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A floodplain with artificially reversed flood pulse is important for migratory and rare bird species

A floodplain with artificially reversed flood pulse is important for migratory and rare bird species Revista Brasileira de Ornitologia 25(3): 155–168. ARTICLE September 2017 A floodplain with artificially reversed flood pulse is important for migratory and rare bird species 1 1,2 Vivian Robinson & Marco A. Pizo Departamento de Zoologia, Universidade Estadual Paulista, Av. 24A, 1515, 13506-900, Rio Claro, SP, Brazil. Corresponding author: pizo@rc.unesp.br Received on 09 March 2017. Accepted on 04 July 2017. ABSTRACT: Wetlands are increasingly scarce and the construction of water-flow regulation structures is predicted to increase in the coming years. The correct management of these impacted areas may play an important role in the conservation of wetland bird species. In a floodplain whose natural flood pulse was reversed in relation to local rainfall seasonality by the construction of a dam (the Tanquã floodplain), we investigated how the composition and abundance of the waterbird community varied with the water depth to understand how artificially maintained flooded areas could sustain different bird functional groups, preventing future biodiversity losses. We recorded 72 waterbird species, 17 reproducing in the area. Seventeen species are short-distance migrants in Brazil, while eight are long-distance migrants. As overall bird abundances are negatively correlated with the water depth, any further modification in the flood-pulse may cause the area to lose its ability to support its biodiversity. Future dam construction projects should take actions to transform or maintain their areas of influence as important habitats for the threatened waterbir d community, thus contributing to their conservation. KEY-WORDS: bird functional groups, dam impacts, waterbirds, wetland management, wetlands. INTRODUCTION (Ma et al. 2004, Acosta et al. 2010, Sebastián-González & Green 2016). As energy demand grows and governments seek for The region known as “Tanquã” is a floodplain located upstream from the estuary formed by the confluence of cleaner forms of energy production, the focus has been set on hydropower plants, which are responsible for the Piracicaba and Tietê Rivers in southeast Brazil (Fig. approximately 16% of the global electricity consumption 1). It encompasses five shallow lakes seasonally connected and is a rapidly growing industry (IHA 2015). The re- to the Piracicaba River and secondary channels. In 1963, accelerating construction of hydropower dams will the construction of Barra Bonita dam downstream from the floodplain led to the elevation of the water level and globally lead to the fragmentation of 25 of the 120 large river systems currently classified as free-flowing, primarily increased the magnitude of the floods, creating a more in South America (Zarfl et al. 2015). dynamic habitat. Furthermore, the dam water retention Dams usually alter the river hydrology, with period is longer during the drier months, as its water consequences for the associated biota, including species discharge is responsible for maintaining the level of the Tietê-Parana waterway, in addition to producing associated with wetlands, one of the most fragile and threatened ecosystems in the world, recognized as priority electricity (Petesse et al. 2007). As a result, the seasonal for biodiversity conservation (Amezaga et al. 2002). At fluctuation of the water depth was altered in Tanquã: in least 64% of wetlands were lost globally during the past the wettest months Tanquã faces a drought period, with century (Gardner et al. 2015). As these areas are drained the water depth at its minimum while the dam is at its maximum discharge, but in the driest months the area is or altered, their ability to sustain viable populations of wetland-dependent organisms decreases. Waterbirds, for flooded because of the longer water retention period in instance, are increasingly threatened to extinction and the the reservoir. successes of conservation measures are being outweighed Preliminary observations indicate that this artificial by their negative response to habitat loss (Paszkowski & hydrological cycle imposed by the dam apparently benefited several waterbir d species, including rare and Tonn 2000, Gardner et al. 2015). In order to compensate for habitat loss, birds often occupy artificial wet lands, migratory ones, an example of what Rosenzweig (2003) whose correct management can contribute to conservation called “happy accident”, a human action that ends Bird species in a floodplain with reversed flood pulse Robinson & Pizo up having an unexpected positive effect on wildlife. lakes that are seasonally connected to the Piracicaba River, Notwithstanding, a project to construct a new dam to forming a complex locally known as Tanquã (Fig. 1). The expand the Tietê-Paraná waterway is planned, providing climate is highly seasonal, with two well-defined seasons, the necessary depths to new sections of the river that a warmer and humid season from October to April, with would cause a further rise and stabilization of the water the remainder of the year being cooler and drier. level. Tanquã is surrounded by pastures and sugarcane Because water depth and flood-pulses are the most plantations, with only two small fragments remaining important features determining the quality and quantity from the original riparian forest. The vegetation in the of habitat for waterbirds (Ntiamoa-Baidu et al. 1998, floodplain is composed by herbs and bushes in the Lantz et al. 2011, Baschuk et al. 2012, Tavares et al. 2015), dryer margins and islands, while floating and emergent in this study we investigated how the composition and macrophytes dominate the flooded areas. abundance of the waterbird community varied with the river depth seasonality, to understand how Tanquã may Bird survey be impacted by the construction of new water retention structures, and how artificially maintained flooded areas We surveyed birds once a month from October 2014 to could sustain different bird functional groups, preventing September 2015 (66 h of sampling effort) in seven sampling future biodiversity losses. In a scenario where wetlands points separated by at least 500 m from each other, which are becoming increasingly scarce and the construction were accessed by boat and permitted an unobstructed of many new water-flow regulation structures is view of the birds. Points were sampled by two researchers predicted, it is essential to find solutions that take into from 07:00 h to 11:30 h for 20 min each, period in which consideration the preservation of the biodiversity of the boat engine was turned off. The sampling or der of the wetlands while meeting human needs. For this, properly points was randomized for each month. All individuals managed artificial areas may play an important role in the resting, foraging or engaging in reproductive activities conservation of waterbird species. within 250 m from sampling points were recorded with the aid of Nikon Prostaff 10 × 42 binoculars. Data on the total number of individuals of each species, number METHODS of females, males, young and offspring were recor ded to investigate the occurrence of reproductive activities. In Study site addition to the quantitative survey, we made 60 h of ad libitum observations during the afternoons, from 15:00 The study was conducted 30 km upstream the estuary h to 18:00 h to complement the bird species list. Birds formed by the confluence of the Piracicaba and Tietê were recorded with a Canon EOS 7D camera and Canon o o Rivers in southeast Brazil (22 39'S; 48 01'W, 452 m 70–300 mm lens. Some of the images were deposited in a.s.l.). The floodplain of 2.4 ha encompasses five shallow digital bases such as WikiAves and IBC (Internet Bird Figure 1. Location of Tanquã floodplains and Barra Bonita dam in the state of São Paulo, southeast Brazil. Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Collection). Species were identified based on field guides (3) foraging substrate (water column, shores, mudflats, (Novelli 1997, Sigrist 2009). Species from Scolopacidae water surface, floating macrop hytes, emerged and Charadriidae families were always photographed. macrophytes, water margins); and (4) migratory status The nomenclature and taxonomic arrangement follow (Piacentini et al. 2015). For the qualitative traits above, the annotated checklist of the birds of Brazil by the a number from one to five representing the affinity of Brazilian Ornithological Records Committee (Piacentini the species with the particular trait was assigned to each et al. 2015). Species conservation status in São Paulo state species based on field o bservations and the literature (Sick follows Decree 60133, from 07 February 2014 (São Paulo & Barruel 1997, Sigrist 2009). A correlation analysis 2014). Migratory status follow Piacentini et al. (2015), performed in FDiversity software was used to certify that while short-distance migrants were identified a ccording none of the functional traits were correlated to each other. to Antas (1994), Sick & Barruel (1997), and Sigrist The relationship between bird abundances (total (2009). The height of the water column of the Piracicaba and separated by functional groups) and water depth River was visually monitored before the start of each bird were tested with GLM (Generalized Linear Model) in the sampling with limnimetric rulers graded every 2 cm. software R, estimating a Poisson regression model with a To compile a species list as complete as possible, dispersion parameter (or quasi-Poisson), as the count data we also considered species recorded by us outside the presented overdispersion. This method a llows the linear censuses, records published in the EIA (Environmental model to be related to the response variable by allowing Impacts Study) of the proposed dam (“Aproveitamento the magnitude of the variance of each measurement to be Múltiplo Santa Maria da Serra”) and reliable and verified a function of its predicted value. An analysis of deviance records published on WikiAves, IBC and EBird websites. was carried out to test all models against null models To do so, records in which the photographer or researcher (Zuur et al. 2009). All eight migratory non-reproductive was known were used; when this was not possible (e.g. species whose presence in the area was not dependent on Anas platalea and Anas georgica) the photographer or his the water depth, and all 12 passerines whose counts were guide were contacted to confirm th e exact location of the not always precise (see Table 1 for a list of these species), photo. were excluded from the GLM analyses. Ardea alba and Nannopterum brasilianus were Data analyses recorded in aggregations too discrepant in relation to the other species in their functional groups (660 and 385, For all the analyses, only waterbird species were respectively), and were excluded from the functional considered, such as typically water dependent families group models as outliers. Both species are habitat (Podicipedidae, Phalacrocoracidae, Anhingidae, Ardeidae, generalists found in great aggregations in a variety of Threskiornithidae, Ciconiidae, Anatidae, Aramidae, water bodies. Rallidae, Pandionidae, Jacanidae, Charadriidae, Scolopacidae, Recurvirostridae, Sternidae, Rynchopidae, RESULTS Alcedinidae and Donacobiidae) and also species from families that are not typically associated to water We recorded 72 water-depending bird species, 12 of (Anhimidae, Accipitridae, Furnaridae, Tyrannidae, Hirundinidae, and Icteridae), but depend on waterbodies which were recorded only during ad libitum observations. for foraging or reproduction. Species that inhabited the Species were distributed in 24 families, being Anatidae (11 species), Ardeidae (10) and Rallidae (9) the most area, but were not dependent on water bodies for foraging or reproducing, were excluded from the analyses. We speciose families. Nannopterum brasilianus was the most abundant species, followed by Gallinula galeata, estimated bird species richness using estimators Jacknife 1 and Chao 2 with the software Past (version 1.81; Ardea alba and Dendrocygna bicolor. The species whose Hammer et al. 2001). abundance varied the most were N. brasilianus and G. To investigate how bird traits affect their response galeata, followed by Himantopus melanurus and A. alba. to fluctuations in the water depth, we classified birds We found signs of reproduction for 17 species, and the presence of five species locally threatened by extinction, in functional groups using a cluster analysis carried out in FDiversity software (Casanoves et al. 2011). Ward's two “Near Threatened ” and one listed as “Data Deficient” method and Gower distance were used since they are (Table 1). Richness estimated with Jacknife 1 was 76.42 suitable for qualitative functional traits as used in this ± 3.94 species, and with Chao 2 73.21 ± 3.40 species, study (Schleuter et al. 2010). The following bird traits figures similar to the species richness actually recor ded. were used for clustering: (1) body mass (Dunning-Jr. The census data plus the compilation of literature 1992); (2) diet (fish, other vertebrates, insects or oth er and online data resulted in 94 species. Of the 22 species invertebrates, benthic macroinvertebrates, macrophytes); that were not recorded in the censuses, eight are migratory Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Table 1. Monthly abundances (number of birds counted) of wetland-dependent bird species recorded from October 2014 to September 2015 in Tanquã floodplains. “x” denotes the presence of a species recoded only in ad libitum observations. Bird nomenclature is based on Piacentini et al. (2015). Species O N D J F M A MJ J A S Group* Anhimidae 1,6 Anhima cornuta x WS Anatidae 5,6 Dendrocygna bicolor 50 44 71 24 5 12 x x 4 100 337 9 WS Dendrocygna viduata 85 148 12 6 x x x x xx WS Dendrocygna autumnalis 43 47 26 21 2 5 x x 9 x 18 5 WS Cairina moschata x1 WS Sarkidiornis sylvicola xxxxx WS Amazonetta brasiliensis 20 1 3017 6 14 4 1017311016 WS Anas bahamensis 20 x 1 10 1 x 2x WS Anas versicolor 25 11 299 x x 2252 x WS Netta erythrophthalma 20 14 x x 5 1 xWS 4,5,6 Netta peposaca 16 8 10 35 10 x x 1 52 9 103 4 WS Nomonix dominicus xx x WS Podicipedidae Tachybaptus dominicus 12 DP Podilymbus podiceps 3333247 14 663 DP Ciconiidae 1,5 Jabiru mycteria 12 19 8 x x x x LP Mycteria americana 26 130 129 99 15 x x 1 LP Phalacrocoracidae Nannopterum brasilianus 662 119 9 2 25 42 106 71 59 86 130 103 DP Anhingidae Anhinga anhinga x2x4 3 3 1 1 1x1 DP Ardeidae Tigrisoma lineatum xxxx x 1 xxxx 2 LP Ixobrychus involucris xEM Nycticorax nycticorax x 423415 582533 14 LP Butorides striata x x x 42 25 143145 LP Bubulcus ibis 2154 xx x LP Ardea cocoi 11 35 12 17 22 30 19 14 29 37 11 28 LP Ardea alba 83 79 49 27 11 122 92 42 136 409 16 79 LP Syrigma sibilatrix x 1LP Egretta thula 207 110 11 9 6 48 60 19 12 12 2 58 LP Egretta caerulea xx xx LP Threskiornithidae Plegadis chihi 28 x xPW Mesembrinibis cayennensis x x2x xx PW Phimosus infuscatus x x2x x2x x1 4 PW Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Species O N D J F M A MJ J A S Group* Theristicus caudatus 2xx PW Platalea ajaja 40 22 10 x x x 1 PW Pandionidae Pandion haliaetus 11 1 LP Accipitridae 1,6 Circus buffoni x1 1x 2 1 PW 5,6 Rostrhamus sociabilis x1x 1x x x PW Aramidae Aramus guarauna 1 1x x x x1x1 x PW Rallidae Aramides cajaneus xx EM Laterallus melanophaius 4 x 1413266 16 11 EM Laterallus exilis 111 x xx xEM Porzana flaviventer 31 xx 1 EM Mustelirallus albicollis xxxx xxxxx EM Pardirallus maculatus xx x EM Pardirallus nigricans xxxx xxxxx EM Pardirallus sanguinolentus xxxxxxx 1 xxx EM Gallinula galeata 468 237 117 45 60 53 21 42 36 35 89 58 WS 5,6 Porphyrio martinicus 3271 10 4524 x 25 WS Charadriidae Charadrius semipalmatus x SW Recurvirostridae Himantopus melanurus 393 53 3 xxxxxxxxx PW Scolopacidae Gallinago paraguaiae xPW Tringa flavipes 13 xx SW Tringa melanoleuca 86 1 SW Tringa solitaria 5 xx SW Calidris melanotos 2SW Calidris fuscicollis x SW Jacanidae Jacana jacana 40 48 26 48 43 46 31 42 51 50 111 68 WS Sternidae Phaetusa simplex 2 xxx x 3 x DP Rynchopidae Rynchops niger 1 xx 1 x xxx DP Alcedinidae Megaceryle torquata x x x 2 x 11112 x DP Chloroceryle amazona x x2x x x x1x x DP Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Species O N D J F M A MJ J A S Group* Furnaridae Certhiaxis cinnamomeus xxxxxx xxxxxx - Cranioleuca vulpina xx - Tyrannidae Pseudocolopteryx sclateri 11 x1x - Fluvicola albiventer xxx 1 xxxxxxxx - Fluvicola nengeta x xx 2 xxxxxx - Arundinicola leucocephala x x1x x xx x - Gubernetes yetapa x - Hirundinidae Tachycineta albiventer 1 xxx 2 x 1 - Donacobiidae Donacobius atricapilla 1x x1x1x1 - Icteridae Agelasticus cyanopus xxxx x xx - Chrysomus ruficapillus xxxxxxxxxxxx - Pseudoleistes guirahuro xxx - – Threatened to extinction (São Paulo 2014) – Near Threatened (São Paulo 2014) – Data Deficient (São Paulo 2014) – Migratory species (Piacentini et al. 2015) – Short-distance migrant species (Antas 1994, Sick & Barruel 1997, Sigrist 2009) – Species with evidences of reproduction * – Functional groups generated in the cluster analyses (PW = Probing waders, SW = Small waders; LP = Large piscivores, DP = Diving piscivores, EM = Emerged macrophytes, and WS = Water surface). that nest in the Northern Hemisphere and spend only that mostly capture fish and other prey while foraging in a few days in Tanquã, and four species make seasonal shallow areas near the shore, without diving, (4) Diving movements throughout the country (Appendix I). piscivores: birds that dive for fishes and other prey, (5) Twenty-one species (29.5%) were recorded in more birds that forage on Emerged macrophytes: small and than 90% of the sampling months, being considered inconspicuous species (mainly rails) found in the dense residents, while 67.8% of the species were recorded in at vegetation that surround the water, and (6) birds that least half of the samplings, thus considered common in feed on the Water surface: a group congregating species the area. Eighteen species are short-distance migrants in that forage by filtering organisms in the water surface, or Brazil, and eight are classified as non-reproductive long- spend most of the time floating in the river surface while distance migrants, although we found more than one searching for food (Table 1). Large piscivores and birds nest and several juveniles of one of these species (Netta that feed on the Water surface were the most abundant peposaca). Except from N. peposaca, which was present all groups, accounting for 87.3% of the total abundance. year round, the other migratory species visited the area The water depth varied monthly from 5.3 m to 9.6 from October to February (Table 1). m, while monthly bird abundance ranged from 294 to The cluster analysis generated six functional groups 2411 individuals, and species richness varied from 24 to 35. with a cophenetic correlation coefficient from the Richness was not correlated to water depth (R = 0.016, P = distance matrix of 0.73. These groups where classified 0.4), but total bird abundance was negatively correlated to it as (1) Probing waders: species that forage mainly on (pseudo R = 0.36 P = 0.041) (Fig. 2, Table 2). The functional the shores and exposed mudflats, feeding primarily groups responded differently to fluctuations in water depth. on macroinvertebrates in the mud, (2) Small waders: The abundances of Water surface, Large piscivores and mainly sandpipes and plovers, this group comprises small Probing waders were negatively correlated to water depth, migratory species (up to 60 cm) that eat small invertebrates while models for Emerged macrophytes and Diving piscivores picked out of the mud or soil, (3) Large piscivores: species groups were non-significant (Fig. 3, Table 2). Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Table 2. Analysis of deviance table for the GLM testing the relationship between the total bird abundance and abundances of functional groups with the water depth. Residual Residual df df Deviance F P(>F) Deviance Null 11 3964.50 Total abundance 1 1463.80 10 2500.70 5.48 0.041 Null 11 696.76 Large piscivores 1 557.95 10 138.81 44.45 <0.01 Null 11 2019.55 Probing waders 1 803.11 10 1216.40 13.77 <0.01 Null 11 24.49 Diving piscivores 1 2.53 10 21.97 1.29 0.283 Null 11 36.18 Emerged macrophytes 1 7.08 10 29.11 2.39 0.153 Null 11 1893.00 Water surface 1 677.89 10 1215.10 4.68 0.055 2006) and 27 species (Rodrigues & Michelin 2005) were recorded in Minas Gerais state, while in São Paulo state, 51 (Crozariol 2010), 49 (Schunck et al. 2016), and 39 (Schunck & Rodrigues 2016) water-dependent species were found. Apart from the high bird species richness, Tanquã is important for rare, migratory and locally threatened species. Eight threatened (Anhima cornuta, Sarkidiornis sylvicola, Ciconia maguari, Jabiru mycteria, Busarellus nigricollis, Circus buffoni, Phaetusa simplex and Sternula superciliaris) and five “Near Threatened ” species (Nomonyx dominicus, Mycteria americana, Tryngites subruficollis, Pluvialis dominica and Gallinago undulata) (São Paulo 2014) occur at the area (Table 2). Other noteworthy bird records are (1) N. peposaca, a migratory species that nests west of Brazil or in the south of the country (Antas 1994), but was found all year around and reproducing in Tanquã, the first place outside of the south region of Brazil w here Figure 2. Quasi-Poisson regression model showing the response reproductive activities were recorded. (2) M. americana of total bird abundance to variation in the water depth. was recorded in 50% of surveys and in flocks of up to 150 individuals. This species also migrates through t he Paraná River Valley, staying in the Pantanal from November to DISCUSSION April where it breeds and then migrates to feeding areas in Rio Grande do Sul, south Brazil (Antas 1994). This is The importance of Tanquã for birds the same period when the species was found in Tanquã, but we could not find any signs of reproduction. Many of Compared to other wetlands in southeast Brazil, Tanquã the birds we recorded were juveniles that could be using have the highest number of water-dependent bird the area only for foraging. (3) Pseudocolopteryx sclateri, a bird discovered in the state of São Paulo only in 2009, species, representing 53.3% (or 69.6% if we add the species reported in the literature and online data) of all with pairs engaging in mating activities at Tanquã. (4) 135 wetland species found in the Atlantic Forest Biome Porzana flaviventer, a bir d common in Tanquã, but rarely (Moreira-Lima 2013). In a natural coastal lagoon in Rio seen in other parts of Brazil whose biology and regional de Janeiro state, 46 water-dependent bird species were movements are not yet understood in the country. Only 29.5% of the species recorded were residents, recorded (Tavares & Siciliano 2014), 37 (Faria et al. Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Figure 3. Quasi-Poisson regression model showing the response of the abundances of different bird functional groups to variation in the water depth. while several species make seasonal movements within the sites (“convenience store”) are structurally heterogeneous Brazilian territory, migrating through the Paraná River sites with freshwater and a variety of food resources where Valley, from south Brazil to the Pantanal region (e.g., J. birds can rest briefly (two days or less) and easily replenish mycteria; Antas 1994). Valente et al. (2011) produced the body reserves. Type 3 sites (“full service hotel”) are first catalogue of important areas for Nearctic migratory extensive areas suitable for migratory birds, where all the birds in Brazil, highlighting six sites in southeastern Brazil. necessary resources are relatively abundant and available. The number of species classified as non-reproductive Type 3 sites can sustain many individuals of many species long-distance migrants (according to Piacentini et al. that can remain there for weeks allowing them to achieve 2015) recorded in our censuses (8 species) is similar to the physiological conditions necessary to continue their the average species richness recorded at these areas (8.14 ± migration to the next stop or final destination. We believe 3.02 species), but our literature review raises this number that Tanquã can be classified as a type 2 or 3 stopover site, to 16 species, thus corroborating the importance of because large agglomerations of species from the families Tanquã for Nearctic birds in Brazil. Scolopacidae and Charadriidae were found during their Mehlman et al. (2005) analyzed the importance wintering periods in Brazil. These families comprise several of migratory passerine stopover sites in the Northern migratory species that require newly exposed mud to forage Hemisphere and generated a useful scale for their (Sick & Barruel 1997). The energy accumulated in sites like categorization. Although designed for terrestrial birds, Tanquã is likely important for these species to return to the Kirby et al. (2008) considered this typology adaptable to Northern Hemisphere, as food obtained in stopovers sites other groups of migratory birds. Type 1 sites (“fire-escape”), provides energy to migration (Davison & Evens 1988), and usually small, isolated habitats surrounded by unsuitable the increase in nutritional reserves is essential to further habitat that are rarely used but vital in emergencies. Type 2 reproductive success (Hvenegaard & Barbieri 2010). Revista Brasileira de Ornitologia 25(3): 2017 *  "+ , # # # # ! $&' !" Bird species in a floodplain with reversed flood pulse Robinson & Pizo Seasonality in the water depth and its alteration of the current flood cycle by the construction effects upon birds of the planned new dam (called Aproveitamento Múltiplo Santa Maria da Serra) carries a real risk of threatening several elements of the local bird community. In the rainy season, the water level falls because the In summary, Tanquã is a large floodplain with power plant is operating and the water is flowing fast high environmental heterogeneity offering a mosaic of out of Tanquã. As a result, the higher abundance of birds habitats, ranging from exposed mudflats to open water observed in this period may be due to the availability of variable depth, with remarkable temporal changes in of shallow waters, which increase prey concentrations environmental characteristics. The seasonal fluctuation (Macedo-Soares et al. 2010, Tavares & Siciliano 2014), of the water level, heterogeneity of habitats, and the and recently exposed mudflats occurring concomitantly size of the floodplain may be the reasons why so many with the arrival of migratory species that feed on this waterbirds species occurring in high abundances were microhabitat. Shallow waters and recently exposed recorded, as these are among the main factors influencing mudflats are likely scar ce in the region in the rainy season, bird abundance in wetlands (Paracuellos & Tellería 2004). making Tanquã an important feeding site for birds. Any further infrastructure project that would maintain The abundances of bir ds of the Water surface, Large Tanquã permanently flooded will lead it to lose its ability piscivores, and Probing waders groups were negatively to support such a diverse community of waterbirds. correlated with the water depth. Species from the Water Apparently, the artificial flood regime imposed surface group forage by filtering organisms in the water by the Barra Bonita dam counteracted the damage surface; when the water level raises, water surface increases expected from the construction of the power plant. As and vegetation become scarce. Baschuk et al. (2012) such, the Tanquã “happy accident” showed that, by observed that it is easier for dabbling ducks to access reproducing natural cycles of floodplains during their submerged aquatic vegetation in shallow waters. Lack of operation, existing and future power plant projects vegetation may also increase the risk of duck predation. may take actions to transform or maintain their areas Furthermore, shallow lakes were considered preferred of influence as important habitats for the threatened habitats for ducks in previous studies (Paszkowski & aquatic bird community. Future studies need to focus on Tonn 2000, Tavares et al. 2015). The Large piscivores better understanding such actions, which likely includes group may be influenced by water depth because of their regulatory provisions foreseeing the establishing of a foraging behavior, as they tend to capture fish in shallow monomodal flood-pulse when possible. As different bird areas near the shore. When the water level rises it gets groups are differently influenced by the water level and more difficult to capture their prey due to an in crease in its variation, maintaining a monomodal and annual flood the dimensional space (Ntiamoa-Baidu et al. 1998, Lantz pulse contributes to the maintenance of a high species and et al. 2010). The water depth has also a strong influence in functional diversity in wetlands. When appropriate flood- vegetation cover (Padial et al. 2009, Ma et al. 2010) that pulse regulation is not an option, then the creation of may act as a barrier reducing visibility to detect predators. habitat heterogeneity, such as shallow shorelines or island Species in the Probing waders group have a preference development should be recommended as mitigation for foraging mainly on the shores and exposed mudflats and restoration actions in response to dam construction (Tavares et al. 2015), a microhabitat that temporarily (Desgranges et al. 2006). As smaller dams probably offer disappear with the rise of the water level. more manageable options and opportunities, they should Abundance of Emerged macrophytes and Diving be taken into consideration when establishing investment piscivores groups were not correlated with water depth. priorities and financing towar ds new dam projects, either However, the Emerged macrophytes group is composed for power generating or any other uses. of several small and inconspicuous species that are recorded mainly by their vocalizations. Because these species sing more frequently during the reproductive ACKNOWLEDGEMENTS period, their abundance may have been underestimated during other seasons. Although the abundance of Diving We thank V. Bortolotti, B. Alleoni, M. Dourado, M. piscivores was not significantly related to the river depth, Afonso, R. Machado, M. Flores, and especially C. Gussoni previous studies have shown that aerially foraging and for helping in the fieldwork. We also thank F. Godoy w ho diving piscivores could be favored by higher water levels first introduced us to the area, and t he birdwatch guide G. Pinto for keeping us updated on Tanquã news. We (Paszkowski & Tonn 2000, Paillisson et al. 2002, Baschuk are also grateful to the boatman Ivanildo for logistical et al. 2012). Our results show that any rise in the water support and the people from the Tanquã community for level can negatively affect bird abundance, especially for welcoming us so warmly. We are grateful to the National species in the Large piscivores, Water surface and Probing Council for Scientific and Te chnological Development waders functional groups. Therefore, the predicted Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Ma Z., Cai Y., Li B. & Chen J. 2010. Managing wetland habitats for (CNPq) for the MSc. scholarship to V.R. M.A.P. receives waterbirds: an international perspective. 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Belém: diversity in created versus natural and restored wetlands. Ecography Conservação Internacional. 39: 1176–1184. Zarfl C., Lumsdon A.E., Berlekamp J., Ty decks L. & Tockner K. Sick H. & Barruel P. 1984. Ornitologia brasileira, v. 1. Brasília: Editora 2015. A global boom in hydropower dam construction. Aquatic Universidade de Brasília. Sciences 77: 161–170. Sigrist T. 2009. The Avis Brasilis field gui de to the birds of Brazil: species Zuur A.F., Ieno E.N., Walker N.J., Saveliev A.A. & Smith G.M. 2009. accounts. São Paulo: Avibrasilis. Mixed effects models and extensions in ecology with R . New York: Tavares D.C., Guadagnin D.L., Moura J.F., Siciliano S. & Merico A. 2015. Environmental and anthropogenic factors structuring Springer. waterbird habitats of tropical coastal lagoons: implications for management. Biological Conservation 186: 12–21. Associate Editor: Luis F. Silveira. APPENDIX I A complete list of bird species recorded in Tanquã based on field samplings, bibliographic records, online records published in Wikiaves, IBC and EBird. Bird nomenclature is based on Piacentini et al. (2015). EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Anhimidae Anhima cornuta xx x R T Chauna torquata xR DD Anatidae Dendrocygna bicolor xx x x R Dendrocygna viduata xx x x R Dendrocygna autumnalis xx x x R Coscoroba coscoroba xR Cairina moschata xx x x R Sarkidiornis sylvicola xx x x R T Amazonetta brasiliensis xx x x R Anas georgica xR Anas bahamensis xx x x R Anas versicolor xx x x R Anas discors xx VN Anas platalea xVS Netta erythrophthalma xx x R Netta peposaca xx x x VO Nomonyx dominicus xx x R NT Podicipedidae Tachybaptus dominicus xx x x R Podilymbus podiceps xx x R Podicephorus major xR Ciconiidae Ciconia maguari xR T Jabiru mycteria xx x R T Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Mycteria americana xx x x R NT Phalacrocoracidae Nannopterum brasilianus xx x x R Anhingidae Anhinga anhinga xx x x R Ardeidae Tigrisoma lineatum xx x R Ixobrychus involucris xx x R Nycticorax nycticorax xx x x R Butorides striata xx x x R Bubulcus ibis xx x x R Ardea cocoi xx x x R Ardea alba xx x x R Syrigma sibilatrix xx x x R Egretta thula xx x x R Egretta caerulea xx x R Threskiornithidae Plegadis chihi xx x x R Mesembrinibis cayennensis xx x R Phimosus infuscatus xx x R Theristicus caudatus xx x x R Platalea ajaja xx x x R Pandionidae Pandion haliaetus xx x x VN Accipitridae Circus buffoni xx x R T Busarellus nigricollis xx R T Rostrhamus sociabilis xx x x R Aramidae Aramus guarauna xx x x R Rallidae Aramides cajaneus xx x x R Laterallus melanophaius xx x x R Laterallus exilis xx x R DD Porzana flaviventer xx x R Mustelirallus albicollis xx x x R Pardirallus maculatus xx x R Pardirallus nigricans xx x x R Pardirallus sanguinolentus xx x x R Gallinula galeata xx x x R Porphyrio martinicus xx x x R Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Porphyrio flavirostris xR Fulica leucoptera xx R Charadriidae Pluvialis dominica x x VN NT Charadrius semipalmatus xx x VN Charadrius collaris xx R Recurvirostridae Himantopus melanurus xx x x R Scolopacidae Gallinago paraguaiae xx x x R Gallinago undulata xR NT Limosa haemastica xVN Actitis macularius xx x VN Tringa solitaria xx x x VN Tringa flavipes xx x x VN Tringa melanoleuca xx x x VN Calidris fuscicollis xx x x VN Calidris melanotos xx x x VN Calidris pugnax xVN Calidris subruficollis xVN NT Phalaropus tricolor xx VN Jacanidae Jacana jacana xx x x R Rostratulidae Nycticryphes semicollaris xR DD Laridae Chroicocephalus maculipennis xR Sternidae Sternula superciliaris xR T Phaetusa simplex xx x x R T Rynchopidae Rynchops niger xx x x R Alcedinidae Megaceryle torquata xx x x R Chloroceryle amazona xx x x R Chloroceryle americana xx R Furnariidae Certhiaxis cinnamomeus xx x x R Cranioleuca vulpina xx x R Tyrannidae Pseudocolopteryx sclateri xR Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Fluvicola albiventer xx x x R Fluvicola nengeta xx x R Arundinicola leucocephala xx x x R Gubernetes yetapa xx x x R Hirundinidae Tachycineta albiventer xx x x R Donacobiidae Donacobius atricapilla xx x x R Icteridae Agelasticus cyanopus xx x R Chrysomus ruficapillus xx x R Pseudoleistes guirahuro xx x R Species recorded in field visits performed before or after the censuses conducted between O ctober 2014 and September 2015. R = resident; VS = Seasonal visitor from the south of the continent; VN = Seasonal visitor from the Northern Hemisphere; VO = Seasonal visitor coming from west of the Brazilian territory (Piacentini et al. 2015). T = Threatened by extinction, NT = Near Threatened and DD = Data Deficient (São Paulo 2014). Revista Brasileira de Ornitologia 25(3): 2017 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

A floodplain with artificially reversed flood pulse is important for migratory and rare bird species

Ornithology Research , Volume 25 (3) – Sep 1, 2017

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Abstract

Revista Brasileira de Ornitologia 25(3): 155–168. ARTICLE September 2017 A floodplain with artificially reversed flood pulse is important for migratory and rare bird species 1 1,2 Vivian Robinson & Marco A. Pizo Departamento de Zoologia, Universidade Estadual Paulista, Av. 24A, 1515, 13506-900, Rio Claro, SP, Brazil. Corresponding author: pizo@rc.unesp.br Received on 09 March 2017. Accepted on 04 July 2017. ABSTRACT: Wetlands are increasingly scarce and the construction of water-flow regulation structures is predicted to increase in the coming years. The correct management of these impacted areas may play an important role in the conservation of wetland bird species. In a floodplain whose natural flood pulse was reversed in relation to local rainfall seasonality by the construction of a dam (the Tanquã floodplain), we investigated how the composition and abundance of the waterbird community varied with the water depth to understand how artificially maintained flooded areas could sustain different bird functional groups, preventing future biodiversity losses. We recorded 72 waterbird species, 17 reproducing in the area. Seventeen species are short-distance migrants in Brazil, while eight are long-distance migrants. As overall bird abundances are negatively correlated with the water depth, any further modification in the flood-pulse may cause the area to lose its ability to support its biodiversity. Future dam construction projects should take actions to transform or maintain their areas of influence as important habitats for the threatened waterbir d community, thus contributing to their conservation. KEY-WORDS: bird functional groups, dam impacts, waterbirds, wetland management, wetlands. INTRODUCTION (Ma et al. 2004, Acosta et al. 2010, Sebastián-González & Green 2016). As energy demand grows and governments seek for The region known as “Tanquã” is a floodplain located upstream from the estuary formed by the confluence of cleaner forms of energy production, the focus has been set on hydropower plants, which are responsible for the Piracicaba and Tietê Rivers in southeast Brazil (Fig. approximately 16% of the global electricity consumption 1). It encompasses five shallow lakes seasonally connected and is a rapidly growing industry (IHA 2015). The re- to the Piracicaba River and secondary channels. In 1963, accelerating construction of hydropower dams will the construction of Barra Bonita dam downstream from the floodplain led to the elevation of the water level and globally lead to the fragmentation of 25 of the 120 large river systems currently classified as free-flowing, primarily increased the magnitude of the floods, creating a more in South America (Zarfl et al. 2015). dynamic habitat. Furthermore, the dam water retention Dams usually alter the river hydrology, with period is longer during the drier months, as its water consequences for the associated biota, including species discharge is responsible for maintaining the level of the Tietê-Parana waterway, in addition to producing associated with wetlands, one of the most fragile and threatened ecosystems in the world, recognized as priority electricity (Petesse et al. 2007). As a result, the seasonal for biodiversity conservation (Amezaga et al. 2002). At fluctuation of the water depth was altered in Tanquã: in least 64% of wetlands were lost globally during the past the wettest months Tanquã faces a drought period, with century (Gardner et al. 2015). As these areas are drained the water depth at its minimum while the dam is at its maximum discharge, but in the driest months the area is or altered, their ability to sustain viable populations of wetland-dependent organisms decreases. Waterbirds, for flooded because of the longer water retention period in instance, are increasingly threatened to extinction and the the reservoir. successes of conservation measures are being outweighed Preliminary observations indicate that this artificial by their negative response to habitat loss (Paszkowski & hydrological cycle imposed by the dam apparently benefited several waterbir d species, including rare and Tonn 2000, Gardner et al. 2015). In order to compensate for habitat loss, birds often occupy artificial wet lands, migratory ones, an example of what Rosenzweig (2003) whose correct management can contribute to conservation called “happy accident”, a human action that ends Bird species in a floodplain with reversed flood pulse Robinson & Pizo up having an unexpected positive effect on wildlife. lakes that are seasonally connected to the Piracicaba River, Notwithstanding, a project to construct a new dam to forming a complex locally known as Tanquã (Fig. 1). The expand the Tietê-Paraná waterway is planned, providing climate is highly seasonal, with two well-defined seasons, the necessary depths to new sections of the river that a warmer and humid season from October to April, with would cause a further rise and stabilization of the water the remainder of the year being cooler and drier. level. Tanquã is surrounded by pastures and sugarcane Because water depth and flood-pulses are the most plantations, with only two small fragments remaining important features determining the quality and quantity from the original riparian forest. The vegetation in the of habitat for waterbirds (Ntiamoa-Baidu et al. 1998, floodplain is composed by herbs and bushes in the Lantz et al. 2011, Baschuk et al. 2012, Tavares et al. 2015), dryer margins and islands, while floating and emergent in this study we investigated how the composition and macrophytes dominate the flooded areas. abundance of the waterbird community varied with the river depth seasonality, to understand how Tanquã may Bird survey be impacted by the construction of new water retention structures, and how artificially maintained flooded areas We surveyed birds once a month from October 2014 to could sustain different bird functional groups, preventing September 2015 (66 h of sampling effort) in seven sampling future biodiversity losses. In a scenario where wetlands points separated by at least 500 m from each other, which are becoming increasingly scarce and the construction were accessed by boat and permitted an unobstructed of many new water-flow regulation structures is view of the birds. Points were sampled by two researchers predicted, it is essential to find solutions that take into from 07:00 h to 11:30 h for 20 min each, period in which consideration the preservation of the biodiversity of the boat engine was turned off. The sampling or der of the wetlands while meeting human needs. For this, properly points was randomized for each month. All individuals managed artificial areas may play an important role in the resting, foraging or engaging in reproductive activities conservation of waterbird species. within 250 m from sampling points were recorded with the aid of Nikon Prostaff 10 × 42 binoculars. Data on the total number of individuals of each species, number METHODS of females, males, young and offspring were recor ded to investigate the occurrence of reproductive activities. In Study site addition to the quantitative survey, we made 60 h of ad libitum observations during the afternoons, from 15:00 The study was conducted 30 km upstream the estuary h to 18:00 h to complement the bird species list. Birds formed by the confluence of the Piracicaba and Tietê were recorded with a Canon EOS 7D camera and Canon o o Rivers in southeast Brazil (22 39'S; 48 01'W, 452 m 70–300 mm lens. Some of the images were deposited in a.s.l.). The floodplain of 2.4 ha encompasses five shallow digital bases such as WikiAves and IBC (Internet Bird Figure 1. Location of Tanquã floodplains and Barra Bonita dam in the state of São Paulo, southeast Brazil. Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Collection). Species were identified based on field guides (3) foraging substrate (water column, shores, mudflats, (Novelli 1997, Sigrist 2009). Species from Scolopacidae water surface, floating macrop hytes, emerged and Charadriidae families were always photographed. macrophytes, water margins); and (4) migratory status The nomenclature and taxonomic arrangement follow (Piacentini et al. 2015). For the qualitative traits above, the annotated checklist of the birds of Brazil by the a number from one to five representing the affinity of Brazilian Ornithological Records Committee (Piacentini the species with the particular trait was assigned to each et al. 2015). Species conservation status in São Paulo state species based on field o bservations and the literature (Sick follows Decree 60133, from 07 February 2014 (São Paulo & Barruel 1997, Sigrist 2009). A correlation analysis 2014). Migratory status follow Piacentini et al. (2015), performed in FDiversity software was used to certify that while short-distance migrants were identified a ccording none of the functional traits were correlated to each other. to Antas (1994), Sick & Barruel (1997), and Sigrist The relationship between bird abundances (total (2009). The height of the water column of the Piracicaba and separated by functional groups) and water depth River was visually monitored before the start of each bird were tested with GLM (Generalized Linear Model) in the sampling with limnimetric rulers graded every 2 cm. software R, estimating a Poisson regression model with a To compile a species list as complete as possible, dispersion parameter (or quasi-Poisson), as the count data we also considered species recorded by us outside the presented overdispersion. This method a llows the linear censuses, records published in the EIA (Environmental model to be related to the response variable by allowing Impacts Study) of the proposed dam (“Aproveitamento the magnitude of the variance of each measurement to be Múltiplo Santa Maria da Serra”) and reliable and verified a function of its predicted value. An analysis of deviance records published on WikiAves, IBC and EBird websites. was carried out to test all models against null models To do so, records in which the photographer or researcher (Zuur et al. 2009). All eight migratory non-reproductive was known were used; when this was not possible (e.g. species whose presence in the area was not dependent on Anas platalea and Anas georgica) the photographer or his the water depth, and all 12 passerines whose counts were guide were contacted to confirm th e exact location of the not always precise (see Table 1 for a list of these species), photo. were excluded from the GLM analyses. Ardea alba and Nannopterum brasilianus were Data analyses recorded in aggregations too discrepant in relation to the other species in their functional groups (660 and 385, For all the analyses, only waterbird species were respectively), and were excluded from the functional considered, such as typically water dependent families group models as outliers. Both species are habitat (Podicipedidae, Phalacrocoracidae, Anhingidae, Ardeidae, generalists found in great aggregations in a variety of Threskiornithidae, Ciconiidae, Anatidae, Aramidae, water bodies. Rallidae, Pandionidae, Jacanidae, Charadriidae, Scolopacidae, Recurvirostridae, Sternidae, Rynchopidae, RESULTS Alcedinidae and Donacobiidae) and also species from families that are not typically associated to water We recorded 72 water-depending bird species, 12 of (Anhimidae, Accipitridae, Furnaridae, Tyrannidae, Hirundinidae, and Icteridae), but depend on waterbodies which were recorded only during ad libitum observations. for foraging or reproduction. Species that inhabited the Species were distributed in 24 families, being Anatidae (11 species), Ardeidae (10) and Rallidae (9) the most area, but were not dependent on water bodies for foraging or reproducing, were excluded from the analyses. We speciose families. Nannopterum brasilianus was the most abundant species, followed by Gallinula galeata, estimated bird species richness using estimators Jacknife 1 and Chao 2 with the software Past (version 1.81; Ardea alba and Dendrocygna bicolor. The species whose Hammer et al. 2001). abundance varied the most were N. brasilianus and G. To investigate how bird traits affect their response galeata, followed by Himantopus melanurus and A. alba. to fluctuations in the water depth, we classified birds We found signs of reproduction for 17 species, and the presence of five species locally threatened by extinction, in functional groups using a cluster analysis carried out in FDiversity software (Casanoves et al. 2011). Ward's two “Near Threatened ” and one listed as “Data Deficient” method and Gower distance were used since they are (Table 1). Richness estimated with Jacknife 1 was 76.42 suitable for qualitative functional traits as used in this ± 3.94 species, and with Chao 2 73.21 ± 3.40 species, study (Schleuter et al. 2010). The following bird traits figures similar to the species richness actually recor ded. were used for clustering: (1) body mass (Dunning-Jr. The census data plus the compilation of literature 1992); (2) diet (fish, other vertebrates, insects or oth er and online data resulted in 94 species. Of the 22 species invertebrates, benthic macroinvertebrates, macrophytes); that were not recorded in the censuses, eight are migratory Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Table 1. Monthly abundances (number of birds counted) of wetland-dependent bird species recorded from October 2014 to September 2015 in Tanquã floodplains. “x” denotes the presence of a species recoded only in ad libitum observations. Bird nomenclature is based on Piacentini et al. (2015). Species O N D J F M A MJ J A S Group* Anhimidae 1,6 Anhima cornuta x WS Anatidae 5,6 Dendrocygna bicolor 50 44 71 24 5 12 x x 4 100 337 9 WS Dendrocygna viduata 85 148 12 6 x x x x xx WS Dendrocygna autumnalis 43 47 26 21 2 5 x x 9 x 18 5 WS Cairina moschata x1 WS Sarkidiornis sylvicola xxxxx WS Amazonetta brasiliensis 20 1 3017 6 14 4 1017311016 WS Anas bahamensis 20 x 1 10 1 x 2x WS Anas versicolor 25 11 299 x x 2252 x WS Netta erythrophthalma 20 14 x x 5 1 xWS 4,5,6 Netta peposaca 16 8 10 35 10 x x 1 52 9 103 4 WS Nomonix dominicus xx x WS Podicipedidae Tachybaptus dominicus 12 DP Podilymbus podiceps 3333247 14 663 DP Ciconiidae 1,5 Jabiru mycteria 12 19 8 x x x x LP Mycteria americana 26 130 129 99 15 x x 1 LP Phalacrocoracidae Nannopterum brasilianus 662 119 9 2 25 42 106 71 59 86 130 103 DP Anhingidae Anhinga anhinga x2x4 3 3 1 1 1x1 DP Ardeidae Tigrisoma lineatum xxxx x 1 xxxx 2 LP Ixobrychus involucris xEM Nycticorax nycticorax x 423415 582533 14 LP Butorides striata x x x 42 25 143145 LP Bubulcus ibis 2154 xx x LP Ardea cocoi 11 35 12 17 22 30 19 14 29 37 11 28 LP Ardea alba 83 79 49 27 11 122 92 42 136 409 16 79 LP Syrigma sibilatrix x 1LP Egretta thula 207 110 11 9 6 48 60 19 12 12 2 58 LP Egretta caerulea xx xx LP Threskiornithidae Plegadis chihi 28 x xPW Mesembrinibis cayennensis x x2x xx PW Phimosus infuscatus x x2x x2x x1 4 PW Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Species O N D J F M A MJ J A S Group* Theristicus caudatus 2xx PW Platalea ajaja 40 22 10 x x x 1 PW Pandionidae Pandion haliaetus 11 1 LP Accipitridae 1,6 Circus buffoni x1 1x 2 1 PW 5,6 Rostrhamus sociabilis x1x 1x x x PW Aramidae Aramus guarauna 1 1x x x x1x1 x PW Rallidae Aramides cajaneus xx EM Laterallus melanophaius 4 x 1413266 16 11 EM Laterallus exilis 111 x xx xEM Porzana flaviventer 31 xx 1 EM Mustelirallus albicollis xxxx xxxxx EM Pardirallus maculatus xx x EM Pardirallus nigricans xxxx xxxxx EM Pardirallus sanguinolentus xxxxxxx 1 xxx EM Gallinula galeata 468 237 117 45 60 53 21 42 36 35 89 58 WS 5,6 Porphyrio martinicus 3271 10 4524 x 25 WS Charadriidae Charadrius semipalmatus x SW Recurvirostridae Himantopus melanurus 393 53 3 xxxxxxxxx PW Scolopacidae Gallinago paraguaiae xPW Tringa flavipes 13 xx SW Tringa melanoleuca 86 1 SW Tringa solitaria 5 xx SW Calidris melanotos 2SW Calidris fuscicollis x SW Jacanidae Jacana jacana 40 48 26 48 43 46 31 42 51 50 111 68 WS Sternidae Phaetusa simplex 2 xxx x 3 x DP Rynchopidae Rynchops niger 1 xx 1 x xxx DP Alcedinidae Megaceryle torquata x x x 2 x 11112 x DP Chloroceryle amazona x x2x x x x1x x DP Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Species O N D J F M A MJ J A S Group* Furnaridae Certhiaxis cinnamomeus xxxxxx xxxxxx - Cranioleuca vulpina xx - Tyrannidae Pseudocolopteryx sclateri 11 x1x - Fluvicola albiventer xxx 1 xxxxxxxx - Fluvicola nengeta x xx 2 xxxxxx - Arundinicola leucocephala x x1x x xx x - Gubernetes yetapa x - Hirundinidae Tachycineta albiventer 1 xxx 2 x 1 - Donacobiidae Donacobius atricapilla 1x x1x1x1 - Icteridae Agelasticus cyanopus xxxx x xx - Chrysomus ruficapillus xxxxxxxxxxxx - Pseudoleistes guirahuro xxx - – Threatened to extinction (São Paulo 2014) – Near Threatened (São Paulo 2014) – Data Deficient (São Paulo 2014) – Migratory species (Piacentini et al. 2015) – Short-distance migrant species (Antas 1994, Sick & Barruel 1997, Sigrist 2009) – Species with evidences of reproduction * – Functional groups generated in the cluster analyses (PW = Probing waders, SW = Small waders; LP = Large piscivores, DP = Diving piscivores, EM = Emerged macrophytes, and WS = Water surface). that nest in the Northern Hemisphere and spend only that mostly capture fish and other prey while foraging in a few days in Tanquã, and four species make seasonal shallow areas near the shore, without diving, (4) Diving movements throughout the country (Appendix I). piscivores: birds that dive for fishes and other prey, (5) Twenty-one species (29.5%) were recorded in more birds that forage on Emerged macrophytes: small and than 90% of the sampling months, being considered inconspicuous species (mainly rails) found in the dense residents, while 67.8% of the species were recorded in at vegetation that surround the water, and (6) birds that least half of the samplings, thus considered common in feed on the Water surface: a group congregating species the area. Eighteen species are short-distance migrants in that forage by filtering organisms in the water surface, or Brazil, and eight are classified as non-reproductive long- spend most of the time floating in the river surface while distance migrants, although we found more than one searching for food (Table 1). Large piscivores and birds nest and several juveniles of one of these species (Netta that feed on the Water surface were the most abundant peposaca). Except from N. peposaca, which was present all groups, accounting for 87.3% of the total abundance. year round, the other migratory species visited the area The water depth varied monthly from 5.3 m to 9.6 from October to February (Table 1). m, while monthly bird abundance ranged from 294 to The cluster analysis generated six functional groups 2411 individuals, and species richness varied from 24 to 35. with a cophenetic correlation coefficient from the Richness was not correlated to water depth (R = 0.016, P = distance matrix of 0.73. These groups where classified 0.4), but total bird abundance was negatively correlated to it as (1) Probing waders: species that forage mainly on (pseudo R = 0.36 P = 0.041) (Fig. 2, Table 2). The functional the shores and exposed mudflats, feeding primarily groups responded differently to fluctuations in water depth. on macroinvertebrates in the mud, (2) Small waders: The abundances of Water surface, Large piscivores and mainly sandpipes and plovers, this group comprises small Probing waders were negatively correlated to water depth, migratory species (up to 60 cm) that eat small invertebrates while models for Emerged macrophytes and Diving piscivores picked out of the mud or soil, (3) Large piscivores: species groups were non-significant (Fig. 3, Table 2). Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Table 2. Analysis of deviance table for the GLM testing the relationship between the total bird abundance and abundances of functional groups with the water depth. Residual Residual df df Deviance F P(>F) Deviance Null 11 3964.50 Total abundance 1 1463.80 10 2500.70 5.48 0.041 Null 11 696.76 Large piscivores 1 557.95 10 138.81 44.45 <0.01 Null 11 2019.55 Probing waders 1 803.11 10 1216.40 13.77 <0.01 Null 11 24.49 Diving piscivores 1 2.53 10 21.97 1.29 0.283 Null 11 36.18 Emerged macrophytes 1 7.08 10 29.11 2.39 0.153 Null 11 1893.00 Water surface 1 677.89 10 1215.10 4.68 0.055 2006) and 27 species (Rodrigues & Michelin 2005) were recorded in Minas Gerais state, while in São Paulo state, 51 (Crozariol 2010), 49 (Schunck et al. 2016), and 39 (Schunck & Rodrigues 2016) water-dependent species were found. Apart from the high bird species richness, Tanquã is important for rare, migratory and locally threatened species. Eight threatened (Anhima cornuta, Sarkidiornis sylvicola, Ciconia maguari, Jabiru mycteria, Busarellus nigricollis, Circus buffoni, Phaetusa simplex and Sternula superciliaris) and five “Near Threatened ” species (Nomonyx dominicus, Mycteria americana, Tryngites subruficollis, Pluvialis dominica and Gallinago undulata) (São Paulo 2014) occur at the area (Table 2). Other noteworthy bird records are (1) N. peposaca, a migratory species that nests west of Brazil or in the south of the country (Antas 1994), but was found all year around and reproducing in Tanquã, the first place outside of the south region of Brazil w here Figure 2. Quasi-Poisson regression model showing the response reproductive activities were recorded. (2) M. americana of total bird abundance to variation in the water depth. was recorded in 50% of surveys and in flocks of up to 150 individuals. This species also migrates through t he Paraná River Valley, staying in the Pantanal from November to DISCUSSION April where it breeds and then migrates to feeding areas in Rio Grande do Sul, south Brazil (Antas 1994). This is The importance of Tanquã for birds the same period when the species was found in Tanquã, but we could not find any signs of reproduction. Many of Compared to other wetlands in southeast Brazil, Tanquã the birds we recorded were juveniles that could be using have the highest number of water-dependent bird the area only for foraging. (3) Pseudocolopteryx sclateri, a bird discovered in the state of São Paulo only in 2009, species, representing 53.3% (or 69.6% if we add the species reported in the literature and online data) of all with pairs engaging in mating activities at Tanquã. (4) 135 wetland species found in the Atlantic Forest Biome Porzana flaviventer, a bir d common in Tanquã, but rarely (Moreira-Lima 2013). In a natural coastal lagoon in Rio seen in other parts of Brazil whose biology and regional de Janeiro state, 46 water-dependent bird species were movements are not yet understood in the country. Only 29.5% of the species recorded were residents, recorded (Tavares & Siciliano 2014), 37 (Faria et al. Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Figure 3. Quasi-Poisson regression model showing the response of the abundances of different bird functional groups to variation in the water depth. while several species make seasonal movements within the sites (“convenience store”) are structurally heterogeneous Brazilian territory, migrating through the Paraná River sites with freshwater and a variety of food resources where Valley, from south Brazil to the Pantanal region (e.g., J. birds can rest briefly (two days or less) and easily replenish mycteria; Antas 1994). Valente et al. (2011) produced the body reserves. Type 3 sites (“full service hotel”) are first catalogue of important areas for Nearctic migratory extensive areas suitable for migratory birds, where all the birds in Brazil, highlighting six sites in southeastern Brazil. necessary resources are relatively abundant and available. The number of species classified as non-reproductive Type 3 sites can sustain many individuals of many species long-distance migrants (according to Piacentini et al. that can remain there for weeks allowing them to achieve 2015) recorded in our censuses (8 species) is similar to the physiological conditions necessary to continue their the average species richness recorded at these areas (8.14 ± migration to the next stop or final destination. We believe 3.02 species), but our literature review raises this number that Tanquã can be classified as a type 2 or 3 stopover site, to 16 species, thus corroborating the importance of because large agglomerations of species from the families Tanquã for Nearctic birds in Brazil. Scolopacidae and Charadriidae were found during their Mehlman et al. (2005) analyzed the importance wintering periods in Brazil. These families comprise several of migratory passerine stopover sites in the Northern migratory species that require newly exposed mud to forage Hemisphere and generated a useful scale for their (Sick & Barruel 1997). The energy accumulated in sites like categorization. Although designed for terrestrial birds, Tanquã is likely important for these species to return to the Kirby et al. (2008) considered this typology adaptable to Northern Hemisphere, as food obtained in stopovers sites other groups of migratory birds. Type 1 sites (“fire-escape”), provides energy to migration (Davison & Evens 1988), and usually small, isolated habitats surrounded by unsuitable the increase in nutritional reserves is essential to further habitat that are rarely used but vital in emergencies. Type 2 reproductive success (Hvenegaard & Barbieri 2010). Revista Brasileira de Ornitologia 25(3): 2017 *  "+ , # # # # ! $&' !" Bird species in a floodplain with reversed flood pulse Robinson & Pizo Seasonality in the water depth and its alteration of the current flood cycle by the construction effects upon birds of the planned new dam (called Aproveitamento Múltiplo Santa Maria da Serra) carries a real risk of threatening several elements of the local bird community. In the rainy season, the water level falls because the In summary, Tanquã is a large floodplain with power plant is operating and the water is flowing fast high environmental heterogeneity offering a mosaic of out of Tanquã. As a result, the higher abundance of birds habitats, ranging from exposed mudflats to open water observed in this period may be due to the availability of variable depth, with remarkable temporal changes in of shallow waters, which increase prey concentrations environmental characteristics. The seasonal fluctuation (Macedo-Soares et al. 2010, Tavares & Siciliano 2014), of the water level, heterogeneity of habitats, and the and recently exposed mudflats occurring concomitantly size of the floodplain may be the reasons why so many with the arrival of migratory species that feed on this waterbirds species occurring in high abundances were microhabitat. Shallow waters and recently exposed recorded, as these are among the main factors influencing mudflats are likely scar ce in the region in the rainy season, bird abundance in wetlands (Paracuellos & Tellería 2004). making Tanquã an important feeding site for birds. Any further infrastructure project that would maintain The abundances of bir ds of the Water surface, Large Tanquã permanently flooded will lead it to lose its ability piscivores, and Probing waders groups were negatively to support such a diverse community of waterbirds. correlated with the water depth. Species from the Water Apparently, the artificial flood regime imposed surface group forage by filtering organisms in the water by the Barra Bonita dam counteracted the damage surface; when the water level raises, water surface increases expected from the construction of the power plant. As and vegetation become scarce. Baschuk et al. (2012) such, the Tanquã “happy accident” showed that, by observed that it is easier for dabbling ducks to access reproducing natural cycles of floodplains during their submerged aquatic vegetation in shallow waters. Lack of operation, existing and future power plant projects vegetation may also increase the risk of duck predation. may take actions to transform or maintain their areas Furthermore, shallow lakes were considered preferred of influence as important habitats for the threatened habitats for ducks in previous studies (Paszkowski & aquatic bird community. Future studies need to focus on Tonn 2000, Tavares et al. 2015). The Large piscivores better understanding such actions, which likely includes group may be influenced by water depth because of their regulatory provisions foreseeing the establishing of a foraging behavior, as they tend to capture fish in shallow monomodal flood-pulse when possible. As different bird areas near the shore. When the water level rises it gets groups are differently influenced by the water level and more difficult to capture their prey due to an in crease in its variation, maintaining a monomodal and annual flood the dimensional space (Ntiamoa-Baidu et al. 1998, Lantz pulse contributes to the maintenance of a high species and et al. 2010). The water depth has also a strong influence in functional diversity in wetlands. When appropriate flood- vegetation cover (Padial et al. 2009, Ma et al. 2010) that pulse regulation is not an option, then the creation of may act as a barrier reducing visibility to detect predators. habitat heterogeneity, such as shallow shorelines or island Species in the Probing waders group have a preference development should be recommended as mitigation for foraging mainly on the shores and exposed mudflats and restoration actions in response to dam construction (Tavares et al. 2015), a microhabitat that temporarily (Desgranges et al. 2006). As smaller dams probably offer disappear with the rise of the water level. more manageable options and opportunities, they should Abundance of Emerged macrophytes and Diving be taken into consideration when establishing investment piscivores groups were not correlated with water depth. priorities and financing towar ds new dam projects, either However, the Emerged macrophytes group is composed for power generating or any other uses. of several small and inconspicuous species that are recorded mainly by their vocalizations. Because these species sing more frequently during the reproductive ACKNOWLEDGEMENTS period, their abundance may have been underestimated during other seasons. Although the abundance of Diving We thank V. Bortolotti, B. Alleoni, M. Dourado, M. piscivores was not significantly related to the river depth, Afonso, R. Machado, M. Flores, and especially C. Gussoni previous studies have shown that aerially foraging and for helping in the fieldwork. We also thank F. Godoy w ho diving piscivores could be favored by higher water levels first introduced us to the area, and t he birdwatch guide G. Pinto for keeping us updated on Tanquã news. We (Paszkowski & Tonn 2000, Paillisson et al. 2002, Baschuk are also grateful to the boatman Ivanildo for logistical et al. 2012). Our results show that any rise in the water support and the people from the Tanquã community for level can negatively affect bird abundance, especially for welcoming us so warmly. We are grateful to the National species in the Large piscivores, Water surface and Probing Council for Scientific and Te chnological Development waders functional groups. Therefore, the predicted Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo Ma Z., Cai Y., Li B. & Chen J. 2010. Managing wetland habitats for (CNPq) for the MSc. scholarship to V.R. M.A.P. receives waterbirds: an international perspective. 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APPENDIX I A complete list of bird species recorded in Tanquã based on field samplings, bibliographic records, online records published in Wikiaves, IBC and EBird. Bird nomenclature is based on Piacentini et al. (2015). EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Anhimidae Anhima cornuta xx x R T Chauna torquata xR DD Anatidae Dendrocygna bicolor xx x x R Dendrocygna viduata xx x x R Dendrocygna autumnalis xx x x R Coscoroba coscoroba xR Cairina moschata xx x x R Sarkidiornis sylvicola xx x x R T Amazonetta brasiliensis xx x x R Anas georgica xR Anas bahamensis xx x x R Anas versicolor xx x x R Anas discors xx VN Anas platalea xVS Netta erythrophthalma xx x R Netta peposaca xx x x VO Nomonyx dominicus xx x R NT Podicipedidae Tachybaptus dominicus xx x x R Podilymbus podiceps xx x R Podicephorus major xR Ciconiidae Ciconia maguari xR T Jabiru mycteria xx x R T Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Mycteria americana xx x x R NT Phalacrocoracidae Nannopterum brasilianus xx x x R Anhingidae Anhinga anhinga xx x x R Ardeidae Tigrisoma lineatum xx x R Ixobrychus involucris xx x R Nycticorax nycticorax xx x x R Butorides striata xx x x R Bubulcus ibis xx x x R Ardea cocoi xx x x R Ardea alba xx x x R Syrigma sibilatrix xx x x R Egretta thula xx x x R Egretta caerulea xx x R Threskiornithidae Plegadis chihi xx x x R Mesembrinibis cayennensis xx x R Phimosus infuscatus xx x R Theristicus caudatus xx x x R Platalea ajaja xx x x R Pandionidae Pandion haliaetus xx x x VN Accipitridae Circus buffoni xx x R T Busarellus nigricollis xx R T Rostrhamus sociabilis xx x x R Aramidae Aramus guarauna xx x x R Rallidae Aramides cajaneus xx x x R Laterallus melanophaius xx x x R Laterallus exilis xx x R DD Porzana flaviventer xx x R Mustelirallus albicollis xx x x R Pardirallus maculatus xx x R Pardirallus nigricans xx x x R Pardirallus sanguinolentus xx x x R Gallinula galeata xx x x R Porphyrio martinicus xx x x R Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Porphyrio flavirostris xR Fulica leucoptera xx R Charadriidae Pluvialis dominica x x VN NT Charadrius semipalmatus xx x VN Charadrius collaris xx R Recurvirostridae Himantopus melanurus xx x x R Scolopacidae Gallinago paraguaiae xx x x R Gallinago undulata xR NT Limosa haemastica xVN Actitis macularius xx x VN Tringa solitaria xx x x VN Tringa flavipes xx x x VN Tringa melanoleuca xx x x VN Calidris fuscicollis xx x x VN Calidris melanotos xx x x VN Calidris pugnax xVN Calidris subruficollis xVN NT Phalaropus tricolor xx VN Jacanidae Jacana jacana xx x x R Rostratulidae Nycticryphes semicollaris xR DD Laridae Chroicocephalus maculipennis xR Sternidae Sternula superciliaris xR T Phaetusa simplex xx x x R T Rynchopidae Rynchops niger xx x x R Alcedinidae Megaceryle torquata xx x x R Chloroceryle amazona xx x x R Chloroceryle americana xx R Furnariidae Certhiaxis cinnamomeus xx x x R Cranioleuca vulpina xx x R Tyrannidae Pseudocolopteryx sclateri xR Revista Brasileira de Ornitologia 25(3): 2017 Bird species in a floodplain with reversed flood pulse Robinson & Pizo EIA Censuses Status Conservation Other field Aproveitamento Internet Species Out/14 in status in São visits Múltiplo Santa Collections 2 3 -Set/15 Brazil Paulo Maria da Serra” Fluvicola albiventer xx x x R Fluvicola nengeta xx x R Arundinicola leucocephala xx x x R Gubernetes yetapa xx x x R Hirundinidae Tachycineta albiventer xx x x R Donacobiidae Donacobius atricapilla xx x x R Icteridae Agelasticus cyanopus xx x R Chrysomus ruficapillus xx x R Pseudoleistes guirahuro xx x R Species recorded in field visits performed before or after the censuses conducted between O ctober 2014 and September 2015. R = resident; VS = Seasonal visitor from the south of the continent; VN = Seasonal visitor from the Northern Hemisphere; VO = Seasonal visitor coming from west of the Brazilian territory (Piacentini et al. 2015). T = Threatened by extinction, NT = Near Threatened and DD = Data Deficient (São Paulo 2014). Revista Brasileira de Ornitologia 25(3): 2017

Journal

Ornithology ResearchSpringer Journals

Published: Sep 1, 2017

Keywords: bird functional groups; dam impacts; waterbirds; wetland management; wetlands

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