Universidad Veracruzana
Instituto de Biotecnología y Ecología Aplicada
MAESTRÍA EN CIENCIAS EN ECOLOGÍA Y BIOTECNOLOGÍA
METALES PESADOS EN AVES RAPACES RESIDENTES Y MIGRATORIAS EN VERACRUZ, MÉXICO
TESIS
PARA OBTENER EL GRADO DE MAESTRA EN CIENCIAS EN ECOLOGÍA Y BIOTECNOLOGÍA
PRESENTA
MEAGAN LINDSEY CAMPBELL
DIRECTOR
DR. ERNESTO RUELAS INZUNZA
ASESORES
Dirección General de Investigaciones Instituto de Biotecnología y Ecología Aplicada
Coordinación del Posgrado
MAESTRÍA EN CIENCIAS EN ECOLOGÍA Y BIOTECNOLOGÍA
ECOBIOT-18DAR
DECLARATORIA DE AUTORIA
Quien suscribe Meagan Lindsey Campbell (S16017543) estudiante de la Maestría en Ciencias en Ecología y Biotecnología, hace constar que es autor del Trabajo para la obtención del Grado de Maestría intitulado: Heavy metals in resident and migratory raptors in Veracruz, Mexico el cual constituye la elaboración personal realizada
únicamente con la Dirección del Comité Tutoral siguiente: Dr. Ernesto Ruelas Inzunza,
Dr. Jaime Rendón Von Osten, Dr. Enrique Alarcón Gutierrez.
En tal sentido, manifiesto la originalidad de los conceptos, base de datos registrados (Bitácora), interpretación de los datos, conclusiones y recomendaciones. Por último, dejo establecido que los aportes intelectuales de otros autores se han referido debidamente en el texto y en la sección de literatura citada de dicho trabajo.
___________________________ Meagan Lindsey Campbell
Dirección General de Investigaciones Instituto de Biotecnología y Ecología Aplicada
Coordinación de Posgrado
MAESTRÍA EN CIENCIAS EN ECOLOGÍA Y
BIOTECNOLOGÍA
ECOBIOT-17A
AGRADECIMIENTOS Y CREDITOS INSTITUCIONALES
El presente trabajo se realizó bajo la dirección del Dr. Ernesto Ruelas Inzunza dentro de la Línea de Generación y Aplicación del Conocimiento: Organismos, ambiente y sus interacciones, pertenecientes a el Cuerpo Académico: Clave “CA-UVER-324” Nombre
Estructura y Funcionamiento de Ecosistemas registrados en el Instituto de Biotecnología y Ecología Aplicada de la Universidad Veracruzana en Xalapa, Veracruz.
El trabajo de Maestría se desarrolló dentro del proyecto: Heavy metals in resident and migratory raptors in Veracruz, Mexico, Aprobado por el fondo CONACYT, APIVER API-GS-CS-62601-046-17 mismo al que se le agradece su apoyo.
Se agradece al Consejo Nacional de Ciencia y Tecnología (CONACYT) por su apoyo al estudiante con una beca académica bajo el No de becario 607620.
Se agradece al programa de posgrado de Maestría en Ciencias en Ecología y Biotecnología, siendo el Coordinador el Dr. Antonio Andrade Torres y al Instituto de Biotecnología y
Xalapa de Enríquez, Veracruz, junio de 2018.
Agradecimientos:
Al Instituto de Biotecnología y Ecología Aplicada por su apoyo a mi tiempo y aprendizaje en su institución, a mi formación profesional y académico. El espacio fue único para mi durante mi tiempo en México, y agradezco el ambiente entre estudiantes y profesores de respeto y apoyo.
A Pronatura Veracruz, A.C. Proyecto Río de Rapaces por la oportunidad de colaboración, y capacitación.
Al Dr. Ernesto Ruelas Inzunza por su dirección de mi tesis. Su consejo, y conocimiento del mundo académico han sido claves en el proceso de mi proyecto.
Al Dr. Jaime Rendón Von Osten. Su asesoría de ecotoxicología y la química de metales pesados apoyó a mi entendimiento de mi trabajo. También el acceso a su laboratorio permitió el análisis de mis muestras. Su ánimo es contagioso que fortalece a los miembros de su laboratorio en ser motivados.
Al Dr. Enrique Alarcón-Gutiérrez por su asesoría en la ordenación de mi proyecto y el análisis estadístico. Su perspectiva en como ordenar, y analizar mi trabajo me ayudó mucho en la clarificación.
Al Mtro. Mauricio González-Jáuregui por su ayuda con el análisis de mis datos después de mi primer ronda, pero también su apoyo a mi investigación y tiempo en Campeche.
Al Mtro. Jimmy Vidal Maldonado por su paciencia durante mi análisis de voltamperometría, y enseñanza.
A mi jurado Dra. Yareni Perroni, Dr. Jorge Galindo Gonzalez, Mtro. Mauricio
González-Jáuregui, y Dr. Angel I. Ortiz Ceballos por sus revisiones y retroalimentación valioso a mi proyecto.
A los profesores de INBIOTECA. Dado que tuvieron mucha paciencia en mi formación
acá entre las diferencias culturales, mi falta de tiempo entre clase y campo, y el idioma.
A mis compañeros de la generación de 2016-2018. Somos una familia, y quedamos muy
unidos después de la graduación.
Xalapa, Veracruz, Junio 2018
Dedicatoria:
Yo dedico este trabajo a varios compañeros que me han inspirado en mi camino profesional. Antes de ellos, me formaba mi familia:
A mi abuela Wilma Jean Blair, por siempre enseñarme que valgo el mismo tiempo que
todos, y que siempre hay espacio para expresar mi opinión. Sobre todo, me da fuerza y optimismo.
A mi abuelo Carl David Campbell, que siempre decía que las cosas más importantes en la
vida son la familia y la educación. Durante su vida hizo todo lo posible para apoyar estos valores en nuestra familia y enseñarlos.
A mi abuela Monte Middlebusher Campbell quien siempre escuchaba mis dudas, y me
enseñó la importancia de viajar y aprender de otras perspectivas.
A mi madre, Julie Kristen Campbell, por su dedicación a mi educación, y apoyo a mis sueños.
A mi padre, Brian Lee Campbell, por enseñarme mi primer rapaz, y plantar la semilla que empezó mi fascinación con la vida silvestre.
A mi esposo, Schuyler Chaim Walling, por darme el espacio de crecer, y escuchar mis sueños como posibilidades en vez de locuras. Sin tu apoyo y paciencia durante estos tres años, sería imposible este trabajo.
A mi hermana, Hannah Jane Campbell Keen, por sus críticas constructivas, y solidaridad. Nadie me conoce como tú.
A mi hermano, Michael Dylan Blair Campbell, por enseñarme tolerancia, y aconsejarme.
A mis compañeros(as): Stephanie Loredo por abrir el mundo de conservación desde la perspectiva de una latinoamericana en un ambiente donde no había mucha conectividad de culturas entre el mundo académico y latinomericano en Oregón. Hemos crecido como pajareras juntas, migrando con ellos siguiendo el aprendizaje.
Al proyecto de Pronatura Veracruz A.C. Río de Rapaces. Me inspiró en querer entender
mejor la maravilla de la migración de las aves rapaces, y entender nuestro impacto como humanos a su viaje. Mi involucración en el proyecto me ha capacitado para dar un gran paso adelante en entender la conservación Mexicana. Estoy encantada con el conteo del otoño y espero seguir observándolo por el resto de mi vida.
Irving Chavez Dominguez por su enseñanza de conocimiento de una vida observando aves, y apoyando mi llegada a Veracruz y seguimiento a la maestría.
A Gustavo Ramón Lara por asesoría en identificaciones, y atrapar la mayoría de mis muestras.
Alfredo Beltrán-Santos, por ser un familiar y apoyo a mi proyecto afuera de mi país natal. A Diana Vasquez-Balbuena por ser mi gemela en un lugar donde puedo ser completamente vulnerable sin juzgarme.
A, Kashmir Wolf Rock, por ver mi potencial, y apoyarme en colaborar con este proyecto (Chichicoatefam!).
A la familia de Jesus Eduardo Martínez-Leyva, Leticia Cruz Paredes, y Selene Anaís
Martinez por su apoyo e interés en tener un proyecto de maestría adentro de la estación de anillado. Me han cuidado como familiares, y aprecio su apoyo.
Mi proyecto ha sido un esfuerzo colectivo, y estoy completamente agradecida a todos (as) los personas involucradas en tomar muestras, revisar mis escritos, alimentarme, y amarme.
Finalmente a las rapaces. Son mis musas que me hicieron llegar a una maestría de ciencias, y que van a inspirarme siempre. Por ser mis musas, tuve la oportunidad de migrar con ellos y aprender.
Gracias,
RESUMEN GENERAL
El estado de Veracruz es uno de los principales corredores para aves rapaces migratorias y
provee una amplia oportunidad de realizar estudios científicos sobre este tipo de aves. Las
aves migratorias pueden adquirir contaminantes en los sitios de anidación o las zonas
invernales. Hay poco conocimiento sobre el efecto de contaminantes durante las estadías
invernales en las aves migratorias y mucho menos en las aves rapaces. El presente proyecto
tuvo como objetivo determinar los niveles de contaminación por los metales pesados (como
zinc (Zn), cobre (Cu), cadmio (Cd), plomo (Pb), mercurio (Hg) y aluminio (Al) ). Las
concentraciones de estos metales en sangre, indican la ingesta dietética reciente, mientras
que las concentraciones en plumas indican la incorporación del contaminante durante la
muda. A partir de muestras de sangre y plumas, busque probar si las aves migratorias tienen
niveles de contaminantes más altos que las residentes, o viceversa. La solución a esta
pregunta de investigación nos puede dar indicaciones el estado del hábitat en Veracruz, así
como el manejo de paisaje y su efecto en las aves rapaces. En este estudio se colectaron
muestras de sangre y plumas de cinco especies de aves rapaces: dos especies migratorias
(Accipiter cooperii, Accipiter striatus) y tres especies residentes (Buteo brachyurus, Falco
femoralies, Rupornis magnirostris) con objetivo de comparar las concentraciones entre los
metales pesados arriba mencionados. Las muestras fueron colectadas durante la migración
de otoño en 2016 y 2017. Ocupando muestras de sangre y plumas se generó conocimiento
de la temporalidad de la exposición a metales pesados por medio de métodos no
destructivos. Por medio de voltamperometría, hice el análsis de Zn, Cu, Cd, Pb, Hg y Al de
194 muestras de sangre y 194 muestras de plumas. Las concentraciones de metales pesados
fueron de 1-2 órdenes de magnitud mayor en plumas que en sangre. Encontré diferencias
entre especies residentes y migratorias. La concentración de metales en la sangre de
residentes (t = -2.527, GL = 73.8, P = 0.013) fue mayor que en las migratorias. Sin
embargo la concentración de metales pesados en plumas fue mayor en migratorias (t =
2.6157, GL=153.31, P = 0.0097). Encontré una correlación negativa entre sangre y plumas
en Zn (Spearman’s rho=-0.363, P<0.0001), también Cu (Spearman’s rho=-0.159, P=0.025),
y Hg (Spearman’s rho=-0.666, P<0.0001). Encontré correlaciones positivas entre sangre y
plumas en Pb (Spearman’s rho=0.547, P<0.0001). No encontré correlaciones entre sangre y
plumas en Cd o Al. Este trabajo nos da información importante sobre la exposición de
ABSTRACT—Veracruz, Mexico, is one of the states with the highest diurnal raptor species richness. It is also a globally significant migratory corridor for raptors, as well as
for other birds. Agriculture, mining, industry, and oil production are possible contamination
sources for birds in this state as well as in the rest of Mexico. The majority of raptor metal
contamination studies occur north of Mexico. Many researchers hence posit that exposure
to metal contaminants is higher in their non-breeding season range. I analyzed blood and
feather samples of raptors to look for traces of six heavy metals (Al, Zn, Cu, Cd, Pb, and
Hg). I took blood and feather samples of 194 Sharp-shinned Hawk (Accipiter striatus),
Cooper’s Hawk (Accipiter cooperii), Aplomado Falcon (Falco femoralis), Short-tailed
Hawk (Buteo brachyurus), and Roadside Hawk (Rupornis magnirostris). I captured most of
the birds during the autumn seasons of 2016 and 2017, at a raptor banding station located
on the coastal plain of Veracruz. From those samples, I analyzed subset of 194 feathers and
194 blood samples using voltammetry. I found statistically significant differences between
resident and migratory species in Hg in blood (residents higher), and Zn in feathers
(migrants with higher concentrations). Metal means between tissues were usually 1-2
orders of magnitude higher in feathers than in blood, with positive correlations in Pb, and
negative correlations in Zn, Cu, and Hg. The high concentrations in Cu, Zn, and Al levels,
as well as the concentration of Pb, are higher than lethal thresholds reported in the
literature. This study is the first to provide information of heavy metal concentrations of
resident and migratory raptors during the autumn migration in Veracruz. These data helps
us further understand the timing and geographic location of heavy metal exposure in
raptors.
Tabla de Contenido
Declaratoria de autoria ... iii
Agradecimientos y creditos institucionales ... iv
Agradecimientos ... v
Dedicatoria ... vi
RESUMEN GENERAL ... viii
Capítulo I Introducción General ... 1
INTRODUCCIÓN ... 2
MARCO TEÓRICO ... 4
ALCANCE DE ESTE TRABAJO ... 6
LITERATURA CITADA ... 7
Capítulo II Contaminant exposure to birds during migration and non-breeding season: A review. ... 10
ABSTRACT ... 12
INTRODUCTION ... 13
Contamination during migration hypothesis ... 14
The mixed-support hypothesis ... 15
Contaminant studies in Latin America ... 15
Organochlorines ... 16
Heavy metals ... 17
Persistent organic pollutants ... 15
Tissues frequently examined ... 17
Exposure Pathways ... 18
Contaminant exposure to migratory birds and future research foci ... 20
ACKNOWLEDGEMENTS ... 21
LITERATURE CITED ... 22
Capítulo III Heavy metals in raptors during their autumn migration ... 28
ABSTRACT ... 29
INTRODUCTION ... 31
METHODS ... 33
Study area ... 33
Collection of samples ... 34
Laboratory analyses ... 35
Statistical analyses ... 36
RESULTS ... 37
Differences between resident and migratory species ... 37
Differences between tissues ... 37
Differences among species ... 38
DISCUSSION ... 40
Differences in resident and migratory and inferred metal exposure ... 40
Tissue differences and timing of exposure... 40
Ecological relevance in species comparisons ... 40
Metal ingestion pathways and toxicity in the literature ... 43
Future research questions developed from the analyses ... 46
ACKNOWLEDGEMENTS ... 47
LITERATURE CITED ... 48
Capítulo IV Conclusión General ... 123
Lista de Tablas y Figuras
Capítulo II
Table 1. Previous avian contamination studies in Latin America………15
Capítulo III
Table 1. Minimum and maximum detection limits (DL) of metals using the Metrohm 747
Computrace voltameter used in this study………49
Table 2. Blood and feather samples of five species raptors collected in……….49 Veracruz, Mexico
Table 3. Means ± standard deviations of metal concentrations by species……….50
Figure 1. The location of the banding station, and trapping area for Roadside hawks. 1) Cansaburro banding station. 2) El Cerro banding stations. 3) The municipality of
Mozomboa. 4) The municipality of Tlalixcoyan…………..………51
Figure 2. Blood means between resident and migratory species with std. dev…..…….52
Figure 3. Feather means between resident and migratory species with std. dev…...…..52
Appendix 1. Frequency of metals by tissue, and species………...….53
Capítulo I
1. INTRODUCCIÓN
En investigaciones previas sobre la adquisición de los contaminantes por aves migratorias
(Lacher et al., 1997, Sodhi et al., 2011), se ha hipotetizado que los contaminantes son
adquiridos en las zonas de anidación (Elliott et al., 2007). Sin embargo, otros estudios en
contraste señalan a las zonas invernales como los lugares donde se presenta la mayor
adquisición de contaminantes (Fyfe et al., 1990). El tema se complica por el hecho de que
varios contaminantes, como los metales pesados, tienen mecanismos de ingestión,
exposición, así como adquisición que son difieren entre sí y de otros químicos.
Hay poco conocimiento sobre el afecto de las estadías anuales en zonas invernales
en las aves migratorias en lo general, y a las aves rapaces en lo particular. Por ejemplo, en
las pampas de Argentina, durante los años de 1995 y 1996, se registraron 5095 muertes de
Buteo swainsonii (Goldstein et al., 1999) como consecuencia del uso del herbicida
organofosfato, monocrótofos, utilizado en los cultivos de soya, algodón, y arroz. Estos
eventos aumentaron la curiosidad de investigar y saber más sobre la contaminación de las
aves rapaces migratorias durante la migración y temporada invernal durante su ciclo anual.
Este caso es uno de los más sobresalientes de mortandad de aves rapaces durante la
temporada invernal. Sin embargo, poco conocemos de otros casos para otras zonas
geográficas en el mundo. Las aves rapaces indican la contaminación por su sensibilidad a
concentraciones de polutantes orgánicos persistentes, y metales pesados por ser
depredadores (Furness, 1993).
Veracruz, , una zona geográfica en la parte central de la costa del Golfo de México
es un embudo geográfico para las aves migratorias, en particular, aves rapaces (Bildstein,
2004). Por ser un corredor migratorio principal entre Norte y Sudamérica, hay grandes
migración de las aves rapaces en Veracruz, generando mucha información sobre su
ecología, así como estimaciones de la variación interanual en las poblaciones de aves que
pasan por los sitios donde se monitorean estas aves (Ruelas et al., 2000).
El hábitat de las aves migratorias ha cambiando rápidamente por el cambio de uso
del suelo: crecimiento de las zonas urbanas, la industria, y la agricultura y ganadería
extensivas (Benítez et al., 2014). Con este paisaje fragmentado se puede contaminar el
ambiente con metales pesados y bioacumularse en la red alimenticia, se podría contaminar
y/o intensificar a las aves rapaces (Tchounwou et al., 2012).
Sabemos sobre el efecto de algunos metales pesados más que de otros. Por ejemplo,
en los Estados Unidos de América y Canadá, se han hecho estudios con mercurio (Hg) y
plomo (Pb) en las aves rapaces (Rattner et al., 2011). El mercurio es un indicador de la
contaminación de varias industrias antropogénicas como la fissión nuclear, refinación de
metales, pesticidas, pilas, y la producción de papel, el cual se acumula en el aire, agua y
suelo (Singh et al., 2011). El plomo es un metal persistente que se puede encontrar en el
ambiente como consecuencia de la industria minera, desechos de municipios, combustibles,
artesanías y pintura (World Health Organization, 2010). En cuanto a sus impactos en la
conservación de las aves rapaces, el plomo también se puede adquirir por medio de balas de
cacería (Pain et al., 2009). El plomo está en los balines de la munición de escopetas, y
varias especies de organismos que cazan los humanos a su vez son presas de las aves
rapaces. Si hay desechos de organismos con postas de plomo, o si sobrevive un organismo
después de que le dispare un cazador, las aves rapaces como depredadores puede adquirir el
problemas neurológicos, cambiando el comportamiento y éxito reproductivo, y en altas
concentraciones, matando al organismo.
Además, existen dos trabajos muy importantes sobre la exposición de aves rapaces
migratorias, fuera sus áreas de reproducción, a contaminantes lejos de sus áreas de
reproducción por organoclorados en Pandion haliatus (Elliott et al., 2007) y Falco
femoralis (Mora et al., 2011). Sin embargo, hay poco o conocimiento en México y
Latinoamérica del nivel de contaminación en las aves rapaces durante la migración.
2. MARCO TEÓRICO
El uso del suelo, el paisaje y el agua son determinantes importantes en la ruta de ingesta de
metales pesados en los organismos. En el estado de Veracruz se presentan cambios
continuos de uso de suelo, que comúnmente involucran un gran impacto humano (Mora et
al., 2011). Los cañaverales y pastizales para la ganadería, así como la industria minera y la
extracción del petróleo, son comunes dentro del estado (INEGI, 2018). Estas actividades
traen consigo una cantidad considerable de productos químicos persistentes que afectan a
los ecosistema y agreocosistemas. Por el lugar que ocupan en las cadenas alimenticias, las
aves rapaces son particularmente sensibles a los contaminantes por efecto de la
bioacumulación (Dauwe et al., 2003). Estudiar los niveles de contaminación en aves
rapaces nos permite obtener información a diferentes niveles tróficos y, por lo tanto, inferir
el grado de contaminación dentro del ecosistema (Castro et al., 2010).
En las aves rapaces, se han estudiado metales pesados como el plomo y el mercurio,
además de organoclorados y compuestos orgánicos persistentes que tienen la ventaja de
ambiente (Bank et al., 2012). Por su persistencia, los metales pesados se pueden muestrear
y detectar fácilmente. El mercurio es un metal que puede presentarse en el ambiente
dependiendo de varios procesos, incluyendo la fábrica de cobre o plomo, desechos de la
producción de electricidad nuclear, bases militares, incineración de desechos de municipios
y fabricas mineras (Henny & Elliott, 2015). En su ciclo, el mercurio sale a la atmósfera
para entrar a sistemas acuáticos y vegetación por el ciclo de agua, y así poder ser
consumido por invertebrados, y consumidores en sistemas acuáticos (Evers et al., 1998).
Por su escala trófica en redes de alimentación, las aves rapaces son indicadoras de
exposición indirecta a metales pesados, y a la vez, muy sensibles cuando están expuestos
(Rattner et al., 2011). Dependiendo de la cantidad de mercurio, es como se puede afectar al
comportamiento y reproducción de las aves, llegando a producir mortalidad (Scheuhammer
et al., 2007)
El plomo es un metal no-esencial que también se encuentra como producto de los
desechos de las fábricas y de las industrias mencionadas en el caso del mercurio (Fisher et
al., 2006). Además, de encontrarlo en los suelos y agua por el mismo proceso que el
mercurio, también se puede encontrar en el barniz de cerámicas mexicanas, tuberías de
agua (Romieu & Lacasana, 1997) y en municiones de cacería (Pain et al., 2009). Los
cartuchos de escopeta son un gran riesgo para las rapaces que son oportunistas y comen
presas que a su vez también son cazadas por humanos. Incluso los Galliformes podrían
comer balines de plomo con la intención de digerir su comida (Fisher et al., 2006). El
plomo afecta al comportamiento, el sistema nervioso, los riñones, el sistema circulatorio y,
metal esencial para los procesos sanguíneos, tal como el cobre, pero en altas
concentraciones puede ser mortales (Eisler, 1993).
El cobre también se puede encontrar en el ambiente por fabricar utensilios de este
metal y en fungicidas (Pohl et al., 2011). Varias cosechas en Veracruz, como el café, tienen
plagas de diferentes hongos, que se combaten mediante la aplicación de fungicidas
metanólicos.
El cadmio es un metal que se encuentra en la producción y uso de fertilizantes, y en
la fabricación de pilas. Normalmente el cadmio es procesado en suelos por plantas, el
cadmio es el séptimo metal más tóxico que tiene una interacción antagonista con el Zn en
los procesos sanguíneos (Jaishankar et al. 2014). El cadmio puede reemplazar a enzimas
conteniendo Zn, duplicándose cuando se une con metanólicos (Castagnetto et al., 2002).
3. ALCANCE DE ESTE TRABAJO
En este trabajo presento mi investigación de las concentraciones de seis metales en dos
tipos de tejidos (plumas y sangre) en aves rapaces (Falconiformes, Accipitriformes)
residentes y migratorias. Las concentraciones de metales en sangre indican una reciente
ingesta, mientras que las concentraciones en las plumas señalan la incorporación del metal
durante la muda (Tsipoura et al., 2017). En el primer capítulo, esta tesis hace una revisión
de los estudios de contaminación de aves hechos en México. En el capítulo 2 comparo los
niveles de metales pesados de rapaces residentes y migratorias. Mi estudio fue llevado a
cabo mediante métodos no letales, tomando muestras de sangre y plumas. Una meta
importante de esta investigación es generar información sobre la temporalidad de la
LITERATURA CITADA
Bank, M., Scheuhammer, A. M., Basu, N., Evers, D. C., Heinz, G. H., Sandheinrich, M. B. 2012. Ecotoxicology of Mercury in Fish and Wildlife: Recent Advances. Toxicology, Risk Analysis, Humans, and Policy, 11: 221-239.
Benitez, J. A., Cerón-Bretón, R. M., Cerón-Bretón, J. G., Rendón-von-Osten, J. 2014. The environmental impact on human activities on the Mexican coast of the Gulf of Mexico: review of status and trends. WIT Trans. Ecology and the Environment, 181: 37-503.
Bildstein, K. 2004. Raptor migration in the neotropics: patterns, processes, and consequences. Ornitología Neotropical. 15: 83-99.
Castagnetto, J.M., Hennessy, S.W., Roberts, V.A., Getzo, E.D., Tainer, J.A., Pique, M.E. 2002. MDB: the metalloprotein database and browser at the Scripps Research Institute. Nucleic Acids Res 30(1): 379–382.
Castro, I., Aboal, J. R., Fernández, J. A., Carballeira, A. 2010. Use of Raptors for Biomonitoring Heavy Metals: Gender, Age, and Tissue Selection. Bull Environ Contam Toxicol. 86: 347-351.
Dauwe, T., Bervoets, L., Pinxten, R., Blust, R., Eens, M., 2003. Variation of heavy metals within and among feathers of birds of prey: effects of molt and external contamination. Environmental Pollution. 124: 429-436.
Eisler, R. 1993. Zinc hazards to fish, wildlife, and invertebrates: A synoptic review. U.S. Department of the Interior Fish and Wildlife Service Patuxent Wildlife Research Center Laurel Maryland 20708.
Elliott, J.E., Morrissey, C.A., Henny, C.J., Inzunza, E.R., Shaw, P. 2007. Satellite Telemetry and prey sampling reveal contaminant sources to pacific northwest ospreys. Ecological Applications. 17(4): 1223-1233.
Fisher, I. J., Pain, D. J., Thomas, V. G., A review of lead poisoning in terrestrial birds. 2006. Biological Conservation. 131: 421-432.
Furness, R.W., Greenwood, J.J.D., Jarvis, P.J. Chapman and Hall. Under Title: Birds as Monitors of Environmental Change. United Kingdom.1993. Print.
Monocrotophos-induced mass mortality of Swainson’s Hawks in Argentina, 1995-1996. Ecotoxicology. 8: 201-214.
Henny, C. J., Elliott, J. E., 2015. Raptor Research Management and Techniques. Chapter 18: 333-350.
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Capítulo II.
Chapter II
CONTAMINANT EXPOSURE TO BIRDS DURING MIGRATION AND NON-BREEDING SEASON: A REVIEW
Meagan L. Campbell1 & Ernesto Ruelas Inzunza1,2
1Universidad Veracruzana, Instituto de Biotecnología y Ecología Aplicada (INBIOTECA),
Av. de las Culturas Veracruzanas 101, Col. Emiliano Zapata, 910910, Xalapa, Veracruz, México.
E- mail: mcampbell.uv@gmail.com
ABSTRACT.—Avian contamination during migration is a long debated topic. After the
ban of DDT in the United States of America and Canada, researchers worried that
migratory birds may be affected by these pesticides, their persistent secondary metabolites,
and other contaminants during the part of their annual cycle away from North America.
After decades of migration research and ecotoxicology research, two hypotheses exist. (1)
Literature continues to publish the idea that migratory birds are probably exposed to more
contaminants than non-migratory birds throughout their annual cycle, given the fact that
migrants spend a significant amount of time away from their breeding areas. (2) A second
possibility, based on a good number of ecotoxicology studies, actually found a decline in
DDT secondary metabolites in Mexico after 1979, and are less conclusive as to where
migratory birds are exposed to more contaminants. After more than 30 years of research,
evidence in support of the former hypothesis is scant, and studies from localities throughout
Latin America support a mosaic of effects with an unclear definitive answer. The outcome
of this literature review is still inconclusive—but a slowly building body of evidence for
this region foresees conclusions that will be easier to draw once the type of contaminant,
tissue, and species of bird are synthesized in order to discover clear patterns of contaminant
exposure.
INTRODUCTION
Neotropical migratory bird populations encounter a wide range of limitations throughout
their annual cycle between North and South America. The majority of migratory research
occurs in the breeding regions, where the patterns of contaminant use are relatively
well-known and regulations more strict, creating assumptions that the greatest risks for
migratory birds occur while migrating south and during the over-wintering period (La Sorte
et al., 2017). Given the broad range of regulations for the use of contaminants throughout
countries in the Americas, many ornithologists assume that migratory birds are exposed to
more contaminants while in Latin America. With less avian ecotoxicology studies
occurring south of the United States and Canada, it is important to review the existing
literature regarding migratory contamination, understand any broad-scale patterns in its
presence in birds, and identify gaps in research (Henny & Elliott, 2015).
Many survey datasets, including migration counts, are helpful at identifying effects
at a population level, whereas information about the health of individuals gives researchers
a more precise insight on the impact of contaminant exposure during winter habitats and its
overall effect on the annual cycle of migratory birds (Lacher et al., 1997). Challenges faced
by birds during migration possibly carry over and affect their fitness beyond the season in
which they were exposed (such as exposure to contaminants or habitat loss, Harrison et al.,
2010).
This paper summarizes known avian ecotoxicology research during southward
migration and the overwintering periods throughout the Americas. We review 27 papers
covering 165 species, 37 localities, and 13 types of contaminants. We, identify regional and
thematic gaps, and project promising avenues for future research.
Contamination during migration hypothesis
South of the United States and Canada, many contaminant regulations are unclear, vague,
or non-existent. It is well known that intensive agriculture, high pesticide application, and
aggressive mining are prevalent landscape uses in Latin America (Servicio Geológico de
México, 2015, Food and Agriculture Organization of the United Nations 2017).
The federal government’s Secretaría de Economía de México boasts that 70% of the
country is under exploration by mining operations, the majority of them done by foreign
companies (SE, 2018). The intensity of these mining operations, augmented by
decades-long use of pesticides, herbicides, and a suite of contaminants from agricultural sources,
plus the management of industrial waste throughout the country under unclear regulations
is an intuitive scenario to hypothesize that migratory birds are exposed to stressful
conditions—and possibly more contaminated ecosystems—while outside of their nesting
grounds (Klaassen et al. 2012).
Although this is a hypothesis accepted as conventional wisdom in the migration
literature, ecotoxicology literature is much less conclusive. The use of
Dichlorodiphenyltrichloroethane, commonly known as DDT and its consequences in
wildlife throughout the western hemisphere, prompted ornithologists and ecotoxicologists
to sample birds during migration and non-breeding season in order to solve this question
The mixed-support hypothesis
An alternative idea, not quite an antonym of the previous one, is that contaminant exposure
patterns do not conclusively support the idea that birds acquire contaminants during their
non-breeding season. Existing evidence shows that these contamination patterns are an
actual mosaic of trends that vary widely among species, contaminant type, and geographic
location of the study (Mora et al., 2016).
Contaminant studies in Latin America
Contamination studies on migratory birds exist throughout North America (Ackerman et
al., 2016; Norstrom et al., 2000; Snyder et al., 1973). However, these studies show a
fragmented scenario with numerous gaps. Ecologically, the species under study belong to
different trophic levels, live in different ecosystems, and the contaminants analyzed are
different chemical compounds and elements (Table 1). The tissues analyzed are many,
species and ecosystems are difficult to correlate, and the processes inferred from patterns
incomplete (Furley et al., 2018). Choosing which contaminant and which species is key to
understanding bioaccumulation and biomagnification in migratory birds. For example,
contamination concentrations in passerines, indicate a different exposure from diet, than
raptors, given that their concentrations usually accumulate from their prey species. A study
on pesticides in warblers would indicate direct exposure, whereas in raptors, it would
indicate accumulation and magnification from their directly exposed prey species.
Convention (1998) were Aldrin, Chlordane, DDT, Dieldrin, Endrin, Heptachlor,
Hexachlorobenzene (HCB), Mirex, Toxaphene, Polychlorinated biphenyls (PCB),
Polychlorinated dibenzo-p-dioxins (PCDD), and Polychlorinated dibenzofurans (PCDF).
After the first 12 POPs were defined, over the years more were added (2017): Apha
hexachlorocyclohexane, Beta hexachlorocyclohexane, Chlordecone, Decabromodiphenyl
ether (commercially known as c-decaBDE), Hexabromobiphenyl,
Hexabromocyclododecane, Hexabromodiphenyl ether and heptabromodiphenyl ether
(commercially known as octabromodiphenyl ether), Hexachlorobutadiene, Lindane,
Pentachlorobenzene, Pentachlorophenol and its salts and esters, Perfluorooctane sulfonic
acid, its salts and perfluorooctane sulfonyl fluoride, Polychlorinated naphthalenes,
Short-chain chlorinated paraffins (SCCPs), Technical endosulfan and its related isomers,
Tetrabromodiphenyl ether and pentabromodiphenyl ether (commercially known as
pentabromodiphenyl ether). These pollutants are declared POPs by their toxic persistence in
the environment. The majority of the POPs studied in avian ecotoxicology studies are
organochlorines, DDT, and DDE, seeing how the use of pesticides over time impact
wildlife (Elliott et al., 2007; Mora et al., 2016).
Organochlorines.—Existing studies from Mexico involve organochlorines and DDT (1,1,1-trichloro-2,2-bis( p-chlorophenyl)ethane) metabolites in raptors, passerines, and
wading birds, as well as heavy metals and stable isotopes in raptors, passerines, and aquatic
birds (Elliott et al., 2007, Torres et al., 2014, Maldonado et al., 2016). Organochlorines are
POPs, however, these particular POPs are more frequently examined in the literature. In the
case of raptors in Mexico, the contamination focus has been organochlorines (Elliott et al.,
DDT in juvenile Sharp-shinned Hawks (Accipiter striatus) returning from their
overwintering grounds after sampling hatch year birds in the fall during their southward
migration (Elliott and Shutt 1993).
Another study comparing DDT and DDE in migrating birds in Mexico and the
southwestern United States did not report significant differences in concentrations of DDT
or DDE in passerines (Mora 1997). A more recent study (Maldonado et al., 2016) that
sampled migratory passerines in Texas, Yucatán, and Costa Rica, found lower mean
concentrations of DDE in the birds sampled in Yucatán and Costa Rica, than the birds
sampled in Texas—further complicating the hypothesis that migratory birds encounter
more contamination in their overwintering grounds with evidence against it. These studies
generate information about DDT compounds in Latin America, given that the regulations
are less clear than in the United States (Table 1).
>> Insert Table 1 here
Heavy metals.—Oil, agriculture, and mining are the other primary industries in Mexico and Latin America, causing heavy metal contamination (Servicio Geológico de México,
2015; Food and Agriculture Organization of the United Nations, 2017). Given that
agriculture and resource extraction are prevalent industries south of the United States and
Canada, further exploring their contamination to migratory birds will help support or falsify
the hypothesis that migratory birds encounter more contamination while migrating south, or
in their overwintering territories.
concentrations indicate body burden during molt (Tsipoura et al., 2017). More importantly,
it will add help answer the hypothesis that birds are exposed to higher levels of
contaminants during the migration than the non breeding season, and illustrate which
exposure pathways affect different organs and tissues (Burger et al., 2014).
Exposure Pathways.—The aforementioned industries in Mexico and Latin America could expose raptors to heavy metals, causing a detrimental carry over effect (COE) (Harrison et
al., 2010). Heavy metals are released into the atmosphere and enter the water cycle through
aquatic ecosystems and soils (Singh et al., 2011). Once low trophic-level organisms
consume heavy metals, they can advance up the food web, and reach top predators. Heavy
metal toxicity affects the function of different parts of organisms in different ways. Lead
binds to hard tissues during the ossification process, and can be inhaled in the air, or
ingested causing neurological and reproductive failures (Rattner et al., 2011). Lead is a
major concern in raptors because leadshot bullets in prey are an additional source of
contamination (Fisher et al., 2006).
Mercury is another popular heavy metal studied in birds. Usually emerging from
aquatic ecosystems, methylmercury levels indicate ingested mercury, from an
anthropogenic source (Nichols et al., 2009). As top predators, ecotoxicologists use raptors
as a sentinel species to try to predict ecosystem health parallel to humans. Raptors indicate
biomagnification of heavy metals because of their trophic level, meaning that they usually
have higher concentrations than their prey because their exposure occurs directly from their
prey, rather than where the heavy metal was initially applied or deposited (Peakal &
Burger, 2003). Along with heavy metals, pesticides especially persistent organic pollutants
and its primary metabolite, 1,1-dichloro-2,2-bis ( p-chlorophenyl)ethylene (DDE) led to
reproductive failures in birds of prey, and researchers still find residues in bird tissues after
Although DDT was banned in Canada and the United States in the early 1970’s,
detections in Mexico continue occurring (Pozo et al., 2009). Along with heavy metals and
POPs, different contaminants such as Thiacloprid
([3-[(6-chloro-3-pyridinyl)methyl]-2-thiazolidinylidene]cyanamide), and other neonicitinoides used to treat agricultural seed for
pests, are newer, and their effects on wildlife are still being determined. In an experiment
by Eng et al. in Canada, white crowned sparrows (Zonotrichia leucophrys) were dosed with
imidacloprid (neonicotinoid) and chlorpyrifos (organophosphate), and the white-crowned
sparrows lost their migratory orientation and fitness, exposing a carry-over effect from
these contaminants (Eng et al., 2017). The duplicity of contaminants in the environment
enter food webs in different ways, adding complexity to how they may affect bird
migration between countries.
Contaminant exposure to migratory birds and future research foci
The wide range of ecotoxicology studies throughout the Americas over the past 30 years
has helped researchers better understand contamination pathways, and how they affect
migratory birds. Further studies that link the migratory pathways, and use similar tissues
paralleled with laboratory experiments will help fine-tune this effort.
Currently, there are multiple studies with multiple contaminants at different trophic
levels, analyzed with different tissues. After decades of research, it is time to tie these
studies together to make a matrix understanding what the results indicate exactly. Field
samples, along with laboratory tests to understand the metabolic patterns of each
contaminant, will help translate concentrations from samples collected in the field.
Tracking technology is now financially available and feasible for researchers to watch
matrix and following individuals throughout their annual cycles will create a
non-destructive methodology, which is more accessible in the field. If researchers could
elucidate what egg, feather, and blood samples indicate with precision for the body burden
of the individuals studied given their trophic levels, individuals could be analyzed with a
non-lethal method, protecting the species. Tracking technology could precisely indicate
where the individual visits, allowing researchers to make contacts, and collect samples in
that environment, quantifying the input exposure. Just as countries have migratory studies
that collaborate, this collaboration could cross institutions, and generate global data,
allowing stakeholders to understand just how interconnected they are. A synthesis in
migration and ecotoxicology studies will make these efforts simple and more complete.
ACKNOWLEDGEMENTS
The authors thank past researchers who have published their work, helping scientists
understand what research has occurred, and which focuses will help with future work.
Mexico’s Consejo Nacional de Ciencia y Tecnología (CONACYT) provided a graduate
fellowship 607620 to MLC during the time it took for this literature review. ERI received
support from CONACYT’s Sistema Nacional de Investigadores (fellowship 47135), the
Secretaría de Educación Publica’s PRODEP Program (UV-PTC-868), and the
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Table 1. Previous avian contamination studies in Latin America
Contaminant Study site Results Author (year)
Tropical
Ecotoxicology Latin America Need to generate more research Lacher and Goldstein, (1997)
Pollutants Gulf California, of
Mexico
Review of pollution in the Gulf of California-most metal pollution
occurs from mining Páez-Osuna et al., (2017)
POPs and
Heavy Metals
Baja California, Mexico
Common Ground-dove and
House Sparrow did not reach
toxic thresholds Jiménez et al. (2005)
POPs Western Hemisphere More DDE in Mexico, but did not significantly effect Ospreys Elliott et al. (2007)
POPs Baja California Sur, Mexico
High levels-not yet toxic of POPs in Osprey in a conserved lagoon
Rivera-Rodríguez and Rodríguez-Estrella (2010)
POPs North America
Did not find more DDE in Mexico in eggs than North along a review of studies along a latitudinal gradient
Mora et al. (2016)
POPs
Texas, USA;
Yucatan,
Mexico; Costa Rica
Least amount of contaminants in CR, next Mexico, and largest
amount in Texas Maldonado et al. (2016)
POPs and
Heavy Metals
Colorado River Delta, Mexico
Did not find concentrations of POPs and metals in eggs above
LOAELs in an intensive
agriculture area
García-Hernández et al. (2006)
Pb San Luis Potosí, Mexico
Found low sub-lethal effects in birds. Saw health effects, but not significant enough frequency in migratory species
Chapa-Vargas et al. (2010)
Hg Jalisco, México No significant differences in waterbirds, trend in length of
trout, and amount of Hg
Torres et al. (2014)
POPs (DDE,
DDT)
SW US, and throughout MX
POPs significantly declined in MX after the 70’s, and many birds in Mex have less DDT and DDE exposure than in the US
Mora (1997)
POPs (PBDEs, PCBs, DDE)
Chihuahua and Veracruz, Mexico
Aplomado Falcon not exposed to
Capítulo III.
Chapter III
HEAVY METALS IN RAPTORS DURING THEIR AUTUMN MIGRATION
ABSTRACT—Veracruz, Mexico, is one of the states with the highest diurnal raptor species richness in North America. It is also a globally significant migratory corridor for
raptors, as well as for other birds. Agriculture, mining, industry, and oil production are
possible contamination sources for birds in this state as well as in the rest of Mexico. The
majority of raptor metal contamination studies occur north of Mexico. Many researchers
hence posit that exposure to metal contaminants is higher in their non-breeding season
range. I analyzed blood and feather samples of raptors to look for traces of six heavy metals
(Al, Zn, Cu, Cd, Pb, and Hg), since the blood concentrations indicated dietary intake, and
feather concentrations indicated body burden during molt. I took blood and feather samples
of 194 hatch year Sharp-shinned Hawk (Accipiter striatus), Cooper’s Hawk (Accipiter
cooperii), Aplomado Falcon (Falco femoralis), Short-tailed (Buteo brachyurus), and
Roadside Hawk (Rupornis magnirostris). I captured most of the birds during the autumn
seasons of 2016 and 2017, at a raptor banding station located on the coastal plain of
Veracruz. From those samples, I analyzed subset of 194 feathers and 194 blood samples
higher in feathers than in blood, with positive correlations in Pb, and negative correlations
in Zn, Cu, and Hg. The high concentrations in Cu, Zn, and Al levels, as well as the
concentration of Pb, are higher than lethal thresholds reported in the literature. This study is
the first to provide information of heavy metal concentrations of resident and migratory
raptors during the autumn migration in Veracruz. These data helps us further understand the
timing and geographic location of heavy metal exposure in raptors.
INTRODUCTION
The coastal plain of Veracruz Mexico is a primary migratory corridor for raptors
during their southbound migration in the autumn (Bildstein, 2006). The continental
geography creates conditions conducive for raptor and soaring bird migration from boreal
habitats in Canada, through the Rocky and Appalachian mountain ranges in the United
States, to a geographic bottleneck from the Neovolcanic Belt where the Sierra Madre
Occidental converges with the Sierra Manuel Díaz between the mountains and the Gulf of
Mexico. Over 3 million raptors of about 23 species (depending on the year, some species
are not observed) pass this point during a 3-month period from August through November,
a phenomenon of a magnitude that does not occur anywhere else in the world (Bildstein et
al., 2004; Ruelas et al., 2009).
Extensive agriculture, cattle ranching, numerous industries, oil extraction, and
mining, are economic activities that influence landscape management in this part of Mexico
(INEGI, 2018). Many of these activities require abundant use of chemical products in order
to be undertaken as well deforest the landscape. The application of pesticides, herbicides,
fertilizers, and byproducts of urban activity has ecological consequences, as these
contaminants enter the food chain through different mechanisms.
The place where migratory raptors accumulate contaminants during their annual
cycle has been the subject of long debates. Some authors assume that stricter controls over
the use of chemicals in the United States and Canada results in a higher likelihood that
contaminants are acquired during the non-breeding season, in Latin America (Lacher &
from the United States of America and Canada (Ackerman et al., 2016). Raptors are
indicators of contaminant accumulation because of their trophic position at a predator level,
which helps researchers understand the severity of toxic elements within the environment.
Heavy metals are among the trace elements that occur in the environment and
bioaccumulate through different metabolic pathways. Once they reach top predators on the
food chain, such as raptors, they reach higher concentrations (Peakall & Burger, 2003).
Sampling different trace elements in Veracruz helps allude to what kind of
landscape management and human activities could be contributing to toxic levels of heavy
metal contamination, and how migrants and resident species reflect these contamination
patterns.
Pronatura Veracruz, A.C. operates the only raptor banding station in Mexico as part
of the Veracruz River of Raptors project. Hundreds of hawks and falcons of around 16
species are banded there every fall (Pronatura Veracruz, A.C. unpublished data). The
majority of the raptors captured at the banding station are juvenile (hatch year) birds,
indicating a relatively recent exposure (e.g., a few months) to trace elements (Pronatura
Veracruz, A.C., unpublished data). This makes non-destructive sampling methods for
heavy metals possible. By collecting feather and blood samples, two types of tissue that
accumulate contaminants at different rates, researchers can avoid euthanizing sample
individuals while obtaining samples adequate to understand short-term and annual exposure
to contaminants. Blood, for example, indicates exposure to a particular metal within the
most recent 3–5 day period, whereas feathers quantify exposure from the place and time
when they were formed (e.g., in the nest, for first-year birds, or in the location where they
the nesting site outside of Mexico, and blood indicates exposure during migration.
Sampling the blood and feathers of resident and migratory raptors compares exposure rates
at different places along the migratory corridor.
My research question was whether raptors acquire higher concentrations of metals
during the breeding or the non-breeding season/geographic range. By comparing metal
concentrations of resident species in Veracruz, with migratory species during their passage
through Veracruz, I expected to find differences in the concentrations between tissues
(blood and feathers) and species, which would indicate when migratory raptors experience
greater metal exposure.
My study objective was to compare metal levels from their nesting areas (in
feathers) to what was acquired in the more recent days in Veracruz (in blood), generating
information about when, where, and how each of the different metals could be entering this
system. I expected to find differences between tissues and species, indicating where
migratory raptors encountered higher exposure to different metals.
METHODS
Study area
The study area was located at banding stations inside of trapping blinds operated by
Pronatura Veracruz A.C. The station’s main trapping blind is located at the coastal plain of
Veracruz, where the Sierra Manuel Díaz mountain range reaches La Mancha, a town in the
municipality of Actopan, Veracruz (Fig. 1). Pronatura Veracruz A.C. operates the
system. In 2017, Pronatura Veracruz, A.C. operated an additional trapping blind on a butte,
2.47 kilometers due west of the Cansaburro main trapping blind (19°32’48.96”N,
96°23’42.68”W). These banding stations are directly south of the geographic bottleneck
that funnels migrants at La Mancha, and the CICOLMA research facility of the Instituto de
Ecología A.C. is visible from both blinds.
Collection of samples
I, along with the Pronatura banding station crew captured raptors with bow nets,
mist nets, and dho gaza nets using living lures, with SEMARNAT permit 08-049
RUEIE680506HNLLNR00. We captured Roadside Hawks with road trapping methods
using bal chatri traps with live mice as lures (Bloom et al., 2007). No raptors died during
the sampling process. I collected most blood and feather samples of raptors in the field at
the primary blind of the CRBS during the autumns of 2016 and 2017. I selected focal
species (Coopers Hawk, Sharp-shinned Hawk, Aplomado Falcon, Short-tailed Hawk, and
Roadside Hawk) for samples and analysis based on their capture frequencies in the banding
stations. We also sampled various migratory and resident species at the secondary blind. I
obtained a sample number relative to the availability of samples from the raptures captured.
For additional resident birds, I obtained Roadside Hawk (Rupornis magnirostris)
samples at various sites in the southeastern region of Veracruz near the wetlands of
Alvarado (Fig. 1).
I took blood samples with standard insulin needles and syringes purchased at local
drug stores (UPC 38290324914) and stored the blood in capillary tubes and Eppendorf
tubes with a 1.5-mL capacity immediately after taking a sample of 80–100 μL. Blood
day was finished. I froze the blood samples until we processed them in the laboratory
(Evers et al., 1998).
I obtained feather samples from the same individuals that we collected blood
samples from. I plucked two chest feathers from the individual, and stored them in paper
envelopes until analysis (Furness et al., 1986).
Laboratory analyses
I performed trace metal analysis using a Metrohm 747 Computrace apparatus.
Before running analyses, I pretreated samples by digesting the blood with 400 μL of 35%
HNO3 and deionized water. After the digesting each blood sample with HNO3, I diluted
them with 1 ml of deionized water. Once the blood samples were ready for analysis, they
were read by the voltameter for zinc (Zn), copper (Cu), lead (Pb), mercury (Hg), cadmium
(Cd), and aluminum (Al) (Metrohm Application Bulletin 186/2 e; 231/2 e). Feathers were
digested in 1 mL of 35% HNO3 and deionized water. After the solids were digested, they
were diluted with 2 mL of deionized water. Feather tests were run for the same metals
using the same buffers, electrolytes, and standard solutions as the blood samples on the
same machine. Results were reported in wet weight.
Zinc, copper, lead, and cadmium were analyzed with the same test, using a buffer
with 5 mL of H2O, 5 mL of acetate, an electrolyte with 10% HNO3 with ammonium acetate,
0.0095 mL of the sample, and Zn, Cu, Pb, Cd standard for comparison. Mercury samples
were analyzed with a buffer of 5 mL of H2O, 0.1 mL of sample, 5 mL of a disodium
