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Dpto. de Biología Aplicada Dpto. de Biología Ambiental y Salud PúblicaESTACIÓN BIOLÓGICA DE DOÑANA UNIVERSIDAD DE HUELVA(CSIC)
TESIS DOCTORAL
RELACIONES ECOLÓGICAS ENTRE LIMÍCOLAS E INVERTEBRADOS ENLAS SALINAS DE LAS MARISMAS DEL ODIEL
Memoria presentada por Marta Isabel Sánchez Ordóñez para optar al grado deDoctora en Biología
Directores
Dr. Andy J. Green Dr. Eloy M. Castellanos VerdugoCientífico Titular Profesor Titular de UniversidadEstación Biológica de Doñana (CSIC) Universidad de Huelva
2005
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3
A mis padres
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INDICE
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INDICE
Introducción general 9
CAPÍTULO 1 19
Seasonal variation in the diet of the Redshank Tringa totanus in the Odiel
Marshes, south-west Spain : a comparison of faecal and pellet analysis.
Marta I. Sánchez, Andy J. Green and Eloy M. Castellanos.
Bird Study 52: 210-216.
CAPÍTULO 2 35
Spatial and temporal fluctuations in use by shorebirds and in availability of
chironomid prey in the Odiel saltpans, south-west Spain.
Marta I. Sánchez, Andy J. Green and Eloy M. Castellanos.
Hydrobiologia 567: 329-340.
CAPÍTULO 3 61
Seasonal and spatial variation in the aquatic invertebrate community at the
Odiel salt pans (SW Spain) and their implications for migratory waders.
Marta I. Sánchez, Andy J. Green & Eloy M. Castellanos.
Archive für Hydrobiologie 166: 199-223.
INDICE
6
CAPÍTULO 4 93
Shorebird predation affects abundance and size distribution of benthic
chironomids in saltpans: an exclosure experiment.
Marta I. Sánchez, Andy J. Green and Raquel Alejandre.
Journal of North American Benthological Society 25(1): 9-18.
CAPÍTULO 5 117
Cestodes from Artemia parthenogenetica (Crustacea, Branchiopoda) in the
Odiel Marshes, Spain: a systematic survey of cysticercoids.
Boyko B. Georgiev, Marta I. Sánchez, Andy J. Green, Pavel N. Nikolov,
Gergana P. Vasileva and Radka S. Mavrodieva.
Acta Parasitologica 50 (2): 105-117.
CAPÍTULO 6 145
Passive internal transport of brine shrimps and seeds by migratory waders in
the Odiel marshes, south-west Spain.
Marta I. Sánchez, Andy J. Green, Francisco Amat & Eloy M. Castellanos.
Marine Biology 151: 1407-1415.
Journal of Avian Biology 37: 201-206.
INDICE
7
CAPÍTULO 7 171
Dispersal of invasive and native brine shrimps Artemia (Anostraca) via
waterbirds.
Andy J. Green, Marta I. Sánchez, Francisco Amat, Jordi Figuerola, Francisco
Hontoria, Olga Ruiz, Francisco Hortas.
Limnology and Oceanography, 50 (2): 737-742.
Apéndices 187
Discusión general 195
Conclusiones 215
Agradecimientos 219
8
INTRODUCCIÓN
9
INTRODUCCIÓN
Justificación de la tesis
Las marismas del Odiel (Huelva, 37º17'N 06º55'W) se encuentran en uno de los más
productivos y diversos estuarios del suroeste de Europa (Castellanos et al. 1998). Su
elevado valor ecológico le ha llevado a su protección como Paraje Natural, Sitio Ramsar
(Bernués 1998), Reserva de la Biosfera y Zona de Especial Protección para las aves en
la Unión Europea. Miles de limícolas que siguen la ruta migratoria del Atlántico Este
dependen de las marismas del Odiel, utilizándolas para descansar y reponer energía año
tras año.
La existencia de hábitats alternativos de alimentación en las zonas estuarinas
reviste una gran importancia para el mantenimiento de las poblaciones de limícolas, ya
que los fangos intermareales donde se alimentan, sólo están disponibles una parte del
ciclo mareal, permaneciendo anegados durante la marea alta. Además su importancia es
aún mayor teniendo en cuenta la degradación y pérdida de hábitats naturales a que
estamos asistiendo durante las últimas décadas, y que afecta de forma especialmente
intensa al litoral, amenazando las poblaciones de limícolas de todo el mundo.
Las salinas costeras son humedales manejados por el hombre que ofrecen unas
condiciones excepcionales para la alimentación y descanso de las aves acuáticas, tanto
migradoras como sedentarias (Pérez-Hurtado & Hortas 1991, Velásquez 1993, Masero
& Pérez-Hurtado 2001). Se estima que aproximadamente la mitad de los 500.000
limícolas migratorios e invernantes que utilizan el Mediterráneo durante los meses de
invierno, se encuentran en salinas (Sadoul et al. 1998), jugando un papel importantísimo
en el ciclo anual y conservación de las poblaciones de estos migradores de largas
distancias.
La producción de sal es, probablemente, la industria con mayor tradición en la
cuenca Mediterránea, modelando el paisaje de toda la costa a lo largo de los siglos. De
las 7158 has que ocupan las marismas del Odiel, 1174 están transformadas en salinas,
siendo la unidad ambiental de la marisma que mayor capacidad de carga soporta. Sin
embargo, junto con los humedales costeros, las salinas continúan desapareciendo en la
región Mediterránea debido a la intensa presión antrópica. La actividad salinera en
INTRODUCCIÓN
10
general ha ido reduciéndose considerablemente, mientras la tradicional prácticamente ha
desaparecido, abandonándose sus instalaciones o utilizándose para otros fines.
La situación actual de crisis ambiental que afecta especialmente a los humedales
costeros demanda de estudios multidisciplinares que incluyan aspectos que relacionen
tanto la dinámica de las aves, como la de sus invertebrados presa y los factores
ambientales que les afectan. En definitiva, estudios que permitan comprender mejor las
relaciones ecológicas de los sistemas acuáticos con el fin de poder compensar el
impacto de la actividad humana sobre los ecosistemas naturales y artificiales. Los
sistemas manejados por el hombre, ofrecen una oportunidad excepcional para
desarrollar este tipo de estudios, ya que con una adecuada gestión es posible aumentar
con creces su valor ecológico de cara a las aves (Rehfisch 1994).
Existen diversos estudios en nuestra región sobre la autoecología de las aves
limicolas. No es prioritario, por tanto, repetir dichos estudios en Odiel, ya que no caben
esperar diferencias sustanciales. En cambio, es prioritario profundizar en el
conocimiento de las comunidades de invertebrados y de sus interacciones con la de las
aves limícolas, estudios aún escasos en la región Mediterránea. El funcionamiento del
ecosistema acuático sólo puede ser entendido cuando se toma en su conjunto. Hurlbert y
colaboradores (1983) demostraron la fuerte influencia que ejercían las aves acuáticas en
general sobre la estructura de los ecosistemas acuáticos, acuñando el término de
ornitolimnología para aunar estas dos disciplinas (ornitología y limnología). Los
limícolas en particular presentan requerimientos energéticos extremadamente altos y
altísimas tasas de alimentación (Nagy 2001), pudiendo ejercer, en un breve periodo de
tiempo, profundos efectos sobre la dinámica de las poblaciones de presa (y especies
asociadas a través de efectos indirectos) y condicionando, en último término, la
dinámica del ecosistema acuático completo. Además de las relaciones predador-presa,
las relaciones parásito-hospedador también juegan un papel clave en estructurar las
comunidades animales. Existe una gran diversidad de caminos por los que los parásitos
pueden afectar a sus hospedadores. La mayoría de los cestodos (Brown et al. 2001)
(muchos de ellos parásitos de limícolas y otras aves acuáticas) utilizan hospedadores
intermedios a los que "manipulan", induciendo cambios en el fenotipo y en el
comportamiento, con el fin de alcanzar a sus hospedadores definitivos. La estrategia de
infección por transmisión trófica, por la que el parásito incrementa la susceptibilidad a
la predación, puede ocasionar profundos efectos sobre las poblaciones del hospedador
intermedio. Además los individuos parasitados pueden considerarse como nuevos
INTRODUCCIÓN
11
organismos en el ecosistema, involucrados en nuevas interacciones con otras especies
(Thomas et al, 1997). Otro tipo de relación interespecífica entre limícolas e
invertebrados, es la dispersión de invertebrados por las aves. Los procesos de dispersión
son centrales para mantener la biodiversidad de los ecosistemas acuáticos y explicar los
patrones de distribución y composición de las comunidades. Las aves acuáticas se han
considerado como uno de los principales vectores de dispersión de propágulos de
invertebrados y plantas acuáticas (Darwin 1859). Sin embargo, las evidencias sobre la
implicación real de las aves en la dispersión son escasas.
Esta tesis pretende ampliar el conocimiento del funcionamiento de los
ecosistemas de salinas, a través del estudio de las relaciones ecológicas entre limícolas e
invertebrados en unas salinas de importancia internacional para las aves acuáticas.
Ahondar en el conocimiento básico de los sistemas artificiales, más susceptibles a la
gestión aplicada a través de estudios como el presente, ayudará a diseñar medidas para
compensar de alguna manera el impacto sobre las poblaciones de limícolas que supone
la pérdida de hábitats costeros en todo el mundo.
Presentación de la tesis
El objetivo de esta tesis lo abordamos desde tres puntos de vista.
1. Relaciones predador-presa
1.1 En primer lugar estudiamos la comunidad de invertebrados y su efecto sobre la
comunidad de limícolas, analizando los requerimientos tróficos, y determinando la
distribución y abundancia de aves e invertebrados (capítulos 1, 2, 3).
1.2. Una vez analizado el efecto de los recursos sobre la distribución y abundancia de
limícolas, abordamos el estudio desde el punto de vista del impacto de las aves sobre
sus recursos, determinando las consecuencias de la predación sobre la densidad,
biomasa y tamaño de presas (capítulo 4).
INTRODUCCIÓN
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2. Relaciones parásito-hospedador
Realizamos una primera aproximación a las relaciones parásito-hospedador en el
sistema Cestodos-Artemia-limícolas, describiendo las diferentes especies de cestodos de
la población de Artemia del Odiel (capitulo 5). Este constituye el estudio más completo
realizado hasta la fecha en nuestro país.
3. Dispersión de propágulos
Finalmente analizamos la capacidad de dispersión de propágulos por los limícolas,
evaluando su implicación en la distribución de especies y estructura de las comunidades
de invertebrados acuáticos y plantas (capítulos 6 y 7).
El estudio de la dieta ha sido y continúa siendo uno de los primeros pasos en el estudio
de la ecología básica de las especies. Para los ecólogos de comunidades, la dieta juega
un papel central en determinar la dinámica de competencia entre especies (Mittelbach &
Osemberg 1994), interacciones predador-presa (Sih et al. 1985) e interacciones
indirectas de la comunidad (Wootton 1993). La forma en que los limícolas explotan los
recursos constituye una primera aproximación para comprender e interpretar su
distribución y abundancia. Por eso, en el capítulo 1 tratamos de identificar las presas
más importantes y su variación a lo largo del año, tomando como modelo el Archibebe
común Tringa totanus. Para ello comparamos los resultados de dos metodologías no
invasivas: análisis de excrementos y egagrópilas. Elegimos esta especie debido a su
abundancia en la zona de estudio y a la facilidad para recoger las muestras. Las larvas y
pupas de Chironomus salinarius, constituyeron la base de la dieta del Archibebe y
probablemente de otras especies durante el paso migratorio de primavera, por lo que en
el capítulo 2, abordamos la dinámica estacional de la comunidad de limícolas en
relación a la dinámica poblacional de su principal presa. De los quironómidos,
invertebrados dominantes en el sedimento, pasamos al estudio de los invertebrados de la
columna de agua, y en el capítulo 3 analizamos la distribución y dinámica estacional de
las diferentes especies (con especial atención a Artemia), así como su relación con las
características químicas del agua y otros factores. Chironomus salinarius en el bentos, y
Artemia parthenogenetica en la columna de agua son los principales invertebrados
INTRODUCCIÓN
13
presentes en la salina y constituyen las dos especies clave que unen los niveles de
detritus y fitoplancton con los niveles tróficos superiores, especialmente las aves.
Una vez estudiado cómo la distribución y abundancia de los recursos influye en
el establecimiento de la dinámica poblacional de los limícolas, analizamos cómo
simultáneamente la comunidad de aves altera las características de las poblaciones de
presa. La predación juega un papel fundamental estructurando las comunidades de
invertebrados bentónicos (Thrush 1999). Así, tras comprobar en los capítulos 1 y 2 la
importancia de los quironómidos para los limícolas, evaluamos, en el capítulo 4, el
efecto de la predación sobre la abundancia, biomasa y tamaño de larvas durante el paso
migratorio de primavera mediante un experimento de exclusión de predadores.
Como parte del estudio de la comunidad de invertebrados, una vez comprobada
la elevada tasa de parasitismo en la zona, y dada la importancia de las interaciones
ecologicas entre estos organismos y las aves, incluimos la descripción y abundancia de
las especies de metacestodos de Artemia (parásitos de limícolas y otras aves acuáticas)
(capítulo 5). La infección a través de Artemia supone una interesante estrategia de
encuentro entre el parásito y el hospedador, ya que la presencia de cisticercoides de
ciertas especies de cestodo está acompañada de cambios en la pigmentación y
modificaciones en el comportamiento de la artemia parasitada, lo cual pensamos,
aumenta la susceptibilidad a la predación, favoreciendo la infección del hospedador
final (Gabrion 1982, Amat 1991, datos propios sin publicar).
Los procesos de dispersión a larga distancia pueden tener efectos sobre la
diversidad y flujo genético entre poblaciones (Bohonak 1999, Freeland et al. 2000,
Figuerola et al. 2005), y afectar a la distribución de especies y estructura de las
comunidades. A pesar de que las aves han sido consideradas como importantes vectores
de dispersión de organismos acuáticos, son escasas las evidencias empíricas de dicho
transporte (Figuerola & Green 2002), particularmente para el caso de los limícolas,
migradores de largas distancias y con un elevado potencial como dispersantes. En el
primer capítulo encontramos que una gran cantidad de propágulos (especialmente
quistes de Artemia y semillas) eran consumidos por los limícolas. Por ello en el
capítulo 6 cuantificamos en detalle el número de propágulos intactos y su viabilidad
tras la ingestión en diferentes especies de limícolas y estaciones del año. Analizamos el
efecto de la dieta y otros factores sobre la probabilidad de ingestión de propágulos y la
supervivencia a la ingestión. El hecho de que las aves puedan actuar de manera efectiva
en la dispersión de organismos, plantea la cuestión, hasta ahora inexplorada, de cuál es
INTRODUCCIÓN
14
la implicación de las aves en un problema de actualidad que amenaza la diversidad a
nivel global como es la expansión de especies exóticas. En el capítulo 7 evaluamos la
capacidad de los limícolas para dispersar Artemia franciscana, una especie invasora
originaria de Norte América, que está desplazando a una gran velocidad a sus
congéneres autóctonos (la especie sexual A. salina, y las líneas partenogenéticas
diploides y tetraploides) poniendo en grave peligro sus poblaciones y aquellas especies
estrechamente asociadas como sus parásitos (Amat et al. 2005). Hasta el momento no se
ha encontrado A. franciscana en el Odiel, donde existe una población partenogenética
principalmente diploide con un pequeño porcentaje tetraploide (Amat et al. 2005). Sin
embargo su vulnerabilidad es evidente teniendo en cuenta que ya ha sido registrada en
los humedales ibéricos más importantes para los limícolas en la ruta migratoria del
Atlántico Este, siendo la única especie presente en Portugal y habiéndose localizado ya
en la bahía de Cádiz. Los resultados de este capítulo permiten valuar el riesgo que
supone el que los limícolas estén transportando quistes de esta especie invasora, de la
bahía de Cádiz o el Algarve, hacia Odiel.
De esta forma hemos abordado el estudio de las relaciones ecológicas entre
limícolas e invertebrados. Por un lado estudiando la distribución y abundancia de
predadores y presas, y analizando los efectos directos que unos ejercen sobre los otros;
por otro lado con una primera aproximación a las relaciones entre limícolas y
metacestodos; y finalmente estudiando las consecuencias derivadas de la predación de
formas de resistencia o propágulos que pueden ser dispersados por las aves.
Los capítulos de esta tesis están presentados en forma de artículos, algunos de los cuales
han sido ya aceptados y otros están enviados pendientes de aceptación. Por esa razón
resulta inevitable el solapamiento de algunas frases de los apartados de introducción y
métodos. No obstante los datos y resultados que se presentan en cada capítulo son
originales y específicos de cada uno.
Bibliografía
Amat, F., Illescas, M.P. & Fernandez, J. 1991. Brine shrimp Artemia parasitized by
Flamigolepis liguloides (Cestoda, Hymenolepidadae) cysticercoids in Spanish
Mediterranean salterns. Vie Milieu 41 (4): 237-244.
INTRODUCCIÓN
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Amat, F., Hontoria, F., Ruiz, O., Green, A.J., Sánchez, M.I., Figuerola, J. & Hortas, F.
2005. The American brine shrimp Artemia franciscana as an exotic invasive species in
the Western Mediterranean. Biological Invasions 7: 37-47.
Bernués, M., ed., 1998. Humedales Españoles inscritos en la Lista del Convenio de
Ramsar. Ministerio de Medio Ambiente, Organismo Autónomo de Parques Nacionales,
Madrid.
Bohonak, A. J. 1999. Dispersal, gene flow and population structure. Quarterly Review
of Biology 74: 21-45.
Brown, S. P., Renaud, F., Guégan, J.-F. & Thomas, F. 2001. Evolution of trophic
transmission in parasites: the need to reach a mating place?. Journal of Evolutionary
Biology 14: 815-820.
Castellanos, E. M., Heredia, C., Figueroa M. E. & Davy, A. J. 1998. Tiller dynamics of
Spartina maritima in successional and non-successional mediterranean salt marsh.
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Darwin, C. 1859. On the Origin of Species by Means of Natural Selection. Murray,
London.
Figuerola, J. & Green, A. J. 2002. Dispersal of aquatic organisms by waterbirds: a
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494.
Figuerola, J., Green, A.J. & Michot, T.C. 2005. Invertebrate eggs can fly: Evidence of
waterfowl mediated gene-flow in aquatic invertebrates. American Naturalist: en prensa.
Freeland, J. R., Romualdi, C. & Okamura, B. 2000. Gene flow and genetic diversity: a
comparison of freshwater bryozoan populations in Europe and North America. Heredity
85: 498-508.
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Gabrion, C., MacDonald-Crivelli, G. & Boy, V. 1982. Dynamique des populations
larvaires du cestode Flamingolepis liguloides dans une population d'Artemia en
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maintaining overwintering shorebirds populations: how redshank use tidal mudflats and
adjacent saltworks in southern Europe. The Condor 103: 21-30.
Mittelbach, G.G. & Osenberg, C.W. 1994. Using foraging Theory to study trophic
interactions. Pages 45-59 in D.J. Stouder, K.L. Fresh, and R.J. Feller (eds.), Theory and
application in fish feeding ecology, Belle W. Baruch Library in Marine Sciences, no.
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Nagy, K. A. 2001. Food requirements of wild animals: Predictive equations for free-
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18
CHAPTER 1 THE DIET OF REDSHANK
19
CHAPTER 1
SEASONAL VARIATION IN THE DIET OF THE REDSHANK TRINGA
TOTANUS IN THE ODIEL MARSHES, SOUTH-WEST SPAIN: A
COMPARISON OF FAECAL AND PELLET ANALYSIS
MARTA I. SÁNCHEZ1, 2, ANDY J. GREEN1 AND ELOY M. CASTELLANOS2
1Departamento de Biología Aplicada, Estación Biológica de Doñana, Avenida de María Luisa s/n,
Pabellón del Perú, 41013 Sevilla, Spain2Departamento de Biología Ambiental y Salud Pública, Facultad de Ciencias Experimentales,
Universidad de Huelva, Campus de El Carmen, Avda. Fuerzas Armadas s/n, 21071 Huelva, Spain
Key words: Tringa totanus, diet, faecal analysis, pellet analysis, Odiel marshes,
migration
Running head: The diet of Redshank
Bird Study 52: 210-216.
CHAPTER 1 THE DIET OF REDSHANK
20
ABSTRACT
Capsule Redshank diet from southern Europe during migration shows spatial and
seasonal variations
Aims To assess seasonal variation in Redshank diet at a major passage site, and to
compare data derived from analysing pellets or faeces.
Methods At the Odiel marshes in 2001, pellets from spring migration (39), autumn
migration (121) and midwinter (15) were analysed, together with faecal samples from
autumn (84).
Results The abundance of different invertebrate groups in pellets varied between
seasons. In spring, Chironomus salinarius pupae and larvae dominated by volume,
followed by Ephydridae larvae and the beetle Paracymus aenus. Polychaetes and
molluscs dominated in autumn, and isopods in midwinter. In autumn, chironomid
larvae, Mesembryanthemum nodiflorum seeds and Artemia cysts were relatively more
abundant in faeces, whereas polychaetes, isopods, molluscs and cestode cysticercoids
were more abundant in pellets. Harder and/or larger items were thus relatively more
abundant in pellets than faeces. Pellet analysis gave more emphasis to mudflat prey, and
faeces to saltpan prey.
Conclusion Pellet and faecal analysis give different results for wader diet, and it is
useful to combine the two methods. However, they show significant correlations both in
diet range and rank abundance of prey items. Redshank diet shows much seasonal and
spatial variation in southern Europe.
CHAPTER 1 THE DIET OF REDSHANK
21
INTRODUCTION
The Odiel Marshes in south-west Spain are protected as a Biosphere Reserve, Ramsar
site, EU-SPA and Natural Park owing to their importance for migratory waterbirds.
They are internationally important for six species of waders including the nominal
subspecies of the Redshank Tringa totanus totanus. Here we present a detailed study of
the diet of Redshank Tringa totanus totanus using the saltpan complex within the Odiel
Marshes. This subspecies is under decline at a flyway scale (Wetlands International
2002). Loss of habitat on passage sites may be one cause of decline since energetic
requirements are particularly high during migration (Recher 1966, Davis & Smith 1998,
Pfister et al. 1998).
We compare Redshank diet during spring migration, autumn migration and
winter and assess the relative importance of prey items from salt pans and from
surrounding tidal mudflats in each period. Salt pans are known as important foraging
habitat for waders on the Atlantic coast (Velasquez et al. 1991, Masero 2003) although
no one has previously assessed their relative importance at different times of the annual
cycle. Ours is the first study of Redshank diet in southern Europe during migration.
Previous studies during migration were carred out in northern Europe where different
prey are available (Goss-Custard & Jones 1976, Goss-Custard et al. 1977).
Many species of shoreirds produce pellets containing the indigestible hard parts
of their prey. Shorebirds known to produce pellets include Turnstone Arenaria interpres
(Jones 1975), Grey plover Pluvialis squatarola (Goss-Custard & Jones 1976), Curlew
Numenius arquata (Pérez-Hurtado et al. 1997) and Common Sandpiper Actitis
hypoleucos (Arcas 2001).
Comparisons of diet between wader species, seasons or sites (e.g. Pérez-Hurtado
et al.1997, Kalejta 1993) are complicated by the use of various methods with distinct
biases (analyses of stomach contents, faeces, pellets or direct observations). We
compare the data on Redshank diet provided by analyses of faeces and pellets. Although
several authors have pointed out the need to combine the results of different methods
(Duffy & Jackson 1986, Jenni et al. 1989, Arcas 1999, Harris & Wanless 1993,
Sheiffarth 2001), as far as we are aware ours is the first study to make a detailed
comparison of methods used at the same time and place. Previous comparisons of
analyses of faeces and pellets have focussed only on the size of prey items of a given
CHAPTER 1 THE DIET OF REDSHANK
22
type (Goss-Custard et al. 1977, Dekinga & Piersma 1993), whereas we focus on the
whole range of prey items including their relative abundance and overall diversity.
STUDY AREA
The Odiel Marshes (37º17'N 06º55'W) is an estuarine complex formed at the mouths of
the rivers Odiel and Tinto, south-west Spain. They contain 6,000 ha of intertidal
mudflats and 1,185 ha of salt pans. During weekly counts throughout 2001 of our study
area which occupied 27% of the total area of salt pans, we counted up to 20,775 waders
including up to 2,170 Redshank. Numbers of Redshank peak during spring and autumn
migration.
METHODS
Samples were collected at different times of the year in 2001 from Redshank at a high
tide roost. We collected 15 pellets from midwinter Jan 13. We then collected a total of
39 pellets during spring migration from late February to late April. Likewise, 121
pellets were collected during autumn migration. In autumn, we collected 84 faecal
samples. To avoid repeated sampling from the same individuals, we only collected fresh
samples and did not collect more than one sample where several were found within 20
cm of each other. We only took samples when a monospecific group of Redshank were
observed with a telescope at the sampling spot for at least 30 minutes.
Samples were stored at 5 ºC. Prior to analysis, they were rehydrated and
separated in water, then observed with a binocular microscope in a Petri dish. Prey
items were identified using suitable keys (see Sánchez et al. 2000). The volume of each
diet component was estimated as a proportion of the total sample volume, using the
following seven categories of relative abundance: absent (assigned the rank of 1 for
non-parametric analysis), <10 % (rank of 2), 10-25 % (3), 26-50 % (4), 51-75 % (5), 76-
90% (6) and >90 % (7).
The percentage of individual samples in which each food item was recorded (i.e.
the percentage occurrence, PO) was calculated for faecal and pellet samples for each
season. Differences in PO of different diet components in pellets between the three
CHAPTER 1 THE DIET OF REDSHANK
23
seasons (spring, autumn and winter) were analysed using Kruskal-Wallis tests
employing Statistica 5.5 (StatSoft 1999). Only food items with a PO > 10% in at least
one season were analysed, and P values were Bonferroni corrected to avoid type I
errors. Mann-Whitney U tests were used as post-hoc tests to determine significant
differences between each season. The numbers of readily countable items (Artemia
cysts (eggs), seeds and cestode cysticercoids) in pellets were compared between seasons
in the same way. All these items were counted, including those that were partially
digested.
The relative abundance of prey items and number of countable items were
compared for faecal samples and pellets collected in autumn in a similar way, using
Bonferroni-corrected Mann-Whitney U tests and analyzing those items with a PO of >
10% in at least one type of sample. In order to compare the diversity of faecal and pellet
contents, we compared the number of prey items recorded in each with Mann-Whitney
U tests. To assess the similarity and repeatability of pellet and faecal contents, we
calculated the average abundance for each prey item (i.e. the average of the seven ranks
defined above), and compared these average ranks with a Spearman's rank correlation.
We excluded green plant material (mainly Chenopodiacea) from our comparison of
pellets and faeces because, in the case of faeces (but not pellets), we were unable to
distinguish reliably between material excreted and material that had become stuck to the
faeces after excretion.
In order to compare the relative abundance of chironomid larvae and pupae in
pellets for a given season, we used a sign test for each season.
RESULTS
Seasonal differences in pellet contents
The prey item recorded most often in spring pellets was chironomid C. salinarius pupae
(74% of pellets). The other prey items occurring in more than 50% of pellets were (in
order of decreasing frequency) the beetle Ochthebius corrugatus, Artemia cysts, C.
salinarius larvae, unidentified Coleoptera and green plant material (Table 1). In winter
pellets, Isopoda were the most frequently recorded prey (67% of pellets), followed by
unidentified Coleoptera, polychaetes and green plant material (Table 1). In autumn
pellets, polychaetes occurred most frequently (84%) followed by molluscs (Table 1).
CHAPTER 1 THE DIET OF REDSHANK
24
Chironomid pupae also dominated in spring pellets by volume (Table 1),
representing >90% of the volume in 13 (33%) of the samples (n = 39). The next most
important prey by volume were Ephydridae larvae and the beetle Paracymus aenus,
representing >50% of volume in 6 (15%) and 5 (13%) samples respectively. In winter
pellets, isopods were dominant, representing >90% of the volume in 6 (40%) of the
samples (n = 15). In autumn pellets, polychaetes were dominant, representing >90% of
the volume in 29 (24%) of the samples (n = 121), followed by molluscs that made up
>50% of the volume of 18 (15%) samples. Grit was unusually abundant in autumn
pellets, constituting >50% of the volume of 11 (9%) samples.
There were significant differences between seasons in the abundance of different
food items in pellets as follows (Table 1). Sonchus oleraceus seeds, chironomid larvae
and pupae, Stratiomyidae larvae, Ephydridae pupae, O. corrugatus, P. aenus and
Artemia cysts were more abundant in spring than in autumn. Chironomid larvae and
pupae and Artemia cysts were more abundant in spring than in winter. Isopods,
polychaetes and molluscs were more abundant in autumn than in spring. Artemia cysts,
polychaetes and molluscs were more abundant in autumn than in winter. Isopods were
more abundant in winter than in the other two seasons, and polychaetes were more
abundant in winter than in spring (Table 1).
We also found significant differences between seasons in the numbers of
countable items recorded in pellets: S. oleraceus seeds were more abundant in spring
than in autumn (U = 1633.5, p < 0.05). Artemia cysts were more numerous in spring
than the other two seasons (autumn: U = 1670, p < 0.05; winter: U = 562.5, p < 0.05),
and more numerous in autumn than in winter (U = 105, p < 0.01). There were no
significant differences between seasons in numbers of Arthrocnemum macrostachyum
seeds, Mesembryanthemum nodiflorum seeds or cestode cysticercoids (Flamingolepis
liguloides)
As measured by categories of volumetric abundance, chironomid pupae were
relatively more abundant in spring pellets than chironomid larvae (Sign test, z = 2.04, p
< 0.05), whereas differences in their relative abundance for other seasons (Table 1) were
not significant.
Differences between pellets and faeces in autumn
The diversity of items varied, with more classes of food items being recorded in pellets
(46) than in faeces (38). Suaeda seeds, S. oleraceus seeds and nematodes, were only
CHAPTER 1 THE DIET OF REDSHANK
25
found in faeces, while Salicornia seeds, bryozoan statoblasts, adult chironomids,
Dolichopodidae, Stratiomyidae, Ephydridae larvae, P. aenus, decapods, cirripeds and
gastropods were only found in pellets.
Polychaetes were the most frequently recorded prey items in both pellets and
faecal samples (Table 1). However, whereas molluscs were the next most important
items for pellets, Artemia cysts and O. notabilis beetles were the next most important
for faeces (Table 1).
Polychaetes were dominant in volumetric terms in both pellets (see above) and
faeces, representing >90% of the volume of 13 (15%) of faecal samples (n = 84).
Unlike pellets, in which molluscs and grit were abundant (see above), the next most
important items in faeces were chironomid larvae, M. nodiflorum seeds and Artemia
cysts (Table 1) which made up >50% of the volume of 8 (10%), 9 (11%) and 2 (2%)
samples respectively.
There were significant differences in the relative abundance of different
components between pellets and faeces. Chironomid larvae were more abundant in
faeces, whereas isopods, polychaetes, molluscs and grit were more abundant in pellets
(Table 1). Amongst countable items, M. nodiflorum seeds and Artemia cysts were more
abundant in faeces (U = 3828, p < 0.01; U = 3824.5, p < 0.01, ), whereas the number of
cestode cysticercoids was higher in pellets (U = 2714, p < 0.01).
The relative abundance of different components in pellets and faeces showed a
highly significant correlation (rs = 0.56, p < 0.01, n = 48) when comparing mean values
of volumetric ranks (see methods). The correlation for percent occurrence of each item
was equally significant (rs = 0.51, p < 0.01). However, each method gave a different
ranking to the abundance of different items (Table 2).
DISCUSSION
The diet of waders can be very variable at different moments of the tidal cycle, and
waders can excrete various pellets differing in composition during the course of one
cycle (Goss-Custard & Jones 1976, Worral 1984). In our study area, it was not possible
to collect samples throughout the tidal cycle, as only roost sites used at high tide were
accessible for sample collection. However, we collected all samples from the same
place and at the same point of the tidal cycle, to make them comparable.
CHAPTER 1 THE DIET OF REDSHANK
26
Many studies of Redshank diet have been carried out in northern Europe, where
different prey items are available (e.g. Goss-Custard 1970, Goss-Custard & Jones
1976). In southern Europe, the few previous studies have been made in winter. In faeces
from the Tagus Estuary in Portugal, the gastropod Hydrobia ulvae was dominant
(Moreira 1996). In pellets collected from salt pans in Cádiz Bay, the dominant prey
were diptera, Coleoptera and H. ulvae (Perez-Hurtado et al. 1997). In our winter pellet
samples, isopods, Coleoptera and polychaetes were dominant.
The contrast between our study and that in the Tagus may be explained by the
different composition of faeces and pellets (see below). The difference with the Cádiz
Bay study is probably explained by different management of salt pans. In Cádiz, the
depth of many evaporation ponds is reduced in autumn and winter (Masero & Pérez-
Hurtado 2001), allowing waders to feed efficiently on chironomids and other prey in the
ponds. In Odiel 90 km to the north-west, there are no drawdowns in this period, and
almost all the ponds remain too deep in winter for Redshank, forcing them to feed in the
mudflats on isopods and polychaetes.
Based on pellet composition, insect prey from salt pans were most important in
the diet in spring, whereas prey from mudflats (polychaetes, molluscs, isopods) were
most important in autumn and winter, suggesting a switch in habitat use (Table 1). The
relative value of the salt pans and mudflats as foraging habitat changes between seasons,
since fluctuations in available biomass in these two habitats are asynchronous (Masero
et al. 1999, Masero & Pérez-Hurtado 2001). Thus, in mudflats in Cádiz the biomass of
available prey dropped by a third from February to March (Masero et al. 1999), when
the biomass of chironomid prey in the Odiel salt pans increased. Furthermore, in Odiel
the depth in salt pans is reduced in spring, favouring their use by waders (Sánchez et al.
unpublished). Hence it is not surprising that the relative importance of mudflat and salt
pan species in Redshank diet changed between seasons. Our data confirm the
complementary importance of both habitat types for Redshank in the Iberian peninsula
at different times of the year (see Masero et al. 1999).
In benthic samples from the salt pans, we have found the density of chironomid
pupae to be low compared with that of larvae (one pupa per 125-162 larvae in January,
March and September 2001). Thus, the greater relative abundance of C. salinarius
pupae in Redshank pellets suggests the pupae are taken from the surface during
emergence events (Armitage et al. 1995), as supported by observations of feeding
CHAPTER 1 THE DIET OF REDSHANK
27
behavior. Pupae were most abundant in pellets in spring, when we recorded the highest
density of pupae in the sediments (64 m-2, Sánchez et al. unpublished).
The consumption of seeds by waders is common, but the reasons for this are
poorly understood (Green et al. 2002). In our study, S. oleraceus seeds were consumed
mainly in spring, coinciding with the time of seed production (Valdés et al. 1987).
Artemia cysts were most abundant in autumn and spring, the peak in cyst production
being in summer (Martínez 1989).
As we have shown, the use of different methods to study wader diet can produce
important differences in results and their associated biases. We found pellets to contain
a greater diversity of prey items than faeces, but all items recorded in more than 7.5% of
general samples were also recorded in pellets and vice versa. Thus, both kinds of
samples include all major prey items, contrary to previous suggestions (Goss-Custard et
al. 1977, Worrall 1984). Although most items are present, those found in faeces are
often more fragmented and harder to identify. Moreby (1988) suggested that the value
of faecal analysis is limited by poor detectability following digestion. In our study,
almost all arthropod groups left detectable hard parts in faeces, although their
identification is time-consuming.
These two methods give different, but correlated, indices of the relative
importance of prey, with polychaetes, isopods and mollusca being particularly abundant
in pellets, and chironomids in faeces. These differences appear to be related to
differences in digestibility, with harder items being more represented in pellets. They
also appear related to size, with smaller items being excreted as faeces. Thus, M.
nodiflorum seeds (<1 mm diameter) and Artemia cysts (<0.3 mm) were more frequent in
faeces, despite their hardness. For a given mollusc species, individuals in pellets are
larger than those in faeces (Goss-Custard et al. 1977, Dekinga & Piersma 1993). At
Cádiz Bay, the selection of prey size by Redshank was studied by comparing the size of
prey in faeces with those available (Masero & Pérez-Hurtado 2001). Our results suggest
it is important to compare both faecal and pellet contents in such studies, since they
represent different fractions of the prey sizes consumed. They also suggest that studies
comparing the diet of wader species that use faecal analysis for some species and pellet
analysis for others (e.g. Pérez-Hurtado et al. 1997) may produce misleading results.
In general, pellets give more representation to larger, harder prey items
consumed on mudflats and faeces to softer, smaller items consumed in the salt pans.We
used the average volumetric category for each prey item to rank them in importance for
CHAPTER 1 THE DIET OF REDSHANK
28
faeces and pellets (Table 2). The sum of these rankings gives a more reliable indication
of the diet composition (Duffy & Jackson 1986). This suggests that polychaetes were
most important in autumn diet, followed by Artemia cysts and O. notabilis (Table 2).
Nevertheless, even this combined method is biased owing to different digestibilities and
detectabilities between prey items. Indeed, to confirm that a combined method is more
representative than either pellets or faeces alone, it would be necessary to undertake
controlled experiments with known ingesta composition. Polychaetes were ranked first
in both sample types because they contained both hard, indigestible mandibles (recorded
mainly in pellets) and fine chaetae (detectable in faeces).
Although pellet and faecal analysis produce different results and combination of
both methods is the best option, the abundances and frequencies of prey items recorded
in the two methods are highly correlated. Thus, either method provides a useful and
related assessment of redshank diet.
ACNOWLEDGEMENTS
The first author was supported by a PhD grant from the Ministerio de Ciencia y
Tecnología. The Consejería de Medio Ambiente, Junta de Andalucía and Aragonesas
Industrias y Energía S.A. provided permission to work in the salt pans. Juan Carlos
Rubio, Director of The Odiel Marshes Natural Park, provided logistical support
and advice. Carmen Elisa Sainz-Cantero helped with invertebrate identifications. Niall
Burton and Will Cresswell provided helpful comments on the manuscript.
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Table 1. Contents of Redshank pellets and faeces, showing the percentage occurrence of each food item (PO) and the percentage of samples in
which each item represented more than 10% of the sample volume (V > 10%).Autumn Autumn (A) Spring (S) Winter (W)faeces, n = 84 pellet, n = 121 pellet, n = 39 pellet, n = 15
PREY Habitat PO V > 10% PO V > 10% PO V > 10% PO V > 10% U H PCSGREEN PLANT MATERIAL 26 7 36 1 51 3 53 ...Angiospermae S 24 7 33 1 51 3 53 ...Algae 5 ... 4 ... ... ... ... ...SEEDS 32 19 12 ... 46 3 17 ...Arthrocnemum macrostachyum M/S 4 1 3 ... 13 ... 13 ... 5.8Salicornia ... ... 2 ... ... ... ... ...Suaeda 1 ... ... ... ... ... ... ...Sonchus oleraceus S 1 ... ... ... 31 3 ... ... 44.6**** S>AMesembryanthemum nodiflorum S 26 18 2 ... 8 ... ... ... 3820**Unidentified seeds 4 1 6 ... ... ... 13 ... 4.2INVERTEBRATES 100 90 100 100 100 100 100 100Bryozoan statoblast ... ... 1 ... ... ... ... ...Chironomus salinarius (L) S 35 18 7 1 59 10 ... ... 3615.5**** 58.6**** S>A,WChironomus salinarius (P) S 33 15 10 5 74 62 7 ... 3889** 77.6**** S>A,WChironomus salinarius ... ... 1 ... ... ... ... ...Dolychopodidae (L) ... ... 2 ... ... ... ... ...Stratiomyidae (L) S ... ... 4 ... 26 ... 7 ... 16.4**** S>AEphydridae (L) ... ... 1 ... 8 5 7 7Ephydridae (P) S 1 1 11 2 28 18 27 20 4766.5 13.8*** S>AUnidentified Diptera (L) 4 1 6 ... 3 ... ... ...Unidentified Diptera (P) 10 1 1 ... ... ... ... ..Ochthebius notabilis (A) S 54 10 26 11 23 ... 33 7 3848.5** 0.70Ochthebius corrugatus (A) S 12 1 16 ... 67 ... 40 ... 4898.5 37.8**** S>AOchthebius (L) 6 ... 1 ... ... ... ... ...Paracymus aenus (A) S ... ... 1 ... 41 21 20 13 48.1**** S>AUnidentified Coleoptera (A) 42 12 33 2 54 3 60 20 4511.5 8.9*Formicidae (A) 6 2 17 3 26 ... 33 7 4553.5 3.10Unidentified Hymenoptera (A) 1 ... 1 ... ... ... 13 ... 13.1***Corixidae (A) 4 ... 1 ... ... ... 13 ... 13.1***Unidentified Insecta (A) 14 1 14 ... 18 3 13 ... 5061.5 0.40
33
Artemia parthenogenetica 17 12 2 1 ... ... ... ... 4348.5A. parthenogenetica cyst S 61 8 38 4 64 ... ... ... 3900** 17.6**** S,A>WFlamingolepis liguloides cysticercoids 23 1 27 2 28 3 ... ... 4844 5.4Isopoda M 4 ... 45 6 3 3 67 60 2985**** 33.2**** W,A>SAnphipoda 1 ... 12 3 ... ... ... ... 4510.5 7.2*Decapoda ... ... 7 ... 3 ... 27 7 9.7**Cirripedia ... ... 1 ... ... ... ... ...Ostracoda M 1 ... 20 ... ... ... ... ... 4134.5* 12.3**Unidentified Crustacea 1 ... 3 ... 10 ... ... ... 4.02Araneida 7 ... 10 ... 21 ... 7 ... 3.5Acarina 2 ... 1 ... ... ... ... ...Polychaeta M 77 39 84 72 8 3 60 20 3466.5**** 71.1**** A,W>SForaminifera M 1 ... 18 ... ... ... ... ... 4218.5* 11.1**Gastropoda ... ... 7 2 8 ... 13 7 0.50Unidentified Mollusca (shells) M 18 4 74 37 15 3 20 ... 1999.5**** 48.9**** A>W,SCestoda 4 1 2 ... ... ... ... ...Nematoda 1 ... ... ... ... ... ... ...Unidentified invertebrate 8 2 7 ... ... ... ... ... 5027.5Invertebrate eggs 11 1 10 ... 13 ... ... ... 5.7FISH 12 4 22 2 3 3 7 ... 4584 9*GRIT M/S 1 ... 56 18 23 18 47 ... 2275.5**** 9.1*OTHERS ... ... 7 ... 3 ... 7 7
L, larvae; P, pupae; A, adults. S, prey from saltpan; M, prey from tidal mudflats. Others, nylon line and other artificial objects. Seasonal
differences for pellets were tested with Kruskal-Wallis tests, H. Differences between faeces and pellets in autumn were tested with Mann-
Whitney U post-hoc tests, U. *P < 0.05, **P < 0.01 without Bonferroni correction, ***P < 0.05 after Bonferroni correction, ****P < 0.01 after
Bonferroni correction. PCS, summary of significant Pair wise Seasonal Comparisons for pellet composition with Mann-Whitney U post-hoc
tests.
CHAPTER 1 THE DIET OF REDSHANK
34
Table 2. Order of importance (by ranks) of different prey items found in autumn faeces
and pellets, and when combining both methods. The ranks were based on the mean
values of seven volumetric categories (see methods). Combined ranks were based on the
means of the two means for pellets and faeces. L, larvae; P, pupae; A, adults.
pellet faeces pellet+faecesPolychaeta 1 1 1A. parthenogenetica cyst 5 3 2Ochthebius notabilis (A) 4 5 3Unidentified Mollusca (shells) 2 9.5 4Mesembryanthemum nodiflorum 8 4 5Unidentified Coleoptera (A) 7 7 6Flamingolepis liguloides cysticercoids 9 9.5 7Chironomus salinarius (P) 13.5 6 8Fish 10 11 9Chironomus salinarius (L) 21 2 10Isopoda 6 21 11.5Formicidae (A) 11 16 11.5Ochthebius corrugatus (A) 16.5 13 12Grit 3 27 13Invertebrate eggs 19.5 12 14Artemia parthenogenetica 26 8 15Ephydridae (P) 13.5 21 16Araneida 19.5 17 17Arthrocnemum macrostachyum 23 14 18Ostracoda 12 27 19Foraminifera 15 27 20Cestoda 28 15 21Anphipoda 16.5 27 22.5Algae 24.5 19 22.5Ochthebius (L) 33.5 18 24Gastropoda 18 35.5 25Corixidae (A) 33.5 21 26Acarina 33.5 23 27Decapoda 22 35.5 28Stratiomyidae (L) 24.5 35.5 29Salicornia 28 35.5 30.5Dolychopodidae (L) 28 35.5 30.5Suaeda 39 27 35.5Sonchus oleraceus 39 27 35.5Nematoda 39 27 35.5Bryozoan statoblast 33.5 35.5 35.5Chironomus salinarius (A) 33.5 35.5 35.5Ephydridae (L) 33.5 35.5 35.5Paracymus aenus (A) 33.5 35.5 35.5Cirripedia 33.5 35.5 35.5
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
35
CHAPTER 2
SPATIAL AND TEMPORAL FLUCTUATIONS IN USE BY SHOREBIRDS AND
IN AVAILABILITY OF CHIRONOMID PREY IN THE ODIEL SALTPANS,
SOUTH-WEST SPAIN
MARTA I. SÁNCHEZ1,2, ANDY J. GREEN1 AND ELOY M. CASTELLANOS2
1Departamento de Biología Aplicada, Estación Biológica de Doñana, Avenida de María Luisa s/n,
Pabellón del Perú, 41013 Sevilla, Spain2Departamento de Biología Ambiental y Salud Pública, Facultad de Ciencias Experimentales,
Universidad de Huelva, Campus de El Carmen, Avda. Fuerzas Armadas s/n 21071 Huelva, Spain
Key words: saltpans, Chironomus salinarius, salinity, shorebirds, foraging habitat,
Odiel marshes
Running head: Spatial and temporal fluctuation in shorebirds and chironomids
Hydrobiologia 567: 329-340.
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
36
ABSTRACT
We studied the seasonal variation in abundance and distribution of shorebirds and
chironomid Chironomus salinarius larvae in both traditional and industrial salines in the
Odiel marshes, south-west Spain, in 2001. We selected 12 ponds that were
representative of the different phases of the salt production process. The benthic
chironomids were sampled in each pond every two months, and the birds were counted
weekly. Chironomid larvae were most abundant in spring and autumn, and in the ponds
of lower salinity. The density of larvae averaged 7023 ± 392 m-2 (± s.e) over the six
sampling events. Shorebirds were always more abundant at high tide than at low tide,
and were especially abundant during the spring and autumn migration periods when up
to 20,775 birds were counted. A total of 24 species were recorded, six of which were
present in internationally important numbers. The salines were especially important as
foraging and roosting habitat during migration. The percentage of birds that were
feeding in the ponds was positively correlated with the abundance of chironomid larvae
at accessible depths. The number of feeding birds was also higher in ponds with more
chironomid larvae available. Despite more intensive management, industrial salines
held higher densities of birds and a similar abundance of chironomids when compared
with traditional salines.
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
37
INTRODUCTION
Many shorebirds or waders (Charadrii) are long distance migrants which migrate
thousands of kilometres between breeding and wintering sites and are heavily dependent
on passage sites along the flyways, where they can rest and refuel (Alexander et al.
1996, Iverson et al. 1996). Natural and artificial coastal wetlands tend to be highly
productive and are a vital habitat for these birds (Velasquez 1992, Masero 1999), which
are very sensitive to habitat change (Alexander et al. 1996). In recent decades, many
coastal wetlands have been destroyed or transformed, resulting in major impacts on
shorebird populations (Goss-Custard et al. 1977a,b, Goss-Custard & Moser 1988).
Artificial wetlands such as salines can provide important foraging habitats for
shorebirds, especially at high tide when intertidal marshes are flooded and inaccessible
(Pérez-Hurtado & Hortas 1991). Salt production via the circulation of sea water through
a system of ponds in salines is an ancient activity in the Mediterranean region and other
warm coastal areas (Britton & Johnson 1987). Aquatic invertebrates in saltpans
represent abundant prey for shorebirds (Velasquez 1992), although there are relatively
few invertebrate taxa owing to the extreme salinities. Amongst these taxa, chironomid
larvae are particularly important (Velasquez 1992, Pérez-Hurtado et al. 1997).
The Odiel marshes in south-west of the Iberian peninsula are one of the most
diverse and productive coastal marsh systems in southern Europe (Castellanos et al.
1998). They are situated on the East Atlantic flyway (Smit & Piersma 1989), and their
importance for waterbirds has led to their protection as a Natural Park, Ramsar site
(Bernués 1998) and Biosphere Reserve. The salines represent 16% of the surface area of
the marshes, and are an important feeding and roosting area for shorebirds. During the
migration periods and in winter, flocks of over 12,000 birds can regularly be observed.
However, there are no previous studies of the shorebird and invertebrate communities
in the salines, or of shorebird habitat use.
In this study, we describe the seasonal variation in the abundance and
distribution of shorebirds in the Odiel salines, as well as in the abundance and
distribution of one of their principle prey species, the chironomid Chironomus
salinarius. We assess the differences between saltpans of different salinities and
between industrial salines (with an intensive salt production process) and traditional
salines in their value for shorebirds and their prey. We test whether or not chironomid
abundance predicts the abundance of foraging shorebirds in space and time. We
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
38
consider what changes to current management may increase the shorebird carrying
capacity of our study site.
STUDY AREA
The Odiel marshes (37º17'N 06º55'W), found in the combined estuaries of the Tinto and
Odiel rivers, are tidal marshes with a total surface area of 7,185 ha. The salines occupy
1,185 ha, of which c.1,118 is an industrial saline complex and c.56 ha is a traditional
saline (Figure 1).
In both kinds of salines, sea water is introduced via a tidal canal to a complex of
large and deep ponds which act as reservoirs (the primary evaporation ponds PEPs),
where the salinity is relatively low and the diversity of invertebrates relatively high.
From there, the water circulates into a system of shallower ponds (the secondary
evaporation ponds SEPs) with intermediate salinity and where the invertebrate
community is dominated by C. salinarius in the benthos and the brine shrimp Artemia
parthenogenetica in the water column. These two species are the most abundant prey
for waterbirds in the salines. C. salinarius is actually a species complex requiring
further taxonomic study (Armitage et al. 1995). The brine shrimp population is
dominated by the diploid form of A. parthenogenetica (F. Amat pers. comm., Amat et
al. 1995).
From the secondary evaporation ponds, the water passes to the pre-
crystallization ponds (PCPs), a group of shallow and hypersaline ponds where water is
stored until it approaches saturation point. Finally, the water then enters the
crystallization ponds (CPs), where the salt precipitates and is harvested (Figure 1). The
abundance of invertebrates in these last two classes of ponds fluctuates according to the
salt concentration.
METHODS
Invertebrate sampling
Twelve ponds covering the range of salinities were selected and sampled throughout
2001, including nine in the industrial salines and three in the traditional salines (Figure
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
39
1). The ponds included two PEPs, six SEPs, two PCPs and two CPs. The traditional
saline is more a labyrinth of canals than a complex of ponds, through which the water
flows continuously. We did not sample the traditional PEP, which was too deep for
shorebirds.
The benthos was sampled every two months, selecting four points at random
from each pond within the depth range accessible to shorebirds (0-20 cm, Ntiamoa-
Baidu et al. 1998). At each point, three core samples were taken to a depth of 3 cm with
a 19.6 cm2 corer. The salinity was measured at the same time using a densometer. In the
laboratory, the sample was filtered through 0.5 and 0.1 mm sieves. In order to separate
chironomids from the sediments retained in the sieves, we floated them in saturated salt
solution collected from a CP. The larvae and pupae were collected from the surface and
preserved in 70% ethanol.
Shorebird counts
In each of the study ponds we counted the number of shorebirds of each species that
were feeding and resting one day each week, using a 20-60x telescope. On each day, we
carried out two counts of three hours duration, one centred around high tide and the
other around low tide. The ponds were always counted at the same time (by choosing to
count on the day that high or low tide occurred around 09:00 h) and always following
the same route between ponds.
Calculation of the available surface area
In most of the ponds, only shallow areas of 0-20 cm around the edge and around islands
are available to foraging shorebirds. The accessible surface area varies with fluctuations
in the overall water level, which were monitored by recorded depth at a reference point
in each pond at the time of conducting surveys. The depth profile of each pond was
established by conducting various transects, and the surface area accessible for foraging
at the time of survey was estimated via image analysis (Sigma Scanpro, version 4.0).
Statistical analysis
The abundance of chironomid larvae and pupae and of shorebirds were analyzed using
generalized linear models (GLMs) following GENMOD procedure in SAS (v. 8.2, SAS
Institute 2000). POND and MONTH were included as fixed factors. POND had 12
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
40
levels for the shorebird model, but only nine for the chironomid models as three ponds
where chironomids were absent in all but one month were removed. MONTH had 12
levels for shorebirds and six for chironomids. For the shorebird model, we also include
TIDE as a fixed factor of two levels (low or high). Owing to overdispersion observed in
the data for larvae and shorebirds, we used a negative binomial error distribution (Bliss
& Fisher, 1953, Kopocinski et al. 1998), log link function and type III tests. Such a
model for pupae did not converge owing to the high proportion of zeros, so we
conducted a non-parametric analysis using ranks in GENMOD with an identity link
(RANK procedure in SAS).
The deviance of each fitted GLM model is analogous to the residual sum of
squares in ordinary linear regression. The reduction in deviance compared to the null
model is used to assess the contribution of the model to the explanation of the variance
in the data set. The significance of the reduction in deviance can be estimated by
comparison with the distribution of the chi-square statistic, with degrees of freedom df
equal to the change in df compared to the null model. Post-hoc differences between two
levels of a factor were tested with the Wald chi-square test for differences between
least-squares means (SAS Institute Inc. 1997).
Spearman’s rank correlations were conducted between the proportion of
shorebirds that were feeding and the number of chironomid larvae available, and
between salinity and the density of larvae.
RESULTS
Abundance of chironomids
Chironomid larvae were present in the sediments all year round but with a marked
pattern in seasonal abundance (Figure 2), with the first and strongest peak in May (mean
of 11,835 ± 1,470 larvae m-2, mean ± s.e., n = 804) and a second peak in November
(9,933 ± 1,063 m-2). The same patterns were observed for large and small larvae
collected from the 0.5 and 0.1 mm sieves, although the larger larvae were relatively
more abundant when the total number of larvae was lower (Figure 2). Larvae were only
recorded in the CPs and the industrial PCP during one month (November for the
traditional CP, March for the other two ponds). In the CPs, this was probably owing to
the compacted sandy nature of the sediments and the effects of salt crystallization, while
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
41
in the PCP it was owing to incrustations of gypsum salts on the sediment surface which
made it impossible for larvae to enter the sediments and construct their tubes.
The annual average density of chironomid larvae varied between different
ponds, with the highest densities recorded in PEPs and SEPs and the lowest in the CPs
(Table 1). This suggests a gradual decrease in larval density during the evaporation and
crystallization process, as confirmed by a significant negative correlation between
average salinity in each pond and the average larval density (rs = -0.713, P = 0.008, n =
12). There were no consistent differences between industrial and traditional salines in
the abundance of larvae for a given salinity type (Table 1).
GLMs revealed highly significant effects of POND, MONTH and the
POND*MONTH interaction on the abundance of benthic chironomid larvae (Table 2).
Thus, there were strong differences in abundance between different ponds and times of
the year, while seasonal differences varied between ponds (as shown by differences
between ponds in the month when abundance peaked, Table 1). Similar results were
recorded for GLMs analysing the numbers of large (those retained on a 0.5mm sieve)
and small (those retained on a 0.1 mm sieves) larvae (Table 2). In a GLM for benthic
pupae, the POND*MONTH interaction was highly significant (Table 2), indicating that
seasonal patterns in chironomid emergence were not consistent between ponds.
Abundance of shorebirds
A total of 24 shorebird species were recorded in the study area, the most abundant
being dunlins (Calidris alpine (L.)), black-tailed godwits (Limosa limosa (L.)), and
curlew sandpiper (Calidris ferruginea (Pontoppidan)) (Table 3). The highest count was
of 20,775 birds in April. The total numbers of shorebirds showed a strong seasonal
pattern, with peak counts in April and August coinciding with the pre and post-breeding
migration periods (Figure 4). The post-breeding migration was the stronger and more
prolonged, with high counts being recorded from July to September. In contrast, the pre-
breeding migration was only marked during April (Figure 4). The number of birds
recorded in the salines was always higher at high than at low tide (Figure 4). The
proportion of birds that remained at low tide varied between seasons, and was higher
during spring migration than autumn migration (Figure 4).
In a GLM, there were highly significant main effects of POND, MONTH and
TIDE on the number of shorebirds (Table 2). All two way interactions were also highly
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
42
significant. Thus, we recorded strong spatial, temporal and tidal effects on the
distribution of shorebirds that interacted in a complex way.
The seasonal patterns in abundance varied greatly between shorebird species.
Amongst the more abundant species (Table 3), dunlins (Calidris alpina) and little stints
(Calidris minuta (Leisler)) showed only a strong spring migration. In contrast, black-
tailed godwits (Limosa limosa), curlew sandpipers (Calidris ferruginea), redshanks
(Tringa tetanus (L.)), avocets (Recurvirostra avosetta (L.)), kentish plovers (Charadrius
alexandrinus (L.)) and black-winged stilts (Himantopus himantopus (L.)) showed only a
strong autumn migration. Ringed plovers (Charadrius hiaticula (L.)) and grey plovers
(Pluvialis squatarola (L.)) showed both a strong spring and a strong autumn migration.
Relationship between the abundance of chironomids and of shorebirds
When we analyze the use of the salines by shorebirds throughout the year, we find that
the proportion of birds observed feeding was strongly correlated with the availability of
chironomid larvae (Rs = 0.88, p = 0.033, n = 6). The proportion of birds feeding was
highest in May when the abundance of chironomid larvae was greatest (Figure 5). There
was also a strong positive correlation between the number of larvae available in each
pond and the number of feeding shorebirds (using annual means, Rs = 0.66, p = 0.019, n
= 12).
In the traditional salines, a higher proportion of the surface area of ponds is
available for foraging (25% on average, compared with 10% for industrial salines, Table
1). Nevertheless, the highest densities of shorebirds were recorded in the industrial
salines, where the peaks corresponding to the spring and autumn migrations were very
pronounced (Figure 6). In the traditional salines the highest density was recorded during
the winter period in February (Figure 6). On average, 8.5% of available foraging habitat
was found in the traditional salines (Table 1). Thus, 15 of 16 shorebird species with
average counts of more than 10 individuals made more use of the industrial salines for
foraging than would be expected at random (Table 3).
DISCUSSION
Chironomus salinarius is a chironomid species (complex) that is particularly tolerant of
high salinities (Armitage 1995) and is often recorded as the only benthic invertebrate
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
43
species. In the nearby Cádiz Bay, this species is thought to have about five generations a
year (Arias & Drake 1995). Such multivoltinism is characteristic of latitudes such as
those of southern Spain, where high temperatures allow high growth rate (Huryn 1990).
The presence of pupae throughout the annual cycle in our samples confirms that this
species must have many generations a year, since the benthic pupal stage lasts a few
days at most (Armitage 1995).
For the salines as a whole, we observed a marked seasonality in the abundance
of larvae of this species, with peaks in May and November. This pattern contrasts with
those observed in marine soft-bottom habitats in temperate regions, where abundance of
invertebrates peaks in winter and spring (Service & Feller 1992). Our results are also
different to those found in a tidal lagoon in Cádiz bay, where the abundance of larvae
peaked from late summer until winter (Drake & Arias 1995). This difference is probably
related to the differences in habitat and management of water levels at each site (see
Drake & Arias 1995). Differences in management of water levels between individual
ponds are also likely to explain the strong POND*MONTH interaction we observed at
our site.
In our study site, the main salinity gradient is spatial between ponds rather than
temporal between months of different temperatures (as observed in other Mediterranean
aquatic systems), and we recorded a negative correlation between the salinity of each
pond and the larval density. Thus, high salinities allow C. salinarius to monopolise
benthic resources, but further increases appear to reduce growth and/or survival rates.
Similar effects of extreme salinities on the density of chironomid larvae have been
recorded in other wetland types (Galat et al. 1988, Hammer et al. 1990). A negative
correlation between larval abundance and salinity was also recorded in Cádiz Bay
(Arias & Drake 1994), but it confounds spatial and temporal variation and is hard to
interpret.
Chironomid larvae are one of the principal food items of shorebirds in the
coastal wetlands of southern Europe (Pérez-Hurtado et al. 1997), unlike northern
Europe where polychaetes, gastropods and bivalves tend to be dominant prey (Goss-
Custard 1977a, Worral 1984, Durell & Kelly 1990, but see Rehfisch 1994). The high
density and availability of Chironomus salinarius (together with that of Artemia) makes
the Odiel salines an important foraging habitat for shorebirds, especially during the
migration periods. During autumn passage, most birds used the salines only at high tide
when the tidal marshes were unavailable, leaving to feed in the tidal marshes at low
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
44
tide. Similar results have been reported in salines elsewhere (Masero et al. 2000).
However, during spring passage we found most shorebirds to remain in the salines at
low tide, suggesting that the salines provided a relatively better foraging habitat in
spring than in autumn. The strong relationship detected between changes in the density
of chironomid larvae and in the numbers of feeding shorebirds suggests that the birds
make decisions about feeding in salines and which pond to feed in based largely on the
availability of chironomids. Previous studies in other regions have shown that
shorebirds respond to variation in prey density, with a positive correlation between prey
density and bird density (Goss-Custard 1970, Goss-Custard et al. 1977a, Goss-Custard
et al. 1991, Velasquez 1992). The same pattern appears to occur in the Odiel salines.
Further evidence that changes in the density of chironomid prey determine these
changes in the use of salines by foraging shorebirds comes from a diet study of the
redshank (Sánchez et al. in press). Pellets collected in spring 2001 were dominated by
invertebrate prey from the salines (chironomid larvae and pupae, and Coleoptera), while
those collected in autumn were dominated by prey from the tidal marshes (isopods,
bivalves and polychaetes). Of 39 pellets collected in spring, 59 % contained chironomid
larvae, compared to only 6.6 % of 121 pellets from the autumn (χ2 = 48.47, P < 0.001).
Nevertheless, the abundance of chironomid pupae in these pellets (found in 74.4 % of
pellets in spring and 9.9% in autumn, χ2 = 60.93, P < 0.001), despite the relative rarity
of pupae in the benthos suggests that, as well as feeding on chironomids in the
sediments, shorebirds also take pupae as they come to the surface and before the adults
have had time to emerge.
Changes in use of the salines by shorebirds will also depend on fluctuations in the
availability of prey in tidal marshes between seasons. We have no data to assess how prey
abundance in tidal marshes differed between spring and autumn. Between the spring and
autumn migrations, we also observed an important shift in the composition of the shorebird
community, e.g. with relatively more dunlins and little stints in spring and more black-
tailed godwits, avocets and black-winged stilts in autumn. Given the differences in diet and
habitat use by these species, these changes may also have influenced the relative increase
in the use of salines for foraging during the spring migration.
We found that the more traditional manner of salt production did not produce a higher
availability of chironomid prey, and did not provide a preferred habitat for waders. Waders
were found at a higher density in the industrial salines, perhaps because these ponds were
larger than traditional ones (Figure 1) and thus permit more effective vigilance against
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
45
predators (Cayford 1993), and because the traditional salines suffered more disturbance
from a road.
The extent to which a high production of chironomid larvae is translated into a
good foraging habitat for shorebirds depends largely on appropriate management of
water levels (Velasquez 1992, Rehfisch 1994). Smaller shorebird species are those that
are most limited in the depth range where they can feed, and also those most dependent
on alternative, artificial habitats such as salines since their low body mass and high
metabolic rate requires them to feed practically all day round (Goss-Custard et al.
1977b, Fasola & Canova 1993). Some species such as avocets are less limited by water
depth, as they also feed on Artemia in deeper parts of our study site (by swimming and
taking brine shrimps close to the surface).
The high ecological and conservation value of the Odiel salines is obvious given
the numbers and diversity of birds that it supports. For six different species, our partial
counts sometimes exceeded the 1% threshold for the flyway population used to identify
wetlands of international importance for a given species (Table 3). The salines offer both a
good food supply and disturbance-free areas for resting, two key factors that determine the
habitat use by shorebirds (Goss-Custard 1969). Nevertheless, the quality of the habitat as a
foraging area could be increased by changing management practices to increase the
accessibility of chironomids to shorebirds, and particularly by using drawdowns to
increase access to deeper areas during the migration periods. At the moment, the
proportion of chironomid production that is consumed by birds is relatively low compared
to lagoons managed specifically for birds (Rehfisch 1994). In most of the ponds, the
majority of the benthos is inaccessible to shorebirds throughout the year (Table 1). On the
other hand, in those areas of our study ponds where shorebirds are able to feed, exclosure
experiments show that shorebird predation has a “top-down” effect in regulating the
density of chironomid larvae (authors, unpublished data). This suggests that the foraging
intake of a shorebird feeding at a given moment is likely to be limited by shorebird use of
the site in the previous weeks, and underlines the potential benefits of drawdowns so that
the Odiel salines can provide a more efficient refuelling site for a larger number of
migratory shorebirds.
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
46
ACKNOWLEDGEMENTS
The first author was supported by a phd grant from the Ministerio de Ciencia y
Tecnología. Consejería de Medio Ambiente, Junta de Andalucía and Aragonesas
Industrias y Energía S.A. provided permission to work in the salines. Juan Carlos
Rubio, Director of the Odiel Marshes Natural Park, provided logistical support
and advice. Claudine de le Court, José Manuel Sayago and Enrique Urbina also
provided helpful advice. Raquel Alejandre and Carlos Roldán helped with field work.
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SAS Institute Inc. (1997) SAS/STAT Software, changes and enhancements through
Release 6.12. Cary, NC.
SAS Institute Inc. (2000) SAS/STAT software, User’s Guide. Cary, NC. Service, S.
K. & Feller, R.J. 1992. Long-term trends of subtidal macrobenthos in North Inlet,
South Carolina. Hydrobiologia 231: 13–40.
Smit, C. J. & Piersma, T. 1989. Numbers, midwinter distribution, and migration of
wader populations using the East Atlantic Flyway. Pages 24-63 in Flyways and reserve
networks for water birds (H. Boyd and J.-Y. Pirot, Ed.). International Waterfowl and
Wetlands Research Bureau, Slimbridge.
Velasquez, C. R. 1992. Managing artificial saltpans as a waterbirds habitat: species'
responses to water level manipulation. Colonial Waterbirds: 15(1): 43-55.
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
50
Worral, D. H. 1984. Diet of the Dunlin Calidris alpina in the Severn estuary. Bird
Study 31: 203-212.
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
51
Table 1. Annual average salinity, size and density of chironomid larvae recorded in
individual saltpans in Odiel, 2001. See methods for details of pond type and how
available surface area was calculated. I = industrial, T = traditional.
Pond Pond type ManageSalinity(g/cm3)
Total surfacearea (m2)
Availablesurface (m2)
Chironomiddensity (m-2,mean ± s.e.)
Peak density(month)
1 PEP I 1.03 842200 550 ± 400 3984 ± 1267 8068 (nov)2 PEP I 1.04 790700 5787 ± 1229 20396 ± 5688 44671(may)3 SEP I 1.09 196100 48039 ± 5948 2505 ± 951 5817(mar)4 SEP I 1.09 171900 37165 ± 14641 5846 ± 1814 13461 (mar)5 SEP I 1.07 176300 34215 ± 2168 9193 ± 2806 19873 (nov)6 SEP I 1.07 512200 43552 ± 3170 13234 ± 3144 25223 (nov)7 SEP I 1.07 179100 13434 ± 951 10389 ± 3564 23524(nov)8 PCP I 1.1 164500 77109 ± 969 106 ± 106 637(mar)9 CP I 1.16 90253 51828 ± 40623 64 ± 44 255(mar)10 SEP T 1.04 41938 8943 ± 0 6723 ± 3563 24331(nov)11 PCP T 1.08 28092 6154 ± 0 5761 ± 2619 17028(may)12 CP T 1.09 37579 11428 ± 0 226 ± 226 1359 (nov)
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATIONS IN SHOREBIRDS AND CHIRONOMIDS
52
Table 2. Summary of GLM models testing the effects of POND, MONTH and TIDE on the
abundance of Chironomidae larvae and pupae and shorebirds in the Odiel salines. For larvae,
totals are modelled as well as the number of larvae retained on 0.5 mm and 0.1 mm sieves. Main
effects shown are those observed when interactions are not included in the model. D =
percentage of additional deviance explained by the final model in comparison to null models.
See methods for more details.
Effect df Chi-Square pTotal larvae pond 8 71.84 < 0.0001
month 5 67.56 < 0.0001N = 216D = 4.92% pond*month 40 99.65 < 0.00010.5 Larvae pond 8 44.6 < 0.0001
month 5 27.25 < 0.0001N = 216D = 4.32% pond*month 40 97.25 < 0.00010.1 Larvae pond 8 85.6 < 0.0001
month 5 101.03 < 0.0001N = 216D = 8.30% pond*month 40 129.48 < 0.0001Pupae pond 8 10.25 0.2477
month 5 6.25 0.2823N = 216D = 35.03% pond*month 40 76.94 0.0004Shorebirds pond 11 671.93 < 0.0001
month 11 213.73 < 0.0001tide 1 84.24 < 0.0001pond*month 121 758.19 < 0.0001pond*tide 11 71.4 < 0.0001
N = 467D = 14.99%
month*tide 11 44.65 < 0.0001
Table 3. Shorebird species recorded in our study site and their abundance. Note figures refer to counts made in the ponds selected for our study
(i.e. only part of the salines). * highest counts exceeded the 1% threshold for the flyway population used to identify wetlands of international
importance for a given species (Delany & Scott 2002).
Common name Latin name Mean count ± s.e. Range of countsMean number offeeding birds ± s.e.
Range of feedingbirds
% feeding intraditional salinas
dunlin* Calidris alpina 1750 ± 453 17-15689 803 ± 262 7-1068 0.3black-tailed godwit* Limosa limosa 1209 ± 254 0-6684 232 ± 56 0-1309 9.5curlew sandpiper Calidris ferruginaea 925 ± 220 0-5567 459 ± 122 0-3214 0.0redshank Tringa totanus 693 ± 91 5-2170 366 ± 50 2-1310 5.3ringed plover* Charadrius hiaticula 332 ± 67 0-1780 97 ± 32 0-1182 0.2avocet* Recurvirostra avosetta 309 ± 43 2-1155 42 ± 9 0-227 1.4grey plover Pluvialis squatarola 253 ± 56 0-1313 30 ± 14 0-480 0.2kentish plover* Charadrius alexandrinus 179 ± 50 0-1561 72 ± 30 0-1180 0.0Little stint Calidris minuta 166 ± 36 0-888 143 ± 29 0-885 1.0black-winged stilt* Himantopus himantopus 148 ± 33 0-817 97 ± 23 0-572 5.3bar-tailed godwit Limosa lapponica 68 ± 21 0-754 16 ± 13 0-507 0.0sanderling Calidris alba 63 ± 14 0-364 47 ± 11 0-332 0.2curlew Numenius arquata 58 ± 22 0-830 0.07 ± 0.05 0-2 0.0spotted redshank Tringa erythropus 43 ± 12 0-351 28 ± 10 0-306 5.0greenshank Tringa nebularia 25 ± 6 0-202 15 ± 4 0-162 6.3turnstone Arenaria interpres 17 ± 5 0-143 10 ± 3 0-101 4.6red knot Calidris canutus 7.32 ± 4.43 0-166 2.97 ± 1.47 0-47 0.0whimbrel Numenius phaeopus 5.5 ± 3.07 0-121 0.07 ± 0.05 0-2 0.0oystercatcher Haematopus ostralegus 3.95 ± 0.79 0-17 0 0 ....ruff Philomachus pugnax 3.1 ± 1.79 0-71 2.2 ± 1.22 0-48 21.6little ringed plover Charadrius dubius 2.07 ± 1.70 0-68 1.65 ± 1.57 0-63 0.0common sandpiper Actitis hypoleucos 0.25 ± 0.08 0-2 0.2 ± 0.07 0-2 75.0marsh sandpiper Tringa stagnatilis 0.15 ± 0.10 0-4 0.02 ± 0.02 0-1 0.0red-necked phalarope Phalaropus lobatus 0.1 ± 0.06 0-2 0.1 ± 0.06 0-2 0.0Total 6253 ± 758 53-20775 2466 ± 368 49-13438 2.2
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATION IN SHOREBIRDS AND CHIRONOMIDS
54
Figure 1. The location of the Odiel salines in SW Spain, and of our study ponds in the
traditional and industrial salines.
Spain
1
OdielRiver
0 1000 m
2
3
6
5
4
87
9
111210
PEPsSEPPCPCP
IndustrialTraditional
Road
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATION IN SHOREBIRDS AND CHIRONOMIDS
55
Figure 2. Seasonal variation in the density of chironomid larvae (mean ± s.e., n = 144
for each month), in the Odiel saltpans in 2001.
Ja Ma My Jl Se No
Chi
rono
mid
larv
ae (N
º. m
-2)
0
2000
4000
6000
8000
10000
12000
14000
Larvae (0.5)Larvae (0.1)Total larvae
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATION IN SHOREBIRDS AND CHIRONOMIDS
56
Figure 3. Seasonal variation in the density of chironomid pupae (mean ± s.e., n = 144
for each month), in the Odiel saltpans in 2001.
Ja Ma My Jl Se No
Chi
rono
mid
pup
ae (N
º. m
-2)
0
20
40
60
80
100
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATION IN SHOREBIRDS AND CHIRONOMIDS
57
Figure 4. Total number of shorebirds counted (mean ± s.e., n = 4 counts for each month)
in our 12 study ponds in the Odiel saltpans at high and low tide, 2001.
Ja Fe Ma Ap My Jn Jl Au Se Oc No De
Nº o
f sho
rebi
rds
0
2000
4000
6000
8000
10000
12000
14000
16000High tideLow tide
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATION IN SHOREBIRDS AND CHIRONOMIDS
58
Figure 5. Fluctuations in the percentage of shorebirds that are feeding, compared with
changes in the number of chironomid larvae available. Using the bird census conducted
at that date closest to the date of benthic sampling, we calculated the proportion of birds
present at high tide that were feeding. Using densities of larvae and the surface area of
ponds that were available to shorebirds (i.e.≤ 20 cm), we estimated the number of larvae
available.
ja ma my jl se no
% o
f fee
ding
sho
rebi
rds
0
10
20
30
40
50
Chi
rono
mid
larv
ae
2.0e+7
4.0e+7
6.0e+7
8.0e+7
1.0e+8
1.2e+8
1.4e+8
1.6e+8
1.8e+8
2.0e+8
2.2e+8
2.4e+8
% of feeding shorebirds at high tideChironomid larvae
CHAPTER 2 SPATIAL AND TEMPORAL FLUCTUATION IN SHOREBIRDS AND CHIRONOMIDS
59
Figure 6. Average monthly density of shorebirds recorded at high tide in industrial and
traditional salines. Densities were recorded based on the total surface area of salines.
Ja Fe Ma Ap My Jn Jl Au Se Oc No De
Sho
rebi
rds
(Nº .
1000
has
-1)
0
20000
40000
60000
80000IndustrialTraditional
60
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
61
CHAPTER 3
SEASONAL AND SPATIAL VARIATION IN THE AQUATIC INVERTEBRATE
COMMUNITY AT THE ODIEL SALT PANS (SW SPAIN) AND THEIR
IMPLICATIONS FOR MIGRATORY WADERS
MARTA I. SÁNCHEZ1,2, ANDY J. GREEN1 AND ELOY M. CASTELLANOS2
1Departamento de Biología Aplicada, Estación Biológica de Doñana, Avenida de María Luisa s/n, Pabellón del
Perú, 41013 Sevilla, Spain2Departamento de Biología Ambiental y Salud Pública, Facultad de Ciencias Experimentales, Universidad de
Huelva. Campus de El Carmen. Avda. Fuerzas Armadas s/n 21071 Huelva, Spain
Key words: Artemia parthenogenetica, Cletocamptus retrogressus, diversity, saltpans,
salinity, shorebirds, species richness, Odiel marshes, wind
Running head: Aquatic invertebrate community in the Odiel salt pans
Archive für Hydrobiologie 166: 199-223.
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
62
ABSTRACT
We studied the seasonal variation in abundance and distribution of invertebrates in the water
column in both traditional and industrial salines in the Odiel marshes, south-west Spain, in
2001. We selected 12 ponds that were representative of the different stages of salt production.
Every two months, the invertebrates were sampled at four points in each pond within the 0-20
cm depth range used by foraging waders. We identified 41 taxa in our samples, including 30
aquatic and nine terrestrial metazoan invertebrates. Invertebrate species richness and diversity
decreased significantly with pond salinity, whereas an index of biomass (sample volume)
showed a non-significant increase. Overall, Artemia parthenogenetica constituted 67.6% of
the total number of invertebrates sampled, and 95.5% of the biomass. The copepod
Cletocamptus retrogressus was next in importance, representing 31.1% of the total number of
invertebrates sampled, and 0.6% of the biomass. Invertebrate biomass and dominance of
Artemia was highest in September and lowest in November. There was significant spatial and
temporal variation in abundance for all major aquatic taxa, and for a given pond and month
the depth, distance to shoreline and fetch (wind effects) all had an important partial effect on
invertebrate distribution. Ordination methods showed a strong relationship between variation
in community structure and in water chemistry (redox potential, pH and salinity), with a clear
separation between ponds with fish and submerged macrophytes and other ponds. The more
intensively managed industrial salines held lower densities and biomass of invertebrates than
traditional salines, perhaps owing to greater protection from wind or inputs of detritus. The
beetle Ochthebius corrugatus was abundant in the traditional ponds but absent from the
industrial ones. The number of feeding waders using each pond was strongly correlated with
the total available biomass of invertebrates.
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
63
INTRODUCTION
Salt pans are widespread, artificial hypersaline habitats that are of great importance for
migratory waterbirds owing to the high productivity and predictability in time and space, as
well as their shallow depth (Britton & Johnson 1987, Warnock et al. 2002). In recent decades,
many salt pans have been abandoned or transformed into other uses, leading to the loss of
their waterbird and invertebrate populations. This has been accompanied by a tendency to
convert small saltpans managed with traditional methods to larger, intensive pans where
heavy machinery is used to extract salt (Sadoul et al. 1998, Consejería de Medio Ambiente
2004).
With the exception of the extensive literature on brine shrimps Artemia (Abatzopoulos
et al. 2002), there are few studies of the invertebrate community in salt pans on which
waterbirds depend. Only a handful of studies have described temporal and spatial fluctuations
in the invertebrate community in salt pans or attempted to identify determinants of
invertebrate abundance (Carpelan 1957, Britton & Johnson 1987, Williams 1998). None of
these studies have compared the effects of different management practices found within a
given saltpan complex.
The Odiel saltpans in south-west Spain hold internationally important numbers of
migratory waders (Sánchez et al. in press a). In this study we describe the seasonal changes in
abundance and distribution of different invertebrate taxa in the water column of saltpans of
different salinities during an annual cycle. We analyze the relationship between this variation
in abundance and variation in depth, wind effects and water chemistry. We compare the
abundance of invertebrate taxa between small, traditional saltpans and larger industrial ones.
We consider how fluctuations in time and space in the available invertebrate biomass affects
the abundance of migratory waders. Finally, we consider the implications of our findings for
management practices.
STUDY AREA
The Odiel marshes (37º17'N 06º55'W), located in the combined estuaries of the Tinto and
Odiel rivers, are tidal marshes with a total surface area of 7,185 ha. Salt pans occupy 1,185
ha, of which 1,118 ha are industrial salt pans and 56 ha are traditional salt pans (Figure 1). In
the industrial complex, sea water is pumped along a series of ponds and salinity increases via
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
64
evaporation until the final crystallizing pans are reached. Sea water first circulates through
eight primary evaporation ponds, followed by 11 secondary evaporation ponds and 12 pre-
crystallization ponds, ending up in 11crystallization ponds where the salt precipitates. Annual
production is 160,000 metric tonnes. A single harvest is extracted between early summer and
late autumn.
The traditional salt pans consist of a circuit of canals following a similar progression,
with approximately 30% of the surface area being dykes, 30% primary evaporation ponds,
30% secondary evaporation ponds and 10% crystallizers. Water circulates via gravity via
sluice gates. From three to five successive harvests are obtained between spring and early
autumn.
In primary evaporation ponds, the submerged macrophytes Ruppia cirrhosa and
Althenia filiformis are present, as well as Chaetomorpha and Enteromorpha algae. As salinity
increases, the biomass of primary producers becomes dominated by microalgae. At the
highest salinities, the chlorophyte Dunaliella salina is dominant.
METHODS
Invertebrate sampling
Samples were collected throughout 2001. Nine industrial ponds (I1-I9) were selected,
reflecting the whole salinity range (Fig. 1). Three traditional ponds (T1-T3) were selected
excluding the primary evaporation ponds which were too deep to be attractive to waders.
Every two months (in January, March, May, July, September and November), four points
were sampled per pond, filtering 20 l of water throughout a plankton net of 47 m. The exact
points varied each month and were selected at random from the depth range of 5-20 cm
accessible to waders (Ntiamoa-Baidu et al. 1998). Depth and hence the position of areas
sampled varied seasonally. At each point, we also took three sediment samples to study the
benthos (data presented in Sánchez et al. in press a). In each pond, we measured the salinity
(with a densometer), temperature, pH and redox potential in one point. At all four points we
measured the depth, distance to the nearest shoreline and fetch (upwind distance to shoreline,
according to the prevailing winds).
The samples were stored in 70% alcohol and the total sample volume was measured
by displacement as an estimate of biomass. The percentage of total volume that was made up
by each taxon was estimated visually. Usually a single species made up over 90% of the
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
65
sample. Taxa were identified to the lowest posible taxonomic level using various keys (Giusti
& Pezzoli 1980, Richoux 1982, Nieser et al. 1994, Arias & Drake 1997, Alonso 1998). Numbers
of each taxon were counted, and their individual volume was estimated based on linear
measurements of average sized individuals and using the volume for a simple geometric
figure. For example, the volume of chironomid larvae was estimated using the formula for a
cylinder. By multiplying this individual volume by the number of each taxon in a sample, we
obtained a second estimate of the total volume of each taxon. We used the average of our two
measures in our analyses.
We include all the invertebrates recorded in our samples in this study, including
terrestrial species owing to their potential value as prey items for waders. The copepod
Cletocamptus retrogressus and Chironomus salinarius larvae were abundant in the water
column, despite the fact that both species are principally benthic. We also included egg stages
such as Artemia cysts, which are important food items for waders (Sánchez et al. in press b).
Shorebird counts
In each of the study ponds we counted the number of shorebirds of each species that were
feeding and resting one day each week, using a 20-60x telescope. On each day, we carried out
a count of three hours duration around high tide when the densities of waders are highest
(Sánchez et al. in press b). The ponds were always counted at about the same time of day and
always following the same route between ponds.
Calculation of the available surface area
In most of the ponds, only shallow areas of 0-20 cm around the edge and around islands are
available to foraging shorebirds. The accessible surface area varies with fluctuations in the
overall water level, which were monitored by recorded depth at a reference point in each pond
at the time of invertebrate sampling. The depth profile of each pond was established by
conducting various transects, and the surface area accessible for foraging at the time of survey
was estimated via image analysis (Sigma Scanpro, version 4.0).
Statistical analysis
We used generalized linear models (GLMs) following GENMOD procedure in SAS (v. 8.2,
SAS Institute 2000) to analyze the spatial and temporal variation in the abundance and
estimated biomass (volume) of those invertebrate taxa present in more than 10% of samples.
These were Artemia parthenogenetica (diploid strain) and their cysts, Cletocamptus
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
66
retrogressus, other unidentified harpacticoid copepods, adults of the coleopteran Ochthebius
notabilis, Ochthebius spp. larvae, Chironomus salinarius larvae and unidentified planarians.
Owing to overdispersion observed in the data, we used a negative binomial error distribution
(Bliss & Fisher 1953, Kopocinski et al. 1998), log link function and type III tests to analyze
abundance. To analyze volume we could find no suitable transformation owing to the high
proportion of zeros. We thus only analysed non-zero data (log transformed), with an identity
link and normal error distribution.
Pond and month were included as fixed factors in all models. We also included depth,
distance to shoreline and fetch. While controlling for pond and month, there were significant
partial correlations between fetch and distance (r = 0.13, p = 0.017) and also between depth
and distance (r = 0.23, p < 0.001), but these r values are too low to cause problems of
multicollinearity (Graham 2003).
The deviance of each fitted GLM model is analogous to the residual sum of squares in
ordinary linear regression. The reduction in deviance compared to the null model is used to
assess the contribution of the model to the explanation of the variance in the data set. The
significance of the reduction in deviance for the models for abundance was estimated by
comparison with chi-square distribution, with degrees of freedom df equal to the change in df
compared to the null model. Significance for the models of volume was derived from F tests
(Crawley 1993). Post-hoc least-squares means tests (SAS Institute Inc., 1997) were used to
compare differences between pairs of traditional and industrial ponds with similar salinities
(two secondary evaporation ponds, two precrystallization ponds and two crystallization
ponds).
In order to test the relationship between different measures of abundance of waders
and of their invertebrate prey in different months or ponds, we calculated the Pearson
correlation coefficient (after confirming that both variables had a normal distribution, using a
Kolmogorov-Smirnov test). We related invertebrate abundance and available surface area on
the days of invertebrate sampling to the data from wader counts carried out on the nearest date
(1-2 days before or after sampling). Similarly, we calculated the correlation coefficient
between the salinity of different ponds and overall measures of invertebrate volume, species
richness and diversity (using the Shannon-Weiner index, Krebs 1989). In cases where
variables did not meet assumptions of normality, we present the Spearman non-parametric
correlation coefficient. In order to determine the partial effects of invertebrate volume and the
area accessible to waders in each pond on the number of waders, we used a multiple
regression with log transformed variables.
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
67
We used multivariate ordination methods and cluster analysis to assess the degree of
association between ponds in relation to their water chemistry, invertebrate community and
the interaction between the two. Principal Components Analysis (PCA) was used to plot
ponds against their chemistry data (log transformed). The affinities between ponds based on
the abundance of different invertebrate taxa were established using MDS (non-metric
multidimensional scaling) together with a cluster analysis using the UPGMA (unweighted
pair group method using arithmetic averages) method. The significance of the ordination in
the MDS) was tested using the Kruskal stress coefficient (Kruskal & Wish 1978).
We used a Canonical Correspondence Analysis (CCA) to explore the relationship
between water chemistry and the invertebrate community. The resulting ordination of the
ponds using this method is directly related to the values of the chemistry data (Ter Braak
1990). Data on the abundance of invertebrates was square root transformed and the Bray-
Curtis similarity index (Sánchez-Moyano et al. 2000) was used to establish the similarity
between ponds based on their invertebrate fauna. These multivariate methods were carried out
using the PRIMER (Plymouth Routines In Multivariate Ecological Analysis) programme
(Clarke & Gorley, 2001) and the PC-ORD programme (McCune & Mefford 1997).
RESULTS
We identified a total of 41 taxa including 30 aquatic metazoan invertebrates, one
foraminiferan, one fish and nine terrestrial invertebrates (Appendix 1). The most diverse
group were the insects with representatives of four orders and nine families (excluding
terrestrial species). The number of aquatic taxa recorded in each pond was negatively
correlated with average salinity (r = -0.78, p = 0.003, n = 12), and varied from four at pond I8
to 27 at pond I1. The Shannon-Weiner diversity index (based on total abundances of each
taxon) showed a significant negative correlation with the salinity of each pond (r = -0.65, p =
0.0217, n = 12) and varied between 0.002 (pond I8) and 1.693 (I2). Similarly, an alternative
diversity index based on the overall volume of each taxon showed a strong negative
correlation with salinity (r = -0.70, p = 0.01) and varied from 0.004 (pond I8) to 1.835 (I1). In
least saline ponds, the fauna included the exotic fish Fundulus heteroclitus and the Copepoda,
Gastropoda, Oligochaeta and Corixidae were abundant. Ponds of intermediate salinity were
dominated by Artemia, C. salinarius larvae and Ochthebius beetles (Fig. 2). In ponds of
highest salinity Artemia were dominant (Fig. 2). Artemia and C. salinarius larvae were the
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
68
only taxa recorded in all the ponds (Appendix 1). The number of aquatic taxa recorded in a
given month ranged from 19 in January to 26 in March.
Water chemistry varied between ponds (Table 1). Overall, salinity varied from 21 g/l
(pond I1 in November) to 231 g/l (T3 in May). Temperatures varied from 8 oC (November) to
37.5 oC (May), pH varied from 7.09 (May) to 9.49 (January) and redox potential from -8.46
(May) to 175.5 (January).
Analyses of abundance
The average annual abundance (number/l) of Artemia and C. salinarius larvae reached a
maximum in ponds of intermediate salinity (around 70-80 g/l, Fig. 2). The total abundance of
aquatic invertebrates (excluding eggs) peaked in March (767.7 ± 121.2 individuals/l, media ±
se) and reached a minimum in November (9.1 ± 1.3 individuals/l). The relative abundance of
the main taxa varied between months (Table 2). Artemia were numerically dominant in all
months except March, when 80% of individuals were Cletocamptus retrogressus (Table 2).
Overall, Artemia constituted 67.6% of the total number of aquatic invertebrates sampled
(excluding cysts).
There were significant differences between ponds and months in the abundance of all
major taxa (Table 3). Depth had a significant partial effect on C. salinarius larvae, Artemia
cysts and planarians, with abundance increasing at lower depths (Table 3). Distance to
shoreline showed a significant negative correlation with abundance of Artemia cysts,
Ochthebius larvae and O. notabilis adults (Table 3). Abundance of C. salinarius larvae and
Artemia cysts also showed a significant positive correlation with fetch (Table 3). Post-hoc
tests showed that, for all taxa, there were significant differences between at least one of the
three pairs of industrial and traditional ponds (Table 4). In 12 of 13 significant differences,
invertebrates were more abundant in traditional than in industrial ponds, the exception being
for unidentified harpacticoids (Table 4, Fig. 2).
Analyses of volume
There was a marked seasonal pattern in the volume of invertebrates in the water column, with
a maximum in September (0.10 ± 0.04 cm3 of invertebrates / l of water, mean ± s.e., n = 40)
and minimum in November (0.004 ± 0.0009, n = 40). The relative volume of the different
taxa varied between seasons (Table 2). Artemia always constituted over 70% of invertebrate
volume, except in november when corixids and chironomid larvae were particularly important
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
69
(Table 5). Overall, Artemia constituted 95.5% of the total volume of aquatic invertebrates
(excluding cysts).
Invertebrate volume was highest in high salinity ponds, with a maximum of 0.14 ±
0.01 cm3of invertebrates / l of water (mean ± s.e., n = 24) in I8 where 99.6 % was constituted
by Artemia. The lowest value (0.003 ± 0.0003) was recorded in low salinity I1 where only
0.7% were Artemia. There was a positive but non-significant correlation between average
invertebrate volume per sample and the salinity of each pond (r = 0.43 , n = 12, p = 0.16).
There were significant differences between both ponds and months in the volume of
Artemia, Cletocampus, C. salinarius larvae and planaria (Table 5). With the exception of
Ochthebius notabilis, there were significant differences between ponds for the volume of
other taxa analyzed (Table 5). Depth had a significant partial effect on volume for four taxa,
with a positive correlation for Artemia and a negative one for Cletocamptus, Ochthebius
larvae and C. salinarius larvae (Table 5). The volume of Artemia cysts showed a significant
negative correlation with depth to shoreline and positive one with fetch (Table 5). The volume
of C. salinarius larvae also showed a significant positive correlation with fetch. Post-hoc tests
showed that, for six taxa, there were significant differences between at least one of the three
pairs of industrial and traditional ponds (Table 4). In seven of eight significant differences, the
volume of invertebrates was greater in traditional than in industrial ponds, the exception being
for unidentified harpacticoids (Table 4).
Relationship between abundance of invertebrates and waders
The numbers of waders using the Odiel saltpans underwent a marked seasonal variation (Fig.
3=, with counts for the 12 study ponds at high tide peaking in september (9701 ± 1782, mean
± s.e., n = 4) with a minimum in march (2338 ± 547, n = 4). There was no significant
relationship between the total number of waders and the food abundance (estimated as mean
volume of invertebrates per litre in our samples, rs = 0.37, p = 0.50, n = 6). Likewise there
was no significant relationship with the number of feeding waders (rs = 0.09, p = 0.92) or
when considering the density of waders in the shallow 0-20 cm area available for feeding (rs
= 0.31, p = 0.56, n = 6).
In contrast, there was some evidence that birds distributed themselves between ponds
in relation to differences in the volume of prey present in the water column. There was a
strong relationship between the mean number of feeding waders in a given pond and the total
food available (estimated as the mean volume of invertebrates per sample multiplied by the
total area in the accessible depth range of 0-20 cm, rs = 0.71, p = 0.008, n = 12). However, it
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
70
is the combination of both differences between ponds in the available surface area and in the
mean food abundance that appears to cause this relationship. On their own, neither the
available surface area (rs = 0.52, p = 0.08, n = 12) nor food abundance (rs = 0.50, p = 0.09)
showed a significant correlation with the number of feeding waders in each pond. Similarly,
when these two variables were considered together as two predictors in a multiple regression
with the number of feeding birds as the dependent variable, each had a positive but non-
significant partial effect.
Ordination analyses
Water chemistry
The first axis of a PCA explained 50.6% of the total variance in chemistry data, and was
significantly positively correlated with salinity (r = 0.66, p < 0.025, n = 12) and negatively
correlated with pH (r = -0.52, p < 0.05, n = 12). The second axis explained 27.9% of the
variance and was positively correlated with temperature (r = 0.69, p < 0.01, n = 12) and redox
potential (r = 0.64, p < 0.025, n = 12). Thus PC1 ordered the ponds mainly in relation to the
salinity gradient and PC2 mainly in relation to temperature and redox potential.
Invertebrate community
The MDS analysis separated the ponds of lowest salinity from the others (Fig. 5). These three
ponds (T1, I1 and I2) had submerged macrophytes and fish and a distinctive invertebrate
fauna (see above). The ordination of ponds in space based on the invertebrate community is
consistent with the results of the PCA (Fig. 4), although in the PCA a gradient is observed
rather than a clear separation as seen in the MDS.
Relationship between water chemistry and the invertebrate community
The relationship between the invertebrate community and environmental variables is
described by the CCA (Fig. 6, Table 6). The first axis explained 43.4% of the variance and
was determined mainly by salinity, but also by pH. Thus the most saline ponds were grouped
on the positive side of the axis and the least saline ones on the negative side. The second axis,
which only explained 1.2% of the variance, was correlated with salinity and redox potential.
Taxa characteristic of more saline ponds were C. salinarius, Artemia and Ochthebius (see also
above). Invertebrates associated with the positive extreme of the second axis, such as the
oligochaetes, gastropods and amphipods dominated the ponds of high redox potential and low
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
71
pH, whereas the Berosus beetles, corixids and the dipteran Nemotelus were characteristic of
ponds with higher pH and lower redox potential (Fig. 6).
DISCUSSION
Ours is the most detailed study to date of spatio-temporal variation in the invertebrate
community in active saltworks of the Mediterranean region. We have recorded a marked
variation in the structure of the invertebrate community and in the abundance of different taxa
in space and time in the Odiel salt pans. As observed in saltpans in Mediterranean France
(Britton & Johnson 1987), we recorded a drop in species richness and diversity as salinity
increases between ponds. We observed a greater diversity of taxa than that recorded in
abandoned saltworks in which the spatial salinity gradient has been lost (Thiéry & Puente
2002). Most of the invertebrates we recorded in our study are important prey for waders
(Durell & Kelly 1990, Kalejta 1993, Pérez-Hurtado et al. 1997). Even the terrestrial
invertebrates we detected in our samples are consumed by waders in an opportunistic manner
(Sánchez et al. in press b).
We found salinity to be the most important chemical factor determining the structure
of the invertebrate community along a spatial gradient. The strong effect of salinity on
primary producers and invertebrates is well known (Hart et al. 1998, López-González et al.
1998, Tripp & Collazo 2003, Thiéry & Puente 2002). However, it is often unclear whether
the distribution of a given taxon is limited directly by salinity itself, or by its association with
other factors such as pH or the influence of salinity on other taxa (especially predators, prey
species or food plants, Williams 1998). Our ordination analyses suggest that the presence of
fish and submerged plants has a dramatic influence on invertebrate community structure.
Submerged macrophytes were only found in the ponds of lowest salinity, and this may be one
reason why the invertebrate community in these ponds was particularly diverse since these
plants have a profound effect on community structure and provide a substrate for many
macroinvertebrates (Wolfram et al. 1999, Weatherhead & James 2001).
Fish were also limited to the ponds of lowest salinity, and these predators also have
profound effects on invertebrate species composition and size distribution (Jeppesen et al.
1997, Hart et al. 1998, Zimmer et al. 2001, Marklund 2002). In Odiel, the fish together with
other predators (notably corixids and copepods) may be directly responsible for the absence
of Artemia from the ponds of lowest salinity (Williams 1998). The number of predatory taxa
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
72
was highest in these ponds, whereas the importance of detritivorous taxa such as C. salinarius
and Ochthebius was highest in ponds of intermediate salinity, in which Artemia were
dominant. In ponds of highest salinity, the food web was at its simplest and Artemia were
highly dominant amongst invertebrates. Despite the drop in species diversity and richness
with salinity, total biomass tended to increase. The relative importance of planktonic food
chains compared to benthic ones appears to increase at extreme salinities, as also suggested
by the negative correlation amongst ponds between salinity and densities of benthic
chironomid larvae (Sánchez et al. in press a).
Most of the taxa we recorded peaked in abundance in spring or summer, in contrast to
studies of benthic chironomids at Odiel and nearby Cádiz Bay, which suggest maximum
abundance in winter (Arias & Drake 1994, Sánchez et al. in press a). The seasonal
fluctuations in abundance of chironomid larvae in the water column observed in this study
were not synchronous with those recorded in benthic samples. Numbers and biomass in the
water column peaked in March and were at a minimum in January, whereas benthic density
peaked in May and was at a minimum in September. This may be a consequence of weather
conditions at the time of sampling. Strong winds and associated turbulence in these shallow
ponds are likely to release more larvae from sediments and make them available to birds
searching visually in the shallows. Our results suggest that a combination of sampling in
sediments and in the water column is essential to obtain a good measure of the availability of
chironomid prey to birds. Verkuil et al. (1993) previously suggested that the density of brine
shrimps in hypersaline lagoons in the Ukraine was strongly influenced by wind direction. We
found no evidence for that for Artemia adults, but a strong influence of fetch on the
abundance of their cysts and of chironomid larvae, both of which are important food items for
waders and other waterbirds (Green et al. 2002, Sánchez et al. in press b).
Verkuil et al. (1993) found that the density of Artemia increased with depth and
suggested that longer legged wader species were thus better able to exploit this food resource.
We also found that the biomass of Artemia increased with depth, supporting their suggestion.
In contrast, we found that the abundance and/or biomass of Artemia cysts, chironomid larvae,
Cletocamptus, Ochthebius and planarians is greatest at the shallowest depths over the 0-20 cm
range studied, suggesting that shorter legged birds may be better able to feed on these
resources. However, the chironomid larvae we have recorded in the water column are less
numerous than those remaining in the sediments, and benthic larval abundance increased with
depth in our ponds (authors, unpublished data).
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
73
The community structure and its relationship with the salinity gradient was generally
similar in the traditional and industrial salt pans. The most striking exception is the absence of
Ochthebius corrugatus in the industrial ponds, and its abundance in traditional ponds.
Invertebrate abundance was generally higher in the traditional ponds, and the reasons for this
are unclear. We could find no evidence for a difference in water chemistry between these two
complexes. The smaller pond size (Fig. 1) and greater relative surface area of dykes in
traditional ponds may be an important factor. The dykes provide greater protection from wind
and, unlike in industrial ponds, are covered in natural vegetation in traditional ponds
providing more detritus and potentially boosting productivity. Traditional ponds are used by
lower densities of feeding waders than industrial ponds (Sánchez et al. in press a). Thus,
reduced predation of invertebrates in traditional ponds may be another factor contributing to
our results. Most waterbirds tend to avoid smaller wetlands surrounded by steep banks
making it hard for them to detect predators from a distance (Green 1998). Although
traditional salt pans are not especially important for waders, they clearly provide a better
habitat for invertebrates as well as plants and some passerines.
Artemia are clearly the most important prey for waders in the water column of salt
pans at Odiel (Sánchez et al. in press b) and elsewhere (Masero & Pérez-Hurtado 2001). We
observed a crash in their abundance during winter months as expected, since many studies
have described the disappearance of adults at cold temperatures and their persistence as
resistant cysts (Amat et al. 1991, Wayne 2001, Thiéry & Puente 2002). In the Camargue,
waterbirds move into areas of lower salinity in winter to look for alternative prey when
Artemia populations in high salinity ponds have collapsed (Britton & Johnson 1987). In
Odiel, waders do not show such a switch to low salinity ponds in winter, although these ponds
do become important in winter for ducks and coot. Alternatively, waders may increase their
dependence on benthic chironomids or on marine prey such as polychaetes and bivalves from
tidal areas at this time (Masero et al. 2000, Sánchez et al. in press b).
We have used volumetric measures as an index of biomass of Artemia and other
invertebrates. However, for a given volume, Artemia are likely to have a lower energetic
value to waders than chironomid larvae and many other prey (Rubega & Inouye 1994,
Ludwing & Naegel 2002). Some wader species (notably Red-necked Phalaropes Phalaropus
lobatus and Broad-billed Sandpiper Limicola falcinellus) appear unable to retain their body
weight when fed exclusively on Artemia (Rubega & Inouye 1994, Verkuil et al. 2003). In
contrast, Artemia have been shown to be profitable prey for Dunlin Calidris alpina and
Curlew Sandpipers C. ferruginea (Verkuil et al. 2003). At Odiel, Black-tailed Godwit Limosa
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
74
limosa are major predators of Artemia. Of 42 droppings collected in August 2001, in 38
Artemia represented over 90% of sample volume (authors, unpublished data).
We have found no evidence that the seasonal changes in the numbers of waders at the
Odiel salt pans are related to changes in abundance and availability of invertebrates in the
water column. They are more likely to be related to other factors determining the timing of
migratory movements. In contrast, we have found evidence that the use of different ponds by
feeding birds is positively related to both the size of the shallow area of 0-20 cm where prey
are accessible, and to the density of prey in that area. Our failure to find stronger evidence is
probably related to the error in our measurements of abundance of such patchily distributed
invertebrate prey, to the importance of benthic prey considered elsewhere (Sánchez et al. in
press a) and to our collective analysis of different wader species varying in dietary
preferences. Use of different ponds is likely to be related to other factors such as pond shape
and size, levels of disturbance (Cayford 1993) and distance to alternative habitats (e.g. tidal
areas used for foraging at low tide, Masero et al. 2000, Luís et al. 2002). Waders may also
take into account the high osmoregulatory costs of feeding in the most saline ponds (Purdue
& Haines 1977, Wollheim & Lovvorn 1995) when making decisions about pond use. We
would need to study a much larger number of ponds to tease apart the importance of so many
different variables.
ACKNOWLEDGEMENTS
The first author was supported by a phd grant from the Ministerio de Ciencia y Tecnología
and an I3P postgraduate grant from the Consejo Superior de Investigaciones Científicas.
Consejería de Medio Ambiente, Junta de Andalucía and Aragonesas Industrias y Energía S.A.
provided permission to work in the salines. Juan Carlos Rubio, Director of the Odiel Marshes
Natural Park, provided logistical support and advice. José Manuel Guerra helped with
statistical analysis. Claudine de le Court, Jordi Figuerola, José Manuel Sayago and Enrique
Urbina also provided helpful advice. Francisco Amat, Dagmar Frisch and and Carmen Elisa
sainz helped to identify invertebrate taxa. Raquel Alejandre and Carlos Roldán helped with
field work.
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
75
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Table 1. Physico-chemical measurements from different ponds in the Odiel salt pans, showing
media ± se and the range (in parentheses). N = 6 for each pond with data taken from one point
every two months from January to November 2001.
Pond Salinity Temperature pH Redox potentialI1 25.12 ± 0.62 (21.19 - 29.28) 21.25 ± 1.56 (13 - 31) 8.41 ± 0.03 (8.20 - 8.64) 82.45 ± 2.46 (70.90 - 103.30)T1 44.10 ± 3.14 (27.00 - 67.54) 19.48 ± 1.13 (12.8 - 25) 8.61 ± 0.06 (8.27 - 9.01) 70.96 ± 3.47 (50.30 - 103.30)I2 44.64 ±1.23 (35.28 - 54.08) 19.17 ± 1.38 (11.5 - 29.5) 8.79 ± 0.04 (8.50 - 9.19) 61.82 ± 2.49 (53.10 - 84.30)I3 66.16 ± 2.82 (46.41 - 83.57) 20.5 ± 1.23 (15 - 31.5) 8.22 ± 0.03 (8.01 - 8.52) 79.70 ± 4.09 (51.60 - 113.50)I4 66.86 ± 2.76 (43.45 - 86.17) 22.67 ± 1.00 (17 - 31) 8.14 ± 0.10 (7.09 - 8.63) 85.83 ± 6.78 (47.10 -141.06)I5 71.22 ± 2.62 (54.82 - 86.92) 23.58 ± 1.25 (15 - 30) 8.26 ± 0.05 (8.01 - 8.66) 58.16 ± 2.80 (34.40 - 73.40)T2 80.46 ± 6.45 (47.06 - 113.50) 23.57 ± 2.24 (10 - 34.4) 8.38 ± 0.07 (7.97 - 8.94) 51.12 ± 6.00 (2.85 - 73.50)I6 86.01 ± 4.65 (58.65 - 118.93) 22.5 ± 1.28 (13 - 29.5) 8.26 ± 0.09 (7.69 - 8.78) 63.56 ± 4.46 (23.43 - 89.60)I7 90.27 ± 5.28 (58.88 - 125.26) 23.75 ± 1.87 (12 - 36) 8.35 ± 0.08 (7.80 - 8.89) 44.01 ± 2.06 (31.30 - 60.80)I8 103.79 ± 8.30 (44.18 - 148.19) 19.42 ± 0.94 (12 - 25.5) 8.57 ± 0.11 (8.02 - 9.49) 47.36 ± 3.15 (29.50 - 68.60)I9 117.72 ± 19.43 (37.43 - 221.28) 21.12 ± 1.46 (15.5 - 30) 8.00 ± 0.07 (7.50 - 8.21) 65.59 ± 17.96 (-8.46 - 175.5)T3 125.77 ± 22.86 (56.21 - 231.23) 20.17 ± 3.79 (8 - 37.5) 7.87 ± 0.12 (7.35 - 8.27) 38.13 ± 7.06 (17.70 - 70.90)
Table 2. Relative abundance (% of individuals or of sample volume) of the major invertebrate taxa recorded in the Odiel saltpans in 2001. L =
larvae. Cletocamptus = Cletocamptus retrogressus. Harpacticoida = unidentified harpacticoids (excluding Cletocamptus). Ochthebius L = larvae
of both O. notabilis and O. corrugatus. Total volume is given in ml.
Artemia Cysts Cletocamptus Harpacticoida O. notabilis Ochthebius L Chironomus L Planaria S. stagnalis Others Total ___________ ____________ ____________ ___________ ___________ ____________ ___________ ___________ ___________ __________ ____________month % ind % S vol % ind % S vol % ind % S vol % ind % S vol % ind % S vol % ind % S vol % ind % S vol % ind % S vol % ind % S vol % ind % S vol sum ind sum volJanuary 52.6 72.55 41.1 7.24 2.91 1.5 0 0 0.03 0.41 0.04 0.15 0.02 1.4 0 0 0 0 3.35 16.74 111333 5.16March 14.9 83.57 3.73 0.56 80.5 7.04 0 0 0 0.04 0.01 0.05 0.07 5.31 0 0 0 0 0.77 3.43 233502 12.73May 76.5 94.34 20.2 0.55 1.23 0.12 0.03 0 0.04 0.1 0.09 0.05 0.12 1.56 0.06 0.02 0 0.06 1.75 3.22 161210 48.75July 74.5 96.92 23.2 0.38 0.51 0.03 0.28 0.01 0.18 0.27 0.13 0.05 0.1 0.79 0.35 0.07 0.07 1.24 0.72 0.25 131550 65.4September 63.2 97.78 33 0.6 3.06 0.2 0.1 0 0.12 0.2 0.05 0.02 0.07 0.59 0.04 0.01 0.01 0.3 0.37 0.29 183737 82.06November 29 49.9 57.6 2.22 8.11 1.1 0.57 0.05 0.22 0.79 0.23 0.19 0.73 13.83 0.04 0.02 0.59 25.14 2.97 6.75 20625 4.37
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
82
Table 3. Results of generalized linear models analyzing effects of pond, month, depth,
distance to shoreline and fetch on the abundance (counts) of those aquatic invertebrates
recorded in more than 10% of samples. A negative binomial error distribution and log
link were used. D = percentage of deviance explained by the model in comparision with
the null model. k = aggregation parameter of the negative binomial distribution, where
the variance of the dependent variable y = µ+k*µ2, and µ is the mean of y. For the
estimates for each pond and month and other details of the models, see Appendix 2.
Effect DF Estimate Chi-Square PArtemia parthenogenetica Pond 11 218.58 < 0.0001N = 264 Month 5 81.78 < 0.0001D = 8.01 Depth 1 0.01 0.35 0.5514K = 1.27 Shore distance 1 -0.002 0.2 0.6575 Fetch 1 -0.0001 0.03 0.8527Artemia Cysts Pond 11 195.31 < 0.0001N = 264 Month 5 22.66 0.0004D = 9.81 Depth 1 -0.06 6.77 0.0093K = 1.30 Shore distance 1 -0.01 7.58 0.0059
Fetch 1 0.002 5.55 0.0184Cletocamptus retrogressus Pond 11 213.16 < 0.0001N = 264 Month 5 68.17 < 0.0001D = 10 Depth 1 -0.04 2.52 0.1124K = 1.03 Shore distance 1 -0.01 1.79 0.1814 Fetch 1 -0.0004 0.13 0.7149Other Harpacticoida Pond 11 64.24 < 0.0001N = 264 Month 5 46.56 < 0.0001D = 9.50 Depth 1 -0.1 3.12 0.0772K = 0.33 Shore distance 1 -0.01 0.08 0.7788
Fetch 1 -0.001 0.31 0.5763Ochthebius notabilis Pond 11 84.21 < 0.0001N = 264 Month 5 16.76 0.005D = 3.05 Depth 1 0.04 1.24 0.2661K = 0.51 Shore distance 1 -0.04 9.61 0.0019 Fetch 1 -0.003 3.79 0.0515Ochthebius spp. larva Pond 11 105.51 < 0.0001N = 264 Month 5 34.03 < 0.0001D = 2.50 Depth 1 -0.06 3.55 0.0637K = 0.63 Shore distance 1 -0.02 6.06 0.0138
Fetch 1 -0.001 0.27 0.6022Chironomus salinarius larva Pond 11 135.07 < 0.0001N = 264 Month 5 54.24 < 0.0001D = 0.04 Depth 1 -0.04 5.58 0.0182K = 0.97 Shore distance 1 -0.01 3.64 0.0565 Fetch 1 0.002 8.44 0.0037Planaria Pond 11 97.24 < 0.0001N = 264 Month 5 92.85 < 0.0001D = 5.06 Depth 1 -0.07 4.49 0.034K = 0.53 Shore distance 1 0.0001 0 0.9911 Fetch 1 0.0003 0.1 0.7548
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
83
Table 4. Summary of post-hoc tests of the differences between industrial (I2, I6, I9) and
traditional (T1, T2, T3) salt pans of comparable salinities, as calculated from
generalized linear models analyzing effects of pond, month, depth, distance to shoreline
and fetch. The estimate for the traditional pond was subtracted from that for the
industrial pond, and (-) indicates that numbers of biomass were greater in the traditional
pond. * p < 0.05, ** p < 0.01, *** p < 0.001
Abundance (counts) Biomass (volume) I2-T1 I6-T2 I9-T3 I2-T1 I6-T2 I9-T3Artemia parthenogenetica (-) * (-) (-) *** (-) (-) (-) **Artemia cysts (-) *** (+) (-) *** (-) *** (-) (-) **Cletocamptus retrogressus (-) *** (-) *** (-) *** (-) *** (-) *** (-)Other harpacticoida (+) ** (-) (-) (+) * ... ...Ochthebius notabilis (-) (-) ** (-) … (-) ...Ochthebius spp. larva (-) *** (-) (-) (-) (-) ...Chironomus salinarius larva (+) (-) ** (-) (-) (-) ** (-)Planaria (-) *** (-) ** (+) (-) ** (-) ...
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
84
Table 5. Results of generalized linear models analyzing effects of pond, month, depth, distance
to shoreline and fetch on the volume (ml/l biomass index) of aquatic invertebrates recorded in
more than 10% of samples. A normal error distribution and identity link were used. Zero values
were excluded from these analyses, owing to problems of model convergence. D = percentage
of deviance explained by the model in comparision with the null model. DFn = DF for
numerator, DFd = DF for denominator. For the estimates for each pond and month and other
details of the models, see Appendix 3.
Effect DFn DFd Estimate F PArtemia parthenogenetica Pond 11 196 15.54 < 0.0001N = 216 Month 5 196 32.55 < 0.0001D = 64.05 Depth 1 196 0.03 8.5 0.0036
Shore distance 1 196 -0.002 1.46 0.2262 Fetch 1 196 -0.0002 0.34 0.5606Artemia Cysts Pond 11 223 14.83 < 0.0001N = 243 Month 5 223 1.98 0.0776D = 47.19 Depth 1 223 -0.01 0.66 0.4169
Shore distance 1 223 -0.004 4.11 0.0425Fetch 1 223 0.001 3.92 0.0479
Cletocamptus retrogressus Pond 10 139 11.73 < 0.0001N = 158 Month 5 139 6.48 < 0.0001D = 55.75 Depth 1 139 -0.03 6.23 0.0126
Shore distance 1 139 -0.0001 1.76 0.1846 Fetch 1 139 0.6308 0.07 0.7887Other Harpacticoida Pond 7 27 2.88 0.0052N = 41 Month 3 27 0.65 0.5831D = 51.48 Depth 1 27 -0.003 0.1 0.7544
Shore distance 1 27 -0.001 0.03 0.8601Fetch 1 27 0.4751 1.17 0.2785
Ochthebius notabilis Pond 8 43 1.1 0.358N = 60 Month 5 43 1.64 0.1464D = 48.37 Depth 1 43 0.01 0.15 0.6966
Shore distance 1 43 -0.01 0.36 0.5486 Fetch 1 43 -0.0003 0.09 0.7648Ochthebius spp. larva Pond 10 57 2.45 0.0063N = 76 Month 5 57 1.29 0.2653D = 58.10 Depth 1 57 -0.03 11.62 0.0007
Shore distance 1 57 0.005 2.37 0.1238Fetch 1 57 -0.0002 0.33 0.5674
Chironomus salinarius larva Pond 11 111 5.62 < 0.0001N = 131 Month 5 111 3.02 0.0099D = 44.94 Depth 1 111 -0.02 10.51 0.0012
Shore distance 1 111 -0.001 1.01 0.3147 Fetch 1 111 0.001 11.01 0.0009Planaria Pond 8 49 2.62 0.0072N = 65 Month 4 49 4.34 0.0016D = 45.07 Depth 1 49 -0.02 2.41 0.1203
Shore distance 1 49 -0.001 0.15 0.6976 Fetch 1 49 0.0004 0.76 0.3845
Table 6. Results of a Canonical Correspondence Analysis (CCA) between measures of
invertebrate abundance and water chemistry. See text for details.
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
85
* p < 0.05, ** p < 0.01, *** p < 0.001
Axis 1 Axis 2
Species-environment correlation 0.95 0.18
Percentage of species variance 43.4 1.2
Correlation with environmental variables
Salinity 0.82*** -0.52*
Temperature 0.5 0.41
pH -0.75** -0.28
Redox -0.28 0.53*
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
86
Figure 1. Location of the Odiel salt pans and of the ponds included in the present study
(industrial ponds I1-I9 and traditional ponds T1-T3) . Arrows indicate the circulation
routes for water between input from the sea and salt precipitation.
Spain
I1
OdielRiver
0 1000 m
I2
I7
I4
I5
I6
I9
T3T1IndustrialTraditional
Road
Water circulation
I3T2I8
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
87
Figure 2. Abundance of the major invertebrate taxa (numbers per litre, mean ± s.e.) in
different ponds in relation to their salinity. Mean salinity in each pond increases from
left to right.
Cletocamptus retrogressus
0
300
400
500
600
700
0
20
40
60
80
100
120
140
160
Other Harpacticoida
Artemiaparthenogenetica
0
100
200
300
400
0.0
0.4
0.6
0.8
1.0
1.2
1.4 Ochthebiusnotabilis
0.0
0.2
0.4
0.6
0.8
Ochthebius spp. larvae
0.0
0.1
0.2
0.3
0.4
0.5
Chironomus salinaris larvae
0.0
0.2
0.4
0.6
0.8
Planaria
I1 T1 I2 I3 I4 I5 T2 I6 I7 I8 I9 T30.0
0.20.8
1.0
1.2
1.4Total invertebrates
I1 T1 I2 I3 I4 I5 T2 I6 I7 I8 I9 T30
100
200
300
400
Industrial pondTraditional pondSalinity
Inve
rtebr
ate
abun
danc
e (li
tres
-1, m
ean
± s.
e.)
Salin
ity (g
/l)
0.15
15
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
88
Figure 3. Seasonal changes in the abundance of waders in our 12 study ponds, in the
mean volume of invertebrates available in the same area (cm3 of invertebrates per l of
water), and in mean salinity. Wader densities were calculated from the high tide count
made closest to the date of invertebrate sampling.
months
Ja Ma My Jl Se No
avai
labl
e in
verte
brat
e vo
lum
e (c
m3/
l)
0.00
0.02
0.04
0.06
0.08
0.10
0.12
Nº o
f sho
rebi
rds
0
2000
4000
6000
8000
10000
12000
14000
16000
18000
salin
ity (g
/l)
40
50
60
70
80
90
100
110invertebratesshorebirdssalinity
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
89
Figure 4. Principal Components Analysis of the physico-chemical data from each pond.
Solid circles represent ponds without fish or macrophytes; open squares represent ponds
with fish and submerged macrophytes.
-2,0 -1,0 0 1,0 2,0
Axis 1
-2,0
-1,0
0
1,0
2,0
Axis 2I9
T3
I1
I4
I5I3 I6
I7
I2
T1
I8
T2
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
90
Figure 5. Cluster analysis (UPGMA method) and MDS ordination of the ponds
according to the abundance of different invertebrate taxa. Solid circles represent ponds
without fish or macrophytes; open squares represent ponds with fish and submerged
macrophytes.
100
80
60
40
20
Similarity (%)
I1 I2 T1 I9 T3 I5 T2 I3 I8 I4 I6 I7
I9
T3
I1
I4
I5I3 I6
I7I2
T1
I8
T2
Stress: 0,01
CHAPTER 3 AQUATIC INVERTEBRATE COMMUNITY IN THE ODIEL SALT PANS
91
Figure 6. Graphical representation of the ponds, invertebrate taxa and environmental
variables with respect to the first two axes of a Canonical Correspondence Analysis
(CCA). Solid circles represent ponds without fish or macrophytes; open squares
represent ponds with fish and submerged macrophytes. Taxa associated with the upper
part of axis 2 are those associated with high redox potential and low pH (see text). L =
larvae, P = Pupae.
I9
T
I1
I4
I5I3
I6I7I2
T1
I8
T2
Artemia parthenogenetica
Cletocamptus retrogressus
Calanoida
Harpacticoida
Ochthebius notabilisOchthebius corrugatus
Chironomus salinarius L
Chironomus salinarius P
Halocladius spp. L
Collembola
Dolychopodidae L
Sirphydae L
Decapoda
Ostracoda
Amphipoda
Fish
NematodaHydrobia ulvae
Hydrobia ulvae L
Paracymus aenus
Ephydra spp. L
Ephydra spp. P
PlanariaDytiscidae L
Bryozoa
Sigara stagnalis
Foraminiphera
Hydrophyllus spp. L
Berosus spinosus
Oligochaeta
Nemotelus spp. L salinity
temperature
ph
redox
Axis 1
Axis 2
Ochthebius spp. L
92
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
93
CHAPTER 4
SHOREBIRD PREDATION AFFECTS ABUNDANCE AND SIZE
DISTRIBUTION OF BENTHIC CHIRONOMIDS IN SALTPANS: AN
EXCLOSURE EXPERIMENT
MARTA I. SÁNCHEZ1, ANDY J. GREEN1 AND RAQUEL ALEJANDRE
1Departamento de Biología Aplicada, Estación Biológica de Doñana, Avenida de María Luisa s/n,
Pabellón del Perú, 41013 Sevilla, Spain
Key words: shorebirds, predation, exclosures, Chironomus salinarius, size distribution,
saltpans, Odiel marshes, top down regulation
Running head: Effect of shorebird predation on Chironomids
Journal of North American Benthological Society 25(1): 9-18.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
94
ABSTRACT
Chironomus salinarius larvae are the dominant benthic organisms in the saltpans of the
Odiel marshes, south-west Spain, an area internationally important for migratory
shorebirds. Using predator exclosures, we examined the effects of shorebirds on
chironomid larvae during spring migration. During the first experimental period from 12
February to 26 March 2002, wader densities were relatively low, peaking at 4 feeding
birds ha-1. During the second period from 19 March to 3 May, densities were higher,
peaking at 32 feeding birds ha-1. Owing to predation by shorebirds, the change in larval
density and biomass from the beginning to the end of each period was significantly
higher in exclosures than in controls. Predation decreased larval density by 35 % during
period 1 and 32 % during period 2, and decreased biomass by 37 % during period 1 and
49 % during period 2. Predation also changed prey size distribution, reducing the
proportion of larger larvae. These effects did not vary significantly between periods,
suggesting that increased predation in period 2 was compensated by higher larval
growth or recruitment. Variation in exclosure effects was not related to variation in the
initial larval density or biomass in a given patch. Predator-prey interactions are complex
in saltpans, with evidence of simultaneous top-down and bottom-up regulation.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
95
INTRODUCTION
It is generally recognised that predation plays a fundamental role in the structuring of
benthic invertebrate communities (Thrush 1999). Chironomidae larvae are extremely
abundant or dominant in the benthos in a variety of aquatic ecosystems, and their
abundance and size distribution is often regulated by insect or fish predators (Armitage
et al. 1995, Kornijów 1997, Batzer 1998). Benthic midge larvae are also major prey for
a variety of waterbirds (Krapu & Reinecke 1992, Rehfisch 1994), yet there is very little
information on the influence that avian predators have on chironomid communities
(Armitage et al. 1995). Only one study has shown an influence of avian predation on
larval abundance (Székely & Bamberger 1992), and no study has shown an influence on
larval size.
Hypersaline systems such as saltpans have relatively simple food webs (Britton
& Johnson 1987), making them ideal for studies of predator-prey interactions. More
than 20,000 shorebirds use saltpans within the Odiel Marshes in south-west Spain
during migration. Chironomid larvae dominate the benthos and are a major prey of
shorebirds (Sánchez et al. in press a, in press b). Shorebirds are episodic predators likely
to have major effects on invertebrate prey owing to their high foraging intake and
energy demand and their formation of large concentrations at stopover and wintering
sites (Wilson 1991, Masero & Pérez-Hurtado 2001, Kvist & Lindström 2003),
especially during migration when they may double their body mass in 20 days (Hicklin
& Smith 1984). They have been shown to reduce benthic prey abundance (Weber &
Haig 1997, Sutherland et al. 2000) and influence prey size (Botto et al. 1998) in
intertidal ecosystems. However, as far as we are aware, their effect on prey abundance
or size in saltpans has not previously been studied.
In this study we investigate the impact of predation by shorebirds on the
population of benthic chironomids in the Odiel saltpans. Using exclosure experiments,
we compare the effects of shorebirds on the density, biomass and size of larvae at two
different bird densities at the beginning and peak of spring migration. We test the
hypotheses that exclosure effects are more pronounced at the time of higher bird
density, and in patches with higher prey density.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
96
STUDY SITE
The study was carried out in spring 2002 within the 1,185 ha of saltpans in the Odiel
Marshes (37º17'N 06º55'W) at the mouths of the rivers Odiel and Tinto. The Odiel
Marshes in south-west Spain are protected as a Natural Park by the regional government
and as a UNESCO Biosphere Reserve, wetland of international importance under the
Ramsar Convention and Specially Protected Area of the European Union (Bernués
1998). The saltpans support internationally important numbers of Black-winged stilt
Himantopus himantopus, Kentish plover Charadrius alexandrinus, Avocet
Recurvirostra avosetta, Ringed plover Charadrius hiaticula, Black-tailed godwit
Limosa limosa and Dunlin Calidris alpina (Sánchez et al., in press a).
The saltpans include a gradient of salinity in relation to salt production, and this
study was conducted in the secondary evaporation ponds that provide good access and
high abundance of chironomids to shorebirds (see Sánchez et al. in press a for details).
Chironomus salinarius Kieffer was the only chironomid species recorded in the
benthos. This is a multivoltine species estimated to have an average of five generations
a year in another coastal system 100 km away in south-west Spain (Drake & Arias
1995). C. salinarius is a widespread species complex requiring further taxonomic study
(Armitage et al. 1995). There were no fish, crabs or shrimps, and shorebirds were the
only abundant predators in the area studied. Flamingos and other waterbirds did not use
the areas selected for exclosures during the experiment. None of the other invertebrates
recorded in the wetlands are known to predate on C. salinarius larvae (authors,
unpublished data).
METHODS
Exclosure experiments were conducted over two different periods. The first (period 1)
coincided with the beginning of spring migration (Fig. 1) when exclosures were in place
from 32 to 38 days between 12/02/02 and 26/03/02. Period 2 included the peak of
migration (Fig. 1) when exclosures were in place from 37 to 46 days between 19/03/02
and 03/05/02. These dates were selected on the basis of regular censuses of shorebirds
during the same months in 2001.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
97
Exclosures
In each period, we installed 20 exclosures paired together with 20 controls. Iron poles of
5 mm diameter were used to mark out squares of 1 x 1 m for both exclosures and
controls. Exclosures included 15 mm PVC mesh netting spread over across a PVC
square frame placed on top of polystyrene floats. These floats were threaded onto the
iron poles so that the net could move up or down but was always suspended about 5 cm
above the water level. Thus, exclosures were not affected by changes in water level
associated with rainfall and management for salt production. Neither did the net touch
the water surface or affect water movement. We deliberately did not place netting
around the sides of the square to avoid influencing water velocity or sedimentation
(Sutherland et al. 2000). There was no algal growth and shading effects were close to
zero.
Five pairs of controls and exclosures were established in each of four ponds,
placing them always in the 0-20 cm water depth range used by feeding shorebirds. Pairs
were separated from each other by 20-30 m. Within each pair, the control and exclosure
were placed at the same water depth, separated by 5 m. The two structures varied
slightly in their relative position to the pond edge, but the decision as to which went
where was taken at random.
Invertebrate sampling
At the beginning and end of each period, three samples of benthos were taken at random
from within each exclosure and control, using a corer of 5 cm diameter to sample the
top 3 cm of soft sediments overlying an impenetrable clay bed. Sampling at the
beginning and end of each period was carried out in different halves (chosen at random)
of the 1 x 1 m plot to avoid resampling disturbed sediments. Each sample was washed
in sieves of 0.5 mm and 0.1 mm within 24 h of collection. Invertebrates were then
separated from remaining sediments by flotation in saturated brine collected from
crystallisation ponds. They were counted and stored in 70 % alcohol.
At the end of period 1, exclosures and controls were moved to new positions 2 m
away. Slight overlap between the two periods (Fig. 1) is due to the delay between
sampling and moving the exclosures and controls in the first pond and doing the same in
the last pond. In a given pond, all the exclosures and controls were established and/or
sampled on the same day. Owing to the time required to extract invertebrates from the
samples en vivo in the laboratory, it was not possible to sample all the ponds together.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
98
We removed two of the exclosure-control pairs from analyses for period 2 because they
dried out due to a drop in water level.
Chironomid larvae retained on the 0.5 mm sieve were later measured to the
nearest 10 m using an image analyzer. Body length data were transformed into
estimated dry mass using the regression equation of Smock (1980). We did not estimate
dry mass of the smaller larvae retained on the 0.1 mm sieve as it was relatively
insignificant. In order to demonstrate this, we compared the actual (not estimated) dry
weight of larvae retained on different sieves in 24 samples taken at different times and
in different periods.
Censuses of shorebirds
We carried out monthly censuses of the study area of 123 ha from January to May 2002,
recording the total number of individuals and the number feeding for each shorebird
species. Censuses were carried out at high tide when tidal flats are unavailable as
alternative foraging habitat and wader densities in the saltpans are highest (Sánchez et
al., in press a).
Statistical analysis
Data from the three benthic samples taken within each exclosure or control were pooled
before analysis. We used Generalized mixed Linear Models (GLMs, McCullagh &
Nelder 1989) to analyze the effects of treatment (exclosure or control) and experimental
period on the abundance, estimated biomass and size distribution of chironomid larvae.
Pond and exclosure-control pairs nested within ponds were included as random factors,
using the GLIMMIX macro (SAS Institute 1996). For abundance and biomass we used
an identity link and normal error distribution, transforming the dependent variable to
overcome heteroscedasticity. We analyzed the change in density of larvae (number
counted in the three samples) from the beginning to the end of an exclusion period as
log10 (final number + 1) - log10 (initial number + 1)) and the change in estimated
biomass (mg in the three samples) in the same way. For size distribution we conducted a
logistic regression using the number of larvae retained on the 0.5 mm sieve (numerator)
and the total number retained on the 0.5 mm and 0.1 mm sieves (denominator) as the
dependent variable (Crawley 1993). We used data from the samples collected at the end
of each exclusion period, with a logit link and binomial error distribution. We also
analyzed the effect of treatment and period on the mean size of larvae retained on the
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
99
0.5 mm sieve at the end of each period, using an identity link and normal error
distribution.
Tests on the effects of each predictor were performed using F-statistics. The
deviance of each fitted GLM is analogous to the residual sum of squares in ordinary
linear regression. The reduction in deviance compared to the null model is used to
assess the explicative power of the model (Crawley 1993). We initially considered the
water depth at each exclosure-control pair as an additional predictor (results not shown).
However, we found no evidence of a depth*treatment interaction as would be expected
if predation effects varied with depth. Period*treatment interactions were not significant
and were excluded from final models.
We used similar GLMs to test whether the exclosure effect in a given patch
depended on the abundance or biomass of larvae in that patch at the beginning of an
experiment. We used the difference between the abundance in an exclosure and its
paired control at the end of a period as the dependent variable (transformed as log10
([final exclosure + 1] / [final control + 1])), and the average abundance for each pair at
the beginning of a period as a predictor. Period was a fixed factor and pond was a
random factor. We used an identity link and a normal error distribution. We repeated
this analysis using biomass data instead of abundance. The interactions between initial
abundance or biomass and period were not significant.
We used matched-paired t tests to analyze the change in the abundance and
biomass of larvae in controls between the beginning and end of each period.
RESULTS
In period 1, C. salinarius larvae and small numbers of C. salinarius pupae were the only
invertebrates recorded (Table 1). In period 2, small numbers of Ochthebius beetles were
also recorded (Table 1).
Density of larvae
At the beginning of each experiment, there was no difference between controls and
exclosures in the density of larvae (Fig. 2). At the end of period 1, 35.0 % more
chironomid larvae were found in exclosures than in controls (Fig. 2a). At the end of
period 2, 32.2 % more larvae were found in exclosures. However, in spite of these
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
100
predation effects, the density of larvae increased in controls throughout the study (Fig.
2a). This increase was not significant between the beginning and end of period 1 (t = -
0.95, p = 0.35), but was highly significant between the beginning and end of period 2 (t
= -3.69, p = 0.002).
We found a significant increase in larval density in exclosures compared to
controls (Table 2). There was a significant effect of period on the change in density over
time, which was greater in period 2 (Table 2). The period*treatment interaction was not
significant (F1,48 = 0.78, P = 0.38).
Biomass of larvae
The dry mass of small larvae retained on the 0.1 mm sieve was relatively unimportant,
representing only 3.8 ± 1.8% (mean ± s.e., n = 24) of total mass from the 0.1 mm and
0.5 sieves combined. At the beginning of each experiment, there was no difference
between controls and exclosures in the estimated biomass of larger larvae retained on
the 0.5 mm sieve (Fig. 2). At the end of period 1, the estimated biomass was 36.7 %
higher in exclosures than in controls (Fig. 2b). At the end of period 2, biomass was 48.9
% higher in exclosures. In controls, biomass decreased significantly during the course of
period 1 (t = 2.37, p = 0.028) but underwent a non-significant increase during period 2 (t
= -2.00, p = 0.062; Fig. 2b).
We found a highly significant increase in larval biomass in exclosures compared
to controls (Table 2). There was a significant effect of period on the change in biomass
over time, which was greater in period 2 (Table 2). The period*treatment interaction
was not significant (F1,48 = 0.03, P = 0.86).
Size distribution of larvae
The larvae retained on the 0.5 mm sieve showed a bimodal size distribution
indicating the presence of third and fourth (final) instars (Fig. 3). Although mean larval
size in exclosures was slightly larger than in controls, this difference was not significant
(using data from the end of periods 1 and 2, F1,48 = 2.12, P = 0.15). Mean size was
significantly larger at the end of period 1 than period 2 (F1,48 = 51.96, P < 0.0001). The
period*treatment interaction for mean size was not significant (F1,47 = 0.27, P = 0.6).
At the end of period 1, the proportion of larvae retained on the 0.5 mm sieve was
43.9 ± 5.5 % (mean ± s.e.) for controls and 52.1 ± 5.6 % for exclosures. At the end of
period 2, the proportion was 47.8 ± 6.1 % for controls and 50.8 ± 5.8 % for exclosures.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
101
The fraction of larvae retained on the 0.5 mm sieve was significantly higher in
exclosures than in controls, but did not differ significantly between periods (Table 2).
The period*treatment interaction was not significant (F1,48 = 0.82, P = 0.37).
Effect of initial larval abundance on predation effects
While controlling for period and pond, we found no effect of initial larval density on the
difference between exclosures and controls at the end of experimental periods (r = -
0.02, F1,31 = 0.03, p=0.85). Similarly, we found no significant effect of initial larval
biomass on the difference between exclosures and controls at the end of experimental
periods (r = -0.19, F1,31 = 1.30, p=0.26).
Shorebirds numbers
During period 1, numbers of migrating shorebirds in the study area were relatively low
with a maximum count of 3116, of which 13.9 % were feeding. Numbers increased
during period 2 to a maximum of 4835, of which a much higher 80.7 % were feeding
(Fig. 1, Table 3). There was also a shift in the composition of the wader community. In
total, 18 species were recorded, all of which were feeding in the saltpans and 12 of
which were observed feeding inside our controls (Table 3). Redshank, Avocets, Black-
tailed godwits were relatively abundant during period 1, whereas Curlew sandpipers
Calidris ferruginea and Dunlins were dominant during period 2 (Table 3). Of 3904
birds recorded feeding at the end of period 2 (30 April), 53 % were Curlew sandpipers
and 43 % Dunlin.
DISCUSSION
We have recorded strong effects of predator exclosure on the density, size distribution
and especially biomass of chironomid larvae,. We observed no effects of our exclosures
on the environment and, in the absence of other predators, our results can only be
explained by predation by shorebirds. Our experiments may have underestimated the
effects of shorebirds because there may have been a net emigration of mobile benthic
chironomid larvae away from our small exclosures where densities were elevated
(Wilson 1989).
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
102
Other authors have shown that shorebirds have high intake rates and have
suggested that they are likely to consume a significant fraction of the production of
benthic chironomid larvae (Rehfisch 1994, Masero & Pérez-Hurtado 2001).
Nevertheless, without exclosure experiments such as ours it is not apparent that such
predation leads to a reduction in the density or standing crop of larvae, since loss via
predation may potentially be compensated for by other effects. In particular, reduced
interspecific competition leading to lower mortality rates or higher growth rates in
midge larvae (Armitage et al. 1995). Indeed, experiments excluding shorebirds or other
avian predators have not always produced detectable effects on chironomids (Smith et
al. 1986, Ashley et al. 2000) or other benthic invertebrates (Raffaelli & Milne 1987,
Wilson 1991, Lopes et al. 2000). As far as we know, the only other study in which
avian predation has been shown to reduce the density of midge larvae is one from an
inland oxbow lake (Székely & Bamberger 1992).
Given our absence of data on chironomid productivity and on feedback
processes, our results from the exclosure experiments can not be translated into a
precise estimate of the proportion of production or standing crop consumed by
shorebirds (Mitchell & Wass 1996). Nevertheless, they demonstrate a top-down control
of chironomids by shorebirds and indicate that shorebirds have an important influence
on chironomid dynamics in this system, at least during spring migration.
The highly significant effect of wader predation on larval biomass was due to a
significant decrease both in larval abundance and in the proportion of large larvae.
Shorebirds appear to have selected larger larvae retained on a 0.5 mm sieve (mean
length ± s.e. = 8.09 ± 0.04 mm, range = 1.55-16.78 mm) at the expense of smaller ones
retained on a 0.1 mm sieve (mainly first and second instars). As far as we are aware, this
is the first evidence of size selection of chironomid larvae by shorebirds, and the first
direct evidence that avian predation changes the size distribution of chironomid prey.
Size selection of invertebrates by shorebirds is well documented (Goss-Custard 1977,
Worral 1984, Dierschke et al. 1999), but in the only other study in which it led to a
measurable change in the size distribution of prey the mean size of polychaetes was
increased by wader predation (Botto et al. 1998). In other studies, size selection by
shorebirds did not influence the size distribution of their prey (Weber & Haig 1997).
Thus, whilst we found no significant evidence that wader predation affects the size
range of those chironomid larvae retained on a 0.5 mm sieve, prey size selection might
still occur in this range.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
103
Some authors have attributed size selection of benthic invertebrates by
vertebrate predators to the vertical stratification of sizes within the sediments,
suggesting that smaller polychaetes or chironomids were selected because they were
closer to the surface (Hershey 1985, Botto et al. 1998). We doubt that larger larvae were
selected in our study because they were more accessible. We only sampled 3 cm of
sediments, all of which were accessible to most of the wader species. The smallest first
instars are likely to be particularly close to the surface since they are the principal stage
for dispersal through the water column (Armitage et al. 1995). On the other hand,
Redshank at Odiel consume more chironomid pupae than expected from their low
density in the benthos, presumably because they become particularly accessible when
preparing for emergence (Sánchez et al. in press b).
We found no evidence that the impact of wader predation was related to water
column depth over the 0-20 cm range studied, perhaps owing to the range of wader
species present and their partitioning between different depths (Ntiamoa-Baidu et al.
1998). Neither did we find that exclosure effects were related to initial biomass or
density. This suggests that shorebirds did not concentrate larval predation in patches
where prey abundance was highest. Different wader species may respond differently to
variation in depth or larval size when foraging optimally, and perhaps the pooling of
their effects means that there is no optimal foraging response detectable at a community
level. At the higher scale of pond selection, shorebirds do select those saltpans
providing higher densities of larvae (Sánchez et al. in press a).
Although the density of foraging shorebirds was much higher in period 2 than in
period 1, this was not reflected in significant differences between periods in the
observed exclosure effects. Thus, detectable predation effects were not greater as
predator density increased (contrary to Botto et al. 1998) and even relatively low
densities of shorebirds produce detectable effects. Indeed, in areas exposed to predation
the biomass decreased significantly during period 1 but increased during period 2.
Higher predation rates in period 2 may have been compensated for by higher larval
recruitment or productivity. Both may have increased between early February and late
April in association with increased water temperature (Drake & Arias 1995). Our results
show that the effects that predation has on benthic prey populations does not only
depend on the intensity of predation, but also on its timing in relation to prey life cycles.
A relatively small amount of consumption at a moment of low recruitment or growth
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
104
may have more consequences for prey populations than much greater consumption at a
time of peak productivity (Mitchell & Wass 1996).
Our results indicate that the availability of chironomid prey to a migratory wader
depends on the absolute time of its arrival, since there is significant variation in larval
abundance with date. Furthermore, it also depends on the number of other individuals
arriving beforehand, since earlier predation reduces prey availability at a given moment.
The foraging intake rates of shorebirds have previously been shown to decrease as the
density of benthic midge larvae decreases (Székely & Bamberger 1992). Thus,
decisions that shorebirds take about when to migrate may be influenced by prey
depletion at stopover sites such as we have recorded in the Odiel saltpans (Schneider &
Harrington 1981). These changes in prey density and intake rates may also influence the
time birds need to spend at stopover sites such as Odiel marshes to reach the body
condition required to continue on to breeding sites. Any delay in arrival at breeding sites
is likely to reduce breeding success (Sandercock et al. 1999). Since all wader species in
our study site feed on chironomid larvae (pers. obs.) and most were seen feeding inside
our experimental controls (Table 3), our results can not be attributed to a single predator
species and suggest that interspecific competition may be an important process in this
system.
Elsewhere we present evidence that changes in the abundance of C. salinarius in
Odiel saltpans during the course of the annual cycle partly determines the numbers of
shorebirds feeding in saltpans instead of alternative intertidal habitats (Sánchez et al. in
press a). Differences in density of midge larvae also explain differences in wader
density between individual ponds (Sánchez et al. in press a). Similarly, changes in the
importance of C. salinarius in wader diet is related to fluctuations in their abundance
(Sánchez et al. in press b). Thus, a localized predator-prey relationship appears to exist
at Odiel in which both bottom-up control and top-down control are important in the
regulation and structuring of predator and prey populations in saltpans. In a given pond,
the abundance of midge larvae undergoes top-down control by shorebirds, but also
exerts a bottom-up control on the abundance of shorebirds.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
105
ACKNOWLEDGEMENTS
The first author was supported by a phd grant from the Ministerio de Ciencia y
Tecnología and a postgraduate grant from the Consejo superior de Investigaciones
Científicas. Consejería de Medio Ambiente, Junta de Andalucía and Aragonesas
Industrias y Energía S.A. provided permission to work in the salines. J.C. Rubio,
Director of the Odiel Marshes Natural Park, provided logistical support
and advice. E. Castellanos, C. de le Court, J.M. Sayago and E. Urbina also provided
helpful advice. J.A. Amat, J. Figuerola and J.A. Masero helped us to improve an earlier
version of this manuscript.
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110
Table 1. Invertebrates recorded in benthic samples, their percentage of occurrence (PO,
i.e. the proportion of samples in which they were recorded) and the percentage of total
individuals (PI) that they represented.
Period I (n = 240) Period II (n = 216) PO (%) PI (%) PO (%) PI (%)C. Salinarius larvae 100 98.3 100 99C. Salinarius pupae 19.2 1.7 21.3 0.92Ochthebius spp. 0 0 0.9 0.026
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
111
Table 2. Summary of Generalized Linear Models testing the partial effects of treatment
(exclosure or control) and period on the density, biomass and size distribution of C.
salinarius larvae recorded in experimental plots (n = 76). Density is the change in total
numbers of larvae recorded in each 1 m2 plot from the beginning to the end of the
experiment. Biomass is the change in estimated dry mass of larvae retained on a 0.5 mm
sieve from the beginning to the end of the experiment. Size is the number of larvae
retained on a 0.5 mm sieve as a proportion of the total. Pond and exclosure-control pair
nested within pond were included as random factors using the GLIMMIX macro. See
methods for more details. Estimates given are those for controls and period 1.
Exclosures and period 2 were aliased.
Effect Estimate SE F1,49 pDensity Constant 0.33 0.08 D = 16.00 Treatment 5.83 0.019
Control -0.15 0.06Period 4.7 0.035
I -0.15 0.07 Biomass Constant 0.47 0.1D = 44.80 Treatment 17.86 0.0001
Control -0.25 0.06Period 41.42 <0.0001
I -0.44 0.07 Frec 0.5 Constant 0.12 0.33D = 14.34 Treatment 5.02 0.03
C -0.34 0.15Period 2.64 0.11
I -0.33 0.2
D = percentage of deviance explained by the final model compared to the null model.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
112
Table 3. Total numbers of shorebirds (and number feeding) counted from January to
May 2002 in the study area of 123 ha.
30-january 28-february 30-march 30-april 29-mayTringa nebularia* 12 (4) 17 (1) 19 (5) 14 (11) 0 (0)Limosa limosa* 164 (146) 36 (3) 0 (0) 0 (0) 0 (0)Limosa lapponica 0 (0) 214 (1) 80 (0) 61 (14) 59 (2)Tringa totanus* 106 (65) 214 (73) 325 (155) 200 (106) 77 (26)Tringa erythropus* 0 (0) 1 (1) 53 (22) 4 (4) 0 (0)Actitis hypoleucos 0 (0) 0 (0) 8 (0) 1 (1) 0 (0)Recurvirostra avosetta* (101) 10 145 (126) 8 (7) 2 (2) 2 (2)Calidris alpina* 9 (9) 16 (13) 5 (5) 2149 (1684) 321 (265)Calidris canutus 0 (0) 0 (0) 0 (0) 13 (0) 44 (38)Calidris minuta* 3 (3) 3 (3) 3 (1) 1 (1) 0 (0)Calidris alba* 12 (12) 14 (9) 0 (0) 17 (14) 141 (131)Calidris ferruginea* 0 (0) 1951 (165) 6 (6) 2306 (2052) 9 (9)Charadrius hiaticula* 0 (0) 0 (0) 0 (0) 12 (8) 25 (17)Charadrius alexandrinus 1 (1) 0 (0) 0 (0) 0 (0) 0 (0)Pluvialis squatarola* 0 (0) 364 (0) 131 (0) 48 (5) 29 (8)Himantopus himantopus* 31 (15) 139 (35) 250 (118) 0 (0) 3 (3)Arenaria interpres 1 (0) 2 (2) 0 (0) 7 (2) 1 (1)Philomachus pugnax 0 (0) 2 (2) 0 (0) 0 (0) 0 (0)TOTAL 440 (265) 3118 (434) 880 (319) 4835 (3904) 711 (502)
* species seen feeding inside the control plots.
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
113
Figure 1. Numbers of shorebirds feeding in the study area in relation to the timing of the
exclosure experiments.
Date
30-1 28-2 30-3 30-4 29-5
Nº o
f fee
ding
sho
rebi
rds
0
1000
2000
3000
4000
5000
PeriodI Period II
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
114
Figure 2. a) Density and b) estimated biomass of C. salinarius larvae (mean ± s.e.) at
the beginning and end of exclosure experiments.
Period I Period II
Initial Final Initial Final0
5000
10000
15000
20000
25000
30000
35000
Chi
rono
mid
larv
ae d
ensi
ty (
nº/m
2)
Control Exclosure
0
20
40
60
80
Period I Period II
Initial Final Initial Final
Chi
rono
mid
larv
ae b
iom
ass
(mg)
Control Exclosure
CHAPTER 4 EFFECT OF SHOREBIRD PREDATION ON CHIRONOMIDS
115
Figure 3. Size frequency distribution of C. salinarius larvae at the beginning and end of
exclosure experiments. Only larvae retained on a 0.5 mm sieve are included. Initial data
are pooled for controls and exclosures. Length category 1 = 0-1mm, etc.
Initial
Category of length (mm)
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
% o
f obs
erva
tions
0
5
10
15
20
25
Final Control
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 190
5
10
15
20
25
Final Exclosure
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 190
5
10
15
20
25
Period I
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 190
5
10
15
20
25
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 190
5
10
15
20
25
Initial
Final Control
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 190
5
10
15
20
25
Final Exclosure
Period II
116
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
117
CHAPTER 5
CESTODES FROM ARTEMIA PARTHENOGENETICA (CRUSTACEA,
BRANCHIOPODA) IN THE ODIEL MARSHES, SPAIN: A SYSTEMATIC
SURVEY OF CYSTICERCOIDS
BOYKO B. GEORGIEV1,2*, MARTA I. SÁNCHEZ3, ANDY J. GREEN3, PAVEL
N. NIKOLOV1, GERGANA P. VASILEVA1 & & RADKA S. MAVRODIEVA1
1Central Laboratory of General Ecology, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113 Sofia,
Bulgaria.2Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, U.K.
3Estación Biológica de Doñana (CSIC), Avda. María Luisa s/n, 41013 Sevilla, Spain.
Key words: Artemia, Cyclophyllidea, cysticercoids, life cycles, intermediate host
Running head: Cysticercoids from Artemia parthenogenetica
Acta Parasitologica 50 (2): 105-117.
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
118
ABSTRACT
A total of 3,300 specimens of brine shrimps Artemia parthenogenetica from the Odiel
Marshes, Huelva Province, SW Spain, were studied during several seasons of 2002 and
2003 for the presence of cestode infections. Cysticercoids were found in 26.8% of brine
shrimps. Eight cestode species were recorded, i.e. Hymenolepididae: Flamingolepis
liguloides (adults parasitic in flamingos) with prevalence (P) 18.5%, mean intensity
(MI) 1.48 and mean abundance (MA) 0.28; F. flamingo (adults parasitic in flamingos),
P 0.9%, MI 1.03, MA 0.01; Confluaria podicipina (adults parasitic in grebes), P 6.5%,
MI 1.42, MA 0.09; Wardium stellorae (adults parasitic in gulls), P 0.2%, MI 1.00, MA
0.002; Dilepididae: Eurycestus avoceti (adults parasitic in waders and flamingos), P
2.7%, MI 1.08, MA 0.03; Anomotaenia sp., probably A. microphallos (adults parasitic
in waders), P 0.8%, MI 1.04, MA 0.01; A. tringae (adults parasitic in waders), P 2.2%,
MI 1.01, MA 0.02; Progynotaeniidae: Gynandrotaenia stammeri (adults parasitic in
flamingos), P 0.6%, MI 1.00, MA 0.01. The cysticercoids are described and
accompanying illustrations are presented. This study provides the first record of
Anomotaenia tringae in an intermediate host and the first records of C. podicipina, E.
avoceti, A. tringae and G. stammeri in Spain.
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
119
INTRODUCTION
Previous studies revealed the role of brine shrimps of the genus Artemia Leach, 1819
(Crustacea, Branchiopoda) as intermediate host in the life cycles of cestodes parasitising
aquatic birds. The most detailed studies were carried out at Tengiz Lake, Kazakhstan
(Maksimova 1973, 1976, 1977, 1981, 1986, 1987, 1988, 1989, 1991, Gvozdev and
Maksimova 1979) and in the Camargue, France (Gabrion and MacDonald 1980, Thiéry
et al. 1990, Robert and Gabrion 1991); in those places, cysticercoids of 11 and 6 avian
cestode species, respectively, were found in brine shrimps. In Spain, only two cestode
species, Flamingolepis liguloides (Gervais, 1874) and Wardium stellorae (Deblock,
Biguet et Capron, 1960), were found in Artemia at the Mediterranean coast (Amat et al.
1991a, 1991b, Varó et al. 2000).
The present study was carried out at one of the largest saltworks in Spain, which
is also a site of major importance for waterbirds (Bernués 1998, Sánchez et al. in press).
It is situated in the estuary of the Odiel and Tinto Rivers, Huelva Province, SW Spain,
near the Atlantic coast of Andalusia. The aim of this article is to characterise the species
composition of the avian cestodes utilising crustaceans of the genus Artemia as
intermediate hosts in the Odiel Marshes. It also provides the taxonomic framework for
ecological studies being carried out on brine shrimps and their cestode parasites (results
to be reported elsewhere).
MATERIALS AND METHODS
The identification of the brine shrimps was based on the work by Abatzopoulos et al.
(2002) and recent studies at the same site (Amat et al. 2005). In the Mediterranean
Region, the native species of Artemia are the bisexual A. salina Leach, 1819 (synonym
A. tunisiana Bowen et Sterling, 1978) together with a heterogeneous group of
parthenogenetic populations known under the binomen A. parthenogenetica Bowen et
Sterling, 1978 (see Abatzopoulos et al. 2002). A. parthenogenetica only has been
recorded in the Odiel Saltworks (Amat et al. 2005).
Samples, each containing 500 specimens of brine shrimps, were collected from
an evaporation pond (E-18) at the Odiel Saltworks in October and December of 2002
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and in February, April, June and August of 2003. In addition, a sample of 200
specimens collected in October, 2002 and a sample of 100 specimens collected in
November, 2003 were examined. In total, 3,300 specimens of brine shrimps were
studied for the presence of cysticercoids. The collected brine shrimps were killed by
heating to 80ºC and preserved in 70% ethanol. They were mounted in temporary
glycerol mounts and examined under a stereomicroscope or compound microscope after
gentle pressure on the coverslip. If the identification of the cysticercoids recorded was
not possible at this stage, whole infected brine shrimps or isolated cysticercoids were
prepared as permanent mounts in Berlese’s medium in order to facilitate observations
on the morphology of rostellar hooks. Data on the prevalence, intensity and abundance
are based on these samples.
Another sample of 380 specimens collected from the same and neighbouring
ponds (E-11, E-18 and E-17) were examined in July, 2004 in order to provide further
information on the morphology of the cysticercoids, so as to complete that gathered on
the basis of the fixed materials. The brine shrimps were examined alive under a
stereomicroscope and a compound microscope. After observations of the cysticercoids
in situ, each infected specimen was gently pressed under the coverslip and the
observations continued on isolated cysticercoids. These were carried out initially in
hypertonic conditions (in water from ponds) and later in hypotonic conditions (in tap
water). The latter was found to provide longer survival of the cysticercoids (for about 1
hour) ex situ and, in some cases (Eurycestus avoceti, Anomotaenia microphallos and
Gynandrotaenia stammeri), to provoke their excystation.
In July, 2004, samples of other invertebrates abundant in the same ponds were
examined. These were adult coleopterans of the families Hydraenidae (Ochthebius
corrugatus Rosenhauer, 1856 – 23 specimens and O. notabilis Rosenhauer, 1856 – 55
specimens) and Dytiscidae (Nebrioporus ceresyi (Aubé, 1836) – 70 specimens,
chironomid larvae tentatively identified as Chironomus salinarius Kieffer in
Thienemann, 1915 – 424 specimens, and harpacticoid copepods Cletocamptus
retrogressus Shmankevich, 1875 – 160 specimens.
Voucher specimens of cysticercoids found are deposited in the collection of The
Natural History Museum, London (BMNH).
The metrical data in the following descriptions are based on specimens mounted
in Berlese’s medium only. They are given as the range, with the mean and the number
of measurements taken in parentheses. The measurements are in micrometres except
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where otherwise stated. The infection descriptors (prevalence, intensity and abundance)
are after the definitions by Bush et al. (1997).
RESULTS
Infection characteristics
Of 3,300 specimens of Artemia studied, 886 specimens (26.8%) were infected with
cysticercoids. The intensity of the infection was 1-13 cysticercoids. The total values of
the mean abundance and the mean intensity were 1.71 and 0.44, respectively.
Cysticercoids of 8 cyclophyllidean species belonging to three families were recorded in
the brine shrimps examined. Among them, Flamingolepis liguloides was the most
prevalent and abundant species (Table 1).
The majority of the infected brine shrimps contained cysticercoids of one cestode
species; 171 specimens (19.3% of the infected shrimps) harboured more than one. Two
cestode species were recorded from 135 shrimps, three species from 32 specimens, four
species from three specimens and one shrimp contained cysticercoids of 5 tapeworm
species (Table 2).
No cysticercoids were recorded in other invertebrate species studied.
Systematic survey of cysticercoids
Family Hymenolepididae
Flamingolepis liguloides (Gervais, 1847)
Voucher specimens: BMNH 2005.2.23.1-5 (5 slides).
Description: Cyst oval (Figs. 9, 10), 560-810 x 372-597 (671 x 479, n = 14). Calcareous
corpuscles numerous. Scolex 358-771 x 339-490 (614 x 423, n = 14). Suckers round or
oval, with diameter 181-288 (233, n = 18). Rostellum elongate, 446-485 x 116-149 (465
x 125, n = 14), with strongly developed circular musculature. Rostellar hooks
skrjabinoid, 8 (n = 15) in number, 186-201 (189, n = 15) long (Figs. 1, 11); length of
blade 105-117 (110, n = 15). Ratio of length of blade / total hook length 0.56-0.60
(0.58, n = 15). When rostellum contracted, blades of hooks are posteriorly directed.
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Cercomer elongate (Fig. 10), with length comparable with that of cyst, 620-810 x 45-68
(710 x 55, n = 8).
Remarks: The present material corresponds to the cysticercoids from Artemia sp.
identified by Robert and Gabrion (1991) as F. liguloides, and from Artemia sp.
(originally identified as A. salina) and Branchinella spinosa (M. Milne-Edwards)
reported by Maksimova (1973, 1989) as F. dolguschini Gvozdev et Maksimova, 1968.
The taxonomy of Flamingolepis Spasskii et Spasskaya, 1954 is poorly known. Amat et
al. (1991b) believed that F. dolguschini is a synonym of F. liguloides. However, the
adult cestodes described by Maksimova (1989) under these two names clearly differed
from each other. Nevertheless, the affiliation of these cysticercoids from France, Spain
and Kazakhstan, all with 8 skrjabinoid hooks 180-190 μm long, to a single species is
justified by their morphology. Pending a revision of the hymenolepidids specific to
flamingos, we follow Robert and Gabrion (1991) and accept F. liguloides as the most
probable identification of these cysticercoids.
Flamingolepis flamingo (Skrjabin, 1914)
Voucher specimens: BMNH 2005.2.23.6-10 (5 slides).
Description: Cyst oval, thick-walled (Figs. 12, 13), 168-270 x 126-207 (231 x 177, n =
14). Calcareous corpuscles numerous, concentrated mostly in anterior part of cyst.
Scolex 141-225 x 108-183 (182 x 145, n = 12). Suckers oval, with diameter 45-75 (66,
n = 16). Rostellum highly elongate, with strong circular musculature, 108-180 x 33-48
(119 x 43, n = 5) when contracted or 177-225 x 33-39 (206 x 36, n = 3) when extended.
Rostellar hooks skrjabinoid, 8 (n = 16) in number, 55-61 (57, n = 15) long (Figs. 2, 14);
length of blade 28-30 (29, n = 15). Ratio of length of blade / total hook length 0.47-0.53
(0.50, n = 15). When rostellum contracted, blades of hooks are posteriorly directed.
Cercomer highly elongate (Figs. 12, 13), 6.5-7.4 mm (n = 3) long, 8-12 (10, n = 14)
wide.
Remarks: F. flamingo is a specific parasite of flamingos in Eurasia (Maksimova 1989).
Robert and Gabrion (1991) found its cysticercoid in Artemia sp. in France. The present
material is in agreement with their description.
Confluaria podicipina (Szymanski, 1905)
Voucher specimens: BMNH 2005.2.23.11-16 (6 slides).
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Description: Cyst oval, thin-walled (Fig. 19), 93-147 x 47-87 (121 x 73, n = 12), often
with distinct transverse striations. Calcareous corpuscles numerous, concentrated in
anterior and in posterior part of cyst (Figs. 18, 19). Scolex 72-104 x 38-72 (92 x 59, n =
12). Suckers slightly oval, with diameter 26-32 (28, n = 10). Rostellum 42-47 (46, n =
7). Rostellar hooks 10 in number, aploparaksoid (Fig. 3), 21-24 (22, n = 12) long; when
rostellum contracted, blades of hooks anteriorly directed. Cercomer very large. Anterior
part of cercomer forms additional envelope surrounding cyst, thus forming external
capsule (Figs. 17, 18) measuring 195-255 x 135-204 (215 x 152, n = 9). Posterior part
of cercomer highly coiled, densely packed in thin membranous envelope (Fig. 16),
which surrounds entire cysticercoid.
Remarks: C. podicipina is a parasite of grebes (Podicipedidae) in the Holarctic Region
(see Vasileva et al. 2000 for a survey). Its cysticercoid was described from Artemia in
Kazakhstan (Maksimova 1981, 1989). We were not able to measure the length of the
cercomer exactly because of its coiled configuration; however, it seems to be close to
the length reported by Maksimova (1981), i.e. 14.5-16.5 cm. We also confirm that the
cysticercoid rostellar hook of this species corresponds to the hook part referred to as the
‘refractive particle’ (Vasileva et al. 2000) or ‘tip hooklet’ (Maksimova 1981, 1989) of
adults, and therefore that hooks do grow in the final host.
Our observations on living specimens lead us to an interpretation of the structure of the
cysticercoid differing from that by Maksimova (1981). She believed that the external
wall of the cyst consisted of 6 layers. In contrast, we consider that only the ‘internal
cyst’ is homologous to the cysts of other hymenolepidid cysticercoids, while the
external 3 layers described by Maksimova (1981) are a modification of the anterior part
of the cercomer, forming an additional protective envelope surrounding the cyst. When
placed in hypotonic conditions, the real cyst is readily detached from the bottom of the
cavity formed by the anterior part of the cercomer (Figs. 18, 19); simultaneously, a
distinct orifice can be seen at the anterior end of the ‘external cyst’ (Fig. 18).
Wardium stellorae (Deblock, Biguet et Capron, 1960)
Synonyms: Hymenolepis stellorae Deblock, Biguet et Capron, 1960; Aploparaksis
parafilum Gąsowska, 1932 sensu Maksimova (1973).
Voucher specimens: BMNH 2005.2.23.17-18 (2 slides).
Description: Cyst oval to lemon-shaped (Fig. 20), 189-213 x 153-189 (199 x 166, n =
5). Scolex 123-132 x 105-123 (126 x 111, n = 5). Rostellum oval, 39-45 x 25-30 (41 x
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
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27, n = 5). When rostellum is contracted blades of rostellar hooks are directed
anteriorly. Suckers slightly oval, with diameter 45-57 (50, n = 7). Rostellar hooks10 in
number, 23 (n = 4) long, aploparaksoid, with distinct handle; blade considerably longer
than guard (Figs. 4, 20). Entire cercomer was not isolated; length of cercomer exceeds
400 (judging from fragmented cercomer), width 25-39.
Remarks: W. stellorae was described as an intestinal parasite of Larus ridibundus L. on
the French Atlantic coast (Deblock et al. 1960). Further studies recorded it from L.
genei Breme in the Ukraine and Kazakhstan and from L. californicus Lawrence in North
America (data summarised by Maksimova 1986, 1989). Its cysticercoid was reported
from brine shrimps from Kazakhstan (Maksimova 1986), France (Robert and Gabrion
1991) and the Mediterranean coast of Spain (Varó et al. 2000). The rostellar hooks of
the present material correspond with the previous descriptions of adults (Deblock et al.
1960, Maksimova 1986, 1989) and cysticercoids (Maksimova 1986, Robert and
Gabrion 1991). Maksimova (1986) mentioned that the cysticercoids from Artemia
identified by her (Maksimova 1973) as Aploparaksis parafilum Gąsowska, 1932 should
also be considered as belonging to W. stellorae.
Recently, Bondarenko and Kontrimavichus (2004a) erected the genus
Branchiopodataenia for a group of species from gulls and previously referred to
Wardium Mayhew, 1925. They used the structure of the female copulatory ducts as a
main distinguishing character and showed that the cysticercoids of these species
develop in branchiopods. None of the cysticercoids described by Bondarenko and
Kontrimavichus (2004b) has rostellar hooks identical to those of the present material. B.
anaticapicirra Bondarenko et Kontrimavichus, 2004, a parasite of Arctic gulls, has
rostellar hooks 18-22 long but with the blade only slightly larger than the guard. The
cysticercoid of B. arctowskii (Jarecka et Ostas, 1984), described from Antarctic gulls
and recorded at various places in the Holarctic Region, has hooks 15-16 long. B.
haldemani (Shiller, 1951) and B. pacifica (Spassky et Jurpalova, 1969) from Arctic
gulls are characterised by rostellar hooks 12-13 and 16-18 long, respectively
(Bondarenko and Kontrimavichus 2004b). Thus, W. stellorae is a distinct form,
differing from Branchiopodataenia spp. Although its cysticercoid develops in
branchiopods, the morphology of the adult worms (Deblock et al. 1960) does not
correspond to the diagnosis of Branchiopodataenia. Therefore, we prefer to consider it
as belonging to Wardium.
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Family Dilepididae
Eurycestus avoceti Clark, 1954
Voucher specimens: BMNH 2005.2.23.19-23 (5 slides).
Description: Outer capsule oval or almost spherical (Fig. 21), brownish, with granular
contents, 240-330 x 230-279 (295 x 255, n = 9). When compressed, outer capsule
breaks down into cercomer fragments (Fig. 22). Cyst oval (Fig. 23), 141-228 x 99-163
(182 x 137, n = 12). Calcareous corpuscles numerous. Scolex rounded (Fig. 23), 111-
150 x 81-114 (135 x 98, n = 8). Suckers round or slightly oval, with diameter 26-36 (30,
n = 15); their anterior margin armed with hooklets, 6-8 long, arranged in 1-2 layers
(Figs. 5c, 24); number of hooklets on 1 sucker 9-17 (n = 18): 9 (n = 1), 10 (n = 2), 11 (n
= 6), 12 (n = 1), 13 (n = 3), 14 (n = 1), 16 (n = 3) and 17 (n = 1). Rhynchus very long
(Figs. 25, 26). Rostellar hooks 14 (n = 1) or 16 (n = 12), in 2 rows (Figs. 25, 26).
Anterior hooks 16-18 (17, n = 12) long, blade 3-4 long (Fig. 5a). Posterior hooks 15-16
(n = 10) long, blade 3 long (Fig. 5b).
Remarks: Adults of E. avoceti are parasites of charadriiform birds, mostly Recurvirostra
spp., throughout the Holarctic Region (Baer 1968, Spasskaya and Spasskii 1978,
Maksimova 1991). In Kazakhstan, this species was also recorded in 23.3% of flamingos
studied (Maksimova 1991). The present identification is based on a correspondence
between the cysticercoids found and previous descriptions of adults (Baer 1968,
Maksimova 1991) and cysticercoids (Gabrion and MacDonald 1980, Maksimova 1991).
However, there are some substantial differences in the lengths of the posterior rostellar
hooks and the number of the sucker hooklets (Table 3), which suggest that cysticercoids
from France, Spain and Kazakhstan may represent more than one species. Until now, E.
avoceti is the only species of the genus that has been recorded in the Palaearctic Region.
Two further species occur in North America (Burt 1979) but their scoleces have not
been described. Furthermore, the two Palaearctic species of Paraliga Belopol’skaya et
Kulachkova, 1973, which includes dilepidids from charadriiform birds (Deblock and
Rosé 1962, Belopol’skaya and Kulachkova 1973), are also characterised by a similar
scolex armament (Table 3). Therefore, although the identification of our material as E.
avoceti is the most probable based on a comparison with Baer’s (1968) description, it is
somewhat provisional.
Anomotaenia sp. (cf. A. microphallos (Krabbe, 1869))
Voucher specimens: BMNH 2005.2.23.24-28 (5 slides).
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Description: Outer capsule spherical to slightly oval (Figs. 27, 28), brownish, with
granular contents, 228-316 x 192-283 (272 x 233, n = 11). Cyst oval (Figs. 28, 29), 186-
209 x 121-150 (194 x 136, n = 12). Calcareous corpuscles numerous, concentrated
mostly in anterior and posterior part of cyst. Scolex rounded (Figs. 29, 30), 135-165 x
105-120 (150 x 109, n = 8). Suckers slightly oval (Fig. 30), with diameter 48-60 (54, n
= 14). Rostellum elongate (Fig. 30), 65-85 x 25-36 (76 x 31, n = 7). Rostellar hooks 26
(n = 1), 28 (n = 8) or 30 (n = 2), form irregular crown (Fig. 29). Anterior hooks situated
one by one; 2 or 3 posterior hooks situated between each 2 anterior hooks; sometimes,
posterior hooks at different level, thus creating impression of crown consisting of three
rows. Anterior hooks with guard almost perpendicular to hook axis (Fig. 6a), 12-13 (n =
10) long; posterior hooks with guard almost parallel to blade (Fig. 6b), 11-12 (n = 10)
long.
Remarks: The number of rostellar hooks of the present material (26-30) suggests its
affiliation with the family Dilepididae. The only dilepidid species from Palaearctic
aquatic birds characterised by numerous (more than 20) rostellar hooks with a length of
about and less than 15 μm is Anomotaenia microphallos (for surveys of Palaearctic
dilepidids from charadriiform birds and from fish-eating birds, see Spasskaya and
Spasskii 1978 and Ryzhikov et al. 1985, respectively). This species was originally
described from Vanellus vanellus (L.) in Germany as having a crown of 24 hooks with a
length of 14-16 μm (anterior) and 12-14 μm (posterior) (Krabbe 1869). Further studies
added to the range of its final hosts waders of the genera Charadrius L., Calidris
Merrem, Gallinago Brisson, Philomachus Merrem and Tringa L. (see Spasskaya and
Spasskii 1978). However, none of the descriptions of adult cestodes of this species
surveyed by Spasskaya and Spasskii (1978) reported more than 24 hooks. Therefore, we
prefer to retain the identification at the generic level only.
Anomotaenia tringae (Burt, 1940)
Voucher specimens: BMNH 2005.2.23.29-33 (5 slides).
Description: Outer capsule oval (Fig. 31), yellowish-brown, with granular contents,
249-316 x 218-297 (279 x 236, n = 12). Cyst oval (Fig. 32), 107-139 x 84-102 (131 x
93, n = 14). Calcareous corpuscles numerous, concentrated mostly in anterior part of
cyst. Scolex rounded, 76-85 x 66-72 (82 x 70, n = 9). Suckers indistinct in available
mounts in Berlese’s medium, obviously with weak musculature. Rostellum 62-66 x 23-
27 (n = 3). Rostellar hooks 18 (n = 6) or 20 (n = 4), in 2 rows forming compact crown
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(Fig. 32); blade slightly shorter than handle (Fig. 7a, b); anterior hooks 20-21 (n = 9)
long; posterior hooks 19-20 (n = 8) long.
Remarks: This species was originally described from Tringa glareola L. and T. totanus
L. in Sri Lanka (Burt 1940). Subsequently, it was recorded from charadriiform birds of
the genera Tringa, Calidris, Charadrius, Gallinago, Philomachus and Vanellus Brisson
throughout the Old World, from Iceland to Zambia and from Kamchatka to Borneo
(Spasskaya and Spasskii 1978). The present study is the first record of A. tringae in an
intermediate host. Our identification is based on a comparison of the number, size and
the shape of rostellar hooks of the cysticercoids with those of the adult worms (syntypes
from Tringa glareola, British Museum (Natural History) Collection no. 1983.7.11.16).
The original description reported 18 rostellar hooks with a length of 17-18 μm “in what
is practically a single row, but they show a slight alteration in arrangement into two
levels but they are all similar in shape and size” (Burt 1940). Our observations show
that the rostellar hooks of the syntypes studied are 18 in number, 21-22 μm long and
have a similar shape (Fig. 7c, d) to those of the cysticercoids from Spain (Fig. 7a, b).
Family Progynotaeniidae
Gynandrotaenia stammeri Fuhrmann, 1936
Voucher specimens: BMNH 2005.2.23.34-38 (5 slides).
Description: Cyst oval or lemon-shaped (Fig. 34), 142-192 x 95-170 (166 x 124, n =
17). Two layers distinguished in cyst wall: external layer hyaline, 9-11 thick; internal
layer finely striated, 5-7 thick. Calcareous corpuscles 70-80. Scolex 113-147 x 89-121
(133 x 103, n = 14). Suckers oval, with diameter 36-45 (39, n = 62); margins armed
with densely arranged spines (Figs. 35, 36). Invaginable anterior part of scolex (termed
‘proscolex’, see Fuhrmann 1936) distinct (Fig. 36), covered with small spines.
Rostellum 65-74 x 25-34 (70 x 29, n = 11). Rostellar hooks 6 (n = 17), 40-46 (43, n =
15) long (Figs. 8, 35, 36); length of blade 13-15 (13.5, n = 15). Ratio length of blade /
total hook length 0.28-0.35 (0.31, n = 15). Cercomer highly elongate, convoluted, much
larger than cyst (Fig. 33), 2.2-2.5 mm long and 47-78 wide (n=3).
Remarks: The morphology of these cysticercoids is in agreement with the previous
descriptions (Gvozdev and Maksimova 1979, Robert and Gabrion 1991). Adults of G.
stammeri have been recorded from Phoenicopterus roseus Pallas and P. minor Geoffroy
Saint-Hilaire in Europe (Fuhrmann 1936a, 1936b, Robert and Gabrion 1991),
Kazakhstan (Gvozdev and Maksimova 1979) and Kenya (Jones and Khalil 1980).
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Cysticercoids were reported from Artemia from Kazakhstan (Gvozdev and Maksimova
1979) and France (Robert and Gabrion 1991).
Robert and Gabrion (1991) cited the paper by Gvozdev and Maksimova (1979)
as a record of cysticercoids of G. stammeri in an ostracod species. However, the only
intermediate host species mentioned in the latter article is Artemia.
DISCUSSION
According to the terminology proposed by Chervy (2002), the cysticercoids of
Flamingolepis liguloides, F. flamingo, Wardium stellorae and Gynandrotaenia
stammeri belong to the group of the cercocysticercoids, while those of Eurycestus
avoceti, Anomotaenia tringae and Anomotaenia sp. are considered monocysticercoids.
The cysticercoid of Confluaria podicipina is close to the modification termed
“ramicysticercoid” but its cercomer is not branching. This suggests the necessity of
further improvement of the terminology proposed by Chervy (2002).
The following 13 cyclophyllidean cestode species were previously known to use
brine shrimps of the genus Artemia as intermediate host in their life cycles:
Hymenolepididae (10 species): Confluaria podicipina (see Maksimova 1981, 1989),
Fimbriarioides tadornae Maksimova, 1976 (see Maksimova 1976, 1989),
Flamingolepis liguloides (synonym F. dolguschini) (see Maksimova 1973, 1989, Robert
and Gabrion 1991, Thiéry et al. 1990, Amat et al. 1991a, 1991b, Varó et al., 2000), F.
caroli (Parona, 1887) (see Robert and Gabrion 1991), F. flamingo (see Robert and
Gabrion 1991), F. tengizi (see Maksimova 1973, 1989), Hymenolepis californicus
Young, 1950 (see Young 1952), Wardium fusa (Krabbe, 1869) (see Maksimova 1987,
1989), W. gvozdevi Maksimova, 1988 (see Maksimova 1988, 1989) and W. stellorae
(Deblock, Biguet et Capron, 1960) (see Maksimova 1986, Robert and Gabrion 1991,
Varó et al., 2000).
Dilepididae (2 species): Eurycestus avoceti (see Gabrion and MacDonald 1980, Robert
and Gabrion 1991, Maksimova 1991) and Anomolepis averini (Spasskii et Yurpalova,
1967) (see Maksimova 1977).
Progynotaeniidae (1 species): Gynandrotaenia stammeri (see Gvozdev and Maksimova
1979, Robert and Gabrion 1991).
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For 6 of these species, i.e., C. podicipina, F. liguloides, F. flamingo, W.
stellorae, E. avoceti and G. stammeri, our study confirms the role of brine shrimps as an
intermediate host in their life cycle. In addition, Anomotaenia tringae is recorded for the
first time in its intermediate host. Therefore, brine shrimps participate in the
transmission of the cestode parasites of flamingos, waders, grebes and gulls at the Odiel
Marshes.
Robert and Gabrion (1991) examined more than 64,000 brine shrimps in the
Camargue, France, and recorded a prevalence of cestode infection of between 1.56 and
5.12% in various seasons; the values of the mean abundance for the species in common
with these in our study are: F. liguloides 0.0506, F. flamingo 0.000743, W. stellorae
0.000077, G. stammeri 0.000031 and E. avoceti 0.00091. The data obtained for the
prevalence of cysticercoids in the Odiel Marshes (Table 1) are 6 times higher, and those
for the mean abundance are between 5 and 322 times higher. These differences suggest
much higher rates of cestode transmission compared to those recorded in the Camargue.
In contrast to the high infection rates in Artemia, no cysticercoids were found in any of
the other 5 invertebrate species studied from the same water body.
The present study is the first record of C. podicipina, E. avoceti, A. tringae and
G. stammeri in Spain.
ACKNOWLEDGEMENTS
We are grateful to Professor F. Amat (Instituto de Acuacultura de Torre de la Sal, CSIC,
Castellón, Spain), Professor V.V. Kornyushin (Institute of Zoology, National Academy
of Sciences, Kiev, Ukraine) and Dr V.V. Tkach (University of North Dakota, Grand
Forks, USA) for the stimulating comments and useful suggestions in the course of the
present study, and to Dr D.I. Gibson (The Natural History Museum, London) for
reading the manuscript. This study was carried out in the framework of a co-operative
project between the Bulgarian Academy of Sciences and the Consejo Superior de
Investigationes Cientificas with the title Ecological aspects of the role of brine shrimps
in the transmission of avian cestodes.
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Thiéry A., Robert F. & Gabrion C. 1990. Distribution des populations d’Artemia et de
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Vasileva G.P., Georgiev B.B. & Genov T. 2000. Palaearctic species of the genus
Confluaria Ablasov (Cestoda, Hymenolepididae): redescriptions of C. podicipina
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sp., a key and final comments. Systematic Parasitology, 45, 109-130.
Young R.T. 1952. The larva of Hymenolepis californicus in the brine shrimp (Artemia
salina). Journal of the Washington Academy of Sciences, 42, 385-388.
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135
Table 1. Infection of brine shrimps with cysticercoids in the Odiel Marshes, Spain.
IntensityCestode species Prevalence(%) Range Mean ± SD
Meanabundance ±
SD
HymenolepididaeFlamingolepis liguloides 18.5 1-8 1.48 ± 0.89 0.28 ± 0.01Flamingolepis flamingo 0.9 1-2 1.03 ± 0.18 0.01 ± 0.10Confluaria podicipina 6.5 1-7 1.42 ± 0.82 0.09 ± 0.40Wardium stellorae 0.2 1-1 1.00 ± 0.00 0.002 ± 0.043
DilepididaeEurycestus avoceti 2.7 1-3 1.08 ± 0.31 0.03 ± 0.18Anomotaenia sp. (cf. A.microphallos)
0.8 1-2 1.04 ± 0.19 0.01 ± 0.10
Anomotaenia tringae 2.2 1-2 1.01 ± 0.12 0.02 ± 0.15
ProgynotaeniidaeGynandrotaenia stammeri 0.6 1-1 1.00 ± 0.00 0.01 ± 0.08
Cysticercoids, total 26.8 1-13 1.71 ± 1.28 0.44 ± 0.99
Table 2. Multiple species infections of brine shrimps with cysticercoids in the Odiel Marshes, Spain.
Number of cestode species participating in the multiple infectionCestode species2 3 4 5
Flamingolepis liguloides + + + + + + + + + + + + + + + + + + +Flamingolepis flamingo + + + + + + + + + + +Confluaria podicipina + + + + + + + + + + + + + + + +Wardium stellorae + + +Eurycestus avoceti + + + + + + + + + +Anomotaenia sp. (cf. A.microphallos)
+ + + + + +
Anomotaenia tringae + + + + + + + +Gynandrotaenia stammeri + + + + + + +Number of specimens ofArtemia infected by thiscombination of species
10 41 29 3 7 8 1 1 1 1 1 2 3 3 19 2 1 2 5 2 1 1 7 8 3 4 1 1 1 1 1
137
Table 3. Morphological characteristics of the scolex armament of adult cestodes and cysticercoids of Eurycestus avoceti and species with similarscoleces.
Rostellar hooks Sucker hookletsLength
Species Locality SourceNumber
Anterior PosteriorNumber Length
Eurycestus avoceti adult cestodes France Baer (1968) 14-16 14-16* 14-16* 10-14 5-6
Kazakhstan Maksimova (1991) 16 16-18 10-12 30-32 5-6 cysticercoids France Gabrion & Mac Donald (1980) 16 18 12 15-16 7
Kazakhstan Maksimova (1991) 16 16-18 10-12 30-32 4-5Spain Present study 14-16 16-18 15-16 9-17 6-8
Paraliga oophorae adult cestodes Russia
(White Sea)Belopol’skaya & Kulachkova(1973)
16 18 14 34-37 4
Paraliga celermatus adult cestodes France Deblock & Rosé (1962) 16 24-26* 24-26* 25-30 4-5
*Lengths of anterior rostellar hooks and length of posterior rostellar hooks not given separately.
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
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Figs 1-8. Rostellar hooks and sucker hooklets of the cysticercoids found. 1.
Flamingolepis liguloides. 2. F. flamingo. 3. Confluaria podicipina. 4. Wardium
stellorae. 5. Eurycestus avoceti – a, anterior hook; b, posterior hook; c, sucker hooklets.
6. Anomotaenia sp., cf A. microphallos – a, anterior hook; b, posterior hooks. 7. A.
tringae. – a, b, rostellar hooks of a metacestode from a brine shrimp; c, d, rostellar
hooks of a syntype specimen from Tringa glareola from Sri Lanka. 8. Gynandrotaenia
stammeri.
20 µm
1
50µm
8
5a 5b 5c
6a 6b 7a 7b 7c 7d
2
43
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
139
Figs 9-14. Flamingolepis spp. 9-11. F. liguloides. 9. Metacestode in situ. 10. General
view of isolated metacestode, phase contrast. 11. Rostellar hooks. 12-14. F. flamingo.
12. General view of isolated metacestode (C, cercomer). 13. Cyst of metacestode, phase
contrast. 14. Rostellar hooks, phase contrast.
200 µm 200 µm
200 µm100 µm
100 µm 50 µm
9 10
12
1413
11
C
C
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
140
Figs 15-20. Confluaria podicipina and Wardium stellorae. 15-19. C. podicipina. 15.
Metacestode in situ; compare the size with that of the metacestode of F. liguloides (C,
cercomer). 16. Highly coiled and densely packed cercomer (C) in the body cavity of the
host. Inset: Portion of the cercomer, phase contrast. Note the thin membranous envelope
(arrow). 17. Isolated metacestode. 18. Isolated metacestode under hypotonic conditions.
Note the anterior orifice of the external capsule (arrow). 19. Metacestode, mounted in
Berlese’s medium. 20. W. stellorae, general view of the metacestode, mounted in
Berlese’s medium, phase contrast. Inset: Rostellar hooks, phase contrast.
200 µm 200 µm
100 µm
50 µm 100 µm
15 16
18
2019
17 200 µm
100 µm
25 µm
C
C
C
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
141
Figs 21-26. Eurycestus avoceti. 21. Metacestode in situ. 22. Isolated metacestode with
outer capsule breaking down into cercomer fragments. 23. Isolated cyst. 24. Anterior
end of isolated cyst. Note protruding rhynchus and sucker hooklets. 25. Isolated
metacestode with entirely protruded rhynchus. Inset: Rostellum. 26. Metacestode
excysted under hypotonic conditions. Inset: Rostellar hooks, phase contrast.
200 µm21
100 µm23
200 µm25 26
50 µm24
200 µm22
50 µm
200 µm
50 µm
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
142
Figs 27-32. Anomotaenia spp. 27-30. Anomotaenia sp., cf. A. microphallos. 27.
Metacestode in situ; compare the size with that of the metacestode of F. liguloides. 28.
Isolated and slightly flattened metacestode. 29. Isolated cyst. Inset: Rostellar hooks,
phase contrast. 30. Anterior part of isolated cyst. 31-32. A. tringae. 31. Isolated
metacestode. 32. Metacestode squashed in Berlese’s medium; note the granular contents
of the external capsule. Inset: Rostellar hooks, phase contrast.
200 µm27
100 µm29
200 µm31 32
50 µm30
200 µm28
100 µm
25 µm
25 µm
CHAPTER 5 CESTODES FROM ARTEMIA PARTHENOGENETICA
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Figs 33-36. Gynandrotaenia stammeri. 33. Metacestode, general view (C, cercomer).
34. Cyst. 35. Armament of rostellum and suckers, mounted in Berlese’s medium. 36.
Cyst, mounted in Berlese’s medium, phase contrast. Note invaginated proscolex
(arrows).
200 µm 100 µm
50 µm50 µm
33
3635
34
144
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
145
CHAPTER 6
PASSIVE INTERNAL TRANSPORT OF BRINE SHRIMPS AND SEEDS BY
MIGRATORY WADERS IN THE ODIEL MARSHES, SOUTH-WEST SPAIN
MARTA I. SÁNCHEZ1,2, ANDY J. GREEN1 , FRANCISCO AMAT3 & ELOY M.
CASTELLANOS2
1Departamento de Biología Aplicada, Estación Biológica de Doñana, Avenida de María Luisa s/n,
Pabellón del Perú, 41013 Sevilla, Spain2Departamento de Biología Ambiental y Salud Pública, Facultad de Ciencias Experimentales,
Universidad de Huelva, Campus de El Carmen, Avda. Fuerzas Armadas s/n 21071 Huelva, Spain3Instituto de Acuicultura de Torre de la Sal, 12595 Ribera de Cabanes, Spain
Key words: Brine shrimp dispersal, seeds dispersal, seed germination, cysts eclosion,
waders
Running head: Propagule dispersal by waders
Finally excinded in two:
“Internal transport of brine shrimps by migratory waders: dispersal probabilities depend on diet
and season”. Marine Biology 151: 1407-1415.
“Internal transport of seeds by migratory waders in the Odiel marshes, south-west Spain:
consequences for long-distance dispersal”. Journal of Avian Biology 37: 201-206.
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
146
ABSTRACT
Waders (Charadriiformes) undergo particularly long migratory flights, making them
ideal vectors for long-distance dispersal. We present a study of dispersal of plant seeds
and brine shrimp Artemia cysts by migratory waders in the Odiel saltworks in south-
west Spain. Viable cysts of Artemia parthenogenetica were abundant in the faeces and
pellets of Redshank Tringa totanus, Spotted Redshank Tringa erythropus, and Black-
tailed Godwit Limosa limosa during spring and autumn migrations, but were absent
during winter. Most cysts were ingested within Artemia adults. The proportion of cysts
destroyed during digestion decreased as the total number ingested increased, and
increased when accompanied by harder food items. More intact cysts were present in
Redshank faeces than in their pellets, but cysts extracted from pellets were more likely
to hatch. Viable seeds of Mesembryanthemum nodiflorum (Aizoaceae), Sonchus
oleraceus (Asteraceae) and Arthrocnemum macrostachyum (Chenopodiaceae) were
frequent in pellets and faeces, with 11 other seed types recorded at low density. This is
the first field study to demonstrate transport of viable seeds by waders. More intact M.
nodiflorum seeds were present in Redshank faeces than in their pellets, but seeds
extracted from pellets were more likely to germinate. More cysts and S. oleraceus seeds
were transported per Redshank pellet in spring, but more Redshank migrated through
the area in autumn. The distribution of the plants and Artemia transported are consistent
with an important role of long-distance dispersal by waders in their biogeography and
metapopulation biology. M. nodiflorum and S. oleraceus are introduced weeds in the
Americas and Australasia, and dispersal by birds may contribute to their rapid spread.
Although S. oleraceus is generally thought to be wind-dispersed, birds may be
responsible for longer distance dispersal events.
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
147
INTRODUCTION
The Charadriiformes (waders, gulls and terns) include species undergoing the longest
migrations of any animal (del Hoyo et al. 1996). Darwin (1859) proposed that migratory
waterbirds played a major role in the dispersal of aquatic invertebrates and plant seeds,
and waders are likely to be particularly important owing to their long-distance
migrations. Seeds lacking a fleshy fruit are often consumed by waders (see Green et al.
2002 for review) and studies in captivity suggest they can retain viability following gut
passage (see Figuerola & Green 2002a for review). Proctor (1962) demonstrated
transport of viable Chara oospores by waders in Texas. However, as far as we know,
dispersal of viable angiosperm seeds by waders has never been demonstrated in the
field. Field evidence of dispersal of invertebrates by waterbirds is also very limited, but
Green et al. (2005) recently showed that viable brine shrimp Artemia (Anostraca) cysts
(resistant eggs) are dispersed by waders on autumn migration.
In this study we document passive internal dispersal of seeds and Artemia cysts
by waders migrating through the Odiel marshes in south-west Spain, quantifying
numbers of intact propagules and assessing their viability. We quantify levels of
dispersal by different wader species at different times of the year, comparing the
potential for long-distance dispersal during spring and autumn migrations. We
investigate the role of diet and other factors in determining dispersal rates, especially the
rates of ingestion of propagules and their survival during the digestive process.
METHODS
A total of 140 faecal samples and 272 pellets were collected from 2001 to 2003 from
waders in the saltworks of the Odiel marshes in Huelva province in south-west Spain
(37°17'N 06°55'W, area 7158 ha, Fig. 1), a site of international importance for
migratory waders migrating through the East Atlantic flyway (Sánchez et al. in press a,
Stroud et al. 2004). For the purpose of seasonal comparison, sampling dates of 18/3/01,
23/4/01 and 7/4/03 were considered as spring, from 22 July to 21 August as summer,
from 5 September to 18 October as autumn and 13/1/01 plus 28/2/01as winter. Spring
samples coincided with the beginning of the northwards wader migration and summer
and autumn samples with the southwards migration (Hortas 1997, Sánchez et al. in
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
148
press a). Pellets and faeces were collected from Redshank Tringa totanus, pellets from
Spotted Redshank Tringa erythropus, and faeces from the Black-tailed Godwit Limosa
limosa, a species that does not regurgitate pellets. These species were selected because
of their abundance in the study area and because their faecal and pellet samples are
relatively large, making it easier to avoid soil contamination. Redshank and Black-tailed
godwit are two of the four most numerous waders at this site (Sánchez et al. in press a).
We collected fresh faeces and pellets from roost sites on dykes in traditional
saltworks used by monospecific flocks at high tide. Collection points were observed for
30 minutes prior to sampling and only fresh samples were taken to ensure accurate
species identification. In spring 2003, 52 pellet samples were collected from a mixed
flock of the two Tringa species and were only used for quantification of seed transport.
Each sample of excreta was carefully separated from the soil (discarding that part in
contact with soil) and placed in a tube. Given the number of birds present we are
confident that each sample was from a different bird.
The samples were stored at 5oC, until the time of analysis (a lapse of one week
for samples collected in 2003, and of six to 12 months for the rest). Seeds and Artemia
cysts were extracted by washing them in a 0.04 mm sieve and flotation in hypersaline
brine. The seeds and cysts were counted, washed in distilled water then dried for 48 h at
40oC, followed by storage at 5oC prior to hatching or germination experiments. The
composition of the rest of the faecal and pellet samples was also identified, assessing
the proportion of sample volume made up of different food items using the following
categories: 0%, <10%, 11-25%, 26-50%, 51-75%, 76-90% and >90% of total volume
(see Sánchez et al. in press b for details).
Hatching and germination experiments
Not all samples were stored so as to retain their viability, so that hatching or
germination was tested for a subset of samples. Cysts were then incubated in diluted
filtered sea water (25 g L -1) at 26ºC and under continuous illumination for at least 48 h.
Hatched nauplii were counted and transferred into 60 cm3 vessels and cultured in 70 g L-1 filtered brine (seawater plus crude sea salt), on a diet of live Dunaliella salina and
Tetraselmis suecica. They were maintained at 24ºC, under aeration on a 12D:12L
photoperiod. The medium was monitored and renewed every two days. Resulting adults
were identified to species morphologically (Amat et al. 2004).
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
149
Extracted seeds were placed on moist filter paper in a petri dish and watered
regularly with distilled water. They were placed inside a WTBbinder KBW 400
germination chamber at 22 oC on a 12D:12L photoperiod, on 2/10/03. They were checked
daily for germination for 30 days. One sample of 84 seeds from a Redshank pellet was
attacked by mould and removed from the experiment. Some seedlings were cultivated to
enable species identification.
Statistical analysis
Owing to the high proportion of zeros in the sample and severe problems of over-
dispersion and model convergence, we were unable to conduct satisfactory parametric
analyses of the numbers of intact cysts or seeds in samples in relation to differences
between season, wader species or sample type (pellet or faeces). We therefore used non-
parametric Kruskal-Wallis and Mann-Whitney U tests employing Statistica 5.5 (StatSoft
1999).
We used generalized linear models (GLMs) following the GENMOD procedure
in SAS (v. 8.2, SAS Institute 2000) to analyze the effects of season, wader species,
sample type (faeces or pellet) and diet on the percentage of cysts in a sample that were
broken, and the percentage of intact cysts that hatched. All these variables were
included as fixed factors in the models. Diet was included as a factor of three levels
according to whether the majority of the sample was made up of soft items (e.g.
Chironomid larvae or Artemia), hard items (e.g. bivalve shells or grit) or items of
intermediate hardness (e.g. Coleoptera, Ephydridae larvae or polychaetes). We used a
normal error distribution and identity link, and a square root transformation for the
dependent variable to overcome heteroscedasticity. There were insufficient data to
conduct GLMs of the percentage of broken seeds, or of the percentage of intact seeds
that germinated. In order to test for a relationship between the proportion of cysts
broken or hatching and the total number of cysts in a sample, we conducted GLMs in
which the total number of cysts (log transformed) was included as an additional
predictor variable. The deviance of each fitted GLM model is analogous to the residual
sum of squares in ordinary linear regression. The reduction in deviance compared to the
null model is used to assess the contribution of the model to the explanation of the
variance in the data set. The significance of the reduction in deviance for the models of
cyst breakage or hatching was derived from F tests, scaled to control for over-dispersion
(Crawley 1993).
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
150
Artemia cysts ingested can potentially be those present in the sediments, those in
the water column, those forming floating masess on the surface or those situated in the
ovisac within female adults. In the latter case, a significant correlation would be
expected between the abundance of adult Artemia and of cysts in different samples. In
order to test for this, we calculated Spearman rank correlations between the abundance
of Artemia adults (using the seven volumetric categories defined above) and the total
number of cysts recorded in Redshank and godwit samples.
Wader counts and migration routes
In 12 different salt ponds representing 27.6 % of the 1174 ha of saltworks, we counted
the number of shorebirds of each species that were feeding and resting one day each
week throughout 2001, using a 20-60x telescope. On each day, we carried out a count of
three hours duration around high tide when the densities of waders are highest (Sánchez
et al. in press a). The ponds were always counted at about the same time of day and
always following the same route between ponds.
Since 1992 there has been an intensive ringing operation at the Odiel saltworks
coinciding with the autumn wader migration. A smaller number of birds have also been
ringed in a second locality in Huelva province, Doñana National Park (37°07'N
06°28'W) found 50 km from Odiel. We present details of recoveries to shed light on the
likely direction and distance of long-distance dispersal events.
RESULTS
Artemia cysts
Intact Artemia cysts were recorded in the droppings and/or pellets of all three wader
species and in all seasons except winter (Table 1). Cysts were most abundant in godwit
faeces in summer 2001, with an average of 222 cysts per dropping.. They were also very
abundant in Redshank pellet in autumn, with an average of 189 cysts per dropping . A
mean of 31 cysts were recorded in Spotted Redshank pellets in spring (Table 1).
Overall, 85.3 % of cysts (n = 57729) recorded in samples were intact.
For Redshank pellets, there were highly significant differences between seasons
in the number of intact cysts per sample (Kruskall-Wallis test, n = 211, H = 44.16, df =
2, p < 0.0001). Post-hoc tests showed that the number of cysts in spring was
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
151
significantly higher than in autumn (Mann-Whitney U test, U = 1247, p < 0.0001) and
in winter (U = 94.5, p < 0.0001) and higher in autumn than in winter (U = 1302, p =
0.021). The real difference between spring and autumn was in the proportion of pellets
containing cysts (χ21 = 34.7, P < 0.0001). For Redshank pellet samples with at least one
intact cyst, there was no difference in the number of cysts between spring (median =
5.5) and autumn (median = 3, U = 392.0, p = 0.95).
Amongst Redshank samples from autumn, the median number of intact cysts
was significantly higher in faecal samples than in pellets (U = 4997, p = 0.0001). In
contrast, the maximum and mean were higher in pellets (Table 1). Amongst spring
pellets, numbers transported by Redshank were higher than those transported by Spotted
Redshank, and the difference was marginally significant (U = 85.00, p = 0.051)
In an analysis of the proportion of cysts that were destroyed during gut passage,
there were no significant effects of season or sample type (Table 2). However, diet had
a highly significant effect, the proportion of cysts destroyed increasing with the
hardness of other food items in the sample (Table 2). With the proportion of cysts
destroyed (arcsine transformed) as the dependent variable and species, season, sample
type (pellet or faeces) and total number of cysts (log transformed) as predictor variables,
there was a negative and significant correlation between the number of cysts and the
proportion destroyed (F1,169 = 19.12, r = -0.35, P < 0.0001).
For both faecal and pellet samples, there was a strong relationship between the
total number of cysts recorded in each sample and the proportion of the volume of that
sample made up by Artemia adults (godwit faeces, rs = 0.783, P < 0.0001, n = 56;
Redshank faeces, rs = 0.424, P < 0.0001, n = 84). for Redshank pellets, rs = 0.237, P <
0.0001, n = 211).
The viability of intact cysts was determined for a smaller number of samples.
Viability was confirmed for samples from all three wader species, and for samples
collected in spring, summer or autumn (Table 3). Viability was highest for Redshank
pellets in autumn, with an average of 19% of cysts in each sample hatching (Table 3).
There were no significant differences between wader species or seasons in the
proportion of cysts hatching, but there was a significant effect of sample type, with a
higher proportion of cysts hatching in Redshank pellets than in Redshank droppings
(Table 2). The partial effect of sample type remained significant when diet was added to
the model of Table 2 (F 1, 65 = 4.84, P = 0.031 ), but diet had no influence on the
proportion of cysts hatching (F2, 65 = 0.79, P = 0.46). Likewise, for godwit droppings
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
152
there was no correlation between the proportion of cysts hatching and diet hardness (n =
41, rs = -0.255, P = 0.11).
With the proportion of cysts hatching as the dependent variable and species,
season, sample type and total number of cysts as predictor variables, there was a
negative but non-significant correlation between the number of cysts and the proportion
hatching (F1, 67 = 0.83, r =-0.11, P = 0.37).
Seeds
Intact angiosperm seeds were recorded in the droppings and/or pellets of all three wader
species and in all seasons (Table 4). Overall, they were recorded in 21.8 % of samples
with 3.19 ± 0.94 intact seeds per sample (mean ± s.e. for those samples with at least one
seed, n = 90). In total, 74.2 % of all seeds recorded were intact (Table 4).
A total of 14 seed species were recorded. The Slender-leaved Iceplant
Mesembryanthemum nodiflorum L. (Aizoaceae) was particularly abundant in Redshank
faeces in autumn. The Common Sowthistle Sonchus oleraceus L. (Asteraceae) was
particularly abundant in spring pellets of Redshank and Spotted Redshank.
Arthrocnemum macrostachyum (Moric.) K.Koch (Chenopodiaceae) was the only
species recorded in samples from all wader species (Table 4). All three plant species are
abundant on the dykes of Odiel salt pans. Other intact seeds recorded were Suaeda spp.
(1 seed), Salicornia spp. (2 seeds) and 9 unidentified taxa (one seed of each).
The maximum number of intact seeds in one sample was 83 S. oleraceus seeds
in a Redshank pellet collected on 18/3/01 (Table 4). There were highly significant
differences between seasons in the abundance of intact S. oleraceus seeds in Redshank
pellets (Kruskal-Wallis test, H = 68.22, 2df, n = 211, p < 0.0001). They were only
recorded in spring, when they were significantly more abundant than autumn (Mann-
Whitney U test, U = 1648.5, p < 0.0001) or winter (U = 220.5, p = 0.0021). A similar
and marginally significant seasonal trend was recorded in the abundance of intact A.
macrostachyum seeds (H = 5.82, 2 df, p = 0.055). In autumn, intact M. nodiflorum seeds
were significantly more abundant in Redshank faeces than in their pellets (Mann-
Whitney U test, U = 5654, p < 0.0001). There were no significant differences in the
abundances of intact seeds of the three species between spring pellets of Redshank or
Spotted Redshank (Mann-Whitney U tests, P > 0.5).
The proportion of all seeds that were intact was 41.0 % for A. macrostachyum,
54.3 % for M. nodiflorum and 84.3 % for S. oleraceus (Table 4). There were insufficient
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
153
data to allow multivariate analyses of differences in the proportion of seeds broken
between wader species or seasons, or of the relationship between the numbers of seeds
in a given sample and the proportion broken.
Overall, 45.5 % of A. macrostachyum, 23.5 % of M. nodiflorum and 76.3 % of S.
oleraceus seeds germinated (Table 5). One unidentified seed also germinated. Amongst
autumn Redshank samples, M. nodiflorum seeds from pellets were significantly more
likely to germinate than those from faeces (Fisher exact test, p= 0.0385, selecting one
seed at random from three samples with more than one seed to avoid pseudoreplication).
Wader abundance and migration routes
Wader species differed in their phenology during migration through the Odiel marshes
(Fig. 2). Redshank had a smaller peak during spring migration in April, and a larger one
between July and October during autumn migration. Spotted Redshank numbers peaked
in October with a lower peak in April. Godwit peaked from July to August at the
beginning of autumn migration.
Ringing recoveries show that Redshank and godwit stopping at the Odiel
marshes share a common flyway and come from as far north as Sweden (Fig. 1). Colour
ringed birds from the Icelandic breeding population of Black-tailed godwit have also
been recorded at Odiel (T. Gunnarsson pers. comm.). There were 70 recoveries of
Redshank ringed at Odiel, 60 from the Odiel marshes, 5 from the Netherlands, 1 from
Belgium, 3 from France and one from Sweden. There were three recoveries of godwits
from the Netherlands. From birds ringed elsewhere in Huelva province, there were six
recoveries of Redshank, three from France, one from Portugal, one from Germany and
one from the Netherlands. There were five recoveries of godwits, one from Germany,
three from the Netherlands and one from Seville. There were no recoveries of Spotted
Redshank.
DISCUSSION
We have found Black-tailed Godwits, Redshank and Spotted Redshank to be effective
dispersers of A. parthenogenetica and three plant species at the Odiel marshes, where
thousands of waders pass through on migration, especially in autumn (Fig. 2) when on
their way to winter in West Africa (Wetlands International 2002, Stroud et al. 2004). The
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
154
East Atlantic Flyway, used by an estimated 15.5 million shorebirds (including 440,000
Redshank, 200,000 Black-tailed Godwit, and 50,000 Spotted Redshank, Stroud et al.
2004), is likely to be a major means of long-distance dispersal of plants and
invertebrates. Artemia cysts and seeds are also likely to be transported internally by some
of the other 24 migratory shorebird species using the East Atlantic Flyway (Stroud et al.
2004), as well as by other birds that use salt pans (Green et al. 2002). Viable cysts and
seeds are also likely to be transported externally on the feathers and feet of waterbirds
(Figuerola & Green 2002b).
The birds we studied included a mixture of birds that had just completed or were
just about to commence long-distance movements, and birds that were making
movements between feeding and roosting sites within our study sites. The average time
spent by shorebirds at stopover sites during migration varies from one to 50 days and is
unknown for sites in south-west Iberia (Hortas 1997). One of two icelandic godwits
seen at Odiel on autumn migration was still there 36 days later (T. G. Gunnarsson, J. A.
Gill & P. M. Potts, unpublished data). Most of the propagules transported in faeces or
pellets by waders at Odiel are likely to be transported short distances of less than 10 km,
and it is currently impossible to assess what proportion would undergo long-distance
dispersal. Godwits and other shorebirds regularly move between saltpans and other
wetlands separated by up to 20 km while at stopover sites (Farmer & Parent 1997, P.M.
Potts, pers. comm.), thus facilitating propagule dispersal between different parts of a
wetland complex. Most major passage and wintering sites on the East Atlantic Flyway
contain saltmarshes and/or saltworks, facilitating the long distance dispersal of Artemia
and plants.
Shorebirds move rapidly between coastal wetlands, and distances between
stopovers can easily exceed 1000 km (Iverson et al. 1996, Pennycuick & Battley 2003).
Black-tailed Godwits, Redshank and other waders are thought to fly non-stop between
Odiel and northern Europe (Beintema & Drost 1986). Redshank and godwits fly at 56-60
km h-1 (Welham 1994). In a laboratory study, the modal retention time (much less than
the mean) of viable Artemia cysts defecated by another shorebird, the Killdeer
Charadrius vociferus (size intermediate between redshank and godwit), was 90 min,
and the maximum was 26 h (Proctor et al. 1967). This suggests that, during migration,
the maximum dispersal distance of viable cysts would be c.1500 km. Laboratory studies
of gut passage of intact seeds suggests that they may be transported even longer
distances. In a study of 13 seed and three wader species, maximum retention time varied
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
155
from 3 h to 14 days (Proctor 1968). There is evidence that species such as godwits that
do not regurgitate compacted pellets from the gizzard can regurgitate seeds on their own
from the gizzard after extraordinary intervals (Proctor 1968). The modal retention time
of Amaranthus and Sagittaria seeds defecated by Killdeer was found to be 1-2 h
(deVlaming & Proctor 1968).
In a previous study at Cadiz Bay and Castro Marim in the south-west of the
Iberian peninsula during autumn migration, Redshank were shown to disperse A.
parthenogenetica, and Black-tailed Godwits and Redshank were both shown to be
effective dispersers of the alien A. franciscana (Green et al. 2005). However, ours is the
first study to demonstrate Artemia dispersal by waterbirds during spring migration.
Although the number of Artemia cysts per sample was higher at Odiel, their viability was
lower than at Cadiz Bay and Castro Marim. This is probably a consequence of the longer
storage time of our samples between collection in the field and hatching (up to 15 months)
which is likely to have reduced viability. A noteable contradiction between these two
studies is that Green et al. (2005) found that the proportion of cysts hatching was higher
for Redshank faeces than for pellets, whereas we found the opposite. Both results were
weakly significant, illustrating the noise and variation in space and time that can be
observed when studying dispersal in the field. Cysts in pellets do not necessarily have the
same origin as those in faeces (e.g. cysts consumed within female Artemia and those
ingested separately may be processed differently), and this may potentially explain
differences in viability. Whereas the mode of ingestion of Artemia cysts has previously
been open to speculation (Green et al. 2005), we found strong evidence that most cysts
recorded in faeces or pellets were ingested within adult females. The absence of cysts
from winter pellets is consistent with such a pattern. Cyst production peaks in spring
and summer and Artemia adults almost disappear in winter, although cysts remain
reasonably abundant in the water column and in the sediments (Martínez 1989, authors
unpublished data). Studies in captivity (Horne 1966, Charalambidou et al. in press)
suggest that gut passage itself does not affect the viability of those A. franciscana cysts that
survive intact, but their viability was reduced by gut passage in flamingos when they were
mixed with sand (MacDonald 1980).
It has often been suggested that dietary variation is likely to influence the
survival rates of propagules ingested by different bird species or individuals (e.g.
Figuerola & Green 2002a), but ours is the first field study to show that diet influences
the survival rate of ingested invertebrate propagules. We found that Artemia cyst
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
156
survival was directly related to the hardness of food items, but other aspects are also
likely to be important. Charalambidou et al. (in press) found that survival of A.
franciscana cysts following gut passage through Mallards Anas platyrhnchos was lower
for birds fed on animal-based pellets than those fed on grains, and suggested that this was
due to higher concentrations of enzymes for digesting animal matter. We also found that,
as the number of cysts in a sample increased, the proportion that were destroyed
decreased. This indicates a positive relationship between the quantity and quality
components (sensu Schupp 1993) of dispersal in this system, with individuals that
consummed more cysts expelling a higher proportion of viable cysts. Such a
relationship has also been reported for seed dispersal by waterfowl (Figuerola et al.
2002a).
We found that M. nodiflorum seeds and Artemia cysts were more abundant in
faeces than in pellets. This is likely to further long distance dispersal, as propagules are
likely to be retained longer when expelled in faeces rather than in pellets (Nogales et al.
2001). In contrast, M. nodiflorum seeds extracted from pellets were more likely to
germinate. This is evidence that longer retention times involved in passage through the
intestines reduces viability. However, Nogales et al. (2001) found no difference in the
viability of seeds extracted from pellets or droppings of gulls.
Ours is the first field study to demonstrate transport of viable angiosperm seeds
by waders. Overall, we recorded seeds (whether intact or not) in 22% of our samples.
This is lower than the frequency of seeds recorded in faeces or pellets for most species
of waders wintering in Cadiz Bay (Pérez-Hurtado et al. 1997). The abundance of seeds
recorded in many other studies of wader diet (Green et al. 2002, Montaltil et al. 2003)
suggests that waders play a widespread and important role in the dispersal of many plant
species. Darwin (1859) recognised that dispersal of propagules by migratory birds such
as waders plays a vital role in explaining the distribution of species. However, he
underestimated the capacity of seeds lacking a fleshy fruit to survive passage through
the digestive tract, and imagined that long-distance dispersal by internal transport may
require a role for birds of prey in extracting seeds from a bird’s crop before they enter
the gizzard. Our study shows that waders can disperse seeds over great distances
without the need for such rare predation events.
The native distribution of dispersed species included in this study
(Triantaphyliidis et al. 1998, Tutin et al. 2001) is consistent with a role of long-distance
dispersal by waders to and from sites such as the Odiel marshes. S. oleraceus seeds
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
157
were transported more readily in spring, coinciding with the timing of seed production
(Valdés et al. 1987). Taking into account the frequencies of viable propagules recorded
in different seasons, and the greater numbers of birds moving through the Odiel
saltworks at different times, our data suggest that there should be greater long distance
dispersal of S. oleraceus seeds northwards from Odiel, and greater dispersal of M.
nodiflorum and A. macrostachyum seeds in a southerly direction. S. oleraceus is
widespread across the range of ringing recoveries (Fig. 1) as far north as Sweden. It has
also been recorded in Iceland where it is considered an alien (A. Gardarsson, pers.
comm.), and is native down to southern Africa which is visited by some Redshank and
other waders breeding in Europe (Wetlands International 2002). M. nodiflorum is
considered a Mediterranean species but is also native in southern Africa. A.
macrostachyum is native across the Mediterranean and down to Mauritania, a major
wintering ground for waders passing through Odiel (Stroud et al. 2004).
Parthenogenetic brine shrimp populations are native down to South Africa and
up to North-west France (Triantaphyliidis et al. 1998). It is difficult to predict what
directionality there may be in effective dispersal of A. parthenogenetica cysts by
waders, as whilst they were present in a higher proportion of Redshank pellets in spring
(76%) than in autumn (30%), there were many more Redshank and godwits passing
through Odiel on autumn migration. Godwit samples from the beginning of the
southwards migration period had the most cysts. Stopover times and the probabilities
that waders move between suitable habitats for the dispersed species are likely to differ
between spring and autumn migration, and to vary between wader species, but there are
currently no data on this issue. Furthermore, there are some wader species at Odiel
(Dunlin Calidris alpina and Little stint Calidris minuta) that are much more abundant
during spring than autumn migration, and it is possible that these species are also good
dispersers of plants or Artemia.
S. oleraceus and M. nodiflorum are also widespread invasive exotics in the
Americas, Australia and in Pacific Islands (Villaseñor et al. 2004,
http://plants.usda.gov). Our study suggests that dispersal by waders and other migratory
birds may play a previously unrecognised role in the spread of these invasive weeds. S.
oleraceus seeds have been recorded in bird droppings in the introduced range (McGrath
& Bass 1999). However, S. oleraceus is generally assumed to be a wind-dispersed
species (Jakobsson & Eriksson 2003). Our study support the proposal of Higgins et al.
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
158
(2003) that birds can sometimes be the main means of long-distance dispersal for seeds
that appear morphologically adapted for wind dispersal.
In summary dispersal via waders is likely to have a significant role in the
distribution and metapopulation biology of plants and aquatic invertebrates. More
detailed studies are required before the true significance of this dispersal can be
established and compared to that of other vectors such as wind, water or man. In
particular, more data are required on the role of wader species not included in this study,
and on the probabilities that propagules are dispersed to suitable habitats (see Nathan et
al. 2003, Green & Figuerola 2005 for further discussion).
ACKNOWLEDGEMENTS
The first author was supported by a phd grant from the Ministerio de Ciencia y
Tecnología and an I3P postgraduate grant from the Consejo Superior de Investigaciones
Científicas. Consejería de Medio Ambiente, Junta de Andalucía and Aragonesas
Industrias y Energía S.A. provided permission to work in the salines. J.C. Rubio
provided logistical support and advice. P. García Murillo helped to identify the plants.
F. Palomares helped with field work. J. Elmberg helped with a literature search. J.
Figuerola provided valuable comments on the manuscript. Ringing data were provided
by the Oficina de Especies Migratorias, Ministerio de Medio Ambiente.
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Table 1. Number of samples with Artemia cysts, number of intact cysts per sample and
proportion of cysts that were broken. Each sample contained only a small fraction of the
cysts excreted in a 24 h period by a given bird.
Nº intact cysts per sample_______________________
% broken cysts________________
n With cysts With intact cysts mean ± se range mean ± se rangeTringa totanus drop. Aut-01 84 51 38 98.1 ± 49.4 (0, 3339) 41.2 ± 5.5 (0, 100)
pell. Spr-01 33 25 24 50.7 ± 36.3 (0, 1187) 14.8 ± 5.9 (0, 100)Aut-01 157 48 33 189.3 ± 105.0 (0, 15445) 41.1 ± 6.3 (0, 100)Win-01 21 0 0 0 ± 0 (0, 0) - -
Limosa limosa drop. Sum-01 42 41 41 221.6 ± 35.4 (0, 980) 0 (0, 0)Sum-02 14 5 3 0.3 ± 0.2 (0, 2) 40 ± 24.5 (0, 100)
Tringa erythropus pell. Spr-01 9 5 3 31.4 ± 31.1 (0, 280) 40 ± 24.5 (0, 100)Total 360 175 142 136.8 ± 47.6 (0, 15445) 27.7 ± 3.0 (0, 100)
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Table 2. Generalized linear models of the effects of season, sample type and diet on the
proportion of Artemia cysts that were broken and the proportion of intact cysts that
hatched in samples from godwits and Redshank. The dependent variable was arcsine
transformed, and an identity link and normal error distribution were used. Summer
(godwit) samples, faecal samples and diet of medium hardness were aliased. Spring and
autumn samples were from Redshank. Samples from spotted redshank were excluded
from the models owing to lack of data.
Effect Estimate SE DFN DFD F P% Broken cysts Constant 0.43 0.13 N = 170 Season 1 164 0.45 0.5018D = 27.23 Autumn 0.19 0.12
Spring 0.10 0.17Summer 0 -Sample type 1 164 0.83 0.3648faeces 0 -pellet -0.10 0.11Diet 2 164 13.29 < 0.0001soft -0.38 0.11medium 0 -hard 0.35 0.12
% Cysts hatching Constant 0.07 0.04 N = 71 Season 1 67 1.94 0.1681D = 10.00 Autumn -0.03 0.08
Spring -0.31 0.22Summer 0 -Sample type 1 67 5.50 0.022Faeces 0 -
pellet 0.24 0.10
D = percentage of deviance explained by the final model compared to the null model.
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
165
Table 3. Number of Artemia nauplii hatched and the proportion of cysts that hatched.
Sample sizes are lower than in Table 1 because not all samples were stored in such a
way as to conserve viable cysts.
Nº nauplii per sample* % cysts hatching ________________ ____________ Nº of samples With intact cysts With nauplii mean ± se range mean ± se rangeTringa totanus drop. Aut-01 58 14 3 0.4 ± 0.2 (0, 3) 3.9 ± 3.5 (0, 50)
pell. Spr-01 5 2 0 0 0 0 0Aut-01 133 13 6 3 ± 1.6 (1, 16) 19.2 ± 10.1 (0, 100)Win-01 21 0 0
Limosa limosa drop. Sum-01 42 41 26 9.7 ± 2.3 (0, 70) 7.4 ± 1.6 (0, 40)Sum-02 14 0 0
Tringa erythropus pell. Spr-01 9 2 1 2 ± 2 (0, 4) 2.3 ± 2.3 (0, 4.6)Total 282 72 36 8.5 ± 1.4 (0, 70) 8.5 ± 2.2 (0, 100)
* For samples with at least one intact cyst. A total of 304 adult Artemia were reared
from nauplii and all were diploid A. parthenogenetica.
Table 4. Abundance of A. macrostachyum, M. nodiflorum, S. oleraceus and other unidentified seeds in wader droppings and pellets from the
Odiel saltpans, listing the numbers of samples with seeds (including those broken) and intact seeds. The total number of seeds in those samples
are given in parentheses. Each sample contains only a small fraction of the seeds excreted in a 24 h period by a given bird.
A. macrostachyum
_____________M. nodiflorum____________
S. oleraceus____________
Others____________
Total______________
N Seeds Intact Seeds Intact Seeds Intact Seeds Intact Seeds IntactTringa totanus drop. Aut-01 84 3 (3) 2 (2) 22 (29) 13 (16) 1 (1) 1 (1) 2 (2) 2 (2) 25 (35) 16 (21)
pell. Spr-01 33 5 (10) 3 (4) 1 (2) 1 (2) 12 (155) 12 (144) 0 (0) 0 (0) 16 (167) 15 (150)Aut-01 157 6 (7) 3 (3) 2 (2) 2 (2) 0 (0) 0 (0) 8 (7) 7 (8) 15 (16) 12 (13)Win-01 21 2 (1) 0 (0) 2 (2) 1 (1) 0 (0) 0 (0) 1 (1) 0 (0) 5 (4) 1 (1)
Limosa limosa drop. Sum-01 42 2 (2) 1 (1) 0 (0) 0 (0) 0 (0) 0 (0) 1 (1) 0 (0) 3 (3) 1 (1)drop. Sum-02 14 1 (1) 0 (0) 0 (0) 0 (0) 1 (1) 0 (0) 1 (1) 0 (0) 2 (3) 0 (0)
Tringa erythropus pell. Spr-01 9 4 (6) 2 (2) 0 (0) 0 (0) 6 (10) 5 (7) 0 (0) 0 (0) 6 (16) 5 (9)Tringa spp. pell. Spr-03 52 5 (8) 4 (4) 0 (0) 0 (0) 15 (31) 8 (13) 1 (1) 1 (1) 18 (40) 12 (18)Total 412 28 (38) 15 (16) 27 (35) 17 (21) 35 (198) 26 (165) 14 (13) 10 (11) 90 (284) 62 (213)
167
Table 5. Germination of A. macrostachyum, M. nodiflorum, S. oleraceus and other unidentified seeds in wader droppings and pellets from the
Odiel saltpans, listing numbers of samples with intact seeds placed for germination, and with at least one seed germinating. The total numbers of
seeds involved are listed in parentheses. Sample sizes are lower than Table 4 because not all samples were stored so to conserve viable seeds.
A. macrostachyum
______________M. nodiflorum
______________S. oleraceus
______________Others
_____________Total
_______________N Intact Germinated Intact Germinated Intact Germinated Intact Germinated Intact Germinated
Tringa totanus drop. Aut-01 84 1 (1) 1 (1) 11 (14) 1 (1) 0 0 0 0 12 (15) 2 (2)pell. Spr-01 33 2 (2) 0 0 0 11 (60) 11 (54) 0 0 13 (62) 11 (54)
Aut-01 157 2 (2) 1 (1) 2 (2) 2 (2) 0 0 3 (3) 0 7 (7) 3 (3)Win-01 21 0 0 1 (1) 1 (1) 0 0 0 0 1 (1) 1 (1)
Limosa limosa drop. Sum-01 42 0 0 0 0 0 0 0 0 0 0drop. Sum-02 14 0 0 0 0 0 0 0 0 0 0
Tringa erythropus pell. Spr-01 9 2 (2) 1 (1) 0 0 5 (7) 3 (4) 0 0 5 (9) 3 (5)Tringa spp. pell. Spr-03 52 4 (4) 2 (2) 0 0 8 (13) 8 (13) 1 (1) 1 (1) 12 (18) 11 (16)Total 412 11 (11) 5 (5) 14 (17) 4 (4) 24 (80) 22 (71) 4 (4) 1 (1) 50 (112) 31 (81)
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
168
Figure 1. Distribution of recoveries of Redshank and Black-tailed Godwit ringed at the
Odiel marshes and adjacent parts of Huelva province from 1992 to 2003, with recovery
distances. Local recoveries are not shown. In total, there were 16 recoveries of
Redshank and seven of godwits from outside Spain (see text).
0 500 1000 Km
1
4
6 7 8 109 12
16
1. Odiel Marshes2. Los Palacios (Seville): 54 Km3. Algarve (Portugal): 133 Km4. Charente Maritime (France): 1065
Km5. Vendeé (France): 1136 Km6. Somme (France): 1605 Km7. Pas de Calais (France): 1605 Km8. West-Vlaanderen (Belgium): 1703
Km9. Zeeland (Holland): 1809 Km10. Gelderland (Holland): 1921 Km11. Overijssel (Holland): 1947 Km12. Noord-Holland (Holland): 1964 Km13. Griend (Holland): 2009 Km14. Hannover (Germany): 2100 Km15. Schleswig-Holstein (Germany): 2272
Km
3
5
1113
1415
2
0ºW 10ºW 20ºW 30ºW
35ºN
50ºN
45ºN
40ºN
55ºN
60ºN
Tringa totanusLimosa limosaT. totanus and L. limosa
CHAPTER 6 PROPAGULE DISPERSAL BY WADERS
169
Figure 2. Seasonal fluctuations in the abundance of waders at the Odiel saltpans in
2001. Numbers shown represent counts at high tide in 27.6 % of the total area of
saltpans.
Tringa erythropus
Months
Ja Fe Ma Ap My Jn Jl Au Se Oc No De0
50
100
150
200
250
300
Limosa limosa
1000
2000
3000
4000
5000
6000
Tringa totanus
200
400
600
800
1000
1200
1400
1600
1800
2000N
º of s
hore
bird
s
170
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
171
CHAPTER 7
DISPERSAL OF INVASIVE AND NATIVE BRINE SHRIMPS ARTEMIA
(ANOSTRACA) VIA WATERBIRDS
ANDY J. GREEN1,5, MARTA I. SÁNCHEZ1,2, FRANCISCO AMAT3, JORDI
FIGUEROLA1, FRANCISCO HONTORIA3, OLGA RUIZ3, FRANCISCO
HORTAS4
1Estación Biológica de Doñana, Avda. María Luisa s/n, 41013 Sevilla, Spain2Departamento de Biología Ambiental y Salud Pública, Universidad de Huelva, Avda Fuerzas Armadas
s/n, 21071 Huelva, Spain3Instituto de Acuicultura de Torre de la Sal, 12595 Ribera de Cabanes, Spain
4Departamento de Biología, Universidad de Cadiz, Apartado 40, 11510 Puerto Real, Spain
Key words: Artemia franciscana, Artemia parthenogenetica, cysts viability, waders,
dispersal
Running head: Dispersal of brine shrimps via birds.
Limnology and Oceanography, 50 (2): 737-742.
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
172
ABSTRACT
North American brine shrimps Artemia franciscana have been exported worldwide
since the 1950s for use in the aquarium trade and fish farming. Aquaculture is
expanding along the Mediterranean coast, leading to the release of A. franciscana into
native Artemia populations. A. franciscana was first detected in 1981 in Portugal, and
has since spread to saltworks along the East Atlantic flyway used by shorebirds. Once
A. franciscana becomes established in a locality, native Artemia tend to disappear. To
test whether migratory shorebirds can disperse invasive and native Artemia between
wetlands, we extracted Artemia cysts from faeces and pellets collected at Castro Marim
(Portugal) and Cadiz Bay (Spain) during southwards migration. We found that large
numbers of viable eggs of A. franciscana and native A. parthenogenetica were dispersed
by Redshank Tringa totanus, Black-tailed Godwit Limosa limosa, and other shorebirds
migrating through the Iberian Peninsula. This is the most extensive field demonstration
to date that invertebrates can disperse readily via gut passage through birds.
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
173
INTRODUCTION
Invasion by non-native species is second only to habitat loss as a threat to global
biodiversity, has a huge economic impact, and has had its greatest impact in aquatic
ecosystems (Ruiz et al. 1999, Mooney & Cleland 2001). Non-native aquatic
invertebrates are typically moved between continents by man, e.g., in the ballast of
ships or intentionally for aquaculture or fisheries purposes (Leppäkoski et al. 2002,
Bailey et al. 2003). Once established, they are generally assumed to disperse using their
own active mechanisms, via ocean or river currents, or via intraregional boat traffic
(Wasson et al. 2001). The role of migratory birds in spreading exotic invertebrates has
not been fully assessed, despite the importance of understanding the dispersal
mechanisms of invasive species so that their spread can be predicted. Some authors
reviewing dispersal mechanisms of aquatic invasives have made no mention of a
potential role for birds (Leppäkoski et al. 2002).
Darwin attributed much importance to the role of migratory waterbirds as
dispersers of invertebrates ("The wide distribution of fresh-water plants and of the lower
animals I believe mainly depends on the wide dispersal of their seeds and eggs by
animals, more especially by fresh-water birds, which have great powers of flight, and
naturally travel from one piece of water to another", Darwin 1859). He suggested that
shorebirds have a particularly important role, and proposed that alien snails extended
their range by dispersing on the feathers or feet of birds (Darwin 1859). Various
laboratory studies have since demonstrated that propagules can survive passage through
the digestive system (Figuerola & Green 2002a). However, few studies have
demonstrated such dispersal in the field (Proctor 1964, Figuerola & Green 2002a).
Owing to similar morphology, until the 1980s all populations of brine shrimps
Artemia (Crustacea, Anostraca) were considered strains of a single species, but six
sexual species are now recognised together with a heterogeneous group of
parthenogenetic populations under the binomen A. parthenogenetica (Abatzopoulos et
al. 2002). The sexual A. franciscana is widespread in the Americas. In the
Mediterranean region, the native species are the sexual A. salina (formerly A. tunisiana)
together with A. parthenogenetica (mainly diploid and tetraploid populations,
Abatzopoulos et al. 2002). Since the 1950s, A. franciscana cysts have been
commercially exported worldwide from San Francisco Bay and Great Salt Lake, U.S.A.
for use in aquaculture and in the aquarium and pet trade (Abatzopoulos et al. 2002). In
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
174
the Mediterranean region, many traditional saltworks where salt production has become
unprofitable are being transformed into aquaculture facilities, leading to the release of
A. franciscana into hatcheries and its escape into habitats with native Artemia
populations (Amat et al. 2004). Given its use in the pet trade and even microscope sets,
indiscriminate releases into other saline wetlands suitable for Artemia are also possible.
Between 1993 and 2003, Artemia cysts (resting eggs) from numerous saltworks in the
West Mediterranean were collected and their species composition determined (Amat et
al. 2004, authors unpubl.). By then, A. franciscana was the only species recorded in
Portugal, where it is found in areas both with and without aquaculture. It is also found in
Cadiz Bay (Spain), two French sites and one in Morocco. A. franciscana was first
detected in 1981 in the Portuguese Algarve (Amat et al. 2004) and has since spread to
all the Iberian sites considered to be most important for shorebirds along the East
Atlantic Flyway: Tejo, Aveiro, Faro and Sado in Portugal and Cadiz Bay (Boyd & Pirot
1989, Amat et al. 2004). To date, there has been no spread detected to the many
saltworks east of Gibraltar outside the flyway (Fig. 1). At Aveiro, only A.
parthenogenetica was recorded in 1985, but by 1991, it had been replaced by A.
franciscana.
In this study, we assessed the ability of shorebirds (the most abundant waterbirds
in coastal saltworks) to disperse A. franciscana and A. parthenogenetica by sampling
two areas where A. franciscana has been recorded: Castro Marim (Portugal, 37°12'N
07°26'W) and Cadiz Bay (36°27'N 06°11'W). Both are situated on the Atlantic coast of the
south-western part of the Iberian Peninsula (Fig. 1) and are listed as wetlands of
international importance under the Ramsar Convention
(http://www.wetlands.org/RSDB/default.htm). Both sites hold saltworks and tens of
thousands of shorebirds during migration periods (Hortas 1997).
MATERIALS AND METHODS
We collected fresh faeces and pellets from roost sites used by monospecific flocks in
saltworks at Castro Marim on 23 July and Cadiz Bay from 22 July to 03 August 2002.
Several shorebirds, including the Redshank Tringa totanus, regurgitate pellets after
digestion. The dates of sampling coincided with the beginning of the southwards
(autumn) shorebird migration (Hortas 1997). Each sample of faeces or pellet was
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
175
carefully separated from the soil (discarding that part in contact with soil) and placed in
a tube. Given the number of birds present and the freshness of the samples, we are
confident that each sample was from a different bird. The samples were stored at 5oC,
and within a month, Artemia cysts were extracted by washing them in a 0.04 mm sieve
and resuspension in hypersaline brine, in which intact cysts float. The cysts were
counted, washed in distilled water then dried for 48 h at 40oC. These cysts were then
incubated in diluted filtered sea water (25 g L -1) at 26ºC and under continuous
illumination for 48 h. Hatched nauplii were counted and transferred into 60 cm3 vessels
and cultured in 70 g L -1 filtered brine (seawater plus crude sea salt), on a diet of live
Dunaliella salina and Tetraselmis suecica. They were maintained at 24ºC, under
aeration on a 12D:12L photoperiod. The medium was monitored and renewed every two
days. Resulting adults were identified morphologically (Amat et al. 2004).
We also collected thousands of cysts from saltpans adjacent to sites where we
collected faeces, determining hatching success, culturing adults and identifying them in
the same way as for cysts extracted from faeces. We also established hatching success
of A. parthenogenetica cysts collected in January 2002 from saltworks at Sanlúcar de
Barrameda (36°50'N 06°20'W), 30 km from Cadiz Bay.
The numbers of cysts transported and their hatchability were compared between
bird species, between localities, and between faeces and pellets using non-parametric
Mann-Whitney U-tests. Initial attempts to use parametric statistics were abandoned owing
to overdispersion and the high proportion of zeros in the data.
RESULTS
In both localities, we found all shorebird species studied to be transporting viable Artemia
cysts during autumn migration (Tables 1,2). At Castro Marim, Redshank and Black-tailed
Godwit Limosa limosa were transporting large numbers of viable A. franciscana cysts, and
a small number of A. parthenogenetica. At Cadiz Bay, Redshank and Dunlin Calidris
alpina were transporting viable A. parthenogenetica cysts, with the occasional presence of
A. franciscana.
At Castro Marim, Redshank faeces held more Artemia cysts than Redshank pellets
(Mann-Whitney U-tests, n = 36, 31, U = 250, p = 0.0001) or godwit faeces (n = 36, 30, U
= 161, p < 0.0001). The proportion of cysts that hatched was also higher for Redshank
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
176
faeces than for godwit faeces (n = 36, 27, U = 142.5, p < 0.0001) or Redshank pellets (n =
36, 30, U = 379.5, p = 0.039). Numbers of cysts recorded at Cadiz Bay were fewer than the
number at Castro Marim for Redshank pellets (n = 31, 55, U = 141.5, p < 0.0001), but the
proportion of cysts that hatched was higher at Cadiz Bay (n = 30, 25, U = 101, p < 0.0001).
However, the total number of viable cysts transported per pellet was more than five times
higher for A. franciscana in Castro Marim than for A. parthenogenetica in Cadiz Bay.
Amongst cyst samples taken directly from saltpans, we found 100% A.
franciscana at both Castro Marim and Cadiz Bay. Hatching success of A. franciscana at
Castro Marim was 74.1% (n = 17,400). Hatching success of A. parthenogenetica at
Sanlúcar de Barrameda was 50.2% (n = 15,200).
DISCUSSION
Redshank and godwits were effective dispersers of A. franciscana. Thousands of
individuals of both species migrate through each of our study sites, and move thousands of
kilometres between breeding and wintering sites (Hortas 1997). An estimated 15.5 million
shorebirds (including 440,000 Redshank, 200,000 Black-tailed Godwit, and 2,340,000
Dunlin) migrate through the East Atlantic Flyway (Stroud et al. 2004), where most major
passage and wintering sites contain saltworks. Banding data shows that some birds stop
at more than one saltwork complex as they migrate along the Iberian Atlantic coast
(details available from first author).
The birds we studied included a mixture of birds that had just completed or were
just about to commence long-distance movements, and birds that were making
movements between feeding and roosting sites within our study sites. The average time
spent by shorebirds at stopover sites during migration is unknown for our study sites,
making it impossible to assess what proportion of the cysts extracted from faeces or
pellets were transported from long distances. However, the poor match between the
species composition of Artemia cysts extracted and those from adjacent saltpans shows
that the birds were transporting cysts between different parts of wetland complexes.
Redshank, godwits and other shorebirds regularly move between saltpans separated by
up to 20 km within stopover sites (Potts, P. M., pers. comm.), favouring rapid Artemia
dispersal within and between nearby saltworks. Dominance of A. parthenogenetica in
bird samples from Cadiz (Table 1) probably reflects feeding in saltpans that had been
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
177
dry since A. franciscana invaded, allowing native Artemia to hatch from cysts in
sediments upon reflooding (cysts can remain viable for decades in sediments,
Abatzopoulos et al. 2002). There are hundreds of pans in Cadiz Bay, and it was not
possible to know exactly where the birds had been feeding when we collected faeces.
Redshank and godwits fly at 56-60 km h-1 (Welham 1994). In a laboratory study, the
modal retention time (much less than the mean) of viable A. franciscana cysts defecated
by another shorebird, the Killdeer Charadrius vociferus (size intermediate between
redshank and godwit), was found to be 90 min, and the maximum was 26 h (Proctor et
al. 1967). This suggests that, during migration, the maximum dispersal distance of
viable cysts would be c.1500 km. Studies of gut passage of viable A. franciscana cysts
in other birds suggests that the maximum retention time increases with body size,
ranging from 3 h in a canary Serinus canarius to at least 38 h in a Shelduck Tadorna
tadorna (Proctor 1964, MacDonald 1980).
Radio and satellite tracking shows that shorebirds move rapidly between coastal
wetlands, and distances between stopovers can exceed 1000 km (Iverson et al. 1996). A.
franciscana cysts are also likely to be transported internally by some of the other 24
migratory shorebird species using the East Atlantic Flyway (Stroud et al. 2004), as well
as other birds that consume Artemia and move frequently between wetlands. Artemia cysts
are consumed by Greater Flamingos Phoenicopterus ruber and Shelduck in the wild
(MacDonald 1980). Viable cysts are also likely to be transported externally on the feathers
and feet of waterbirds (Figuerola & Green 2002b). We do not expect that such dispersal
processes are restricted to these study sites or to autumn migration. In a study of Redshank
diet at the Odiel marshes in Spain (37°17'N 06°55'W), cysts were similarly abundant in
pellets in both spring and autumn migration (Sánchez et al. in press).
We observed much variation between waterbird species and localities in the
number of intact Artemia cysts transported, and in their viability (Tables 1, 2). This
variation is likely to be related to differences between bird populations in habitat use, diet,
gut morphology and/or retention time (Figuerola & Green 2002a). Faeces of both
Redshank and godwits contained remains of adult Artemia, and they are likely to ingest
cysts that are still inside adult Artemia (some of which may have been immature and thus
less viable, see Bohonak & Whiteman 1999), as well as those loose on the water surface or
in sediments. The greater viability of Redshank cysts recovered from faeces rather than
pellets furthers long distance dispersal, as cysts are likely to be retained longer when
expelled as faeces than when regurgitated (Nogales et al. 2001). Cysts expelled in pellets
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
178
may be less viable because they are ground together with grit and hard prey items in the
gizzard (Sánchez et al. in press). Adding grit to cysts fed to flamingos reduces their
viability after gut passage (MacDonald 1980).
At Castro Marim, the hatching success of A. franciscana cysts taken from bird
samples was much lower than for cysts collected in adjacent saltpans. Hatching success of
cysts from Redshank pellets at Cadiz Bay was higher than for cysts from the closest A.
parthenogenetica site we could find at Sanlúcar de Barrameda. Such comparisons are
difficult to interpret as floating cysts collected at the edge of saltpans may not be the ones
ingested by the birds and may have different viabilities. Gut passage through the Greater
Flamingo and Shelduck has been shown experimentally to reduce hatching success of A.
parthenogenetica cysts (MacDonald 1980).
Although there are few data available on the timing of arrival of A. franciscana at
different locations, and on the timing and location of introductions by man, the current
distribution of this exotic in the Iberian Peninsula is consistent with expansion via
shorebirds. Of nine saltworks studied on the main East Atlantic Flyway west of Gibraltar
since 1993 (Amat et al. 2004, authors unpubl.), A. franciscana is dominant at seven of
them (Fig. 1). Yet this species has not been detected in any of the five saltworks studied to
the east of Gibraltar and off the flyway (Fisher exact test, one-tailed p = 0.0105).
Ours is the most extensive field demonstration to date that aquatic metazoans
can disperse readily via gut passage through birds. Recently, ducks and coots were
shown to transport numerous invertebrate eggs of unknown viability (Figuerola et al.
2003). In a previous field demonstration of internal transport, Proctor (1964) found
unknown numbers of viable Cladocera and Ostracoda in three ducks. There are increasing
numbers of exotic crustaceans and bryozoans observed in aquatic systems (Leppäkoski et
al. 2002), and many are likely to have the ability to disperse as resistant eggs via birds
(Figuerola & Green 2002a). The conservation of migratory waterbirds is essential to
maintain connectivity and indigenous invertebrate biodiversity in the world’s wetlands
(Amezaga et al. 2002). Nevertheless, their capacity to disperse invasive species within
and between continents makes the needs to control the importation and release of exotic
species at a global level all the more urgent.
There is evidence of competitive exclusion of native Artemia by an exotic
species. The data available suggest that, once A. franciscana is detected amongst native
Artemia in existing populations, native Artemia disappear within a few years (Amat et
al. 2004). A. franciscana outcompetes A. parthenogenetica and A. salina within two or
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
179
three generations under laboratory conditions using few individuals (Abatzopoulos et al.
2002). We expect viable A. franciscana propagules to eventually reach all coastal
saltworks in the Mediterranean region via birds, but there may be conditions under
which invasion can be resisted, as in other zooplankton communities (Havel & Shurin
2004). Preventing the expansion of aquaculture into protected coastal areas still holding
native Artemia populations (see Abatzopoulos et al. 2002 for inventory) is likely to be
the most effective measure to facilitate their conservation in the short term.
Limnological effects of birds are extremely complex (Daborn et al. 1993). In
their seminal paper on ornitholimnology, Hurlbert & Chang (1983) showed how
waterbirds may affect the dynamics of invertebrate populations and, indirectly, of entire
aquatic ecosystems via predation effects. We suggest they may also do so via dispersal
effects.
ACKNOWLEDGMENTS
We are indebted to C. de le Court, N. Grade and E. Moreno for help collecting samples.
This study has been partially funded by the Spanish R+D National Plan (projects
AGL2001-4582 and BOS2003-02846). M. I. S. was supported by a grant from the
Ministry of Science and Technology. O. R. was supported by a fellowship from the
Ministry of Education and Culture. Comments by P. Jordano, C. Rico, L. Santamaría,
K. Schwenk, and D. M. Wilkinson helped to improve the manuscript. P. M. Potts
provided valuable information
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CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
183
Table 1. Number of samples with intact Artemia cysts, number that produced nauplius
larvae, and number of adult Artemia reared. Not all nauplii hatched from cysts survived
to the adult stage that permitted species identification, thus the numbers of samples
containing each taxon may be underestimated. Each sample contains only a small
fraction of the cysts excreted in a 24 h period by a given bird.
Total With cysts With nauplii With A.franciscana
With nativeArtemia*
Total A.franciscana†
Total nativeArtemia*
Castro Marim Redshank faeces 36 36 36 35 7 522 10 Redshank pellets 31 30 26 23 4 180 4 Godwit faeces 30 27 18 12 7 24 10Cadiz Bay Redshank pellets 55 25 24 1 15 1 40 Dunlin faeces 103 8 1 0 1 0 1
* diploid A. parthenogenetica females.
† 52% were males.
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
184
Table 2. Number of intact Artemia cysts collected, numbers of nauplii hatched and the
proportion of cysts that hatched.
* For samples with at least one cyst (see Table 1 for n).
No. cysts per sample No. nauplii per sample* % cysts hatching
_____________________ ______________________ mean ± SE
No. ofsamples
mean ± SE Range mean ± SE range Castro Marim Redshank faeces 36 65.0 ± 13.1 6 - 379 18.0 ± 3.3 ene-98 33.3 ± 2.5 Redshank pellets 31 26.3 ± 6.9 0 - 160 7.5 ± 2.7 0 - 62 25.8 ± 4.2 Godwit faeces 30 27.8 ± 14.9 0 - 447 1.6 ± 0.4 0 - 8 12.4 ± 2.7Cadiz Bay Redshank pellets 55 1.7 ± 0.3 0 - 13 2.5 ± 0.4 0 - 8 68.8 ± 5.9 Dunlin faeces 103 0.1 ± 0.04 0 - 2 0.1 ± 0.1 0 - 1 12.5 ± 12.5
CHAPTER 7 DISPERSAL OF BRINE SHRIMPS VIA BIRDS
185
Fig. 1. Castro Marim (left insert) and Cadiz Bay (right) on a map of the Iberian
Peninsula, showing the current distribution of A. franciscana (black squares) and native
Artemia (white dots) in relation to the East Atlantic Flyway (shaded after Stroud et al.
2004). Hatched areas within inserts represent saltworks. Other Artemia sites with no
information on species composition since 1992 are not shown.
0 2 4 km
0 1 2Atlantic Ocean
AtlanticOcean
42º00 N
37º00 N
1º00 W
0 2 4 km
186
APPENDIXES
187
APPENDIXES
APPENDIXES
188
APPENDIXES
189
Appendix 1 (Chapter 3). Taxonomic classification of invertebrate taxa showing spatial
distribution in its presence. Cl: Class; O: Order; F: Family; sF: Subfamily; L: larva; P:
pupa; A: adult; I1-I9: industrial ponds; T1-T3: traditional ponds.
Invertebrates Ponds
Cl. Phylactolaemata (Bryozoa)
O. Plumatellida
F. Plumatellidae
Plumatella spp. I1, I6
Cl . Annelida
O. Oligochaeta I1
Cl. Cestoda
O Cyclophillidea
F. Hymenolepididae
Flamingolepis liguloides (Cysticercoids) I1, I2, I3, I4, I5, I6, I7, I8, I9, T1,
T2, T3
Cl. Nematoda I1, I2, I7, T2
Cl. Turbellaria I1, I2, I3, I4, I5, I6, I7, T1, T2
Cl. Gastropoda
O Mesogastropoda
F. Hydrobiidae
Hydrobia ulvae (L, A) I1, T1, T2
Other Gastropoda I1
Cl. Copepoda
APPENDIXES
190
O. Calanoida (L, A) I1, I2, T1
O. Harpacticoida
F. Cletodidae
Cletocamptus retrogressus (L, A) I1, I2, I3, I4, I5, I6, I7, I9, T1, T2,
T3
Other Harpacticoida (L, A) I1, I2, I3, I4, I7, T1, T2, T3
Cl. Ostracoda I1, I2, I4
Cl. Malacostraca
O. Amphipoda
F. Gammaridae I1
Other Malacostraca I1, I4, T1
Cl. Branchiopoda
O. Anostraca
F. Artemiidae
Artemia parthenogenetica (L, A) I1, I2, I3, I4, I5, I6, I7, I8, I9, T1,
T2, T3
Cl. Insecta
O. Heteroptera
F. Corixidae
Sigara stagnalis (L, A) I1, I2, T1, T3
O. Coleoptera
F. Dytiscidae (L) I3, I5, I6, I7, T1
F. Hydrophilidae
Berosus spinosus (A) I6
Paracymus aenas (A) I1, T1, T2
Hydrophilus spp. (L) I1, I2, T1
F. Hydraenidae
Ochthebius notabilis (L, A) I1, I2, I3, I4, I5, I6, I7, I8, T1, T2,
T3
Ochthebius corrugatus (L, A) T1, T2, T3
APPENDIXES
191
O. Diptera
F. Chironomidae
sF. Orthocladiinae
Halocladius spp. (L) I1, I2
sF. Chironominae
Tr. Chironomini
Chironomus type salinarius (L, P, A) I1, I2, I3, I4, I5, I6, I7, I8, I9, T1,
T2, T3
Other Chironomidae (L) I3, T1
F. Ephydridae
Ephydra spp. (L, P) I3, I1, I2, I4, I6, I9, T1, T2
F. Stratiomyidae
Nemotelus spp. (L) I2, T1, T2
F. Dolychopodidae (L) I2, I5, I6, T1, T2
F. Syrphidae (L) T2
Other Diptera (L) I1, I2, I3, I6, I7, I8, T1, T2, T3
O. Collembola I1, I7, T1, T2, T3
Terrestrial Invertebrates
O. Hymenoptera I5, I7, T1, T2
O. Hemiptera I1, I4, I6, T1, T2
O. Mallophaga I1, T1
O. Diptera I3, I9
O. Coleoptera I2, T1, T3
Other insecta I3, I5, I6, I8, I9, T1, T2, T3
O. Araneida I1, I2, I4, I6, T1, T3
O. Acarina I1, I2, I3, I6, I7, T1, T2, T3
Vertebrates
Cl. Ostheichthyes
O. Ciprinodontiforme
APPENDIXES
192
F. Fundulidae
Fundulus heteroclitus I1, I2, T1
Foraminiferans
Cl. Granuloreticulosea (Protozoa) I2, I3
Appendix 2 (Chapter 3). Details of the GLMs of abundance (counts) summarised in Table 3, showing the estimates and their standard errors for
each parameter, and thus the relative abundance for each month and pond.
A.parthenogenetica Artemia cyst C. retrogressus
OtherHarpacticoida O. notabilis
Ochthebius spp.larva C. salinarius larva Planaria
_________________ ______________ ______________ _________________ _______________ _________________ _______________ ______________Parameter Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SEIntercept 5.75 0.58 7.62 0.47 6.55 0.62 1.6 0.88 0.9 0.71 1 0.58 3.33 0.38 -0.4 0.65I9 -1.45 0.6 -3.16 0.51 -8.21 1.04 -15.52 1174.59 -24.51 34634 -24.7 28978.98 -4.71 0.83 -16.99 1825.34T3 2.62 0.58 -0.75 0.55 -3.01 0.72 -0.96 1.11 -0.6 0.67 1.63 0.62 -3.19 0.6 -17.33 1907.08I1 -8.88 0.63 -7.78 0.5 -2.3 0.52 3.49 0.78 -27 42369 -5.38 1.13 -3.22 0.44 -2.34 0.81I4 -0.77 0.57 -2.49 0.47 -3.24 0.66 -1.1 1.41 -2.6 0.91 -2.79 0.76 -2.14 0.42 0.07 0.61I5 -0.3 0.56 -1.75 0.47 -5.39 0.61 -16.3 978.23 -3 0.7 -3.44 0.75 -2.15 0.39 -0.28 0.61I3 -0.63 0.56 -0.61 0.46 -4.97 0.6 -2.1 1.42 -2 0.7 -2.46 0.67 -1.39 0.37 0.02 0.58I6 -0.74 0.57 -0.02 0.5 -5.01 0.6 -16.48 1068.64 -2.2 0.74 -0.78 0.61 -1.03 0.37 -2.58 0.88I7 -0.62 0.55 -1.38 0.48 -3.45 0.59 -0.43 1.1041 -1.72 0.71 -1.56 0.64 -1.97 0.38 -1.33 0.66I2 -5.33 0.61 -4.04 0.51 -2.09 0.55 3.07 0.79 -26.24 35832 -4.45 0.9 -3.12 0.45 -1.27 0.65T1 -4.11 0.54 -2.22 0.43 1.23 0.55 0.7 0.76 -0.34 0.49 -0.67 0.5 -3.6 0.48 2.34 0.51I8 -0.51 0.59 -0.82 0.45 -22.48 706.5 -16.16 1002.16 -4.04 1.21 -3.26 0.88 -3.85 0.51 -18.17 1396.07T2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0January -0.09 0.46 -0.08 0.34 -0.99 0.5 -19.31 794.6 0.19 0.64 -0.3 0.56 -2.36 0.4 -17.01 1056.43March 1.75 0.41 -0.21 0.36 2.25 0.53 -19.26 847.31 0.12 0.79 2.18 0.63 0.52 0.3 -1.75 0.83May 2.85 0.37 0.72 0.36 -0.46 0.51 -2.3 0.76 1 0.61 2.36 0.54 0.003 0.3 1.5 0.54July 2.55 0.38 0.31 0.36 -0.66 0.48 -0.65 0.67 2.11 0.62 2.21 0.53 -0.25 0.31 2.82 0.52September 3.27 0.41 1.14 0.36 -0.95 0.49 -1.01 0.74 1.68 0.61 2.07 0.55 -0.22 0.31 1.37 0.55November 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0Depth 0.01 0.02 -0.06 0.02 -0.04 0.03 -0.09 0.05 0.04 0.04 -0.06 0.03 -0.04 0.02 -0.07 0.03Shore distance -0.002 0.004 -0.01 0.004 -0.01 0.01 -0.01 0.02 -0.04 0.02 -0.02 0.01 -0.01 0.004 0.0001 0.007Fetch -0.0001 0.0008 0.002 0.0008 -0.0004 0.001 -0.001 0.002 -0.003 0.002 -0.001 0.001 0.001 0.001 0.0003 0.001
Appendix 3 (Chapter 3). Details of the GLMs of volume (biomass) summarised in Table 4, showing the estimates and their standard errors for
each parameter, and thus the relative abundance for each month and pond. Zero values were excluded from these models, hence the removal of
some ponds and months from some models.A.
partenogenética Artemia cyst C. retrogressusOther
Harpacticoida O. notabilisOchthebius spp.
larvaC. salinarius
larva Planaria ________________ _____________ ______________ _______________ _______________ _________________ ______________ ______________Parameter Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SEIntercept -1.84 0.21 -2.55 0.21 -2.3 0.22 -4.4 0.28 -2.64 0.23 -2.83 0.18 -1.07 0.13 -3.77 0.23I9 -0.25 0.23 -1.19 0.24 -1.74 0.49 ... ... ... ... ... ... -0.94 0.26 ... ...T3 0.53 0.29 -0.46 0.25 -1.02 0.33 -0.2 0.4 -0.05 0.22 0.31 0.18 -0.82 0.22 ... ...I1 -2.41 0.37 -2.33 0.3 -0.81 0.2 1 0.24 ... ... -0.77 0.33 -0.8 0.16 -0.13 0.33I4 -0.23 0.22 -0.65 0.22 -1.13 0.23 0.45 0.73 -0.42 0.35 -0.52 0.2 -0.81 0.13 0.04 0.24I5 0.07 0.21 -0.47 0.22 -1.62 0.25 ... ... -0.35 0.34 -0.75 0.19 -0.79 0.13 -0.17 0.21I3 0.06 0.21 0.03 0.21 -1.43 0.24 0.03 0.87 -0.46 0.24 -0.36 0.18 -0.55 0.12 0.09 0.21I6 -0.05 0.22 -0.11 0.22 -1.19 0.28 ... ... -0.51 0.27 -0.17 0.17 -0.37 0.13 -0.16 0.35I7 0.08 0.21 -0.22 0.22 -0.92 0.24 -0.43 0.6 -0.32 0.25 -0.29 0.15 -0.63 0.13 -0.32 0.22I2 -1.84 0.28 -1.77 0.22 -0.7 0.21 0.77 0.27 ... ... -0.53 0.33 -0.81 0.17 -0.04 0.26T1 -1.44 0.24 -0.78 0.21 0.44 0.2 0.24 0.26 0.26 0.16 0.06 0.13 -0.56 0.18 0.62 0.19I8 0.4 0.22 -0.26 0.22 ... ... ... ... -0.72 0.53 -0.29 0.29 -0.81 0.22 ... ...T2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0January -0.26 0.15 -0.09 0.15 -0.01 0.19 ... ... -0.17 0.2 -0.11 0.18 -0.35 0.17 ... ...March 0.88 0.17 -0.08 0.16 0.68 0.18 ... ... 0.05 0.3 0.23 0.2 0.15 0.11 -0.48 0.35May 0.99 0.15 0.19 0.14 -0.13 0.17 0.38 0.42 0.16 0.21 0.14 0.17 -0.05 0.1 0.26 0.18July 1.21 0.16 0.17 0.15 -0.25 0.18 0.04 0.21 0.44 0.22 0.38 0.18 -0.18 0.1 0.59 0.17September 1.4 0.16 0.31 0.15 -0.25 0.19 -0.26 0.24 0.35 0.21 0.27 0.18 -0.2 0.11 0.23 0.18November 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0Depth 0.03 0.01 -0.01 0.01 -0.03 0.01 -0.01 0.02 0.006 0.01 -0.03 0.01 -0.02 0.01 -0.02 0.01Shore distance -0.002 0.002 -0.004 0.002 -0.003 0.002 -0.003 0.01 -0.005 0.01 -0.005 0.003 -0.001 0.001 -0.001 0.003Fetch -0.0002 0.0003 0.001 0.0003 0.0001 4.00E-04 -0.001 0.001 -0.0003 0.001 -0.0002 0.0003 0.001 0.0002 0.0004 0.0004
DISCUSIÓN GENERAL
195
DISCUSIÓN GENERAL
Los resultados de esta tesis se discutieron en detalle en cada capítulo, por lo que me
limitaré en esta sección a presentar una visión general de las aportaciones de este trabajo
al conocimiento de los ecosistemas de salinas (a través de las relaciones entre
invertebrados y limícolas), la aplicación de los resultados obtenidos a la gestión, así
como a plantear aquellas cuestiones que considero importantes para desarrollar en el
futuro.
Aportaciones de la tesis
Esta tesis confirma la importancia de las salinas como hábitat de alimentación y
descanso para los limícolas (ver Velásquez y Hockey 1992, Masero 2003) y destaca el
valor de las salinas del Odiel a nivel internacional para al menos 6 especies de limícolas.
Dado que sólo se censó el 27% de la superficie de la salina, es de esperar que la zona
alcance importancia internacional para un mayor número de especies. Con más de
20.000 aves censadas durante los pasos migratorios en la superficie estudiada,
demostramos que las salinas del Odiel constituyen una de las zonas más importantes
para los limícolas en la ruta migratoria de Atlántico Este (ver Stroud et al. 2004), junto
con Doñana y la Bahía de Cádiz (Martí y del Moral 2002).
La calidad de un hábitat se define en gran medida por la disponibilidad de
recursos (para el caso de los limícolas por la disponibilidad de invertebrados). En el
Odiel dominaron los quironómidos (Chironomus salinarius) y las artemias (Artemia
parthenogenetica), donde constituyen recursos complementarios, alcanzando sus
máximas densidades en momentos diferentes del ciclo anual. Mientras que a finales de
primavera (mayo) la densidad de ambos es elevada, a comienzos del periodo invernal
(noviembre) Artemia prácticamente ha desaparecido, siendo muy abundantes las larvas
de quironómido. La salinidad parece ser el principal condicionante de la presencia y
abundancia de invertebrados, tanto a nivel espacial como temporal. No obstante otros
factores correlacionados con la salinidad podrían estar implicados (como la presencia de
macrófitos o de predadores, ver Williams 1998), siendo necesarios experimentos
detallados para poder discernir entre uno y otros efectos.
Comprobamos la importancia relativa de la salina tradicional e industrial para las
comunidades de limícolas e invertebrados. La salina industrial destacó especialmente
DISCUSIÓN GENERAL
196
desde el punto de vista de las aves, mientras que la tradicional lo hizo desde el punto de
vista de los invertebrados, con una alta productividad y especies únicas, como
Ochthebius corragatus (abundante y ampliamente distribuido) que nunca se registraron
en la salina industrial.
Comprobamos el valor de combinar el análisis de excrementos y egagrópilas
para evaluar la dieta de los limícolas. En base a dicho análisis realizamos el estudio de
la dieta del Archibebe común (Tringa totanus) más detallado hasta el momento.
Observamos un cambio en la dieta entre el paso migratorio de primavera y el de otoño,
con predominio de presas típicas de la salina en primavera y especies típicas de los
fangos intermareales en otoño, lo que sugiere un cambio en el uso del hábitat entre
estaciones.
Hemos visto cómo las relaciones entre limícolas e invertebrados son complejas,
existiendo diversas vías por las que aves e invertebrados interaccionan y afectan
mutuamente. En primer lugar consideramos las relaciones predador-presa. Los
quironómidos, invertebrados dominantes en el bentos, jugaron un papel clave en el
establecimiento de la dinámica de la comunidad de limícolas, condicionando cambios
en la dieta y en el uso de las salinas a lo largo del ciclo anual. Durante el paso
migratorio de primavera los limícolas dependen en gran medida de larvas y pupas de
quironómido, ejerciendo una fuerte influencia sobre la dinámica de la población de
presas, incluso a densidades de aves relativamente bajas. Sin embargo no encontramos
relación entre abundancia de aves (y uso del hábitat) y abundancia de invertebrados de
la columna de agua a lo largo del tiempo, a diferencia de lo observado para las larvas de
quironómido, lo que sugiere que éstos no están implicados en la fenología de los
movimientos migratorios de estas aves. Artemia fue el metazooplancton dominante en
la mayor parte del proceso de producción de sal, tanto en términos de abundancia como
de biomasa, ocurriendo sólo de forma ocasional en las balsas de primera evaporación,
donde son predadas por la comunidad de peces (Britton y Johnson 1987). No obstante,
de cara a las aves, no sólo es importante la cantidad, sino la calidad del recurso. En este
sentido el valor nutritivo de Artemia es bajo en comparación con el de otras presas
como las larvas de díptero (Rubega & Inouye 1994), lo que apoya la hipótesis de que en
las salinas del Odiel son las larvas de quironómido las que juegan el papel más
importante en las interacciones predador-presa. No obstante, es posible que la escasa
respuesta de las aves a los cambios en la abundancia de Artemia se deba al hecho de
encontrarse las máximas densidades en las balsas de elevada salinidad, donde
DISCUSIÓN GENERAL
197
alimentarse puede conllevar elevados costes por osmorregulación (Purdue & Haines
1977). Sin embargo, encontramos evidencias de que los limícolas seleccionaron las
balsas con mayor biomasa de invertebrados, tanto para el caso de los quironómidos
como de Artemia. Es posible que la correlación entre aves e invertebrados estuviera
enmascarada al tratar la comunidad de limícolas en su conjunto, mezclando especies
con diferentes preferencias de dieta. Por ejemplo, existe una gran variabilidad
interespecífica en la capacidad de los limícolas para utilizar Artemia como recurso.
Mientras que unas especies son capaces de compensar la baja calidad de un recurso,
consumiendo mayores cantidades (Berkuil et al 2003), otras se encuentran
fisiológicamente limitadas (Rubega, 1994). Por ejemplo se ha comprobado que una
dieta basada en Artemia es rentable para los Correlimos común (Calidris alpina) y
zarapitín (C. ferruginea) (con una tasa de ganancia de masa corporal de más de 0.5 g/dia
en condiciones óptimas) pero no para el Correlimos falcinelo (Limicola falcinellus)
(Berkuil et al (2003). Es posible que la relación relativamente débil encontrada entre la
disponibilidad de invertebrados planctónicos y la abundancia de aves se deba a un error
en el diseño del muestreo. Monitorizar las poblaciones de Artemia es complicado
debido a su distribución altamente contagiosa (Lenz, 1980) y heterogénea en las balsas,
influida entre otros factores por el viento, la intensidad de la luz y la temperatura,
factores altamente cambiantes, que determinan la disponibilidad de recursos y por tanto
la producción de biomasa de Artemia (Naegel & Rodríguez-A 2002). Por tanto, para
obtener una estima adecuada con un error estándar suficientemente pequeño es
necesario muestrear una gran cantidad de puntos usando un procedimiento de muestreo
estratificado (Baert et al. 2002). Un muestreo a menor escala, comparando la
abundancia de presas entre puntos con mayor y menor densidad de limícolas, dentro de
una balsa, sería más adecuado para contestar esta pregunta; no obstante, esta no fue la
prioridad de la tesis.
Un segundo nivel de interacciones es el que se refiere a las relaciones parásito-
hospedador. En esta tesis abordamos una primera aproximación al estudio de las
interacciones del sistema cestodos-Artemia-limícolas, describiendo la comunidad de
metacestodos que portaba la población de Artemia parthenogenetica del Odiel. Se trata
del estudio más completo de este grupo de parásitos realizado en la Península Ibérica
hasta la fecha. Nuestros resultados revelaron una alta tasa de parasitismo por cestodos,
así como una elevada diversidad, con un total de 8 especies identificadas. Destacó
Flamingolepis liguloides (cuyos adultos parasitan flamencos) por su elevada
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prevalencia, y Anomotaenia tringae (parásito de limícolas) por ser el primer registro en
hospedador intermedio.
Existen evidencias de que los parásitos juegan un papel fundamental en la
dinámica de poblaciones y estructuración de las comunidades animales (Price et al
1986, Dunn & Dick 1998). Los parásitos puede además afectar las interacciones
predador-presa. Muchas especies de parásitos, como la mayoría de los cestodos, poseen
complejos ciclos de vida que involucran la transmisión trófica de un hospedador a otro
por consumo un hospedador intermedio. Algunas tienen la capacidad de alterar el
comportamiento de sus hospedadores intermedios y hacerlos más vulnerables a la
predación por el hospedador definitivo (Bakker et al. 1997, Fuller et al. 2003). El
consumo de artemias parasitadas por los limícolas es un hecho habitual en el Odiel,
como pone de manifiesto la presencia de cisticercoides en los excrementos y
egagrópilas de archibebes. Diversos trabajos muestran que las artemias parasitadas por
Flamingolepis liguloides (Cestoda: Ciclophillidea) presentan un color rojo intenso y
ocupan un micro hábitat diferente al de los individuos no parasitados (Gabrion et al.
1982, Amat 1991, datos propios sin publicar). Datos propios no publicados sugieren que
los cambios morfológicos provocados por la infección aumenta el riesgo de predación
por los limícolas. Cuando el costo energético del parasitismo es moderado, y la captura
de la presa está facilitada por los parásitos, el consumo de las presas infectadas puede
ser beneficioso, lo que explica que en muchos casos no exista una presión selectiva para
evitar las presas infectadas (Lafferty 1992). Sin embargo, es probable que en Odiel los
limícolas se estén alimentando de artemias parasitadas por Flamingolepis liguloides u
otros parásitos no específicos de limícolas, de manera que ello no represente ningún
coste. En el caso opuesto, un predador podría reducir los efectos negativos del
parasitismo cambiando su dieta óptima (Lozano 1991). El papel de los parásitos ha sido
enormemente ignorada en la Teoría del forrajeo óptimo, por la cual los animales
maximizan su "fitness" maximizando la tasa a la que consumen los recursos. Sin
embargo existen ejemplos en la literatura que contradicen dicha teoría (Norris 1999), en
los que la maximización de la tasa de ingesta de energía conlleva costos derivados de
una mayor exposición a parásitos.
Otra importante vía por la que las aves son capaces de afectar la estructura de las
comunidades de invertebrados es mediante la dispersión. Aunque se ha asumido que las
aves son importantes vectores de dispersión de propágulos de animales y plantas, son
escasos los estudios empíricos que demuestren dicha capacidad (Figuerola & Green
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2002, Bohonak & Jenkins 2003). En esta tesis se presenta el trabajo más exhaustivo
realizado en el campo hasta la fecha que demuestra que los invertebrados pueden ser
dispersados vía tracto digestivo de las aves. Los limícolas transportaron quistes viables
de Artemia, tanto en el paso migratorio de primavera como en el paso de otoño.
Además, demostramos por primera vez en el campo que los limícolas son capaces de
dispersar semillas de angiospermas viables. Los limícolas son migradores de largas
distancias, implicados en los procesos de dispersión a larga distancia. La distribución
nativa de Artemia y de semillas de angiospermas registradas en este estudio es
consistente con dicha hipótesis. Investigamos la implicación de diversos factores en la
viabilidad de los propágulos, como por ejemplo la dieta, la forma de excreción
(mediante egagrópilas o excrementos) o el número total de propágulos ingeridos,
encontrando una mayor viabilidad con dietas blandas y a mayor número de quistes
ingeridos. Aunque se ha sugerido que las variaciones en la dieta pueden influir la tasa de
supervivencia de los propágulos, esta es la primera vez que se demuestra en el campo su
implicación real. La relación de la viabilidad con la forma de excreción no estuvo clara,
hallando resultados opuestos en dos trabajos diferentes. No obstante los resultados
fueron débilmente significativos, lo que sugiere que otras variables pudieran estar
creando extra variabilidad, confundiendo los resultados. Este tipo de problemas son
inherentes a los estudios de campo, donde se tiene un escaso o nulo control sobre el
sistema.
La implicación de los limícolas en la dispersión de especies exóticas es otro
resultado interesante de esta tesis. El hallazgo de semillas de Sonchus oleraceus y
Mesembryanthemum nodiflorum en los excrementos y egagrópilas de los limícolas,
sugiere que las aves podrían contribuir a la dispersión y expansión de estas especies en
sus rangos, introducidas en América y Australia. Especialmente importante y revelador
fue el hallazgo de quistes de Artemia franciscana viables en las egagrópilas y
excrementos de los limícolas. A. franciscana es una especie invasora procedente de
Norte América que está desplazando a gran velocidad a las especies autóctonas (Amat
et al. 2005). En España existe una especie sexual, A. salina, y una línea partenogenética,
reconocida como A. parthenogenetica, con poblaciones tanto diploides como
tetrapliodes. En el Odiel coexiste una población mayoritariamente dipliode con una
pequeña proporción de individuos tetrapliodes. Actualmente A franciscana es la única
especie presente en Portugal y ya ha alcanzado las salinas de la bahía de Cádiz. Existen
evidencias de exclusión competitiva de las artemias nativas por A franciscana (Browne
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1980, Browne & Halanych 1989). La llegada de esta especie introducida al Odiel a
través de los limícolas es inevitable. No obstante su efecto sobre las poblaciones nativas
del Odiel y otras partes del mediterráneo no está claro, ya que existen mecanismos por
los que la invasión puede ser resistida. A pesar de su alta capacidad competitiva en el
laboratorio, los propágulos de A. franciscana dispersados a nuevas áreas podrían no
establecerse debido al "efecto de prioridad" de las especies autóctonas que ocupan el
hábitat en grandes densidades (Jenkins & Buikema 1998). Las poblaciones de Artemia
establecidas tienen bancos extremadamente abundantes de propágulos, con los que
deben competir los quites de las invasoras. Se ha demostrado experimentalmente que las
comunidades de zooplancton son capaces de resistir a la invasión por nuevas especies
(Shurin 2000). Además cabe esperar que las poblaciones nativas de Artemia presenten
resistencia a la invasión, ya que los machos de A. franciscana no muestran preferencia
para aparearse con las hembras de su propia especie, al menos en el laboratorio (Browne
1980). Así, es improbable que A. franciscana pueda reproducirse cuando la especie
nativa es mucho más abundante. Sin embargo, los datos disponibles sobre su
distribución actual sugieren que, una vez llega a ser suficientemente abundante para ser
detectada entre las elevadas densidades de Artemia nativa de la población preexistente,
rápidamente la desplaza (Amat et al. en prensa). Si un lugar ocupado por Artemia está
cerca de un lugar infectado y hay un alto grado de conectividad vía movimiento de aves,
la tasa de inmigración de propágulos invasores podría ser suficiente para, en poco
tiempo, superar la resistencia a la invasión. Sin embargo, dada la actual incertidumbre
sobre la biología de la invasión por A. franciscana, prevenir la expansión de la
acuicultura en el Odiel, salinas de Sanlúcar, Cabo de Gata y otras áreas costeras
protegidas que aún albergan poblaciones nativas de Artemia, es probablemente la
medida más efectiva para facilitar su conservación.
Con esta tesis hemos profundizado en el conocimiento de las relaciones entre
limícolas e invertebrados explorando distintos niveles de dichas interacciones. Durante
el estudio se han suscitado muchas preguntas, unas las hemos abordado y muchas
quedan aún por resolver. Ahondar en las cuestiones planteadas permitirá entender mejor
las complejas relaciones ecológicas que se dan en los ecosistemas acuáticos y ayudará a
conservar tan amenazados hábitas.
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Gestión y conservación
Como se indicó en la introducción, la pérdida de hábitats es actualmente el principal
problema ambiental a nivel global, estando especialmente afectados los sistemas
acuáticos (Sadoul et al. 1998, Wilcove et al. 1998). Los humedales artificiales se han
propuesto como alternativa a dicha pérdida de hábitat (Velasquez 1992; Masero et al.
1999), ya que con un adecuado manejo pueden llegar a ser tan productivos como los
sistemas naturales e igualmente atractivos para las aves (Davison y Evans, 1986;
Rehfisch, 1994). En este sentido, la información recogida en esta tesis puede ser de una
gran utilidad para el manejo y gestión de las salinas del Odiel, y otros humedales de
similares características.
Manejo del agua. Los limícolas dependen de la elevada productividad de quironómidos
en la salina, especialmente durante el paso migratorio de primavera, cuando basan su
dieta fundamentalmente en larvas y pupas de Chironomus salinarius. C. salinarius
dominó en el bentos a lo largo de la mayor parte del proceso de cristalización,
presentando un marcado patrón estacional con picos de abundancia en primavera (1470
larvas/m2) y en otoño (1063 larvas/m2). No obstante, una gran parte de la productividad
no está accesible a las aves debido a los niveles de agua de las balsas. En nuestro área
de estudio los limícolas explotaron profundidades de hasta 20 cm (salvo las avocetas,
que se alimentaron a 25 cm nadando), variando según las especies. En promedio sólo un
10% de la superficie del conjunto de las balsas estudiadas fue menor de 20 cm,
quedando la mayor parte inaccesible a las aves. Una reducción del 16% de la superficie
accesible, observada durante el paso de otoño respecto al paso de primavera,
acompañado de una mayor afluencia de aves y de forma más prolongada en el tiempo,
podría justificar parcialmente el menor uso de la salina en ese periodo, aunque otros
factores podrían estar implicados (como cambios estacionales en los beneficios de
alimentarse en los fangos intermareales, o de Artemia por diferencias en la prevalencia
de parásitos, cambios en su distribución, tamaño, etc). En cualquier caso, un descenso
general de los niveles de agua durante ambos periodos migratorios, que garantizase el
acceso a una superficie somera más amplia, aumentaría enormemente el valor de las
salinas del Odiel como hábitat de forrajeo para los limícolas. Como ya se comentó en la
discusión, la predación por limícolas ejerce una regulación "top-down" sobre los
quironómidos durante el paso de primavera, afectando a diversos parámetros
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poblacionales, como la abundancia, biomasa y distribución de tamaños de larvas. Este
efecto es significativo incluso a densidades de aves relativamente bajas, lo que sugiere
que la tasa de ingesta de las aves esté limitada por el uso que hayan hecho previamente
las primeras en llegar. Por tanto proponemos que el descenso general de los niveles de
agua vaya acompañado de un descenso paulatino (drawdown) en los niveles de algunas
balsas, por ejemplo con una velocidad de 1 cm por día en los momentos máximos de
paso (aproximadamente entre el 15 y el 30 de abril y entre el 1 de agosto y 15 de
septiembre). Dicho drawdown hace que haya continuamente nuevas zonas de
sedimentos disponibles para las aves de manera que puedan acceder a altas densidades
de larvas que no han sido consumidas días anteriores. El descenso gradual también evita
la mortandad de larvas si grandes superficies quedaran completamente drenadas
(Rehfisch 1994). El manejo debería favorecer igualmente el acceso a Artemia, más
abundantes en las zonas profundas (menos accesibles) como muestran nuestros
resultados Un descenso de los niveles de agua pondría disponible un gran número de
ellas al quedar concentradas en la superficie somera. Las balsas más adecuadas para
manejar los niveles de agua son las de segunda evaporación. De todo el conjunto de la
salina es la zona que reúne mejores condiciones para la alimentación de los limícolas.
Son balsas en general someras, con suaves orillas, de grandes superficies y los niveles
de perturbación antrópica son bajos. La salinidad oscila en torno a 45 y 125 g/l, lo que
promueve altas densidades tanto de quironómidos como de artemias. No obstante el
óptimo varía entre ambos, y mientras que los quironómidos alcanzan las máximas
densidades (hasta 24.000 larvas/m2) al principio del rango (entre 45 y 80 g/l), Artemia
lo hace al final (hasta 400 individuos/l por encima de 80 g/l,). Las balsas de segunda
evaporación son además las que menos perturbación pueden crear desde el punto de
vista de los intereses industriales de la salina. En este sentido, tanto las balsas de
primera evaporación, que actúan de reservorio de agua con que se nutre el resto de la
salina, como la zona de cristalización, que requiere de un fino manejo que garantice el
precipitado del cloruro sódico lo más puro posible, constituyen las áreas más sensibles
al manejo de agua de cara a la producción de sal y por tanto son las balsas menos
susceptibles al manejo del agua de cara a las aves.
En conclusión, ligeras modificaciones en el manejo del agua de las salinas,
especialmente de ciertas balsas, a través de las medidas que proponemos, incrementaría
notablemente la proporción de la producción de quironómidos, artemias y otros
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invertebrados consumida por las aves, cabiendo esperar un efecto positivo sobre sus
tamaños poblacionales a lo largo de su ruta migratoria (Sutherland 1996, 1998).
Suavizado de las pendientes de las orillas. Las labores de mantenimiento y construcción
de muros en las salinas son actividades prácticamente constantes. En las salinas
industriales como la que estudiamos, con una gran superficie, las actividades de
reparación requieren, la mayor parte de las veces, de maquinaria pesada. El trasiego de
estas máquinas por las orillas, destroza con frecuencia las escasas zonas someras que
tienen los limícolas para alimentarse, promoviendo orillas con pendientes abruptas
difíciles de utilizar para una gran cantidad de aves, especialmente las de pequeño
tamaño. Entre la fauna de limícolas existen especies de muy variado tamaño, con
diferentes longitudes de picos y patas, y estrategias de forrajeo. Por ejemplo, en nuestro
área de estudio las avocetas explotaron las mayores profundidades, observándose
nadando a profundidades de hasta 25 cm, mientras que los pequeños correlimos lo
hicieron entre 1 y 3 cm de profundidad. Por tanto para garantizar un hábitat adecuado
para todas las especies es necesario el mantenimiento de orillas con suaves pendientes
que permitan ser explotadas por toda la comunidad de limícolas. Una alternativa es la
construcción de islas de pendientes suaves en medio de cada balsa, de manera que las
aves puedan alimentarse en sus bordes en lugar de en la orilla de la propia balsa.
Además ello constituye una medida eficaz contra predadores terrestres como los gatos.
Las escasas islas que existen en actualmente en la salina industrial (por ejemplo en E11
(I3)) son utilizadas por un gran número de limícolas tanto para descansar como para
alimentarse en sus bordes, lo que demuestra la eficacia real las elevaciones del terreno
en el interior de las balsas y cuya construcción mejoraría notablemente el hábitat para
los limícolas.
Control del uso de especies invasoras. Nuestros resultados demostraron que especies
exóticas como Artemia franciscana pueden ser eficazmente dispersadas vía limícolas.
La invasión por especies exóticas es, después de la pérdida de hábitat, el principal
problema que afecta a la diversidad a nivel global (Wilcove et al. 1998, Money &
Cleland 2001). Una vez que esta especie es detectada entre las artemias nativas, estas
últimas tienden a desaparecer en sólo unos pocos años (Amat et al. 2005). Los quistes
de A. franciscana se comercializan para acuicultura en todo el mundo. El abandono de
salinas y cambio de usos hacia actividades piscícolas está favoreciendo la dispersión de
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A. franciscana a una gran velocidad a lo largo de la costa mediterránea. A diferencia de
la Bahía de Cádiz, con una gran tradición en acuicultura, y donde ya ha llegado A.
franciscana, en el Odiel no ha existido tradición alguna y hasta el momento sólo la
autóctona A. parthenogenetica ha sido registrada. No obstante, la llegada de individuos
de zonas próximas como el Algarve en Portugal o la Bahía de Cádiz es inminente. Sin
embargo, especialmente preocupante es la transformación, en Odiel, de una antiguas
salinas abandonadas, en piscifactorías, justamente al otro lado del canal mareal que
suministra agua a la salina estudiada, lo que destaca la necesidad de evitar el uso de A.
franciscana como fuente de alimento para los peces. Dado que los limícolas se mueven
regularmente entre zonas de descanso y alimentación distancias de hasta 20 km, el paso
de aves de un complejo a otro sería extremadamente fácil. Además, es altamente
probable las artemias exóticas escapen de las instalaciones de la piscifactoría,
contaminando directamente las balsas de la salina. La expansión de A. franciscana no
sólo amenaza las poblaciones nativas de Artemia, sino también la comunidad de
parásitos asociada, muy diversa en las salinas estudiadas, y prácticamente ausentes en
ejemplares de A. franciscana analizados (datos propios sin publicar). También
ignoramos el efecto que podría tener para los limícolas, el cambio de artemias
autóctonas a exóticas. Si, como sugieren nuestras observaciones, las aves están
predando en gran medida sobre artemias parasitadas (especialmente con cestodos
parásirtos de flamencos), dado que la prevalencia de parásitos en la especie exótica
parece ser muy escasa, sería probable que la tasa de ingestión de los limícolas se viera
reducida considerablemente tras el cambio a un sistema dominado por A. franciscana.
En conclusión, prevenir la expansión de la acuicultura en los espacios protegidos, donde
existen poblaciones de Artemia nativas, es probablemente la medida más adecuada para
frenar su expansión y conservar la biodiversidad de los sistemas de salinas.
Por otro lado, las poblaciones de especies autóctonas de invertebrados y plantas, en
humedales como las salinas de Odiel, están en parte sostenidas a través de la dispersión
por limícolas y otras aves que mantienen la conectividad entre poblaciones de distintos
humedales (Amezaga et al. 2002). Esta es una razón más de la necesidad de conservar la
salinas del Odiel, y evitar su abandono o cambios de uso que impliquen la
transformación a otro tipo de hábitat como supondría por ejemplo la acuicultura. En tal
caso cabría esperar un impacto negativo no sólo sobre las poblaciones de aves,
invertebrados y plantas en la propia salina sino también en otras partes de la ruta
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migratoria del Atlántico Este, al perderse una pieza fundamental en el conjunto de
humedales que mantiene la biodiversidad de plantas e invertebrados a través de su
conectividad vía vectores de dispersión como las aves. En definitiva, la necesidad de
conservar las salinas del Odiel trasciende a las fronteras de Andalucía y España, siendo
fundamental para mantener las poblaciones, por ejemplo de Artemia autóctonas o de
Arthrocnemum en países colindantes.
Importancia de las salinas tradiciones. En la región mediterránea los humedales
costeros y las salinas continúan desapareciendo. La actividad tradicional prácticamente
ha sido abandonada, o transformada en otros usos. En las marismas del Odiel aún se
mantiene el uso tradicional coexistiendo con el industrial, que habría que hacer un
esfuerzo en conservar. Los resultados de nuestro estudio muestran que ambos manejos,
industrial y tradicional, no son equivalentes en cuanto a la comunidad de invertebrados
y uso por las aves que uno y otro favorecen. Al contrario de lo que podría esperarse por
su manejo menos intensivo, el uso tradicional no proporciona un hábitat preferido para
los limícolas, siendo la salina industrial, de grandes superficies, la que albergara
mayores densidades de aves. No obstante, el manejo tradicional, proporciona un tipo de
hábitat distinto, con mayor diversidad y biomasa de invertebrados acuáticos, mayor
diversidad de plantas y probablemente de aves e invertebrados terrestres. El uso
tradicional favorece la diversidad biológica por su integración en el entorno y
adaptación a los ciclos naturales. Por todo ello, consideramos que su conservación en su
estado actual es una prioridad para el espacio protegido. La combinación de salinas
industriales y tradicionales aumenta la biodiversidad en el espacio, lo que puede ser un
buen modelo de gestión para otras zonas mediterráneas con salinas activas.
Prioridades para el futuro
A lo largo de esta tesis hemos abordado diversas cuestiones relacionadas con las
relaciones ecológicas entre limícolas e invertebrados. No obstante también se han
suscitado muchas cuestiones que habrá que abordar en futuros estudios. Es prioridad
seguir profundizando en el trabajo iniciado en esta tesis, en cada unos de los temas
tratados. A continuación se proponen las líneas de trabajo que se consideran prioritarias.
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1. En primer lugar proponemos la necesidad de realizar censos más completos que
incluyan toda la salina para, evaluar su importancia a escala global, y poder determinar,
por ejemplo, qué especies cumplen el criterio RAMSAR que concede importancia
internacional a aquellos humedales que albergan el 1% de la población de una especie
2. Son necesarios estudios que evalúen los cambios en el uso de las salinas, en base a las
fluctuaciones en la disponibilidad de presas en los fangos intermareales. Al igual que
hemos hecho para las salinas, habrá que analizar cómo cambia la abundancia y
estructura de las comunidades de invertebrados entre primavera y otoño en los caños,
principal hábitat de alimentación intermareal para los limícolas durante la marea baja
(Velásquez et al. 1991, Kalejta 1993). Asimismo habría que evaluar, mediante
experimentos de exclusión, el efecto de la predación sobre las comunidades de
invertebrados de los fangos intermareales. Sería interesante repetir también los
experimentos de exclusión durante el paso migratorio de otoño en la salina. De nuevo,
diferencias en el uso de las salinas entre primavera y otoño podrían estar ocasionados
por diferencias en la abundancia de las diferentes especies de limícolas entre ambos
periodos, que utilizan de forma diferencial los recursos.
3. Proponemos igualmente ahondar en las relaciones tróficas entre invertebrados y
limícolas, con estudios detallados analizando las respuestas de las especies más
importantes de limícolas (como las agujas o los archibebes), a los cambios de sus
principales presas (tanto entre balsas como a una escala más fina dentro de una balsa).
Para ello será necesario identificar las presas más importantes para las diferentes
especies, con más estudios de dieta. Una forma alternativa al análisis de egagrópilas y
excrementos, con un gran potencial, es el uso de isótopos estables. Estas técnicas
permiten evaluar la dieta de las aves analizando la composición isotópica los tejidos del
consumidor (íntimamente relacionado con la dieta), evitando el sesgo inherente al
análisis de excremetos y egagrópilas (Duffy & Jackson 1986). No obstante, estas
técnicas también son susceptibles al sesgo, por ejemplo en el caso de no tener estimas
del tiempo empleado alimentándose en distintas zonas dentro de un área con una alta
variabilidad isotópica (Alexander et al. 1996). No obstante es una técnica potente que
bien utilizada puede aportar una valiosísima información. Además presenta otras
ventajas adicionales, ya que debido a diferencias en las tasas metabólicas entre tejidos,
el análisis de isótopos estables puede indicar la dieta en una variedad de periodos que va
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desde unos días (análisis de hígados), a varias semanas (análisis del músculo), y hasta
años (análisis de huesos) (Hobson & Clark 1992). Además de profundizar en las
relaciones tróficas entre limícolas e invertebrados, proponemos estudios que ahonden en
las relaciones tróficas dentro de la comunidad de invertebrados.
4. En esta tesis se realizó una primera aproximación a las relaciones parásito-
hospedador. Son necesarios estudios que ahonden en las relaciones cestodos-Artemia-
limícolas, realizando experimentos que permitan ampliar el conocimiento del efecto del
parasitismo sobre Artemia. Parece ser que ciertas especies de cestodos provocan
cambios en la coloración de Artemia (adquiriendo un intenso color rojo) y modifican su
micro distribución, entre otras cosas (Amat et al. 1991, Gabrion et al. 1982). No
obstante es muy escasa la información que existe al respecto. En un segundo nivel será
necesario evaluar si los cambios provocados por los parásitos aumentan la
susceptibilidad a la predación por el hospedador final. Experimentos con aves en
cautividad permitirán testar dicha hipótesis, además de otras relacionadas con la
selección de presas parasitadas. Por ejemplo, si los limícolas pueden o no distinguir
entre artemias con cestodos parásitos de ellos mismos (por ejemplo Anomotaenia
tringae) y cestodos específicos de otra aves (como Flamingolepis loguloides, parásito
de flamencos).
Un paso más en el estudio de las relaciones parásito-hospedador, será descifrar
las interacciones entre parásitos que infectan simultáneamente un mismo individuo así
como el efecto que tiene la infección mixta sobre el comportamiento y morfología de
Artemia, y en última instancia el efecto sobre la selección de presas por las aves. De
especial interés, y que aún no ha sido evaluado, es el papel que pudieran desempeñar los
parásitos en las relaciones de competencia entre A. franciscana y las especies
autóctonas. Se ha demostrado la implicación de los parásitos en los procesos de
invasiones biológicas, mediando en la competencia entre especies autóctonas e
invasoras (Hudson & Greenman, 1998, Bauer et al. 2000). La tasa de parasitismo de
especies exóticas a menudo es muy baja en comparación con las especies nativas (Dunn
& Dick 1998), bien por una menor susceptibilidad de las especies invasoras a la
infección por parásitos autóctonos, bien porque en el proceso de invasión se
seleccionaron individuos resistentes. Ello conferiría ventajas competitivas sobre las
especies autóctonas, facilitando la invasión (Settle & Wilson 1990). Por otro lado, el
efecto de una especie de parásito puede variar según el hospedador al que parasite,
DISCUSIÓN GENERAL
208
como demostraron Bauer et al. (2000) al comprobar una menor eficacia del parásito
acantocéfalo Pomphorhynchus laévis cuando infectaba una especie invasora de un
anfípodo gammárido que infectaba a la autóctona. Los parásitos tienen una gran
influencia sobre la comunidad de invertebrados a través de muy variados efectos, que
incluyen relaciones predador-presa, competencia interespecífica etc. No obstante la
mayoría de estudios de ecología de poblaciones dejan al margen el papel de los
parásitos en la estructuración y dinámica de las comunidades animales, que habría que
empezar a tener en cuenta.
5. En cuanto a la dispersión de propágulos por limícolas son necesarios estudios más
amplios, para evaluar la direccionalidad de la dispersión, incluyendo un mayor número
de muestras entre otoño y primavera, y un mayor número especies de limícolas.
Estudios de la dispersión de semillas de Sonchus oleraceus y Mesembryanthemum
nodiflorum en su rango introducido ayudarían a esclarecer el papel de las aves en su
expansión. Habría que profundizar en el estudio de los movimientos de los limícolas
entre el Odiel y otras localidades, para evaluar la probabilidad de dispersión a sitios y
hábitats adecuados. A este respecto un enorme potencial tiene el seguimiento por radio-
telemetría (via satélite) utilizado ya en numerosos estudios con limícolas y que está
proporcionando excelentes resultados (Takekawa et al. 2002).
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214
CONCLUSIONES
215
CONCLUSIONES
1. Las salinas del Odiel sustenta de manera regular más de 20.000 limícolas, albergando
el 1% de los individuos de la población de 6 especies de limícolas, criterio que estipula
el convenio RAMSAR para considerar un humedal de importancia internacional para
las aves acuáticas.
2. La comunidad de invertebrados de las salinas del Odiel está dominada por larvas de
Chironomus salinarius (en el bentos) y Artemia parthenogenética (en la columna de
agua), salvo en las balsas de primera evaporación donde la diversidad de invertebrados
es alta (con 27 especies diferentes registradas).
3. Entre los factores químicos, la salinidad fue el más importante condicionante de la
abundancia y diversidad de invertebrados, determinando la estructura de la comunidad a
lo largo del gradiente espacial. No obstante el efecto de la salinidad difirió para los
invertebrados planctónicos y bentónicos, estando favorecidas las cadenas tróficas
planctónicas frente a las bentonicas con el aumento de la salinidad. Entre los factores
biológicos destacaron la presencia de peces y macrófitos.
4. El estudio de la dieta de los limícolas rinde resultados diferentes para el análisis de
egagrópilas y excrementos, pero ambos están correlacionados en la abundancia y rango
de presa consumidos. Los dos métodos son complementarios y una combinación de
ambos es la opción más adecuada para describir la dieta de los limícolas.
5. Los cambios estacionales en la abundancia de quironómidos, determinan cambios en
la dieta y uso de las salinas por los limícolas a lo largo del ciclo anual. Durante el paso
migratorio de primavera, los Archibebes comunes se alimentaron preferentemente en las
salinas, consumiendo larvas y pupas de Chironomus salinarius; en el paso de otoño
utilizaron los fangos intermareales, alimentándose fundamentalmente de poliquetos y
moluscos.
6. Las variaciones espaciales en la abundancia de invertebrados y superficie disponible,
de forma conjunta, explicaron diferencias en la densidad de aves. A pesar del manejo
menos intensivo de las salinas tradicionales y la mayor biomasa de invertebrados que
CONCLUSIONES
216
sustentaron, las salinas industriales albergaron mayores densidades de aves.
7. Los limícolas ejercieron una importante influencia sobre la dinámica de larvas de
quironómidos en las salinas el Odiel. La exclusión de aves mediante cercados produjo
un fuerte efecto sobre la densidad, biomasa y distribución de tamaño de larvas.
8. Los experimentos de exclusión mostraron que el efecto de la predación no fue más
intenso a mayor densidad de aves, existiendo un profundo efecto incluso a baja
densidades de predadores. Por tanto la llegada de los primeros limícolas afecta la tasa de
ingesta de los migrantes más tardíos. La intensidad del efecto de la predación no sólo
depende de la densidad de predadores sino del momento en que tiene lugar la predación
en relación al los ciclos de productividad de las presas.
9. Las relaciones predador-presa en las salinas del Odiel son complejas, existiendo
evidencias de un doble control "top down" y "bottom up" en la regulación y
estructuración de las poblaciones de predador y presa.
10. La población de Artemia parthenogenetica del Odiel mostró una diversa comunidad
de metacestodos con un total de 8 especies identificadas, 4 de ellas parásitos de
flamencos, 3 de limícolas, 1 de zampullines y 1 de láridos. Destacaron Flaminolepis
liguloides (parásito de flamencos) por su elevada prevalencia, Anomotaenia tringae
(parásito de limícolas) por ser el primer registro en hospedador intermedio y Confluaria
podicipina (parásito de zampullines), Euricestus avoceti (parásito de limícolas y
flamencos) y Gynandrotaenia stammeri (parásitos de flamencos) por registrarse por
primera vez en España.
11. Los limícolas son eficaces vectores de dispersión de propágulos de invertebrados y
plantas. En el Odiel encontramos que Archibebes comues, Archibebes oscuros y Agujas
colinegras transportaron quistes de Artemia parthenogenetica y semillas de Sonchus
oleraceus, Mesembryanthemum nodiflorum y Arthrocnemum macrostachyum viables, lo
que sugiere una importante implicación de los limícolas en la distribución de estas
especies y flujo génico entre poblaciones.
CONCLUSIONES
217
12. El transporte y viabilidad de quistes y semillas varió con la localidad, la estación, el
tipo de muestra (excrementos o egagrópilas) y la especie de limícola, lo cual tiene
implicaciones sobre la probabilidad y direccionalidad de la dispersión.
13. La dieta tuvo una fuerte influencia sobre la tasa de supervivencia de los quistes de
Artemia, observándose una mayor cantidad de quistes intactos a medida que disminuyó
la dureza de la dieta. Otros factores como forma de excreción de los propágulos
(mediante excrementos o egagrópilas) o el número de popágulos ingeridos también
afectó a la viabilidad de los mismos, encontrándose en este último caso una correlación
positiva entre los componentes de cantidad y calidad de la dispersión (a mayor ingesta
de quistes, mayor proporción de quistes viables).
14. Los limícolas tienen una importante función en la dispersión de especies exóticas,
tanto de invertebrados (Artemia franciscana) como de plantas (Sonchus oleraceus y
Mesembryanthemum nodiflorum). La expansión de Artemia franciscana vía limícolas
pone en serio peligro las poblaciones de Artemia autóctonas en toda Europa, así como a
las especies estrechamente asociadas a ella, como sus parásitos.
218
AGRADECIMIENTOS
219
AGRADECIMIENTOS
No podría poner punto y final al trabajo de estos últimos años sin dar las gracias a todas
las personas que han colaborado de una u otra manera haciendo posible la realización de
esta tesis y por su puesto haciendo mucho más ameno el trabajo. Ellos han sido
imprescindibles durante estos años, y a todos les dedico mi esfuerzo.
En primer lugar me gustaría dar las gracias a mis directores de tesis, Andy y
Eloy, por haberme ofrecido la oportunidad de trabajar con ellos. Con Andy me inicié en
este apasionante mundo y de él he aprendido muchísimo. Nada más acabar la carrera me
ofreció trabajar con la dieta de la Malvasía y accedí sin pensarlo dos veces. Aquel fue
mi primer contacto con la investigación, que acabó de reafirmar mi interés por las aves
acuáticas y los ecosistemas acuáticos en general, y del que guardo un entrañable
recuerdo. Andy confió en mí desde el primer momento (mucho más que yo misma!), y
espero no haberle defraudado. Trabajar con él ha sido todo un privilegio para mí,
tremendamente estimulante y enriquecedor. Le agradezco su implicación, dedicación y
asesoramiento con mi trabajo, y su amistad.
Con Eloy aprendí muchas cosas sobre el funcionamiento de las marismas del
Odiel, despertando en mí el interés y la pasión que ahora siento por la marisma. Le
agradezco su ayuda e implicación, inestimables, durante el arranque y primera fase de
mi tesis. De esa época guardo muy buenos recuerdos.
A la Estación Biológica de Doñana y a la Universidad de Huelva agradezco el
haberme acogido, permitiéndome trabajar en sus centros y poniendo a mi alcance todos
los medios que necesité.
Juan Carlos Rubio, Director Conservador del Paraje Natural Marismas del Odiel,
defendió desde el principio mi proyecto de tesis, proporcionándonos los permisos para
trabajar en la salina y poniendo todos los medios del paraje a nuestra disposición. Le
agradezco el interés mostrado en todo momento por mi trabajo y su colaboración.
Gracias a Javier Aranda, director de las Salinas, por permitirme trabajar en las
salinas, poniendo todos los medios de ARAGONESAS a mi alcance.
La mayor parte de mi tesis ha sido sustentada económicamente por una beca FPI
de Acción MIT financiada por el Ministerio de Ciencia y Tecnología. Durante el último
año disfruté de una beca I3P de postgrado del CSIC.
K. Schwenk, D. M. Wilkinson, N. Burton, W. Cresswell, J. Figuerola, P.
Jordano, C. Rico, L Santamaría, F. Amat, V.V. Kornyushin y V.V. Tkach, aportaron
AGRADECIMIENTOS
220
interesantes comentarios y sugerencias a los manuscritos. Pablo García Murillo y Carlos
Luque ayudaron con la identificación de semillas y Dagmar Frisch, Carmen Elisa Sanz
y Francisco Amat con la identificación de invertebrados.
Los datos de anillamiento fueron proporcionados por la Oficina de Especies
Migratorias (Ministerio de Medio Ambiente).
Durante estos años he tenido la suerte de convivir con gente de una gran calidad
científica y humana. Claudine me ofreció su ayuda y colaboración durante toda mi tesis,
desde el primer momento cuando me sugirió la posibilidad de optar a la beca que he
disfrutando durante estos años. Gracias por tu interés y por tu amistad. Los guardas de
las marismas del Odiel, especialmente José Manuel Sayago y Enrique Urbina, me
ayudaron a reducir el inmenso mundo que suponía para mí la identificación de los
limícolas. Con ellos aprendí a distinguir los correlimos zarapitines de los comunes en
invierno, las aguja colinegras de las colipintas, y muchas cosas más. Ramona, Gerardo y
las niñas me cuidaron como a una más de la familia. Sin esos colacaos calentitos, las
noches de trabajo hubieran sido muy distintas!. Gracias, Jeni, por tu ayuda, "pescando"
quironómidos. Y gracias por supuesto por vuestra grata compañía, vuestro cariño y
hospitalidad, que nunca olvidaré. Antonio el Topo, Juan Luis Benítez y Benito López
Iñiguez me enseñaron el funcionamiento de la salina y el manejo del agua, y me
facilitaron amablemente toda la información y datos que necesité. Los trabajadores de la
salina, "El Lobo" y compañía, también me prestaron su ayuda siempre que la necesité.
Los estudiantes de Ambientales de Huelva, especialmente Jorge, Eduard, Cristina,
María José, Jacinto y Carlos, me echaron buena mano con los muestreos, censos y
demás labores del campo. Con ellos compartí muy buenos momentos, además de tortilla
de patatas y gazpacho!. Gracias a mis compañeros de grupo Cristina, Héctor y Jordi; a
Esther y Patricia del laboratorio acuático; a Maria del Mar y a Raquel, que me ayudaron
de una u otra forma con el trabajo. Especialmente quiero dar las gracias a Cristina, a
quien he acudido infinidad de veces, siempre dispuesta a echarme una mano y
apoyándome cuando más lo he necesitado. Gracias guapa, y ahora a por la tuya!. Hugo
y Esther me han ayudado muchísimo, más de lo que ellos piensan. Con ellos he
compartido risas y lágrimas (a partir de ahora prometo compartir sólo risas!). Gracias
por vuestra amistad y complicidad. Espero no perderos de vista a ninguno. Raquel,
Carlos, Elvira, Mari Carmen, Paz, Gema, Jose, Juan, Nico (espero no dejarme a
ninguno) no dudaron en ponerse las botas o los prismáticos cada vez que lo necesité.
Gracias a todos por vuestra ayuda y amistad. Nuria y Josefina también estuvieron
AGRADECIMIENTOS
221
siempre conmigo, en los momentos más difíciles, y en los mejores también. Gracias a
Luis por tantos "chutes" compartidos de energía. Emilio no dudó en echarme un cable
cada vez que lo necesité, por sólo unas cervecillas!. La "limilla que corre" te está
tremendamente agradecida (y su padre también). De Miguel Delibes nunca me faltaron
sus ánimos, su cariño y su amistad. Gracias a Manolo Carrión, mi artista revelación
preferido, por recordarme casi todas las mañanas que "la prisa mata" y por sacarme cada
día, sin excepción, una sonrisa (o una carcajada). Con Paco compartí gran parte del
tiempo de la tesis y aprendí mucho de su experiencia; me echó buena mano en el campo
(de lo que guardo un bonito recuerdo) y con mis infinitas dudas estadísticas. El
responsable de tan preciosa portada, el artista, es Francis, que no dudó en cederme uno
de sus maravillosos dibujos. Gracias!!!. Manolo me ha ayudado mucho con su cariño y
amistad, y ha hecho mucho más llevadero el tirón final.
Finalmente, mi más sincero agradecimiento a mi familia por su apoyo
incondicional, por haber confiado en mi en todo momento y animado a seguir siempre
mi camino. A mis padres y a mi abuelo les debo mi amor y respeto por los "bichos" y el
campo.
A todos quisiera tener cerca y no perderos de vista, al menos, en los próximos 50 años!
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