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Revista Brasileira de Ornitologia 25(2): 110 0 0–121. ARTICLE June 2017 Breeding biology of Pale-breasted Th rush Turdus leucomelas s (Turdidae) in the north of Atlantic Forest, Brazil 1,3 1,2 2 Nicolás Luciano Ruiz , Priscilla Sabino Amorim de Araújo , José Victor Fernandes de Lima a a , Pedro Vitor Silva 2 2 1,2 Ferreira a a , Lidiane Medeiros de Andrade & Mauro Pichorim Programa de Pós-Graduação em Ciências Biológicas, Universidade Federal do Rio Grande do Norte, 59090-002, Natal, RN, Brazil. Laboratório de Ornitologia, Departamento de Botânica e Zoologia, Centro de Biociências, Universidade Federal do Rio Grande do Norte, 59078-900, Natal, RN, Brazil. Corresponding author: nicolaslruiz@hotmail.com Received on 27 September 2016. Accepted on 11 July 2017. ABSTRACT: Reproduction is a key process in the life of organisms and represents high-energy cost to the parents, and often a tradeoff between survival and reproductive success. The breeding biology is an important aspect to be studied, which has inspired theories about bird life history evolution, such as the latitudinal gradient in the clutch size related to diff erent survival rates between the temperate and tropical regions. To contribute with the knowledge of breeding ecology of tropical birds we monitored two reproductive periods of the Pale-breasted Thrush Turdus leucomelas in the northeastern Brazil. The breeding period in the studied area occurred from December through April. We found the nests mainly on Facheiro cactus (Cactaceae) at 1.43 ± 0.35 m above the ground. Th ey were composed by roots, mosses, fungus mycelium, leaves, twigs, and a mix of fragmented vegetal material with soil and sand at the base. We found clutch sizes of three (n = 9), two (n = 3) and one (n = 1) eggs. The e ggs (n = 21) had mass of 5.1 ± 0.9 g and measured 26.6 ± 1.3 mm by 19.5 ± 0.5 mm. We observed 12 days of incubation and 14 days of nestling period. Th e Mayfi eld nest success in 2013 was 7.3% and in 2014 it was 4.5%, lower during the nestling period than during the incubation in both years. Our results show that T. leucomelas breeds in the area in the beginning of rainy season, when the frequency of occurrence of the migrant Turdus amaurochalinus is low. In addition, the low nest success observed may be a consequence of the localization of the studied area in the periphery of the species range, where limited resources probably result in reduced fi tness. KEY-WORDS: breeding success, egg, Mayfield, nest, northeastern Brazil, predation. INTRODUCTION alll. 2000). Basically, breeding depends on environmental and ecological circumstances throughout the annual cycle, necessitating the integration of these components Th e breeding knowledge of many tropical species remains poorly understood, where we do not know many basic to understand it (Sherry et alll. 2015). aspects, such as breeding season, nest characteristics, and Density-dependent feedback is not restricted to the same population, sometimes the increase of clutch size (Martin 1996, Stutchbury & Morton 2000). In addition, accurate estimates of nest success are necessary competitor presence can be an important driver of for improving our understanding of life-history strategies nesting. Interspecifi c competition can reduce breeding of tropical birds, and how those strategies may differ opportunities for subordinate species, resulting in lower among regions of the tropics and, also, from temperate fled gling rates and breeding density (Brazill-Boast et alll. zones. Reproduction is an important life history trait, 2011, Edworthy 2016). Competition-mediated habitat which aff ects both parental fi tness and population selection is widely believed to change the range of persistence (Berl et alll. 2014). It is regulated basically by a habitats or resources exploited by diff erent species (Sherry density-dependent feedback of adult population (Ricklefs & Holmes 1988, Dhondt 2012). The dominance is a 1997), area-dependent changes (Hoover et alll. 1995), primary factor in determining the realized niche among habitat structure (Zanette & Jenkins 2000), predator species and the community structure of an area (Dhondt assemblages (Thompson-III 2007, Klassen et alll. 2012), 2012, Thornton et alll. 2015). Thus, the seasonal variation food availability (Norris et alll. 2013), weather conditions in the frequency of occurrence of possible competitors (Collister & Wilson 2007) and nest parasitism (Budnik et may infl uence the breeding biology of a resident species. Revista Brasileira de Ornitologia 25(2): 2017 Breeding biology of Pale-breasted Thrush Tur dus leucomelas Ruiz et al. Additionally, different predator assemblages METHODS can change in distinct ways the reproductive success of the species. Predators are widely accepted as one Study area and species of the main cause of breeding loss in tropical bird populations (Lack 1954, Nice 1957, Ricklefs 1969, We monitored T. leucomelas s breeding biology in a plot Oniki 1979, Skutch 1985, Martin 1993). Nest of 550 × 550 m (30.25 ha) formed by an array of eleven predation influences reproductive strategies and rows and columns (50 m apart) located at Centro de nest-site selection (Martin 1995, Fontaine & Martin Lançamento Barreira do Inferno - CLBI I (Barreira do Inferno 2006). Consequently, nests are not randomly spread Launch Center, Brazilian Air Force) city of Parnamirim, o o across the environment, they are generally hidden in Rio Grande do Norte state, Brazil (05 54'S; 35 10'W, the habitat or in places difficult to access (Klopfer 1800 ha). Th e area has tropical coastal vegetation of 1963, Cink 1976, Ricklefs 1984, Sonerud 1985, Atlantic Forest sandbank (Scarano 2002) and classified Martin & Roper 1988). Nest concealment is known as semi deciduous forest of lowlands (Cestaro 2002). to improve nest survival for a variety of open-cup According to the Köppen (1936) classification system, avian species (Berl et al. 2014). The mechanism the climate of the region is AS (tropical and humid) for this is linked to the effect of vegetative cover with dry summer and rainy winter (IBAMA 2003). The on predator foraging efficiency (Li & Martin 1991, species T. leucomelas s is widespread in central, east and Segura et al. 2012). In consequence, birds in general north of South America (Sick 1997, Collar 2005), where have applied a plethora of behavioral techniques it inhabits pristine and disturbed humid forests, drier to avoid predation (Martin 1998, Clark & Shutler deciduous woodland, savannas, gallery woodland, and 1999, Rauter et al. 2002, Davis 2005). Therefore, anthropogenic environments (Collar & Garcia 2016). predators are a powerful ecological force shaping Th is common, non-threatened, species feeds mainly on many aspects of breeding biology and life histories fruits, arthropods, worms and small lizards (Collar & of birds (Clark & Wilson 1981). Garcia 2016). Another important environmental aspect for bird nesting is the precipitation, considered the main Data collecting and analysis weather condition perceived by birds at tropical areas (Boag & Grant 1984, Lloyd 1999, Hau et al. 2008). From 2010–2012 we determined the breeding period Th e onset of rains is associated with greater food of the species through records of the brood patches availability, either fruits or arthropods (Wolda 1978, occurrence resulting from a monthly demographic Grant & Boag 1980, Leigh-Jr. et al. 1996, Ahumada monitoring captures at the same study area. In 2013– 2001, Dantas et al. 2002). Presumably, this peak must 2014, we started the search for active nests one month also match with the greater breeding period energy before the breeding season and extended it to one month demand for egg production (Lack 1968, Ewald & after to avoid loss of any reproduction attempt. During Rohwer 1982, Martin 1987), parental care (Lack 1954) this time interval, we searched the whole study area or juveniles' dispersal (Morton 1971). Additionally, the for nests at least once a week in the early hours of the breeding season may be adjusted by molting process morning (05:00–10:00 h), using previous established that also occurs most often in the rainy season, when parallel paths at 50 m each (1050 h-observer in total). there is plenty of food supply (Poulin et al. 1992). We applied ordinary nest-searching methods through The Pale-breasted Thrush ( Turdus leucomelas) the area, looking for visual contacts and behavioral clues is a common species with breeding biology poorly of adults in breeding activity (vocalizations, territory studied (Collar 2005, Davanço et alll. 2013). Its large defense, carrying of nest materials or food for nestlings) occurrence in South America makes it a good model (Lopes & Marini 2005). We photographed, georeferenced species to investigate the variations of reproductive and described the active nests found according its stage traits among regions, habitats and climate conditions. (construction, incubation, nestling) and we monitored The present study contributes to this knowled ge them and the parental behavior at intervals between 2 describing the nesting biology of the species in the to 4 days until it became inactive. We manipulated the extreme of its distribution. In addition, our objectives contents once in the incubation stage (to measure and were to correlate some aspects of the reproduction of to weigh the eggs with a 20 g scale and 0.05 mm caliper) the species with habitat characteristics, precipitation and another time in the end of the nestling stage for and molt occurrence. We also discussed the eff ects of ringing. Th e description of the egg shape was based on the frequency of occurrence of the migrant congener Baicich & Harrison (1997) and the colors on Smithe Creamy-bellied Th rush (Turdus amaurochalinus), a (1975). Th e nestlings were marked with aluminum bands possible competitor in the area. provided by the Centro Nacional de Pesquisa e Conservação Revista Brasileira de Ornitologia 25(2): 2017 Breeding biology of Pale-breasted Thrush Turdus leucomelas Ruiz et al. de Aves Silvestres (CEMAVE/ICMBio), and with colored size 19 mm and fi ve shelves). Th ese records and the molt bands to follow them during the post-nestling period. occurrence were obtained from our monthly demographic We also monitored the nests after each breeding attempt monitoring program developed at the same study area. (successfully or not) in order to check reuse. We considered as incubation period the time between the laying and hatching of the last egg, and the RESULTS nestling period between the hatching of the last egg and when the last nestling leaving the nest. When we could During the monthly captures from demographic not register the exact day of an event, we assumed the monitoring, we found brood patches mainly between day at half of the period from the last research visit to January and April, with isolated records in November establish these periods. We considered successful nests (1), December (2) and May (1). Th us, the nest searching those that produced at least one nestling, and failure when and monitoring in the breeding seasons of 2012/2013 no eggs hatched (during incubation) or no off spring was and 2013/2014 occurred from December through April. produced (during nestling period). We estimated the During the first breeding season monitored, we recorded breeding success as a simple ratio of successful nests to 12 active nests, starting on 22 January and ending on 6 total nests found (apparent success, see Jehle et al. 2004) April 2013. In the second breeding season monitored, we and by using Mayfield's method, which estimates the recorded seven nests (from 12 January through 09 April mortality rate as a ratio between failures and observation 2014). period (Mayfield 1961, 1975). Since the nests were not Th e apparent success of nests was 10.8% and 12.5% monitored daily, we assumed as the exact date of loss or each year, respectively. Th e Mayfi eld success in 2013 was success the middle day between the last two consecutive 33.6% during the incubation, and 21.7% during the visits (following Mayfi eld 1975). Based on our results, we nestling period, resulting in the annual success of 7.3%. considered 12 days the incubation period and 14 days the In 2014 it was 49.7% during the incubation, and 9.0% nestling period to obtain the survival rates. during the nestling period, resulting in the annual success For each nest, we identifi ed the plant species where of 4.5% (Table 1, Fig. 1). Th e nest survival was lower it was built, the perpendicular distance of the superior during the nestling period than during the incubation ridge of the nest to the ground (height from the ground) for both years. Th e losses occurred on whole clutch, with and its position in the plant support (branches or main none individual losses registered. Among the 16 nests axis). We also measured the largest and smallest internal preyed, 87.5% (n = 14) presented intact structure, and and external diameter, depth and height of the nest using with no signs of destruction or displacement of the nest a ruler and caliper. Th e description of the nests followed original position. After the use of the nest (with success the proposal of standardization for Neotropical birds or loss), there was no reuse or second attempt in all nest (Simon & Pacheco 2005). At the end of each reproductive monitored. period, we collected and dried each nest to identify the All nests monitored (n = 19) were built above the material composition of the base and the incubation ground on vegetation (average height from the ground chamber. Th e dried materials were weighed using a digital of 1.43 ± 0.35 m, range between 0.86–2 m). Only once precision scale (0.01 g). the nest was built away from the main trunk of the plant The frequency of occurrence of the mi grant T. support (~95 cm), all others were built on forks of the amaurochalinus s was estimated monthly as the number of main axis. The nests were mainly built on the arboreal captures per 100 h-net (nets Ecotone® 18 × 3 m, mesh cactus called locally as Facheiro (Pilosocereus catingicola, Table 1. Nesting survival rates of Turdus leucomelas s obtained on 2013 and 2014 in the north of Atlantic Forest, Brazil. Exposure Nests Daily survival Mayfi eld Apparent Year Breeding period (days) lost (n) rate survival rate survival rate 2013 Incubation 46 4 of 7 0.9130 0.3355 0.4286 Nestling 58 6 of 8 0.8966 0.2170 0.2500 Entire breeding period 0.0728 0.1071 2014 Incubation 53 3 of 6 0.9434 0.4970 0.500 Nestling 19 3 of 4 0.8421 0.0902 0.250 Entire breeding period 0.0448 0.1250 Assumed 12 days for incubation period and 14 days for nestling period. Revista Brasileira de Ornitologia 25(2): 2017 Breeding biology of Pale-breasted Thrush Tur dus leucomelas Ruiz et al. Figure 1. History of nests of Pale-breasted Th rush (Turdus leucomelas s) monitored in 2013 and 2014 in the north of Atlantic Forest, Brazil (the numbers before each line means the date (day/month) when the nest was found; S = success and L = loss). Cactaceae) (57.9%; n = 11) followed by the Mangabeira chamber, composing 9.4% and 65.2%, respectively, tree (Hancornia speciosa, Apocynaceae) (26.3%; n = and present on all the nests. Leaves and mosses had 5), Myrtaceae (10.5%; n = 2) and Coccoloba mollis high representativeness in the bases and chambers of the (Polygonaceae) (5.3%; n = 1). During the incubation nests; while the woody plant twigs had presented at high period the apparent success of nests built on arboreal frequency on the bases. Instead, we recorded a few items cactus was 73% (8 of 11), and during nestling period it in a single nest, but with a signifi cant participation, as was 25% (2 of 8). Polycarpaea corymbosa a (Caryophyllaceae), Eriocaulaceae, Th e nest shape varied between circular and oval, with Facheiro, bromeliad infl orescence and, in a lesser ratio, the diameter ranging from 94–155 mm (mean largest Lycopodium sp. (Lycopodiaceae). external diameter = 132.0 ± 12.8 mm; mean smallest During the incubation period, we found clutch sizes external diameter = 113.3 ± 12.6 mm). The incubation of three (n = 9), two (n = 3) and one (n = 1) eggs. The clutch chamber was oval with highest and lowest diameters with just one egg was preyed a day after the last visit, and ranging from 60–90 mm (mean largest internal diameter probably it was not greater because the loss. Th e observed = 81.5 ± 6.8 mm; mean smallest internal diameter = eggs (n = 34) had coloration ranging from 168D Light 71.3 ± 4.9 mm) and its depth varied between 35–55 mm Sky Blue and 93 Robin's Egg Blue, with spots ranging (mean depth = 44.9 ± 5.4 mm). Th e nest height ranged from 121A Prout's Brown and 121B Brussels Brown. Th e from 82–170 mm (mean height = 102.6 ± 22.6 mm). spots concentration prevailed at rhombic pole, but we The general structure fits in the definition of “low cup / also recorded the fully spotted pattern, with intermediary base” following Simon & Pacheco (2005) (Fig. 2). stages (Fig. 3). The e ggs shape were intermediate between Th e nests were composed basically by roots, mosses, “Oval” and “Short-Oval” and they measured (n = 21): fungus mycelium, leaves, twigs, and a mix of fragmented length = 26.6 ± 1.3 mm (range 22.2–28.4 mm), width = vegetal material with soil and sand at the base (Table 19.5 ± 0.5 mm (range 18.0–21.1 mm), and mass = 5.1 ± 2). It is worth mentioning that the mycelia were found 0.9 g (range 4.2–6.1 g). At the nests in which we could in 83.3% of the nests, however this last mass may be follow the parental care during incubation (n = 3), we biased by the aggregate material added to it (e.g. sand, have always recorded the same parental (marked with mosses, leaves), which was not separated in order do not colored bands) at incubation duties and territory defense. compromise the integrity and identification. Also, it is We observed in four nests the maximum incubation noteworthy the representativeness of the roots, most period of 12 days (Fig. 1). used material at the nest bottom and the incubation During the nestling period, individuals of 0–3 Revista Brasileira de Ornitologia 25(2): 2017 Breeding biology of Pale-breasted Thrush Turdus leucomelas Ruiz et al. Table 2. Nest materials of Pale-breasted Th rush (Turdus leucomelas s) in the north of Atlantic Forest, Brazil ( Mass = sum of masses recorded for each item; % Relat = relative frequency of the item based on the mass; Freq = number of nests with the item). Whole nest Base Camera Material Mass (g) % Relat Freq Mass (g) % Relat Freq Mass (g) % Relat Freq Roots 302.16 0.1468 19 177.21 0.0947 17 124.95 0.6661 13 Mosses 82.66 0.0402 15 74.23 0.0397 15 8.43 0.0449 8 Fungus mycelium 64.89 0.0315 15 64.89 0.0347 16 0.15 0.0008 2 Leaves 49.53 0.0241 19 46.73 0.0250 19 2.80 0.0149 11 Bryaceae 47.12 0.0229 9 46.84 0.0250 8 0.28 0.0015 4 Woody plant twigs 40.80 0.0198 17 39.86 0.0213 17 0.94 0.0050 5 Araceae- Anthurium affi ni 23.42 0.0114 13 22.25 0.0119 12 1.17 0.0062 4 Bromeliaceae 15.64 0.0076 10 18.65 0.0099 9 Cattleya granulosa (root) 12.62 0.0061 3 12.62 0.0067 3 Gramineae 11.73 0.0057 10 10.19 0.0054 10 1.54 0.0082 2 Microgramma sp. 9.53 0.0046 4 8.19 0.0044 4 1.34 0.0071 2 Lichens 4.87 0.0024 1 4.43 0.0024 1 0.44 0.0023 1 Bromeliad inflorescence 3.01 0.0015 1 3.01 0.0016 1 Polycarpaea corymbosa 2.06 0.0010 1 2.06 0.0011 1 Eriocaulaceae 1.17 0.0006 1 1.17 0.0007 1 Pilosocereus catingicola 1.10 0.0005 1 1.51 0.0006 1 Unknown Vegetable Fiber 0.99 0.0005 3 0.99 0.0005 3 Lycopodium 0.77 0.0004 1 0.77 0.0004 1 Residues not identified * 1383.66 0.6724 19 1338.11 0.7155 19 45.55 0.2428 6 (*) Fragmented vegetal material, including soil and sand. Figure 2. Upper and lateral views of Pale-breasted Th rush (Turdus leucomelas s) nest recorded in the north of Atlantic Forest, Brazil. Revista Brasileira de Ornitologia 25(2): 2017 Breeding biology of Pale-breasted Th rush Turdus leucomelas Ruiz et al. Figure 3. Pale-breasted Th rush (Turdus leucomelas s) eggs spotted patterns ( ( (A-C) and shape (B) recorded in the north of Atlantic Forest, Brazil. Figure 4. Nestlings development stages of Pale-breasted Th rush (Turdus leucomelas s) in the north of Atlantic Forest, Brazil (A = 0–3 days; B = 4–5 days; C = 8–10 days; D = 11–12 days, age of ringing; E = 13–14 days). Revista Brasileira de Ornitologia 25(2): 2017 C N J Breeding biology of Pale-breasted Thrush Turdus leucomelas Ruiz et al. days old (n = 11) were naked with yellow skin and a nestlings at this age, and when they were being removed narrow spinal pteryla (dorsal tract) extending from nape from the nest, they held fast to the nest material. On two to rump with thin beige pinfeathers. The beak and the occasions, two of them jumped out of the nest in this tarsus were beige, the eyes closed, the abdomen skin situation, and they were returned after handling (Fig. was pale and wrinkled, and they begged for food (Fig. 4D). Between 13–14 living days the nestlings (n = 3) 4A). Between 4–5 days the nestlings (n = 10) began to had plumage similar of juvenile pattern, with beige and open their eyes and being more active (begging behavior gray spots at belly and upper cover feathers. The tarsus only with parents). Th e pinfeathers of the remiges were and beak were dark gray, with yellow gape flanges in the already visible as a narrow gray strip, but the tips had not later. At this age the nestlings leaved the nest (Fig. 4E), yet erupted (Fig. 4B). Between 6–7 days (n = 7 nestlings) and the maximum nestling period observed was of 14 the rectrices were visible, but without external tips. The days (Fig. 1, Nest 2). From all nestlings monitored (n = spinal pteryla had pinfeathers from head to rump, and 29), we recovered two after leaving the nest (17 days and the beak and tarsus were slightly dimmed. At age of 8–10 108 days after ringing), both showed juvenile plumage days (n = 5 nestlings) they always opened eyes during pattern, and were captured close to their nests (< 40 m). the visit, showing off dark brown iris, and they were Finally, through the demographic analysis of ringing curious with the surroundings, following movements. data from November 2010 until November 2014, we The pinfeathers of the spinal and ventral pteryla showed found in March a marked overlapping of brood patches unsheathed tips (larger on back), and also the remiges and molt (remiges, rectrices and both of them) and the began to show unsheathed tips (~2–5 mm, Fig. 4C). frequency on individuals captured with brood patch and Between 11–12 days (n = 5 nestlings) they had the body the months considered as breeding period (Fig. 5). Also ~70% covered with feathers, naked areas remained on central belly and fl anks, and the rectrices began to show through this data, we have recorded the highest frequency unsheathed tips. Th ey have tried to hide themselves of occurrence of the migrant T. amaurochalinus s in June with the researcher approaching, and after touched (2010 to 2014) in synchrony with the largest annual peak they moved up and fl apped the wings. We ringed the of rainfall (Fig. 5). X J O H N P MU P O MZ U B J MN P MU P O MZ X J O H B O E U B J MN P MU C S P P E Q B U D I E E D F F S S B V U V U M U Q P Q E B B P G G B J Z J Z T D D O O F E F V O V R R F F J S S ' ' 0 D U / P W % F D + B O ' F C . B S " Q S . B Z + V O + V M " V H 4 F Q N J H S B O U Q S F D J Q J U B U J P O N U J E Q O J J F U 0 D U / P W % F D + B O ' F C . B S " Q S . B Z + V O + V M " V H 4 F Q Figure 5. Annual conjugation between molt, brood patch, precipitation and migrant frequency of occurrence of Creamy-bellied Thrush T urdus amaurochalinus between 2010 and 2014 in the north of Atlantic Forest, Brazil. Revista Brasileira de Ornitologia 25(2): 2017 P D P D X Breeding biology of Pale-breasted Thrush Tur dus leucomelas Ruiz et al. DISCUSSION (Cebidae). Marmosets have been recorded widely in the literature as a common predator of bird nests, including We estimated a very low (< 10%) and unexpected nest T. leucomelas, and they have skills to prey without nest destruction (Pontes & Soares 2005, Lyra-Neves et alll. 2007, success for a tropical passerine. Previous estimate for T. leucomelas s was of 57% in the southeast of Brazil Alexandrino et alll. 2012, Vinhas & Souza-Alves 2014). (Davanço et alll. 2013), and for Turdus rufiventris s 35–41% Th erefore, the high level of predation in the studied area seems to constrain the nest productiveness of T. leucomelas in Argentina (Ferreti et alll. 2005). For temperate thrushes, like Turdus migratorius s and Turdus merula, the nest in this extreme site of distribution of the species. Another important aspect related to predation survival is ~30–50% (Knupp et alll. 1977, Cresswell 1997, Djemadi et alll. 2015). One explanation for the low nest in the area was the preference for nest building on the survival we found is the fact that the studied area is in the Facheiro cacti. This plant support was the most common periphery of the species range. In the extreme northeast and provided greater nest success during incubation. Brazil T. leucomelas s occurs in a narrow strip of forest close Probably, the protection given by its thorny stems and branches is the main beneficial characteristic of this plant. to the coast, and it is rarely found in the drier countryside covered by Caatinga vegetation. In addition, the numbers It is interesting to highlight that those nests on cacti were of nests that we found was low, even with a great effort more exposed and without concealment, even thus, this (1050 h in total). It seems that the studied area represents plant was the most frequent nest support. an extreme of distribution with few nest attempts and low Th e nest shape observed is consistent with what has been described by other authors for tropical thrushes nesting success. In many species, reproductive success is lower near the boundary of distribution, where limited (Euler 1900, von Ihering 1900, de la Peña 1987, Sick resources can result in reduced fi tness (Sexton et alll. 1997). However, we identifi ed the proportionality of the 2009). Usually, in the border of occurrence of a species used items, where fragmented vegetal material, including there are “sink populations” because of the environmental soil and sand predominated at the base and roots in the incubator chamber. It is worth mentioning the and ecological restrictions. It is possible that our results represent an example of this demographic limitation, plasticity of the species to adapt to the environment of its where the local productivity is perhaps not enough to surroundings. In the study area, there is little availability maintain the population level, an hypothesis which needs of mud, because the soil is predominantly sandy. Hence, to be tested. the base was composed of fragmented vegetal material, soil and sand mixed with fungal mycelium to promote Th ere are basically two factors that can potentially affect breedin g performance in birds: resources and the adhesion among these materials. In some cases, predation (Paradis et alll. 2000). We did not measure living roots of Cattleya granulosa a and Microgramma sp., the resource availability in our area, but considering the and mosses promoted the adhesion of the materials. occurrence of other thrushes, and many other frugivorous Therefore, the nests were quite compact and adhered to the substrate, regardless of the absence of mud. species, we suspect that food per se e is not a limitation. Actually, food limitation is much less important to life- Our records about height of the nest, eggs history in birds than suggested by traditional theory measurements (mass, length and width) and predominance (Ferreti et alll. 2005). However, predation seems to be of clutch sizes of three eggs were similar to those reported the main factor accounting for low nest success in our previously for this species (Carvalho 1957, Haverschmidt 1959, Camargo & Höflin g 1993, Collar 2005, Rodrigues study area. Th e majority of nest losses that we detected was caused by predation, probably by reptiles and birds, 2005, Marini et alll. 2007, Davanço et alll. 2013). It seems due the intact structure of the left nests. Birds and snakes that the clutch size in T. leucomelas does not vary much normally do not destroy the nest when they are preying, along its latitudinal gradient. Th e incubation period of while mammals do (Martin 1993, Woodworth 1997, 12 days that we observed was similar to other studies Marini et al. 2007). At the study area, there is a record of (Carvalho 1957, Haverschmidt 1959, Sick 1997, Collar a T. leucomelas s nestling predation by the snake Leptophis 2005, Davanço et alll. 2013). However, the nestling period ahaetulla a (Colubridae) (Ribeiro et al. 2014). Some other has been reported as longer in the literature (16–17 days, known bird predators recorded in the area were Oxyrhopus Carvalho 1957, Haverschmidt 1959, Sick 1997, Collar trigeminus s (Colubridae) (Alencar et alll. 2012), Caracara 2005, Davanço et alll. 2013). Maybe, the short nestling plancus s (Falconidae), Rupornis magnirostris s (Accipitridae), period that we recorded represents an adaptation against and Cyanocorax cyanopogon (Corvidae) (Sick 1997). For the high level of predation in the area. Sometimes young possible mammal predators, we frequently observed in should grow faster to reduce predation risk (Bosque & the area the opossums (Didelphidae) Didelphis albiventris Bosque 1995, Remeš & Martin 2002). Probably, the (Cáceres 2000) and Caluromys philander (Eisenberg & premature leaving from the nest is compensated by a Redford 1999), and also the marmoset Callithrix jacchus longer period of parental care of the fl edglings, behavior Revista Brasileira de Ornitologia 25(2): 2017 Breeding biology of Pale-breasted Thrush Turdus leucomelas Ruiz et al. already cited to other tropical birds (Russell et alll. 2004, variable possibly shaping the breeding period of resident Schaefer et al. 2006, Tarwater & Brawn 2010). We birds in the studied area, avoiding the peak frequency of could record at least one juvenile close to the nest site occurrence of this migrant. The breeding season can also after ~3.5 months. Inversely to our observations, several be adjusted by the molting process. In general, for birds multiple breeding attempts of T. leucomelas s during the of temperate zones the feathers molt does not overlap breeding period were related (Davanço et alll. 2013), even with the breeding period (Miller 1961, Payne 1969, four diff erent attempts for the same nest have been cited Foster 1975, Poulin et alll. 1992, Ralph & Fancy 1994, (Collar 2005). Tallman & Tallman 1997, Stutchbury & Morton 2000, Previous records have indicated that T. leucomelas Newton & Rothery 2005). However, for tropical regions, breeds throughout the year, but in different periods these events may occur simultaneously (Foster 1975). We among regions. The northernmost nest records (Surinam) saw some individuals with brood patches and molt, but are between November and May, avoiding the long rainy the peak of molting occurred at the middle of the rainy season in the region (April– –August, Haverschmidt 1959). season. Thus, there was overlap only at the end of the In Colombia, breeding occurs between January and breeding period. August (Hilty & Brown 1986). In Brazil there are nest Finally, our findings confirm some patterns o f records in the north between July and February (Oniki reproductive biology of tropical birds, as high nest & Willis 1983a, b), in the central between August and predation and low clutch size. However, the nest survival October (Antas & Cavalcanti 1988), in the southeast was low, and the breeding season was not extended. Th ese between August and January (Marini et al. 2007, Davanço happened probably due to the studied area situated in the et alll. 2013), and in the south in November (Belton 1994). peripheral distribution of the species, coupled with a high In Argentina, there is a record of nest in October (de la frequency of competitors and the infl uence of the rainy Peña 1987). Th ese records show that the reproduction of season. Th ese results show how poorly we understand the species starts at the end of the dry season or at the the ecology and limiting factors of bird populations in beginning of the rainy season, and rarely coincides with the South America. Th us, we emphasize the necessity the peak of precipitation in each region. Our observations to expand geographical breeding analysis in tropical in the northeastern of Brazil reinforce this idea, because environments. This is essential for the com prehension the reproduction occurred from December through April, of the factors that change the life history attributes before the annual peak of rainfall in the area. Probably, the across diff erent ecosystems. Knowing the importance of extension of the breeding season is more associated with limiting factors for a species, and when they operate, are the rain cycle in the region than other factors, like latitude. essential for the understanding of life history traits and We could not confirm the idea that the breedin g season the evolutionary ecology in the tropics. is extended in lower latitudes, as suggested in previous studies (Hemborg et alll. 2001, Davanço et alll. 2013). For example, we observed a breeding season of fi ve months in ACKNOWLEDGEMENTS our area (~6°S), while Davanço et alll. (2013) reported the same period in the southeast of Brazil (~23°S). However, Th is study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq in the central Brazil it seems to be shorter (five months, ) of the Antas & Cavalcanti 1988). We suggest, for this tropical Ministry of Science, Technology and Innovation of Brazil thrush, that the length of the breeding season is more (Scholarship Process 134336/2013-5). We are grateful influenced by rain than latitude . to the Centro de Lançamento Barreira do Inferno (CLBI) Actually, this pattern of integrating the rainy of the Brazilian Air Force for permission to access the season with the breeding period has been observed for study area, and to the Brazilian National Center for other tropical bird species (Lack 1968, Morton 1971, Bird Conservation (CEMAVE/ICMBio) for supplying Wyndham 1986, Martin 1987, Wikelski et al. 2000, the aluminum leg bands. The Graduate Program in Aguilar et al. 2000, Marini & Durães 2001, Mezquida Biological Sciences of Universidade Federal do Rio Grande & Marone 2002, Rubolini et alll. 2002, Duca & Marini do Norte (UFRN) provided institutional support. For 2011). The avoidance of the peak of precipitation can be the indispensable field assistance, we es pecially thank an adaptation to prevent nest loss, as mentioned for other Guilherme S.T. de Lima, Phoeve Macario, Than yria P.F. species (Medeiros & Marini 2007). Câmara, Julia G.B. Salgado, Tonny M. de Oliveira-Jr., Another important factor in our region is that the Marcelo C. Rodrigues, Priscila de C. Stedile, Damião V. rainfall peak is associated with the highest capture rates de Oliveira, Shirley M.N.T. Melo. We also thank Jomar of the migrant T. amaurochalinus. Probably, this species G. Jardim, Bruno T. Goto, Bruno C. Bellini, Charles G.D. competes for resources with T. leucomelas, and its massive Soares for their very useful comments and suggestions on presence in the area during the rainy season is another this manuscript. Revista Brasileira de Ornitologia 25(2): 2017 Breeding biology of Pale-breasted Thrush Tur dus leucomelas Ruiz et al. Collister D.M. & Wilson S. 2007. 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Ornithology Research – Springer Journals
Published: Jun 1, 2017
Keywords: breeding success; egg; Mayfield; nest; northeastern Brazil; predation
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