mOTC productive, an indication that P is typically the most limiting nutrient in fresh water. The simple an swer to the question, 'Why are oligotrophic surface.
•
V~rh. Intemat. Verein. Limnol.
29
St,,~gart.
J 877- 1886
October 2006
Aluminum, phosphorus, and oligotrophy assembling the pieces of the puzzle s. Norton, l. Fernandez, A. Amirbarunan, K. Introduction Pho sphoru s (P) is probably the most-studied elem ent in surface waters, largely because of the eutrophica tion of surface waters caused by agriculture, industri
alization and biosoli ds di sposa l. Oligotrophic waters 19 19) arc characterized by low primary
(NAUMAl\,'N
productivity by {he phytoplankton. Nearly a bundred
years of study clearl y in dicates that surface waters that become enriched in P ( i.e. eutrophy) become mOTC productive, an indication that P is typically the most limiting nutrient in fresh water. The simple an swer to the question, 'Why are oligotrophic surface waters oligotrophi c?' is that the concen tration of di s solved P (commonly referred to as soluble reactive p hosphorus, SRP) is low on a sustained basis. That answer raises the question, 'Why is P concentra tion low in o ligotrophjc waters?' The answer to this ques tion is less clear. Further. th ~ question ' Is acidifica rion linked with oligotrophic status o r does acidifica li on exacerhate o ligotrophy?' is largely uucxplored. The literature documents various aspects of the biogeochemistry and hi oavai lahility of P at points alon g hydrologic flow path s, including precipjtation
Coolidge and 1. Navratil
is nea rly unmentioned and unstudied in a systematic way with respect to acidificati on. As recently as 1994, SCHJN DLER (1994) suggested th at there was lit tic understanding about the effect of ccosystem ac id ifica tio n on P concentrations in surface water. Since th en, substantial progress has been made. Here we at tem pt to compile the separate studies of the Al-P sto ry into a continuum. Key words: acidification, aluminum , lakes . olig otrophication, oligotrophy, ph osphorus, sediment, so il, streams
The model
Above gro und The concentration of dissolved P varies sub stantially along flow paths (Fig. I). Phosphorus in precipitation likely varies spatially, depend ent on soil dust and other aerosols (POLLMAN et a!. 2002). Phosphorus in lhroughfall varies sea sonally, by vegctalion type and leaf-status, and spatially (NEAL et a!. 2003). It is typically (POLLMAN et al. 2002), throughJaJI (NEAL et al. greater than in precipitation because of canopy 2003), soil horizon s (FERNA NDEZ & STRLUnEMEY ER leaching. (985), soil solutions and solid phases (WOOD et al. (984), shallow g roundwater, strea ms and lakes (hun
dreds of papers), and estuaries. Few studies hav e as sessed the biogeoch emi stry along thc continuum. Some of the studies were in the contcxt of ecosystem responsc to acidic depositio n, eommonly in olig otrophic systems. NORTON ( 1976) suggested that aCid ification of soils (and thus surface waters) because of acidic dep osition would re su lt in th e mobilization of aluminum (AI), a tOXIn for fi sh (reviewed in Haines (986). Since then, acidificati on of soil s and surface waters in oligotroph ic low AN C ecosystems, in particular the mobilizat ion of AI frorn soi ls, ha s been th e focus of ac idic deposition rt s(..'arc h (e.g., CRONA.N & SCHOFI ELD 1979, DRJSCOLL et a1. 1980, WIGINGTON et .1. 1990, BAKER et . 1. 1990, TIPPING ct al. 1991 and hundreds more). The biol ogically lirnili.ng nutrient P
Soils Podzolization (i.e. Spodosol formation) in volves the eluvia tion of AI and iron (Fe) from the upper horizons of mineral soil profiles (the E or A horizons) and illuviation of these metals into the B horizon. The accumulation of AI and Fe in the B horizon as amorphous coatings (AI(OH)3 and Fe(OHl3) on less-weathered pri mary mineral particles is well understood (WOOD et a!. 1984). AI also forms a large frac tion of the exchangeable cations in soils with low base saturation (FERNANDEZ 1992). The ability of freshly precipitated Al(OHh to ad sorb PO. may exceed that of Fe(OH)3 (LUKLE MA 1980). Both of these hydroxides have high 0368-0770/06/0029-1877 $ 2.50 C2006 E Schwe12erbart·sche
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Verlz. Internar. Vere in. Lim nol. 29
Low/High Flow Concentration
water typi cally bas intermediate in silLi pH (6 to 7) because of cbemical wea thering (release of
1- 2 Ilg/ l
Precipitation
2-10 Throughfall
, I
~
IForest Canopy I
Soil So lu tion "(--
Mineral Soil
2-50
!....-
2-50
2-4
Stream/lake
--+ I
Sediment
Outlet
Fig. 1. Model of P concentration al ong a low and
high flow path in an oligotrop hic system. Width of butterfly diagram is generally proportional to con centration. Shaded area corresponds to additional P mobilized by rerouting of shallow soil wa ter.
adsorption capacity fo r PO, (SIMS & ELLIS 1983, FROELICH 1988, GRUNDL & DELWIClIE 1993). Tbe concentration of secondary P is typ ically highest in the Bs horizon o f podzolic soils and is dominated by AI-occluded P (FER NANDEZ & STRUCHTEMEYER 1985). So il solutions Root uptake of PO, and equilibria between the solid soil and soil solutions yield variable soil solution chemistries with depth in the mineral soil profi le. Prtcipitatioo and ion exchange re actiOns are rap id, with equilibrium approached within minutes to hours (DAVID et al. 199 1, GRUNDL & DELWlCHE 1993). Sballow ground
base cations and consumption of H+ during pri mary wea th ering of silica te minerals), and bio logical reductio n of N03 and SO, (consuming H+). Biological degradation of di ssolved organ ic carbon (DOC) reduces organic acidity (about 5 !-leq organi c anion mg- ' DOC L- I) wbi le con currently increasing the so il air PC02 to values up to 10- 1 l bars (FERNANDEZ et al. 1993). The loss of organic acidi ty at a pH near 4.5- 5 may cause a decrease in solu tion ac idity as solutions percolate deeper in soils , despite potential in creased PC02 from respiration in subsoils. Higb PCO, buffers pH increases from weather ing, favoring increased desorption of base cations and AI, and depressed pH . The interac tions between soi l and soil-water with eleva ted PC02 have been documented in situ and suc cessfully modeled witb MAGIC (FERNA'H)17 et al. 2003 , NORTON et a!. 2001). Dissolved AI, Fe and P concentrations in soil solutions genera lly decrease with depth in tbe mineral soil (LAWRENCE & FeRNANDEZ 1991 ) as pH and base saturation increase (Fig. I). Consequently, PO, is typically lost to adso rption sites as soil waters percolate deeper in the soil. However. during periods of high input of precipi tation or snowmel t, "horizontal" flow paths become in creasingly important in the saturated zone as active flow is routed along shallow flow paths and magnifying th e linkages between shallow soil layers and surface water (Fig. 1). Under such circumstances. neutralization o f inorganic aci dity (largely S04 and N03) and organic acid ity is less complete (BORG 1986, HRUS KA et a!. 1999, BISHOP et al. 2000). Tbe lower pH and higher DOC alo ng shall ow flow paths results in increased deso rption and dissolution ofAl (and of Fe to a lesser degree; TtPPING et al. 199 1). Concurrently, higher concentrations of dis solved PO, may be routed directly to streams (Fig. 1). Increased export 0 f base cations from soils due to soil ac idification has been produced ex perimentally at the bench-scale (DAVID et a!. 1991 ) and at the whole ecosystem scale at the Bear Brook Watershed in Maine (BBWM) (FERNANDEZ et a!. 2003), and has been modeled successfull y by MAGIC in sbort- and lo ng term acidificati on tim eframes (COSBY et a!.
·, •
S. Norton el aI. , Aluminium. phospborus, and oligotrophr
2 1 0
.
...:l
::; ~
I\.
"
-J -2
< -5 O!> 0
" ,,,
-3 -4
Fig.2. Dominant dissol ved AI species and the solubility surface for amorphous AI(OH h. The dilTcrcncc in Al concent rdtion for solutions 1 and 2 corresponds to the mol es AI L- 1 that are precipitated as pH ri ses in a saturated solution.
1879
"1 3+
" 2"""-
AI(OH)J
...........
..........
.,
I
-6
I
-7
Al(OH)z+
-8 3
1985a, 1985b, 1996). Mobilizatio n o f AI fro m soil isolates from BBWM was demonstrated experimentally by DAVID et aJ. (19 9 1) using H 2S0, and elevated C02, but they did no t measure PO,. During periods 0 f higher dis charge (and lower pH) at BBWM, mono meric AI increases in concentration in stream water concurrently with total reactive P. We hypothe sized that adsorbed PO. from soil or stream
sediment became mobilized as the Al was dis solved from soil or stream sedinnent (RoY et aJ. 1999, REtNJ-IARl1T ot at 2004) . The AI and PO. may then be removed from solution down stream through uptake by biota (P), or re sorbed (P) or precipillted (Al and P; M ULHOL LAND et aJ. 1986) a s pH increases.
Stream water Elevated PCO, in soil air can mobilize Al in soil water due to depressed pH (NORTON & HE"Rt:KSEN 1983 ). Precipitation of A I(OH h in streams from AI-rich groundwater may result from degassing o f excess CO" mixing o f groundwater with stream water of higber pH,
and mixing of water from an acidic stream with a less acidic stream (ROSSELAND et aL 1992). The amount of A1(OH), that is precipitated is maximized just above pH 4 .7, where decreas ing PCO, is effective at increasing pH and de creasing Al solubility by several o rders o f mag nitude (> 90% reductio n o f di ssolved Al) with respect to a unit change in pH (Fig. 2). This may occur when soil peo, of about 10- 1 5 aim de creases to about 10. 3 .< atm (ambient atrnospher
Al(OH)4
I I
I
5
7
9
pH ic co nditions). The precipitated AI(OH), may
either coat stream sediments or remain in tbe water column, eventually sedimenting in qui eter water. Mobilization of precipitated Al(OH)3 has been demonstrated in stream acid ification experiments in Europe (TlPPlNG & HOPWOOD 1988 in England, H ENRIKSEN et aL 1988 in Norway, NAVRATIL et a1. 2003 in Czech Republic) and in the US.A (HALL et aL 1984 in New Hampshire, NORTON et aL 1992, 2002 in Maine), and precipitation of AI(OH)3 was demonstrated by AI addition (HALL et aL 1985). The experiments demonstrated that Al may be released from the stream bed with the probable stoichiometry of Al(OH)J, and that the process is rcversible. ORMl:ROD et aL (1987) experimen tally demonstrated that Al was not mobilized in a stream with a pH -7. PresU01ab1y Al was not
delivered to the stream by groundwater during any flow regime. Phosphorus additions to streams also indicate uptake of dissol ved P by stream substrate (MEYER 1979). MULHOLLAND et aL (1986), PLAN AS & MOREAU (1986), and ELWOOD & MULHOLLAND ( 1989) suggested that P may be partly controlled in streams by inter action with Al solid phases. At tbe Bear Brook Watershed in Maine ( BB WM), one of two watersheds has been artifi· cially acidified with additions of (NH.), SO. (NORTON & r f RNANDEZ 1999). In the artificial ly acidified watershed, the export of P in the stream increased as pH declined (ROY et a1. 1999). The increased export of P was largely in
particulate fonn, associated with acid-soluble
," •
11180
Verh. internal. Verein. Linmol. 29
5 c:
.,.
4
0
til
........c: ~
c: 0
tJ
Cl
0
'7
Cl :::J
""'"
3
~
- .. -'c
2 1
~
~
•
~~
l~
- .. - - Cisso"ed P
""
*
",. '
0 < ' -..
)(
A
- -¢ V '
1h
-1
r... )(-)(
~
n
99% of the Fe-bound PO, (HlELTJES & LIJKLE MA 1980). For the high-P lake, the ratio of the sediment dithionate-extractable P:Fe was sig nificantly higher tban for the two low-P lakes suggesting that a significantly larger fraction of P was associated with the reducible Fe(lIl) hy droxides in the high-P lake than in tbe low-P lakes. As such, P release in the high-P lake was more susceptible to changes in the hypolimnet ic redox conditions (COOLIDGE 2004). However, for low P lakes, P assoc iated with AI- and Fe bydroxide surfaces is largely retained in the sediment during summer hypolimnetic anoxia. The concentration of total extractable AI, aver aged over 50 cm sediment cores, in the low-P lakes was 845±1 11 f'mol g- I and 746±80 f'mol g- I for Higbland and Pennesseewassee lakes, respectively. These values were 150-200% of tbat in the high-P lake (530 ± 5S f'mol g-I; Fig.5; COOLIDGE 2004). Tbis sequestration would be irreversible because tbe sediment en vironment typically has a pH bigher than that of the overlying water co lumn. and Al is not sub ject to redox transformation.
Long-term P dynamics The availability of di ssolved P and the nux of total P from oligotrophic (or strongly acidified) ecosystems is conceptualized througb time (Fig.6; follows the approacb of FERNANDEZ et al. 2003). During Period A, a steady state pre vails witb concentrations of dissolved and par ticulate P in streams controlled by the net dif ference between inputs (atmospheric + chemi cal weathering) and net storage (biomass and soil net accumulation). Period B corresponds to a period of ongoing acidification of tbe water shed. In the early stages of B, base cation de pletion occurs because base cation exchange is the principal acid-neutralizing mechanism. Lat er in B, Al from relatively labile secondary mineral soiJ pbases is mobilized along with ad sorbed P and transported to the stream. As acid ification progresses (Period C), mobilization of AI and P continues, with Al mobilization from
,
.•
.,
s. Norton et aI., Alumin ium, phosphorus, and oligotrophy
1883
Highland Pond umoleslg
o E (J
...
.c
Q. Q)
C
10
20
30
40
50
,
,
,
,
,,,
0 2 3 5 6 8
, , , , , , , , ,, , ,
9
12
-
,
-,'
'-
,
,,
80
" NH4CI
, -
70
I
, ,
-
60
.SD ,
. NaOH-25
,
OHCI
Ii!! NaOH-85
,
I
Salmon Pond umoleslg
0
E (J
...
.t: Q. Q)
C
10
20
30
1 3 4 6 7 9 11 14 17 20 25 31 37
40
50
60
70
80
I [D NH4CI
.SD NaOH-25 DHCI
Ii!! NaOH-85
Fig.5. Speciation of P iu sediment of oligotrophic Highland Lake and mesotrophi cleutrophi c Salmon
Pond, Maine, U.S.A. large mineral soil pools dominating soil and so lution chemistries. During this period, even as dissolved Al increases in the stream, precipita tion of PJ in the stream increases, which has a
disproportionate effect on the smaller mobi lized P pool, consequently decreasing dissolved P in the stream until it falls below the original steady state values (Period D). By tbe end of D,
•
••
1&84
Verh. internal. Verein. Limnol. 29
(8)
(e)
(D)
t
""
+
........
.......
------- - .---,.' ,' "
.......
, . ' .'
.,'
,.'
..... _
'"
Time Labile Soil P Phases
Stream Pdissolved
Stream AI, Pparticulale
Soil solution AI, PdIssolved
Fig.6. Long-term behavior of Al and P during chronic acidifica tion of soil phases, soil solutions, and streams.
export of particulate P and AI reaches a maxi mum as export of dissolved P reaches a mini mum . Tbe depletion of Iablle AI-soil phases causes a shift from export of dissolved Al as tbe principal acid-neutralizing mechanis m to ex port of Fe (Period E). Few ecosystems have been documented to be in this advanced state of acidification. Those that do exhibit evidence of active Fe mobilization have been either severe ly acidified over a long period of time or were without significant labile Al soil phases when acidification stressors began (BORG 1986, RELN IIARDT et al. 2004) .
Acknowledgments We gratefu lly acknowledge financial support hom the U. S. Geological Survey (200IMEI4 8 IG), the Czeeh Acade my of Science (CEZ Z 3·0 13· 91 2 and 83013203), the Main e Department of Environmental Protection, International Paper, and the 'G, S. Nation al Scie nce Founda tion ( 0"£1-3 -041534 8). Thi s is con tribution #. 2881 rrom the Maine Agricultural Experi ment Station.
References AMlR~AlIMA N, A. , PEARCE,
A.R., Bout:HARD, RJ., NOR
TO1\", S.A. & K AI-IL, 1.S., 2003 : Rclationship bern'cen hypolimnetic phosphorus and iro n release from eleven lakes in Maine, USA. - Biogeochem. 65 : 369 - 386. S."KER. L.A . et aI., 1990: Currenl Status of surfaee wate r acid-base chemi stry: National Aeidic PrecIpitati on Assessment Program, Washington, D.C., Repon 9, 367 pp. plus appcndiet:s. BISHOP, K., LAUDON, H. & KOHLER, S., 2000: Separating the naturaJ and anthropogen.ic components of spring fl ood pH decl ine: A method for areas that are not c hronically aCIdifi ed. - Wat . Resour. Res. 36:
1873-1884. BORG, H., 1986: Metal speciation in acidified mountain streams in central Sweden. - Water Air Soil Pollut.
30: 1007-1014. B1WBERG, 0 ., 1984 : Phosphate re moval in acidified and limed lake water. - Wat . Res . 18: 1273-1278. BROBERG, 0. , 198 7: N utrient resp onses to the liming of Lake Gardsj6n. - Hydrobiol. 150: 11 - 24. C."RACO, N.F., COLE, 1.1. & LlKEl\'S, G.E., 1989: Evidence for sulfate-controlled phosphoru s release from sedi me nts of aquatic systems. - Nature 341 : 316-31 8. COOLIDGE, K., A MIRBA HMAN, A . & N ORTON, S . A ., 2003 : Does aluminum geochemistry con trol the trophic sta tus of oligotrophic lakes? - Int. Conf. Paleolimn .,
Helsinki Finland.
S. Norton et al., Aluminium, ph osphorus, and oligotropby COOLIDGE, K .M., 2004: Phosphoru s cycling in Maine Lakes: A sedimentary anslysis. - M.S . Thesis, Civil and 'Environmental Engineering, Univ. of Maine, Orono, ME. COSBY, B.1., H ORNBERGER., O.M. , GALLOWI\Y, 1.N. & WRtGHT, R.F., 1985a: Time scales ofa catchment acid ification : a quantitative model for estimating fresh wa ter ac idific.1AGGIN1, L., 2003: The rcspomc of a small stream in the Lesni potak fores ted catch
ment, central Czech Republic to a short-term in strea m acidification. - Hydro\. Earth Syst. Sci. 7: 41 1-422. NEAL, c., RE YNOLDS, 8., N EAL, M., H UGHES, S., WICK HAM, H., HJLL, L., ROWlAND, P. & PUGH, 6. , 2003:
Soluble reaeti ve phosphorus levels in rain fa ll , cloud water, throughfaU, stem flow, soil waters, stream wa ters, and groundwaters for the Upper River Severn area, Plynlimon, mid-Wales . - Sei. Tola l Env iron. 314-3 16: 99- 120. NORTON, S.A., 1976: Changes in ehcm ical processes in soils caused by aeid prccipitatlon. - Water Air So il Poll. 7: 487-499. NORTON, S.A. & H£NRIKSEN, A. , 1983: Thc importance of C02 in evaluation of effects of acidic deposllion. Vanen 39: 346- 354. NORTON, S. A., BRO'l'.'NLEE, 1 & KA HL, J.S., 1992; Artifi cia l acidi fi cation of a non-ac id ic and an aCIdic hcad water strC
