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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)
Spatio-temporal composition of aquatic birds community
in Juluapan Lagoon, Colima, Mexican Central Pacific
Yareni Saharai Pablo-López1; https://orcid.org/0000-0001-7958-1108
Christian Daniel Ortega-Ortiz1; https://orcid.org/0000-0002-5691-9388
Salvador Hernández-Vázquez2*; https://orcid.org/0000-0002-3219-786X
José Alfredo Castillo-Guerrero2; https://orcid.org/0000-0001-5922-9342
Aramis Olivos-Ortiz3; https://orcid.org/0000-0002-9886-9817
Marco Agustín Liñán-Cabello4; https://orcid.org/0000-0002-9930-421X
1. Facultad de Ciencias Marinas, Universidad de Colima, Campus El Naranjo, km 20 carretera Manzanillo-Cihuatlán,
Manzanillo, C.P. 28860, Colima, México; yarenisaharai_pablo@ucol.mx, christian_ortega@ucol.mx
2. Departamento de Estudios para el Desarrollo Sustentable de Zona Costera, Centro Universitario de la Costa
Sur, Universidad de Guadalajara. Gómez Farías 82, San Patricio-Melaque, Cihuatlán, Jalisco, C.P. 48980, México;
s.hernandez@academicos.udg.mx (*Correspondence), alfredocas@gmail.com
3. Centro Universitario de Investigaciones Oceanológicas, Universidad de Colima, Campus El Naranjo, km 20 carretera
Manzanillo-Cihuatlán, Manzanillo, C.P. 28860, Colima, México; aolivos@ucol.mx
4. Acuacultura/Biotecnología, Facultad de Ciencias Marinas, Universidad de Colima, Campus El Naranjo, km 20 car-
retera Manzanillo-Cihuatlán, Manzanillo, C.P. 28860, Colima, México; linanm@ucol.mx
Received 12-XII-2020. Corrected 18-VII-2023. Accepted 09-I-2024.
ABSTRACT
Introduction: Aquatic birds (AB) are usually associated with wetlands, which provide refuge, food, and/or nest-
ing sites for resident and migratory species. Despite their ecological importance, there is little knowledge on AB
in some tropical environments, such as those found on the Colima coast.
Objective: To investigate the spatial and temporal composition of the AB community in Juluapan Lagoon,
Colima, Central Mexican Pacific.
Methods: Monthly counts were conducted between June 2017 and May 2018 during low-tide conditions to
record habitat use by AB. Species richness and bird counts were obtained to compare sampling areas; mean rich-
ness and number of individuals were compared between seasons.
Results: We detected 53 species and 5 750 individuals. The highest species richness and relative abundance
values were obtained in winter at the lagoon area farthest from the connection with the marine system, where
anthropogenic activity is lower. Diversity was greater in zones 2 and 3 in spring, summer, and fall. Muddy flats
were the most used environment, and the most frequent activity was resting. Nesting activity was only recorded
in the middle of the lagoon at the mangrove during spring. “Shorebirds” and “waders” were the most dominant
groups in the bird community of the Juluapan lagoon.
Conclusions: This coastal wetland is a site of great biological importance for aquatic birds; thus, conserva-
tion measures should be implemented, and there should be a continuous study of the effects of anthropogenic
pressure.
Key words: avifauna structure; coastal lagoon; ecological aspects; substrates; ecosystem use.
https://doi.org/10.15517/rev.biol.trop..v72i1.52860
AQUATIC ECOLOGY
2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)
INTRODUCTION
Wetlands are among the most productive
ecosystems on the planet due to the physi-
cal, biological, and chemical processes that
arise from interactions between the continent
and ocean (Mitsch & Gosselink, 2007). Aquat-
ic birds are usually associated with wetland
ecosystems, where they obtain a number of
resources that allow them to fulfill their life
cycle; they find food, resting areas, and some
species use certain habitats to nest (Batzer &
Shartitz, 2007). This group of birds presents
morphological and physiological adaptations
and feeding strategies that allow them to inhab-
it these ecosystems and make good use of the
resources available in wetlands. Adaptations
include long necks, legs, and bills (herons, ibis,
and storks), webbed feet (ducks and seabirds),
semi-webbed feet (sandpipers and plovers),
lobed feet (coots), and relatively small feet
with webbing adapted for diving, swimming,
or floating on the surface of the water (Shealer,
2001). In addition, many of these environments
function as important stopover areas during
annual migrations (Batzer & Shartitz, 2007;
Kushlan et al., 2002), where birds can feed, rest,
and store energy to continue their migration
(Howes & Bakewell, 1989; Palacios et al., 1991).
Several studies have been undertaken on
aquatic bird ecology in coastal wetlands of the
Mexican Central Pacific (MCP); in particular
for the state of Colima, general studies such as
that by Vega-Rivera et al. (2016) reported 441
resident and migratory species, of which only
26 % (115 species) were associated with coastal
or continental wetlands. There is more infor-
mation on aquatic birds present in Cuyutlán
Lagoon (7 200 ha), one of the largest coastal
wetlands in the MCP (Mellink & Riojas-López,
2009), than for smaller adjacent wetlands (Ver-
dugo-Munguía & Gómez-del Castillo, 2012).
Some studies have focused on the reproduction
of some aquatic bird species (Mellink & Riojas-
López, 2006; Mellink & Riojas-López, 2008;
Mellink et al., 2007; Mellink et al., 2009a; Rio-
jas-López & Mellink, 2016), or described the
richness, abundance, and distribution of aquat-
ic birds (Mellink & de la Riva, 2005). Some
studies analyzed changes in bird abundance
with respect to physical modifications of the
RESUMEN
Composición espacio-temporal de las aves acuáticas
en la laguna Juluapan, Colima, en el Pacífico Central Mexicano
Introducción: Las aves acuáticas (AA) son usualmente relacionadas a los humedales debido a que éstos funcionan
como sitios de refugio, alimentación y anidación de diferentes especies residentes y migratorias. Sin embargo, el
conocimiento sobre las aves acuáticas en algunos humedales es nulo.
Objetivo: Investigar la composición espacio-temporal de la comunidad de AA en la laguna Juluapan, Colima, en
el Pacífico Central Mexicano.
Métodos: Entre junio de 2017 y mayo de 2018 se llevaron a cabo conteos mensuales en condiciones de marea baja
para registrar el uso de hábitat de las AA. Se obtuvieron valores de riqueza de especies y número de individuos
para realizar comparaciones entre zonas de muestreo, así como el promedio del número de especies y número de
individuos para comparaciones entre temporadas.
Resultados: Se registraron un total de 53 especies y 5 750 individuos. Los valores de riqueza de especies y densidad
de individuos fueron más altos durante invierno, en la zona más alejada al ambiente marino, donde la actividad
antropogénica es menor. La diversidad tuvo valores más altos en la zona 2 y 3, durante primavera, verano y otoño.
El ambiente más explotado por las aves fueron las planicies lodosas; y el descanso fue la actividad más frecuente.
Asimismo, la actividad de anidación sólo se registró en el manglar de la zona media durante primavera. Las “aves
playeras” y “aves zancudas” fueron los grupos más predominantes en la comunidad de aves de la laguna Juluapan.
Conclusiones: Este humedal costero es un sitio de gran importancia biológica para aves acuáticas, por lo que
resulta necesario la implementación de medidas de conservación, así como el estudio de los efectos por la presión
antropogénica.
Palabras clave: estructura de avifauna; laguna costera; aspectos ecológicos; sustratos; uso del ecosistema.
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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)
lagoon system (Mellink et al., 2009b), or pro-
vided information on anthropogenic activities
and their effects on bird conservation (Mellink
& Riojas-López, 2009). However, all these stud-
ies have been undertaken in Cuyutlán Lagoon,
which is also located in the state of Colima and
is considered one of the largest coastal wetlands
in the MCP (Vega-Rivera et al., 2016), whereas
there is scarce knowledge of aquatic birds in
smaller adjacent wetlands.
There is no information on the birds pres-
ent in Juluapan coastal lagoon, a small wetland
(98 hectares) near Cuyutlán Lagoon. Currently,
this coastal lagoon is affected by anthropogenic
activities (tourism development, residual water
discharge, badly planned urban development,
and the addition of nutrients from agricul-
tural activities) (Liñán-Cabello et al., 2016); it
is therefore essential to establish the ecological
importance of this site for birds. The objective
of this study was to analyze the richness and
abundance (considering all birds in general and
by bird groups) of aquatic birds in Juluapan
Lagoon. We also described their spatial (by
zone) and temporal (by season of the year)
distribution and the activities they carried out
on the different lagoon substrates. This research
is the first to describe ecological aspects of
waterfowl in Juluapan Lagoon and will provide
a baseline for future studies focused on the
conservation and sustainable management of
habitats and birds.
MATERIALS AND METHODS
Study area: Juluapan Lagoon is a small
wetland that is permanently linked to the ocean
through a 20 m wide by 75 m long artificial
canal. It is located on the Mexican Central
Pacific coast (19°06’ - 19°07’ N & 104°23’ -
104°24’ W), West of Santiago de Manzanillo
Bay, Colima (Fig. 1). It has an approximate sur-
face of 98 ha and ranges between 0.2 m and 5
m in depth (Liñán-Cabello et al., 2016). To the
North of the lagoon, there are muddy substrates
that are exposed during low tides, whereas
Fig. 1. Geographical location of Juluapan Lagoon, indicating the three sampling zones (Map adapted from Google Earth Pro).
4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)
to the South there are sand banks (Luna &
Zepeda, 1980). The margins of this wetland are
covered mainly by red mangrove (Rhizophora
mangle) and white mangrove (Laguncularia
racemosa) (Jiménez-Quiroz & González-Oroz-
co, 1996). The bottom of the lagoon is made up
of fine alternating stratifications of silt, clay, and
sand (Luna & Zepeda, 1980). The zone closest
to the beach and where there is communication
with the sea (labelled zone 1 in this study) is
dominated by small plains of sandy substrate
that are exposed at low tide. This area is where
the influence of tourism and fishing activities
is greatest. The center of the lagoon (zone 2)
is surrounded by mangroves and small muddy
areas, and is the area least affected by anthropo-
genic activities. The northernmost part (zone
3) is dominated by mangroves, as well as by
large areas of soft sediments that have been
exposed by human activities. There is marked
coastal urban growth in the northeast area,
where the El Naranjo campus of the University
of Colima and the Club Santiago residential
development are located (zones 3 and 2, Fig.
1); there are rural shellfish restaurants in the
Southeast, as well as tourism influence and
a dock for smaller vessels (zone 1, Fig. 1);
whereas anthropogenic impact is minimal or
null in the Northern (zone 3) and Western
(zones 2 and 3) areas. The Miramar stream is
located in the extreme Northeast; this stream
presents an important fluvial contribution from
agricultural and urban areas in the rainy season
(summer) that can modify littoral morphology
during the tropical cyclone season (Lancin &
Carranza, 1976; Liñán-Cabello et al., 2016).
Bird surveys: Monthly visits to Juluapan
Lagoon were undertaken from June 2017 to
May 2018. Bird counts were performed during
the lowest monthly tide in order to detect the
greatest number of birds in the different envi-
ronments. The lagoon was divided into three
zones (1, 2, and 3, described in study area).
The same route was followed in each zone (30
m from the inner edge of the lagoon) during
each monthly visit; approximately 1.5 hours
were required to survey each zone. A 3-m long
aluminum boat with a 5-hp outboard motor
was used at a navigation speed of less than 3
knots. Birds were counted along a transect par-
allel to the inside edge of the lagoon, covering
a 25-m wide band on each side of the transect.
The observation area was 9.0 ha in zone 1 (tran-
sect length: 1 811 m; width: 50 m), 9.2 ha in
zone 2 (transect length: 1 842 m; width: 50 m);
and 8.9 ha in zone 3 (transect length: 1 779 m;
width: 50 m). Information on the number of
species and individuals was obtained during
counts, as well as on the type of substrate where
birds were found (body of water, sand flat, mud
flat, or mangrove); the activity undertaken by
birds was also documented as feeding, resting,
or nesting.
The identified aquatic bird species were
separated into four functional groups, consid-
ering their morphological characteristics and
ecological affinity; seabirds (including the fol-
lowing families: Pelecanidae, Laridae, Frega-
tidae, and Phalacrocoracidae) (Mellink & de la
Riva, 2005; Schreiber & Burger, 2001), ducks
and rails (Anatidae and Rallidae) (Hernán-
dez-Vázquez, 2005a; Mellink & de la Riva,
2005), shorebirds (Charadriidae, Recurvi-
rostridae, Scolopacidae, and Haematopodi-
dae) (Alonzo-Parra, 2009; Mellink & de la
Riva, 2005; Warnock et al., 2001), and waders
(Ardeidae, Threskiornithidiae, and Ciconiidae)
(Frederick, 2001, Mellink & de la Riva, 2005). A
fifth group called “others” was created for this
study; it included birds that did not belong to
the previous groups (Anhingidae, Pandionidae,
and Cerylidae).
Bird identification was performed using
10 x 50 binoculars and field guides by Hernán-
dez-Vázquez and Esparza-Salas (2008), and
by the National Geographic Society (Dunn &
Alderfer, 2017). Common names and scien-
tific nomenclature were based on the Ameri-
can Ornithological Society (AOS; Chesser et
al., 2021). Risk categories were determined
according to the Official Mexican Norm NOM-
059-SEMARNAT-2019 (DOF, 2019) and the
International Union for Conservation of Nature
(IUCN, 2021).
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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)
Data analysis: The density of species and
individuals was calculated to compare among
sampling zones (1, 2, and 3), according to
(Mandujano-Rodríguez, 2011):
D = n/2wL, (Eq. 1)
where D is density, n is the number of species or
individuals counted, L is transect length, and w
is transect width on each side of the center line.
The average number of species and num-
ber of individuals for each season (summer:
June-August 2017, fall: September-November
2017, winter: December 2017-February 2018,
and spring: March-May 2018) was obtained to
compare between seasons. Fewer than 50 data
points were obtained, so tests of normality were
performed; Shapiro-Wilks (W) and Bartlett
tests were used to determine homogeneity of
variances. Nonparametric statistical tests were
used when data were not normal (P < 0.05), and
parametric statistical tests were used when the
normality assumption was met (P > 0.05).
A nonparametric Kruskal-Wallis (K-W)
test was used to evaluate possible differences
among zones (1, 2, and 3) in the number of
species and number of individuals per group. A
one-way Analysis of Variance (ANOVA: F) was
used to evaluate total bird density (considering
all groups), as data were normal (P > 0.05). A
Kruskal-Wallis test was used to evaluate dif-
ferences in activity (feeding or resting) among
zones, for all bird groups and for each group
separately. A one-way ANOVA was used to
analyze seasonal differences in the total num-
ber of species and individuals (including all
groups), and a Kruskal-Wallis test was used to
perform the analysis for each group. A Mann-
Whitney (U) test was used to compare seasonal
activities (feeding vs. resting) for the number of
species and individuals (Zar, 2010). Statistical
analyses were undertaken using the STATIS-
TICA program (v. 10, StatSoft, Inc., 2011),
considering a 0.05 significance level.
The Shannon-Weaver (H’) proportional
diversity index (Shannon & Weaver, 1949) was
used to calculate total diversity (for the entire
lagoon and all birds), as well as for study areas
and seasons of the year, as follows:
(Eq. 2)
where H’ is the Shannon diversity index, k is the
number of species, and pi is the proportion of
species i in the sample. Differences in diversity
values were obtained with Hutchesons “t” test
(Hutcheson, 1970).
RESULTS
Total richness and abundance: A total
of 53 species were identified, 5 750 individu-
als were recorded (considering all seasons and
zones), and a total alpha diversity of H’= 3.10
was obtained. Of all recorded species, three are
included in the IUCN Red List (IUCN, 2021)
as Near Threatened (Egretta rufescens, Larus
heermanni, and Thalasseus elegans). Six spe-
cies are included under a protection category
according to the Mexican Official Norm NOM-
059-SEMARNAT-2019 (DOF, 2019); two are
threatened (Calidris mauri and Limosa fedoa),
three are under special protection (L. heerman-
ni, T. elegans, and Mycteria americana), and one
is in danger of extinction (E. rufescens) (MS1).
The three species with highest number of
birds were: the black-bellied whistling duck
(Dendrocygna autumnalis) (1 184 individuals;
20.59 % of the total), the white ibis (Eudo-
cimus albus) (457 individuals; 7.95 % of the
total), and the elegant tern (T. elegans) (371
individuals; 6.45 % of the total). The number
of species per group ranged between 5 and 16;
it was greater in shorebirds (16 species, 30.2
% of the total) and waders (14 species, 26.4
% of the total). All groups, excepting “others,
showed similar abundances; the most abun-
dant group were waders (1 531 individuals,
26.6 %) and ducks and rails (1 470 individuals,
25.6 %) (Table 1). The most abundant waders
were E. albus, Nyctanassa violacea, and Egretta
caerulea, which together comprised 59 % of all
individual records in this group. Dendrocygna
autumnalis represented 81 % of individuals in
the ducks and rails group (MS1).
6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)
Distribution by zone: Based on the general
analysis (including all groups), there were sig-
nificant differences in species richness among
zones (standardized by area; K-W = 7.03, df
= 2, P < 0.05); species richness was greater in
zone 3 (Fig. 2A). There were also significant
differences in diversity between zones: zone 1
(H’ = 2.58) vs. zone 2 (H’ = 2.78) (t = 3.87, df =
553, P < 0.05), zone 1 vs. zone 3 (H’= 2.72) (t =
3.95, df = 333, P < 0.05), but not zone 2 vs. zone
3 (t =1.29, df = 431, p = 0.19). However, com-
parisons by group showed a different pattern of
species richness, with no significant differences
among zones between seabirds and shorebirds
(K-W = 3.92, df = 2, P = 0.14 and K-W = 2.93,
df = 2, P = 0.23, respectively). There were dif-
ferences in wader species richness among the
three zones (K-W = 10.32, df =2, P = 0.005),
with greater richness in zone 3. It should be
noted that species belonging to the group of
ducks and rails were only observed in zone 3
(Fig. 2A).
Bird density differed between the three
zones (F2, 156 = 5.40, P = 0.045); these differenc-
es were also observed for each group (seabirds
K-W = 10.31, df = 2, P = 0.005; shorebirds K-W
= 13.15, df = 2, P = 0.001; waders K-W = 10.32,
df = 2, P = 0.005). There more birds in zone 3
for almost all groups, except for seabirds, which
presented greater density in zone 1. Ducks and
rails were only recorded in zone 3 (Fig. 2B).
There were greater diversity values in zone
2 (H’ = 2.78) and 3 (H’ = 2.72) compared with
zone 1 (H’ = 2.58) (Fig. 2C). The comparisons
between pairs indicated significant differences
between zone 1 vs zone 2 (t = 3.83, df = 553,
P < 0.05) and 3 (t = 3.95, df = 3341, P < 0.05),
while zones 2 vs 3 were similar (t = 1.29, df =
431, P = 0.19).
Activity by group and zone: Species rich-
ness was not associated with any particular
activity in the three lagoon zones (feeding
K-W = 3.96, df = 2, P = 0.13; resting K-W =
3.57, df = 2, P = 0.16); however, the analysis by
Tabl e 1
Number of species and individuals of aquatic birds recorded
in Juluapan Lagoon
Functional group Species Individuals
Number %Number %
Seabirds 10 18.9 1 306 22.7
Shorebirds 16 30.2 1 352 23.5
Waders 14 26.4 1 531 26.6
Ducks and rails 8 15.1 1 470 25.6
Others 5 9.4 91 1.6
Total 53 5 750
Fig. 2. A. Species density, B. density of individuals, and
C. Shannon diversity index with confidence intervals of
aquatic bird groups in the three sampling zones in Juluapan
Lagoon.