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Southeastern Brazilian tyrannulets as flower watchers

Southeastern Brazilian tyrannulets as flower watchers Revista Brasileira de Ornitologia 27(3): 158–163. ARTICLE September 2019 1,2 3,4 Edwin O'Neill Willis & Glayson Ariel Bencke Instituto de Estudos da Natureza, Rio Claro, SP, Brazil. In memoriam. Museu de Ciências Naturais, Fundação Zoobotânica do Rio Grande do Sul, Porto Alegre, RS, Brazil. Corresponding author: gabencke@sema.rs.gov.br Received on 01 March 2018. Accepted on 02 September 2019. ABSTRACT: Several species of insect-eating birds occasionally visit flowering trees or shru bs to feed on arthropods at flowers instead of nectar or petals. In southeastern Brazil, the Planalto Tyrannulet Phyllomyias fasciatus (10.3 g) and the Gray-headed Tody- Flycatcher Todirostrum poliocephalum (7 g) often watch flowers to get insects and can visit flowering trees for hours or for several days. We describe the foraging behavior of these two tyrannulets at flowering trees and a lso report observations on several other species, mostly tyrant-fly catchers and tanagers. As an opportunistic foraging strategy, flower watching can be expected to be more common among small, canopy or edge birds that sally or hover-glean to catch small insects on or near foliage. KEY-WORDS: foraging behavior, insects, Phyllomyias fasciatus, tanagers, Todirostrum poliocephalum, tyrant-fly catchers. INTRODUCTION METHODS Birds often visit flowers for nec tar or to eat petals (Willis Most observations were at the Santa Lúcia Biological o o 2002). Insects attracted to flowers provid e another Station (19 58'S; 40 32'W, 650 m a.s.l.) in the Santa type of food, and certain birds watch flowers to c atch Teresa mountain range of central Espírito Santo state, them. Pereyra (1941) noted many birds eating insects Brazil. Flowering trees were mainly cultivated avocados in flowering c orn fields, and suggested that such birds Persea americana (Lauraceae) and Japanese Plums as the Spectacled Tyrant Hymenops perspicillatus could Eriobotrya japonica (Rosaceae) by the laboratory and help pollinate the crop. Beehler (1980) reported several several native yellow-flowered Senna multijuga var. species catching insects in flowering trees in New lindleyana (Fabaceae) along the entry road, 500 m Guinea, and the Green Honeycreeper Chlorophanes upriver. Observations were made with 8 × 30 and 10 × spiza in Panama (as described earlier by Snow & Snow 42 binoculars from an appropriate distance so as not to 1971). Stiles et al. (1989) reported the Tropical Kingbird disturb the birds. Tyrannus melancholicus getting butterflies near flowers, G.A.B. studied insectivorous and omnivorous birds and stated that the Black-headed Tody-Flycatcher foraging at flowers of three neighboring avocados on 04, Todirostrum nigriceps often forages in flowering trees. 05 and 09 September 1994, for a total of 1405 min. Tampson (1990) noted the Cattle Tyrant Machetornis For each bird visitation, data recorded included species, rixosa catching insects in palm flowers. Dobbs & number of individuals, arrival and departure time, foraging Greeney (2006) observed that nearly 1% of insects maneuvers and substrate of captures. Whenever it was captured by the Rufous-breasted Flycatcher Leptopogon not possible to record an individual's arrival or departure rufipectus are taken on flowers. time, we used the average visit length calculated for the Here, we discuss flower watching in south eastern species. Foraging maneuvers were classified a ccording to Brazil by the Gray-headed Tody-Flycatcher Todirostrum Remsen & Robinson (1990) into eight categories. These poliocephalum, a close relative of T. nigriceps, and the categories were then combined with substrates of capture Planalto Tyrannulet Phyllomyias fasciatus. These two to generate composite codes representing foraging tactics tyrannulets occasionally visit flowers for h ours, or for (e.g., SH/F indicates a sally-hover to capture an insect on a several days. We also report some observations for flower). E.O.W. studied P. fasciatus, M. fasciatus and other the Bran-colored Flycatcher Myiophobus fasciatus and species at flowers mainly April–May 1996. We also report others. observations on tyrant-fly catchers and other passerines Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke made elsewhere in southeastern Brazil. Scientific names throughout the morning and early afternoon (Table 1). Usually only one or two birds foraged in the trees of birds follow Piacentini et al. (2015). Bird body masses at the same time, but up to four were present on some are from Wilman et al. (2014). occasions. Prey were mostly captured in the air or at flowers with sally-strikes and, less frequently, sally-hover RESULTS and sally-pounce maneuvers. Nearly 62% of insect- catching attempts were at or near flowers ( Table 2). This species showed the greatest range of foraging maneuvers In September 1994, twelve species foraged on insects attracted to avocado flowers at Santa Lúcia (Table among all visitors. 1). Ten others visited flowers ex clusively for nectar The avocado flowers were visited earlier by a T. (Thalurania glaucopis, Coereba flaveola and Dacnis cayana) poliocephalum on 03 September 1994, with short strikes or perched/foraged away from flowers (Cranioleuca under leaves near the flowers. We have often seen it sallying under leaves away from flowers, at dense vine pallida, Xenops rutilans, Piprites chloris, Camptostoma obsoletum, Lathrotriccus euleri, Euphonia violacea and tangles in woods or at edges. E.O.W. also noted visits Tangara cayana). Todirostrum poliocephalum, P. fasciatus by two P. fasciatus, which sallied to the air or leaves near and three tanagers visited the trees in more than one day flowers at 10–12 h. Later, two bir ds were sallying in a small and made considerably more visits or spent considerably flowering tree (not identified) in the woods downriver. We have seen it sallying away from flowers, or getting more time foraging at flowers than other species (Table 1). Todirostrum poliocephalum spent the largest amount Myrsine fruit or Alchornea arils, on other occasions. of time on trees and made long visits concentrated in the On 24 April 1996, 16:22–16:28 h, one P. fasciatus second half of the morning, when it was a regular and sallied for insects in the Senna. On the 25 April, between constant visitor. Typically, one bird of a pair that held a 9–10 h, two were now and then near Japanese Plum flowers by the lab, between visits by tanagers and relatives that territory in the area would forage for long periods in the avocados, sometimes accompanied by its mate. Aerial poked their bills deep into the flowers ( D. cayana, Tangara maneuvers (short sally-strikes and, to a lesser extent, sally- seledon and Schistochlamys ruficapillus) . A T. poliocephalum pounces and leaps) were used to capture prey mainly on worked briefly near one of th e P. fasciatus, but soon left. On substrates other than air, and about 65% of captures were the 26 April, E.O.W. watched at the Senna from 15:24 h to dark at 17:30 h. The main visitor was a M. fasciatus, but on or very close to flowers ( Table 2). Phyllomyias fasciatus was the most frequent species two P. fasciatus worked 16:00 h in the crowns, sallying to in the avocados. It made medium-length regular visits catch insects on flowers several times. Table 1. Number of visits on each day of observation, total number of visits, mean length of visits (min), total time spent on trees (min) and average number of individuals per visit for birds recorded foraging on insects attracted to avocado flowers at Santa Lúcia, Espírito Santo state, Brazil, in September 1994. No. of visits/day Total time Average No. Total No. Mean length Species spent on of individuals 04 05 09 of visits of visits trees per visit Sept Sept Sept Todirostrum poliocephalum - 3 8 11 26.3 289 1.1 Phyllomyias fasciatus - 8 19 27 9.2 249 1.2 Saltator maximus - 1 7 8 8.9 71 1.0 Tangara ornata - 3 17 20 2.8 56 1.3 Tangara sayaca - 1 4 5 5.0 25 1.6 Tolmomyias sulphurescens - - 6 6 3.2* 19.5* +1.0 Hemitriccus nidipendulus 2 - 1 3 3.0 9 1.0 Pachyramphus castaneus - 1 2 3 1.7 5 1.0 Pachyramphus viridis - - 2 2 1.2 2.5 1.0 Contopus cinereus - - 2 2 0.7 1.5 1.0 Piaya cayana - - 1 1 1.0 1 1.0 Hylophilus poicilotis - 1 - 1 1.0 1 1.0 Total 218 69 89- - - *possibly overestimated because the length of some visits could not be determined. Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke Table 2. Frequency of use of foraging tactics by five species with t he longest time of association with flowering avocados at Santa Lúcia, Espírito Santo state, Brazil, in September 1994. Attack maneuvers: SS – sally-strike; SP – sally-pounce; SH – sally-hover; FCh – flutter-chase; Le – leap; Lu – lunge; RO – reach-out; RU – reach-up (from Remsen & Robinson 1990). Substrates: A – air; F – flower; UL – upper surface of leaves; LL – lower surface of leaves; B – branch; Fo – foliage (used when a substrate other than air could not be determined). An asterisk after the substrate code indicates captures near flowers. Maneuver/ Phyllomyias Todirostrum Tangara Tangara Saltator substrate fasciatus poliocephalum ornata sayaca maximus SS/A (SS/A*) 49 (26) 7 (5) -3 (2) 2 SS/F 26 18 2 - 2 SS/LL 2 3 - - - SS/UL 3 ---- SS/Fo 5 - - - 1 SS/B 2 4 - - - SP - -1-1 SP/F 6 5 - - - SP/Fo 1 ---- SH 1 ---- SH/F 6 ---- FCh -- 1 1 - Le - -3- - Le/A 2 ---- Le/B (Le/B*) 1 (1) 2 --- Le/F 2 2-1- Le/LL - 2 - - - Le/Fo - 2 - - - Lu 2-1 1- Lu/F - - - 1 - RO - 1 --- RO/F 1 1 - - - RO/A* 1-1- - RO/UP - 1 - - - RU/F 1 ---- RU/A* - - 1 - - n 111 48 10 7 6 On 14 May, 15:54 h, two P. fasciatus were back (all next to flowers or leaves). At 15:44 h, two were in to the Senna and worked near flowers, at times pecking the Senna trees, sallying four times before moving to a deep inside, 16:00–16:10 h. After 5 min in the low Myrsine bush with tiny flowers. Between 16:01–16:04 h, bushes below, one returned for 3 min to sally to air or two P. fasciatus returned, sallying eight times or more to leaves near flowers, and again at 16:21 h for several sallies the air by flowers. Between 16:10–16:34 h one worked to the air, then dropping to a Cecropia below. A third bird the flowers, preening and regurgitating two seeds on a and the two moved into the Senna 16:24 h to 16:32 h, twig and defecating another, before 32 short sallies to then wandered off. At 16:42 h, a P. fasciatus returned for near flowers 16:19–16:32 h. Between 16:36–16:38 h, six more short sallies to the air, moving off b y 16:50 h. one returned for five short sallies, then to a Cecropia off On 19 May, there were several visits by P. fasciatus. east. Two and then three birds continued to sally in the Between 14:38–14:51 h one did ten air sallies and three area 16:40 h on, using other trees and a telephone wire, pecks into flowers before preening, then five other sallies but between 17:00–17:10 h some sallies were again near Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke flowers, after which bir ds wandered off for the night. flavogaster and t he White-crested Tyrannulet Serpophaga On most days, the M. fasciatus worked low bushes subcristata. under or near the Senna. On 26 April, however, one In southern Brazil, G.A.B. noticed two other sallied in the midlevels of the Senna at 15:46 h, returning tyrant-fly catchers watching flowers of bushes to catch 15:52 h after some long calls and sallying to near flowers. insects (Table 3). In addition, in the Pampas grasslands o o It fle d if people or bicycles passed, but returned to catch around Lavras do Sul (30 48'S; 53 54'W, 315 m a.s.l.), insects with sallies to flowers, the air, or foliage; at 16:23 05–08 January 2018, at least three species of tyrant- h it dropped to bushes, sallied to the ground in the road fly catchers were plucking soldier beetles Chauliognathus a few times, and did not return to the flowers. The next flavipes (Cantharidae) from the umbellate flower stalks of morning, 08:05–08:15 h, the M. fasciatus was less timid Eryngium chamissonis (Urb., 1879) (Apiaceae) in densely and sallied to or near flowers up one tree several times. vegetated upland swales dominated by this spiny sedge. Elsewhere, E.O.W. noted P. fasciatus, M. fasciatus These polymorphic, soft-elytra beetles are distinctly and six other small fly catchers sallying or hovering for colored with yellow and black and gather by the thousands insects near flowers of trees or bushes in southeastern on the upright inflorescences of E. chamissonis, which Brazil (Table 3). Late on 15 August 2002, fallen flowers rise up to 1.5 m above the vegetative stratum in mid- of Tabebuia chrysotricha (Bignoniaceae) on the lawn of summer to form a temporary emergent layer of flowering o o the UNESP Campus (22 23'S; 47 33'W, 620 m a.s.l.), shoots. Birds seen capturing the beetles in a more or less Rio Claro, São Paulo state, attracted insect-eating birds systematic way included a family group of Yellow-browed such as the Great Kiskadee Pitangus sulphuratus, M. rixosa, Tyrants Satrapa icterophrys on the 04 January, plus a woodpeckers, wrens and others, while flowers in the solitary individual on the 06 January, and two M. fasciatus trees nearby attracted the Yellow-bellied Elaenia Elaenia on the 05 and 08 January, at four different locations. One Table 3. Observations of tyrant-fly catchers (Rhynchocyclidae and Tyrannidae) foraging on insects attracted by flowers in southeastern Brazil. Locality (coordinates, altitude, Species Plant (family) Date (observer)** a.s.l.)* Phylloscartes ventralis Rubus rosifolius Mariana Pimentel, RS Mottle-cheeked 18 July 1997 (1) o o (Rosaceae) (30 19'S; 51 36'W, 230 m) Tyrannulet Tolmomyias sulphurescens Ceiba speciosa near Broa Reservoir, SP 25 March 1984 (2) o o Yellow-olive Flycatcher (Malvaceae) (22 08'S; 47 52'W, 740 m) Todirostrum cinereum Sooretama, ES Common Tody- Inga sp. (Fabaceae) 27 December 1992 (2) o o (19 03'S; 40 09'W, 85 m) Flycatcher Vochysia sp. Rio do Cipó, MG 20 December 1997 (2) o o (Vochysiaceae) (18 40'; 43 59', 570 m) Phyllomyias fasciatus Planalto Tyrannulet Campos do Jordão, SP unidentified bush 11 August 2001 (2) o o (22 38'S; 45 26'W, 1600 m) Phyllomyias griseocapilla Augusto Ruschi Biological Reserve, ES unidentified flowers September 2002 (2) o o Gray-capped Tyrannulet (19 54'S; 40 33'W, 850 m) Culicivora caudacuta Broa prairie, SP tiny flowers of bushes 14 June 2002 (2) o o Sharp-tailed Tyrant (22 14'S; 47 52'W, 715 m) Myiarchus swainsoni unidentified ye llow Intervales, SP 04 March 1988 (2) o o Swainson's Flycatcher flowers (24 16'S; 48 25'W, 830 m) Myiarchus ferox Croton floribundus Fazenda São José, SP 12 January 1992 (2) o o Short-crested Flycatcher (Euphorbiaceae) (22 21'S; 47 29'W, 650 m) Myiophobus fasciatus Inga sp. (Fabaceae) Fazenda São José, SP 09 September 2001 (2) Bran-colored Flycatcher Muscipipra vetula Shear- Tecoma stans Monte Alverne, RS 23 September 1995 (1) o o tailed Gray Tyrant (Bignoniaceae) (29 34'S; 52 22'W, 350 m) *Acronyms of states: ES – Espírito Santo, MG – Minas Gerais, SP – São Paulo, RS – Rio Grande do Sul. **Observers: 1: G.A. Bencke, 2: E.O. Willis. Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke Highland Elaenia Elaenia obscura also briefly fed on the periods as compared to similarly sized species that also insects on the first day. Beetles were picked or snapped off feed on fruits, presumably because they are able to find flower heads and outermost peduncles mostly with glean, most of their food items in the flowers and/or foliage, and reach and leap maneuvers, and the birds seemed to make also because arthropods at flowers are a rapidly renewing little effort to catch t hem, since prey was everywhere and resource (Beehler 1980). In contrast, P. fasciatus and almost stationary. several tanagers make more frequent but shorter visits to flowering trees, possibly because insects are only part Other species of their diet. Individuals of P. fasciatus observed at Santa Lúcia often regurgitated mistletoe seeds upon arriving at On 27 April 1996, a tanager flock visited Senna trees by the flowering trees, indicating they had been feeding on the lab of the Museu de Biologia Mello Leitão (19 58'S; fruit shortly before. 40 36'W, 680 m a.s.l.), Santa Teresa, sallying to air or leaves Several other Tyrannoidea visit eucalyptus or other for insects near or far from flowers (Tangara palmarum, flowers, but more study is needed to establish whether T. ornata, T. sayaca, and T. cayana). A female Barred arthropods, nectar, or pollen are used. We did not Antshrike Thamnophilus doliatus pecked an insect from confirm any activity that could have pollinated flowers, a Bauhinia flower (Fa baceae) at Barão Geraldo District except when one bird put its head in a flower. F light near o o (22 50'S; 47 05'W, 620 m a.s.l.), Campinas, São Paulo flowers could have picked up some pollen, but tanagers state, on 06 June 1998 (E.O.W.). On 15 October 1995, and others that visit flowers directly are more likely to a male Hepatic Tanager Piranga flava worked t he crown pollinate. of a flowering Phytolacca dioica tree (Phytolaccaceae) for o o ACKNOWLEDGEMENTS about 25 min at Itati (29 23'S; 50 11'W, 230 m a.s.l.), Rio Grande do Sul state, hopping and jumping along branches to catch insects on or near flowers with s hort We wish to express our gratitude to Yoshika Oniki-Willis for her generous assistance and to two anonymous referees sallies, flutter-chases and one reach-out; the bird often for valuable comments on the manuscript. We appreciate watched closely the movements of flying insects around the logistic support and permission provided by the flowers before attempting to capture its prey (G.A.B.). managers of the various protected areas we visited. G.A.B. benefited from scholarship support b y the Coordenação DISCUSSION de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Publication number 79 of the Institute for Studies of Nature. The temporary association of insect-eating birds with flowering trees or shru bs is scarcely documented in the literature. We expect this opportunistic behavior to be REFERENCES more common among small-bodied, edge or canopy- dwelling birds that sally or hover-glean to catch small Baker H.G., Bawa K.S., Frankie G.W. & Opler P.A. 1983. insects on or near foliage, because i) insects attracted to Reproductive biology of plants in tropical forests, p. 183–215. flowers are usually small (mostly hymenopterans, flies and In: Golley F.B. (ed.). Tropical rainforest ecosystems: ecosystems of the beetles, but also butterflies and moths; Willmer 2011), world. New York: Elsevier. making them non-rewarding prey for larger birds; ii) Beehler B. 1980. A comparison of avian foraging at flowering trees in Panama and New Guinea. Wilson Bulletin 92: 513–519. plant species showing massive flowering (i.e., producing Cronk Q. & Ojeda I. 2008. Bird-pollinated flowers in an evolutionary large numbers of exposed flowers to attract relatively non- and molecular context. Journal of Experimental Botany 59: 715– specialized pollinators) predominate in the upper strata of tropical forests and along borders (Janzen 1975, Baker et Dobbs R.C. & Greeney H.F. 2006. Nesting and foraging ecology of the Rufous-breasted Flycatcher (Leptopogon rufipectus). Ornitología al. 1983); and iii) flowers are rarely accessible directly to Neotropical 17: 173–181. perching birds in the New World (Cronk & Ojeda 2008). Janzen D.H. 1975. Ecology of plants in the tropics. London: Edward In southeastern Brazil, P. fasciatus (10.3 g) often Arnold. watches flowers and sallies for or pecks insects, T. Pereyra J.A. 1941. Polinización de las flores por las aves. Hornero 8: poliocephalum (7 g) and M. fasciatus (9.9 g) less. As 222–224. Piacentini V.Q., Aleixo A., Agne C.E., Maurício G.N., Pacheco J.F., illustrated here, many other birds (mass range 6.3–102 g) Bravo G.A., Brito R.R.R., Naka L.N., Olmos F., Posso S., Silveira visit flowering trees to get insects, but they move through L.F., Betini G.S., Carrano E., Franz I., Lees A.C., Lima L.M., the trees and do not obviously watch flowers as do the Pioli D., Schunck F., Amaral F.R., Bencke G.A., Cohn-Haft M., tyrannulets above, or perhaps do it for shorter periods Figueiredo L.F.A., Straube F.C. & Cesari E. 2015. Annotated checklist of the birds of Brazil by the Brazilian Ornithological (e.g., Piranga flava). Wholly insectivorous birds such as Records Committee. Revista Brasileira de Ornitologia 23: 91–298. T. poliocephalum may forage in flowering trees for longer Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke Remsen J.V. & Robinson S.K. 1990. A classification scheme for Brasil (1983–1988). Acta Biologica Leopoldensia 12: 19–37. foraging behavior of birds in terrestrial habitats, p. 144–160. In: Willis E.O. 2002. Birds at Eucalyptus and other flowers in southern Morrison M.L., Ralph C.J., Verner J. & Jehl-Jr. J.R. (eds.). Avian Brazil: a review. Ararajuba 10: 43–66. foraging: theory, methodology, and applications. San Diego: Cooper Wilman H., Belmaker J., Simpson J., Rosa C., Rivadeneira M.M. & Ornithological Society (Studies in Avian Biology No. 13). Jetz W. 2014. EltonTraits 1.0: species-level foraging attributes of Snow B.K. & Snow D.W. 1971. The feeding ecology of tanagers and the world's birds and mammals. Ecology 95: 2027. honeycreepers in Trinidad. Auk 88: 291–322. Willmer P. 2011. Pollination and floral ecology. Oxfor d: Princeton Stiles F.G., Skutch A.F. & Gardner D. 1989. A guide to the birds of University Press. Costa Rica. Ithaca: Cornell University Press. Tampson V.E. 1990. Lista comentada das espécies de aves registradas para o Morro do Espelho, São Leopoldo, Rio Grande do Sul, Associate Editor: Caio G. Machado. Revista Brasileira de Ornitologia 27(3): 2019 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Southeastern Brazilian tyrannulets as flower watchers

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Revista Brasileira de Ornitologia 27(3): 158–163. ARTICLE September 2019 1,2 3,4 Edwin O'Neill Willis & Glayson Ariel Bencke Instituto de Estudos da Natureza, Rio Claro, SP, Brazil. In memoriam. Museu de Ciências Naturais, Fundação Zoobotânica do Rio Grande do Sul, Porto Alegre, RS, Brazil. Corresponding author: gabencke@sema.rs.gov.br Received on 01 March 2018. Accepted on 02 September 2019. ABSTRACT: Several species of insect-eating birds occasionally visit flowering trees or shru bs to feed on arthropods at flowers instead of nectar or petals. In southeastern Brazil, the Planalto Tyrannulet Phyllomyias fasciatus (10.3 g) and the Gray-headed Tody- Flycatcher Todirostrum poliocephalum (7 g) often watch flowers to get insects and can visit flowering trees for hours or for several days. We describe the foraging behavior of these two tyrannulets at flowering trees and a lso report observations on several other species, mostly tyrant-fly catchers and tanagers. As an opportunistic foraging strategy, flower watching can be expected to be more common among small, canopy or edge birds that sally or hover-glean to catch small insects on or near foliage. KEY-WORDS: foraging behavior, insects, Phyllomyias fasciatus, tanagers, Todirostrum poliocephalum, tyrant-fly catchers. INTRODUCTION METHODS Birds often visit flowers for nec tar or to eat petals (Willis Most observations were at the Santa Lúcia Biological o o 2002). Insects attracted to flowers provid e another Station (19 58'S; 40 32'W, 650 m a.s.l.) in the Santa type of food, and certain birds watch flowers to c atch Teresa mountain range of central Espírito Santo state, them. Pereyra (1941) noted many birds eating insects Brazil. Flowering trees were mainly cultivated avocados in flowering c orn fields, and suggested that such birds Persea americana (Lauraceae) and Japanese Plums as the Spectacled Tyrant Hymenops perspicillatus could Eriobotrya japonica (Rosaceae) by the laboratory and help pollinate the crop. Beehler (1980) reported several several native yellow-flowered Senna multijuga var. species catching insects in flowering trees in New lindleyana (Fabaceae) along the entry road, 500 m Guinea, and the Green Honeycreeper Chlorophanes upriver. Observations were made with 8 × 30 and 10 × spiza in Panama (as described earlier by Snow & Snow 42 binoculars from an appropriate distance so as not to 1971). Stiles et al. (1989) reported the Tropical Kingbird disturb the birds. Tyrannus melancholicus getting butterflies near flowers, G.A.B. studied insectivorous and omnivorous birds and stated that the Black-headed Tody-Flycatcher foraging at flowers of three neighboring avocados on 04, Todirostrum nigriceps often forages in flowering trees. 05 and 09 September 1994, for a total of 1405 min. Tampson (1990) noted the Cattle Tyrant Machetornis For each bird visitation, data recorded included species, rixosa catching insects in palm flowers. Dobbs & number of individuals, arrival and departure time, foraging Greeney (2006) observed that nearly 1% of insects maneuvers and substrate of captures. Whenever it was captured by the Rufous-breasted Flycatcher Leptopogon not possible to record an individual's arrival or departure rufipectus are taken on flowers. time, we used the average visit length calculated for the Here, we discuss flower watching in south eastern species. Foraging maneuvers were classified a ccording to Brazil by the Gray-headed Tody-Flycatcher Todirostrum Remsen & Robinson (1990) into eight categories. These poliocephalum, a close relative of T. nigriceps, and the categories were then combined with substrates of capture Planalto Tyrannulet Phyllomyias fasciatus. These two to generate composite codes representing foraging tactics tyrannulets occasionally visit flowers for h ours, or for (e.g., SH/F indicates a sally-hover to capture an insect on a several days. We also report some observations for flower). E.O.W. studied P. fasciatus, M. fasciatus and other the Bran-colored Flycatcher Myiophobus fasciatus and species at flowers mainly April–May 1996. We also report others. observations on tyrant-fly catchers and other passerines Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke made elsewhere in southeastern Brazil. Scientific names throughout the morning and early afternoon (Table 1). Usually only one or two birds foraged in the trees of birds follow Piacentini et al. (2015). Bird body masses at the same time, but up to four were present on some are from Wilman et al. (2014). occasions. Prey were mostly captured in the air or at flowers with sally-strikes and, less frequently, sally-hover RESULTS and sally-pounce maneuvers. Nearly 62% of insect- catching attempts were at or near flowers ( Table 2). This species showed the greatest range of foraging maneuvers In September 1994, twelve species foraged on insects attracted to avocado flowers at Santa Lúcia (Table among all visitors. 1). Ten others visited flowers ex clusively for nectar The avocado flowers were visited earlier by a T. (Thalurania glaucopis, Coereba flaveola and Dacnis cayana) poliocephalum on 03 September 1994, with short strikes or perched/foraged away from flowers (Cranioleuca under leaves near the flowers. We have often seen it sallying under leaves away from flowers, at dense vine pallida, Xenops rutilans, Piprites chloris, Camptostoma obsoletum, Lathrotriccus euleri, Euphonia violacea and tangles in woods or at edges. E.O.W. also noted visits Tangara cayana). Todirostrum poliocephalum, P. fasciatus by two P. fasciatus, which sallied to the air or leaves near and three tanagers visited the trees in more than one day flowers at 10–12 h. Later, two bir ds were sallying in a small and made considerably more visits or spent considerably flowering tree (not identified) in the woods downriver. We have seen it sallying away from flowers, or getting more time foraging at flowers than other species (Table 1). Todirostrum poliocephalum spent the largest amount Myrsine fruit or Alchornea arils, on other occasions. of time on trees and made long visits concentrated in the On 24 April 1996, 16:22–16:28 h, one P. fasciatus second half of the morning, when it was a regular and sallied for insects in the Senna. On the 25 April, between constant visitor. Typically, one bird of a pair that held a 9–10 h, two were now and then near Japanese Plum flowers by the lab, between visits by tanagers and relatives that territory in the area would forage for long periods in the avocados, sometimes accompanied by its mate. Aerial poked their bills deep into the flowers ( D. cayana, Tangara maneuvers (short sally-strikes and, to a lesser extent, sally- seledon and Schistochlamys ruficapillus) . A T. poliocephalum pounces and leaps) were used to capture prey mainly on worked briefly near one of th e P. fasciatus, but soon left. On substrates other than air, and about 65% of captures were the 26 April, E.O.W. watched at the Senna from 15:24 h to dark at 17:30 h. The main visitor was a M. fasciatus, but on or very close to flowers ( Table 2). Phyllomyias fasciatus was the most frequent species two P. fasciatus worked 16:00 h in the crowns, sallying to in the avocados. It made medium-length regular visits catch insects on flowers several times. Table 1. Number of visits on each day of observation, total number of visits, mean length of visits (min), total time spent on trees (min) and average number of individuals per visit for birds recorded foraging on insects attracted to avocado flowers at Santa Lúcia, Espírito Santo state, Brazil, in September 1994. No. of visits/day Total time Average No. Total No. Mean length Species spent on of individuals 04 05 09 of visits of visits trees per visit Sept Sept Sept Todirostrum poliocephalum - 3 8 11 26.3 289 1.1 Phyllomyias fasciatus - 8 19 27 9.2 249 1.2 Saltator maximus - 1 7 8 8.9 71 1.0 Tangara ornata - 3 17 20 2.8 56 1.3 Tangara sayaca - 1 4 5 5.0 25 1.6 Tolmomyias sulphurescens - - 6 6 3.2* 19.5* +1.0 Hemitriccus nidipendulus 2 - 1 3 3.0 9 1.0 Pachyramphus castaneus - 1 2 3 1.7 5 1.0 Pachyramphus viridis - - 2 2 1.2 2.5 1.0 Contopus cinereus - - 2 2 0.7 1.5 1.0 Piaya cayana - - 1 1 1.0 1 1.0 Hylophilus poicilotis - 1 - 1 1.0 1 1.0 Total 218 69 89- - - *possibly overestimated because the length of some visits could not be determined. Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke Table 2. Frequency of use of foraging tactics by five species with t he longest time of association with flowering avocados at Santa Lúcia, Espírito Santo state, Brazil, in September 1994. Attack maneuvers: SS – sally-strike; SP – sally-pounce; SH – sally-hover; FCh – flutter-chase; Le – leap; Lu – lunge; RO – reach-out; RU – reach-up (from Remsen & Robinson 1990). Substrates: A – air; F – flower; UL – upper surface of leaves; LL – lower surface of leaves; B – branch; Fo – foliage (used when a substrate other than air could not be determined). An asterisk after the substrate code indicates captures near flowers. Maneuver/ Phyllomyias Todirostrum Tangara Tangara Saltator substrate fasciatus poliocephalum ornata sayaca maximus SS/A (SS/A*) 49 (26) 7 (5) -3 (2) 2 SS/F 26 18 2 - 2 SS/LL 2 3 - - - SS/UL 3 ---- SS/Fo 5 - - - 1 SS/B 2 4 - - - SP - -1-1 SP/F 6 5 - - - SP/Fo 1 ---- SH 1 ---- SH/F 6 ---- FCh -- 1 1 - Le - -3- - Le/A 2 ---- Le/B (Le/B*) 1 (1) 2 --- Le/F 2 2-1- Le/LL - 2 - - - Le/Fo - 2 - - - Lu 2-1 1- Lu/F - - - 1 - RO - 1 --- RO/F 1 1 - - - RO/A* 1-1- - RO/UP - 1 - - - RU/F 1 ---- RU/A* - - 1 - - n 111 48 10 7 6 On 14 May, 15:54 h, two P. fasciatus were back (all next to flowers or leaves). At 15:44 h, two were in to the Senna and worked near flowers, at times pecking the Senna trees, sallying four times before moving to a deep inside, 16:00–16:10 h. After 5 min in the low Myrsine bush with tiny flowers. Between 16:01–16:04 h, bushes below, one returned for 3 min to sally to air or two P. fasciatus returned, sallying eight times or more to leaves near flowers, and again at 16:21 h for several sallies the air by flowers. Between 16:10–16:34 h one worked to the air, then dropping to a Cecropia below. A third bird the flowers, preening and regurgitating two seeds on a and the two moved into the Senna 16:24 h to 16:32 h, twig and defecating another, before 32 short sallies to then wandered off. At 16:42 h, a P. fasciatus returned for near flowers 16:19–16:32 h. Between 16:36–16:38 h, six more short sallies to the air, moving off b y 16:50 h. one returned for five short sallies, then to a Cecropia off On 19 May, there were several visits by P. fasciatus. east. Two and then three birds continued to sally in the Between 14:38–14:51 h one did ten air sallies and three area 16:40 h on, using other trees and a telephone wire, pecks into flowers before preening, then five other sallies but between 17:00–17:10 h some sallies were again near Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke flowers, after which bir ds wandered off for the night. flavogaster and t he White-crested Tyrannulet Serpophaga On most days, the M. fasciatus worked low bushes subcristata. under or near the Senna. On 26 April, however, one In southern Brazil, G.A.B. noticed two other sallied in the midlevels of the Senna at 15:46 h, returning tyrant-fly catchers watching flowers of bushes to catch 15:52 h after some long calls and sallying to near flowers. insects (Table 3). In addition, in the Pampas grasslands o o It fle d if people or bicycles passed, but returned to catch around Lavras do Sul (30 48'S; 53 54'W, 315 m a.s.l.), insects with sallies to flowers, the air, or foliage; at 16:23 05–08 January 2018, at least three species of tyrant- h it dropped to bushes, sallied to the ground in the road fly catchers were plucking soldier beetles Chauliognathus a few times, and did not return to the flowers. The next flavipes (Cantharidae) from the umbellate flower stalks of morning, 08:05–08:15 h, the M. fasciatus was less timid Eryngium chamissonis (Urb., 1879) (Apiaceae) in densely and sallied to or near flowers up one tree several times. vegetated upland swales dominated by this spiny sedge. Elsewhere, E.O.W. noted P. fasciatus, M. fasciatus These polymorphic, soft-elytra beetles are distinctly and six other small fly catchers sallying or hovering for colored with yellow and black and gather by the thousands insects near flowers of trees or bushes in southeastern on the upright inflorescences of E. chamissonis, which Brazil (Table 3). Late on 15 August 2002, fallen flowers rise up to 1.5 m above the vegetative stratum in mid- of Tabebuia chrysotricha (Bignoniaceae) on the lawn of summer to form a temporary emergent layer of flowering o o the UNESP Campus (22 23'S; 47 33'W, 620 m a.s.l.), shoots. Birds seen capturing the beetles in a more or less Rio Claro, São Paulo state, attracted insect-eating birds systematic way included a family group of Yellow-browed such as the Great Kiskadee Pitangus sulphuratus, M. rixosa, Tyrants Satrapa icterophrys on the 04 January, plus a woodpeckers, wrens and others, while flowers in the solitary individual on the 06 January, and two M. fasciatus trees nearby attracted the Yellow-bellied Elaenia Elaenia on the 05 and 08 January, at four different locations. One Table 3. Observations of tyrant-fly catchers (Rhynchocyclidae and Tyrannidae) foraging on insects attracted by flowers in southeastern Brazil. Locality (coordinates, altitude, Species Plant (family) Date (observer)** a.s.l.)* Phylloscartes ventralis Rubus rosifolius Mariana Pimentel, RS Mottle-cheeked 18 July 1997 (1) o o (Rosaceae) (30 19'S; 51 36'W, 230 m) Tyrannulet Tolmomyias sulphurescens Ceiba speciosa near Broa Reservoir, SP 25 March 1984 (2) o o Yellow-olive Flycatcher (Malvaceae) (22 08'S; 47 52'W, 740 m) Todirostrum cinereum Sooretama, ES Common Tody- Inga sp. (Fabaceae) 27 December 1992 (2) o o (19 03'S; 40 09'W, 85 m) Flycatcher Vochysia sp. Rio do Cipó, MG 20 December 1997 (2) o o (Vochysiaceae) (18 40'; 43 59', 570 m) Phyllomyias fasciatus Planalto Tyrannulet Campos do Jordão, SP unidentified bush 11 August 2001 (2) o o (22 38'S; 45 26'W, 1600 m) Phyllomyias griseocapilla Augusto Ruschi Biological Reserve, ES unidentified flowers September 2002 (2) o o Gray-capped Tyrannulet (19 54'S; 40 33'W, 850 m) Culicivora caudacuta Broa prairie, SP tiny flowers of bushes 14 June 2002 (2) o o Sharp-tailed Tyrant (22 14'S; 47 52'W, 715 m) Myiarchus swainsoni unidentified ye llow Intervales, SP 04 March 1988 (2) o o Swainson's Flycatcher flowers (24 16'S; 48 25'W, 830 m) Myiarchus ferox Croton floribundus Fazenda São José, SP 12 January 1992 (2) o o Short-crested Flycatcher (Euphorbiaceae) (22 21'S; 47 29'W, 650 m) Myiophobus fasciatus Inga sp. (Fabaceae) Fazenda São José, SP 09 September 2001 (2) Bran-colored Flycatcher Muscipipra vetula Shear- Tecoma stans Monte Alverne, RS 23 September 1995 (1) o o tailed Gray Tyrant (Bignoniaceae) (29 34'S; 52 22'W, 350 m) *Acronyms of states: ES – Espírito Santo, MG – Minas Gerais, SP – São Paulo, RS – Rio Grande do Sul. **Observers: 1: G.A. Bencke, 2: E.O. Willis. Revista Brasileira de Ornitologia 27(3): 2019 Tyrannulets as flower watchers Willis & Bencke Highland Elaenia Elaenia obscura also briefly fed on the periods as compared to similarly sized species that also insects on the first day. Beetles were picked or snapped off feed on fruits, presumably because they are able to find flower heads and outermost peduncles mostly with glean, most of their food items in the flowers and/or foliage, and reach and leap maneuvers, and the birds seemed to make also because arthropods at flowers are a rapidly renewing little effort to catch t hem, since prey was everywhere and resource (Beehler 1980). In contrast, P. fasciatus and almost stationary. several tanagers make more frequent but shorter visits to flowering trees, possibly because insects are only part Other species of their diet. Individuals of P. fasciatus observed at Santa Lúcia often regurgitated mistletoe seeds upon arriving at On 27 April 1996, a tanager flock visited Senna trees by the flowering trees, indicating they had been feeding on the lab of the Museu de Biologia Mello Leitão (19 58'S; fruit shortly before. 40 36'W, 680 m a.s.l.), Santa Teresa, sallying to air or leaves Several other Tyrannoidea visit eucalyptus or other for insects near or far from flowers (Tangara palmarum, flowers, but more study is needed to establish whether T. ornata, T. sayaca, and T. cayana). A female Barred arthropods, nectar, or pollen are used. We did not Antshrike Thamnophilus doliatus pecked an insect from confirm any activity that could have pollinated flowers, a Bauhinia flower (Fa baceae) at Barão Geraldo District except when one bird put its head in a flower. F light near o o (22 50'S; 47 05'W, 620 m a.s.l.), Campinas, São Paulo flowers could have picked up some pollen, but tanagers state, on 06 June 1998 (E.O.W.). On 15 October 1995, and others that visit flowers directly are more likely to a male Hepatic Tanager Piranga flava worked t he crown pollinate. of a flowering Phytolacca dioica tree (Phytolaccaceae) for o o ACKNOWLEDGEMENTS about 25 min at Itati (29 23'S; 50 11'W, 230 m a.s.l.), Rio Grande do Sul state, hopping and jumping along branches to catch insects on or near flowers with s hort We wish to express our gratitude to Yoshika Oniki-Willis for her generous assistance and to two anonymous referees sallies, flutter-chases and one reach-out; the bird often for valuable comments on the manuscript. We appreciate watched closely the movements of flying insects around the logistic support and permission provided by the flowers before attempting to capture its prey (G.A.B.). managers of the various protected areas we visited. G.A.B. benefited from scholarship support b y the Coordenação DISCUSSION de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Publication number 79 of the Institute for Studies of Nature. The temporary association of insect-eating birds with flowering trees or shru bs is scarcely documented in the literature. We expect this opportunistic behavior to be REFERENCES more common among small-bodied, edge or canopy- dwelling birds that sally or hover-glean to catch small Baker H.G., Bawa K.S., Frankie G.W. & Opler P.A. 1983. insects on or near foliage, because i) insects attracted to Reproductive biology of plants in tropical forests, p. 183–215. flowers are usually small (mostly hymenopterans, flies and In: Golley F.B. (ed.). Tropical rainforest ecosystems: ecosystems of the beetles, but also butterflies and moths; Willmer 2011), world. New York: Elsevier. making them non-rewarding prey for larger birds; ii) Beehler B. 1980. 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Lista comentada das espécies de aves registradas para o Morro do Espelho, São Leopoldo, Rio Grande do Sul, Associate Editor: Caio G. Machado. Revista Brasileira de Ornitologia 27(3): 2019

Journal

Ornithology ResearchSpringer Journals

Published: Sep 1, 2019

Keywords: foraging behavior; insects; Phyllomyias fasciatus; tanagers; Todirostrum poliocephalum; tyrant-flycatchers

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