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

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.


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, 1996).
Birds, especially hummingbirds, represent a group numerically and ecologically dominant in flower-animal interactions in the Neotropics (Stiles, 1981).They are also very successful in urban areas (Gilbert, 1989;Marsluff et. al., 2001) where they play an important role in the pollination of many flowering plants (Mendonça and Anjos, 2003).However, there are few studies conducted in urban areas of the Brazilian Biomes (Mendonça and Anjos, 2003).
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, 1979).However, the majority of flower-animal interaction studies has been focussed on areas that have been little disturbed (Ragusa-Neto, 2002;Antunes 2003;and Machado et. al., 2007), 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, 1997).
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., 2003).Nogueira-Neto (1970) 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, 2005;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.

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, 1994).
The birds were observed with binoculars (8x25 and 8x42).We first recorded the bird species, then we verified how it exploited the resources of the flower according to Machado (2009): 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).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.
We calculated the frequency of occurrence of species, inter and intraspecific antagonistic behaviour, and foraging strategy of nectarivorous birds on S. nilotica.

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. 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).
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.
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. Braz. J. Biol., 2013, vol. 73, no. 4, p. 737-741 739 Potential pollinator of the Spathodea nilotica  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.

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) 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) 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) 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).Machado et. al. (2007) 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, 2006;Silva, 2008).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, 1997).
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 antago-740 Braz.J. Biol., 2013, vol. 73, no. 5, p. 737-741 Previatto, DM., Mizobe, R. and Posso, SR ).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).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).

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

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.

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