Enteric bacteria in Olrog’s Gull (Larus atlanticus) and Kelp Gull (Larus dominicanus) from the Bahía Blanca Estuary, Argentina

Luciano F. La Sala; Pablo F. Petracci; Viviana Randazzo; Mariano E. Fernández-Miyakawa

doi:10.56178/eh.v28i2.629

Artículos Publicado 01 diciembre 2013 https://doi.org/10.56178/eh.v28i2.629

Bacterias entéricas en la Gaviota Cangrejera (Larus atlanticus) y la Gaviota Cocinera (Larus dominicanus) en el estuario de Bahía Blanca, Argentina

contaminación microbiológica especies centinela estuario de Bahía Blanca Gaviota Cangrejera Gaviota Cocinera Larus atlanticus Larus dominicanus patógenos zoonóticos

Luciano F. La Sala Centro de Estudios Cuantitativos en Sanidad Animal (CECSA). Boulevard Ovidio Lagos y Ruta 33, 2170 Casilda, Santa Fe, Argentina | Cátedra de Epidemiología, Universidad Nacional del Sur. San Juan 670, 8000 Bahía Blanca, Buenos Aires, Argentina

Pablo F. Petracci Programa de Conservación de la Gaviota Cangrejera en el Estuario de Bahía Blanca. Patricios 712, 8000 Bahía Blanca, Buenos Aires, Argentina

Viviana Randazzo Cátedra de Parasitología Clínica, Universidad Nacional del Sur. San Juan 670, 8000 Bahía Blanca, Buenos Aires, Argentina

Mariano E. Fernández-Miyakawa Instituto de Patobiología, Centro Nacional de Investigaciones Agropecuarias, Instituto Nacional de Tecnología Agropecuaria. Los Reseros y Las Cabañas, 1712 Castelar, Buenos Aires, Argentina

Resumen

El estuario de Bahía Blanca en Argentina se encuentra bajo el efecto de la contaminación microbiológica a partir del vertido de desagües cloacales sin tratamiento previo y los patógenos asociados. En este estuario existen colonias reproductivas de Gaviota Cangrejera (Larus atlanticus) y Gaviota Cocinera (Larus dominicanus) y los adultos alimentan a sus crías con presas obtenidas en sitios contaminados con desagües cloacales y en basurales a cielo abierto donde pueden estar expuestas a patógenos de origen humano y animal. El objetivo de este estudio fue evaluar el rol de la Gaviota Cangrejera y de la Gaviota Cocinera como portadores de patógenos zoonóticos de origen fecal. A partir de las muestras de material fecal se recuperaron Salmonella enterica var. Typhimurium, Salmonella enterica var. Gallinarum, Escherichia coli, Shigella dysenteriae, Enterobacter cloacae y Klebsiella pneumoniae. La prevalencia y diversidad de patógenos varió entre las dos especies de gaviotas, y la Gaviota Cangrejera fue positiva para una mayor variedad de patógenos que la Gaviota Cocinera. Escherichia coli fue la bacteria más prevalente en pichones y adultos de ambas especies, seguida por Salmonella spp. en pichones de Gaviota Cangrejera, y Enterobacter cloacae y Shigella dysenteriae en adultos de Gaviota Cangrejera. Se propone el uso de estas especies de gaviotas como centinelas de contaminación microbiológica en el estuario de Bahía Blanca.

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Referencias

ALBARNAZ JD, TOSO J, CORREA AA, SIMOES CM ANDBARARDIAB CRM (2007) Relationship between thecontamination of gulls (Larus dominicanus) and oys-ters (Crassostrea gigas) with Salmonella serovarTyphimurium by PCR-RFLP. International Journal ofEnvironmental HealthResearch 17:133–140
BREZINA SS AND BALDINI MD (2008) Detection ofsomatic coliphages as indicators of faecal contami-nation in estuarine waters. Revista Argentina deMicrobiología 40:72–74
BUTTERFIELD J, COULSON JC, KEARSEY SV AND MONA-GHAN P (1983) The herring gull Larus argentatus as acarrier of salmonella. Journal of Hygiene 91:429–436
CÍZEK A, LITERÁK I, HEJLÍCEK K, TREML F AND SMOLA J(1994) Salmonella contamination in the environmentand its incidence in wild birds. Journal of VeterinaryMedicine B 41:320–327
COULSON JC, BUTTERFIELD J AND THOMAS C (1983) Theherring gull Larus argentatus as a likely transmittingagent of Salmonella montevideo to sheep and cattle.Journal of Hygiene 91:437–443
COULSON R AND COULSON G (1993) Diets of the PacificGull Larus pacificus and the Kelp Gull Larusdominicanus in Tasmania. Emu 93:50–53
CRAMP S (1983) Handbook of the birds of Europe, theMiddle East and North Africa. The birds of the WesternPalearctic. Volume 3. Waders to gulls. Oxford Univer-sity Press, Oxford
DELHEY JKV, CARRETE M AND MARTÍNEZ M (2001a) Dietand feeding behaviour of Olrog’s gull Larus atlanti-cus in Bahía Blanca, Argentina. Ardea 89:319–329
DELHEY JKV, PETRACCI PF AND GRASSINI CM (2001b)Hallazgo de una nueva colonia de Gaviota de Olrog(Larus atlanticus) en la ría de Bahía Blanca, Argen-tina. Hornero 16:39–42
FENLON DR (1983) A comparison of salmonellaserotypes found in the faeces of gulls feeding at asewage works with serotypes present in the sew-age. Journal of Hygiene 91:47–52
FERNS PN AND MUDGE GP (2000) Abundance, diet andSalmonella contamination of gulls feeding at sew-age outfalls. Water Research 34:2653–2660
FLEISHER JM, KAY D, WYERA MD AND GODFREE AF(1998) Estimates of the severity of illnesses associ-ated with bathing in marine recreational waterscontaminated with domestic sewage. InternationalJournal of Epidemiology 27:722–726
FOSTER G, EVANS J, KNIGHT HI, SMITH AW, GUNN GJ,ALLISON LJ, SYNGE BA AND PENNYCOTT TW (2006)Analysis of feces samples collected from a wild-birdgarden feeding station in Scotland for the presenceof verocytotoxin-producing Escherichia coli O157.Applied and Environmental Microbiology 72:2265–2267
FRERE E, GANDINI P AND MARTÍNEZ PR (2000) Gaviotacocinera (Larus dominicanus) como vector potencialde patógenos en la costa Patagónica. Hornero15:93–97
GIRDWOOD RWA, FRICKER CR, MUNRO D, SHEDDEN CBAND MONAGHAN P (1985) The incidence and signifi-cance of salmonella carriage by gulls (Larus spp.) inScotland. Journal of Hygiene 95:229–241
HENDRIKSEN RS, VIEIRA AR, KARLSMOSE S, LO FOWONG DM, JENSEN AB, WEGENER HC ANDAARESTRUP FM (2011) Global monitoring of Salmo-nella serovar distribution from the World HealthOrganization Global Foodborne Infections NetworkCountry Data Bank: results of quality assured labo-ratories from 2001 to 2007. Foodborne Pathogens andDisease 8:887–900
HUBÁLEK Z (2004) An annotated checklist of patho-genic microorganisms associated with migratorybirds. Journal of Wildlife Diseases 40:639–659
KAPPERUD G, STENWIG H AND LASSEN J (1998) Epide-miology of Salmonella typhimurium O:4-12 infectionin Norway: evidence of transmission from an avianwildlife reservoir. American Journal of Epidemiology147:774–782
KARAGÜZEL A, KÖKSAL I, BAKI A, UÇAR F, GÖK I ANDCIRAV Z (1993) Salmonella and Shigella carriage bygulls (Larus sp.) on the east Black Sea region of Tur-key. Microbios 74:77–80
KAY D, FLEISHER JM, SALMON RI, JONES F, WYER MD,GODFREE AF, ZELENAUCH-JACQUOTTE Z AND SHORE R(1994) Predicting likelihood of gastro-enteritis fromsea bathing: results form randomized exposure.Lancet 344:905–909
KOBAYASHI H, POHJANVIRTA T AND PELKONEN S (2002)Prevalence and characteristics of intimin- and shigatoxin-producing Escherichia coli from gulls, pigeonsand broilers in Finland. Journal of Veterinary MedicalSciences 64:1071–1073
KOTLOFF KL, WINICKOFF JP, IVANOFF B, CLEMENS JD,SWERDLOW DL, SANSONETTI PJ, ADAK GK AND LEVINEMM (1999) Global burden of Shigella infections:implications for vaccine development and imple-mentation of control strategies. Bulletin of the WorldHealth Organization 77:651–666
LÓPEZ-MARTÍN J, TANIA J, RIQUELME F, CONTRERAS CAND GONZÁLEZ-ACUÑA D (2011) Detección deespecies de Salmonella y Mycobacterium en gaviotasdominicanas (Larus dominicanus) y gaviotas deFranklin (Leucophaeus pipixcan) en la ciudad deTalcahuano, Chile. Revista Médica de Chile139:1496–1502
MAKINO S, KOBORI H, ASAKURA H, WATARAI M,SHIRAHATA T, IKEDA T, TAKESHI K AND TSUKAMOTO T(2000) Detection and characterization of shiga toxin-producing Escherichia coli from seagulls. Epidemiol-ogy and Infection 125:55–61
MONAGHAN P, SHEDDEN CB, ENSOR K, FRICKER CR ANDGIRDWOOD RWA (1985) Salmonella carriage by her-ring gulls in the Clyde area of Scotland in relationto their feeding ecology. Journal of Applied Ecology22:669–680
PETRACCI P, LA SALA LF, AGUERRE G, PÉREZ C, ACOSTAN, SOTELO M AND PAMPARANA C (2004) Dieta de laGaviota Cocinera (Larus dominicanus) durante elperíodo reproductivo en el estuario de Bahía Blan-ca, Buenos Aires, Argentina. Hornero 19:23–28
PRUSS A (1998) Review of epidemiological studies onhealth effects from exposure to recreational waters.International Journal of Epidemiology 27:1–9
QUESSY S AND MESSIER S (1992) Prevalence of Salmo-nella spp., Campylobacter spp., and Listeria spp. inring-billed gulls (Larus delawarensis). Journal of Wild-life Diseases 28:526–531
REILLY WJ, FORBES CI, PATERSON CM AND SHARP JCM(1981) Human and animal salmonellosis in Scotlandassociated with environmental contamination,1973–79. Veterinary Record 108:553–555
ROBINSON RA AND DANIEL MJ (1968) The significance ofSalmonella isolations from wild birds and rats in NewZealand. New Zealand Veterinary Journal 16:53–55
STREITENBERGER ME AND BALDINI MD (2010) Deteriorode un área recreacional por efectos del volcado delíquidos cloacales. Revista Argentina de Microbiología42:307–310
TIZARD I (2004) Salmonellosis in wild birds. Seminarsin Avian and Exotic Pet Medicine 13:50–66
US ENVIRONMENTAL PROTECTION AGENCY (2003)Bacterial water quality standards for recreational waters(freshwater and marine waters). Status report. USEnvironmental Protection Agency ReportEPA-823-R-03-008, Washington DC
WALLACE JS, CHEASTY T AND JONES K (1997) Isolationof vero cytotoxin-producing Escherichia coli O157 fromwild bids. Journal of Applied Microbiology 82:399–404
YORIO P, BERTELLOTTI M AND GARCÍA BORBOROGLU P(2005) Estado poblacional y de conservación degaviotas que se reproducen en el litoral marítimoargentino. Hornero 20:53–74

Cómo citar

Luciano F. La Sala, Pablo F. Petracci, Viviana Randazzo, Mariano E. Fernández-Miyakawa (2013). Bacterias entéricas en la Gaviota Cangrejera (Larus atlanticus) y la Gaviota Cocinera (Larus dominicanus) en el estuario de Bahía Blanca, Argentina. El Hornero, Vol. 28 Núm. 2 (2013), 59-64. https://doi.org/10.56178/eh.v28i2.629

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[1] ALBARNAZ JD, TOSO J, CORREA AA, SIMOES CM ANDBARARDIAB CRM (2007) Relationship between thecontamination of gulls (Larus dominicanus) and oys-ters (Crassostrea gigas) with Salmonella serovarTyphimurium by PCR-RFLP. International Journal ofEnvironmental HealthResearch 17:133–140

[2] BREZINA SS AND BALDINI MD (2008) Detection ofsomatic coliphages as indicators of faecal contami-nation in estuarine waters. Revista Argentina deMicrobiología 40:72–74

[3] BUTTERFIELD J, COULSON JC, KEARSEY SV AND MONA-GHAN P (1983) The herring gull Larus argentatus as acarrier of salmonella. Journal of Hygiene 91:429–436

[4] CÍZEK A, LITERÁK I, HEJLÍCEK K, TREML F AND SMOLA J(1994) Salmonella contamination in the environmentand its incidence in wild birds. Journal of VeterinaryMedicine B 41:320–327

[5] COULSON JC, BUTTERFIELD J AND THOMAS C (1983) Theherring gull Larus argentatus as a likely transmittingagent of Salmonella montevideo to sheep and cattle.Journal of Hygiene 91:437–443

[6] COULSON R AND COULSON G (1993) Diets of the PacificGull Larus pacificus and the Kelp Gull Larusdominicanus in Tasmania. Emu 93:50–53

[7] CRAMP S (1983) Handbook of the birds of Europe, theMiddle East and North Africa. The birds of the WesternPalearctic. Volume 3. Waders to gulls. Oxford Univer-sity Press, Oxford

[8] DELHEY JKV, CARRETE M AND MARTÍNEZ M (2001a) Dietand feeding behaviour of Olrog’s gull Larus atlanti-cus in Bahía Blanca, Argentina. Ardea 89:319–329

[9] DELHEY JKV, PETRACCI PF AND GRASSINI CM (2001b)Hallazgo de una nueva colonia de Gaviota de Olrog(Larus atlanticus) en la ría de Bahía Blanca, Argen-tina. Hornero 16:39–42

[10] FENLON DR (1983) A comparison of salmonellaserotypes found in the faeces of gulls feeding at asewage works with serotypes present in the sew-age. Journal of Hygiene 91:47–52

[11] FERNS PN AND MUDGE GP (2000) Abundance, diet andSalmonella contamination of gulls feeding at sew-age outfalls. Water Research 34:2653–2660

[12] FLEISHER JM, KAY D, WYERA MD AND GODFREE AF(1998) Estimates of the severity of illnesses associ-ated with bathing in marine recreational waterscontaminated with domestic sewage. InternationalJournal of Epidemiology 27:722–726

[13] FOSTER G, EVANS J, KNIGHT HI, SMITH AW, GUNN GJ,ALLISON LJ, SYNGE BA AND PENNYCOTT TW (2006)Analysis of feces samples collected from a wild-birdgarden feeding station in Scotland for the presenceof verocytotoxin-producing Escherichia coli O157.Applied and Environmental Microbiology 72:2265–2267

[14] FRERE E, GANDINI P AND MARTÍNEZ PR (2000) Gaviotacocinera (Larus dominicanus) como vector potencialde patógenos en la costa Patagónica. Hornero15:93–97

[15] GIRDWOOD RWA, FRICKER CR, MUNRO D, SHEDDEN CBAND MONAGHAN P (1985) The incidence and signifi-cance of salmonella carriage by gulls (Larus spp.) inScotland. Journal of Hygiene 95:229–241

[16] HENDRIKSEN RS, VIEIRA AR, KARLSMOSE S, LO FOWONG DM, JENSEN AB, WEGENER HC ANDAARESTRUP FM (2011) Global monitoring of Salmo-nella serovar distribution from the World HealthOrganization Global Foodborne Infections NetworkCountry Data Bank: results of quality assured labo-ratories from 2001 to 2007. Foodborne Pathogens andDisease 8:887–900

[17] HUBÁLEK Z (2004) An annotated checklist of patho-genic microorganisms associated with migratorybirds. Journal of Wildlife Diseases 40:639–659

[18] KAPPERUD G, STENWIG H AND LASSEN J (1998) Epide-miology of Salmonella typhimurium O:4-12 infectionin Norway: evidence of transmission from an avianwildlife reservoir. American Journal of Epidemiology147:774–782

[19] KARAGÜZEL A, KÖKSAL I, BAKI A, UÇAR F, GÖK I ANDCIRAV Z (1993) Salmonella and Shigella carriage bygulls (Larus sp.) on the east Black Sea region of Tur-key. Microbios 74:77–80

[20] KAY D, FLEISHER JM, SALMON RI, JONES F, WYER MD,GODFREE AF, ZELENAUCH-JACQUOTTE Z AND SHORE R(1994) Predicting likelihood of gastro-enteritis fromsea bathing: results form randomized exposure.Lancet 344:905–909

[21] KOBAYASHI H, POHJANVIRTA T AND PELKONEN S (2002)Prevalence and characteristics of intimin- and shigatoxin-producing Escherichia coli from gulls, pigeonsand broilers in Finland. Journal of Veterinary MedicalSciences 64:1071–1073

[22] KOTLOFF KL, WINICKOFF JP, IVANOFF B, CLEMENS JD,SWERDLOW DL, SANSONETTI PJ, ADAK GK AND LEVINEMM (1999) Global burden of Shigella infections:implications for vaccine development and imple-mentation of control strategies. Bulletin of the WorldHealth Organization 77:651–666

[23] LÓPEZ-MARTÍN J, TANIA J, RIQUELME F, CONTRERAS CAND GONZÁLEZ-ACUÑA D (2011) Detección deespecies de Salmonella y Mycobacterium en gaviotasdominicanas (Larus dominicanus) y gaviotas deFranklin (Leucophaeus pipixcan) en la ciudad deTalcahuano, Chile. Revista Médica de Chile139:1496–1502

[24] MAKINO S, KOBORI H, ASAKURA H, WATARAI M,SHIRAHATA T, IKEDA T, TAKESHI K AND TSUKAMOTO T(2000) Detection and characterization of shiga toxin-producing Escherichia coli from seagulls. Epidemiol-ogy and Infection 125:55–61

[25] MONAGHAN P, SHEDDEN CB, ENSOR K, FRICKER CR ANDGIRDWOOD RWA (1985) Salmonella carriage by her-ring gulls in the Clyde area of Scotland in relationto their feeding ecology. Journal of Applied Ecology22:669–680

[26] PETRACCI P, LA SALA LF, AGUERRE G, PÉREZ C, ACOSTAN, SOTELO M AND PAMPARANA C (2004) Dieta de laGaviota Cocinera (Larus dominicanus) durante elperíodo reproductivo en el estuario de Bahía Blan-ca, Buenos Aires, Argentina. Hornero 19:23–28

[27] PRUSS A (1998) Review of epidemiological studies onhealth effects from exposure to recreational waters.International Journal of Epidemiology 27:1–9

[28] QUESSY S AND MESSIER S (1992) Prevalence of Salmo-nella spp., Campylobacter spp., and Listeria spp. inring-billed gulls (Larus delawarensis). Journal of Wild-life Diseases 28:526–531

[29] REILLY WJ, FORBES CI, PATERSON CM AND SHARP JCM(1981) Human and animal salmonellosis in Scotlandassociated with environmental contamination,1973–79. Veterinary Record 108:553–555

[30] ROBINSON RA AND DANIEL MJ (1968) The significance ofSalmonella isolations from wild birds and rats in NewZealand. New Zealand Veterinary Journal 16:53–55

[31] STREITENBERGER ME AND BALDINI MD (2010) Deteriorode un área recreacional por efectos del volcado delíquidos cloacales. Revista Argentina de Microbiología42:307–310

[32] TIZARD I (2004) Salmonellosis in wild birds. Seminarsin Avian and Exotic Pet Medicine 13:50–66

[33] US ENVIRONMENTAL PROTECTION AGENCY (2003)Bacterial water quality standards for recreational waters(freshwater and marine waters). Status report. USEnvironmental Protection Agency ReportEPA-823-R-03-008, Washington DC

[34] WALLACE JS, CHEASTY T AND JONES K (1997) Isolationof vero cytotoxin-producing Escherichia coli O157 fromwild bids. Journal of Applied Microbiology 82:399–404

[35] YORIO P, BERTELLOTTI M AND GARCÍA BORBOROGLU P(2005) Estado poblacional y de conservación degaviotas que se reproducen en el litoral marítimoargentino. Hornero 20:53–74