Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

Space-time patterns and drivers of migrant bird communities

in coastal Piauí State, Brazil

Cleiton O. Cardoso¹*; https://orcid.org/0000-0002-0340-2553

Davi da S. Sales¹; https://orcid.org/0000-0002-2093-5239.

Muryllo dos S. Nascimento²; https://orcid.org/0000-0002-7013-443X

Airton Janes da S. Siqueira²; https://orcid.org/0000-0002-1709-0490

Ocivana A. Pereira²; https://orcid.org/0000-0003-0088-3686

Suely S. dos Santos²; https://orcid.org/0000-0002-4971-1458

Francisco das Chagas V. dos Santos²; https://orcid.org/0000-0001-7855-7069

Pedro B. de M. Carneiro3; https://orcid.org/0000-0002-4577-3803

Anderson Guzzi2,3; https://orcid.org/0000-0001-7206-7683

1. Secretaria de Estado da Educação – SEDUC, 1ª GRE, Avenida das Normalistas, SN, Bairro Nova Parnaíba, Parnaíba,

Piauí, Brazil; cleitonoliveiraphb@hotmail.com (*Correspondence), davigenial@gmail.com

2. Programa de Pós-graduação em Desenvolvimento e Meio Ambiente (PRODEMA), Universidade Federal do Piauí,

Avenida Universitária, N°1310, Teresina, PI, Brazil; muryllobiologo84@gmail.com, airtonjanes_@hotmail.com,

ocivanaaraujo@gmail.com, suelysantos.bio@gmail.com, fcovieira2@gmail.com, guzzi@ufpi.edu.br

3. Centro de Ciências do Mar, Curso de Ciências Biológicas, Universidade Federal do Delta do Parnaíba (UFDPAR), Av.

São Sebastião, 2819, Planalto Horizonte, 64202-020, Parnaíba, Piauí, Brazil; pedrocarneiro@ufpi.edu.br

Received 07-VI-2022. Corrected 15-VIII-2022. Accepted 20-II-2023.

ABSTRACT

Introduction: Migration is a natural phenomenon that includes annual movements of many bird species in

response to seasonal cycles. With approximately one third of all living bird species, South America has an

important avifauna, and many migrants land in Brazil at stopping points and wintering sites.

Objective: To identify associations between migrant birds and coastal vegetation, and environmental influence

of on migration.

Methods: At 10 points along the coast of Piauí State, Brazil, we made visual censuses and mist net captures,

between April 2009 and February 2016.

Results: We identified 82 migrant bird species (13 orders; 28 families) that represented 41 intracontinental

migrating species, 26 northern visiting species, 14 nomad species and one vagrant species. The richness peaks

were at the beginning and end of both dry and rainy seasons, matching insolation and atmospheric pressure.

There were spatial pattern differences among vegetation complexes. Chrysolampis mosquitus is an indicator of

caatinga vegetation, Numenius phaeopus of wetland, Charadrius collaris of non-flooding fields, Rostrhamus

sociabilis of forest-grassland transition, and Columbina picui of orchards. Despite differences in number and

species composition within vegetation types, the temporal pattern in species richness was similar among flooded

fields, non-flooded fields, and transition grassland categories.

Conclusions: Migrant birds occupy specific environments during their permanence along the coast of Piauí

State, with richness matching insolation and atmospheric pressure.

Key words: climatic variables; environment; movements; migration chronology; stopover.

https://doi.org/10.15517/rev.biol.trop..v71i1.47300

TERRESTRIAL ECOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

INTRODUCTION

In total, 1 971 bird species are distributed

in the Brazilian territory, based on the Bra-

zilian Committee of Ornithological Records,

also known as CBRO (Pacheco et al., 2021).

The National Research Center for Wild Birds

Conservation, also known as CEMAVE, often

published the Annual Report of Migrant Birds

Routes and Concentration Sites in Brazil.

Based on this report, coastal Piauí State (BR)

holds two migratory routes; this state is pointed

out as concentration site for shorebirds and

migrant birds in the country; it also empha-

sizes the important role played by this site for

these species’ conservation (CEMAVE, 2020).

Oftentimes, these birds get to the wintering

sites by late August and early September; they

stay in this location until April, when they once

more return to their breeding grounds (Cabral

et al., 2006; Silva & Rodrigues, 2015; Somen-

zari et al., 2018).

Several localities along the coast of Piauí

State (BR) are wintering sites for migrant

birds. Guzzi et al. (2012) reported 17 migrant

species in Parnaíba River Delta; 7 species were

observed at Parnaíba International Airport - they

were identified as Nearctic migrants belonging

to families Charadriidae, Scolopacidae and

Hirundinidae (Cardoso et al, 2013). Guzzi et al.

(2015) reported 16 Nearctic migrant species at

Pedra do Sal Beach (in Parnaíba River Delta),

as well as three austral migrants and one par-

tially Nearctic migrant species.

Some factors have influenced the distribu-

tion and abundance of migrant birds; among

them, one finds habitat conditions and the

availability or food resources. (Neima et al.,

2020; Rodrigues et al., 2015). Studies carried

out in neotropic areas, for example, have shown

the importance of migrant birds in tropical bird

communities, with emphasis on the fact that

this group cannot be taken as element external

to these communities because they showed

domination over and segregation patterns of

habitats inside a wintering site (Kelsey, 1992).

However, they can be particularly vulnerable to

climate changes, either in wintering sites or in

breeding grounds (Sanderson et al., 2006).

RESUMEN

Patrones y factores espacio-temporales de comunidades

de aves migratorias en el estado costero de Piauí, Brasil

Introducción: La migración es un fenómeno natural que incluye los movimientos anuales de muchas especies

de aves en respuesta a los ciclos estacionales. Con aproximadamente un tercio de todas las especies de aves

conocidas, América del Sur tiene una avifauna importante y muchas aves migratorias tienen puntos de parada e

invernada en Brasil.

Objetivo: Identificar asociaciones entre las aves migratorias y la vegetación costera, y la influencia del medio

ambiente en la migración.

Métodos: En 10 puntos a lo largo de la costa del Estado de Piauí, Brasil, realizamos censos visuales y capturas

con redes de niebla, entre abril 2009 y febrero 2016.

Resultados: Identificamos 82 especies de aves migratorias (13 órdenes; 28 familias) que representaron 41

especies migratorias intracontinentales, 26 especies visitantes del norte, 14 especies nómadas y una especie

vagante. Los picos de riqueza se dieron al principio y al final de las estaciones seca y lluviosa, coincidiendo

con la insolación y la presión atmosférica. Hubo diferencias en el patrón espacial entre los complejos de veg-

etación. Chrysolampis mosquitus es un indicador de vegetación de caatinga, Numenius phaeopus de humedales,

Charadrius collaris de campos que no se inundan, Rostrhamus sociabilis de transición bosque-pastizales y

Columbina picui de huertos. A pesar de las diferencias en el número y composición de especies dentro de los

tipos de vegetación, el patrón temporal en la riqueza de especies fue similar entre las categorías de campos inun-

dados, campos no inundados y pastizales de transición.

Conclusiones: Las aves migratorias ocupan ambientes específicos durante su permanencia a lo largo de la costa

del estado de Piauí, con una riqueza acorde con la insolación y la presión atmosférica.

Palabras clave: variables climáticas; ambiente; movimientos; cronología migratoria; escala.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

Climate changes can also influence indi-

vidual behaviors, breeding success and the

population dynamics of migrant birds, a fact

that can change the patterns and connections

between specific summer and winter popu-

lations (Webster & Marra, 2005). Breeding

locations are linked to wintering sites by the

movements of individuals belonging to any

migratory organism (Webster et al., 2002).

Many different connectivity patters are pos-

sible to happen, in other words, connectivity is

strong if most individuals who reproduce in a

given site also spend winter together in a given

location (Salomonsen, 1995).

The conservation of migrant birds is

closely associated with the identification and

protection of sites used for resting, feeding

and breeding, since the loss of some of these

locations can be decisive for some species’ sur-

vival. Continuity and expansion of monitoring

procedures applied to Nearctic migrant birds

visiting Brazil are essential for their survival

(Graff et al., 2016; Somenzari et al., 2018).

Thus, the aim of the present study was to

investigate spatiotemporal patterns of migrant

bird species richness and composition along the

coast of Piauí State, Brazil, by correlating these

community features to both local climate and

vegetation features.

MATERIALS AND METHODS

Study site: Data were collected at 10

sites along the coast of Piauí State, Brazil

(Fig. 1), one site in Ilha Grande County, two

in Luis Correia County and seven sites in Par-

naíba County. These sites were chosen because

of previous knowledge on their occupation

by migrant birds. Each site was classified

based on its prevalent vegetation type, accord-

ing to Santos-Filho et al. (2010). The points

were classified into two main vegetation types,

based on this scheme: “caatinga” (typical of

dry inland areas) and “restinga” (typical of

coastal regions). Restinga was divided into four

subtypes: flooded fields (2 sites), non-flooded

Fig. 1. Sampling points along the coast of Piauí State, Brazil.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

fields (3 sites), transition grasslands (1 site)

and orchards (3 sites).

Data collection: Quantitative survey on

migrant birds was carried out between April

2009 and February 2016 based on visual obser-

vations (with binoculars) and mist net captures.

Visual observations were performed in study

sites, which were divided into transects that

were surveyed at dawn and dusk with the aid

of binoculars (10X50) and digital recorder

equipped with directional microphone to cap-

ture and replay birds’ vocalizations. Mist nets

(2.5 m × 30 mm × 12 m) were used at dusk

and dawn; they were visited every 20 min. The

nets were extended near vegetation formations

and/or aquatic sites. Stotz et al. (1996), Nunes

and Tomas (2008), Pacheco et al. (2021) and

Somenzari et al. (2018) were used as reference

for birds’ identification. Their conservation

statuses were determined by following the

classification by the International Union for

Conservation of Nature (IUCN, 2022).

Data processing and analyses: The

sampling effort among sites and months was

first equalized through rarefaction analysis

to determine the spatial and temporal pat-

terns of migrant bird species’ richness. The

expected richness (i.e., the rarefied number

of species) plus or minus twice its standard

deviation was the calculation used to make the

comparisons. Expected (rarefied) richness per

month was regressed against monthly values

recorded for five climatic variables to help

explaining the temporal patterns, namely: mean

temperature (ºC), total rainfall (mm), mean

wind speed (m/s), mean insolation (W/m2) and

mean atmospheric pressure (Pa), which were

collected from the Agrometeorological Bul-

letin of EMBRAPA Meio-Norte. An elastic net

regression was used, since these five variables

can be highly correlated and, consequently,

hinder model interpretation and applicability.

It was done by assuming the Gaussian error

distribution and by estimating penalization

(α) and shrinkage (λ) parameters via leave-

one-out cross-validation, in order to select

variables and regulate model coefficients (Zou

& Hastie, 2005). Finally, spatial patterns were

investigated through PERMANOVA by using a

Bray-Curtis dissimilarity matrix of field cam-

paigns grouped by vegetation type. Therefore,

we investigated vegetation’s likely influence

on bird assemblies’ composition in each sam-

pling site. The IndVal test was used to identify

potential indicator species for each vegetation

type, among the migratory birds, in order to

qualify these differences among communities.

All statistical analyses were run in R software

(R Core Team, 2019), in packages vegan 2.4-6

and glmnet 2.0-16 - values were considered sta-

tistically significant when P < 0.05. The trophic

categories followed the classification proposed

by Motta-Júnior (1990): granivores (GRAN),

with ¾ or more grains; frugivores (FRU), with

¾ or more fruits; insectivores (INSET), with

¾ or more insects and other arthropods in the

diet; omnivores (ONIV), with more than ¾ of

insects, other arthropods and fruits, in similar

proportions; aquatic invertebrates (INVAQ),

diet with more than ¾ of aquatic invertebrates;

carnivores (CARN) and scavengers (NECRO),

living and dead vertebrates, respectively, at

least in ¾ of the diet; malacophagi (MAL),

with ¾ or more of mollusks and piscivores

(PISC), with ¾ or more of fish.

RESULTS

Eighty-two migrant bird species were

recorded along the coast of Piauí State. They

belonged to 13 orders and 28 families, and

represented 41 intracontinental migrant spe-

cies (50 %) in South America, 26 species of

Northern visitors (31.7 %), 14 nomad species

(17.07 %) and 1 vagrant species (1.21 %).

These species were distributed into 10 feeding

guilds, with the prevalence of trophic guilds,

namely: 22 species (26.8 %) feeding on aquatic

arthropods; 19 species (23.2 %) of insectivo-

rous birds; 16 omnivore species (19.5 %); 10

piscivorous species (12.2 %); 6 granivore spe-

cies (7.3 %); three nectarivore species (3.7 %);

2 carnivore species (2.4 %); 2 molluscivorous

species (2.4 %); one frugivore species (1.2 %);

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

and one insectivore/granivore species (1.2 %).

With respect to sensitivity to environmental

changes, 47 bird species (57.3 %) were clas-

sified as low-sensitivity species, 24 (29.3 %)

as medium-sensitivity species, 6 (7.3 %) as

high-sensitivity species; 5 (6.1 %) species did

not record any sensitivity at all. As for depen-

dence on forest environments, 61 species (74.4

%) were independent, 9 (10.1 %) were semi-

dependent, 7 (8.5 %) were dependent, and 5

species (6.1 %) did not record any dependence.

Finally, when it comes to conservation status,

80 species (97.56 %) were of least concern,

whereas 2 species (2.44 %) were considered as

close to endangering (Calidris canutus and C.

pusilla) (Table 1).

TABLE 1

Migrant birds recorded along the coast of Piauí State, Brazil

TAXON NAME STATUS GUILD SE UH SC EN FR

ANSERIFORMES Linnaeus, 1758

ANATIDAE Leach, 1820

DENDROCYGNINAE Reichenbach, 1850

Dendrocygna viduata (Linnaeus, 1766) INTRA ONI BAI IN LC OS 17

ANATINAE Leach, 1820

Amazonetta brasiliensis (Gmelin, 1789) NO PIS BAI IN LC OS 2

PODICIPEDIFORMES Fürbringer, 1888

PODICIPEDIDAE Bonaparte, 1831

Podilymbus podiceps (Linnaeus, 1758) INTRA PIS MED IN LC

Tachybaptus dominicus (Linnaeus, 1766) INTRA PIS MED IN LC

SULIFORMES Sharpe, 1891

PHALACROCORACIDAE Reichenbach, 1849

Nannopterum brasilianum (Gmelin, 1789) INTRA PIS BAI IN LC TG 98

PELECANIFORMES Sharpe, 1891

ARDEIDAE Leach, 1820

Ardea alba Linnaeus, 1758 INTRA ONI BAI IN LC FF 89

Ardea cocoi Linnaeus, 1766 NO ONI BAI IN LC FF 4

Bubulcus ibis (Linnaeus, 1758) NO INS BAI IN LC NF 152

Egretta caerulea (Linnaeus, 1758) INTRA ONI MED IN LC FF 30

ACCIPITRIFORMES Bonaparte, 1831

PANDIONIDAE Bonaparte, 1854

Pandion haliaetus (Linnaeus, 1758) VN PIS MED IN LC FF 16

ACCIPITRIDAE Vigors, 1824

Elanus leucurus (Vieillot, 1818) INTRA CAR BAI IN LC

Rostrhamus sociabilis (Vieillot, 1817) INTRA MAL BAI IN LC TG 148

GRUIFORMES Bonaparte, 1854

ARAMIDAE Bonaparte, 1852

Aramus guarauna (Linnaeus, 1766) INTRA MAL MED IN LC TG 88

RALLIDAE Rafinesque, 1815

Laterallus melanophaius (Vieillot, 1819) NO ONI BAI SD LC OS 2

Porphyrio martinica (Linnaeus, 1766) INTRA ONI BAI IN LC NF 4

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

TAXON NAME STATUS GUILD SE UH SC EN FR

CHARADRIIFORMES Huxley, 1867

CHARADRII Huxley, 1867

CHARADRIIDAE Leach, 1820

Charadrius collaris Vieillot, 1818 INTRA INVAQ ALT IN LC NF 150

Charadrius semipalmatus Bonaparte, 1825 VN INVAQ MED IN LC NF 68

Pluvialis dominica (Statius Muller, 1776) VN INVAQ ND ND LC NF 6

Pluvialis squatarola (Linnaeus, 1758) VN INVAQ BAI IN LC FF 26

RECURVIROSTRIDAE Bonaparte, 1831

Himantopus melanurus Vieillot, 1817 VN INVAQ MED IN LC NF 25

Himantopus mexicanus (Statius Muller, 1776) VN INVAQ MED IN LC FF 7

SCOLOPACI Steijneger, 1885

SCOLOPACIDAE Rafinesque, 1815

Actitis macularius (Linnaeus, 1766) VN INVAQ BAI IN LC NF 27

Arenaria interpres (Linnaeus, 1758) VN INVAQ ALT IN LC FF 25

Calidris alba (Pallas, 1764) VN INVAQ ND ND LC

Calidris bairdii (Coues, 1861) VN INVAQ ND ND LC

Calidris canutus (Linnaeus, 1758) VN INVAQ ALT IN AT FF 13

Calidris fuscicollis (Vieillot, 1819) VN INVAQ MED IN LC FF 4

Calidris minutilla (Vieillot, 1819) VN INVAQ MED IN LC NF 8

Calidris pusilla (Linnaeus, 1766) VN INVAQ MED DP AT NF 30

Gallinago paraguaiae (Vieillot, 1816) INTRA INVAQ BAI IN LC TG 41

Limnodromus griseus (Gmelin, 1789) VN INVAQ ALT IN LC FF 12

Numenius hudsonicus Latham, 1790 VN INVAQ ND ND LC FF 14

Numenius phaeopus (Linnaeus, 1758) VA (N) INVAQ MED DP LC FF 38

Tringa flavipes (Gmelin, 1789) VN INVAQ BAI IN LC NF 26

Tringa melanoleuca (Gmelin, 1789) VN INVAQ BAI IN LC NF 31

Tringa semipalmata (Gmelin, 1789) VN INVAQ ND ND LC

Tringa solitaria Wilson, 1813 VN INVAQ BAI IN LC NF 24

LARI Sharpe, 1891

LARIDAE Rafinesque, 1815

Leucophaeus atricilla (Linnaeus, 1758) VN PIS MED IN LC

STERNIDAE Vigors, 1825

Phaetusa simplex (Gmelin, 1789) INTRA PIS ALT IN LC

Sterna hirundo Linnaeus, 1758 VN PIS MED SD LC NF 2

Sternula superciliaris (Vieillot, 1819) INTRA PIS BAI IN LC NF 23

RYNCHOPIDAE Bonaparte, 1838

Rynchops Níger Linnaeus, 1758 INTRA PIS ALT IN LC NF 5

COLUMBIFORMES Latham, 1790

COLUMBIDAE Leach, 1820

Columbina picui (Temminck, 1813) NO GRA BAI IN LC OS 128

Patagioenas picazuro (Temminck, 1813) INTRA FRU MED SD LC FF 14

CUCULIFORMES Wagler, 1830

CUCULIDAE Leach, 1820

CUCULINAE Leach, 1820

Coccyzus americanus (Linnaeus, 1758) VN INS MED SD LC

Coccyzus euleri Cabanis, 1873 INTRA INS MED SD LC CA 4

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

TAXON NAME STATUS GUILD SE UH SC EN FR

CAPRIMULGIFORMES Ridgway, 1881

CAPRIMULGIDAE Vigors, 1825

Chordeiles acutipennis (Hermann, 1783) INTRA INS BAI IN LC CA 9

Podager nacunda (Vieillot, 1817) INTRA INS BAI IN LC NF 12

APODIFORMES Peters, 1940

APODIDAE Olphe-Galliard, 1887

Tachornis squamata (Cassin, 1853) NO INS BAI IN LC NF 3

TROCHILIDAE Vigors, 1825

POLYTMINAE Reichenbach, 1849

Anthracothorax nigricollis (Vieillot, 1817) INTRA NEC BAI SD LC

Chrysolampis mosquitus (Linnaeus, 1758) NO NEC BAI IN LC CA 10

TROCHILINAE Vigors, 1825

Thalurania furcata (Gmelin, 1788) NO NEC MED SD LC CA 4

FALCONIFORMES Bonaparte, 1831

FALCONIDAE Leach, 1820

Falco peregrinus Tunstall, 1771 VN CAR MED IN LC

PASSERIFORMES Linnaeus, 1758

TYRANNIDA Wetmore & Miller, 1926

TITYRIDAE Gray, 1840

Xenopsaris albinucha (Burmeister, 1869) INTRA INS MED IN LC CA 1

TYRANNIDAE Vigors, 1825

ELAENIINAE Cabanis & Heine, 1860

Elaenia cristata Pelzeln, 1868 INTRA ONI MED IN LC CA 7

Elaenia mesoleuca (Deppe, 1830) NO INS BAI DP LC CA 2

Elaenia spectabilis Pelzeln, 1868 INTRA ONI BAI DP LC CA 1

Phaeomyias murina (Spix, 1825) INTRA ONI BAI IN LC

Suiriri suiriri (Vieillot, 1818) INTRA INS MED IN LC OS 4

TYRANNINAE Vigors, 1825

Myiarchus swainsoni Cabanis & Heine, 1859 INTRA INS BAI IN LC FF 4

Myiodynastes maculatus (Statius Muller, 1776) INTRA ONI BAI DP LC

Myiozetetes cayanensis (Linnaeus, 1766) INTRA INS BAI DP LC

Myiozetetes similis (Spix, 1825) INTRA ONI BAI SD LC CA 4

Tyrannus melancholicus Vieillot, 1819 INTRA INS BAI IN LC FF 100

FLUVICOLINAE Swainson, 1832

Arundinicola leucocephala (Linnaeus, 1764) NO INS MED IN LC

Fluvicola albiventer (Spix, 1825) NO INS MED IN LC NF 6

Fluvicola nengeta (Linnaeus, 1766) NO INS BAI IN LC OS 11

PASSERI Linnaeus, 1758

CORVIDA Wagler 1830

VIREONIDAE Swainson, 1837

Vireo olivaceus (Linnaeus, 1766) VN ONI BAI DP LC CA 5

PASSERIDA Linnaeus, 1758

HIRUNDINIDAE Rafinesque, 1815

Hirundo rústica Linnaeus, 1758 VN INS BAI IN LC NF 10

Progne chalybea (Gmelin, 1789) INTRA INS BAI IN LC

Progne tapera (Linnaeus, 1766) INTRA INS BAI IN LC

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Migrant birds were recorded over the year.

However, richness peaks, which were estimated

by rarefying the sampling effort of each month,

were mainly observed during season transitions

after major changes in weather conditions in the

assessed region, mainly at the beginning of the

rainy season, or in the beginning and at the end

of the dry season - this pattern was observed in

all three classes of migrants, i.e., intracontinen-

tal, Northern visitors and nomads (Fig. 2).

The elastic net regression led to a model

capable of explaining 30.6 % of species rich-

ness variance based on only two of the five

original climatic variables, namely: insolation

and atmospheric pressure. These two variables

had negative and positive influence on the num-

ber of migrant bird species at the coast of Piauí

State, respectively. This finding suggested the

preference of some species for the easy weather

conditions observed in the region, namely:

little rain and low wind speed (as reflected by

the barometric trend), without excessive solar

radiation - represented by insolation. (Fig. 3).

Vegetation type was a good predictor of

migrant birds’ spatial distribution, since the

habitats were occupied by each species (PER-

MANOVAF4,472 = 16.5, R2 = 0.12, P = 0.001).

Thus, there were significant differences in

bird assemblies’ composition among different

vegetation types observed in coastal Piauí State

(Fig. 4). Despite such a statistical significance,

based on many superpositions observed in

Fig. 4, some species seem to be found in more

than one habitat, or at least in transition sites

among them.

These differences in avifauna can be repre-

sented by different bird species that can work as

indicators for each vegetation type; i.e., some

species were more closely associated with cer-

tain habitats, such as the ruby-topaz humming

bird (Chrysolampis mosquitus), which was

associated with caatinga sites; the whimbrel

(Numenius phaeopus) species, which was asso-

ciated with flooded fields; the collared plover

(Charadrius collaris) species, which was cor-

related to non-flooded fields; the snail kite

TAXON NAME STATUS GUILD SE UH SC EN FR

Tachycineta albiventer (Boddaert, 1783) INTRA INS BAI IN LC

TURDIDAE Rafinesque, 1815

Turdus amaurochalinus Cabanis, 1850 INTRA ONI BAI SD LC CA 21

MOTACILLIDAE Horsfield, 1821

Anthus chii Vieillot, 1818 INTRA INS/GRA BAI IN LC NF 76

PASSERELLIDAE Cabanis & Heine, 1850

Ammodramus humeralis (Bosc, 1792) NO GRA BAI IN LC CA 12

ICTERIDAE Vigors, 1825

Chrysomus ruficapillus (Vieillot, 1819) INTRA ONI BAI IN LC OS 10

Molothrus bonariensis (Gmelin, 1789) NO ONI BAI IN LC

Leistes superciliaris (Bonaparte, 1850) INTRA ONI BAI IN LC OS 74

THRAUPIDAE Cabanis, 1847

Sporophila caerulescens (Vieillot, 1823) INTRA GRA BAI IN LC CA 1

Sporophila lineola (Linnaeus, 1758) INTRA GRA BAI IN LC

Sporophila nigricollis (Vieillot, 1823) INTRA GRA BAI IN LC CA 2

Volatinia jacarina (Linnaeus, 1766) INTRA GRA BAI IN LC OS 9

STATUS: INTRA (intracontinental migrants); NO (nomads); VN (Northern visitors); VA(N) (vagrant species originating

from the Northern hemisphere). GUILDS: ONI (omnivores); PIS (piscivores); INS (insectivores); CAR (carnivores); MAL

(molluscivores); ONI (omnivores); INVAQ (aquatic invertebrates); GRA (granivores); FRU (frugivores); NEC (necrophagic);

INS/GRA (insectivore and granivore). SE (sensitivity): ALT (high); BAI (low); MED (medium); ND (not determined). UH

(habitat use): IN (independent); SD (semi-dependent); DP (dependent); ND (not determined). SC (conservation status):

LC (little concern); AT (almost endangered). EN (Environment): CA (Caatinga); FF (Flooding Fields); NF (Non-Flooding

Fields); TG (TRANSITION GRASSLANDS); OS (Orchard Sites). FR (frequency).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

(Rostrhamus sociabilis) species, which was

associated with transition grasslands; and the

Picui ground dove (Columbina picui) species,

which was mostly related to orchards (Table 1).

It is noteworthy that transition grasslands

were the only vegetation type sampled in

2 discontinuous periods (between 2009-2011

and 2015-2016); they presented differences

in bird assemblies between these two-time

intervals: TG1 and TG2, respectively (Fig. 4).

However, both intervals seemed consistently

different from those of other vegetation types.

Thus, snail kite was the main indicator-species

between 2009-2011, whereas white-browed

meadowlark (Sturnella superciliaris) became

more abundant between 2015 and 2016. This

finding suggests that other factors, besides

vegetation - although associated with it -, may

influence the wintering site of migrant birds at

the coast of Piauí State.

Besides the composition of assemblies, the

species richness of migrant birds also differed

Fig. 2. Barplot of the expected (i.e., rarefied) number of migrant bird species per month at the coast of Piauí State, Brazil.

Groups of bars indicate migratory status: NO (nomad species); IN (intracontinental migrants); VN (Northern visitor

species). Bar colors indicate different seasons often observed in the site.

Fig. 3. Scatterplot depicting the association among monthly migrant bird species richness, mean insolation (SI) and mean

atmospheric pressure (AP) at the coast of Piauí State, Brazil. The model’s equation derived from an elastic net regression.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

among vegetation types - orchards and non-

flooded fields were the richest ones, and tran-

sition grasslands were the poorest categories

(Fig. 5).

Despite differences in number and compo-

sition of species among vegetation types, the

temporal pattern recorded for species richness

was relatively similar among flooded fields,

non-flooded fields and transition grassland

categories - which were the only categories

with samples collected in all assessed months

(Fig. 6).

This temporal pattern was also similar

to the one observed when the whole site was

taken into account, including the different types

of migrant species, namely: intracontinental,

Northern visitors and nomads.

DISCUSSION

In order for shorebirds to survive the

annual migration from the Southern hemi-

sphere to breeding sites in the Artic, they count

on a series of locations throughout their route.

These places provide them with food for them

to replace the energy lost during the flight

(Clark, 2015). The coastal region of Piauí State

has the potential to house a large number of

migrant shorebirds because it is an estuarine

environment (Putra et al., 2017). Muddy habi-

tats in these locations provide a broader source

of food, and it can be observed from the large

number of bird species foraging on them (Silva

& Rodrigues, 2015).

Fig. 4. Biplot of Non-metric Multidimentional Scalling (NMDS) generated from the Bray-Curtis dissimilarity of sampling

campaigns; it depicts differences in species composition of migrant bird assemblies from different vegetation types at the

coast of Piauí State.

Fig. 5. Barplots depicting the expected (i.e., rarefied

to equalize sampling effort) number of migrant bird

species in each vegetation type along the coast of Piauí

State, Brazil. Lines represent 2x the standard deviation of

the expected richness. CA = Caatinga; TG = Transition

grasslands; FF = Flooding Fields; NFF = Non-flooding

Fields; OS = Orchards.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

It is essential highlighting that sites are

influenced by tides and habitat physiognomy

at different times of the year, a fact that makes

food available for birds throughout the whole

seasonal cycle. This feature reduces the need

of these species to move to other physiogno-

mies in order to find food (Cabrera-Cruz et al.,

2020; Palacín et al., 2017). Species may not

finish their trajectory if only one of these sites

is compromised (Clark, 2015).

Migrant species are notably consistent in

terms of their wintering sites, since they sys-

tematically visit habitats known for their food-

resource availability to satisfy their feeding

needs and foraging strategies (Nunes & Tomas,

2008). These requirements help explaining

the significant differences observed in species

compositions between different analyzed sites,

as well as why some species are found in very

specific sites - therefore, they are considered

indicator species. Different sites present dif-

ferent resources, and they determine species

compositions among migrant birds. On the

other hand, despite the generally observed

differences among environments, the coast of

Piauí State is a dense mosaic of different land-

scapes (Santos-Filho et al., 2010); thus, it is

not surprising that several superpositions take

place in it. Therefore, at least some species can

be distributed in transition zones, or even in

more than one habitat; eventually, it results in

complex patterns at species level.

According to the classification system

by Santos-Filho et al. (2010), the study site

includes non-flooding, flooding and grassland

fields, as well as orchards. The first two site

types are basically covered by herbaceous veg-

etation, and they mainly differ from each other

because of their water accumulation during

the rainy season. These differences in vegeta-

tion are followed by differences in avifauna,

as expressed by the indicator-species. Wet

environments seasonally received more water

birds (such as Numenius phaeopus and Ros-

trhamus sociabilis) than dry environments, for

example. Although birds always return to the

same wintering sites, severe changes in these

environments can induce species to search for

other, and more favorable, locations. Assum-

ingly, it happened in sites TG1 and TG2, which

recorded significant differences in their species

compositions overtime. These observations

corroborated Sick (1997), who emphasized the

importance of habitat conservation for species

conservation and noticed that birds are totally

dependent on their environments; therefore,

Fig. 6. Barplots depicting monthly variation in the expected (i.e., rarefied to equalize sampling effort) number of migrant

bird species in each vegetation type along the coast of Piauí State, Brazil. TG = transition grasslands, FF = flooding fields,

NFF = non-flooding fields. Bar colors represent different seasons.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

habitat losses have negative impact on migrant

bird populations (Howard et al., 2018).

Other determining factors regarding

migratory movements lie on climatic influenc-

es. Certain environmental variables are related

to the arrival and departure of intercontinental

migrants, mainly to insolation and atmospheric

pressure. At first, both variables can emerge as

uncommon biodiversity pattern drivers in tropi-

cal regions; however, Romero et al. (2000);

Panuccio et al. (2010) and Ben-Hamo et al.

(2013) considered climatic factors as deter-

minant for migrant birds’ flight paths. They

emphasized that weak winds and high baro-

metric pressure represented ideal climatic con-

ditions for migrant birds’ high-altitude flights.

On the other hand, de Carvalho Melo (2017)

reported that the number of adult marine birds

in their focal species was positively related to

mean wind velocity and negatively associated

with atmospheric pressure. Results in the cur-

rent study seem to be following those recorded

by the aforementioned authors, when it comes

to atmospheric pressure. According to the posi-

tive association with atmospheric pressure and

to the negative correlation to solar radiation,

at least some species prefer milder weather

conditions when they get to Piauí State. The

Brazilian equatorial coast is notoriously ener-

getic due to its high temperatures over the year,

intense (but highly variable) rainfall during the

wet season and strong winds in the dry season

(Soares et al., 2021). Accordingly, some spe-

cies may adjust their arrival timing to transition

times between seasons, and it forms the herein

observed richness peaks.

It is noteworthy that although insolation

and atmospheric pressure were selected by the

model-building algorithm, they only explained

a small portion of variations in migrant bird

species’ richness. This finding reflects the

complexity of the probable species-specific

processes driving the arrival of migrant bird

species in the Brazilian equatorial coast. There-

fore, caution is advisable at the time to take

into consideration the model presented in Fig.

3. It should be regarded as no more than pre-

liminary assessment on how weather clues can

be important to migrant bird species’ arrival in

Piauí State - this subject should be more thor-

oughly investigated in future studies. Howard

et al. (2018) commented that climatic changes

would most likely increase the effective migra-

tion distances crossed by many migrant spe-

cies, a fact that would force them to travel

longer distances, to increase the numbers of

stopovers and, consequently, the total duration

of their long-distance migrations – this factor

is not commonly considered in studies on cli-

mate change. Furthermore, lack of correlation

between migratory movements and climatic

factors, other than insolation and atmospheric

pressure, can be related to the presence of

some migrant individuals throughout the year.

Sick (1997) noticed that birds who are not able

to accumulate sufficient energy resources to

return to their breeding grounds may remain in

the wintering sites and only return during the

next migratory cycle.

Additional factors also need to be con-

sidered; for example, there was remarkable

coincidence of bird richness peaks and plant

fructification peaks nearby restinga vegeta-

tion sites (Ribeiro, 2011). This coincidence is

noteworthy because only one of the bird species

recorded in the present study was classified as

frugivore. Thus, increased fructification cannot

be the direct cause of higher avifauna diversity.

Therefore, other mechanisms should be investi-

gated in order to clarify the association between

food availability and bird migration in coastal

Piauí State, such as the case of plant-insect phe-

nological synchrony or spatiotemporal varia-

tions in benthic fauna composition.

Only two species were classified as nearly

endangered: Calidris canutus and C. pusilla.

Rosenberg et al. (2017) noticed that resources

available for conservation purposes are usu-

ally quite limited, and that the recognition of

vulnerable species (or of endangered ones)

is an essential component for effective con-

servation planning. Surveys can identify and

compare population trends recorded for focal

species during different seasons of the year;

these results can be used to identify proximal

factors accountable for population changes.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e47300, enero-diciembre 2023 (Publicado Mar. 02, 2023)

Information gathered during long-term bird

populations’ monitoring can be used to guide

and optimize management activities critical

to maintain or reestablish viable avian popula-

tions (Lynn et al., 2017). Up-to-date knowledge

about the origin and destination sites of migrant

birds, as well as environmental details of each

wintering site, will be essential to maintain

viable populations.

It was never so urgent taking conservation

actions, and actions to avoid climate changes

given the large volume of migrant bird spe-

cies suffering with the drastic decline in their

populations in the last few years, since these

changes can have impact on migrant shore-

birds who breed in the Artic, and change their

breeding locations and conditions (Wauchope

et al., 2017). Some evidence suggest that the

magnitude of migratory movements taken by

these species can influence their vulnerability

to environmental changes (Webster & Marra,

2005). Although it is not fully understood, the

decline in migrant species is a constant con-

cern (Hardesty-Moore et al., 2017). However,

a study on migratory movements has shown

that greater population variability within these

movements leads to higher resilience towards

environmental changes (Gilroy et al., 2016).

Data in the present study reinforced the obser-

vation that migrant birds occupy specific envi-

ronments during their permanence along the

coast of Piauí State and that these birds are seen

at higher concentrations during the most humid

months of the year.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict 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 acknowledge-

ments section. A signed document has been

filed in the journal archives.

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