1206 Habitat heterogeneity and climatic seasonality structure the avifauna trophic guilds in the Brazilian Pantanal wetland

J.E.C. Figueira, F.A. Mourão, and A.S. Coelho

Abstract: Landscape heterogeneity and annual flood pulses characterize the Brazilian Pantanal, the largest floodplain in South America. The objective of this work was to explain spatial and temporal variations in the trophic structure of a assemblage consisting of 316 species of terrestrial and aquatic , out of which 88 are visitors. The food items potentially consumed by these species were combined into 12 trophic guilds and were compared based on habitats (terrestrial or aquatic), periods of the year, and visitor or resident species. Nonmetric multidimensional scaling was used to determine which trophic guilds characterize the different habitats and months. The habitats were separated into a gradient of trophic guild similarity ranging from woodlands to purely aquatic, with swamps and floodable fields in intermediate positions. Spe- cies that consume invertebrates and plants predominate in the terrestrial habitats, whereas the consumption of terrestrial and (or) aquatic invertebrates, vertebrates, and plants predominate in the aquatic habitats. The monthly similarities in trophic structure vary with rainfall, and the period of receding waters is characterized by an increase in the number of species in guilds that consume nectar, invertebrates, vertebrates, and (or) plant parts obtained or captured in the drying landscape and terrestrial habitats. Visitor species do not exploit new resource types; instead they accommodate themselves in the pre-exist- ing trophic guilds. Résumé : L’hétérogénéité du paysage et les poussées annuelles de crue caractérisent le Pantanal brésilien, la plus grande plaine d’inondation de l’Amérique du Sud. L’objectif de notre travail est d’expliquer les variations spatiales et temporelles de la structure trophique d’un peuplement d’oiseaux comprenant 316 espèces d’oiseaux terrestres et aquatiques, dont 88 sont des visiteurs. Les sources potentielles de nourriture consommée par ces espèces ont été regroupées en 12 guildes trophiques et comparées en fonction des habitats (terrestres ou aquatiques), des périodes de l’année et des espèces résidantes ou visiteu- ses. Un cadrage multidimensionnel non métrique a servi à déterminer quelles guildes trophiques caractérisent les différents habitats et mois. Les habitats sont séparés en un gradient de similarité de guildes trophiques à partir des zones boisées aux zones purement aquatiques, avec les marécages et les champs inondables en position intermédiaire. Les espèces qui consom-

For personal use only. ment des invertébrés et des plantes prédominent dans les habitats terrestres, alors que la consommation d’invertébrés terres- tres et(ou) aquatiques, de vertébrés et de plantes prédomine dans les habitats aquatiques. Les similarités mensuelles de structure trophique varient en fonction des précipitations; la période du retrait des eaux se caractérise par l’augmentation du nombre d’espèces dans les guildes qui consomment du nectar, des invertébrés, des vertébrés et(ou) des parties de plantes, obtenus ou capturés dans le paysage qui s’assèche et les habitats terrestres. Les visiteurs n’exploitent pas de nouveaux types de ressources; ils s’accommodent plutôt des guildes trophiques préexistantes. [Traduit par la Rédaction]

Introduction namic equilibrium in response to alternate periods of re- source depletion and super abundance. Some species closely Bird assemblages are subjected to a range, from moderate track these variations through short-term adjustments in their to strong, of annual climatic variability and erratic climatic foraging behavior, demography, and distribution; others can- extremes, like those attributed to El Niño events, which are not track closely these variations and a common strategy is sometimes combined with flooding, drought, and (or) fire (e. to escape through migration (Wiens 1991). Can. J. Zool. Downloaded from www.nrcresearchpress.com by MCGILL UNIVERSITY on 12/31/12 g., Grant et al. 2000; Frederick and Ogden 2001; Barlow et Many terrestrial and aquatic ecosystems are influenced by al. 2002; López de Casenave et al. 2008). Strong variations pulsed resources that temporarily attain higher than normal in resource levels and habitat quality typify temporally their levels and are exploited by highly mobile consumers that dis- environments. Consequently, they change, maintaining a dy- perse to other areas as the resource levels decline (Ostfeld

Received 9 February 2011. Accepted 16 September 2011. Published at www.nrcresearchpress.com/cjz on 2 December 2011. J.E.C. Figueira. Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Avenida Antônio Carlos 6627, Pampulha, CEP 30161-970, Belo Horizonte, MG, Brasil. F.A. Mourão. Programa de Pós-Graduação em Ecologia, Conservação e Manejo de Vida Silvestre(PG-ECMVS), Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, CEP 30161-970, Belo Horizonte, MG, Brasil. A.S. Coelho. Laboratório de Comportamento , Departamento de Zoologia, Instituto Central de Ciências, Universidade de Brasília, CEP 70910-900, Brasília, DF, Brasil. Corresponding author: José Eugênio Côrtes-Figueira (e-mails: [email protected] and [email protected]).

Can. J. Zool. 89: 1206–1213 (2011) doi:10.1139/Z11-099 Published by NRC Research Press Figueira et al. 1207

Table 1. Description of the habitat categories sampled by Cintra and Yamashita (1990).

Habitat Group Description Terrestrial (T) Semideciduous forest (SDF) Forest with scattered tall trees that lose entirely or partially their leaves during the dry season, usually in the form of levees locally called “cordilheiras” found above the flooding level Gallery forest (GAF) Forest with tall trees with abundant lianas and epiphytes, located along rivers and subjected to flooding Cerrado (CER) Savannah with shrubs and trees up to 3 m high, in a matrix of grasses and forbs Pasture field (PAS) Pasture and agriculture fields located in farms Aquatic (A) Floodable field (FLF) Fields of grasses and herbs subjected to submersion during flooding. They may contain small vegetation islands (murundus) and woodland islands Swamp (SWA) Permanently inundated swamps, covered by aquatic submersed and aquatic emergent vegetation Oxbows (OXB) Temporary sinuous water bodies linking rivers and bays, which sometimes dry out completely during the dry season River (RIV) Lotic sinuous water bodies, permanent even during the dry season Bay (BAY) Lentic, small to large circular or elliptical permanent water bodies surrounded by woodlands or Cerrado and rich in fish

and Keesing 2000). This is characteristic of the Brazilian Our four main predictions are as follows. (1) The trophic Pantanal, a mosaic ecosystem where annual floods and structure of the terrestrial and aquatic habitats will be very droughts, determined by the rising and receding waters of distinct, but common guilds are also expected because of the Paraguay River and its tributaries, are the driving forces their overlapping boundaries. (2) The trophic structure will (da Silva et al. 2001; Junk et al. 2006). Severe weather and vary with the amount of rainfall, which is lag-correlated with the unpredictable duration of the dry periods result in strong floodable area (Hamilton et al. 2002). (3) Receding waters pressures on the flora and fauna populations, favoring disper- will be characterized, mainly, by an increase in the number sive or migratory species capable of taking advantage of the of species in guilds that consume aquatic food types. abundant, yet seasonal and transitory resources within the (4) There will be no addition of new guilds with the arrival floodplain (Brown 1986). Recently, Nunes and Tomas of visitor birds, but only an increase in the number of species (2008) reported that the Pantanal shelters 553 bird species, per guild. of which 192 are migratory or nomadic. Multispecies con- centration of birds that feed on aquatic plants, fish, molluscs, Materials and methods worms, and (or) insects, such as ducks, egrets, sandpipers,

For personal use only. spoonbills, herons, kites, storks, anhingas, terns, and cormor- This study was based on a 3-year monthly record of 316 ants are more commonly seen, characterizing the Pantanal bird species from northern Pantanal published by Cintra and when the water level drops (da Silva et al. 2001; Antas and Yamashita (1990). Their study site is an environmental mo- Palo 2004; Junk et al. 2006). saic dominated by floodable fields, savannas, swamps, semi- There are not many studies correlating changes in wetland deciduous forests, with gallery forests also well represented avian trophic guilds in response to variations in water level or (Silva et al. 2000). Their surveys were conducted from 0600 flooded area, as that of Roshier et al. (2002) on waterbirds of and 0900 and (or) from 1600 and 1800 in nine habitat cate- the Australian arid zone, but among others, we found studies gories: semideciduous and gallery forests, cerrado, pastures, focusing on wading birds in the Florida Everglades (Bancroft rivers, bays, swamps, floodplains, and temporary oxbows et al. 2002; Russell et al. 2002), and even wading birds in (Table 1); the majority of them located in farms along the experimental ponds (Gawlik 2002). Studies relating changes Transpantaneira Road (16°24′25″S, 56°40′11″W and 17°21′ in both terrestrial and aquatic birds (e.g., Beja et al. 2010) 13″S, 56°45′17″W). The annual rainfall during the study var- are rare. In spite of its importance, no Pantanal bird invento- ied from 1231 to 1686 mm, and monthly rainfall was highly ries have yet been analyzed to describe spatial variations in correlated to the Pantanal long-term means (rS = 0.919, n =

Can. J. Zool. Downloaded from www.nrcresearchpress.com by MCGILL UNIVERSITY on 12/31/12 their trophic guilds or their temporal dynamics. 12, P < 0.001; Fig. 1A). The species richness and composi- In a previous study, Figueira et al. (2006) described the tion registered by Cintra and Yamashita (1990) are very sim- spatial and temporal variation in species richness of 316 Pan- ilar to those registered at the SESC Pantanal Reserve, in the tanal birds in a mosaic landscape, reporting a large number same region, by Antas and Palo (2004), and correspond to of habitat generalist species, with 89 being considered visi- 49% of the species reported for the whole of Pantanal (Tube- tors (migratory or nomadic); the majority of them associated lis and Tomas 2003). For each species, there was information with aquatic habitats. The main objective of the present study on habitat category and presence throughout the year. The is to test the hypothesis that the rainfall and flood pulse is a potential diets of each species were established based on An- strong driving force structuring the trophic structure of terres- tas and Palo (2004), Del Hoyo et al. (1992–2002), Del Hoyo trial and aquatic birds throughout the year. To do so, these et al. (2003–2005), and Sick (1997). The more frequent food 316 species were classified into coarse diet categories, a par- types were then combined into 12 trophic guilds (Table 2) tial indication of their feeding guild, as defined by Root and the trophic structures were defined by the number of res- (1967). Also, we explain variations in the trophic structure ident and (or) visitor species in each trophic guild. The clas- of this bird assemblage based on habitats. sification of species as visitors was based on their presence

Published by NRC Research Press 1208 Can. J. Zool. Vol. 89, 2011

Fig. 1. (A) Mean monthly rainfall (broken line) and flooded area (solid line) for the whole Pantanal (after Hamilton et al. 2002), as well as mean monthly rainfall during the study of Cintra and Yamashita (from 1982 to 1986; dotted line). (B) Relationship between flooded area and mean monthly rainfall for the whole Pantanal.

Table 2. Trophic guild codes and their respective food items.

Trophic cat. Food items Example TP Terrestrial plants Blue-fronted Amazon, Amazona aestiva (L., 1758) N Nectar (and small arthropods) Bananaquit, Coereba flaveola (L., 1758) TI Terrestrial invertebrates Unicolored Blackbird, Agelasticus cyanopus (Vieillot, 1819) TV Terrestrial vertebrates White-tailed Kite, Elanus leucurus (Vieillot, 1818) C Carrion Turkey Vulture, Cathartes aura (L., 1758) TIP Terrestrial invertebrates and plants Helmeted Manakin, Antilophia galeata (Lichtenstein, 1823) TIV Terrestrial vertebrates and invertebrates Red-legged Seriema, Cariama cristata (L., 1766) TAIV Terrestrial and (or) aquatic invertebrates and vertebrates Great Black Hawk, Buteogallus urubitinga (Gmelin, 1788) TAI Terrestrial and (or) aquatic invertebrates Limpkin, Aramus guarauna (L., 1766) AIV Aquatic invertebrates and (or) vertebrates Striated Heron, Butorides striata (L., 1758) AIP Aquatic invertebrates and plants Muscovy Duck, Cairina moschata (L., 1758) For personal use only. TAIVP Terrestrial and (or) aquatic invertebrates, vertebrates, and plants Purplish ( cyanomelas (Vieillot, 1818) Note: Trophic categories (Trophic cat.) are as follows: T, terrestrial habitats; A, aquatic habitats; P, plant parts (flowers, fruits, seeds, leaves, and (or) shoots); I, invertebrates; V, vertebrates; N, nectar; C, carrion.

for less than 9 months (Figueira et al. 2006). However, some were expected to promote predictable and gradual variations species classified as visitors are rare and (or) temporarily rare in guild structure. To test this prediction, we correlated the or reclusive during unfavourable conditions, as is the case of scores of NMDS axis I and II (trophic structures vs. months the Black-crowned Night-Heron (Nycticorax nycticorax (L., of the year) with mean monthly rainfall and mean monthly 1758)) (Antas and Palo 2004). flooded area for the whole of Pantanal, using Spearman’s Nonmetric multidimensional scaling (NMDS) was used to rank correlation (Zar 2009), after accounting for possible ordinate the nine habitat categories and months of the year time lags. The rainfall data for the studied period was meas- according to their ranked similarities in trophic structures. ured in the city of Cuiabá, the nearest meteorological station, This technique does not require multivariate normality and whereas long-term mean monthly rainfall and mean flooded

Can. J. Zool. Downloaded from www.nrcresearchpress.com by MCGILL UNIVERSITY on 12/31/12 yields the most accurate representation of underlying data area for the whole of Pantanal was based on Hamilton et al. structure (Clarke 1993). NMDS was performed using the au- (2002). topilot mode in PC-ORD. Prior to the analysis, we standar- Thereafter, the nine habitat categories were grouped into dized each trophic guild according to the number of species terrestrial (gallery and semideciduous forests, cerrado, and in the richest species guild, and used the Bray–Curtis dis- pastures) and aquatic (rivers, bays, swamps, floodplains, and tance. The number of dimensions was defined by the final temporary oxbows) habitats, and their trophic guilds were stress values that were compared with randomized runs of compared using a c2 test (Zar 2009) (for this test, TIV, TV, the data set (McCune and Grace 2002). PC-ORD plots habi- and C guilds were combined). The same test was used to tat categories or months in a one or multidimensional space compare the trophic guilds between resident and visitor spe- defined by their similarity in trophic structures. Additionally, cies (TIV, TV, and C guilds were combined) but could not be the trophic guilds that most characterize each habitat type or used to compare flooding (November–March) and the reced- month are also plotted. ing water seasons (April–October), owing to the large num- As flooding pulses rule the Pantanal dynamics, monthly ber of trophic guilds that needed to be added to attain variations in the amount of rainfall and (or) flooded area expected frequencies >5%.

Published by NRC Research Press Figueira et al. 1209

Results Fig. 2. Ordination of habitats defined by their trophic guilds along nonmetric multidimensional scaling (NMDS) axis I, plotted against Habitats and trophic categories ranked distances in the original space. For habitats and guild codes In the forest, there was a dominance of species that fed see Tables 1 and 2. upon TIP, TI, and TP. Together these three groups accounted for about 70% of the diet of birds in these habitats. Among the less frequently found guilds were those that included aquatic food items. The trophic structure of the cerrado and pastures was similar to that of forests, although TIP and TP were less frequent. As in the forests, aquatic food items were poorly represented. The aquatic habitats presented the lowest richness and the distribution of the guilds was different from that found in the previous habitats, with higher equitability. The addition of species is noticeable in the AIV, TAI, TAIV, and AIP guilds (supplementary Fig. S1).1

NMDS ordination for terrestrial and aquatic habitats and their associated trophic guilds The NMDS procedure recommended one dimensional sol- flooding and the receding water seasons, the higher differen- ution (final stress = 4.978, P < 0.020). The main axes, which ces were associated with the TAIV and N guilds (Fig. 4A). explain 97% of the total variance, clearly distinguish the woodlands (cerrado plus forests, with positive scores) from Trophic guilds of resident and seasonal visitor species the aquatic habitats (negative scores), whereas pastures, The trophic structure differed in the resident and visitor 2 flooded fields, and swamps are situated in between (Fig. 2). species (c½9 = 253.045, P < 0.01; Fig. 4B), except for AIP TAI, AIV, TAIV, AIP, and C captured underwater or in the and TAIVP (partial c2 test: P > 0.05). Among the visitors, banks of rivers, bays, and drying fields comprise the diets of there were neither TV nor C guilds, whereas N, AIV, and guilds associated with the aquatic habitats, whereas TIV,TV, TAI were more frequent. and N are associated with woodlands. A c2 test comparing the frequency of trophic guilds between the terrestrial and Discussion aquatic habitats was highly significant (c2 = 210.23, P < ½8 All predictions were confirmed. Not only did the guild tro- 0.001). For this test, the guilds TIV,TV, and C, and TP and phic structures vary according to landscape units, they also N, were added to obtain expected frequencies >5%. varied along the year, in response to rainfall and flooding

For personal use only. pulse, with the arrival or departure of visitor species that shift NMDS ordination for visitor trophic guilds through the from terrestrial to predominantly aquatic food types within a year pre-existing guild space. NMDS resulted in a two-dimensional solution (final stress = 3.073, P < 0.020). Axis I and II explained 66% and Spatial variations in trophic structure 31% of the variance, respectively. The counterclockwise loca- The landscape mosaic of the Pantanal floodplain explains tion of the months relative to these two axes is a clear cyclic the extreme richness and broad habitats used by most of the temporal sequence that could begin in November or Decem- resident and seasonal bird species, as suggested for the birds ber with the arrival of the rainy season and could end in Sep- of the Venezuelan Llanos (Vilella and Baldassarre 2010). tember or October at the peak of the dry season (compare Desgranges et al. (2006) also describe different bird assemb- with Fig. 1B). From the rainy to the dry months, there were lages associated with an environmental gradient in Lake On- increases in guilds that consume AIV, TAI, and TAIV cap- tario and the St. Lawrence River, ranging from marsh tured in aquatic and (or) nearby terrestrial habitats. Also no- habitats to seasonally floodable forest, determined by water ticeable is the increase in the N guild associated with the level and duration of flooding. Miller et al. (2004) found

Can. J. Zool. Downloaded from www.nrcresearchpress.com by MCGILL UNIVERSITY on 12/31/12 cerrado and forests (Fig. 3A). The scores of these guilds that the bird community along the Wiscosin River forest was were significantly correlated to axis I (Kendall’s t < 0.05, not related to landscape metrics, which should be associated n = 12), and as expected, the scores of axis I were correlated with naturally fragmented ecosystems, as occur in the Panta- with mean monthly rainfall during the study (rS = 0.937, P < nal. The Pantanal birds probably behave like those of Doñana 0.001; Fig. 3B). There was a decrease in similarity of guild wetland, Spain, redistributing themselves inside the landscape structure from January to October and a tendency to increase mosaic when searching for alternative or complementary onwards. The scores of axis I were also correlated to the feeding sites (Rendón et al. 2008). The common trophic mean flooded area, with a time lag of 2 months (rS = 0.863, guilds, such as TIP, TI, and TP, found on different habitats, P < 0.001). On the other hand, axis II was correlated with such as in forests and the cerrado, can be accounted for by a the mean flooded area (rS = 0.783, P < 0.01). large number of common species, resembling those described Although a c2 test could not be performed to compare the for some Brazilian Cerrado and Atlantic forest fragments guild trophic structures of the visitor species between the (e.g., Giraudo et al. 2008; Telles and Dias 2010). Pastures

1Supplementary Fig. S1 is available with the article through the journal Web site (http://nrcresearchpress.com/doi/suppl/10.1139/z11-099).

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Fig. 3. (A) Temporal ordination of the trophic guilds of visitor species along nonmetric multidimensional scaling (NMDS) axes I and II. For habitats and guild codes see Tables 1 and 2. (B) Variation in the similarity of trophic structures (Bray–Curtis index, taking January as a reference month) as a function of the mean precipitation. Lines connect the temporal sequence. Notice the reversed x-axis scale.

Fig. 4. (A) Trophic structure of the visitor species in the dry (April–October; gray) and wet (December–March; black) seasons and (B) trophic structure of the resident (black) and visitor (gray) species. For guild codes see Table 2. For personal use only.

and flooded fields comprise the transition habitats between Temporal variation in trophic structure the cerrado and forests and the aquatic habitats. They may As expected, the variations in the visitor trophic guilds are be occupied by fish and aquatic invertebrates during the correlated to the local and regional amount of rainfall and high water period, may surround gallery and dry forests, and flooding level (Hamilton et al. 2002), suggesting that in in some places are punctuated by small islands of cerrado northern Pantanal, trophic dynamics is also related to a

Can. J. Zool. Downloaded from www.nrcresearchpress.com by MCGILL UNIVERSITY on 12/31/12 vegetation (de Oliveira-Filho 1992). As a consequence, they broad-scale ecological process. From the rainy or flooding to harbor aquatic and terrestrial food consumers. For similar the dry or receding water months, there was a reduction in reason, mixed guild structures also characterize the Pantanal TP and TIV guilds and an increase in guilds feeding on ter- aquatic habitats. Cintra et al.(2007) reported a large percent- restrial and (or) aquatic invertebrates, vertebrates, and (or) age of birds associated with seasonally flooded lakes in the aquatic plants captured in the drying landscape and frontier Amazonia, gathering fish, insects, fruits in the neighboring terrestrial habitats that also attract nectarivorous birds. forests during the high waters. Baxter et al. (2005) highlights Thirty out of the 89 species of visitor birds included the importance of reciprocal across-habitat prey flux to main- aquatic food items in their diets, attesting to the importance tain trophic webs in riparian forest during unfavorable periods. and influence of flood pulses. The remaining visitor species These results confirm our first prediction that the trophic use the diversified vegetation array of cerrados, forests, and structure of the terrestrial and aquatic habitats are distinct fields, where the influence of rainfall prevails. It is possible but retain guilds in common. In addition, the habitats form a that in regular years, the assemblage presents a “core struc- gradient of trophic similarities determined by the competing ture” characterized by resident species that feed mainly upon influence of the terrestrial and aquatic vegetation and resources. TI, as well as TP and TAIV. To this core structure, there

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would be the temporary addition of visitor species belonging resident and seasonal species, indicating a high redundancy to the TI, TP, TIP, and N guilds. In addition, the increase in of mobile links, whereas others are poor. Thus, the functional the number of species belonging to AIV and TAIV guilds compartments in this ecosystem have different resiliencies during the receding waters confirms our third prediction. (Elmqvist et al. 2003). Several highly mobile waterbird species found in the Pantanal In the Everglades, supranormal nesting events may be as- also “boom and bust” annually in the Florida Everglades sociated with droughts and fire, leading to an increase in pri- (Frederick and Ogden 2001; Bancroft et al. 2002; Russell et mary productivity and (or) availability of fish. Most of the al. 2002), whereas frequent and (or) irregular “booms and birds recruited to breed on these occasions probably come busts” occur in the drylands of Australia (Roshier et al. from outside the area (Frederick and Ogden 2001). The Pan- 2002) and Kalahari Basin (Herremans 1999). tanal is also subjected to multiannual extreme drought events Open habitats in South America harbor some of the most (Hamilton et al. 2002) combined with intense fires (Junk et temporarily and diverse predator–scavenger avian assemb- al. 2006). During these events, the avian assemblage structure lages in the world (Bildstein 2004), with 28 species regis- undoubtedly will be disrupted longer than usual, and this tered in the study area. Fish, amphibians, insects, snails, and ecosystem relies on the re-establishment of the natural flood- bird eggs and chicks in large colonial nests are among the re- ing cycles, the integrity of its interior landscape units, and on sources that can be easily captured or consumed by the multi- neighboring biomes for its restoration. The Paraná River wet- species concentration of birds belonging to C, AIV, and lands (Antas 1994), and some of the largest South America TAIV guilds. These bursts of resources can occur during floodplains pulsing in synchrony or asynchrony with the Pan- flooding, receding waters, or both (Heckman 1999; da Silva tanal (Hamilton et al. 2002), are a potential sources of water- et al. 2001). In addition, man-made fires are very common birds after unfavorable periods. in the Pantanal, killing many slow-moving (Alho et However, severe changes in hydrology could be expected al. 1988), and raptors are attracted to large-scale fires where with future hydroelectric power plants and the Pantanal they feed along fire lines (Sick 1997). Besides, both the dry waterway project. Additionally, the Pantanal and its neighbor- season and the flooding season impose heavy losses on cattle ing biomes have been seriously threatened by intense defores- populations (Allem and Valls 1987). Contrary to our expect- tation and fires associated with agriculture and cattle farming ation, there was no species addition in the C guild and no (Harris et al. 2005; Junk et al. 2006; Alho and Sabino 2011). reference of scavenger concentrations in the literature on Pan- Therefore, the year 2010 was characterized by a large number tanal, whereas it has been reported for African savanna parks of big fires in and nearly 31% of the 133 133 fires oc- (Houston 1974). curred in the states of Mato Grosso and Mato Grosso do Sul, Conversely, the N guild was inflated, mainly during the where the Pantanal is situated, and 46% in the neighboring dry season, which is a time of high reproductive activity in states that harbor part of the Brazilian Cerrado, Atlantic, and cerrado trees (Oliveira 1998). Tubelis (2004) describe the Amazon forests (http://sigma.cptec.inpe.br/queimadas/; mixed-species flocks attracted by the nectar of cerrado trees, accessed 22 November 2010; satellite NOAA-15). As a re-

For personal use only. whereas Ragusa-Netto (2002, 2004) discusses the role of gal- sult, we can expect a fast decline in the populations of birds lery forests trees as a source of nectar and fruits. that comprise guilds such as N, TI, and TIP, and in the near Since the Pantanal maintains an extremely species-rich res- future, AIV and TAIV. ident bird assemblage in a mosaic landscape, it was not sur- The spatial patchiness in the trophic structure of the Panta- prising that the observed seasonal changes in guild structure nal bird assemblage is determined by resource types and were due to the addition of species into pre-existing guilds, abundance of their associated habitat units. Conversely, the confirming our last prediction. This result contrasts with that simultaneous numeric response of the visitor birds to the of López de Casenave et al. (2008), who studied a desert bird flood pulses and rainfall attest to the temporal component of assemblage where three out of five guilds had a seasonal oc- this strong bottom–up controlled assemblage. Together, these currence determined by the use of seasonal super abundant factors allow the coexistence of a large number of bird spe- – resources. Each region of the Pantanal has a different vegeta- cies, as predicted by the resource consumer models of Til- tion cover (Silva et al. 2000) and flooding dynamics (Heck- man (1986). man 1999), and as a consequence, the described distribution and temporal changes in the trophic structure cannot be gen- Acknowledgements

Can. J. Zool. Downloaded from www.nrcresearchpress.com by MCGILL UNIVERSITY on 12/31/12 eralized. Thus, time lags of several months are expected be- We are very grateful to several anonymous reviewers for tween the western regions under the more predictable their valuable contributions to the manuscript. We thank influence of the Rio Paraguai floodings and the northeastern P.L. Ruiz and R. Gough for the translation of the manuscript; regions under the more erratic influence of rainfall. J. Batista Pinho for checking the bird diets; and R. Parentoni Owing to their mainly generalist habit regarding habitat Martins and R. Cintra for suggestions that improved the use (Figueira et al.2006), both seasonal and resident bird spe- manuscript. cies provide links among different habitats in the Pantanal ecosystem, temporarily establishing new trophic and mutual- References istic interactions. Conversely, seasonal bird species link the Alho, C.J.R., and Sabino, J. 2011. A conservation agenda for the Pantanal to other Brazilian terrestrial ecosystems (Cerrado, Pantanal’s biodiversity. Braz. J. Biol. 71(Suppl. 1): 327–335. Atlantic, and Amazon forests) and to the Paraguayan Chaco, PMID:21537606. southern South America, and North America (Antas and Palo Alho, C.J.R., Lacher, T.E., Jr., and Gonçalves, H.C. 1988. 2004; Junk et al. 2006; Nunes and Tomas 2008). Some tro- Environmental degradation in the Pantanal ecosystem of Brazil. phic guilds found in the Pantanal bird community are rich in Bioscience, 38(3): 164–171. doi:10.2307/1310449.

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