Chemical Weathering of Bone in Archaeological Soils

Society for American Archaeology

Chemical Weathering of Bone in Archaeological SoilsAuthor(s): E. M. White and L. A. HannusSource: American Antiquity, Vol. 48, No. 2 (Apr., 1983), pp. 316-322Published by: Society for American ArchaeologyStable URL: http://www.jstor.org/stable/280453 .

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CHEMICAL WEATHERING OF BONE IN ARCHAEOLOGICAL SOILS

E. M. White and L. A. Hannus

Weathering of hydroxyapatite, Ca5(P043 (OH), in bone probably is initiated by organic and carbonic acids formed by the microbial decomposition of collagen. This weathering, independent of soil properties, is caused by protons replacing Ca from hydroxyapatite. As collagen is depleted, proton production decreases and weathering may either continue if protons are available from the soil or be arrested if Ca from the soil displaces the protons previously added to the hydroxyapatite. The theoretical Ca/P weight ratio of unweathered bones is 2.15. Weathered bones that have been stabilized by Ca may have this ratio or a higher one if extra Ca has been added. A group of weathered bones from one site with a slightly acid soil had an average ratio of 1.67, which probably promotes further weathering, while bone at the same site with an average ratio of 4.09 was less weathered and apparently stabilized.

Physical properties of bones change in recognizable stages as bones weather (Behrensmeyer 1978). These changes in the physical properties are contemporaneous with chemical changes which occur in the organic and inorganic bone constituents. In an aerobic weathering environ- ment suitable for microorganisms, the organic collagen could be expected to weather more rapidly than the inorganic hydroxyapatite [Ca5 (PO4)3 OH] which has a low solubility in aqueous systems that are alkaline to slightly acid. Individual elongated hydroxyapatite crystals are enclosed in a network of collagen so that the loss of the collagen weakens the rigidity of the bone. The rigidity is greatest in the dense outer part of the bone where the hydroxyapatite crystals are

tightly packed and weathering is slowest. Inorganic weathering of bone is mainly the weathering of hydroxyapatite.

Ca and P04 ions in a soil solution are in equilibrium with those ions in the surface of hydroxyapatite. Hydroxyapatite loses or gains Ca and/or P04 ions, respectively, if the solution contains fewer or more of these ions than can be in equilibrium with the mineral. If the solution Ca ion concentration is large, fewer PO4 ions can be in the solution, and the reverse is true if the PO4 ion concentration is large. Thus, the ratio of the two ions in the solution affects the hydroxyapatite solubility as well as the actual amount of one of the ions. Hydrogen ions (protons) from acids can

replace Ca from hydroxyapatite so that Ca can be leached from bone by soil solutions. This

leaching would create a hydrogen-rich, Ca-poor hydroxyapatite, particularly in the surfaces of the mineral. However, if the solution becomes less acid, Ca could replace protons in the hydroxyapatite and the original mineral would be reconstituted. In more acidic soils, hydroxyapatite weathering may be increased because PO4 ions are precipitated as Fe and Al phosphates- strengite and variscite, respectively (Lindsay 1979:180). This removes P04 ions from the solution and increases the dissolution of the hydroxyapatite. Soils in the Great Plains have mainly Ca as the cation in the solution phase so that hydroxyapatite weathering is determined by the mass action chemistry of Ca and PO4 ions. The objective of this study is to propose mechanisms for the chemical decomposition or preservation of bone in archaeological soils.

E. M. White, Plant Science Department (Soils), South Dakota State University, Brookings, SD 57006 L. A. Hannus, Sociology Department (Archaeology), South Dakota State University, Brookings, SD 57006

Copyright ? 1983 by the Society for American Archaeology 0002-7316/83/020316-07$1.20/1

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METHODS AND SAMPLE SITES

Bone fragments were collected from excavations at archaeological sites at Oakwood Lake (39BK7), Belle Fourche (39BU2) and near the Lange-Ferguson site (39SH33) from a hearth former- ly buried in calcareous alluvium. All bone fragments are from large mammals, presumably bison, which was the dominant species at all sites. In addition, modern samples were collected from the remains of cows that had drowned two years earlier near the Lange-Ferguson site.

The Oakwood Lake site (E 1/2 SE 1/4 NE 1/4 sec 7, T111N, R51W, Brookings County, South Dakota) is a three-sided knoll bordered by lakes on the west and north and a swamp to the southeast. The knoll is a kame in Late Wisconsin (Cary?) dead ice moraine that was deposited in a preglacial valley. The area is nearly isolated by water except for the swamp and a narrow tombolo-like disintegration ridge (Flint 1971) that extends to an island which in turn is connected to the shore by a second disintegration ridge. Because of isolation from fire and the proximity to groundwater, the area supported forest during the first part of the Holocene and a forest soil (White et al. 1969) developed. Forest soils characteristically have a thin, dark-colored Al horizon underlain by a light-colored platy A2 horizon and a B horizon with prismatic structure that is bet- ter developed than that which occurs in prairie soils of an equivalent age. The forest soil was the surface at the beginning of the first habitation; abitation; about A.D. 300 to 600 during the Middle Woodland period. During and after this habitation, approximately a meter of calcareous eolian sediment was blown from the adjacent lake beach and bank. The eolian sediment contains the cultural horizon and the bones. The lake level, higher during the first part of the Holocene, decreased when the outlet stream eroded a deeper channel. Mixed prairie, probably with trees along the beach, was dominant during the second habitation by horticultural people after A.D. 1000. More recently, forest has expanded into prairie, possibly because the precipitation (518 mm [20.4 inches]) is greater.

The Belle Fourche site (NW 1/4 SE 1/4 sec 5, T8N, R2E, Butte County, South Dakota) is on a Pleistocene-age terrace, about 9 m above the Belle Fourche River. Graneros shale, which underlies the terrace alluvium, is a limb of the Black Hills dome which has been truncated by erosion. The Dakota (Lakota) sandstone hogback lies to the south of the site which is in the transition zone between the semiarid plains to the north and the more more humid, forested Black Hills to the south. Annual precipitation varies and is and is commonly reported to be 380 mm (15 inches), but the 1900-1970 average is about 444 mm (17.5 inches). A few ponderosa pine grow along the escarp- ment at the edge of the floodplain and in favorable slopes in the adjacent upland. Because the soil morphology formed under forest (White et al. 1969), the area must have been dominantly forest when it was inhabited about 1,000 years ago, although it is prairie today. The cultural horizon from which the bone samples were taken is in a 10-15-cm thick eolian-silt layer which was de- rived from either the adjacent floodplain when vegetation was sparse or from point bars along the channel. The stream is perennial today and, presumably, it would have had a larger discharge when forests were more extensive and the climate more humid.

The hearth near the Lange-Ferguson site (NW 1/4 SW 1/4 SW 1/4 sec 22, T39N, R45W, Shan- non County, South Dakota) was recently exposed by erosion of a cliff, 3-4 m high, formed in unweathered calcareous alluvium eroded from an adjacent "badland wall" of Tertiary siltstone. Badland basins, which formed by erosion of Tertiary-age White River beds, had only a thin discontinuous alluvial mantle in the last part of the Pleistocene, some 10,000 years ago. At that time, boreal vegetation protected steep slopes from erosion so that soils could form. The weakly developed soils were eroded and the sediment was deposited in the valleys when prairie became dominant. This alluviation continued during the Hypsithermal and has been replaced more recently by rapid erosion with intermittent filling. The hearth and bones probably were buried by calcareous alluvium that filled a dissected area 1,000 to 3,000 years ago. Intermittent streams in the area flow only during rainstorms or when snow melts; they can change rapidly from aggrada- tion to degradation. The annual precipitation is about 381 mm (15 inches) and prairie is dominant with a few trees along streams or in favorable upland positions. Because of the low precipitation, slow leaching, and the short length of time for soil formation, soils formed on the alluvial fill have

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very thin dark-colored surfaces, which usually are calcareous. The alluvium probably was deposited near the end of the Hypsithermal, but the hearth has not been dated. Soil samples were collected at the sites for pH determination with a glass-electrode pH meter.

Bone from Oakwood Lake was examined under the microscope and classified by a relative, visual comparison according to the nature of the fragment (cancellous tissue, dense compact outer part, or both), weathering (on a scale increasing from 1 through 8), porosity (1 increasing through 4), and charcoal amount in surface (0, few, or many black flakes). The bone was ground in a micromill, 0.5 g digested in nitric and perchloric acid, and total Ca and P determined, respectively, by flame photometry (Jackson 1958) and the colorimetric, molybdate blue, ascorbic acid procedure (Watanabe and Olsen 1965). Organic matter in the bone was estimated with the titrimetric Walkley-Black technique (Jackson 1958) that oxidizes organic matter in a chromic- sulfuric acid system. The presence of carbonates in the bones was estimated visually by effervescence (Soil Survey Staff 1951:140, 238) as observed with a binocular microscope. Through a microscope, effervescence from small carbonate fragments can be observed and separated from bubbling caused by air displacement from the bone. Bones from Belle Fourche were classified as to the bone part, porosity, and superficial charcoal amount. Bone from the Belle Fourche and Lange-Ferguson areas were analyzed for Ca, P. and organic matter contents.

RESULTS AND DISCUSSION

Oakwood Lake Site (39BK7)

Bone hydroxyapatite contains about 18.5% P and 39.9% Ca. If bone is 70% mineral (Matthews et al. 1973:188), unweathered bone should contain 12.95% P and 27.9% Ca. Thus, the theoretical Ca/P ratio should be 2.15; however, the ratio ranged from 0.97 to 6.89 for the bone at the Oakwood Lake site (Table 1). Ratios larger than 2.16 were found only with bone that had a weathering scale value of 3 or less (Table 1) except for sample 17. The mean Ca/P ratio was 4.09 for samples 2 through 8 and 1.67 for the other samples. Bone in samples 2 through 8 apparently had been enriched in Ca while the other samples, except for 17, have been impoverished of Ca. The enriched samples may have been located in the soil zone of CaCO3 accumulation or below a limestone peb- ble where CaCO3 could precipitate. Limestone pebbles in the soil frequently have secondary CaCO3 pendants on the lower side even though the matrix soil is slightly acid. Conversion of

hydroxyapatite to dahllite [Ca10 (PO4) CO03], the apatite common in fossil bone, would not change the ratio significantly. Addition of CaCO3 would increase the ratio. Effervescence with HCl was largest from samples ground to a small size, even from the relatively unweathered cow bones. This effervescence was not caused by the evolution of CO2 during the conversion of CaCO3 to the CaC12 but was caused by the displacement of air from the small Haversian canals that permeate bone. Effervescence from discrete masses of carbonates was not observed, and it is unlikely that the effervescence was from thin coatings of carbonates in the Haversian canals. In nature, very small carbonate crystals are unstable and tend to dissolve (Krauskopf 1967) particularly where the bicarbonate ion concentration is greater than in other parts of the system. The higher bicarbonate concentration would arise from the CO2 released from collagen decomposition. Car- bonate, as a substituent for PO4 ions in the structure, increases apatite solubility because of "its weakening effect on the bonds in the structure" (Le Geros et al. 1967). If CO3 ions did substitute for PO4 ions in the structure, the Ca/P ratio would be larger than 2.15. Therefore, samples with a mean Ca/P ratio of 1.63 must have had Ca replaced by protons. Posner (1960) reported that low Ca

hydroxyapatite occurs in bone, and the Ca/P weight ratio may be as low as 1.82 instead of the theoretical 2.15 ratio. The low Ca hydroxyapatite will adsorb bases and release protons if Ca or another suitable cation is added.

The different bone porosity groups did not have significantly different Ca/P ratios by analysis of variance. Thus, weathering was not directly related to pore size. Logically, weathering should increase as the pore size increases so that solutions could flow through the bone. Groupings accord-

ing to the amount of superficial charcoal observed also did not have a significant effect on the

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Table 1. Percent Organic Matter, Ca, and P in Bone Collected Randomly from the Oakwood Lake Archaeologic Site (39BK7) and Bone Weathering, Porosity and Charcoal Residue.

Sample Bone Bone Characteristicsb P Ca Organic Ca/P Number Parta Weathering Porosity Charcoal Percent Matter Ratio

1 OM 1 2 F 16.0 25.5 8.09 1.59 2 M 1 2 M 8.3 26.5 8.08 3.19 3 M 1 1 0 8.8 26.5 8.00 3.01 4 O 2 2 F 3.7 25.5 _c 6.89 5 0 2 2 F 4.1 22.0 7.61 5.37 6 0 2 2 M 4.4 22.0 - 5.00 7 OM 3 2 F 10.1 24.0 8.04 2.38 8 0 3 2 F 8.1 23.0 8.51 2.84 9 0 3 2 F 15.0 14.6 - .97

10 OM 4 3 F 15.0 24.9 - 1.66 11 0 4 2 F 12.5 27.0 8.75 2.16 12 OM 4 2 F 15.3 27.0 8.30 1.76 13 0 5 3 F 12.0 21.0 8.14 1.75 14 0 5 2 F 15.6 27.0 - 1.73 15 0 5 3 M 12.7 23.0 - 1.81 16 0 6 3 M 14.8 26.5 8.87 1.79 17 M 6 2 0 11.4 26.5 - 2.32 18 OM 6 3 F 15.0 23.0 8.36 1.53 19 M 7 3 F 15.0 23.0 8.27 1.53 20 0 7 2 F 15.6 31.6 - 2.02 21 0 7 4 0 15.1 22.4 - 1.48 22 M 8 3 0 13.6 21.0 8.83 1.54 23 OM 8 3 F 15.0 21.0 8.79 1.41 24 OM 8 2 F 15.3 21.0 8.05 1.37

Means 12.2 24.0 8.31 2.37

a OM equals outer part of bone and cancellous tissue, 0 = outer part, M = cancellous tissue. b Weathering: 1 = slight to 8 = very weathered; Porosity: 1 = none, 2 = powder-size, 3 = salt-size, 4 =

granular; Charcoal: 0 = none, F = few flakes, M = many flakes in bone surface. c Insufficient sample to determine organic matter.

Ca/P ratio. Thus, either contact with fire did not accelerate weathering or charcoal presence on the bone's surface did not indicate a fire treatment.

The pH of the eolian mantle at the Oakwood Lake site ranges from about 6 to 7.5. Hydroxy- apatite is relatively insoluble at the higher pH, but the solubility increases as the pH decreases to 6.5 or 6, and the solubility increases rapidly below a pH of 6 (Lindsay 1979: 181-182). Leaching of Ca has occurred because limestone pebbles in the noncalcareous eolian mantle are pitted. Limestone weathering must have occurred when the soil solution was undersaturated with Ca, and these same solutions may have weathered the bone. Soil beneath the mantle was developed under forest and has a pH of 5.6 to 5.7. This pH may originally have been lower but was increased by the deposition of Ca leached from the overlying eolian mantle. Calcium carbonates must be ac- cumulating in the subsoil today because hackberry seeds had been calcified in the lower part of the mantle at one location although the matrix soil is not strongly calcareous. Thus, the pH of both the buried soil and the anthropic zone probably was more acid when most of the bone was first buried. Most of the weathering may have occurred before the upper layers of the calcareous eolian sediment were deposited.

If the Ca or P percentages of the 16 more highly weathered bone samples (samples 9 through 24) are divided by the theoretical Ca or P amounts, the relative removal of Ca and P can be estimated. The value for Ca is lower (0.85) than the value of P (1.11). If the estimated organic matter content (Table 1) is considered in the calculation, the ratios are 0.95 and 1.23 for Ca and P, respectively. Ca apparently has been preferentially leached.

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Belle Fourche Site (39BU2)

The mean percentages of Ca and P (Table 2) are similar to those found for the Oakwood Lake site. The mean Ca/P ratio is 1.77 and only two values (2.39 and 2.18) exceed the 2.15 theoretical ratio for hydroxyapatite. The bone is in a thin eolian mantle, 10 to 15 cm thick, that is underlain by a forested soil. The flux of Ca cycled through the eolian mantle with the bone probably has been less than that at the Oakwood Lake site where a thicker calcareous eolian mantle has accumu- lated. The bone is in the superficial layer where biological activity, organic acid production, and leaching from small rainstorms are greater than in the lower soil layers. In the subsoil, Ca leached from the upper layers is deposited to form secondary CaCO3 which may cause Ca enrich- ment of the bone. Weathering of bone is more active near the surface of the soil at the Belle Fourche site than for the bone buried to a greater depth at the Oakwood Lake site. The initial habitation at Belle Fourche probably was more recent than 1,000 years B.P. in comparison to shortly before 1750 + 50 years B.P. for the Oakwood Lake site. Thus, weathering at the two sites is difficult to compare because of the time factor and because the climate is drier and leaching less rapid at Belle Fourche. The Ca/P ratio was not correlated with the part of the bone, porosity, or charcoal scale groupings.

Lange-Ferguson (39SH33) Area

Samples of relatively unweathered cow bones and, presumably, buffalo bones from hearths that were buried beneath sediment, have a Ca/P ratio of 2.16 and 2.18 (Table 3). They probably contain unweathered hydroxyapatite. However, the prehistoric bones were in a deteriorated state even though the Ca/P ratio of 2.18 would indicate Ca has not been preferentially leached. Weathering apparently had occurred, and the Ca/P ratio decreased and increased, respectively, first as Ca was leached from the bone and second as it was added to the bone by soil water moving through the enclosing calcareous sediment and bone.

The P content of the unweathered cow bones is much lower than the amount one could expect if

"Living bone consists of about 65-70% mineral" (Matthews et al. 1973) and if the mineral part was mainly hydroxyapatite (Posner 1960). Hydroxyapatite contains about 18.5% P. Thus, the P

Table 2. Percent Organic Matter, Ca, and P in Bone Collected at the Belle Fourche Archaeological Site (39BU2) and Bone Porosity and Charcoal Residue.u

Sample Bone Bone Characteristicb P Ca Organic Ca/P Number Parta Porosity Charcoal Percent Matter Ratio

1 0 1 F 12.4 22.5 10.0 1.81 2 0 2 F 11.0 22.5 - 2.04 3 0 1 0 14.5 22.5 - 1.55 4 0 2 F 14.0 17.5 - 1.25 5 0 2 F 9.6 23.0 10.1 2.39 6 0 1 0 13.7 23.0 11.1 1.68 7 OM 2 F 14.6 23.0 10.4 1.57 8 OM 1 F 13.9 24.5 10.1 1.76 9 0 2 F 16.2 24.5 - 1.51

10 0 1 F 14.9 20.5 10.5 1.38 11 M 2 0 11.7 25.5 - 2.18 12 M 2 F 16.2 31.9 - 1.97 13 M 2 0 15.4 26.1 - 1.69 14 M 2 0 11.5 23.7 - 2.06 15 0 2 F 14.7 24.5 10.1 1.66 16 0 2 F 13.1 24.0 10.3 1.83

Means 13.6 23.7 10.3 1.77

d See Table 1 for footnote legend.

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Table 3. Percent Organic Matter, Ca, and P in Cow Bone and in Bone Collected from Buried Hearths

in the Badlands near Archaeological Site (39SH33).

Sample P Ca Organic Ca/P Number Percent Matter Ratio

Cow bones

(unweathered) 1 12.4 12.0 22.3 0.97 2 9.9 20.5 22.2 2.07 3 5.7 20.5 22.5 3.59 4 8.8 19.0 22.9 2.16 5 11.0 22.0 22.8 2.00

Means 9.56 18.8 22.5 2.16

Bones from hearths 1 8.1 24.5 20.7 3.02 2 11.6 24.5 20.1 2.11 3 11.7 24.5 20.6 2.09 4 11.5 24.5 20.7 2.13 5 11.0 24.5 20.6 2.22 6 13.6 24.5 - 1.80 7 5.6 12.0 - 2.14 8 12.0 23.0 - 1.92

Means 10.64 22.75 20.5 2.18

content of bone that contains 30 to 35% organic material should be 12 to 14%. In comparison, Sauchelli (1965) reported the P contents are 9.4% for raw bone meal, 14.4% for steamed bone meal, 15.2% for spent bone char, and 17.7% for bone ash. The 9.4% value is similar to the 9.6% P content of the cow bone, and the contents after steaming, charring, and ashing are similar to the values found for bone collected at the Oakwood Lake site and probably result from the loss of collagen. The 17.7% P for bone ash is about 96% of the 18.5% P content of hydroxyapatite. Obvious- ly, some inorganic impurities would occur in bone.

PROPOSED CHEMICAL WEATHERING SEQUENCE FOR BONE ENCLOSED IN ARCHAEOLOGICAL SOILS

Chemical weathering of bone in South Dakota soils probably is initiated by acids created as microorganisms decompose collagen. Protons from organic and carbonic acids replace some Ca in the hydroxyapatite structure of bone without destroying it. Because of the loss of organic material (Tables 1, 2, and 3) and Ca, the average P percentage in bone increased from 9.6% in unweathered cow bone to 10.6% for the Badlands sites to 12.2% for the Oakwood Lake site and to 13.6% for the Belle Fourche site. Hydroxyapatite weathering apparently can occur inside bone buried in calcareous sediment because it is not in complete equilibrium with the soil. After collagen decomposition and CO2 production decrease, the CO2 partial pressure inside the bone would decrease so that the solution bicarbonate and Ca activities also would decrease. This would reduce the gradient for Ca diffusion out into the soil. Ca in calcareous soils then could dif- fuse back into the bone and replace protons from hydroxyapatite to stabilize the partially weathered bone. An excess of Ca may be added during this stage.

Bone weathering can be described as overlapping reactions that are controlled by water, acid, oxygen, and Ca contents in the bone and soil.

1. Bone collagen is decomposed by microorganisms when water and oxygen are present to form C02, HCO3 ions, and H ions, which in turn react with

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2. Ca5(P04)30H to form (Ca5_xH2x) (P04)3(OH) and Ca ions, which can then react further either as

3. C02, HC03 ions, and H ions continue to react with the hydrogen-enriched hydroxyapatite to decompose it to Ca and HP04 ions, or

4. Ca ions from the soil solution replace protons from the hydrogen-enriched hydroxyapatite to stop or retard the dissolution of the bone.

The first two reactions could occur inside the bone and are dependent on collagen decomposition and independent of pH and ions in the soil solution, but the third reaction would predominate in acid soils and the fourth in calcareous soils and be dependent on soil properties.

Acknowledgments. Contribution from the South Dakota Agricultural Experiment Station, Journal Paper Number 1772.

REFERENCES CITED

Behrensmeyer, A. K. 1978 Taphonomic and Ecologic Information from Bone Weathering. Paleobiology 4:150-162.

Flint, R. F. 1971 Glacial and Quaternary Geology. Wiley, New York.

Jackson, M. L. 1958 Soil Chemical Analysis. Prentice-Hall, Englewood Cliffs, N.J.

Krauskopf, K. B. 1967 Introduction to Geochemistry. McGraw-Hill, New York.

Le Geros, R. Z., 0. R. Trantz, J. P. Le Geros, and E. Klein 1967 Apatite Crystallites: Effects of Carbonate on Morphology. Science 155:1409-1411.

Lindsay, W. L. 1979 Chemical Equilibria in Soils. Wiley, New York.

Matthews, J. L., J. H. Martin, J. W. Kennedy, III, and E. J. Collins 1973 An Ultrastructural Study of Calcium and Phosphate Deposition and Exchange in Tissues. In Hard

Tissues, Growth, Repair, and Remineralization. Ciba Foundation Symposium 11(n.s.):187-211. Elsevier, New York.

Posner, A. S. 1960 The nature of the Inorganic Phase in Calcified Tissue. In Calcification in Biological Systems, edited

by R. F. Sognnaes, pp. 373-394. American Association for the Advancement of Science Publication 64. Washington, D.C.

Sauchelli, V. 1965 Phosphate in Agriculture. Reinhold, New York.

Soil Survey Staff 1951 Soil Survey Manual. U.S. Department of Agriculture Handbook 18. Washington, D.C.

Watanabe, F. S., and S. R. Olsen 1965 Test of an Ascorbic Acid Method for Determining Phosphorus in Water and NaHCO3 Extracts from

Soil. Proceedings of the Soil Science Society of America 29:677-678. White, E. M., J. R. Johnson, and J. T. Nichols

1969 Prairie-forest Transition Soils of the South Dakota Black Hills. Proceedings of the Soil Science So- ciety of America 33:932-936.

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Chemical Weathering of Bone in Archaeological Soils