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Plankton disturbance at Suape estuarine area -

Pernambuco - Brazil after a port complex

implantation

S. Neumann-Leitao, M. L. Koening, S. J. Macedo,

C. Medeiros, K. Muniz and F. A. N. Feitosa

Department of Oceanography of the Federal University of Pernambuco,Campus Universitdrio, 50.679-901, Recife, Pernambuco, Brazil

Abstract

The plankton structure was investigated at the estuary of the River Ipojuca after1 0 years implantation of a Port Complex. Plankton was sampled in one fixedstation. Concurrent hydrological, climatological and chlorophyll a data weretaken. The course of the river alteration resulted into an estuary that tends toevolves from a classical towards a coastal lagoon type. Chlorophyll a presentedlow values for an estuarine mangrove area. Plankton high diversity (> 3.0bits.ind"*) can be explained by the spatial heterogeneity, although a generalbiodiversity decrease was registered after port implantation. Phytoplanktonpresented 98 taxa outranking diatoms (72 species). Zooplankton presented 63taxa outranking rotifers (29 species) and copepods (21 species). Less than 5% ofthese taxa were very frequent. Irregular fluctuations in plankton densities wereobserved with a sharp abundance decrease after port implantation. Thecommunity was dominated by marine eurihaline species with a high proportionof littoral taxa. Meroplanktonic larval recruitment was reduced by landing anddredging. The anthropic impacts affected the system balance.

1 Introduction

A Port Complex was implanted in the south coast of Pernambuco State,Noth eastern Brazil in 1979/1980 as a solution to the State economy collapse.Two years before (1977/1978), an Ecological Study Program was introduced to

Transactions on Ecology and the Environment vol 27 © 1999 WIT Press, www.witpress.com, ISSN 1743-3541

48 Ecosystems and Sustainable Development

obtain the general diagnosis of the area. These studies (Melo Filho\ Cavalcantiet al\ Eskinazi-Lega & Koening^, Paranagua , Neumann-Leitao et a/7, andothers) revealed a high productive balanced ecosystem and suggestions weremade to minimize the impacts.

After the Port implantation, ecological studies were made by theDepartment of Oceanography of the Federal University of Pernambuco, from1886 to 1991; the present paper focalizes the reef area in 1990-1991 at themouth of the River Ipojuca to assess some of the impacts and summarizes theseasonal and nyctemeral structure of the plankton dynamics.

2 Study area

The Suape coastal estuarine complex is located at 8°15' - 8°30' S and 34°55' -35°05' W, about 40 km south of Recife City (Figure 1). Climate is warm-humid, pseudo-tropical (Koppen As') with mean annual temperature 24°C andrainfall 1500-2000 mm.yr"\ concentrated from March to August. Humidity ishigher than 80%. Predominant winds are from the southeast. The formerAtlantic plain forest has largely been replaced by sugar cane culture (Neumann-Leitao & Matsumura-Tundisi®).

Before the port implantation four rivers (Massangana, Tatuoca, Ipojuca andMerepe) converged to Suape Bay, itself an estuary partly isolated from theocean by an extensive arenitic reefline. Today, converge into Suape Bay therivers Massangana and Tatuoca. The Ipojuca and Merepe had theircommunication with the bay interrupted by intensive embankment to build thePort Complex. As a result of the weak communication with the sea, the reflowof these rivers flooded the surrounding fields causing damage to agriculture.The Government solution was a partial breakage of the reefline. In consequencea high amount of suspended material now pass through the reefline openingsettling inside the Port, with a high cost dredging. In Suape area more than 600hectares of mangrove have been destroyed (Neumann et al ).

3 Material and Methods

Climatologycal data were obtained from the Usina Salgado MeteorologicalStation, located 5 km southwest Suape Port.

Samples were collected at 1 fixed station close to the reef, in a spring tide,during consecutive 24 h, each 1 hour interval (hydrology) and each 2 hoursinterval (plankton and clorophyll a), in August/90 (rainy season) and January/91(dry season).

Hydrological data were collected at surface and at 1m from the bottom witha Nansen bottle. Water temperature - reversion thermometer affixed toNansen bottle; salinity - Mohr-Knudsen method (Strickland & Parsons ); pH -Beckman Zeromatic II pHmeter; dissolved oxygen - Winkler method(Strickland & Parsons ); nutrients - (Strickland & Parsons ); watertransparency - Secchi disc.

For sampling the phytoplankton it was filtered 60 liters of water through aPVC pipe 30 cm high and 10 cm diameter with a mesh size 45 urn fitted in one


Ecosystems and Sustainable Development 49

end. For the zooplankton it was used the same methodology although the meshsize was 65 jj,m. After filtration the material of each sample was transferred to aproper flask and preserved in 4% formaldehyde-seawater solution.Phytoplankton analysis was made in an inverted microscope. Zooplanktonentire samples were analysed in a Sedwick-Rafter chamber under Zeissmicroscope.

Chlorophyll a was collected with 1 liter Van Dorn bottle at surface and0.1% of surface incident light intensity. Chlorophyll a was measured byMicronal B280 Spectrophotometer according to Strickland & Parsons^.

Species diversity was calculated by the Shannon^ index. Persons'sproduct-moment correlation was calculated to measure the relationshipsbetween species of all samples after a matrix of log transformed abundances(number of taxa per nf). A cluster analysis was performed using the WeightedPair Group Method, Arithmetic Averages (WPGMA). The Principal ComponentAnalyses was computed based in the matrix formed by planktonic taxa (> 35%occurrence), Chlorophyll a, Species Diversity and hydrological data.Standardization was performed to all data.

Statistical analyses were carried out using the Numerical Taxonomy andMultivariate Analyses System - NTSYS - ver. 1.30 (Metagraphics SoftwareCorporation, California - USA, 1987).

ATLANTICOCEAN

-8"22'S

-8°23'S

- 8°24'S

35°W1

34°57W

Figure 1 - River Ipojuca area, Suape, Pernambuco, Brazil*A - Sampling station



4 Results and Discussion

4.1 Abiotic dynamics

The average rainfall from 1970-1990 was minimum in October (51.40 mm) andmaximum in July (396.30 mm). The total annual average was 1,814 mm and therainy season occurring from March to August.

The water temperature was not a limitant factor due the narrow range ofvalues measured. A clear minimum (26.2°C) during rainy season (July/90) anda maximum (30.0 °C) in the dry season (January/91), reflected the tropicalcondition of Suape area.

Salinity showed an irregular pattern. At the rainy season, the surfacesalinity decreased from 36.41%o (5:30 h) to 11.7%o (13:30 h), rising to36.00%o at 16:30 h followed by a decrease to its minimum of 4.17%o at 1:30h. The bottom salinity presented a similar pattern. At the dry season, the salinitycontinuously oscillated up and down, both surface and bottom, with maximumat 5:30 h (37.18%o - surface; 39.04%o - bottom) and minimum of 11.15%o at3:30 h (surface) and 21:30 h (bottom). Vertical stratification was restricted tothe rainy season when a complete flushing of the estuary by freshwater occurredduring ebb and low tide. In 1990 and 1991 the salinity regime was polihaline,while in 1986 to 1987 it had a strong limnetic influence; and according toCavalcanti et at' it was polihaline to limnetic before port implantation.

Salinity fluctuations reflected a complex set of factors, namely thecirculation in the estuary with the continuous discharge of the River Ipojucapartialy darned at its mouth. It is worth mentioning the change of the surfacesediment distribution in the estuary that had high influence in the depthdecrease and higher evaporation. Before the port implantation the sedimentdistribution in the estuary was predominantly determined by river action. Thecirculation was controlled by tidal movements and only a small contribution toestuarine sedimentation was made by marine sediments. After the reef partialopening the sediment was characterized by a fluvio-marine sand facies. Marinesediments that previously were transported to Suape Bay became traped at theestuary resulting in a sandfilling of the mouth area and the shifting of the mainchannel of the Ipojuca River (Neumann et a//).

Surface and bottom dissolved oxygen saturation showed no clear trends,ranging from supersaturation to very low levels. Significant oxygen depletionwas found during the ebb and low tide, mostly at dry season.

The pH was always above 7.5. Water transparency was high during hightide for both seasons. Reduced levels were registered at the rainy season at lowtide, due intense fine clay resuspension. A strong sedimentation near the rivermouth decreased the local depth. This sedimentation summed up to the river-ocean partial closure transformed the estuary into a lagoon (Neumann et al. ).

Rates of nutrient suply (NO?, NO^ PC>4 and SidJ varied seasonally;rainfall brought pulses from terrestrial run-off. Nutrients levels indicatedeutrophy.

Chlorophyll a oscillated continuously with higher values at the 1% lightdepth. Low tide and rainy season showed higher values (maximum 7.86



mg.m ). Chlorophyll a had strong correlation with nitrate and was consideredlow to a mangrove estuarine area (average of 3.07 mg.m"^ to the rainy seasonand 2.11 mg.m"^ to the dry season).

4.2 Plankton community analysis

Tables 1 and 2 present the phytoplankton biodiversity. It was identified 98 taxaoutranking diatoms with 72 species. Phytoplankton was characterized by marineplanktonic neritic, marine oceanic and marine littoral species. Freshwaterspecies was not significant, mostly registered at rainy season. Five species werevery frequent: Gyrosigma balticum, Oscillatoria princeps, Chaetoceroslorenzianus, Climacosphenia moniligera and Licmophora abbreviata.Phytoplankton density was higher at the dry season (minimum 262,000 cel.T* at3:30 h and maximum of 1,789,000 cel.l^ at 15:30 h). Two diurnal cycles wereobserved a higher from 11:30 to 15:30 h and a smaller from 1:30 to 3:30 h. Atthe rainy season densities varied from 142,000 cell"* at 19:30 h to 740,000 cel.l"'at 13:30 h (Figure 2).

High loads of suspended material, mainly at the rainy season, caused adecrease in phytoplankton reproduction. Phytoflagellate was abundant in thenanophytoplankton fraction.

Phytoplankton biodiversity and ecology changed with the portimplantation (Eskinazi-Leca & Koening ), predominating now epyphytic andbenthic species; a decrease of about 70% in cells density was registered to thisarea.

The 63 identified zooplankton taxa are listed in Tables 3 and 4. The listcontains tycoplanktonics reflecting the shallowness of the estuarine area at theriver mouth, tides turbulence and continuous dredging.

Table 1 - List of the phytoplankton taxa (except for CHRYSOPHYTA) recorded at theIpojuca River Estuary in August/90 (rainy season) and January/91 (dry season).

CYANOPHYTAMen'smopedia tenuissima LemmermannOscillatoria limosa Agardh ex GomontOscillatoria princeps Vaucher ex GomontOscillatoria tetwis Agardh ex GomontOscillatoria willei GardnerOscillatoria spSpindina major KiitzingAnabaena spEUGLENOPHYTAEuglena spPYRROPHYTACeratiumjitiica (Ekenbag) Clapaitde & LachmanCeratium fusus (Ehrenberg) Dujardin

Ceratium massiliense (Gourret) JoigensenCeratium pentagonum GourretCeratium teres KofoidCeratium trichoceros (Ehrenberg) KofoidCei-atam tiipos vwpulchettum (Schroder) LopezProtoperidinium claiidicans (Paulsen)Protoperidinium grande (Kofoid)Protoperidinium venustrum (Matzenauer)Protoperidinium spCHLOROPHYTAPediastrum duplex MeyenPediastnim simplex (Meyen) LemmermannScenedesmus quadiicauda (Turpin) BrebissonClosterium setaceum Ehrenberg

Ceratium macroceros (Ehrenberg) VanhofFen Staui'astrum sp



Table 2- List of the CHRYSOPHYTA recorded at the Ipojuca River Estuary inAugust/90 (rainy season) and January/91 (dry season).

Dictyochafibida EhrenbergCoscinodiscits centralis EhrenbergCoscinodiscus oculusiridis EhrenbergCoscinodisciis spCyclotella stylorum BrigjhtwellMelosira moniliformis (O. Muller) AgardhParalia sidcata (Ehrenberg) CleveThalassiosira leptopus (Grunow) Hasle & FryxActinoptychus spendens (Shadbolt) RalfsGiiinardiastolterfothii(P&gal\o) HasleRhizosolenia imbricata BrightwellRhizosolenia setigera BrightwellBacteriaslrm delicatulum CleveBacteriastrum hyalinum LauderChaetoceros cwvisetus CleveChaetoceros decipiens CleveQiaetoceros diversus CleveChaetoceros laeve Leuduger- FortmorelChaetoceros lorenzianus GrunowChaetoceros peruvianus BrightwellChaetoceros spBellerochea malleus (Brightwell) Van HeurkBiddulphiapulchella GrayBiddulphia tridens EhrenbergCerataulus twgidus EhrenbergDityhim brightwelli (West) GrunowHeliotheca thamesis ShrubsoleHemiaulus niembranaceus CleveHemiaulits sinensis GrevilleIsthmia enervis EhrenbergOdontella awita (Lyngbye) AgardliTriceratiumfavus iqwdrata GrunowTriceratiumpentacrinus EhrenbergTerpsinoe miisica EhrenbergHemidisais hardmardanus (Greville) ManAstenonella notata Grunow

Asterionellopsis glacialis (Castracane) RoundClimacosphenia moniligera EhrenbergFragilariacapuciriaDcsmazieKS&, KutzingGrammatophora hamulifera KutzingGrammatophora marina (Lyngjbye) KutzingGrammatophora oceanica EhrenbergLicmophora abbreviata AgardhPodocystis adriatica KutzingRhabdonema adriaticum KutzingRliabdonemapwictatum (Harvey & Bailey) StodderStriatella interrupta (Ehrenberg) HeibergSynedraspTlialassionema nitzschioides GrunowThalassiothrixfrauenfeldii GrunowAchnanthes brevipes AgardhCampyloneis grevillei (Wm. Smith) GrunowDiploneis spGyrosigma balticum (Ehrenberg) RabenhorstLyrella lyra (Ehrenberg) KarajevaMastogloiasplendida(GrQV\[\e) GrunowNavicula Immerosa BrebissonNavicula spPinnularia nobilis EhrenbergAmplwra aj"enai"ia DonkinAmphiprora alata (Ehrenberg) KutzingBacillariapaxillifer GmelinCylindivthecadostejium (Ehrenberg) Reiman&LewisNi(zschialongissima(BrQb\sson) GrunowNitzschiapungens var atlantica CleveNitzschia scalaris (Ehrenberg) Wm. SmithNitzschia sigma (Kutzing) Wm. SmithCampylodiscus biangulatus GrevilleCainpylodiscus ctypeus EhrenbergSiirirellafastuosa EhrenbergSwirellafebigerii LewisSimrella sp

The zooplankton was essentially composed of typical marine estuarinespecies. The most diversified taxon was Rotifera (28 species and 2 varieties)followed by Copepoda (21 species) and Tintinnina (11 species). Most of theRotifera were limnetic estuarine and had less than 1% of numerical abundance.Most abundant were Rotaria rotatoria, Rotaria sp, Platyias quadhcornis,Brachionus plicatilis and Filinia longiseta, all eutrophy indicators.

Among the Copepoda it was distinguished a dominant group of marineeuryhaline species: Paracalanus crassirostris, Acartia lilljeborgi, Oithonahebes, O. oswaldocruzi and Euterpina acutifrons.



Among Tintinnina Leprotintinnus nordqvisti was dominant. The mostfrequent meroplanktonic group was Bivalvia veliger followed by Cirripedianauplii. Meroplanktonic larval recruitment was reduced by landing, dredgingand low estuary-ocean communication.

Total zooplankton density varied from 585 org.m to 65,989 org.m'l Thedry season presented higher abundance (Figure 2). Copepoda (Paracalanuscrassirostris and Oithona hebes) was the most abundant group (maximum23,690 org.m'3).

Table 3. List of the zooplankton (without ROTIFERA) recorded at the Ipojuca RiverEstuary in August/90 (rainy season) and January/91 (dry season).* tycoplankton

TESTACEAArcellavulgaris Ehrenberg, 1838Arcella dentata Ehrenberg, 1838

Centropyxis acureata Stein, 1840FORAMTN1FERA*Textulariasp* Quinqueloculina sp* Planispirillina denticulata (Brady, 1884)Globorotalia spTretornphalus bulloides d'Orbigny 1826RADIOLARIA (Spumellaria)TINTINNIDALeprotintinnus nordqvisti (Brandt, 1906)Tintinnopsis compressa Daday. 1 887Tintinnopsis lobiancoi Daday, 1887Tuitinnopsis mortensenii Schmidt 1901Tintinnopsis directa Hada, 1932Tintinnopsis tocantinensis Kofoid& Campbell, 1929Codonellopsis morchella (Cleve, 1900)Favella a W ^ (Oapai & Laadimann, 1858)

l, 1881)

Eutintinniis tennis Kofoid & Campbell, 1929HYDROIDA - Obelia spS1PHONOPHORAE (others) -Izw/aspNEMATODAGASTROPODA (veliger)PELECYPODA (veliger)POLYCHAETAMaupasia spNereis sp (larvae)COPEPODAParacalanus quasimodo Bowman, 1 97 1Paracalanus crassirostris?. Dahl, 1894

Centropages velificatus (Oliveira, 1947)

Calanopia americana F. Dahl, 1894LabidocerafluviatilisE. Dahl 1894AcartialilljeborgiGiesbrocfa, 1892Oithona nana Giesbrecht, 1892Oithona hebes Giesbrecht 1891Oithona oswaldocruzi Oliveira, 1945Halicyclops oraeeburnensis Lindberg, 1957Halicyclops thermophilus Kiefer, 1929

Coiycaeusgiesbrechti¥. Dahl, 1894Euterpina acutifrons (Dana, 1852)*Nifroca sp 1*Nifroca sp 2*Longipedia spNatwopuspalusfris Brady, 1880*Ecriinosomatidae*(%GfzcQ3np6# /WKyywW (Blanchad &Ridiaid, 1891)CIRRIPEDIALepas sp(nauplius)Balanus sp (nauplius and cypris)ISOPODA(manca)AMPHIPODAPENAEIDAE (mysis)SEGEST1DAE-Luciferfaxoni Borradaile, 1915BRACHYURA (zoea and megalopa)INSECTA (larvae)BRYOZOA (cyphonauta)CHAEIOGNAIHA -6qgz%z rg/wA9 Conant, 18%LARVACEAOikopleura longicauda (Vogt, 1854)OikopleuradioicaFol, 1872Fritillaria spQSTEICHTHYES (egg and larvae)



Table 4. List of the ROTIFERA recorded at the Ipojuca River Estuary inAugust/90 (rainy season) and January/91 (dry season). ).* tycoplankton

*Rotariamtatoria(Pattas, 1766) *Lecanepapuana (Murray, 1913)*Rotaria neptunia (Ehrenberg, 1832) *Lecane leontiw (Turner, 1892)

*Lecanefiti'cata (Murray, 1913)*Lecane unguitata (Fadeew, 1925)*Lecanestenroasi(MQissii\er, 1908)*Lecane lunaris (Ehrenberg, 1832)*I cme W/a (Gosse, 1886)*Lecawquadridentata(E\\rzrkxxg, 1832)*Lecane sp*Cephalodellasp

, 1832) PofyarthravulgarisCzrlm 1943, 1886) Aspkwckna sp

3. F. Muller, 1786) *Testudiwllapatina (Hermann, 1783)*Lecane ciirvicomis (Murray, 1913) Filinia longiseta (Ehrenberg, 1834)

F. Muller, 1776)

Platyias quadricomis (Ehrenberg, 1832)*Bmchionuspatuluspatulus (O. F. Muller, 1786)*Brachionuspatuh4s macracanthus (Daday, 1905)Bivdwnus quadridentatus w#i3My(Daday, 1897)

Bmchionnsplicotilis (0. F. Muller, 1786), 1851)

PHYTOPLANKTON

200000018000001600000140000012000001000000800000600000400000200000

0

RAINY SEASON DRYSEASON

£E>o

ZOOPLANKTON

70000600005000040000300002000010000

0o o o o o o oCO CO CO CO CO CO CO£ g T- ro «o r£ o>

RAINY SEASON5 S

3 8 8 8 r oi ^ co T-: co inDRY SEASON

Figure 2-Plankton density at the Ipojuca River Estuary, Pernambuco, Brazil, inAugust/90 (rainy season) and January/91 (dry season).



At the rainy season it was registered a peak of zooplankton at 7:30 h and atthe dry season two peaks were registered one at 9:30 h and another smaller at20:30 h. Phytoplankton presented similar peaks which match inversely thezooplankton, showing intense grazing.

Plankton Species Diversity was high (> 3 bits.ind"') in most samples. Nosignificant difference was observed between tides and seasons. Eveness wasalso high (> 0.5). The high diversity can be explained by the spatialheterogeneity.

Plankton species association presented 3 groups: i) marine planktonic; ii)marine-littoral and tycoplankton; iii) and marine estuarine residents. The lowcorrelations in cluster mean according to Guzman del Proo et al? a complexfood web. All these groups were most composed of r-strategists. However, in aconstant impacted estuary many organisms are living in their maximumtolerance limit (Neumann-Leitao & Matsumura-Tundisi®).

The 3 first Principal components were responsable for 52.97% of thevariance. The first axis (21,04% of the variance) was related to the greaterplankton abundance and contained the more frequent taxa in the area (marineestuarine residents); this group was influenced by salinity, transparence,dissolved oxygen and pH. Axis 2 (17,39% of the variance) was related to themarine littoral and tycoplankton. Axis 3 (14.54% of the variance) associatedthe eutrophic indicators species to nutrients, chlorophyll a and low oxygen. Thearea balance was strongly affected suggesting a disturbed plankton community.

5 References

1. Cavalcanti, L. B., Coelho, P. A., Eskinazi-Leca, E., Luna, J. A. C., Macedo,S. J. & Paranagua, M.N. Condiciones ecologicas en el area de Suape(Pernambuco - Brasil). Mem. del Seminario sobre el Estudio Cientifico eImpacto Humano en el Ecossistema de Manglares, ed. UNESCO, OficinaRegional de Ciencia y Tecnologia para America Latina y el Caribe, Cali,pp. 243-256, 1980.

2. Eskinazi-Leca, E. & Koening, M. L. Distribuicao das diatomaceas(Bacillariophyceae) na area de Suape (Pernambuco-Brasil). TrabalhosOceanogrdficos da Universidade Federal de Pernambuco, 19, pp. 73-100,1985/86.

3. Gusman del Proo, S. A., Chavez, E. A., Alatriste, F. M., Campa, S., Cruz,G., Gomez, L., Guadarrama, R., Guerra, A., Mille, S. & Torruco, D. Theimpact of the Ixtoc-I oil spill on zooplankton. Journal of Plankton/feyewc/z, 8 (3), pp. 557-581, 1986.

4. Melo Filho, J. A. S. Caracterizacao da situacao atual da area ProgramaSuape sob o ponto de vista poluicao ambiental. Recife, CONDEPE,Comunicaqao Tecnica, 1, pp. 1-15, 1977.



5. Neumann, V. H. M. L., Queiroz, C. M. & Ivo, P. S. Bottom sediments ofthe Suape lagoon, Pernambuco - Brazil. Proc. of the 14^ InternationalSedimentological Congress, Recife, 1994.

6. Neumann, V. H., Medeiros, C., Parente, L., Neumann-Leitao, S. &Koening, M. L. Hydrodynamism, Sedimentology, Geomorphology andPlankton Changes at Suape Area (Pernambuco - Brazil) after a PortComplex Implantation. Anais da Academia Brasileira de Cencias, 70(2),pp. 313-323, 1998.

7. Neumann-Leitao, S., Paranagua, M. N. & Valentin, J. L. Ecology ofplanktonic rotifers of the estuarine lagunar complex at Suape, Pernambuco(Brazil). Hydrobiologia, 232, pp. 133-143, 1992.

8. Neumann-Leitao, S & Matsumura Tundisi, T. Dynamics of a perturbedestuarine zooplanktonic community: Port of Suape, PE, Brazil. Verh.

., 26, pp. 1981-1988, 1998.

9. Paranagua, M. N. Zooplankton of Suape area (Pernambuco-Brazil).Trabalhos Oceanogrdficos da Universidade Federal de Pernambuco, 19,pp. 113-124, 1985/86.

10. Shannon, C. E. A mathematical theory of communication. Boll. Syst. Tech.J. 27, pp. 379-423, 1948.

11. Strickland, J. D. H. & Parsons, T. R. Production organic matter in theprimary stages of marine food chain. Chemical oceanography, eds. J.P.Riley & B. Kirrow, London, Academic Press, pp. 477-610, 1963.

12. Strickland, J. D. H. & Parsons, T. R. A manual of seawater analysis.Bulletin Fisheries Research Board of Canada, 125, pp. 1-205, 1965.


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