Nectar robbing behavior of the Horned Sungem Hummingbird ( Heliactin bilophus ) ( Birds : Trochilidae ) in two species plant the genus Amphilophium Kunth ( Bignoniaceae ) and Sinningia Nees ( Gesneriaceae )

Biota Amazônia ISSN 2179-5746 ABSTRACT. The Horned Sungem Hummingbird (Heliactin bilophus) is a typical savannah hummingbird inhabiting opened phytophysiognomies in areas of Cerrado, Caatinga, highlands and plains with low vegetation. There are few studies about its feeding habits and little known about its behavior patterns. Here we report the bird feed behavior on two plant species Amphilophium elongatum and Sinningia sp. Trough illegitimate visits to the floral nectary, H. bilophus obtained food acting as a nectar robber. This foraging strategy included new sources of food for the hummingbird and could represent negative effects to the related plant species.

Foraging strategies by Trochilidae enables the breeding success of plants and can guarantee higher genetic variability besides providing food for the floral visitor (ARAÚJO; OLIVEIRA, 2007;MACHADO, 2009).However, there are cases where the visitors do not act in the pollination, accessing only the nectar of the plant through holes made at the base of the external part of the flower going directly to the floral nectar.This usually happens when the hummingbird size and morphology are not compatible with the flower.This interaction to obtain food is known as nectar robbery (MACHADO; ROCCA, 2010).
Plants that uses hummingbirds for its own pollination often present specific characteristics, as flowers in the shape of tubes and pending, suitable to the capacity of hoover and long and thin bill, making a natural visit.While plants with long corolla prevents that visitors with short bills have accesses to the nectar (MACHADO, 2014), those been more robbed over the ones that presents small flowers (LARA; ORNELAS, 2011).
The species Amphilophium elongatum (Vahl) L.G. Lohmann is a plant from the Bignoniaceae family which occurs in stricto sensu Cerrado areas, riparian forest, rupestrian field, and secondary growth vegetation capoeira from north, west-center and southeast Brazil.It has an aroma strongly sweetish, with a colored cream corolla, internally yellowish and curved pipe down, attracting mainly bees as pollinators (SILVA et al., 2012;MACHADO;ROMERO, 2014).
With neotropical occurrence, the genus Sinningia Nees includes about 70 species of shrubs, subshrubs or tuberous herbs.In Brazil, its distribution is concentrated in the Southeast.The flowers are pollinated by bats, bees and predominantly by birds.Among those pollinated by hummingbirds, the species that stand out are the ones with reddish and odorless flowers.They consist 67% of species of the genus (BARROSO et al., 1991;PERRET et al., 2001).
The Horned Sungem (Heliactin bilophus) (TEMMINK, 1820) is a typical savannah species, inhabits open phytophysiognomies in areas of Cerrado, Caatinga, highlands and plains with low vegetation.They occur in the Southeast, Midwest, Northeast and Northern Brazil, Bolivia and Suiriname.The species presents sexual dimorphism, male with a crest forming a red-gold horn format and black throat.Female without horn, with brown throat and smaller tail (SICK, 1997).
Research on bird-flower interaction represents a rich field in Ecology, regarding both ecological and evolutionary aspects.The understanding such relationships is becomes indispensable to species conservation (MENDONÇA; ANJOS, 2003).However, few studies addressed the feeding habits of H. bilophus and little knows about their behavioral patterns.Therefore, the present work has the aim to report de nectar robbery behavior of H. bilophus at A. elongatum and Sinningia sp..
The visits records to the species A. elongatum made on 5th February 2014, in a stricto sensu Cerrado area, at the municipality of Rondonópolis, Southeast of Mato Grosso state.A H. bilophus female was observed visiting the flower three times (Figure 1).On each one of the visits the bird invested sequentially from three to four times at a hole located just after the receptacle, accessing the plants nectar (Figure 2).The visit at Sinningia sp. was record on the 22nd January 2015 in a stricto sensu Cerrado area with pasture influence, at the municipality of Paracatu, Northwest of Minas Gerais.On the occasion, was observed a male of H. accessing the nectar trough a role next to the sepals of three plants flowers (Figure 3).
On both cases reported, it was not possible watch if the bird was responsible for the opening of the holes, that could have been made by the hummingbird, as well as another bird or even some insect such as Trigona spinipes (LÍRIO et al., 2001;CARVALHO et al., 2007;COSTA;MORAIS, 2008;PARRINI;RAPOUSO, 2010).Similar tactic as the one adopted by H. bilophus was reported for other Trochilidae, where birds with short bill in relation to the morphology of some flowers were frequently observed obtaining nectar by perforation of the base of the corollas (MENDONÇA; ANJOS, 2005).
At certain environments, the hummingbird community may present a flexibility on their strategies of behavior or expected seasonal patterns, and also for being able to explore non-ornitholophilous resources.Thus, the availability of nectar associated with the species Amphilophium elongatum and Sinningia sp. may serve as an important food supply for H. bilophus in a period of scarcity of floral resources (MACHADO, 2014).
Data involving the illegitimate visits of H. bilophus and its interaction with the species A. elongatum and Sinningia sp. were not documented until now.Both in A. elongatum and in Sinningia sp., the bird accessed floral nectaries without entering in contact with the reproductive system of the flowers, therefore characterizing as robbery.
The process of robbing at elevated frequency and intensity could decrease significantly the availability of nectar, and alter in a negative manner the visit rate of pollinators (MALOOF;INOUYE, 2000;CASTRO et al., 2008).Visits at low frequency do not change directly in the production of seeds.However, the presence of the robbing hummingbirds suggests competition with the legitimate groups of visitors, as observed in Passiflora speciosa (Passifloraceae) (LONGO;FISCHER, 2008).Besides those factors, González-Gomes and Valdivia (2005) point out that the robber could also damage the floral nectary, so preventing the replenishment of nectar by the vegetal species.
It is noteworthy that if it were not for the process of robbing, H. bilophus possibly would not be able to access the nectar of those plants, due to incompatibility of the species with the morphology of flowers.This strategy of foraging includes new feeding sources for the bird besides to be able to represent negative effects for the referred vegetal species.