then have declined to the lowest on record (<100 mol ha−1 yr−1)in 1993–1994 (Likens, 2001a, b). Increased streamwater fluxes during 1969–1970to 1976–1977, 1979–1989 to 1980–1981 and 1989–1990 may have been relatedto soil freezing (in 1970, 1974, 1980, 1991–1993; Likens and Bormann, 1995;Mitchell et al., 1996; Fitzhugh et al., 2003), insect defoliation (in 1969–1971;Bormann and Likens, 1979); prior drought conditions (Aber et al., 2002), andice-storms (in 1998; Houlton et al., 2003). Since forest biomass accumulation hasbeen negligible since 1982 (Likens et al., 1994; Likens, 2001a) it is surprising thatstreamwater fluxes of DIN have been so low since 1982.

A highly regular seasonal pattern is apparent in concentrations of streamwaterNO−

3 at HBEF (Figure 1), with highest values during the winter and lowest duringsummer. The magnitude of the seasonal values has varied for different periodsthroughout the past 37 yr in response to the annual pattern (Figure 2). Only about5–15% of annual N mineralization by soil heterotrophs occurs during the periodof snow cover at the HBEF, typically from late November to mid April (Groffmanet al., 2001). Thus, the highest monthly streamwater values for NO−

3 during thedormant period for this largely deciduous forest are more likely due to reducedvegetation uptake than to microbial activity, but why have the maximum valuesoccurred earlier with time (Figure 3)? The explanation for this change in timingis not clear, but may be related to anecdotal evidence that snowmelt began earlierand was more likely to be accompanied by rain after about 1983. April air tem-

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Figure 2. Mean (± SD) monthly streamwater concentrations for Watershed 6 of the HBEF duringfour different periods of the long-term record.

peratures also have increased significantly with time during this period (Likens,2000). Because of the thaw concentration effect when the snowpack begins to melt(Hornbeck et al., 1977), NO−

3 concentrations would be highest in stream water atthat time. Thus, even after long periods of intensive study, interesting and importantquestions remain about the flux and cycling of N in natural systems.

Recently, an entire issue of Ambio (2002, Vol. 31, No. 2) was devoted to thebiogeochemistry of reactive N, and various synthesis volumes are emerging (e.g.,Boyer and Howarth, 2002; Neal, 2002). Complicated and exciting large-scale ques-tions are posed by these efforts, such as, what are the effects of projected futurechanges in amounts of atmospheric deposition of reactive N throughout the globeand especially in developing countries and, what are the effects of reactive nitrogenflows as a result of production, transport and consumption of food containing N(Galloway and Cowling, 2002b). The location, extent (urban sprawl) and mag-nitude of future urban agglomerations (e.g., Likens 2001b) are particularly relevantto these flows and sinks (e.g., Baker et al., 2001), and as such, represent majorbiogeochemical questions of great importance to human societies.

Galloway and Cowling (2002a) suggest two critical topics for research in Nbiogeochemistry: What is the fate of reactive N released to the environment by


Figure 3. Highest and lowest, volume-weighted average streamwater NO−3 concentrations for

Watershed 6 of the HBEF during 1964–2000.

human action? And, how can this increasing amount of reactive N produced byenergy production and food production be decreased? Given this call ‘to optim-ize nitrogen management in food, fiber and energy production, and to minimize

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detrimental human and environmental impacts’, they propose four opportunities:‘– Increase nitrogen-use efficiency in food production; – Recycle reactive nitro-gen within agroecosystems and managed forests; – Decrease NOx emissions fromfossil-fuel combustion by capturing NOx for other uses or by eliminating its form-ation; – To the extent that the above are not possible, convert reactive nitrogen backto nonreactive N2 before it is lost to the environment’. Clearly, these are critical and‘big’ questions for understanding and managing the flux and cycling of reactive Nrelative to human societies.

4. Weathering Release

What is the difference between and what controls apparent and actual weatheringrates in terrestrial ecosystems, and what is the fate of the weathered products? Verysophisticated tools, e.g., stable isotopes, are now available for studies of weatheringrelease of nutrients, but the challenges are to ask the penetrating question, aided bythe use of these tools, and to interpret the results obtained.

Using a mass-balance approach, Likens et al. (1998) estimated that about 50 molCa ha−1 a−1 was released by weathering (based on plagioclase weathering), com-pared to ∼30 mol Ca ha−1 a−1 input in atmospheric deposition. The weatheringrelease supplied ∼25% of annual streamwater export and ∼3% of the annual grossplant uptake of Ca2+ during 1987–1992 at the HBEF. Recently, Blum et al. (2002)used Sr isotopes and Sr Ca−1 ratios to estimate that weathering of apatite by my-corrhizal ‘mining’ could account for significant Ca2+ in stream water and couldprovide an additional ‘direct’ source of Ca2+ for some trees at the HBEF. (Internalrock ‘mining’ by ectomycorrhizal mycelia is a developing ‘hot topic’ in weatheringand plant nutrition – e.g., van Breemen et al., 2000). Blum et al. (2002) estimatedthat the current sources of Ca2+ in stream water were ∼30% from the atmosphere,∼35% from silicate minerals and ∼35% from apatite. Also using Sr isotopes,Bailey et al. (1996) suggested that vegetation obtained about 4% of its annualCa2+ uptake from atmospheric inputs and weathering release represented ∼30%of streamwater output in a nearby watershed. Kennedy et al. (2002), however, usedSr isotopes to conclude that atmospheric input provided >90% of the Ca2+ used byvegetation in a remote Chilean forest and that weathering inputs of Ca2+ to plantnutrition were minimal.

Even though weathering has been studied for as long as any biogeochemicalflux, uncertainties still remain in spite of the use of powerful tools. There are majorbiotic, geologic and atmospheric differences between these two systems (HBEF;remote Chilean forest) in opposite hemispheres. For example, the Chilean systemis an old-growth forest, dominated by ‘clean’, atmospheric inputs, whereas the NewHampshire system is a relatively young forest, disturbed during the last century bylogging, hurricanes and acid rain. There also are major differences in depth andtype (till vs. bedrock) of weatherable materials (e.g., Likens et al., 1977; Kennedy


et al., 1998) and cloudwater inputs (e.g., Weathers et al., 2000). Do these factorsexplain the differences in results/conclusions relative to Ca2+ biogeochemistry, orare there even more fundamental differences? How do these differences affect theinterpretation of effects due to air pollution and sustainable management of forestsin both regions, and particularly as atmospheric inputs may change with time?

5. Legacies and Lags

So-called ‘chemical time bombs’ or legacies of past human actions or materialdisplacements can profoundly impact current biogeochemical flux and cycling.Moreover, how have biogeochemical fluxes and cycles changed over geologic andhistorical time? What clues and tracers indicate their rates and magnitudes overtime? Lags and legacies affecting questions of biogeochemical flux and cyclingmay be among the most challenging and interesting, to understand quantitatively.There are many examples known, and many more to be explored. Of the more obvi-ous are avian guano deposits mined in Peru and Chile and deposited in the northernhemisphere as fertilizer; evapotranspiration to produce crops, with N transferredvia the harvest to intensive utilization and waste generation areas, such as urbanagglomerations and animal feedlots (such transfers often result in the transfer oftoxic elements, e.g., pesticides); groundwater contaminants, such as chromium,can be used to track water and pollution movement and remediation of this re-source over long times (Blowes, 2002); transfer of N, S and C condensed in fossilresources (coal and oil) to a dispersed form in the atmosphere with combustion andthen returned at some distance from the source, via wet and dry deposition. Manybiogeochemical legacies, e.g., effects on soil fertility, may be very old and wide-spread, yet are important to modern ecosystems as shown recently by anthropogicaldata from Brazilian rainforests (Moffat, 2002).

6. Antibiotics, Hormones, Steroids and other Biologically-ActiveCompounds

The occurrence, persistence, flux and cycling, and thus the biogeochemical import-ance of substances such as antibiotics, steroids, hormones and pharmaceuticals, arevery poorly known in natural ecosystems. These substances are increasingly usedby human societies, and potentially active forms are released widely to soils, tosurface and ground waters, and to the atmosphere (e.g., Mallin, 2000). Unfortu-nately, there are few reliable data on the amounts of antimicrobials used in animalproduction in the U.S. One estimate suggests that about 11 200 metric tons peryear of antimicrobials are used for nontherapeutic purposes on livestock, some8 times more than used in human medicines (Mellon et al., 2001). Worse, thereare no quantitative data on the release of antimicrobials to the environment. Data

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Figure 4. Frequency of detection and percent of total measured organic wastewater contaminants in139 streams in 30 U.S. states during 1999 and 2000 (from Kolpin et al., 2002).

on the release of hormonally-active compounds are even more scarce, or at leastnot available publicly (J. P. Meyers, personal communication). Apparently, manyof these contaminants can pass through wastewater treatment plants and domesticseptic systems into the environment relatively intact (Halling-Sorensen et al., 1998;Kolpin et al., 2002). A recent study (Kolpin et al., 2002) found such organic con-taminants in 80% of 139 streams sampled across the United States. ‘The mostfrequently detected compounds were coprostanol (fecal steroid), cholesterol (plant


and animal steroid), N,N-diethyltoluamide (insect repellant), caffeine (stimulant),triclosan (antimicrobial disinfectant), tri(2-chloroethyl)phosphate (fire retardant)and 4-nonylphenol (nonionic detergent metabolite)’ (Kolpin et al., 2002). A me-dian of 7 and as many as 38 of these contaminants were found in single watersamples (Figure 4).

A significant impediment to studies of such components is the lack of appropri-ate or widely available methodology for their detection. Such contaminants oftenexist at very low concentrations. Also currently, the cost of such analyses is pro-hibitive to routine monitoring. Kolpin and colleagues (2002) needed to developor modify 5 methods for their study. The development of specific molecular andmicrobial tools may be appropriate and particularly helpful for such studies in thefuture.

These biologically active compounds probably have major direct and indirectimpacts on biogeochemical cycles. I believe that this subject deserves much atten-tion in the future, particularly given the rapid development of high-density animalagriculture (e.g., Batie, 1993) around the world.

7. Final Thoughts

Biogeochemical information is critical for identifying the control points for man-agement of environmental problems. ‘Acid rain’ (Odén, 1968; Likens et al., 1972)is a good example, as is the cultural eutrophication of freshwater lakes or coastalmarine areas where control is managed largely by limiting the inputs of S, Nor P (e.g., Hasler, 1947; Vollenweider, 1968; Schindler, 1977; Howarth, 1993;Vitousek and Howarth, 1991; Smith, 1998; Boyer and Howarth, 2002). Based on anunderstanding of these relationships, a need and an opportunity develop for directhuman intervention in managing biogeochemical cycles to alleviate environmentalproblems, as may be required by managers and decision makers. Such widespreadenvironmental problems persist and are likely to continue for the foreseeable fu-ture. Two media headlines during July 2002 proclaimed that acid rain damage isworse than ‘previously believed/thought’ based on studies of Ca2+ availability andplant uptake (Schaberg et al., 2001; Kennedy et al., 2002). It is always difficult toknow what was previously ‘thought’, but clearly the ecological and biogeochemicalimpact of acid rain has not gone away and this environmental problem providesmany challenges and research opportunities for the future. Using computer sim-ulation approaches, Driscoll et al. (2001) and Evans et al. (2001) have suggestedthat surface waters in areas sensitive to acid rain in the northeastern U.S. and inthe United Kingdom, respectively, would not recover to positive acid-neutralizingcapacity for many decades under current emission reduction protocols. Resolvingsuch complicated issues necessitates, as is always the case, dealing with the details,and ‘the devil is in the details’. But, scientists thrive on studying, understanding,

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and integrating details to resolve the biogeochemical ‘torments’ of importance tohuman societies.

8. Conclusions

The dominant and enlarging role of humans in altering biogeochemical cycles,particularly fluxes – >100% of natural mobilization of N, S and probably P(Schlesinger, 1997); somewhat less to intermediate mobilization of others, e.g.,B (Park and Schlesinger, 2002) and a smaller proportional impact on for example,C (but of great import relative to climate), throughout the planet is now obvious.

Controversial environmental issues and problems associated with large-scaledisruption of natural biogeochemical cycles are continuing or increasing and arecoupled with a need for increased understanding of the effects of direct human in-tervention (e.g., fertilizing ocean with Fe to combat global increases in atmosphericCO2 (e.g., Chisholm et al., 2001; Johnson et al., 2002); hypoxia in coastal watersfrom agricultural N runoff (e.g., Rabalais and Turner, 2001); regional degradationof surface waters, forests and soils from acid rain (e.g., Likens et al., 1979; Driscollet al., 2001; Evans et al., 2001; Stoddard et al., 1999), but areal ‘hot spots’ remain,such as intensive animal agriculture (e.g., Mallin, 2000).

Long-term data and sustained study are critical for understanding patterns andtrends in biogeochemical problems.

There is a critical role for multidisciplinary teams in tackling complicated bio-geochemical problems, but training of team leaders, team members and the teamsthemselves is largely lacking or grossly deficient. There appear to be major oppor-tunities for improvement in team efficiency and productivity (e.g., Likens, 2001b;Edmondson, 1999). There is a need to sustain a strong and healthy mix of investi-gator-initiated research and large, team projects. There is a need for more large-scale, biogeochemical experiments to examine multiple stressors simultaneously.Such experiments provide powerful and dynamic opportunities for unraveling bio-geochemical problems.

Several ‘old’, but still important biogeochemical problems persist in terms ofscientific understanding and utilization and integration of knowledge in the man-agement of these problems, e.g., eutrophication of aquatic ecosystems and acidrain.

There is a need for more and better synoptic study, and integration and inter-pretation of results over large scales (regional to global).

There is a need for better use of new and powerful tools (e.g., stable isotopes,spatial statistics, fractal analysis (e.g., Kirchner et al., 2000), genomics and othermolecular techniques) in biogeochemical studies, but development of clear ques-tions and interpretation of results remain a challenge. A ‘tool’ that potentially hasgreat value for future biogeochemical studies is the archiving of samples for futureanalysis. Museum collections have been used in a variety of ways for biogeochem-


ical studies and should be in the future. At the HBEF we established a formalarchive of soil, water, wood, etc. samples in the early 1990s. Samples are bar codedand procedures have been established for protection and use of these samples.Alewell et al. (1999 and 2000) successfully measured 34S in stored water samples,collected over several decades, to elucidate critical aspects of S biogeochemistry atthe HBEF.

There is a need for greater understanding of the quantitative role of microorgan-isms in biogeochemical cycles.

Currently we live in a world characterized by significant bioterrorism (e.g.,Likens, 2002). What are the potential impacts of bioterrorism on biogeochemicalflux and cycling and on human welfare that depends on these cycles?

Acknowledgements

I thank J. Aber, E. S. Bernhardt, N. Caraco, J. J. Cole, R. Goldberg, J. P. Meyers,M. J. Mitchell, W. H. Schlesinger and J. S. Warner, for stimulating discussions andsuggestions. D. Buso assisted with illustrations and P. Likens and H. Dahl withmanuscript preparation. Two anonymous reviewers provided helpful comments.Financial support was provided by The Andrew W. Mellon Foundation, NationalScience Foundation and the Institute of Ecosystem Studies. This is a contributionto the program of the Institute of Ecosystem Studies.

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