Abstract
Neotropical Heliconius and Laparus butterflies actively collect pollen onto the proboscis and extract nutrients from it. This study investigates the impact of the processing behaviour on the condition of the pollen grains. Pollen samples (n = 72) were collected from proboscides of various Heliconius species and Laparus doris in surrounding habitats of the Tropical Research Station La Gamba (Costa Rica). Examination using a light microscope revealed that pollen loads contained 74.88 ± 53.67% of damaged Psychotria pollen, 72.04 ± 23.4% of damaged Psiguria/Gurania pollen, and 21.35 ± 14.5% of damaged Lantana pollen (numbers represent median ± first quartile). Damaged pollen grains showed deformed contours, inhomogeneous and/or leaking contents, or they were empty. Experiments with Heliconius and Laparus doris from a natural population in Costa Rica demonstrated that 200 min of pollen processing behaviour significantly increased the percentage of damaged pollen of Psychotria compared to pollen from anthers (P = 0.015, Z = −2.44, Mann–Whitney U-test). Examination of pollen loads from green house reared Heliconius butterflies resulted in significantly greater amounts of damaged Psiguria pollen after 200 min of processing behaviour compared to pollen from flowers (P < 0.001, Z = −4.583, Mann–Whitney U-test). These results indicate that pollen processing functions as extra oral digestion whereby pollen grains are ruptured to make the content available for ingestion.
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References
Beltrán M, Jiggins CD, Brower AVZ, Bermingham E, Mallet J (2007) Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data. Biol J Linn Soc 92:221–239
Boggs CL (1981) Selection pressures affecting male nutrient investment at mating in Heliconiine butterflies. Evolution 35:931–940
Boggs CL (1987) Ecology of nectar and pollen feeding in Lepidoptera. In: Slansky F, Rodriguez JG (eds) Nutritional ecology of insects, mites and spiders. John Wiley and Sons, New York, pp 369–389
Boggs CL, Gilbert LE (1979) Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83–84
Boggs CL, Smiley JT, Gilbert LE (1981) Patterns of pollen exploitation by Heliconius butterflies. Oecologia (Berlin) 48:284–289
Cardoso MZ (2001) Patterns of pollen collection and flower visitation by Heliconius butterflies in southeastern Mexico. J Trop Ecol 17:763–768
Cardoso MZ, Gilbert LE (2007) A male gift to its partner? Cyanogenic glycosides in the spermatophore of long wing butterflies (Heliconius). Naturwissenschaften 94:39–42
Condon MA, Gilbert LE (1990) Reproductive biology and natural history of neotropical vines Gurania and Psiguria. In: Bates D, Robinson RW, Jeffrey C (eds) Biology and utilization of the Cucurbitaceae. Cornell University Press, Ithaca, NY, pp 150–166
Dunlap-Pianka H, Boggs CL, Gilbert LE (1977) Ovarian dynamics in Heliconiine butterflies: programmed senescence versus eternal youth. Science 197:487–490
Eberhard SH, Krenn HW (2003) Salivary glands and salivary pumps in adult Nymphalidae (Lepidoptera). Zoomorphology 122:161–167
Eberhard SH, Hrassnigg N, Crailsheim K, Krenn HW (2007) Evidence of protease in the saliva of the butterfly Heliconius melpomene (L.) (Nymphalidae, Lepidoptera). J Insect Physiol 53:126–131
Eberhard SH, Nemeschkal H–L, Krenn HW (2009) Biometrical evidence for adaptations of the salivary glands to pollen feeding in Heliconius butterflies (Lepidoptera: Nymphalidae). Biol J Linn Soc 97:604–612
Erhardt A, Baker I (1990) Pollen amino acids—an additional diet for a nectar feeding butterfly? Plant Syst Evol 169:111–121
Estrada C, Jiggins CD (2002) Patterns of pollen feeding and habitat preference among Heliconius species. Ecol Entomol 27:448–456
Gilbert LE (1972) Pollen feeding and reproductive biology of Heliconius butterflies. Proc Nat Acad Sci USA 69:1403–1407
Gilbert LE (1991) Biodiversity of a Central American Heliconius community: pattern, process, and problems. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: Evolutionary ecology in tropical and temperate regions. John Wiley and Sons Inc., New York, Chichester, Brisbane, Toronto, Singapore, pp 403–427
Krenn HW (2008) Feeding behaviours of neotropical butterflies. In: Weissenhofer A, Huber W, Mayer V, Pamperl S, Weber A, Aubrecht G (eds) Natural and Cultural History of the Golfo Dulce Region, Costa Rica. Biologiezentrum der Oberösterreichischen Landesmuseen, Linz, Austria, Stapfia 88:295-304
Krenn HW, Penz CM (1998) Mouthparts of Heliconius butterflies (Lepidoptera: Nymphalidae): A search for anatomical adaptations to pollen-feeding behaviour. Int J Insect Morphol Embryol 27:301–309
Murawski DA (1986) Pollen ecology of a Costa Rica population of Psiguria warscewiczii in relation to foraging behaviour of Heliconius butterflies. Dissertation, University of Texas at Austin
Murawski DA (1987) Floral resource variation, pollinator response, and potential pollen flow in Psiguria warscewiczii. Ecology 68:1273–1282
Murawski DA, Gilbert LE (1986) Pollen flow in Psiguria warscewiczii: A comparison of Heliconius butterflies and hummingbirds. Oecologia (Berlin) 68:161–167
Nahrstedt A, Davis RH (1983) Occurrence, variation and biosynthesis of the cyanogenic glucosides linamarin and lotaustralin in species of the Heliconiini (Insecta: Lepidoptera). Comp Biochem Physiol 75:65–73
O’Brien DM, Boggs CL, Flogel ML (2003) Pollen feeding in the butterfly Heliconius charitonia: isotopic evidence for essential amino acid transfer from pollen to eggs. Proc R Soc Ser B 270:2631–2636
Penz CM (1999) Higher level phylogeny for the passion-vine butterflies (Nymphalidae, Heliconiinae) based on early stage and adult morphology. Zool J Linn Soc 127:277–344
Penz CM, Krenn HW (2000) Behavioural adaptations to pollen-feeding in Heliconius butterflies (Nymphalidae: Heliconiinae): an experiment using Lantana flowers. J Insect Behav 13:865–880
Roubik DW, Moreno JEP (1991) Pollen and spores of Barro Colorado Island. Monographs in Systematic Botany from the Missouri Botanical Garden 36:1–268
Weber A (ed) (2001) An introductory field guide to the flowering plants of the Golfo Dulce rain forests Costa Rica Biologiezentrum der Oberösterreichischen Landesmuseen, Linz, Austria, Stapfia 78:1-462
Weissenhofer A, Huber W, Mayer V, Pamperl S, Weber A, Aubrecht G (eds) (2008) Natural and cultural history of the Golfo Dulce region, Costa Rica. Biologiezentrum der Oberösterreichischen Landesmuseen, Linz, Austria, Stapfia 88:1–768
Acknowledgments
We are grateful to A. Demetz, T. Buchegger, S. Hufnagl for assistance in capturing butterflies, preparation of the pollen and counting pollen grains. Fieldwork was aided by the excellent facilities provided by the staff of the Tropical Research Station La Gamba (Costa Rica). The Costa Rican Ministerio del Ambients y Energia kindly granted research permits. We thank the Brackenridge Field Laboratory, University of Texas at Austin (USA) for logistic support as well as J. Bauder and J. Plant for editorial help. Funding was provided from the Austrian Science Fund (FWF project number P 18425 B03).
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Krenn, H.W., Eberhard, M.J.B., Eberhard, S.H. et al. Mechanical damage to pollen aids nutrient acquisition in Heliconius butterflies (Nymphalidae). Arthropod-Plant Interactions 3, 203–208 (2009). https://doi.org/10.1007/s11829-009-9074-7
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DOI: https://doi.org/10.1007/s11829-009-9074-7