Southeastern Brazilian tyrannulets as flower watchers

Several species of insect-eating birds occasionally visit flowering trees or shrubs 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 TodyFlycatcher 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 also report observations on several other species, mostly tyrant-flycatchers 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-flycatchers.


MetHODS
Most observations were at the Santa Lúcia Biological Station (19 o 58'S; 40 o 32'W, 650 m a.s.l.) in the Santa Teresa mountain range of central Espírito Santo state, Brazil. Flowering trees were mainly cultivated avocados Persea americana (Lauraceae) and Japanese Plums Eriobotrya japonica (Rosaceae) by the laboratory and several native yellow-flowered Senna multijuga var. lindleyana (Fabaceae) along the entry road, 500 m upriver. Observations were made with 8 × 30 and 10 × 42 binoculars from an appropriate distance so as not to disturb the birds. G.A.B. studied insectivorous and omnivorous birds foraging at flowers of three neighboring avocados on 04, 05 and 09 September 1994, for a total of 1405 min. For each bird visitation, data recorded included species, number of individuals, arrival and departure time, foraging maneuvers and substrate of captures. Whenever it was not possible to record an individual's arrival or departure time, we used the average visit length calculated for the species. Foraging maneuvers were classified according to Remsen & Robinson (1990) into eight categories. These categories were then combined with substrates of capture to generate composite codes representing foraging tactics (e.g., SH/F indicates a sally-hover to capture an insect on a flower). E.O.W. studied P. fasciatus, M. fasciatus and other species at flowers mainly April-May 1996. We also report observations on tyrant-flycatchers and other passerines made elsewhere in southeastern Brazil. Scientific names of birds follow Piacentini et al. (2015). Bird body masses are from Wilman et al. (2014).

reSUltS
In September 1994, twelve species foraged on insects attracted to avocado flowers at Santa Lúcia (Table  1). Ten others visited flowers exclusively for nectar (Thalurania glaucopis, Coereba flaveola and Dacnis cayana) or perched/foraged away from flowers (Cranioleuca pallida, Xenops rutilans, Piprites chloris, Camptostoma obsoletum, Lathrotriccus euleri, Euphonia violacea and Tangara cayana). Todirostrum poliocephalum, P. fasciatus and three tanagers visited the trees in more than one day and made considerably more visits or spent considerably more time foraging at flowers than other species (Table  1). Todirostrum poliocephalum spent the largest amount of time on trees and made long visits concentrated in the second half of the morning, when it was a regular and constant visitor. Typically, one bird of a pair that held a territory in the area would forage for long periods in the avocados, sometimes accompanied by its mate. Aerial maneuvers (short sally-strikes and, to a lesser extent, sallypounces and leaps) were used to capture prey mainly on substrates other than air, and about 65% of captures were on or very close to flowers (Table 2).
Phyllomyias fasciatus was the most frequent species in the avocados. It made medium-length regular visits throughout the morning and early afternoon (Table  1). Usually only one or two birds foraged in the trees at the same time, but up to four were present on some occasions. Prey were mostly captured in the air or at flowers with sally-strikes and, less frequently, sally-hover and sally-pounce maneuvers. Nearly 62% of insectcatching attempts were at or near flowers (Table 2). This species showed the greatest range of foraging maneuvers among all visitors.
The avocado flowers were visited earlier by a T. poliocephalum on 03 September 1994, with short strikes under leaves near the flowers. We have often seen it sallying under leaves away from flowers, at dense vine tangles in woods or at edges. E.O.W. also noted visits by two P. fasciatus, which sallied to the air or leaves near flowers at 10-12 h. Later, two birds were sallying in a small flowering tree (not identified) in the woods downriver. We have seen it sallying away from flowers, or getting Myrsine fruit or Alchornea arils, on other occasions.
On 24 April 1996, 16:22-16:28 h, one P. fasciatus sallied for insects in the Senna. On the 25 April, between 9-10 h, two were now and then near Japanese Plum flowers by the lab, between visits by tanagers and relatives that poked their bills deep into the flowers (D. cayana, Tangara seledon and Schistochlamys ruficapillus). A T. poliocephalum worked briefly near one of the P. fasciatus, but soon left. On 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 two P. fasciatus worked 16:00 h in the crowns, sallying to catch insects on flowers several times.
flowers, after which birds wandered off for the night. On most days, the M. fasciatus worked low bushes under or near the Senna. On 26 April, however, one sallied in the midlevels of the Senna at 15:46 h, returning 15:52 h after some long calls and sallying to near flowers. It fled if people or bicycles passed, but returned to catch insects with sallies to flowers, the air, or foliage; at 16:23 h it dropped to bushes, sallied to the ground in the road a few times, and did not return to the flowers. The next morning, 08:05-08:15 h, the M. fasciatus was less timid and sallied to or near flowers up one tree several times.
Elsewhere, E.O.W. noted P. fasciatus, M. fasciatus and six other small flycatchers sallying or hovering for insects near flowers of trees or bushes in southeastern Brazil (Table 3) In southern Brazil, G.A.B. noticed two other tyrant-flycatchers watching flowers of bushes to catch insects (Table 3). In addition, in the Pampas grasslands around Lavras do Sul (30 o 48'S; 53 o 54'W, 315 m a.s.l.), 05-08 January 2018, at least three species of tyrantflycatchers were plucking soldier beetles Chauliognathus flavipes (Cantharidae) from the umbellate flower stalks of Eryngium chamissonis (Urb., 1879) (Apiaceae) in densely vegetated upland swales dominated by this spiny sedge. These polymorphic, soft-elytra beetles are distinctly colored with yellow and black and gather by the thousands on the upright inflorescences of E. chamissonis, which rise up to 1.5 m above the vegetative stratum in midsummer to form a temporary emergent layer of flowering shoots. Birds seen capturing the beetles in a more or less systematic way included a family group of Yellow-browed Tyrants Satrapa icterophrys on the 04 January, plus a solitary individual on the 06 January, and two M. fasciatus on the 05 and 08 January, at four different locations. One Highland Elaenia Elaenia obscura also briefly fed on the insects on the first day. Beetles were picked or snapped off flower heads and outermost peduncles mostly with glean, reach and leap maneuvers, and the birds seemed to make little effort to catch them, since prey was everywhere and almost stationary.

Other species
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DiScUSSiON
The temporary association of insect-eating birds with flowering trees or shrubs is scarcely documented in the literature. We expect this opportunistic behavior to be more common among small-bodied, edge or canopydwelling birds that sally or hover-glean to catch small insects on or near foliage, because i) insects attracted to flowers are usually small (mostly hymenopterans, flies and beetles, but also butterflies and moths; Willmer 2011), making them non-rewarding prey for larger birds; ii) plant species showing massive flowering (i.e., producing large numbers of exposed flowers to attract relatively nonspecialized pollinators) predominate in the upper strata of tropical forests and along borders (Janzen 1975, Baker et al. 1983; and iii) flowers are rarely accessible directly to perching birds in the New World (Cronk & Ojeda 2008). In southeastern Brazil, P. fasciatus (10.3 g) often watches flowers and sallies for or pecks insects, T. poliocephalum (7 g) and M. fasciatus (9.9 g) less. As illustrated here, many other birds (mass range 6.3-102 g) visit flowering trees to get insects, but they move through the trees and do not obviously watch flowers as do the tyrannulets above, or perhaps do it for shorter periods (e.g., Piranga flava). Wholly insectivorous birds such as T. poliocephalum may forage in flowering trees for longer periods as compared to similarly sized species that also feed on fruits, presumably because they are able to find most of their food items in the flowers and/or foliage, and also because arthropods at flowers are a rapidly renewing resource (Beehler 1980). In contrast, P. fasciatus and several tanagers make more frequent but shorter visits to flowering trees, possibly because insects are only part of their diet. Individuals of P. fasciatus observed at Santa Lúcia often regurgitated mistletoe seeds upon arriving at the flowering trees, indicating they had been feeding on fruit shortly before.
Several other Tyrannoidea visit eucalyptus or other flowers, but more study is needed to establish whether arthropods, nectar, or pollen are used. We did not confirm any activity that could have pollinated flowers, except when one bird put its head in a flower. Flight near flowers could have picked up some pollen, but tanagers and others that visit flowers directly are more likely to pollinate.

acKNOWleDGeMeNtS
We wish to express our gratitude to Yoshika Oniki-Willis for her generous assistance and to two anonymous referees for valuable comments on the manuscript. We appreciate the logistic support and permission provided by the managers of the various protected areas we visited. G.A.B. benefited from scholarship support by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Publication number 79 of the Institute for Studies of Nature.