Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene.

23, 2024) 1

AQUATIC ECOLOGY

https://doi.org/10.15517/rev.biol.trop..v72i1.52860

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; [email protected], [email protected]
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;
[email protected] (*Correspondence), [email protected]
3. Centro Universitario de Investigaciones Oceanológicas, Universidad de Colima, Campus El Naranjo, km 20 carretera
Manzanillo-Cihuatlán, Manzanillo, C.P. 28860, Colima, México; [email protected]
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; [email protected]

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.
2 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)

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.

INTRODUCTION Kushlan et al., 2002), where birds can feed, rest,

and store energy to continue their migration
Wetlands are among the most productive (Howes & Bakewell, 1989; Palacios et al., 1991).
ecosystems on the planet due to the physi- Several studies have been undertaken on
cal, biological, and chemical processes that aquatic bird ecology in coastal wetlands of the
arise from interactions between the continent Mexican Central Pacific (MCP); in particular
and ocean (Mitsch & Gosselink, 2007). Aquat-
for the state of Colima, general studies such as
ic birds are usually associated with wetland
that by Vega-Rivera et al. (2016) reported 441
ecosystems, where they obtain a number of
resident and migratory species, of which only
resources that allow them to fulfill their life
26 % (115 species) were associated with coastal
cycle; they find food, resting areas, and some
or continental wetlands. There is more infor-
species use certain habitats to nest (Batzer &
Shartitz, 2007). This group of birds presents mation on aquatic birds present in Cuyutlán
morphological and physiological adaptations Lagoon (7 200 ha), one of the largest coastal
and feeding strategies that allow them to inhab- wetlands in the MCP (Mellink & Riojas-López,
it these ecosystems and make good use of the 2009), than for smaller adjacent wetlands (Ver-
resources available in wetlands. Adaptations dugo-Munguía & Gómez-del Castillo, 2012).
include long necks, legs, and bills (herons, ibis, Some studies have focused on the reproduction
and storks), webbed feet (ducks and seabirds), of some aquatic bird species (Mellink & Riojas-
semi-webbed feet (sandpipers and plovers), López, 2006; Mellink & Riojas-López, 2008;
lobed feet (coots), and relatively small feet Mellink et al., 2007; Mellink et al., 2009a; Rio-
with webbing adapted for diving, swimming, jas-López & Mellink, 2016), or described the
or floating on the surface of the water (Shealer, richness, abundance, and distribution of aquat-
2001). In addition, many of these environments ic birds (Mellink & de la Riva, 2005). Some
function as important stopover areas during studies analyzed changes in bird abundance
annual migrations (Batzer & Shartitz, 2007; with respect to physical modifications of the
 Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024) 3

lagoon system (Mellink et al., 2009b), or pro- Lagoon. We also described their spatial (by
vided information on anthropogenic activities zone) and temporal (by season of the year)
and their effects on bird conservation (Mellink distribution and the activities they carried out
& Riojas-López, 2009). However, all these stud- on the different lagoon substrates. This research
ies have been undertaken in Cuyutlán Lagoon, is the first to describe ecological aspects of
which is also located in the state of Colima and waterfowl in Juluapan Lagoon and will provide
is considered one of the largest coastal wetlands a baseline for future studies focused on the
in the MCP (Vega-Rivera et al., 2016), whereas conservation and sustainable management of
there is scarce knowledge of aquatic birds in habitats and birds.
smaller adjacent wetlands.
There is no information on the birds pres- MATERIALS AND METHODS
ent in Juluapan coastal lagoon, a small wetland
(98 hectares) near Cuyutlán Lagoon. Currently, Study area: Juluapan Lagoon is a small
this coastal lagoon is affected by anthropogenic wetland that is permanently linked to the ocean
activities (tourism development, residual water through a 20 m wide by 75 m long artificial
discharge, badly planned urban development, canal. It is located on the Mexican Central
and the addition of nutrients from agricul- Pacific coast (19°06’ - 19°07’ N & 104°23’ -
tural activities) (Liñán-Cabello et al., 2016); it 104°24’ W), West of Santiago de Manzanillo
is therefore essential to establish the ecological Bay, Colima (Fig. 1). It has an approximate sur-
importance of this site for birds. The objective face of 98 ha and ranges between 0.2 m and 5
of this study was to analyze the richness and m in depth (Liñán-Cabello et al., 2016). To the
abundance (considering all birds in general and North of the lagoon, there are muddy substrates
by bird groups) of aquatic birds in Juluapan 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).
4 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)

to the South there are sand banks (Luna & aluminum boat with a 5-hp outboard motor
Zepeda, 1980). The margins of this wetland are was used at a navigation speed of less than 3
covered mainly by red mangrove (Rhizophora knots. Birds were counted along a transect par-
mangle) and white mangrove (Laguncularia allel to the inside edge of the lagoon, covering
racemosa) (Jiménez-Quiroz & González-Oroz- a 25-m wide band on each side of the transect.
co, 1996). The bottom of the lagoon is made up The observation area was 9.0 ha in zone 1 (tran-
of fine alternating stratifications of silt, clay, and sect length: 1 811 m; width: 50 m), 9.2 ha in
sand (Luna & Zepeda, 1980). The zone closest zone 2 (transect length: 1 842 m; width: 50 m);
to the beach and where there is communication and 8.9 ha in zone 3 (transect length: 1 779 m;
with the sea (labelled zone 1 in this study) is width: 50 m). Information on the number of
dominated by small plains of sandy substrate species and individuals was obtained during
that are exposed at low tide. This area is where counts, as well as on the type of substrate where
the influence of tourism and fishing activities birds were found (body of water, sand flat, mud
is greatest. The center of the lagoon (zone 2) flat, or mangrove); the activity undertaken by
is surrounded by mangroves and small muddy birds was also documented as feeding, resting,
areas, and is the area least affected by anthropo- or nesting.
genic activities. The northernmost part (zone The identified aquatic bird species were
3) is dominated by mangroves, as well as by separated into four functional groups, consid-
large areas of soft sediments that have been ering their morphological characteristics and
exposed by human activities. There is marked ecological affinity; seabirds (including the fol-
coastal urban growth in the northeast area, lowing families: Pelecanidae, Laridae, Frega-
where the El Naranjo campus of the University tidae, and Phalacrocoracidae) (Mellink & de la
of Colima and the Club Santiago residential Riva, 2005; Schreiber & Burger, 2001), ducks
development are located (zones 3 and 2, Fig.
and rails (Anatidae and Rallidae) (Hernán-
1); there are rural shellfish restaurants in the
dez-Vázquez, 2005a; Mellink & de la Riva,
Southeast, as well as tourism influence and
2005), shorebirds (Charadriidae, Recurvi-
a dock for smaller vessels (zone 1, Fig. 1);
rostridae, Scolopacidae, and Haematopodi-
whereas anthropogenic impact is minimal or
dae) (Alonzo-Parra, 2009; Mellink & de la
null in the Northern (zone 3) and Western
Riva, 2005; Warnock et al., 2001), and waders
(zones 2 and 3) areas. The Miramar stream is
(Ardeidae, Threskiornithidiae, and Ciconiidae)
located in the extreme Northeast; this stream
presents an important fluvial contribution from (Frederick, 2001, Mellink & de la Riva, 2005). A
agricultural and urban areas in the rainy season fifth group called “others” was created for this
(summer) that can modify littoral morphology study; it included birds that did not belong to
during the tropical cyclone season (Lancin & the previous groups (Anhingidae, Pandionidae,
Carranza, 1976; Liñán-Cabello et al., 2016). and Cerylidae).
Bird identification was performed using
Bird surveys: Monthly visits to Juluapan 10 x 50 binoculars and field guides by Hernán-
Lagoon were undertaken from June 2017 to dez-Vázquez and Esparza-Salas (2008), and
May 2018. Bird counts were performed during by the National Geographic Society (Dunn &
the lowest monthly tide in order to detect the Alderfer, 2017). Common names and scien-
greatest number of birds in the different envi- tific nomenclature were based on the Ameri-
ronments. The lagoon was divided into three can Ornithological Society (AOS; Chesser et
zones (1, 2, and 3, described in study area). al., 2021). Risk categories were determined
The same route was followed in each zone (30 according to the Official Mexican Norm NOM-
m from the inner edge of the lagoon) during 059-SEMARNAT-2019 (DOF, 2019) and the
each monthly visit; approximately 1.5 hours International Union for Conservation of Nature
were required to survey each zone. A 3-m long (IUCN, 2021).
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Data analysis: The density of species and lagoon and all birds), as well as for study areas
individuals was calculated to compare among and seasons of the year, as follows:
sampling zones (1, 2, and 3), according to
(Mandujano-Rodríguez, 2011): (Eq. 2)

D = n/2wL, (Eq. 1) where H’ is the Shannon diversity index, k is the

number of species, and pi is the proportion of
where D is density, n is the number of species or species i in the sample. Differences in diversity
individuals counted, L is transect length, and w values were obtained with Hutcheson’s “t” test
is transect width on each side of the center line. (Hutcheson, 1970).
The average number of species and num-
ber of individuals for each season (summer: RESULTS
June-August 2017, fall: September-November
2017, winter: December 2017-February 2018, Total richness and abundance: A total
and spring: March-May 2018) was obtained to of 53 species were identified, 5 750 individu-
compare between seasons. Fewer than 50 data als were recorded (considering all seasons and
points were obtained, so tests of normality were zones), and a total alpha diversity of H’= 3.10
performed; Shapiro-Wilks (W) and Bartlett was obtained. Of all recorded species, three are
tests were used to determine homogeneity of included in the IUCN Red List (IUCN, 2021)
variances. Nonparametric statistical tests were as Near Threatened (Egretta rufescens, Larus
used when data were not normal (P < 0.05), and heermanni, and Thalasseus elegans). Six spe-
parametric statistical tests were used when the cies are included under a protection category
normality assumption was met (P > 0.05). according to the Mexican Official Norm NOM-
A nonparametric Kruskal-Wallis (K-W) 059-SEMARNAT-2019 (DOF, 2019); two are
test was used to evaluate possible differences threatened (Calidris mauri and Limosa fedoa),
three are under special protection (L. heerman-
among zones (1, 2, and 3) in the number of
ni, T. elegans, and Mycteria americana), and one
species and number of individuals per group. A
is in danger of extinction (E. rufescens) (MS1).
one-way Analysis of Variance (ANOVA: F) was
The three species with highest number of
used to evaluate total bird density (considering
birds were: the black-bellied whistling duck
all groups), as data were normal (P > 0.05). A
(Dendrocygna autumnalis) (1 184 individuals;
Kruskal-Wallis test was used to evaluate dif-
20.59 % of the total), the white ibis (Eudo-
ferences in activity (feeding or resting) among cimus albus) (457 individuals; 7.95 % of the
zones, for all bird groups and for each group total), and the elegant tern (T. elegans) (371
separately. A one-way ANOVA was used to individuals; 6.45 % of the total). The number
analyze seasonal differences in the total num- of species per group ranged between 5 and 16;
ber of species and individuals (including all it was greater in shorebirds (16 species, 30.2
groups), and a Kruskal-Wallis test was used to % of the total) and waders (14 species, 26.4
perform the analysis for each group. A Mann- % of the total). All groups, excepting “others”,
Whitney (U) test was used to compare seasonal showed similar abundances; the most abun-
activities (feeding vs. resting) for the number of dant group were waders (1 531 individuals,
species and individuals (Zar, 2010). Statistical 26.6 %) and ducks and rails (1 470 individuals,
analyses were undertaken using the STATIS- 25.6 %) (Table 1). The most abundant waders
TICA program (v. 10, StatSoft, Inc., 2011), were E. albus, Nyctanassa violacea, and Egretta
considering a 0.05 significance level. caerulea, which together comprised 59 % of all
The Shannon-Weaver (H’) proportional individual records in this group. Dendrocygna
diversity index (Shannon & Weaver, 1949) was autumnalis represented 81 % of individuals in
used to calculate total diversity (for the entire the ducks and rails group (MS1).
6 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)

Table 1 between pairs indicated significant differences

Number of species and individuals of aquatic birds recorded between zone 1 vs zone 2 (t = 3.83, df = 553,
in Juluapan Lagoon.
P < 0.05) and 3 (t = 3.95, df = 3341, P < 0.05),
Species Individuals while zones 2 vs 3 were similar (t = 1.29, df =
Functional group
Number % Number % 431, P = 0.19).
Seabirds 10 18.9 1 306 22.7
Shorebirds 16 30.2 1 352 23.5 Activity by group and zone: Species rich-
Waders 14 26.4 1 531 26.6 ness was not associated with any particular
Ducks and rails 8 15.1 1 470 25.6 activity in the three lagoon zones (feeding
Others 5 9.4 91 1.6 K-W = 3.96, df = 2, P = 0.13; resting K-W =
Total 53 5 750 3.57, df = 2, P = 0.16); however, the analysis by

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).
Fig. 2. A. Species density, B. density of individuals, and
There were greater diversity values in zone C. Shannon diversity index with confidence intervals of
2 (H’ = 2.78) and 3 (H’ = 2.72) compared with aquatic bird groups in the three sampling zones in Juluapan
zone 1 (H’ = 2.58) (Fig. 2C). The comparisons Lagoon.
 Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024) 7

group showed that certain zones were used for were shorebirds and waders. This dominance
particular activities. For example, there were was observed during the four seasons of the
more seabirds resting on the sandy substrates year (Fig. 4A). However, there were significant
and shallow areas of the water body in zone 1. differences among seasons in the average num-
Shorebirds and waders used all substrates for ber of birds (F3,16=3.46, P=0.04), with greater
feeding and resting, although shorebirds were abundance in winter ( = 1 245 individuals) and
present in zone 2 to feed. Ducks and rails only spring ( = 561 records). The comparison by
used zone 3, where they fed and rested mainly group also detected significant differences in
in muddy areas (Fig. 3A). There was also great- bird abundance among seasons; seabirds (K-W
er seabird density in zone 1, where birds used = 8.15, df = 3, P = 0.042), ducks and rails (K-W
sandy substrates to rest. There was greater bird = 8.57, df = 3, P = 0.03), and shorebirds (K-W
density of other groups in zone 3, on muddy = 14.18, df = 3, P = 0.002). In all cases, there
substrates and shallow areas of the water body were more birds in winter ( = 265.5 seabirds,
that birds used to feed and to rest, to a lesser 351.5 shorebirds, and 225.7 ducks and rails)
extent. Ducks and rails used the muddy areas and spring ( = 118.2 seabirds and = 119.7 ducks
of zone 3 mainly to rest (Fig. 3B). and rails), whereas the number of waders was
not significantly different among seasons (K-W
Seasonal abundance and activity: The = 2.63, df = 3, P = 0.45) (Fig. 4B).
total number of species (considering all groups) There were no significant differences in
was similar among the four seasons (F3,16 = 0.90, the number of species between the two activi-
P = 0.90). Average species richness fluctuated ties (feeding vs. resting) for ducks and rails
between 11.3 species in summer and 14.7 spe- (U = 122.00, P = 0.82) and waders (U = 86.00,
cies in winter; the groups with most species P = 0.11), whereas there were significant

Fig. 3. A. Density of species and B. individuals, classified by zones, activity, and substrates. Red bar: feeding; orange bar;
resting. WB= Water Body, M= Mangrove, SF= Sand Flat, MF= Mud Flat.
8 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)

= 96.5, P = 0.23), ducks and rails (U = 125.5, P

= 0.92), and waders (U = 86.0, P = 0.11), except
for seabirds (U = 56.0, P = 0.006). Most birds
used Juluapan Lagoon to rest; this activity was
more common on muddy substrates during
winter and spring (Fig. 5B).
Diversity obtained by season of the year
varied from H’= 2.73 in winter to H’= 2.94 in
autumn, with significant differences between
seasons (Summer vs. Autumn, t = 2.41, df =
1678, P = 0.01; Summer vs. Winter, t = 3.07,
df = 1848, P = 0.002; Fall vs. Winter, t = 5.92,
df = 2144, P < 0.05; Fall vs. Spring, t = 2.58, df
= 2089, P = 0.01; Winter vs. Spring, t = 3.66,
df = 3874, P < 0.05), except between Spring
and Summer (t = 0.16, df = 1835, P = 0.87)
(Fig. 4C).

DISCUSSION

Although Juluapan Lagoon is relatively

small, its richness is comparable to that of larger
coastal wetlands, and its diversity is greater
than that of several wetlands in the Mexican
Central Pacific (Table 2). An example is Cuyut-
lán Lagoon, which has an area of 7 200 ha (73
times larger than Juluapan) and 57 aquatic bird
species during the non-reproductive season
(Mellink & de la Riva, 2005), which indicates
that Juluapan contributes importantly to aquat-
ic bird richness and diversity on the Colima
coast. Shorebirds and waders were the most
Fig. 4. A. Average number of species, B. individuals C. representative groups by number of species
and Shannon diversity index with confidence intervals of in Juluapan, which corresponds to a common
aquatic bird groups during the four sampling seasons in pattern observed in nearby wetlands, such as
Juluapan Lagoon. the Agua Dulce Lagoon, El Ermitaño Estuary
(Hernández-Vázquez, 2005a), and Barra de
differences for seabirds and shorebirds (U = Navidad Lagoon (Hernández-Vázquez et al.,
44.00, P = 0.001; U = 50.50, P = 0.003, respec- 2022). These wetlands present similar char-
tively). In the case of seabirds, there were more acteristics in terms of the availability of soft
species resting on all substrates; a similar pat- substrates exposed at low tides, dense vegeta-
tern was detected during all seasons. Shorebirds tion, and mangroves in the surrounding area,
used substrates to feed, mainly on muddy, which favors the presence of more birds, mainly
sandy substrates, and shallow waters of the shorebirds and waders.
lagoon; this activity was more common in fall Although the number individuals recorded
and winter (Fig. 5A). There was a similar pat- in the lagoon was not as high as that report-
tern for the number of birds, with no significant ed for nearby wetlands (Table 2), there was
differences between activities for shorebirds (U an important number of migratory species
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Fig. 5. A. Average number of species and B. individuals, classified by bird groups, seasons, substrates, and activity; green bars:
resting; blue bars: feeding. WB= Water Body; M= Mangrove, SF= Sand Flat, MF= Mud Flat.

in winter (31 species, MS1) that used this this species concentrates in coastal wetlands
lagoon as a resting and feeding place dur- when the reproductive season is over in Agua
ing their migratory journey to the North and Dulce Lagoon and El Ermitaño Estuary.
South of the continent. The shorebirds Tringa Species richness, density, and diversity
semipalmata and C. mauri, and some sea- of most bird groups were greater in zone 3,
birds such as T. elegans were among the most although diversity was also high in zone 2. This
abundant migratory species. D. autumnalis is zone presented shallow environments with a
considered a resident species and presented the large surface area of exposed mud flats during
greatest abundance, with 1 184 records (MS1). low tide and reduced impacts from tourism
Hernández-Vázquez (2005a) pointed out that or fishermen due to the difficult access. These
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Table 2
Number of aquatic bird species, individuals, and diversity recorded in coastal wetlands in the Mexican Central Pacific.

Area Records of Diversity

Wetlands Species Source of information
(ha) individuals H´
Barra de Navidad 375.98 68 16 469 3.351* Hernández-Vázquez et al., 2023,
Agua Dulce 696 78 66 976 2.601* Hernández-Vázquez, 2005a
Ermitaño 318 73 112 832 1.886* Hernández-Vázquez, 2005a
Chalacatepec 808 59 22 252 2.156* Hernández-Vázquez et al., 2010,
Hernández-Vázquez et al., 2014
Xola-Paraman 622 66 96 564 1.927* Hernández-Vázquez et al., 2010,
Hernández-Vázquez et al., 2014
Cuyutlán Lagoon 7 200 57 54 370 - Mellink & de la Riva, 2005
Juluapan Lagoon 98 53 5 750 3.10 This study
*Diversity calculated from the Hernandez-Vázquez (2005b) data for purposes of comparison with this work.

conditions influenced the fact that some indi- species, as was observed mainly for Fregata
viduals aggregated to rest and/or feed, as prey magnificens, P. occidentalis, and Nannopterum
capture is more effective in shallower areas brasilianum, and several wader species. These
(David, 1994). In some Jalisco wetlands, such results highlight the functional importance of
as La Manzanilla Estuary, Barra de Navidad mangroves for the life cycle of some species
Lagoon, and Agua Dulce Lagoon, as well as (Flores-Verdugo, 1989).
Cuyutlán Lagoon in Colima, the number of spe- The low species richness and individual
cies, number of individuals, and diversity were density values (zone 1 and 2) and diversity
influenced by variations in water levels caused values (zone 1) could be related to the charac-
by tide changes, and the existence of substrates teristics of their habitat, because soft substrata
suitable for foraging (Hernández-Vázquez, (sandy and muddy) for resting or feeding are
2000: Hernández-Vázquez, 2005a; Hernández- scarce, and there was also more frequent con-
Vázquez, 2005b; Hernández-Vázquez et al., tact with human activity, due to the proximity
2012; Mellink & de la Riva, 2005). of sandbanks where tourist activities are carried
The alpha-diversity composition of water- out. There is evidence of the negative effects
bird species fluctuated not only due to annual of human presence on the feeding and resting
changes in water levels (time), but also to activities of aquatic birds (Burger, 1981; Burger,
wetland specificities (space), reinforcing habi- 1994; Burger & Gochfeld, 1998), as it leads to a
tat selection Neotropical aquatic birds species decrease in feeding efficiency and resting time,
(Lima et al., 2021; Ronchi-Virgolini et al., resulting in greater energy spent to constantly
2009). The expanse of soft substrates was low escape humans (Burger, 1986). A similar pat-
in zone 2 due to the presence of a dense strip tern was observed in Barra de Navidad Lagoon,
of mangrove in its margin. This substrate was Jalisco, where bird richness and abundance
used for the construction of four N. violacea were affected in areas with greater anthropo-
nests and one Butorides virescens nest. During genic activity (presence of tourists and boat
later visits (eight visits from May to August traffic), which was more evident in the shore-
2018), approximately 64 nests of three wader bird group (Hernández-Vázquez et al., 2022).
species (N. violacea, B. virescens, and Cochle- There is a common pattern of greater spe-
arius cochlearius) were recorded (Hernández- cies and individual richness in winter in coastal
Vázquez et al., 2022); these data represent the wetlands of the Mexican Pacific. Several migra-
first reports of nesting in this lagoon. In addi- tory species arrive to rest and feed during this
tion to nesting, mangroves in zone 2 also pro- time of year, mainly on substrates that have
vided refuge and protection for several marine been exposed by the decrease in water levels.
 Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024) 11

For example, shorebirds were found mainly on place for resting, feeding, and reproduction for
sandy substrates and mud flats, whereas ducks resident birds. For migratory birds, it is a stop-
and rails chose open areas with submerged ping place to feed and rest during their migra-
vegetation and shallow areas with weak circu- tion to the North or South.
lation and low salinity (Hernández-Vázquez, The present study showed that aquatic
2000; Hernández-Vázquez, 2005a; Hernández- birds used Juluapan Lagoon for different eco-
Vázquez & Mellink, 2001; Hernández-Vázquez logical activities, with greater use of the North-
et al., 2010; Ysebaert et al., 2000). This coin- ern part of the lagoon, mainly in winter. We
cides with the characteristics of substrates used also provide basic information that reveals the
by shorebirds and ducks and rails during the importance of the different substrates that con-
cold season. This trend is a result of the migra- stitute this wetland, specifically mud flats and
tory movements of some bird species from sand flats that are exposed during low tides.
the Northern part of the continent; these spe- Therefore, we present evidence of the relevance
cies move towards wetlands located in Mexico of this body of water as a fundamental site for
and to the South of the continent to winter feeding and resting birds. It should be noted
(Recher, 1966). This study shows that C. mauri, that the species are migratory and that some
Himantopus mexicanus, T. semipalmata (shore- are greatly vulnerable. The presence of some
birds), Spatula clypeata, and S. discors (ducks species that are included under a protection
and rails) were among the most representative category in Mexico (six species) and interna-
migratory species that arrived in winter to tionally (3 species), evidences the need to apply
Juluapan Lagoon. conservation measures to this lagoon, and to
The presence of more migratory than resi- the species that live in it.
dent species, mainly in winter, is similar to what
was observed in Las Garzas Lagoon (Verdugo- Ethical statement: the authors declare that
Munguía & Gómez-del Castillo, 2012) and in they all agree with this publication and made
Cuyutlán Lagoon (Mellink & Riojas-López, significant contributions; that there is no con-
2008). The opposite occurred in the estuaries flict of interest of any kind; and that we fol-
of La Manzanilla, El Salado, and Rancho Bueno lowed all pertinent ethical and legal procedures
(Amador et al., 2006; Cupul-Magaña, 2000; and requirements. All financial sources are fully
Hernández-Vázquez, 2000), where there were and clearly stated in the acknowledgments sec-
more resident species reported. Low diver- tion. A signed document has been filed in the
sity values were caused by differences in the journal archives.
number of individuals of migratory and resi-
dent species during winter, since the Shannon- See supplementary material a03v72n1-MS1
Weaver index combines the number of species
and the relative abundance. The difference ACKNOWLEDGMENTS
between migratory and resident species could
be related to the particular characteristics of We thank the Marine Science Faculty
each wetland; it has been documented that (FACIMAR) of the University of Colima and
there are natural (local climate, lagoon surface, the Department of Studies of the Sustainable
variations in physical parameters, and produc- Development of the Coastal Zone, CUCSUR,
tivity) and anthropogenic (perturbations due to University of Guadalajara for logistical sup-
agriculture, residual discharge, deforestation, port. This study was financed by the CUCSUR,
silting, and tourism) factors that affect species University of Guadalajara, through research
richness and abundance (Hernández-Vázquez calls 2017 and 2018. This study was undertaken
et al., 2012; Mellink & Riojas-López, 2009; thanks to a collaboration agreement of two
Sánchez-Bon et al., 2010). Given the above, it academic groups: Marine and Coastal Ecol-
is evident that Juluapan Lagoon functions as a ogy of Ecosystems (743) of the University of
12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)

Guadalajara and Multidisciplinary Research dof.gob.mx/nota_detalle.php?codigo=5578808&fec

ha=14/11/2019.
in Aquatic Systems (95) of the University of
Colima. Thank you to Laura Sampson for her Dunn, J. L., & Alderfer, J. (2017). Field guide to the birds of
support in language edits. North America. National Geographic Books.

Flores-Verdugo, F. J. (1989). Algunos aspectos sobre la

ecología, uso e importancia de los ecosistemas de
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