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Bee in the nose: raptors let or let not stingless bees enter their nostrils

Bee in the nose: raptors let or let not stingless bees enter their nostrils Revista Brasileira de Ornitologia, 23(3), 323-326 ARTICLE September 2015 Bee in the nose: raptors let or let not stingless bees enter their nostrils 1,2 Ivan Sazima Museu de Zoologia, C.P. 6109, Universidade Estadual de Campinas, CEP 13083-970, Campinas, SP, Brazil. Corresponding author: isazima@gmail.com Received on 9 March 2015. Accepted on 2 June 2015. ABSTRACT T T: Relationships between birds and social insects include birds following ants, birds nesting close to active colonies of wasps or bees, and nesting inside termitaria. A little known relationship between birds and colonial insects is that of stingless bees (Meliponina) entering the nostrils of hawks and owls. Herein I report on a stingless bee entering the nostrils of the Roadside Hawk (Rupornis magnirostris s), and on avoiding behaviours displayed by the same hawk species and a Burrowing Owl ( ( (Athene cunicularia) in presence of stingless bees hovering in front of their faces. Th e bees probably were seeking mucus inside the raptors’ nostrils, as already reported for a few birds of prey. Avoiding behaviour seems a novelty in this relationship between raptors and bees. Th e role stingless bees play in the lives of some bird species remains little known, and merits closer attention by field ornitholo gists and apidolologist. KE E EY Y Y-WORDS: Rupornis magnirostris, Athene cunicularia, Meliponina bees, mucus foraging, avoiding behaviour. INTRODUCTION 19 November 2007 and 22 February 2015 at midmorning (8:59 and 9:35 h respectively). Additionally, I recorded an Th e relationships between birds and social insects include encounter of a stingless bee with an owl at the campus of birds that follow ants, birds that nest on branches close a local university (22°49'23"S, 47°04'01"W, 620 m a.s.l) in Campinas, on 3 January 2010 at late morning (10:32 to active colonies of wasps or bees, and birds that nest inside active or vacant termitaria (Myers 1935, Willis & h). I observed the birds through a 70-300 mm telephoto Oniki 1978, Brightsmith 2000, Quinn & Ueta 2008, lens mounted on a camera from a distance of 2-5 m. I Sazima & D’Angelo 2015. A little known relationship used the “ad libitum” and “sequence” observational between birds and colonial insects is that of stingless samplings (Altmann 1974), which are adequate to record rare or fortuitous events. Bee’s sizes were estimated by bees (Meliponina) entering the nostrils of hawks and owls to take mucus (Lobato et alll. 2007). However, this enlarging the digital photos to actual measurements of relationship remains little known and I am unaware of the raptors’ bill length taken from museum specimens (3 any reference on the subject other than the short report adult hawks, 1 young owl) and measuring the total length by Lobato et alll. (2007) and a brief mention of this raptor- of the insects with a fl exible scale directly on the screen. Digital photos of the hawks and the owl interacting bee relationship based on claims by indigenous people in Northern Brazil (Santos & Antonini 2008). Th erefore, with stingless bees are on fil e in the Museu de Zoologia, I report herein on a stingless bee entering the nostrils Universidade Estadual de Campinas (ZUEC). of the Roadside Hawk (Rupornis magnirostris s), and on avoiding behaviours displayed by the same hawk species RESULTS and a Burrowing Owl ( ( (Athene cunicularia) in presence of stingless bees hovering in front of their faces. One encounter between an unidentified, small ( ca. 4 mm) Meliponina bee and an adult Roadside Hawk began METHODS with the bee hovering in front and above the cere of the bird (Figure 1a), then landing on the left nostril (Figure 1b) and performing brushing movements with its forelegs I recorded two encounters of stingless bees with hawks at an urban recreational park (22°48'42"S, 47°04'26"W, 587 to scrape what seemed dry mucus. Afterwards, the bee m a.s.l) in Campinas, São Paulo, Southeastern Brazil, on moved to the right nostril (Figure 1c), where it performed Bee in the nose: raptors let or let not stingless bees enter their nostrils Ivan Sazima FIGURE 1. A stingless bee (Meliponina) visits the nostrils of an adult Roadside Hawk (Rupornis magnirostris s). The bee hovers close to the cere (a) and then alights in the left nostril (b); the bee is now in the right nostril (c), and hovers again near the hawk’s head (d). FIGURE 2. Stingless bees (Meliponina) approaching an adult Roadside Hawk (Rupornis magnisrostris s) and a young Burrowing Owl ( ( (Athene cunicularia), and the birds’ response. Upon noticing the hovering bee (a), the hawk hides most of its bill among the wing coverts (b). The owl watches the bee closely (c), and bill-snaps at the bee, which retreats (d). Revista Brasileira de Ornitologia, 23(3), 2015 Bee in the nose: raptors let or let not stingless bees enter their nostrils Ivan Sazima similar leg movements. The bee left the nostril and be gan Th e apparent avoidance behaviour displayed by to hover again near the hawk’s head (Figure 1d), but had one adult Roadside Hawk (lowering the head and hiding no opportunity to land because the bird took wing. Th e most of the bill) might be related to the larger size of interaction lasted ca. 1 min. the bee. Although the bee’s size would allow it to enter Another encounter between a larger (ca. 10 mm) the bird’s nostrils, even if partially, its presence there may stingless bee, apparently Trigona a sp., and an adult well be a nuisance to the hawk. Since the hawk was not Roadside Hawk also began with the bee hovering in front preening its plumage before or after the bee arrival, its of the bird’s head (Figure 2a). Upon noticing the bee, head lowering and hiding the bill was unrelated to this the hawk fi rst lowered its head and then hid most of its comfort behaviour (Marks et alll. 1999). The response of bill between the wing coverts (Figure 2b). This behaviour the juvenile Burrowing Owl differs from that of the haw k apparently discouraged the bee, which retreated from the basically by the bird’s bill-snapping towards the hovering proximity of the bird. The interaction lasted ca. 1 min. bee. Similarly, the young owl was not preening its One encounter between an unidentified, small (ca. plumage before or after the bee arrival. Bill-snapping (or 5 mm) Meliponina bee and a juvenile Burrowing Owl bill-clapping) is a common response of owls to individual began with the bee approaching the bird and hovering disturbance (Gehlbach 2009), and may partly explain in front of its head. The bird noticed the bee at once , the young bird’s reaction towards the bee. Avoidance lowered its head and watched the insect closely (Figure behaviour seems a novelty in the relationship between 2c). Th en the apparently disturbed owl bill-snapped 2-3 raptors and stingless bees (Lobato et alll. 2007). times towards the bee, which retreated (Figure 2d). The In conclusion, it seems that raptors let or let not interaction lasted ca. 30-40 sec. stingless bees in. Th e outcome may depend on various circumstances, including the predisposition (or tolerance) of the bird, the bee size relative to the bird, and the DISCUSSION apparent disturbance caused by the bee to the bird. Th e role stingless bees play in the lives of some bird species From the three encounters of raptors with stingless bees remains little known, and this relationship ought to be recorded here, only one adult Roadside Hawk appeared studied both in the fi eld and in captivity (Lobato et al. to tolerate, or perhaps even allow, the bee to enter its 2007). I suspect that the association of birds and stingless nostrils and scrap mucus there. Alternatively, instead bees is not restricted to raptors, and other bird groups of letting the bee to enter its nostrils, the hawk could may be involved. Natural history-oriented studies may simply be undisturbed with the bee’s presence. Since the disclose additional bird species whose nostrils are visited bird remained in plain view and did not show signs of by stingless bees. To detect a tiny bee entering the nostrils disturbance due to the observer and two other people of a bird in the fi eld is admittedly a diffi cult task, but standing by, distraction seems an unlikely cause for the ornithologists and apidologists alike may help to unravel hawk’s absence of aversive behaviour towards the bee. this captivating relationship between birds and bees. Whatever the cause, the bee successfully obtained the resource it was seeking and reduced the mucus in the A A ACKNOWLEDGEMENTS hawk’s nostrils. Reduction of secretion in nostrils improve breathing in captive raptors and is viewed as an instance I thank the staff of the Parque Ecológico Prof. Hermógenes of facultative mutualism between birds of prey and de Freitas Leitão Filho for allowing my field studies at stingless bees (Lobato et alll. 2007). These authors report the park; Marlies Sazima for her loving support in the on seven species of hawks, including R. magnirostris, and fi eld and at home; an anonymous referee for enriching two owl species whose nostrils are visited by Meliponina the manuscript with a thoughtful review; the CNPq for bees to collect mucus as a source of proteins and minerals earlier fi nancial support. (Lobato et alll. 2007). Based on claims of indigenous people in Northern Brazil, Santos & Antonini (2008) mention that a stingless bee species visits the beak and R R REFERENCES nostrils of captive Harpy Eagle (Harpia harpyja) to collect food there. To obtain nutrients or nest material, stingless Altmann, J. 1974. Observational study of behaviour: sampling bees collect the most unusual sources, including carrion, methods. Behaviour, 49(3): 227-267. faeces, urine, blood, human sweat, and ashes (Roubik Brightsmith, D. J. 2000. Use of arboreal termitaria by nesting birds 1982, 1992, Santos & Antonini 2008, IS pers. obs.). in the Peruvian Amazon. The Condo r, 102(3): 529-538. Gehlbach, F.R. 2009. Eastern Screech Owl: life history, ecology, and Th us, collecting mucus should not come as a surprise for behavior in the suburbs and countryside. The W. L. Mood y Jr. the versatile Meliponina, even if to obtain this material Natural History Series, no 16. College Station, Texas A & M the bees must enter the nostrils of raptors. University Press. Revista Brasileira de Ornitologia, 23(3), 2015 Bee in the nose: raptors let or let not stingless bees enter their nostrils Ivan Sazima Lobato, D. N. C.; Antonini, Y Y Y.; Martins, R. P. & Azeredo, R. Roubik, D. W. 1992. Ecology and natural history of tropical bees. 2007. Visita de abelhas a narinas de aves de rapina (Accipitridae Cambridge, Cambridge University Press. e Strigidae): mutualismo facultativo? Anais do VIII Congresso de Santos, G. M. & Antonini, Y Y Y. 2008. The traditional knowledge on Ecologia do Brasil, Caxambu – MG: 1-2. stingless bees (Apidae: Meliponina) used by the Enawene-Nawe Marks, J. S.; Cunnings, R. J. & Mikkola, H. 1999. Family Strigidae tribe in western Brazil. Journal of Ethnobiology and Ethnomedicine, (typical owls), p. 76-242. In: del Hoyo, J.; Elliot, A. & Sargatal, J. 4:19. doi:10.1186/1746-4269-4-19. (eds.). Handbook of the birds of the world. Vol. 5, Barn-owls to Sazima, I. & D’Angelo, G. 2015. Associações de aves com insetos hummingbirds. Barcelona, Lynx Edicions. sociais: um sumário no Sudeste do Brasil. Iheringia, Série Zoologia, Myers, J. G. 1935. Nesting associations of birds with social insects. 105: 333-338. Transactions of the Royal Entomological Society of London, Willis, E. O. & Oniki, Y Y Y. 1978. Birds and army ants. Annual Review 83(1): 11-23. of Ecology and Systematics, 9: 243-263. Quinn, J. L. & Ueta, M. 2008. Protective nesting associations in birds. Ibis, 150(Supplement 1): 146-167. Roubik, D. W. 1982. Obligate necrophagy in a social bee. Science, Associate Editor: Carlos A. Bianchi 217(4564): 1059-1060. Revista Brasileira de Ornitologia, 23(3), 2015 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Bee in the nose: raptors let or let not stingless bees enter their nostrils

Ornithology Research , Volume 23 (3) – Sep 1, 2015

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Abstract

Revista Brasileira de Ornitologia, 23(3), 323-326 ARTICLE September 2015 Bee in the nose: raptors let or let not stingless bees enter their nostrils 1,2 Ivan Sazima Museu de Zoologia, C.P. 6109, Universidade Estadual de Campinas, CEP 13083-970, Campinas, SP, Brazil. Corresponding author: isazima@gmail.com Received on 9 March 2015. Accepted on 2 June 2015. ABSTRACT T T: Relationships between birds and social insects include birds following ants, birds nesting close to active colonies of wasps or bees, and nesting inside termitaria. A little known relationship between birds and colonial insects is that of stingless bees (Meliponina) entering the nostrils of hawks and owls. Herein I report on a stingless bee entering the nostrils of the Roadside Hawk (Rupornis magnirostris s), and on avoiding behaviours displayed by the same hawk species and a Burrowing Owl ( ( (Athene cunicularia) in presence of stingless bees hovering in front of their faces. Th e bees probably were seeking mucus inside the raptors’ nostrils, as already reported for a few birds of prey. Avoiding behaviour seems a novelty in this relationship between raptors and bees. Th e role stingless bees play in the lives of some bird species remains little known, and merits closer attention by field ornitholo gists and apidolologist. KE E EY Y Y-WORDS: Rupornis magnirostris, Athene cunicularia, Meliponina bees, mucus foraging, avoiding behaviour. INTRODUCTION 19 November 2007 and 22 February 2015 at midmorning (8:59 and 9:35 h respectively). Additionally, I recorded an Th e relationships between birds and social insects include encounter of a stingless bee with an owl at the campus of birds that follow ants, birds that nest on branches close a local university (22°49'23"S, 47°04'01"W, 620 m a.s.l) in Campinas, on 3 January 2010 at late morning (10:32 to active colonies of wasps or bees, and birds that nest inside active or vacant termitaria (Myers 1935, Willis & h). I observed the birds through a 70-300 mm telephoto Oniki 1978, Brightsmith 2000, Quinn & Ueta 2008, lens mounted on a camera from a distance of 2-5 m. I Sazima & D’Angelo 2015. A little known relationship used the “ad libitum” and “sequence” observational between birds and colonial insects is that of stingless samplings (Altmann 1974), which are adequate to record rare or fortuitous events. Bee’s sizes were estimated by bees (Meliponina) entering the nostrils of hawks and owls to take mucus (Lobato et alll. 2007). However, this enlarging the digital photos to actual measurements of relationship remains little known and I am unaware of the raptors’ bill length taken from museum specimens (3 any reference on the subject other than the short report adult hawks, 1 young owl) and measuring the total length by Lobato et alll. (2007) and a brief mention of this raptor- of the insects with a fl exible scale directly on the screen. Digital photos of the hawks and the owl interacting bee relationship based on claims by indigenous people in Northern Brazil (Santos & Antonini 2008). Th erefore, with stingless bees are on fil e in the Museu de Zoologia, I report herein on a stingless bee entering the nostrils Universidade Estadual de Campinas (ZUEC). of the Roadside Hawk (Rupornis magnirostris s), and on avoiding behaviours displayed by the same hawk species RESULTS and a Burrowing Owl ( ( (Athene cunicularia) in presence of stingless bees hovering in front of their faces. One encounter between an unidentified, small ( ca. 4 mm) Meliponina bee and an adult Roadside Hawk began METHODS with the bee hovering in front and above the cere of the bird (Figure 1a), then landing on the left nostril (Figure 1b) and performing brushing movements with its forelegs I recorded two encounters of stingless bees with hawks at an urban recreational park (22°48'42"S, 47°04'26"W, 587 to scrape what seemed dry mucus. Afterwards, the bee m a.s.l) in Campinas, São Paulo, Southeastern Brazil, on moved to the right nostril (Figure 1c), where it performed Bee in the nose: raptors let or let not stingless bees enter their nostrils Ivan Sazima FIGURE 1. A stingless bee (Meliponina) visits the nostrils of an adult Roadside Hawk (Rupornis magnirostris s). The bee hovers close to the cere (a) and then alights in the left nostril (b); the bee is now in the right nostril (c), and hovers again near the hawk’s head (d). FIGURE 2. Stingless bees (Meliponina) approaching an adult Roadside Hawk (Rupornis magnisrostris s) and a young Burrowing Owl ( ( (Athene cunicularia), and the birds’ response. Upon noticing the hovering bee (a), the hawk hides most of its bill among the wing coverts (b). The owl watches the bee closely (c), and bill-snaps at the bee, which retreats (d). Revista Brasileira de Ornitologia, 23(3), 2015 Bee in the nose: raptors let or let not stingless bees enter their nostrils Ivan Sazima similar leg movements. The bee left the nostril and be gan Th e apparent avoidance behaviour displayed by to hover again near the hawk’s head (Figure 1d), but had one adult Roadside Hawk (lowering the head and hiding no opportunity to land because the bird took wing. Th e most of the bill) might be related to the larger size of interaction lasted ca. 1 min. the bee. Although the bee’s size would allow it to enter Another encounter between a larger (ca. 10 mm) the bird’s nostrils, even if partially, its presence there may stingless bee, apparently Trigona a sp., and an adult well be a nuisance to the hawk. Since the hawk was not Roadside Hawk also began with the bee hovering in front preening its plumage before or after the bee arrival, its of the bird’s head (Figure 2a). Upon noticing the bee, head lowering and hiding the bill was unrelated to this the hawk fi rst lowered its head and then hid most of its comfort behaviour (Marks et alll. 1999). The response of bill between the wing coverts (Figure 2b). This behaviour the juvenile Burrowing Owl differs from that of the haw k apparently discouraged the bee, which retreated from the basically by the bird’s bill-snapping towards the hovering proximity of the bird. The interaction lasted ca. 1 min. bee. Similarly, the young owl was not preening its One encounter between an unidentified, small (ca. plumage before or after the bee arrival. Bill-snapping (or 5 mm) Meliponina bee and a juvenile Burrowing Owl bill-clapping) is a common response of owls to individual began with the bee approaching the bird and hovering disturbance (Gehlbach 2009), and may partly explain in front of its head. The bird noticed the bee at once , the young bird’s reaction towards the bee. Avoidance lowered its head and watched the insect closely (Figure behaviour seems a novelty in the relationship between 2c). Th en the apparently disturbed owl bill-snapped 2-3 raptors and stingless bees (Lobato et alll. 2007). times towards the bee, which retreated (Figure 2d). The In conclusion, it seems that raptors let or let not interaction lasted ca. 30-40 sec. stingless bees in. Th e outcome may depend on various circumstances, including the predisposition (or tolerance) of the bird, the bee size relative to the bird, and the DISCUSSION apparent disturbance caused by the bee to the bird. Th e role stingless bees play in the lives of some bird species From the three encounters of raptors with stingless bees remains little known, and this relationship ought to be recorded here, only one adult Roadside Hawk appeared studied both in the fi eld and in captivity (Lobato et al. to tolerate, or perhaps even allow, the bee to enter its 2007). I suspect that the association of birds and stingless nostrils and scrap mucus there. Alternatively, instead bees is not restricted to raptors, and other bird groups of letting the bee to enter its nostrils, the hawk could may be involved. Natural history-oriented studies may simply be undisturbed with the bee’s presence. Since the disclose additional bird species whose nostrils are visited bird remained in plain view and did not show signs of by stingless bees. To detect a tiny bee entering the nostrils disturbance due to the observer and two other people of a bird in the fi eld is admittedly a diffi cult task, but standing by, distraction seems an unlikely cause for the ornithologists and apidologists alike may help to unravel hawk’s absence of aversive behaviour towards the bee. this captivating relationship between birds and bees. Whatever the cause, the bee successfully obtained the resource it was seeking and reduced the mucus in the A A ACKNOWLEDGEMENTS hawk’s nostrils. Reduction of secretion in nostrils improve breathing in captive raptors and is viewed as an instance I thank the staff of the Parque Ecológico Prof. Hermógenes of facultative mutualism between birds of prey and de Freitas Leitão Filho for allowing my field studies at stingless bees (Lobato et alll. 2007). These authors report the park; Marlies Sazima for her loving support in the on seven species of hawks, including R. magnirostris, and fi eld and at home; an anonymous referee for enriching two owl species whose nostrils are visited by Meliponina the manuscript with a thoughtful review; the CNPq for bees to collect mucus as a source of proteins and minerals earlier fi nancial support. (Lobato et alll. 2007). Based on claims of indigenous people in Northern Brazil, Santos & Antonini (2008) mention that a stingless bee species visits the beak and R R REFERENCES nostrils of captive Harpy Eagle (Harpia harpyja) to collect food there. To obtain nutrients or nest material, stingless Altmann, J. 1974. Observational study of behaviour: sampling bees collect the most unusual sources, including carrion, methods. Behaviour, 49(3): 227-267. faeces, urine, blood, human sweat, and ashes (Roubik Brightsmith, D. J. 2000. Use of arboreal termitaria by nesting birds 1982, 1992, Santos & Antonini 2008, IS pers. obs.). in the Peruvian Amazon. The Condo r, 102(3): 529-538. Gehlbach, F.R. 2009. Eastern Screech Owl: life history, ecology, and Th us, collecting mucus should not come as a surprise for behavior in the suburbs and countryside. The W. L. Mood y Jr. the versatile Meliponina, even if to obtain this material Natural History Series, no 16. College Station, Texas A & M the bees must enter the nostrils of raptors. University Press. Revista Brasileira de Ornitologia, 23(3), 2015 Bee in the nose: raptors let or let not stingless bees enter their nostrils Ivan Sazima Lobato, D. N. C.; Antonini, Y Y Y.; Martins, R. P. & Azeredo, R. Roubik, D. W. 1992. Ecology and natural history of tropical bees. 2007. Visita de abelhas a narinas de aves de rapina (Accipitridae Cambridge, Cambridge University Press. e Strigidae): mutualismo facultativo? Anais do VIII Congresso de Santos, G. M. & Antonini, Y Y Y. 2008. The traditional knowledge on Ecologia do Brasil, Caxambu – MG: 1-2. stingless bees (Apidae: Meliponina) used by the Enawene-Nawe Marks, J. S.; Cunnings, R. J. & Mikkola, H. 1999. Family Strigidae tribe in western Brazil. Journal of Ethnobiology and Ethnomedicine, (typical owls), p. 76-242. In: del Hoyo, J.; Elliot, A. & Sargatal, J. 4:19. doi:10.1186/1746-4269-4-19. (eds.). Handbook of the birds of the world. Vol. 5, Barn-owls to Sazima, I. & D’Angelo, G. 2015. Associações de aves com insetos hummingbirds. Barcelona, Lynx Edicions. sociais: um sumário no Sudeste do Brasil. Iheringia, Série Zoologia, Myers, J. G. 1935. Nesting associations of birds with social insects. 105: 333-338. Transactions of the Royal Entomological Society of London, Willis, E. O. & Oniki, Y Y Y. 1978. Birds and army ants. Annual Review 83(1): 11-23. of Ecology and Systematics, 9: 243-263. Quinn, J. L. & Ueta, M. 2008. Protective nesting associations in birds. Ibis, 150(Supplement 1): 146-167. Roubik, D. W. 1982. Obligate necrophagy in a social bee. Science, Associate Editor: Carlos A. Bianchi 217(4564): 1059-1060. Revista Brasileira de Ornitologia, 23(3), 2015

Journal

Ornithology ResearchSpringer Journals

Published: Sep 1, 2015

Keywords: Rupornis magnirostris; Athene cunicularia; Meliponina bees; mucus foraging; avoiding behaviour

References