Research Article |
Corresponding author: Cristiano S. de Azevedo ( cristianoroxette@yahoo.com ) Academic editor: Luis Fabio Silveira
© 2017 Lucas L. Lanna, Cristiano S. de Azevedo, Ricardo M. Claudino, Reisla Oliveira, Yasmine Antonini.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Lanna LL, de Azevedo CS, Claudino RM, Oliveira R, Antonini Y (2017) Feeding behavior by hummingbirds (Aves: Trochilidae) in artificial food patches in an Atlantic Forest remnant in southeastern Brazil. Zoologia 34: 1-9. https://doi.org/10.3897/zoologia.34.e13228
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During flight, hummingbirds achieve the maximum aerobic metabolism rates within vertebrates. To meet such demands, these birds have to take in as much energy as possible, using strategies such as selecting the best food resources and adopting behaviors that allow the greatest energy gains. We tested whether hummingbirds choose sources that have higher sugar concentrations, and investigated their behaviors near and at food resources. The study was conducted at Atlantic forest remnant in Brazil, between June and December 2012. Four patches were provided with artificial feeders, containing sucrose solutions at concentrations of 5%, 15%, 25% and 35% weight/volume. Hummingbird behaviors were recorded using the ad libitum method with continuous recording of behaviors. The following species were observed: the Brazilian ruby Clytolaema rubricauda (Boddaert, 1783), Violet-capped woodnymph Thalurania glaucopis (Gmelin, 1788), Scale-throated hermit Phaethornis eurynome (Lesson, 1832), White-throated hummingbird Leucochloris albicollis (Vieillot, 1818), Versicoloured emerald Amazilia versicolor (Vieillot, 1818), Glittering-bellied emerald Chlorostilbon lucidus (Shaw, 1812) and other Phaethornis spp. C. rubricauda, P. eurynome and Phaethornis spp. visited the 35%-sucrose feeders more often, while the T. glaucopis visited the 25%-sucrose feeders more often. L. albicollis and A. versicolor visited more often solutions with sugar concentration of 15%. C. lucidus visited all patches equally. Three behavioral strategies were observed: 1) C. rubricauda and T. glaucopis exhibited interspecific and intraspecific dominance; 2) the remaining species exhibited subordinance to the dominant hummingbirds, and 3) P. eurynome and Phaethornis spp. adopted a hide-and-wait strategy to the dominant hummingbird species. The frequency of aggressive behaviors was correlated with the time the hummingbird spent feeding, and bird size. Our results showed that hummingbirds can adopt different strategies to enhance food acquisition; that more aggressive species feeding more than less aggressive species; and that the birds, especially if they were dominant species, visited high quality food resources more often.
Behavioral strategies, dominance, food resources, subordination, trapline
Hummingbirds are specialized birds that consume predominantly nectar, but can also consume small arthropods (
The net energy concept postulates that energetic costs during foraging must be lower than energy intake during foraging (
Three behavioral strategies can be adopted by hummingbirds when foraging: (A) dominance/territoriality, when an individual defends a territory containing food resources and excludes competitors from the resource (
Typical behaviors exhibited by territorial hummingbirds are “perching near the food resource” (
The aim of this study was to evaluate the feeding behavior of hummingbirds in artificial food patches at an Atlantic Forest fragment in Brazil. We described the behavior exhibited by the hummingbirds in the food patches and identified the sugar concentration most visited by the birds. We hypothesized that: 1) most feeding visits would be to the feeders that have 35% sugar-concentration, since this food resource provides more energy to the birds (
The study was conducted in the Itacolomi State Park, in the city of Ouro Preto, Minas Gerais, southeastern Brazil (20°23’S, 43°30’W), in an Atlantic Forest remnant, from June to December 2012. Four artificial food patches, distant linearly 1.5-2.5 m from each other in a 6 m2 area, were constructed in the core of the forest fragment (70m distant from the forest edges), each containing five artificial hummingbird feeders (200 ml plastic feeders Mr Pet®, with three red plastic flowers with short corollas) filled with a sugar-water solution of 5, 15, 25 or 35%. Nectar sugar concentration was computed diluting commercial sucrose in filtered water; e.g., in 35% sugar concentration, 350 g of sucrose was diluted in 750 ml of filtered water. Each food patch contained feeders filled with only one concentration, which remained available all day long. The solution was replaced each morning after the feeders were cleaned.
Behavioral recording sessions occurred continuously from 07:00 to 10:00 a.m. and from 02:00 to 05:00 p.m. each day, totaling 325 hours of observation (54 non-consecutive days in total). The birds were observed at a distance of 10m, using a 10x50 (Nikon TX Extreme) binocular. Hummingbirds were observed ad libitum with continuous recording of behaviors (
Friedman’s non-parametric ANOVA with Dunn’s post-hoc tests were used to evaluate if the hummingbird species differed in the frequency of the behaviors they exhibited. Both frequency of behaviors and the time spent in the behavior were used in the analyses of the “feeding”, “alert” and “vocalizing” behaviors; only the number of observations was used in the analysis of the other behaviors evaluated. Time spent feeding was used to evaluate sugar concentrations most visited by each hummingbird species. The frequency of aggression behaviors recorded were summed (“expelling”, “fighting”, “frightening”, “expel attempt”, “alert” and “vocalizing”) and correlated with the time spent feeding on all sugar concentrations (5-35%) and with hummingbird sizes and weights – according to
Ethogram for the hummingbirds recorded at the Itacolomi State Park, Ouro Preto, Minas Gerais, Brazil.
Abbreviation | Behavior | Description |
---|---|---|
FEE | Feeding | Hummingbird feeds in the artificial feeder, hovering or perched. |
EXP | Expelling* | Hummingbird 1 expels hummingbird 2, pursuing it for long or small distances. |
FLE | Fleeing** | Hummingbird 1 flees from hummingbird 2, who expelled it. |
FIG | Fighting* | Hummingbirds fight using their beak. |
FRI | Frightening* | Hummingbird 1 frightens hummingbird 2 simply due to its appearance in the area. |
FRIED | Frightened** | Hummingbird 2 was frightened by hummingbird 1 simply due to its appearance in the area. |
EXA | Expel attempt* | Hummingbird 1 tries to expel hummingbird 2, but hummingbird 2 continues to feed without caring about the presence of hummingbird 1. |
IMP | Impassive | Hummingbird 2 behaves normally when hummingbird 1 tries to expel it from the feeders. |
PRS | Persecution with only one individual identified* | Hummingbird 1 pursue hummingbird 2, but only one individual is identified. |
AL | Alert* | Hummingbird perched, observing the food patches. |
VOC | Vocalizing* | Hummingbird vocalizes in or near the food patches. |
Average lengths (with tails and bills included) and weights of the hummingbird species recorded at Itacolomi State Park, Ouro Preto, according to
Species | Mean length (cm) | Mean weight (g) | Social status in this study |
---|---|---|---|
Amazilia versicolor | 8.5 | 4.1 | Subordinate |
Chlorostilbon lucidus | 8.5 | 2.5 | Subordinate |
Clytolaema rubricauda | 12.0 | 7.9 | Dominant |
Leucochloris albicollis | 10.5 | 6.3 | Subordinate |
Phaethornis eurynome | 15.5 | 5.3 | Subordinate |
Phaethornis spp. | 15.5 | 5.3 | Subordinate |
Thalurania glaucopis | 11.1 | 4.8 | Dominant |
Six species of hummingbirds of were recorded visiting the feeders during the study: Brazilian ruby Clytolaema rubricauda (Boddaert, 1783), Violet-capped woodnymph Thalurania glaucopis (Gmelin, 1788), Scale-throated hermit Phaethornis eurynome (Lesson, 1832), White-throated hummingbird Leucochloris albicollis (Vieillot, 1818), Versicoloured emerald Amazilia versicolor (Vieillot, 1818), Glittering-bellied emerald Chlorostilbon lucidus (Shaw, 1812) and an unidentified species of Phaethornis spp. [four species of Phaethornis Swainson, 1827 occur in the Itacolomi State Park: P. eurynome, P. pretrei (Lesson & Delattre, 1839), P. squalidus (Temminck, 1822) and P. ruber (Linnaeus, 1758) (
The most-visited feeders were those containing a solution of 35% sugar, and the least-visited feeders were those containing a solution of 5% sugar; the frequency of visitations differed between the feeders (F = 177.380, d.f. = 3, p < 0.001, n = 94).
Clytolaema rubricauda, P. eurynome and Phaethornis spp. visited the feeders with sugar solution of 35% more often (C. rubricauda: F = 164.5, d.f. = 3, p < 0.001, n = 4568; P. eurynome: F = 41.7, d.f. = 3, P < 0.001, n = 409; Phaethornis sp.: F = 9.6, d.f. = 3, p = 0.023, n = 71). Thalurania glaucopis visited more often the feeders containing a sugar solution of 25% (F = 154.6, d.f. = 3, p < 0.001, n = 5992). L. albicollis and A. versicolor visited the feeders containing a sugar solution of 15% more often (L. albicollis: F = 28.81, d.f. = 3, p < 0.001, n = 97; A. versicolor: F = 19.93, d.f. = 3, p < 0.001, n = 15). Chlorostilbon lucidus was the species that less frequently visited the food patches, and no differences were found between the number of visits in each food patch (F = 3.67, d.f. = 3, p = 0.34, n = 3, Fig.
The outcomes of aggressive encounters between different hummingbird species in relation to different sugar solution.
Winners | Losers | ||||||
Aggressive winning percentages between species | |||||||
A. versicolor | C. lucidus | C. rubricauda | L. albicollis | P. eurynome | Phaethornis sp. | T. glaucopis | |
C. rubricauda | – | – | – | 100.00% (12) | 100.00% (44) | 100.00% (9) | 87.66% (334) |
T. glaucopis | 100.00% (1) | 100.00% (1) | 12.34% (47) | 100.00% (20) | 100.00% (43) | 100.00% (10) | – |
Aggressive winning percentages between species in 5% patch | |||||||
A. versicolor | C. lucidus | C. rubricauda | L. albicollis | P. eurynome | Phaethornis sp. | T. glaucopis | |
C. rubricauda | – | – | – | – | – | – | 100.00% (7) |
T. glaucopis | 100.00% (1) | – | – | – | – | – | – |
Aggressive winning percentages between species in 15% patch | |||||||
A. versicolor | C. lucidus | C. rubricauda | L. albicollis | P. eurynome | Phaethornis sp. | T. glaucopis | |
C. rubricauda | – | – | – | 100.00% (2) | 100.00% (3) | – | 89.39% (59) |
T. glaucopis | – | – | 10.61% (7) | 100.00% (5) | 100.00% (4) | 100.00% (1) | – |
Aggressive winning percentages between species in 25% patch | |||||||
A. versicolor | C. lucidus | C. rubricauda | L. albicollis | P. eurynome | Phaethornis sp. | T. glaucopis | |
C. rubricauda | – | – | – | 100.00% (2) | 100.00% (9) | 100.00% (3) | 87.59% (120) |
T. glaucopis | – | 100.00% (1) | 12.41% (17) | 100.00% (5) | 100.00% (3) | 100.00% (3) | – |
Aggressive winning percentages between species in 35% patch | |||||||
A. versicolor | C. lucidus | C. rubricauda | L. albicollis | P. eurynome | Phaethornis sp. | T. glaucopis | |
C. rubricauda | – | – | – | 100.00% (3) | 100.00% (27) | 100.00% (6) | 88.55% (116) |
T. glaucopis | – | – | 11.45% (15) | 100.00% (7) | 100.00% (35) | 100.00% (4) | – |
Clytolaema rubricauda won most of the aggressive encounters with other hummingbird species, both in total and in each different sugar solution concentrations, followed by T. glaucopis (Table
Aggressive behaviors (“expelling”, “fighting”, and “expel attempt”) were exhibited by C. rubricauda, T. glaucopis, P. eurynome and L. albicollis. Among the aggressive behaviors, P. eurynome and L. albicollis exhibited only “expel attempts” against other hummingbirds (Table
Clytolaema rubricauda and T. glaucopis behaved similarly, being the most aggressive species observed (Table
Thalurania glaucopis got involved in the greatest number of pursuits in which only one bird was identified, and they also expressed more “expel attempts” (Table
Time spent feeding was positively correlated with the expression of aggressive behaviors (r = 0.86, p < 0.0001) (Fig.
Behaviors (mean number of total recordings ± standard error) exhibited by the six hummingbird species visiting artificial flowers in an Atlantic Forest remnant of Brazil, from June to December 2012.
Behaviors | Species | F | P-value | ||||||
A. versicolor | C. lucidus | C. rubricauda | L. albicollis | P. eurynome | Phaethornis spp. | T. glaucopis | |||
FEE | 0.16 ± 0.06 ª | 0.03 ± 0.02 ª | 48.45 ± 2.02 b | 1.05 ± 0.27 ª | 4.44 ± 0.56 c | 0.76 ± 0.16 ªc | 63.67 ± 3.71 b | 383.09 | < 0.001 |
EXP | – | – | 16.49 ± 1.65 ª | – | – | – | 7.62 ± 0.70 ª | 325.66 | < 0.001 |
FLE | 0.02 ± 0.02 ª | 0.03 ± 0.02 ª | 9.60 ± 0.02 b | 0.67 ± 0.19 ª | 1.26 ± 0.19 ª | 0.46 ± 0.10 ª | 12.13 ± 0.84 b | 324.56 | < 0.001 |
FIG | – | – | 0.58 ± 0.10 ª | – | – | – | 2.04 ± 0.27 ª | 72.66 | < 0.001 |
FRI | – | – | 0.96 ± 0.13 ª | 0.01 ± 0.01 b | 0.03 ± 0.09 bc | – | 0.51 ± 0.10 ªc | 59.06 | < 0.001 |
FRIED | 0.02 ± 0.02 ª | – | 0.32 ± 0.08 ª | 0.32 ± 0.02 ª | 0.53 ± 0.17 ª | 0.32 ± 0.02 ª | 0.87 ± 0.12 b | 47.68 | < 0.001 |
EXA | – | – | 0.03 ± 0.02 ªb | 0.01 ± 0.01 ª | 0.02 ± 0.02 ªb | – | 0.39 ± 0.07 b | 17.00 | 0.01 |
IMP | – | – | 0.36 ± 0.07 ª | – | 0.01 ± 0.01 b | – | 0.11 ± 0.04 ªb | 17.19 | 0.01 |
PRS | – | 0.01 ± 0.01 ª | 1.56 ± 0.33 b | – | 0.01 ± 0.01 ª | – | 1.88 ± 0.30 b | 77.11 | < 0.001 |
AL | 0.02 ± 0.02 ª | 0.03 ± 0.02 ª | 24.87 ± 1.84 b | 0.34 ± 0.11 ª | 0.10 ± 0.05 ª | 0.02 ± 0.02 ª | 18.40 ± 1.31 b | 341.38 | < 0.001 |
VOC | 0.10 ± 0.06 ª | 0.11 ± 0.04 ª | 2.44 ± 0.29 b | 0.22 ± 0.06 ª | 0.14 ± 0.04 ª | – | 1.67 ± 0.28 b | 138.76 | < 0.001 |
Positive correlation between the time spent feeding and the exhibition of aggressive behaviors by the hummingbirds. For this analysis, we included the time spent feeding by all hummingbird species in all sugar concentrations, and we summed the aggressive behaviors “expelling”, “fighting”, “frightening”, “expel attempt”, “alert” and “vocalizing”.
Positive correlation between size (cm) and the exhibition of aggressive (3) and submissive (4) behaviors by the hummingbirds. Positive correlation between weight (g) and the exhibition of aggressive (5) and submissive (6) behaviors by the hummingbirds. For both analysis, we included aggressive and submissive behaviors exhibited by all hummingbird species in all sugar concentrations, and we summed the aggressive behaviors “expelling”, “fighting”, “frightening”, “expel attempt”, “alert” and “vocalizing”, and the submissive behaviors “fleeing” and “frightened”.
Clytolaema rubricauda and T. glaucopis were considered dominant hummingbirds in this study since they presented the greatest feeding frequencies and were the most aggressive. Besides, since they expressed the behaviors “alert”, “expelling” and “vocalizing” more often than other species, they were also considered territorial. All other hummingbird species in our data fed less and expressed fewer aggressive behaviors, and were therefore considered subordinates.
Thalurania glaucopis and C. rubricauda also exhibited the “fleeing” behavior more often, due to the great number of pursuits within and between individuals of these two species. The frequency of aggressive behaviors exhibited by A. versicolor, L. albicollis, P. eurynome and Phaethornis spp. was statistically lower than by T. glaucopis and C. rubricauda; the former species were expelled from the feeders by the latter dominant species, therefore feeding less in the artificial patches. Dominant species limit the access of subordinate species to food sources (
One of the factors determining aggressive behavior in hummingbirds is body size; the bigger and heavier the hummingbird is, the more dominant it is (
Hummingbirds often show food preferences (
In conclusion, all three behavioral strategies related to food resources were recorded for this area of Atlantic Forest. Clytolaema rubricauda and T. glaucopis were the dominant species; A. versicolor, C. lucidus, and L. albicollis are the subordinate species, and P. eurynome and Phaethornis spp. are the species that used the trapline strategy or acted as subordinate species with an evasive strategy to avoid confrontations with the dominants. The richest sugar solutions, with 25% and 35% sugar concentration, were most visited by the dominant species and by Phaetornithinae species; subordinate species visited less rich food patches. Finally, aggression was directly linked to the time that a hummingbird spent feeding; the more aggressive it was, the more it fed.
We thank the staff of the Itacolomi State Park for the permission to use their facilities during the study. We would also like to thank UFOP for providing scholarship and logistic support to L. Lanna. CNPq and CAPES provided scholarship support to Y. Antonini (CNPq 306840/2015-4) and R. Oliveira (CAPES/PNPD-1432299), respectively. Finally, we thank R.J. Young for invaluable suggestions on this paper. We appreciate the improvements in English usage made by R. Cramer through the Association of Field Ornithologists’ program of editorial assistance.