Bolm Inst. oceanogr., S Paulo, 33(1):79-91, 1985

SESSILE CILIATES ON ARTIFICIAL SUBSTRATA SUBMERGED IN A POLLUTED ESTIJARY (SANTOS J SP J BRAZIL)

Verena Rapp de ESTON

Instituto Oceanografico da Universidade de são Paulo

Synopsis

Primary grohlth hlas analysed on artificial substrata submerged at three sites of the Santos estuary (State of são Paulo, BrazilJ. Research on sessile ciliates was emphasized because they hlere the most conspicuous organisms of the primary growth developed along this estuary. Zoo~harnnium ~ommun~ dominated near the headwaters of the estuary, u,here the greatest amount of suspended matter in the water was found. Ephelo~a g~m~paha dominated downstream. Although short time variability was observed in the colonization of substrata submerged on subsequent days, seasonal patterns could be determined. These patterns were characterized by a greater number of rare species of sessile ciliates, and a higher density of the most frequent ones, during spring and summer.

Descriptors: Periphyton, Artificial substrata, Estuaries, Pollution, Sessi le ciliates, Cil iata, Santos-SP, Southern Brazilian coast.

Descritores: Perifiton, Substratos artificiais, Estuários, Poluição, Ci liados sésseis, Ci liata, Santos-SP, Costa sul-Brasil.

Introduction

Associations of protozoa or diatoms have been used by several authors to define a polluted environment, since the abundance and composition of these organisms may change quickly according to water quality (Patrick ~~ al., 1954; Heulekian & Crosby, 1956; Genovese & Gangemi, 1966; Burbank & Spoon, 1967; Persoone, 1968; Wilbert, 1969; Parrish & Lucas, 1970; Relini ~ al., 1976; Cairns Jr ~ al., 1978; Henebry & Cairns Jr, 1980; Marcus, 1980). The primary colonizers of substrata, either natural or artificial surfaces, are protozoa, diatoms, bacteria, and eventually macroscopic organisms (Persoone 1968; 1971). Artificial substrata have been used for quantitative studies and for comparisons of the primary growth between environments, since natural surfaces are irregular, rugose, and not favorable for quanti­tative analysis (Sladeckova, 1962).

In the present paper, sessile ciliates were studied to determine changes in the community structure with distance frompollution sources as well as temporal variation, since they are the most conspicuous organisms of the primary growth developed in the Santos estuary.

Publ . n. 622 do In6t. o~eanog~. da U6p.

Material and Inethods

S~u.dif 6il~

Santos estuary is placed at southern Brazilian coast (23°56'S - 46°20'W) (Fig. 1). It is a coastal plain estuary which receives coarse sediments carried by the rivers descending from "Serra do Mar" mountains (Goldenstein, 1972). The fluvial system is the main source of the existing pollution: the estuary receives urban and industrial effluents, presenting a decreasing gradient of nitrate, phosphate, mercury, pesticides, and sediments in suspension in the water from the headwaters downstream (Tommasi, 1979).

M~h.od6

Three collection sites positioned in a transect along the estuary were chosen (Fig. 1). Samples were obtained every 45-60 days from May 1979 to March 1980 at all three sites. An experiment related to short time variability was made at site C in January 1980, for 8 consecutive days. Microscope cover slips (22 x 22 mm), used as surfaces for colonization, were maintained in a vertical position fastened by acrylic supports. These supports were placed 0.5 m deep in the water anchored to local piers, where they remained for 5 days. Pairs of cover slips were held

80 Bolm Inst. oceanogr., S Paulo, 33(1), 1985

together in order to avoid colonization on both sides. Immersion time was previously determined in order to sample a community that represented the primary growth. Once removed irom the water, four replicas of cover slips of each collecting ~ite were fixed with Bouin and stained using the Protargol technique, following the methodology modified by Eugene B. Small (Laboratory notes in protozoology, Fall 1976, Dept. Zoology, Univ. Maryland, MD, U.S.A.).

Fig. 1 - Santos estuary, with position of collection sites (A, B and C) •

Ten percent of the surface of the cover slips was established as the minimum area necessary to quantify the sessile species with random distribution, sampled in random plots of 1 mm 2 • Rare species or species with gregarious distribution were counted on the total area of the cover slips. Since points of fixation of the organisms to the substrata were counted, the number of individuals of colonial species is underestimated. Vagile ciliates were not quantified. Morisita's similarity coefficient CÀ (Grassle & Smith, 1976) was calculated between samples, and the results were clustered by the weighted pair-group method using arithmetic averages (Davis, 1973; Sneath & Sokal, 1973).

Measurements of salinity, temper­ature, transparency, dissolved oxygen, suspended matter (inorganic and organic),

chlorophyll-a and pheophytin-a of the water were estimated_ at the collection sites by the time of placement of the substrata and a fortnight later. Dupli­cate samples of the last four parameters were averaged. Indexes of rainfall were obtained from Instituto Nacional de Meteorologia (79 distrito), Minist~rio da Agricultura.

Results

Two types of association were formed by the sessile ciliates in the Santos estuary: 1) the primary growth at sampling site A, where Zoothamnium eommu~e dominated; 2) primary growth at sites B and C, where Ephelota gemmipana predominated. The dominance, either of Z. eomm~e or of E. gemmipana, was responsable for setting apart site A from sampling sites B and C when data were clustered (Figs 2-3).

Zootham~um eommu~e was found on all substrata submerged at the three collecting sites. It was the dominant species atsite A, followed by Zootham~um sp (sensu Kahl, 1935) (Table 1). At site B Z. eommu~e also occurred in great numbers although in rather less amount than Ephelota gemmipana (Table 2). Small co~onies of Zootham~um were more commonly found than large ones, and a decrease in the size of the colonies towards the mouth of the estuary was observed. Few large colonies of these species, with 500 to 1000 zooids, were observed during October and December of 1979 at site A. At site B the bigger colonies had 250 individuals (December of 1979) while at site C the maximum number of zooids per colony was 50 (December of 1979).

Ephelota gemmipana was the dominant species in almost every sample obtained at sites B and C (Tables 2-3). Encysted individuals predominated over nou encysted ones in about 50% of the substrata submerged at these two places. At site A only 4 individuals of this species were observed during the sampling period, all encysted (Table 1). Some of the cysts were found parasitezed; parasitism of E. gemmipana by Hypoeoma sp was observed in May, December, January, and March at sampling sites B and C, periods of great abundance of E. gemmipaha.

ESTON: sessile ciliates: artificial substrata 81

o.zo 0,4 0 I ,

-A/MAY04 ---A IAUG 09 -MNOVJO ---/J./Mt.R07

~----~ =--A/-JA-"-O tl/JUN2 L_~~~~~ -81 AUG09

---A/ocrDS -CI AUG09 ---CIJANI6 -8/MAY~ ---CIJANI7 -C/NOV30 ---C/MlhQ4 -C/MAR07 ---C/JUN2/ -C/ocro~ ---CIJANI3 -C/JANIS

=~-CIJANI4 -B/NOVJO

---C/JANI2 -B/JUN21 --- B/"JANIQ -S/acrDS ---C/JAN IO -CIJAN 1 1

Fig. 2 - Results af the cluster analysis between substrata submerged at the callectian sites in different periads af the year. Data af the repl icate samples were gathered. Date of submersion af the substrata is indi­cated.

0 ,20 0 ,40 0.60 , I I 1 ,

r--------~~i ~

Fig. 3 - Results of the repl icate samples af the substrata submerged at the col­lection sites clustered by the time af the year. Date of submers i an of the substrate is indicated.

In the short time variabi1ity experiment A~ineta tub~o~a dominated fo11owed by Z. ~ommun~ in great numbers on the cover slips submerged on January 10 and 11 at site C. From January 11 onwards, the numbers of E. g~mmip~a started to increase whi1e Z. ~ommun~ decreased. From January 12 on, the number of A. tub~o~a decreased as we11 whi1e E. g~mmipana became dominant (Tab1e 4).

High densities of sessi1e ci1iates and a greater number of rare species

were observed during spring and summer. The heavier co1onization periods were observed from October to March, with more than 1000 points of fixation / cm2

(Fig. 4). In addition to Zoothamnium ~ommun~, both A~ineta tub~o~a and Zoo.thamnium sp (sensu Kah1, 1935) occurred in great numbers during October at site A. In the other samp1ing periods on1y Z. ~ommun~ was dominant at this collecting site (Tab1e 1). Ephe10ta g~mmip~a shared its dominance with A. tub~o~a during December and with Z. ~ommun~ during January at site B, and with A. tub~o~a and Z. ~ommun~ during January at samp1ing site C (Tab1es 2-3). A change in the density of the sessi1e ci1iates was observed on substrata submerged at site C on consecutive days during January of 1980 (Fig. 4B).

The greatest number of species was found during October at site B and during December at sites A and C (Fig. 5). Ineividua1s of A~ineta sp, Cot~nia sp, Epi~ttj.e.~ sp, P.e.a;ttj~o.e.a gfta~~, P. ~~gut~, Podop~htja 6ixa, Ptjxi~o.e.a ~o~ia~, Vagini~o.e.a ~~tj~ta.e..e.ina, VO~­~~a sp 1 and Vo~~~a sp 2 were found on1y in the warmer months and in sma11 numbers. Coth~nia m~a and Vo~[~~a n~bu.ti6~a were found in varying numbers troughout the year (Tab1es 1-4).

Vagi1e ci1iates such as H~miop~tj~, Htjpo~oma, Thlgmog~t~, T~o~hiua and some unidentified Gymnostomata, were found at alI samp1ing sites. Herbivores, such as N~~u.e.a and Chl.e.o­done1.e.a (Faure-Fremiet, 1961; Dragesco, 1962; Bick, 1972), were never present at samp1ing site A. Great numbers of certain vagiQe ci1iates occurred oc­casiona11y a1though never surpassing the amount of the sessi1e ones: H~­

miop~tj~ at sit e A in October; Thigmog~t~ at sites A and B in May and January, and at A a1so in October, December and March; Htjpo~oma at sites B and C in May, and at C a1so in December arid January; Vi.e.~pt~ at C in May; and Chl.e.odon~.e..e.a at site C in January. A1though the number of species of vagi1e ci1iates increased towards the mouth of the estuary, predators of peritrichs, such as Vi.e. ~pt~ and H~mio pIVltj~ (Dragesco, 1962; Curds, 1969; Sma11, 1973), were sporadica11y f ound in gre a t numbers both at the he adwaters and downstream.

Table Density of sessile ciliates on artificial substrata sampl ing peri od

Period of·

~ M<lY 0/t-09 Jun 21-26 Aug 2)-28 Uct 05-10

Specl e'i

(phr(C'ra q(,ItIIl('pa'la

PI' d('vlt'tlj(l ~t __ a

.4.cúlC'fa tubl!ltOM li .7 23 1\ 31 1683 1835 1025 997

A('(",('ta sp

fpiA tfjt i.h sp

VC'ltticrlla n('but.i~Ha li 12 10 10 33 135 22

Vf'"-tic,,Ua sp 1

Volttic"lla sp 2

Vo'ttü('Ua sp 3

Zoothalllttútlll COllltlU.ltt 176 15' 113 92 68 8. 7. 118 39. .39 528 5.5 3.80 2530 2570 zlt 1 O

Zootkltlr",(.u," sp J7 70 5. 31 119 170 130 136 2073 2870 2770 2520

CothUILrU4 maJL.itÚna 21 17 1/ 1\ 20 16 .8 123 \2 63 .7

CothWtni.a sp 16 2\

PlatlJcota ollac.il.i.6

Pla..ttjcClla uqultVLi6

Pljúcola 60C.i..n.Li6

Vaginic.ola CIf.lj6ta.t.li..na

Total density (t'II) 239 230 186 1\9 93 103 96 12\ 58. 663 721 76. 7502 7308 6.67 6001

N/cm2 5. 52 \2 3. 21 23 22 28 133 151 16. 17' 1705 1661 1\70 136.

submerged at site A

Nov 30-Dec os

251 32 .6 29 80

31 30 12 32

2680 1710 2752 2162 \17

350 700 520 620 1\

165 168 168 773 192

11 16

3.82 265. 3512 3606 7'3

791 603 878 819 169

th roughout the

Jan 10-15 "ar 07-12

12 28 .6 305 .83 652

28 87 .5

602 327 218

3.5 2R7 379 .670 5200 3100

.6 95

32 90 90 127 112

397 \19 .82 5705 6232 4222

90 95 109 1297 1416 959

178

20

33

3690

1)1

\2

4106

933

00 N

tD O

3

::l Cf)

rt

~ lU)

-O !li C

O

w w

I..D 00 V1

rn Ul -I o z

VI (1) VI VI

(1)

Table 2 - Density of sessile ciliates on artificial substrata submerged at site B throughout the In sampl ing period.

!li rT

Period of I~ ~

May 04-09 Jun 21-26 Aug 23-28 OC' 05-10 No .... 30-Dec OS Jan 10-15

Spec I es !li

fphrfota 9, ... <pa!ta 1290 2200 3700 1761 404 653 318 285 48 13 4040 4880 3020 3830 2180 2540 4150 3070 4830 4620 3J70 2550 -, rT

PC'rlo .l'Jh·UJll ~h:a -To

Acineta tube'L06a 17 46 67 13 244 187 258 30 I 2412 181 302 806 25 23 63 n Ac Ú1e ta sp !li

fpütylu, sp

VQ~t<ce(la "obuu~rJ,a 12 32 25 95 25 21 17 11 40 42 127 VI

16 10 182 19 IA 12 366 448 35 I 126 C CT

Vrltt.iceUa sp 1 58 19 14 16 55 13 VI rT

VoH {colla sp 2 -,

V(I't('<c"Ua sp 3 rT !li

Z(> (I thaml1úun c.orrwnu.ne. 152 472 360 134 187 196 271 321 474 452 497 364 921 78 1479 1311 822 1066 319 35 I 2560 1020 1370 1380

ZoothamtUum sp 88 28 48 36 25 54 24 17 1303 102 38 70

CothWtrWt maJU...tima 91 144 74 62 104 18 10 19 18 11 19 42 145 131 24 15 20 11 85 827 130 186

CothuJtn.ia sp

Platycola g,acilM

Platycola .. gulaJLió

Pljx.i.cola 6oc.iaw

Vagin-icot'a Cltlj6taU-ina ]I 25 64 75 26 67

Total density (N) 1695 2897 4230 2111 739 872 666 ]lO 589 565 584 529 6583 5404 5117 5560 5564 3840 4803 4258 7918 7022 5286 4372

N/cm 2 385 658 961 480 168 198 151 161 134 128 IJl 120 1496 1228 1163 1264 12S4 873 1092 968 1799 1596 120 I 994

ICO

Table 3 - Density af sessile ci 1 iates an artificial sampling per i ad

Period of

Hay 04 -0 9 Jun 21-26 Aug 23-28

r p/I{' r (' t (l Ç1('II~II()xt ~(l 2880 19;; 1910 880 916 3376 1850 1067 302 103 83 96 13320

r(·rl(').1/I~If(t ~q(l

A.(IIH'ta r/l bn('~(l 23 13

A.c(lIrfa 'p

f 1-'( ~ t~/r {~ sp

Vc,ticdfll lI('bldd("1I1

Vt"(ccr(fa. 'p I

Vt"t(cr/'i'a ,p 2

V('Hic{'Cia ,p 3

Zoothamtt.iUnl (""",lUI"- 11 16 21 90 21 2; I; 21 15 36 31 22 70

Z(·(·t/UltIUICum 'p

C('(/ru'wia lIut'Litútra 17

(,('tlru~IIÚt sp ;5

peatl/e(·ia !1Mcd'(~

Pf(ltyct'fa "'<1IIf(ni~

P~{J( «'('(a ~(lC iae (~

Vaoitl(c1'fa C ' Ij~t(lfCÚUI

Total density (N) 2900 2012 195; 977 937 3401 1865 1116 319 1;0 123 123 13;11

N/em' 659 ;57 ;;; 222 213 773 ;2; 25; )2 32 28 28 30;8

substrata submerged at site C

Oçt 05-10 ~o." 30-Dec 05

8390 6500 9660 3830 2)10 2560 2590

20 ;1 13 289 590 2;3 510 ;185

;8 169 56 97 21

125 169 181 162 257 286 203 1110

11 63 13

85;; 6735 9873 ;3;0 3JJ4 3158 3;)2 5336

1942 1531 2244 986 758 718 789 1213

thraughaut the

Jan 10-15 Mar 07-12

12 2320 ;156 7161

2;60 ;704 3126 109

17 26 ;9 16 35 25

;10 380 380 66 ;1 115

208 11 ;1

310; 5130 3616 2511 4235 7301

705 1166 822 571 962 1659

3873

17

30

6;

3985

906

o::> J::-

OJ a -3

:J lJl rt

o n (l) QJ

:J o lO .,

I~ QJ C

O

VJ VJ

\.O o::> V"1

rn (j')

-.oi o z

(Jl

(i) (Jl

(Jl

(i)

()

Table 4 Density of sessile ci 1 iates artificial substrata s ubme rged in January of 1980 Q.I - on at rt

site C for 8 consecutive days (i) (Jl

Q.I Period of ..,

subfllers ion rt Jan 10-15 Jan I I ~ 16 Jan 12-17 J<ln 13-18 J<ln 14-19 J,Jn 15-20 J.Jn 16-21 Jan 17-22

Spec ies

--------------

-ti

f~-,hd'l' t<1 tl('~I"il-h1~(l 12 3540 2180 6JOO 3222 5100 6320 5000 11880 1"500 11160 14520 13ZltO 7960 3]00 1400 1760 5]40 ]520 ]690 6650 4490 1630 163 899 1221 1968 3437 1105 -()

POdUpit!I1JD. Ú m 2S " 11 Q.I

A,c (111' ta rllb(""~(l 418S 2460 47011 3126 7606 3191 2238 5519 3621 2940 J050 3500 101 156 '31 191 155 17 180 15 7' 51 10 " 67 15

A.c lurra sp (Jl

C f!'i ~ ry! (~ sp O-lI,-, t(rI'(!'o I!\'bu('( '('~11 11 17 16 '9 68 101 16 136 31 96 65 61 13 11 11 58 15 1'8 13 17 16 11 105

(Jl

rt [I",(I('I,ri<1 sp I ..,

Q.I 1,("tirrfl'll sp 2 rt

l"',(,cl'l'r(l sp 3 Q.I

l,'" rhm~lIIi It'I! (',.,,'1111111' 1110 "O 380 380 '59 300 731 376 159 JJ7 58 161 I" 50 78 38 77 61 97 116 98 183 195 185 183 "9 J69 197 9' 135 2" 118

Z<'e' 011'''111 lu·" sp

1,·(11l11l1111 ~1,nltillPa 13 108 11 " 10 3' 15 10 17 39 38

r,'(/IU"1!1l sp 27

P{'a (,/c"I'{1 ,nacit i ~

Pfl1.f(lc1'Í'a "'!lui'<"n I ~ 10 12 " 13 11

PI/H((·Fa kCÚlrO

V(((101(('(>(11 nlj~tllfeilla

Total densi ty (N) 5336 3104 5130 3616 11663 5765 9330 9266 8916 9714 8177 15607 14631 11388 1~036 13579 8194 3617 1705 1908 5521 3936 3929 6925 4831 1907 586 1146 1390 2236 3777 1554

N/ cm2 1213 705 1166 822 2655 1315 2120 2106 2027 2206 1858 3547 3]71 2588 3417 3086 1862 867 J87 '3' 1255 89' 893 1574 1 0~8 '33 t33 260 316 508 858 353

(X)

86 Bo1m Inst. oceanogr., S Paulo, 33(1), 1985

1 1000

100

t\1 \

\

~. -,

k--8 ----c ·

M Jun A o D J M

1979/1980

- 2 ~ N/em I ®

r

10']0 I 11 I

10 /I 12 1314 15 16 11

JANUARY/1980

Fig. 4 - Mean number of points of fixation of the sessi1e ci1iates by substratum area (N/cm 2 ). Bars indicate standard deviation of the mean. A) Seasona1 variabi1 ity at the samp1 ing sites; B) Dai1y variabi1 ity at site C of co11ection. Date of submersion of the substrata is indicated.

x 10

5

@

I,

1

M Jun A O O J M

1979/1981

X 10

5

2

®

I

10 /I 12 13 14 15 16 17

JANUARY/1980

Fig. 5 - Mean number of species found (;). Bars indicate standard deviation of the mean. A) Seasona1 variabi1ity at the samp1ing sites; B) Dai1y variabi 1ity at site C of co11ection. Date of submersion of the substrata is indicated.

ESTON: sessile cil iates: artificial substrata 87

Temperature of the water presented a seasonal pattern, with maximum values during summer (November to March), from 24 to 29°e, and minimum values during winter (June to August), from 19 to 22°e (Fig. 6). Annual fluctuations of temperature were about 100e. An oscillation of 5°e was observed in the daily samples obtained during January of

mg/l

60

a:: 50 w ~ ~

<t 40 ~

o w 30 O z w Q 2 0 (f)

::l (f)

10

o JJg 11 ?I -.J -.J 20 >-5: O

10 a:: O -.J I

O o

De w 30 a:: :::> I-<t

26 a:: w Q

-

A 8 C

/.:.- - '-: .. --' / I

- ~.-~' .. . ..

19 4 21 5 9 23 A M J J A

, \

\ . - - _,o

. " -4\." I \

I \

: I ', °'0 o" ,

-.....J , ': / , /

'--- ~--.... '" I I I I !

5 1930 14 /023 7 O N O J M

/979//980

1980 at collection site e. Salinity varied from 1.6 to 12.1 %0 at collecting site A, from 3.7 to 22,1 %0

at site B and from 4.1 to 23.4 %0 a t site e. During the short time varia­bility experiment, salinity values at site e varied from 4.1 to 21.4 %0

(Fig. 6). Minimum rainfall indexes were registered in June and August while the maximum one was attained in November (Table 5).

I m 2 ~>-Cf)Ü ZZ <l~ a:: ~ o

010

z O I- 60 <t a:: :::> I-

4 0 <t li)

Z w

2 0 o ).. )(

O O

).1gl/

tll I 20 z ~ >-I 10 Q

O

.. - ;'y

......... ~ W I O~~~~~~~~~~~~ Q /9 4 21 5 9 23 5 1930 14 1023 7

o' "

., ),-I~ '/ "

A MJ J A O NO J M

.'-:,--" ,

De w 30 a:: :::> ~

<t 26 a:: w

19791 1980

~ , '. 22

, w , ,

v

,.1"-'; :':" · ~· .. II ~ 22 l-

18 . I

0 100 I

~ 2'0l~"/"'-'/"\\· · · · · · ······· ·· ·· · ···· · ii .. " "/ ' " ......... ,';"

;;i , _/ ' , ____ .'-- "v' " ... ' ~ __ . (f) '\...- . _-..,....: .... --/

o ~ 2 924 4 921 26 5 9 142328 5 10 1930 5 14 101523 7 I A M J J to O NO J M

1979/ 1980

w ~

>-~

Z -.J <t Cf)

20

10

O 10

Fig. 6 - Environmental data at collection sites.

.... .... :

14 18 22 JAN I 1980

88 Bolm Inst. oceanogr., S Paulo, 33(1), 1985

Table 5 - Monthly indexes of rainfall (data granted from Institu­to Nacional de Meterorolo­gia - 7? distrito - Minis­tério da Agricultura)

Da te Indexes o f rainfall ( mm)

May 1979 103.7

Jun 56. I

Jul 159.3

Au g 57. 8

Se p 234. 7

Det 147. O

No v 3 I 4.4

Dee 256.6

Jan 1980 255.7

Feb 294. 4

Mar 260. 3

The amount of suspended matter decreased from the headwaters to the mouth of the estuary (Fig. 6). Inorganic matter represented the bulk of the suspended matter, and varied from 4.7 to 57.1 mg/l at site A, from 4.9 to 20.2 mg/l at site B and from 0.7 to 11.7 mg/l at site C. Concentrations of insoluble organic matter amounts varied between 0.1 and 7.2 mg/l at site A, between 0.9 and 4.6 mg/l at site B and between 0.5 and 6.3 mg/l at site C (Table 6). Transparency of the water was low (Fig. 6), an inverse relationship being noticed between transparency of the water and the amount of suspended matter present at the three sample sites.

Dissolved oxygen was always below saturation leveIs (Fig. 6), the lowest and most variable values observed at site A (11.68 to 62.97 %). Percent saturation from 37.65 to 78.02 % were determined at site B, and from 46.04 to 71.58% at site C. Chlorophyll-a concentrations varied from 1.89 to 16.57 Wg/l at site A, from 4.15 to 19.82 Wg/l at site B and from 2.67 to 31.13 Wg/l at site C (Fig. 6). Amounts of pheophytin-a varied from 0.73 to 12.24 Wg/l at site A, from 2.97 to 10.52 Wg/l at site B and from 2.02 to 8.97 Wg/l at site C (Fig. 6) denoting the presence of unhealthy or dead phytoplankton cells in the samples.

Discussion

Ciliates are tolerant with respect to several environmental factors (Corliss, 1973). Salinitity and temperature, usually the most important features determining the distribution of marine animaIs, are not as significant for the distribution of benthonic marine ciliates (Webb, 1956; Fenchel, 1969; Borror, 1975; Wilbert & Kahan, 1981). Occurrence and local abundance of the species of ciliates are related to the type of available food (Noland, 1925 ~J.;t. ~lH: Taylor & Berger, 1976; Webb, 1956; Reid, 1969; Wi1bert, 1969; Borror, 1975; Taylor, 1978) and to oxygen concentration (Stout, 1956; Taylor, 1979). At low leve1s of oxygen, number and amount of the aerobic species are reduced, even when abundant food reserves seem to be availab1e (Wilbert, 1969; Bick, 1973).

The quicker colonization of the substrata by ZoothamnZum co1onies towards the headwaters of the estuary may be indirectly related to increasing amount of suspended matter. Peritrichous ci1iates feed essentially on bacteria and when abundant they indicate an organical1y polluted environment (Parrish & Lucas, 1970; Bick, 1973; Finley, 1974; Henebry & Ridgeway, 1979). Bastida (1968) considers Z. ~ommune an indicator of po11uted waters since, in harbors, it increases in number with raising contamination. Z. ~ommune was also the most frequent species observed on the primary growth of an interna1 p1ace of the harbor at Genoa, Italy, po1luted by urban wastes (Relini et al., 1976), and it was observed by Persoone (1968) in the harbor of Ostend, Belgium, a po1ysaprobic estuary.

The unexpected low numbers of Z. ~ommune in the January samples of site A seem to be re1ated to low percentage of oxygen saturation (Fig. 6), instead of 1itt1e amount of organic matter availa­b1e, which was not the case (Table 6). A1so during May and June, other periods of very low oxygen saturation leve1s at this samp1ing site, the density of Zoothamn~um ~ommune was low.

Vagile ci1iates can not be responsi­b1e for the decreasing amount of Z. ~ommune down the estuary for predators of peritrichs were sporadica1ly found ~n

great numbers, both at headwaters and

ESTON: sessile ciliates: artificial substrata 89

Table 6 - Inorganic and organic fraction of the suspended matter (mg/l)

Sa mp ling

Da te

Apr 19 . 1979

J un 21

J ui 05

Au g 09

Au g 23

Oct 05

Oct 19

Nov 30

Dec 14

Jan 10. 1980

Jan 23

Mar 07

In o r ganic

ma t t e r

9.8

1 I . 2

8.4

32.4

16.5

29.3

11 .2

5. 3

6.5

7.3

4.7

57.1

A

organic

matter

5. O

7.2

3.4

3.6

2.7

4.6

3.6

O. 1

2.3

4.8

0 . 6

6 . 1

downstream. Also immigration was not being prevented since there was still space available for colonization when cover slips were removed from the water (Eston, 1981).

Decrease in the Aci~eta tub~o~a numbers on consecutive days in the January samples of site C seems to be related to the reestablishment of the E. g~mmipaha population. As they are both carnivorous species (Grell, 1973), competition for food between them or mutual predation on young stages shoud be investigated in order to understand their replacement on the cover slips.

Although short time variability was obse rved in the colonization of substrata submerged on subsequent days, seasonal patterns could be determined. They were characterized by higher densities of sessile ciliates and a greater number of the rare species during spring and summer. Increase ~n the mobility and reproductive rate during the warmer periods (see Schoener, 1974) was certainly responsible for the seasonal patterns observed. On the other hand, the local variability observed among replicate samples was probably caused by random colonization of the organisms (see Sutherland & Karlson, 1977).

Conclusion

Th e two types of association formed by

inorganic

ma t t e r

5.5

7 . 6

6.9

8.0

20.2

9.6

8 . 5

8 . O

4.9

4.9

5. 1

5.8

B

organic

ma t t e r

2.9

4.3

4.6

2.6

3.8

1.6

2.7

I. I

2.8

3 . 9

1 . O

0.9

inorganic

matt e r

6.0

7.5

5.3

8 . I

6 . 2

9.4

11.7

6.0

4.4

0.7

1.7

5.7

the sessile ciliates denote

c o r ganic

matt e r

6.3

4.8

6 . 1

0 · 5

I . O

I . O

0 . 9

2.5

3.8

2.8

0.7

0 . 8

the existence of different environmental conditions along the estuary of Santos. Shift in the dominance from Ephelota g~mmipaha to Zootham~um eommu~~ towards the headwaters of this estuary seemed to be related to increasing amount of suspended matter in the water, whenever oxygen concentration levels were not extremely low.

Acknowledgements

This paper is based on a thesis su~mitted in partial fulfilment of the requirements for the Degree of Master in Biological Oceanography at the "Instituto Oceanográfico" of the University of são Paulo. I wish to acknowledge Luiz A. Zavala-Camin who provided laboratory space and facilities in Santos at the "Divisão de Pesca Mari­tima" of the "Instituto de Pesca da Se­cretaria da Agricultura do Estado de são Paulo" as well as the Fire-Brigade of Santos, for boat facilities. This research was possible thanks to FAPESP (Proc. n9 1118/77) and CAPES fellowships.

References

BASTIDA, R. 1968. Las incrustaciones biologicas en el Puerto de Mar del Plata, período 1966/67 (lª parte). La Plata, Laboratorio de Ensayo de Materiales e Investigaciones de la Provincia de Buenos Aires, 68 p.

90 Bo1m Inst. oceanogr., S Paulo, 33(1), 1985

BICK, H. 1972. Ci1iated protozoa: an i11ustrated guide to the species us e d as bio10 gica1 indicators in freshwater bio10gy. Geneva, W. H. C., 198 p.

----- 1973. Popu1ation dynamic of protozoa associated with decay of or ganic materia1s in fresh water. Am. Zool., 13:149-160.

BORRO R , A. C. 1975. Environmenta1 requirements of se1ected estuarine ci1iated protozoa. Corva11is, U.S. Environmenta1 Protection Agency, 49 p.

BURBANCK, W. D. & SPOON, D. M. 1967. The use of sessi1e ci1iates co11ected in p1astic Petri dishes for rapid assessment of water pol1ution. J. Protozoo1., 14:739-744;

CAIRNS Jr, J.;KUHN, D. K. L. & PLAFKIN, J. L. 1978. Protozoan co10nization of artificial substrates. In: Weitze1, R. L., ed. Methods and measurements of periphyton com­muties: a review. Philade1phia, ASTM, p. 34-57.

CORLISS, J. O. 1973. Protozoaneco10gy: a note ou its current status. Am. Zool., 13:145-148.

CURDS, C. R. 1969. An i11ustrated key to the British freshwater ci1iated protozoa common1y found in activated sludge. Wat. Po11ut. Res., 12:1-90.

DAVIS, J. C. 1973. Statistics and data ana1ysis in geo10gy. New York, John Wi1ey, 55 p.

DRAGESCO, J. 1962. Capture et in­gestion des proies chez 1es infusoi res ci1i~s. Bu11. bio1. Fr. Be1g., 96: 123-167.

ESTON, V. R. de 1981. Recobrimento primário de substratos artificiais submersos no estuário de Santos (São Paulo, Brasil). Dissertação de mestrado. Instituto Oceanográfi­co, Universidade de são Paulo, 116 p.

FAURÉ-FREMIET, E. 1961. Documents et obs e rvations ~co10g iques et pratiques s ur la cu1tur e des infusoires ci1i~s. Hydr obi o 10g ia, 18: 300-320.

FENCHEL, T. 1969. The eco10gy of mar~ne microbenthos. IV - Structure and function of the benthic ecosystem, its chemica1 and physica1 factors and the microfauna communities with specia1 references to the ci1iated protozoa. Ophe1ia, 6:1-182.

FINLEY, H. E. 1974. The peritrichs now and then: 1676 to 1973. Trans. AM. micros. Soc., 93:307-313.

GENOVESE, S. & GANGEMI, G. 1966. Primo contributo a110 studio de forme fissate su vetrini immersi in un ambiente sa1mastro meromittico. Atti Soc. pe10rit. Sci. fis. mato nat., 12:509-519.

GOLDENSTEIN, L. 1972. A industrializa­ção da Baixada Santista: estudo de um centro industrial sat~lite. Ser. Te­ses Monogr., Inst. Geogr. Univ. S Paulo, 7:1-342.

GRASSLE, J. F. & SMITH, W. 1976. A simi1arity measure sensitive to the contribution of the rare species and its use in investigation of variation in marine benthic communities. Oeco10gia, 25:13-22.

GRELL, K. G. 1973. Protozoo10gy. Ber1in, Springer-Ver1ag, 554 p.

HENEBRY, M. S. & CAIRNS Jr, J. 1980. Monitoring of stream po11ution using protozoan communities on artificial substrates. Trans. Am. m~cros. Soc., 99:151-160.

------- & RIDGEWAY, B. T. 1979. Epizoic ciliated protozoa of p1anktonic copepods and c1adocerans and their possib1e use as indicators of organic po11ution. Trans. Am. m~cros. Soc., 98:495-508.

HEULEKIAN, H. & CROSBY, E. S. 1956. Slime formation in po11uted waters. 111 - Nature and composition of slimes. Sewage indo Wastes, 28:206-210.

KAHL, A. 1935. Urtiere ode r Protozoa. 1- Wimpertiere oder Ci1iata (Infusoria), eine Be a rbeitung der frei1ebend em und e c tocomme nsa1 en

ESTON: sessile cil iates: artificial substrata 91

Infusorien der Erde, unter Aussch1uss der marinen Tintinnidae. Tierwe1t Dtl., 30:651-805.

MARCUS, M. D. 1980. Periphytic community response to chronic nutrient enrichment by a reservoir discharge. Eco10gy, 61: 387-399.

PARRISH, L. P. & LUCAS, A. M. 1970. The effects of wastewaters on periphyton growths in the Missouri river. Cincinnati, U.S.F.W.P.C.A. Nat'l Fie1d Investigation Center, 26 p.

PATRICK, R.; HOHN, M. H. & WALLACE, J. H. 1954. A new method for determining the pattern of the diatom flora. Notu1. Nat., 259:1-12.

PERSOONE, G. 1968. Eco10gie des infusoires dans 1es sa1issures de substrats immerges dans un port de mero 1- Le fi1m prÍmaire et 1e re­couvrement primaire. Protisto10gica, 4:187-194.

1971. Eco10gy of fou1ing of submerged surfaces in a po11uted harbor. vie Mi1ieu, 22 (supp1. 2): 613-639.

REID, R. 1969. F1uctuations in popu1ations of 3 Vo~~etfa species from an activated-s1udge sewage p1ant. J. Protozoo1., 16:103-111.

RELINI, G.; MONTANARY, M.; VIALE, S. & PISANO, E. 1976. Prime fasi de insediamento su substrati duri immersi in acque de1 porto di Genova a diverso grado de inquinamento. Archo Oceanogr. Limno1., 1&(supp1. 3):113-140.

SCHOENER, A. 1974. Co10nization curves for planar marine is1ands. Eco10gy, 55:818-827.

SLÃDECKOVÁ, A. 1962. Limno10gica1 investigation methods for the periphyton ("Aufwuchs") community. ~ot. Rev., 28:286-350.

SMALL, E. B. 1973. protozoa from a in east-centra1 13:225-230.

A study of ci1iate sma11 po11uted stream I11inois. Am. Zool.,

SNEATH, ~. H. A. & SOKAL, R. R. 1973, Numer~ca1 taxonomy: the princip1es and practice of numerica1 c1assifi­cation. San Francisco W H , . . Freeman, 573 p.

STOUT, J. D. ciliates Eco10gy,

1956. Reaction of to environmenta1 factors.

37:178-191.

SUTHERLAND, J. P. & KARLSON, R. H. 1977. Deve10pment and stabi1ity of the fou1ing community at Beaufort, North Carolina. Eco1. Monogr., 47: 425-446.

TAYLOR, W. D. 197R. Growth responses of ci1iates to the density of their bacteria1 prey. Microb. Eco1., 4: 207-214.

1979. Samp1ing data on the bactivorous ci1iates of a sma11 pond compared to neutra1 mode1s of community structure. Eco10gy, 60: 876-883.

& BERGER, J. 1976. Growth responses of cohabiting ci1iate protozoa to various prey bacteria. Cano J. Zool., 54:1111-1114.

TOMMASI, L. R. 1979. Considerações ecológicas sobre o sistema estuarino de Santos (SP). Tese de livre-do­cência. Universidade de são Paulo, Instituto Oceanográfico, 489 p.

WEBB, M. 1956. An eco10gica1 of brackish water ci1iates. Anim. Eco1., 25:148-175.

study J.

WILBERT, N. 1969. ~ko10gische Untersuchung der Aufwuchs und Plankton-ciliaten eines eutrophen Weihers. Arch. Hydrobio1., (Supp1. 35):411-518.

----- & KAHAN, D. 1981. Ci1iates of Solar Lake on the Red Sea shore. Arch. Protistenk., 124:70-95.

(Received 03-Jul-1984; accepted 07-May-1985)