Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

Avian diversity in river levee forest:

the effect of microscale heterogeneity

Carolina Antonella Brarda1,2; https://orcid.org/0000-0002-0832-7679

Adriana Silvina Manzano1,2; https://orcid.org/0000-0002-6862-857X

Carlos Ignacio Piña3,4; https://orcid.org/0000-0002-6706-5138

Antonio Esteban Frutos3,4*; https://orcid.org/0000-0001-5500-3637

1. Laboratorio de Herpetología, Centro de Investigación Científica y de Transferencia Tecnológica a la Producción.

Consejo Nacional de Investigaciones Científicas y Técnicas CICYTTP (CONICET-Prov. ER-UADER). España 149

(E3105BWA), Diamante, Entre Ríos, Argentina; carolinabrarda@gmail.com, herpetologia@gmail.com

2. CIBTA. Facultad de Ciencia y Tecnología-CONICET. España 149 (E3105BWA), Diamante, Entre Ríos, Argentina.

3. Laboratorio de Ecología Animal. Universidad Autónoma de Entre Ríos. Facultad de Ciencia y Tecnología.

España 149 (E3105BWA), Diamante, Entre Ríos, Argentina; pina.carlos@uader.edu.ar, antoniofrutos.af@gmail.com

(*Correspondence)

4. Centro de Investigación Científica y de Transferencia Tecnológica a la Producción. Consejo Nacional de Investigaciones

Científicas y Técnicas CICYTTP (CONICET-Prov. ER-UADER). Laboratorio de Ecología Animal, España 149

(E3105BWA), Diamante, Entre Ríos, Argentina.

Received 11-VIII-2023. Corrected 10-IV-2024. Accepted 30-VII-2024.

ABSTRACT

Introduction: Levee forests exhibit a vertical stratification that may contribute to structural complexity allow-

ing a great diversity of birds to thrive on the islands. In deltaic ecosystems there is scarce or no data to prove it.

Objectives: To assess variations in the composition of the bird community within levee forests.

Methods: Two areas of protected wetlands belonging to the Paraná River Delta in Argentina were sampled for

three years. A comparative analysis of richness, abundance, and diversity was performed in different levee forests

using the point count method.

Results: Three distinct types of levee forests -open, intermediate, and closed- were identified based on the struc-

ture of their vegetation, hosting a total of 85 bird species. Variation in avian community structure among forest

types revealed greater diversity in open forests during winter (3.26 ± 0.13, P < 0.01) and spring (3.58 ± 0.05, P

< 0.01), and greater richness in autumn (35.33 ± 3.01, P < 0.01). The closed forests exhibited increased diversity

during autumn (3.16 ± 0.13, P < 0.05) and summer (3.24 ± 0.06, P < 0.05), along with elevated abundance in

autumn (114 ± 13.70, P < 0.05) and richness in spring (39.17 ± 4.71, P = 0.01). Due to the evolutionary history

between sites, significant variation was observed in the most recently created national park, influencing abun-

dance in winter (141 ± 22.06, P < 0.01) and spring (176 ± 12.83, P < 0.01), as well as diversity in winter (3.25 ±

0.10, P < 0.01) and spring (3.50 ± 0.10, P < 0.01).

Conclusions: The microhabitat in the different levee forests allows the birds to organize differently. Focusing on

microspatial dynamics is key to a deep understanding of the biological processes within subtropical islands and

to plan conservation strategies and demonstrate the transition of a recovering riparian forest towards its natural

state, where the pulse of the river and the effect of seasonality do not stop operating.

Key words: microstructure; Ramsar site; bird community ecology; riparian environments; vegetation strata.

https://doi.org/10.15517/rev.biol.trop..v72i1.56175

TERRESTRIAL ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

INTRODUCTION

In South America, the Paraná River Delta

is an important island and wetland ecosystem

composed of groups of islands interconnected

and separated by water courses. It is charac-

terized by a high environmental heterogene-

ity driven by current fluvial activity, as well

as historical components (geomorphology of

the early Neogene, different flow intensities,

marine ingressions, and Pleistocene aeolian

processes). All these factors have generated a

diverse and dynamic habitat structure, both at

spatial and temporal scales. This system is in

constant activity, with regular flood pulses of

different magnitude and intensity that generate

a macrosystem of wetlands in the lower Paraná

River (Naiman et al., 2005; Neiff & Malvárez,

2004). These features depend on the water level

at a given time and influence the island geo-

morphology and biology, contributing to the

landscape heterogeneity (Beltzer & Quiroga,

2007; Lorenzón, 2014).

Islands comprising these wetland systems

exhibit distinctive vegetation that colonizes

the territory by seed dispersal in various ways.

Seeds are dispersed by anemochory, endo-

zoochory (internal dispersal by fauna), epizo-

ochory (external dispersal by fauna), by certain

non-standard dispersal vectors due to alterna-

tive morphologies of seed diaspores (Hele-

no & Vargas, 2014) and through hydrochory

(through river courses) (Kubitzk & Ziburski,

1994). All these mechanisms operate together

to generate the vegetation of the wetland sys-

tem, which in turn is different from that of

the continent.

Associated with the particularity of the

vegetation of the wetland system, the bird com-

munities in the floodplain of the Paraná River

behave differently than those in other areas,

such as higher topographic areas, which are

not directly influenced by the river (Ronchi-

Virgolini et al., 2011). Besides the environmen-

tal variability mediated by seasonality, there

are also the temporal dynamics of the seasonal

RESUMEN

Diversidad de aves en bosques de albardón: el efecto de la heterogeneidad a microescala

Introducción: Los bosques de albardón exhiben una estratificación vertical que puede contribuir en la compleji-

dad estructural, permitiendo que una gran diversidad de aves prospere en las islas. En ecosistemas deltaicos hay

escasos datos que lo demuestren.

Objetivos: Evaluar las variaciones en la composición de la comunidad de aves dentro de los bosques de albardón.

Método: Se muestrearon durante tres años, dos áreas protegidas de humedales pertenecientes al Delta del Río

Paraná, Argentina. Se realizó un análisis comparativo de riqueza, abundancia y diversidad de aves en tres diferen-

tes bosques de albardón, utilizando el método de conteo por puntos.

Resultados: Tres distintos tipos de bosque de albardón -abiertos, intermedios y cerrados- fueron identificados

con base en la estructura de su vegetación, hospedando un total de 85 especies de aves. La variación en la estructu-

ra de la comunidad de aves entre tipos de bosque revela mayor diversidad en bosques abiertos durante el invierno

(3.26 ± 0.13, P < 0.01) y la primavera (3.58 ± 0.05, P < 0.01), y mayor riqueza en otoño (35.33 ± 3.01, P < 0.01).

Los bosques cerrados exhibieron mayor diversidad en el otoño (3.16 ± 0.13, P < 0.05) y en verano (3.24 ± 0.06, P <

0.05), junto con elevada abundancia en otoño (114 ± 13.70, P < 0.05) y elevada riqueza en primavera (39.17 ± 4.71,

P=0.01). Debido a la historia evolutiva entre sitios, se observó variación significativa en el parque nacional de más

reciente creación, influyendo en la abundancia del invierno (141 ± 22.06, P < 0.01) y de la primavera (176 ± 12.83,

P < 0.01), así como en la diversidad en el invierno (3.25 ± 0.10, P < 0.01) y en la primavera (3.50 ± 0.10, P < 0.01).

Conclusiones: El microhábitat en los diferentes bosques de albardón permite a las aves organizarse diferen-

cialmente. Enfocarse en la dinámica microespacial es clave para una comprensión profunda de los procesos

biológicos dentro de las islas subtropicales, planificar estrategias de conservación y evidenciar la transición de un

bosque ripario en recuperación hacia su estado natural, donde el pulso del río y el efecto de la estacionalidad no

dejan de operar.

Palabras clave: microestructura; sitio Ramsar; ecología de comunidades de aves; ambientes riparios; estratos de

vegetación.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

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

2008; Tockner et al., 2000a). In fluvial forests,

vertical stratification of the vegetation provides

structural complexity, which allows the occur-

rence of greater bird richness, abundance and

diversity than in the surrounding areas, as well

as the provision of protection, nesting and

feeding sources (Anjos et al., 2007; Di Giacomo

& Contreras, 2002; Giraudo & Ordano, 2003;

Lima et al., 2021).

Several studies exploring bird communi-

ties in fluvial systems have shown the impact of

spatial heterogeneity of vegetation on avifauna.

These investigations entailed comparisons of

bird assemblages across diverse environmental

units on levees, including wetlands, forests, and

grasslands (Beltzer & Neiff, 1992; Berduc et al.,

2015; Frutos et al., 2020a, Frutos et al., 2020b;

Lorenzón et al., 2016; Lima et al., 2021; Ronchi-

Virgolini et al., 2010; Ronchi-Virgolini et al.,

2011; Ronchi-Virgolini et al., 2013; Rossetti &

Giraudo, 2003). Additionally, studies specifi-

cally delved into the distinctions between bird

communities in upland forests (located outside

flood-prone areas) and levee forests, treat-

ing these as contrasting environmental units

(Ronchi-Virgolini et al., 2011).

Spatial heterogeneity plays a crucial role

in shaping bird communities. Changes in bird

communities, such as population density, spe-

cies richness and dominant species composi-

tion, have been attributed to variations in

forest vegetation conditions, water supply to

floodplains and the density of population in

different areas of the landscape (Gureev et al.,

2019). In addition to hydrological disturbances

on floodplains, latitudinal changes along riv-

ers coupled with local habitat characteristics

contribute to shaping the conditions that influ-

ence bird to habitat affinities (Munes et al.,

2015). The intrinsic characteristics of river

microenvironments change along the water

corridors and are not transferable between

regions (Miller et al., 2004), highlighting the

unique micro-environmental heterogeneity of

each region. Different responses have previ-

ously been proposed in relation to the vari-

ation in bird assemblages for anthropically

intervened riparian environments, depending

on the changes generated in spatial heteroge-

neity (Hernández-Belloso et al., 2018; Martin

& Possingham, 2005; Rannestad et al., 2015;

Velásquez-Valencia, 2018).

Silvopastoral and agroforestry environ-

ments generate patches of dense vegetation with

greater richness and diversity of species, such as

those reported for Amazonian riparian systems

(Velásquez-Valencia, 2018). On the contrary,

livestock pressure would compete with bird

resources in the lower strata, generating a

decrease in bird species (seen in the Australian

riparian system) (Martin & Possingham, 2005).

Some environments that have been recov-

ered have exhibited greater associated heteroge-

neity, thus hosting the greatest diversity of birds,

or have demonstrated greater richness and

relative abundance. Reported examples include

the Kilombero Valley in East Africa (following

recent livestock removal) (Rannestad et al.,

2015) and Spanish lake environments undergo-

ing restoration (Hernández-Belloso et al., 2018).

Considering that levee forests differ in the

structure and composition of the vegetation

(Aceñolaza et al., 2005), we focus on evaluating

the differences in the structure of the levee for-

est and how it would affect the bird communi-

ties of the Paraná basin. In this work, we focus

on differences in bird assemblage between

environments within an environmental unit,

in our case the floodplain levee forest. We

hypothesize that birds use the different levee

types differently and that this variation in the

use is reflected in the bird assemblage structure

within each forest.

MATERIALS AND METHODS

Study area: The study sites included Wet-

lands in the Pre-Delta National Park (PDNP),

Diamante, Entre Ríos, Argentina (32º 03’43”

S & 60º38’39” W) (PDNP, 2022) and in the

Islas de Santa Fe National Park (ISFNP), San

Jerónimo, Santa Fe, Argentina (32°6’10.70”-

32°19’42.18” S & 60°43’52.36”-60°36’7.42” W)

(Fig. 1) (ISFNP, 2022). These wetland areas

correspond to the Delta e Islas del Paraná

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

ecoregion (Matteucci, 2012; Quintana & Bó,

2010). They conform to the Ramsar site ‘Paraná

Delta,’ a globally significant wetland located in

Argentina (Giacosa et al., 2019). Located in

a transition segment in the Paraná River, it is

the area where the delta system begins, and is

influenced by the biota present in the previous

section of this river, the segment called middle

Paraná (Lorenzón et al., 2019; Nestler et al.,

2007; Sabattini & Lallana, 2007).

The Pre-Delta National Park (PDNP) cov-

ers 2 458 hectares of island area and has been

under the jurisdiction of the National Parks

Administration since 1992. This is the only

IBA (Important Bird and Biodiversity Con-

servation Area) located in the Upper Delta, in

the area called “Forests, prairies and meander

floodplains” (Coconier & Di Giacomo, 2009).

The Islas de Santa Fe National Park (ISFNP)

was created in November 2010. It covers 4 096

hectares, including eight islands that have been

under the jurisdiction of the National Parks

Administration since 2010 (https://www.argen-

tina.gob.ar/parquesnacionales).

Levee forests are located at the highest zone

of the floodplain. They have characteristics due

to their topographic position, susceptible to

floods (Aceñolaza et al., 2004). These forests

cover about 20 % of the island area (Boro-

dowski, 2006), whereas the central zones of the

islands hold marshes and ponds. In the Paraná

Delta, levees are simple, low diversity and open

canopy forests, composed of high colonizer

trees dominated by Salix humboldtiana and

Tessaria integrifolia, with possible occurrence

of Albizia inundata, Erythrina crista-galli or

Sapium haematospermum. There are mature

and better preserved forests (of equal ages)

with one or two vegetation strata composed of

Nectandra falcifolia and Inga uraguensis, Vach-

ellia caven, and Croton urucurana. There may

also be Morus spp. and Ligustrum lucidum as

invasive introduced species as a result of orni-

thochorous dispersal (Ronchi-Virgolini et al.,

2010). These forests are complemented by an

herb stratum, composed of short gramineous

species and grasslands of different species, and

a shrub stratum characterized by several vines,

Fig. 1. Map of the study area. The lower polygon represents the limit of the Islas de Santa Fe National Park (ISFNP) and the

upper polygon represents the limit of the Pre-Delta National Park (PDNP). Points represent the vegetation sampling points

and bird count points (OF= open forests, IF= intermediate forests, CF= closed forests).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

sapling and medium-sized trees of Myrsine

laetevirens and Zanthoxylum fagara (Aceñolaza

et al., 2004; Aceñolaza et al., 2005; Beltzer &

Neiff, 1992).

Climate and biogeography: The climate

is temperate/warm humid (Kottek et al., 2006).

The annual average temperature is about 19 ºC

and annual rainfall is ~900 mm, with warmer

and rainier summer periods than in winter.

Biogeographically, the subtropical biota reaches

the temperate zone of the Paraná Delta through

the Paraná River, which acts as a biological cor-

ridor of great latitudinal extension (Cabrera,

1994; Malvárez, 1999). Thus, the area holds

floristic components of the Amazonian domain

(with elements from the Paranaense province)

and the Chaco domain (with elements from the

Chaco, Pampean and Espinal provinces), both

domains belonging to the Neotropical Region

(Cabrera, 1994); fauna with components of the

Mesopotamian District (Subtropical Domain,

Guyana-Brazilian subregion) with influence

of the Pampean District (Ringuelet, 1961),

and overlap of three ornithogeographic zones:

the Paranaense province (Forests district) and

the Mesopotamian and Pampean provinces

(Nores, 1987).

Experimental design for vegetation: The

forest types were defined by visually determin-

ing the tree cover percentage (on a horizontal

plane), in sampling units, following Matteucci

& Colma (1982). The area of the vegetation

sample points coincided with the area of the

bird count points. All the studied forests were

considered levee forests because they are pres-

ent in the highest zone, on the island edges,

within the floodplain, without discriminating

between young or mature forests, with greater

or lower susceptibility to hydrometric fluctua-

tions (Neiff, 2005; Placci, 1994).

A total of 18 vegetation and bird com-

munities sampling points were selected; they

were determined according to the vegetation

traits (physiognomic-structural categories). Six

replicates homogeneously distributed in both

national parks were established for each forest

category (three replicates in each forest type

for each park) (Fig. 1). Forest characteriza-

tions based on tree cover ranges were up to

30 % for open forests, between 30 % and 60 %

for intermediate forests, and more than 60 %

for closed forests (Symonds & Johnson, 2008)

(Fig. 2). Percent cover of shrub and herb strata

was also recorded, as well as height (cm) of

herb stratum.

Experimental design for birds: Bird sam-

pling was conducted twice in each season, in

the same points used for vegetation, at 45-day

intervals for three years (2014, 2015 and 2016)

and under favorable climatic conditions for

bird observation. Birds were counted using

the point counting method. To ensure sample

independence, distance between points was

greater than 250 m. All the birds in the forest

environment seen and heard at each point for

ten minutes were recorded (Blake, 1992; Ron-

chi-Virgolini et al., 2011). The total sampling

Fig. 2. Physiognomy of the different levee forests. A. Open forest. B. Intermediate forest. C. Closed forest.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

effort at each point was four hours throughout

the entire sampling period. This means that in

each type of forest, in each park, the total sam-

pling effort during the three years was 12 hours

(given the three counting points for each forest

type located in each of the two parks). All the

birds that made use of the habitat were record-

ed, except for those that were seen only flying

over the area. The estimated radius of the count

point was 75 m. Counts began at sunrise and

continued for four hours, the period of greatest

stability for bird detection (Huff et al., 2000;

Ralph et al., 1996). On each visit, sampling

order was shifted among points to reduce the

effects associated with bird activity and time of

the day (Verner & Milne, 1989). All the species

were identified in situ (Narosky & Yzurieta,

2010) and then classified systematically accord-

ing to SAAC (Remsen et al., 2022).

Sample processing: The bird community

was analyzed for each season from the 18

samples homogeneously distributed between

the different forest types in both national parks,

using a balanced and complete sampling design

(Quinn & Kough, 2002). The total observa-

tion time for each type of forest was 24 hours

during the entire study period, contemplating

all points between the two parks, with 6 hours

allocated to each season. To obtain more rep-

resentative estimations of the bird community,

seasonal estimates made across three years were

grouped in a single point; thus, each sample

resulted in the sum of six (6) individual esti-

mates made for each point.

Where P is the sampling point, i is each

estimation of bird counts made from a seasonal

sampling, and N is the number of terms of the

sum or the total estimations throughout the

sampling. Bird richness and abundance, species

composition and diversity were determined to

describe the community structure of each forest

type. Diversity was calculated using the Shan-

non and Weaver diversity index (H´).

Statistical analysis: Composition and rela-

tive abundances of tree species were analyzed

using an analysis of similarities (ANOSIM)

(Clarke & Warwick, 2001) and a non-metric

multidimensional scaling (NMDS) (McCune

& Mefford, 1999), with the Vegan package

(Oksanen, 2011), using the Bray Curtis dis-

similarity index on a matrix of relative abun-

dances. Differences in tree, shrub and herb

cover among seasons and between sites, and

physiognomic differences inherent to forests

(forest types) were analyzed using the Kruskall-

Wallis non-parametric test (α = 0.05).

The relationship between bird commu-

nity structure (richness, abundance and diver-

sity) and forest type and sites were evaluated

using generalized linear models for each season

(Supplementary Material SM1). The models

were fitted with the error distribution assumed

according to the nature of the data, considering

under and/or overdispersion (Gaussian, Pois-

son and Negative Binomial). Assumptions were

evaluated for each model with their residuals

(homoscedasticity and normality of Gaussian

distribution and under and/or overdispersion

in Poisson or Negative Binomial distributions).

Models were selected using the Akaike

Information Criteria, as recommended for

small samples (AICc) (Burnham et al., 2011;

Matthew & Moussalli, 2011). When the best

model was not achieved, the multiple model

inference (MMI) of those with a Δi < 2 (Mat-

thew & Moussalli, 2011) was used to obtain the

relative importance of each predictor variable.

The software packages R Studio version 3.6.1

(R Core Team, 2019) and R-medic (Mangeaud

& Elías-Panigo, 2018) were used. Response

variables whose explanatory variables were sta-

tistically significant are reported in Table 2 and

Table 3. The figures were done with package

Ggplot2 and the editing was done with Corel

Draw 2021.5 Licence Adriana Manzano.

RESULTS

Vegetation structure: The analysis of tree

composition and relative abundance using

the similarity analysis (ANOSIM) and the

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

multidimensional ordination (NMDS) allowed

us to differentiate three groups of forests and

to associate Tessaria integrifolia and Salix hum-

boldtiana with open forests, Albizia inundata,

Myrsine laetevirens, Sapium haematospermum,

Enterolobium contortisiliquum, Inga uraguensis

and Vachellia caven with intermediate forests,

and Erythrina crista galli, Nectandra falcifolia,

Croton urucurana and Ligustrus lucidum with

closed forests (ANOSIM R = 0.59, P = 0.001;

Fig. 3).

Regarding vegetation cover, no seasonal

variation was recorded in tree or shrub cover.

The herb stratum showed variation in spring,

with its cover being the highest of all seasons

(H = 36.77, P < 0.001). The height of this stra-

tum was lowest in winter and highest in spring

(H = 29.74, P < 0.001), with no differences

between autumn and summer. No differences

in cover were detected in any stratum, showing

homogeneity in the values of both sites (Fig. 4

and Fig. 5). Regarding the inherent levee forest

structure, three physiognomies were detected

in the levee forests: open forests (OF), interme-

diate forests (IF), and closed forests (CF), which

were determined by the tree cover (H = 42.52,

P < 0.001) and height of the herb stratum (H

= 18.69, P < 0.001). In the OF, the lowest tree

cover percentage and the highest herb height

were recorded. In the IF, both variables had

intermediate values, and in CF, the highest per-

centage of tree cover, and the lowest percentage

of herb cover were recorded (Fig. 6.A and Fig.

6.D; Table 1). While tree cover and herb height

determined three forest physiognomies, in IF

shrub cover was the highest, with no differenc-

es between OF and CF (H= 34.71, P < 0.001).

The OF herb stratum cover was the highest,

with no differences between the IF and the CF

(H = 6.97, P < 0.05) (Table 1) (Fig. 6B, Fig. 6C).

The results of the Kruskall-Wallis tests are

shown.

Fig. 3. Non-metric multidimensional scaling (NMDS) of relative abundance of tree species in 18 count points. In black empty

symbols, points of the Pre-Delta National Park site; in black filled symbols, points of the Islas de Santa Fe National Park.

Open, intermediate, and closed forests are represented by squares, circles and triangles, respectively. Red crosses symbols

stand for the relative positions of the different tree species. Tes.int.: Tessaria integrifolia; Sal.hum.: Salix humboldtiana;

Alb. inu.: Albizia inundata; Myr. lae.: Myrsine laetevirens; Sap. hae.: Sapium haematospermum; Ent. con.: Enterolobium

contortisiliquum; Ing. ura.: Inga uraguensis; Vac. cav.: Vachellia caven; Ery. cri.: Erythrina crista galli; Nec. fal.: Nectandra

falcifolia; Cro. uru.: Croton urucurana; Lig. luc.: Ligustum lucidum.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

Fig. 4. Seasonal changes in the cover of the different vegetation strata. A. Percentage of tree cover. B. Percentage of shrub

cover. C. Percentage of herb cover. D. Height of herb stratum.

Fig. 5. Differences in cover of vegetation strata between national parks. A. Percentage of tree over. B. Percentage of shrub

cover. C. Percentage of herb cover. D. Height of herb stratum.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

Bird community: The number of contacts

with birds recorded amounted to 9 908, cor-

responding to 85 bird species belonging to 29

families and 13 orders (Table 3). In autumn,

37.61 % of variation in species richness was

explained by physiognomic variables of levee

forests (AICc = 104.50, w = 0.60), with OF hav-

ing higher values than CF (P < 0.01). In spring,

richness had the lowest value in PDNP and

varied among forest types, with CF showing the

lowest value and differing from OF and IF (P <

0.05). In summer, richness had the lowest value

Fig. 6. Intrinsic physiognomic differences among levee forests are determined by percentage of tree, shrub and herb cover,

and height of herb stratum. Open forests (OF), intermediate jDifferentiation of shrub cover percentage. C. Differentiation of

herb cover. D. Differentiation of herb stratum height (cm).

Table 1

Differences among vegetation strata with respect to seasons, sites and forest types.

Dependent variable Explanatory variable Statistical (H) P

Tree cover Season 0.44 0.930

Shrub cover Season 0.01 0.990

Herbaceous cover Season 36.77 < 0.001*

Herbaceous height Season 29.74 < 0.001*

Tree cover Site 1.67 0.199

Shrub cover Site 3.61 0.060

Herbaceous cover Site 3.42 0.060

Herbaceous height Site 0.62 0.430

Tree cover Forest type 42.52 < 0.001*

Shrub cover Forest type 34.71 < 0.001*

Herbaceous cover Forest type 6.97 0.030 *

Herbaceous height Forest type 18.69 < 0.001*

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

Table 2

Seasonal variation in bird richness, abundance and diversity, related to levee forest structure.

Dependent Variable AICc delta Weight Coeficient Coef.Standard

deviation Confidence interval p-value Null

deviance

Residual

deviance Devianza Mean ± sd

Explanatory variable 2.50 % 97.50 %

Winter Richness MMI -0.344 0.235 PDNP site -0.842 0.153 0.175 - - - -

Autumn Richness 104.50 2 0.57 35.333 1.452 Open forests* 32.49 38.18 < 0.01 304.00 189.67 37.61 35.33 ± 3.01

    -6.167 2.053 Closed forests* -10.19 -2.14 < 0.01    29.17 ± 3.60

Spring Richness MMI   -0.518 0.192 Closed forests* -0.93 -0.11 0.01    39.17 ± 4.71

    -0.641 0.178 PDNP site* -1.02 -0.26 < 0.01    38.78 ± 3.89

Summer Richness MMI   -3.633

-5.674

1.506

Intermediate forests*

Closed forest*

-1.05

-1.11

-0.01

-0.06

< 0.05

< 0.05    35.17 ± 3.31

34.67 ± 3.20

Winter Abundance 160.30 ~2 0.59 -0.142 0.042 PDNP site* -0.26 -0.02 < 0.05 23.53 18.00 23.49 122 ± 12.38

   4.947 0.060 ISFNP site* 4.87 5.03 < 0.01    141 ± 22.06

Autumn Abundance MMI   -0.005 0.002 Closed forests* -0.01 0.00 < 0.05    114 ± 13.70

Spring Abundance 145.10 > 2 0.77 5.171 0.025 ISFNP site* 5.12 5.22 < 0.01 34.26 15.60 54.46 176 ± 12.83

    -0.160 0.037 PDNP site* -0.23 -0.09 < 0.01    150 ± 12.37

Summer Abundance MMI   -0.003 0.001 Intermediate forests* -0.01 0.00 < 0.05    126 ± 17.85

    -0.004 0.001 PDNP site* -0.01 0.00 < 0.01    122 ± 15.80

Winter Diversity -26.60 ~2 0.67 3.328 0.041 Open forests* 3.25 3.41 < 0.01 0.24 0.10 56.76 3.26 ± 0.13

    -0.157 0.050 Closed forests* -0.26 -0.06 < 0.01    3.11 ± 0.07

    3.328 0.041 ISFNP site* 3.25 3.41 < 0.01    3.25 ± 0.10

    -0.118 0.041 PDNP site* -0.20 -0.04 < 0.05    3.13 ± 0.11

Autumn Diversity MMI   -0.962 0.375 Closed forests* -1.73 -0.19 < 0.05   3.16 ± 0.13

    0.895 0.285 Closed forests in PDNP

site* 0.27 1.52 < 0.01    3.18 ± 0.06

Spring Diversity -28.10 > 2 0.77 3.590 0.039 Open forest* 3.51 3.67 < 0.01 0.26 0.10 63.08 3.58 ± 0.05

    -0.122 0.048 Intermediate forests* -0.22 -0.03 < 0.05    3.40 ± 0.10

    -0.144 0.048 Closed forests* -0.24 -0.05 < 0.01    3.37 ± 0.14

    3.590 0.039 ISFNP site* 3.51 3.67 < 0.01    3.50 ± 0.10

    -0.143 0.039 PDNP site* -0.22 -0.07 < 0.01    3.36 ± 0.11

Summer Diversity MMI  -0.629 0.244 Closed forests* -1.15 -0.11 < 0.05 3.24 ± 0.06

Seasonal variation in the community attributes related to forests structure. MMI: Multiple Model Inference. PDNP: Pre-Delta National Park. ISFNP: Islas de Santa Fe National Park.

AICc value (small samples), delta and weight of the best model, coefficient value and standard deviation, confidence interval and P of the explanatory variables (*significance).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

in PDNP and varied among forest types with

differences between IF and CF. IF had higher

richness than CF (P < 0.01). In winter, richness

was similar among forest types (Table 2, Table

3, Fig. 8).

Bird abundance varied among forest types

in autumn and summer. In autumn, CF was the

least abundant, whereas in summer, IF was the

least abundant (P < 0.05). In spring, as in win-

ter, there was higher abundance in the ISFNP;

the best model explained 54.46 % (AICc =

145.10, w = 0.80), and 23.49 % (AICc = 160.30,

w = 0.60), respectively (Table 2, Table 3, Fig. 7,

Fig. 8).

Bird diversity varied among forest types

in all the seasons. In winter, 56.76 % of bird

Table 3

Systematic classification of bird species in each site, their richness and number of contacts of each one.

Species

Status ISFNP PDNP

Conservation Richnnes Number of

Contacts Richnnes Number of

Contacts

OF IF CF OF IF CF OF IF CF OF IF CF

Hydropsalis torquata* LC - - X - - 1 - - - X - - 1

Butorides striata LC - - - X - - 1 X X X 1 1 1

Columbina picui LC - X - - 2 - - X X - 2 4 -

Columbina talpacoti LC X - - 1 - - X X X 5 1 2

Leptotila verreauxi LC - X X X 62 85 95 X X X 105 142 155

Patagioenas maculosa LC X--1--------

Patagioenas picazuro LC X X X 39 53 61 X X X 60 75 74

Zenaida auriculata LC X X X 33 44 24 X X X 28 17 9

Chloroceryle amazona LC X - X 1 - 1 - X - - 2 -

Chloroceryle americana LC X - X 2 - 2 X X - 1 3 -

Megaceryle torquata LC - X - X 1 - 1 - X - - 3 -

Coccycua cinérea* LC X X - 3 1 - X - - 1 - -

Coccyzus melacoryphus* LC - X X X 4 1 4 X X X 2 2 3

Guira guira LC X X X 4 2 10 - X X 1 4 2

Tapera naevia* LC - X - - 1 - - X - - 2 - -

Rostrhamus sociabilis LC - X - - 1 - - - X X - 1 1

Rupornis magnirostris LC X X X 17 13 14 X X X 7 4 13

Caracara plancus LC X X X 8 5 5 X X X 19 6 9

Aramus guarauna LC - - - X - - 1 - - - - - -

Aramides ypecaha LC - X X - 3 2 - - - - - -

Campylorhamphus trochilirostris LC X X X 1 6 1 X X X 6 4 5

Lepidocolaptes angustirostris LC X X X 89 43 54 X X X 68 52 69

Microspingus melanoleucus LC - X X X 44 15 7 X X X 11 7 5

Saltator aurantiirostris LC Unk X X X 66 80 76 X X X 74 71 69

Saltator coerulescens LC X X X 124 162 134 X X X 126 114 125

Saltator similis LC - X - - 1 - - - - - - -

Paroaria capitata LC - X X X 45 26 45 X X X 22 5 8

Paroaria coronata LC - X X X 27 24 23 X X X 25 13 17

Poospiza nigrorufa LC - - X X - 2 2 X - X 3 - 2

Sicalis flaveola LC - X X X 6 9 2 X X X 4 8 4

Zonotrichia capensis LC - X X X 30 35 47 X X X 16 9 22

Spinus magellanicus LC - X X X 16 1 2 X X - 12 4 -

Asthenes pyrrholeuca** LC X X X 6 10 4 - - - - - -

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

Species

Status ISFNP PDNP

Conservation Richnnes Number of

Contacts Richnnes Number of

Contacts

OF IF CF OF IF CF OF IF CF OF IF CF

Certhiaxis cinnamomeus LC X X - 2 2 - X - - 1 - -

Phacellodomus ruber LC X X X 139 111 156 X X X 148 127 134

Phacellodomus striaticollis LC - X X - 1 1 - - - - - - -

Synallaxis frontalis LC X X X 36 56 39 X X X 34 57 43

Limnoctites sulphuriferus LC X X X 1 2 4 - - - - - -

Furnarius rufus LC X X X 56 70 66 X X X 53 48 62

Progne tapera* LC X X X 38 14 18 X X X 35 24 19

Tachycineta leucorrhoa LC X X X 55 31 17 X X X 27 13 16

Agelasticus cyanopus LC - X X X 3 8 5 X X - 2 2 -

Cacicus solitarius LC - X X X 4 17 5 X X X 14 9 23

Icterus pyrrhopterus LC - X X X 28 10 18 X X X 18 13 13

Agelaioides badius LC - X X X 52 54 39 X X X 26 39 23

Molothrus bonariensis LC X X X 7 4 5 X X X 9 7 1

Molothrus rufoaxillaris LC - X X X 13 16 8 X X X 10 12 8

Geothlypis aequinoctialis LC - X X X 1 1 2 X - X 2 - 1

Setophaga pitiayumi LC X X X 7 2 1 - X X - 2 1

Myiothlypis leucoblephara LC - - - - - - X X X 9 12 38

Polioptila dumicola LC X X X 63 105 90 X X X 45 38 49

Taraba major LC X X X 72 68 59 X X X 69 65 54

Thamnophilus caerulescens LC - X X - 9 8 X X X 3 6 12

Thlypopsis sordida LC - X X X 7 13 3 X X - 4 2 -

Thraupis sayaca LC - X X X 14 6 5 X X X 37 30 29

Turdus amaurochalinus LC - X X X 42 23 22 X X X 38 39 31

Turdus rufiventris LC - X X X 66 106 80 X X X 76 58 76

Troglodytes aedon LC X X X 30 10 9 X X X 20 14 7

Elaenia parvirostris LC - X X X 5 3 2 - X - - 1 -

Elaenia spectabilis LC X X X 1 10 6 X X X 3 5 4

Myiophobus fasciatus* LC X X X 7 4 6 X X X 3 6 3

Pitangus sulphuratus LC X X X 64 53 55 X X X 47 39 31

Serpophaga griseicapilla LC - X X - 1 1 - X - - 3 - -

Serpophaga subcristata LC - X X X 30 20 7 X X X 9 9 15

Hemitriccus margaritaceiventer LC - X X X 11 21 12 X X X 2 2 11

Myiarchus swainsoni* LC - X X X 15 12 9 X X X 13 11 9

Camptostoma obsoletum LC - X X X 13 5 5 X X X 7 7 3

Myiodynastes maculatus* LC - X - X 7 - 1 X X X 15 5 3

Suiriri suiriri LC X X X 33 17 7 X X X 31 12 11

Tyrannus melancholicus* LC X X X 9 12 14 X X X 10 10 14

Tyrannus savana* LC - X X X 6 6 4 X X - 3 4 -

Machetornis rixosa LC - X X X 1 2 2 X - - 1 - -

Pachyramphus polychopterus* LC - X X X 33 33 29 X X X 22 19 22

Pachyramphus viridis LC - X -X 2 - - - X X - 3 1

Vireo olivaceus* LC X X X 54 46 44 X X X 21 21 22

Cyclarhis gujanensis LC X X X 50 47 37 X X X 32 48 44

Colaptes melanochloros LC - X X X 46 20 11 X X X 30 21 21

Melanerpes cactorum LC X X X 8 4 2 X X X 8 4 2

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

diversity variation was explained by an additive

model including forests and sites (AICc = -26.6,

w = 0.67), with differences between OF and CF

types (P < 0.01), with OF being more diverse

than CF. Regarding sites, ISFNP was more

diverse than PDNP (P < 0.05). In autumn, the

greatest diversity occurred in CF of PDNP (P =

0.004). In spring, the additive model of forests

and sites explained 63.08 % of the variation

(AICc = -28.10, w = 0.78), with diversity being

highest in OF, intermediate in IF, and lowest

in CF (P < 0.05). According to the differences

between sites, the ISFNP was the most diverse

(P < 0.05). In summer, CF were the least diverse

(P < 0.01) (Table 2, Table 3, Fig. 7, Fig. 8).

DISCUSSION

Differences in vegetation structures (tree

cover, shrub cover, herbaceous cover, and

Species

Status ISFNP PDNP

Conservation Richnnes Number of

Contacts Richnnes Number of

Contacts

OF IF CF OF IF CF OF IF CF OF IF CF

Melanerpes candidus LC X X - 4 1 - - X - - 2 -

Picumnus cirratus LC X X X 30 18 21 X X X 14 16 21

Dryobates mixtus LC - X X X 35 19 20 X X X 29 21 32

Myiopsitta monachus LC X X X 6 21 21 X X X 14 43 35

Bubo virginianus LC - - X - - 5 - X - - 2 - -

Chlorostilbon lucidus LC Unk X X X 3 4 4 X X X 1 6 1

Hylocharis chrysura LC X X X 19 25 15 X X X 11 16 10

76 72 71 1 864 1 770 1611 69 69 69 1 612 1 500 1 551

Fig. 7. Most abundant species in the levee forest physiognomies. The relative abundance (Pi) value for each species is shown

on the bars.

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

height) were found to be related to forest

types mainly. The maximum shrub cover was

recorded in Intermediate Forests (IF) and herb

cover in Open Forests (OF) might be due to

the greater light availability at the lower veg-

etation levels, reaching the lower forest strata

due to the open canopy structure. OF might

be considered edge environments favored by

abiotic factors, especially light, which gen-

erates microclimatic variations that increase

plant diversity (Granados-Sánchez et al., 2006;

Nieves-Vele & Orellana-Peralta, 2018); in turn,

these conditions are considered optimal for

bird diversity (Baker et al., 2002; Rannestad

et al., 2015). It is known that the develop-

ment of the different vertical vegetation strata

is enhanced when a disturbance of the forest

canopy increases light availability (Anderson

et al., 1978), with solar radiation being a factor

determining the natural regeneration of forest

vegetation (Viana & Jardim, 2013). In closed

canopy forests, most of the light is absorbed by

the tree canopy, reducing the development of

the understory vegetation.

Our records of birds for the Delta wetland

area were like those previously reported (eBird,

2020; Frutos et al., 2020a; Frutos et al., 2020b;

Magnano et al., 2019; Ronchi-Virgolini et al.,

2011; Rossetti & Giraudo, 2003). Overall, our

results show that closed forests (CF) had the

lowest richness, abundance and diversity values

in their bird communities, whereas the high-

est values of richness, abundance and diversity

were detected in OF. In a highly heterogeneous

environment, niche availability is high; there-

fore, species richness is high while evenness

Fig. 8. Bird differences of richness, abundance and diversity among forest types in each season, in each park. A. Winter

richness in PDNP. B. Winter richness in ISFNP. C. Winter abundance in PDNP. D. Winter abundance in ISFNP. E. Winter

diversity in PDNP. F. Winter diversity in ISFNP. G. Autumn richness in PDNP. H. Autumn richness in ISFNP. I. Autumn

abundance in PDNP. J. Autumn abundance in ISFNP. K. Autumn diversity in PDNP. L. Autumn diversity in ISFNP. M. Spring

richness in PDNP. N. Spring richness in ISFNP. O. Spring abundance in PDNP. P. Spring abundance in ISFNP. Q. Spring

diversity in PDNP. R. Spring diversity in ISFNP. S. Summer richness in PDNP. T. Summer richness in ISFNP. U. Summer

abundance in PDNP. V. Summer abundance in ISFNP. W. Summer diversity in PDNP. X. Summer diversity in ISFNP.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

is low, reducing diversity (Rosenzweig, 1995;

Symonds & Johnson, 2008). Other authors

argue that a greater niche availability drives

greater evenness (Cotgreave & Harvey, 1994).

However, community structure depends on

landscape structure and spatial scale (Drobner

et al., 1998; Horlent et al., 2003). Based on the

results of our analyses of forest types and birds,

we could suggest that a more heterogenous

ambient could host more diversity, regardless

of the bird community evenness. The richness

record observed in the OF zone exemplifies

this phenomenon, where the environmental

heterogeneity manifests through variations in

the vegetation strata. Similar results have been

reported for the extensive floodplain of El

Kilombero in Tanzania, a prominent wetland

in East Africa (Rannestad et al., 2015). Further

investigations emphasize the pivotal role played

by edge habitats (Baker et al., 2002; Miller et

al., 2004) in structuring avian communities.

Considering that the levees of the OF zone

host the most diverse avian communities and

are near water, it is plausible to suggest that

they function as well as exhibit characteristics

emblematic of edge environments.

PD National Park has held protected status

for several decades, while ISF National Park

attained protection approximately a decade ago,

resulting in the recent cessation of livestock

farming activities (Frutos et al., 2018). Given

the disturbing effects of recent livestock farm-

ing, it was expected that ISFNP would present

some difference with respect to PDNP in terms

of the lower vegetation strata, as suggested

by Olff & Ritchie (1998) and Frutos (2018)

as an effect associated with the intermedi-

ate disturbance hypothesis. Our findings show

no differences in vegetation strata among the

study sites, despite their different management

histories. Nevertheless, the avian variation pat-

tern proved to be non-uniform, which could

be attributable to the influence of the charac-

teristics of the area and seasonal fluctuations

in vegetation. The recent cessation of livestock

activities in ISFNP may have contributed to the

proliferation of shrubs, resulting in subtly ele-

vated coverage values at this location. Despite

the increase in the prevalence of shrubs, typi-

cally correlated with higher avian diversity

(Godoi et al., 2017; Martin, 1993), this trend

was not conspicuously apparent. Considering

potential seasonal disparities linked to abiotic/

climatic factors in the coverage of lower strata

(Zerda & Tiedemann, 2010), we could attribute

the differences in the presence or absence of

certain species in the parks. Examples include

Phacellodomus striaticollis (insectivore of the

shrub stratum), Asthenes pyrrholeuca (migra-

tory insectivore of the shrub stratum), Saltator

similis (fruit-insectivore of the low canopy), and

Patagioenas maculosa (terrestrial granivore), all

of which were notably absent in PNPD. This

absence could be correlated with reduced habi-

tat diversity in the understory and soil strata.

This phenomenon could be correlated with an

increased herbaceous vegetation density in the

early stages of plant succession, a result of the

absence of herbivory, particularly by livestock.

In contrast, this form of herbivorous activity

was prevalent in ISFNP in the past but has been

systematically excluded from the site since its

official designation as a national park, slight-

ly over a decade ago. This exclusion creates

more open space in the lower vegetation stra-

ta, potentially enhancing resource availability

and eliciting corresponding avian responses to

intermediate disturbance states in the environ-

ments (Frutos et al., 2018). In this context, the

absence of Myiothlypis leucoblephara (insecti-

vore inhabiting shrubbery and soil strata) in

ISFNP can also be ascribed to a scenario favor-

ing the occupation of other dominant species

in the soil stratum, resulting in displacements

of less dominant species within the assem-

blage. Additional species such as Limnoctites

sulphuriferus, Aramus guarauna, and Aramides

ypecaha (species associated with salt marshes)

were absent in PDNP (yet present in ISFNP),

potentially linked to the lower prevalence of salt

marshes near the sampling points in this park.

These absences are not of particular concern,

as these species do not hold emblematic status

for the region. According to the International

Union for Conservation of Nature [IUCN]

(2023), none of the species is classified as

16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

threatened, vulnerable, or endangered globally;

instead, all are categorized as least concern.

This aligns with the regional survey conducted

by specialists from Aves Argentinas (2015).

However, we found differences in the

arrangement of birds associated with parks,

in terms of richness, abundance and diversity,

with seasonal influence. This result suggests

that despite past anthropogenic activities in the

study sites, spatial heterogeneity of the forests

in the floodplains is still high, possibly due to

the dynamics contributed by the pulses. Thus,

taking into account that the significance of

the analysis that compared vegetation strata

between sites was very close to the acceptance

limit, it could be considered that the natural

history of parks associated with livestock in

natural riparian environments in some cases

favor bird diversity (Frutos et al., 2020a; Fru-

tos et al., 2020b; García et al., 2008; Martin &

Mcintyre, 2007), however, it is not a necessary

requirement to maintain a heterogeneous and

beneficial structure for the dynamics of birds

in riverine environments. Vegetation in the

islands reveals ecological processes with several

successional stages, caused by regimes of sea-

sonal hydrological disturbances (Aceñolaza et

al., 2005; Malvárez, 1999). Therefore, river wet-

lands are highly heterogeneous and maintain a

high array of small habitats and microhabitats

(Miller et al., 2004; Tavares et al., 2015).

The distinct resource offerings determined

by the floristic composition in each type of

forests and in each park were not analyzed

to observe seasonal changes in that aspect.

However, the analysis of vegetation cover in

each forests type revealed variations through-

out the seasons, particularly in the herbaceous

layer (in terms of both coverage and height

of the plants). Regarding the seasonal varia-

tion detected in the bird community, we can

highlight that OF were not consistently able

to distinguish themselves with a higher rich-

ness value in all seasons. Nevertheless, during

the summer, lower abundance values were

evident in the interior forests. Conversely, in

autumn, there was a notable increase, particu-

larly in PNPD. In CF, we found the lowest bird

abundance value in autumn, and in general,

the lowest value of diversity across seasons.

There may be a relationship among the type of

resources offered by the CF, a decrease of those

resources in cool seasons and preferences for

these resources by the species present there. To

explain this relationship, a species composition

analysis might be necessary to detect species

preferences for different physiognomies (Hor-

lent et al., 2003). We speculate, based on our

results, about the existence of a dynamism that

is not easy to identify in the arrangement of

the community. This dynamism appears to be

generated by the combination of seasonal and

microspatial factors.

According to the classical niche theory, dif-

ferent species are associated with different habi-

tat types; therefore, a few small and overlapping

habitats may hold a high number of species

(Allouche et al., 2012; Laanisto et al., 2013;

MacArthur & MacArthur, 1961). Environmen-

tal heterogeneity is the degree of variation

of the landscape components (physiognomy,

structure, size, relative spatial arrangement)

both at the spatial (different successional stag-

es) and temporal levels (relationship between

flooded areas and emergent areas in flood-

plains). It acts as a stabilizing mechanism that

smooths the shift from stable to alternative

states (van Nes & Scheffer, 2005) and deter-

mines the degree of habitat suitability for wild

species, conditioning their richness, abundance

and permanence in the area (Bó & Malvárez,

1999; Bó et al., 2010, Robinson et al., 2002).

Therefore, environmental heterogeneity is a

more important predictor of spatial variation

of bird richness than the area covered by each

habitat type (Lorenzón et al., 2016).

Beta diversity and species turnover from

one area to another have a substantial influ-

ence on general species richness in a region

(Ronchi-Virgolini et al., 2011; Vellend, 2001).

The variation of the assemblage between sites,

independently of the variation contributed by

the physiognomies of the forests, could be

related to the floristic composition. This varia-

tion would provide specific perches, shelters,

or feeding sites for the birds and influence the

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

decision to choose one site over another. But

the seasonal differences in bird assemblage

between sites also might be influenced by the

migratory effect. Seasonal variations in the

bird assemblages, caused by migrations, have

been widely studied (Capllonch et al., 2008;

Capllonch, 2018; Carvalho et al., 2013; Lima et

al, 2021). The studied wetlands are in the flu-

vial biological corridor of the Paraná River. The

relative position of the national parks studied in

the great corridor and their proximity to migra-

tory routes might be additional variables that

influence the preference for one site or another

and, therefore, in the arrangement of bird com-

munities between sites.

In bird assemblages of highly heteroge-

neous riparian environments, seasonal changes

are very evident (Lima et al, 2021; Lorenzón et

al., 2019; Ronchi-Virgolini et al., 2013), which

may explain the high seasonal variation of our

results, regardless of microspatial variation.

However, it should be noted that the migratory

condition would not allow us to predict habitat

selection (Horlent et al., 2003); therefore, the

effect of migration on forests preference would

rather be random.

The variation detected within levee for-

ests shows that a deeper analysis is needed

for differences in composition among verti-

cal strata of the understory (De Stefano et al.,

2012). Thus, the differential niche offer that

optimizes resources for birds could be more

clearly evidenced, considering that the turn-

over rate in plant composition is high in these

environments. Therefore, deeper analyses of

the differences in the bird assemblage using a

functional classification criterion, i.e., guild,

may reveal subtle aspects that are poorly detect-

able from a general perspective (Farías et al.,

2007; Milesi et al., 2002; Ronchi-Virgolini et

al., 2011; Root, 1967). Guild-based analyses

would contribute more specific information

to properly guide conservation efforts in these

wetland environments, where variation at dif-

ferent scales is clear.

We conclude that there are at least three

categories of levee forests on floodplains deter-

mined by differences in their vegetation cover,

and that birds respond differentially to these

conditions. These findings show the impor-

tance of habitat heterogeneity in river-asso-

ciated island environments and highlight the

importance of the microhabitat scale in the

levees of floodplains. This allows us to focus

on the underlying dynamics at this scale and

understand the changes that occur in line with

the evolutionary histories of the sites, and the

recovery of environments, while also consid-

ering the changes associated with seasonal

cycles. It is evident to us that, within these wet-

land landscapes, emphasis should not solely

be placed on the mosaic at a macro scale. It is

crucial to concentrate on microspatial dynam-

ics to gain a more profound understanding of

the concealed biological processes within the

islands of these tropical and subtropical envi-

ronments, where heterogeneity is apparent.

We believe that considering the micro-scale

environmental heterogeneity of levee forests in

riparian environments is an important strategy

for planning wetland conservation manage-

ment. This study, in addition to evidencing and

highlighting the existence of differential micro-

habitats within the levee forests, reflects upon

the vegetation dynamics, bird behavior and the

transition of the riparian forest in its recovering

towards a more natural state, where the pulse

of the river and the effect of seasonality do not

stop operating.

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.

ACKNOWLEDGMENTS

We thank Malena Maroli, Arnaldo Mange-

aud, Pablo Aceñolaza, Estela Rodríguez,

Griselda Urich, and Virginia Piani for valuable

debates and contributions to the elaboration of

18 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

this manuscript. We are grateful to Leonardo

Scarpa for field work. The project was funded

through a Stimulus Scholarship for Scientific

Vocations granted by the National Interuniver-

sity Board, and PICT Piña 2014; PIDAC Piña

2015 and PUE 056-CONICET.

REFERENCES

Aceñolaza, P. G., Povedano, H. E., Manzano, A. S., Muñoz,

J. de D., Areta, J., & Ronchi-Virgolini, A. L. (2004).

Biodiversidad del Parque Nacional Pre-Delta. En F. G.

Aceñolaza (Ed.), Temas de la biodiversidad del litoral

fluvial argentino (Miscelánea, pp. 169–184). Instituto

Superior de Correlación Geológica.

Aceñolaza, P. G., Sione, W. F., Kalesnik, F., & Serafin, M. S.

(2005). Determinación de unidades homogéneas de

vegetación en el Parque Nacional Pre-Delta (Argen-

tina). In F. G. Aceñolaza (Ed.), Temas de la biodi-

versidad del litoral fluvial argentino II (pp. 81–90).

Instituto Superior de Correlación Geológica.

Allouche, O., Kalyuzhny, M., Moreno-Rueda, G., Pizarro,

M., & Kadmon, R. (2012). Area-heterogeneity tra-

deoff and the diversity of ecological communities.

Proceedings of the National Academy of Sciences,

109(43), 17495–17500.

Anderson, N. H., Sedell, J. R., Roberts, L. M., & Triska, F. J.

(1978). The role of aquatic invertebrates in processing

of wood debris in coniferous forest streams. American

Midland Naturalist, 100(1), 64–82.

Anjos, L. D., Volpato, G. H., Lopes, E. V., Serafini, P. P.,

Poletto, F., & Aleixo, A. (2007). The importance of

riparian forest for the maintenance of bird species

richness in an Atlantic Forest remnant, southern Bra-

zil. Revista Brasileira de Zoología, 24(4), 1078–1086.

https://doi.org/10.1590/S0101-81752007000400027

Aves Argentinas. (2015). Categorización de las aves de la

Argentina según su estado de conservación. Ministerio

de Ambiente y Desarrollo Sustentable de la Nación.

https://avesargentinas.org.ar/sites/default/files/Cate-

gorizacion-de-aves-de-la-Argentina.pdf

Baker, J., French, K., & Whelan, R. J. (2002). The edge effect

and ecotonal species: bird communities across a natu-

ral edge in southeastern Australia. Ecology, 83(11),

3048–3059. https://doi.org/10.2307/3071841

Beltzer, A. H., & Neiff, J. (1992). Distribución de las aves en

el valle del río Paraná. Relación con el régimen pul-

sátil y la vegetación. Ambiente Subtropical, 2(1992),

77–102.

Beltzer, A. H., & Quiroga, M. A. (2007). Birds. In M. H.

Iriondo, J. C. Paggi, M. J. Parma (Eds.), The middle

Paraná River. limnology of a subtropical wetland (pp.

363–377). Springer.

Berduc, A., Lorenzón, R. E., & Beltzer, A. H. (2015).

Patrones de diversidad de aves a lo largo de un

gradiente latitudinal de bosques ribereños del río

Paraná medio, Argentina. Revista Mexicana de Biodi-

versidad, 86(2015), 419–430. https://doi.org/10.1016/j.

rmb.2015.04.003

Blake, J. G. (1992). Temporal variation in point counts of

bird in a lowland wet forest in Costa Rica. Condor,

94(1), 265–275. https://doi.org/10.2307/1368816

Bó, R. F., & Malvárez, A. I. (1999). Las inundaciones y la

biodiversidad en humedales: Un análisis del efecto

de eventos extremos sobre la fauna silvestre. En A. I.

Malvárez (Ed.), Tópicos sobre humedales subtropicales

y templados de Sudamérica (pp. 140–161). Oficina

Regional de Ciencia y Tecnología de la UNESCO para

América Latina y el Caribe.

Bó, R. F., Quintana, R.D., Courtalón, P., Astrada, E., Bolko-

vic, M. L., Lo Coco, G., Magnano, A. (2010). Efectos

de los Cambios en el régimen hidrológico por las

actividades humanas sobre la vegetación y la fauna

silvestre del Delta del Río Paraná In D.E. Blanco &

F. M. Méndez (Eds.) Endicamientos y terraplenes en

el Delta del Paraná. Situación, efectos ambientales y

marco jurídico (pp. 106). Secretaría de Ambiente y

Desarrollo Sustentable de la Nación.

Borodowski, E. (2006). Álamos y sauces en el Delta del

Paraná: Situación del sector y silvicultura. Jornadas

Argentinas de Salicáceas, Argentina.

Burnham, K. P., Anderson, D. R., & Huyvaert, K. P.

(2011). AIC model selection and multimodel inferen-

ce in behavioral ecology: Some background, obser-

vations, and comparisons. Behavorial Ecology and

Sociobiology, 65(2011), 23–35. http://doi.org/10.1007/

s00265-010-1029-6

Cabrera, A. L. (1994). Regiones fitogeográficas argentinas.

En W. F. Kugler (Ed.), Enciclopedia Argentina de agri-

cultura y jardinería (pp. 1–85). ACME.

Capllonch, P. (2018). Un panorama de las migraciones de

aves en Argentina. Hornero, 33(1), 1–18.

Capllonch, P., Ortiz, D., & Soria, K. (2008). Importancia del

litoral fluvial argentino como corredor migratorio de

aves. En F.G. Aceñolaza (Ed.), Temas de Biodiversidad

del Litoral III (pp. 107–120). INSUGEO.

Carvalho, D., Horta, P., Raposeira, H., Santos, M., Luís,

A., & Cabral, J. A. (2013). How do hydrological

and climatic conditions influence the diversity and

behavioural trends of water birds in small Medite-

rranean reservoirs? A community-level modelling

approach. Ecological Modelling, 257, 80–87. https://

doi.org/10.1016/j.ecolmodel.2013.02.012

Clarke, K. R., & Warwick, R. M. (2001). Change in marine

communities: An approach to statistical analysis and

interpretation (2nd Ed.). PRIMER-E Plymouth.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

Coconier, E. G., & Di Giacomo, A. S. (2009). Áreas impor-

tantes para la conservación de las aves, América,

Argentina. En C. Devenish, D. F. Díaz-Fernández, R.

P. Clay, I. Davidson, & I. Yépez-Zabala (Eds.), Impor-

tant bird areas Americas-priority sites for biodiversi-

ty conservation (pp. 59–70). BirdLife Conservation

Series.

Cotgreave, P., & Harvey, P. H. (1994). Evenness of abundan-

ce in bird communities. Journal of Animal Ecology,

63(2), 365–374. https://doi.org/10.2307/5554

De Stefano, K., Merler, J. A., Magnano, A. L., Nanni, A.

S., Kandus, P., & Quintana, R. D. (2012). Relation

between environmental heterogeneity and bird distri-

bution and richness in two units of landscapes of the

Delta of the Paraná, Argentina. Ornitologia Neotropi-

cal, 23(2), 169–184.

Di Giacomo, A., & Contreras, J. (2002). Consideraciones

acerca de la diversidad de las aves en relación con el

eje fluvial Paraguay-Paraná en Sudamérica. Historia

Natural, 1(5), 23–29.

Drobner, U., Bibby, J., Smith, B., & Wilson, J. B. (1998). The

relation between community biomass and evenness:

What does community theory predict, and can these

predictions be tested? Oikos, 82(2), 295–302. https://

doi.org/10.2307/3546969

eBird. (March, 2020). An online database of bird distribution

and abundance. Cornell Lab of Ornithology, Ithaca,

New York. http://www.ebird.org.

Farías, A. A., Marone, L., & Jaksic, F. M. (2007). Gremios.

En F. M. Jaksic, & L. Marone (Eds.), Ecología de

comunidades (pp. 145–336). Ediciones Universidad

Católica de Chile.

Frutos, A. E., Ronchi-Virgolini, A. L., Giraudo, A. R., &

Piña, C. I. (2020a). How does cattle raising affect bird

communities in the delta of the Paraná River? Journal

for Nature Conservation, 57(2020), 125872. https://

doi.org/10.1016/j.jnc.2020.125872

Frutos, A. E., Leiva, P. M. L., & Piña, C. I. (2020b). Bird

community changes associated with cattle raising

management in the delta forests of the Paraná River.

Basic and Applied Ecology, 49(2020), 13–21. https://

doi.org/10.1016/j.baae.2020.09.011

Frutos, A. E. (2018). Efecto de la ganadería sobre ensambles

de aves en bosques fluviales de la región del Delta del

río Paraná (Tesis doctoral). Universidad Nacional del

Litoral, Argentina. http://hdl.handle.net/11185/1156

García, C., Renison, D., Cingolani, A. M., & Fernández-Juricic,

E. (2008). Avifaunal changes as a consequence of large

scale livestock exclusion in the mountains of Central

Argentina. Journal of Applied Ecology, 45(1), 351–360.

https://doi.org/10.1111/j.1365-2664.2007.01388.x

Giacosa, B., Andelman, M., Balderrama, D., Matarasso,

M. (2019). Plan de manejo del sitio Ramsar Delta e

Islas del Paraná. Fundación Humedales, Wetlands

International.

Giraudo, A., & Ordano, M. A. (2003). Patrones de diver-

sidad de las aves del Iberá: variación de la riqueza,

abundancia y diversidad entre localidades, regiones y

hábitats. En B.B. Álavarez (Ed.), Fauna del Iberá (pp.

235–256). Universidad Nacional del Nordeste.

Godoi, M. N., Laps, R. R., Ribeiro, D. B., Aoki, C., & de

Souza, F. L. (2017). Bird species richness, composition

and abundance in pastures are affected by vegetation

structure and distance from natural habitats: A single

tree in pastures matters. Emu-Austral Ornithology,

118(2), 201–211. https://doi.org/10.1080/01584197.2

017.1398591

Granados-Sánchez, D., Hernández-García, M. A., López-

Ríos, G. F. (2006). Ecología de las Zonas Ribere-

ñas. Revista Chapingo. Serie Ciencias Forestales y del

Ambiente, 12(1), 55–69.

Gureev, S. P., Nekhoroshev, O. G., & Mitchell, P. J. (2019).

Spatial heterogeneity of bird communities in the

natural landscapes of the Southern Taiga of the

Ob–Yenisei Interfluve and the Chulym River Valley

(Tomsk Region). IOP Conference Series: Earth and

Environmental Science, 400, 012014. https://doi.

org/10.1088/1755-1315/400/1/012014

Heleno, R., & Vargas, P. (2015). How do islands become

green? Global Ecology and Biogeography, 24, 518-526.

https://doi.org/10.1111/geb.12273

Hernández-Belloso, C. M., García-Prieto, J. C., Martín, R.,

de Tapia, R., García-Roig, M., Silla, F., Núñez-Nuñez,

C., & Proal-Nájera, J. B. (2018). Efectos de la calidad

del agua y la heterogeneidad del hábitat en las comuni-

dades de aves de graveras restauradas y activas [Comu-

nicación técnica escrita]. XIV Congreso Nacional del

Medio Ambiente, Madrid, España.

Horlent, N., Juárez, M. C., & Arturi, M. (2003). Incidencia

de la estructura del paisaje sobre la composición de

especies de aves de los talares del noreste de la provin-

cia de Buenos Aires. Ecología Austral, 13(2), 173–182.

Huff, M. H., Bettinger, K. A., Ferguson, H. L., Brown, M. J.,

& Altman, B. (2000). A habitat based point-count pro-

tocol for terrestrial birds, emphasizing Washington and

Oregon. General Technical Report Pacific Northwest

Research Station, Forest Service, U.S. Department of

Agriculture.

Islands of Santa Fe National Park (ISFNP). (Septiembre,

2022). Parque Nacional Islas de Santa Fe. https://www.

argentina.gob.ar/parquesnacionales/islasdesantafe

International Union for Conservation of Nature (IUCN).

(2023). The Red List of Threatened Species. https://

www.iucnredlist.org/

Kottek, M., Grieser, J., Beck, C., Rudolf, B., & Rubel, F. (2006).

World map of the Köppen-Geiger climate classification

20 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

updated. Meteorologische Zeitschrift, 15(3), 259–263.

https://doi.org/10.1127/0941-2948/2006/0130

Kubitz & Ziburski Kubitzki, K. & Ziburski, A. (1994). Seed

dispersal in flood plain forests of Amazonia. Biotropi-

ca, 26(1), 30-46. http://www.jstor.org/stable/2389108

Laanisto, L., Tamme, R., Hiiesalu, I., Szava-Kovats, R.,

Gazol, A., & Pärtel, M. (2013). Microfragmentation

concept explains non positive environmental hete-

rogeneity-diversity relationships. Oecología, 171(1),

217–226. https://doi.org/10.1007/s00442-012-2398-5

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 Para-

na Atlantic Forest. Brazilian Journal of Biology, 84(25),

e251438. https://doi.org/10.1590/1519-6984.251438

Lorenzón, R. E. (2014). Respuestas biológicas de ensambles

de aves no-paseriformes a la variación espacio-tem-

poral de ambientes acuáticos a escalas local y regional

en la planicie de inundación del Paraná Medio (Tesis

Doctoral). Universidad Nacional del Litoral.

Lorenzón, R. E., Beltzer, A. H., Olguin, P. F., & Ronchi-

Virgolini, A. L. (2016). Habitat heterogeneity drives

bird species richness, nestedness and habitat selection

by individual species in fluvial wetlands of the Paraná

River, Argentina. Austral Ecology, 41(7), 829–841.

https://doi.org/10.1111/aec.12375

Lorenzón, R. E., Beltzer, A. H., Olguin, P. F., León, E. J.,

Sovrano, L. V., Antoniazzi, C. E., & Ronchi‐Virgolini,

A. L. (2019). Temporal variation of bird assemblages

in dynamic fluvial wetlands: seasonality and influen-

ce of water level and habitat availability. Revista

de Biología Tropical, 67(6), 1131–1145. https://doi.

org/10.15517/RBT.V67I6.36734

MacArthur, R. H., & MacArthur, J. W. (1961). On bird

species diversity. Ecology, 42(3), 594–598. https://doi.

org/10.2307/1932254

Magnano, A. L., Fracassi, N. G., Nanni, A. S., & Quintana,

R. D. (2019). Changes in bird assemblages in an affo-

restation landscape in the Lower Delta of the Paraná

River, Argentina. Emu-Austral Ornithology, 2019, 1–9.

https://doi.org/10.1080/01584197.2019.1581032

Malvárez, A. I. (1999). El Delta del Río Paraná como

mosaico de humedales. En A. I. Malvárez (Ed.),

Tópicos sobre humedales subtropicales y templados de

Sudamérica (pp. 35–53). Oficina Regional de Ciencia

y Tecnología de la UNESCO para América Latina y el

Caribe (ORCYT).

Mangeaud, A., & Elías-Panigo, D. H. (2018). R-Medic:

Un programa de análisis estadísticos sencillo e

intuitivo. Revista Methodo, 3(1), 18-22. https://doi.

org/10.22529/me.2018.3(1)05

Martin, T. E. (1993). Nest predation among vegetation

layers and habitat types: Revising the dogmas. The

American Naturalist, 141(6), 897–913. https://doi.

org/10.1086/285515

Martin, T. G., & McIntyre, S. (2007). Impacts of livestock gra-

zing and tree clearing on birds of woodland and ripa-

rian habitats. Conservation Biology, 21(2), 504–514.

https://doi.org/10.1111/j.1523-1739.2006.00624.x

Martin, T. G., & Possingham, H. P. (2005). Predicting the

impact of livestock grazing on birds using foraging

height data. Journal of Apllied Ecology, 42(2), 400–408.

https://doi.org/10.1111/j.1365-2664.2005.01012.x

Matteucci, D. S., & Colma, A. (1982). Metodología para

el estudio de la vegetación. Secretaría General de la

Organización de los Estados Americanos.

Matteucci, D. S. (2012). Ecorregión delta e islas de los ríos

Paraná y Uruguay. En J. Morello, S. D. Matteucci,

& A. F. Rodríguez (Eds.), Ecorregiones y complejos

ecosistémicos argentinos (pp. 447–488). Orientación

Gráfica Editora.

Matthew, R. E. S., & Moussalli, A. (2011). A brief guide to

model selection, multimodel inference and model

averaging in behavioural ecology using Akaike’s

information criterion. Behavioral Ecology and Socio-

biology, 65(2011), 13–21. https://doi.org/10.1007/

s00265-010-1037-6

McCune, B., & Mefford, M. J. (1999). PC-ORD. Multiva-

riate analysis of ecological data, version 4.28. MjM

Software Design, Gleneden Beach, OR.

Milesi, F. A., Marone, L., Lopez de Casenave, J., Cueto, V. R.,

& Mezquida, E. T. (2002). Gremios de manejo como

indicadores de las condiciones del ambiente: un estu-

dio de caso con aves y perturbaciones del hábitat en

el Monte central, Argentina. Ecología Austral, 12(2),

149–161.

Miller, J. R., Dixon, M. D., & Turner, M. G. (2004). Respon-

se of avian communities in large-river floodplains to

environmental variation at multiple scales. Ecological

Applications, 14(5), 1394–1410. https://www.jstor.org/

stable/4493659

Munes, E. C., Dixon, M. D., Swanson, D. L., Merkord, C. L.,

& Benson, A. R. (2015). Large, infrequent disturbance

on a regulated river: response of floodplain forest

birds to the 2011 Missouri River flood. Ecosphere,

6(11), 212.

Naiman, R. J., Décamps, H., & McClain, M. (2005). Riparia:

Ecology, Conservation and Management of Streamside

Communities. Elsevier.

Narosky, T., & Yzurieta, D. (2010). Guía para la identifi-

cación de las aves de Argentina y Uruguay. Vázquez

Mazzini Editores.

Neiff, J. J., & Malvárez, A. I. (2004). Grandes humedales

fluviales. In I. Malvárez & R. F. Bó (Eds.), Documentos

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

del curso taller bases ecológicas para la clasificación e

inventario de humedales en Argentina (pp. 77–85).

Neiff, J. J. (2005). Bosques fluviales de la cuenca del Paraná.

En J. F. Goya, J. L. Frangi, & M. F. Arturi (Eds.), Eco-

logía y manejo de los bosques de Argentina (pp. 1–26).

Editorial de la Universidad Nacional de La Plata.

Nestler, J. M., Baigún, C. R., Oldani, N., & Weber, L. J.

(2007). Contrasting the middle Paraná and Missis-

sippi Rivers to develop a template for restoring large

floodplain river ecosystems. International Journal of

River Basin Management, 5(2), 305–319. https://doi.

org/10.1080/15715124.2007.9635329

Nieves-Vele, K. A., & Orellana-Peralta, D. G. (2018).

Regeneración natural de especies leñosas en claros del

Área de Bosque y Vegetación Protectora Aguarongo

(ABVPA): influencia de factores abióticos e implicacio-

nes para la restauración. Universidad del Azuay.

Nores, M. (1987). Zonas ornitogeográficas de Argentina.

En T. E. Narosky, & D. Yzurieta (Eds.), Guía para la

identificación de las aves de Argentina y Uruguay (pp.

295–305). Asociación Ornitológica del Plata.

Oksanen, J. (2011). Multivariate analysis of ecological com-

munities. R: vegan tutorial. http://cran.rproject.org

Olff, H., & Ritchie, M. E. (1998). Effects of herbivores

on grassland plant diversity. Trends in Ecology &

Evolution, 13(7), 261–265. https://doi.org/10.1016/

S0169-5347(98)01364-0

Pre-Delta National Park (PDNP). (September, 2022). Par-

que Nacional Pre-Delta, Provincia de Entre Ríos.

https://www.argentina.gob.ar/parquesnacionales/

predelta

Placci, L. G. (1994). Estructura y funcionamiento fenológico

en relación a un gradiente hídrico en bosques del Este

de Formosa (Tesis doctoral). Universidad Nacional

de La Plata.

Quinn, G., & Keough, M. (2002). Experimental design and

data analysis for biologists. Cambridge University

Press.

Quintana, R. D., & Bó, R. F. (2010). Caracterización general

de la región del Delta del Paraná. En D. E. Blanco,

& F. M. Méndez (Eds.), Endicamientos y terraplenes

en el Delta del Paraná: situación, efectos ambientales

y marco jurídico (pp. 5–14). Wetlands International.

R Core Team. (2019). R: A language and environment for

statistical computing. R Foundation for Statistical

Computing. Vienna, Austria. https://www.R-project.

org/

Ralph, C., Geupel, G., Pyle, P., Martin, T., De Sante, D., &

Mila, B. (1996). Manual de métodos de campo para

el monitoreo de aves terrestres. Pacific Southwest

Research Station, Forest Service, U.S. Department of

Agriculture.

Rannestad, O. T., Tsegaye, D., Munishi, P. K. T., & Moe,

S. R. (2015). Bird abundance, diversity, and habitat

preferences in the riparian zone of a disturbed wet-

land ecosystem: The Kilombero Valley, Tanzania.

Wetlands, 35(3), 521–532. https://doi.org/10.1007/

s13157-015-0640-8

Remsen, J. V. Jr., Areta, J. I., Bonaccorso, E., Claramunt, S.,

Jaramillo, A., Lane, D. F., Pacheco, J. F., Robbins, M.

B., Stiles, F. G., & Zimmer, K. J. (2022). A classifica-

tion of the bird species of South America. American

Ornithological Society.

Ringuelet, R. A. (1961). Rasgos de la zoogeografía de la

Argentina. Physis, 22(63), 151–170.

Robinson, C. T., Tockner, K., & Ward, J. V. (2002).

The fauna of dynamic riverine landscapes. Fres-

hwater Biology, 47(4), 661–677. https://doi.

org/10.1046/j.1365-2427.2002.00921.x.

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

A. (2008). Bird Communities in wetlands along

the Lower Paraná River, Entre Ríos, Argentina.

Avian Biology Research, 1(4), 153–163. https://doi.

org/10.3184/175815508X404282

Ronchi-Virgolini, A. L., Lorenzón, R. E., Blake, J. G., & Belt-

zer, A. H. (2013). Temporal variation of bird assem-

blages in a wetland: influence of spatial heterogeneity.

Avian Biology Research, 6(3), 198–206.

Ronchi-Virgolini, A. L., Blake, J. G., Lorenzón, R. E., &

Beltzer, A. H. (2011). Bird assemblages in two types

of forests in the floodplain of the lower Paraná River

(Argentina). Ornitología Neotropical, 22(3), 387–404.

Ronchi-Virgolini, A. L., Lorenzón, R. E., Beltzer, A. H., &

Alonso, J. M. (2010). Ensambles de aves del Parque

Nacional Pre-Delta (Entre Ríos, Argentina): análisis

de la importancia ornitológica de distintas unida-

des ambientales. Hornero, 25(1), 27–40. https://doi.

org/10.56178/eh.v25i1.709

Root, R. B. (1967). The niche explotation pattern of the

blue-gray gnatcatcher. Ecological monographs, 37(4),

317–350. https://doi.org/10.2307/1942327

Rosenzweig, M. L. (1995). Species diversity in space and time.

Cambridge University Press. https://doi.org/10.1017/

CBO9780511623387

Rossetti, M. A., & Giraudo, A. R. (2003). Comunidades de

aves de bosques fluviales habitados y no habitados por

el hombre en el río Paraná medio, Argentina. Horne-

ro, 18(2), 89–96. http://hdl.handle.net/20.500.12110/

hornero_v018_n02_p089

Sabattini, R. A., & Lallana, V. H. (2007). Aquatic macro-

phytes. In M. H. Iriondo, J. C. Paggi, & M. J. Parma

(Eds.), The middle Paraná River (pp. 205–226).

Springer.

22 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56175, enero-diciembre 2024 (Publicado Set. 10, 2024)

Symonds, M. R. E., & Johnson, C. N. (2008). Species richness

and evenness in Australian birds. American Natura-

list, 171(4), 480–490. https://doi.org/10.1086/528960

Tavares, D. C., Guadagnin, D. L., de Moura, J. F., Sici-

liano, S., & Merico, A. (2015). Environmental and

anthropogenic factors structuring waterbird habitats

of tropical coastal lagoons: Implications for manage-

ment. Biological Conservation, 186, 12–21. https://doi.

org/10.1016/J.BIOCON.2015.02.027

Tockner, K., Malard, F., & Ward, J. V. (2000a). An extension

of the ﬂood pulse concept. Hydrological Processes,

14(16-17), 2861–2883. https://doi.org/10.1002/1099-

1085(200011/12)14:16/17<2861::AID-

HYP124>3.0.CO;2-F

van Nes, E. H. & Scheffer, M. (2005). Implications of spatial

heterogeneity for catastrophic regime shifts in ecosys-

tems. Ecology, 86(7), 1797–1807.

Velásquez-Valencia, A. (2018). Influencia de la configu-

ración y composición de los paisajes agroforestal y

silvopastoril en la estructura de la comunidad de aves

del piedemonte amazónico (Tesis doctoral). Univer-

sidad de Colombia. https://repositorio.unal.edu.co/

handle/unal/64065

Vellend, M. (2001). Do commonly used indices of diversity

measure species turnover? Journal of Vegetation Scien-

ce, 12(4), 545–552. https://doi.org/10.2307/3237006

Verner, J., & Milne, K. A. (1989). Coping with sources of

variability when monitoring population trends. Anna-

les Zoologici Fennici, 26, 191–199.

Viana, A. C. M., & Jardim, F. C. (2013). Natural regenera-

tion dynamics of Couratari guianensis in a tropical

forest selectively logges in Moju, state of Para, Brazil.

Amazonian Journal of Agricultural and Environment

Sciences, 56(2), 112–119.

Zerda, H. R., & Tiedemann, J. L. (2010). Dinámica temporal

del NDVI del bosque y pastizal natural en el Chaco

Seco de la Provincia de Santiago del Estero, Argenti-

na. Ambiencia, 6(1), 1–11.