Polarized short odor-trail recruitment communication by a stingless bee, Trigona spinipes

Behavioral Ecology and Sociobiology - Tập 56 - Trang 435-448 - 2004
James C. Nieh1, Felipe A. L. Contrera2, Ryan R. Yoon3, Lillian S. Barreto4, Vera L. Imperatriz-Fonseca2
1Division of Biological Sciences, Section of Ecology, Behavior, and Evolution, University of California San Diego, La Jolla, USA
2Instituto de Biociências, Laboratório de Abelhas, Universidade de São Paulo, São Paulo, Brazil
3University of California San Diego, La Jolla, USA
4Laboratório de Abelhas (LABE), Empresa Baiana de Desenvolvimento Agrícola, Salvador-Bahia, Brazil

Tóm tắt

Polarized odor-trail communication, in which a receiver can orient towards the correct endpoint from within the trail, is documented in relatively few animals and is poorly understood, although such directionality could significantly enhance resource localization. Among animals, stingless bees exhibit the unique behavior of depositing long substrate-borne odor trails that assist the orientation of flying nestmates to a specific three-dimensional food location. However, relatively little is known about the spatial structure of such odor trails, particularly vertical trails, and whether these trails are polarized to indicate the correct terminus. We show that a stingless bee, Trigona spinipes, can rapidly recruit nestmates in large bursts to a food source at a specific distance, direction, and height. In conjunction with a major recruitment burst, foragers deposited odor marks that attracted nestmates for up to 20 min. Surprisingly, these odor marks formed a short odor trail instead of a complete odor trail extending from the feeder to the nest (the classic description of a meliponine odor trail). The length of the odor trails varied between different feeder locations with different colonies, from a minimum of 3 m to a maximum of 29 m. The odor marks formed a polarized trail that newcomers followed to the end with the most concentrated odor marks (the feeder), even when the entire odor trail was rotated 180° and clean test feeders were set out at locations that foragers had never previously fed at. Thus locale odor or the potential communication of food location inside the nest do not account for the ability of newcomers to find the correct terminus. This result provides the first strong evidence for odor-trail polarization in social insects.

Tài liệu tham khảo

Almeida MC, Laroca S (1988) Trigona spinipes (Apidae, Meliponinae): taxonomy, bionomy, and trophic relationships in restricted areas. Acta Biol Paran 17:67–108 Barbosa AAA (1999) Hortia brasiliana Vand. (Rutaceae): pollination by Passeriformes in cerrado, Southeastern Brazil. Rev Bras Bot 22:99–105 Biesmeijer JC, Ermers MCW (1999) Social foraging in stingless bees: how colonies of Melipona fasciata choose among nectar sources. Behav Ecol Sociobiol 46:129–140 Biesmeijer JC, Richter JAP, Smeets MAJP, Sommeijer MJ (1999) Niche differentiation in nectar-collecting stingless bees: the influence of morphology, floral choice and interference competition. Ecol Entomol 24:380–388 Bradbury J, Vehrencamp SL (1988) Principles of animal communication. Sinauer, Sunderland, Mass Cameron SA, Whitfield JB (1996) Use of walking trails. Nature 379:125 Chittka L, Williams NM, Rasmussen H, Thomson JD (1999) Navigation without vision: bumblebee orientation in complete darkness. Proc R Soc Lond B Biol Sci:45–50 Cobert SA, Willmer PG (1980) Pollination of the yellow passion fruit: nectar, pollen and carpenter bees. J Agric Sci 95:655–666 Cooper WEJ, Vitt LJ (1987) Intraspecific and interspecific aggression in lizards of the scincid genus Eumeces: chemical detection of conspecific sexual competitors. Herpetologica 43:7–14 Cortopassi-Laurino M, Ramalho M (1988) Pollen harvest by Africanized Apis mellifera and Trigona spinipes in São Paulo: botanical and ecological views. Apidologie 19:1–24 Eltz T, Brühl CA, van der Kaars S, Chey VK, Linsenmair KE (2001) Pollen foraging and resource partitioning of stingless bees in relation to flowering dynamics in a Southeast Asian tropical rainforest. Insectes Soc 48:273–279 Eltz T, Brühl CA, van der Kaars S, Linsenmair KE (2002) Determinants of stingless bee nest density in lowland dipterocarp forests of Sabah, Malaysia. Oecologia 131:27–34 Ford NB, Low JR (1984) Sex pheromone source location by garter snakes: a mechanism of detection of direction in nonvolatile trails. J Chem Ecol 10:1193–1199 Gallo D, Nakano O, Silveira Neto S, Carvalho RPL, de Batista GC, Berti Filho E, Parra JRP, Zucchi RA, Alves SB, Vendramim JD (1988) Manual de entomologia agrícola, 2nd edn. Agronômica Ceres, São Paulo Gill FB, Mack AL, Russell TR (1982) Competition between hermit hummingbirds Phaethorninae and insects for nectar in a Costa Rican rain forest. Ibis 124:44–49 Grasso FW (2001) Invertebrate-inspired sensory-motor systems and autonomous, olfactory-guided exploration. Biol Bull 200:160–168 Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, New York Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14 Guilford T, Dawkins MS (1993) Receiver psychology and the design of animal signals. Trends Neurosci 16:430–436 Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge, Mass Hrncir M, Jarau S, Zucchi R, Barth FG (2004) On the origin and properties of scent marks deposited at the food source by a stingless bee, Melipona seminigra. Apidologie 35:3–13 Hubbell SP, Johnson LK (1978) Comparative foraging behavior of six stingless bee species exploiting a standardized resource. Ecology 59:1123–1136 Jarau S, Hrncir M, Zucchi R, Barth FG (2000) Recruitment behavior in stingless bee, Melipona scutellaris and M. quadrifasciata. I. Foraging at food sources differing in direction and distance. Apidologie 31:81–91 Jarau S, Hrncir M, Schmidt VM, Zucchi R, Barth FG (2003) Effectiveness of recruitment behavior in stingless bees (Apidae, Meliponini). Insectes Soc 50:365–374 Jarau S, Hrncir M, Zucchi R, Barth FG (2004) A stingless bee uses labial gland secretions for scent trail communication (Trigona recursa Smith 1863). J Comp Physiol A 190:233–239 Johnson LK (1974) The role of agonistic behavior in the foraging strategies of Trigona bees. PhD Thesis, University of California Berkeley Johnson LK, Hubbell SP (1974) Aggression and competition among stingless bees: field studies. Ecology 55:120–127 Johnson LK, Hubbell SP (1987) Defense of food supply by eusocial colonies. Am Zool 27:347–358 Kerr WE (1960) Evolution of communication in bees and its role in speciation. Evolution 14:326–327 Kerr WE (1972) Orientação pelo sol em Trigona spinipes. Ciênc Cult Suppl:341–342 Kerr WE (1973) Sun compass orientation in the stingless bees, Trigona (Trigona) spinipes (Fabricius, 1793) (Apidae). An Acad Bras Ciênc 45:301–308 Kerr WE, Ferreira A, Simões de Mattos N (1963) Communication among stingless bees—additional data (Hymenoptera: Apidae). J N Y Entomol Soc 71:80–90 Kerr WE, Blum M, Fales HM (1981) Communication of food sources between workers of Trigona (Trigona) spinipes. Rev Bras Biol 41:619–623 Lindauer M, Kerr WE (1958) Die gegenseitige Verständigung bei den stachellosen Bienen. Z Vgl Physiol 41:405–434 Lindauer M, Kerr WE (1960) Communication between the workers of stingless bees. Bee World 41:29–41, 65–71 Martinez DE, Bullock SH (1990) Floral parasitism by social bees (Meliponinae, Apidae) on the chiropterophilous tree Crescentia alata (Bignoniaceae). Bol Soc Bot Mexico:69–76 Michener CD (1974) The social behavior of the bees. Harvard University Press, Cambridge, Mass Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore Nagamitsu T, Inoue T (1997) Aggressive foraging of social bees as a mechanism of floral resource partitioning in an Asian tropical rainforest. Oecologia 110:432–439 Nieh JC, Contrera FAL, Nogueira-Neto P (2003a) Pulsed mass-recruitment by a stingless bee, Trigona hyalinata. Proc R Soc Lond B 270:2191–2196 Nieh JC, Contrera FAL, Ramírez S, Imperatriz-Fonseca VL (2003b) Variation in the ability to communicate 3-D resource location by stingless bees from different habitats. Anim Behav 66:1129–1139 Nieh JC, Barreto LS, Contrera FAL, Imperatriz-Fonseca VL (2004) Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proc R Soc Lond B (in press) Ramalho M, Giannini C, Malagodi-Braga KS, Imperatriz-Fonseca VL (1994) Pollen harvest by stingless bee foragers (Hymenoptera, Apidae, Meliponinae). Grana 33:239–244 Roubik DW (1978) Competitive interactions between neotropical pollinators and Africanized honey bees. Science 201:1030–1032 Roubik DW (1980) Foraging behavior of competing Africanized honeybees and stingless bees. Ecology 61:836–845 Roubik DW (1982) Seasonality in colony food storage, brood production, and adult survivorship: studies of Melipona in tropical forest (Hymenoptera: Apidae). J Kans Entomol Soc 55:789–800 Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New York Sazima I, Sazima M (1989) Carpenter bees and stingless honeybees (Hymenoptera, Apoidea): visiting, interactions and consequences for the pollination of the passionflower (Passifloraceae). Rev Bras Entomol 33:109–118 Schmidt VM, Zucchi R, Barth FG (2003) A stingless bee marks the feeding site in addition to the scent path (Scaptotrigona aff. deplis). Apidologie 34:237–248 Silva MM, Buckner CH, Picanço M, Cruz CD (1997) Influência de Trigona spinipes Fabr. (Hymenoptera: Apidae) na Polinização do Maracujazeiro Amarelo. An Soc Entomol Bras 26:217–221 Slaa EJ, Wassenberg J, Biesmeijer JC (2003) The use of field-based social information in eusocial foragers: local enhancement among nestmates and heterospecifics in stingless bees. Ecol Entomol 28:369–379 Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, New York Vitt LJ, Cooper WEJ (1985) The evolution of sexual dimorphism in the skink Eumeces laticeps: an example of sexual selection. Can J Zool 63:995–1002 von Frisch K (1967) The dance language and orientation of bees, 1993 edn. Belknap, Cambridge, Mass Willmer PG, Corbet SA (1981) Temporal and microclimactic partitioning of the floral resources of Justica aurea amongst a concourse of pollen vectors and nectar robbers. Oecologia 51:67–78