Where did they go? Understanding the effects of urbanization on bird diversity in a Brazilian coastal city

doi:10.21203/rs.3.rs-4003927/v1

Urbanization is recognized as an important cause of biodiversity loss. Urban areas present reduced number of bird species if compared to non-urban more pristine areas nearby. The goal of this research is to help improving the diversity of birds in urban areas by investigating why an urban area in the coast of Brazil sustains a small fraction of the species that could occur in the region. We conducted observations during two years in Serra, Brazil, resulting in the identification of 27 bird species visiting a residential garden. Studies in the region have reported 275 species. We used GIS maps and aerial photos to analyse the landscape, then discussed that numeric discrepancy and the possible reasons for the reduced diversity, contrasting it to the resources available in that landscape. Recent urbanization is likely to be a major cause of the low diversity, but the study area has been subject of change from the original ombrophilous dense forest to agriculture and pasture before the consolidation of the current urban land uses. Albeit the landscape is highly fragmented, diverse landcover types have recovered in recent decades, creating a mosaic of small isolated patches of forest, mangrove and restinga, the three major ecosystems in the region. We expect that our findings create a foundation for further exploration of measures and policies for implementing greenspace within cities that help reverting the current status and improving the diversity of birds in tropical cities.

avifauna

birds

Atlantic Forest

urban landscape

greenspace

biodiversity

Birds are commonly perceivable in our daily lives. After years of living in apartments, moving to a house with a garden allowed us to observe and record many visiting creatures otherwise unnoticed in other urban living spaces. The surprising high number of bird species observed in a small garden seemed to be an opportunity to investigate how an urbanized area sustained such a variety of species. As the study developed, however, it became clear that the number of species was actually a small fraction of the region’s original avian diversity and very different from non-urbanized areas in similar geographical and ecological contexts. As birds are useful indicators of habitat quality and the degree of disturbance in the tropics (Morante-Filho et al., 2021), the low diversity led us to assume that urbanization had a strong influence on the reduced number of species.

Urbanization impacts on bird populations and species diversity have been widely documented and discussed (Marzluff & Rodewald, 2008; Aronson et al., 2014; Snep et al., 2016; Petersen et al., 2022; Afrifa et al., 2023). Landcover changes directly influence climatic conditions, food resources, introduce predation by pets or exotic species; urban development potentially affects animal behaviour, reproduction, survival, immigration and emigration, increasing or decreasing the viability of animal populations (Marzluff & Rodewald, 2008). Urban landcover negatively correlates to the density of bird species (Aronson et al., 2014; Afrifa et al., 2023). As the city expands, species richness decline, specially affected by the decline of insectivores (likely because of air pollution) and granivores, counterpartyed by the increase of scavengers and predators caused by human waste (Chamberlain et al., 2018). The urban environment has also a reduced number of plant species, which provide certain services such as shade and aesthetics, but do not provide a variety of ecological benefits (Clergeau, 2019).

Nevertheless, there has been a constant increase of recognition of urban biodiversity research since the 1990s (Rega-Brodsky et al., 2022). Evidence shows that biodiversity can coexist with people in cities if appropriate urban planning, conservation and education actions focus on their natural resources (Aronson et al., 2014). Urban greenspaces may provide heterogeneous habitats and, thus, likely sustain high diversity of species (Callaghan et al., 2019). Cities might even supporting an unexpected diversity of birds (Pautasso et al., 2011). There are indications that urban forest patches can sustain simplified sets of resident birds (Curtis et al., 2022), especially when these greenspaces are inserted in an inhospitable urban matrix that will hinder the dispersal of bird species (MacArthur & Wilson, 1967).

In Brazil, most of the urbanization occurs along the eastern coastal states, largely corresponding to the Brazilian Atlantic Forest biome domain (Rezende et al., 2018). This biome is one of the most diverse and threatened by human disturbances (Joly et al., 2014). Because of the number of species, especially endemic ones, and the degree of urbanization along the Brazilian coast, there is a need of studies on urban birds and to improve the conditions of urban areas to sustain birds in tropical zones. Urban ornithology studies have grown in the southern hemisphere, but most still come from temperate climates, particularly Europe, USA and Canada (Marzluff, 2017), with significant gaps in biodiversity research within the Global South (Rega-Brodsky et al., 2022) and urgent need to analyse the effects of urbanization on animal and plant communities in tropical cities (de Matos Fragata et al., 2022). The conservation, restoration, and ecological investigation of the Atlantic Forest represent important actions for conservation in this biome.

The purpose of this research is to investigate effects of urbanization on bird diversity in the coastal region of Brazil. We do so by contrasting the observed diversity in an urban site in the city of Serra, Brazil, to that of large parks and non-urbanized areas, and analyse the landscape and the land use and land cover changes that lead to the present conditions. We expect that this knowledge contributes to inform policy making and future planning and design decisions that prevent loss and promote increase of urban avian diversity, therefore contributing to biodiversity conservation in the tropics.

Over a 2-year period, we observed, photographed and identified birds that visited our own garden. Through a review of the literature, we identified six studies that reported observations in the State of Espirito Santo, in areas at relatively short distances from our study area. We realised that many more species occur in those nearby areas, as recorded in those studies. We contrasted their findings with the list of birds we had recorded. We then analysed the surrounding landscape and the spatial qualities that possibly allowed certain species to be present in that area and/or prevented the presence of other species.

2.1 Site and study area

Observations took place in the city of Serra, state of Espirito Santo, Brazil (-20.16342 S, -40.18472 W) (Fig. 1), between January 2018 and December 2019. With an estimated population of 536,765 (2021), 99.31% of its inhabitants lives in urban areas (IBGE, 2010). Its territory covers 547 km² (54,741 hectares).

The site is a small residential garden (120 m²) within an oceanfront urban lot (300 m²), adjacent to a restinga formation in early successional stage (Fig. 2). Restingas are pioneer formations in areas of marine influence, on sandy soils, composed of herbaceous plants, shrubs and forests (Garbin et al., 2017). Two feeders were provided to attract fauna, one containing fruits (banana and papaya) at 1.5 m above ground, another with grains (cracked corn, millet and birdseed) at a height of 0.75 m, and one small nesting box. Native and non-native plants in the garden provided additional fruits and nectar: Eugenia uniflora (pitanga), Plinia cauliflora (jaboticaba), Morus nigra (blackberry), Heliconia psittacorum (parrot’s beak), Schinus terebinthifolius (Brazilian peppertree), Carica papaya (papaya), Capsicum frutescens (malagueta pepper), and Pachystachys lutea (lollipop plant). Other plants were used for perching only: Triplaris americana (ant tree), Handroanthus albus (golden trumpet tree), and Citrus × limonia (rangpur). The lawn was composed mostly of Zoysia japonica (Japanese lawn grass) with small patches of Paspalum notatum (Bahia grass). Two trees hanging from the neighbour’s garden were visited by woodpeckers: Annona muricata (soursop) and Cocos nucifera (coconut tree). An early successional restinga vegetation area is adjacent to the site, dominated by the trailing vine Ipomoea pes-caprae (morning glory), with several dispersed small Eugenia uniflora and a few large exotic Terminalia catappa (Indian almond).

2.2 Observations

Observations occurred between January 2018 and December 2019. We recorded only birds that visited the garden or that could be seen from the garden, perching or foraging in the surrounding vegetation or structures such as buildings, walls or wires. Birds were initially photographed and identified in the literature (Frisch & Frisch, 2005). We then confirmed and/or reviewed each entry and obtained life history data from other sources (Dario, 2009, 2010; Billerman et al., 2020). The scientific nomenclature and taxonomic order used the new systematic list of the Comitê Brasileiro de Registros Ornitológicos (Pacheco et al., 2021). The classification of the species in agreement with the respective ecological groups was based on that proposed for bird communities by Willis (1979). Therefore, the birds were grouped together according to their alimentary diet and to their forest layers, classifying those species that present feeding and similar biotope in distinct ecological groups (trophic guilds).

3.1. Observed birds

We recorded 27 bird species in the garden and in its immediate surroundings, all sighted and photographed from the garden (Table 1, examples in Fig. 3). The birds belong to 15 families, the most common being Thraupidae (seven species) and Tyrannidae (four species). Two thirds of the observed species were Passeriformes (Table 2). All are adapted to open areas and/or forest edges (Table 3). Omnivores are the most abundant, with 12 species (44.5%); eight are insectivores (29.6%), four granivores (14.8%), one carnivore (3.7%), one frugivore (3.7%) and one nectivore (3.7%) (Table 4).

Table 1. List of species observed:

Trophic Guilds (TG): carnivores (C), detritivores (D), frugivores (F), granivores (G), insectivores (I), nectarivores (N), omnivores (O);

Habitat according to: (A) Bauer (1999); (B) Simon et al. (2007); (C) Dario (2009); (D) Dario (2010); (E) Zorzal (2016); (F) dos Santos et al. (2019);

Habitats: Forest including edge (F), Open areas (O), Forest edge (E), Pasture (P), habitat not reported (✓), species not reported (-);

Month: numbers refer to months of recording (photo);

Behaviour (Beh): Foraging (F), perched (P), hunting (H);

Location of observation (Loc): bird feeder (BF), building (BD), nest box (NB), Annona muricata Am), Capsicum frutescens (Cf), Citrus × limonia (Cl), Cocos nucifera (Cn), Carica papaya (Cp), Eugenia uniflora (Eu), grass (G), Handroanthus albus (Ha), Heliconia psittacorum (Hp), Morus nigra (Mn), Plinia cauliflora (Pc), Pachystachys lutea (Pl), Schinus terebinthifolius (Sc), Triplaris americana (Ta), Terminalia catappa (Tc).

Species	Common Name	Family	TG	Size	Habitat						This study
Species	Common Name	Family	TG	(cm)	A	B	C	D	E	F	Month	Loc	Beh
Columbina talpacoti	Ruddy ground dove	Columbidae	G	17	O	✓	E	P	O	✓	5, 9	BF, Mn, Lc	F
Guira guira	Guira cuckoo	Cuculidae	I	38	O	✓	E	E	E	-	6,7	Lc, Am, W, Cn, G	H
Crotophaga ani	Smooth-billed Ani	Cuculidae	I	35	O	✓	E	E	E	-	9	Am	F
Eupetomena macroura	Swallow-tailed hummingbird	Trochilidae	N	18	FO	✓	E	E	E	✓	9,11	Hp, Pl	F
Rupornis magnirostris	Roadside hawk	Accipitridae	C	31–41	FO	✓	E	E	E	-	10	Tc	P
Picumnus cirratus	White-barred piculet	Picidae	I	10	F	✓	E	E	E	✓	1	Am	F/H
Melanerpes candidus	White woodpecker	Picidae	O	28.5	O	-	-	E	-	-	12	Cn	H
Colaptes campestris	Campo flicker	Picidae	I	32	O	✓	E	P	E	-	5	Cn	F
Primolius maracana	Blue-winged Macaw	Psittacidae	F	24.5	F	✓	-	-	-	-	5, 9	Tc	P
Furnarius rufus	Rufous hornero	Furnariidae	I	19	O	-	E	E	O	✓	9, 10	G	H
Fluvicola nengeta	Masked water tyrant	Tyrannidae	I	21.5	A	-	E	E	O	✓	5	G	H
Pitangus sulphuratus	Great kiskadee	Tyrannidae	O	22.5	FO	✓	E	E	O	✓	8,9	BF, Cl, Am	F/P
Serpophaga subcristata	White-crested tyrannulet	Tyrannidae	I	11	FO	-	-	E	-	-	10	BD	P
Tyrannus melancholicus	White-throated Kingbird	Tyrannidae	O	20	FO	✓	E	E	O	✓	4, 5, 10	G, BD, W	F
Euphonia chlorotica	Purple-throated euphonia	Fringillidae	O	10	FO	✓	E	E	E	✓	4, 8, 9, 10	BF, Tb	F
Progne chalybea	Gray-breasted Martin	Hirundinidae	I	16–22	O	✓	-	P	O	✓	9	Wire	P
Icterus jamacaii	Campo troupial	Icteridae	O	23–26	-	-	-	-	-	-	5, 8, 9	BF, Lc, Am	H
Mimus gilvus	Tropical mockingbird	Mimidae	O	25	F	-	E	E	O	✓	6, 9	BF, BD, Cf, Mn, Am	F
Passer domesticus	House sparrow	Passeridae	O	15	-	-	-	E	O	✓	2, 4, 9	BF, Am, Pc, G	F
Coereba flaveola	Bananaquit	Thraupidae	O	11	FO	✓	E	E	O	✓	2, 5, 7, 8, 9	BF, NB, Am, G	F
Paroaria dominicana	Red-cowled cardinal	Thraupidae	G	17.5	-	-	-	-	-	✓	6, 7, 8	BF, G	F
Sicalis flaveola	Saffron finch	Thraupidae	G	14	O	✓	E	P	O	-	2, 5, 7, 8, 9, 10, 11	BF, G	F
Stilpnia cayana	Burnished-buff tanager	Thraupidae	O	14	FO	-	E	E	-	-	5, 6, 8, 9, 10	BF, Pc, W	F
Thraupis palmarum	Palm tanager	Thraupidae	O	18	FO	✓	E	E	O	-	5, 9, 10	Tb, BF	P/F
Thraupis sayaca	Sayaca Tanager	Thraupidae	O	17	FO	✓	E	E	O	✓	8, 9, 10	Tb, BF	P/F
Volatinia jacarina	Blue-black Grassquit	Thraupidae	G	11.5	O	✓	E	P	O	-	9, 11	BF, G	F
Turdus leucomelas	Pale-breasted thrush	Turdidae	O	23	F	✓	-	E	O	✓	5, 7, 8, 9, 10	BF, G	F

3.2. Other studies

To better understand the bird diversity of the region, we consulted six studies that describe the avifauna composition in areas geographically similar to the study area (Fig. 4). Tables 2, 3 and 4 present a summary of our findings.

Table 2

Summary of findings: Number of observed species in all studies
	This study	Bauer 1999	Simon 2007	Dario 2009	Dario 2010	Zorzal 2016	Santos 2019	All studies
Non-Passeriformes	9	102	55	34	79	57	10	136
Passeriformes	18	93	65	53	89	69	26	142
Total	27	195	120	87	168	126	36	278

Table 3

Summary of findings: Number of observed species in all studies, according to preferred habitats
Preferred habitats	All studies	%	This study	%
Aquatic	39	14.0	-	-
Aquatic or Forest edge	10	3.6	-	-
Aquatic, edge or Open areas	2	0.7	1	3.7
Aquatic and Open areas	13	4.7	-	-
Edge	67	24.1	2	7.4
Edge or Forest	3	1.1	1	3.7
Edge or Open areas	52	18.7	20	74.1
Forest	56	20.15	1	3.7
Open area or pasture	36	12.95	2	7.4

Table 4

Summary of findings: Number of observed species in all studies according to trophic guilds
Trophic guild	All studies	%	This study	%
Carnivore	55	19.8	1	3.7
Detritivores	3	1.1	-	-
Frugivore	19	6.8	1	3.7
Granivore	23	8.3	4	14.8
Insectivore	83	29.8	8	29.6
Insectivore/Frugivore	6	2.1	-	-
Insectivore/Granivore	1	0.4	-	-
Nectivore	15	5.4	1	3.7
Omnivore	73	26.3	12	44.5

Bauer (1999) inventoried, in her field observations, an extensive list of birds (462 species) in a southern portion of the state of Espirito Santo, and 51 species additional species from the literature. She surveyed 195 species in the coastal portion of her study area, which includes a well preserved restinga within a state park (20^o36’S − 40^o25’W) and an arboreous restinga in the south of the state (21^o16’S − 40^o57’W). Simon et al. (2007) recorded 120 species from their field observations in the Fonte Grande State Park (20^o18’S − 40^o20’W), dominated by secondary ombrophilous dense forest in advanced degree of regeneration, approximately 22 km southwest of our study area.

Dario (2009) recorded 87 species in fragments of restinga in the city of Anchieta, located approximately 80 km southwest of the study area. Another, more comprehensive report by Dario (2010), reported 168 species in a 20,000 ha area originally covered by dense ombrophilous forest, now fragmented by pastures and agriculture, also in Anchieta (between 20^o40’ and 20^o48’S and 40^o34’ and 40^o42’W). Zorzal (2016) observed seven urban open space areas ranging from 2.4 to 216 hectares in two cities adjacent to Serra. In his study, 126 species were present. He reported 24 species in the smallest greenspace (an urban park in the city centre of Vitoria, 20^o19’S − 40^o 20’W), while the largest area had 76 species (a state park in Vitoria, same area where Simon et al., 2007 identified 120 species). The second largest site, a 168 ha city park in Vila Velha (20 ^o19’S − 40 ^o19’W), presented 86 species. Lastly, a study by dos Santos et al. (2019) reported 36 species in a 159.25 ha university campus, approximately 20 km southwest of our study site (20°19’09”S − 40°20’50”).

From the group of 195 species recorded by Bauer (1999), 56 were sighted in forests, 30 in both forests and open areas, 66 in open areas, and 38 in aquatic habitats. From the 68 additional species surveyed by Dario (2009) in a restinga formation, he describes 10 as sighted at the understory, this group being more dependent on forests than the following ones; 41 as edge species, three as aquatic species and 14 were seen in tree canopy. Dario (2010) reports 21 understory species, 57 forest edge, 16 canopy, 25 in pastures and 24 aquatic species. Zorzal (2016) includes 101 not sighted in our observations. Among them, he classifies 10 as forest dependent species, 47 semi-dependent, and 43 independent from forests. Simon et al. (2007) do not specify the habitats where each bird was sighted or their habitat association.

Contrasting to our own observations, Icterus jamacaii was not documented in any of the cited studies and Paroaria dominicana in only one. Melanerpes candidus, Primolius maracana, Stilpnia cayana, and Serpophaga subcristata are not mentioned in three of the previous studies. Bauer (1999) records Primolius maracana as observed in forest areas, including forest edge, in conditions different from the urban setting of this study. She also recorded Mimus gilvus, Picumnus cirratus, and Turdus leucomelas being sighted exclusively in forests. Fluvicola nengeta is reported to be seen in an aquatic environment (Bauer, 1999). The three species observed by Bauer in forest environments (Mimus gilvus, Picumnus cirratus, and Turdus leucomelas) were, distinctively, recorded as forest edge species by Dario (2010).

3.3. The context

The state of Espirito Santo holds, in a relatively small territory (46,089 km²), a large diversity of ecosystems within the Atlantic Forest biome, with multiple types of vegetation such as ombrophilous dense forest, ombrophilous open forest, seasonal semideciduous forest, restinga and mangrove (Garbin et al., 2017). Because it has lost its original landcover to agriculture, silviculture and urbanization, forest habitats are scarce, and likely their associated species.

We looked at the site’s context to analyse an area that contains most of the observed species’ likely daily range (Fig. 5). We used datasets to represent and describe major land use and landcover (LULC) types (IEMA, 2012). A series of aerial photographs depicts the landscape’s evolution since 1970.

The landscape within the study area reveals a fragmented and patchy structure (Fig. 5). Out of a total of 449.7 hectares of the area studied (Table 5), 183.5 consist of built-up area (40.8%) containing medium density, single and multifamily housing, including vacation homes, commerce and service, and industry, with several vacant lots. The large red portion of the map (Fig. 5), however, hides the diversity of numerous small patches of green in residential gardens, vacant lots, and greenspaces as Fig. 2 exemplifies. The other large portion on the map is classified as others (101.2 ha or 22.5%), which includes large private open spaces with no or incipient vegetation cover. Other areas of higher ecological value represent 23.9% of the area and include swamps (11.4 ha), scrubland (27.9 ha), mangroves (3.1 ha), native forest in various stages of regeneration (59.7 ha) and restinga (5.4 ha), in addition to 9.3 ha of water bodies and 6.6 ha of beach. Pastures add up to 21.1 ha, areas with exposed soils 12.8 ha and silviculture 7.7 ha.

Table 5

Landscape composition: area and percentage of LULC classes
LULC	Municipality		Study area
LULC	Hectares	%	Hectares	%
Agriculture	1491	2.7	0	0
Beach	NA	-	6.6	1.47
Built	6402	11.7	183.5	40.80
Exposed soil	256	0.5	12.8	2.85
Mangrove	460	0.8	3.1	0.69
Mining	88	0.2	0	0
Native forest	8247	15.1	59.7	13.28
Native forest in regeneration	5786	10.6	59.7	13.28
Other	4224	7.7	101.2	22.50
Pasture	15823	28.9	21.1	4.69
Restinga	6	0.01	5.4	1.20
Rock outcrop	751	1.4	0	0
Scrubland	1426	2.6	27.9	6.20
Silviculture	4187	7.6	7.7	1.71
Swamp	4397	8.0	11.4	2.54
Water	1197	2.2	9.3	2.07
Total area	54741		449.7

Three streams run in this landscape: the Jacaraípe river to the north is the largest; to the south, the Irema creek flows from the Jacuném lagoon (west of this area), which is legally protected since 1998 and surrounded by remnants of Atlantic forest at multiple successional stages; at the centre, a small, unnamed creek is culverted in its lower, eastern stretch. The Atlantic Ocean makes the eastern limit.

Figure 6 depicts the evolution of the area over approximately 50 years. It is possible to observe that, in the beginning of this period (ca. 1970), the landscape was already deprived of its original forest cover in its upper areas (western portion on the photos), with large expanses of pasture; urbanization, consisted mainly of vacation homes, had started to expand near the water. In the following decades, pasture gave place to new subdivisions and multifamily developments (1986, 1994, 1998). Since then, development has consolidated, with most of the subdivision areas occupied.

Two major remaining greenspaces present some improvement of their vegetation cover, with pasture evolving into forests in some areas, and a strip of restinga expanding along the beach. A stand of Eucalyptus was planted adjacent to the largest forest patch. The existing forest may sustain some forest-dependent species, but it is likely that its size is prone to host only edge species.

The existing adjacent restinga vegetation is at an early stage of succession. Legally protected as an environmental protection zone by municipal law (Serra, 2016), the restinga strip has been slowly recovering. However, it is highly managed and kept as a low scrubland by the city’s administration. Proximity to the beach, which is a major recreation destination, exposes the restinga to additional disturbance, including incidental fires that affect the vegetation (see dark area on the northern portion of Fig. 2) and trampling by people accessing the beach. Community composition is limited to a few plant species and not as complex as in other areas (Dario & De Vincenzo, 2011), hence lacking the heterogeneity and strata that create conditions for a more diverse set of bird species that depend on tree canopy or understory. Several areas are also covered by clumps of Terminalia catappa, which project large shades and inhibits growth of some plants.

Mangroves along the Jacaraipe river have somehow expanded in the last few decades, but are still reduced and fragmented, impacting populations of aquatic birds associated with that ecosystem. Urbanization has densified along its margins.

4.1. Species

Accounts on the amount of bird species in the state of Espirito Santo report over 700 species (Lepage, 2021). The Atlantic Forest hosts a large number of endemic species, many considered to be under some risk of extinction, specially forest-dwelling birds because of habitat fragmentation, in opposition to the increase of generalist species (Oliveira et al., 2018). The studies we approached, including our own, reported a sum of 278 species in coastal areas, most with lesser degrees of urbanization and urban land cover than our study area.

Despite the recognition of their impact on bird diversity, urban environments are valuable for birds and may accommodate a rich diversity of bird species (Snep et al., 2016); many species have adapted to urbanization and may benefit from protection provided by built structures or the absence of certain nest predators (Møller, 2010). Aronson et al. (2014) reveal that nearly 20% of all bird species already occur in cities. However, fragmentation and less availability of habitats, native vegetation and vegetation structure threaten conservation of birds in cities (Snep et al., 2016), which causes them to contain substantially lower densities of species compared with non-urban levels (Aronson et al., 2014). In our case, our observations recorded less than 10% of the total number of species observed in other studies.

Species, habitats, foraging and behaviour

Because we observed all species in an urban area, it is assumed that they are well adapted to open areas. Bauer (1999) associates four of the species we observed (Picumnus cirratus, Primolius maracana, Mimus gilvus, and Turdus leucomelas) to forest habitats, but that author’s habitat classification includes forest edges. The other authors associated those species to forest edges or open areas, except for Primolius maracana, which is not mentioned in the other studies.

Most of the observed bird species have broad distribution in Brazil, some ranging to neighbouring countries and to Central and North America, like Progne chalybea, a Neotropical migrant that reproduces in southern Brazil (Chesser, 1994). Two species, Paroaria dominicana and Icterus jamacaii, appear to be outside of their documented ranges, what may indicate that they could be expanding their ranges, as reported by Jaramillo (2020), for whom Paroaria dominicana is expanding from Brazil’s north-eastern region to south and west due to escapes. Fraga (2020) states that Icterus jamacaii is spreading into the south-eastern states of Espirito Santo and Rio de Janeiro.

Almost all birds visited the garden in search for food. Bird feeders had fruit and grain provided daily, while fruit from most trees were subject to seasonality. Exception was Carica papaya, which more frequently bore fruit: birds often fed on leftovers left by opossums on the tree or on the ground.

The garden provided foraging resources, but resources were limited for nesting. Only one species nested in the nest box (Coereba flaveola); another nest was sighted high on the adjacent Terminalia catappa (Furnarius rufus).

Among the 27 observed birds, only one is currently considered near threatened (Collar et al., 2020), the Blue-winged Macaw (Primolius maracana). If measures are not taken, this species could go into extinction (Convention on International Trade in Endangered Species of Wild Fauna and Flora [CITES], 2021). It was observed perching and foraging on the Terminalia catappa. Another, Mimus gilvus, is endemic to the coastal portion of the Atlantic Forest and considered endangered in the state of Espirito Santo (IEMA, 2017). The House Sparrow (Passer domesticus) is the only exotic bird, introduced in the twentieth century into cities in eastern Brazil (Sick, 1997).

Commonalities with other studies and missing species in our observations

The six studies that describe the avifauna composition in areas geographically similar to the study area helped comprehending the bird diversity of the region, specially that many are not present in our site. Almost all reported significantly larger numbers of species than those from our observations. From Bauer’s 195 species (Bauer, 1999), 24 also appear in our study area, while three species from our observations do not show in her list: Icterus jamacaii, Paroaria dominicana and Passer domesticus. The author recorded 171 species more than our observations. We documented 18 species in common with Simon et al. (2007), all typical of open areas. Nine species we observed did not appear in their study: Furnarius rufus, Icterus jamacaii, Mimus gilvus, Passer domesticus, Melanerpes candidus, Paroaria dominicana, Stilpnia cayana, Fluvicola nengeta and Serpophaga subcristata. Their list includes 102 species we did not record. Eight of the species we recorded are not present in Dario (2009): Melanerpes candidus, Primolius maracana, Progne chalybea, Icterus jamacaii, Passer domesticus, Paroaria dominicana, Turdus leucomelas, and Serpophaga subcristata. Several of our species (24) were also recorded by Dario (2010). Three of our species are not present in his list: Icterus jamacaii, Primolius maracana, and Paroaria dominicana. Six of the species from our study are not present in Zorzal (2016): Icterus jamacaii, Melanerpes candidus, Primolius maracana, Paroaria dominicana, Stilpnia cayana, and Serpophaga subcristata. Our study shares 12 species with dos Santos et al. (2019). Fifteen of our species were not observed by those authors, while they have 24 that we haven’t recorded.

In the general account (278 species), 136 (48.9%) were non-Passeriformes, while 142 (51.1%) were Passeriformes. In our study, the distribution was less balanced: one third of the species were non-Passeriformes.

Trophic guilds

Omnivores and granivores are the guilds most adaptable to urbanization (Chace & Walsh, 2006). In fact, 16 of our species (59.2%) are either of those categories. The percentage of omnivores was much higher than the other six studies (44.4 vs. 26.3%).

Granivores and insectivores were expected to be the most impacted trophic guilds (Chamberlain et al., 2018). However, a larger proportion of granivores was expected because of the provision of forage. The four species – Columbina talpacoti, Sicalis flaveola, Volatinia jacarina, and Paroaria dominicana – made up 14.8% of our species, while among the 278 they represented only 8.3%. In addition, we encountered eight insectivore species in our area (29.6%), a proportion comparable to that of the sum of all studies (29.8%). Insectivorous birds usually have greater spatial stability and are more site-attached than frugivorous ones (Manhães & Dias, 2011), but this does not mean that fluctuations do not occur, since insectivorous birds may have spatial distribution related to the availability of arthropods (Martin & Karr, 1986).

A smaller percentage of carnivores was expected, as there were limited or no foraging resources for this guild. One species, Rupornis magnirostris, was sighted roosting on the Terminalia catappa. It is one of the most common hawks in Brazilian cities, adapting successively to anthropic environments, due to the large supply of food. Like all birds of prey, it plays an indispensable role in the balance of the fauna, as a regulator of selection (Sick, 1997). Outside our study area, multiple Caracara plancus specimens, not included in our list, were frequently spotted in the vicinity. The record of a limited number of birds of prey indicates that the environment is out of balance, as these species are at the top of the food chain (Willis, 1979).

Although multiple omnivores fed on fruit (Coereba flaveola, Euphonia chlorotica, Icterus jamacaii, Mimus gilvus, Stilpnia cayana, Thraupis palmarum, Thraupis sayaca, Turdus leucomelas, and Pitangus sulphuratus), no strictly frugivorous species visited the garden, despite two native plants (Capsicum frutescens and Schinus terebinthifolius) and one exotic (Carica papaya) bore fruit most of the year, three other trees seasonally, and fruit been provided in the bird feeder. The other studies reported 18 species. The only frugivorous bird in our list, Primolius maracana, was spotted visiting the adjacent Terminalia catappa.

The absence of a greater number of frugivorous species was already expected, as well as the absence of understory species, large omnivorous species and omnivorous species that feed on insects and large fruits. These species are considered the most sensitive to anthropogenic changes and demanding in the quality of the environment (Willis, 1979). Many of these species have probably already disappeared from the urban region in question. The composition and diversity of the birds should vary mostly in response to fluctuations in the supply of food. Isolation of the area from preserved natural environments, the human presence, and environmental noise must also have much influenced bird diversity.

Nectar was available during most of the year, but only one nectivore was present (Eupetomena macroura), feeding on Heliconia psittacorum and Pachystachys lutea. Coereba flaveola has been reported to feed from nectar (Previatto et al., 2013), but this habit was not noticed.

4.2. Habitats

The study area is situated within the Atlantic Forest domain, where the high level of endemism and species richness make it a priority for biodiversity conservation (Morante-Filho et al., 2021). Because of the degree of urbanization, the observed low diversity was assumed to be directly related to urbanization, but a long history of land use changes, including deforestation for agriculture and livestock, is likely to have contributed to an earlier loss of diversity. In Brazil, urban development, agriculture, logging, and mining have been major causes of suppression of the Atlantic Forest, which is now a patchwork of remaining ecosystem fragments distributed among agricultural and urban matrices (Ribeiro et al., 2009).

The reduced bird diversity observed in the urban landscape we approached results from the land use and landcover transformations it suffered during its recent history. The current composition of such landscape supports a certain number of species whilst preventing the occurrence of a larger number. Reduced habitats altered the original composition of species, from a more diverse assemblage that included forest dependent species, to one where generalists and edge habitat species prevail. The existing landscape contains certain types of greenspace that provide habitats. Small forest patches, fragmented and isolated patches of mangrove, and an early successional restinga appear throughout the area, interspersed by small gardens, vacant lots, among others.

From the 278 species reported in all studies, 56 are strictly associated with forests, none in our observations. The largest patch of native forest has been under regeneration in the last decades, but has recently been segmented by a major arterial. The study area lacks large, vertically complex greenspaces connected by green corridors to sustain species with various vagilities and metacommunities (Chen & Cheng, 2022). Machar et al. (2022) indicate that large urban parks containing native vegetation structures have high importance for the maintenance of bird diversity. Murphy et al. (2023) warn that, in the context of their research, parks below 10 ha sustained few forest-dependent species. Humphrey et al. (2023) highlight the importance of native vegetation surrounding a landscape as source habitat for urban bird populations.

The surrounding landscape also plays an important role for aquatic species (Chen et al., 2022). Aquatic species are also less likely to inhabit urban areas, as human-driven changes drive aquatic bird population to decline (Chen et al., 2022). The study area’s context, however, contains multiple water bodies. The studies we consulted reported 64 aquatic species that could somehow be contemplated in that location. Riparian zones and mangroves along the water bodies present are highly depauperated, and could play an important role to improve connectivity in the urban landscape (Ribeiro et al., 2022). Along the Jacaraípe river, a few small patches of mangrove remain. The lowest section of the Irema creek has been completely stripped of its riparian vegetation. In the central portion of the area, an unnamed creek is partially culverted for several blocks, close to the beach.

Another threat to aquatic birds is caused by the attractiveness of oceanfront areas to real estate development. The impacts of urbanization on the three streams and vegetation cover, especially the restinga, are likely to have caused the disappearance of species directly associated with mangroves and riparian vegetation. The restinga adjacent to the site has also experienced some regeneration. Its northern portion, between the site and the Jacaraípe river, however, is subject to trampling, as multiple kiosks attract people to the locale. Increased building densities have a negative effect on richness and abundance of native and insectivorous species (Amaya-Espinel et al., 2019). However, maintaining lower building densities may incur in demands for more urbanized areas and increased road network, contradictorily causing further reduction and fragmentation of habitats.

Many of the species we observed are classified by the aforementioned authors as edge species (e.g., Crotophaga ani, Guira guira, Pitangus sulphuratus, Coereba flaveola, Tyrannus melancholicus, Turdus leucomelas, Mimus gilvus, and Thraupis sayaca). Most of them, because they prefer to visit the forest edge, are less affected by forest fragmentation, especially when considering that the anthropic transformations caused in natural environments produce environments favourable to the development of pioneer vegetation, which is characterized by great production of fruits, increasing the availability of food for many of these birds that have in them the base of the feeding. Even though, excluding forest dependent, aquatic and the 27 from our inventory, 131 species observed in the other studies that are adapted to open areas or the transitions between forest and open areas were not recorded by our observations and could potentially inhabit urban greenspaces in the region if appropriate resources were provided.

Residential lawns are widely recognized that have low ecological value (Smith et al., 2015). They still represent a large portion of Brazilian gardens, both private and public. However, four of our 27 species were observed foraging in the lawn (Furnarius rufus, Turdus leucomelas, Fluvicola nengeta, and Tyrannus melancholicus), often preying on insects during or shortly after mowing.

Lastly, it is important to recognize the role of urban noise, particularly road noise, as this component of the urban landscape has a strong negative influence on the richness of bird species (Cicort-Lucaciu et al., 2022).

As we consider the site and context of our site, we realize that the diversity of birds we observed can be considered high if contrasted to some of the sites surveyed in the other studies. For example, the university campus surveyed by dos Santos et al. (2019) is highly maintained, but keeps a large fragment of mangrove (nearly half of its area, approximately 800 ha) and small fragments of forest, where 36 species were identified, while Zorzal (2016) reported 24 species in a 2.4 ha urban park. The 27 species we observed were attracted by the resources made available (bird feeders), but also because of the diversity of plants that provided fruits and nectar along the year. It also indicates that looking only at the red portion of the map (Fig. 5) does not reveal the peppered mosaic of small gardens and private greenspaces that contribute to the overall diversity of birds. Still, to support species with more particular habitat and foraging demands, larger habitat areas are necessary.

In this paper, we reported our findings from two-years of observations, contrasted to reports from the literature, and examined the landscape to understand the existing local avian diversity, which species were missing and the possible reasons why they were not there. We investigated the current landscape composition in order to identify the causes of the diversity loss in that area as urbanization affected bird diversity.

The loss of biodiversity caused by urbanization is a serious problem. However, in cities, urban greenspaces can play an important ecological role, serving as resting and feeding areas for many species of birds. Wildlife habitat management in urban greenspaces could be a way to protect biodiversity in urban environments. Our study highlights the importance of the urban greenspaces in the conservation of bird diversity. Factors that shape the characteristics of urban avifauna are the availability of food, nesting sites, presence of watercourses and proximity to natural areas. Therefore, it is important to investigate the key factors affecting bird diversity in anthropic areas, to propose actions to improve these environments, so as to maintain and enhance bird diversity.

Our results reveal that cities can support a certain degree of avian diversity, but that diversity is far from that of non-urban sites. Therefore, measures are required to improve the urban landscape. The incorporation of greenspaces within urban development are key for the conservation of avian diversity (Muvengwi et al., 2022). By identifying the pitfalls of that landscape in supporting a more diverse community of birds, we provide a foundation for proposing policies, designs and interventions to improve urban greenspaces in existing urban areas and/or future development. Still, we need studies that address those pitfalls and propose policies and landscape interventions to overcome the loss of avian diversity.

Funding Declaration

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author Contribution

HMP conceptualized the study and wrote the manuscript draft; BMP was responsible for observations, photographs and identification of species, and preparation of maps; FRD contributed to the manuscript text and review of taxonomic classification; JCA edited the manuscript; all authors. All authors commented on previous versions and reviewed the manuscript, as well as read and approved the final manuscript.

Funding Declaration

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Data Availability declaration

Data will be made available on request.

Competing Interest declaration

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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No competing interests reported.

SupMatListofSpeciesallstudies.pdf

Where did they go? Understanding the effects of urbanization on bird diversity in a Brazilian coastal city

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Abstract

Figures

1. INTRODUCTION

2. METHODS

3. RESULTS

4. DISCUSSION

5. CONCLUSIONS

Declarations

Author Contribution

Funding Declaration

Data Availability declaration

Competing Interest declaration

References

Additional Declarations

Supplementary Files

Status:

Version 1