Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae) in native and planted forests of southern Brazil

Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae) in native and planted forests... Iheringia, Série Zoologia DOI: 10.1590/1678-476620141044391398 Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae) in native and planted forests of southern Brazil André de Mendonça-Lima & Sandra M. Hartz Programa de Pós-graduação em Ecologia, Laboratório de Ecologia de Populações e Comunidades, Universidade Federal do Rio Grande do Sul., Av. Bento Gonçalves 9500, Prédio 43411/209, 91501-970 Porto Alegre, RS, Brazil. (mendoncalima@hotmail.com; corresponding author: sandra.hartz@ufrgs.br) ABSTRACT. Few studies have related the effects of silviculture practices to the behavior of bird species in the Neotropics. The present study examined the foraging behavior of Phylloscartes ventralis (Temminck, 1824) in a native forest and in silviculture areas of Pinus elliotti and Araucaria angustifolia with different structures and ages. We tested two general hypotheses: (1) areas of commercial forest plantation change the foraging behavior of P. ventralis in relation to native forest, and (2) the foraging behavior of P. ventralis in silviculture areas with understories (complex structures) is different from its behavior in areas without understory. The results showed that P. ventralis changed its foraging behavior depending on the type of forest, and on the presence of an understory in silviculture areas. Main changes involved the height and angle of substrate where the prey was captured. Phylloscartes ventralis showed the same set of attack maneuvers, with more maneuvers type in young Pinus planted without understory. The frequency of use of attack maneuvers was more similar in areas of silviculture with understory and in the native forest. The results highlight the importance of an understory structure and the utilization of native plant species in silviculture practices, to the foraging behavior of native bird species. KEYWORDS. Mottle-cheeked Tyrannulet, attack maneuvers, Araucaria angustifolia, Pinus elliotti, habitat structure. RESUMO. Comportamento de forrageio de Phylloscartes ventralis (Aves, Tyrannidae) em florestas nativas e plantadas no sul do Brasil. Poucos estudos têm relacionado os efeitos que práticas silviculturais exercem sobre o comportamento de aves neotropicais. O presente estudo analisou o comportamento de forrageio de Phylloscartes ventralis (Temminck, 1824) em uma floresta nativa e em áreas de silvicultura de Pinus elliottii e Araucaria angustifolia com diferentes estruturas e idades. Foram testadas duas hipóteses gerais: (1) áreas de plantio comercial alteram o comportamento e forrageio de P. ventralis em relação à mata nativa e (2) o comportamento de forrageio de P. ventralis em áreas de silvicultura com sub-bosque (estruturalmente mais complexas) é diferente do registrado em áreas sem sub-bosque. Os resultados demonstram que P. ventralis alterou seu comportamento de forrageio dependendo do tipo de floresta e da presença de sub-bosque em áreas de silvicultura. As principais mudanças envolvem a altura e o ângulo de substrato onde a presa foi capturada. Phylloscartes ventralis exibiu o mesmo grupo de manobras de ataque a presas, com um maior número de tipos de manobras em plantações jovens de Pinus sem sub-bosque. A frequência de uso de manobras de ataque a presas foi mais similar em áreas de silvicultura com sub-bosque e na floresta nativa. Os resultados destacam a importância do sub-bosque e da utilização de espécies nativas em práticas silviculturais para a manutenção do comportamento de forrageio de uma espécie de ave nativa. PALAVRAS-CHAVE. Borboletinha-do-mato, manobras de ataque, Araucaria angustifolia, Pinus elliottii, estrutura de hábitat. The structure of the habitat is an important factor Neotropics are usually done in forest ecosystems (Marini affecting the foraging behavior of animal species in & c alcanti v a , 1993; l a tt a & Wunderle , 1998; SoareS different areas (Mca a ruhtr & Paknai , 1966; Mreo Mdno , & a njoS , 1999; Mendonça -l iMa et al., 2004; Gabriel & 1979; Mrerua & Wtih Mero , 1981; Soba & h lo Me S, 1983; Pozi , 2005; Grebneer G & b reihci , 2005, among others) and Whelan , 2001). Alterations in the habitat structure can studies in silviculture areas or commercial forest plantations change the quantity and quality of available resources. are scarce, compared with native areas (Wunderle & Therefore, in altered habitats, species are forced to change l a tt a , 1998; PoMara et al., 2003; d ietSch et al., 2007). their foraging mode, or they may be replaced by other Assessments of foraging strategy patterns can help in the species (Grubb , 1979; k uSch et al., 2004). For instance, understanding of population and community dynamics, plant species with different foliage structures can affect because these patterns can influence the fluctuations of bird behavior, which in turn changes the habitat availability abundance and occurrence of a species in a particular and the resource exploitation (Franzeb , 1978; h olMeS & habitat (h t lo & k ir Mlleb , 2007; k relto & b or Wn , 2007). r nibo Sno , 1988). Among vertebrates, the foraging behavior Therefore, it is important to study the foraging behavior of of insectivorous birds is particularly well studied, mainly species in silviculture areas compared with native areas, in Europe and North America (h lo Me S & r nibo Sno , 1981; because tree plantations markedly alter the habitat, and Whelan , 2001). Although knowledge of the foraging these changes may lead to the local extinction of some behavior of bird species is a key question for successful species, whereas others may be able to colonize the altered management of populations, communities and ecosystems habitats. (l oše & k or Pli , 2007), the use of different tree species by The New World family Tyrannidae is one of the most insectivorous birds in tropical habitats has received little representative bird taxa and is among the most numerous attention (GreenberG & b ichier , 2005). in the world (Fitz Ptrick a , 1980, 2004; Sick , 1997). The Studies of the foraging behavior of birds in the forest-dwelling species of this family occupy all forest Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 392 Mendonça -LiMa & Htzar vertical strata (Sick , 1997). Less diverse at the ground (Podocarpus) (c âMara , 2003). layer, they increase in richness toward the upper layer of The sampling was performed in a native forest, and the forests (t roly ar & Fzti Pkcirt a , 1982; Skci , 1997). The in commercial forest stands of P. elliotti and A. angustifolia. Mottle-cheeked Tyrannulet (Phylloscartes ventralis) is a The P. elliotti plantations were distinguished by age and by common inhabitant of forests in south and southeast Brazil the presence of an understory: (1) 7-year-old plantations (b ont el , 1985; r oSário , 1996; Sick , 1997). It also occurs without understory (MP), (2) 25-year-old plantations in Argentina, Uruguay and Paraguay, and in a disjunct area without understory (OP), and (3) 27-year old plantations from northwest Argentina to Bolivia and Peru (r id Gy el with understory (PS). The 30-year-old A. angustifolia & t udor , 2009). The species is typically found in the plantation had an understory too (AP). All forest plantation middle to upper layers of forests and woodlands (b ont el , areas were contiguous (edge area) with the native forest 1985; Sick , 1997). The foraging maneuver commonly (NF). The native forest was located on hillsides and in the used by Mottle-cheeked Tyrannulet is the Sally-strike, a valley of the region, and had a dense understory. The mean very stereotyped maneuver and mainly characteristic of distance between the areas was 8 km, and between each area the small-bodied tyrant flycatchers ( Fitz Ptricka , 1980; in the same vegetation type was 2 km. Four sampling sites r eMSen & r obinSon , 1990). were marked, within each of five different forest treatments Assessment of the patterns of foraging behavior of (three Pinus plantations, the Araucaria plantation and the native bird species in the managed and native forests of native forest). The sampling sites were located at least the Araucaria forest ecosystem is particularly important to 100 m from any edge area, and were 500 x 100 m wide. fill a gap in knowledge about the impact of habitat change The overstory of each plantation was uniform in height; on bird populations in this region. Therefore, in this study however, there were differences between the treatments: we evaluated whether there are differences in the foraging the 27-year old P. elliottii plantations with understory and behavior of Mottle-cheeked Tyrannulets associated with 25-year-old P. elliottii plantations without understory had the habitat structure of planted and native forests. These the highest canopy heights (25 m and 23 m respectively); forests differ in their understory structure (Maçnodne -l i Ma followed by native forest (21.9 m), 7-year-old P. elliottii et al., 2014), when it is present (depending on the type plantations without understory (16 m), and 30-year-old A. of management) and this can lead to changes in foraging angustifolia plantations with understory (13 m). Understory behavior of insectivorous birds. We specifically tested the composition and diversity of planted and native forests are hypothesis that the frequency of foraging behavior variables described in Mendonça -l iMa et al. (2014). including prey-attack maneuvers, the type and angle of Data collection. Bird behavior was observed during substrate, the height at which foraging is conducted, and the breeding season of spring 2008 (between 3–10 October) the horizontal position where the attack was directed were and 2009 (between 2 October–11 November), starting 30 different in native and managed forests. min after sunrise; the total sampling effort was 199.74 hr. We used the focal-animal sampling (a t l Mnna , 1974) with MATERIAL AND METHODS modifications ( Marini & c alcanti v a , 1993; Mendonça - l i Ma et al., 2004). Individuals of Mottle-cheeked Tyrannulet Study area. The study was carried out in stands were identified and observed from a distance > 7 m, using of commercial plantations of Pinus elliottii and Araucaria binoculars. After the first sighting of an individual, the data angustifolia, as well as in areas of native forests on a recording started when it first attacked the prey, always commercial tree farm located in the Campo Belo do Sul taking care to not disturb the bird during foraging. When municipality, southern Brazil (1,000 m a.s.l.; 28°00’S, this was perceptible (e.g., attention directed to the observer, 50°49’W). The tree farm has an area of 14,200 ha, of which more frequent and nervous vocalizations), the distance 6,300 ha is part of a sustainable-use conservation unit. The of observation was increased and the data recording was remaining area is planted with different-aged stands of resumed after the bird resumed its usual behavior. Two or Pinus spp. The climate is typical of the southern Brazilian more observations of the same individual were considered highlands, with cool summers, no dry season, and frequent valid only when they were separated by a minimum interval severe frosts in winter (Köppen Cfb classification). The of 5 min, to assure independence of observations. mean annual temperature is 16°C (Sa tna c anira t a , 1986). We recorded data on the following behavior The characteristic regional native vegetation is variables: position of the individual in relation to the ground the Araucaria forest, which occurs mainly between 400 (height), attack maneuvers to prey (r eMSen & r obinSon , and 1,000 m a.s.l. along watercourses, valleys, hillsides, 1990), the substrate type where the attack occurred, the and grasslands on the plateau (k lein , 1978; ibGe, 1992). substrate angle, and the horizontal position in relation to The presence of A. angustifolia comprises the main the main axis of the focus tree. The position of the birds physiognomy; these trees occur in continuous forest in relation to the ground was defined by visual estimation habitats as well as in patches embedded in the plateau at 2-m intervals. The foraging substrate was classified grasslands (r a Mbo , 1951). Besides this species there as: green and dry leaves (included Pinus and Araucaria are several genera of laurel trees in this forest, such as needles), branch with a maximum diameter of 1 cm, branch Ocotea and Nectandra, and another native genera of conifer with a diameter thicker than 1 cm, and air. The substrate Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae)... 393 angle was divided into vertical (equal to or more than 45° in relation to the ground) and horizontal (less than 45° in relation to the ground) (Minira & c itnacla v a , 1993). When the individual bird attacked a prey on leaves or branches, the horizontal position in relation to the central axis of the focal tree was divided into three equal parts and defined as proximal, medial or distal (Mac a thurr , 1958). Statistical analyses. We evaluated the sampling effort by the analysis of cumulative estimates of prey attack- maneuver frequencies. In order to analyze the patterns of foraging behavior, we constructed a frequency matrix of sampling units and various classes of attack maneuvers, heights, foraging substrates, angles, and the position in relation to the central axis of a focal tree. Therefore, we consider a sampling unit within each treatment was composed by the frequency of set of six consecutive records of behavioral variables. The variation in the composition of behavioral-variable frequencies between forest treatments was analyzed by performing a Permanova based on a Gower or Euclidean distance (for heights analysis) dissimilarity matrix between sampling units. The age of the stands and the presence of understory were used as blocks in the analysis. The comparison between groups of sampling units belonging to the forest treatments was based on a sum of squares between groups as test criterion – Qb statistics (My anl , 1991, 1994; Pillar & o rlóci , 1996). The results are interpreted similarly to those in an ANOVA table. Significant differences between treatments were based on a P-value <= 0.05. A Principal Coordinates Analysis (PCoA) was carried out (using chord distance) to visualize the pattern of distribution of foraging behavioral variables within treatments. All data were analyzed in the MULTIV 2.63 statistical package (Pillar , 2006). RESULTS A total of 265 observations of Mottle-cheeked Tyrannulet foraging behavior were made during the study. The highest frequency of observations occurred in 30-year- old A. angustifolia plantation with understory (1.93 obs./ hr), followed by 27-year old P. elliottii plantations with understory (1.55), native forest (1.51), 7-year-old P. elliottii plantations without understory (1.25), and 25-year-old P. elliottii plantations without understory (0.98). Therefore, the treatments without understory showed the lowest frequency of observations. The mean height of foraging differed between areas (P = 0.001) and was smaller in the Pinus plantations with understory (Fig. 1). Mean height was 18.95 m in 25-year-old Fig. 1. Distribution of foraging-height class frequencies of Mottle-cheeked P. elliottii plantations without understory (SD = 2.99) and Tyrannulet in native and plantation forests. Legends: NF (native forest 12.01 m (SD = 2.29) in 7-year-old P. elliottii plantations more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria without understory, while in plantations with understory angustifolia with understory, n = 53), PS (25-year-old plantations of Pinus elliotti without understory, n = 52), OP (25-year-old plantations the mean height was 4.36 m (SD = 2.65) in 27-year old of P. elliotti without understory, n = 59), MP (7-year-old plantations of P. elliottii plantations with understory and around 9.00 m P. elliotti without understory, n = 71), H1 (height class 0-2 m), H2 (class (SD = 2.46) in 30-year-old A. angustifolia plantation with 2-4 m), H3 (class 4-6 m), H4 (class 6-8 m), H5 (class 8-10 m), H6 (class understory and in the native forest (Fig. 1). 10-12 m), H7 (class 12-14 m), H8 (class 14-16 m), H9 (class 16-18 m), H10 (class 18-20 m), H11 (class 20-22 m), H12 (class 22-24 m). Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 394 Mendonça -LiMa & Htzar Mottle-cheeked Tyrannulet used a wider range of attack maneuvers in 7-year-old P. elliottii plantations without understory compared to the other treatments (Fig. 2); however, there was no significant difference between the areas (P = 0.354). Taking all treatments into account, there was a higher frequency of maneuvers that involved flight (Fig. 2). As a result, the attack maneuvers oriented to prey away from the bird’s perch were more frequent for all treatments. The treatments did not differ regarding the substrates to which foraging maneuvers were oriented (P = 0.16). There was a high frequency of attacks directed to green leaves in all areas and the species again used all the substrates in Pinus plantations without understory (Fig. 3). The angle of substrate where prey was attacked was horizontal in native forest and forest plantations with understory, while this proportion decreased in plantations without understory (P = 0.04, Fig. 4). The frequency of maneuvers directed to proximal spots was higher in native forest, while the maneuvers were more often directed to distal spots in 30-year-old A. angustifolia plantation with understory and in 27-year old P. elliottii plantations with understory (Fig. 5), but there was no significant difference between the areas (P = 0.61). Considering all the foraging behavior variables the dispersion diagram for the PCoA clearly showed differences, where the frequency of occurrence of height of foraging, prey-attack behavior, and substrate directions were important to characterize the foraging behavior among treatments (Fig. 6). Planted forests with understory (Pinus and Araucaria) were close to the native forest in the first axis of the ordination. The second axis of ordination segregated the 25-year-old plantations of Pinus elliotti without understory from other ones. DISCUSSION The morphology of a bird restricts the kind of foraging maneuvers it can effectively utilize during prey-attacks. Therefore, foraging maneuvers tend to be conservative compared to other behaviors (e.g., foraging height), which are not linked to the bird’s shape and structure (h outt , 1981; Mtinar & k arr , 1990). Consequently, the foraging tactics and the morphology combined with the habitat structure indicate which species can be found in a certain habitat (h olMeS & r obinSon , 1988; ForStMeier & k e βler , 2001). Mottle-cheeked Tyrannulet altered significantly the height and angle of the maneuvers between native and planted forests, and changed the frequency of use of prey-attack maneuvers. This was apparent from the ordination scatterplot, where the maneuver behaviors Fig. 2. Distribution of prey-attack maneuver frequencies in native and correlated with the first axis, which described the differences plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria angustifolia with understory, in the foraging behavior among the treatments (sally-pounce n = 53), PS (25-year-old plantations of Pinus elliotti without understory, and vertical substrate in positive axis versus sally-hover n = 52), OP (25-year-old plantations of P. elliotti without understory, n and horizontal substrate in negative axis). Bird species = 59), MP (7-year-old plantations of P. elliotti without understory, n = using flight maneuvers seem not to alter the foraging tactic 71), Le (leap), Lu (lunge), Ro (reach-out), Sh (sally-hover), Sp (sally- pounce), Ss (sally-strike), St (sally-stall). between stands of different tree species; therefore, this Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae)... 395 Fig. 4. Distribution of frequencies of the angles used during the foraging in native and plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria angustifolia with understory, n = 53), PS (25-year-old plantations of Pinus elliotti without understory, n = 52), OP (25-year-old plantations of P. elliotti without understory, n = 58), MP (7-year-old plantations of P. elliotti without understory, n = 71). Fig. 5. Distribution of the frequencies of the positions where prey-attacks occurred during foraging in native and plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria angustifolia with understory, n = 53), PS (25-year-old plantations of Pinus elliotti with understory, n = 52), OP (25-year-old plantations of P. elliotti without understory, n = 59), MP (7-year-old plantations of P. elliotti without understory, n = 71). Fig. 6. Ordination diagram of the first and second axes of the PCoA based on the frequencies of foraging behaviors of Mottle-cheeked Tyrannulet in native and plantation forests. The foraging behavior variables represented in the diagram showed higher correlations with either one or both axes Fig. 3. Distribution of frequencies of the substrates used during the (r > 0.5). Legends: filled triangles = 25-year-old plantations of Pinus elliotti without understory, filled circles = 30-year-old plantations of foraging in native and plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria Araucaria angustifolia with understory, open diamond = native forest more than 40 years old, filled squares = 7-year-old plantations of P. elliotti angustifolia with understory, n = 53), PS (25-year-old plantations of without understory, open squares = 25-year-old plantations of P. elliotti Pinus elliotti without understory, n = 52), OP (25-year-old plantations of P. elliotti without understory, n = 59), MP (7-year-old plantations of with understory. H7-11 (foraging-height class), Spou (sally-pounce), Shov (sally-hover), Sstri (sally-strike), Hor (horizontal substrate), and P. elliotti without understory, n = 71), Gl (green leaves), Dl (dry leaves), B1 (branches < 1 cm), B2 (branches > 1 cm), Ar (Air). Ver (vertical substrate). Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 396 Mendonça -LiMa & Htzar strategy could function as a tactic to reduce the effects The restrictions imposed by the vegetation structure and of habitat structure on the foraging behavior (h olMeS & prey abundance determine the opportunities for foraging. r obinSon , 1981). The foraging characteristics of bird species that enable Despite substrate did not differ in the areas, in successful exploitation of resources in a particular habitat planted forests most maneuvers were made in Pinus and can be affected by these structural variables (r obinSon & Araucaria needles, compared with angiosperms in native h ol Me S, 1982). The Mottle-cheeked Tyrannulet occurs forest. Hence, we found that the major changes Mottle- in the medium/high forest strata, and demonstrated the cheeked Tyrannulet made to occupy the different habitats capacity to adapt to habitats with different structures. were related to the structure of the vegetation (substrate Therefore, the plasticity of its foraging behavior enabled type, horizontal location, and height) and to the frequency this flycatcher to occupy the commercial forest stands. of occurrence of certain aerial maneuvers used in its native Mottle-cheeked Tyrannulet changed its height of foraging habitat. This plasticity enabled Mottle-cheeked Tyrannulet in plantation stands. This alteration may be common in a to occupy all the forests investigated. species that uses the middle forest stratum, because birds The differences in the structure and composition foraging in this stratum use a greater range of heights of plants among the forest stands (Mendonça -l iMa et al., compared to species foraging in the canopy (Wtheral , 2014) can alter the distribution of resources, which may 2002). Bird species using flight maneuvers tend to take be an important factor influencing the observed changes in advantage of different opportunities for foraging, compared the bird’s foraging behavior (Mrerua & Wtih Mero , 1981). to species that use other forms of prey capture (Maurer Differences in the structure of native and managed forests & Whit More , 1981). Therefore, it is suggested that the may affect the distribution and density of bird prey species capacity to capture prey in the different substrates within (Franzeb , 1983; Parri Sh , 1995; Greenber G & b ichier , the treatments was possible due to the plasticity of foraging 2005). The foraging behavior encompasses diverse phases, behavior, by altering the frequencies of maneuvers used among which are the search to locate the food, and the by Mottle-cheeked Tyrannulet in the different habitats. prey-attack to capture the food (r e MSne & r nibo Sno , 1990), The present study showed alterations in the foraging which can be changed by the location of the resource. In behavior of Mottle-cheeked Tyrannulet among different this study, Mottle-cheeked Tyrannulet changed the mode forest habitats. The change in the behavior of Mottle- of prey capture, although it could have changed the mode cheeked Tyrannulet among plantations with different plant of prey searching as well. Previous studies showed that species (one native and one exotic) was important, wherein the distribution and density of foliage influenced the food- planted Araucaria was more similar to native forest. This searching tactics of species that usually attack the prey result emphasizes the importance of using native plant by flight ( r obinSon & h olMeS , 1984; h olMeS & r echer , species in silviculture systems, which reduces the negative 1986). impact on the local fauna. Studies of bird assemblages In our study, the frequency of behavior observations confirm this statement ( z a tiru et al., 2006; v lo Pot a et al., was higher in the native forest and in the forest plantations 2010). The presence of the understory in exotic plantations with understory, which may be related to resource allowed Mottle-cheeked Tyrannulet to use the different availability or to differences in species abundance. Some foraging substrates, showing differences in the height, species show a positive correlation between the attack rate angle and frequency of utilization of attack maneuvers and food availability (j ohnSon , 2000; l yonS , 2005). Two between the Pinus plantations. The observations of the hypotheses related to resource availability may explain foraging behavior in Pinus with and without understory this general pattern of habitat use: (1) the species may indicated that vegetation structure may be determining the use a wide variety of prey in the different habitats, and presence of Mottle-cheeked Tyrannulet in the plantations. (2) high productivity in the breeding season can force Then, the dominant tree in the stands may play an important the individuals to utilize sub-optimal habitats (r a PPole , role in determining the bird species occurring in this type 1996). These two explanations held for Mottle-cheeked of habitat (e.g., Grebneer G & b reihci , 2005). Commercial Tyrannulet in the areas of commercial plantations, where plantations have expanded greatly in recent years. Hence, this generalist species can benefit from a wide variety there is a need to study the effects of this kind of system on of prey, occupying habitats with fewer resources, but animal populations and communities, in order to suggest also with fewer competitors. This may explain the use management practices to mitigate possible deleterious of a larger set of maneuvers and higher heights in Pinus effects. The findings of this study highlighted the importance without understory by the species. In shaded-coffee farms, of the presence of an understory and the native tree species j akcilde et al. (2006) found shift in the behavioral foraging A. angustifolia in commercial plantations to the foraging (mainly in height) by Rufous-capped Warbler (Basileuterus behavior of the species studied. Proper management of this rufifrons Swainson, 1838) to avoid seasonal competition forest habitat, with maintenance of understory and planting with migrant species. native species, may provide an important commercial The habitat structure of forest monocultures is alternative, and may also help in the conservation of the simpler than the native forests (a da Mík et al., 2003). fauna in silviculture areas contiguous to native forests. Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae)... 397 Acknowledgements. We thank the CNPq for a productivity k niel , r . M. 1978. Mapa fitogeográfico do estado de Santa Catarina: research grant received by SMH (306816/2010-5) and CAPES the resenha descritiva da cobertura original. Itajaí, SUDESUL, doctorate scholarship received by AML. We are grateful for the logistical FATMA e Herbário Barbosa Rodrigues. support of the staff of the Fazenda Florestal Gateados, especially Valdir k otler , b. P. & b roWn , j. S . 2007. Community ecology. In: StePhenS , Dhiel, Mário Dobner, and Maite Ribeiro. Andreas Kindel, Luiz dos Anjos, d. W.; b roWn , j. S. & y denberG , r. c. eds. Foraging: behavior and Paulo de Tarso Zuquim Antas made valuable suggestions during the and ecology. Chicago, The Chicago University Press, p. 397-476. manuscript preparation. k uSch , j.; W eber , c.; i delberGer , S. & k oob , t . 2004. Foraging habitat preferences of bats in relation to food supply and spatial vegetation REFERENCES structures in a western European low mountain range forest. Folia Zoologica 53:113-128. a ad Mkí , P.; k nanro , M. & v ketjo , j . 2003. The effect of habitat structure l att a , S. c . & Wunderle j r ., j . M. 1998. The assemblage of birds on guild patterns and the foraging strategies of insectivorous birds foraging in native West Indian pine (Pinus occidentalis) forests of in forests. Biologia 58:275-285. the Dominican Republic during the nonbreeding season. Biotropica a tM l ann , j . 1974. Observation study of behavior: sampling, methods. 30:645-656. Behaviour 49:227-267. l oše , P. & k or Pli , r . 2007. A comparison of three different approaches for b not le , W. 1985. Birds of Rio Grande do Sul, Brazil. Part 2. Formicariidae the classification of bird foraging guilds: an effect of leaf phenophase. through Corvidae. Bulletin of the American Museum of Natural Folia Zoologica 56:51-70. History 180:1-242. l yonS , j. e . 2005. Habitat-specific foraging of Prothonotary Warblers: c â Mara , i . c . 2003. Brief history conservation in the Atlantic Forest. In: deducing habitat quality. Condor 107:41-49. Godnila -l lae , c . & c â Mara , i . G. eds. The Atlantic Forest of South Mac a thrur , r . h . 1958. Population ecology of some warblers of America: biodiversity status, threats, and outlook. Washington, northeastern coniferous forests. Ecology 39:599-619. Conservation International, Island Press, p. 31-42. Mac a thurr , r. h. & Pianka , e. r . 1966. On optimal use of a patchy d iet Sch , t . v .; Per Fecot , i . & Greenber G, r . 2007. Avian foraging environment. American Naturalist 100:603-609. behavior in two different types of coffee agroecosystem in Chiapas, My anl , b. F. j . 1991. Randomisation and Monte Carlo methods in Mexico. Biotropica 39:232-240. biology. London, Chapman and Hall. 281p. Fitz Ptricak , j . W. 1980. Foraging behavior of Neotropical Tyrant _____. 1994. Multivariate statistical methods. London, Chapman Flycatchers. Condor 82:43-57. and Hall. 232p. _____. 2004. Family Tyrannidae (Tyrant-flycatchers). In: d el h oyo , j.; Marini , M. a. & c alcanti v a , r. b . 1993. Habitat and foraging substrate e lliott , a. & c hriStie , d. a. eds. Handbook of the birds of the use of three Basileuterus warblers from central Brazil. Ornitologia world. Vol. 9. Cotingas to Pipits and Wagtails. Barcelona, Lynx Neotropical 2:69-76. Edicions, p. 170-462. Mtinar , t . e . & k arr , j . r . 1990. Behavioral plasticity of foraging ForStMeier , W. & k e βler , a . 2001. Morphology and foraging behavior maneuvers of migratory Warblers: multiple selection periods for of Siberian Phylloscopus warblers. Journal of Avian Biology niches? Studies in Avian Biology 13:353-359. 32:127-138. Mreaur , b. a. & Wthi Meor , r. c . 1981. Foraging of five bird species in Franzeb , k. e. 1978. Tree species used by birds in logged and unlogged two forests with different vegetation structure. The Wilson Bulletin Mixed-coniferous Forests. The Wilson Bulletin 90:221-238. 93:478-490. _____. 1983. A comparison of avian foraging behavior in unlogged and Maçnodne -l i Ma , a .; h zt ra , S. M. & k ledni , a . 2004. Foraging behavior logged Mixed-coniferous Forest. The Wilson Bulletin 96:60-76. of the White-browed (Basileuterus leucoblepharus) and the Golden- Gleirba , v . a . & Pozi , M. a . 2005. Foraging behavior of tyrant flycatchers crowned (B. culicivorus) Warblers in a Semidecidual Forest in (Aves, Tyrannidae) in Brazil. Revista Brasileira de Zoologia Southern Brazil. Ornitologia Neotropical 15:5-15. 22:1072-1077. Mendonça -l i Ma , a .; d tuear , l . & h tzar , S. M. 2014. Comparing Grebneer G, r . & b reihci , P. 2005. Determinants of tree species preference diversity and dispersal traits of tree communities in plantations and of birds in Oak-Acacia woodlands of Central America. Journal of native forests in Southern Brazil. Natureza & Conservação 12:24-29. Tropical Ecology 21:57-66. Moer Mond , t . c . 1979. The influence of habitat structure on Anolis Gbbur , t . c . 1979. Factors controlling foraging strategies of insectivorous foraging behavior. Behaviour 70:147-167. birds. In: d ickSon , j. G.; c onnor , r. n.; F leet , r. r.; j ackSon , j. Parri Sh , j . d . 1995. Effects of needle architecture on warbler habitat a . & k roll , j . c . eds. The role of insectivorous birds in forest selection in a coastal Spruce Forest. Ecology 76:1813-1820. ecosystems. London, Academic Press, p. 119-135. Pillar , v . d . 2006. MULTIV: Multivariate exploratory analysis, h ol Me S, r . t . & r echer , h . F. 1986. Search tactics of insectivorous randomization testing and bootstrapping resampling, user’s guide birds foraging in an Australian eucalypt forest. Auk 103:515-530. v. 2. 4. Universidade Federal do Rio Grande do Sul, Porto Alegre, h lo Me S, r . t . & r nibo Sno , S. k . 1981. Tree species preferences of foraging Brazil. Available at: <http://ecoqua.ecologia.ufrgs.br/arquivos/ insectivorous birds in a northern Hardwoods Forest. Oecologia Software/Multiv/MultivManual.pdf >. Accessed at: 04.jan.2013. 48:31-35. Pralli , v . d . & o icólr , l . 1996. On randomization testing in vegetation _____. 1988. Spatial patterns, foraging tactics, and diets of ground- science: multifactor comparisons of revelé groups. Journal of foraging birds in a northern Hardwoods Forest. The Wilson Bulletin Vegetation Science 7:585-592. 100:377-394. Po Mara , l . y .; c oo Pre , r . j . & Ptite , l . j . 2003. Mixed-species flocking h t ol , r. d. & k riMbell , t . 2007. Foraging and population dynamics. and foraging behavior of four neotropical warblers in Panamanian In: Set Pneh S, d . W.; b or Wn , j . S. & y rebned G, r . c . eds. Foraging: shade coffee fields and forests. Auk 120:1000-1012. behavior and ecology. Chicago, The Chicago University Press, p. r a Mbo , b . a . 1951. A imigração da selva higrófila no Rio Grande do 365-396. Sul. Anais Botânicos do Herbário “Barbosa Rodrigues” 3:55-91. h utot , r . l . 1981. Seasonal variation in foraging behavior of some r aPPole , j. h . 1996. The importance of forest for the world’s migratory migratory western wood warblers. Auk 98:765-777. bird species. In: d e Gaar F, r . M. & Mrelli , r . i . eds. Conservation ibGe. 1992. Manual técnico da vegetação brasileira. Série manuais of faunal diversity in forested landscapes. London, Chapman and técnicos em geociências. Rio de Janeiro, IBGE. 92p. Hall, p. 389-406. j edlicka , j .; Greenber G, r .; Per Feoct , i .; Phil Pott , S. & d iet Sch , t . r eMSen , j. v ., j r . & r obinSon , S. k . 1990. A classification scheme for 2006. Seasonal shift in the foraging niche of a tropical avian resident: foraging behavior of birds in terrestrial habitats. Studies in Avian resource competition at work? Journal of Tropical Ecology 22:385- Biology 13:144-160. 395. r di Gy le , r . S. & t rodu , G. 2009. Field guide to the songbirds of South j nho Sno , M. d . 2000. Evaluation of an arthropod sampling technique for America: the passerines. Austin, University of Texas Press. 736p. measuring food availability for forest insectivorous birds. Journal r nibo Sno , S. k . & h lo Me S, r . t . 1982. Foraging behavior of forest birds: of Field Ornithology 71:88-109. the relationships among search tactics, diet, and habitat structure. Ecology 63:1918-1931. Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 398 Mendonça -LiMa & Htzar r nibo Sno , S. k . & h lo Me S, r . t . 1984. Effects of plant species and foliage v lo Pot a , G. h .; Podar , v . M. & a ojn S, l . 2010. What can tree plantations structure on the foraging behavior of forest birds. Auk 101:672-684. do for forest birds in fragmented forest landscapes? A case study in r o Sário , l . a . M. 1996. As aves em Santa Catarina: distribuição southern Brazil. Forest Ecology and Management 260:1156-1163. geográfica e meio ambiente . Florianópolis, FATMA. 326p. Wther al , b. a . 2002. Grounded ground birds and surfing canopy birds: Sabo , S. r. & h olMeS , r. t . 1983. Foraging niches and the structure of variation of foraging stratum breadth observed in neotropical forest forest bird communities in contrasting montane habitats. Condor birds and tested with simulation models using boundary constraints. 85:121-138. Auk 119:658-675. Saant c artinaa . 1986. Atlas de Santa Catarina. Florianópolis, Wnaleh , c . j . 2001. Foliage structure influences foraging of insectivorous GAPLAN/SUEGI. 173p. forest birds: an experimental study. Ecology 82:219-231. Sick , h . 1997. Ornitologia brasileira. Rio de Janeiro, Nova Fronteira. Welrednu , j . M., j r . & l a tt a , S. c . 1998. Avian resource use in Dominican 912p. Shade Coffee Plantations. The Wilson Bulletin 110:271-281. SoareS , e. S. & a njoS , l . 1999. Efeito da fragmentação florestal sobre z a urit , G. a.; r ey , n.; v arela , d. M.; v illaGra , M. & b ellocq , M. i . aves escaladoras de tronco e galho na região de Londrina, norte 2006. Conversion of the Atlantic Forest into native and exotic tree do Estado do Paraná, Brasil. Ornitologia Neotropical 10:61-68. plantations: Effects on bird communities from the local and regional t ylor ra , M. a ., j r . & Fitz Ptrick a , j . W. 1982. A survey of the tyrant perspectives. Forest Ecology and Management 235:164-173. flycatchers. Living Bird 19:7-45. Received 12 August 2013. Accepted 23 December 2014. ISSN 0073-4721 Article available at: www.scielo.br/isz Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Iheringia. Série Zoologia Unpaywall

Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae) in native and planted forests of southern Brazil

Iheringia. Série ZoologiaDec 1, 2014

Loading next page...
 
/lp/unpaywall/foraging-behavioral-of-phylloscartes-ventralis-aves-tyrannidae-in-u3ge4NIRjL

References

References for this paper are not available at this time. We will be adding them shortly, thank you for your patience.

Publisher
Unpaywall
ISSN
0073-4721
DOI
10.1590/1678-476620141044391398
Publisher site
See Article on Publisher Site

Abstract

Iheringia, Série Zoologia DOI: 10.1590/1678-476620141044391398 Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae) in native and planted forests of southern Brazil André de Mendonça-Lima & Sandra M. Hartz Programa de Pós-graduação em Ecologia, Laboratório de Ecologia de Populações e Comunidades, Universidade Federal do Rio Grande do Sul., Av. Bento Gonçalves 9500, Prédio 43411/209, 91501-970 Porto Alegre, RS, Brazil. (mendoncalima@hotmail.com; corresponding author: sandra.hartz@ufrgs.br) ABSTRACT. Few studies have related the effects of silviculture practices to the behavior of bird species in the Neotropics. The present study examined the foraging behavior of Phylloscartes ventralis (Temminck, 1824) in a native forest and in silviculture areas of Pinus elliotti and Araucaria angustifolia with different structures and ages. We tested two general hypotheses: (1) areas of commercial forest plantation change the foraging behavior of P. ventralis in relation to native forest, and (2) the foraging behavior of P. ventralis in silviculture areas with understories (complex structures) is different from its behavior in areas without understory. The results showed that P. ventralis changed its foraging behavior depending on the type of forest, and on the presence of an understory in silviculture areas. Main changes involved the height and angle of substrate where the prey was captured. Phylloscartes ventralis showed the same set of attack maneuvers, with more maneuvers type in young Pinus planted without understory. The frequency of use of attack maneuvers was more similar in areas of silviculture with understory and in the native forest. The results highlight the importance of an understory structure and the utilization of native plant species in silviculture practices, to the foraging behavior of native bird species. KEYWORDS. Mottle-cheeked Tyrannulet, attack maneuvers, Araucaria angustifolia, Pinus elliotti, habitat structure. RESUMO. Comportamento de forrageio de Phylloscartes ventralis (Aves, Tyrannidae) em florestas nativas e plantadas no sul do Brasil. Poucos estudos têm relacionado os efeitos que práticas silviculturais exercem sobre o comportamento de aves neotropicais. O presente estudo analisou o comportamento de forrageio de Phylloscartes ventralis (Temminck, 1824) em uma floresta nativa e em áreas de silvicultura de Pinus elliottii e Araucaria angustifolia com diferentes estruturas e idades. Foram testadas duas hipóteses gerais: (1) áreas de plantio comercial alteram o comportamento e forrageio de P. ventralis em relação à mata nativa e (2) o comportamento de forrageio de P. ventralis em áreas de silvicultura com sub-bosque (estruturalmente mais complexas) é diferente do registrado em áreas sem sub-bosque. Os resultados demonstram que P. ventralis alterou seu comportamento de forrageio dependendo do tipo de floresta e da presença de sub-bosque em áreas de silvicultura. As principais mudanças envolvem a altura e o ângulo de substrato onde a presa foi capturada. Phylloscartes ventralis exibiu o mesmo grupo de manobras de ataque a presas, com um maior número de tipos de manobras em plantações jovens de Pinus sem sub-bosque. A frequência de uso de manobras de ataque a presas foi mais similar em áreas de silvicultura com sub-bosque e na floresta nativa. Os resultados destacam a importância do sub-bosque e da utilização de espécies nativas em práticas silviculturais para a manutenção do comportamento de forrageio de uma espécie de ave nativa. PALAVRAS-CHAVE. Borboletinha-do-mato, manobras de ataque, Araucaria angustifolia, Pinus elliottii, estrutura de hábitat. The structure of the habitat is an important factor Neotropics are usually done in forest ecosystems (Marini affecting the foraging behavior of animal species in & c alcanti v a , 1993; l a tt a & Wunderle , 1998; SoareS different areas (Mca a ruhtr & Paknai , 1966; Mreo Mdno , & a njoS , 1999; Mendonça -l iMa et al., 2004; Gabriel & 1979; Mrerua & Wtih Mero , 1981; Soba & h lo Me S, 1983; Pozi , 2005; Grebneer G & b reihci , 2005, among others) and Whelan , 2001). Alterations in the habitat structure can studies in silviculture areas or commercial forest plantations change the quantity and quality of available resources. are scarce, compared with native areas (Wunderle & Therefore, in altered habitats, species are forced to change l a tt a , 1998; PoMara et al., 2003; d ietSch et al., 2007). their foraging mode, or they may be replaced by other Assessments of foraging strategy patterns can help in the species (Grubb , 1979; k uSch et al., 2004). For instance, understanding of population and community dynamics, plant species with different foliage structures can affect because these patterns can influence the fluctuations of bird behavior, which in turn changes the habitat availability abundance and occurrence of a species in a particular and the resource exploitation (Franzeb , 1978; h olMeS & habitat (h t lo & k ir Mlleb , 2007; k relto & b or Wn , 2007). r nibo Sno , 1988). Among vertebrates, the foraging behavior Therefore, it is important to study the foraging behavior of of insectivorous birds is particularly well studied, mainly species in silviculture areas compared with native areas, in Europe and North America (h lo Me S & r nibo Sno , 1981; because tree plantations markedly alter the habitat, and Whelan , 2001). Although knowledge of the foraging these changes may lead to the local extinction of some behavior of bird species is a key question for successful species, whereas others may be able to colonize the altered management of populations, communities and ecosystems habitats. (l oše & k or Pli , 2007), the use of different tree species by The New World family Tyrannidae is one of the most insectivorous birds in tropical habitats has received little representative bird taxa and is among the most numerous attention (GreenberG & b ichier , 2005). in the world (Fitz Ptrick a , 1980, 2004; Sick , 1997). The Studies of the foraging behavior of birds in the forest-dwelling species of this family occupy all forest Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 392 Mendonça -LiMa & Htzar vertical strata (Sick , 1997). Less diverse at the ground (Podocarpus) (c âMara , 2003). layer, they increase in richness toward the upper layer of The sampling was performed in a native forest, and the forests (t roly ar & Fzti Pkcirt a , 1982; Skci , 1997). The in commercial forest stands of P. elliotti and A. angustifolia. Mottle-cheeked Tyrannulet (Phylloscartes ventralis) is a The P. elliotti plantations were distinguished by age and by common inhabitant of forests in south and southeast Brazil the presence of an understory: (1) 7-year-old plantations (b ont el , 1985; r oSário , 1996; Sick , 1997). It also occurs without understory (MP), (2) 25-year-old plantations in Argentina, Uruguay and Paraguay, and in a disjunct area without understory (OP), and (3) 27-year old plantations from northwest Argentina to Bolivia and Peru (r id Gy el with understory (PS). The 30-year-old A. angustifolia & t udor , 2009). The species is typically found in the plantation had an understory too (AP). All forest plantation middle to upper layers of forests and woodlands (b ont el , areas were contiguous (edge area) with the native forest 1985; Sick , 1997). The foraging maneuver commonly (NF). The native forest was located on hillsides and in the used by Mottle-cheeked Tyrannulet is the Sally-strike, a valley of the region, and had a dense understory. The mean very stereotyped maneuver and mainly characteristic of distance between the areas was 8 km, and between each area the small-bodied tyrant flycatchers ( Fitz Ptricka , 1980; in the same vegetation type was 2 km. Four sampling sites r eMSen & r obinSon , 1990). were marked, within each of five different forest treatments Assessment of the patterns of foraging behavior of (three Pinus plantations, the Araucaria plantation and the native bird species in the managed and native forests of native forest). The sampling sites were located at least the Araucaria forest ecosystem is particularly important to 100 m from any edge area, and were 500 x 100 m wide. fill a gap in knowledge about the impact of habitat change The overstory of each plantation was uniform in height; on bird populations in this region. Therefore, in this study however, there were differences between the treatments: we evaluated whether there are differences in the foraging the 27-year old P. elliottii plantations with understory and behavior of Mottle-cheeked Tyrannulets associated with 25-year-old P. elliottii plantations without understory had the habitat structure of planted and native forests. These the highest canopy heights (25 m and 23 m respectively); forests differ in their understory structure (Maçnodne -l i Ma followed by native forest (21.9 m), 7-year-old P. elliottii et al., 2014), when it is present (depending on the type plantations without understory (16 m), and 30-year-old A. of management) and this can lead to changes in foraging angustifolia plantations with understory (13 m). Understory behavior of insectivorous birds. We specifically tested the composition and diversity of planted and native forests are hypothesis that the frequency of foraging behavior variables described in Mendonça -l iMa et al. (2014). including prey-attack maneuvers, the type and angle of Data collection. Bird behavior was observed during substrate, the height at which foraging is conducted, and the breeding season of spring 2008 (between 3–10 October) the horizontal position where the attack was directed were and 2009 (between 2 October–11 November), starting 30 different in native and managed forests. min after sunrise; the total sampling effort was 199.74 hr. We used the focal-animal sampling (a t l Mnna , 1974) with MATERIAL AND METHODS modifications ( Marini & c alcanti v a , 1993; Mendonça - l i Ma et al., 2004). Individuals of Mottle-cheeked Tyrannulet Study area. The study was carried out in stands were identified and observed from a distance > 7 m, using of commercial plantations of Pinus elliottii and Araucaria binoculars. After the first sighting of an individual, the data angustifolia, as well as in areas of native forests on a recording started when it first attacked the prey, always commercial tree farm located in the Campo Belo do Sul taking care to not disturb the bird during foraging. When municipality, southern Brazil (1,000 m a.s.l.; 28°00’S, this was perceptible (e.g., attention directed to the observer, 50°49’W). The tree farm has an area of 14,200 ha, of which more frequent and nervous vocalizations), the distance 6,300 ha is part of a sustainable-use conservation unit. The of observation was increased and the data recording was remaining area is planted with different-aged stands of resumed after the bird resumed its usual behavior. Two or Pinus spp. The climate is typical of the southern Brazilian more observations of the same individual were considered highlands, with cool summers, no dry season, and frequent valid only when they were separated by a minimum interval severe frosts in winter (Köppen Cfb classification). The of 5 min, to assure independence of observations. mean annual temperature is 16°C (Sa tna c anira t a , 1986). We recorded data on the following behavior The characteristic regional native vegetation is variables: position of the individual in relation to the ground the Araucaria forest, which occurs mainly between 400 (height), attack maneuvers to prey (r eMSen & r obinSon , and 1,000 m a.s.l. along watercourses, valleys, hillsides, 1990), the substrate type where the attack occurred, the and grasslands on the plateau (k lein , 1978; ibGe, 1992). substrate angle, and the horizontal position in relation to The presence of A. angustifolia comprises the main the main axis of the focus tree. The position of the birds physiognomy; these trees occur in continuous forest in relation to the ground was defined by visual estimation habitats as well as in patches embedded in the plateau at 2-m intervals. The foraging substrate was classified grasslands (r a Mbo , 1951). Besides this species there as: green and dry leaves (included Pinus and Araucaria are several genera of laurel trees in this forest, such as needles), branch with a maximum diameter of 1 cm, branch Ocotea and Nectandra, and another native genera of conifer with a diameter thicker than 1 cm, and air. The substrate Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae)... 393 angle was divided into vertical (equal to or more than 45° in relation to the ground) and horizontal (less than 45° in relation to the ground) (Minira & c itnacla v a , 1993). When the individual bird attacked a prey on leaves or branches, the horizontal position in relation to the central axis of the focal tree was divided into three equal parts and defined as proximal, medial or distal (Mac a thurr , 1958). Statistical analyses. We evaluated the sampling effort by the analysis of cumulative estimates of prey attack- maneuver frequencies. In order to analyze the patterns of foraging behavior, we constructed a frequency matrix of sampling units and various classes of attack maneuvers, heights, foraging substrates, angles, and the position in relation to the central axis of a focal tree. Therefore, we consider a sampling unit within each treatment was composed by the frequency of set of six consecutive records of behavioral variables. The variation in the composition of behavioral-variable frequencies between forest treatments was analyzed by performing a Permanova based on a Gower or Euclidean distance (for heights analysis) dissimilarity matrix between sampling units. The age of the stands and the presence of understory were used as blocks in the analysis. The comparison between groups of sampling units belonging to the forest treatments was based on a sum of squares between groups as test criterion – Qb statistics (My anl , 1991, 1994; Pillar & o rlóci , 1996). The results are interpreted similarly to those in an ANOVA table. Significant differences between treatments were based on a P-value <= 0.05. A Principal Coordinates Analysis (PCoA) was carried out (using chord distance) to visualize the pattern of distribution of foraging behavioral variables within treatments. All data were analyzed in the MULTIV 2.63 statistical package (Pillar , 2006). RESULTS A total of 265 observations of Mottle-cheeked Tyrannulet foraging behavior were made during the study. The highest frequency of observations occurred in 30-year- old A. angustifolia plantation with understory (1.93 obs./ hr), followed by 27-year old P. elliottii plantations with understory (1.55), native forest (1.51), 7-year-old P. elliottii plantations without understory (1.25), and 25-year-old P. elliottii plantations without understory (0.98). Therefore, the treatments without understory showed the lowest frequency of observations. The mean height of foraging differed between areas (P = 0.001) and was smaller in the Pinus plantations with understory (Fig. 1). Mean height was 18.95 m in 25-year-old Fig. 1. Distribution of foraging-height class frequencies of Mottle-cheeked P. elliottii plantations without understory (SD = 2.99) and Tyrannulet in native and plantation forests. Legends: NF (native forest 12.01 m (SD = 2.29) in 7-year-old P. elliottii plantations more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria without understory, while in plantations with understory angustifolia with understory, n = 53), PS (25-year-old plantations of Pinus elliotti without understory, n = 52), OP (25-year-old plantations the mean height was 4.36 m (SD = 2.65) in 27-year old of P. elliotti without understory, n = 59), MP (7-year-old plantations of P. elliottii plantations with understory and around 9.00 m P. elliotti without understory, n = 71), H1 (height class 0-2 m), H2 (class (SD = 2.46) in 30-year-old A. angustifolia plantation with 2-4 m), H3 (class 4-6 m), H4 (class 6-8 m), H5 (class 8-10 m), H6 (class understory and in the native forest (Fig. 1). 10-12 m), H7 (class 12-14 m), H8 (class 14-16 m), H9 (class 16-18 m), H10 (class 18-20 m), H11 (class 20-22 m), H12 (class 22-24 m). Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 394 Mendonça -LiMa & Htzar Mottle-cheeked Tyrannulet used a wider range of attack maneuvers in 7-year-old P. elliottii plantations without understory compared to the other treatments (Fig. 2); however, there was no significant difference between the areas (P = 0.354). Taking all treatments into account, there was a higher frequency of maneuvers that involved flight (Fig. 2). As a result, the attack maneuvers oriented to prey away from the bird’s perch were more frequent for all treatments. The treatments did not differ regarding the substrates to which foraging maneuvers were oriented (P = 0.16). There was a high frequency of attacks directed to green leaves in all areas and the species again used all the substrates in Pinus plantations without understory (Fig. 3). The angle of substrate where prey was attacked was horizontal in native forest and forest plantations with understory, while this proportion decreased in plantations without understory (P = 0.04, Fig. 4). The frequency of maneuvers directed to proximal spots was higher in native forest, while the maneuvers were more often directed to distal spots in 30-year-old A. angustifolia plantation with understory and in 27-year old P. elliottii plantations with understory (Fig. 5), but there was no significant difference between the areas (P = 0.61). Considering all the foraging behavior variables the dispersion diagram for the PCoA clearly showed differences, where the frequency of occurrence of height of foraging, prey-attack behavior, and substrate directions were important to characterize the foraging behavior among treatments (Fig. 6). Planted forests with understory (Pinus and Araucaria) were close to the native forest in the first axis of the ordination. The second axis of ordination segregated the 25-year-old plantations of Pinus elliotti without understory from other ones. DISCUSSION The morphology of a bird restricts the kind of foraging maneuvers it can effectively utilize during prey-attacks. Therefore, foraging maneuvers tend to be conservative compared to other behaviors (e.g., foraging height), which are not linked to the bird’s shape and structure (h outt , 1981; Mtinar & k arr , 1990). Consequently, the foraging tactics and the morphology combined with the habitat structure indicate which species can be found in a certain habitat (h olMeS & r obinSon , 1988; ForStMeier & k e βler , 2001). Mottle-cheeked Tyrannulet altered significantly the height and angle of the maneuvers between native and planted forests, and changed the frequency of use of prey-attack maneuvers. This was apparent from the ordination scatterplot, where the maneuver behaviors Fig. 2. Distribution of prey-attack maneuver frequencies in native and correlated with the first axis, which described the differences plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria angustifolia with understory, in the foraging behavior among the treatments (sally-pounce n = 53), PS (25-year-old plantations of Pinus elliotti without understory, and vertical substrate in positive axis versus sally-hover n = 52), OP (25-year-old plantations of P. elliotti without understory, n and horizontal substrate in negative axis). Bird species = 59), MP (7-year-old plantations of P. elliotti without understory, n = using flight maneuvers seem not to alter the foraging tactic 71), Le (leap), Lu (lunge), Ro (reach-out), Sh (sally-hover), Sp (sally- pounce), Ss (sally-strike), St (sally-stall). between stands of different tree species; therefore, this Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae)... 395 Fig. 4. Distribution of frequencies of the angles used during the foraging in native and plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria angustifolia with understory, n = 53), PS (25-year-old plantations of Pinus elliotti without understory, n = 52), OP (25-year-old plantations of P. elliotti without understory, n = 58), MP (7-year-old plantations of P. elliotti without understory, n = 71). Fig. 5. Distribution of the frequencies of the positions where prey-attacks occurred during foraging in native and plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria angustifolia with understory, n = 53), PS (25-year-old plantations of Pinus elliotti with understory, n = 52), OP (25-year-old plantations of P. elliotti without understory, n = 59), MP (7-year-old plantations of P. elliotti without understory, n = 71). Fig. 6. Ordination diagram of the first and second axes of the PCoA based on the frequencies of foraging behaviors of Mottle-cheeked Tyrannulet in native and plantation forests. The foraging behavior variables represented in the diagram showed higher correlations with either one or both axes Fig. 3. Distribution of frequencies of the substrates used during the (r > 0.5). Legends: filled triangles = 25-year-old plantations of Pinus elliotti without understory, filled circles = 30-year-old plantations of foraging in native and plantation forests. Legends: NF (native forest more than 40 years old, n = 30), AP (30-year-old plantations of Araucaria Araucaria angustifolia with understory, open diamond = native forest more than 40 years old, filled squares = 7-year-old plantations of P. elliotti angustifolia with understory, n = 53), PS (25-year-old plantations of without understory, open squares = 25-year-old plantations of P. elliotti Pinus elliotti without understory, n = 52), OP (25-year-old plantations of P. elliotti without understory, n = 59), MP (7-year-old plantations of with understory. H7-11 (foraging-height class), Spou (sally-pounce), Shov (sally-hover), Sstri (sally-strike), Hor (horizontal substrate), and P. elliotti without understory, n = 71), Gl (green leaves), Dl (dry leaves), B1 (branches < 1 cm), B2 (branches > 1 cm), Ar (Air). Ver (vertical substrate). Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 396 Mendonça -LiMa & Htzar strategy could function as a tactic to reduce the effects The restrictions imposed by the vegetation structure and of habitat structure on the foraging behavior (h olMeS & prey abundance determine the opportunities for foraging. r obinSon , 1981). The foraging characteristics of bird species that enable Despite substrate did not differ in the areas, in successful exploitation of resources in a particular habitat planted forests most maneuvers were made in Pinus and can be affected by these structural variables (r obinSon & Araucaria needles, compared with angiosperms in native h ol Me S, 1982). The Mottle-cheeked Tyrannulet occurs forest. Hence, we found that the major changes Mottle- in the medium/high forest strata, and demonstrated the cheeked Tyrannulet made to occupy the different habitats capacity to adapt to habitats with different structures. were related to the structure of the vegetation (substrate Therefore, the plasticity of its foraging behavior enabled type, horizontal location, and height) and to the frequency this flycatcher to occupy the commercial forest stands. of occurrence of certain aerial maneuvers used in its native Mottle-cheeked Tyrannulet changed its height of foraging habitat. This plasticity enabled Mottle-cheeked Tyrannulet in plantation stands. This alteration may be common in a to occupy all the forests investigated. species that uses the middle forest stratum, because birds The differences in the structure and composition foraging in this stratum use a greater range of heights of plants among the forest stands (Mendonça -l iMa et al., compared to species foraging in the canopy (Wtheral , 2014) can alter the distribution of resources, which may 2002). Bird species using flight maneuvers tend to take be an important factor influencing the observed changes in advantage of different opportunities for foraging, compared the bird’s foraging behavior (Mrerua & Wtih Mero , 1981). to species that use other forms of prey capture (Maurer Differences in the structure of native and managed forests & Whit More , 1981). Therefore, it is suggested that the may affect the distribution and density of bird prey species capacity to capture prey in the different substrates within (Franzeb , 1983; Parri Sh , 1995; Greenber G & b ichier , the treatments was possible due to the plasticity of foraging 2005). The foraging behavior encompasses diverse phases, behavior, by altering the frequencies of maneuvers used among which are the search to locate the food, and the by Mottle-cheeked Tyrannulet in the different habitats. prey-attack to capture the food (r e MSne & r nibo Sno , 1990), The present study showed alterations in the foraging which can be changed by the location of the resource. In behavior of Mottle-cheeked Tyrannulet among different this study, Mottle-cheeked Tyrannulet changed the mode forest habitats. The change in the behavior of Mottle- of prey capture, although it could have changed the mode cheeked Tyrannulet among plantations with different plant of prey searching as well. Previous studies showed that species (one native and one exotic) was important, wherein the distribution and density of foliage influenced the food- planted Araucaria was more similar to native forest. This searching tactics of species that usually attack the prey result emphasizes the importance of using native plant by flight ( r obinSon & h olMeS , 1984; h olMeS & r echer , species in silviculture systems, which reduces the negative 1986). impact on the local fauna. Studies of bird assemblages In our study, the frequency of behavior observations confirm this statement ( z a tiru et al., 2006; v lo Pot a et al., was higher in the native forest and in the forest plantations 2010). The presence of the understory in exotic plantations with understory, which may be related to resource allowed Mottle-cheeked Tyrannulet to use the different availability or to differences in species abundance. Some foraging substrates, showing differences in the height, species show a positive correlation between the attack rate angle and frequency of utilization of attack maneuvers and food availability (j ohnSon , 2000; l yonS , 2005). Two between the Pinus plantations. The observations of the hypotheses related to resource availability may explain foraging behavior in Pinus with and without understory this general pattern of habitat use: (1) the species may indicated that vegetation structure may be determining the use a wide variety of prey in the different habitats, and presence of Mottle-cheeked Tyrannulet in the plantations. (2) high productivity in the breeding season can force Then, the dominant tree in the stands may play an important the individuals to utilize sub-optimal habitats (r a PPole , role in determining the bird species occurring in this type 1996). These two explanations held for Mottle-cheeked of habitat (e.g., Grebneer G & b reihci , 2005). Commercial Tyrannulet in the areas of commercial plantations, where plantations have expanded greatly in recent years. Hence, this generalist species can benefit from a wide variety there is a need to study the effects of this kind of system on of prey, occupying habitats with fewer resources, but animal populations and communities, in order to suggest also with fewer competitors. This may explain the use management practices to mitigate possible deleterious of a larger set of maneuvers and higher heights in Pinus effects. The findings of this study highlighted the importance without understory by the species. In shaded-coffee farms, of the presence of an understory and the native tree species j akcilde et al. (2006) found shift in the behavioral foraging A. angustifolia in commercial plantations to the foraging (mainly in height) by Rufous-capped Warbler (Basileuterus behavior of the species studied. Proper management of this rufifrons Swainson, 1838) to avoid seasonal competition forest habitat, with maintenance of understory and planting with migrant species. native species, may provide an important commercial The habitat structure of forest monocultures is alternative, and may also help in the conservation of the simpler than the native forests (a da Mík et al., 2003). fauna in silviculture areas contiguous to native forests. Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com Foraging behavioral of Phylloscartes ventralis (Aves, Tyrannidae)... 397 Acknowledgements. We thank the CNPq for a productivity k niel , r . M. 1978. Mapa fitogeográfico do estado de Santa Catarina: research grant received by SMH (306816/2010-5) and CAPES the resenha descritiva da cobertura original. Itajaí, SUDESUL, doctorate scholarship received by AML. We are grateful for the logistical FATMA e Herbário Barbosa Rodrigues. support of the staff of the Fazenda Florestal Gateados, especially Valdir k otler , b. P. & b roWn , j. S . 2007. Community ecology. In: StePhenS , Dhiel, Mário Dobner, and Maite Ribeiro. Andreas Kindel, Luiz dos Anjos, d. W.; b roWn , j. S. & y denberG , r. c. eds. Foraging: behavior and Paulo de Tarso Zuquim Antas made valuable suggestions during the and ecology. Chicago, The Chicago University Press, p. 397-476. manuscript preparation. k uSch , j.; W eber , c.; i delberGer , S. & k oob , t . 2004. Foraging habitat preferences of bats in relation to food supply and spatial vegetation REFERENCES structures in a western European low mountain range forest. Folia Zoologica 53:113-128. a ad Mkí , P.; k nanro , M. & v ketjo , j . 2003. The effect of habitat structure l att a , S. c . & Wunderle j r ., j . M. 1998. The assemblage of birds on guild patterns and the foraging strategies of insectivorous birds foraging in native West Indian pine (Pinus occidentalis) forests of in forests. Biologia 58:275-285. the Dominican Republic during the nonbreeding season. Biotropica a tM l ann , j . 1974. Observation study of behavior: sampling, methods. 30:645-656. Behaviour 49:227-267. l oše , P. & k or Pli , r . 2007. A comparison of three different approaches for b not le , W. 1985. Birds of Rio Grande do Sul, Brazil. Part 2. Formicariidae the classification of bird foraging guilds: an effect of leaf phenophase. through Corvidae. Bulletin of the American Museum of Natural Folia Zoologica 56:51-70. History 180:1-242. l yonS , j. e . 2005. Habitat-specific foraging of Prothonotary Warblers: c â Mara , i . c . 2003. Brief history conservation in the Atlantic Forest. In: deducing habitat quality. Condor 107:41-49. Godnila -l lae , c . & c â Mara , i . G. eds. The Atlantic Forest of South Mac a thrur , r . h . 1958. Population ecology of some warblers of America: biodiversity status, threats, and outlook. Washington, northeastern coniferous forests. Ecology 39:599-619. Conservation International, Island Press, p. 31-42. Mac a thurr , r. h. & Pianka , e. r . 1966. On optimal use of a patchy d iet Sch , t . v .; Per Fecot , i . & Greenber G, r . 2007. Avian foraging environment. American Naturalist 100:603-609. behavior in two different types of coffee agroecosystem in Chiapas, My anl , b. F. j . 1991. Randomisation and Monte Carlo methods in Mexico. Biotropica 39:232-240. biology. London, Chapman and Hall. 281p. Fitz Ptricak , j . W. 1980. Foraging behavior of Neotropical Tyrant _____. 1994. Multivariate statistical methods. London, Chapman Flycatchers. Condor 82:43-57. and Hall. 232p. _____. 2004. Family Tyrannidae (Tyrant-flycatchers). In: d el h oyo , j.; Marini , M. a. & c alcanti v a , r. b . 1993. Habitat and foraging substrate e lliott , a. & c hriStie , d. a. eds. Handbook of the birds of the use of three Basileuterus warblers from central Brazil. Ornitologia world. Vol. 9. Cotingas to Pipits and Wagtails. Barcelona, Lynx Neotropical 2:69-76. Edicions, p. 170-462. Mtinar , t . e . & k arr , j . r . 1990. Behavioral plasticity of foraging ForStMeier , W. & k e βler , a . 2001. Morphology and foraging behavior maneuvers of migratory Warblers: multiple selection periods for of Siberian Phylloscopus warblers. Journal of Avian Biology niches? Studies in Avian Biology 13:353-359. 32:127-138. Mreaur , b. a. & Wthi Meor , r. c . 1981. Foraging of five bird species in Franzeb , k. e. 1978. Tree species used by birds in logged and unlogged two forests with different vegetation structure. The Wilson Bulletin Mixed-coniferous Forests. The Wilson Bulletin 90:221-238. 93:478-490. _____. 1983. A comparison of avian foraging behavior in unlogged and Maçnodne -l i Ma , a .; h zt ra , S. M. & k ledni , a . 2004. Foraging behavior logged Mixed-coniferous Forest. The Wilson Bulletin 96:60-76. of the White-browed (Basileuterus leucoblepharus) and the Golden- Gleirba , v . a . & Pozi , M. a . 2005. Foraging behavior of tyrant flycatchers crowned (B. culicivorus) Warblers in a Semidecidual Forest in (Aves, Tyrannidae) in Brazil. Revista Brasileira de Zoologia Southern Brazil. Ornitologia Neotropical 15:5-15. 22:1072-1077. Mendonça -l i Ma , a .; d tuear , l . & h tzar , S. M. 2014. Comparing Grebneer G, r . & b reihci , P. 2005. Determinants of tree species preference diversity and dispersal traits of tree communities in plantations and of birds in Oak-Acacia woodlands of Central America. Journal of native forests in Southern Brazil. Natureza & Conservação 12:24-29. Tropical Ecology 21:57-66. Moer Mond , t . c . 1979. The influence of habitat structure on Anolis Gbbur , t . c . 1979. Factors controlling foraging strategies of insectivorous foraging behavior. Behaviour 70:147-167. birds. In: d ickSon , j. G.; c onnor , r. n.; F leet , r. r.; j ackSon , j. Parri Sh , j . d . 1995. Effects of needle architecture on warbler habitat a . & k roll , j . c . eds. The role of insectivorous birds in forest selection in a coastal Spruce Forest. Ecology 76:1813-1820. ecosystems. London, Academic Press, p. 119-135. Pillar , v . d . 2006. MULTIV: Multivariate exploratory analysis, h ol Me S, r . t . & r echer , h . F. 1986. Search tactics of insectivorous randomization testing and bootstrapping resampling, user’s guide birds foraging in an Australian eucalypt forest. Auk 103:515-530. v. 2. 4. Universidade Federal do Rio Grande do Sul, Porto Alegre, h lo Me S, r . t . & r nibo Sno , S. k . 1981. Tree species preferences of foraging Brazil. Available at: <http://ecoqua.ecologia.ufrgs.br/arquivos/ insectivorous birds in a northern Hardwoods Forest. Oecologia Software/Multiv/MultivManual.pdf >. Accessed at: 04.jan.2013. 48:31-35. Pralli , v . d . & o icólr , l . 1996. On randomization testing in vegetation _____. 1988. Spatial patterns, foraging tactics, and diets of ground- science: multifactor comparisons of revelé groups. Journal of foraging birds in a northern Hardwoods Forest. The Wilson Bulletin Vegetation Science 7:585-592. 100:377-394. Po Mara , l . y .; c oo Pre , r . j . & Ptite , l . j . 2003. Mixed-species flocking h t ol , r. d. & k riMbell , t . 2007. Foraging and population dynamics. and foraging behavior of four neotropical warblers in Panamanian In: Set Pneh S, d . W.; b or Wn , j . S. & y rebned G, r . c . eds. Foraging: shade coffee fields and forests. Auk 120:1000-1012. behavior and ecology. Chicago, The Chicago University Press, p. r a Mbo , b . a . 1951. A imigração da selva higrófila no Rio Grande do 365-396. Sul. Anais Botânicos do Herbário “Barbosa Rodrigues” 3:55-91. h utot , r . l . 1981. Seasonal variation in foraging behavior of some r aPPole , j. h . 1996. The importance of forest for the world’s migratory migratory western wood warblers. Auk 98:765-777. bird species. In: d e Gaar F, r . M. & Mrelli , r . i . eds. Conservation ibGe. 1992. Manual técnico da vegetação brasileira. Série manuais of faunal diversity in forested landscapes. London, Chapman and técnicos em geociências. Rio de Janeiro, IBGE. 92p. Hall, p. 389-406. j edlicka , j .; Greenber G, r .; Per Feoct , i .; Phil Pott , S. & d iet Sch , t . r eMSen , j. v ., j r . & r obinSon , S. k . 1990. A classification scheme for 2006. Seasonal shift in the foraging niche of a tropical avian resident: foraging behavior of birds in terrestrial habitats. Studies in Avian resource competition at work? Journal of Tropical Ecology 22:385- Biology 13:144-160. 395. r di Gy le , r . S. & t rodu , G. 2009. Field guide to the songbirds of South j nho Sno , M. d . 2000. Evaluation of an arthropod sampling technique for America: the passerines. Austin, University of Texas Press. 736p. measuring food availability for forest insectivorous birds. Journal r nibo Sno , S. k . & h lo Me S, r . t . 1982. Foraging behavior of forest birds: of Field Ornithology 71:88-109. the relationships among search tactics, diet, and habitat structure. Ecology 63:1918-1931. Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com 398 Mendonça -LiMa & Htzar r nibo Sno , S. k . & h lo Me S, r . t . 1984. Effects of plant species and foliage v lo Pot a , G. h .; Podar , v . M. & a ojn S, l . 2010. What can tree plantations structure on the foraging behavior of forest birds. Auk 101:672-684. do for forest birds in fragmented forest landscapes? A case study in r o Sário , l . a . M. 1996. As aves em Santa Catarina: distribuição southern Brazil. Forest Ecology and Management 260:1156-1163. geográfica e meio ambiente . Florianópolis, FATMA. 326p. Wther al , b. a . 2002. Grounded ground birds and surfing canopy birds: Sabo , S. r. & h olMeS , r. t . 1983. Foraging niches and the structure of variation of foraging stratum breadth observed in neotropical forest forest bird communities in contrasting montane habitats. Condor birds and tested with simulation models using boundary constraints. 85:121-138. Auk 119:658-675. Saant c artinaa . 1986. Atlas de Santa Catarina. Florianópolis, Wnaleh , c . j . 2001. Foliage structure influences foraging of insectivorous GAPLAN/SUEGI. 173p. forest birds: an experimental study. Ecology 82:219-231. Sick , h . 1997. Ornitologia brasileira. Rio de Janeiro, Nova Fronteira. Welrednu , j . M., j r . & l a tt a , S. c . 1998. Avian resource use in Dominican 912p. Shade Coffee Plantations. The Wilson Bulletin 110:271-281. SoareS , e. S. & a njoS , l . 1999. Efeito da fragmentação florestal sobre z a urit , G. a.; r ey , n.; v arela , d. M.; v illaGra , M. & b ellocq , M. i . aves escaladoras de tronco e galho na região de Londrina, norte 2006. Conversion of the Atlantic Forest into native and exotic tree do Estado do Paraná, Brasil. Ornitologia Neotropical 10:61-68. plantations: Effects on bird communities from the local and regional t ylor ra , M. a ., j r . & Fitz Ptrick a , j . W. 1982. A survey of the tyrant perspectives. Forest Ecology and Management 235:164-173. flycatchers. Living Bird 19:7-45. Received 12 August 2013. Accepted 23 December 2014. ISSN 0073-4721 Article available at: www.scielo.br/isz Iheringia, Série Zoologia, Porto Alegre, 104(4):391-398, 31 de dezembro de 2014 diagramação: letra1@editoraletra1.com

Journal

Iheringia. Série ZoologiaUnpaywall

Published: Dec 1, 2014

There are no references for this article.