Cotinga 43 Short Communications

Juan C. Ocaña-Canales Facultad de Ciencias Forestales de la Universidad Nacional Agraria La Molina, Lima, Peru. E-mail: [email protected].

Carlos Garnica-Philipps Consultores Asociados en Naturaleza y Desarrollo (CANDES), Calle Rodín 129 Int. 101, Surquillo, Lima, Peru. E-mail: [email protected].

Received 20 November 2020; final revision accepted 23 March 2021; published online 5 July 2021

Secondary nectar robbing by a Purple-collared Woodstar Myrtis fanny Nectar robbing, in which an animal obtains nectar from a flower without providing pollination services, has been observed in many taxa, including bees, wasps, ants, beetles, moths, butterflies, birds, and mammals6. Among Neotropical birds, flowerpiercers of the genus Diglossa are well-known primary nectar robbers5 that have specialised bills and tongues for piercing the base of a flower’s corolla and extracting nectar15. Primary nectar robbers also include several species of hummingbirds, which pierce the Figure 2. Current distribution of Royal Cinclodes Cinclodes aricomae, with the base of a flower with their bill new record indicated by a star; circles = previous published records, based on tip1,8, or perhaps use serrations Aucca et al.1, Ávalos & Gómez2, eBird4 and Witt & Lane9. (‘tomial teeth’) near the bill tip to cut into the base of a flower9,12. Other hummingbirds http://www.ebird.org matrix habitats: implications are secondary nectar robbers that (accessed 6 March 2021). for biodiversity conservation access nectar via holes made by 5. Engblom, G., Aucca, C., within a high Andean other species, especially bees and Ferro-Meza, G., Palomino, landscape. Biodiver. Conserv. flowerpiercers6,7,14. Secondary W. & Samochuallpa, E. 17: 2645–2660. nectar robbing is confined to (2002) The conservation of 8. Schulenberg, T. S., Stotz, D. flowers whose corollas are longer Polylepis-adapted birds at F., Lane, D. F., O’Neill, J. than the bills of the robbing birds. Abra Málaga, Cuzco, Peru. P. & Parker, T. A. (2007) All species of hummingbirds Cotinga 17: 56–59. Birds of Peru. Princeton, NJ: known to practice nectar robbing 6. Fjeldså, J. (1993) The avifauna Princeton University Press. are believed to do so facultatively, of the Polylepis woodlands 9. Witt, C. C. & Lane, D. F. because they typically forage on of the Andean highlands: (2009) Range extensions for flowers whose corollas match their the efficiency of basing two rare high-Andean birds bill morphology, and access nectar conservation priorities on in central Peru. Cotinga 31: via the floral entrance6. patterns of endemism. Bird 90–94. Distinguishing primary from Conserv. Intern. 3: 37–55. secondary nectar robbing in 7. Lloyd, H. & Marsden, S. J. Nicolás W. Mamani-Cabana hummingbirds can be difficult, (2008) Bird community Universidad Nacional de San and information as to which variation across Polylepis Agustín de Arequipa (UNSA), species rob nectar is incomplete3. woodland fragments and Arequipa, Peru. E-mail: Nevertheless, nectar robbing has [email protected].

104 Cotinga 43 Short Communications been documented in >20 species of I see them forage in the Cantua 3. Igic´, B., Nguyen, I. & Fenberg, hummingbirds; 17 of these were simultaneously. P. B. (2020) Nectar robbing reported to be secondary nectar With its relatively short bill in the trainbearers (Lesbia, robbers3,6,19. Here, I provide the (16–18 mm20), a Purple-collared Trochilidae). PeerJ 8: e9561. first report of nectar robbing by a Woodstar would be unable to 4. iNaturalist (2020) http://www. Purple-collared Woodstar Myrtis obtain nectar through the floral inaturalist.org/ (accessed 1 fanny. opening of a C. buxifolia flower, September 2020). Purple-collared Woodstar is even if we take into account 5. Inouye, D. W. (1980) The a small hummingbird (c.2.4 g16) that hummingbirds can extend terminology of floral larceny. found in northern Ecuador to their tongues from one-third to Ecology 61: 1251–1253. southern Peru. It occurs in coastal nearly twice the length of their 6. Irwin, R. E., Bronstein, J. L., and montane scrub, arid valleys, bills to obtain nectar2,11,18. Thus, Manson, J. S. & Richardson, and urban gardens from sea the only way the woodstar can L. (2010) Nectar robbing: level to 3,200 m13,17. Although feed on Cantua flowers is to rob ecological and evolutionary publications on its foraging nectar, either by piercing the perspectives. Ann. Rev. behaviour are scarce16, the species base of the corolla, or by probing Ecol., Evol., Syst. 41: is known to feed on a variety of a hole in the corolla made by a 271–292. flowers with corollas shorter than primary nectar robber. Because 7. Kjonaas, C. & Rengifo, C. its bill4, in addition to arthropods10. each of the hummingbird’s visits (2006) Differential effects I have found no reports of nectar occurred so soon after the Rusty of avian nectar-robbing on robbing by this species. Flowerpiercer had foraged in the fruit set of two Venezuelan I observed nectar robbing on same flowers, I am convinced that Andean cloud forest plants. the grounds of Hotel El Abuelo the hummingbird was engaged Biotropica 38: 276–279. in Carhauz, dpto. Ancash, in secondary nectar robbing. 8. Lara, C. & Ornelas, J. F. west-central Peru (09°16’46”S My observations represent the (2001) Preferential nectar 77°38’47”W; 2,660 m), between first report of nectar robbing by robbing of flowers with 16h30 and 18h00 on 23 July 2019. Purple-collared Woodstar. Left long corollas: experimental I was not present for the entire unanswered is the extent to studies of two hummingbird observation period and thus was which this species obtains nectar species visiting three plant unable to record all events that by opportunistic robbing vs. the species. Oecologia 128: might have occurred. I took brief ‘legitimate’ technique of inserting 263–273. notes on each nectar-robbing its bill into the floral opening, 9. Ornelas, J. F. (1994) Serrate event by the hummingbird that I which is the normal manner in tomia: an adaptation witnessed and also noted details of which hummingbirds pollinate for nectar robbing in visits by a primary nectar robber flowers. hummingbirds? Auk 111: to the same shrub in which the 703–710. hummingbird foraged. Acknowledgements 10. Remsen, J. V., Stiles, F. G. & I observed a male Rusty I thank Ramiro Yábar for Scott, P. E. (1986) Frequency Flowerpiercer Diglossa sittoides identifying the Cantua buxifolia of arthropods in stomachs of foraging on flowers of a Cantua and for cheerfully accompanying tropical hummingbirds. Auk buxifolia (Polemoniaceae), c.2.5 m me on several birding expeditions 103: 436–441. tall, with tubular corollas, c.8 cm in Peru. I also thank two 11. Rico-Guevara, A. (2017) long, and bright reddish pink in anonymous reviewers for their Relating form to function in colour. I saw the flowerpiercer valuable comments on the the hummingbird feeding visit the plant six times. On each manuscript. apparatus. PeerJ 8: e3449. visit, it pierced the base of several 12. Rico-Guevara, A., Rubega, M. corollas in the usual manner in References A., Hurme, K. J. & Dudley, which flowerpiercers forage. On 1. Boehm, M. M. A. (2018) Biting R. (2019) Shifting paradigms three occasions, a female-type (i.e. the hand that feeds you: in the mechanics of nectar female or juvenile male) Purple- Wedge-billed Hummingbird extraction and hummingbird collared Woodstar visited the is a nectar robber of a bill morphology. Integrat. Cantua and probed at the base of sicklebill-adapted Andean Organ. Biol. 1: oby006. 3–5 corollas as if feeding. In each bellflower. Acta Amazonica 13. Ridgely, R. S. & Greenfield, case, the trochilid began foraging 48: 146–150. P. J. (2001) The birds of <5 minutes after the flowerpiercer 2. González, O. & Loiselle, B. A. Ecuador, 2. Ithaca, NY: had visited the same patch of (2016) Species interactions Cornell University Press. flowers, although I did not record in an Andean bird-flowering 14. Roubik, D. W., Holbrook, N. whether it probed the same flowers plant network: phenology M. & Parra, G. V. (1985) as the flowerpiercer. I never is more important than Roles of nectar robbers in observed the hummingbird and abundance or morphology. reproduction of the tropical the flowerpiercer interact, nor did PeerJ 4: e2789. treelet Quassia amara

105 Cotinga 43 Short Communications

(Simaroubaceae). Oecologia Nest, nest site and early study period (1 July–5 December 66: 161–167. growth of Crestless 2004). Despite this, no other nest 15. Schondube, J. E. & Martínez Curassow Mitu tomentosum was found. The specific forest type del Río, C. (2002) The in northern Amazonia where the nests were found forms flowerpiercers’ hook: an Cracids are among the most a small part of the whole mosaic of 1 experimental test of an conspicuous forest-dwelling white-sand forests in the region , evolutionary trade-off. Proc. birds in the Neotropics. Due being <10% of the entire area Roy. Soc. Lond. Ser. B 270: to their relatively large body surveyed by us, perhaps indicating 195–198. sizes, members of the Cracidae a preference for this habitat to nest. 16. Schuchmann, K. L. & are vulnerable to anthropogenic Additional studies are necessary to Boesman, P. F. D. (2020) disturbance, being heavily confirm this. Purple-collared Woodstar affected across their ranges by Both nests were sited c.4 m (Myrtis fanny), version 1.0. deforestation and subsistence above ground (Fig. 1A) and were In: del Hoyo, J., Elliott, A., hunting11,13. At present, 22 of 56 constructed of small sticks, thin Sargatal, J., Christie, D. A. species of cracids are listed as roots, lianas, and fully covered & de Juana, E. (eds.) Birds Vulnerable or in higher IUCN by dry and green leaves, many of the world. Ithaca, NY: threat categories6, making them from the trees where they were Cornell Lab of Ornithology. priority taxa for conservation7. built (Fig. 1A, C). The nests were https://doi.org/10.2173/bow. Curassows, in particular, are of bowl-shaped, supported by several pucwoo1.01 (accessed 1 special interest as 13 species are small thin branches, and both September 2020). globally threatened. were c.40 cm in diameter. Two 17. Schulenberg, T. S., Stotz, D. Despite their relevance white eggs were present in one F., Lane, D. F., O’Neill, J. to subsistence rural human of the nests, the same clutch size P. & Parker, T. A. (2010) populations and for the integrity of previously reported for the species 9 Birds of Peru. Revised edn. natural ecosystems12, many cracids in Venezuela , whilst the other was Princeton, NJ: Princeton are poorly studied9, and Crestless empty. Identification of the species University Press. Curassow Mitu tomentosum to which both nests belonged was 18. Vizentin-Bugoni, J., is no exception as evidenced confirmed by local hunters. Maruyama, P. K. & Sazima, by the lack of estimates of its Although neither egg was M. (2014) Processes current population6. Although examined closely, they were both entangling interactions in the species occurs in Brazil, collected by local Baniwa with the communities: forbidden Colombia, Venezuela and Guyana, purpose of hatching them. One was links are more important information on its natural history accidentally broken en route to the than abundance in a is scarce, especially its breeding village, but the other successfully hummingbird-plant network. ecology10. Here, we describe the hatched, possibly being incubated Proc. Roy. Soc. Lond. Ser. B species’ nest, nest site and early by a hen, a practice already 281: 20132397. nestling development. reported among other indigenous 3,4 19. Vogt, C. A. (2006) Secondary On 30 August 2004 we found groups in Amazonia . The egg nectar robbing, a previously two nests of Crestless Curassows hatched on 4 September 2004. unsubstantiated foraging in the upper Rio Negro region, The villagers kept the hatchling behavior of the Cinereous along the Içana River, near the alive and it was examined by the Conebill (Conirostrum Brazil / Colombia border (01º29’N authors twice subsequently, firstly cinereum). Orn. Neotrop. 17: 68º16’W; 125 m). The area is one of on 5 September 2004, one day 613–617. the few large patches of Amazonian after hatching, when it had light 20. Zimmer, J. T. (1930) Birds of white-sand forest known in Brazil brown down feathers with black the Marshall Field Peruvian as campinarana2,14. The nests stripes on its head and body, red Expedition, 1922–1923. Field were found near a recently opened legs, and measured c.15 cm (Fig. Mus. Nat. Hist. Zool. Ser. 17: trail used by us to conduct wildlife 2A–B). Eighty-seven days later, on 233–480. surveys, in a type of white-sand 1 December 2004, the young was forest known locally by the Baniwa larger and mainly covered by black Jeffrey S. Marks indigenous group as Ttiñalima, feathers, the head had a small crest Montana Bird Advocacy, 909 or caraná palm Mauritia carana with feathers still missing around Locust Street, Missoula, Montana, forest. It is a relatively low, open the eyes, the belly was fully covered USA. E-mail: [email protected]. white-sand forest with a dense by chestnut feathers, and the bill 1 was still dark with a reddish base Received 30 September 2020; final shrub and herbaceous layer . Nest (Fig. 2C). No other visits were revision accepted 17 November sites were c.3–4 km from the edges made to this village to further 2020; published online 5 July 2021 of the Içana River and relatively close to each other, c.480 m apart. investigate the bird’s development. A total of 37 km of trails was Our observations suggest a

opened in the region across distinct potential preference by Crestless

white-sand forest types, and were Curassow for relatively open visited several times during the forests as nest sites and that

106