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Birds as potential pollinators of the Spathodea nilotica (Bignoniaceae) in the urban environment

Aves como potenciais polinizadoras de Spathodea nilotica (Bignoniaceae) em ambiente urbano

Abstracts

Birds play crucial role on the pollination of many plants. However, little is known about the interactions between nectarivorous neotropical birds and exotic Angiosperms. S. nilotica is an exotic African plant widely used in Brazilian urban landscaping. However, it has been poorly studied in relation to its interactions with Neotropical birds. In this way, we studied the feeding nectar strategies and the interspecific antagonistic behaviours among nectarivorous Neotropical birds to verify the bird contributions to the S. nilotica pollination. The study was conducted from May 2008 to April 2011, but only in months of S. nilotica flowering (April to May). From 148 hours of sampling we identified 16 species feeding nectar on S. nilotica: 13 hummingbirds (Trochilidae), Aratinga aurea (Psittacidae), Tangara palmarum (Thraupidae) and Coereba flaveola (Coerebidae). Eupetomena macroura was the most frequent (96.88%), followed by Chlorostilbon lucidus (78.13%) and Coereba flaveola (59.38%). Most birds obtained nectar by punching at the base of the corolla, except for A. aurea that obtained the nectar by the upper opening of the petals in 100% of its visits, Heliomaster furcifer (95.65%), F. fusca (95%) and A. nigricollis (70.27%). Despite E. macroura also obtains nectar only by punching at the base of the corolla, it showed the highest level of legitimate visits. Antagonistic events were more frequent in E. macroura (58.65%), Florisuga fusca (11.04%) and Amazilia fimbriata (10.87%), being E. macroura dominant in all events. These results showed E. macroura plays an important role on this plant being the most important bird as a potential pollinator. Moreover, other birds contribute partially to the S. nilotica pollination. Most probably it is a result of recent Neotropical bird interactions with this African plant.

nectarivorus Neotropical birds; african-tulip-tree; nectar exploitation


As aves representam um grupo ecologicamente importante nas interações animais-flores na região Neotropical, onde desempenham respeitável papel na polinização de diversas angiospermas. Entretanto, pouco se conhece sobre a organização das comunidades e as interações bióticas entre animais/plantas em ambientes urbanos. Como exemplo, S. nilotica, planta exótica africana amplamente explorada para fins de paisagismo urbano, têm sido pouco estudada em relação às suas interações com aves. Assim, analisamos quais espécies de aves visitam S. nilotica, o tipo de exploração dos recursos nectarívoros pelas aves e o comportamento antagonístico intra e interespecífico das aves que visitaram esta planta. O estudo foi realizado de maio de 2008 a abril de 2011, nos meses de florescimento de S. nilotica (abril a maio). Foram totalizadas 148 horas de amostragem e identificadas 16 espécies se alimentando de néctar, 13 beija-flores (Trochilidae), Aratinga aurea (Psittacidae), Tangara palmarum (Thraupidae) e Coereba flaveola (Coerebidae). As aves mais frequentes foram Eupetomena macroura (96,88%), Chlorostilbon lucidus (78,13%) e Coereba flaveola (59,38%). A frequência de visitas foi maior no período matutino, exceto para E. macroura, H. longirostris e T. palmarum. A maioria das aves obteve o néctar através de rompimento na base da corola (orifícios), com exceção de A. aurea que obteve néctar pela abertura superior entre as pétalas em 100% de suas visitas e H. furcifer (95,65%), F. fusca (95%) e A. nigricollis (70,27%). Eventos antagonísticos foram mais acentuados em E. macroura (58,65%), Florisuga fusca (11,04%) e Amazilia fimbriata (10,87%), sendo E. macroura dominante durante os eventos. Os resultados demonstram que E. macroura é a ave dominante em S. nilotica e a que se apresenta com maior potencial para sua polinização. Entretanto, as outras aves contribuem parcialmente como potenciais polinizadoras de S. nilotica. Muito provavelmente isto é resultado de uma interação recente entre as aves neotropicais e esta planta Africana.

aves nectarívoras; tulipeira; exploração de néctar


1.

Introduction

Urbanisation modifies significantly both the physical structure and biotic habitat and it may affect many ecological processes. As a result of human intervention, the urban landscape generally has fragmented into a mosaic of different environments and both vegetation structure and floristic composition usually differ from that was originally present (Argel-de-Oliveira, 1996ARGEL-DE-OLIVEIRA, MM., 1996. Aves urbanas. In VIELLIARD, JM., SILVA, ML. and SILVA, WR. (Eds.). Anais V Congresso Brasileiro de Ornitologia, Campinas. p. 151-162.).

Birds, especially hummingbirds, represent a group numerically and ecologically dominant in flower-animal interactions in the Neotropics (Stiles, 1981STILES, FG., 1981. Geographical aspects of bird-flower coevolution, with particular reference to Central America. Annals of the Missouri Botanical Garden, vol. 68, p. 323-351.). They are also very successful in urban areas (Gilbert, 1989GILBERT, OL., 1989. The ecology of urban habitats, New York: Chapman and Hall, 369 p.; Marsluff et. al., 2001MARSLUFF, JM., BOWMAN, R. and DONNELLY, R., 2001. Avian ecology and conservation in an urbanizing world. Boston: Kluwer Academic Publishers. 585 p.) where they play an important role in the pollination of many flowering plants (Mendonça and Anjos, 2003MENDONÇA, LB. and ANJOS, L., 2003. Bird flower interactions in Brazil: a review. Ararajuba, vol. 11, no. 2, p. 195-205.). However, there are few studies conducted in urban areas of the Brazilian Biomes (Mendonça and Anjos, 2003MENDONÇA, LB. and ANJOS, L., 2003. Bird flower interactions in Brazil: a review. Ararajuba, vol. 11, no. 2, p. 195-205.).

Ornithophilous plants are characterised by the presence of diurnal anthesis flowers, odourless, of conspicuous coloration, with the production of large amounts of nectar, but low concentration of sugars in their nectarines. In addition their nectarines are not close to the fertile parts, normally exposed (Faegri and Pijl, 1979FAEGRI, K. and PIJL, L., 1979. The principles of pollination ecology. New York: Pergamon Press. 244 p.). However, the majority of flower-animal interaction studies has been focussed on areas that have been little disturbed (Ragusa-Neto, 2002RAGUSA-NETO, J., 2002. Exploitation of Erythrina dominguezii Hassl. (Fabaceae) nectar by perching birds in a dry forest in western Brazil. Brazilian Journal of Biology, vol. 62, no. 4B, p. 877-883.; Antunes 2003ANTUNES, AZ., 2003. Partilha de néctar de Eucalyptus spp., territorialidade e hierarquia de dominância em beija-flores (Aves: Trochilidae) no sudeste do Brasil. Ararajuba, vol. 11, no. 1, p. 39-44.; and Machado et. al., 2007MACHADO, CG., COELHO, AG., SANTANA, CS. and RODRIGUES, M., 2007. Beija-flores e seus recursos florais em uma área de campo rupestre da Chapada Diamantina, Bahia. Revista Brasileira de Ornitologia, vol. 15, no. 2, p. 267-279.), and as a result, little is known about the organisation of communities and biotic interactions between plants and animals in urban environments (Mendonça and Anjos, 2005). The understanding of these issues supports the choice of more effective measures for bird conservation, which in turn ensures the reproduction of visited plants and the supply of food resources needed (Piratelli, 1997PIRATELLI, AJ., 1997. Comportamento alimentar de beija-flores em duas espécies de Hippeastrum HERB. (Amaryllidaceae). Brazilian Journal of Biology, vol. 57, no. 2, p. 261-273.).

Spathodea nilotica is an exotic plant, originated in Central Africa. It is typical from warm regions and it is widely introduced in Brazilian urban environments (Lorenzi et. al., 2003LORENZI, H., SOUZA, HM., TORRES, MAV. and BACHER, LB., 2003. Árvores exóticas no Brasil. Madeireiras, ornamentais e aromáticas. Nova Odessa, Brasil: Instituto Plantarum de Estudos da Flora. 368 p.). Nogueira-Neto (1970)NOGUEIRA-NETO, P., 1970. A criação de abelhas indígenas sem ferrão (Meliponinae). São Paulo: Tecnapis. 365 p. noted that since S. nilotica was introduced into Brazil, this has been the cause of substantial mortality of native bees.

Exotic plants used in ornamental gardens are exploited by birds and they can contribute to the persistence of many bird species, including migratory ones (Corlett, 2005CORLETT, RT., 2005. Interactions between birds, fruit bats and exotic plants in urban Hong Kong, South China. Urban Ecology, vol. 8, p. 275-283.; Mendonça and Anjos, 2005). However, studies are rare on the ecological interactions between S. nilotica and Neotropical birds (Mendonça and Anjos, 2005). So further investigations are necessary on how Neotropical birds explore the nectarivorous resources from S. nilotica.

Thus, we recorded the birds that visited S. nilotica to: a) describe how the nectarivorous resources are exploited by birds; b) determine if these birds are potential pollinators of the S. nilotica and c) observe the bird territoriality and domination at flowering periods.

2.

Material and Methods

We conducted this study in different urban regions in the Três Lagoas municipality, Mato Grosso do Sul state. The climate is tropical humid, AW type, according to Köppen, with the dry season from April to September and wet season, from October to March. There is no significant variation on temperature and the annual medial temperature is 24.1 °C (Pinto, 1994PINTO, MN., 1994. Cerrado. Brasília: Editora Universidade de Brasília. 681 p.).

We observed five specimens of S. nilotica (Bignoniaceae) during tree flowering periods: May 2008, February, May and June 2009 and April 2011. Observations were made during daytime in two periods: 1) morning, from 6:00 to 9:00; 2) afternoon, from 14:00 to 17:00. The rainy days were discarded.

The birds were observed with binoculars (8×25 and 8×42). We first recorded the bird species, then we verified how it exploited the resources of the flower according to Machado (2009)MACHADO, CG., 2009. Beija-flores (Aves: Trochilidae) e seus recursos florais em uma área de caatinga da Chapada Diamantina, Bahia. Revista Brasileira de Zoologia, vol. 26, no. 2, p. 255-265.: a) the legitimate visit is characterised by contacting the reproductive organs of the plant and it leads the pollen attached to the beak or to the dorsal or ventral portions of the head b) the illegitimate visits, in which the bird pierces the flower at the base of the corolla, absorbing the nectar directly without contact with the pollen. We considered only the legitimate visits in order to identify those birds that would be potential pollinators on S. nilotica.

Finally, we observed whether there were intra and interspecific antagonistic interactions. The interaction is considered by the attacks and/or persecution, but the vocalisations are ignored, as proposed by Machado (2009)MACHADO, CG., 2009. Beija-flores (Aves: Trochilidae) e seus recursos florais em uma área de caatinga da Chapada Diamantina, Bahia. Revista Brasileira de Zoologia, vol. 26, no. 2, p. 255-265.. This approach is important to point out the most dominant birds that explore the S. nilotica nectar in order to determine their potential importance in pollination.

For bird identification we used field guides (Dunning 1987DUNNING, JS., 1987. South american birds. Newtown Square: Harrowod Books. 351 p., Develey and Endrigo, 2004DEVELEY, PF. and ENDRIGO, E., 2004. Guia de campo das aves da grande São Paulo. São Paulo: Aves e Fotos. 295 p.; Erize et. al., 2006ERIZE, F., MATA, JR. and RUMBOLL, M., 2006. Birds of South America. Princeton: Princeton University Press. 384 p.). For the plant identification we used Lorenzi (2003)LORENZI, H., SOUZA, HM., TORRES, MAV. and BACHER, LB., 2003. Árvores exóticas no Brasil. Madeireiras, ornamentais e aromáticas. Nova Odessa, Brasil: Instituto Plantarum de Estudos da Flora. 368 p.. The classification and taxonomy of the bird species followed the CBRO list (2011).

We calculated the frequency of occurrence of species, inter and intraspecific antagonistic behaviour, and foraging strategy of nectarivorous birds on S. nilotica.

3.

Results

We performed 148 hours of observation, 74 in the morning and 74 in the afternoon, over 32 days. We recorded 16 nectarivorous bird species exploiting S. nilotica. They belong to four families: a) Psittacidae: Aratinga aurea (Gmelin, 1788); b) Trochilidae: Amazilia fimbriata (Gmelin, 1788), A. versicolor (Vieillot, 1818), Anthracothorax nigricollis (Vieillot, 1817), Campylopterus largipennis (Boddaert, 1783), Chlorostilbon lucidus (Shaw, 1812), Chrysolampis mosquitus (Linnaeus, 1758), Eupetomena macroura (Gmelin, 1788), Florisuga fusca (Vieillot, 1817), Heliomaster furcifer (Shaw, 1812), H. longirostris (Audebert and Vieillot, 1801), Hylocharis chrysura (Shaw, 1812), H. sapphirina (Gmelin, 1788), Polytmus guainumbi (Pallas, 1764); c) Thraupidae: Tangara palmarum (Wied, 1823) and d) Coerebidae: Coereba flaveola (Linnaeus, 1758).

Eupetomena macroura was the most frequent species (51 events of visits = 20.39%), followed by C. lucidus with 33 events (16.45%) and C. flaveola with 25 events (12.50%) (Table 1). Most birds were more frequent in the morning, but E. macroura visited the periods equally (49.02% and 50.98%, respectively). On the other hand, T. palmarum and H. longirostris were only observed in the afternoon (Table 1).

Table 1 -
Frequency of bird visitation in Spathodea nilotica according to the period of day and to the visits for all days sampled. The bird sequence follows the frequency percentage.

Only six species were observed performing legitimate visits: A. aurea 100% of legitimate visits, followed by H furcifer (95.65%), F. fusca (95%), A. nigricolis (70.27%), C. largipennis (20%) and E. macroura (18.76%) (see Figure 1). A. aurea and A. nigricollis presented as potential efficient pollinators of S. nilotica by mostly extracting the nectar through the opening of the corolla. They reached the nectar by entering their entire body inside of the corolla. On the other hand, F. fusca and H. furcifer present both body and beak elongated enough to reach the bottom of the corolla, where the nectar is found.

Figure 1 -
Frequency of feeding on nectar according to the bird foraging strategy.

E. macroura was presented in 58.65% of all antagonistic interactions recorded, followed by F. fusca and A. fimbriata to 11.04% and 10.87%, respectively. Seven species (A. nigricollis, C. largipennis, C. lucidus, H. chrysura, H. sapphirina, P. guainumbi and T. palmarum) showed only interspecific behaviour. E. macroura and C. flaveola showed the higher rates of intraspecific agonistic behaviour (52.81%) and (75%) respectively (Table 2).

Table 2 -
Frequency of the intra/interspecific antagonistic interactions among birds on Spathodea nilotica. The bird sequence follows the frequency percentage.

According to the total antagonistic interactions, E. macroura (n = 356), F. fusca (n = 67) and A. fimbriata (n = 66) were the most aggressive species. A. fimbriata unlike E. macroura, was not successful in warding off the intruders (F. fusca and A. nigricollis). Subordinate species (C. lucidus, A. fimbriata and H. furcifer) took the opportunity to forage quickly while the dominant species was absent or performing another activity.

E. macroura is the main territorial bird of S. nilotica. In addition it is considered resident since it was observed in the same and specific locations in the flowering period of S. nilotica. It was observed in 97% of the sample days, and it accounts for 20.39% of the total visits. Notable is the strong territoriality of this species. It was possible to observe a tree being divided and defended into different S. nilotica stratification by E. macroura residents. E. macroura was observed perched on the flowers to feed on nectar or in its petiole. In warmer periods of day, E. macroura was perched on tree branches just defending its territory from other invaders. In general, this behaviour decreased as soon as the intensity of heat increased.

4.

Discussion

Mendonça and Anjos (2005) studied hummingbirds in urban areas in southern Brazil and they recorded seven species visiting S. nilotica, five in common with our study (A. nigricollis, C. lucidus, E. macroura, F. fusca and H. chrysura). Machado (2009)MACHADO, CG., 2009. Beija-flores (Aves: Trochilidae) e seus recursos florais em uma área de caatinga da Chapada Diamantina, Bahia. Revista Brasileira de Zoologia, vol. 26, no. 2, p. 255-265. observed eight hummingbirds exploiting the resources of Bigononiaceae trees, three of which were also observed in S. nilotica (C. lucidus, C. mosquitus and E. macroura).

Antunes (2003)ANTUNES, AZ., 2003. Partilha de néctar de Eucalyptus spp., territorialidade e hierarquia de dominância em beija-flores (Aves: Trochilidae) no sudeste do Brasil. Ararajuba, vol. 11, no. 1, p. 39-44. noted that species of dominant hummingbirds in eucalyptus flowers were more frequent in the morning and the non-dominant ones in the afternoon. However this is not in agreement if we consider E. macroura. This discrepancy was probably due to the fact that E. macroura is resident (see results).

Feinsinger and Colwell (1978)FEINSINGER, P. and COLWELL, RK., 1978. Community organization among neotropical nectar-feeding birds. American Zoologist, vol. 18, p. 779-795. suggested that the hummingbirds are traveller species that use the spaces left by others. In addition, they are opportunistic, stealing the nectar when the defender is absent. The data obtained in S. nilotica corroborate this hypothesis, mainly in relation to C. lucidus, A. fimbriata and H. furcifer (see results). This behaviour was also observed by Antunes (2003)ANTUNES, AZ., 2003. Partilha de néctar de Eucalyptus spp., territorialidade e hierarquia de dominância em beija-flores (Aves: Trochilidae) no sudeste do Brasil. Ararajuba, vol. 11, no. 1, p. 39-44..

Machado et. al. (2007)MACHADO, CG., COELHO, AG., SANTANA, CS. and RODRIGUES, M., 2007. Beija-flores e seus recursos florais em uma área de campo rupestre da Chapada Diamantina, Bahia. Revista Brasileira de Ornitologia, vol. 15, no. 2, p. 267-279. observed all hummingbirds in the Chapada Diamantina (Bahia state, Brazil) making legitimate visits to flowers, including plants such as the Bignoniaceae Jacaranda irwinii (AH Gentry). It indicates they probably disperse the pollen of this species. In this study, most species only pillaged nectar, not pollinating the plant. The same was observed for S. nilotica by Mendonça and Anjos (2005). Thus, the most frequently species, such as E. macroura, C. lucidus and C. flaveola damaged the reproductive strategy of this plant, not constantly plundering nectar in exchange for offering a great chance of spreading pollen. As a result, most species only pillaged nectar without contributing to the reproductive strategy of the plant. Most probably it is a result of recent Neotropical bird interactions with this African plant.

Despite the low number of contacts, A. aurea A. nigricollis, F. fusca and H. furcifer presented as possible efficient pollinators of S. nilotica by mostly extracting the nectar through the opening of the corolla. The large flocks of A. aurea move over long distances to new areas in search of nectar. This species made frequent inter-tree movements and it promotes cross-pollination (Ragusa-Netto and Fecchio, 2006RAGUSA-NETTO, J. and FECCHIO, A. 2006. Plant food resources and the diet of a parrot community in a gallery forest of the south Pantanal (Brazil). Brazilian Journal of Biology, vol. 66, p. 1021-1032.; Silva, 2008SILVA, PA., 2008. Periquitos (Aratinga aurea e Brotogeris chiriri, Psittacidae) como potenciais polinizadores de Mabea fistulifera Mart. (Euphorbiaceae). Revista Brasileira de Ornitologia, vol. 16, no.1, p. 23-28.). Although their movements are not well understood, A. nigricollis, F. fusca and H. furcifer are local or seasonal migrant hummingbirds that visit thousands of flowers per day promoting efficient pollination (Sick, 1997SICK, H., 1997. Ornitologia brasileira. Rio de Janeiro: Nova Fronteira. 912 p.).

Apparently E. macroura seems to be a “harmful species” to the reproductive strategy of S. nilotica. However this species performed legitimate visits in 18.7% of occasions (103 of 549 contacts observed). It exceeds in high quantity of the others legitimate visitors, as F. fusca, A. nigricolis and H. furcifer.

Mendonça and Anjos (2005) observed that most of the birds showed territorial behaviours as observed in this paper. The F. fusca, together with A. nigricollis, did not show territoriality in S. nilotica, but Mendonça and Anjos (2006) observed that F. fusca was the main bird to show antagonistic behaviour among bird species observed in Erythrina speciosa (Fabaceae). Most probably this species was less aggressive in the present study because it is migratory and E. macroura is an extremely territorial bird already resident in S. nilotica. Although there was little visitation in most species, the interspecific antagonistic behaviour was predominant, except for E. macroura and C. flaveola (see results). This highest rate in E. macroura is explained by the fact this species is extremely territorial and also it is the main consumer of the S. nilotica nectar. In relation to C. flaveola perhaps E. macroura does not identify this species as a major threat to the consumption of nectar of S. nilotica, since different strategies to exploit nectar may reduce competition between them, as suggested by Dreisig (1997)DREISIG, H., 1997. Why do some foragers perch and other hover whle probing flowers? Evolutionary Ecology, vol. 11, p. 543-555.. Occasionally E. macroura was observed attacking other birds of major weight, but they do not make use of nectarivores resources at all, such as Passer domesticus (Linnaeus, 1758) and Zenaida auriculata (Des Murs, 1847).

We are grateful to Estela Eiko Miyaji, Fernanda Andrade Bueno, Laucídio Carvalheiro Pinheiro and Mateus Antônio Berni for helping us with the field observations. We also thank the anonymous referees for improving the manuscript and Maria Fernanda Martins e Ortiz for the English revision.

References

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Publication Dates

  • Publication in this collection
    Nov 2013

History

  • Received
    31 July 2012
  • Accepted
    3 Oct 2012
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br