Anais da Academia Brasileira de Ciências (2015) 87(4): 2163-2175 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201520140349 www.scielo.br/aabc Plant-hummingbird interactions and temporal nectar availability in a restinga from Brazil LORENA C.N. FONSECA1,5, JEFERSON VIZENTIN-BUGONI2,6, ANDRÉ R. RECH3 and MARIA ALICE S. ALVES4 1Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro/ UFRJ, CCS, IB, Caixa Postal 68020, 21941-590 Rio de Janeiro, RJ, Brasil 2Programa de Pós-Graduação em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas/ UNICAMP, Rua Monteiro Lobato, 970, Barão Geraldo, 13083-970 Campinas, SP, Brasil 3Instituto de Biologia, Universidade Federal de Uberlândia/UFU, Av. Pará, 1720, Campus Umuarama, 38405-320 Uberlândia, MG, Brasil 4Departamento de Ecologia, Instituto de Biologia Roberto Alcantara Gomes, Universidade do Estado do Rio de Janeiro/UERJ, Rua São Francisco Xavier, 524, Maracanã, 20550-011 Rio de Janeiro, RJ, Brasil 5Companhia Ambiental do Estado de São Paulo/CETESB, Av. Professor Frederico Hermann Jr, 345, Pinheiros, 05459-900 São Paulo, SP, Brasil 6Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark Manuscript received on July 10, 2014; accepted for publication on April 27, 2015 ABSTRACT Hummingbirds are the most important and specialized group of pollinating birds in the Neotropics and their interactions with plants are key components to many communities. In the present study we identified the assemblage of plants visited by hummingbirds and investigated the temporal availability of floral resources in an area of restinga, sandy plain coastal vegetation associated with the Atlantic forest, in Southeastern Brazil. We recorded flower and nectar features, flowering phenology and interactions between plants and hummingbirds and estimated the amount of calories produced per hectare from June 2005 to August 2006. Ten plant species were visited by two hummingbirds, Amazilia fimbriata and Eupetomena macroura. Resource availability was highly variable among plant species and over time. Nectar volume and concentration per flower were similar to other Neotropical hummingbird-visited plant assemblages. The estimated nectar resource availability between months varied from 0.85 to 5.97 Kcal per hectare/day, demanding an area between one and 6.8 ha to support a single hummingbird. Our study reports an unusual tropical setting where almost all interactions between hummingbirds and plants were performed by a single hummingbird species, A. fimbriata. Hence, the variable nectar availability is probably influencing hummingbird movements, its foraging area, and consequently plant pollination. Key words: Amazilia fimbriata, Atlantic rainforest, floral resources, ornitophily, pollination, restinga. INTRODUCTION many plant species in different ecosystems (Stiles 1981, Mendonça and Anjos 2003). These birds Hummingbirds are numerically and ecologically also feed on small arthropods but they obtain most dominant in bird-flower interactions in the New of their energy requirement from nectar, being World, where they play a crucial role pollinating highly specialized on this diet (Stiles 1978, Cronk Correspondence to: Maria Alice S. Alves and Ojeda 2008). While feeding, hummingbirds E-mail: [email protected] may pollinate flowers, establishing therefore a An Acad Bras Cienc (2015) 87 (4) 2164 LORENA C.N. FONSECA, JEFERSON VIZENTIN-BUGONI, ANDRÉ R. RECH and MARIA ALICE S. ALVES mutualistic relationship with many of the plants they and the structure of plant-pollinator interactions visit (Bawa 1990, Buzato et al. 2000, Abrahamczyc in this region. Restingas are geologically recent and Kessler 2015, but see Maruyama et al. 2013). environments (less than 120,000 years before However, nectar production is costly for plants and present) where shrubland vegetation grows on near- its availability in nature is highly complex giving shore, sandy soils (Souza et al. 2008). The soil of rise to a wide array of nectar production strategies restinga tends to require plant adaptations to support (Pyke 1991, McDade and Weeks 2004). For drought, salinity and/or low nutrient availability instance, at the community level, plant species can (Scarano et al. 2001). Given the harsh conditions produce nectar with distinct sugar compositions of restingas, plant colonization is hampered and (Galetto and Bernardello 2003) or rates (MacDade often facilitation by nurse plants is crucial for the and Weeks 2004). Furthermore, hummingbird- establishment of other plant species (Scarano 2002, flowers vary greatly on flowering seazonality and Sampaio et al. 2005). In the Southeastern Brazilian length (e.g. Buzato et al. 2000, Maruyama et al. restingas, one of the most important nurse plants 2014, Vizentin-Bugoni et al. 2014). The resulting is the mainly hummingbird-pollinated bromeliad spatial and temporal dynamics of food resources Aechmea nudicaulis (Sampaio et al. 2005, Schmid may have direct effects on the hummingbird et al. 2011). Therefore, the maintenance of these assemblages (Cotton 2000) and, consequently nurse plants, and consequently its ecological influence plant pollination (Stiles 1978, 1985). role, rely to some extent on the hummingbirds. According to patterns of nectar availability, Despite the importance of these interactions for the hummingbirds present a continuum of behavioral ecosystem functioning, to our best knowledge there strategies, from trapliners (commonly species are no previous studies on plant-hummingbirds from the Hermits clade) that usually visit dispersed interactions at community level in restingas. flowers that produces higher amount of reward In this context, here we described the structure per flower, to territorial species (usually non- of a plant-hummingbird assemblage in a restinga hermits species) which generally feed on grouped area and estimated the energy production by the flowers producing a lower volume of more diluted plants. In order to characterize the relationship nectar (Stiles 1975, Feinsinger and Colwell 1978). between hummingbirds and their resources, we Therefore both, behavioral strategy and nectar also described the floral morphology, phenology availability, play a central role in determining and nectar production for the hummingbird-visited the foraging area of a hummingbird (Feinsinger plants in the assemblage. Based on our findings, and Colwell 1978). Moreover, entire plant we discuss the possible implications of nectar assemblage studies in seasonal areas of Central dynamics on hummingbird foraging area and plant South America have reported most hummingbirds reproduction. as being generalists, feeding on a wide array of ornithophilous and non-ornithophilous flowers MATERIALS AND METHODS (Oliveira and Gibbs 2000, Araújo and Sazima 2003, STUDY AREA Maruyama et al. 2013 and references therein). Some simpler tropical ecosystems, like The present study was carried out in the “Restinga the Brazilian restingas which present lower de Jurubatiba” National Park (RJNP, 22o16’41’’S; diversity, productivity and structural complexity in 41o39’41’’W), located on the coast of the state of comparison to Atlantic Forest, for instance (Scarano Rio de Janeiro, Brazil (Fig. 1). The RJNP is the 2002), offer the opportunity to better understand the only national protected area specifically designed ecological issues concerning the nectar dynamics to preserve restinga ecosystems in Brazil. The An Acad Bras Cienc (2015) 87 (4) PLANT-HUMMINGBIRD interactions IN restinga 2165 restinga is characterized by geologically recent Fonseca) monitored the transects (five transects of sandy coastal plain adjacent to the core Atlantic 200 m each) twice a day. Monitoring was carried rainforest (Souza et al. 2008). The vegetation of out by walking slowly across each quadrant the study area is dominated by patches of Clusia starting between 6:00-8:00 and 16:00-18:00 and hilariana called “non-flooded open shrubland” expending around 3 h per turn/month observing, (“restinga arbustiva aberta não inundável”, in summing 78 h of observations. Along the transects Portuguese) (Magnano et al. 2011), with the we identified and quantified hummingbirds, flower forested physiognomy nearby (Araujo et al. 1998). visitation and agonistic interactions. Legitimate The rainfall is seasonally distributed varying from visits by insects were also quantified. According 40 mm per month during winter (from June to to our previous observations, our sampling period September) to 190 mm per month during summer coincides with higher activity of hummingbirds. (from December to February, Henriques et al. Flower morphology and nectar measurements were taken from June 2005 to May 2006 along 1986). Mean annual temperature varies around 22 the same quadrants. We randomly set 30 plots °C (Araujo et al. 1998). (20 X 20 m) totalling 12,000 m2 inside the five SAMPLING METHOD bigger 200 x 40 m quadrants. Inside these plots, we described flowering phenology and number of Data collection was carried out from June 2005 opened flowers once a month and measured nectar to August 2006. We established five consecutive features from the hummingbird-visited plants. 2 quadrants of 200 x 40 m (8,000 m ) covering a total Although occurring only nearby and not inside the area of 40,000 m2. Each month, from August 2005 plots, we also included the Quesnelia