The Biologist
(Lima)
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
WATERBIRDS OF PÍRITU LAGOON, VENEZUELA, AS A KEY ELEMENT FOR ITS LEGAL
RESTORATION AND MANAGEMENT: A PRELIMINARY STUDY
AVES ACUÁTICAS DE LA LAGUNA DE PÍRITU, COMO ELEMENTO CLAVE PARA SU
RESTAURACION Y MANEJO LEGAL: UN ESTUDIO PRELIMINAR
1Postgrado del Instituto Oceanográco de Venezuela, Universidad de Oriente, Cumaná, Venezuela.
2Laboratorio de Ecología de Aves, Departamento de Biología, Universidad de Oriente, Cumaná, Venezuela.
3Centro de Investigaciones Ecológicas Guayacán, Universidad de Oriente, Venezuela.
Post Address: Urbanización Villa Olímpica, Bloque 03, Apto. 01-03, Cumaná, State of Sucre, Venezuela.
*Corresponding author: E-mail: gediom@yahoo.com
1 2 3
Steffani Olivares-Márquez ; Gedio Marín-Espinoza * & Jorge Muñoz-Gi
ABSTRACT
Key words: abundance – aquatic birds – coastal wetland – diversity – richness
Coastal lagoons ecosystems in Venezuela are recognized as important habitats for birds. However the
seasonal community of these waterbird communities and factors influencing the use of these wetlands
habitats have not been sufficiently studied. We estimated waterbird richness and individual abundance in
the Píritu lagoon, state of Anzoátegui, in the channel area leading out to the sea from monthly surveys
conducted during August to November 2015 and January 2016. Overall, we recorded 45 waterbird
species, belonging to 12 families. Richness was lesser in August, greater in November following the
inflow of Nearctic migrants. Waterbird families with the most number of species included Scolopacidae
(12 spp.), Ardeidae (10 spp.) and Laridae (9 spp.). Six species accounted for 78.44% of all individuals
detected (Pelecanus occidentalis L. 1758, Thalasseus maximus Boddaert 1783, Ardea alba L. 1758,
Sterna hirundo L. 1758, Phalacrocorax brasilianus Gmelin 1789 and Phaetusa simplex Gmelin 1789).
Diversity and evenness indices varied moderately from 2.41 to 3.14 and 0.55 to 0.69, respectively.
Shallow waters habitats (<0.5 m depth) contributed to high waterbird richness in this lagoon, around
which many people live. Long term investigations are essential to formulate management and
conservation plans for waterbird species. The integrity of the Píritu lagoon ecosystem may not survive the
next decades unless more citizens engage in its conservation. We propose protection and integrated
management through cooperative action of the two municipalities sharing the Píritu lagoon.
The Biologist (Lima)
ISSN Versión Impresa 1816-0719
ISSN Versión en linea 1994-9073 ISSN Versión CD ROM 1994-9081
41
The Biologist (Lima), 201 , 1 ( ), - : 9 7 1 ene jun 41-50
RESUMEN
Palabras clave: abundancia – aves acuáticas – diversidad – humedal costero – riqueza
En Venezuela, los ecosistemas de lagunas costeras están reconocidos como hábitat importantes para las
aves. No obstante, la dinámica estacional en la comunidad de aves acuáticas y los factores que la
condicionan no ha sido suficientemente estudiada. Se estimó la abundancia individual y riqueza de
especies en el área del canal que conduce hacia el mar de la Laguna de Píritu, estado Anzoátegui,
mediante inventarios mensuales desarrollados desde agosto a noviembre de 2015 y enero de 2016. En
total se registraron 45 especies de aves acuáticas pertenecientes a 12 familias. La riqueza fue menor en
agosto y mucho mayor en noviembre, debido al arribo de especies migratorias del Neártico. Las familias
con mayor número de especies fueron Scolopacidae (12 spp.), Ardeidae (10 spp.) y Laridae (9 spp.). Seis
especies acumularon el 78,44% del total de la abundancia (Pelecanus occidentalis L. 1758, Thalasseus
maximus Boddaert 1783, Ardea alba L. 1758, Sterna hirundo L. 1758, Phalacrocorax brasilianus Gmelin
1789 y Phaetusa simplex Gmelin 1789). La diversidad y equitabilidad variaron moderadamente: de 2,41 a
3,14 y 0,55 a 0,69, respectivamente. Los hábitat de aguas someras (<0,5 m de profundidad) aportaron la
más alta contribución a la riqueza de especies en esta laguna, alrededor de la cual habita una gran cantidad
de personas. Investigaciones a largo plazo serán vitales para formular planes de manejo y conservación de
las aves acuáticas que utilizan la laguna. La integridad y supervivencia de los ecosistemas de la Laguna de
Píritu se verá comprometida en las próximas décadas si la mayoría de sus ciudadanos no se involucra en su
conservación. Se propone la protección ambiental de la laguna de Píritu mediante el manejo cooperativo
por parte de los dos gobiernos municipales que comparten este importante humedal.
INTRODUCTION
42
Waterbirds, comprising a large group of species
including Anseriformes, Ardeiformes,
Charadriiformes, Gaviiformes, Gruiformes,
Pelec an iform es , Pho eni co pteri fo rmes,
Podicipediformes and Procellariformes, exploit
coastal lagoons given the diversity of habitats for
feeding, nesting and resting. Waterbirds
communities experience seasonal and anual
fluctuations in abundance and species
composition. Variations may be associated with the
habitat characteristics and the arrival of seasonal
migratory species (Brown & Dinsmore, 1986;
Elmberg et al., 1994; Gimenes & dos Anjos, 2003).
Abundance of invertebrates and fishes (Mercier &
McNeil, 1994; Paszkowski & Tonn, 2000; Shealer,
2002; Marín et al., 2003) are major factors
contributing to the distribution and density of
waterbird populations. Finally, human disturbance
can has a considerable effect on the numbers of
waterbirds using a site and in some circumstances
may have consequences for the size of populations
(Robinson & Cranswick, 2003).
Given the documented species-habitat
relationships of waterbirds and wetlands, they are
an important useful taxonomic group to monitor
The ecological dynamic of coastal lagoons is
influenced by the exchange processes between
freshwater inputs and the adjacent sea (Kennish &
Paerl, 2010). Coastal lagoon ecosystems located
along densely populated areas in developing
countries render these systems among the most
threatened in the world. Disorganized human
occupation around impacts coastal lagoons
through eutrophication, salinization, exotic species
introduction, imposing stressors on the
biodiversity of these wetlands (Gattenlöhner et al.,
2004; Nagarajan & Thiyagesan, 2006; Esteves et
al., 2008; Lloret et al., 2008; Marín & Marín, 2011;
Newton et al., 2014).
Waterbirds represent one of the best monitored
biological components of coastal lagoons and other
transitional coastal waters. Moreover, the
functional role of waterbirds as bioindicators of
enviromental changes has been discussed in
previous studies (Kushlan, 1993; Comin &
Herrera-Silveira, 2000; Amat & Green, 2010;
Farinós & Robledano, 2010).
Olivares-Márquez et al.
The Biologist (Lima). Vol. 17, Nº1, ene - jun 2019
43
given their value as indicators of ecosystem
conditions and as tools (Bibby et al., 2002; USEPA
EPA, 2002; Hollamby et al., 2006; Sekercioglu,
2006; Esteves et al., 2008; Conway, 2011).
The importance of Venezuelan coastal lagoons as
waterbird habitats have been reported by previous
authors (McNeil et al., 1985; Rodner, 2006; Marín
& Marín, 2011). However, the seasonal dynamics
of the waterbird community of waterbird species in
the Píritu lagoon, a site of regional importance for
birds (BirdLife International and Conservation
International, 2005), and the factors influencing
wetland have not been studied. Our objective in
this study was to generate information on the
ecological characteristics of this wetland and
seasonal variation of abundance and richness of
waterbirds, as a key element for its legal restoration
and management. We discuss the conservation
implications of our findings, and hope they serve to
formulate the rationale for its legal restoration and
management.
Study site
Píritu lagoon, located in Anzoátegui state
(10°02′~10°03′N and 65°00′~65°09′ W) is
the second largest saltwater continental lagoon in
notheastern Venezuela (Fig. 1). The open water
2
covers ca. 2600 km ; surrounded by an extense area
of mangroves (Rhizophora mangle L. 1753 and
Avicennia germinans L. 1753). Like most lagoons
located in the Venezuelan northeastern coast, Píritu
lagoon is separated from the sea by a narrow sand
barrier (ca. 13.5 km in lenght) which is ca. 390 m at
its widest sector and ca. 250 m at its narrowest
portion, with a xeric and psamophilic vegetation.
There is only one outlet to sea at the northeastern
sector of the lagoon. Mean annual rainfall
pluviosity is 700 mm peaking during the rainy
season months between June and November and
high temperature, i.e., Min/Max: 27-32°C
(González, 1987; Rodríguez & González, 2001).
The lagoon volume varies throughout the day
because the marine water tidal input through the
mouth. This oulet was partially refilled reducing
marine water influx (Suárez, 1994). The main
freshwater inputs to the lagoon are direct rainfall,
sewage spills and surface runoff. One shrimp farm,
located on the western end of the lagoon has altered
its natural hydrodynamic. In addition, artisanal
fishing and tourism boating remain uncontrolled
(Ramírez et al., 1986; Bravo & Silva, 2012; Suárez,
2016).
Field methods
We surveyed birds using line transects with aid of a
boat (according to Bibby et al., 2000), with which
the lagoon channel leading out to the sea (length:
ca. 1,9 km, width: ca. 100 m) (Fig. 2). Waterbird
observations were made along a ca. 3.5 km
continuous transect covering both lagoon north and
south borders. Transparency and salinity were
measured, in the morning (always beginning two
hours after sunrise) and in the afternoon (always
beginning two hours after midday), every ca. 300
m in five stations (Fig. 2), using a Secchi disk and
refractometer, respectively.
We estimated waterbird richness and abundance
using binoculars (Celestron Outland 10x42) during
counts. Surveys were conducted in August,
September, October, November 2015 (rainy
season) and January 2016 (transition rainy-dry
season). Monthly surveys were conducted in the
morning (beginning two hours after sunrise), each
sighted bird was identified to species (AOU, 1983;
Hilty, 2003) and status recorded (resident, nearctic
migrant, intratropical migrant, local migrant).
Individuals flying were not recorded, unless these
were observed leaving from the lagoon or landing
in it.
Relative abundance was obtained by dividing the
number of individuals registered a the given month
overall all individuals periods. The monthly data
abundance was pooled to compare species
composition and eveness in each month, estimated
using Simpson's Diversity Index (Krebs, 1989;
Moreno, 2001). Simpson's Index gives more
weight to the more abundant species in a sample.
The taxonomy, nomenclature and common names
of the bird species were according to Verea et al.
(2017).
Ethic aspects
Authors indicate that procedures followed ethical
standards of the country.
MATERIALS AND METHODS
waterbirds of Píritu Lagoon, Venezuela
The Biologist (Lima). Vol. 17, Nº1, ene - jun 2019
44
(Tringa melanoleuca Gmelin 1789) and Lesser
Yellowlegs (Tringa flavipes Gmelin 1789)
exploited water depths less than 10 cm for feeding,
while the relatively big egrets and herons fed in
water up to 17 cm deep (Ardea spp., Egretta spp.),
or they fed on the mangroves at the branches near
the water (mainly, Butorides striatus L. 1758 and
Nycticorax spp.).
Roosting sites comprised dry mud banks within the
lagoon, and mangroves. Herons, egrets, Brown
Pelican and Olivaceus Cormorant roosted
commonly on mangroves branches, or structures
such as sticks used by fishermen for fishingworks.
All the tern and gull species used the exposed mud
banks of the lagoon as roosting habitat (Figure 1)
and foraged mainly at sea; however, Large-billed
Tern, Least Tern (Sternula antillarum Lesson
1847), Common Tern (Sterna hirundo) and
Laughing Gull (Leucophaeus atricilla L. 1758)
sometimes foraged on the lagoon.
During the study period, monthly and spatial
patterns of waterbirds were distinct. The local
abundance and composition of waterbird
assemblages seemed to be affected by the interplay
of several environmental and human factors.
The seasonal pattern in individuals and species
observed coincides with expected fluctuations due
to regional movements and interhemispheric
migration (Brandolin & Blendinger, 2016).
Additionally, differences in abundance and
richness values may be related to variations in tidal
regimens (Ma et al., 2010; Calle et al., 2016).
Water depth and clear water phases are also
important (Kushlan, 1986; David, 1994; Lantz et
al., 2011; Moreno-Ostos et al., 2008; Bolduc &
Afton, 2008), for instance, water depth regulates
the bird's feeding capacity over the benthic fauna
(except diving birds) (Erwin et al., 1994); on the
other hand, because of shallowness caused by tidal
fluctuations in the water level, a coastal lagoon
usually provides waterbirds with different feeding
opportunities at varying water depths (Ntiamoa-
Baidu et al., 1998). Vegetation type and
Mean salinity in the lagoon oscillated between 32.0
and 34.0 ppt and mean transparency ranged
between 24.0 and 49.1 cm (Table 2), whereas
intertidal water height averaged ca. 1,6 m.
Overall, 45 waterbird species, belonging to 12
families (Table 1) were recorded in five census
carried out during the study period (included the
Osprey, Pandion haliaetus L. 1758, the most
conspiscuously water-associated of all Venezuelan
Falconiformes). Except for August, species
occurrence varied lightly month after month, being
August with the lowest species richness, whereas
November species richness was higher especially
with the inflow of Nearctic migratory birds; in fact,
of the 45 bird species, 17 (37.7%) were migrants
from the boreal latitudes.
The total abundance was 2.390 individuals; it was
greater in November than other months. The total
number of species and monthly abundance of
waterbirds is shown in the Table 2. The higher
value for Simpson's diversity index was observed
in January.
The most representative families noted were
Scolopacidae (12 spp.), Ardeidae (10 spp.), and
Laridae (9 spp.). Six species concentrated 78.44%
of abundance, i.e., Brown Pelican (Pelecanus
occidentalis L. 1758), Royal Tern (Thalasseus
maximus Boddaert 1783), Great Egret (Ardea alba
L. 1758), Common Tern (Sterna hirundo L. 1758),
Olivaceus Cormorant (Phalacrocorax brasilianus
Gmelin 1789) and Large-billed Tern (Phaetusa
simplex Gmelin 1789).
Waterbirds observed were observed mostly
feeding and roosting. Feeding habitats varied from
dry mudflats to wet mud and shallow waters of no
more than 20 cm. Small shorebirds and plovers,
e.g., Semipalmated Plover (Charadrius
semipalmatus Bonaparte 1825), Gray Plover
(Pluvialis squatarola L. 1758), Ruddy Turnstone
(Arenaria interpres L. 1758) and Calidris spp.,
foraged on the dry banks, wet mud and/or water
which was less than 3 cm deep; medium sized
waders such as Black-necked Stilt (Himantopus
mexicanus Müller 1776), Willet (Tringa
semipalmata Gmelin 1789), Greater Yellowlegs
RESULTS
DISCUSSION
Olivares-Márquez et al.
The Biologist (Lima). Vol. 17, Nº1, ene - jun 2019
45
N
Venezuela
N
Píritu lagoon
Caribbean Sea
65°09’ W 65°00’W
Colombia
Brasil
10°03’ N
10°02’ N
Figure 1. Panoramic view of Píritu lagoon with study area framed within a white rectangle.
whether or not habitat is available (Kushlan, 1986;
Bolduc & Afton, 2008; Raposa et al., 2009; Lantz
et al., 2011; Calle et al., 2016); in fact, shorebirds,
terns and gulls were most abundant on the lagoon
during the low tide when water levels in the lagoon
were falling and the shallow waters and exposed
mudflats offer favourable conditions for foraging
and resting (Ntiamoa-Baidu et al., 1998; Mercier &
McNeil, 1994).
Although the differences in abundance and
distribution are also an important criteria for avian
distribution and diversity in coastal wetlands
(Hoyer & Canfield, 1994; Paracuellos & Telleria,
2004; Hassen-Aboushiba, 2015; Jahanbakhsh et
al., 2017).
Habitats with shallow waters (<0.5 m depth) seem
to be crucial determinants of high waterbird
richness in this lagoon sector around which many
people live. Indeed, water depth is paramount in
explaining waterbird density, and determining
waterbirds of Píritu Lagoon, Venezuela
The Biologist (Lima). Vol. 17, Nº1, ene - jun 2019
46
inlet
Figure 2. Sampling transect (dotted line), sampling abiotic sites (white circles) and tidal mudbanks and shallow waters (white
polygons).
this area is estimated to be approximately ca.
10,000 (Espinoza, 2014).
Likewise, Brown Pelican in the Píritu lagoon
exhibited the greater abundance (34.42% of total
abundance). Although brown pelicans have few
natural enemies and nests are sometimes destroyed
by natural disasters (e.g., hurricanes), the biggest
threat to pelicans comes from people (Collazo,
2000; U.S. Fish and Wildlife Service, 2009).
Indeed, disturbance from human activity in their
coastal nesting habitats can cause problems. For
instance, although disturbances to breeding
colonies and consumption of chicks by humans
may be inusual, in northeastern Venezuela this
activity is surprisingly common. Abandoned
fishing line also threatens this species.
In effect, directly or indirectly, the major threat of
wetlands is the pressure of increase human
population growth (Watzin & Gosselink, 1992).
Most coastal lagoons in Venezuela are under some
richness between the five months may be a function
of low sampling effort, the observed abundance
patterns likely reflect the presence of Neartic
migrants (mainly gulls and terns), which were
observed roosting in flocks mainly in the dry mud
banks. The relative lesser abundance of the some
Ardeiformes in January may be asssociated to their
breeding cycle as most species nest during the dry
season in the savannas of Venezuela (McNeil et al.,
1985; Vilella & Baldassarre, 2010). Similarly,
Large-billed Tern and Black Skimmer (Rynchops
niger L. 1758) nest in sandbanks during shallow
waters pulses in Orinoco river corresponding to
drought period (Navarro et al., 2010).
Our sampling methodology resulted in failure to
account for some waterbird species due to lack of
access. For example, Caribbean Flamingo
(Phoenicopterus ruber L. 1758) was observed
periodically in the shallower areas on its western
sector (not included in study area), an area
inaccessible by boat. The flamingo population in
Olivares-Márquez et al.
The Biologist (Lima). Vol. 17, Nº1, ene - jun 2019
47
and cannot be readily evaluated using a priori
criteria.
We wish to thank the Venezuelan company ICM
Proyectos 2001 which funded this investigation.
degree of threat because habitat destruction, human
encroachment especially from recreational uses,
and pollution of industrial and untreated sewage
origin, sedimentation and drainage (Suárez, 2016).
For instance, we observed wastewater discharges
in our sampling area but we have no study as to how
or if nutrient enrichment has played a role in
altering patterns of waterbirds distribution in Píritu
lagoon. In the Everglades, USA, bird abundance
appeared to increase in nutrient-enriched areas;
however, this increase was accompanied by a shift
in species composition (Crozier & Gawlik, 2002).
For the coastal lagoons of Unare and Píritu, the
BirdLife Venezuelan partner designed a program
focused on the local fishermen communities and
aimed to create an awareness of the value of the
local avifauna, and developing human resources
for birding tourism (Rodner, 2006); however, as we
have seen recently public indifference and
goverment policies encourage, unfortunately, the
lagoon degradation and it has revealed that this
valuable program has been failed.
Our study contributed information on the waterbird
community of Píritu lagoon and highlight the need
for the adoption of conservation strategies.
However, we recognize the short-term recognize
nature of our study does not account for the
particular dynamics of this lagoon. Thus, long-
term studies will be needed to address management
and conservation needs of the waterbird
community Píritu lagoon. The area is under intense
pressure from hydrological alterations, sewage
discharges, shrimp aquaculture, overfishing and
human-induced urbanism, as in other lagoons of
Northeastern Venezuela (Pagavino, 1993; Marín et
al., 2006; Marín et al., 2012a; Marín et al., 2012b;
Suárez, 2016; Marín et al., 2017). Thus, future
studies should evaluate waterbirds habitat use in
this coastal lagoon, in order to improve restoration
and management strategies. In addition, the
interpretation of ecological preferences and the
response of waterbirds to environmental pressures
can serve to assess the conservation status of
species at local or regional scales, and act as a
warning tool for changes in similar ecosystems
(O'Neal et al., 2008; Farinós & Robledano, 2010).
However, our preliminary investigation suggests
that the cultural, hydrological and biological
settings of the lagoon is extremely heterogeneous,
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