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carbon nanotubes help to Environments as its absorb the pollutant from environmentSubscriber access provided by UNIV MASSACHUSETTS AMHERST Environmental Science & Technology is published by the American Chemical Society. 1155 Sixteenth Street N.W., Washington, DC 20036 Critical Review Adsorption Mechanisms of Organic Chemicals on Carbon Nanotubes Bo Pan, and Baoshan Xing Environ. Sci. Technol., 2008, 42 (24), 9005-9013• DOI: 10.1021/es801777n • Publication Date (Web): 13 November 2008 Downloaded from ACS Publications Home Page on March 19, 2009 More About This Article Additional resources and features associated with this article are available within the HTML version: • Supporting Information • Access to high resolution figures • Links to articles and content related to this article • Copyright permission to reproduce figures and/or text from this article Critical Review Adsorption Mechanisms of Organic Chemicals on Carbon Nanotubes BO PAN AND BAOSHAN XING* Department of Plant, Soil and Insect Sciences, University of Massachusetts, Amherst, Massachusetts 01003 Received July 8, 2008. Revised manuscript received October 15, 2008. Accepted October 16, 2008. Carbon nanotubes (CNTs) have drawn special research attention because of their unique properties and potential applications. This review summarizes the research progress of organic chemical adsorption on CNTs, and will provide useful information for CNT application and risk assessment. Adsorption heterogeneity and hysteresis are two widely recognized features of organic chemical-CNT interactions. However, because differentmechanismsmay act simultaneously, mainly hydrophobic interactions, π-π bonds, electrostatic interactions, and hydrogen bonds, the prediction of organic chemical adsorption on CNTs is not straightforward. The dominant adsorption mechanism is different for different types of organic chemicals (such as polar and nonpolar), thus different models may be needed to predict organic chemical-CNT interaction. Adsorption mechanisms will be better understood by investigating the effects of properties of both CNTs and organic chemicals along with environmental conditions. Another majorfactor affecting adsorption by CNTs istheir suspendability, which also strongly affects their mobility, exposure, and risk in the environment. Therefore, organic chemical-CNT interactions as affected by CNT dispersion and suspending merit further experimental research. In addition, CNTs have potential applications in water treatment due to their adsorption characteristics. Thus column and pilot studies are needed to evaluate their performance and operational cost. Introduction Carbon nanotubes (CNTs) have attracted special attention because of their unique properties, such as electrical conductivity, optical activity, and mechanical strength. This fascinating new class of materials has shown promising application inmany areas since its discovery. However, CNTs are being spread quickly in the environment because of their growing use (1, 2). Several studies indicate that they are toxic to organisms and human beings (3), and their presence in the environment affects the behavior of pollutants, such as heavy metals as reviewed by Rao et al. (4). Because of their hydrophobic surfaces, strong interactions between CNTs and organic chemicals are expected. Numerous studies suggest CNTs as effective adsorbents for organic chemicals in solidphase extraction and water treatment after compared with C18 (5, 6) and activated carbon (AC) (7, 8). This strong interaction also greatly alters the mobility, bioavailability, and environmental risk of organic chemicals (9, 10). In addition, because the structures of CNTs are well defined and their surfaces are relatively uniform in contrast to AC, CNTs are considered to be a good choice to study adsorption mechanisms. Therefore, the understanding of organic chemical-CNT interactions will provide important information on assessing CNT environmental risks and in exploring their applications. Nevertheless, research in this area is still fragmentary and not complete enough for making clear conclusions. An overview of research progress on the interactions between organic chemicals and CNTs is urgently needed. Thus, in this review, we first summarize general features of organic chemical adsorption on CNTs, and then discuss adsorption mechanisms in detail by probing into how the properties of CNTs and organic molecules, coupled with environmental conditions, affect adsorption of organic chemicals by CNTs. General Features of Organic Chemical Adsorption on CNTs Heterogeneous Adsorption. Most directly, heterogeneous adsorption indicates that organic chemical adsorption on CNTs could not be described using a single adsorption coefficient. If a single coefficient were used, significant error would occur when predicting the organic chemical-CNT interaction, and would consequently lead to a wrong conclusion regarding the environmental risk of both organic chemicals and CNTs. To date, various models have been applied to describe the adsorption of organic molecules on CNTs in aqueous phases, such as Freundlich (5, 6, 11), Langmuir (7, 8, 12, 13), BET (14), and Polanyi-Manes models (15, 16). Two reasons have been provided to explain the heterogeneous adsorption. The first is the presence of highenergy adsorption sites, such as CNT defects (17), functional groups (18), and interstitial and groove regions between CNT bundles (Figure S1 in the Supporting Information) (19). These adsorption sites commonly exist on as-grown CNTs (20), thus heterogeneous adsorption is a general feature. The second reason is condensation, such as surface and capillary condensation of gas or liquid adsorbates. Multilayer adsorption could occur when organic chemicals were adsorbed on CNT surfaces (21, 22). In this process, the first couple of layers interact with the surface, while molecules beyond the first two layers interact with each other. This process is called surface condensation. The energy of this process varies depending on the distance between the adsorbed molecules and the CNT surface, thus causing a distribution of adsorption energy. The inner pore of an open-end CNT or interstitial area in a CNT bundle forms a hollow column with both ends open. If the pore size follows the Kelvin-Laplace equation, * Corresponding author phone: 413-545-5212; fax: 413-545-3958; e-mail: [email protected]. 10.1021/es801777n CCC: $40.75  2008 American Chemical Society VOL. 42, NO. 24, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 9005 Published on Web 11/13/2008 capillary condensation takes place andis responsible for loaddependent adsorption energy and heterogeneous adsorption (23, 24). Both the aforementioned reasons indicate distributed adsorption energy of adsorption sites. Organic chemicalsmay occupy high-energy adsorption sites first, and then spread to sites with lower energy (25). This hypothesis indicates concentration-dependent thermodynamics and kinetics. Concentration-dependent thermodynamics has been observed in laboratory studies for organic vapors (11, 23), but has not been studied for the aqueous phase. Researchers also tried to explain prolonged adsorption/desorption kinetics by heterogeneous adsorption sites (26, 27). However,more direct evidence would be concentration-dependent kinetics, which has not been reported. Hysteresis. Adsorption/desorption hysteresis was observed for small molecules (such as organic vapors of methane, ethylene, and benzene) as well as polymers (such as poly(aryleneethynylene)s) on CNTs (28). Hysteresis was presented as deviation of desorption curves from adsorption ones (29) and the absence of adsorbate in the supernatant when CNTs were repeatedly washed using organic solvents (30), buffers (31), or water (32). Real hysteresis is emphasized by conducting recovery tests, verification of equilibrium (29), or direct observation using transmission electronmicroscopy (TEM) and atomic force microscopy (30, 32). However, a lack of hysteresis was reported for butane (14), PAHs (9), and atrazine (15). Different hysteresis phenomena result in different opinions on CNT-related risk. For example, high adsorption capacity and reversible desorption of organic chemicals on CNTs imply the potential release of organic chemicals after intake by animals or human (9). In this case, CNTs act like pollutant collectors and thus pose high health risk. However, significant adsorption/desorption hysteresis can make CNTs pollutant sinks. This would result in decreased organic chemical mobility, bioavailability, and environmental risk (10). Therefore, proper understanding of hysteresis mechanisms is a key step toward assessing CNTled risk and application. Different mechanisms have been proposed to explain the hysteresis, e.g., the strong π-π coupling of benzene-ringcontaining chemicals with the CNT surface (30, 32) and capillary condensation (23). In addition, alteration of adsorbent structure or reorganization after adsorption has been widely accepted to explain desorption hysteresis for organic chemicals on soils/sediments (33). This explanation is applicable in organic chemical-CNT adsorption systems. For example, CNTs with adsorbed tetra-tert-butylphthalocyanine could be easily dispersed in CHCl3, while the pure CNTs could not (30). This result indicated that the π-π bonds between organic chemicals and CNTs disrupted Van der Waalsinteractions between CNTs andinhibited the formation of bundles. Therefore, the interference of CNT-CNT interactions by adsorption of organic chemicals results in different pathways between desorption and adsorption, which consequently induces hysteresis. The absence of adsorption/desorption hysteresis was previously observed, which is an exception to the aforementioned mechanisms. When CNTs had few particleparticle contacts (as shown by TEM images in ref 14), CNT bundles were hardly formed and no interstitial regions were available for butane adsorption. The pore condensation accounted for less than 1% of the uptake (14). Therefore, the lack of hysteresis was explained well by the morphology of CNTs during sorption process. In another system, the KHW (hexadecane-water distribution coefficient) normalized adsorption coefficients (K/KHW) of PAHs (9) were more than 1000 times lower than those of two estrogens containing phenolic groups (29). The adsorption of PAHs on CNTs may not be strong enough to disrupt or disassociate CNT bundles, and thus no hysteresis was observed (9). Multiple Mechanisms Acting Simultaneously. The outer surface of individual CNTs provides evenly distributed hydrophobic sites for organic chemicals. Hydrophobic interactions were emphasized in several studies that discussed protein (31), naphthalene (22), acidic herbicides (6), and streptavidin (34) adsorption on CNTs. If hydrophobic interactions are the only mechanism for the interactions between organic chemicals and CNTs, the adsorption can be predicted using the hydrophobic parameters of organic chemicals, such as KOW (octane-water distribution coef- ficient) or KHW. If this is the case, fate modeling on the environmental behavior of organic chemicals in the presence of CNTs would be straightforward. However, this is not true for most cases. For example, Chen et al. (35) reported poor correlations between the adsorption affinity and hydrophobicity of several aromatic derivatives. Furthermore, the KHW normalized adsorption coefficient varied more than 1000 times for several organic chemicals on CNTs (29). An analysis of literature data also failed to establish a general relationship between KOW and adsorption coefficients (Figure 1 and Figures S2, S3, and Table SI, Supporting Information). Thus, hydrophobic interactions cannot completely explain the interaction between organic chemicals and CNTs. Other mechanisms include π-π interactions (between bulk π systems on CNT surfaces and organic molecules with CdC double bonds or benzene rings), hydrogen bonds (because of the functional groups on CNT surfaces), and electrostatic interactions (because of the charged CNT surface) (36, 37). Different adsorption mechanisms respond to the change of environmental conditions differently, thus, the relative contribution of an individual mechanism to the overall adsorptionis ofmajorimportance to predict organic chemical adsorption on CNTs. However, present studies mostly emphasize the importance of individual mechanisms, but never propose a method to quantitatively determine the relative contribution of individualmechanisms. For example, the importance of π-π interactions was demonstrated by comparing the adsorption of several carefully selected organic chemicals on CNTs (38) or by comparing the adsorption FIGURE 1. Relationships between the adsorption coefficient (K) of organic chemicals on SWCNTs (a) or MWCNTs (b) and their KOW. K was calculated at the equilibrium concentration of 100 µg/L. The database for this analysis is provided in Table SI, Supporting Information. More analysis on detailed classification of CNTs is presented in Figures S1 and S2. No explicit relationship between K and KOW was observed indicating that hydrophobic interactions are not the only mechanism for the adsorption of organic chemicals on CNTs. 9006 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 42, NO. 24, 2008 before and after a π-π system was interrupted (30). However, the authors did not further discuss the quantification of π-π bond contribution relative to the overall adsorption. The following method may be considered in order to reveal the relative contribution of a given mechanism: (1) Normalization of the sorption coefficient by KHW may screen out the hydrophobic effect, and thus investigators could focus on factors other than hydrophobicity (35). Although KOW has been widely used to describe hydrophobicity, it has been reported to be unsuitable to normalize adsorption coefficients because of the possible interaction between -OH on octanol with organic chemicals (29). Normalization of the adsorption coefficient by KHW is probably a better and more reliable method. (2) A comparison of the adsorption of various organic chemicals on a given type of CNTs will present important information about the contribution of different adsorption mechanisms. For example, sorption comparison of a series of nonpolar chemicals with the same KHW but different numbers of π electrons could reflect the contribution of π-π interactions. Adsorption of a given organic chemical on CNTs with different extents of oxidation or functionalization should be compared with great caution because oxidation or functionalization changes not only CNT functional groups, but also surface area, surfacecharge, andCNThydrophobicity. (3) More directly, sorption experiments could be conducted in organic solvents. A comparison of the adsorption of a given chemical on CNTs from organic solvents with different polarities could directly derive the relative contribution of hydrophobic effects or other mechanisms (Figure S4). Another benefit for studying adsorption in organic solvents is to ensure reliable detection by keeping the adsorbate concentration well above the detection limit due to high solubility in organic solvents. Adsorption Affected by CNT Properties Correlation of Adsorption with CNT Physical Properties. CNT surface areas are normally in the range of 290 ( 170 m2/g (mean ( standard error, Table SI) and are generally lower than that of ACs (39). But organic chemical adsorption on CNTs (especially on single-walled CNTs, SWCNTs) is comparable to or even higher than that on ACs (29). Thus, surface area may not be a direct parameter to predict organic chemical-CNT interactions. Su and Lu (7) attributed the higher adsorption of dissolved organic matter (DOM) on CNTs to larger average pore diameter and volume. However, in most studies, CNT porosity could not be applied to explain high adsorption. Decreased CNT diameter increases surface curvature, leading to increased number of multilayers (14), stronger adsorption (16, 40, 41), and increased separation of molecular species in a binary mixture (42). But for molecules with planar structures, adsorption increases with increased diameter because the flat surface results in better contact, such as tetracene (43) and benzene (44). The balance between these two opposite effects deserves further study. Therefore, it seems that neither CNT surface area and porosity, nor diameter alone, could be used to explain CNT adsorption characteristics completely. Adsorption that is affected by other CNT properties, such as morphology and functional groups, will be further addressed in the following sections. Morphology of CNTs. The CNT that contains one layer of a rolled graphite sheet is called SWCNT, whereas several SWCNTs with different diameters concentrically nested together is called multiwalled CNT (MWCNT). The distance between the layers of MWCNTs is too small for any organic molecule to fit into (45). CNTs tend to aggregate together as bundles because of Van der Waals interactions (19). Thus, for an ideal case, the available sorption sites of CNT bundles include the surface area, the interstitial and groove areas formed between the CNTs, and the inner pores of the tubes (Figure S1). External surface and groove areas are generally available for adsorption, but the interstitial and inner pores are not. For example, the external surface of SWCNT is the main area for naphthalene adsorption, but the inner pore sites are not due to the dimensional restrictions (22). On the other hand, molecules as big as enzymes were reported to enter the inner pores of CNTs with diameter 3-5 nm (46). The presence of amorphous carbon, functional groups, and metal catalysts could block the inner pores (16). The blocked inner pores can be opened up by acid treatment using HCl to eliminate metal catalysts located at the end of the CNTs (47), or using H2O2 (21), nitric acid (22), base (48), or heat treatment (563 K in ref 43) to remove the amorphous carbon. The reason for the unavailable interstitial sites is that no bundle was formed (14) or that the organic molecules are too large to fit into this area (45). Thus, the availability of sites for organic chemical adsorption on CNTs is highly dependent on CNT properties as well as their aggregation. Liu et al. (49) observed higher sorption of organic dyes on CNTs in water than in ethanol. However, they mostly discussed the different ionic states of the dyes in different solvents. As the authors presented in their TEM results, most of the dye-functionalized CNT showed debundled structure. Hence, the change of CNT aggregation could be another key factor for organic chemical adsorption. Another character of CNT morphology is related to the angle between the graphite plane and the tube axis, which determines the chirality of CNTs: zigzag, armchair, and chiral structures. The C-C bonds in graphite are all the same, but C-C bonds in CNTs are different by length and orientation to the tube axis (44). Thus both adsorption energy and the distance between organic chemicals and CNT surfaces could differ between zigzag and armchair tubes of a same curvature (diameter). However, no experiments have been conducted for organic chemical sorption on CNTs with different chiralities. Functional Groups of CNTs. CNTs possibly contain functional groups such as sOH, sCdO, and sCOOH depending on the synthetic procedure and purification process. Functional groups can also be intentionally added by oxidation (22) or removed by heat treatment (such as 2200 °C in ref 50). In a well controlled experiment, 3.3-14% surface oxides could be sequentially incorporated on CNTs using nitric acid (39). Ago et al. (51) quantified surface functional groups of acid-oxidized CNT using X-ray photoelectron spectroscopy, and presented that 5, 2, and 7% of the carbon atoms were sCsOs, sCdO, and sCOOs, respectively. The air-oxidized CNTs showed higher sCsOs (9%), but lower sCOOs (3%) content. Functionalization of CNTs is aimed for easy processing, but at the same time, their adsorption properties with organic chemicals can be altered greatly. Functional groups can change the wettability of CNT surfaces, and consequently make CNT more hydrophilic and suitable for the adsorption of relatively low molecular weight and polar compounds (13, 50, 52). On the other hand, functional groups may increase diffusional resistance (47) and reduce the accessibility and affinity of CNT surfaces for organic chemicals (39, 53). An overall view of the effect of CNT functional groups on organic molecule adsorption is summarized in Figure 2. In previous studies, hydrogen bonds (H-bond) have been discussed extensively to understand organic chemical sorption on ACs (54). However, several studies reported that increased oxygen-containing functional groups on ACs decreased the adsorption of chemicals which can form H-bonds (55). These opposite results call for further research on the H-bond mechanism. In addition, water molecules could also form H-bonds with functional groups on ACs, which will either compete with organic chemicals for adsorption sites (54) or form a three-dimensional cluster VOL. 42, NO. 24, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 9007 and block the sorption sites nearby (56). Thus, the H-bond formation between water and AC functional groups could effectively decrease the sorption of organic chemicals. Therefore, the relative H-bond strength of water-ACs to organic chemicals-ACs determines the extent for adsorption of organic chemicals. Similar arguments apply for organic chemical sorption on CNTs. Although H-bonds are reported unlikely to be a primary interaction mechanism (36, 37), benzene ring on CNT surface may act as H-bond donor and form H-bonds with oxygen-containing functional groups on organic chemicals (57). In addition, H-bonds may play an important role for ionic chemical adsorption on oxidized CNTs. Clearly, further study is required to systematically evaluate H-bonds in organic chemical-CNT interactions. During CNT surface functionalization, purification, or exposure to oxidizing agents after release to the environment, CNTs will eventually be oxidized (39). Therefore, a better understanding of toxicology and adsorption properties of oxidized CNTs is important for CNT environmental risk assessment. Adsorption Mechanisms of Different types of Organic Chemicals on CNTs Molecular Morphology.Molecular size and shape determine the availability of different adsorption sites on CNTs. The discussion of the relative size between organic molecules and CNTs applies here, too. Specifically for organic chemicals, larger molecules have higher adsorption energies, and thus larger differences in molecular size result in better separation in a system with mixed chemicals (42). Linear hydrocarbons (42) and planar chemicals (49), especially linear planar chemicals (such as tetracene in ref 58), have a better contact with the CNT surface than other chemicals, and hence show stronger adsorption on CNTs. The bottleneck for the rate of organic chemical diffusion is also dependent on molecular size. An example is given by slow diffusion of water and ethanol as compared to that of n-hexane (26). Sorption of n-hexane on CNTs reached equilibrium in 20-30 min, while water and ethanol took more than 10 h. This phenomenonmay be partially explained by the higher hydrophobicity of hexane as the authors presented. However, their data could be reevaluated because the much higher sorption capacity (more than 10 times higher) for water and ethanol may indicate different availability of adsorption sites for chemicals with different sizes. For smaller molecules (water and ethanol), the diffusion into inner sites of CNTs can be the rate-limiting process, and could result in extremely low diffusivities. However, bigger molecules (hexane) have a much faster sorption rate because contribution of hexane adsorption in the inner pores is very low. Molecules, especially the larger ones, can twist themselves so that they match with the curvature surface, thus forming stable complexes with the CNTs (59-61). This molecular reorganization is possible because the adsorption energy can compensate the steric energy required for conformational changes of organic chemicals (29). Wang et al. (30) reported lower decomposition temperature for tetra-tert-butylphthalocyanines after adsorption on CNTs, which is a result of the increased internal energy. A similar result was also reported for L-phenylalanine sorption on CNTs (52), however, the authors attributed the reduced decomposition temperature to the catalysis of CNTs. The geometrical configurations of both chemicals and CNTs affect their interactions. It is reasonable to expect a significant effect of the geometrical configurations of both chemicals and CNTs on their interactions because the surface curvature of CNTs is comparable to the dimensions of organicmolecules. However, few studies have yet focused on conformational rearrangement of organic chemicals on CNTs. Functional Groups of Organic Chemicals. Each carbon atom in a CNT has a π electron orbit perpendicular to CNT surface (62). Therefore, organic molecules containing π electrons can form π-π bonds with CNTs, such as organic molecules with CdC double bonds or benzene rings, which has been confirmed by experimental data (36, 37, 63), molecular dynamic simulations (64-66), Raman band (58), Fourier transform infrared spectra (43), and nuclearmagnetic resonance spectra (28). Themost widely recognized influence of organic chemical functional groups on organic chemicalCNT interactions is on the electron-donor-acceptor (EDA) π-π interaction, i.e., the strength of π-π bond is greatly dependent on the functional groups attached to the benzenerings for organic chemicals (37). Because CNTs could be viewed as either electron-donors or acceptors, adsorption of either electron-acceptors (such as nitroaromatics in ref 35) or electron-donors (such as phenols in ref 53) on CNTs is expected to be stronger as compared to unsubstituted FIGURE 2. Adsorption properties as affected by CNT functional groups. This figure shows the general trend for the changes of CNT adsorption properties after different treatments. The surfaces of raw CNTs are hydrophobic as demonstrated by the strong preference for adsorption of hydrocarbons (such as hexane, benzene, and cyclohexane) over alcohols (such as ethanol, 2-propanol). Functionalization will lead to increased oxygen content, decreased surface area, and reduced adsorption of nonpolar hydrocarbons due to reduced hydrophobicity, and so do planar chemicals due to insufficient contact between CNT and the chemical. Graphitization will eliminate functional groups, and decrease the adsorption of polar chemicals, but will increase the adsorption of nonpolar and/or planar hydrocarbons. 9008 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 42, NO. 24, 2008 aromatic hydrocarbons. In addition, the tendency of a molecule to accept or donate electrons also determines the strength of the π-π bond, as in the case with strong charge donors over weak charge donors (such as 2,3-dichloro-5,6- dicyano-1,4-benzoquinone over benzene in ref 65). The introduction of carboxylic groups to CNTs made CNTs electron acceptors. Thus increased adsorption of electron donors (such as phenanthrene in ref 43 and BTEX in ref 67), and decreased adsorption of electron acceptors (such as chlorophenol in ref 68) were observed. Therefore, quantification of EDA strength could provide a valuable parameter to predicting organic chemical-CNT interactions. Zhao et al. (65) used a charge transfer parameter, specifically, the total Mulliken charge number on several molecules, to quantitatively describe the ability of a certain molecule to donate or withdraw electrons. Sone et al. (69) proposed that aromatic compounds with a smaller gap between the highest occupied molecular orbital energy and the lowest unoccupied molecular orbital will have a higher affinity toward CNTs. Both methods seem to be promising to predict the strength of organic chemical-CNTinteractions. However, no information is available on how well these theories could explain experimental data. Additional laboratory experiments should be conducted. Functional groups also greatly determine organic chemical polarity. Because the predominant mechanisms are different for polar and nonpolar chemicals, predictions of their adsorption on CNTs require different models. For example, for polar organic chemicals, the adsorption tends to increase with increased CNT oxygen content because of the enhanced H-bond or EDAinteraction. However, for nonpolar chemicals, the adsorption may decrease with increased CNT oxygen content because of the depressed hydrophobic interaction (Figure S4). These opposite trends have not been examined extensively in literature, but could be very important for CNT applications. For example, if CNTs are to be used in water treatment, chemical-specific modification may be needed to improve treatment performance. For the same reason, chemical-specific models may also be needed to predict organic chemical-CNT interactions. The present data are too limited for further discussion on predictive models. Adsorption Affected by Environmental Conditions Environmental conditions have not been widely studied for their impact on organic chemical-CNT interactions. However, a limited number of studies in this area have demonstrated their importance. pH and Ionic Strength. For ionizable organic chemicals, the variation in pH can result in a change in chemical speciation, consequently altering their adsorption characteristics. Increased pH generally leads to increased ionization, solubility, and hydrophilicity, and thus decreased adsorption of natural organic matter (8, 70), resorcinol (53), and herbicides (6, 71) on CNTs. This type of trend is more obvious for functionalized CNTs compared with graphitized ones, which was attributed to the enhanced formation of water clusters or reduced H-bond formation when CNT carboxylic groups were ionized at elevated pHs (50). On the other hand, increased adsorption with increased pH was also observed and was attributed to enhanced EDA interactions (3, 37). The apparent pH influence on organic chemical adsorption depends on how the increase in attractive forces (e.g., EDA) counteracts the increase of repulsive forces (e.g., charge repulsion) and/or the decline of certain attractiveinteractions (e.g., H-bond formation and hydrophobic interaction). Valuable data may also be derived by comparing solution pH, the pKa of the organic chemical, and the pHpzc (point of zero charge) of CNTs. Low adsorption would be expected at pH > pKa and pHpzc because both adsorbent and adsorbate are negatively charged and electrostatic repulsion may be one of the dominant mechanisms. On the other hand, the organic chemical would show high adsorption under conditions with pHpzc > pH > pKa because of their electrostatic attraction with CNTs. The presence ofmetalions can bridge DOM and functional groups on CNTs, compress the double layer, neutralize negative charges of DOM, and thus weaken the repulsion between DOM molecules, and between DOM and CNTs (8, 70, 72). However, several questions remain unanswered. It is still unknown how the adsorption of metal ions alters the aggregation of CNT bundles, which consequently changes CNT adsorption with organic chemicals. Also, adsorption of mixed pollutants (including metals and organic chemicals) has not been widely investigated. The adsorption that is affected by the presence of another organic chemical could be understood from the competition between organic chemicals (73). But the presence of both metals and organic chemicals is a more complicated situation. Studies on wood charcoal adsorption properties have shown that coadsorption of copper ions decreased organic chemical sorption because of the formation of hydration shell (74). However, coadsorption of silver ions increased organic chemical sorption owing to the declined hydrophilicity of thelocal region around adsorbed silver ions, and thus reduced competitive sorption of water. Similar study on CNTs could provide useful information on organic chemical sorption mechanisms. Although significant effects of ionic strength on CNT adsorption characteristics has not been observed (43, 63), further research is needed, which will facilitate the prediction of organic chemical sorption on CNTs in a real environment. Dispersion of CNTs by Surfactants or DOM. Both surfactants (60, 75, 76) and DOM (7, 77, 78) have been reported to suspend CNTs significantly. Different dispersion mechanisms have been proposed, such as CNT solubilization inside surfactant columnar micelles (79), surfactant or DOM monolayer coatings on CNT surfaces (80), and “unzippering” of CNT bundles (81). Among all these mechanisms, surface coating of surfactants or DOM on CNTs is a key process. Although aromatic carbon content was observed to be proportional to DOM adsorption on CNTs, the amount of stable CNT suspension in aqueous phase did not follow a simple linear relationship with the adsorbed DOM concentration (72). The ability of a certain DOM to suspend CNTs is highly dependent on DOM properties. For example, hydrophobic DOM fraction may suspend CNTs more ef- ficiently than hydrophilic DOM fraction simply because of better contact of the hydrophobic fraction with the CNT surface (Figure 3). This speculation could be easily tested and may serve as a useful theory for effectively dispersing and suspending CNTs. Organic chemical-CNT interactions could be remarkably altered after CNT suspension. On one hand, the presence of surfactants or DOM could enhance the solubility of organic chemicals, and decrease their adsorption. On the other hand, surfactants or DOM can disperse CNT bundles and make more adsorption sites available for adsorbates, thus increasing the adsorption (82). The net impact depends on the balance of these two opposite factors as summarizedin Figure 4. Enhanced adsorption of phenanthrene (21), benzene, toluene, and n-undecane (82) on CNTs after being dispersed by surfactants was observed. The authors concluded that organic chemicals were able to interact more strongly with CNT surfaces in the presence of surfactants than without surfactants because of CNT dispersion by surfactants. Very few studies focused on CNT adsorption properties after being suspended by DOM. Although a humic acid (HA) had much lower sorption for phenanthrene, naphthalene, and Rnaphthol than CNTs, the HA-coated CNTs did not show distinct changes in sorption of these compounds relative to the original CNTs, probably due to the newly exposed sites VOL. 42, NO. 24, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 9009 from enhanced dispersion as a result of the HA coating (83). Chen et al. (63) observed decreased adsorption of CNTs in the presence of DOM in the aqueous phase. However, no CNT suspension was involved in their study. Future studies need to consider the complexity of organic chemical behavior in an organic chemical-DOM-CNT three-phase system including fractionation of DOM upon adsorption on CNTs, nonideal interactions between organic chemicals and DOM, and disaggregation of CNT bundles. Dispersed CNTs are stable in various solvents, such as in water, toluene, and chloroform (84, 85). Thus dispersed CNTs and CNT-adsorbed organic chemicals can readily move in environmental media, which would subsequently facilitate the spread of various organic chemicals and thus increase their environmental risk, as expected from CNT’s high adsorption capacity. However, previous studies have rarely focused on CNT dispersion in relation to their adsorption with organic chemicals. One of the major reasons could be the difficulty in separating free dissolved organic chemicals from suspended CNTs. Because environmental risks of both CNTs and organic chemicals could be accurately assessed only if free dissolved organic chemicals could be separated and analyzed, proper separation methods need to be developed to study adsorption properties of suspended CNTs. Filtration (72, 78) and/or dialysis systems (86) may be applicable for separation purposes in future studies. Adsorption of Organic Chemicals by CNTs in Comparison with ACs CNTs, especially SWCNTs, have shown to be more efficient adsorbents than ACs and other adsorbents (Table SIII), with higher adsorption capacity (7, 13, 87), shorter equilibrium time (13, 50, 87), higher adsorption energy (88), and easier and more efficient regeneration (7, 8). As presented in Figure S5, SWCNTs generally have higher adsorption coefficients than ACs. For the above reasons, SWCNTs have the potential to be adsorbents for air purification and water treatment. Some studies reported low adsorption capacities of CNTs depending on their properties (27, 89). However, these authors speculate that an important part of CNT surfaces does not participate in adsorption processes (89), and adsorption capacity could be enhanced after proper treatment and processing, e.g., end-opening and functionalization. The unit price for ACs is currently much cheaper than that for SWCNTs, and thus they are widely used in air and water treatment. For the purpose of application in water treatment, numerous experiments have been conducted in column and pilot scales to evaluate ACs performance and operational cost (e.g., ref 90). However, such experiments are not available for CNTs. It should be emphasized that CNTs can be regenerated, maintaining high adsorption efficiency. Thus, they last longer than ACs do. Therefore, the FIGURE 3. CNT suspension as affected by DOM adsorption. HiDOM (solid line) stands for hydrophilic DOM fraction and HoDOM (dotted line) stands for hydrophobic fraction. Adsorption of HoDOM decreases with increased CNT oxygen content because of the decreased hydrophobicity of CNTs after oxidation. For the same reason, HiDOM follows the opposite trend (a). HoDOM suspends CNTs more efficiently than HiDOM (b) because a better contact between CNT and HoDOM is expected (c). FIGURE 4. Schematic diagram for dispersion of CNTs and their properties. The CNT aggregates can be dispersed after oxidation (a) or after coating with DOM or surfactants (c). Aggregate sizes (solid line) and zeta potentials (dotted line) decrease with increasing oxygen content (d) or DOM/surfactant concentration (e). For the adsorption of organic chemicals on CNTs dominated by hydrophobic effects, the oxidation of CNTs results in a decrease of adsorption because of the increased hydrophilicity of CNT surface. As they are further oxidized, the CNTs are dispersed and more adsorption sites are available, which may result in a slow rate of adsorption reduction (dashed line in panel d). However, for the adsorption of organic chemicals on CNTs dominated by H-bonds, adsorption would proportionally increase with oxygen content (dashed/dotted line in panel d). The adsorption of organic chemicals on CNTs may increase dramatically with the concentration of DOM or surfactant because of DOM fractionation and CNT dispersion (dashed and dashed/lines in panel e). Further increase of DOM or surfactants concentration in solution increases the solubility of organic chemicals strikingly, thus the apparent adsorption would decrease. 9010 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 42, NO. 24, 2008 operational expense for CNTs in water treatment could be lower if they are properly regenerated. However, accurate estimate of these benefits and operational performance warrant investigations. Perspectives Various mechanisms may simultaneously control organic chemical adsorption on CNTs. Each adsorption mechanism may be affected differently by environmental conditions. For example, when H-bonds are the predominant mechanism, increased oxygen-containing functional groups on CNTs would increase the sorption. However, for sorption controlled by hydrophobic interactions, the increased functional groups would decrease the accessibility and affinity of CNTs for organic chemicals. Therefore, it is of great importance to obtain the relative contribution of different mechanisms to the overall sorption in the future. Comparisons between sorption results with or without a given mechanism may clarify the contribution and importance of individual mechanisms. For instance, sorption experiments conducted in aqueous phase complicate the discussion of sorption mechanisms because of the overwhelming hydrophobic effect. Analysis of sorption results obtained from sorption experiments in organic solvents with various polarities may help understand the contribution of hydrophobic effect. Nearly half of the current studies are theoretical simulations. Theoretical simulations often use vacuum conditions, not as they would behave in the real environment. Therefore, the results from the simulations may hardly be applicable in environmental conditions. More laboratory studies are required to systematically investigate the sorption of organic chemicals with different functional groups, hydrophobicity, and ability to donate or withdraw electrons (e.g., total Mulliken charge number). Also, very limited studies reported the effect of water chemistry on organic chemical sorption on CNTs. Extensive work is needed to examine the pH-, ionic strength-, and DOM-dependent sorption. Special concern should be directed to investigating CNT aggregation in different water chemistry conditions, and the resulting influence on sorption properties. As more and more CNTs enter the environment during CNT production, application, and disposal, environmental risk posed by CNTs will be controlled by their transport, exposure, and interaction with other pollutants. A better understanding of organic chemical-CNT interaction mechanisms and subsequent environmental behavior of both organic chemicals and CNTs will provide a fundamental basis for the prediction of CNT risk. In addition, being aware of CNT environmental risk helps to develop guidelines for safe design and application of CNTs. Numerous studies have recommended CNTs as alterative adsorbents in water treatment over ACs after batch adsorption experiments, but further work should investigate the performance and operational cost of CNTs in column and pilot scales. Acknowledgments This research was supported by the Massachusetts Water Resource Center (2007MA73B) and Massachusetts Agricultural Experiment Station (MA 90). We are also thankful to the four anonymous reviewers for their valuable comments to improve this manuscript. Supporting Information Available Three tables and five figures. These materials are available free of charge via the Internet at ACS Publications Home Page. Literature Cited (1) Nowack, B.; Bucheli, T. D. Occurrence, behavior and effects of nanoparticles in the environment. Environ. Pollut. 2007, 150, 5–22. (2) Mauter, M. S.; Elimelech, M. Environmental applications of carbon-based nanomaterials. Environ. Sci. Technol. 2008, 42, 5843–5859. (3) Helland, A.; Wick, P.; Koehler, A.; Schmid, K.; Som, C. Reviewing the environmental and human health knowledge base of carbon nanotubes. Environ. Health Persp. 2007, 115, 1125–1131. (4) Rao, G. P.; Lu, C.; Su, F. 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Sea otters: their role in structuring nearshore communities . Science 185:1058–https://www.ncbi.nlm.nih.gov/books/NBK224412/#_NBK224412_pubdet_The individual components of biodiversity—genes, species, and ecosystems—provide society with a wide array of goods and services. Genes, species, and ecosystems of direct, indirect, or potential use to humanity are often referred to as "biological resources" (McNeely and others 1990; Reid and Miller 1989; Wood 1997). Examples that we use directly include the genes that plant breeders use to develop new crop varieties; the species that we use for various foods, medicines, and industrial products; and the ecosystems that provide services, such as water purification and flood control. The components of biodiversity are interconnected. For example, genetic diversity provides the basis of continuing adaptation to changing conditions, and continued crop productivity rests on the diversity in crop species and on the variety of soil invertebrates and microorganisms that maintain soil fertility. Similarly, a change in the composition and abundance of the species that make up an ecosystem can alter the services that can be obtained from the system. In this chapter, we review the types of goods and services that mankind obtains directly and indirectly from biodiversity and its components.Biodiversity contributes to our knowledge in ways that are both informative and transformative. Knowledge about the components of biodiversity is valuable in stimulating technological innovation and in learning about human biology and ecology. Experiencing and increasing our knowledge about biodiversity transform our values and beliefs. There is a fairly large literature characterizing nonextractive ecosystem services with direct benefit to society, such as water pollution and purification, flood control, pollination, and pest control. In addition, such services in biophysical and economic terms characterize the institutional mechanisms needed to generate incentives for their preservation (Daily 1997; Missouri Botanical Garden forthcoming). In this chapter, we review the types of social and cultural values associated with knowledge of biodiversity. We use those values in chapter 4 to discuss how they can contribute to decisions on management of biodiversity.Biological ValuesThe components of biodiversity are the source of all our food and many of our medicines, fibers, fuels, and industrial products. The direct uses of the components of biodiversity contribute substantially to the economy. In 1989, US agriculture, forestry, and fisheries contributed $113 billion1 to the US gross domestic product (GDP), equal to the contribution of the chemical and petroleum industries combined (DOC 1993). The full contribution of biodiversity-related industries to the economy is higher still, in that it includes shares of such sectors as recreation (see Everglades and Boulder, Colo., case studies in this chapter and Lake Washington case study in chapter 6), hunting (see Quabbin Reservoir case study in chapter 6), tourism (see Costa Rica case study in chapter 2), and pharmaceuticals.The economies of most developing countries depend more heavily on natural resources, so biodiversity-related sectors contribute larger shares of their GDPs. For example, the sum of the agriculture, forestry, and forest-industry products in Costa Rica in 1987 accounted for 19% of the nation's GDP (TSC/WRI 1991), whereas these sectors accounted for only 2% of the US GDP (DOC 1993). The relatively small direct economic contribution of biological resources in the two countries illustrates the difficulty of "valuing" biodiversity. The small fraction of the value of these ecological systems that is accounted for in US economic ledgers contrasts starkly with the fact that our survival depends on functioning ecological systems. At the same time, our limited ability to value ecological parallels our limited appreciation of our dependence on these systems. The imperfections of our knowledge are seen in the $200 million Biosphere 2 trial—in the unsuccessful attempt to house eight people for 2 years in an ecologically closed system. Cohen and Tilman (1996) concluded that "no one yet knows how to engineer systems that provide humans with the life-supporting services that natural ecosystems produce for free."Biodiversity in Domesticated SystemsHumans rely on a relatively small fraction of species diversity for food. Only about 150 species of plants have entered world commerce, and 103 species account for 90% of the supply of food plants by weight, calories, protein, and fat for most of the world's countries (Prescott-Allen and Prescott-Allen 1990). Just three crops—wheat, rice, and maize—account for roughly 60% of the calories and 56% of the protein consumed directly from plants (Wilkes 1985). Relatively few species that have not already been used as foods are likely to enter our food supply, but many species now consumed only locally are likely to be introduced into larger markets and grown in different regions. For example, the kiwi fruit was introduced into the United States as recently as 1961; within 20 years, US sales had grown to some $22 million per year (Myers 1997).Although relatively few species are consumed for food, their productivity in both traditional and modern agricultural systems depends on genetic diversity within the species and interactions with other species found in the agroecosystem. Claims that such biodiversity "archives" can serve as substitutes for biodiversity in natural habitats are more fanciful than factual. Genetic diversity provides the raw material for plant breeding, which is responsible for much of the increases in productivity in modern agricultural systems. In the United States from 1930 to 1980, plant breeders' use of genetic diversity accounted for at least the doubling in yields of rice, barley, soybeans, wheat, cotton, and sugarcane; a threefold increase in tomato yields; and a fourfold increase in yields of maize, sorghum, and potato. An estimated $1 billion has been added to the value of US agricultural output each year by this widened genetic base (OTA 1987). Breeders rely on access to a wide range of traditional cultivars and wild relatives of crops as sources of genetic material that is used to enhance productivity or quality. Different landraces can contain genes that confer resistance to specific diseases or pests, make crops more responsive to inputs such as water or fertilizers, or confer hardiness enabling the crop to be grown in more extreme weather or soil conditions.Much of the genetic diversity available for crop breeding is now stored in a network of national and international genebanks administered by the UN Food and Agriculture Organization, the Consultative Group on International Agricultural Research, and various national agricultural research programs, such as the US Department of Agriculture's National Seed Storage Laboratory in Fort Collins, Colorado. The value of these genebanks for agricultural improvement is substantial. For example, in a presentation to this committee,2 Evenson and Gollin estimated the present net value of adding 1,000 cataloged accessions of rice landraces to the International Rice Research Institute's genebank at $325 million (on the basis of empirical estimates that these accessions would generate 5.8 additional new varieties, which would generate an annual $145 million income stream with a delay of 10 years). As important as they are in agriculture, genebanks, and other in situ collections (cyropreserved and in zoos) are viable only for a very narrow array of species.The important contribution of genebanks to agricultural productivity has been recognized by government since the 18th century. It led to the rise of botanical gardens and expeditions in search of new plant varieties, including the fabled voyage of the HMS Bounty (Fowler 1994), and is growing substantially as traditional landraces continue to be replaced by modern varieties.Genetic engineering has greatly increased the supply of genetic material available for introduction into crop varieties. Genes from any species of plant, animal, or microorganism can now be moved into a particular plant. For example, genes from the winter flounder have been transferred into the tobacco genome to increase its frost resistance, and genes from the microorganism Bacillus thuringiensis have been transferred into corn, wheat, and rice to give them resistance to insect pests. Genetic engineering is not without considerable risks, and its ultimate success will depend on genetic variability in natural populations. It is clear that the rapid increase in uses of genetic engineering will continue as knowledge and applications of new techniques increase.Not only are specific genes valuable in modern agricultural systems, but the maintenance of genetic diversity is also valuable in traditional agricultural systems. The greater the genetic uniformity of a crop, the greater the risk of catastrophic losses to disease or unusual weather. In 1970, for example, the US corn harvest was reduced by 15%—for a net economic cost of $1 billion—when a leaf fungus spread quickly through a relatively uniform crop (Tatum 1971). Since then, breeders have taken greater precautions to ensure that a heterogeneous array of genetic strains are present in fields, but problems due to reduced diversity still recur. The loss of a large portion of the Soviet Union's wheat crop to cold weather in 1972 and the citrus canker outbreak in Florida in 1984 both stemmed from reductions in genetic diversity (Reid and Miller 1989).Humans also use a relatively small number of livestock species for food and transportation: only about 50 species have been domesticated. Here, too, genetic diversity is the raw material for maintaining and increasing the productivity of species.Biodiversity in Wild SystemsHumans still harvest considerable quantities of food, fuel, and fiber from nondomesticated ecosystems. For example, gross revenue from the world marine fisheries in 1989 amounted to $69 billion (WRI 1994). Fish contribute only 5% of the protein consumed worldwide, but the proportion can be much higher locally. In Japan, the Philippines, the Seychelles, and Ghana, for example, fish account for more than 20% of protein intake (PAI 1995). In some developing countries and among some population segments in developed countries, terrestrial wildlife also continues to be an important subsistence resource. In some areas of Botswana, for example, over 50 species of wild animals provide as much as 40% of the protein in the diet; and in Nigeria, game accounts for about 20% of the animal protein consumed by people in rural areas (McNeely and others 1990).Increased diversity of livestock can sometimes improve productivity. In Africa, for example, "game ranching"—in which wild species of antelope replace domesticated livestock on particular ranches—can result in higher yields of meat than could be obtained from domesticated animals (WRI 1987). Naturally diverse ungulates can use grassland resources more efficiently than domesticated varieties in these situations.In rural Alaska, more than 90% of the people harvest and use wild animals for both food and clothing. The cash value of wild food constitutes 49% of residents' mean income (ADFG 1994). The marine mammals of the northern Bering, Chukchi, and Beaufort seas are among the most diverse in the world; many of the species are used for subsistence purposes by Alaskan Natives, and many have important symbolic roles in cultural identity (NRC 1994).Most of the world's timber production still comes from nondomesticated systems, although a growing share is now harvested on plantations. In tropical forests, for example, the area of plantations increased from 18 million hectares in 1980 to 40 million in 1990. Although statistics on the world value of internal and externally traded timber products are not available, the world value of forest-product exports alone in 1993 was to $100 billion (FAOSTAT 1995).Recreational uses of biodiversity—fishing, hunting, and various nonconsumptive uses, such as bird-watching—also contribute to the economy (see Everglades and Boulder, Colo., case studies in this chapter and Lake Washington case study in chapter 6). In the United States alone, such activities involved about 77 million persons over the age of 16 in 1996 and resulted in expenditures of $101.2 billion (DOI/DOC 1997). Wildlife watchers made up the largest group (62.9 million participants in 1996); their expenditures included $16.7 billion for equipment, $9.4 billion for travel, and $3.1 billion in other expenses. Of a total of 39.7 million sportspersons, 35.2 million were adult anglers and 14.0 million were hunters; this group spent $72 billion in 1996, including $37.8 billion for fishing, $20.6 billion for hunting, and $13.5 billion in unspecified expenses (DOI/DOC 1997).One of the most rapidly growing values of biodiversity in wild ecosystems is related to tourism. Worldwide receipts from international tourism in 1990 totaled $250 billion (WCMC 1992), and domestic tourism is believed to be as much as 10 times higher. How much of the tourist trade is attracted specifically by biodiversity is difficult to tell. Of the $55 billion in tourism revenues accruing to developing countries in 1988, an estimated 4–22% was due to "nature tourism" (Lindberg 1991). More than half of the visitors in Costa Rica, for example, state that the national parks are their "principal reason" for traveling to the country (see the case study on Costa Rica in chapter 2). Costa Rica's protected areas are estimated to account for $87 million annually in tourism revenues.As in domesticated agroecosystems, the diversity of genes and species undergirds the continued productivity of these components of biodiversity in nondomesticated ecosystems. The genetic diversity in a species provides the basis for the species to adapt to changing environmental conditions. Reduced genetic diversity increases the probability of species extinction or of substantial reductions in the population of a species due to changing environmental conditions (such as, a change in climate or the introduction of a new disease). For example, wild exotic trout in the western United States can be destroyed by whirling disease, which is caused by the microorganism Myxobolus cerebralis; the only way to restore infected populations is to find genetically resistant populations (Hoffman 1990).The productivity of an ecosystem can be high both in systems with large numbers of species, such as tropical forests, and in systems with relatively small numbers of species, such as wetlands.The extirpation of the California sea otter from much of its range in the 1800s resulted in substantial changes in near-shore ecosystems (Estes and Palmisano 1974). Recovery of otter populations to their original densities affects other ecosystem components of commercial or recreational value: giant kelp, sea urchins, abalone, and surf clams. The sea otter is a primary predator (top of the food chain) of mollusks and urchins, which graze on stands of algae that are primary producers (of calories consumed) in coastal regions extending from California through the Aleutian Islands. As a consequence of the extirpation of sea otters, grazing urchins became common and reduced the biomass of primary producers.Just like the loss of specific species, the manipulation of the food chain structure can alter the productivity of direct value to humans. For example, in areas where intense gillnet fisheries have seriously depleted Nile perch stocks, many African cichlids have recovered in Lake Victoria (Kaufman 1992). Equivalently, the introduction of the Nile perch into Lake Victoria led to the extinction of many species of the native cichlid fish and substantially reduced the total harvest of this important food source (Johnson and others 1996).Biodiversity in the Pharmaceutical and Biotechnology IndustryWild species of plants and animals have long been the source of important pharmaceutical products. Natural products play a central role in traditional healthcare systems. The World Health Organization estimates that some 80% of people in developing countries obtain their primary health care in the form of traditional medicines (Farnsworth 1988). Systems of ayurvedic medicine (traditional Hindu medical practices) in India and the traditional systems of Chinese herbal medicine, for example, reach hundreds of millions of people. Total sales of herbal medicines in Europe, Asia, and North America were estimated at $8.4 billion in 1993 (Laird and Wynberg 1996). That total is not large on a global scale, but sales of herbal medicines can often be an important source of income for local communities and business.Natural products also continue to play a central role in the pharmacopeia of industrialized nations. Of the highest-selling 150 prescription drugs sold in the United States in 1993, 18% of the 150 consisted of essentially unaltered natural products, and natural products provided essential information used to synthesize an additional 39% (Grifo and others 1997). In total, 57% owed their existence either directly or indirectly to natural products.Natural products were once the only source of pharmaceuticals, but by the 1960s synthetic chemistry had advanced to the point where the pharmaceutical industry's interest in natural products for drug development had declined greatly and it declined further with the introduction of "rational drug design". Several technological advances led to a resurgence of interest in research in natural products in the 1980s. The development of modern techniques involving computers, robotics, and highly sensitive instrumentation for the extraction, fractionation, and chemical identification of natural products has dramatically increased the efficiency and decreased the cost of screening for natural products. Before the 1980s, a laboratory using test-tube and in vivo assays could screen 100–1,000 samples per week. Now, a laboratory using in vitro mechanism-based assays and robotics can screen 10,000 samples per week. Where the screening of 10,000 plant extracts would have cost $6 million a decade ago, it can now be accomplished for $150,000 (Reid and others 1995). In the next decade, throughput could grow by a factor of 10–100.As the new technologies became available in the 1980s, many companies established natural-products research divisions. Of 27 companies interviewed in 1991, two-thirds had established their natural-products programs within the preceding 6 years (Reid and others 1993). In most large pharmaceutical companies, natural-products research accounts for 10% or less of overall research. But some smaller companies now focus exclusively on natural products. For example, Shaman Pharmaceuticals bases all its drug-discovery research on natural products used in traditional healing systems, and it currently has two drugs in clinical trials.How long the interest in natural-products drug discovery will last is impossible to know. New techniques of combinatorial chemistry and other advances in drug design might reduce interest in natural-products research. Even so, many chemists feel that current synthetic chemistry is still unable to match, the complexity of many of the natural compounds that have proved effective as drugs. For example, paclitaxel, known as Taxol, a compound from the Pacific yew tree (which is not considered economically important for timber or other commercial purposes), is being used in treatment for ovarian and breast cancer. The compound was discovered in the 1960s but could not be synthesized until the 1990s; and even now, the process is so time-consuming and expensive that natural precursors are used in the production of the drug.Drugs developed from natural products often generate large profits for drug companies, but the actual value of biodiversity as a ''raw material'' for drug development is much smaller (Simpson and others 1996). On the average, some $235 million and 12 years of work are required to produce a single marketable product in the drug industry. Moreover, less than 1 in 10,000 chemicals is likely to result in a potential new drug and only 1 in 4 of those candidates will make it to the pharmacy. On the basis of typical royalties paid for raw materials, the likelihood of discovering a new drug, the length of patent protection, and the discount rate, the present net value of an arrangement whereby a nation contributes 1,000 extracts for screening by industry would be only about $50,000. Moreover, there would be a 97.5% chance that no product at all would be produced. The likelihood that any particular plant or animal will yield a new drug is extremely small, but endangered species in the United States have yielded new drugs. We can to some degree aggregate the plants and animals that are most likely to lead to new drugs. These are likely to have considerable value as prospects (Rausser and Small in press).BiotechnologyUntil recently, pharmaceutical, agricultural, and industrial uses of biodiversity relied on largely different methods of research and development. Today, with the help of the new biotechnologies, individual samples of plants or microorganisms can be maintained in culture and screened for potential use in any of those industries. Companies are screening the properties of organisms to develop new antifouling compounds for ships, new glues, and to isolate new genes and proteins for use in industry. A thermophilic bacterium collected from Yellowstone hot springs provided the heat-stable enzyme Taq polymerase, which makes it possible, in a process known as polymerase chain reaction (PCR), to amplify specific DNA target sequences derived from minute quantities of DNA. PCR has provided the basis of medical diagnoses, forensic analyses, and basic research that were impossible just 10 years ago. The current world market for Taq polymerase, is $80–85 million per year (Rabinow 1996). Biodiversity is the essential "raw material" of the biotechnology industry, but the process of examining biodiversity for new applications in that industry has only begun.Biodiversity and BioremediationIt has become clear in recent years that the fundamental role of microorganisms in global processes can be exploited in maintaining and restoring environmental productivity and quality. Indeed, microorganisms are already playing important roles, both in the prevention of pollution (for example, through waste processing and environmental monitoring) and in environmental restoration (for example, through bioremediation of spilled oil). Modern biotechnology is providing tools that will enhance the environmental roles of microorganisms, and this trend should accelerate as the appropriate basic and applied sciences mature (Colwell 1995; Zilinskas and others 1995). A variety of probes and diagnostics for monitoring food and environmental quality have been developed (Dooley 1994), and there is much discussion of the development of genetically engineered organisms for speeding the clean up of wastes, spills, and contaminated sediments. Furthermore, marine biotechnology is being pursued avidly and on a larger scale in Japan (Yamaguchi 1996), where one major goal is to find ways to lower global atmospheric CO2concentrations. Without doubt, the prediction of climate change will be much improved by a better understanding of global cycles, and the tools of marine biotechnology will be heavily involved in this endeavor.The fundamental premise here is that chronic pollution reduces system species diversity and diminishes ecosystem function. Thus, restoring perceived environmental quality and productivity cannot easily be separated from basic biodiversity issues.Ecosystem ServicesA substantial risk of undesirable and unexpected changes in ecosystem services is posed when the abundance of any species in an ecosystem is changed greatly. Our ability to predict which species are important for particular services is limited by the absence of detailed experimental studies of the ecosystem in question. Nonetheless, the available data indicate that a higher level of species diversity in an ecosystem tends to increase the likelihood that particular ecosystem services will be maintained in the face of changing ecological or climatic conditions (below, "Species Diversity and Ecosystem Services").Both wild and human-modified ecosystems provide humankind with a variety of services that we often take for granted (see box 3-1). The services include the provision of clean water, regulation of water flows, modification of local and regional climate and rainfall, maintenance of soil fertility, flood control, pest control, and the protection of coastal zones from storm damage. All those are "products" of ecosystems and thus a product of biodiversity. The characteristics and maintenance of these ecosystem services are linked to the diversity of species in the systems and ultimately to the genetic diversity within those species. However, the nature of this relationship between ecosystem services and biodiversity at the lower levels of species and genetic diversity is complex and only partially understood.Types of Ecosystem Services Linked to BiodiversityBOX 3-1 Types of Ecosystem Services Linked to Biodiversity Atmospheric—Climatic Gaseous composition of the atmosphere Moderation of local and regional weather, including temperature and precipitation Hydrological Water quality and quantity Stream-bank stability Control of severity of floods Stability of coastal zones (through presence of coastal communities, such as coral reefs, mangroves, or seagrass beds) Biological and Chemical Biotransformation, detoxification, and dispersal of wastes Cycling of elements, particularly carbon, nitrogen, oxygen, and sulfur Buffering and moderation of the hydrological cycle Nutrient cycling and decay of organic matter Control of parasites and disease, pest control Maintenance of genetic library Habitat and food-chain support Agricultural Economic and Social SOURCE: Adapted from Daily 1997.https://www.ncbi.nlm.nih.gov/books/NBK224412/box/bbb00002/?report=objectonlyTypes of Ecosystem Services Linked to Biodiversity. Atmospheric—Climatic Gaseous composition of the atmosphereBiodiversity and Ecosystem ServicesHumankind derives considerable benefits not only from the products of biodiversity but also from services of ecological systems, such as water purification, erosion control, and pollination. The relationship between biodiversity and ecosystem services is complex and will be discussed in greater detail later, but in general, most ecosystem services are degraded or diminished if the biodiversity of an ecosystem is substantially diminished. Because most ecosystem services are provided freely by natural systems, we typically become aware of their value and importance only when they are lost or diminished.Historically, ecosystem services were not generally scarce and management decisions were rarely based on their low marginal value. That is decreasingly true, particularly with regard to drinking-water quality, flood control, pollination, soil fertility, and carbon sequestration. This trend is prompting interest in developing institutional frameworks through which to restore and safeguard these services in the United States and internationally.The cost of the loss of various ecosystem services can be high. The US National Marine Fisheries Service estimated that the destruction of US coastal estuaries in 1954–1978 costs the nation over $200 million per year in revenues lost from commercial and sport fisheries (McNeely and others 1990). Hodgson and Dixon (1988) calculated the cost of the potential loss of the service that the forested watershed of Bacuit Bay in the Philippines provides in preventing siltation of the coastal coral ecosystem. The forest prevents siltation: if it were cut, siltation would increase, thereby reducing tourism and fisheries revenues. In a scenario in which logging is banned in the basin, the net present value of a 10-year sum of gross revenues from all three sources would be $42 million. In a scenario of continued logging, the net present value would be only $25 million. One recent and controversial set of global estimates of the value of ecosystem services is discussed in chapter 5.The value of various ecosystem services can also be seen in the costs that must be incurred to replace them. For example, natural soil ecosystems help to maintain high crop productivity, and the productivity that is lost if soil is degraded through erosion or through changes in species composition can sometimes be restored through the introduction of relatively expensive fertilizers or irrigation. Forested watersheds slow siltation of downstream reservoirs used for hydropower; a forest is altered and sedimentation increases, the hydroelectric power generating capacity lost could be replaced through the construction of new dams. Wetlands play important roles as "buffers", absorbing much stream runoff and preventing floods; if wetlands are filled, their flood-control role could be assumed by new flood-control dams. The US Army Corps of Engineers estimated that retaining a wetlands complex outside Boston, Massachusetts, realized an annual cost savings of $17 million in flood protection (McNeely and others 1990).The conversion of one type of habitat to another—such as a conversion of natural forest to agriculture or of agricultural land to suburban development—can dramatically affect a wide variety of ecosystem services. Historically, the impacts of such conversions on ecosystem services have not received attention from policy-makers and managers, for two main reasons. First, the relationship between an ecosystem and a service is typically poorly understood. The conversion of a park to a parking lot will obviously change patterns of water runoff, but other effects of habitat conversions are difficult to predict. For example, the replacement of native vegetation in the western Australian wheatbelt with annual crops and pastures reduced rates of transpiration, increased runoff, and consequently raised the water table, creating waterlogged soil. Salts that had accumulated deep in the soil salinized the soil surface. The saline wet conditions altered ecosystem services by reducing farmland productivity and reducing the supply of freshwater. Restoring such degraded ecosystems can take decades and be accomplished at high cost. In addition, the changes threatened the remaining fragments of native communities and salinized the region's freshwater lakes. Careful research could probably have predicted many of those effects, but such research is rarely undertaken before a land-use change (Heywood 1995).Second, ecosystem services are often public goods. Individual landowners who cut their forests bear little if any of the cost associated with the reduction of water quality experienced by downstream water-users. Similarly, the flood control service that is lost when landowners fill their wetlands might have little direct effect on those landowners, but the private economic benefits of land conversion to agriculture will be important (see the following case study on the Everglades). Such losses are described in economic terms as "externalities"; the changes in the environment occur as a result of economic activity, such as land development or cutting forests for lumber, but the losses are external to the market transactions.Case Study: The EvergladesThis case study shows the complexity of valuing ecological resources and developing achievable scenarios for ecological and economic sustainability in a watershed system, particularly one in which human activities that change the quality or flow of water in one area affect the biological uniqueness, aesthetic value, and local economy of other areas.The Everglades are part of the largest wetland ecosystem in the lower 48 states. Historically, water from the Kissimmee River flowed southward into Lake Okeechobee and during wet years overflowed the southern rim of the lake, spreading across the Everglades in a broad "river of grass" that slowly flowed southward to the Florida Bay estuary. The large spatial scale of the system, the highly variable seasonal and interannual patterns of water storage and sheet flow across the landscape, and the very low concentrations of nutrients in the surface waters led to a unique assemblage of wading birds, large vertebrates, and fish and plant communities in a mosaic of habitats over the region (Davis and Ogden 1994).Since the early 1990s, the environment of Southern Florida has undergone extensive habitat degradation associated with hydrological alterations by humans. Initially, these were to drain land for agriculture and human settlements; later alterations were to protect against flooding. The resulting Central and Southern Florida Project (the C&SF Project) of the US Army Corps of Engineers is one of the most massive engineered hydrological systems in the world. The human population of Southern Florida is now 4.5 million and growing at a rate of almost 1 million per decade, mostly concentrated along the lower eastern coast.The Everglades has been compartmentalized for a variety of land uses: agriculture in the north, where the largest accumulations of organic soils once existed; water conservation areas in the central portions; and the Everglades National Park in the south. The Everglades Agricultural Area (EAA) covers about 27% of the historical system, the water conservation areas 33%, the park 21%, urban areas about 12%, and various nondeveloped areas about 7% (Gunderson and Loftus 1993). About half the original Everglades remains in some semblance of its natural state in the water-conservation areas and the park (Gunderson and others 1995).The construction of canals, levees, and pumping stations has changed the hydrology of the entire system, leaving it vulnerable to a variety of influences. There have been population declines in native species; for example, during the last decade, populations of wading birds averaged less than 10% of their historical highs. Populations of a dozen animal species and 14 plant species have been so reduced that they are now endangered or threatened. Nonnative and nuisance species, such as Melaleuca quinquinervia (a tree introduced from Australia in the early 1990s to help drain the Everglades) and the Brazilian pepper tree (Schinus terebinthifolius), have invaded extensive areas, outcompeting native plants. In the converted agricultural areas, soil subsidence and water-level declines so great that they are measured in feet (Alexander and Cook 1973) have increased the susceptibility of the Everglades to drought and fires. Agriculture has introduced excessive nutrients into the system, and the decreased overland flow of freshwater has resulted in salt-water intrusion into the Everglades National Park and along areas of urban development to the east. If the present ecosystem continues to degrade, ecological sustainability cannot be achieved without fundamental changes (Davis and Ogden 1994).Over the last several decades, state and federal programs have been created to address water-conservation problems in the Everglades. Crises resulting from a failure of existing policies have led to major reconfigurations and new institutions, structures, and policies (Gunderson and others 1995). Even among the agencies and institutions that were concerned primarily with the ecological functioning of the Everglades, there were conflicts over specific management objectives, owing in part to differences in the legal mandates governing the different management agencies. Conflicts were also generated by a lack of critical data needed to evaluate the likely effects of potential manipulations of the hydrological regimes of today's Everglades and by legal and other constraints on the options considered and evaluated by the agencies.The agencies recognized that single-purpose interventions were unlikely to succeed and that restoration activities needed to be evaluated in a system-wide context. There was also common recognition that it was impossible to recreate precisely the original ecological conditions, because the drainage system had been altered in irreversible or very difficult-to-reverse ways. At issue were maintenance of the integrity of the watershed and water quality, preservation of biodiversity in a region of great interest, conservation of endangered species as required by law, and the sustainability of natural resources in a setting of rapid economic and population growth. Two current examples illustrate the complexity of the process.The US Army Corps of Engineers recently completed a reconnaissance report for the C&SF Project (COE 1994). This represented the first phase of the corps's effort to examine ways to modify the C&SF Project to restore the Everglades and Florida Bay ecosystems while providing for other water-related needs of the area. Restoration objectives included increasing the total spatial extent of wetlands, increasing habitat heterogeneity, restoring hydrologic structure and function, restoring water quality, improving availability of water, and reducing flood damage on tribal lands. Recognized constraints included protection of threatened and endangered species, minimizing loss of services provided by the C&SF Project, and minimizing regional and local social and economic disruption. The reconnaissance study was the first step in development of a restoration plan. It set the stage for feasibility studies to develop further the most promising alternatives and recommend a plan for authorization by Congress.The second example is a 4-year US Man and the Biosphere (US MAB) study on ecosystem management for sustainability of southern Florida ecological and associated societal systems (Harwell and others in press). This project places water-management and biodiversity issues into an ecosystem-management framework that presumes that the last century's fragmented and compartmentalized approach to management must evolve to one that explicitly recognizes the mutual interdependence of society and the environment. Such an approach will require integration of theory and knowledge from the natural sciences with analyses of societal and ecological costs and benefits of ecosystem restoration.The US MAB project defined ecological sustainability goals for each component of the landscape with a focus on core areas of maximal ecological goals and buffer areas to support the attainment of those goals, established plausible management scenarios, and examined how the scenarios were related to the desired goals for sustainability of the regional ecological and societal systems (Harwell and Long 1995).Three management scenarios were examined. The report concluded that only one was ecologically sustainable. It involves using portions of the EAA for dynamic water storage while it remains entirely or partly under private ownership; the EAA consists of 280,000 hectares, used primarily for sugar production, with total annual economic activity of about $1.2 billion (Bottcher and Izuno 1994). A National Audubon Society report on the endangered species in the Everglades made a similar recommendation (National Audubon Society 1992). Although this scenario was considered sufficient to achieve the ecological goals for the core areas it was concluded that complete acquisition of the EAA would have too high an economic and social cost (Bottcher and Izuno 1994). However, on the other hand, the sustainability of the sugar industry in the EAA itself is at risk because of extensive soil degradation, possible changes in the subsidies that support sugar prices, political efforts to tax the sugar industry exclusively for funds to restore the Everglades, and economic pressure to acquire EAA lands for residential development. Thus, it was seen that putting part of the EAA in a buffer to support ecological systems might counteract some of the risks to sustainability of the agricultural system.The US MAB report suggested possible uses for the EAA that would allow for sugar production to continue and for the water-management needs to be met, thereby linking the sustainability of the ecological system with the societal sustainability of the local community. The analysis concluded that sugar is probably the most desirable form of agriculture for the EAA, in that its nutrient demands and nutrient exports to the Everglades are considerably lower than those of vegetable crops. Sugar agriculture was seen as much preferable to the alternative of housing developments or urbanization. The study concluded that the environment of southern Florida has more than enough water, except in severe drought years, to support all expected urban, agricultural, and ecological needs but that currently the greatest fraction of the freshwater is lost directly to the sea through the engineered system of drainage canals. The critical issue, then, is not competition for resources, but the storage and wise management of this renewable resource.Risk Management of Ecosystem Diversity and ServicesFrom the standpoint of resource management and policy-making, the link between species diversity and ecosystem services can best be characterized in a risk-management framework. For any given service, a number of changes in the relative abundance of species in an ecosystem could often be made with relatively little impact on the service in question. But addition or removal of particular species could profoundly alter one or more services. Moreover, the presence of a diversity of species—and the genetic diversity in those species—will aid in the persistence of a particular service in the face of changing ecological and climatic conditions. We rarely have sufficient ecological knowledge of a system to allow an accurate assessment of how a change in species diversity is likely to affect one or more services, although we often can identify at least some of the species whose depletion or addition is likely to matter. Management decisions involving potential impacts of changes in species populations on ecosystem services thus typically confront the problem of analyzing and managing risk in the face of scientific uncertainty.No two species are identical, so, in a general sense no species in any ecosystem is "redundant". Nevertheless, for any particular ecosystem service, some species could be added or removed from the ecosystem or be replaced with other, nonnative species with little detectable influence on that service. In such cases, one species functionally compensates for another (Menge and others 1994). A clear example is the service that different plant species provide in slowing soil erosion and thereby maintaining clean water and soil productivity. A natural forest is often extremely effective at minimizing soil loss from an ecosystem. However, knowledge of the plant species in a particular forest ecosystem is necessary before one decides what plant species might be removed without changing the efficiency of erosion control.Although the species in an ecosystem might perform similar functions, there is insufficient knowledge to predict when removing a species from an ecosystem will have an impact. Species in each ecosystem interact—are linked—and removing them might have serious effect; a change that has little effect on one ecosystem service might affect other services profoundly. Species whose low relative abundance would not suggest their large impact on populations of other species in a community are referred to as "keystone" species (Paine 1969; Power and others 1996). The chestnut blight largely eliminated the once-dominant chestnut from eastern deciduous forests (the species is still present, but now grows only in a bushy form), but its loss seems to have had relatively little influence on patterns of water runoff or sedimentation in the region because diverse species of hardwoods growing in similar habitats with similar canopy coverage and similar patterns of evapotranspiration were present in the system. However, if a keystone species were removed or added in this example, it could profoundly affect one or more services. The loss of a keystone species is likely to influence many of the functional processes in an ecosystem, as in the sea otter example earlier in this chapter.Few communities and virtually no regional ecosystems have been studied in sufficient detail to allow an accurate assessment of all the species that are likely to play keystone roles in relation to various ecosystem services. Often, some species can be identified as likely keystone species in the absence of careful study and experimentation, but ecological science can help little in predicting which other species will play such roles. A virus, for example, could play a keystone role in a particular ecosystem. The rinderpest virus has gradually been eliminated from wild cattle near the Serengeti, and their populations have increased spectacularly over the last 20 years, as have predator populations (Dobson 1995; Dobson and Hudson 1986). The dramatic growth in the population of grazers, however, has reduced recruitment of trees in the area. Indeed, the ages of trees growing in several areas of East Africa suggest that recruitment of trees occurs only rarely and might be strongly influenced by the patterns of disease in the ungulate populations (Dobson and Crawley 1994). Box 3-2 presents some changes in species or populations of particular species that have had substantial effects on ecosystem services.Effects of Changes in Species Diversity or Abundance on Ecosystem ServicesFrom: 3, The Values of Biodiversity Perspectives on Biodiversity: Valuing Its Role in an Everchanging World. National Research Council (US) Committee on Noneconomic and Economic Value of Biodiversity. Copyright 1999 by the National Academy of Sciences. All rights reserved. NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.https://www.ncbi.nlm.nih.gov/books/NBK224412/box/bbb00003/?report=objectonlyEffects of Changes in Species Diversity or Abundance on Ecosystem Services. The introduction of exotic species of Myrica faya with nitrogen fixing-symbionts into Hawaii dramatically increased productivity and nitrogen cycling and altered the species composition (more...)A particular species might compensate functionally for another that is removed from an ecosystem, but a simplified ecosystem is less likely to maintain a particular ecosystem service than one with a greater diversity of species playing similar functional roles. A reduction in the diversity of species performing similar functions in an ecosystem reduces the likelihood that the related service can persist in the face of changing ecological or climatic conditions. Reduction in the population of a species due to the introduction of a pest or pathogen is less likely to disrupt a particular service if species that are unaffected by the pest or pathogen play similar functional roles. Similarly, climatic change is less likely to affect a particular service if a diversity of species perform similar functional roles. Each species is likely to be affected differently by a given change in climate, so the risk that all species involved in a particular service will be lost from a system is lessened.Another way that diversity could affect ecosystem services is by increasing their stability. Again, the underlying idea is simple. In the face of year-to-year fluctuations or sustained directional changes in climate or soil fertility or other environmental conditions, productivity and nutrient cycling are more likely to be sustained at high rates if a number of species are present. Some species might be most effective under current conditions; while others might become more important unless conditions change. For example, in an 11-year field experiment based on 207 grassland plots, increased plant species diversity resulted in greater stability in the community and ecosystem process in experimental plots, especially in the face of a severe drought (Tilman 1996; Tilman and Downing 1994). Experimental studies also indicate, for example, that species diversity itself can influence some ecosystem services, particularly in species-poor systems. In their study of artificial tropical communities in which experimental plots contained 0, 1, and 100 species of plants, Ewel and colleagues found that the total number of species had a greater effect than species composition on a variety of biogeochemical processes (Ewel and others 1991). Artificial communities with different combinations of one to four species also differed dramatically in net primary productivity: productivity was higher with more species (Naeem and others 1994).Those results are all consistent with the idea that one of the benefits of diversity is that it increases the likelihood that a species that is highly productive under any particular conditions will be present in the community (Hooper 1998; Hooper and Vitousek 1998). Where highly productive species have been identified in advance and conditions are managed so as to be suitable (as in agricultural monocultures), very high rates of productivity can be attained without much onsite diversity. For example, American farmers produce on average about 7 tons of corn per hectare, but when challenged, as in National Corngrowers' Association competitions, farmers have tripled those yields, producing 21 tons per hectare. Annual yields of biomass up to 550 tons/ha are theoretically possible for algal cultures; yields half as great have been achieved (Waggoner 1994).Social and Cultural ValuesMany people develop a deep aesthetic appreciation for biodiversity and its components. This appreciation has several dimensions, including an appreciation of how biodiversity reveals the complex and intertwined history of life on Earth and a resonance with important personal experiences and familiar or special landscapes. Interest in nature is manifest in many hobby activities, including bird-watching and butterfly-watching; keeping reptiles, tropical fish, and other ''exotic'' species as pets; raising orchids or cacti; participating in native-plant societies; viewing nature photographs and reading nature writing; and watching nature televisions shows. Kiester (1997) has suggested that such experiences provide the basis for a connoisseur's appreciation of biodiversity. By cultivating a connoisseur's perspective, we might develop a better understanding of the aesthetic value of biodiversity just as art critics and scholars help us to appreciate art.InformationBiodiversity holds the potential for applied knowledge through the discovery of how different species have adapted to their varied environments (Wilson 1992). That is, biodiversity holds potential insights for solutions to biological problems, both current and future. We might discover bacteria that inhabit hot springs and have evolved enzymes that function at unusually high temperatures, as in the case of PCR described earlier. We might discover novel predator defense mechanisms of plants and develop previously unimagined alternatives to pesticides for our foods. Or from indigenous peoples we learn about poison-dart frogs; study of the toxins of poison dart frogs is providing insight into fundamental neural mechanisms. Such new insights and tools came not from our imaginations but from observations of other peoples and other species. Even with the dazzling power of modern molecular biology, is it reasonable to expect that we can imagine all the new solutions that can be devised? The diversity of life supplies us not only with new tools and techniques, but also with the inspiration to imagine innovations. "There are more things in Heaven and Earth, Horatio, than are dreamt of in your philosophy" (Shakespeare, Hamlet, act I, scene V).Biodiversity holds the potential for us to understand ourselves better. We have developed profound insights about our own culture and society through the study of other peoples. Likewise, we can learn about our physiology through the study of other species. Many of our insights about ourselves could only have come through the study of other species. For example, our knowledge of our development and reproduction rests on the study of many diverse species beyond the common laboratory species, such as bacteria, nematodes, rats, mice, and monkeys. It had long been presumed that testosterone is necessary for mating behavior in males—except possibly in humans—because it was the case for all animals that had been studied. However, the discovery that this was not the case in the red-sided garter snake showed that the correlation between testosterone and behavior in vertebrates was not, after all, axiomatic (Joy and Crews 1988). The zebra fish has recently proved to be an especially useful model for understanding the molecular genetics of neural development (Brown 1997). Even plants reveal important cues to our physiology. Research on the circadian clock of the mustard plant (Arabidopsis) has led to techniques for studying circadian clocks in animals in more detail and with greater precision than ever before possible (Kay 1996). Considerable advances in understanding of the human nervous system have come from studying nonhuman vertebrates and invertebrates. For example, the nematode Caenorhabditis elegans has provided insights into nervous disorders and diseases, such as Alzheimer's disease.Biodiversity has often served as an early-warning system that has foretold threats to human health before sufficient data had been collected to detect effects directly. Rachel Carson's (1962) Silent Spring, for example, established a strong case against the use of pesticides primarily on the basis of threats to wildlife populations. The same pesticides have since been found to present serious public-health risks. Similarly, declines in populations of the common seal in the Wadden Sea and reproductive failure in the Beluga whale in the St. Lawrence River in Canada might stem from the ingestion of PCB-contaminated fish—if so, caution should be used to ensure the safety of marine food supplies for human consumption (Chivian 1997).Wildlife studies have shown evidence of effects of various chlorinated organic compounds on the immune systems of animals (reviewed in Repetto and Baliga 1995) and on their reproductive physiology (Colborn and others 1993).The evidence is much less conclusive that these compounds have an effect on human physiology, but the accumulation of evidence from wildlife studies points to the need for more-detailed research on possible effects on humans.Much of the study of biodiversity might have no immediate applied value, but it is valuable nonetheless. It is impossible to predict how new knowledge will be used. Knowledge about various forms of life has, as seen in the above examples, had direct effects on improving human health and has led to revolutions in science, such as our understanding of molecular genetics. Few people in Darwin's time would have imagined how his fascination with animal variation would transform the study of biology and so profoundly alter our notions. Bacterial genetics was an obscure field of research in the 1950s, but it led directly to what we now call molecular biology. Even the small cadre of bacterial geneticists could not have known how their research would revolutionize biology and medicine.TransformationBiodiversity can transform our values in the sense that experiences with and knowledge of biodiversity provide opportunities for self-knowledge—knowledge of our own values, attitudes, and beliefs and our place within life as a whole. Although we often regard our natural environment as either a means or a hindrance to such ends as satisfying our physical needs and accumulating material goods, our interactions with our environment also develop our sense of aesthetic pleasure, our curiosity, and our sense of where we fit in the broader scheme of things. A biologically diverse environment offers broad opportunities for developing new ways of appreciating one's place, the scope of one's enjoyments, and oneself (Kellert and Wilson 1993; Norton 1986; Wilson 1984).Sometimes, the contributions of biodiversity are indirect: knowledge expands experience, as evident in a comment made by a recent graduate of an adult literacy program in Washington, DC: "You know, I never even cared about the trees in my neighborhood until I read about how they grow." Children who are exposed to activities and direct experiences with wildlife gain more than knowledge about wildlife. Their attitudes change (Hair and Pomerantz 1987). They become more concerned about wildlife in general; that is, about wildlife in other parts of the world. There is a small but growing literature on how experience with wildlife—and especially with wilderness and outdoor recreation—influences values, beliefs, and attitudes (Finger 1994; Hendee and Pitstick 1993; Kaplan and Talbot 1983; Orams 1996; Rossman and Ulehla 1977; Shearl 1988; Shin 1993).One's conception of self is related to nature in highly symbolic ways. Few Americans wish to live in the kind of society that poisons the Bald Eagle, our symbol of national strength and pride. The grandeur of the symbol is enhanced by the opportunity to watch the Bald Eagle in flight. Conversely, the symbolic power of the eagle would inevitably be diminished if there were no eagles living in the wild.People are motivated by more than the satisfaction of their physical needs; they are moved by the possibility of expanding their horizons—both their own experience and also knowledge "for its own sake". The experience of biodiversity provides such opportunities. The examples cited above suggest that diverse environments contribute to a self-knowledge that, although it can take a multitude of forms and is difficult to catalog, is nonetheless irreducibly valuable in its own right.AestheticsTo superkill a species is to shut down a story of millennia and leave no future possibilities [Holmes Rolston III, quoted in Natural History 1996, p 75].Many people develop a deep aesthetic appreciation for biodiversity and its components. This appreciation has several dimensions, including an appreciation of how biodiversity reveals the complex and intertwined history of life on Earth and a resonance with important personal experiences and familiar or special landscapes.In addition to moral, ethical, and religious values, there also are deeply intellectual reasons for conservation of biodiversity; chapter 4 reviews these in detail. The Copernican revolution was an intellectual breakthrough that changed our view of ourselves. The self-awareness that comes from knowledge of biodiversity is only beginning to be realized. Biodiversity ultimately arises from the fact that there has been one evolutionary history of life on Earth, with vertical (through time) inheritance. It follows that the species present today have unique histories. There are many definitions of organic evolution, but two that are especially relevant in this connection are "descent with modification" (Darwin) and "accumulated history" (Salthe). Species contain the histories of their lineages. It is the concept of lineage that is central to the imagery of evolution, and the vast panoply of life through time has become part of our culture. Equally central is the notion of relationship: some pairs of lineages are more closely related than others, in the sense that they have a more recent common ancestor. There are now well worked-out methods for assessing degree of phylogenetic relationship and for reconstructing the history of life on Earth. These developments have made it possible to express values in new ways.Sense of PlaceLong-branch taxa frequently have played special cultural roles or have been recognized as having intrinsic value (Dworkin 1994). The Ginkgo tree was saved from extinction in Buddhist monasteries because of a concern that is moral and cultural in origin. It now has a "sense of place" value in many parts of the world. Surprisingly, this is a case in which other values also come into play, in that Ginkgo extracts now constitute one of the most widely used medicines in Europe, prescribed by German medical doctors to over 10 million patients annually.Many writers have noted that biodiversity, especially the habitats of native and indigenous species, helps to root not only plants but also people by giving them a sense of place. As noted in chapter 2, it is a characteristic association of species that usually leads us to categorize a place. Indeed, some have suggested that the conservation of landscapes is the best remedy we might have to counter the transience, or rootlessness, that has become one of the most salient characteristics of American society. For example, Wallace Stegner (1962) wrote about American rootlessness and restlessness especially in the American West. He understood the lure of freedom in the absence of obligation. But that rootlessness, Stegner wrote, has often been a curse.Our migratoriness has hindered us from becoming a people of communities and traditions, especially in the West. It has robbed us of the gods who make places holy. It has cut off individuals and families and communities from memory and the continuum of time.Gary Snyder (1996) and Carolyn Merchant (1992) have suggested that our ethics and by implication the value we place on biodiversity, must be grounded in an understanding of local habitats and the functioning of ecosystems. This work, especially Leopold's notion of a "land ethic" has inspired work in both environmental philosophy and social psychology; the latter has indicated that concern with the intrinsic value of biodiversity is widespread in the United States (Karp 1996; Stern and others 1993, 1998).A sense of place is founded on relationships—for example, with nature, with the past, with future generations, and with those with whom one shares responsibility for maintaining the essential character of one's surroundings (Gussow 1972). To belong to or in a landscape, one must feel connected to its past, both natural and human. One is then aware of the moral obligation to cultivate the landscape in ways that maintain its identifying characteristics so that future generations can recognize it as one does now. The work of protecting native flora and fauna establishes a continuity with the future through a consistency with the past. Thus, we maintain a connection with a landscape through time (Cronon 1991; Worster 1985).The effort that we make to protect the habitats of native species entrenches a relationship between people and places. One sees one's own activities and those of one's community as rooted in a particular place; one's experiences, in other words, depend on where one is (Gallagher 1993; Light and Smith 1998).The protection of biodiversity is often the catalyst that turns generic locations into distinct places. The difference is that a place is a location that we have filled with meaning and thus have claimed with our feelings. History, natural or human, insofar as we claim it as our own, must be imbedded in places that we cherish in shared memory and whose symbols we maintain and respect. Native and indigenous species are living parts of our community history (Baily 1915). (See the case study below on Boulder, Colo., open space.)Space is the symbol of freedom in the western world; it is a frontier to conquer; it is the potential, not the actual. It is an ever-receding horizon. Place, in contrast, involves commitment and responsibility, actuality rather than potential. It is not the realm of conquest, but the sphere of concern and conservation. The reintroduction and protection of native species, in contrast, follows Virgil's counsel:It is well to be informed about the winds,About the variations of the sky,The native traits and habits of the place,What each locale permits and what denies.Much of what many people deplore about the human subversion of nature—and fear about the destruction of the environment—has to do with the loss of places that they keep in shared memory and cherish with collective loyalty. Many fears stem from the loss of the particular—the specific characteristics of places that make them ours—and so from the loss of the security one has when one is able to rely on the lore and the love of places and communities that one knows well.The beauty and majesty of nature have always affected human beings: we take pleasure in perceiving nature's beauty, and we feel wonder and awe at its enormous scale (the starry skies) and its dynamic power (a hurricane). The aesthetic categories of the beautiful and the sublime, which became prominent in the writings of 18th-century philosophers, apply to our understanding of the value of biodiversity today. Plants and animals in their intricate and functional design are beautiful; we perceive that beauty with pleasure. We garden; we cut flowers for our homes; we keep birds, fish, and many other animals in our homes; we frequent zoos; and so on. Ecotourism is based largely on people's enjoyment of natural beauty. Artists celebrate that beauty in paintings and sculptures drawn from nature. Indeed, nature is the primary object of representation in art and a constant theme of poetry.The record of evolution stretches the limits of our understanding and imagination. Those who study this record—paleontologists, zoologists, ecologists, botanists, and many others—discover in every kind of plant and animal a story worth telling, a complex tale of adaptation that exemplifies evolutionary processes. About 99% of the species that have ever existed on Earth are now extinct, and the ones that exist today are the latest descendants and deeply reward study for the historical record that they contain. No less than the artifacts of great civilizations gone by, rare species descended from organisms that lived eons ago possess a historical value and authenticity that demand attention and appreciation. When we take pleasure in the qualities of these organisms—when we enjoy simply knowing and perceiving them with no further use or application in mind—we are engaged in the experience of the aesthetic.Case Study: Boulder, Colo., Open SpaceThe city of Boulder, Colo., lies at the intersection of the eastern face of the Rocky Mountains and the western edge of the Great Plains in an area of high diversity of mountain and prairie species. The citizens of Boulder, an affluent educated community, have long valued and protected its natural setting, most recently by establishing the so-called blue line, a contour at the city's western edge above which no development is to be extended, and by approving an increase in the city sales tax of 0.4% to buy and protect land adjacent to the city as open space. Boulder now has the highest per capita acreage of municipally owned natural area of cities in the United States.The purposes of open space, as codified in a charter amendment approved by voters in 1986, are preserving and restoring natural areas and their biota, preserving land for passive recreational use, retaining traditional agricultural land uses, limiting urban sprawl, and preserving aesthetic values (City of Boulder Open Space Department 1995). Loss of natural areas to urban sprawl is proceeding rapidly throughout most of the region around Boulder, and there have been attempts to curtail the open-space program, initiated primarily by the real-estate, development, and general business communities in the Boulder Valley. However, care has been taken to get city council and general public support and involvement during all phases of land purchase and policy implementation.Public-opinion polls conducted in 1994 and 1995 indicate that although conservation of biodiversity is a factor in public support for open space, the primary purpose in the minds of most people is to keep urban and suburban sprawl at bay (Miller 1994; Miller and Caldwell 1995). It is clear that, to the great majority of Boulder's population, the value of open space as natural viewscape exceeds the value of the same land for possible commercial and residential development.In recent years, the Open Space Department has begun shifting its emphasis from the purchase of new land to the development of management plans that will ensure its ecological integrity into the future. Of particular concern is the increasing use of open space for outdoor recreation (Zaslowsky 1995). Two issues illustrate the growing conflicts between the value of Boulder open space as a biodiversity reserve and its value as a template for outdoor recreation. The first involves closing a trail to protect the high biodiversity of habitats and replacing it with a nearby trail. The second involves an attempt to implement leash laws in some areas where dog owners traditionally had been permitted to walk their pets off-leash. In both cases, the managers in the Open Space Department recommended restricting, but not prohibiting, recreation uses. Neither the users nor those who favored protection were satisfied.Those examples suggest three general lessons about the challenges that managers of suburban open spaces can expect to face. First, it is more difficult to impose restrictions on the use of open space after its establishment than at the time of its establishment. Second, hard data on the consequences of recreation on the biodiversity of open space will be helpful in resolving conflicts. Third, the ecological integrity of suburban open spaces will persist only if citizen users can be educated as to the consequences of their collective impacts. It is a daunting educational challenge. Public participation has long been an integral part of the planning process regarding Boulder open space. The relative success of the program is attributable largely to deliberate efforts to integrate public opinion and participation into the decision-making process.Ethics and ReligionVery often, people value biodiversity for ethical and religious reasons. These reasons are often part of a comprehensive ethical or cosmological world view that, on the one hand, is anchored in a self-conception or identity and, on the other hand, is supported by an interpretative tradition and the communities that share it. Such values—and the worldly points of reference that support them—are held not in the form of needs or preferences, but rather as judgments that attach to identity. One does not "choose" these values; they are the deeply held values that form our identity.SummaryIn this chapter, we have discussed how the many dimensions of biodiversity and its components contribute to decisions on management of biodiversity. The goods and services, present and potential, that humans derive directly or indirectly from biodiversity can be viewed from different social and cultural perspectives. The case study examples of the Everglades and Boulder illustrate why a broadened understanding is necessary for management considerations. In the next chapter, we see that information on the many philosophical and systematic approaches to valuing biodiversity can favor particular outcomes in management decisions. 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