FIRST REPORT OF NECTAR ROBBING BY SWORD-BILLED HUMMINGBIRDS ENSIFERA ENSIFERA

· A growing number of hummingbird species are known to prac@ce nectar robbing. Hummingbirds that rob nectar tend to have short bills and to rob ﬂowers with tubular corollas that are so long they prevent the birds from accessing nectar through the ﬂoral openings. Here, we document that Sword-billed Hummingbirds Ensifera ensifera , which have the longest bills of any hummingbird species, are secondary nectar robbers on ﬂowers of the red angel’s trumpet Brugmansia sanguinea , which have long tubular corollas and are regularly pollinated by Sword-billed Hummingbirds. When obtaining nectar through the ﬂoral opening of B. sanguinea , Sword-billed Hummingbirds some@mes probe so far into the corolla that their heads are completely enveloped by the ﬂower, which would severely limit their vision. Sword-billed Hummingbirds that feed on B. sanguinea ﬂowers might be at a lower risk of preda@on when they rob nectar than when they insert their heads into the ﬂoral opening. Thus, nectar robbing in this species might func@on to reduce preda@on risk, although we have no data to support this specula@on.


INTRODUCTION
More than 30 species of hummingbirds have been reported to be secondary robbers that steal nectar through holes in flowers made by primary robbers such as flowerpiercers Diglossa spp. and bees (Marks et al. 2023). Hummingbirds that rob nectar tend to have short bills and to rob flowers with corollas that are too long for the birds to obtain nectar through the floral opening (Lara & Ornelas 2001, Igić et al. 2020, Marks 2021. Not surprisingly, nectar robbing has not been reported in hummingbird species with especially long bills (Irwin et al. 2010, Marks et al. 2023).
The Sword-billed Hummingbird Ensifera ensifera is a large trochilid (10-12 g; King 1991, Echeverry-Galvis et al. 2005 with an extraordinarily long bill (90-110 mm; Züchner & Kirwan 2020). It occurs in humid and semi-humid montane forest and edge habitats from 1,700-3,600 m a.s.l. in the Andes from western Venezuela south through Colombia, Ecuador, and Peru to north-central Bolivia (Schulenberg et al. 2010, Züchner & Kirwan 2020. With such a long bill, this species would not be expected to rob nectar, and several studies of its foraging behavior reported that it was a "legi@mate" visitor that fed solely through the floral openings of the flowers it frequented (e.g., Snow & Snow 1980, Lindberg & Olesen 2001, Pelayo et al. 2011, Soteras et al. 2018. Moreover, the Sword-billed Hummingbird has coevolved with a host of plants (e.g., Passiflora spp., Aetanthus spp., Tacsonia spp., and Brug-mansia spp.) whose flowers have tubular corollas that are so long, no other hummingbirds can feed through the floral openings and pollinate the flowers (Lindberg & Olesen 2001, Abrahamczyk et al. 2014, Soteras et al. 2018). The specialized coevolu@onary rela@onships between E. ensifera and the flowers it pollinates very likely would not be maintained if the hummingbirds robbed nectar from these flowers at a high rate. Here, we provide the first documenta@on of nectar robbing by Sword-billed Hummingbirds and suggest that the behavior func@ons, in part, to reduce preda@on risk during foraging bouts. Nectar robbing by Ensifera apparently is quite rare and almost surely does not weaken coevolu@onary rela-@onships with the plants it pollinates.

RESULTS AND DISCUSSION
JSM examined photographs in databases of the Macaulay Library (2023; N = 3,360) and iNaturalist (2023; N = 511) for evidence of nectar robbing by Sword-billed Hummingbirds. He found three instances of nectar robbing (see Figures 1A, 1B) and contacted each of the photographers. Two of them, MR and RV, confirmed that the hummingbirds were robbing nectar through holes made by a Black Flowerpiercer Diglossa humeralis; the third, Mélianie Raymond, did not see any primary nectar robbers in the area. Each event occurred in Napo Province, Ecuador, at eleva@ons that ranged from 3,200-3,350 m a.s.l. (Table 1). Also in each case, the plant species whose flowers were robbed was red angel's trumpet Brugmansia sanguinea, which has long red-and-yellow flowers (mean corolla length = 172.6 mm) and is pollinated exclusively by Sword-billed Hummingbirds (Soteras et al. 2018). When not robbing nectar, Sword-billed Hummingbirds some@mes feed so far into the opening of a B. sanguinea flower that their heads are completely enveloped by the corolla (Figures 2A,  2B). In these cases, the birds' vision is completely obstructed while they feed.
Ours is the first report of nectar robbing by Sword-billed Hummingbirds and brings the number of hummingbird species known to be secondary nectar robbers to 35 (Marks et al. 2023). Nectar robbing by Sword-billed Hummingbirds appears to be rare and thus far is known only when birds feed on B. sanguinea, whose tubular flowers are among the longest of any plant on which Sword-billed Hummingbirds feed (Soteras et al. 2018: Figure 1).
In nearly all reports of nectar robbing by hummingbirds,  robbing is restricted to flowers whose corollas are too long for the birds to access nectar through the floral opening. Occasionally, hummingbirds have been reported to rob nectar from the same species of flower on which they also feed through the floral opening (McDade & Kinsman 1980, Lara & Ornelas 2001, but in all such reports, the hummingbirds appeared to be primary versus secondary nectar robbers. Why would Sword-billed Hummingbirds feed legi@mately and rob nectar from the same species of flower? One possibility is that the birds are at a lower risk of preda@on when they rob nectar than when they feed so far into the floral opening that their vision is obstructed by the corolla. Another possibility is that Sword-billed Hummingbirds extract nectar more efficiently when robbing B. sanguinea flowers than when feeding through the floral opening. Our results call into ques@on the conven@onal wisdom that nectar robbing by hummingbirds is restricted to shortbilled species, and we suspect that the number of hummingbird species that rob nectar is much larger than that reported by Marks et al. (2023). We found no informa@on about preda-@on on Sword-billed Hummingbirds or on how their maneuverability-and thus vulnerability to predators-might be compromised by their long bill. We also found no data on the efficiency of nectar extrac@on when hummingbirds feed legi@mately through the floral opening versus when they rob nectar. Some bees have been reported to obtain nectar more efficiently when robbing than when feeding through the floral opening (Free 1968, Dedej & Delaplane 2005), but we are not aware of similar reports for avian nectar robbers. In the absence of data on preda@on of foraging Sword-billed Hummingbirds, our sugges@on that nectar robbing func@ons to reduce their risk of preda@on is specula@ve but worthy of a)en@on. Addi@onal observa@ons of foraging Sword-billed Hummingbirds may reveal that they rob plant species other than B. sanguinea, which could shed light on addi@onal reasons for nectar robbing.