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Cascading effects of caffeine intake by primary consumers to the upper trophic level

Published online by Cambridge University Press:  03 September 2021

Kévin Tougeron*
Affiliation:
Earth and Life Institute, Ecology and Biodiversity, Université catholique de Louvain, 1348Louvain-la-Neuve, Belgium
Thierry Hance
Affiliation:
Earth and Life Institute, Ecology and Biodiversity, Université catholique de Louvain, 1348Louvain-la-Neuve, Belgium
*
Author for correspondence: Kévin Tougeron, Email: [email protected]

Abstract

Secondary metabolites are central to understanding the evolution of plant–animal interactions. Direct effects on phytophagous animals are well-known, but how secondary consumers adjust their behavioural and physiological responses to the herbivore's diet remains more scarcely explored for some metabolites. Caffeine is a neuroactive compound that affects both the behaviour and physiology of several animal species, from humans to insects. It is an alkaloid present in nectar, leaves and even sap of numerous species of plants where it plays a role in chemical defences against herbivores and pathogens. Caffeine effects have been overlooked in generalist herbivores that are not specialized in coffee or tea plants. Using a host–parasitoid system, we show that caffeine intake at a relatively low dose affects longevity and fecundity of the primary consumer, but also indirectly of the secondary one, suggesting that this alkaloid and/or its effects can be transmitted through trophic levels and persist in the food chain. Parasitism success was lowered by ≈16% on hosts fed with caffeine, and parasitoids of the next generation that have developed in hosts fed on caffeine showed a reduced longevity, but no differences in mass and size were found. This study helps at better understanding how plant secondary metabolites, such as caffeine involved in plant–animal interactions, could affect primary consumers, could have knock-on effects on upper trophic levels over generations, and could modify interspecific interactions in multitrophic systems.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Adler, LS (2000) The ecological significance of toxic nectar. Oikos 91, 409420.10.1034/j.1600-0706.2000.910301.xCrossRefGoogle Scholar
Ashihara, H, Sano, H and Crozier, A (2008) Caffeine and related purine alkaloids: biosynthesis, catabolism, function and genetic engineering. Phytochemistry 69, 841856.10.1016/j.phytochem.2007.10.029CrossRefGoogle ScholarPubMed
Barbosa, P, Saunders, JA, Kemper, J, Trumbule, R, Olechno, J and Martinat, P (1986) Plant allelochemicals and insect parasitoids effects of nicotine on Cotesia congregata (say) (Hymenoptera: Braconidae) and Hyposoter annulipes (Cresson) (Hymenoptera: Ichneumonidae). Journal of Chemical Ecology 12, 13191328.10.1007/BF01012351CrossRefGoogle Scholar
Bukovinszky, T, Poelman, EH, Gols, R, Prekatsakis, G, Vet, LE, Harvey, JA and Dicke, M (2009) Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160, 299308.10.1007/s00442-009-1308-yCrossRefGoogle ScholarPubMed
Cambier, V, Hance, T and De Hoffmann, E (2001) Effects of 1, 4-benzoxazin-3-one derivatives from maize on survival and fecundity of Metopolophium dirhodum (Walker) on artificial diet. Journal of Chemical Ecology 27, 359370.10.1023/A:1005636607138CrossRefGoogle ScholarPubMed
Campbell, BC and Duffey, SS (1979) Tomatine and parasitic wasps: potential incompatibility of plant antibiosis with biological control. Science (New York, N.Y.) 205, 700702.10.1126/science.205.4407.700CrossRefGoogle ScholarPubMed
Cardoso, DC, Martinati, JC, Giachetto, PF, Vidal, RO, Carazzolle, MF, Padilha, L, Guerreiro-Filho, O and Maluf, MP (2014) Large-scale analysis of differential gene expression in coffee genotypes resistant and susceptible to leaf miner–toward the identification of candidate genes for marker assisted-selection. BMC Genomics 15, 66.10.1186/1471-2164-15-66CrossRefGoogle ScholarPubMed
Cardoza, YJ, Wang, SF, Reidy-Crofts, J and Edwards, OR (2006) Phloem alkaloid tolerance allows feeding on resistant Lupinus angustifolius by the aphid Myzus persicae. Journal of Chemical Ecology 32, 19651976.10.1007/s10886-006-9121-0CrossRefGoogle ScholarPubMed
Couty, A, Down, R, Gatehouse, A, Kaiser, L, Pham-Delegue, M-H and Poppy, G (2001) Effects of artificial diet containing GNA and GNA-expressing potatoes on the development of the aphid parasitoid Aphidius ervi Haliday (Hymenoptera: Aphidiidae). Journal of Insect Physiology 47, 13571366.10.1016/S0022-1910(01)00111-1CrossRefGoogle Scholar
Couvillon, MJ, Al Toufailia, H, Butterfield, TM, Schrell, F, Ratnieks, FL and Schürch, R (2015) Caffeinated forage tricks honeybees into increasing foraging and recruitment behaviors. Current Biology 25, 28152818.10.1016/j.cub.2015.08.052CrossRefGoogle ScholarPubMed
Cutler, GC and Rix, RR (2015) Can poisons stimulate bees? Appreciating the potential of hormesis in bee-pesticide research: appreciating the potential of hormesis in bee-pesticide research. Pest Management Science 71, 13681370.10.1002/ps.4042CrossRefGoogle ScholarPubMed
Dado, AT, Asresahegn, YA and Goroya, KG (2019) Comparative study of caffeine content in beans and leaves of Coffea arabica using UV/Vis spectrophotometer. International Journal of Physical Science 14, 171176.Google Scholar
Damon, A (2000) A review of the biology and control of the coffee berry borer, Hypothenemus hampei (Coleoptera: Scolytidae). Bulletin of Entomological Research 90, 453465.10.1017/S0007485300000584CrossRefGoogle Scholar
Dearing, MD, Foley, WJ and McLean, S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annual Review of Ecology, Evolution, and Systematics 36, 169189.10.1146/annurev.ecolsys.36.102003.152617CrossRefGoogle Scholar
Dicke, M and Baldwin, IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15, 167175.10.1016/j.tplants.2009.12.002CrossRefGoogle ScholarPubMed
Duffey, SS (1980) Sequestration of plant natural products by insects. Annual Review of Entomology 25, 447477.10.1146/annurev.en.25.010180.002311CrossRefGoogle Scholar
Erb, M and Robert, CA (2016) Sequestration of plant secondary metabolites by insect herbivores: molecular mechanisms and ecological consequences. Current Opinion in Insect Science 14, 811.10.1016/j.cois.2015.11.005CrossRefGoogle ScholarPubMed
Fox, J and Weisberg, HS (2011) An R Companion to Applied Regression, 2nd Edn., Thousand Oaks, CA, USA: Sage.Google Scholar
Gerling, D, Roitberg, BD and Mackauer, M (1990) Instar-specific defense of the pea aphid, Acyrthosiphon pisum: influence on oviposition success of the parasite Aphelinusasychis (Hymenoptera: Aphelinidae). Journal of Insect Behavior 3, 501514.10.1007/BF01052014CrossRefGoogle Scholar
Ghosh, A, Das, A, Lepcha, R, Majumdar, K and Baranwal, V (2015) Identification and distribution of aphid vectors spreading Citrus tristeza virus in Darjeeling hills and Dooars of India. Journal of Asia-Pacific Entomology 18, 601605.10.1016/j.aspen.2015.07.001CrossRefGoogle Scholar
Godfray, HCJ (1994) Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ, USA: Princeton University Press.10.1515/9780691207025CrossRefGoogle Scholar
Gols, R (2014) Direct and indirect chemical defences against insects in a multitrophic framework. Plant, Cell & Environment 37, 17411752.10.1111/pce.12318CrossRefGoogle Scholar
Gonthier, DJ, Witter, JD, Spongberg, AL and Philpott, SM (2011) Effect of nitrogen fertilization on caffeine production in coffee (Coffea arabica). Chemoecology 21, 123130.10.1007/s00049-011-0073-7CrossRefGoogle Scholar
Green, PWC, Davis, AP, Cossé, AA and Vega, FE (2015) Can coffee chemical compounds and insecticidal plants be harnessed for control of major coffee pests? Journal of Agricultural and Food Chemistry 63, 94279434.10.1021/acs.jafc.5b03914CrossRefGoogle ScholarPubMed
Hance, T, Kohandani-Tafresh, F and Munaut, F (2017) Biological control. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests. Wallingford, United Kingdom: CABI Press, pp. 448493.10.1079/9781780647098.0448CrossRefGoogle Scholar
Harvey, JA (2000) Dynamic effects of parasitism by an endoparasitoid wasp on the development of two host species: implications for host quality and parasitoid fitness: development of Cotesia glomerata in different hosts. Ecological Entomology 25, 267278.10.1046/j.1365-2311.2000.00265.xCrossRefGoogle Scholar
Harvey, JA and Gols, R (2018) Effects of plant-mediated differences in host quality on the development of two related endoparasitoids with different host-utilization strategies. Journal of Insect Physiology 107, 110115.CrossRefGoogle ScholarPubMed
Hendricks, JC, Finn, SM, Panckeri, KA, Chavkin, J, Williams, JA, Sehgal, A and Pack, AI (2000) Rest in Drosophila is a sleep-like state. Neuron 25, 129138.10.1016/S0896-6273(00)80877-6CrossRefGoogle ScholarPubMed
Hullé, M, Chaubet, B, Turpeau, E and Simon, J-C (2020) Encyclop'Aphid: a website on aphids and their natural enemies. Entomologia Generalis 40, 97101.CrossRefGoogle Scholar
Infante, F (2018) Pest management strategies against the coffee berry borer (Coleoptera: Curculionidae: Scolytinae). Journal of Agricultural and Food Chemistry 66, 52755280.CrossRefGoogle Scholar
Jaramillo, J, Borgemeister, C and Baker, P (2006) Coffee berry borer Hypothenemus hampei (Coleoptera: Curculionidae): searching for sustainable control strategies. Bulletin of Entomological Research 96, 223233.CrossRefGoogle ScholarPubMed
Keebaugh, ES, Park, JH, Su, C, Yamada, R and Ja, WW (2017) Nutrition influences caffeine-mediated sleep loss in Drosophila. Sleep 40, zsx146.CrossRefGoogle ScholarPubMed
Kim, Y-S, Lim, S, Kang, K-K, Jung, Y-J, Lee, Y-H, Choi, Y-E and Sano, H (2011) Resistance against beet armyworms and cotton aphids in caffeine-producing transgenic chrysanthemum. Plant Biotechnology 28, 393395.CrossRefGoogle Scholar
Kretschmar, JA and Baumann, TW (1999) Caffeine in Citrus flowers. Phytochemistry 52, 1923.CrossRefGoogle Scholar
Mazzafera, P and Gonçalves, KV (1999) Nitrogen compounds in the xylem sap of coffee. Phytochemistry 50, 383386.CrossRefGoogle Scholar
Mendes, VM, Coelho, M, Tomé, AR, Cunha, RA and Manadas, B (2019) Validation of an LC-MS/MS method for the quantification of caffeine and theobromine using Non-matched matrix calibration curve. Molecules 24, 2863.CrossRefGoogle ScholarPubMed
Muñoz, IJ, Schilman, PE and Barrozo, RB (2020) Impact of alkaloids in food consumption, metabolism and survival in a blood-sucking insect. Scientific Reports 10, 9443.CrossRefGoogle Scholar
Mustard, JA (2014) The buzz on caffeine in invertebrates: effects on behavior and molecular mechanisms. Cellular and Molecular Life Sciences 71, 13751382.CrossRefGoogle ScholarPubMed
Mustard, JA (2020) Neuroactive nectar: compounds in nectar that interact with neurons. Arthropod-Plant Interactions 14, 151159.CrossRefGoogle Scholar
Naef, R, Jaquier, A, Velluz, A and Bachofen, B (2004) From the linden flower to linden honey–volatile constituents of linden nectar, the extract of bee-stomach and ripe honey. Chemistry & Biodiversity 1, 18701879.CrossRefGoogle ScholarPubMed
Nall, AH, Shakhmantsir, I, Cichewicz, K, Birman, S, Hirsh, J and Sehgal, A (2016) Caffeine promotes wakefulness via dopamine signaling in Drosophila. Scientific Reports 6, 20938.CrossRefGoogle ScholarPubMed
Nikitin, AG, Navitskas, S and Nicole Gordon, L-A (2008) Effect of varying doses of caffeine on life span of Drosophila melanogaster. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 63, 149150.CrossRefGoogle ScholarPubMed
Ode, PJ (2019) Plant toxins and parasitoid trophic ecology. Current Opinion in Insect Science 32, 118123.CrossRefGoogle ScholarPubMed
Pham, VTT, Ismail, T, Mishyna, M, Appiah, KS, Oikawa, Y and Fujii, Y (2019) Caffeine: the allelochemical responsible for the plant growth inhibitory activity of Vietnamese tea (Camellia sinensis L. Kuntze). Agronomy 9, 396.CrossRefGoogle Scholar
Pirotte, JA-LM, Lorenzi, A, Foray, V and Hance, T (2018) Impact of differences in nutritional quality of wingless and winged aphids on parasitoid fitness. The Journal of Experimental Biology 221, jeb185645.CrossRefGoogle ScholarPubMed
Power, FB and Chesnut, VK (1919) Ilex vomitoria as a native source of caffeine. Journal of the American Chemical Society 41, 13071312.CrossRefGoogle Scholar
Prado, SG, Collazo, JA, Marand, MH and Irwin, RE (2021) The influence of floral resources and microclimate on pollinator visitation in an agro-ecosystem. Agriculture, Ecosystems & Environment 307, 107196.CrossRefGoogle Scholar
Ramsey, JS, Elzinga, DA, Sarkar, P, Xin, Y-R, Ghanim, M and Jander, G (2014) Adaptation to nicotine feeding in Myzus persicae. Journal of Chemical Ecology 40, 869877.CrossRefGoogle ScholarPubMed
R Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rezaei, M, Talebi, A, Fathipour, Y, Karimzadeh, J and Mehrabadi, M (2019) Foraging behavior of Aphidius matricariae (Hymenoptera: Braconidae) on tobacco aphid, Myzus persicae nicotianae (Hemiptera: Aphididae). Bulletin of Entomological Research 109, 840848.CrossRefGoogle Scholar
Sano, H, Kim, Y-S and Choi, Y-E (2013) Like cures like: caffeine immunizes plants against biotic stresses. Advances in Botanical Research 68, 273300.CrossRefGoogle Scholar
Schmidt, A, Brack, V Jr, Rommé, R, Tyrell, K and Gehrt, A (2000) Bioaccumulation of Pesticides in Bats from Missouri. Washington, DC, USA: ACS Publications.CrossRefGoogle Scholar
Schoonhoven, LM, Van Loon, B, van Loon, JJ and Dicke, M (2005) Insect-plant Biology. Oxford, United Kingdom: Oxford University Press.Google Scholar
Sedio, BE (2019) Recent advances in understanding the role of secondary metabolites in species-rich multitrophic networks. Current Opinion in Insect Science 32, 124130.CrossRefGoogle ScholarPubMed
Stevenson, PC, Nicolson, SW and Wright, GA (2017) Plant secondary metabolites in nectar: impacts on pollinators and ecological functions. Functional Ecology 31, 6575.CrossRefGoogle Scholar
Szentesi, A and Wink, M (1991) Fate of quinolizidine alkaloids through three trophic levels: Laburnum anagyroides (Leguminosae) and associated organisms. Journal of Chemical Ecology 17, 15571573.CrossRefGoogle ScholarPubMed
Therneau, TM (2015) Package ‘coxme.’ Mixed Effects Cox Models. R Package Version, 2.Google Scholar
Thomson, JD, Draguleasa, MA and Tan, MG (2015) Flowers with caffeinated nectar receive more pollination. Arthropod-Plant Interactions 9, 17.CrossRefGoogle Scholar
Thurston, R and Fox, P (1972) Inhibition by nicotine of emergence of Apanteles congregatus from its host, the tobacco hornworm. Annals of the Entomological Society of America 65, 547550.CrossRefGoogle Scholar
Tougeron, K and Abram, PK (2017) An ecological perspective on sleep disruption. The American Naturalist 190, E55E66.CrossRefGoogle ScholarPubMed
van Breda, SV, van der Merwe, CF, Robbertse, H and Apostolides, Z (2013) Immunohistochemical localization of caffeine in young Camellia sinensis (L.) O. Kuntze (tea) leaves. Planta 237, 849858.CrossRefGoogle ScholarPubMed
van Emden, HF and Wild, EA (2020) A fully defined artificial diet for Myzus persicae – the detailed technical manual. Entomologia Experimentalis et Applicata 168, 582586.CrossRefGoogle Scholar
Vega, F, Infante, F, Castillo, A and Jaramillo, J (2009) The coffee berry borer, Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae): a short review, with recent findings and future research directions. Terrestrial Arthropod Reviews 2, 129147.Google Scholar
Vet, LE and Dicke, M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141172.CrossRefGoogle Scholar
Wajnberg, É (2006) Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms. Behavioral Ecology and Sociobiology 60, 589611.CrossRefGoogle Scholar
Wright, GA, Baker, DD, Palmer, MJ, Stabler, D, Mustard, JA, Power, EF, Borland, AM and Stevenson, PC (2013) Caffeine in floral nectar enhances a pollinator's memory of reward. Science (New York, N.Y.) 339, 12021204.CrossRefGoogle Scholar
Zepeda-Paulo, F, Simon, J, Ramirez, C, Fuentes-Contreras, E, Margaritopoulos, J, Wilson, A, Sorenson, C, Briones, L, Azevedo, R and Ohashi, D (2010) The invasion route for an insect pest species: the tobacco aphid in the New World. Molecular Ecology 19, 47384752.CrossRefGoogle ScholarPubMed
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