Brito, Lucilene

Melo, Celine

Silva, Paulo Antonio

English

Ornitología Neotropical (E-Journal)

201SHORT COMMUNICATIONSORNITOLOGIA NEOTROPICAL 26: 201–206, 2015© The Neotropical Ornithological SocietyCALYX-WATER CONSUMPTION BY BLUE-AND-YELLOW MACAWS IN SPATHODEA CAMPANULATA (BIGNONIACEAE) FLORAL BUDSPaulo Antonio Silva1,3, Celine Melo2, & Lucilene Brito11Universidade do Oeste Paulista – UNOESTE, Rodovia Raposo Tavares, km 572, Bairro do Limoeiro, CEP: 19.067-175, Presidente Prudente, SP, Brazil.2Universidade Federal de Uberlândia – UFU, INBIO, Campus Umuarama, bloco 2D-15C, CEP: 38400-902, Uberlândia, MG, Brazil.3Corresponding author. E-mail: pauloantonio@unoeste.brConsumo de água do cálice por Araras Canindé em botões florais de Spathodea campanulata(Bignoniaceae).Key words: Amino acids, anthropogenic environment, Ara ararauna, bird-plant interaction, calyx water,dry season, exotic plant, Spathodea campanulata, water source.Handling editor: Juan Masello; Receipt: 24 January 2015; First decision: 1 April 2015;Final  acceptance: 17 June 2015.INTRODUCTIONBirds of different feeding guilds visit theflowers of plants in the Neotropics (Rocca &Sazima 2010). The use of flowers can be animportant strategy to obtain water, especiallywhen there is low or no precipitation (Janzen1980). For example, several parrot specieswere reported to visit flowers to cover someof their daily water demands during the dryseason (Ragusa-Netto 2005). Additionally,floral rewards, such as nectar, provide a valu-able source of calories and nutrients to visi-tors, e.g., sugars and amino acids (e.g., Heil2011). In some plants (c. 11 species), floralbuds contain water, called calyx water(Endress 1996). One example is Spathodeacampanulata P. Beauv. (Bignoniaceae), whosecalyx water from buds provides a valuablesource of nutrients (e.g., amino acids) to birds(Bahadur et al. 1986), including parrots (Ran-gaiah et al. 2004). Additionally, in S. campanu-lata calyx water is also available in openflowers, but mixed with nectar (Rangaiah et al.2004).Large Neotropical parrots, such asmacaws of the genus Ara, are very mobilebirds, commuting daily from communalroosts to feeding areas and vice versa (Roth1984, Tubelis 2010, Santo & Ragusa-Netto2014). These birds have high energy andnutritional requirements (Koutsos et al. 2009,202SILVA ET AL.Gilardi & Toft 2012), and appear to search forhighly profitable food resources to compen-sate for the cost of daily trips (Santos &Ragusa-Netto 2014). They feed mainly onseeds and solid matter from fruits, such aspulp (Roth 1984, Gilardi & Toft 2012, Lee etal. 2014), which provide a valuable source ofenergy and nutrients (Barbosa et al. 2009,Koutsos et al. 2009). Floral resources can alsobe important in the diet of macaws, contribut-ing to the daily supply of nutrients and water(sensu Ragusa-Netto 2005). However, theexploitation of flowers by macaws has beenreported only through fortuitous foragingrecords (e.g., Munn 1988, Tubelis 2009,Gilardi & Toft 2012, Silva 2013, Lee et al.2014). Here, we report on observations ofBlue-and-yellow Macaws (Ara ararauna) con-suming nectar and calyx water from openflowers and calyx water from the floral budsof S. campanulata. We discuss the importanceof buds as a source of water and nutrients forthis large seed-eating parrot. METHODSStudy area and macaws in the region. This studytook place in Ilha Solteira (20°25’S, 51°20’W;380 m a.s.l.), in the northwest of the State ofSão Paulo, southeastern Brazil, bordering theState of Mato Grosso do Sul. Detaileddescriptions of the area can be obtained fromSilva & Melo (2013). Wild Blue-and-yellowMacaws have been increasingly seen occupy-ing the urban area in the region, where theyfeed on several native and exotic plants (Silva2013, Santos & Ragusa-Netto 2014). Macawsbreeding in the urban areas of northwesternSão Paulo have also been increasinglyreported, especially on television news (PASpers. observ.). Macaws in these areas use deadRoystonea oleracea palm trees (Arecaceae) fornesting (PAS pers. observ.). This exotic palmspecies is widely planted in urbanized areas ofthe Ilha Solteira, and many are used by Blue-and-yellow Macaws as roosting sites (Silva2013).Specific observation site. Feeding activity of Blue-and-yellow Macaws on blooming S. campanu-lata were observed in a gardened cemetery(approx. 4 ha) located in the suburban area ofIlha Solteira (20°26’12.04”S, 51°20’31.55”W,361 m a.s.l.). This public space is surroundedby residential, commercial, and horticulturalareas, vacant lots, reforestation, and riparianforest dominated by exotic invasive plants,e.g., Leucaena leucocephala (Fabaceae). Althoughbeing diverse, the plant composition in thecemetery is dominated by exotic tree species,including Magifera indica (Anacardiaceae),Schefflera actinophylla (Araliaceae), Cupressusspp. (Cupressaceae), Tipuana tipu (Fabaceae),Callistemon viminalis (Myrtaceae), and S. cam-panulata.Feeding plant and floral traits. Spathodea campanu-lata (syn. S. nilotica Seem.) is an African tree(15–20 m tall) introduced to Neotropicalregion for ornamental purposes (e.g., Francis2000, Lorenzi et al. 2003). It is a potentialinvader in several tropical habitats, such asundisturbed forests, secondary forests, defor-ested lands, ruderal areas, agricultural areas,and abandoned agricultural lands (Francis2000, Labrada & Díaz Medina 2009, Larrue etal. 2014). This plant is ranked as one of the100 worst invasive exotic species in the world(Lowe et al. 2000), thus threatening nativetropical biodiversity (Larrue et al. 2014). Itcreates a shading effect that can reduce nativeplant species’ richness under its canopy(Weber 2003). Spathodea campanulata blooms for up tonine months per year, from January to Sep-tember (Silva 2013). The floral bud stage con-sists of a conical closed calyx (Fig. 1A), whichis rich in water (Rangaiah et al. 2004). Thiswater reservoir supplies the development offloral organs (Rangaiah et al. 2004) as well as203SHORT COMMUNICATIONSprotects them against herbivorous arthropods(cf. Carlson & Harms 2007). The mean watervolume in the calyx varies with its size, from0.54 ml in a 2.5 cm-long calyx to 2.96 ml ofwater in a 6.5 cm-long calyx (Rangaiah et al.2004). Calyx water has a constant 1-% sugarconcentration, though its production stopsjust before anthesis (Rangaiah et al. 2004). Asmall amount of the calyx water drops offduring flower opening, but a portion of thewater remains accumulated in the open flow-ers (Rangaiah et al. 2004). In addition to calyxwater, large open flowers (9 cm long, 6 cm indiameter) produce a large amount of nectar(Rangaiah et al. 2004). On average, the totalvolume of nectar and calyx water is 1 ml perflower (Rangaiah et al. 2004). Due to the evap-oration of water content, the nectar-sugarconcentration increases throughout the daywith a mean of 9.5% in the early morning to25.3% in the late afternoon (Rangaiah et al.2004).Observations. The observation of floral exploi-tation by Blue-and-yellow Macaws was madeduring a systematic parrot study conducted innine 5-km long transects from March2010–February 2012 (Silva 2013). As the openflowers contain nectar and a remainingamount of calyx water (Rangaiah et al. 2004),we assumed that the macaws ingested thesetwo liquids. Ad libitum observations (Altman 1974) ofmacaws consuming calyx water were obtainedin May 2014. This month corresponds toautumn in southeastern Brazil, and it also rep-resents the second month of the dry season(which lasts for a total of six months). When aflock of macaws perched on an individual ofS. campanulata, we recorded the number ofbirds, number of floral buds exploited, andthe time of floral bud exploitation until theparrots flew away. A single observation,defined as foraging bout, can include multiplefeeding flocks. Details of the feeding behaviorwere obtained using 8 x 40 binoculars as wellas by videotaping and photographing at leastone macaw in the flock that explored thebuds.RESULTSOn 26 July 2011 at 08:20 h, a flock of fourBlue-and-yellow Macaws was observed visit-ing an individual of S. campanulata blooming inthe cemetery. Each macaw cut 4–6 open flow-ers with the beak, removing the petals andconsuming the nectar and calyx water. Thisfeeding activity lasted ca. 5 min, and birds leftafterwards. In the late afternoon (mainly between17:20 and 18:00 h) on 1–3 and 9–10 May2014, we observed 10 foraging bouts, duringwhich 13 groups of Blue-and-yellow Macaws(mean = 2.54, SD = 0.97 macaws/flock,range 2–5 birds) were exploiting buds in twoS. campanulata plants. The Blue-and-yellowMacaws exploited 54–117 floral buds (mean= 87.0, SD = 23.8, n = 5 macaws) for 6 to 24min (mean = 14.5, SD = 6.4, n = 8 foragingbouts). In the following we describe in moredetail typical foraging events based on videoanalysis.Upon arrival to the plant, all macawssearched for floral buds, ignoring the openflowers. After finding the clustered floral buds(Figs 1A, B), the macaws removed one floralbud at a time with their beaks. Then, punctur-ing the floral bud with their beaks, they tiltedtheir head up (Fig. 1B), squeezing the budrepeatedly so that water flowed out. A copi-ous amount of water ran down the tongue ofthe macaw, which then swallowed. The macawthen licked the inside and outside of the floralbud before discarding it. The macaws of aflock stopped feeding activity on floral budssynchronously, leaving the S. campanulata treeand heading towards a roost probably locatedon a R. oleracea palm tree some 1–3 km fromthe cemetery.204SILVA ET AL.DISCUSSIONThe exploitation of calyx water has not previ-ously been reported for any Neotropical par-rot. Thus, this study provides a novelobservation and a new food item for theBlue-and-yellow Macaw. However, we notethat calyces containing water are rare in plants(Endress 1996). In fact, calyx-water ingestionhas only been reported for the Afro-AsianRing-necked Parakeet (Psittacula krameri), alsoin S. campanulata (Rangaiah et al. 2004). How-ever, pictures of another Neotropical parrot,the Blue-winged Macaw (Primolius maracana),consuming calyx water on buds of S. campa-nulata can be found on a Brazilian website(Brazil 2015; http://www.wikiaves.com.br/1656672&p=7&t=s&s=10416). CollaredLories (Phigys solitarius) feed on the flowers ofthis plant in Fiji (Forshaw 1989) while theNeotropical Peach-fronted Parakeet (Eupsit-tula aurea) feeds on its nectar (Previatto et al.2013), and the Yellow-chevroned Parakeet(Brotogeris chiriri) feeds on petals, pollen, andnectar (PAS pers. observ.).Despite several opportunities to observeforaging macaws from 2010 to 2012, theywere only recorded visiting open flowers of S.campanulata once. In contrast, in only five daysof observation in May 2014, we observedsubstantial calyx-water consumption bymacaws on the floral buds of this introducedplant. It should be noted that during theseobservations the open flowers with largeamounts of nectar were ignored by themacaws. This suggests that they prefer calyxwater from floral buds. Notably, the calyxwater was consumed in the dry season.Because parrots usually drink rainwater thatbuilds up in holes in tree trunks (Sick 1997),they may struggle to find water in the dryseason. Sometimes, parrots can also goFIG. 1. A) Floral buds of Spathodea campanulata. B) A Blue-and-yellow Macaw drinking water from a S. cam-panulata floral bud in Ilha Solteira, State of São Paulo, SE Brazil; buds are indicated by yellow arrows. Pho-tographs by Paulo Antonio Silva.205SHORT COMMUNICATIONSdown to the ground to drink water (Sick1997), but the risks of predation can be high.It has been previously suggested that flowerscan be important water sources for animals inthe dry season (Janzen 1980). In this sense,flowers high up in the crowns of tree seemto be safer places to obtain water. Therefore,it is possible that the exploitation of S. campan-ulata floral buds allows Blue-and-yellowMacaws to safely obtain water during the dryseason.The consumption of calyx water may alsoprovide nutritional benefits as well as providephysiological advantages for Blue-and-yellowMacaws. Macaws tend to consume nutritious-rich parts of plants, such as seeds, which arehigh in protein and thus amino acids (Koutsoset al. 2009, Gilardi & Toft 2012). The calyxwater of S. campanulata floral buds is also richin amino acids (Bahadur et al. 1986), and con-sequently of high nutritional quality. There-fore, it is not surprising that our observationof the large number of floral buds exploited(c. 87) and prolonged time invested in thisfeeding activity (c. 15 min) may be associatedwith nutritional benefits. It is noteworthy thatmacaws spend a similar amount of time whenfeeding on the large and nutritious seeds ofTerminalia catappa (Combretaceae) and Platypo-dium elegans (Fabaceae) trees (PAS pers.observ.). It must also be emphasized that thecalyx water of S. campanulata floral buds con-tains sugar, even though it is greatly diluted(Rangaiah et al. 2004). In this case, by exploit-ing many floral buds the macaws can supple-ment their energy intake by consuming largequantities of calyx water (cf. Martinez del Rioet al. 2001). The calyx water of S. campanulata floralbuds constitutes a novel food source for theBlue-and-yellow Macaw (sensu Rodriguez2006). However, this parrot is a floral-budpredator. Like other parrots that damageflowers (e.g., Ragusa-Netto 2005), it mayinhibit fruit and seed production in S. campa-nulata. Since this exotic plant is considered tobe highly invasive in Brazil (Zenni & Ziller2011), and thus a threat to local native plants(sensu Weber 2003), at least at the local levelthe Blue-and-yellow Macaw could reduce thespreading of S. campanulata.ACKNOWLEDGMENTSOur sincere thanks to Donald J. Brightsmith,Juan F. Masello, Katherine Renton, AndréWeller and Rafael F. Juliano for contributingto the improvement of this paper. Financialsupport was provided by FAPEMIG andCAPES.REFERENCESAltmann, J. 1974. 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CALYX-WATER CONSUMPTION BY BLUE-AND-YELLOW MACAWS IN SPATHODEA CAMPANULATA (BIGNONIACEAE) FLORAL BUDS

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CALYX-WATER CONSUMPTION BY BLUE-AND-YELLOW MACAWS IN SPATHODEA CAMPANULATA (BIGNONIACEAE) FLORAL BUDS

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