Access the full text.
Sign up today, get DeepDyve free for 14 days.
Revista Brasileira de Ornitologia 25(1): 54–59. ARTICLE March 2017 The invas ive species rules: competitive exclusion in forest avian mixed-species flocks in a fragmented landscape 1,4 2 1 3 Marcos Maldonado-Coelho , Miguel Ângelo Marini , Fábio Raposo do Amaral & Rômulo Ribon Departamento de Ecologia e Biologia Evolutiva, Universidade Federal de São Paulo, CEP 09972-270, Diadema, SP, Brazil. Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade de Brasília, CEP 70910-900, Brasília, DF, Brazil. Museu de Zoologia João Moojen de Oliveira, Departamento de Biologia Animal, Universidade Federal de Viçosa, CEP 36570-000, Viçosa, MG, Brazil. Corresponding author: firstname.lastname@example.org Received on 30 September 2016. Accepted on 26 May 2017. This study contains Supplementary Information (Table S1) available only online. ABSTRACT: Evidence of checkerboard patterns of species' distribution in avian mixed-species flocks suggest that competition is one of the forces shaping the composition and structure of these associations. However, evidence of competition among flock species comes from studies performed in well-preserved regions and no study has reported the interactions between invasive and native flocking species in human-modified landscapes. Such studies are important because evidence show that avian social systems such as mixed-species flocks suffer several negative impacts of habitat fragmentation. In this study, it is shown that an invasive woodcreeper (Lepidocolaptes angustirostris) from open areas of central and western South America is: 1) expanding its range into that of a native Atlantic Forest woodcreeper (L. squamatus); 2) using the same forest fragments in which the native woodcreeper occurs; 3) regularly joining Atlantic Forest mixed-species flocks that contain the native woodcreeper; 4) overlapping in foraging height with the native woodcreeper during flocking; and 5) engaging in aggressive encounters and excluding the native woodcreeper from flocks. We suggest that this aggressive behavior is a consequence of the overlap in foraging height between the invasive and native species in their original habitats and that their contact has so recently been established. This study suggests that competitive interactions mediated by aggressive behaviors of invasive species may have a negative impact on the fitness of native mixed-species flock species in a fragmented landscape. KEY-WORDS: Atlantic Forest, biological invasion, foraging behavior, habitat fragmentation, multispecific interactions. INTRODUCTION programs performed in relatively well-preserved regions (e.g. Graves & Gotelli 1993, Colorado & Rodewald Interspecific competition and aggression mediate species' 2015) and no study has yet documented the interactions spatial segregation and occupation in a number of avian between invasive and native flocking species in human- communities (e.g. Robinson & Terborgh 1995, Jankowski modified landscapes. This is relevant because Neotropical avian social systems such as mixed-species flocks and et al. 2010). Evidence of assembly patterns suggest that these deterministic processes also shape the composition army ant followers are known to be negatively affected and structure of avian mixed-species flocks (e.g. Graves by habitat disturbance, including forest fragmentation & Gotelli 1993, Colorado & Rodewald 2015). Mixed- (Stouffer & Bierregaar d-Jr. 1995, Maldonado-Coelho species flocks are mutualistic associations between two & Marini 2004, Mokross et al. 2014). In this study, we show that the Cerrado Woodcreeper, Lepidocolaptes or more species, and hypothesized advantages for birds that join such flocks are decreased predation risks and/ angustirostris (hereafter “invasive woodcreeper”) is: 1) or increased foraging efficiency (e.g. Morse 1977, Powell expanding its range into that of the native Atlantic Forest 1985). However, direct aggressive interactions in these woodcreeper, Lepidocolaptes squamatus (hereafter “native associations can lead to local exclusion of subordinate bird woodcreeper”); 2) using the same forest fragments in which the native woodcreeper occurs; 3) regularly joining species by the dominant species (Pierpont 1986, Graves & Gotelli 1993). Thus, avian mixed-species flocks offer an Atlantic Forest mixed-species flocks containing the exceptional opportunity to investigate species interactions native woodcreeper; 4) overlapping in foraging height as many species, including closely related ones, can be with the native woodcreeper during flocking; and 5) found in the same flock. E vidence of competition among engaging in aggressive encounters and excluding the native woodcreeper from flocks. The invasive species avian mixed-species flocking species come from research Revista Brasileira de Ornitologia 25(1): 2017 The invasive species rules: competitive exclusion in forest avian mixed-species flocks in a fragmented landscape Maldonado-Coelho et al. either aggressively interfere with foraging activities or 42°48'45'' – 42°56'15''W), southeastern state of Minas completely exclude the subordinate native species from Gerais, Brazil (Fig. 1). This region was covered by pristine the flocks. We discuss how these negative interactions forest until the middle 1800's, when scattered farms could affect the fitness of the native species. producing food for the gold mines of the municipality of Ouro Preto, Minas Gerais, began to appear (Brandt 2004). Several habitat sensitive Atlantic Forest endemic METHODS birds were still present in the area in the 1930's (Ribon et al. 2003). Currently, the original Atlantic Forest is Species studied, study area and mixed-species flock highly fragmented (33.5% of native forest remains) and observations the forest remnants are second-growth forests embedded in a matrix of pastures and crops. Details on the studied The native woodcreeper is commonly observed foraging area, on the bird communities, and on mixed-species in the canopy and sub-canopy of primary and secondary flock sampling can be found in previous published works growth of moist, semideciduous and dry forests in (Ribon et al. 2003, Maldonado-Coelho & Marini 2004). eastern Brazil, where it regularly participates in mixed- species flocks (Develey & Peres 2000, Maldonado- Geographic expansion of the invasive woodcreeper Coelho & Marini 2004). The invasive woodcreeper has a broader geographic distribution, inhabiting semi-open We did not rely on geographic distributions described and forested vegetation physiognomies of the Cerrado, in field guides as these may present large inaccuracies Chaco and Caatinga Biomes (Sick 1997). It is a regular on species' ranges (e.g. Lopes 2008). For example, species in mixed-species flocks in open habitats in central range maps of the invasive woodcreeper in the most South America (Alves & Cavalcanti 1996). The invasive popular Neotropical guide (Ridgely & Tudor 1994) is woodcreeper is slightly larger (average 31 g, Marini et misleading, as it shows an erroneous historical (i.e. prior al. 1997) than the native woodcreeper (average 30 g, to deforestation) occurrence of this species in the Atlantic M.Â.M, unpubl. data). In the Atlantic Forest, the invasive Forest. Instead, we used an extensive database that woodcreeper is expanding its distribution in the wake of includes geographical localities from museum specimens forest destruction (Sick 1997). (Bolívar-Leguizamón & Silveira 2015) and from reliable The study region is located in the municipality of photographic records deposited in the Wikiaves database Viçosa and Paula Cândido (20°42'30'' – 20°50'00''S; (Table S1, Supplementary Information). Figure 1. Geographic distribution of the invasive woodcreeper (gray dots), Lepidocolaptes angustirostris, and the native woodcreeper (black stars) (A). The native woodcreeper is represented by the two Atlantic Forest species of the complex Lepidocolaptes squamatus/falcinellus/wagleri. The distribution of the third member of this species complex, L. wagleri, from the dry forests of central Brazil is not presented here. In (B), region of sympatry between the invasive and the native woodcreepers in the Atlantic Forest. The red circle represents the study area and t he green shaded area depicts the historical distribution of the Atlantic Forest, before large-scale deforestation. See Table S1 (Supplementary Information) for records used and descriptions of coordinate sources. Revista Brasileira de Ornitologia 25(1): 2017 The invasive species rules: competitive exclusion in forest avian mixed-species flocks in a fragmented landscape Maldonado-Coelho et al. Forest fragment use and abundance of the invasive the aim was to assess if the two woodcreeper species and native woodcreepers presented any differences in behavior when associated in mixed-species flocks. Seven 2 m c lasses of foraging heights From May 1996 to November 1999, 236 points located were defined and estimated by eye. Information on each in 41 forest fragments were sampled six times each. Forest foraging bout was collected in intervals of 5 minutes to fragment sizes ranged from 1 to 384.5 ha. All the point avoid pseudoreplication. In all recorded foraging bouts, counts were located by at least 50 m from forest fragment the individuals were always searching for prey on tree borders and were separated from one another by at trunks; hence, the foraging heights recorded were assumed least 150 m. All the birds seen or heard were recorded, to represent the actual foraging heights, even though independently of their distance from the observer individuals were only occasionally seen capturing prey. (unlimited point-count). Counting birds lasted 10 min at each sampling point, starting at sunrise to about 10:00 RESULTS h and from 16:00–17:00 h to sunset. No sampling was conducted under rain or strong wind. A bird was only Geographic expansion of the invasive woodcreeper recorded when the observer was sure that it was inside the forest fragment. An index of abundance per point (IAP) When mapping the invasive woodcreeper records onto the for both species was obtained by dividing the detected historical distribution of the Atlantic Forest (prior to forest number of individuals of each species by the total number destruction), a clear colonization pattern into this biome of samples (i.e. point-counts) in each fragment. IAP was emerges (Fig. 1). A detailed account of the colonization plotted against fragment size to show the distribution history of the invasive woodcreeper is beyond the scope of and abundance of both species in forest fragments in the this study, but two important aspects uncovered here are studied region. that: 1) this species has invaded the Atlantic Forest Biome in the central and southeastern regions (Fig. 1); and 2) Mixed-species flocks par ticipation by the invasive currently, this species overlaps extensively with the native woodcreeper woodcreeper in central Atlantic Forest (Fig. 1). The forest fragments studied had sizes of 3.6, 7.6, 9.4, Forest fragment use and abundance of the invasive 38.8, 45.1, 75.0, 120.0, 181.2 and 384.5 ha. These and native woodcreepers forest fragments were included in the same set of fragments sampled by point-counts. Mixed-species flock The invasive woodcreeper was recor ded in only a observations were performed during the rainy (October few forest remnants and, in all instances, had low 1998–January 1999) and dry (May–August 1999) seasons abundance. On the other hand, the native woodcreeper and flock observations were conducted between 06:30 was widespread in the studied area and its abundance h and 12:00 h and between 15:00 h and 18:00 h. The was not affected by the area of forest fragments (r = invasive woodcreeper was observed interacting with the 0.011, P > 0.05; Fig. 2). native woodcreeper species in flocks in the forest fragment of 9.4 ha. From the nine forest fragments studied, this was the only forest fragment in which the invasive woodcreeper was observed participating in mixed-species flocks - probably because of its recent colonization in the region (R.R., pers. obs.). Foraging height use pattern of the invasive and native woodcreepers The foraging observations on the native woodcreeper were carried out in all nine forest fragments in which flocks were studied, whereas foraging behavior of the invasive woodcreeper and all interactions between the two species were observed only in the 9.4 ha forest fragment (see Figure 2. Abundance of the invasive (Lepidocolaptes angustirostris, above). Foraging observations were performed during black diamonds) and native (Lepidocolaptes squamatus, open circles) the rainy and dry seasons and foraging heights were only woodcreepers as a function of forest fragment size in the area of study. obtained when the species were associated in mixed- Unbroken and broken lines represent respectively the fit of a linear species flocks. In a comparison of foraging height use, model and associated confidence intervals. Revista Brasileira de Ornitologia 25(1): 2017 The invasive species rules: competitive exclusion in forest avian mixed-species flocks in a fragmented landscape Maldonado-Coelho et al. Foraging height use pattern of the invasive and native shifts in foraging height of the native woodcreeper in woodcreepers response to the presence of the invasive woodcreeper in mixed-species flocks. That is, we wanted to assess if The analysis indicates that the two species differed in individuals of the native woodcreeper exhibited a pattern foraging height distribution (Kolmogorov-Smirnov two- of ecological character displacement (Pfennig & Pfennig sample test; D = 0.289, P < 0.05; n = 64, 2009). Native woodcreepers in mixed-species flocks in invasive-woodcreeper n = 94; Fig. 3). This difference in foraging which the invasive woodcreeper participated did not native-woodcreeper height distribution is because individuals of the invasive show differences in foraging height distribution from woodcreeper did not show preferences in foraging height native woodcreepers in mixed-species flocks in which t he classes whereas individuals of the native woodcreeper invasive woodcreeper was absent (i.e. in the other eight exhibited a preference for the upper levels of trees. In forest fragments; Kolmogorov-Smirnov two-sample test; the second comparison of foraging height use, the goal D = 0.131, P > 0.05; n = 94, n = 9.4 forest fragment other forest fragments was to assess if there were any detectable behavioral 323; Fig. 3). A B Figure 3. Proportion of foraging height distribution use for the two Lepidocolaptes species when associated with mixed-species flocks in the 9.4 ha forest fragment (A). Proportion of foraging height distribution use for the native woodcreeper (L. squamatus) individuals when associated with mixed-species flocks in the 9.4 ha forest fragment and for individuals of this species when associated with mixed-species flocks in the other eight forest fragments (B). Agonistic interactions between the invasive and will often be dominant (Willis & Oniki 1978, Pierpont native woodcreepers 1986, Graves & Gotelli 1993). The invasive woodcreeper is only slightly larger than the native woodcreeper; Twenty-nine mixed species flocks were followe d in the 9.4 hence, its dominance over the native species could be forest fragment. The invasive woodcreeper was observed mediated by some behavioral aspect such as a stronger joining six flocks, all in which t he native woodcreeper interspecific territoriality. The invasive woodcreeper was was participating. Six aggressive interactions in different regularly observed in isolated trees along pastures and flocks were observed between the two species. In two of agricultural lands surrounding the 9.4 ha forest fragment. the interactions, the native woodcreeper was excluded Most Cerrado bird species that join flocks (sensu A lves completely from the flocks after being attacked by the & Cavalcanti 1996) and Cerrado mixed-species flocks invasive woodcreeper and it was not observed rejoining themselves are absent from the region. Thus, one possibility the flocks after the next two hours of observation. In is that, in order to gain the two main benefits of mixed- the remaining four interactions, the native woodcreeper species flocking—predator avoidance and increased shifted foraging height and branch (n = 2) or tree (n = 2) foraging efficiency (Morse 1977, Powell 1985)—the when attacked by the invasive woodcreeper. invasive woodcreeper enters the forest fragment to join flocks. It is noteworthy that five out of the six recor ds of the invasive woodcreeper in mixed-species forest flocks DISCUSSION were made in the dry season, a period of food shortage for insectivorous birds in the Atlantic Forest (Develey & Peres Competitive exclusion by more aggressive bird species 2000). Thus, the invasive woodcreeper likely increases is a common pattern in mixed-species flocks and over its frequency of participation in forest flocks during this army ants. In such social organizations, the larger species season to augment food intake. However, a consequence Revista Brasileira de Ornitologia 25(1): 2017 The invasive species rules: competitive exclusion in forest avian mixed-species flocks in a fragmented landscape Maldonado-Coelho et al. of its mixed-species forest flock attendance is disturbance but they may not be extensive at the population level. and exclusion of the subordinate native woodcreeper. Future studies should assess this possibility by comparing Sympatric species may be under selective pressures to fitness of native woodcreeper individuals in the presence avoid the negative effects of competition and consequently and absence of the invasive woodcreeper. evolve differences in habitat use, foraging behavior and Finally, two caveats of this study are the lack of body dimensions (Schoener 1965, Murray-Jr. 1971). replicates of fragments in which the invasive and native Species that interact in mixed-species flocks in any region woodcreepers interact in mixed-species flocks and t he could have co-evolved syntopically for thousands of small sample size of their agonistic interactions. Although generations and hence could have had enough time to this limits the generalization of our study, the preliminary evolve ecological segregation in one or more dimensions. evidence of negative interactions in flocks highlights the Although the two woodcreeper species exhibited distinct importance of additional studies, both in the Atlantic foraging height distributions, the overlap was extensive. Forest and elsewhere in the Neotropics. The observed interspecific aggression in this study can be a transitory phase given the short period of contact ACKNOWLEDGEMENTS between them (Murray-Jr. 1971). In fact, it is expected that the frequency in which negative interactions occur Funding was provided by Coordenação de Aperfeiçoamento will decrease over time. As such, interactions can be de Pessoal de Nível Superior (CAPES) to M.M.-C. at energetically costly for both subordinate and dominant the Graduate Program in Ecology and Evolution from species. Thus, that the two woodcreepers only recently Federal University of São Paulo (UNIFESP-Diadema), came into contact implies that ecological segregation Fundação de Amparo à Pesquisa do Estado de São Paulo (i.e. character displacement) have not had time to evolve. (FAPESP) and the Biota Program (2010/05445-2 and Evidence in support of this idea is the overlapping 2015/18287-0 to M.M.-C.; 2011/50143-7, 2011/23155- foraging height distributions of native woodcreepers in 4 and 2013/50297-0 to F.R.A.) and National Science flocks in which t he invasive woodcreeper is absent and in Foundation DOB 1343578 (F.R.A). We thank World which it is present. Wildlife Fund (WWF) and the Graduate Program In the present study, we have shown that the process of Ecology, Conservation and Wildlife Management of Atlantic Forest fragmentation has led to the invasion (ECMVS) from Federal University of Minas Gerais of an aggressively dominant species from the adjacent (UFMG) for financial support. The Conselho Brasileiro de Cerrado Biome. We have also shown that the native Desenvolvimento Científico e Tecnológico (CNPq) provi ded woodcreeper, which regularly join mixed-species flocks fellowships to all authors. M.Â.M. received a researcher all year round (Maldonado-Coelho & Marini 2003), fellowship from CNPq. R.R. is thankful to Programa experiences foraging interference and flock exclusion as a Natureza e Sociedade WWF/SUNY projeto CSR 142-00, result of agonistic interactions with the invasive species. CNPq, CAPES, PROBIO-Ministério do Meio Ambiente/ It is reasonable to expect that such foraging interference World Bank/Global Environmental Facility. M.M.-C., and competitive exclusion will result in reduced fitness in M.Â.M., F.R.A. and R.R. conceived the idea, design, the native woodcreeper, as the benefits of participating in experiment (supervised research, formulated question or mixed-species flocks would be lost or largely diminished. hypothesis) and wrote the paper. M.M.-C., F.R.A. and Those individuals disturbed when foraging, and certainly R.R. performed the experiments and analyzed the data those excluded from flocks, are likely to experience a (collected data, conducted the research). This study was decrease in foraging efficiency and an elevated risk of carried out in strict accordance with the recommendations predation. This can be critical because: i) the frequency of in the use of animals for research in Brazilian universities. the invasive woodcreeper in flocks were higher during the period of food shortage (i.e. the dry season), ii) competitive exclusion from flocks can be detrimental to the fitness of REFERENCES the native species mainly in small and potentially food depleted forest fragments (e.g. Zanette et al. 2000), and Alves M.A.S. & Cavalcanti R.B. 1996. Sentinel behavior, seasonality, iii) sympatry between the two woodcreepers is extensive and the structure of bird flocks in a Brazilian savanna. Orni tología in southeastern Atlantic Forest, and ongoing competition Neotropical 7: 43–51. can be pervasive across their area of overlap. However, one Bolívar-Leguizamón S. & Silveira L.F. 2015. Morphological variation and taxonomy of Lepidocolaptes angustirostris (Vieillot, 1818) positive finding of this study is the reduced a bundance (Passeriformes: Dendrocolaptidae). Papéis Avulsos de Zoologia, São and occurrence of the invasive woodcreeper in the Paulo 55: 281–316. sampled forest fragments. This implies that the negative Brandt A. 2004. Desbravamento, caminhos antigos e povoamento dos interactions reported here could have an impact on the Sertões do Leste: uma aventura de pioneiros. Viçosa: Centro de native woodcreeper at the level of interacting individuals, Referência do Professor. Revista Brasileira de Ornitologia 25(1): 2017 The invasive species rules: competitive exclusion in forest avian mixed-species flocks in a fragmented landscape Maldonado-Coelho et al. Colorado G.J. & Rodewald A.D. 2015. Assembly patterns of mixed- Pfennig K.S. & Pfennig D.W. 2009. Character displacement: species avian flocks in the Andes. Journal of Animal Ecology 84: ecological and reproductive responses to a common evolutionary 386–395. problem. Quarterly Review of Biology 84: 253–276. Develey P.F. & Peres C.A. 2000. Resource seasonality and the Pierpont N. 1986. Interspecific aggression and the ecology of woodcreepers structure of mixed species bird flocks in a coastal At lantic Forest (Aves: Dendrocolaptidae). Ph.D. Thesis. Princeton: Princeton of southeastern Brazil. Journal of Tropical Ecology 16: 33–53. University. Graves G.R. & Gotelli N.J. 1993. Assembly of avian mixed-species Powell G.V.N. 1985. Sociobiology and adaptive significance of flocks in Amazonia. Proceedings of the National Academy of Sciences interspecific foraging flocks in the Neotropics, p. 713–732. In: of the United States of America 90: 1388–1391. Buckley P.A., Foster M.S., Morton E.S., Ridgely R.S. & Buckley Jankowski J.E., Robinson S.K. & Levey D.J. 2010. Squeezed at the F.G. (eds.). Neotropical ornithology. Ornithological Monographs 36: top: interspecific aggression may constrain elevational ranges in 713–732. tropical birds. Ecology 91: 1877–1884. Ribon R., Simon J.E. & Mattos G.T. 2003. Bird extinctions in Lopes L.E. 2008. The range of the Curl-crested Jay: lessons for Atlantic Forest fragments of the Viçosa region, southeastern evaluating bird endemism in the South American Cerrado. Brazil. Conservation Biology 17: 1827–1839. Diversity and Distributions 14: 561–568. Ridgely R.S. & Tudor G. 1994. The bir ds of South America, v. 2, the Maldonado-Coelho M. & Marini M.Â. 2003. Composição de bandos Suboscine Passerines. Austin: University of Texas Press. mistos de aves em fragmentos de Mata Atlântica no sudeste do Robinson S.K. & Terborgh J. 1995. Interspecific aggression and Brasil. Papéis Avulsos de Zoologia, São Paulo 43: 31–54. habitat selection by Amazonian birds. Journal of Animal Ecology Maldonado-Coelho M. & Marini M.Â. 2004. Mixed-species 64: 1–11. bird flocks from Brazilian Atlantic Forest: the effects of forest Schoener T.W. 1965. The evolution of bill size differences among fragmentation and seasonality on their size, richness and stability. sympatric congeneric species of birds. Evolution 19: 189–213. Biological Conservation 116: 19–26. Sick H. 1997. Ornitologia Brasileira. Rio de Janeiro: Editora Nova Marini M.Â., Motta-Junior J.C., Vasconcellos L.A.S. & Cavalcanti Fronteira. R.B. 1997. Avian body masses from the Cerrado region of central Stouffer P.C. & Bierregaar d-Jr. R.O. 1995. Use of Amazonian Forest Brazil. Ornitología Neotropical 8: 93–99. fragments by understory insectivorous birds. Ecology 76: 2429– Mokross K., Ryder T.B., Côrtes M.C., Wolfe J.D. & Stouffer P.C. 2445. 2014. Decay of interspecific avian flock networks along a Willis E.O. & Oniki Y. 1978. Birds and army ants. Annual Review of disturbance gradient in Amazonia. Proceedings of the Royal Society Ecology and Systematics 9: 243–263. of London B: Biological Sciences 281: 20132599. Zanette L., Doyle P. & Trémont S.M. 2000. Food shortage in small Morse D.H. 1977. Feeding behavior and predator avoidance in fragments: evidence from an area-sensitive passerine. Ecology 81: heterospecific groups. BioScience 27: 332–339. 1654–1666. Murray-Jr., B.G. 1971. The ecological consequences of interspecific territorial behavior in birds. Ecology 52: 414–423. Associate Editor: Gustavo S. Cabanne. Revista Brasileira de Ornitologia 25(1): 2017
Ornithology Research – Springer Journals
Published: Mar 1, 2017
Keywords: Atlantic Forest; biological invasion; foraging behavior; habitat fragmentation; multispecific interactions
Access the full text.
Sign up today, get DeepDyve free for 14 days.