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.

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).

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 Hutcheson’s “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.

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

group showed that certain zones were used for

particular activities. For example, there were

more seabirds resting on the sandy substrates

and shallow areas of the water body in zone 1.

Shorebirds and waders used all substrates for

feeding and resting, although shorebirds were

present in zone 2 to feed. Ducks and rails only

used zone 3, where they fed and rested mainly

in muddy areas (Fig. 3A). There was also great-

er seabird density in zone 1, where birds used

sandy substrates to rest. There was greater bird

density of other groups in zone 3, on muddy

substrates and shallow areas of the water body

that birds used to feed and to rest, to a lesser

extent. Ducks and rails used the muddy areas

of zone 3 mainly to rest (Fig. 3B).

Seasonal abundance and activity: The

total number of species (considering all groups)

was similar among the four seasons (F3,16 = 0.90,

P = 0.90). Average species richness fluctuated

between 11.3 species in summer and 14.7 spe-

cies in winter; the groups with most species

were shorebirds and waders. This dominance

was observed during the four seasons of the

year (Fig. 4A). However, there were significant

differences among seasons in the average num-

ber of birds (F3,16=3.46, P=0.04), with greater

abundance in winter ( = 1 245 individuals) and

spring ( = 561 records). The comparison by

group also detected significant differences in

bird abundance among seasons; seabirds (K-W

= 8.15, df = 3, P = 0.042), ducks and rails (K-W

= 8.57, df = 3, P = 0.03), and shorebirds (K-W

= 14.18, df = 3, P = 0.002). In all cases, there

were more birds in winter ( = 265.5 seabirds,

351.5 shorebirds, and 225.7 ducks and rails)

and spring ( = 118.2 seabirds and = 119.7 ducks

and rails), whereas the number of waders was

not significantly different among seasons (K-W

= 2.63, df = 3, P = 0.45) (Fig. 4B).

There were no significant differences in

the number of species between the two activi-

ties (feeding vs. resting) for ducks and rails

(U = 122.00, P = 0.82) and waders (U = 86.00,

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.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e52860, enero-diciembre 2024 (Publicado Ene. 23, 2024)

differences for seabirds and shorebirds (U =

44.00, P = 0.001; U = 50.50, P = 0.003, respec-

tively). In the case of seabirds, there were more

species resting on all substrates; a similar pat-

tern was detected during all seasons. Shorebirds

used substrates to feed, mainly on muddy,

sandy substrates, and shallow waters of the

lagoon; this activity was more common in fall

and winter (Fig. 5A). There was a similar pat-

tern for the number of birds, with no significant

differences between activities for shorebirds (U

= 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

representative groups by number of species

in Juluapan, which corresponds to a common

pattern observed in nearby wetlands, such as

the Agua Dulce Lagoon, El Ermitaño Estuary

(Hernández-Vázquez, 2005a), and Barra de

Navidad Lagoon (Hernández-Vázquez et al.,

2022). These wetlands present similar char-

acteristics in terms of the availability of soft

substrates exposed at low tides, dense vegeta-

tion, and mangroves in the surrounding area,

which favors the presence of more birds, mainly

shorebirds and waders.

Although the number individuals recorded

in the lagoon was not as high as that report-

ed for nearby wetlands (Table 2), there was

an important number of migratory species

Fig. 4. A. Average number of species, B. individuals C.

and Shannon diversity index with confidence intervals of

aquatic bird groups during the four sampling seasons in

Juluapan Lagoon.

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

in winter (31 species, MS1) that used this

lagoon as a resting and feeding place dur-

ing their migratory journey to the North and

South of the continent. The shorebirds Tringa

semipalmata and C. mauri, and some sea-

birds such as T. elegans were among the most

abundant migratory species. D. autumnalis is

considered a resident species and presented the

greatest abundance, with 1 184 records (MS1).

Hernández-Vázquez (2005a) pointed out that

this species concentrates in coastal wetlands

when the reproductive season is over in Agua

Dulce Lagoon and El Ermitaño Estuary.

Species richness, density, and diversity

of most bird groups were greater in zone 3,

although diversity was also high in zone 2. This

zone presented shallow environments with a

large surface area of exposed mud flats during

low tide and reduced impacts from tourism

or fishermen due to the difficult access. These

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.

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

conditions influenced the fact that some indi-

viduals aggregated to rest and/or feed, as prey

capture is more effective in shallower areas

(David, 1994). In some Jalisco wetlands, such

as La Manzanilla Estuary, Barra de Navidad

Lagoon, and Agua Dulce Lagoon, as well as

Cuyutlán Lagoon in Colima, the number of spe-

cies, number of individuals, and diversity were

influenced by variations in water levels caused

by tide changes, and the existence of substrates

suitable for foraging (Hernández-Vázquez,

2000: Hernández-Vázquez, 2005a; Hernández-

Vázquez, 2005b; Hernández-Vázquez et al.,

2012; Mellink & de la Riva, 2005).

The alpha-diversity composition of water-

bird species fluctuated not only due to annual

changes in water levels (time), but also to

wetland specificities (space), reinforcing habi-

tat selection Neotropical aquatic birds species

(Lima et al., 2021; Ronchi-Virgolini et al.,

2009). The expanse of soft substrates was low

in zone 2 due to the presence of a dense strip

of mangrove in its margin. This substrate was

used for the construction of four N. violacea

nests and one Butorides virescens nest. During

later visits (eight visits from May to August

2018), approximately 64 nests of three wader

species (N. violacea, B. virescens, and Cochle-

arius cochlearius) were recorded (Hernández-

Vázquez et al., 2022); these data represent the

first reports of nesting in this lagoon. In addi-

tion to nesting, mangroves in zone 2 also pro-

vided refuge and protection for several marine

species, as was observed mainly for Fregata

magnificens, P. occidentalis, and Nannopterum

brasilianum, and several wader species. These

results highlight the functional importance of

mangroves for the life cycle of some species

(Flores-Verdugo, 1989).

The low species richness and individual

density values (zone 1 and 2) and diversity

values (zone 1) could be related to the charac-

teristics of their habitat, because soft substrata

(sandy and muddy) for resting or feeding are

scarce, and there was also more frequent con-

tact with human activity, due to the proximity

of sandbanks where tourist activities are carried

out. There is evidence of the negative effects

of human presence on the feeding and resting

activities of aquatic birds (Burger, 1981; Burger,

1994; Burger & Gochfeld, 1998), as it leads to a

decrease in feeding efficiency and resting time,

resulting in greater energy spent to constantly

escape humans (Burger, 1986). A similar pat-

tern was observed in Barra de Navidad Lagoon,

Jalisco, where bird richness and abundance

were affected in areas with greater anthropo-

genic activity (presence of tourists and boat

traffic), which was more evident in the shore-

bird group (Hernández-Vázquez et al., 2022).

There is a common pattern of greater spe-

cies and individual richness in winter in coastal

wetlands of the Mexican Pacific. Several migra-

tory species arrive to rest and feed during this

time of year, mainly on substrates that have

been exposed by the decrease in water levels.

Tabl e 2

Number of aquatic bird species, individuals, and diversity recorded in coastal wetlands in the Mexican Central Pacific

Wet l ands Area Species Records of

individuals

Diversity Source of information

(ha) 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.

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

For example, shorebirds were found mainly on

sandy substrates and mud flats, whereas ducks

and rails chose open areas with submerged

vegetation and shallow areas with weak circu-

lation and low salinity (Hernández-Vázquez,

2000; Hernández-Vázquez, 2005a; Hernández-

Vázquez & Mellink, 2001; Hernández-Vázquez

et al., 2010; Ysebaert et al., 2000). This coin-

cides with the characteristics of substrates used

by shorebirds and ducks and rails during the

cold season. This trend is a result of the migra-

tory movements of some bird species from

the Northern part of the continent; these spe-

cies move towards wetlands located in Mexico

and to the South of the continent to winter

(Recher, 1966). This study shows that C. mauri,

Himantopus mexicanus, T. semipalmata (shore-

birds), Spatula clypeata, and S. discors (ducks

and rails) were among the most representative

migratory species that arrived in winter to

Juluapan Lagoon.

The presence of more migratory than resi-

dent species, mainly in winter, is similar to what

was observed in Las Garzas Lagoon (Verdugo-

Munguía & Gómez-del Castillo, 2012) and in

Cuyutlán Lagoon (Mellink & Riojas-López,

2008). The opposite occurred in the estuaries

of La Manzanilla, El Salado, and Rancho Bueno

(Amador et al., 2006; Cupul-Magaña, 2000;

Hernández-Vázquez, 2000), where there were

more resident species reported. Low diver-

sity values were caused by differences in the

number of individuals of migratory and resi-

dent species during winter, since the Shannon-

Weaver index combines the number of species

and the relative abundance. The difference

between migratory and resident species could

be related to the particular characteristics of

each wetland; it has been documented that

there are natural (local climate, lagoon surface,

variations in physical parameters, and produc-

tivity) and anthropogenic (perturbations due to

agriculture, residual discharge, deforestation,

silting, and tourism) factors that affect species

richness and abundance (Hernández-Vázquez

et al., 2012; Mellink & Riojas-López, 2009;

Sánchez-Bon et al., 2010). Given the above, it

is evident that Juluapan Lagoon functions as a

place for resting, feeding, and reproduction for

resident birds. For migratory birds, it is a stop-

ping place to feed and rest during their migra-

tion to the North or South.

The present study showed that aquatic

birds used Juluapan Lagoon for different eco-

logical activities, with greater use of the North-

ern part of the lagoon, mainly in winter. We

also provide basic information that reveals the

importance of the different substrates that con-

stitute this wetland, specifically mud flats and

sand flats that are exposed during low tides.

Therefore, we present evidence of the relevance

of this body of water as a fundamental site for

feeding and resting birds. It should be noted

that the species are migratory and that some

are greatly vulnerable. The presence of some

species that are included under a protection

category in Mexico (six species) and interna-

tionally (3 species), evidences the need to apply

conservation measures to this lagoon, and to

the species that live in it.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

See supplementary material a03v72n1-MS1

ACKNOWLEDGMENTS

We thank the Marine Science Faculty

(FACIMAR) of the University of Colima and

the Department of Studies of the Sustainable

Development of the Coastal Zone, CUCSUR,

University of Guadalajara for logistical sup-

port. This study was financed by the CUCSUR,

University of Guadalajara, through research

calls 2017 and 2018. This study was undertaken

thanks to a collaboration agreement of two

academic groups: Marine and Coastal Ecol-

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

in Aquatic Systems (95) of the University of

Colima. Thank you to Laura Sampson for her

support in language edits.

REFERENCES

Alonzo-Parra, D. E. (Ed). (2009). Guía para la identificación

de chorlos y playeros en México (2ª Edición). Ducks

Unlimited de México, A.C.

Amador, E., Mendoza-Salgado, R., & de Anda-Montañez, J.

A. (2006). Estructura de la avifauna durante el perio-

do invierno-primavera en el Estero Rancho Bueno,

Baja California Sur, México. Revista Mexicana de

Biodiversidad, 77(2), 251‒259.

Batzer, D. P., & Shartitz, R. R. (2007). Ecology of freshwater

and estuarine wetlands. Ecology of Freshwater and

Estuarine Wetlands. University of California Press.

Burger, J. (1981). The effect of human activity on birds at a

coastal bay. Biological Conservation, 21(3), 231‒241.

Burger, J. (1986). The effect of human activity on shorebirds

in two coastal bays in northeastern Unites States.

Environmental Conservation, 13(2), 123‒130.

Burger, J. (1994). The effect of human disturbance on fora-

ging behavior and habitat use in piping plover (Cha-

radrius melodus). Estuaries, 17(3), 695‒701.

Burger, J., & Gochfeld, M. (1998). Effects of ecotourists on

bird behavior at Loxahatchee National Wildlife Refu-

ge, Florida. Environmental Conservation, 25(1), 13‒21.

Chesser, R. T., Billerman, S. M., Burns, K. J., Cicero, C.,

Dunn, J. L., Hernández-Baños, B. E., Kratter, A. W.,

Lovette, I. J., Mason, N. A., Rasmussen, P. C., Remsen,

J. V., Stotz, D. F., & Winker, K. (2021). Sixty-second

Supplement to the American Ornithological Society’s

Check-list of North American Birds. Ornithology,

138(3), 1‒18.

Cupul-Magaña, F. G. (2000). Aves acuáticas del estero El

Salado, Puerto Vallarta, Jalisco. Huitzil, 1(1), 3‒8.

David, P. G. (1994). Wading bird use of lake Okeechobee

relative to fluctuating water levels. The Wilson Bulle-

tin, 106(4), 719‒732.

DOF (Diario Oficial de la Federación). (2019). Modifi-

cación del Anexo Normativo III, Lista de especies en

riesgo de la Norma Oficial Mexicana NOM-059-SE-

MARNAT-2010, Protección ambiental-Especies nativas

de México de flora y fauna silvestres-Categorías de

riesgo y especificaciones para su inclusión, exclusión

o cambio-Lista de especies en riesgo, publicada el 30

de diciembre de 2010. Diario Oficial de la Federa-

ción 17 de noviembre de 2020, México. http://www.

dof.gob.mx/nota_detalle.php?codigo=5578808&fec

ha=14/11/2019.

Dunn, J. L., & Alderfer, J. (2017). Field guide to the birds of

North America. National Geographic Books.

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

ecología, uso e importancia de los ecosistemas de

manglar. En J. de la. Rosa-Vélez, & F. González-

Farías (Eds.), Temas de Oceanografía Biológica en

México (pp. 21‒56). Universidad Autónoma de Baja

California.

Frederick, P. C. (2001). Wading birds in the marine envi-

ronment. In E. A. Schreiber, & J. Burger (Eds.), Biolo-

gy of Marine Birds (pp. 618‒655). CRC Press.

Hernández-Vázquez, S. (2000). Aves acuáticas del estero la

Manzanilla, Jalisco, México. Acta Zoológica Mexicana,

(80), 143‒153.

Hernández-Vázquez, S. (2005a). Aves acuáticas de la Lagu-

na de Agua Dulce y el Estero El Ermitaño, Jalisco,

México. Revista de Biología Tropical, 53(1-2), 229‒238.

Hernández-Vázquez, S. (2005b). Aves estuarinas de la costa

de Jalisco, México: análisis de la comunidad, repro-

ducción e identificación de áreas de importancia para

la conservación de las aves (Tesis doctoral). Instituto

Politécnico Nacional, Centro Interdisciplinario de

Ciencias Marinas, México.

Hernández-Vázquez, S., Bojórquez-Castro, J. M., Gonzá-

lez-Zamora, D. A., Hernández-Vázquez, F., Rojo-

Vázquez, J. A., & Galván-Piña, V. H. (2014). Ecología

de aves acuáticas. En J. L. Cifuentes Lemus, & F. G.

Cupul Magaña (Eds.), Temas sobre Investigaciones

Costeras (pp. 214‒243, 1ª Ed.). Editorial Universidad

de Guadalajara.

Hernández-Vázquez, S., & Esparza-Salas, R. (2008). Sal

a pajarear: guía de campo: aves de la península El

Tamarindo y áreas aledañas. Fundación de la Costa

de Jalisco, México.

Hernández-Vázquez, S., González-Sansón, G., Aguilar-

Betancourt, C. A., & Castillo-Guerrero, J. A. (2022).

Asociaciones espaciales y temporales de aves acuáti-

cas durante los ciclos de mareas diurnos, en la laguna

costera Barra de Navidad, del Pacífico central mexica-

no. Revista de Biología Marina y Oceanografía, 57(2).

https://doi.org/10.22370/rbmo.2022.57.2.3527

Hernández-Vázquez, S., & Mellink, E. (2001). Coastal

waterbirds of El Chorro and Majahuas, Jalisco, Méxi-

co, during the non-breeding season, 1995-1996.

Revista de Biología Tropical, 49(1), 359‒367.

Hernández-Vázquez, S., Rodríguez-Estrella, R., Vega-Rive-

ra, J. H., Hernández-Vázquez, F., Rojo-Vázquez, J. A.,

& Galván-Piña, V. H. (2010). Estructura, dinámica

y reproducción de las asociaciones de aves acuáti-

cas de la costa de Jalisco, México. En E. Godínez-

Domínguez, C. Franco-Gordo, J. A. Rojo-Vázquez,

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

F. Silva-Bátiz, & G. González-Sansón (Eds.), Eco-

sistemas marinos de la costa Sur de Jalisco y Colima

(pp.151‒188). Universidad de Guadalajara, Centro

Universitario de la Costa Sur.

Hernández-Vázquez, S., Serrano, S., Hernández, X. A., &

Robles, M. I. (2012). Variación temporal y espacial de

aves playeras en la laguna Barra de Navidad, Jalisco,

en tres temporadas no reproductivas. Revista de Bio-

logía Tropical, 60(3), 1317‒1326.

Howes, J., & Bakewell, D. (1989). Shorebird Studies Manual.

Asian Wetland Bureau Publication No. 55, Kuala

Lumpur, Malaysia.

Hutcheson, K. (1970). A test for comparing diversities

based on the Shannon formula. Journal of Theoretical

Biology, 29, 151‒154.

IUCN. (2021). The IUCN Red List of Threatened Species

(Version 2021-3). Recuperado 13 de abril de 2021, de

https://www.iucnredlist.org

Jiménez-Quiroz, C., & González-Orozco, F. (1996). Análisis

de la estructura del manglar de la laguna de Juluapan,

Col., México. Ciencia Pesquera, 12, 76‒84.

Kushlan, J. A., Steinkamp, M. J., Parsons, K. C., Capp, J.,

Cruz, M. A., Coulter, M., & Erwin, R. M. (2002).

Waterbird conservation for the Americas: The North

American waterbird conservation plan (version 1). U.

S. Fish and Wildlife Service, USA.

Lancin, M., & Carranza, E. A. (1976). Estudio geomorfoló-

gico de la bahía y de la playa de Santiago en Manzani-

llo, Colima. Revista Mexicana de Ciencias Geológicas,

2, 43‒66.

Lima, B. M., Ragusa-Netto, J., Donatelli, R. J., & Posso, S. R.

(2021). Composition and spatio-temporal dynamics

of aquatic bird community in humid areas of Alto

Parana Atlantic Forest. Brazilian Journal of Biology,

84, 1‒10. https://doi.org/10.1590/1519-6984.251438

Liñán-Cabello, M. A., Olivos-Ortiz, A., Quijano-Scheggia,

S., Anguiano, D. M., Reséndiz-Flores, M. L., & Orte-

ga-Ortiz, C. D. (2016). Effects of terrestrial runoff

on the coral communities in Santiago Bay, Colima,

Mexican Pacific Coast. Revista de Biología Tropical,

64(3), 1185‒1200.

Luna, J. R., & Zepeda, J. A. (1980). Hidrología y estratigrafía

de la Laguna de Juluapan, Col. Dirección General de

Oceanografía. Instituto Oceanográfico, México.

Mandujano-Rodríguez, S. (2011). Conceptos generales de

ecología poblacional en el manejo de fauna silvestre.

En S. Gallina-Tessaro, & C. A. López-González (Eds.),

Manual de técnicas para el estudio de la fauna (Vol.

I, pp. 37‒60). Universidad Autónoma de Querétaro-

Instituto de Ecología, A. C.

Mellink, E., & de la Riva, G. (2005). Non-breeding water-

birds at Laguna de Cuyutlán and its associated

wetlands, Colima, México. Journal of Field Ornitho-

logy, 76(2), 158‒167.

Mellink, E., Palacios, E., & Amador, E. (2007). Colonies of

four species of terns and the black skimmer in wes-

tern Mexico. Waterbirds, 30(3), 358‒366.

Mellink, E., & Riojas-López, M. E. (2006). Nesting of

Forster’s tern in a tropical coastal lagoon, Cuyutlán,

Colima, Mexico. Western Birds, 37(1), 45‒47.

Mellink, E., & Riojas-López, M. E. (2008). Waterbirds

(other than Laridae) nesting in the middle section of

Laguna Cuyutlán, Colima, México. Revista de Biología

Tropical, 56(1), 391‒397.

Mellink, E., & Riojas-López, M. E. (2009). Waterbirds and

human-related threats to their conservation in Lagu-

na Cuyutlán, Colima, México. Revista de Biología

Tropical, 57(1-2),1‒12.

Mellink, E., Riojas-López, M. E., & Luévano, J. (2009a). Bre-

eding locations of seven Charadriiformes in coastal

southwestern Mexico. Waterbirds, 32(1), 44‒53.

Mellink, E., Riojas-López, M. E., Luévano, J., & Wheeler,

J. A. (2009b). Historic changes in mid-winter use

of Laguna Cuyutlán, Colima, México, by waterfowl.

Ornitología Neotropical, 20(2),171‒179.

Mitsch, W. J., & Gosselink, J. G. (2007). Wetlands (4th Edi-

tion). John Wiley & Sons, Inc.

Palacios, E., Escofet, A., & Loya-Salinas, D. H. (1991). El

estero de Punta Banda, B.C., México como eslabón del

“Corredor del Pacífico”: abundancia de aves playeras.

Ciencias Marinas, 17(3), 109‒131.

Recher, H. F. (1966). Some aspects of the ecology of migrant

shorebirds. Ecology, 47(3), 393‒407.

Riojas-López, M. E., & Mellink, E. (2016). A New Wood

Stork (Mycteria americana) Colony in Western Méxi-

co. Waterbirds, 39(1), 104‒107.

Ronchi-Virgolini, A. L., Beltzer, A. H., & Manzano, A.

S. (2009). Bird communities in wetlands along the

Lower Paraná River, Entre Ríos, Argentina. Avian

Biology Research, 1(4), 153‒163. http://dx.doi.

org/10.3184/175815508X404282

Sánchez-Bon, G., Fernández, G., Escobedo-Urías, D.,

Torres-Torner, J., & Cid-Becerra, J. A. (2010). Com-

posición espacial y temporal de la avifauna de las islas

de barrera del complejo lagunar San Ignacio-Nava-

chiste-Macapule, Sinaloa, México. Ciencias Marinas,

36(4), 355‒370.

Schreiber, E. A., & Burger, J. (2001). Seabirds in the marine

environment. In E. A. Schreiber & J. Burger (Eds.),

Biology of Marine Birds (pp. 1‒16). CRC Press.

Shannon, C. E., & Weaver, W. (1949). The mathematical

theory of communication. University of Illinois Press.

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

Shealer, D. A. (2001). Foraging behavior and food of sea-

birds. In E. A. Schreiber, & J. Burger (Eds.), Biology of

Marine Birds (pp. 137‒177). CRC Press.

StatSoft, Inc. (2011) STATISTICA (Data Analysis Software

System, Version 10). StatSoft Inc. http://www.statsoft.

com

Vega-Rivera, J. H., Santana, E., Hernández-Vázquez, S.,

& Verdugo-Munguía, H. (2016). Aves. En La Biodi-

versidad en Colima. Estudio de Estado (pp.445‒461).

CONABIO.

Verdugo-Munguía, H., & Gómez-del Castillo, E. A. (2012).

Catálogo de aves, Laguna Las Garzas, Manzanillo,

Colima (Documento Técnico). México.

Warnock, N., Elphick, C., & Rubega, M. A. (2001). Shore-

birds in the marine environment. In E. A. Schreiber, &

J. Burger (Eds.), Biology of marine birds (pp. 581‒615).

CRC Press.

Ysebaert, T., Meininger, P. L., Meire, P., Devos, K., Berre-

voets, C. M., Strucker, R. C. W., & Kuijken, E. (2000).

Waterbird communities along the estuarine salinity

gradient of the Schelde estuary, NW-Europe. Biodi-

versity and Conservation, 9(9), 1275‒1296.

Zar, J. H. (2010). Multisample hypotheses and the analy-

sis of variance. En Biostatistical Analysis (5a ed.,

pp.189‒224). Pearson Prentice Hall.