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REVIEW OF DISPERSAL MEANS OF A NEWLY REPORTED Ruppia maritima L.
(RUPPIACEAE) POPULATION IN NORTH CENTRAL CUBA
REVISIÓN SOBRE LAS VÍAS DE DISPERSIÓN DE UNA POBLACIÓN DE Ruppia maritima
L. (RUPPIACEAE) RECIENTEMENTE REGISTRADA EN LA ZONA CENTRAL NORTE
DE CUBA
Alain Parada Isada* and Mayrene Guimarais Bermejo
Centro de Investigaciones de Ecosistemas Costeros, Cayo Coco, Morón, Ciego de Ávila, ZIP 69 400, Cuba
*Autor de correspondencia: alain@ciec.fica.inf.cu
Fecha de recepción: 26 de marzo de 2009 - Fecha de aceptado: 25 de julio de 2009
ABSTRACT. Cayo Coco, located in the central northern coast of Cuba is considered a new locality for Ruppia maritima L.
Main wigeongrass dispersal means were casuistically assessed; and hydrochory and fish-mediated endozoochory were
discarded based on the geographical distance, hydrological patterns as well as the occurrence and movement patterns of
Ruppia-consuming fish species inhabiting the coastal and estuarine ecosystems in the study area. North American
migratory waterfowls came out as the best candidate for the seed dispersion involved in Laguna Larga. Specifically, species
such as Anas discors, A. americana, and A. clypeata were most important based on the abundance and permanence, the
importance of drupelets in the diet, bill eco-morphology, and the habitat preference.
Keywords: Cayo Coco, dispersion, waterbirds, Laguna Larga, seeds.
RESUMEN. Cayo Coco ubicado en el sector centro-norte de Cuba es considerada nueva localidad para Ruppia maritima
L. Se analizaron casuísticamente las principales vías de dispersión de esta fanerógama y los procesos de hidrocoría y
zoocoría por peces se descartaron, teniendo en cuenta la distancia geográfica, los patrones hidrológicos, así como la
presencia y los patrones de movimiento de las especies de peces que consumen Ruppia maritima que habitan en los
ecosistemas costeros y estuarinos presentes en el área de estudio. Las aves acuáticas migratorias de Norteamérica fueron
los mejores candidatos como vía de dispersión en Laguna Larga. Más específicamente, las especies Anas discors, A.
americana y A. clypeata fueron los más importantes teniendo en cuenta criterios como la abundancia y permanencia de la
especie durante la residencia invernal, la importancia de las semillas en la dieta, la ecomorfología del pico, así como la
preferencia del hábitat.
Palabras clave: Cayo Coco, dispersión, aves acuáticas, Laguna Larga, semillas.
INTRODUCTION
Ruppia maritima L. (wigeongrass) is a submerged
angiosperm that inhabits brackish coastal and inland
saline waters and presents a world-wide distribution
(Verhoeven, 1979). The genus Ruppia has been classified
in the past in various manners; several authors considered
it as a family on its own, the Ruppiaceae, but it has also
been regarded as a subfamily of the Potamogetonaceae
(den Hartog and Kuo, 2006). In fact, as a consequence of
the great morphological variation between populations,
partly due to environmental differences and partly
genetically determined, the taxonomy of the genus is still
unresolved.
This plant exhibits a broad range of environmental
tolerance so that it is able to colonize marine, estuarine,
and freshwater habitats (Lazar and Dawes, 1991). In
addition, it is the main source of primary production in
many subtropical lagoons (Edwards, 1978; Paton, 1982)
and provides both food and cover for a large invertebrate
biota. For instance, in Western Europe, invertebrates
associated with Ruppia-dominated communities have
2
been numbered up to 43 800/m with biomasses of up to
2
22.9 g/m ash-free dry weight (Verhoeven, 1980).
Taxonomic groups such as small worms, nematodes,
ciliates, ostracods, and copepods (Kantrud, 1991),
amphipods (Nixon and Oviatt, 1973) and the annelid
worm Peloscolex gabriellae (Poff, 1973) were found to be
favored by the soft and highly organic sediments where
these plants grow. On the other hand, wigeongrass has
been referred to be an important food item for various
classes of mollusks such as the gastropod Cerithidea
mazatlanica in a Mexican lagoon (Edwards, 1978), the
marine crabs (Callinectes spp.) in a North Carolina estuary
(Copeland et al., 1974) and in south Florida (Zieman,
1982).
Wigeongrass beds are heavily used by fish in coastal
wetlands (Kantrud, 1991) and in some inland waters
(Terrell, 1923) by providing excellent food and cover.
Generally, the plant stands are more often used as a
nursery than as a food resource since just a few species
consume this angiosperm and its detritus (Hildebrand and
Cable, 1938; Sculthorpe, 1967; Austin and Austin, 1971;
Congdon and McComb, 1981).
Among amphibians and reptiles, the Rana and
Xenopus tadpoles in an African estuary (Millard and Scott,
1953) and water snakes (Natrix sipedon) and American
alligators (Alligator mississippiensis) in the SE United States
(Heitzman, 1978; Epstein and Joyner, 1986), were found
common where wigeongrass was abundant. Besides, the
plant has also been noted to be an important food of
some sea turtles (Felger et al., 1979).
This angiosperm is also recognized worldwide as an
important food of migrant and wintering waterfowl,
wading birds and shorebirds (Figuerola et al., 2002); and its
stands can be quickly and entirely consumed by the
wintering waterfowl in subtropical climates according to
Kantrud (1991). In general, various families of waterbirds
are known for feeding on different parts of the
wigeongrass plants such as coots (Fulica spp.) (Swiderek,
1982), red knots (Calidris canutus); dowitchers
(Limnodromus spp.) and common snipes (Gallinago gallinago)
(Sperry, 1940), purple gallinules (Porphyrio martinica),
black-necked stilts (Himantopus mexicanus), and king rails
(Rallus elegans) (Martin et al., 1951), yellowlegs (Tringa spp.)
and willets (Catoptrophorus semipalmatus) (Bourn and
Cottam, 1950) as well as flamingoes (Phoenicopterus spp.)
(Allen, 1956).
Lastly, in the case of mammals, only some wild
species are known to consume living wigeongrass such as
West Indian manatees (Trichechus manatus latirostris)
(Hartman, 1971), muskrats (Ondatra zibethicus) (McCabe,
1982), and nutria (Myocastor coypu) (R. H. Chabreck, pers.
comm. in Garner, 1962). Deer and cattle sometimes eat
detached plants windrowed along shorelines (Campbell,
1946).
However, despite the high diversity of the taxonomic
groups aforementioned, birds have been especially
highlighted due to being long considered the main
candidate for dispersion of numerous organisms lacking
autonomous long-distance dispersal, but showing wide
geographic ranges (Malone, 1965). For any bird-mediated
dispersal (internal transport) event to occur a series of
main steps should be followed according to the
statements of Figuerola and Green (2002): (1) propagule
ingestion process (diet composition), (2) survival after
digestion and (3) gut time retention. These three steps
have been treated in recent literature, for instance, diet
studies of migratory waterfowl (Anatidae) have shown
that large quantities of propagules of aquatic organisms
are consumed by a wide variety of species, especially
ducks (Cramp and Simmons, 1977; Thomas, 1982).
However, there is little information about retention times
of propagules in waterbirds; most of them referred to
Anas duck species (Swanson and Bartonek, 1970; Agami
and Waisel, 1986). These authors reported retention times
of 10–12 h and over 72 h for Najas marina seeds in Anas
platyrhynchos (Mallard) and Scirpus seeds for Anas discors
(Blue-winged teal).
Among the main insular groups surrounding the isle
of Cuba, the Sabana-Camagüey archipelago and
specifically Cayo Coco, has been the best studied one in
regard to its ornithofauna (Rodríguez et al., 1997) and
highlighted for sheltering numerous species, up to 221
(Parada et al., 2006), as well as abundant populations of
neotropical migrant birds travelling southward through
the Atlantic coast corridor. In this respect, Cayo Coco
exhibits the highest values of abundance of the
aforementioned species compared to other locations in
Cuba (Rodríguez and Sánchez, 1995; Wallace et al., 1996)
and that is why the conservation of these coastal
ecosystems has a striking significance at the local and
regional scales (Rodríguez et al., 1997).
Knowing the importance of the ecology of this
macrophyte for the management of waterfowl habitat
worldwide, and the numerical representativeness of
waterfowls in Cuba, especially ducks in coastal and
freshwater wetlands during winter season, we here discuss
the probable dispersal means involved in the newly
discovered locality of R. maritima in a coastal lagoon in
Cayo Coco, based on published literature approaching
endozoochory processes and previous inventory surveys
on waterfowl.
Mesoamericana 13 (1) Agosto de 2009 Mesoamericana 13 (1) Agosto de 2009
28 29
REVIEW OF DISPERSAL MEANS OF A NEWLY REPORTED Ruppia maritima L.
(RUPPIACEAE) POPULATION IN NORTH CENTRAL CUBA
REVISIÓN SOBRE LAS VÍAS DE DISPERSIÓN DE UNA POBLACIÓN DE Ruppia maritima
L. (RUPPIACEAE) RECIENTEMENTE REGISTRADA EN LA ZONA CENTRAL NORTE
DE CUBA
Alain Parada Isada* and Mayrene Guimarais Bermejo
Centro de Investigaciones de Ecosistemas Costeros, Cayo Coco, Morón, Ciego de Ávila, ZIP 69 400, Cuba
*Autor de correspondencia: alain@ciec.fica.inf.cu
Fecha de recepción: 26 de marzo de 2009 - Fecha de aceptado: 25 de julio de 2009
ABSTRACT. Cayo Coco, located in the central northern coast of Cuba is considered a new locality for Ruppia maritima L.
Main wigeongrass dispersal means were casuistically assessed; and hydrochory and fish-mediated endozoochory were
discarded based on the geographical distance, hydrological patterns as well as the occurrence and movement patterns of
Ruppia-consuming fish species inhabiting the coastal and estuarine ecosystems in the study area. North American
migratory waterfowls came out as the best candidate for the seed dispersion involved in Laguna Larga. Specifically, species
such as Anas discors, A. americana, and A. clypeata were most important based on the abundance and permanence, the
importance of drupelets in the diet, bill eco-morphology, and the habitat preference.
Keywords: Cayo Coco, dispersion, waterbirds, Laguna Larga, seeds.
RESUMEN. Cayo Coco ubicado en el sector centro-norte de Cuba es considerada nueva localidad para Ruppia maritima
L. Se analizaron casuísticamente las principales vías de dispersión de esta fanerógama y los procesos de hidrocoría y
zoocoría por peces se descartaron, teniendo en cuenta la distancia geográfica, los patrones hidrológicos, así como la
presencia y los patrones de movimiento de las especies de peces que consumen Ruppia maritima que habitan en los
ecosistemas costeros y estuarinos presentes en el área de estudio. Las aves acuáticas migratorias de Norteamérica fueron
los mejores candidatos como vía de dispersión en Laguna Larga. Más específicamente, las especies Anas discors, A.
americana y A. clypeata fueron los más importantes teniendo en cuenta criterios como la abundancia y permanencia de la
especie durante la residencia invernal, la importancia de las semillas en la dieta, la ecomorfología del pico, así como la
preferencia del hábitat.
Palabras clave: Cayo Coco, dispersión, aves acuáticas, Laguna Larga, semillas.
INTRODUCTION
Ruppia maritima L. (wigeongrass) is a submerged
angiosperm that inhabits brackish coastal and inland
saline waters and presents a world-wide distribution
(Verhoeven, 1979). The genus Ruppia has been classified
in the past in various manners; several authors considered
it as a family on its own, the Ruppiaceae, but it has also
been regarded as a subfamily of the Potamogetonaceae
(den Hartog and Kuo, 2006). In fact, as a consequence of
the great morphological variation between populations,
partly due to environmental differences and partly
genetically determined, the taxonomy of the genus is still
unresolved.
This plant exhibits a broad range of environmental
tolerance so that it is able to colonize marine, estuarine,
and freshwater habitats (Lazar and Dawes, 1991). In
addition, it is the main source of primary production in
many subtropical lagoons (Edwards, 1978; Paton, 1982)
and provides both food and cover for a large invertebrate
biota. For instance, in Western Europe, invertebrates
associated with Ruppia-dominated communities have
2
been numbered up to 43 800/m with biomasses of up to
2
22.9 g/m ash-free dry weight (Verhoeven, 1980).
Taxonomic groups such as small worms, nematodes,
ciliates, ostracods, and copepods (Kantrud, 1991),
amphipods (Nixon and Oviatt, 1973) and the annelid
worm Peloscolex gabriellae (Poff, 1973) were found to be
favored by the soft and highly organic sediments where
these plants grow. On the other hand, wigeongrass has
been referred to be an important food item for various
classes of mollusks such as the gastropod Cerithidea
mazatlanica in a Mexican lagoon (Edwards, 1978), the
marine crabs (Callinectes spp.) in a North Carolina estuary
(Copeland et al., 1974) and in south Florida (Zieman,
1982).
Wigeongrass beds are heavily used by fish in coastal
wetlands (Kantrud, 1991) and in some inland waters
(Terrell, 1923) by providing excellent food and cover.
Generally, the plant stands are more often used as a
nursery than as a food resource since just a few species
consume this angiosperm and its detritus (Hildebrand and
Cable, 1938; Sculthorpe, 1967; Austin and Austin, 1971;
Congdon and McComb, 1981).
Among amphibians and reptiles, the Rana and
Xenopus tadpoles in an African estuary (Millard and Scott,
1953) and water snakes (Natrix sipedon) and American
alligators (Alligator mississippiensis) in the SE United States
(Heitzman, 1978; Epstein and Joyner, 1986), were found
common where wigeongrass was abundant. Besides, the
plant has also been noted to be an important food of
some sea turtles (Felger et al., 1979).
This angiosperm is also recognized worldwide as an
important food of migrant and wintering waterfowl,
wading birds and shorebirds (Figuerola et al., 2002); and its
stands can be quickly and entirely consumed by the
wintering waterfowl in subtropical climates according to
Kantrud (1991). In general, various families of waterbirds
are known for feeding on different parts of the
wigeongrass plants such as coots (Fulica spp.) (Swiderek,
1982), red knots (Calidris canutus); dowitchers
(Limnodromus spp.) and common snipes (Gallinago gallinago)
(Sperry, 1940), purple gallinules (Porphyrio martinica),
black-necked stilts (Himantopus mexicanus), and king rails
(Rallus elegans) (Martin et al., 1951), yellowlegs (Tringa spp.)
and willets (Catoptrophorus semipalmatus) (Bourn and
Cottam, 1950) as well as flamingoes (Phoenicopterus spp.)
(Allen, 1956).
Lastly, in the case of mammals, only some wild
species are known to consume living wigeongrass such as
West Indian manatees (Trichechus manatus latirostris)
(Hartman, 1971), muskrats (Ondatra zibethicus) (McCabe,
1982), and nutria (Myocastor coypu) (R. H. Chabreck, pers.
comm. in Garner, 1962). Deer and cattle sometimes eat
detached plants windrowed along shorelines (Campbell,
1946).
However, despite the high diversity of the taxonomic
groups aforementioned, birds have been especially
highlighted due to being long considered the main
candidate for dispersion of numerous organisms lacking
autonomous long-distance dispersal, but showing wide
geographic ranges (Malone, 1965). For any bird-mediated
dispersal (internal transport) event to occur a series of
main steps should be followed according to the
statements of Figuerola and Green (2002): (1) propagule
ingestion process (diet composition), (2) survival after
digestion and (3) gut time retention. These three steps
have been treated in recent literature, for instance, diet
studies of migratory waterfowl (Anatidae) have shown
that large quantities of propagules of aquatic organisms
are consumed by a wide variety of species, especially
ducks (Cramp and Simmons, 1977; Thomas, 1982).
However, there is little information about retention times
of propagules in waterbirds; most of them referred to
Anas duck species (Swanson and Bartonek, 1970; Agami
and Waisel, 1986). These authors reported retention times
of 10–12 h and over 72 h for Najas marina seeds in Anas
platyrhynchos (Mallard) and Scirpus seeds for Anas discors
(Blue-winged teal).
Among the main insular groups surrounding the isle
of Cuba, the Sabana-Camagüey archipelago and
specifically Cayo Coco, has been the best studied one in
regard to its ornithofauna (Rodríguez et al., 1997) and
highlighted for sheltering numerous species, up to 221
(Parada et al., 2006), as well as abundant populations of
neotropical migrant birds travelling southward through
the Atlantic coast corridor. In this respect, Cayo Coco
exhibits the highest values of abundance of the
aforementioned species compared to other locations in
Cuba (Rodríguez and Sánchez, 1995; Wallace et al., 1996)
and that is why the conservation of these coastal
ecosystems has a striking significance at the local and
regional scales (Rodríguez et al., 1997).
Knowing the importance of the ecology of this
macrophyte for the management of waterfowl habitat
worldwide, and the numerical representativeness of
waterfowls in Cuba, especially ducks in coastal and
freshwater wetlands during winter season, we here discuss
the probable dispersal means involved in the newly
discovered locality of R. maritima in a coastal lagoon in
Cayo Coco, based on published literature approaching
endozoochory processes and previous inventory surveys
on waterfowl.
Mesoamericana 13 (1) Agosto de 2009 Mesoamericana 13 (1) Agosto de 2009
28 29
MATERIAL AND METHODS
Cayo Coco is one of the islands of the Sabana-Camagüey
Archipelago and the fourth largest island within the
2
Cuban archipelago, with an extension of 370 km . It is
located offshore the northern coast of Ciego de Avila
province; historically separated by a shallow interior sea
known as “Bahía de Los Perros”, but connected to the isle
of Cuba by a 17 km long causeway since 1989, the
beginning of the tourism development in this insular
region. Its climate is characterized by a moderate and
stable thermal regime, with an annual average temperature
of 25.6 ºC and the sea water temperature ranging from
17.7 to 33 ºC. Easterly winds of an average of 16 km/h
prevailing all along the year and the annual average
precipitation are of 1076 mm.
Laguna Larga is located on the northern-central
coast of Cayo Coco, (22º32'14” N, 78º21'25” W) (Fig. 1), it
has a long and narrow shape with an extension of 0.22
2
km , and has just one exit to the open sea through a 6 m
wide channel in its easternmost point. Local tides exhibit a
synodi c regular
s e m i d i u r n a l
patter n, with a
maximum average
amplitude of 0.74
m (Zúñiga and
González, 2000)
generating a flow
ranging between 0.8
3
and 1.2 m /s at the
exchange channel.
The natural
evolution of this
coastal wetland has
been influenced by
the growth of Rhizophora mangle (red mangrove) towards
the exit to the open sea, bringing about a continuous
decreasing of water exchange with the rest of the lagoon.
In addition, tourist resorts built during the 90´s have
altered its physical-chemical conditions due to dredging,
stuffing and temporal damping. Bathymetry and sediment
have been also altered by the accumulation of building
debris, and eutrophication conditions have been caused
by the occurrence of solid and liquid wastes spills.
Based on the current known geographical
distribution of R. maritima in Cuba according to Urquiola
and Cabrera (2000), its main dispersion means cited by
Kantrud (1991) were casuistically analyzed (hydrochory,
endozoochory by fishes and birds). In order to make a
checklist of the bird species consuming R. maritima
present in Cayo Coco: (1) several technical reports, papers
and inventory lists from surveys conducted in Cayo Coco
and neighbouring islets wetlands for the last 30 yr were
revised (Garrido, 1976; ACC e ICGC, 1990; López and
Martínez, 1995; Socarrás et al., 1995; Kirkconnell, 1998;
Sánchez and Rodríguez, 2001; Morgado, 2002; Parada et
al., 2006); (2) the initial bird list was consecutively
narrowed down based on the following criteria: bird
migratory behaviour (migratory corridors having an effect
on the study area) according to González (2002), eco-
morphology, abundance and permanence status of
aquatic bird species (Llanes et al., 2002), waterbirds habitat
preference described in Cayo Coco according to Parada et
al. (2006); and (3) dietary importance of R. maritima
drupelets in waterfowls species inhabiting the study area
classified as high, moderate and low, according to the
criteria of Kantrud (1991).
RESULTS
The feasibility of a probable occurrence of hydrochory
and fish-mediated
endozo o ch ory i n
Laguna Larga were
ruled out by taking
into consideration
both geographical
d i s t a n c e a n d
hydrological patterns
in the archipelago as
well as the occurrence
a n d m o v e m e n t
patterns of Ruppia-
c o n su mi n g f i sh
species inhabiting the
coastal and estuarine
ecosystems in the study area.
On the other hand, bird-mediated endozoochory
was considered the most plausible way of dispersion
explaining the occurrence of the angiosperm in the
coastal wetlands of Cayo Coco, in which a group of
migratory waterfowl species became the most effective
dispersers. In this regard, 22 migratory waterbirds
consuming this wigeongrass were identified in our study
area, and 10 of them are dabbling ducks (Anas spp.).
Within this latter species grouping, Anas discors, A.
americana and A. clypeata were identified as the “best”
dispersers based on the criteria of the abundance and
permanence, the importance of drupelets in the diet, bill
eco-morphology, and the habitat preference in the
Figure 1. Location of Laguna Larga in the north-central area of Cayo Coco,
Sabana-Camaguey Archipelago, Cuba.
wintering grounds (Table 1). Other bird families such as
Rallidae, Scolopacidae and diving ducks (Aythya sp.) were
ruled out.
DISCUSSION
Recording the occurrence of R. maritima in Laguna Larga
in 2001 entails taking into consideration the current
described distribution of this macrophyte in Cuba.
According to Urquiola and Cabrera (2000), the nearest
population is located in Cayo Guajaba (about 120 km
away), but most localities have also been recorded in the
western provinces such as Pinar del Río (Playa La Salina),
Habana (Batabanó), Ciudad Habana (Playa de Marianao),
and in the eastern region in Granma (Manzanillo). Known
dispersal means of this angiosperm are water, fish and
birds (Kantrud, 1991) and in this regard, the discontinuity
of the coast line in the study area (arrays of cays) and the
predominant wave patterns, especially during fall, do not
significantly favour effective movements of drupelets
from one site to another in a consistent manner.
On the other hand, fish-mediated dispersion is ruled
out as few fish species feed on this aquatic plant and its
detritus (Austin and Austin, 1971; Congdon and
Table 1. Waterfowl species consuming Ruppia maritima drupelets reported in wetlands of the northern cays
of Ciego de Avila. Abundance: A (abundant), NC (non-common), C (common), R (rare). Permanence:
WR (winter resident), PR (permanent resident), T (transient), BR (bimodal resident). Locality: CC (Cayo Coco),
CG (Cayo Guillermo), CPG (Cayo Paredón Grande), BP (bahía de Los Perros). Habitat: LE (tideland and lagoons),
1
ZC (coastal zone).
Scientific name Abundance and
permanence status
Dietary
importance
Ciego de Ávila Northern Cays
CC CG CPG BP
Habitat
LE ZC
Order Anseriformes
Family Anatidae
Anas discors A, WR High * * * * *
Anas acuta NC, WR-T High * *
Anas bahamensis NC, PR High * * *
Anas strepera V High * * * *
Anas americana C, WR High * * *
Anas clypeata C, WR High * * *
Aythya affinis NC, WR-T Moderate * *
Aythya collaris NC, WR-T Moderate * *
Lophodytes cucullatus V Moderate * * *
Oxyura jamaicensis NC, BR-T Moderate * *
Order Gruiformes
Family Rallidae
Rallus longirostris C, PR Low * * * * *
Porphyrio martinica C, BR Low * * *
Gallinula chloropus A, BR Low * * * *
Fulica americana A, BR Moderate * * * *
Order Chraradiiformes
Family Recurvirostridae
Himantopus mexicanus A, BR-T Low * * * * * *
Family Scolopacidae
Tringa melanoleuca C, WR-T Low * * * * *
Tringa flavipes C, WR-T Low * * * * *
Tringa solitaria NC, WR Low * * * *
Tringa semipalmata C, WR-T Low * * * * * *
Calidris canutus R, T-WR Low * * *
Limnodromus griseus C, WR-T Low * * * * * *
Gallinago gallinago C, WR Low * * * *
1
(sandy shores and coastal shallow waters).
Mesoamericana 13 (1) Agosto de 2009 Mesoamericana 13 (1) Agosto de 2009
30 31
MATERIAL AND METHODS
Cayo Coco is one of the islands of the Sabana-Camagüey
Archipelago and the fourth largest island within the
2
Cuban archipelago, with an extension of 370 km . It is
located offshore the northern coast of Ciego de Avila
province; historically separated by a shallow interior sea
known as “Bahía de Los Perros”, but connected to the isle
of Cuba by a 17 km long causeway since 1989, the
beginning of the tourism development in this insular
region. Its climate is characterized by a moderate and
stable thermal regime, with an annual average temperature
of 25.6 ºC and the sea water temperature ranging from
17.7 to 33 ºC. Easterly winds of an average of 16 km/h
prevailing all along the year and the annual average
precipitation are of 1076 mm.
Laguna Larga is located on the northern-central
coast of Cayo Coco, (22º32'14” N, 78º21'25” W) (Fig. 1), it
has a long and narrow shape with an extension of 0.22
2
km , and has just one exit to the open sea through a 6 m
wide channel in its easternmost point. Local tides exhibit a
synodi c regular
s e m i d i u r n a l
patter n, with a
maximum average
amplitude of 0.74
m (Zúñiga and
González, 2000)
generating a flow
ranging between 0.8
3
and 1.2 m /s at the
exchange channel.
The natural
evolution of this
coastal wetland has
been influenced by
the growth of Rhizophora mangle (red mangrove) towards
the exit to the open sea, bringing about a continuous
decreasing of water exchange with the rest of the lagoon.
In addition, tourist resorts built during the 90´s have
altered its physical-chemical conditions due to dredging,
stuffing and temporal damping. Bathymetry and sediment
have been also altered by the accumulation of building
debris, and eutrophication conditions have been caused
by the occurrence of solid and liquid wastes spills.
Based on the current known geographical
distribution of R. maritima in Cuba according to Urquiola
and Cabrera (2000), its main dispersion means cited by
Kantrud (1991) were casuistically analyzed (hydrochory,
endozoochory by fishes and birds). In order to make a
checklist of the bird species consuming R. maritima
present in Cayo Coco: (1) several technical reports, papers
and inventory lists from surveys conducted in Cayo Coco
and neighbouring islets wetlands for the last 30 yr were
revised (Garrido, 1976; ACC e ICGC, 1990; López and
Martínez, 1995; Socarrás et al., 1995; Kirkconnell, 1998;
Sánchez and Rodríguez, 2001; Morgado, 2002; Parada et
al., 2006); (2) the initial bird list was consecutively
narrowed down based on the following criteria: bird
migratory behaviour (migratory corridors having an effect
on the study area) according to González (2002), eco-
morphology, abundance and permanence status of
aquatic bird species (Llanes et al., 2002), waterbirds habitat
preference described in Cayo Coco according to Parada et
al. (2006); and (3) dietary importance of R. maritima
drupelets in waterfowls species inhabiting the study area
classified as high, moderate and low, according to the
criteria of Kantrud (1991).
RESULTS
The feasibility of a probable occurrence of hydrochory
and fish-mediated
endozo o ch ory i n
Laguna Larga were
ruled out by taking
into consideration
both geographical
d i s t a n c e a n d
hydrological patterns
in the archipelago as
well as the occurrence
a n d m o v e m e n t
patterns of Ruppia-
c o n su mi n g f i sh
species inhabiting the
coastal and estuarine
ecosystems in the study area.
On the other hand, bird-mediated endozoochory
was considered the most plausible way of dispersion
explaining the occurrence of the angiosperm in the
coastal wetlands of Cayo Coco, in which a group of
migratory waterfowl species became the most effective
dispersers. In this regard, 22 migratory waterbirds
consuming this wigeongrass were identified in our study
area, and 10 of them are dabbling ducks (Anas spp.).
Within this latter species grouping, Anas discors, A.
americana and A. clypeata were identified as the “best”
dispersers based on the criteria of the abundance and
permanence, the importance of drupelets in the diet, bill
eco-morphology, and the habitat preference in the
Figure 1. Location of Laguna Larga in the north-central area of Cayo Coco,
Sabana-Camaguey Archipelago, Cuba.
wintering grounds (Table 1). Other bird families such as
Rallidae, Scolopacidae and diving ducks (Aythya sp.) were
ruled out.
DISCUSSION
Recording the occurrence of R. maritima in Laguna Larga
in 2001 entails taking into consideration the current
described distribution of this macrophyte in Cuba.
According to Urquiola and Cabrera (2000), the nearest
population is located in Cayo Guajaba (about 120 km
away), but most localities have also been recorded in the
western provinces such as Pinar del Río (Playa La Salina),
Habana (Batabanó), Ciudad Habana (Playa de Marianao),
and in the eastern region in Granma (Manzanillo). Known
dispersal means of this angiosperm are water, fish and
birds (Kantrud, 1991) and in this regard, the discontinuity
of the coast line in the study area (arrays of cays) and the
predominant wave patterns, especially during fall, do not
significantly favour effective movements of drupelets
from one site to another in a consistent manner.
On the other hand, fish-mediated dispersion is ruled
out as few fish species feed on this aquatic plant and its
detritus (Austin and Austin, 1971; Congdon and
Table 1. Waterfowl species consuming Ruppia maritima drupelets reported in wetlands of the northern cays
of Ciego de Avila. Abundance: A (abundant), NC (non-common), C (common), R (rare). Permanence:
WR (winter resident), PR (permanent resident), T (transient), BR (bimodal resident). Locality: CC (Cayo Coco),
CG (Cayo Guillermo), CPG (Cayo Paredón Grande), BP (bahía de Los Perros). Habitat: LE (tideland and lagoons),
1
ZC (coastal zone).
Scientific name Abundance and
permanence status
Dietary
importance
Ciego de Ávila Northern Cays
CC CG CPG BP
Habitat
LE ZC
Order Anseriformes
Family Anatidae
Anas discors A, WR High * * * * *
Anas acuta NC, WR-T High * *
Anas bahamensis NC, PR High * * *
Anas strepera V High * * * *
Anas americana C, WR High * * *
Anas clypeata C, WR High * * *
Aythya affinis NC, WR-T Moderate * *
Aythya collaris NC, WR-T Moderate * *
Lophodytes cucullatus V Moderate * * *
Oxyura jamaicensis NC, BR-T Moderate * *
Order Gruiformes
Family Rallidae
Rallus longirostris C, PR Low * * * * *
Porphyrio martinica C, BR Low * * *
Gallinula chloropus A, BR Low * * * *
Fulica americana A, BR Moderate * * * *
Order Chraradiiformes
Family Recurvirostridae
Himantopus mexicanus A, BR-T Low * * * * * *
Family Scolopacidae
Tringa melanoleuca C, WR-T Low * * * * *
Tringa flavipes C, WR-T Low * * * * *
Tringa solitaria NC, WR Low * * * *
Tringa semipalmata C, WR-T Low * * * * * *
Calidris canutus R, T-WR Low * * *
Limnodromus griseus C, WR-T Low * * * * * *
Gallinago gallinago C, WR Low * * * *
1
(sandy shores and coastal shallow waters).
Mesoamericana 13 (1) Agosto de 2009 Mesoamericana 13 (1) Agosto de 2009
30 31
McComb, 1981) and wigeongrass is more frequently used
as nursery areas (Congdon and McComb, 1981). With
regards this issue, Darnell (1958) found out that just one
species consumes significant amount of this plant in
Luoisiana state; and Carr and Adams (1973) found low
rates of consumption among 10 foraging groups of fish
in Florida, out of three just developed an herbivory stage.
In our study area, there are just two species of genera
Opsanus and Archosargus, but considered as local residents
(F. P. Amargós, pers. comm.), just migrating towards coral
reefs during breeding seasons.
In th e particul ar case of bird-m ediated
endozoochory, the broad spatial overlap between the
angiosperm geographic distribution in Northamerica and
the Atlantic Coast Migratory Route must be taken into
account. Such a fact could have favoured the accessibility
of this important food resource to various waterfowl
species for refuelling in critical stopovers during fall
migrations movements. In fact, there is a trend for
migratory ducks in the northern hemisphere to feed more
on seeds with high carbohydrate levels during fall and
winter (Baldassarre and Bolen, 1994). Endozoochory
experienced by these ducks is based on the fact that this
group of birds is widely recognized as important
dispersers of various aquatic organisms due to their
abundance, wide distribution ranges and long-distance
migrations along the wetlands of the world. Besides, the
importance of the R. maritima drupelets in dabbling ducks
diet has been broadly pointed out by an extensive
literature compiled for over 70 yr (McAtee, 1915;
Mabbott, 1920; Campbell, 1946; Smith, 1951;
Chamberlain, 1959; Stewart, 1962; Tamisier, 1971;
Johnsgard, 1975; Krapu and Swanson, 1978; Prevost et al.,
1978; Saunders and Saunders, 1981; Swiderek, 1982;
Euliss, 1989).
Once the plausibility of waterfowl feeding on the R.
maritima seeds while migrating southward is considered,
another key phase involved in a possible internal transport
is the retention time of drupelets in the gut. Such a factor
determines the distance range these seeds can travel
(Proctor, 1968). Therefore, the farthermost distance the
seeds can be transported will be limited by their duration
in the gut and how far the disperser can fly during this
time. For instance, if the flight speed of Anas sp. ranges
between 60 to 78 km/h (Welham, 1994), and the pattern
of retrieved seeds from the disperser indicates that
dispersion will take place some hours after ingestion, then
endozoochory could be a feasible event between southern
regions of the U.S.A. and Cayo Coco during fall
migrations. Such a statement is supported by the fact that
the highest probabilities of dispersion can occur about 4 h
after ingestion, comprising distances ranging from 80 to
320 km, even though periods of time exceeding 8 h could
be also attainable (Charalambidou et al., 2003), but at lower
probabilities.
In addition, the proportion of seeds capable of
germination once excreted must be also considered as key
factor involved in the occurrence of any dispersion event.
Despite the fact the proportion of seeds successfully
germinating after being released by any given duck is low,
ranging from 0.4 to 1.3% (Charalambidou et al., 2003), in
wetlands where hundreds and thousands of individuals
are passing through during fall migration, coinciding with
the peak of consumption of R. maritma seeds (Cramp and
Simmons, 1977), the overall figures become significantly
higher. Besides, as the number of individuals carrying the
propagule increases, the probability of one of them
dispersing the seeds over a long distance to a suitable
habitat will be favoured, according to Green et al. (2002).
According to the criteria of abundance and
permanence during winter season in the salty and brackish
wetlands of Cayo Coco, the species Anas discors, A.
americana and A. clypeata, are thought to be possible
dispersers in the study site. On the contrary, species such
as A. strepera (Gadwall), A. bahamensis (White-cheeked
Teal), A. acuta (Northern Pintail), Aythya affinis (Lesser
Scaup) and A. collaris (Ring-necked Duck) considered as
rare and vagrants, are represented by only small
populations in this insular territory. Particularly, A. clypeata
should be an interesting candidate based on the fact this
species showed the highest probability of germinating
seeds per digested seeds recorded in SE Spain (Figuerola et
al., 2002, 2003), and because of its lamellar density,
particularly high among the northern hemisphere ducks
(Nudds et al., 1994). In this regard, the range sizes of
Ruppia drupelets (0.5-4 mm) can be easily ingested as the
high lamellar densities enable ducks to filter smaller
particles (Crome, 1985) by reducing the costs of filtering
small items, leading to negative correlations between
lamellar densities and seed size (Nummi, 1993; Tamisier
and Dehorter, 1999).
Other species presented in the study area, have also
been reported as possible dispersers of R. maritima, such
as shorebirds (Scolopacidae) (Sperry, 1940; Bourn and
Cottam, 1950; Martin et al., 1951), and gallinules (Rallidae)
(Quay and Critcher, 1962; Gaevskaya, 1966). Nonetheless,
more updated researches approaching the feeding ecology
of Himantopus mexicanus (Black-necked Stilt) (Hamilton,
1975), Tringa melanoleuca (Greater-yellow Legs) (Elphick
and Tibbitts, 1998), Tringa flavipes (Lesser-yellow Legs)
(Tibbitts and Moskoff, 1999), Tringa semipalmata (Willet)
(Moskoff, 1995), Porphyrio martinica (Purple Gallinule)
(West and Hess, 2002) and Gallinula chloropus (Common
Moorhen) (Bannor and Kiviat, 2002), agree in stating that
R. maritima seeds seem not to be an important food item in
its diet.
For attaining a deeper insight on the actual role of
migrant waterfowls as effective dispersers of R. martima
seeds in Cayo Coco and neighboring islet wetlands, the
feeding ecology of dabbling ducks must be addressed by
analysing stomach contents (dietary preference) and
subsequent experiments aimed at testing the survival rate
of retrieved propagules under the abiotic and biotic
conditions of the new possible habitat. On the other
hand, more scientific scrutiny for determining the actual
distribution of the angiosperm in the wetlands of Cuba
also demands attention.
ACKNOWLEDGEMENT
We would like to thank Jill Key and Vicente O. Rodríguez
and who patiently revised the versions of the draft.
Valuable and timely suggestions and comments were
made by Adán Zúñiga Ríos, Eneider Pérez Mena who also
improved the writing.
LITERATURE CITED
Academia de Ciencias de Cuba (ACC) e Instituto Cubano
de Geodesia y Cartografía (ICGC). 1990. Estudio de
los grupos insulares y zonas litorales del archipiélago
cubano con fines turísticos. Cayos: Coco, Guillermo y
Paredón Grande. Instituto de Ecología y Sistemática,
CITMA. Editorial Científico-Técnica. Cuba.
Agami, M. and Y. Waisel. 1986. The role of mallard ducks
(Anas platyrhynchos) in the distribution and germination
of seeds of the submerged hydrophyte Najas marina L.
Oecologia 68: 473-475.
Allen, R. P. 1956. The flamingoes: their life history and
survival, with special reference to the American or
West Indian flamingo (Phoenicopterus ruber). National
Audubon Society, New York. USA.
Austin, H. and S. Austin. 1971. The feeding habits of
some juvenile marine fishes from the mangroves in
western Puerto Rico. Caribbean Journal of Science 11:
171-178.
Baldassarre, G. A. and E. G. Bolen. 1994. Waterfowl
ecology and management. John Wiley and Sons, Inc.,
New York, USA.
Bannor, B. K. and E. Kiviat. 2002. Common Moorhen
(Gallinula chloropus), the birds of North America
online. In Poole, A. (ed.). Ithaca: Cornell Lab of
Ornithology; Retrieved from the Birds of North
A m e r i c a O n l i n e :
http://bna.birds.cornell.edu/bna/species/685.
Bourn, W. S. and C. Cottam. 1950. Some biological effects
of ditching tidewater marshes. U. S. Fish Wildl. Serv.,
Res. Rep. 19. Bull. 205.
Campbell, J. W. 1946. The food of the wigeon and brent
goose. British Birds 39: 194-200, 226-232.
Carr, W. E. S. and C. A. Adams. 1973. Food habits of
juvenile marine fishes occupying seagrass beds in the
estuarine zone near Crystal River, Florida. Trans. Am.
Fish. Soc. 102: 511-540.
Chamberlain, J. L. 1959. Gulf Coast marsh vegetation as
food of wintering waterfowl. Journal Wildlife
Management 23: 97-102.
Charalambidou, I., L. Santamaría and O. Langevoord.
2003. Effect of ingestion by five avian dispersers on
the retention time, retrieval and germination of Ruppia
maritima seeds. Functional Ecology 17(6): 747-753.
Congdon, R. A. and A. J. McComb. 1981. The vegetation
of the Blackwood River Estuary, Southwest Australia.
Journal of Ecology 69: 1-16.
Copeland, B. J., K. R. Tenore and D. B. Horton. 1974.
Oligohaline regime. p. 315-357 In: Odum, H. T., B. J.
Copeland and E. A. McMahan (eds.). Coastal
ecosystems of the United States II. Conservation
Foundation, Washington, D.C. USA.
Cramp, S. and K. E. L. Simmons. 1977. Handbook of the
birds of Europe, the Middle East and North Africa.
Vol. 1. Oxford University Press. USA.
Crome, F. H. J. 1985. An experimental investigation of
filter-feeding on zooplankton by some specialized
waterfowl. Australian Journal of Zoology 33: 849-862.
Darnell, R. M. 1958. Food habits of fishes and larger
invertebrates of Lake Ponchartrain, Louisiana, an
estuarine community. Publ. Inst. Mar. Sci. Univ. Tex. 5:
353-416.
den Hartog, C. and J. Kuo. 2006. Taxonomy and
biogeography of seagrasses. USA. p. 1-23.
Edwards, R. R. C. 1978. Ecology of a coastal lagoon
Mesoamericana 13 (1) Agosto de 2009 Mesoamericana 13 (1) Agosto de 2009
32 33
McComb, 1981) and wigeongrass is more frequently used
as nursery areas (Congdon and McComb, 1981). With
regards this issue, Darnell (1958) found out that just one
species consumes significant amount of this plant in
Luoisiana state; and Carr and Adams (1973) found low
rates of consumption among 10 foraging groups of fish
in Florida, out of three just developed an herbivory stage.
In our study area, there are just two species of genera
Opsanus and Archosargus, but considered as local residents
(F. P. Amargós, pers. comm.), just migrating towards coral
reefs during breeding seasons.
In th e particul ar case of bird-m ediated
endozoochory, the broad spatial overlap between the
angiosperm geographic distribution in Northamerica and
the Atlantic Coast Migratory Route must be taken into
account. Such a fact could have favoured the accessibility
of this important food resource to various waterfowl
species for refuelling in critical stopovers during fall
migrations movements. In fact, there is a trend for
migratory ducks in the northern hemisphere to feed more
on seeds with high carbohydrate levels during fall and
winter (Baldassarre and Bolen, 1994). Endozoochory
experienced by these ducks is based on the fact that this
group of birds is widely recognized as important
dispersers of various aquatic organisms due to their
abundance, wide distribution ranges and long-distance
migrations along the wetlands of the world. Besides, the
importance of the R. maritima drupelets in dabbling ducks
diet has been broadly pointed out by an extensive
literature compiled for over 70 yr (McAtee, 1915;
Mabbott, 1920; Campbell, 1946; Smith, 1951;
Chamberlain, 1959; Stewart, 1962; Tamisier, 1971;
Johnsgard, 1975; Krapu and Swanson, 1978; Prevost et al.,
1978; Saunders and Saunders, 1981; Swiderek, 1982;
Euliss, 1989).
Once the plausibility of waterfowl feeding on the R.
maritima seeds while migrating southward is considered,
another key phase involved in a possible internal transport
is the retention time of drupelets in the gut. Such a factor
determines the distance range these seeds can travel
(Proctor, 1968). Therefore, the farthermost distance the
seeds can be transported will be limited by their duration
in the gut and how far the disperser can fly during this
time. For instance, if the flight speed of Anas sp. ranges
between 60 to 78 km/h (Welham, 1994), and the pattern
of retrieved seeds from the disperser indicates that
dispersion will take place some hours after ingestion, then
endozoochory could be a feasible event between southern
regions of the U.S.A. and Cayo Coco during fall
migrations. Such a statement is supported by the fact that
the highest probabilities of dispersion can occur about 4 h
after ingestion, comprising distances ranging from 80 to
320 km, even though periods of time exceeding 8 h could
be also attainable (Charalambidou et al., 2003), but at lower
probabilities.
In addition, the proportion of seeds capable of
germination once excreted must be also considered as key
factor involved in the occurrence of any dispersion event.
Despite the fact the proportion of seeds successfully
germinating after being released by any given duck is low,
ranging from 0.4 to 1.3% (Charalambidou et al., 2003), in
wetlands where hundreds and thousands of individuals
are passing through during fall migration, coinciding with
the peak of consumption of R. maritma seeds (Cramp and
Simmons, 1977), the overall figures become significantly
higher. Besides, as the number of individuals carrying the
propagule increases, the probability of one of them
dispersing the seeds over a long distance to a suitable
habitat will be favoured, according to Green et al. (2002).
According to the criteria of abundance and
permanence during winter season in the salty and brackish
wetlands of Cayo Coco, the species Anas discors, A.
americana and A. clypeata, are thought to be possible
dispersers in the study site. On the contrary, species such
as A. strepera (Gadwall), A. bahamensis (White-cheeked
Teal), A. acuta (Northern Pintail), Aythya affinis (Lesser
Scaup) and A. collaris (Ring-necked Duck) considered as
rare and vagrants, are represented by only small
populations in this insular territory. Particularly, A. clypeata
should be an interesting candidate based on the fact this
species showed the highest probability of germinating
seeds per digested seeds recorded in SE Spain (Figuerola et
al., 2002, 2003), and because of its lamellar density,
particularly high among the northern hemisphere ducks
(Nudds et al., 1994). In this regard, the range sizes of
Ruppia drupelets (0.5-4 mm) can be easily ingested as the
high lamellar densities enable ducks to filter smaller
particles (Crome, 1985) by reducing the costs of filtering
small items, leading to negative correlations between
lamellar densities and seed size (Nummi, 1993; Tamisier
and Dehorter, 1999).
Other species presented in the study area, have also
been reported as possible dispersers of R. maritima, such
as shorebirds (Scolopacidae) (Sperry, 1940; Bourn and
Cottam, 1950; Martin et al., 1951), and gallinules (Rallidae)
(Quay and Critcher, 1962; Gaevskaya, 1966). Nonetheless,
more updated researches approaching the feeding ecology
of Himantopus mexicanus (Black-necked Stilt) (Hamilton,
1975), Tringa melanoleuca (Greater-yellow Legs) (Elphick
and Tibbitts, 1998), Tringa flavipes (Lesser-yellow Legs)
(Tibbitts and Moskoff, 1999), Tringa semipalmata (Willet)
(Moskoff, 1995), Porphyrio martinica (Purple Gallinule)
(West and Hess, 2002) and Gallinula chloropus (Common
Moorhen) (Bannor and Kiviat, 2002), agree in stating that
R. maritima seeds seem not to be an important food item in
its diet.
For attaining a deeper insight on the actual role of
migrant waterfowls as effective dispersers of R. martima
seeds in Cayo Coco and neighboring islet wetlands, the
feeding ecology of dabbling ducks must be addressed by
analysing stomach contents (dietary preference) and
subsequent experiments aimed at testing the survival rate
of retrieved propagules under the abiotic and biotic
conditions of the new possible habitat. On the other
hand, more scientific scrutiny for determining the actual
distribution of the angiosperm in the wetlands of Cuba
also demands attention.
ACKNOWLEDGEMENT
We would like to thank Jill Key and Vicente O. Rodríguez
and who patiently revised the versions of the draft.
Valuable and timely suggestions and comments were
made by Adán Zúñiga Ríos, Eneider Pérez Mena who also
improved the writing.
LITERATURE CITED
Academia de Ciencias de Cuba (ACC) e Instituto Cubano
de Geodesia y Cartografía (ICGC). 1990. Estudio de
los grupos insulares y zonas litorales del archipiélago
cubano con fines turísticos. Cayos: Coco, Guillermo y
Paredón Grande. Instituto de Ecología y Sistemática,
CITMA. Editorial Científico-Técnica. Cuba.
Agami, M. and Y. Waisel. 1986. The role of mallard ducks
(Anas platyrhynchos) in the distribution and germination
of seeds of the submerged hydrophyte Najas marina L.
Oecologia 68: 473-475.
Allen, R. P. 1956. The flamingoes: their life history and
survival, with special reference to the American or
West Indian flamingo (Phoenicopterus ruber). National
Audubon Society, New York. USA.
Austin, H. and S. Austin. 1971. The feeding habits of
some juvenile marine fishes from the mangroves in
western Puerto Rico. Caribbean Journal of Science 11:
171-178.
Baldassarre, G. A. and E. G. Bolen. 1994. Waterfowl
ecology and management. John Wiley and Sons, Inc.,
New York, USA.
Bannor, B. K. and E. Kiviat. 2002. Common Moorhen
(Gallinula chloropus), the birds of North America
online. In Poole, A. (ed.). Ithaca: Cornell Lab of
Ornithology; Retrieved from the Birds of North
A m e r i c a O n l i n e :
http://bna.birds.cornell.edu/bna/species/685.
Bourn, W. S. and C. Cottam. 1950. Some biological effects
of ditching tidewater marshes. U. S. Fish Wildl. Serv.,
Res. Rep. 19. Bull. 205.
Campbell, J. W. 1946. The food of the wigeon and brent
goose. British Birds 39: 194-200, 226-232.
Carr, W. E. S. and C. A. Adams. 1973. Food habits of
juvenile marine fishes occupying seagrass beds in the
estuarine zone near Crystal River, Florida. Trans. Am.
Fish. Soc. 102: 511-540.
Chamberlain, J. L. 1959. Gulf Coast marsh vegetation as
food of wintering waterfowl. Journal Wildlife
Management 23: 97-102.
Charalambidou, I., L. Santamaría and O. Langevoord.
2003. Effect of ingestion by five avian dispersers on
the retention time, retrieval and germination of Ruppia
maritima seeds. Functional Ecology 17(6): 747-753.
Congdon, R. A. and A. J. McComb. 1981. The vegetation
of the Blackwood River Estuary, Southwest Australia.
Journal of Ecology 69: 1-16.
Copeland, B. J., K. R. Tenore and D. B. Horton. 1974.
Oligohaline regime. p. 315-357 In: Odum, H. T., B. J.
Copeland and E. A. McMahan (eds.). Coastal
ecosystems of the United States II. Conservation
Foundation, Washington, D.C. USA.
Cramp, S. and K. E. L. Simmons. 1977. Handbook of the
birds of Europe, the Middle East and North Africa.
Vol. 1. Oxford University Press. USA.
Crome, F. H. J. 1985. An experimental investigation of
filter-feeding on zooplankton by some specialized
waterfowl. Australian Journal of Zoology 33: 849-862.
Darnell, R. M. 1958. Food habits of fishes and larger
invertebrates of Lake Ponchartrain, Louisiana, an
estuarine community. Publ. Inst. Mar. Sci. Univ. Tex. 5:
353-416.
den Hartog, C. and J. Kuo. 2006. Taxonomy and
biogeography of seagrasses. USA. p. 1-23.
Edwards, R. R. C. 1978. Ecology of a coastal lagoon
Mesoamericana 13 (1) Agosto de 2009 Mesoamericana 13 (1) Agosto de 2009
32 33
complex in Mexico. Estuarine Coastal Marine Science
6: 75-92.
Elphick, Ch. S. and T. L. Tibbitts. 1998. Greater
Yellowlegs (Tringa melanoleuca), the birds of North
America online. In: Poole, A. (ed.). Ithaca: Cornell Lab
of Ornithology; Retrieved from the Birds of North
A m e r i c a O n l i n e :
http://bna.birds.cornell.edu/bna/species/355.
Epstein, M. B. and D. S. Baughman. 1986. Study site
description. Chapter 4 In: DeVoe, M. R. and D. S.
Baughman (eds.). South Carolina coastal wetland
impoundments: ecological characterization,
management, status, and use. Vol. II: Technical
synthesis. Publ. SC-SG-TR-86-2. South Carolina Sea
Grant Consortium, Charleston.
Euliss, N. H., Jr. 1989. Assessment of drainwater
evaporation ponds as waterfowl habitat in the San
Joaquin Valley, California. Ph. D. Thesis, Oregon State
University, Corvallis. USA.
Felger, R. S., M. B. Moser and E. W. Moser. 1979.
Seagrasses in Seri Indian culture. p. 260-276. In
Phillips, R. C. and C. P. McRoy (eds.). Handbook of
seagrass biology: an ecosystem perspective. Garland
STPM Press, New York. USA.
Figuerola, J. and A. J. Green. 2002. Dispersal of aquatic
organisms by waterbirds: a review of past research and
priorities for future studies. Freshwater Biology 47:
483-494.
Figuerola, J., A. J. Green and L. Santamaría. 2002.
Comparative dispersal effectiveness of wigeongrass
seeds by waterfowl wintering in south-west Spain:
quantitative and qualitative aspects. Journal of
Ecology 90(6): 989-1001.
Figuerola, J., A. J. Green, and L. Santamaría. 2003. Passive
internal transport of aquatic organisms by waterfowl
in Doñana, south-west Spain. Global Ecology and
Biogeography 12: 427-436.
Gaevskaya, N. S. 1966. The role of higher aquatic plants in
the nutrition of the animals of freshwater basins,
Nauka, Moscow. Natural Lending for Science and
Technology, Boston Spa, England.
Garner, K. M. 1962. Nutritive values and digestibility of
some wetland wildlife foods in Louisiana. M. S. Thesis,
Louisiana State University, Baton Rouge. USA.
Garrido, O. H. 1976. Aves y reptiles de Cayo Coco, Cuba.
Misc. Zool., Academia de Cuba 3: 3-4.
González, H. A. 2002. Las migraciones de las aves. In
González, H. (ed.). Ave de Cuba. UPC Print, Vaasa,
Finland. p. 16-19.
Green, J. A., J. Figuerola and M. I. Sánchez. 2002.
Implications of waterbird ecology for the dispersal of
aquatic organisms. Acta Oecologica 23: 177-189.
Hamilton, R. B. 1975. Comparative behavior of the
American Avocet and the Black-necked Stilt
(Recurvirostridae). Ornithological Monographs 17 p.
Hartman, D. 1971. Behavior and ecology of the American
manatee Trichechus manatus latirostris (Harlan), at Crystal
River, Citrus County. Ph. D. Thesis, Cornell University,
Ithaca, New York. USA.
Heitzman, B. 1978. Management of salt marsh
impoundments for waterfowl in North Carolina. N.C.
Wildl. Resour. Comm. 35 p.
Hildebrand, S. F. and L. E. Cable. 1938. Further notes on
the development and life history of some teleosts at
Beaufort, N.C. Bull. U.S. Bur. Fish. 48(1940): 505-642.
Johnsgard, P.A. 1975. Waterfowl of North America.
Indiana University Press, Bloomington. USA.
Kantrud, H. A. 1991. Wigeongrass (Ruppia maritima): a
literature review. U. S. Fish and Wildlife Service, Fish
and Wildlife Research 10. Jamestown, ND. Northern
Prairie Wildlife Research Center Home Page.
Kirkconnell, A. 1998. Aves de Cayo Coco, Archipiélago
Sabana-Camagüey, Cuba. Torreia, Nueva Serie 43: 22-
39.
Krapu, G. L. and G. A. Swanson. 1978. Foods of juvenile,
brood hen, and post-breeding pintails in North
Dakota. Condor 79: 504-507.
Llanes, A., H. González, B. Sánchez O. and E. Pérez M.
2002. Lista de las aves registradas en Cuba. In
González, H. (ed.). Ave de Cuba. UPC Print, Vaasa,
Finland. p. 147-155.
López, M. and O. Martínez. 1995. Inventario y evaluación
de las comunidades de aves acuáticas de los humedales
de Cayo Coco, Guillermo, Paredón Grande y Bahía de
Los Perros. Trabajo de Diploma. Biblioteca CIEC.
Cuba.
Mabbott, D. C. 1920. Food habits of seven species of
American shoal-water ducks. U.S. Dep. Agric. Bull.
862: 67.
Malone, C. R. 1965. Dispersal of plankton: rate of food
passage in mallard ducks. Journal of Wildlife
Management 29: 529-533.
Martin, A. C., H. S. Zim and A. L. Nelson. 1951. American
wildlife and plants - a guide to wildlife food habits.
McGraw-Hill, New York, USA.
McAtee, W. L. 1915. Eleven important wild duck foods.
U.S. Dep. Agric.
McCabe, T. R. 1982. Muskrat population levels and
vegetation utilization: a basis for an index. Ph. D.
Thesis, Utah State University, Logan. USA.
Millard, N. A. H. and K. M. F. Scott. 1953. The ecology of
South African estuaries. Part VI. Milnerton Estuary
and the Diep River, Cape. Trans. Roy. Soc. S. Afr. 34:
279-324.
Morgado, P. 2002. Dinámica espacio-temporal de las
comunidades de aves acuáticas de las lagunas Pupi I y
II en Cayo Coco, Ciego de Ávila. Tesis de Diploma.
Facultad de Biología, Universidad de la Habana, Cuba.
Moskoff, W. 1995. Solitary Sandpiper (Tringa solitaria), T
the birds of North America online. In: Poole, A. (ed.).
Ithaca: Cornell Lab of Ornithology; Retrieved from
t h e B ir ds o f N o rt h A me ri ca O nl in e:
http://bna.birds.cornell.edu/bna/species/156.
Nixon, S. W. and C. A. Oviatt. 1973. The ecology of a New
England salt marsh. Ecological Monographs 43: 463-
498.
Nudds, T. D., K. Sjöberg and P. Lundberg. 1994.
Ecomorphological relationships among Palearctic
dabbling ducks on Baltic coastal wetlands and a
comparison with the Nearctic. Oikos 69: 295-303.
Nummi, P. 1993. Food-niche relationships of sympatric
mallards and green-winged teals. Canadian Journal of
Zoology 71: 49-55.
Parada, A., E. Socarrás T., M. López R., R. Gómez F., A.
Aguilar V., L. Menéndez C. and J. M. Guzmán M. 2006.
Biota terrestre del norte de la provincia Ciego de Ávila.
In: Ecosistemas costeros: biodiversidad y gestión de
recursos naturales. Compilación por el XV Aniversario
del CIEC. Sección I. Ecosistemas del norte de la
provincia Ciego de Ávila. CIEC. Editorial CUJAE.
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Cardwell Buckingham Committee. Department of
Environment and Planning. S.A.D.E.P. 55, Adelaide.
Poff, M. J. 1973. Species composition, distribution and
abundance of macrobenthic organisms in the intake
and discharge areas after construction and operation
of the Cedar Bayou electric power station. M. S.
Thesis, Texas A & M University, College Station. USA.
Prevost, M. B., A. S. Johnson and J. L. Landers. 1978.
Production and utilization of waterfowl foods in
brackish impoundments in South Carolina. Proc.
Annu. Conf. Southeast. Assoc. Fish Wildl. Agencies
32: 60-70.
Proctor, V. W. 1968. Long-distance dispersal of seeds by
retention in digestive tract of birds. Science 160: 321-
322.
Quay, T. L. and T. S. Critcher. 1962. Food habits of
waterfowl in Currituck Sound, North Carolina. Proc.
Annu. Conf. Southeast. Assoc. Game Fish Comm. 16:
200-208.
Rodríguez, D. and B. Sánchez. 1995. Avifauna del matorral
xeromorfo costero de la región oriental de Cuba
durante la migración otoñal (octubre de 1989, 1990,
1991). Poeyana 447: 1-12.
Rodríguez, D., R. Rodríguez-León, I. Fernández, M.
Martínez, F. Cejas, I. Ramos, L. Bidart, A. Llanes, C.
Mancina, A. Ávila, A. Pérez, D. Rodríguez, A.
Chamizoy V. Rivalta. 1997. Compendio de resultados
sobre fauna terrestre del Archipiélago Sabana-
Camagüey. Informe Técnico, Proyecto GEF/PNUD,
Cub/92/G31. Cuba.
Sánchez, B. and D. Rodríguez. 2001. Avifauna asociada a
hábitats acuáticos y costeros de Cayo Coco, Cuba. El
Pitirre 13(3): 68-75.
Saunders, G. B. and D. C. Saunders. 1981. Waterfowl and
their wintering grounds in Mexico, 1937-1964. U.S.
Fish Wildl. Serv., Resour. Pub. 138.
Sculthorpe, C. D. 1967. The biology of aquatic vascular
plants. Edward Arnold Ltd., London.
Smith, M. M. 1951. The winter foods of river and pond
ducks in the Phoenix area of Plaquemines Parish,
Louisiana. M. S. Thesis, Louisiana State University,
Baton Rouge. USA.
Socarrás, E. T., L. O. Melían, O. Martínez and M. López R.
1995. Inventario y caracterización de los humedales de
importancia para las aves acuáticas en los cayos Coco,
Guillermo, Paredón Grande y la bahía de Los Perros.
Biblioteca CIEC. Cuba.
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Garrido, O. H. 1976. Aves y reptiles de Cayo Coco, Cuba.
Misc. Zool., Academia de Cuba 3: 3-4.
González, H. A. 2002. Las migraciones de las aves. In
González, H. (ed.). Ave de Cuba. UPC Print, Vaasa,
Finland. p. 16-19.
Green, J. A., J. Figuerola and M. I. Sánchez. 2002.
Implications of waterbird ecology for the dispersal of
aquatic organisms. Acta Oecologica 23: 177-189.
Hamilton, R. B. 1975. Comparative behavior of the
American Avocet and the Black-necked Stilt
(Recurvirostridae). Ornithological Monographs 17 p.
Hartman, D. 1971. Behavior and ecology of the American
manatee Trichechus manatus latirostris (Harlan), at Crystal
River, Citrus County. Ph. D. Thesis, Cornell University,
Ithaca, New York. USA.
Heitzman, B. 1978. Management of salt marsh
impoundments for waterfowl in North Carolina. N.C.
Wildl. Resour. Comm. 35 p.
Hildebrand, S. F. and L. E. Cable. 1938. Further notes on
the development and life history of some teleosts at
Beaufort, N.C. Bull. U.S. Bur. Fish. 48(1940): 505-642.
Johnsgard, P.A. 1975. Waterfowl of North America.
Indiana University Press, Bloomington. USA.
Kantrud, H. A. 1991. Wigeongrass (Ruppia maritima): a
literature review. U. S. Fish and Wildlife Service, Fish
and Wildlife Research 10. Jamestown, ND. Northern
Prairie Wildlife Research Center Home Page.
Kirkconnell, A. 1998. Aves de Cayo Coco, Archipiélago
Sabana-Camagüey, Cuba. Torreia, Nueva Serie 43: 22-
39.
Krapu, G. L. and G. A. Swanson. 1978. Foods of juvenile,
brood hen, and post-breeding pintails in North
Dakota. Condor 79: 504-507.
Llanes, A., H. González, B. Sánchez O. and E. Pérez M.
2002. Lista de las aves registradas en Cuba. In
González, H. (ed.). Ave de Cuba. UPC Print, Vaasa,
Finland. p. 147-155.
López, M. and O. Martínez. 1995. Inventario y evaluación
de las comunidades de aves acuáticas de los humedales
de Cayo Coco, Guillermo, Paredón Grande y Bahía de
Los Perros. Trabajo de Diploma. Biblioteca CIEC.
Cuba.
Mabbott, D. C. 1920. Food habits of seven species of
American shoal-water ducks. U.S. Dep. Agric. Bull.
862: 67.
Malone, C. R. 1965. Dispersal of plankton: rate of food
passage in mallard ducks. Journal of Wildlife
Management 29: 529-533.
Martin, A. C., H. S. Zim and A. L. Nelson. 1951. American
wildlife and plants - a guide to wildlife food habits.
McGraw-Hill, New York, USA.
McAtee, W. L. 1915. Eleven important wild duck foods.
U.S. Dep. Agric.
McCabe, T. R. 1982. Muskrat population levels and
vegetation utilization: a basis for an index. Ph. D.
Thesis, Utah State University, Logan. USA.
Millard, N. A. H. and K. M. F. Scott. 1953. The ecology of
South African estuaries. Part VI. Milnerton Estuary
and the Diep River, Cape. Trans. Roy. Soc. S. Afr. 34:
279-324.
Morgado, P. 2002. Dinámica espacio-temporal de las
comunidades de aves acuáticas de las lagunas Pupi I y
II en Cayo Coco, Ciego de Ávila. Tesis de Diploma.
Facultad de Biología, Universidad de la Habana, Cuba.
Moskoff, W. 1995. Solitary Sandpiper (Tringa solitaria), T
the birds of North America online. In: Poole, A. (ed.).
Ithaca: Cornell Lab of Ornithology; Retrieved from
t h e B ir ds o f N o rt h A me ri ca O nl in e:
http://bna.birds.cornell.edu/bna/species/156.
Nixon, S. W. and C. A. Oviatt. 1973. The ecology of a New
England salt marsh. Ecological Monographs 43: 463-
498.
Nudds, T. D., K. Sjöberg and P. Lundberg. 1994.
Ecomorphological relationships among Palearctic
dabbling ducks on Baltic coastal wetlands and a
comparison with the Nearctic. Oikos 69: 295-303.
Nummi, P. 1993. Food-niche relationships of sympatric
mallards and green-winged teals. Canadian Journal of
Zoology 71: 49-55.
Parada, A., E. Socarrás T., M. López R., R. Gómez F., A.
Aguilar V., L. Menéndez C. and J. M. Guzmán M. 2006.
Biota terrestre del norte de la provincia Ciego de Ávila.
In: Ecosistemas costeros: biodiversidad y gestión de
recursos naturales. Compilación por el XV Aniversario
del CIEC. Sección I. Ecosistemas del norte de la
provincia Ciego de Ávila. CIEC. Editorial CUJAE.
Paton, P. 1982. Biota of the Coorong. A study for the
Cardwell Buckingham Committee. Department of
Environment and Planning. S.A.D.E.P. 55, Adelaide.
Poff, M. J. 1973. Species composition, distribution and
abundance of macrobenthic organisms in the intake
and discharge areas after construction and operation
of the Cedar Bayou electric power station. M. S.
Thesis, Texas A & M University, College Station. USA.
Prevost, M. B., A. S. Johnson and J. L. Landers. 1978.
Production and utilization of waterfowl foods in
brackish impoundments in South Carolina. Proc.
Annu. Conf. Southeast. Assoc. Fish Wildl. Agencies
32: 60-70.
Proctor, V. W. 1968. Long-distance dispersal of seeds by
retention in digestive tract of birds. Science 160: 321-
322.
Quay, T. L. and T. S. Critcher. 1962. Food habits of
waterfowl in Currituck Sound, North Carolina. Proc.
Annu. Conf. Southeast. Assoc. Game Fish Comm. 16:
200-208.
Rodríguez, D. and B. Sánchez. 1995. Avifauna del matorral
xeromorfo costero de la región oriental de Cuba
durante la migración otoñal (octubre de 1989, 1990,
1991). Poeyana 447: 1-12.
Rodríguez, D., R. Rodríguez-León, I. Fernández, M.
Martínez, F. Cejas, I. Ramos, L. Bidart, A. Llanes, C.
Mancina, A. Ávila, A. Pérez, D. Rodríguez, A.
Chamizoy V. Rivalta. 1997. Compendio de resultados
sobre fauna terrestre del Archipiélago Sabana-
Camagüey. Informe Técnico, Proyecto GEF/PNUD,
Cub/92/G31. Cuba.
Sánchez, B. and D. Rodríguez. 2001. Avifauna asociada a
hábitats acuáticos y costeros de Cayo Coco, Cuba. El
Pitirre 13(3): 68-75.
Saunders, G. B. and D. C. Saunders. 1981. Waterfowl and
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Fish Wildl. Serv., Resour. Pub. 138.
Sculthorpe, C. D. 1967. The biology of aquatic vascular
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Baton Rouge. USA.
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importancia para las aves acuáticas en los cayos Coco,
Guillermo, Paredón Grande y la bahía de Los Perros.
Biblioteca CIEC. Cuba.
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FACTORES QUE AFECTAN LOS ECOSISTEMAS ACUÁTICOS Y SU INFLUENCIA EN LA
DISTRIBUCIÓN Y PROPAGACIÓN DE PLANTAS ACUÁTICAS MEXICANAS
FACTORS AFFECTING AQUATIC ECOSYSTEMS AND ITS INFLUENCE IN THE
DISTRIBUTION AND PROPAGATION OF MEXICAN AQUATIC PLANTS
Jaime Raúl Bonilla-Barbosa
Laboratorio de Hidrobotánica, Departamento de Biología Vegetal, Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de
Morelos. Av. Universidad 1001, Col. Chamilpa. 62209 Cuernavaca, Morelos, México
Autor de correspondenica: bonilla@uaem.mx
Fecha de recepción: 25 de enero de 2009 - Fecha de aceptado: 19 de mayo de 2009
RESUMEN. México es un país que se caracteriza por poseer una variada topografía que favorece la presencia de una gran
diversidad de ambientes acuáticos. Estos ecosistemas varían entre ellos más que los ambientes terrestres, permitiendo que
se desarrolle la vida de una gran diversidad de organismos. Sin embargo, las plantas acuáticas en nuestro país han sido
pobremente estudiadas con relación a los factores ambientales que influyen en su crecimiento. Por tal motivo, el objetivo
del presente trabajo es dar a conocer cuales son los factores que influyen en la presencia, desarrollo y distribución de las
fanerógamas acuáticas y señalar las estrategias que se deben tomar en cuenta para su manejo y conservación. El análisis
realizado consideró a algunos ecosistemas acuáticos (lagos y ríos) situados en el centro de México, basándose
principalmente en las características particulares de cada uno de ellos, esto es, movimiento del agua, origen, geología,
topografía, clima, cantidad de nutrimentos, contaminación y actividades humanas, así como el efecto que tienen en la
propagación de plantas acuáticas. Con base en este análisis, se indica que los ambientes acuáticos constituyen un grupo
diverso que presenta variaciones entre ellos y dentro de ellos, por lo que se han categorizado en numerosas vías, usando
diferentes parámetros químicos o físicos. En este sentido, también se ha considerado que las plantas acuáticas sean
clasificadas con base en estos elementos, de los cuales es importante indicar que algunos de ellos influyen directamente en
las condiciones del agua, lo que ocasiona el crecimiento excesivo de ellas o su desaparición. Aunado a ello, y considerando
las estrategias reproductivas de las plantas acuáticas, se señalan los mecanismos de propagación que con el paso del tiempo
influirán fuertemente en la pérdida del recurso agua como de los componentes biológicos en donde ellas se desarrollan.
Palabras clave: factores ambientales, plantas acuáticas, propagación, México.
ABSTRACT. Mexico is a country characterized by a varied topography that favors the presence of a great diversity of
aquatic ecosystems. These ecosystems vary between them more than terrestrial environments, allowing the development
of a great diversity of organisms. However, aquatic plants in our country have been poorly studied with relationship to the
environmental factors that influence their growth. For such reason, the objective of the present work is to point out at the
factors that affect the presence, development and distribution of aquatic flowering plants, and to point out strategies that
should be considered for their management and conservation. The analysis carried out considered some aquatic
ecosystems (lakes and rivers) located in the center of the country, mainly focused on their specific characteristics, such as
water movement, origin, geology, topography, climate, nutriments, pollution and human activities, as well as the effect on
the propagation of aquatic plants. According to this analysis, we indicate that aquatic ecosystems constitute a diverse
group that presents inter and intra variations, reason why they have been categorized in numerous ways, by means of
different chemical and physical parameters. In this sense, we also considered that aquatic plants may be classified on the
basis of these parameters, of those which it is relevant to indicate that some of them directly affect water conditions, which
causes their excessive growth or their disappearance. Furthermore, and considering the reproductive strategies of aquatic
plants, we point out at the mechanisms of propagation that with time will strongly affect the loss of water resources as well
as the biological components where they thrive.
Keywords: environmental factors, aquatic plants, propagation, Mexico.
Mesoamericana 13 (1) Agosto de 2009 Mesoamericana 13 (1) Agosto de 2009
36 37
