microorganisms in a tropical lagoon

Relationships between fecal indicators and pathogenic
microorganisms in a tropical lagoon
in Rio de Janeiro, Brazil
A]e~dta
M. Gonzalez·
Marda s. Lutterbach
Hodolro Paranhos
•
Ab~trllet Rodrigo de Freilas Lagoon is an urban
eco~~~m
UJldergoing a~lcratcd
degradation,
therefore selected ~ a model for micruhiological
qU<llily studies of tropkallagoun~.
The aim of thi~
study wm; to evaluate tbe abumJaoGc': and the spatial distribution 01 leeal pollution indiC<:lttlrs and
pathogenic microorgani~ms. in the lagoon. lnf;' relationships between microbial gmups and abiotic
measurements were also determined to l,;valuate
tb~ inlluence of environmental conditioD!> on b~·
teria] di~t:rihution aDd to identil)' the capability
of coliform!i
Enterococcus to predict the occurrence of Vibrio. Staphylococcus aureus, and
Salmondla, Surface water liamplcs were collected
monthly, from December 1999 to October 2000.
Analyses were perfunned by traditional culture
teclmique~. A uniform spatial distrihutjon was ob~..yvcd for all bacterial groups. The fecal pollutlon
incJi~tors occurred in low abundances while P{l~
tentially pathogenic microorganisms were consistently found. Therefore, our study !iupported the
u..~c of counts of coliforms and Enterococnu to
indkate only recenl fecal contamination.
A. M. Gun"alef (~ . R. Paranhl)~
Oepa~Lamento de BiolDg;1\ Marinha,
IIl~tituto de BiolDgill,
Ulliversidade Foder~ldo Rio de Janeiro.
Predjo do CC'S. 611>\,:0A, !>ala A 1-071,
Udadc L;ni ver~i!aria,
Ilha do FumHio. Rio de Janeiro.
Rio de Jan~Lru. nrazil. eEl' 21944-lYlO
c-mllil: ~1(:~;[email protected],;tlTlI
Coastal ecos>~tems are frequently used ;l.i'> recreational and touristic area~ and for other economic
purposes (Costanza et aL 1997). Unfortunately,
pollutjon in the~c :)~tcms is widespread, and are<1~impacted by human Cl~Li•••ity may be severely
degraded. The~e ar~as normally lJlow high con~cntrations of pathogtms that may cause di:x:ascs
and oth\;t problems for human health. Environ·
mental cont~1111natioo associated with bacterial
proHferation has b~n descrjbed for many aquaLk cc.::osystems in the wodd (Kolm et aL 1997;
Trous!iellier ct al. 2004; Elm<lnama ct aL 2005).
Sanitary water conditions arc normally e"aluat~d
,.nu
M. S. Lutterbach
Lallorllt6rio d~Biow •.r~o e Hiodegradll~iiu,
Uio"jr.ao de Corro~aQ e lJegrada~ao,
lnslituto NII~iol1a1de TecnoJogia.
Avcnju~ VeT'leJ:uela. ~ala
614. Sao.de,
Rio de J"neim, Rio de hneiro, Brw,il, eEl' 20081· 310
Keywords Rodrigo de Fr~ita...•Lagoon. BrazilPollution indicators. SlaphytQwc;c~~aureus·
Vibrio. Salmonella
by fecal <':01ifOlID counts using
traditional
culture
t<;e;hlliques {APHA 199~). Coliform group h/l~ of·
ten been usw as an indicator of W/ltl;r suitability, partly because tbese mkroorg<1nisIIlS originatc
t:)(dusively from fccc~ (Hagler et at 1986). Coliforms show goud conelation with other pollution
inJi'.:'ltors (Pagnocca el aL 19'91) and can iudie,He;
recent environmental contamination.
AlltlllWgh they are used cxtemively, there is
a l;(]ntToversy regarding coliform counts (Satiha
,mu Helmer 1990). l'I1~~e microorganisms .survi\'e
poorly in marin~ (lnu chlorinated wat~r and are
strongly affected by solar raJi"lion (Solie and
K~tulovic 1992). Col!form~ (;aDnot be used tl-l
monitor
non fcC;:lI oonlaminatioo
(Araujo el (II.
1(1){)) or lC> indicate the presence or pathogens.
Th I;: n;:fore, <ll~ernativc microhiological indicators
have beenlJ.';cd for w,ll~rqua1ity monitoring, such
as neterotrophic bacteria (Kolm et a1. 1997), Hnferococcus (Evison lWl8), Staphylocoa:I4.'· aureus
(Araujo d at. 1990), Pseudom()nas. ae.rugino.~a
(Guim<ir~es et al. 194-.13), Vibrio (Watkins and.
<.:abelli 1985), SaJm(}n(~lt(J (BCludart ct aI. 2()()O),
Closr,Wtum p(~rfringens spores (White ~l al. 1993),
and YC::l~ts and [ungj (Hagler f.Jt at 1986). Ct)pr~l.anol, a sterol found in hwnan feces, ha.\ also
been &hown to he a good chemical indicator of
fecal pollution (hube et a1. 20(4).
A multiparametric
arrroal:h using count\ of
both coliforms and pathogenic microorg.misms
has hcl:n I)uggested for USe in sanitary evaluation programs {Hagler et at. 19~fi}. J low~ver,
in aquatic I;w~y~leIll5 in Bra7.iJ, few .studies using thb approac1l have hecn C<'lrriell out (Hagler
e;t aL. 1986; Araujo el al. ]Y91: Vieira et al. 20Ul;
Gonzalez et aL 2006). In such tropical ~nvironments. induding me Rodrigo d~ Freitas LagOOtl
(I{FL) in Rio de Jam:iro, there is no informalion about pathogcm at all. nle studied region
is cbaracterizl,;u b)' differences on pluviumetric
index along the year (EMBRAPA and IDAMA
1992). The highe!iot and lowest precipitiltion
levels
arc ob~t'rved, respeeti"'d)', in the rainy summe;r
(December to M.mh) and dry winter (July to
Septetnl'lr.:r) s.ea~ons. On average, th~ annual ralnfall in this area is estimal.Cd tlsl.075 mm of water
(EMBRAPA and IHAMA 1992).
RFL i~an important urban coa~tal ecosY6tem
USl;U for tourism, leL\urc, and water 6porK it ha~
7.2 km of pt.::rimeter, 4.3 III or ltWfctge dep(h,
2.5 x I (f' m" of total area,
6.5 x ]00 mJ 01
water volume (Torres ·199D). RFL l'CCeiWl; the
inlluence of three polluted rivers whost; Lolal and
fecal coliforms values rangl;~between 2.3 x lo-l
<lnd >1.6 x 106 most probable number (MPN)
100 mL -J {Lu~s and Cunha 2(07). The Macaco,
Cab~H. '.lIld Rainha rivers Ji!>Charges in the northwe~l region of the lagoon by the T.1bu;i Channel
(Brito and Lemos 1982) with a wlitcr flux of 0.03.
,mu
0.03, and 0.08 m3 S-I, rcspccLivcly.
The lagoon i~ undergoing acrelerakJ ul,:gra
dation. mainJy I,:au~ed by human [nl~rrerence
(Luttel'hach r.:l 'II. 2001). Garhagc, oil, aod domestit; ~t'wage, with no previous treatment. are
di~charged into it dHily. The high content 01 nulriellts and organi'.: matter, together with the 610".\'
rate of water renewal, all(lw~ bacteria to proliferate (Lutternlll:h el a1. 2001). The spalial distribution of the lotal and cuhivat.ed heterotrophic
bal.:lt:.ria and their re la tionsltip with tll ~ RFL
trophic stalll~ were recently reported (Gonzalez
et al. 2(06),
The aim of this stouy 'rViJ~ to determine tnl; occurrence, aoundanw, ,md distribution or tol<ll anu
fecal colHorm~, EmerococclJ..~, S. tlureus. Vibrio,
and Salmonella in RFL in order to contribute to a
helter understanding of lhis eC06ystem. Moreover,
the relation,~hip between these microbial groups
wa.<;also observed to evaJual(; huw effective fecal
indicators arc 10 prtldict the presence of other
pathogenic miCIoorgan[~m~_ The analyses were
perrorme.d by traditional culture methods L1~jng
t:nricbment broth ami agar medium. Thi~ 1>ludy
was performed in a Brazilian coar-;tal lagooll and
l'cporl~d what fecal indiclitm~ nr~ or not adequate
fQr predictIng th(; prt:stlnce of pathogens,
A sillgk waler samr1c from ~urface (0.5 m) was
coUected monlhly (December 1994;l to October
2000) from ea(;h of the five diJfcrent area& of
RilL (Fig. 1: Lutterbacl1 c.t ••I. 2001). The Rehc}U~s Tunnel statkm (Stl) is locatcd farth~sl
from the lagoon entrance and rceci ••.~~ uDl.Ieated
••..• ~
••.•
, ••••• J:' ••••.
,e. J:.~
_-
Rcooucas Tunnel (5tl),
Pirnque hlllnd (St2).
C~nlrlll Ch~[m<:l{Sr3).
C~i~ra Jslntld {S.4). and
(''-aI001b\1 Curw (.~15)
Jardlm de
Alah
C!ln~1 ,
c1ande::;.line dome'>tie sew<Jge. Thi5 area has albo
poor water renewal, and storm drains are present.
The Pir(;lqu~ hilaml slaLion (SI2) li~:sin the norlh·
we::;.lpart '.>fthe lagoon and receives the discharges
of thre e rivers. Tbe Central Channel station (Sn)
is located in the main Ia.goon channel, an area of
~Uer wah:rdn;l1lation. The <.:ai.,:ara l~la1JJ poinl
(St4) ties near the entrance of tbe Jardim de Alab
Canal, whieh cOtlncds the RFL to the Atlantic
O~an. making water r~new[ll prns.sible (Torres
1990). The Calombo Curve site (St5) js situated
in the soulhc~sl an:a. clo~e to lb~ JarJim de Alah
Canal, where unauthorized wa6tes are discharged.
Samplc!> for physical and chemical measurements
were Qblailll:u wilh a 3-L V,m Dum boUle.
Sample6 for microbiological
aDalyses were directly coHeeled with 500 mL sterile polypropylene
bottles. All 6amples were preserved
the analyses wcn~ pert'<.lntll;J.
Abiotic
measurements
on ice until
were analyzed
by stan-
dard oceanographic methods (Strickland and
Parsons 1972). Watcr
tcmpcTatl1r~ wn~ m~w;u.red
in tbl: Held wilb <l graduate thermometer, Salinity and dissolved oxygen {DO) were determined,
by chJorinity and Winkler-azide methods, respectively. CblorophyU a determinations
were performed aflc.:r vacuum lIItTlllion «25 c.m or Hg).
The fillers (0.45 I-lffi Whatman GFfC) were extracted overnight
in 9{J% acetone at 4 C and
the readings done wilb a H ITACH I lJ·1tJ()O
{Hitachi High Technologies America Inc., USA}
Q
spectrophotometel'.
Suspcndl.:d parliculate matter
(SPM) W<:l~ Jl:Lerrnined by gravimetry on Mill.pore AIlI5 glass-fiber filtcr~. Inorganic nutTieols
were evaluated as it follow::;;,!mmoniacal nitrogen
hy indophenol, nitrile by diazotalion, nitrate by
reduction in Cd-Cu column followed hy uia:lAllCllion, and orthophosphate
hy Te;acti,m with a~corbie acid. Water transparl:ncy was determioed with
a Seo.:hi disk.
Total ~n[j fecal coliforms were analyzed bj' the
IvlPN methoo, foUowing thc recomm<;nuations
of API fA (APHAI99~).
B<Jcterial growth was
f.k:t{,:nnlol:d on Brila F1uorocuH Broth (Merck
1.12587) at 36 ± )QC for 24 h. The nll;mbnmc
filtration techniqUl; (:sterile cellulose MillipOI'e
0.45 I-lm, 47 mm diameter) was used for detection of pathogens. Membrane~ [nr f:merQCOCCUS
detcrmintttion::; wure lmmferred to Petri dishe.~
wntaining t;;elective agar (Merck: I.052tl2) and incubated at 36 ± Joe Colony-forming uT1il~(cru)
CflUltb
Weft; pfo\rrllJmfo\llafter 48 h. Filters for
S. aurr.w analyses were placed on Vogcl-JnhnsnTl
medium with potassiLlm tellllTitc.;(ME::rck.1.05405)
added. Bl~~k wlonie:s with yellow haloes wen~
enumerated after 48 h of incuhatiOJl (it 36 ±
Pc. Vibrio SI)P. counts wcre m"dl: un thiosulfatr; citratt bile tiuCJotie agar (Merck 1.1026:\)
after growth at 36 ± PC for 4R h. 'l'h~ (11:;r;urreDCCof Salmonella wa~ omerved on RappaportVas:>iHadl~enrichment broth (Merck 1.07700; 4& h
at 35 ± r'C). The positive resu!t~ were coorjrm~d
jn Salmonella-..~higeJl~ medium (Mr;rck 1.07667;
~6 ± 1°(; l"ur4~ h).
All J<1la were log-transformed
and tested hy
nonparamctric
slathti(,:s {7.<:l' 1~~9). A Pearson
matrix ww; llSfo\dto determine the correlation~
between microbiological aDd environmental mC4isurements. Corre Lation~ wc.;n;(,:l)nsidcrcu sta til;tically significant when ~ ::;ignificance level of 95%
(p < 0,05) wa~ found. The relationsbjp between
aU variable/; was assessed by prindl)al compOlll;nt
analysi~ (L~gcndn: <lnd Ugl:ndre 1998).
N() (,;viJent /)patial differences were found on
physicai and chem.ical valu~s obtained In Rl'"L
(Table 1). Waler temperature was nearly l:on~wnt
in aU sampling statl0n& ranging [rom H~~C
(St4) to
3] 0(; (Sl2, St3, and St5; Fig. 2a). The low salinity
levels (5.22 S St4 to 9.85 S Sl:;~Fig. 2b) rdkctt:u
the cil'culation paUl;m~of the fo\cu~yslern,wbich
11>
(;haraclerized by great freshwater influence and
poor oceanic input~ ('l'nrre:> l(,ll)O).A:>the 1,lgOUn
is an enclo:>ed ec.osystt:rn, ills.br<lckj~h water can
he; <l .:omeq uence of the Macaco, Ca be.;a, and
Rainha. rivers [n!1ucncc over the reduceu tidal
circul at ion from ~bc ~hallow J ardim de Alah Canal
(Kl'l ill uf leogth, 9.8 m of widtb, and [),7D m of
depth), The continental lnHU(:Ilcr; I'.';iS .dso confirmed by SPM (16 mg L -1 St2 to 6t) mg L -l St1;
Fig. 2c) values. Although no remarkable diffcr~DceShad been ol"M>cl'vcdanllmg tht; fivl; 1jtaliullS,
th~ higbt;~t SPM (;On~ntralioDti were found iD the
irtut:rmosl areas oftbe lagoon, directly affected by
st mID gaUerjes and un trc atc d d3nd~,tin e u.(]m fo\~.
tic sewage (Lutterbaeh et a1. 20(1),
00 concentrations
varied in a broad range
(1.74 to 11.65 mL L-I) with tbl; m<1;\imum value/)
ol.:Cuning in the areas more directly affected by
Jardim de AJah Canal (Pig. 2d). The low vtllul;~
found in St)me sampling oQc;<l&ionsrelle.:ted the
gJ'C4itul.lmping ot organic matter that consumes
lh-: oxygen of the water during aerobic hacte1i<11 metaboljsm. Otherwise. the highe-,t kw!s of
DO oh~l;rv~tl in RFL may be attributed to the
imeo!ie phytopJankton activity promoted hy high
nutrient~ and light availability. 'lllrbJuily is anotnCT fal;lor th<lt significantly affects tIle phytopJankton production
(Cloern 19~7). In RI-'L,
watel' tran~parcncy nmg(,;J bctw~en 0.37 and
H! m, with the highest and lowest va luc~ being. respectively, found In Sl"i and Sl1 (daLa nut ~hOWD).
The high phytt.lplankton activity was indicated by
chlorophyll a values (1.65 ~g L -I St3 and St4 to
438.87 ~g L -I St3; Pig. 2c.;), which <:l1"('; lypical of
eutrophicatcd
cnviToomcn~ wilh limited water
dn;;ulatioo, Tbe high degree of organic poll ntion jn RFL was confirmed hy ammoniacal ni·
trogen (1. 15 IJ-M Sl~ to 55.!:H ~
St1; Fig. 3<1),
TlI~e 1 Aycras~ (X). standml.i dnialinll
(SO), Ilumocr of '\ample. (IV), Inillimum (min). and rn~1\imuCll (Tntlx) val~s of teOlpt=Tllwre, ~:lliniry, s\L~p~ndcd paT~i<,;ulare
matter. di~soJYCd o"ygt;n, chloTiJphyJJ Il, ammoniacal
nilrogcn. nitrite, nitra~,
orthoph(l.'jphate.
trtllll and fe~1l1 ooJifOTm~. t;wemi·(lccu.t, s. ml~.t.
Vibrio sp., Ilnd
S(JlmQ11f'i/a sp. nbtaincd jn Rodrigo de Freitas ug(lun
~t1, X ± SD (N)
Mir •...m.1X
St2, X
± SD
( N)
Mifl-max
Sn,X±SD(N)
Min-ma:l:
SL4. X :i
sn
(foI'}
$15. X ± Sf> (N)
Min-max
X ±SD
Sal (S)
SPM (mg L-1}
DO (mL L -I)
Chla{I'.~L-l)
26.24 ± 148 (ll)
19nH-3().OO
7 _\{l ± 1.5!'l (11)
39.78 ± 1l0H (Q)
21.00--66.00
6.:34 ± 2.2~ (II)
12~.99 ± 129.88 (t 1)
3.30--353.0&
5.34-9.54
7.12 ± L4I'> (11)
2605 ± 3.64 (ll)
lH.(JO-:l1.00
(IV)
Mi'l-ma:t
St2, X ± SIJ (N}
Min-rnax
6.58 ± 2.82 (l I)
2.4Q-l1.54
1W.W ± 132.37 (11)
]6.'i--438.87
u,()9 ± 3.63 (11 )
18,00- 30.{;()
705 ± 1 .45 (11 )
5.22-9.58
31.7S ± 10.8D (9)
17.(J(l-49.00
6.27 ± 21\6 (11)
1.74-11.54
Rn.70
26-01 ± 3.n (11)
·19.6Q...31.00
nH ± 1.46 (II)
527-9.1&
36.00 ± 14.44 (LJ)
HHIO ...58.00
7.13 ± 2.75 (11)
3.53-11.2{i
~. 75 ± 75.60 (11)
4.95-!97.9<I
~HJlJ\nt (~M)
NOZ (\J.M)
:>10.1 (14~)
pol
TC (MPN 100 mI.-I)
16.00 ±17.50
1.16-5581
1.17 ± 1.2!'l (11)
Q.16--4.24
2.86 ± 2.5~ (II)
0.29-S,M
1.<W± 0.96 (11)
4.26 x 103± 7.74 x 10:' (IO
04l-2.90
U6 ± 1.31 (1l)
O.0C}..4J6
2.47 ± 2.11 (111
0.52-6.:):)
9.00 x 101-2.40 x llr
1.79 x WJ± ~.:,)1l( 103 (HI
1.29 ± l:JQ (11)
2.50 ± B.1 (11)
0.06-4.5Q
0.60-·ILS2
0.31-4.84
1.42 ± 0.92 (11 j
O..15-J.3{)
U[J ± 153 (ll)
OJ (l-5.05
139 ± 1.5], (II)
2.00 ± 2.11 (11)
,
0.14-6.73
1.75 ± 137 (n)
0.18-425
2.5~ J: 1.06 (11)
0.48-9.11
1.66 ± 1.20 (H)
4.00 )( 10J-2.40 X l(}1
'1.41 'x llP.±: 14, )( 103 (10)
O.24-3.~K
.100 x ]01-4.60
Staphyim:l,Kcus (lU.r"u~·
(CFU 100 mL -J)
Vibrio (CFtJ 100 mL -I)
S~l1m(mr!lla (%)
7.77 x WI:t: 1,08 x 1fp2 (11)
54.~.'i ± 36.77 (11)
UOO-l00.o;)
1.71 x l(l2± 4.7'1 x 10}' (II)
1~2 x I04± 4.04 x 1(J~ (10)
1.00 x ]{j1-1.:lO l( UP
2.49 x lrtl± 4.2.'5 x l(f (10)
OJJ(l-·I.60
O.OO-l.I 0
lL6.1
±
(ll)
lUl2
(11)
12U-J9.J8
*
Min-max
Sl'i. X ±SD
Mjrt-max
UJ-37.04
JOO)
± 11.10
(11)
IOX~ ± 12 ..1fi (11)
141-41.05
O.I~S.03
.•
1)
Enluor:of.CUS
(CFLIOO
I
II
mL-1)
1.22)( 10J± 3.44)( 10] (10)
3.m x 10J -1.W)( HJ4
8.93 x W'± UiH x 102 (Il)
O.UO....6.40 l( Il}'!
SL2. X ± SO (N)
150 x 1~±
Min-max.
SkI, X ± Sf) (N)
3.00 x IOl-7.50 x 1O~'
1.1 Q x H}l ± 3.45 x 1(J] (10)
9.12 x W±
15.'i x 102 (II)
lJ.0/}....5.30 x IO~
5.42 x 1O! ± 7.fJ7 )( IOl (1'1)
Min-ma~
St4.
± SD (fly')
1.00 x HJl_1.10 x
X ± SD (.71,')
Min-1llaX
x
2.45
.>C
1~t2 (10)
m'
Min-mal(
5.64 x I(¥± 1.42 x W1 (10)
~.OO x lOI-4.60 x 10]
So, x
4.80 x 1(JI ± 3Jm x '101 (10)
± SD (N)
Min-Il'lll~
Tem" l~mpcrOltu~,
85.64 ± 79.90 (1'1)
3.~(l-219,43
(9)
IJ.l!4
13.08 (I I}
1.15....
4()J4
SlI,
252-11.65
39.22 ± lJ.4t
1 8.00-6l.00
Fe (MPN It):} rnlJ
II
2Jin-IO.28
6.0'i :;I-2.44 (II )
5.2Y-9.85
St1, X ± SD (N)
Mirl-max
St4, X ± SO ( fI,')
(N)
.~'22 ± l/iA'i (Q)
16.00--0 l.on
5.29-~52
7.10± 1.56 (11)
26J6±-3.59
(11)
19.1o--31.UU
Min-maJl
Stl,
TertiI' (0e)
3.00 x 10'-1.50
SaJ ~linily.
~itrll tc. l'()~ OIthoph(l~phate.
x 1{f
SPM suspocnded
TC wtal colifurm,
O.QO-2.30 x 1~
1.22 x ](j2± 8.92 x l!~ (1J)
0.00-3.00
x 1O~
4.23 x In!± 935
2,00 x lO....6.40)(
~rticulat~
x lOI {11}
Ilt2
matt~r,
Fe f~al coliform
no
0.00-3.10
x 1()l
>(
10'
2.81 "J02±
5Kl x 1()2 (11)
O.()I}....2.00 x 1(~1
2.56 x lU2±5.Q6 x lO~ (11)
n.00--2.00 x 10-1
2JN l( W± :1.82 x H~ (11)
fl.OO-2.00 xl O~
LoO
<I'M}
:t: 1.33 ( II )
1(
± 71S7
(11)
U'i5-20'U9
:3.0() x 101-1.I0
x 104
3.51 x loJ±73S
x lU3 (IC
3.00 x 101-2.40 )( lit
3.14 )( 103 J: 7.38 x W] (1(,
lOS
>< H~
59.09 ± 47.79 (11)
O.OO-WO.()(J
1.51 x l(f± 3.12 xl ()4 (10)
1.00 x H)1_1.00 x
S6.82 ± 33.71 (n)
0.00- ](Xl.!'.(I
UK)(
65.91 ± .17.54 (ll)
0.00-100.00
lo-~
1~±
1.'12 x 10" (lO)
5.m x 10C.6.nO x 1()4
9.&') x 1O'± 170 x 10~ (Hl)
0.00 ....5.10 x IW
diS{'\()'•.~d m::ygen. Chi a Cl1klIOphyll a, NHJ1NH1
59.()Ij ± :lCf.15 (1I)
25 .(Kl-I 00.00
!lmmol1Lat:~1 nitrosen.
NO;; nitrile, NO']
~=
H~ 2 T jTT't.'~erit~
b
di~tt,h ul,(Jj) of
temperature (II). saJinit)'
(b), suspended parli(;u llItc
mlltter (t), d i~ul Vl:;U
ox}'getl (d), and
chlofOJ'lhyll u (e) obUined
at'itl (-+-),SI2
10
C.··),
St3 (-.6.-), St4 (·x").
and St5 (-0-)
d 12
Fig. 3 Timc-5Cric~
diitTibu tion uf
<lmmuniQcaJ nitrogen (II).
nil rite (b), "'tfille (~), and
~OTtuph~lljrhate (II)
ohlai'led at St I (-+-),
St2 C· •.. ·), Sr3 l-~-),
St4 {... x"'J, and
a
b
t;()
6
... 4~
4
:;::l.
~
2
2~
Sl'i (-0-)
0
~~ ~ ~ ~ ~!s.. ~~ ~5 !
::.
.., ~ :!:•• <: ~ '"
..
c
..• ..•
'l~
<l!
:l5
c
~
~
"" ~ ""~ ""~ ~
!i'
],
10. ~
~ ~
~
"'
~ •.. ~ < :; ~
Q
fti~
r1. C
~
d {l
10
~
".
4
~:I.
~
;0.
2
2
U
~
~1~~i~~
-< ~ •••
i!~
Q ~
~ ::;
.:;
0
~ ee
~ ~ il
c 4
;.;.
•• ••l5 ••~
~~ c:r. •..
~ -< ~••
••1; ••
~ ~~~
..," ...•
.< J! :;
nitrite (0.06 f.lM 5t3 to 5.05 f.lM St4; Fig. 3b), ni·
~rate (0.14 ,..M St4 to 9.11 ~M St5: Fig, 3c), and
orthophosphatc (0.18 f.lM Sl4 10 4.84 f.lM S12;
Fig, ~d) level~. As a general pattern, jnurganic
nutrients wc~ predominantly higher in areas submitted 10 raw sewage inpuLs.
A dear sca~onal ratl~m was observed in the
RFL watcn) for the abiotk parameters,
with
lhe eXCl.-'}Jlion of DO, SPM, and ortopbosphate.
Thc highest temperat ures and lowest ~aIinitics
Were recorded in the summer season, wht:n
preciplt<llion ratio is higher (EMBRAPA
and
IDAMA 191)2).High~~t values of chlorophyll a
wcre also found in the rainy ~ummcr. These re~
suits can be explained hy incrca~~ in primal)'
produ<.:livity during summer seaSOn in rcsponse to
the more sunlight avail,lbihty nOJDlally oooerveu
at this time of the. year. Otherwise, the highc!>l
valu(;~ of ammoniacal nitrogen, nilrite, anu nitratc
w~re ob~rved in th~ wintcr months_ 'rhe highl.:-st
o~trient values observed uuring ~he dry season
can bi; a cons~4ueDce of the low~[ water dilution
iu RFL due to <I decrca!>e in pr~ipitation
Jevels
and runoff,
A uniform ~patial di~tributit)n was ob~crved for
bacterial data that were similar to water quality patterns. The highest avcrllge abundances
were predominantly t'ound in areas located fatthcr from lhe entrllnce of the lagt10n (Table 1).
Total llnd fecal coliform~ (Fig. 4a. b) vuried
from 3,0 x 101 MPN 100 mL-1 (St2, SL3, and
St'i) to 4.fl x 1O~ MPN 100 mL -I (stS) and
3,0 x ]()I MPK 100 mL -I {all stations) 10 1.1 x
an
]~ MPN 100 mL -J (Sll and ~t:l), resp~lively.
Ilig. 4 Ti m~-5Cries
di'lributtClTl of total
cotiform (a), rroil
colirl"lrm (b),
tnle:r(>Cocc.~\ ~p.(~), S,
(d), Vibrio ~p.(e),
and So/ttlQn~Ua
{f)
obtained ~t Stl (-+-l.
Sl2 (" •... ), St3 (-li-),
St4 { )(.,.), al'u.I
aUWH
St5 to.
sr,
~
i
l.\lE~
~
1MAo04
Ii!
!UMilJ
~
f~
f::;; IlIT•.•il2
1~I!.o:l
l.{JI!+O.1
0-)
l.Ot>+~3
"'..l \.5£+03
~
1,IIF•.•I1~
~
~
E
'":;!
lJ'Ill~
1.()t.:+Q.3
=i
~
5.01l-w2
s.
TJllJI~ 2 Pearson correlation> obtained batweell lnul and f~-';H.Iculiforms, t;rtl"n,,:ou:tI.~ ~p.,
ar~~e'us. Vibria 5pp., S{l!mom?J[u ~I)'>tnm,sparcncy, lempetaturl;:. Slliinit~"
di~~)lved Qxygen, alnmorlii!l<,:~1 llitro~cn, nitrite, nitrate, ortl\i)p"\.l~phBt<:. chlorophyll a, arid ,us!~ndl;:d partil;;u!.lltcmaner in lhe Rodrig(, ~IeFrdtas LagOOl1
TC
FC
EN
TC
FC
EN
LOI)
0.77'"
l.OO
0.02
SA
0.26
0.11
0,14
1.00
-0.07
SA
VB
SM
1.00
S1I.l
Transp
Ten1r
S~!
DO
NOJ
-o.n
0.25
-0.53*
-0.41'"
NHl
0.18
N02
-0.01
-0.30
-O.1.~*
0,04
-0.06
U.1!'l
-014
-0.01
Ollll*
-1),1e>
0.09
-0.03
-0.19*
-OJ4,.
0.13
-0.(,(,.
-0.36*
0.45"
-031
0,3&"
0,05
O,.3Y~
-0.14
0,58"
-0.%.
0.34"
0.'11
-0.38*
-f).5D,.
-0.18,
OJ7
U.01
L.(lO
0,12
018
0.14
-OJ5*
-0.02
--0.26
-OJ) .•
vn
0.:36*
'1.00
LOt)
Tran:;p
Tt'mp
-0.27
-0.30
1.00
S81
no
NI1,J
-0.17
-0.:14,.
0.10
0.50'"
-0.'14",
1.00
-OJj•.
-u,o~
-C),4Z",
O.46~
-0.19
1.00
0.30
-0.1l2",
U~~
N02
N01
PO~
C'hla
SPM
J'e tl1[1\l <,:.)lirorm. Fe fecal colifnfltl.
~Jinlt}'. uo dis'L)lv~~1 oxygen. NH)
'p < 0,0.5
O_~·
0.27
U,40*
-0.17
-0.40*
-O.ln
-o,n
IU2
0.22
-0.12
0.16
-0,48*
O.4J~
-O.la
O.42~
1.00
-0.3611'
1"04
-0.02
-0.20
0.3f'"
-0.07
-0.5R.*
Chla
-0,2(1
0,25
-0.81*
SPM
O.Otl
-0.0;
-0,[)4
0.1&
0.21
0,22
-0.29
O.:.'l7*
D.37'"
-C}.4(h
D.24
a.54'"
-0.49",
O.7P
-0.l3
-0.751'"
-0.17
(),86~
-0.0')
-0.29
LOO
-Cl.29
1.00
-{),23
-0.32'"
-0.18,.
0.07
O.33~
0,00
0,27
-0.20
0.10
1,00
F-.~rEmerococr.:lJ..~ ~p.,.\11 Strrplryh'w(;cus
{/~lIS, VB VilJrio ~pp,.SJf SaJmm.elltJ ~!~.,Tr(/IlSp lnmsparcncy, Temp lr;mJj(:ntturt',
nitrogm. NO~ nitrile, ,1't,'().l nilratc, PO~ ortllophL1~phak.
Chia chloroph)'11 '1. SI'M ~1J~Jj(:TlJ<:dparticulate maHer
alllllWl'lia~~r
O.4{)*
l.OO
511{
nfi!erococcu.s
counts rangea rrom a mmlffillffi
zero in Sl1, ~12, St3, and St4 to a maximum
6.4 x 102 CFU 100 mL -l in Stl (Fig. 44;).
01
of
PathogeDlc microorganisms were oom;~ientJy
observed in RFL waten. S. aweus was isolated
from 60% to M% of samples, in a range of
zero (all statiom) 10 2.0 x 10~ CFU 100 mL-J
(SI 3, S14. and St5; Fig, 4d). High indices of
Vibrio were obtained (88% to 1O()%). The higbest and lowest counts occurred> N!>peetively, at
oSt1 (1.3 x 1O~ eFl) 100 mL I) and St2 and St5
(zero: Fig. 4e). Salmonella were also isolated in
high pel'centages-70%
to 100% ()r~~mpl~s.This
bacterial group varied from zero (St1. St2, S8, and
$(4) LO 100% (all stations) in the water ~mrle&
collected {Fig, 4f}.
The highest abundancc~ or Lotal I:lllifoJDl, fecal
colilOlm, amI Vibrio were found in the rainy sumll1(;l' s.cawn cOl1Jirming Lhe contribution
of OOIllinl;t11c1l ~unolI to increase the microorganisms'
n umbers in tne RFL ecosystem, 0 espi Ie (l r this, 110
1iea.<;onal trend!\ were observed lor Enterococcus,
.\. aurelL), and Salmonella.
A P(;i:tIson matrix correlation was used to determine rhe relatjonsh ips octw~cn analyzed pa'
ramctcn and to verify tbe influence of abiotic
oonditions on RFL bacterial survivaL For eX.ampic, the inllu(;ln~ of !>eawater 00. enteric bacteria
Willi confirmed
by tbe negative correlations observed between total coliform and ~alinlL}' (r =
-0.53, P < 0.05) and fecal wliform and salinity
(,..= -0.36. p < 0.05: Table 2). The effect of sunligh I un RFL coliforms Wa5 also observed and
supported by the negative but l1onslgniJic.:<lllt oorrelations rOll"l.! bclwec;n total coliform and water
Iramsparenl:y and fectll coliform and water transparency. In this study, transparency "alllcHang~tl
from 0.37 10 2,8 nl while water samples were
ooUecred at 0.5 m depth. The negative wTTelalioDfi
ohscrved between /::,'ntcrococcus and temperature
(r = -0,66, P < 0.05) indicated the probable influence of temperall.lrc On Hn((!TVCOCCWi survival.
In addhion, cnlerie mi ••.
·worganisrns are faculta·
tiw <1naerobes and the negative effect!; of oxygen
on their cells was confirmed by the ••.
-orrclatiuns
found between total culiform (r = -0041, p-<
u,u5), fecal coliform (non~igniflcant), £merococ·
m~ (,..= -0.54, P < 0.05), and DO.
The discharge of potentially pathogenic microorganisms in l{FL hy dome~tic sewage inputs
wa.~ wpported by the positive and nonsignjf·
icanr correlations observed belween S. aureus
aDd indic"Il)T~ like lutul oolLtOIID, fecal coliform,
Salmonella sp., and ammoniacal nitrogen. The
high and constant occurrence of SCllmoneila ~p.
in the lagoon suggesl" the c)(ten~ive fecal con·
tamination in this ~o~ystem. corroborated
by
Ihe pusili ve correlations noted with EilIeroMCCu.\'
(1 = 0,6, P < 0.05), nitrite (nonsignilicanl), 'lOd
orthophosphate {r = 0,364. P < 0.05). Moreover,
positive but nonsignificant
correlations between
S, aureus, Vibrio spp., and Salmonella ~p. were
found with suspended p,jrLicul~~ matter.
The principal component analysis was applied
to the matrix (If <.:UTn:lation coeIfident between
15 \'(lrillble" and 11 observations to cOlTelate all
monthly collected data. The projection OJl the
f8£torial plan:\ 1-2 ~Kplained 48.89% uf the total dat~l varinbility (Fig. 5) and factors 1 and 2
corresponded, respectively, 27.91 % and W.~'X.
1.5·
lAI
i;lr
O,j
z
'"
""~
..
--,••
Q8
••
III
0.0
.3
~
•
I'
.f?
~
~lS
NO,
coo
..
<P~
"0
Cnl.
a
.l.()
.]3
.4),ii
·IS
o.~
WI
flartQrl: :1.91 'lli
Fj~!i Princ.ip<tlcomponent anatY'lls of 15 Y.lriable~ (para.
mele~~ ilTl~ly"~w)lInd 11 s!lmplc~ (observations) obtaincd
in RFL The gt'<lph ~hov •.~ lheir projoclion on factorial
plan~ 1-2. wit~ 4K~9% t;xplanation of data ~·ariability.
remp temrer.ature,
S~i saHuily, DO dis:;oI"t;lI 01lygcn, Chi
a chlorophyll a, ~'J'M suspendlold particulate m€l~t.er. NII~
lImrnonjacaJ
nitrogen,
N02 nitrile.
NOJ
IlilJ'aLl!,
ro~~IJT-
lhophusphatc. TC total coliform. PC fecal coliform, B!t~·
f()(:CH:m~·, S. u-ureus. Vibrio, !Ind Salnwmrra. Rainy mmrner
(0) .and dty winle:r (.)
Tllbl~ 3 Cines r .;()trelati Lln coefficients netWE:Cll vafL'
abl~ and factnrial axi8 ffClm principal oomp0[lcnt analysis
(n = J I)
Factors
VarLability
or explanation
Temperature
S~li"il)'
SII~pc;"YI;:d parti.:ulSle malter
DiSllol~'cd oKygcn
Cn]o,ophy Ila
AmmQnill(;1I1 nilrogen
1'i tritl:
l'iitrate
Orluph.)~phlllc;
T u till (;oliforTTl
Fcclil coliform
Efltf'rococcus sp.
.'i1Uph yl()~YI<t:u.1 fltl.tetd
Viluir'/8p.
SuJmQJI(d~:sp.
1
2
27.9\%
20.98%
O.11108J
-O.8&4610~
O.729802~
-0.3746.10·
-0.669766
-O.M-63g~·
-O.74~Y03·
(L7.1tiCJfJl ~
-O.2W4U6
(n'i7IfJ7~
O.6..'i579J~
0.474597~
0.4J331i5~
-O.J53369~
0.133413
-0.4474n8*
-05W096*
0.~1\99
-O.16ti171
O.&4t 14r;~
-O.1328M
O.7J'J914~
O,6M.'i88~
001 37874
a.Wall
0.672356"
0.471748"
(JJ~KJHO'I
-(}11!;l~29
(Ll1J.'7H7
Rcldtcll tu Fig . .'i
~p <: O.O~
of IhJ~ vanatIon.
The homogeneous
spatial
distribution and lh\; M':aJ)utllddjfh;reTlcc~ of biolic
and abiotic parameters in RFL were <.:onOrmcd.
The data obtained during the summer season were
distrihuled in the left region of the grapb. Samples
coHected in winter occurred predominantly at the
negative side of the axis 1. The linem correlation
ooelIicir;nl~ bi;tw~~n variahlcs and the factorial
plans are Ii/;ted in Table 3. Tcmp\;nmm:. ~alinit}',
SPM, chlorophyll {I, ammoniacal nitrogen. nitrite,
nitratt:., orthophosphate,
and Enterococcus were
significantly correlated wilh factM 1. Otherwise,
the factor 2 correlated significantly with salinity,
di~solvcd OX yg\;n , nitrogen ammoniacal, nitrite.
nitrate. total coliform. fecal cllliIoTTIl, S. (lure-us,
and Vibrio.
.lUlL is a highly clltrophicated
ecosystem dearlj-'
affected br drculation
POiItt:.Tn.<;
and domestic
sewage inputs (Gonzalez et aL 20(6). The hlgoon
is connL':cted to the sea by the Jardim de Alah
Canal, which is fn;4ucnLly lilkd by silt and alluvial
deposits. These conditions restrict the ocean water
influw and renew,ll of the lagoon's water, which
remains stagnated (Torres 1990). The relativel)'
long residence lime of the RFL waters, associated
with th~ high uVllilability of nutri.enl~ and organic
matter, favor th.e development of rni<.-Tuoil!l<.:ommuni ties and aft'eel the en vironmen tal sanitary
<.:onditions (Lldtr,;rbach Cl at 2001 ).
The relationship between nl"ltrien~ and bac~c·
rial growth was demonstrated in mel>ocosm experiments (Lebaron ct 1'1. l(99), which may be
compared to long-residence time environm~nh
(Troussellier et al. 2004). Beside of thlli. nontrc<HcU wa~lewatcr tliM.:biilrgc5il1crcasc the numbers and types of allochthonoU/; mi'-Toorg<lni~m"
in RFL. Although unable to grow in aquatic
L::e(Jsy~tems,these sewage-related microorganisms
CUll (;u[I,'ive in uutural walen:; depending
()n Ihe
environmental conditions (Diolli::>ioeL <11. 20(0).
In ~pite of its accelerated
eutrophication
pro~ss (Lullerbach et al. 2001; GUIlZale:l et aL
2(06), RFL coliform and Enrerococcm [lumber~
iippeared low. The <J;ita were nol in agreement
witl. previouf> studies in tbis tlreLl, wbich reported l~vcl~ of total and fecal colifol'n15 varying
from l.O x 10~ Lo ~.8 x 10~ MPN 100 mL-1
and
U.l x 10 to ].6 x lO>MPN 100 mL . I , n:l>pf;:ctiv~ly
(Scerctaria Municipal de Melo 'Ambiente 1998;
Lullerna<.:h ~t at 200l). However, it oowd be Ii
consequence of several biotic and abiotic interactions which acted distinctly and synergistically
on the ~urvival ()f RFL microorganisms along the
time.
Studies of regulation (Solie and Krstulovic
1992) hl1YCJ<.:mon~lrl1ted the inl)ueoce of seawater and :sunlight on ~oJiform llurvi~'"L Mitrinr,;
and brackish waters, such those of RFL. are toxic
to mo~t cnl.t;ric;;hactcri.ll. eliminating rapidly aJlochtonous microorganibms introduced inlo lhe
environment. Sunlight radiation affecls tb.e colilonn ~un ..iY'll promCJting cdlular die off (Fujioka
et aI. 1981) OJ bacterial damLlges which allow:s the
prodst predation (McCambridge and McMeekin
1981).
Death and inhibition of enteric bacterill by high
tempera.ture,<; have also beell reported (Pereira
und Akantura 1Y93; I:lrunl et lli. 19c;l7). Thcre~
fore, tb.e local wilter temperatures mnging from
1ROC to J l 0 c.: may explain the low occurrence
of Emerococcus
in RFL ~()Systcm.
Bcsides
this, phytoplankton growth is stimulated by higb
tcmpt'ratures (Ishizaka et a1. 1983). Tile intunse
phytoplanktonic activity in the lagoon was indicated hy thl: high chlorophyll a concentrations,
Algal metabolism con~e4uently increa~l:~ the DO
leveh which arc e()n~idered InatJl:quate for 1;01iform and linterococcU3 ~orviva1.
Although coliforms and Entemc(){;cus numbe r.!i
had been low in RFL. potentially pathogl;mic
microorgani~ms were conMstently found (cutoff
~){)jntof 1 eFU 10U mL -l). Simihlr results were
oln;erved in others aquatic environments in the
world (Dionisio ct aL 2000; Piancni et al 20M)
~ugge::;ting that anal~es of Ct)liformf> and f.'neer()cocCUS are nOl enou..gh to provide accur~jl.e information about water quality and to indicate
the prc~nce of nont"Cl;C,llorigin con wmina tion.
For cxample. S. aurcus ~ a natural inhabitant of
tile human skill which is wasbed off the body
surfa'X5 during rce.-'n'::lltionalbathing contarnin>uing the aquat!c \;OO,';ystems(Araujo et al. 1990).
S, aUlet./~' can also enter th~ aquatic eCOSY8temsvia
dome!ilic f>ewagc.
The waste input in RFL W1l5indicated by the
high counts of Salmonella and Vibrio, Although
Vibrio spp. arc autochthonou~ microorga[lism!i,
lheir growth j:; [Clvored hy high availahility of
nutrient~ (see positive oorreJation with ammoniacal nitrogen in Table 2), wttich can lead to the
dcvelopment of npportunistic pathogens (Pianetti
et al. 2004). Ca:ies of vibrioses related to environmental pollution have been reported in marine
(,X:U~)'l>tems (H~i el a1. 1998). Growth af Vibrio
~pp. is al~o r~vOIed by high water temperatures
(Tahle 2), It is interesting to note that human
pnthugenic ~peeies of Vibrio, such as Vibrio 'HA/ni}icus arc predominantly found in waters with
range!> of temp(;(alures similar to RFL (West
1989: Wrigtll el a1. 1996). Although we have
not foclL<o;cJour study ~() determine the different
speci~ uf Vibrio, thi~ kind ofrcluliom.hip poinled
.oul to the p~~jbJe presence o( human pathogenic
Vibrio in RFL waters.
Sewage inpl1l~ associated with rivers dischllrges
llml poor wa1t:r circulation I1l!>ooontrihutl;\ to increase thl; turbidity of the lagoon favoring the mi·
crohial uevelopmen\.. In this study. ~oncentralion!>
of SPM were devated 16 to 66 mg L-1• Tbese
panicles <illow the adsurption of microol'gani~m~ functioning <i~sites of intense heterotrophic
me ta bolism due to the pre~C"1;e of several ~.
~,eted degradative exoenzym~ (Azam and Long
2001).
The matrix correlation (Table 2) was lIllio used
to evaluate the rdCttionship betwc.;cn the microorganif>IDs and lo verify whether mkrohiological
indicatorb are sufficicTlt to predict th~ presence
of pClthogen~. In RFL, Vibrio and Saltnonell.a
were, respectively, bc~l.er predicted bJ total coliform~ and Enterococcus connts. Our data agree
wilh tbase of Efbtratiou ct al. (1998), who. working in the polluted aTl;\<JS
of tbe Saronikos GuLf
in Greece, obserwtl that coJifoTm bacteria Were
moderate and positively correillted to S, Ull.rew
and that the presence or Saimonelki wa~ better
predktcd by Entem,'()ccuS count.,. W<.::akcorrelaliot'ls between microbiological indicators and
pathogens have also bccn (ljpurted for utber
areas (Borrego et a1. 1987). Our T~UJtS demonstrated that bOlh coliform and Ente,ococcu~' cannot bc w;ed as sole indicators of the pa thogens
()C(urrence. This il>explalnahk by the modifications in microorganism relation!>hips with c~anges
in environmental pollutiun levels.. Despite their
low counts in the RFL, EnterQWCCUS were h~ltel 5uited to indicate fecal pollution than (;01·
iforms. Th i:) pattern h as been reported for otber
aq ua tic ecosystemSI ~ from waters frce or with
low cQncentratinm of coJiforms (Bruni et aL 1997;
Dionisio et ai, 2000). The issue whether colHorms
are able to predict the presencc of pathogens i~
~till discussed due to the frequently occurr\;nce
of pathogenic.: microorganism" in areas where the
fern indicators arc io luw numhen;,
Based on this, we recommend the use of 00liforms and Enterococcu,I' to detect only rec:ent
fecal contaminatioll.
Determinations
of path~)gt'nic microorganisms should always he used in
sanitary ~\',lluation prograrm to compkment coliform ilnd Enfe"'OCQccus counts. This is the first
study that U~9 both micrubiological indii;;utors
and potentially pathogenic micmnrganis!D5 to
e'Valuate a Brazi1i<Jn coastal l<lgtlOn. Hence, our
rt'~u1ts provided some insight~ 011 the RFL l;\oosystern. Hnwever, we support the need [or a continu~lu!>monitoting to determine the trend~ of
water quality of this iml,ort,mL coastal arc~, The
data pr~ented in thi:) ~tudy also COll tribute to a
be~t.er undcr~t •.mding of the correlations nt;tween
miLTt)biaJ indicators and pUleotially plllhogenic
microorganisms in a tropil.:<ll ecosystem.
Bruni, V., Maugeri, T. L.. & MOllli,elli, L (1997). Facc.:ll pOlltlliQn indicaLu~ in the Ttln'il. NU'r'll liay (R~5
Ackn,""ledl:~eDtll
We thanl: Dr. Jcanetc MilTon
Ramo~, Chan~-c:lLor of Salll<t Ursula \;l'Ii"'cn;ify for her
ill<:~nliv{;during lhi~ work. We (m grateful In ~hc Piraqili!
Cll.lb lor the 8Up~rt during tlll~ fleld activities. WI,;;thank
Dr. Frwenco Kur~ >loti Dr. Ricardo Pollcry for t1lcir help
during the ~llmpJing'3. Our~pccial tbartk~ lo TatiaJla (Ialvllo
tor her help with the micrubiological anlllyscs, We Lnarlk
Dr. Luciana Andrlid~ and Roseni Olrvalho lor [ne helj'llul
wmmcnts anIJ English eotr~liuffi. We are grateful to the
Mi("Tobiolo8~' allcj Chemical (A:eanograpll)'
I.jlburatorle~
S<mta Ursula
Cniversity
For the micNbiQlogjcal
allc,l <.:hcmical anlll~cs.. reipeclivt:ly,
We tha!IK tu the
allen ~·nlt.U5reviewer for slJggc~[i{ln~ Ihill improved u ur
rnllnu.~crjp~. Thi~ '3tudJ WllS financially wpported
h)' I he
Mrlta (In-ulll Uni,,'er~ily A.ssodation SlTld PliTt of the MSc.
(If
lhc5i~ of A.M.G,
APHA (1Q98), Standarc] melhods tor the examination
of waler llnd wa~tewtller, In L. ~. Cle:;ocri. A l2,
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on
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und
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Iy
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