The Auk 125(1):60–66, 2008 c The American Ornithologists’ Union, 2008.
Printed in USA.

SUGAR PREFERENCES OF THE GREEN-BACKED FIRECROWN HUMMINGBIRD (SEPHANOIDES SEPHANIODES): A FIELD EXPERIMENT VANINA R. C HALCOFF, 1,3 M ARCELO A. A IZEN , 1 1 Laboratorio 2 Instituto

AND

L EONARDO G ALETTO 2

Ecotono, Universidad Nacional del Comahue, Quintral 1250, 8400, Bariloche, Rio Negro, Argentina; and Multidisciplinario de Biolog´ıa Vegetal (CONICET-UNC), Casilla de Correo 495, C´ordoba, Argentina

Abstract.—Many flowers associated with hummingbirds (Trochilidae) produce nectar rich in sucrose, a characteristic that reflects innate preferences or the metabolic capacities of their putative pollinators or both. However, studies on nectar sugar selectivity by hummingbirds in the field are lacking. Under natural field conditions, we studied the sugar preferences of the Green-backed Firecrown Hummingbird (Sephanoides sephaniodes), the southernmost hummingbird in the world and a key pollinator in the temperate forest of South America. We considered potential differences between males and females and the influence of environmental temperature on those preferences. To free-foraging Green-backed Firecrown Hummingbirds, we simultaneously offered four different sugar solutions with the same concentration (24% wt/wt): (1) sucrose, (2) glucose, (3) fructose, and (4) a 1:1:1 mixture of these three solutions, as well as a control of pure water. The experimental design involved three replicates per treatment assigned to three different “blocks” of five feeders each, during eight periods of seven days each. We scored the number of Green-backed Firecrown Hummingbirds feeding on each feeder, the number of consumptions made by each individual, and the amount of sugar (g) consumed per sampling period. Greenbacked Firecrown Hummingbirds clearly discriminated against pure water, favoring sugar solutions; of the latter, they preferred sucrose over glucose and fructose. The mixed-sugar solution showed intermediate preference values. Neither sex nor temperature affected sugar preferences. Sugar preferences by the Green-backed Firecrown Hummingbird could influence the nectar composition of the flowers it pollinates through differential selection. Received 14 September 2006, accepted 25 February 2007. Key words: environmental temperature, Green-backed Firecrown Hummingbird, Sephanoides sephaniodes, sex, sugar preferences, temperate forest of southern South America.

Preferencia de Az´ucares en Sephanoides sephaniodes: un Experimento de Campo Resumen.—Muchas flores que se encuentran asociadas con colibr´ıes (Trochilidae) producen n´ectar rico en sacarosa, una caracter´ıstica que refleja las preferencias innatas y/o las capacidades metab´olicas de sus supuestos polinizadores. Sin embargo, no existen estudios sobre la selecci´on de az´ucares presentes en el n´ectar por parte de los colibr´ıes en el campo. En este estudio, evaluamos las preferencias de az´ucares en Sephanoides sephaniodes, el colibr´ı con distribuci´on m´as austral del mundo, que es un polinizador clave en los bosques templados de Sudam´erica. Consideramos las diferencias potenciales entre machos y hembras, y la influencia de la temperatura ambiental sobre esas preferencias. A individuos que forrajeaban libremente, les ofrecimos cuatro soluciones de az´ucares con la misma concentraci´on (24% peso a peso) simult´aneamente: (1) sacarosa, (2) glucosa, (3) fructosa y (4) una mezcla 1:1:1 de esas tres soluciones, adem´as de agua pura como control. El dise˜no experimental incluy´o tres r´eplicas por tratamiento asignadas a tres “bloques” diferentes de cinco alimentadores cada uno, durante ocho per´ıodos de siete d´ıas. Registramos el n´umero de colibr´ıes que se alimentaron en cada alimentador, el n´umero de eventos de consumo para cada individuo, y la cantidad de az´ucar (g) consumida por per´ıodo de muestreo. Los colibr´ıes claramente evitaron el agua pura, y prefirieron las soluciones azucaradas. Entre e´ stas, prefirieron la soluci´on de sacarosa por encima de las de glucosa y fructosa. La soluci´on mixta mostr´o niveles de preferencia intermedios. Las preferencias no fueron afectadas por el sexo ni por la temperatura. Las preferencias por los diferentes tipos de az´ucares por parte de S. sephaniodes podr´ıan influenciar la composici´on del n´ectar de las flores que esta especie poliniza por medio de selecci´on diferencial. Nectar, a dilute aqueous solution composed of sugar, water, amino acids, electrolytes, and other components, is the main food reward and source of energy for most pollinators. The three most common sugars in nectar are disaccharide sucrose

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and two monosaccharides, the hexoses fructose and glucose (Percival 1961). Different proportions of these three sugars have been associated with different types of pollinators as part of the “pollination syndrome” concept (Baker and Baker 1983, Proctor

vchalcoff@gmail.com

c 2008 by The American Ornithologists’ Union. All rights reserved. The Auk, Vol. 125, Number 1, pages 60–66. ISSN 0004-8038, electronic ISSN 1938-4254.
Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals.com/reprintInfo.asp. DOI: 10.1525/auk.2008.125.1.60

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et al. 1996). Although these nectar–pollinator associations have been questioned (van Wyk 1993, Perret et al. 2001, Galetto and Bernardello 2003), the composition of the floral nectars consumed by birds shows distinctive sugar signatures. Particularly, the nectars produced by flowers associated with hummingbirds tend to be rich in sucrose (Baker and Baker 1983, Freeman et al. 1984, Stiles and Freeman 1993, Baker et al. 1998, Perret et al. 2001). To explore the adaptive nature of this association, several sugar-preference trials have been done using captive hummingbirds, with mixed results. Although some of these experiments have confirmed the presumed hummingbird preference for sucrose over hexose solutions (Van Riper 1958, Stiles 1976, Mart´ınez del Rio 1990), other studies have shown variable preferences or none at all (Hainsworth and Wolf 1976, Schondube and Mart´ınez del Rio 2003, Fleming et al. 2004). In any event, there is little evidence to suggest that results obtained in the laboratory can be extrapolated to the field, because in the wild, hummingbirds may show stronger preference plasticity because of variation in flower availability and plant assemblage composition, environmental conditions (e.g., temperature), behavior (e.g., territoriality), and metabolic needs (e.g., reproduction). We analyzed sugar preferences of the Green-backed Firecrown Hummingbird (Sephanoides sephaniodes; hereafter “firecrown hummingbird”) in the field. This species is a key pollinator in the temperate forest of southern South America (Armesto et al. 1996, Aizen et al. 2002) and is the southernmost hummingbird in the world (Fjelds˚a and Krabbe 1990). We explored the existence of sex-related differences in sugar preferences and whether these preferences vary seasonally, particularly in relation to changes in temperature. To our knowledge, this is the first sugar-preference trial performed under natural conditions with free-foraging hummingbirds, thus avoiding the interpretative limitations of traditional laboratory trials.

M ETHODS The firecrown hummingbird is the only resident hummingbird species in the temperate forest of southern South America. This biome is characterized by a high incidence of biotic pollination, particularly by birds (Armesto et al. 1996, Aizen and Ezcurra 1998). In this temperate forest, ∼85% of the woody plant genera are visited and presumably pollinated by animals, and nearly 20% (principally endemic genera) are pollinated by the firecrown hummingbird (Smith-Ram´ırez 1993, Fraga et al. 1997). The firecrown hummingbird exhibits a seasonal territorial behavior and marked sexual dimorphism. Males are distinguished by a red– yellow iridescent reflection on the plumage of the forehead and crown, a trait that is absent in the females (Fjelds˚a and Krabbe 1990). We conducted the study in the Llao-Llao reserve (41◦ 0 S, 71◦ 30 W; altitude 760 m), a conservation area within the township of San Carlos de Bariloche and adjacent to Nahuel Huapi National Park, Argentina, during December 1999, February through May 2000, and January and February 2001. The vegetation at the study area is old-growth forest dominated by Coigue (Nothofagus dombeyi), a large evergreen tree (>2 m diameter at breast height [DBH] and >30 m high). Although the firecrown hummingbird

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is present all year-round in the area (Aizen 2003), the preference trials could not be carried out during the winter because the sugar solutions froze. We simultaneously offered four different sugar solutions, 350 mL each, with the same concentration (24% wt/wt), as well as a control of pure water (i.e., no sugar), in commercial feeders (Hummingbird Feeder Picasso, 400 mL). Solutes were pure sucrose, pure glucose, pure fructose, and a 1:1:1 mixture of these three. The 24% concentration was based on previous results by Lopez Calleja et al. (1997). To prepare the solutions, we transformed wt/wt to wt/mL concentration values following Bolten et al. (1979). We placed a transparent plastic bell over each feeder so that rainwater did not dilute the solutions. Feeders were placed in three groups ≤100 m apart under the forest canopy. To avoid site biases, we placed these feeder groups at different locations within an area approximately 0.5 × 0.5 km chosen randomly at the start of each sampling period. Each group (“block”) was composed of five feeders, each containing one of the four sugar solutions or the control. Thus, there were three replicates of each sugar treatment “running” simultaneously. Within each group, feeders were hung from a rope 1.5–2 m high and 1 m apart. Treatments were assigned randomly to the different positions along this linear feeder array at the beginning of each sampling period to avoid side biases (Jackson et al. 1998). Feeders were accessible to free-foraging firecrown hummingbirds for 10 consecutive days during each of the 8 sampling months. Visitation observations started three days after the placement of the feeders in the forest, to ensure their localization by the birds. We observed each feeder group for 45 min per day over seven consecutive days during each of the eight sampling months (i.e., a total of 126 h). During each observation period, we recorded the number of individuals feeding on each feeder and the number of times each bird introduced its bill into a feeder during a visit. We also identified the sex of each visiting firecrown hummingbird and measured air temperature at the beginning of each observation period. We removed the remaining solution from each feeder at the end of each 10-day sampling period, measured its final volume, and rechecked its concentration. Because evaporation was negligible, we estimated the total amount of sugar consumed in grams (g) by substracting the final from the initial volume. Solutions could not be checked at the end of the sampling period in May 2000 because of a severe snowstorm. Thus, data on sugar consumption were obtained for a total of seven sampling periods instead of eight. Statistical analyses.—We analyzed data by means of factorial analysis of variance (ANOVA) that considered type of sugar solution, sex, and sampling month as categorical factors, and feeder group as a blocking factor. The dependent variables were (1) mean number of firecrown hummingbird visits per 45 min, (2) mean number of consumptions made by all visiting firecrown hummingbirds per 45 min, and (3) mean number of consumptions made per visiting firecrown hummingbird. Variables 1–3 were averaged over each seven-day sampling period. Birds of undetermined sex were excluded from these analyses. To analyze the amount of sugar consumed over each 10-day period, we used a factorial ANOVA that considered type of sugar solution and sampling month as categorical factors, and feeder group as a blocking factor. The pure-water treatment was excluded from this analysis. In addition, sex was not included in this latter analysis, because we could not

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determine the amount of sugar consumed by males and females separately. Within the framework of the ANOVAs, we carried out planned comparisons, because we had a priori hypotheses about preferences of firecrown hummingbirds (Sokal and Rohlf 1981). The sum of squares associated with the sugar solution factor was decomposed into four contrasts: (1) sugar solutions versus water, (2) mixed versus pure-sugar solutions, (3) sucrose versus hexoses, and (4) fructose versus glucose. We expected a preference for sugar solutions over pure water and for the sucrose solution over the two hexose solutions. We excluded the first contrast from the analysis of the total grams of sugar consumed. We examined whether sugar preferences were related to environmental temperature by means of an analysis of covariance (ANCOVA). Here, the type of sugar solution was the main factor, as above; mean temperature, averaged over all observations at each sampling month, was the covariate and the feeder group was the blocking factor. Using this model, we analyzed only the amount of sugar consumed per 10-day period because this was the most integrative of all dependent variables.

R ESULTS We recorded 377 individual visits of firecrown hummingbirds during this experiment: 47.7% were by males, 33.7% by females, and 18.6% by individuals whose sex could not be determined, probably mostly juveniles. No other hummingbird or bird species was observed visiting the feeders. Firecrown hummingbirds showed preferences not only for sugar solutions, but also for some particular sugars (Figs. 1 and 2). The ANOVA analyses indicated differences associated with the sugar factor for all four dependent variables (Tables 1 and 2). For the number of visits, total number of consumptions, and number of consumptions per hummingbird, the orthogonal-contrast analysis confirmed a strong preference for sugar solutions over pure water (Table 1 and Fig. 1). Of the single-sugar solutions, the sucrose solution was, in general terms, the most preferred, followed by fructose and glucose (Figs. 1 and 2). The preference for the mixedsugar solution tended to be intermediate between the sucrose and the two hexose solutions (Figs. 1 and 2). Despite a stronger preference for sucrose over the two hexoses shown by all the different dependent variables (Figs. 1 and 2), this contrast achieved statistical significance only in the case of the most integrative variable, total amount of sugar consumed (Table 2). Firecrown hummingbirds consumed 24.4% and 68.4% more grams of sucrose than of fructose and glucose, respectively. Males visited the feeders more frequently than females (Figs. 1A–B and 3 and Table 1). These sex-related differences were more marked in some months than in others (significant “sex ∗ month” interaction for mean number of visiting hummingbirds; Table 1). Males were more frequent visitors during February and March (Fig. 3). Once at the feeders, males tended to insert their bills into the feeders about the same number of times as the females (4.02 ± 0.42 vs. 4.76 ± 0.84 for males and females, respectively; Fig. 1C). The interaction between type of sugar solution and sex was nonsignificant for all dependent variables (Table 1). Thus, there was no evidence that males and females differed in their sugar preferences.

FIG. 1. Male and female firecrown hummingbirds strongly preferred sugar solutions over pure water, and certain sugar solutions over others (see Table 1 for statistical results). Preferences are indicated by (A) number of visiting hummingbirds per 45 min, (B) number of consumptions per 45 min, and (C) number of consumptions per hummingbird. Values are means + SE.

There were significant differences among sampling months in visitation frequency, number of consumptions per visit, total number of consumptions, and amount of sugar consumed (Tables 1 and 2). Nevertheless, sugar preferences were seasonally

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D ISCUSSION Firecrown hummingbirds discriminated clearly between water and sugar solutions and preferred sucrose over hexose solutions. Preference for the mixed solution, which had equal representation of the three elementary sugars, may have resulted from the average preference for the three single-sugar solutions. Sugar preference of hummingbirds has been the focus of several studies during the past 50 years, with conflicting results. Van Riper (1958), Stiles (1976), and Mart´ınez del Rio (1990) reported significant preferences for sucrose over monosaccharide solutions (i.e., fructose and glucose). By contrast, Hainsworth and Wolf (1976) found a preference for mixed-sugar solutions and Schondube and Mart´ınez del Rio (2003) reported preferences of sucrose at high concentrations but hexose at low concentrations. Fleming et al. (2004) also found a preference for hexose solutions at low concentrations, though there was no significant preference for sucrose at high concentrations. Mart´ınez del Rio et al. (1992) argued that different sugar preferences may reflect different experimental protocols. Hummingbirds that showed no significant sucrose preferences had been exposed to the solutions for only 0.5 to 6 hours; whereas in experiments where clear sucrose preferences were recorded, exposure had been for 4 to 48 hours, which indicates that sucrose preferences may develop over time. Although our study included exposure to solutions for >48 hours, differential preferences were not identified in any of the variables analyzed. Nevertheless, firecrown hummingbird selectivity for sucrose over the two hexoses was detected statistically when preference was estimated as total sugar consumed over 10 days. Component variables (i.e., visitation frequency and number of intakes per individual) followed the general trend but exhibited greater variability than total sugar consumption. The preference for sucrose was not only statistical, but also biologically significant,

FIG. 2. Firecrown hummingbirds consumed more sucrose and mixedsugar solutions than fructose and glucose solutions (see Table 2 for statistical results). Values are means + SE.

independent (i.e., no significant “sugar ∗ month” interaction; Tables 1 and 2). The strong seasonal variation in visitation frequency and sugar consumption could represent a response to changing environmental temperatures. When considered as a covariate, temperature was associated with sugar consumption (F = 32.03, df = 1 and 74, P < 0.001), however, it did not differentially affect the type of sugar consumed (i.e., nonsignificant “sugar ∗ temperature” interaction; F = 0.68, df = 3 and 74, P > 0.10). The relationship between temperature and sugar consumption was negative (i.e., a given temperature increase caused similar decreases in the amount of sugar consumed for all sugar solutions; Fig. 4).

TABLE 1. Effects of sugar type, sex, and sampling month on (1) mean number of visiting firecrown hummingbirds per 45 min, (2) mean number of consumptions per 45 min, and (3) mean number of consumptions per hummingbird. The sum of squares associated with sugar type was decomposed into four a priori hypotheses about sugar preferences of firecrown hummingbirds (see text for description). Number of visiting firecrown hummingbirds per 45 min Source Sugar Sugar solutions vs. water Mixed vs. pure-sugar solutions Sucrose vs. hexoses Fructose vs. glucose Sex Month Sugar ∗ sex Sugar ∗ month Sex ∗ month Sugar ∗ sex ∗ month Block Error

Number of consumptions per 45 min

df

MS

F

MS

4 1 1 1 1 1 6 4 24 6 24 2 138

1.047 3.827 0.009 0.072 0.280 1.367 1.840 0.012 0.091 0.246 0.032 0.233 0.079

13.19∗∗∗ 48.22∗∗∗ 0.11 0.91 3.53 17.22∗∗∗ 23.19∗∗∗ 0.15 1.14 3.10∗ 0.4 2.93

5.123 18.492 0.050 0.444 1.506 2.821 3.727 0.057 0.430 0.542 0.227 0.293 0.355

Note: The feeder group was included as a blocking factor. ∗ P < 0.05, ∗∗ P < 0.001, and ∗∗∗ P < 0.0001.

F 14.42∗∗∗ 52.06∗∗∗ 0.14 1.25 4.24∗ 7.94∗∗ 10.49∗∗∗ 0.16 1.21 1.53 0.64 0.82

Number of consumptions per firecrown hummingbirds MS 1.722 6.246 0.002 0.098 0.540 0.392 0.572 0.027 0.129 0.193 0.122 0.088 0.169

F 10.20∗∗∗ 37.01∗∗∗ 0.01 0.58 3.2 2.32 3.39∗∗ 0.16 0.76 1.14 0.72 0.52

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TABLE 2. Effect of sugar type and sampling month on the amount of sugar consumed per sampling month (over a 10-day period). The sum of squares associated with sugar type factor was decomposed into three a priori hypotheses about sugar preferences of firecrown hummingbirds (see text for description). Sugar consumed Source

df

MS

F

Sugar Mixed vs. pure-sugar solutions Sucrose vs. hexoses Fructose vs. glucose Month Sugar ∗ month Block Error

3 1 1 1 6 18 2 54

104.198 27.376 208.851 76.370 294.704 12.929 70.819 32.944

3.16∗ 0.83 6.34∗ 2.33 8.95∗∗∗ 0.39 2.15

Note: The feeder group was included as a blocking factor. ∗ P < 0.05, ∗∗ P < 0.001, and ∗∗∗ P < 0.0001.

given that the consumption of this sugar was >50% higher than that of the least-preferred sugar (i.e., glucose). Males and females did not differ in their preferences for any particular sugar solution, as was reported for another nectarivorous bird (Markman et al. 2006), and both sexes followed the same selectivity pattern (Fig. 1). Despite this result, males were more frequent visitors than females during some months. Strong territorial behavior by males (Fraga et al. 1997, V. R. Chalcoff et al. pers. obs.) or female nesting (September, October, and November; Fjelds˚a and Krabbe 1990) could underlie these seasonal differences. The present study is the first to test for sugar preferences under field conditions. Blem et al. (2000) also studied preferences of free-foraging Rufous Hummingbirds (Selasphorus rufus) but for solutions of different sugar concentration rather than for different sugar types. In addition to potential intrinsic differences in sugar preference among hummingbird species, experiments under

FIG. 3. Males were more frequent visitors than the females, and this difference in frequency of visits was more accentuated in some months than in others. Values are means + SE.

FIG. 4. For all sugar solutions, the amount of sugar consumed by firecrown hummingbirds tended to decrease when environmental temperature increased. The lines are the best-fitted linear regressions (for sucrose solutions: y = 24.72–0.86, r 2 = 0.32; for hexose solutions: y = 37.33–1.40, r 2 = 0.35; and for mixed solutions: y = 21.93–0.75, r 2 = 0.26).

artificial laboratory conditions may involve different behavioral biases, which could be the cause of discrepancies among studies. We also offered the sugar solutions simultaneously, in a multiplechoice fashion, whereas in other studies the sugar solutions were typically offered in pairs (Hainsworth and Wolf 1976, Stiles 1976, Mart´ınez del Rio 1990, Jackson et al. 1998, Schondube and Mart´ınez del Rio 2003, Fleming et al. 2004). Fleming et al. (2004) reported that hummingbirds preferred hexoses over sucrose at low temperatures, although that results were influenced by the particular concentration. In our study, in which sugar concentration was constant, air temperature did not influence the preference for any particular solution. Overall, the consumption of both sucrose and hexoses increased with decreasing temperatures. Low temperatures should increase the energetic requirements of a homeotherm (Snow and Snow 1988) and, indeed, firecrown hummingbirds exhibited one of the highest maximal metabolic rates reported (L´opez-Calleja and Bozinovic 1995). An alternative explanation for an increase in sugar consumption during cold weather could be related to food scarcity. From late winter to early spring, firecrown hummingbirds feed exclusively on the flowers of the mistletoe Tristerix corymbosus (Loranthaceae), the only species in bloom during that part of the year (Aizen 2003). In other ornitophilous species from this temperate forest, flowering occurs with the onset of spring (Aizen and V´azquez 2006). Alternative resources that are more widely distributed could also explain the decrease in the number of hummingbirds visiting the feeders during warmer months. Throughout the Americas, flowers associated with hummingbirds produce nectars rich in sucrose (Baker and Baker 1983, Freeman et al. 1984, Stiles and Freeman 1993, Perret et al. 2001, Galetto and Bernardello 2003). The flora of the temperate forest of southern South America is no exception. We reported that sucrose was the predominant sugar (∼65%) component of nectar of 11

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hummingbird-pollinated plant species from this biome (Chalcoff et al. 2006). Several hypotheses have been posited to explain variation in sugar composition, particularly between nectars preferred by hummingbirds and those preferred by passerines, the latter composed mostly of hexoses rather than of sucrose (Baker and Baker 1983, van Wyk 1993, Baker et al. 1998, Dupont et al. 2004). The “ornithocentric explanation” (Fleming et al. 2004) assumes that nectar composition is an adaptation of the plant to different bird preferences, which in turn is related to disparate intestinal abilities to assimilate different sugar types. To be absorbed, sucrose must be hydrolyzed into its two hexose components, glucose and fructose, a process carried out by the intestinal enzyme, sucrase. The differential preferences exhibited by hummingbirds and passerines have been linked to the presence of sucrase and to different assimilation efficiencies associated with either sucrose hydrolysis or osmotic limitations (Mart´ınez del Rio et al. 1989, 1992; Mart´ınez del Rio 1990; Schondube and Mart´ınez del Rio 2004). The “plant-centered explanation” assumes that plant physiology and floral morphology are the decisive factors in nectar composition and the birds adapt. Sugar concentration is positively related to sucrose content in floral nectar (Nicolson 2002, V. R. Chalcoff unpubl. data). Although nectars preferred by birds are typically less concentrated than nectars preferred by insects, hummingbirds seem to prefer nectars with a high sugar concentration and with a larger proportion of sucrose than nectars preferred by passerines, probably owing to differences in body size, metabolism, and renal function (Fleming et al. 2004). Although both explanations provide plausible hypotheses, the key factors determining nectar composition remain to be identified. A CKNOWLEDGMENTS We thank to C. Mart´ınez del Rio, A. Christianini, V. Ojeda, and C. Ezcurra for their comments on an earlier draft of this manuscript; S. R. McWilliams and three anonymous reviewers for useful suggestions and ideas that improved early versions of this manuscript; and CONICET and FONCYT for financial support. We also thank the staff of the Reserva Municipal Llao-Llao, Argentina, for allowing us to conduct research in the park. V.R.C. holds a doctoral scholarship from the National Research Council of Argentina (CONICET) and M.A.A. and L.G. are researchers from the same institution. L ITERATURE C ITED Aizen, M. A. 2003. Influences of animal pollination and seed dispersal on winter flowering in a temperate mistletoe. Ecology 84:2613–2627. Aizen, M. A., and C. Ezcurra. 1998. High incidence of plant– animal mutualisms in the woody flora of the temperate forest of southern South America: Biogeographical origin and present ecological significance. Ecolog´ıa Austral 8:217– 236. ´ Aizen, M. A., and D. P. Vazquez. 2006. Flowering phenologies of hummingbird plants from the temperate forest of southern South America: Is there evidence of competitive displacement? Ecography 29:357–366.

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