Plant–insect interactions: the role of ecological stoichiometry

Warianty tytułu

PL

Interakcje roślin z owadami mogą być kształtowane przez stechiometrię ekologiczną

• Języki publikacji: EN

Abstrakty

EN

The energy budget of organisms is a primary factor used to generate hypotheses in ecosystem ecology and evolutionary theory. Therefore, previous studies have focused on the energy costs and benefits of adaptations, the efficiency of energy acquisition and investment, and energy budget limitations. The maintenance of stoichiometric balance is equally important because inconsistency between the chemical composition of the consumer’s tissues and that of its food sources strongly affects the major life-history traits of the consumer and may influence the consumer’s fitness and shape plant–herbivore interactions. In this short review, the framework of ecological stoichiometry is introduced, focusing on plant–insect interactions in terrestrial ecosystems. The use of the trophic stoichiometric ratio (TSR) index is presented as a useful tool for indicating the chemical elements that are scarce in food and have the potential to limit the growth and development of herbivores, thereby influencing plant – herbivorous insect interactions. As an example, the elemental composition and stoichiometry of a pollen consumer (mason bee Osmia bicornis) and its preferred pollen are compared. The growth and development of O. bicornis may be colimited by the scarcity of K, Na, and N in pollen, whereas the development of the cocoon might be colimited by the scarcity of P, Mg, K, Na, Zn, Ca, and N. A literature review of the elemental composition of pollen shows high taxonomical variability in the concentrations of bee-limiting elements. The optimized collection of pollen species based on the elemental composition may represent a strategy used by bees to overcome stoichiometric mismatches, influencing their interactions with plants. It is concluded that the dependence of life-history traits on food stoichiometry should be considered when discussing life history evolution and plant–herbivore interactions. The TSR index may serve as a convenient and powerful tool in studies investigating plant-insect interactions.

PL

Głównym czynnikiem, którego wpływ na organizmy uwzględnia się w ekologii ekosystemów i ekologii ewolucyjnej jest bilans energetyczny. Wskutek tego badacze skupiają się na energetycznych korzyściach i kosztach adaptacji, wydajności przyswajania i inwestycji energii oraz ograniczeniach budżetu energetycznego. Jednak równie ważny jest problem bilansu stechiometrycznego i rozbieżności pomiędzy składem budulca tworzącego tkanki konsumenta oraz jego pokarmu. Ta rozbieżność kształtuje cechy historii życiowych organizmów (np. tempo wzrostu, wielkość ciała czy strategię reprodukcji) oraz wpływa na interakcje roślin z roślinożercami. W związku z tym stechiometria (proporcje pierwiastków) tkanek konsumenta i jego pokarmu może służyć jako narzędzie badawcze podczas studiowania mechanizmów kształtujących interakcje roślin z owadami roślinożernymi. W części przeglądowej niniejszej pracy przedstawione są ramy programu badawczego stechiometrii ekologicznej, w kontekście oddziaływań roślina– owad w ekosystemach lądowych. Zaproponowany jest wskaźnik trophic stoichiometric ratio (TSR) – narzędzie użyteczne do wykrywania pierwiastków stężonych w pożywieniu w zbyt małych ilościach względem potrzeb konsumenta, potencjalnie limitujących wzrost i rozwój roślinożercy, tym samym kształtując zależności między roślinami, a roślinożercami. Rozwijając idee przedstawione w części przeglądowej, zaprezentowano, na przykładzie murarki ogrodowej (Osmia bicornis – pszczoła samotna, pyłkożerca), jak zastosowanie programu stechiometrii ekologicznej do badania interakcji roślina–owad, może owocować interesującymi hipotezami i ważkimi wyjaśnieniami. Wzrost i rozwój murarki może być kolimitowany przez niedobór K, Na oraz N w pożywieniu (pyłku roślinnym), natomiast produkcja kokonu może być kolimitowana przez niedobór P, Mg, K, Na, Zn, Ca oraz N. Skład pierwiastkowy pyłku odznacza się wysoką zmiennością taksonomiczną. Konieczność stechiometrycznego zbilansowania diety może kształtować strategie zdobywania pokarmu i reprodukcji oraz wpływać na śmiertelność i dostosowanie pyłkożercy, kształtując interakcje owada z roślinami. Zależność cech historii życiowych od stechiometrii pożywienia powinna być brana pod uwagę podczas badania ewolucji historii życiowych oraz interakcji roślin z owadami. Wskaźnik TSR może służyć jako poręczne, a zarazem skuteczne narzędzie podczas takich badań.

• Wydawca: -
• Czasopismo: Acta Agrobotanica
• Rocznik: 2017
• Tom: 70
• Numer: 1
• Opis fizyczny: Article 1710 [16p.], fig.,ref.

Twórcy

Bibliografia

• 1. Sterner RW, Elser JJ. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton, NJ: Princeton University Press; 2002.
• 2. Cherif M. Biological stoichiometry: the elements at the heart of biological interactions. In: Innocenti A, editor. Stoichiometry and research – the importance of quantity in biomedicine. Rijeka: InTech; 2012. p. 357–376. https://doi.org/10.5772/34528
• 3. Kaspari M, Powers JS. Biogeochemistry and geographical ecology: embracing all twenty-five elements required to build organisms. Am Nat. 2016;188(S1):S62–S73. https://doi.org/10.1086/687576
• 4. Sterner RW, Hessen DO. Algal nutrient limitation and the nutrition of aquatic herbivores. Annu Rev Ecol Syst. 1994;25(1):1–29. https://doi.org/10.1146/annurev.es.25.110194.000245
• 5. Pokarzhevskii AD, van Straalen NM, Zaboev DP, Zaitsev AS. Microbial links and element flows in nested detrital food-webs. Pedobiologia (Jena). 2003;47(3):213–224. https://doi.org/10.1078/0031-4056-00185
• 6. Vernadskiĭ VI. La Géochimie. Paris: Alcan; 1924.
• 7. Tilman D. Resource competition and community structure. Princeton, NJ: Princeton University Press; 1982. (Monographs in Population Biology).
• 8. Reiners WA. Complementary models for ecosystems. Am Nat. 1986;127(1):59–73. https://doi.org/10.1086/284467
• 9. Hessen DO, Elser JJ, Sterner RW, Urabe J. Ecological stoichiometry: an elementary approach using basic principles. Limnol Oceanogr. 2013;58(6):2219–2236. https://doi.org/10.4319/lo.2013.58.6.2219
• 10. Cherif M, Loreau M. Plant–herbivore–decomposer stoichiometric mismatches and nutrient cycling in ecosystems. Proc Biol Sci. 2013;280: 20122453. https://doi.org/10.1098/rspb.2012.2453
• 11. Wilder SM, Jeyasingh PD. Merging elemental and macronutrient approaches for a comprehensive study of energy and nutrient flows. J Anim Ecol. 2016;85(6):1427–1430. https://doi.org/10.1111/1365-2656.12573
• 12. Zhang C, Jansen M, de Meester L, Stoks R. Energy storage and fecundity explain deviations from ecological stoichiometry predictions under global warming and size-selective predation. J Anim Ecol. 2016;85(6):1431–1441. https://doi.org/10.1111/1365-2656.12531
• 13. Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ. Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett. 2003;6(2):96–101. https://doi.org/10.1046/j.1461-0248.2003.00409.x
• 14. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, et al. Nutritional constraints in terrestrial and freshwater food webs. Nature. 2000;408(6812):578–580. https://doi.org/10.1038/35046058
• 15. Yoshida T. Ecological stoichiometry and the shape of resource-based tradeoffs. Oikos. 2006;112(2):406–411. https://doi.org/10.1111/j.0030-1299.2006.14231.x
• 16. Denno RF, Fagan WF. Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology. 2003;84(10):2522–2531. https://doi.org/10.1890/02-0370
• 17. Fagan WF, Denno RF. Stoichiometry of actual vs. potential predator-prey interactions: insights into nitrogen limitation for arthropod predators. Ecol Lett. 2004;7(9):876–883.m https://doi.org/10.1111/j.1461-0248.2004.00641.x
• 18. Zhang G, Han X, Elser JJ. Rapid top–down regulation of plant C:N:P stoichiometry by grasshoppers in an Inner Mongolia grassland ecosystem. Oecologia. 2011;166(1):253–264. https://doi.org/10.1007/s00442-011-1904-5
• 19. Sitters J, Olde Venterink H. The need for a novel integrative theory on feedbacks between herbivores, plants and soil nutrient cycling. Plant Soil. 2015;396(1–2):421–426. https://doi.org/10.1007/s11104-015-2679-y
• 20. Daufresne T, Loreau M. Plant–herbivore interactions and ecological stoichiometry: when do herbivores determine plant nutrient limitation? Ecol Lett. 2001;4(3):196–206. https://doi.org/10.1046/j.1461-0248.2001.00210.x
• 21. Hillebrand H, Borer ET, Bracken MES, Cardinale BJ, Cebrian J, Cleland EE, et al. Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems. Ecol Lett. 2009;12(6):516–527. https://doi.org/10.1111/j.1461-0248.2009.01304.x
• 22. Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ. Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol Lett. 2003;6(2):96–101. https://doi.org/10.1046/j.1461-0248.2003.00409.x
• 23. Awmack CS, Leather SR. Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol. 2002;47(1):817–844. https://doi.org/10.1146/annurev.ento.47.091201.145300
• 24. Smil V. Cycles of life: civilization and the biosphere. New York, NY: Scientific American Library; 2000.
• 25. Liebig J, Playfair LP, Webster JW. Chemistry in its application to agriculture and physiology. Cambridge: J. Owen; 1843. https://doi.org/10.5962/bhl.title.41248
• 26. Lotka AJ. Elements of physical biology. Baltimore, MD: Williams and Wilkins Company; 1925.
• 27. Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH. Organism size, life history, and N:P stoichiometry. Bioscience. 1996;46(9):674–684. https://doi.org/10.2307/1312897
• 28. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow T, Cotner JB, et al. Biological stoichiometry from genes to ecosystems. Ecol Lett. 2000;3(6):540–550. https://doi.org/10.1046/j.1461-0248.2000.00185.x
• 29. Association for the Sciences of Limnology and Oceanography. ASLO honors “Algal nutrient limitation and the nutrition of aquatic herbivores” with the 2017 John H. Martin Award [Internet]. 2016 [cited 2017 Mar 16]. Available from: http://aslo.org/awards/2017/sternerhessen.html
• 30. Moe SJ, Stelzer RS, Forman MR, Harpole WS, Daufresne T, Yoshida T. Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos. 2005;109(1):29–39. https://doi.org/10.1111/j.0030-1299.2005.14056.x
• 31. Klausmeier CA, Litchman E, Daufresne T, Levin SA. Phytoplankton stoichiometry. Ecol Res. 2008;23(3):479–485. https://doi.org/10.1007/s11284-008-0470-8
• 32. Sardans J, Rivas-Ubach A, Peñuelas J. The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry. 2012;111(1–3):1–39. https://doi.org/10.1007/s10533-011-9640-9
• 33. Lemoine NP, Giery ST, Burkepile DE. Differing nutritional constraints of consumers across ecosystems. Oecologia. 2014;174(4):1367–1376. https://doi.org/10.1007/s00442-013-2860-z
• 34. Sperfeld E, Wagner ND, Halvorson HM, Malishev M, Raubenheimer D. Bridging ecological stoichiometry and nutritional geometry with homeostasis concepts and integrative models of organism nutrition. Funct Ecol. 2017;31(2):286–296. https://doi.org/10.1111/1365-2435.12707
• 35. Sperfeld E, Halvorson HM, Malishev M, Clissold FJ, Wagner ND. Woodstoich III: integrating tools of nutritional geometry and ecological stoichiometry to advance nutrient budgeting and the prediction of consumer-driven nutrient recycling. Oikos. 2016;125(11):1539–1553. https://doi.org/10.1111/oik.03529
• 36. Danger M, Arce Funck J, Devin S, Heberle J, Felten V. Phosphorus content in detritus controls life-history traits of a detritivore. Funct Ecol. 2013;27(3):807–815. https://doi.org/10.1111/1365-2435.12079
• 37. Laspoumaderes C, Modenutti B, Elser JJ, Balseiro E. Does the stoichiometric carbon:phosphorus knife edge apply for predaceous copepods? Oecologia. 2015;178(2):557–569. https://doi.org/10.1007/s00442-014-3155-8
• 38. Elser JJ, Kyle M, Learned J, McCrackin M, Peace A, Steger L. Life on the stoichiometric knife-edge: effects of high and low food C:P ratio on growth, feeding, and respiration in three Daphnia species. Inland Waters. 2016;6(2):136–146. https://doi.org/10.5268/IW-6.2.908
• 39. Huberty AF, Denno RF. Consequences of nitrogen and phosphorus limitation for the performance of two planthoppers with divergent life-history strategies. Oecologia. 2006;149(3):444–455. https://doi.org/10.1007/s00442-006-0462-8
• 40. González AL, Fariña JM, Kay AD, Pinto R, Marquet PA. Exploring patterns and mechanisms of interspecific and intraspecific variation in body elemental composition of desert consumers. Oikos. 2011;120(8):1247–1255. https://doi.org/10.1111/j.1600-0706.2010.19151.x
• 41. Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, et al. Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat. 2002;160(6):784–802. https://doi.org/10.1086/343879
• 42. Hambäck P, Gilbert J, Schneider K, Martinson HM, Kolb G, Fagan WF. Effects of body size, trophic mode and larval habitat on Diptera stoichiometry: a regional comparison. Oikos. 2009;118(4):615–623. https://doi.org/10.1111/j.1600-0706.2008.17177.x
• 43. Martinson HM, Schneider K, Gilbert J, Hines JE, Hambäck PA, Fagan WF. Detritivory: stoichiometry of a neglected trophic level. Ecol Res. 2008;23(3):487–491. https://doi.org/10.1007/s11284-008-0471-7
• 44. Elser JJ, Elser MM, MacKay NA, Carpenter SR. Zooplankton-mediated transitions between N- and P-limited algal growth. Limnol Oceanogr. 1988;33(1):1–14. https://doi.org/10.4319/lo.1988.33.1.0001
• 45. Elser JJ, Urabe J. The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology. 1999;80(3):735–751. https://doi.org/10.1890/0012-9658(1999)080[0735:TSOCDN]2.0.CO;2
• 46. Chen Y, Forschler BT. Elemental concentrations in the frass of saproxylic insects suggest a role in micronutrient cycling. Ecosphere. 2016;7(3):e01300. https://doi.org/10.1002/ecs2.1300
• 47. Bärlocher F, Rennenberg H. Food chains and nutrient cycles. In: Krauss GJ, Nies DH, editors. Ecological biochemistry. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA. p. 92–122. https://doi.org/10.1002/9783527686063.ch6
• 48. Vanni MJ, McIntyre PB. Predicting nutrient excretion of aquatic animals with metabolic ecology and ecological stoichiometry: a global synthesis. Ecology. 2016;97(12):3460–3471. https://doi.org/10.1002/ecy.1582
• 49. Elser JJ, Hamilton A. Stoichiometry and the new biology: the future is now. PLoS Biol. 2007;5(7):e181. https://doi.org/10.1371/journal.pbio.0050181
• 50. Boersma M, Aberle N, Hantzsche FM, Schoo KL, Wiltshire KH, Malzahn AM. Nutritional limitation travels up the food chain. Int Rev Hydrobiol. 2008;93(4–5):479–488. https://doi.org/10.1002/iroh.200811066
• 51. Spohn M. Element cycling as driven by stoichiometric homeostasis of soil microorganisms. Basic Appl Ecol. 2016;17(6):471–478. https://doi.org/10.1016/j.baae.2016.05.003
• 52. Ott D, Digel C, Klarner B, Maraun M, Pollierer M, Rall BC, et al. Litter elemental stoichiometry and biomass densities of forest soil invertebrates. Oikos. 2014;123(10):1212–1223. https://doi.org/10.1111/oik.01670
• 53. Purahong W, Wubet T, Lentendu G, Schloter M, Pecyna MJ, Kapturska D, et al. Life in leaf litter: novel insights into community dynamics of bacteria and fungi during litter decomposition. Mol Ecol. 2016;25(16):4059–4074. https://doi.org/10.1111/mec.13739
• 54. Liu D, Keiblinger KM, Leitner S, Mentler A, Zechmeister-Boltenstern S. Is there a convergence of deciduous leaf litter stoichiometry, biochemistry and microbial population during decay? Geoderma. 2016;272:93–100. https://doi.org/10.1016/j.geoderma.2016.03.005
• 55. Čapek P, Kotas P, Manzoni S & Šantrůčková H Drivers of phosphorus limitation across soil microbial communities. Funct Ecol. 2016;30(10):1705–1713. https://doi.org/10.1111/1365-2435.12650
• 56. Elser JJ, Loladze I, Peace AL, Kuang Y. Lotka re-loaded: modeling trophic interactions under stoichiometric constraints. Ecol Modell. 2012;245:3–11. https://doi.org/10.1016/j.ecolmodel.2012.02.006
• 57. Andersen T, Elser JJ, Hessen DO. Stoichiometry and population dynamics. Ecol Lett. 2004;7(9):884–900. https://doi.org/10.1111/j.1461-0248.2004.00646.x
• 58. Kaspari M, Roeder KA, Benson B, Weiser MD, Sanders NJ. Sodium co-limits and catalyzes macronutrients in a prairie food web. Ecology. 2017;98(2):315–320. https://doi.org/10.1002/ecy.1677
• 59. Sperfeld E, Raubenheimer D, Wacker A. Bridging factorial and gradient concepts of resource co-limitation: towards a general framework applied to consumers. Ecol Lett. 2016;19(2):201–215. https://doi.org/10.1111/ele.12554
• 60. Marleau JN, Guichard F, Loreau M. Emergence of nutrient co-limitation through movement in stoichiometric meta-ecosystems. Ecol Lett. 2015;18(11):1163–1173. https://doi.org/10.1111/ele.12495
• 61. Wirtz KW, Kerimoglu O. Autotrophic stoichiometry emerging from optimality and variable co-limitation. Front Ecol Evol. 2016;4. https://doi.org/10.3389/fevo.2016.00131
• 62. Anderson TR, Pond DW. Stoichiometric theory extended to micronutrients: comparison of the roles of essential fatty acids, carbon, and nitrogen in the nutrition of marine copepods. Limnol Oceanogr. 2000;45(5):1162–1167. https://doi.org/10.4319/lo.2000.45.5.1162
• 63. Anderson TR, Pond DW, Mayor DJ. The role of microbes in the nutrition of detritivorous invertebrates: a stoichiometric analysis. Front Microbiol. 2017;7. https://doi.org/10.3389/fmicb.2016.02113
• 64. Delgado-Baquerizo M, Reich PB, Khachane AN, Campbell CD, Thomas N, Freitag TE, et al. It is elemental: soil nutrient stoichiometry drives bacterial diversity. Environ Microbiol. 2017. https://doi.org/10.1111/1462-2920.13642
• 65. Bradshaw C, Kautsky U, Kumblad L. Ecological stoichiometry and multielement transfer in a coastal ecosystem. Ecosystems. 2012;15(4):591–603. https://doi.org/10.1007/s10021-012-9531-5
• 66. Schlesinger WH, Bernhardt ES. Biogeochemistry: an analysis of global change. Waltham, MA: Elsevier, Academic Press; 2013. https://doi.org/10.1093/obo/9780199830060-0111
• 67. Tiegs SD, Berven KA, Carmack DJ, Capps KA. Stoichiometric implications of a biphasic life cycle. Oecologia. 2016;180(3):853–863. https://doi.org/10.1007/s00442-015-3504-2
• 68. Swanson EM, Espeset A, Mikati I, Bolduc I, Kulhanek R, White WA, et al. Nutrition shapes life-history evolution across species. Proc R Soc B. 2016;283(1834):20152764. https://doi.org/10.1098/rspb.2015.2764
• 69. Halvorson HM, Small GE. Observational field studies are not appropriate tests of consumer stoichiometric homeostasis. Freshw Sci. 2016;35(4):1103–1116. https://doi.org/10.1086/689212
• 70. González AL, Kominoski JS, Danger M, Ishida S, Iwai N, Rubach A. Can ecological stoichiometry help explain patterns of biological invasions? Oikos. 2010;119(5):779–790. https://doi.org/10.1111/j.1600-0706.2009.18549.x
• 71. Filipiak M, Weiner J. How to make a beetle out of wood: multi-elemental stoichiometry of wood decay, xylophagy and fungivory. PLoS One. 2014;9(12):e115104. https://doi.org/10.1371/journal.pone.0115104
• 72. Filipiak M, Sobczyk Ł, Weiner J. Fungal transformation of tree stumps into a suitable resource for xylophagous beetles via changes in elemental ratios. Insects. 2016;7(2):13. https://doi.org/10.3390/insects7020013
• 73. Filipiak M, Weiner J. Nutritional dynamics during the development of xylophagous beetles related to changes in the stoichiometry of 11 elements. Physiol Entomol. 2017;42(1):73–84. https://doi.org/10.1111/phen.12168
• 74. Filipiak M. Pollen stoichiometry may influence detrital terrestrial and aquatic food webs. Front Ecol Evol. 2016;4:138. https://doi.org/10.3389/fevo.2016.00138
• 75. Mulder C, Boit A, Mori S, Vonk JA, Dyer SD, Faggiano L, et al. Distributional (in)congruence of biodiversity–ecosystem functioning. In: Woodward G, editor. Advances in ecological research. London: Elsevier Ltd.; 2012. p. 1–88. https://doi.org/10.1016/B978-0-12-396992-7.00001-0
• 76. Abbas M, Klein AM, Ebeling A, Oelmann Y, Ptacnik R, Weisser WW, et al. Plant diversity effects on pollinating and herbivorous insects can be linked to plant stoichiometry. Basic Appl Ecol. 2014;15(2):169–178. https://doi.org/10.1016/j.baae.2014.02.001
• 77. Urabe J, Watanabe Y. Possibility of N or P limitation for planktonic cladocerans: an experimental test. Limnol Oceanogr. 1992;37(2):244–251. https://doi.org/10.4319/lo.1992.37.2.0244
• 78. Frost PC, Benstead JP, Cross WF, Hillebrand H, Larson JH, Xenopoulos MA, et al. Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett. 2006;9(7):774–779. https://doi.org/10.1111/j.1461-0248.2006.00919.x
• 79. Doi H, Cherif M, Iwabuchi T, Katano I, Stegen JC, Striebel M. Integrating elements and energy through the metabolic dependencies of gross growth efficiency and the threshold elemental ratio. Oikos. 2010;119(5):752–765. https://doi.org/10.1111/j.1600-0706.2009.18540.x
• 80. Taha EKA. Chemical composition and amounts of mineral elements in honeybeecollected pollen in relation to botanical origin. Journal of Agricultural Science. 2015;59(1):75–81. https://doi.org/10.1515/jas-2015-0008
• 81. Szczęsna T. Concentration of selected elements in honeybee-collected pollen. Journal of Agricultural Science. 2007;51(1):5–13.
• 82. Kostić AŽ, Pešić MB, Mosić MD, Dojčinović BP, Natić MM, Trifković JĐ. Mineral content of bee pollen from Serbia. Arh Hig Rada Toksikol. 2015;66(4):251–258. https://doi.org/10.1515/aiht-2015-66-2630
• 83. Orzáez Villanueva MT, Díaz Marquina A, Bravo Serrano R, Blaźquez Abellán G. Mineral content of commercial pollen. Int J Food Sci Nutr. 2001;52(3):243–249. https://doi.org/10.1080/09637480020027000-3-1
• 84. Stanciu OG, Marghitas LA, Dezmirean D, Campos MG. A comparison between the mineral content of flower and honeybee collected pollen of selected plant origin (Helianthus annuus L. and Salix sp.). Rom Biotechnol Lett. 2011;16(4):6291–6296.
• 85. Todd FE, Bretherick O. The composition of pollens. J Econ Entomol. 1942;35(3):312–317. https://doi.org/10.1093/jee/35.3.312
• 86. Nielsen N, Grömmer J, Lunden R. Investigations on the chemical composition of pollen from some plants. Acta Chem Scand. 1955;9:1100–1106. https://doi.org/10.3891/acta.chem.scand.09-1100
• 87. Roulston T, Cane J. Pollen nutritional content and digestibility for animals. Plant Syst Evol. 2000;222:187–209. https://doi.org/10.1007/BF00984102
• 88. Campos MGR, Bogdanov S, de Almeida-Muradian LB, Szczesna T, Mancebo Y, Frigerio C, et al. Pollen composition and standardisation of analytical methods. J Apic Res. 2008;47(2):154–161. https://doi.org/10.1080/00218839.2008.11101443
• 89. Nicolson SW. Bee Food: The chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr Zool. 2011;46(2):197–204. https://doi.org/10.1080/15627020.2011.11407495
• 90. Morgano MA, Teixeira Martins, Márcia C. Rabonato LC, Milani RF, Yotsuyanagi K, Rodriguez-Amaya DB A. Comprehensive investigation of the mineral composition of Brazilian bee pollen: geographic and seasonal variations and contribution to human diet. J Braz Chem Soc. 2012;23(4):727–736. https://doi.org/10.1590/s0103-50532012000400019
• 91. Yang K, Wu D, Ye X, Liu D, Chen J, Sun P. Characterization of chemical composition of bee pollen in China. J Agric Food Chem. 2013;61(3):708–718. https://doi.org/10.1021/jf304056b
• 92. Roulston TH, Goodell K. The role of resources and risks in regulating wild bee populations. Annu Rev Entomol. 2011;56(1):293–312. https://doi.org/10.1146/annurev-ento-120709-144802
• 93. Naug D. Nutritional stress due to habitat loss may explain recent honeybee colony collapses. Biol Conserv. 2009;142(10):2369–2372. https://doi.org/10.1016/j.biocon.2009.04.007
• 94. Bonoan RE, Tai TM, Tagle Rodriguez M, Feller L, Daddario SR, Czaja RA, et al. Seasonality of salt foraging in honey bees (Apis mellifera). Ecol Entomol. 2017;42(2):195–201. https://doi.org/10.1111/een.12375
• 95. Cane JH. Adult pollen diet essential for egg maturation by a solitary Osmia bee. J Insect Physiol. 2016;95:105–109. https://doi.org/10.1016/j.jinsphys.2016.09.011
• 96. Frias BED, Barbosa CD, Lourenço AP. Pollen nutrition in honey bees (Apis mellifera): impact on adult health. Apidologie. 2016;47(1):15–25. https://doi.org/10.1007/s13592-015-0373-y
• 97. Brodschneider R, Crailsheim K. Nutrition and health in honey bees. Apidologie. 2010;41(3):278–294. https://doi.org/10.1051/apido/2010012
• 98. Ruedenauer FA, Spaethe J, Leonhardt SD. Hungry for quality – individual bumblebees forage flexibly to collect high-quality pollen. Behav Ecol Sociobiol. 2016;70(8):1209–1217. https://doi.org/10.1007/s00265-016-2129-8
• 99. Hendriksma HP, Shafir S. Honey bee foragers balance colony nutritional deficiencies. Behav Ecol Sociobiol. 2016;70(4):509–517. https://doi.org/10.1007/s00265-016-2067-5
• 100. Di Pasquale G, Salignon M, Le Conte Y, Belzunces LP, Decourtye A, Kretzschmar A, et al. Influence of pollen nutrition on honey bee health: do pollen quality and diversity matter? PLoS One. 2013;8(8):e72016. https://doi.org/10.1371/journal.pone.0072016
• 101. Vaudo AD, Patch HM, Mortensen DA, Tooker JF, Grozinger CM. Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proc Natl Acad Sci USA. 2016;113(28):E4035–E4042. https://doi.org/10.1073/pnas.1606101113
• 102. Peterson JH, Roitberg BD. Variable flight distance to resources results in changing sex allocation decisions, Megachile rotundata. Behav Ecol Sociobiol. 2016;70(2):247–253. https://doi.org/10.1007/s00265-015-2043-5
• 103. Schmidt JO, Thoenes SC, Levin MD. Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Ann Entomol Soc Am. 1987;80(2):176–183. https://doi.org/10.1093/aesa/80.2.176
• 104. Peterson JH. Sex allocation in a solitary bee: a behavioural ecology approach [Master thesis]. Burnaby, BC: Simon Fraser University; 2004.
• 105. Raw A. The biology of the solitary bee Osmia rufa (L.) (Megachilidae). Transactions of the Royal Entomological Society of London. 2009;124(3):213–229. https://doi.org/10.1111/j.1365-2311.1972.tb00364.x
• 106. Giejdasz K, Fliszkiewicz M, Bednárová A, Krishnan N. Reproductive potential and nesting effects of Osmia rufa (syn. bicornis) female (Hymenoptera: Megachilidae). Journal of Apicultural Science. 2016;60(1):75–86. https://doi.org/10.1515/jas-2016-0003
• 107. Terra WR, de Bianchi AG. Chemical composition of the cocoon of the fly, Rhynchosciara americana. Insect Biochem. 1974;4(2):173–183. https://doi.org/10.1016/0020-1790(74)90005-5
• 108. Ashfaq M, Ahmad N, Ali A. Effects of optimum dosages of nitrogen, potassium, calcium and copper on silkworm, Bombyx mori L. Development and silk yield. South Pacific Studies. 1998;18(2):47–50.
• 109. Khan MA, Akram W, Ashfaq M, Khan HAA, Kim YK, Lee JJ. Effects of optimum doses of nitrogen, phosphorus, potassium and calcium on silkworm, Bombyx mori L., growth and yield. Entomol Res. 2010;40(6):285–289. https://doi.org/10.1111/j.1748-5967.2010.00300.x
• 110. Villanueva-G. R, Roubik DW. Why are African honey bees and not European bees invasive? Pollen diet diversity in community experiments. Apidologie. 2004;35(5):481–491. https://doi.org/10.1051/apido:2004041
• 111. Boelter A, Wilson W. Attempts to condition the pollen preference of honey bees. American Bee Journal. 1984;124(8):609–610.
• 112. Boch R. Relative attractiveness of different pollens to honeybees when foraging in a flight room and when fed in the hive. J Apic Res. 1982;21(2):104–106. https://doi.org/10.1080/00218839.1982.11100523
• 113. Free JB. The pollination of fruit trees. Bee World. 1960;41(6):141–151. https://doi.org/10.1080/0005772X.1960.11096783
• 114. Levin MD, Bohart GE. Selection of pollens by honey bees. American Bee Journal. 1955;95(10):392–393.
• 115. Schmidt JO. Pollen foraging preference of honey bees. Southwest Entomol. 1982;7(4):255–259.
• 116. Doull KM. The relative attractiveness to pollen-collecting honeybees of some different pollens. J Apic Res. 1966;5(1):9–13. https://doi.org/10.1080/00218839.1966.11100125
• 117. Schmidt J. Feeding preferences of Apis mellifera L.(Hymenoptera: Apidae): individual versus mixed pollen species. J Kans Entomol Soc. 1984;57(2):323–327.
• 118. Schmidt J, Johnson B. Pollen feeding preferences of Apis mellifera, a polyectic bee. Southwest Entomol. 1984;9(1):41–47.
• 119. Vaudo AD, Tooker JF, Grozinger CM, Patch HM. Bee nutrition and floral resource restoration. Curr Opin Insect Sci. 2015;10133–141. https://doi.org/10.1016/j.cois.2015.05.008
• 120. Fewell J, Winston M. Colony state and regulation of pollen foraging in the honey bee, Apis mellifera L. Behav Ecol Sociobiol. 1992;30(6):387–393. https://doi.org/10.1007/BF00176173
• 121. Campana BJ, Moeller FE. Honey bees: preference for and nutritive value of pollen from five plant sources. J Econ Entomol. 1977;70(1):39–41. https://doi.org/10.1093/jee/70.1.39
• 122. Bukovinszky T, Rikken I, Evers S, Wäckers FL, Biesmeijer JC, Prins HHT, et al. Effects of pollen species composition on the foraging behaviour and offspring performance of the mason bee Osmia bicornis (L.). Basic Appl Ecol. 2017;18:21–30. https://doi.org/10.1016/j.baae.2016.11.001
• 123. Leal MC, Seehausen O, Matthews B The ecology and evolution of stoichiometric phenotypes. Trends Ecol Evol. 2017;32(2):108–117. https://doi.org/10.1016/j.tree.2016.11.006

Identyfikatory

DOI

10.5586/aa.1710