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EPA
United States Office of Water EPA 440/5-88-004Environmental Protection Regulations and Standards April 1989Agency Criteria and Standards Division
Washington, DC 20460Water
Ambient Water QualityCriteria for Ammonia(Saltwater)-1989
AMBIENT AQUATIC LIFE WATER QUALITY CRITERIA FOR AMMONIA
(SALT WATER)
U.S. ENVIRONMENTAL PROTECTION AGENCYOFFICE OF RESEARCH AND DEVELOPMENTENVIRONMENTAL RESEARCH LABORATORY
NARRAGANSETT, RHODE ISLAND
NOTICES
This report has been reviewed by the Criteria and Standards Division,
Office of water Regulations and standards, U.S. Environmental Protection
Agency, and approved for publication.
Mention of trade names of commercial products does not constitute
endorsement or recommendation for use.
This document is available to the public through the National Technical
Information Service (NTIS), 5285 Port Royal Road, Springfield, VA 22161.
i i
FOREWORD
Section 304(a)(1) of the Clean Water Act of 1977 (P.L. 95-217requires the Administrator of the Environmental Protection Agency topub l i sh wa te r qua l i t y c r i t e r i a t ha t a ccu ra t e ly r e f l ec t t he l a t e s tscientific knowledge on the kind and extent of all identifiable effects onhealth and welfare which might be expected from the presence ofpollutants in any body of water, including ground water. This document is arevision of proposed criteria based upon a consideration of commentsreceived f rom other Federal agencies , Sta te agencies , specia l in teres tgroups , and individual sc ient is t s . Cr i ter ia conta ined in th is documentreplace any previously published EPA aquatic life criteria for the samep o l l u t a n t s .
The term "water qual i ty cr i ter ia” is used in two sect ions of theClean water Act , sec t ion 304 (a)(1) and sect ion 303 (c)(2) . The termhas a d i f ferent program impact in each sect ion. In sect ion 304, theterm represents a non-regulatory, sc ient i f ic assessment of ecologicale f f ec t s . C r i t e r i a p r e sen t ed i n t h i s documen t a r e such s c i en t i f i c a s se s s -meri ts . I f water qual i ty cr i ter ia associated with specif ic s t ream uses areadopted by a state as water quality standards under section 303,they become enforceable maximum acceptable pollutant concentration inambient waters wi thin that s ta te . Water qual i ty cr i ter ia adopted inState water quality standards could have the same numerical values asthe criteria developed under section 304. However, in many situationsSta tes might want to adjus t water qual i ty cr i ter ia developed under sect ion304 to reflect local environmental conditions and human exposure patternsbe fo re i nco rpo ra t i on i n to wa t e r qua l i t y s t anda rds . I t i s no t un t i lt he i r adop t ion a s pa r t o f S t a t e wa te r qua l i t y s t anda rds t ha t t he c r i t e r i abecome regulatory.
G u i d e l i n e s t o a s s i s t t h e S t a t e s i n t h e m o d i f i c a t i o n o f c r i t e r i apresented in this document, in the development of water quality standards,and in other water-related programs of this Agency, have been developed byEPA.
Martha G. ProthroDirectorOffice of Water Regulations and Standards
i i i
ACKNOWLEDGEMENTS
Don C. Miller David J. Hansen(sal twater author) (saltwater coordinator)U.S. Environmental Protection AgencyEnvironmental Research Laboratory
U.S. Environmental Protection Agency
South Ferry RoadEnvironmental Research Laboratory
Narragansett, Rhode Island 02882south retry RoadNarragansett, Rhode Island 02882
i v
CONTENTS
Foreword. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. .iii
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. iv
Tables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vi
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1
Acute Toxicity to Saltwater Animals . . . . . . . . . . . . . . . . . . . . . . .7
Chronic Toxicity to Saltwater Animals. . . . . . . . . . . . . . . . . . . . . . . 14
Toxicity to Aquatic Plants . . . . . . . . . . . . . . . . . . . . . . . 17
Other Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
Unused Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22
Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24
National Criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 27
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 48
v
TABLES
1. Acute Toxicity Of Ammonia to Saltwater Animals. . . . . . . . . . . . .32
2. Chronic Toxicity of Ammonia to Aquatic Animals . . . . . . . . . . . . . . . . .39
3. Ranked Genus Mean Acute Values with Species Mean Acute-Chronic Ratios . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .43
4. Other Data on Effects of Ammonia on Saltwater Organism. . . . . . . 45
v i
INTRODUCTION*
in aqueous solutions, the ammonium ion dissociates to un-ionized ammonia
and the hydrogen ion. The equilibrium equation can be written:
H2O + NH+ NH3 + H3O+
(1)
The total ammonia concentration is the sum of NH3 and NH4+.
The toxicity of aqueous ammonia solutions to aquatic organisms is
primarily attributable to the un-ionized form, the ammonium ion being less
toxic (Armstrong et al. 1978; Chipman 1934; Tabata 1962; Thurston et al.
1981; Wuhrmann et al. 1947; Wuhrmann and Woker 1948). It is necessary,
therefore, to know the percentage of total ammonia which is in the un-ionized
form in order to establish the corresponding total ammonia concentration
toxic to aquatic life. The percentage of un-ionized ammonia (UIA) can be
calculated from the solution pH and pKa*, the negative log of stoichiometric
d i s s o c i a t i o n ,-1*
% UIA = 100 [ 1 + 10 (( p K - pH)] a
The s to ichmetr ic d issocia t ion constant i s def ined:
(2)
[NH3] [H+]K a
* (3)[NH4
+]
where the brackets represent molal concentra t ions . K a* i s a funct ion of the
temperature and ionic s t rength of the solut ion .
* An understanding of the "Guidelines for Deriving Numerical NationalWater Quality Criteria for the Protection of Aquatic Organisms and TheirUses” (Stephan e t a l . 1985) , hereaf ter referred to as the Guidel ines , and theResponse to public Comment (U.S. EPA 1985c), is necessary in order tounders tand the fo l lowing text , tables , and calcula t ions .
Whitfield (1974 developed theoretical models to determine the pKa* of
the ammonium ion in seawater. He combined his models with the infinite
dilution data of Bates and Pinching (1949) to define general equations for
the pKa* of ammonium ion as a function of salinity and temperature.
Whitfield’s models allow reasonable approximations of the percent un-
ionized ammonia in sea water and have been substantiated experimentally by
Khoo et al. (1977). Hampson's (1977) program for Whitfield’s full seawater
model has been used to calculate the un-ionized ammonia fraction of measured
total ammonia concentrations in toxicity studies conducted by EPA and also in
the derivation of most other acute and chronic ammonia values which
contr ibute to the cr i ter ia . The equat ions for th is model are :
% UIA = 100 [ 1 + 10 (X + 0.0324 (298-T) + 0.0415 P/T - pH)]-1(4)
where
P = 1 ATM for all toxicity testing reported to date;
T - temperature (°K);
X = pKas or the stoichiometric acid hydrolysis constant of ammonium ions in
sal ine water based on I ,
I = 19.9273 S (1000-1.005109 S)-1
where
(5)
I = molal ionic s t rength of the sea water ;
S = sa l in i ty (g /kg ) .
The Hampson program calculator the value for I for the tes t sa l in i ty (Eq. 5) ,
finds the corresponding pKas, then calculates % UIA (Eq. 4).
2
Ze ?d:Cr f3CZZ:s '-6‘.qerr*-q -,".e iegree :f mc:a ~~ss;c;atr=n -..--- ..bb.. I zre ;.i!
& temperat-dre. 30th czrrelste g0sltrq;ely *drth 2n-lznlztd -nLa.
Sallr.lt’(, *-he least rnfluent:al sf c,C.c three water p.allty fact3rs ‘,ia t
cmtr31 L_?e fractim of lm-ionized mania, is rnversely correlated.
In ammnia toxicity testing, the pH is nonaally calibrated using 1%
ionic strength National Bureau of Standards (NBS) buffers. In contrast,
Rho0 et al. (1977) used the free hydrogen ion sea water scale (ph(~)) in
their masurermnts of ammnium ion hydrolysis in sea water. ‘While the ph(F)
scale is desirable frcm the themdynamic sta&point, these seawater buffers
are not available from a central source, precluding their us0 in toxicity
testing. Calibration of pi with Ems buffers does contribute an error in the
calculation of 1 un-ionized amnnia, although, fortuitously the error is
sa~ll, presmably due to a coqensation of the liquid junction potential by
changes in activity coefficients (Bates a& Culkrson 1977). tillero (1986)
fourd the pH(NES) scale to uverestimata pf4 relative to the free hydrogen ion
scale by 0.02 pi4 unit at 30 g/kg salinity, 0.045 unit at 20 g/kg and 0.075
unit at 10 q/kg. The residual jmction potential is a proprty of the
reference electrcd8 used and may vary ,+ 0.03 pH unit witf! salinity, timb, and
electrode type (Whitfield et al. 1985).
Controlling pn in salt vater anraia toxicity tests is difficult.
Amwniwn salt solutions are acidic, but are slow to teach equilibrium in sea
water. Conmqwntly, @! typically declines during toxicity tests and the
decline may k rrqlified by artabolism of test organisms. Also, tests
conducted akm oc klou the seawater equilibrium pH (7.8-8.2) eqrience
strong shifts toward the bufferod state. Inconsistency in degree of control
of test pH is a major source of variability in ammia toxicity studies
3
~swc:ally ir: sea ;acer. .i - :.I $4 ~~7;: ‘,‘ar:.mce kmld :esuir: ,n a
~sesc:sat:on 3f ‘-?.a ?;H3 effec: zncent:at:m of abut f 25% at pi 8 and
25’C.
A nuder of amlytlcal scthods are available for direct detemunat&on of
totaL ammnia concentrations in aquamm solutioru (Richards and Healey 1984).
Once total amxxi3 is measured, and the pti, salinity and teqerature of the
solution date. -A concentration of NH3 present CM k calculated bar&
on the aammia-seamcer equilibrium expression.
hmnia conc8ntration.s have been reported in a variety of forms in the
aquatic toxicity literature, such as NH3, NHq+, M13-N, MIqoLI, NITqCl and
others. me us4 in the literature of tha terms M3, Ept3+4,0c -la-
nitrogen may not necessarily man un-ionized ma, but msy be ths author*s
way of expressing total aammnia. CaaporPdrumdintho -a toxicity
tasts -fired bore ace NXqCl, PU14M3 ad (MQ)$O,.
Throqimt the resmin&r of this doamnt, all quntitative anmania
data havw been l xorrsmd in terms of me/L m-ionizad ma for easo in
discwrion and coqmrison, ad since urkionized ma is the principal
toxic form. ma concentratims reported &y authors are given as reported
if ths author ( s 1 provided data expressed as iag MI+, or ccmvortsd to mq/t if
reported in 0th~ units. Xl authors report& only total ma, or if they
calculatsd 9 caac8ntrrthn by a unique mmthad (e.g., m W. 19861, the
total II vdrr ud reported j#I, teqsrrture, ad dtnity codition8
kwr* used to alculatm og MffL, par th8 s (1977) proparr. This
approach prakm 9 valuer that arm consistently drriwd.
Scam literature citad in this dommnt fail to providr MI3 CQeym-
trations or total umnia conc8ntrations along with sufficient Per, t-r-
papers were not US& but are clteci Iunder “‘Jnused Sata”. :n some :nstances
rnfomat1on UliSSlng rn published papers on expermental conditions was
obtained througtl correspondence with authors; data obtained in this manner
are so indicated by footnotes and are available from U.S. EPA, CRL,
Narragansett.
A number of criteria domnents, review articles and books dealing with
ammnia as an aquatic pollutant ace available. Armstrong ( 19791, Becker and
Thatcher (19731, Colt and Armstrong (19811, Eplet (19711, Hanpson (19761,
Licbann (19601, McKee and Wolf (19631, Steffenr (19761, atxl Tsai (1975) have
published suamarirs of ammnis toxicity. Literature reviewe, including
factors affecting ammnia toxicity and physiological conmqwnces of ammmia
toxicity to aquatic organisms, have been publish& by Kinno ( 1976 1, Lloyd
(19611, Lloyd and Herbert (19621, Lloyd and Swift (19761, Visek (19681, and
Warren (1962). Literature review of aaamnia toxicity information relating
to criteria reconmmndatfons have been published by ifdabaster and Lloyd
(19801, European Inland Pbheries Advisory Conmission (19701, National
Academy of Sciences and National AC- of Engineering (19741, National
Research Council (19791, U.S. Environmntal Protection Agency (1976, 1980,
1985a), U.S. federal Water Pollution Control Administration (19661,
willin- (19761, arid Willingham et al. (1979).
TM ctitoria presented herein supersede prwious saltwater aquatic life
water quality criteria for mia because these new criteria were derived
using iqruved procdurer and additid information. Mmmver adequately
justified, a national criterion may k replaced by a sit*sp=ific criterion
(U.S. EPA 1983a), which may include not only sit+speific criterion
~37ce~trat~ons ad mxing zone cons:deratlons ‘J.S. EPA, L983bi , mt also
sita-specific durations of averaging periods and sita-spcific frequencies
of all4 exmedencer (U.S. ePA 198Sb). This criterion doe8 not apply to
saltwater lake8. There water bodies may require developmnt of site
specific water quality criteria. T!w latert coqreheruive literature
March for infocmatfon for this documnt war coducted in June, 1986; sonm
more recent informtim ha8 bmn included.
ACUTE TOXICITY TO SALTWATER ANIMALS
The acute toxicity of ammonia to saltwater animals has been studied in
crustaceans, bivalve mollusks, and fishes. Acute values are summarized in.
Table 1 for 21 species in 18 genera. The winter flounder, Pseudopleuronectes
americanus, represents the most sensitive gems, with a Species Mean Acute
Value (SMAV) of 0.492 (Cardin 1986). Fourteen (eight fish, five crustaceans
and one mollusc) of the remaining 17 genera have Genus Mean Acute Values
within the order of magnitude of that for the winter flounder. The three
most tolerant species are mollusks. The SMAVs are 19.1 mg/L for the Eastern
oyster, Crassostrea virginica, 5.36 mq/L for the quahog clam, Mercenaria
mercenaria, and 3.08 mg/L for the brackish water clan, Rangia cuneata.
Except for these mol lusks , there i s no phyle t ic pat tern in acute sensi t iv i ty
to ammonia. Fishes and crustaceans are well represented among both the more
sens i t ive and the more to lerant species tes ted .
Few consis tent t rends or pat terns are evident in the acute toxic i ty
values c i ted in Table 1 wi th respect to b io logical or environmenta l var i -
a b l e s . C o n t r i b u t i n g t o t h i s , i n p a r t , i s t e s t v a r i a b i l i t y . T h i s i s e v i d e n t
in multiple tests with the same species, even when conducted under closely
comparable conditions. Variability in acute toxicity values for ammonia may
ref lect d i f ferences in coal i t ion of the tes t organisms, changes in the
exposure condi t ions dur ing tes t ing, par t icular ly pH, and var iance incurred
through calculation of un-ionized ammonia concentrations. As noted in the
Introduction, pH has a strong influence on the concentration of un-ionized
ammonia in water, such that a variation of ± 0.1 pH unit during the test my
result in ± 25% variation in the NH3 exposure concentration. The NH3
exposure concentrations are calculated values dependent on accurate
7
measurement of exposure pH. However, pH monitoring during a test may not
always detect potentially significant pH excursions. Also, non-systematic
errors on the order of ± 0.03 pH unit may also occur with seawater pH
measurements due to variation in the liquid junction potential between and
within e lec t rode pai rs . In addi t ion to these sources of er ror ,
in terpre ta t ion of tes t resul ts should consider known repl icabi l i ty of
tox i c i t y t e s t s . I n t r a - and in t e r - l abo ra to ry compar i sons o f acu t e t ox i c i t y
test results using saltwater species show LC50s may differ by as much as a
factor of two for the same chemical tested with the same species (Hansen
1984; Schimmel 1986) . In l ight of a l l these sources of var iabi l i ty , LC50s
for un-ionized ammonia are in this document considered similar unless they
d i f f e r by a t l eas t a f ac to r o f two .
Few marked differences are evident in the acute toxicity of ammonia with
respect to di f ferences in l i fe s tage or s ize of the tes t organism. Yolk-sac
larval s t r iped bass (Morone saxat i l is) seem s l ight ly less sens i t ive to un-
ionized ammonia (LC50s - 0.70 and 1.09 mg/L) than 9 or 10 day old post-yolk
sac larvae (LC50s - 0.33 and 0.58 mg/L) (Poucher 1986). Juvenile striped
bass also seem less sensitive than post yolk-sac larvae (LC50s range from
0.91 to 1.66 mg/L) in tests by EA Eng. (1986) and Hazel et al. (1971). Acute
values for s t r iped mul le t (Mugi l cephalus) suggest a factor of two decrease
in sensitivity (LC50 - 1.19 vs. 2.38 mg/L) to ammonia with increase in weight
from 0.7 to 10.0g (Venkataramiah et a l . 1981) . Larval grass shr imp
(Palaemonetes pugio) appear to be more acutely sensitive (LC50 - 1.06) (EA
Eng. 1986) than juveniles and adults (LC50 - 2.57) (Fava et al. 1984),
a l t hough the con t r a s t i ng l i f e s t ages we re t e s t ed a t d i f f e r en t s a l i n i t i e s . A
sl ight decrease in the acute sensi t iv i ty of Eastern oysters , Crassosr t rea
8
. . . V”. 7’ ‘j .-&4&i a- I :S e’/:dent fec**neeq 13 & 1’ . --, - . m ,&.=b -3.5 t 15.rno~L, a--d ;: -3
52 elm (LCSO - 24 to 43 rng/L) zp~fano and 5rm L975). NO site rciattd
iiffercnC* in amte Sensltivrty to afmmma .kdas seen Sctwetn 4.7 to 5.2 35 and
28 to 32 run quahog clams, (Hcrcenarra mercenarla) (Epifanio and Srna 1975).
3evcrai data sets in Table 1 permit an evaluation of t!!c inf?ucncc sf
salinity, tenperaturc and pH on the acute toxicity of ammnia to saltwater
animals. Few differences are evident in acute toxicity at different
salinities in tests with Similar life Stages ti similar pH and teqerature
conditions . wids (Wsidopsis bahia) have owrlappinq LCSOs at four
salinities in tests at pH ) 7.8 and 2S.C. At 10 to 11 e/kg salin$ty, NH3
LCSOs range from 1.04 to 3.19 mq/L; at 20 9/kg, 2.82 to 2.87 mq/L; at 30
g/cg, 1.47 to 3.41 mq/L (CardIn 1986); and at 14 to 18 g/kg, 0.92 to 1.68
mg/L (EA Ehg. 1986). At pM 7.0, the LCSO was lmmt at a 1~ salinity by a
factor of 2.2 (Cardin 1986) (KS0 - 0.23 me/t at II Q/kg; O.SO ad 0.54 mgfi
at 31 g/kg salinity). Acute values for larval inlamd silwrsider (Menidia
baryllina) tested at pH 8 Md 2S’C are approximately a factor of 2 1cn-m at
I1 en<g salinity vith the LCSO - 0.88 mg/t, relatiw to 1.94 me/L at 19 g/kg
and 1.77 mqF at 30 g/kg salinity (Puucher 1986). Hmmwr, at pl4 7 and 9, the
LC5Os for theu larva8 an slightly higher at 11 Q/kg than at 31 g/kg
salinity (by a factor of 1.7 a& 1.5, tcspmxiwly, casprrring flow throuQh
test valws unly). Athntic silwrsidr (Meniclia wnidia) juvwniles at pH 8
and 1 20.C hava MI3 US08 ranging from 0.97 to 1.24 mqF at 9 to 10 g/kg
salinity (m m. 1986) Mch correspandr ~11 with the 0.98 19% value
reported at 30 g/kg salinity by Fava et al. ( 1964 1. Acute valws overlap for
bm fishes tested at low a& high salinities by ~uol et al. (1971). For the
three spined stickleback (Gasterosteus aculeatus), LCSOr range~from 2.09 to
9
- ‘5 33,: 3: - . ACJrCx:=tel*/ 11 ; ‘<ri jal:.?.::~ 3.r.d 1.58 ‘I: 3. j .m,', 3:
appr:xzrately 34 g/kg. ilic,cI ;-,-Jcntle str~ged k-ass ??crme saxa::lisi , ~52s
are 9.91 (EA mg. 1986) and 1.83 to 1.58 .nq/L at aoprcxlaately ?L . ?.bg
salinity; 0.75 Wd 1.4 rag/L at approxmately 34 g/kg !!iazel et al. 1971).
reqerature also has little influence on the acute toxicity of axmmnia
with mst saltwater animals tested. Acute values for thermally acclimated
lawal inland silwrsids (Nsnidia kryllina) tested at three teqeratures and
at similar pH Md caimity (8.0 pH; 31 g/kg salinity) differ by less than a
factor of 2. For this species tested at 18*C, the LCSO is 0.98 w; at
tS*C, LCSOs are 1.7s and 1.77 mg/L; and at 32.S'C, the LCSO is 1.7 meft
(Paxher 1986). The LCSO for ttmrmally acclimated larval shmpshmd miranow
(Qprfnodon varieqatw) at 13.C is 2.10 aq/L; at 2S*C, 2.79 aryt; m at
32.S*C, 3.5 mq/t (Patcher 1986). Acute valws for juvsnile stripd bsss
(Norone saxatilis) tested at 1S.C aruI 23.C avwrlap wtmn trstsd at
approximately 11 e/kg ulinity srxl diffsr by less than a factor of 2 at
approximstely 34 g/k0 salinity (Hszsl et al. 1971). With three spined
sticklebsck (Gssterosteus aculratus) there war little difference in
sensitivity to NF$ at 1S.C (-0 - 2.75 mg/L) and 23.C (LCSO - 2.09 me/t) at
approximately 11 9/kg salinity, but in tssts at approximtely 34 9/kg,
sensitivity vas about 2 tims greater at the higher taqorature (at 23T,
LCSO - 1.68 Md 2.7 arq/t; at lS°C, LCSO m 4.35 ad 5.6 nrqF) t-z.1 et al.
1971).
S8vw8l data sets r *-ha effect of pii on th toxicity of un-ionitsd
anwnia suqg#t tht .a tha data on frmhwatw spociss, tha ptCt=icity
rrlatlonship is not conrir;tent bebeen spuies. Text Table 1 summrizrs
LCSOs of acute tssts comhctec! at different pii cordftions. Results ars
10
Text Table 1.
Acute Toxicity of l&b-ionized mia to the Prawn (Hacrobrachium rosenber ii), Hysid (Rysidopis I&ld), hrva1 Inland Silverside (Henidia bebeina). - .--_
pli Corditions. and Juvenile Athntlc 51 vlers& (nenidia =nidTai, at chtteLtibit
m~ici ty expressed as US rg tw3/L.
m-+L _c_- -
and salinity conditiorY iadicated. Flew-through test resultsunderIined, amn teqxrdtule
- ---_-.-_ -
Pram Hyrid Inland Athntlc Silverside
~hl-mstrong (Car&n (Cardin lElr Enq. ( Douche c ( Pouch@ c (LA thy. et al. 1978) 1986) 1986) 1986) 1986) 1986 1 l!m)
PH 28.C, 12 g/kg 24.5’C, llq/kg ZS’C, 31 g/kg 20°C, 31 g/kg 25T, 11 q/kg 25“C, 31 g/kg 22”c, 9.5 g/kq - ---___
6.5-6.9 0.38
7.0-7.4 1.64 0.93, 0.97, 0.91 i-36
7.5-7.9 0.95 1.18 1.47 0.40, 0.92, 1.40 1.05, l.).! --- 1.0
8.0-8.4 1.3 1.04, 3.19 1.70, 2.49 0.76 Z.Qe, 3.41
0.88 1.77, 1.75 0.97, 1.01, 1.10, 1.24
8.5-8.9 2.76, 0.77 1.51, 1.68 1.08 1.41
9.0-9.4 2.02 1.16 0.75, 0.49 1.21
-
11
;egresacecf -zy ‘,7e :eTrwr3~**-0 p.d -4- - jai _..- _- ’ ‘-*“i ~~F.dlt~XS 2f c,le :ps:j ‘-3
?reclda variabillcy fra LYCSC scurces; X509 also are Listed by autk.cr 5.3
any :nccrlaboratOrj var:ability nay be cecqnlred. For t!!c cm inverCebra:e
specrcs, -A acute sensitivity to .mJ is greater (> factor 2) at luu pH for
the pram !pH 6.83) !Annstrong et al. 1978) and for the qmid !pH 7.0)
(Cardin 1986; EA Eng. 19861, than at hiqher pH values. This response with
rupidr was consistent at low bed high salinity. T?m twu fishes tested differ
from the aysid and prawn in their respmse to pfi. Larval inland silverside
(Henidfa bryllina) do S~CYW increassd acute sensitivity to aarponia as pH
decreases from 8 to 7, but differ from ths mysid responss at pH 9.0, with
appreciably increased sensitivity (> factor of 21 in 31 g/kg salinity, In
contrast, in 11 Q/kg salinity wster, inlard silversids ham a nearly tww
fold decrease in acuto sensitivity at ptr 7.0,whilo mysib havm a twwfold
increase in aeuts senritlvity at #I 7.0. A furthst contrsst exists in ths
response of jwenilo Atlantic silversib (Mnidir mnidia), with tort pH over
the range of 7.0 to 9.0 having little l ffut an tha acut toxicity of
ammonia (EA Eng. 1986). The inflwnce of pfI on aamnia toxicity in these tsro
saltwater fishes is also a msrksd contrast tith the tesporus of several
freshwater fisher (Erickson 1985) a& my reflect bssic differencss in
o-tic and ionic regulatory physiology which could inflwncs their response
to elsvatsd l xtwzml Ia cuxmtratfanr of ovw a rsngm of pit, rrlinity
ad teqor8turm caditiau.
EPA bslimaa that t)w data available on all wrtst qulity-toxicity
relationships for un-iahod anrnia are insufficient to canclti that bny of
theso factors, wtmn acting al-, has a cmsistmt rarjor inflwna 01 m3
toxicity in salt water. Therefore, a water quality dqmd-t fmctfm ms
12
The 18 avaihblt saltmter Gentis Zean Acute values range from 0.492
mg mfL fcr Pseudoplcuronectes :o 19.102 mg “H3fi for Crassostrea, a factor
of less t!!an 100. Acute values are available for more than one species in
thr l e genera. he rang0 of Species Mean Acute Values within two of these
genera is less than a factor of 1.2; in the remaining genus, they differ by a
factor of 4.5. &ighty-eight percent of the Gem Hean Acute Values wre
within a factor of ten and 71 percent wre a factor of ficn of tha acute
valw for Pseudopleuronectes. A saltwater ?l~l Acute Valw of 0.465 mq
NH~ was obtained using the Gefnas Hean Acute Valws in Table 3 and the
calculation procedure described in the GA&lines. This valw is slightly
1-r than Species Mean Acute Value of 0.492 nq/L for winter flounder.
13
CHRONIC TOXICITY TO SALTWATER ANIMALS
Chronic toxicity tests have been conducted on ammonia with twelve
freshwater and sal twater species of aquat ic organisms (Table 2) . Of the ten
freshwater species tested, two are cladocerans and eight are fishes. The
deta i ls of the resul ts of the f reshwater tes ts are d iscussed in the “Ambient
Water Quality Criteria for Ammonia - 1984” (U.S. EPA 1985a). In saltwater, a
life-cycle toxicity test has been conducted with the mysid, Mysidopsis bahia,
and an ear ly l i fe-s tage tes t has been completed wi th the in land s i lvers ide ,
Menidia beryllina (Table 2).
The effect of ammonia on survival, growth and reproduction of M. bahia
was assessed in a l i fe-cycle toxici ty tes t las t ing 32 days (Cardin 1986) .
Survival was reduced to 35 percent of that for controls and length of males
and females was significantly reduced in 0.331 mg NH3/L. Although
reproduction was markedly diminished in this concentration, it did not differ
s ignif icant ly f rom controls . Lengths of females were s ignif icant ly reduced
in 0 .163 mg/L, but th is i s not considered b io logica l ly s igni f icant s ince
reproduct ion was not affected. No s ignif icant effects on mysids were
detected at 0.092 mg/L. The chronic limits are 0.163 and 0.331 mg/L for a
chronic value of 0.232. The Acute Value from a flow-through test conducted
at s imi lar coal i t ions (7 .95 pH, 26.5°C, 30.5 g/kg sa l in i ty) wi th M. bahia i s
1 .70 mg/L which resul ts in an acute-chronic ra t io of 7 .2 wi th th is species .
The effect of ammonia on survival and growth of the inland silverside
(Menidia beryl l im) was assessed in an ear ly l i fe-s tage tes t las t ing 28 days
(Poucher 1986). Fry survival was reduced to 40 percent in 0.38 mg NH3/L,
re la t ive to 93% survival of control f ish , which is a s ignif icant d i f ference.
Average weights of fish surviving in concentrations > 0.074 mg/L were
14
s ignif icant ly less than weights of controls , an effect which pers is ted as the
concentration of ammonia increased. No significant effects were detected in
silversides exposed to 0.050 mg/L. Thus, the chronic limits are 0.050 and
0.074 mg/L for a chronic value of 3.061 mg/L. The acute value, derived as
the geometric mean of flow-through tests with this fish at full strength sea
water between pH 7.0 and 8.0, is 1.30 mg/L, resulting in an acute-chronic
rat io of 21.3 .
Acute-chronic ratios are available for ten freshwater and two saltwater
species (Table 2) . Rat ios for the sa l twater species are 7 .2 for the mysid
and 21.3 for in land s i lvers ides . These sa l twater species have s imilar acute
sensitivities to ammonia, with LC50s near the median for the 21 saltwater
species tes ted. The acute-chronic ra t ios for the f reshwater species vary
from 1.4 to 53, so they should not be directly applied to the derivation of a
Final Chronic Value. Guidance on how to interpret and apply ratios from
tests with freshwater species to derive the freshwater criterion for ammonia
has been detailed in U.S. EPA 1985a which should be consulted. This document
concludes that : (1) acute-chronic ra t ios of f reshwater species appear to
increase with decrease in pH; (2) data on temperature effects on the ratios
ace lacking; and (3) acute-chronic ra t ios for the most acute ly and
chronical ly sensi t ive species are technical ly more appl icable when t ry ing to
def ine concentra t iona chronical ly acceptable to acute ly sensi t ive species .
Therefore, mean acute-chronic ratios were selected from freshwater tests with
species whose chronic sensitivity was less than or equal to the median
conducted at pH > 7.7. These included the channel catfish, with a mean
acute-chronic ra t io of 10; b luegi l l , 12; ra inbow t rout , 14; and fa thead
minnow, 20. The mean acute-chronic ratios for these four freshwater and the
1 5
two saltwater species are within a factor of 3. The geometric mean of these
six values, 13.1, which divided into the Final Acute Value of 0.465 mg/L
yields the Final Chronic Value of 0.035 mg NH3/L.
16
TOXICITY TO AQUATIC PLANTS
Nitrogen in the saltwater environment is an important nutrient affecting
primary production, the composition of phytoplankton, macroalgal and vascular
plant communities, and the extent of eutrophication. Ammonia is an important
part of nitrogen metabolism in aquatic plants, but excess ammonia is toxic to
saltwater plants (Table 4). Limited data on mixed populations of saltwater
benthic microalgae (Admiraal 1977) show that ammonia is more toxic at high
than at low pH (Admiraal 1977). This suggests that toxicity may be
primarily due to NH3 rather than NH4+.
Information on the toxicity of ammonia to saltwater plants is limited to
tests on ten species of benthic diatoms and on the red macroalgal species,
Champia parvula. A concentration of 0.247 mg NH3/L retarded growth of seven
species of benthic diatoms (Admiraal 1977). A concentration of 0.039 mg/L
reduced reproduction of Champia parvula gametophytes; no effect was observed
at 0.005 mg/L (Thursby 1986). Tetrasporophytes of C. parvula exposed to
0.005 to 0.026 mg/L for 14 days reproduced less but grew faster; no effect
was observed at 0.003 mg/L.
17
OTHER DATA
A number of researchers have studied the effects of ammonia under test
conditions that differed from those applicable to acute and chronic test
requirements as specified in the Guidelines (Table 4). Animals studied
included rotifers, nemertine worms, echinoderms, mollusks, arthopods,
polychraetes, and fishes. Concentra t ions af fect ing the species tes ted are
generally greater than than Final Acute Value and are all greater than the
Final Chronic Value.
Among the lower invertebrates, Brown (1974) found the time to 50 percent
mortality of the nemertine worm, Cerebratulus fuscus, exposed to 2.3 mg NH3/L
is 106 minutes. In the rotifer, Brachionus plicatilis, the 24-hr LC50 is 20.9
mg NH3/L, the net reproduction rate was reduced 50 percent by 9.6 mg/L, and
the intrinsic rate of population increase was reduced 50 percent by 16.2
mg/L (Yu and Hirayama 1986).
In tes ts wi th mollusks , the ra te of removal of a lgae (Isochryris
galbana) from suspension (filtration rate) was reduced > 50% during a 20-hr
exposure to 0.16 and 0.32 mg NH3/L in juvenile and adult quahog clan
(Mercenaria mercenaria) and to 0.08 mg/L in juvenile eastern oysters
(Crassostrea virginica) (Epifanio and Srna 1975) . The ra te of c i l iary beat ing
in the mussel , Myt i lus edul is , is reduced from 50 percent to complete
inhibition in < 1 hour by 0.097 to 0.12 mg/L (Anderson et al. 1978).
Excretion of ammonia is inhibited in channeled whelk (Busycon
canaliculatum), common rangia (Rangia cuneata), and a nereid worm (Nereis
succinea) exposed to sublethal concentrations of 0.37, 0.85 and 2.7 mg/L,
respectively (Mangum et al. 1978). The authors conclude that ammonia crosses
the excre tory epi thel ium in the ionized form, ad tha t process i s l inked to
18
Na+ and K+ ATPases. In the common bloodworm (Glycera dibrachiata), Sousa et
al. (1977) found no competition exists between NH3 and oxygen in binding
hemoglobin.
Ammonium chloride (about 0.01 mg NH3/L) exposure of unfertilized eggs
of the sea urchins, Lytechinus pictus, Strongylocentrotus purpuratus, and S.
drobachiens is increased the amount and ra te of re lease of “fer t i l iza t ion
acid” above that occurring post-insemination (Johnson et al. 1976; Paul et
al. 1976). Exposure of unfertilized sea urchin (L. pictus) eggs to NH4Cl
resul ted in s t imulat ion of the in i t ia l ra te of prote in synthes is , an event
that normal ly fol low fer t i l iza t ion (Winkler and Grainger 1978) . Act ivat ion
of unfertilized L. pictus eggs by NH4Cl exposure (ranging from 0.005 to 0.1
mg NH3/L was demonstrated by an increase in intracellular pH (Shen and
Steinhardt 1978; Steinhardt and Mazia 1973). Ammonia treatment activated
phosphorylation of thymidine and synthesis of histones in unfertilized eggs
of the sea urchin S. purpuratus (Nishioka 1976). Premature chromosome
condensation was induced by ammonia treatment of eggs of L. pictus and S.
purpuratus (Epel et al. 1974: Krystal and Poccia 1979; Wilt and Mazia 1974).
Ammonium chloride treatment (0.01 mg NH3/L) of S. purpuratus and S.
drobachienris fertilized eggs resulted in absence of normal calcium uptake
following insemination, but did not inhibit calcium uptake if ammonia
treatment preceded insemination (Paul and Johnston 1978).
In exposures of crustaceans, the 7-day LC50 is 0.666 mg NH3/L for the
copepod, Euclaanus elongatus, while 38 percent of the E. pileatus died after
7 days in 0.706 mg/L, (Venkataramiah et al. 1982). No sargassum shrimp
(Latreutes fucorum) died after 21 days in < 0.44 mg/L (Venkataramiah et al.
1982). The EC50 bared on reduction in growth of white shrimp (Penaeus
19
se t L f e rJ s J a6cPr - --. :-.:ee xee,qs :f px~sure :S 2, ‘2 x, L *dlcxer.s 13’5 . 2.e
erght&y X50 1s 1. ‘3 3-g/L f3c 9,~ XmierrcM !zcster ‘Hanurd anmr~canus 1
3elistraty et al. 1377). i;hen blue crabs iCallinec:es sapidusj iRte mved
from mter of 28 g/kg salinity to ater of 5 g/kg, a doublinq of ammonia
excretion rate 0ccJrred; addition of excess NH4Cl to the luu salinity water
inhibited ammnia excretion and decreased net acid output (MMqum et al.
1976). Wickins (1976) found that the timr to SO percent mrtality for the
prawn, ,tlacrobrachiuan rosenberqii, decreased from 1700 minutes at 1.7 mg/L to
560 minutes at 3.4 mqyL. In a six-ueek test with this prawn, growth was
ceduced 32 percent at 0.12 mq/t (Wickins 1976).
me relationship bemeen decrease in toxicity of un-ionized amnxlia with
increase in pH seen in 964our tests with the prawn (Nacrobrachim
cosenbergii) is also exhibited in data from tests lasting 24 a& 144 hours
(Table 4) (Armstrong et al. 1978). Prams wro three t-8 mre sensitive to
NH3 at pli 6.83 than at 7.6. Abuve pn 7.6, the decrease in acute toxicity was
not as great, declining only by a factor of 1.7 at pli 8.34. A similar effect
of low pH was seen with growth of the pram, which after seven days at pti
7.60 was reduced in 0.63 q/I, and at p&4 6.83 by 0.11 mcyt (Armstrong et al.
1970).
Few “other data” are available an the effects of ma on dtwator
fishes (Table 4). III three saltwater tarts lasting 24 hours, tha LCSOS for
chinook salma (Qltorhync)nrr tshawytscha) canqd fraa 1.1s to 2.19 mg W3/L
(Harider ad Allen 1963). The 24-h LCSOS frcn bm tests with Atlantic
salnun (S8lm tit) wr* 0.11s and 0.28 me/L (Alabaster et al. 1979). --
Mortality of the Atlantic silverside (Mnidia mnidia) MS higbr in 0.44
mg/L than the 43 pmcent control mortality in a 28day early life-stage test
20
21
UNUSED DATA
Studies conducted with species that are not resident to North America
were not used (Alderson 1979; Arizzi and Nicotra 1980; Brown and Currie 1973;
Brownell 1980; Chin 1976; Currie et al. 1973; Greenwood and Brown 1974;
Inamura 1951; Nicotra and Arizzi 1980; Oshima 1931; Reddy and Menon 1979;
Sadler 1981; Yamagata and Niwa 1982). Other data were not used because
exposure concentrations were not reported for un-ionized ammonia and/or data
on salinity, temperature, and pH necessary to calculate NH3 concentrations
were not available (Binstock and Lecar 1969; Linden et al. 1978; Oshima 1931;
Pinter and Provasoli 1963; Pruvasoli and McLaughlin 1963; Sigel et al. 1972;
Sousa et al. 1974; Thomas et al. 1980; Zgurvskaya and Kustenko 1968). Data
of Hall et al. (1978) were not used since the form of ammonia reported in the
results is not stated. Data were also not used if ammonia was a component of
an effluent (Miknea 1978; Natarojan 1970; Okaichi and Nishio 1976: Rosenberg
et al. 1967; Thomas et al. 1980: Ward et al. 1982). Data reported by
Sullivan and Ritacco (1985) were not used because the pH was highly variable
between treatments. Data from a report by Curtis et al. (1979) were not used
because the sa l t tes ted, ammonium f luor ide , n ight have dual toxic i ty . Data
reported by Katz and Pierro (1967) were not used because test exposure time
and salinity cited in the summary data table and appendix do not agree.
Results of a field study by Shilo and Shilo (1953, 1955) were not used since
the ammonia concentration was highly variable. The Ministry of Technology,
U.K. (1963) report was not used because the ammonia toxicity data were
previously publ ished e lsewhere and the re levant informat ion is c i ted in th is
document . References were not used i f they re la te more to ammonia
metabol ism in sa l twater species than to ammonia toxic i ty ; e .g . , Bar tberger
22
and Pierce, Jr. 1976; Cameron 1986; Girard and Payan 1980; Goldstein and
Forster 1961; Goldstein et al. 1964; Grollman 1929; Hays et al. 1977; McBean
et al. 1966; Nelson et al. 1977; Read 1971; Raguse-Degener et al. 1980;
Schooler et al. 1966; Wood 1958. Publications reporting the effects of
ammonia as a nutrient in stimulation of primary production were not used,
e.g., Byerrum and Benson (1975).
23
SUMMARY
All of the following concentrations are un-ionized ammonia (NH3) because
NH3, not the ammonium ion (NH4+), has been demonstrated to be the more toxic
form of ammonia. Data used in deriving the criteria are predominantly from
tests in which total ammonia concentrations were measured.
Data available on the acute toxicity of ammonia to 21 saltwater animals
in 18 genera showed LC50 concentrations ranging from 0.23 to 43 mg NH3/L.
me winter flounder, Pseudopleuronectes americanus, is the most sensitive
species, with a mean LC50 of 0.492 mg/L. The mean acute sensitivity of 88
percent of the species tes ted is wi thin a fac tor of ten of that for the
winter fluunder. Fisher and crustaceans are well represented among both the
more sensi t ive and more res is tant species ; mol lusks are general ly res is tant .
Water qual i ty , par t icular ly pH and temperature , but a lso sal ini ty ,
affects the propor t ion of un- ionized ammonia . With f reshwater species , the
r e l a t i o n s h i p b e t w e e n t h e t o x i c i t y o f u n - i o n i z e d a n d p H a n d
temperature is similar for most species and was used to derive pH and
temperature dependent f reshwater cr i ter ia for NH 3 . For sa l twater species ,
the avai lable data provide no evidence that temperature or sa l in i ty have a
major or consis tent inf luence on the toxic i ty of NH 3 . Hydrogen ion
concentration does increase toxicity of NH3 at pH below 7.5 in some, but not
a l l species tes ted; above pH 8, toxic i ty may increase , decrease , or be l i t t le
altered as pH increases, depending on species.
The chronic effects of ammonia have been evaluated in tests with two
sa l twa te r and t en f r e shwa te r spec i e s . I n a l i f e - cyc l e t e s t w i th a myr id ,
adverse effects were observed at 0.331 mg NH3/L but not at 0.163 mg/L. In an
ea r ly l i f e - s t age t e s t w i th i n l and s i l ve r r ib s , adve r se e f f ec t s we re obse rved
24
at 0.074 mg/L NH3 but not at 0.050 mg/L. Acute-chronic ratios are available
for 12 species and range from 1.4 to 53. Ratios for the four most sensitive
freshwater species, tested at pH values greater than 7.7, and for the two
saltwater species tested, range from 7.2 to 21.3.
Available data on the toxicity of un-ionized ammonia to plants suggests
significant effects may occur in benthic diatoms exposed to concentrations
only s l ight ly greater than those acutely le thal to sa l t -water animals .
Ammonia at concentrations slightly less than those chronically toxic to
animals my stimulate growth and reduce reproduction of a red macroalgal
species .
The key research needs that should be addressed in or&r to provide a
more complete assessment of toxicity of ammonia to saltwater species are:
(1) assess repor ted pH-toxic i ty re la t ionships and tes t o ther species by
conducting additional acute toxicity tests using flow-through techniques and
continuous pH control both with and without pH acclimation; (2) determine the
effects of water qual i ty var iables on acute-chronic ra t ios by conduct ing
L i fe -cyc l e and ea r ly l i f e s t age t e s t s w i th s a l twa te r spec i e s ; (3 ) i nves t iga t e
temperature inf luence by addi t ional acute toxic i ty tes ts wi th species that
can to lera te both low and high temperature extremes; (4) tes t the effects of
constant total ammonia exposure and cyclic water quality charger to mimic
p o t e n t i a l t i d a l a d d i a l s h i f t s i n s a l i n i t y a n d p H ; ( 5 ) t e s t t h e e f f e c t s o f
f luctuat ing and intermit tent exposures wi th a var ie ty of species ; and (6)
invest igate the tota l of other water qual i ty var iables on ammonia toxici ty:
e .g . , d issolved oxygen and chlor ine; and (7) invest igate the contr ibut ion of
NH4+ to the toxicity of aqueous ammonia solutions to better resolve how the
25
ammonia criterion should be expressed if pH dependence continued to be
demonstra ted .
2 6
NATIONAL CRITERIA
The procedures described in the “Guidelines for Deriving Numerical
National Water Quality Criteria for the Protection of Aquatic Organisms and
Their Uses” indicate that, except possibly where a locally important species
is very sensitive, saltwater aquatic organisms should not be affected
unacceptably if the four-day average concentration of un-ionized ammonia does
not exceed 0.035 mg/L more than once every three years on the average and if
the one-hour average concentration does not exceed 0.233 mg/L more than once
every three years on the average. Because sensitive saltwater animals appear
to have a narrow range of acute susceptibilities to ammonia, this criterion
till probably be as protective as intended only when the magnitudes and/or
durat ions of excurs ions are appropr ia te ly mal l .
Criteria concentrations based cm total ammonia for the pH range of 7.0
to 9.0, temperature range of 0 to 35°C, and salinities of 10, 20 and 30 g/kg
are provided in Text Tables 2 and 3. These values were calculated by
Hampson’s (1977) program of Whitfield’s (1974) model for hydrolysis of
ammonium ions in sea water.
Three years is the Agency's best scientific judgment of the average
amount of time aquatic ecosystem should be provided between excursions. The
abi l i ty of ecosystems to recover differ great ly .
S i t e - spec i f i c c r i t e r i a may be e s t ab l i shed i f adequa t e j u s t i f i c a t i on i s
p r o v i d e d . T h i s s i t e - s p e c i f i c c r i t e r i o n m a y i n c l u d e n o t o n l y s i t s - s p e c i f i c
criteria concentrations, and mixing zone considerations (U.S. EPA, 1983b),
but a lso s i te-specif ic durat ions of averaging per iods and s i te-specif ic
frequencies of allowed exceedances (U.S. EPA 1985b).
27
Use of criteria for developing water quality-based permit limits and
for des igning waste t rea tment faci l i t ies requires the se lect ion of an
appropriate wasteload allocation model. Dynamic models are preferred for the
appl icat ion of those cr i ter ia (U.S. EPA 1985b) . Limited data or o ther
considerations might make their use impractical, in which case one should
rely on a steady-state model (U.S. &PA 1986).
IMPLEMENTATION
Water quality standards for ammonia developed from then criteria should
specify use of environmental monitoring methods which are comparable to the
analyt ical methods employed to generate the toxic i ty data base . Tota l
ammonia may be measured using an automated idophenol blue method, such as
described by Technicon Industrial System (1973) or U.S. EPA (1979) method
350.1. Un-ionized ammonia concentrations should be calculated during the
dissociation model of Whitfield (1974) as programmed by Hampson (1977). This
program was used to calculate most of the un-ionized values for saltwater
organisms listed in Table 1 and 2 of this document. Accurate measurement of
sample pH is crucial in the calculation of the un-ionized ammonia fraction.
The following equipment and procedures were used by EPA in the ammonia
toxicity studies to enhance the precision of pH measurements in salt water.
The pH meter reported two decimal places. A Ross electrode with ceramic
junction was used due to its rapid response time; an automatic temperature
compensation probe provided temperature correction. Note that the
responsiveness of a new electrode may be enhanced by holding it in sea water
for several days pr ior to use . Two Nat ional Bureau of Standards buffer
so lu t i ons fo r c a l i b r a t i on p r e f e r r ed fo r t he i r s t ab i l i t y we re (1 ) po t a s s ium
28
hydrogen phthalate (pH 4.00) and (2) disodium hydrogen phosphate (pH 7.4).
For overnight or weekend storage, the electrode was held in salt water,
l e av ing t he f i l l ho l e open . Fo r da i l y u se , t he ou t e r ha l f - ce l l was f i l l ed
with e lec t ro lyte to the f i l l hole and the e lec t rode checked for s tabi l i ty .
The electrode pair MS calibrated once daily prior to measuring pH of
samples; it was never recalibrated during a series of measurements.
Following calibration, the electrode was soaked in sea water, of salinity
similar to the sample, for at least 15 minutes to achieve chemical
equilibrium and a steady state junction potential. When measuring pH, the
sample was initially gently agitated or stirred to assure good mixing at the
elec t rode t ip , but wi thout ent ra in ing a i r bubbles in the sample . S t i r r ing
was stopped to read the meter. The electrode was allowed to equilibrate so
the change in meter reading was less than 0.02 pH unit/minute before
recording. Following each measurement, the electrode was rinsed with sea
water and placed in fresh sea water for the temporary storage between
measurements. Additional suggestions to improve precision of saltwater pH
measurements may be found in Zirno (1975), Grasshoff (1983), and Butler et
a l . ( 1985 ) .
29
E!! Salinity - 10 q/kg
7.0 7.2 7.4 7.6 7.8 a.0 a.2
i:: a.8 9.0
270 17s 110
69
ii 18
if3 4.6 2.9
191 121
77
:: 19 12
2; 3.3 2.1
131 92 62 83 52 :s ii
:: 23 16 1s
f's 9.4 ii04
5:4 5.8 4:2
3.5 2; 2.7
2.3 1.7 :*: 1.5 1.1 ohs
Salinity - 20 g/kg
7.0 7.2 7.4 7.6 7.8 a.0 a.2 a.4 8.6 a.8 9.0
291 183 116
73
:8 19 12 7.5
i::
200 12s
79 so
:; ld
5::
:::
137 87 ix
64
54 :3
2 :: 17 1s
i'9 9.8 :t7
S:6 6.2
:*i
::: t:; 1:9 1.7
1.6 1.2 ii::7
Salinity - 30 g/kg
7.0 7.2 7.4 7.6 7.8
:*i a:4
ii*: 9:o
312 196 12s
79 50 31 20
12.7 8.1 5.2 3.3
208 13s
8s 54
if
it'7 S:6
::;
148 102 71 94 64 S8
:: :"s
:: 21
16 1s 10 if3
::"o 6.7 4.2 :-ii
::i 2.7 2:o 1.8 1.3
1.7 1.2 0.94
44 27 17 11 7.1
::i
:*i 0:92 0.67
f d 18
PS 4:8
::ii
K4 0.69
29 19 12
2;
2: 1.4 0.98 0.71 0.52
:i 12
24
:*: 1:s 1.0 0.73 o.s4
::
i35 s:4 3.5 2.3 1.6
i!AS 0156
21 13 a.3 5.6 3.5
:::
o’% 0:56 0.44
21 14 a.7 5.6 3.5 2.3 1.5 l.L 0 .77 0.56 0.44
23 1s 9.4 6.0 3.7 2.5 1.7 1.1 0.81 0.58 0.36
30
pH 7.0 7.2 7.4 7.5
zi 012 0.4 8.6
9"::
7.0 7.2 7.4 7.6
2: a.2 8.4 8.6 8.8 9.0
7.0 7.2 7.4 7.6
87:: 8.2 8.4
:I: 9.0
41 29 26 18 17 12 10 7.2 6.6 4.7 4.1 2.9 2.7 1.8 1.7 1.2 1.1 0.75 0.69 0.50 0.44 0.31
if 18 11 6.9
X 1.8 1.1 0.72. 0.47
47 29
:s 7.5
PO' 1:9
k:8 0.50
30
if 7.5 4.7 3.0
:*s 0:7e 0.50 0.34
2
::1
3::
f-f ohs 0.53 0.34
Salinity - 10
20 12
2:
::i 1.3 0.81 0.53 0.34 0.23
F7 5.3 3.4
:::o 0.07 0.56 0.37 0.25 0.17
Salinity - 20 g/kg
21
ii'1 5.3
::: 1.3 0.84 0.56 0.37 0.24
14 9.0 5.6
i*: 1:s 0.94 0.59 0.41 0.26 0.18
Salinity - 30 g/kg
22
i!7 S.6
2: 1.4 0.90 0.59 0.37 0.26
1s 9.7 5.9
:*: 1:6
:::2 0.41 0.27 0.19
g/kg
;:; 1-i 1:s 0.97 0.62 0.41 0.27 0.18 0.13
i:;
:*; 1:6
t.606 0:44 0.20 0.19 0.13
11 6.6 4.1 3.1 1.7
ii*:9 a:44 0.30 0.20 0.14
6.6
2; 1.7
ki9 0.44 0.29 0.20 0.14 0.10
6.6
::: 1.7
;::2 0.47 0.30 0.20 0.14 0.10
7.2
4:;
:*; 0:75 0.50 0.31 0.22 0.15 0.11
xl 1.8 1.2 0.75 0.47 0.31 0.21 0.15 0.11 0.08
4.7 3.0
:*i 0178 0.50 0.31 0.22 0.15 0.11 0.08
5.0
:-; 113 0.81 0.53 0.34 0.23 0.16 0.11 0.08
3.1 2.0 1. 2 9.a4 0.53 0.34 0.23 0.15 (1.11 0.08 0.07
3.1 2.1 1.3 3.84 0.53 3.34 0.21 0.15 ,3 .?2 3.38 0.137
3.4 2.2 1.4 0.90 0.56 0.37 0.25 3 1 0::; 0.09 0.07
31
bdUl t
4)-bA ma
11-17 -1
10-11 mm
4.7-5.1 ma
bdult
bdul t
.a45 9
.a54 Q
Ibrve
lb-10 l rn
)uvoer 1.
l-5 deym Old
Char.
YY4Cl
YY4Cl
YY4C 1
YY4c.i
YY4CI
YYIC L
WY4Cl
IY4Cl
MY4CI
IY4CI
YY4CI
WbltCl
YYIC 1
Lc-‘5a 0‘ cc-50 gw tag/L MY-J)
-_--_-_--_ --- --
b 1 .a4
24-4,‘
c a .b-15
I.l-5..=
E 4.*-4.4
..d-
. .w=
B.SAb
c @.b14
b 1 .Ob
a.51
b 0.21
b a .4Q
J. 95
J JO- ) 96
J.lO- I. 94
J.lO- 0. II
J. -to- 4.21
b.2
4 a
8.01
4.01
1.92
4.1
J.OC
l.Sb
Imp ( cl ---_
20.2
20
20
20
20
20.5
20.1
21.4
22.4
JO. 4
19.)
21.2
19.4
S8l tg/kgt
---
9.1
a1
11
21
11
24
14
28
10
10
14.4
lb.0
14.6
32
Char
YYICl
YY4Cl
YY4Cl
YY4CI
WY4Cl
YYICL
rY4Cl
YY4Ci
YY4CI
UY4CA
UY4CL
UY4Cl
IY4Cl
UYICL
IY4Cl
8Y4CI
IY4Cl
I4et hods LC-50 or cc-50 py T*mp S*l (-q/L MY-b) ( cl lY/k9) - ___--__- ---_ -_ ---- ---
b 0.92
b 1.00
b 0.16
b I .Sl
b l.b(
0.2b
0.50
0.54
1.18
1.44
L .78
b.IS
2.0
2.0)
1.47
1.49
a. 94
1.91 19.4 11.7
J.92 19.4 1I.b
I.99
4.4b
I.92
b.O4- 1.12
*.I 4.9- 7.0
‘4: 7.2
7.7
l .r 7.4- 8.1
l .t 1.9- 0.0
7.0- 0.2
7.9- 0.1
‘).9- 0.1
1.7- 4.0
1.4- 8.1
7.4- 9.1
19.4 14.5
a1 .a lb.0
20.b 15.b
24 II
a5 31
a5 bl
25 10
24 I1
2b. 5 bO.5
a5
a5
as
I5
a5
as
10
a0
a0
bl
Jl
33
YYdCl
YY4Cl
lY4Cl
IYICl
YYICl
lY4Cl
IY4CI
Ill4Cl
UYICI
IIYICl
lY4Cl
IY4CI
WI4Cl
IM4Cl
lY4Cl
BY4Cl
l u4c1
lY4Cl
J.41
a.92
a. lb
E a.86
d a.06
9 b.10
..95O
d
L1lC
L.9c
A.‘.=
C
1.1
2.75=
5.‘IC
c 4.15
I .as
1.1s
0. t
J 9- 1.a
*et 9 o- 9.a
4. J: 9.9
0.1 4.4- 9.4
4.2
4 .a- (.a
4.41
l.b@
0. J4
9.1
l-50- I.75
‘).95- ‘).9b
9.9J- I.94
2.85- 7.97
O.OL- 0.1)
Cl@- 4.24
8.08
4.14
15
24
a5
as
19.1
10.0
aa
a4
aa
II .9
a3
a1
a)
I5
I5
15
ai .o
1a 0
---
10
11.5
11
JO
JO. I
a5
ia
Ia
11
JJ.4
-11
-14
-84
-11
-14
-34
10
10
--_--_-
Slrrpbd l ullbt, Muqlb C.~h~lU~
Plbaohobd Irl.:~~h, roaocbathur hbrpbdub
Plbaobobd I~lotr~L, loaocamthus htrptdua
Imd dsua. sc1~oropr oc~llalua
Allbrt,C srlv.rmbdo. pbnrdbb l aaidtr
AllantIC S1~v.1S1d.. Otoardra l mrrdrb
Allbrtlc bb~raSbbd4. aerrdra l errdra
AtlAmtlC 611v.r~14., Noa1dia araidra
rtlentrc l 1Lvormrdo. roardra l mrrdra
Atlaatrc l rlvarrrde. taoradl~ roa1dra
&tlamtrc srluerarda. ttOBi41~ l ~aldaa
Atlbntlc 6rlvorsrd.. tteardib l mmrdr,
All~atrC b~lv~r~1d*. ta.a~dta a.abdia
AllAatrC l rlvor*rd=. aeardba l oardr~
Allbat1C l IlV.#Sld.. nmardb. l *ardba
In&&ad tirlvrrb1d.. n.rrdrr b*ryllIafi
L&I. stay. 0‘ .L‘.
-__--_----
10.0 q
0.1 9
6.4 9
)Muaar lo
)UV.81 A.
~ur*r11.
)UYaall*
Juvon1lo
)uv.m11.
]uvanr lo
)uv.allo
)urmarl.
11.5 aa
YHbCl 5.H
YY4Cl 5.n
YY4Cl 0.n
YY4Cl 5.n
tun4baso4 S.M
IY4Cl
UY4CA
YY4Cl
IY4Cl
WlICl
YYICl
IY4Cl
YYICA
YY4CA
YU4Cl
YW4Cl
YU4Cl
5.n
5.H
5.1
s.Jt
5.n
+.I
S.I
rr,n
s.n
5.n
S.H
rt.n
LC-50 QC cc-54 yn tap/l. MY-I)
--_------ ---- --
1 .bJ
a. 14
O.bO
0.914
0.545=
b 0.14
b a.91
b 1. )a
b 1.a1
b 1 . 1e
b
b.91
b 1.24
b 1.05
b 1.0
b 1.21
0.94
1 .b4
J.99
a. 00
4.0)
I 01
a II- 4.a
1.9b
1.01
1.50
1.9b
1.9b
4.00
0.00
2.9a
a.5
4.94
6.1
l .t 4.9- 1.1
tory 4 c1 -_-_
Al 0
al. J
al.4
a1.4
a5-ar
10 9
I0.b
IO. 1
10.0
JO.1
14.0
a0.a
A4.4
al. 1
al. i
19.1
15.0
Sal I9/kY 1
---
10
10
a4
a4
10-10
4.5
10.4
10.1
9.0
9.1
9.1
10.2
9.9
10.2
10. i
19 I
11
3s
Ch9rn
nntc I
Yll4Cl
YYIC I
YH4Cl
YY4Cl
YYlCA
YY4CI
lY4Cl
YYICI
YY4Cl
WYIC L
YY4CI
IIY4CA
YYICA
YU4Cl
Yt44Cl
YY4CI
YIl4l.l
LC-50 or cc-50 y"
tnq/l- III-J) t*ry I El
15.5
15 5
16.5
IS .o
14
II
>b
15.5
14.5
11.5
25
A4
1b
Ab. 5
IO. J
14.6
1Q. 6
14 .a
1Y 5 Pouch-a IYIL
JO
Jl Pouch-r lY4b
JO. 5 Poucbmt l99b
IS rouctbr1 19tr
JO. 5 l ouchrti LYbb
JJ roucher 19tr
I1 .o Poucber l91b
JO Puucbar lY4b
JJ .5
9.a
I9
IO. 4
IU 4
roucb.1 IYIb
CA cnq IPLL
CA faq IYIb
CA cnq l98b
CA cay IYIb
36
chmr
YHICI
IlH4CJ
YU4CJ
YlI4CJ
nn4cI
nu4cb
UY4Cl
w4ci
nn4cl
YI4Cl
UY4CJ
YY4CI
YlIIC&
YY4CA
nlI4c1
YY4CJ
I4olhuJs
--- -_-
rt,fl
rt.n
rt.n
S.M
S.M
f.(l
S,M
s.n
1.1
rt.n
s.n
rt.n
S.M
0.M
S.fI
5.N
l-c-50 0, cc-50 y* rrnp Irq/L NM-J) t Cl
_--__-_______ __ ----
2.79
1.5
1. JO
c I .ba
E 1.25
‘ 1 .bS
c I .o
c a. 15
E 1.4
O.JJ
I .o*
0.10
b 0.91
J.lJ
b 1.04
..I 1 b- J.9
l .t I b- 7.9
..I a.o- a.1
7 5b- ? bl
1.59- I. 72
J. bO- l.Jl
1 .Ob- a.11
a Ob- b.12
&04- 4.14
l .I J. lo- l.JJ
. 1.4- J.1
l .t J a-
1.b
.
7.15-
1.45
25
11.5
JJ
15
ZJ
15
15
ZJ
II .5
JO. 5
10
IL
10 4
JO
J2
11.5
‘11
‘11
‘11
-11
‘J4
‘J4
5
5
5
5
JO.2
14
Y b
37
L&I. Slry* 8‘ b,..
._-- __-_ --
JaIV* 1 day old
YU4CL
larva 1 day old
YY4CJ
larva WY4CJ
luoltlodr
s.n
5.n
S.N
LC-50 oc EC-50 &I” tarp lnq/L MY-J) 4 Cl
--- -----_ --_- __ ----
a.5) I Y- J 5 0.1
0.51 I 9- 1 5 a.1
0.44 KS- J.5 a.1 l saudoplmuronoctea A day old
•*~rLC~DM~ __-------------------------- _---- -----L-____-__---_-_------------------------------
Jl
II
II
-_-_--_
CArdrIb IYIb
------ - ----_ - _._.
38
5y.c I*K -------
. Nathad RM ------ --
LC
Lc
LC
LC
CIA
ELS
CLS
LC
ELS
CLS
LLS
LC
LC
CLS
l.O- 1.5
9.09
1.6
l.bl- b-lb
b.l- b.9
b. B- b.5
1.4
J.bI- 1.11
I.(- l.b
1.4- 1.b
(.I- I.5
1.01
1.99
7.b)- 1.1)
rYcstlY*Tcll SPCCIES
0.199-0.0411 0. JO4
0.)14-O.li5 0.521
14.2 0.5J-O.lb 0.6)
17.b- 20.0
4
0.94-l .4 1.2
0.4024-0.004 0.00~1
4 0.0012-0.0024 0.0011
14.5 0.010-0.025 O.Olb
9.) 0.0111-0.04J9 0.0311
IO- 11
lo- 12
II
o.ob-o.Aa 0.045
o.oaa-0.01 0 .Ol
14.0 0.011-0.111 0.11
14.2 O.OOI-O.Ibl
21.1- 2b. J
0.15-O. 14
0.1)
0.21
39
. nbtbud
ILLS
ELI
6U
maa
CL1
LLS
ELI
LLS
LC
CLS
01
_- ,I
1 b- 7.0
I. J4- 1.95
1.9
I.74
b.bb
I.25
1.8)
6.bI
7. I- O..
7.9- b.0
L1m1ra Chtunrc value (*g/L IYJ) tag/L IYJ)
---- ._____ ------_-. ._--
0.OlJ-0.146 0.10)
O.lJ-O.A4 0.18
0.11-4.49 O.JJ
0.0&J-O.LJ4 0.092L
..OJ4J-0.055. 4.0417
O.IAO-0.161 0.144
0.412-0.7bO 0.599
0.431-O.bb5 O.bAA
15-27 30 O.l6J-O.Jll
1J.5- IO- 0.050-0.074 a5.0 11.5
0.111
0.011 Pouchbr IYIb
*cut.-Cbromrc l &tro
40
*cut0 V*lu.
lrn9/L WWJJ
4 .b
0 094
0.090 Q.OOJl
a.411 0.0111
0. IS O.Olb
1.54 0.11
2.5L
I .I5
1.41 4.101 15
A.Sr,
a.12
I. 58
1.05
I .Q1
0.11
I. 14
4.0011
0.11
0.11
to.25
b.2.J
a.11
0.11
0 .a914
O.Q4Jl
0.148
4-14
1.5
0.4
b 1
I2
19
1 7
SraJlroutb bar+. nrcroptorur dolorceu&
J JO
1 11 Q-b11
tar ialbrd l rluor~rde . 21.1 _-____----____-_-_-_--------------------------------------------------------------------------------
G2
a.nL* ----
IO
LJ
lb
41
14
11
11
II
10
0.619
21 Jb
7 lC
4 0. 171
J 0. JJA 0.11)
1 0.545 Ied drum, 8cIaooop* ocollatu~
a. 545
L
------------------------------------------------------------------------------------------
sp*c1.1 ChoOIcal
--------
01at0.. Aopblprora pdludo6a
_-____--
YY4Cl
JUdCl
oIAtoO,
Iavrcula .(.O.‘L. UtcJ
014t00, Uav~cula cryptoc.pbAlA
IJl4CJ
uI4CJ
0L~10.. rItrAchIa cloatarIum
ol~too.
Irtrrcbca dtsarpata
Ot4too. (Iltaacb&a dubrtormra
01at00, Irtracbra w
04~too. Staurooara coostrtcta
YY4Cl
IY4Cl
YYICl
UY4Cl
YY4Cl
UY4Cl
rm4c1
Botrc~r, Brrcbronur plrc~tll~~
rotrr.r,
9racbiroaun plIcetIlI*
n0t1t.r.
Iracbloaus PlIC~tIl~~
IY4C 1
IY4Cl I.5
YY4Cl I.1
IIYIYOJ 7 9
Tab10 4
PM t*oprr~tur. Sdlrnrty 1 C) (q/k91
-- ------_---- -_-_-_--
0.0
8.0
0.0
a.0
0.0
6.0
0.0
I.6
1.0
6.0
7.9-7.9
7.8-J.)
12
II
11
11
12
11
II
12
11
11
II-24
11-14
11
21
1J
IS
11. J
15.0
11.7
15.0
15.0
11.7
11. J
11.1
15.0
11.7
JO
J-10 d&ya 4bt IaductIon in
cblocopbyll . 0.20
J-14 dayr bbt reductroa Ia
chlorogbyll . 0.241
J-10 dayr 15I raductIoa in
chlorophyll . 0.241
J-10 dayr bJb roductloa In
cbloropbyll . 1 .OlI
J-14 daya 149 roductrocr in
cbloropbyll . I .lJ4
J-10 daya lJ\ caductiom em
cbloro~byl1 . I .2J4
J-10 d&ys bib roductroa in
cbloropbyll . 0.14 J
J-IO day6 JJ\ raductroa In
cbloropbyll .
0.141
J-10 dayr bbb raductloa III
cbloro@bylJ .
0.141
J-10 deya 114 roductlon ~a
cbloroghyll a
0.241
4a bouca r sduced
roproductrom,
.O l ttoct at 0.005
O.OJ9
14 d&y* reduced
reproductaon L
atr.ulat.d qrortb no .croct at 9.001
o.oos-
0.01b
14 bourr LCSO
504 r*4uctroa In
popul~t,oa 9rorth
509 roductrun II)
not productron
Iate
.
10.9
. II. 1
. 9.b
101 OII)~ LTSO 1.1
Fraua.
llbcrebracbtur roeorborqrr
Prawn,
aacrobtachlum rosonborgrl
yI4Cl
YYICl
IU4Cl
UU4Cl
YYICI
rY4Cl
IYICJ
JWICJ
YY4CJ
MYICI
WICI
YYICJ
YYICJ
wwac1
b.aJ
b.4)
I. LO
l.bO
8.14
( 14
SAllnrty
l9/hqJ .--___-_
J4
J4
J4
10
J4
J
la- 14
J
1
1
.5-4
IA
IA
11
11
Jl
12
24 *our*
144 hour9
14 boura
LCSO
LT50
EC50
LTSO
LT5O
LT50
JOI-4OI
qroutb reductiar
LC50
LC5Q
u5a
LCSO
LCSO
LCSO
0. bbb
J 1
.
0.11
.
1.1
l
1. I
.
J.4
.
0.1)
0 bb
0.1A
1. LO
0 .a0
J.54
1 I5
46
_-----_-
WY*Cl
WYICL
(IY4CI
W4CI
IY4CI
rw4c1
*I4CL
IIY4CI
UYICI
(IYOCI
UY4Cl
IY4CL
WYICA
WlICl
UY4CL
l .0
4.4-9.2
0.15
4.A
1.49-1.51
7.59
b.95-l.lb
9.4-4.1
l.l-6.b
6.AS-0.55
1.95
1.92
0.1
Jb a
Jb 4
20 0
11.1
11 9
15.0
II.7
Ll.7
11.7
lJ.0
IA.0
1.J
LJ.0
15.0
11. J
Iq/kqJ --------
12 1 days
II 7 days
14
JJ.4
15
e
5.2
9.b
Lb.9
A7.b
10.)
le.2
18
_-_-_-
r*ductton Lab
qrouLb r&t.
raduct LOI) rn
qrowtb rat.
LC50
0 11
0 bl
LCO
LCSO b
L 19
IL50 a. 50
LC50 0 Jb
LCSO
LC50
LC50
LCW
LC5.
LC5@
LC50
0 bl
J. 19
1.1.
I I5
c 0 Jb
d 0 II5
0 II
. 0 951
lrq/LJ
knuraal, W. 1977. ~oltrance crf estuarinc Senthic diatoms to hiqh concentrations of ammma, mtrrte 13n, .wr. Bfol. 43(4) :307-315.
xtrate 13n and or~~0phosphatc.
Ahbaster. J.S., D.G. Shurkn, and G. Knowles. 1979. The effect of dissolved oxygen and salinity on the toxicity of wxmmia to snmlts of salmon, Salnm salar L. J. Fish Bid. 15:7OS-712, --
Alabaster, J.S. and R. Lloyd. 1980. Ammnia. Pages 85-102 in: Water Quality Criteria for Freshwater Fish. Semnd Ed. J. AL&stcr and R. Lloyd (Edr. 1, Buttemurth and Co. Ltd., Lmkn.
Alderson, R. 1979. TM effect of ammonia on the growth of juvenile Dover sole, Solea solea (L.1 and turbot Scophttulms maximus (L.). Aquaml ture Vi27 :231-309.
Anderson, K.B., R.L. Sparks, and A.A. Paparo. 1978. Rapid assessiwnt of water quality, usinq the fingernail clam, Husculium traruversm.
Rarourcrr Center, Lbiversity of Illfnois, ‘WRC Res. iep. Go. 133; Mater Urbana, IL: 11s p.
Arizzi, U. and A. Nicotra. 1980. Effects of mia activation in sea urchin l qgs. Ultrastructural ObSOMtiOM. Ultraaicrorcupy 5(3):401.
Annstrung, D.A., 0. Chippndale, A.W. might, and J.E. Colt. 1978. Interaction of ionized and m-ionized amwnia on short-term suwival and growth of prawn larvae, Uacrobrachius rosenberqii. Biol. Bull. 154(1):15-31.
Armstrong, D.A. 1979. Nitrogm toxicity to cmstacea and aspmts of its dynamics in culture system. Pagmr 329-360 in: Proc. Second Biennial Cmstacmn Health Workshop. D. ti ad J. Lecmg (EdS. 1, Texas A c PI Sea Grant, TAW-SG79-114.
Bartberqer, C.A. a& S.A. Pierce, Jr. 1976. Relationship ktwen aammia excretion rates arrj haolyaph nitrogwmus cqmunda of a euqhalina bivalve during low salinity acclimtion. Biol. 6u.U. lSO(l):l-14.
Bates, R.G. ad C.E. Culhrsm. 1977. Hydtogm ians and ti the-c state ot mtlno syrtm. Pa-8 45-63 in: The Fat* of ?osril e\lol CO in the Ocamm, N.R. arson and A. Hal&f (t5.1. PIWIt=, N-Y., N. . ?
Bates, R.G. UK! G.D. Plnchlng. 1949. Acidic dissociation constant of anmmium ion at 0 to 50.C d the barn strength of asmnia. J. Res. Nat. Bur. Stard.# 43419-430.
Becker, C.D. and T.O. That&et. 1973. -ia, amine8 and related compounds. Pages D.l-0.28 in: Toxicity of Pmmr Plant Cbmicah to
48
.kpxerc t:.fe. :m:ec! States Accmc c Lye ryy ~cxrmss~on, EatteiLe Jactfic Nort!!tt L.&orator:es, 31:5land, XA. XASH-i249.
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