Despite a long tradition of research, our understanding of mechanisms driving prey selectivity in predatory insects is limited. According to optimal foraging theory, predators should prefer prey which provides the highest amount of energy per unit time. However, prey selectivity may also depend on previous diet and specific nutritional demands of the predator. From the long-term perspective, diet composition affects predator fitness. An open question is whether short-term selectivity of predators provides a diet which is optimal in the long-term. To shed more light on these issues, we conducted laboratory experiments on prey selectivity and its long-term consequences in larvae of the dragonfly Sympetrum sanguineum. We conditioned the larvae to one of two prey types, the cladoceran Daphnia magna and larvae of a non-biting midge Chironomus sp., and then exposed them to various combinations of the two prey types. We found that dragonfly larvae conditioned to Chironomus larvae consumed the same amount of D. magna, but significantly less Chironomus larvae compared to dragonfly larvae conditioned to D. magna. However, there was no effect of previous diet on their success of capture and handling time, suggesting a limited role of learning in their ability to process prey. We then tested the long-term effects of diets with different proportions of both prey for survival and growth of the dragonfly larvae. Individuals fed Chironomus-only diet had higher mortality and slower growth than dragonflies fed D. magna, while larvae fed a mixed diet had the highest survival and growth rate. In conclusion, we show that dragonfly larvae fed by Chironomus larvae performed poorly and compensated by preferring D. magna when both prey types were available. The superiority of the mixed diet suggests that a diverse diet may be needed to satisfy nutritional demands in S. sanguineum larvae. We demonstrate that merging short-term predation experiments with relevant data on predator fitness may provide better understanding of predator-prey interactions and conclude that detailed information on the (mis)matches between prey composition and predator nutritional demands is needed for further progress.

Czech Academy of Sciences Biology Centre Institute of Entomology České Budějovice Czech Republic

Department of Ecosystem Biology and Soil and Water Research Infrastructure Faculty of Science University of South Bohemia České Budějovice Czech Republic

Department of Zoology Faculty of Science University of South Bohemia České Budějovice Czech Republic

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Akre BG, Johnson DM. Switching and sigmoid functional response curves by damselfly naiads with alternative prey available. Journal of Animal Ecology. 1979;48(3):703–720. doi: 10.2307/4191. DOI

Allan J, Flecker A, McClintock N. Prey preference of stoneflies: sedentary vs mobile prey. Oikos. 1987;49(3):323–331. doi: 10.2307/3565768. DOI

Baker RL. Condition and size of damselflies: a field study of food limitation. Oecologia. 1989;81(1):111–119. doi: 10.1007/bf00377019. PubMed DOI

Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. Journal of Statistical Software. 2015;67(1):1–48.

Beckerman AP, Petchey OL, Warren PH. Foraging biology predicts food web complexity. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(37):13745–13749. doi: 10.1073/pnas.0603039103. PubMed DOI PMC

Bergelson JM. A mechanistic interpretation of prey selection by Anax junius larvae (Odonata: Aeschnidae) Ecology. 1985;66(6):1699–1705. doi: 10.2307/2937365. DOI

Bernays E, Bright K, Gonzalez N, Angel J. Dietary mixing in a generalist herbivore: tests of two hypotheses. Ecology. 1994;75(7):1997–2006. doi: 10.2307/1941604. DOI

Boukal DS. Trait-and size-based descriptions of trophic links in freshwater food webs: current status and perspectives. Journal of Limnology. 2014;73(s1):171–185. doi: 10.4081/jlimnol.2014.826. DOI

Brett MT, Bunn SE, Chandra S, Galloway AW, Guo F, Kainz MJ, Kankaala P, Lau DC, Moulton TP, Power ME, Rasmussen JB, Taipale SJ, Thorp JH, Wehr JD. How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshwater Biology. 2017;62(5):833–853. doi: 10.1111/fwb.12909. DOI

Brose U, Jonsson T, Berlow EL, Warren P, Banasek-Richter C, Bersier L-F, Blanchard JL, Brey T, Carpenter SR, Blandenier M-FC, Cushing L, Dawah HA, Dell T, Edwards F, Harper-Smith S, Jacob U, Ledger ME, Martinez ND, Memmott J, Mintenbeck K, Pinnegar JK, Rall BC, Rayner TS, Reuman DC, Ruess L, Ulrich W, Williams RJ, Woodward G, Cohen JE. Consumer–resource body-size relationships in natural food webs. Ecology. 2006;87(10):2411–2417. PubMed

Chesson J. The estimation and analysis of preference and its relationship to foraging models. Ecology. 1983;64(5):1297–1304. doi: 10.2307/1937838. DOI

Cooper SD, Smith DW, Bence JR. Prey selection by freshwater predators with different foraging strategies. Canadian Journal of Fisheries and Aquatic Sciences. 1985;42(11):1720–1732. doi: 10.1139/f85-216. DOI

Cumminns KW, Wuycheck JC. Caloric equivalents for investigations in ecological energetics. Internationale Vereinigung für Theoretische und Angewandte Limnologie: Mitteilungen. 1971;18(1):1–158. doi: 10.1080/05384680.1971.11903918. DOI

Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW. Nutritional constraints in terrestrial and freshwater food webs. Nature. 2000;408(6812):578–580. doi: 10.1038/35046058. PubMed DOI

Emlen JM. The role of time and energy in food preference. American Naturalist. 1966;100(916):611–617. doi: 10.1086/282455. DOI

Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ. Nitrogen in insects: implications for trophic complexity and species diversification. American Naturalist. 2002;160(6):784–802. doi: 10.1086/343879. PubMed DOI

Freeland WJ, Janzen DH. Strategies in herbivory by mammals: the role of plant secondary compounds. American Naturalist. 1974;108(961):269–289. doi: 10.1086/282907. DOI

Guo F, Bunn SE, Brett MT, Fry B, Hager H, Ouyang X, Kainz MJ. Feeding strategies for the acquisition of high-quality food sources in stream macroinvertebrates: collecting, integrating, and mixed feeding. Limnology and Oceanography. 2018;63(5):1964–1978. PubMed PMC

Harwood JD, Phillips SW, Lello J, Sunderland KD, Glen DM, Bruford MW, Harper GL, Symondson WO. Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops. Biological Control. 2009;51(3):499–506. doi: 10.1016/j.biocontrol.2009.09.007. DOI

Hirvonen H, Ranta E. Prey to predator size ratio influences foraging efficiency of larval Aeshna juncea dragonflies. Oecologia. 1996;106(3):407–415. doi: 10.1007/bf00334569. PubMed DOI

Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biometrical Journal. 2008;50(3):346–363. doi: 10.1002/bimj.200810425. PubMed DOI

Hottenbacher N, Koch K. Influence of egg size on egg and larval development of Sympetrum striolatum at different prey availability (Odonata: Libellulidae) International Journal of Odonatology. 2006;9(2):165–174. doi: 10.1080/13887890.2006.9748275. DOI

Jensen K, Mayntz D, Toft S, Clissold FJ, Hunt J, Raubenheimer D, Simpson SJ. Optimal foraging for specific nutrients in predatory beetles. Proceedings of the Royal Society B: Biological Sciences. 2012;279(1736):2212–2218. doi: 10.1098/rspb.2011.2410. PubMed DOI PMC

Johansson F. Intraguild predation and cannibalism in odonate larvae: effects of foraging behaviour and zooplankton availability. Oikos. 1993;66(1):80–87. doi: 10.2307/3545198. DOI

Karimi R, Folt CL. Beyond macronutrients: element variability and multielement stoichiometry in freshwater invertebrates. Ecology Letters. 2006;9(12):1273–1283. doi: 10.1111/j.1461-0248.2006.00979.x. PubMed DOI

Klecka J, Boukal DS. Who eats whom in a pool? A comparative study of prey selectivity by predatory aquatic insects. PLOS ONE. 2012;7(6):e37741. doi: 10.1371/journal.pone.0037741. PubMed DOI PMC

Klecka J, Boukal DS. Foraging and vulnerability traits modify predator-prey body mass allometry: freshwater macroinvertebrates as a case study. Journal of Animal Ecology. 2013;82(5):1031–1041. doi: 10.1111/1365-2656.12078. PubMed DOI

Klecka J, Boukal DS. The effect of habitat structure on prey mortality depends on predator and prey microhabitat use. Oecologia. 2014;176(1):183–191. doi: 10.1007/s00442-014-3007-6. PubMed DOI

Koemel NA, Barnes CL, Wilder SM. Metabolic and behavioral responses of predators to prey nutrient content. Journal of Insect Physiology. 2019;116:25–31. doi: 10.1016/j.jinsphys.2019.04.006. PubMed DOI

Lawton J, Beddington J, Bonser R. Switching in invertebrate predators. In: Usher MB, Williamson MH, editors. Ecological Stability. London: Chapman and Hall; 1974. pp. 141–158.

Lefcheck JS, Whalen MA, Davenport TM, Stone JP, Duffy JE. Physiological effects of diet mixing on consumer fitness: a meta-analysis. Ecology. 2013;94(3):565–572. doi: 10.1890/12-0192.1. PubMed DOI

MacArthur RH, Pianka ER. On optimal use of a patchy environment. American Naturalist. 1966;100(916):603–609. doi: 10.1086/282454. DOI

Manly B. A model for certain types of selection experiments. Biometrics. 1974;30(2):281–294. doi: 10.2307/2529649. DOI

Marques RV, Sarmento RA, Lemos F, Pedro-Neto M, Sabelis MW, Venzon M, Pallini A, Janssen A. Active prey mixing as an explanation for polyphagy in predatory arthropods: synergistic dietary effects on egg production despite a behavioural cost. Functional Ecology. 2015;29(10):1317–1324. doi: 10.1111/1365-2435.12439. DOI

Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ. Nutrient-specific foraging in invertebrate predators. Science. 2005;307(5706):111–113. doi: 10.1126/science.1105493. PubMed DOI

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. doi: 10.1111/j.0030-1299.2005.14056.x. DOI

Muñoz-Cárdenas K, Fuentes LS, Cantor RF, Rodríguez CD, Janssen A, Sabelis MW. Generalist red velvet mite predator (Balaustium sp.) performs better on a mixed diet. Experimental and Applied Acarology. 2014;62(1):19–32. doi: 10.1007/s10493-013-9727-1. PubMed DOI

Oelbermann K, Scheu S. Effects of prey type and mixed diets on survival, growth and development of a generalist predator, Pardosa lugubris (Araneae: Lycosidae) Basic and Applied Ecology. 2002;3(3):285–291. doi: 10.1078/1439-1791-00094. PubMed DOI

Ottoni EB. EthoLog 2.2: a tool for the transcription and timing of behavior observation sessions. Behavior Research Methods, Instruments & Computers. 2000;32(3):446–449. PubMed

Petchey OL, Beckerman AP, Riede JO, Warren PH. Size, foraging, and food web structure. Proceedings of the National Academy of Sciences of the United States of America. 2008;105(11):4191–4196. PubMed PMC

Pierce GJ, Ollason J. Eight reasons why optimal foraging theory is a complete waste of time. Oikos. 1987;49(1):111–118. doi: 10.2307/3565560. DOI

Pulliam HR. Diet optimization with nutrient constraints. American Naturalist. 1975;109(970):765–768. doi: 10.1086/283041. DOI

Pyke GH. Optimal foraging theory: a critical review. Annual Review of Ecology and Systematics. 1984;15(1):523–575. doi: 10.1146/annurev.ecolsys.15.1.523. DOI

R Core Team . R: a language and environment for statistical computing. Vienna: The R Foundation for Statistical Computing; 2018.

Raubenheimer D, Simpson SJ. Integrative models of nutrient balancing: application to insects and vertebrates. Nutrition Research Reviews. 1997;10(1):151–179. doi: 10.1079/nrr19970009. PubMed DOI

Raubenheimer D, Simpson SJ, Mayntz D. Nutrition, ecology and nutritional ecology: toward an integrated framework. Functional Ecology. 2009;23(1):4–16. doi: 10.1111/j.1365-2435.2009.01522.x. DOI

Riede JO, Brose U, Ebenman B, Jacob U, Thompson R, Townsend CR, Jonsson T. Stepping in elton’s footprints: a general scaling model for body masses and trophic levels across ecosystems. Ecology Letters. 2011;14(2):169–178. doi: 10.1111/j.1461-0248.2010.01568.x. PubMed DOI

Rowe R. Predatory behaviour and predatory versatility in young larvae of the dragonfly Xanthocnemis zealandica (Odonata, Coenagrionidae) New Zealand Journal of Zoology. 1994;21(2):151–166. doi: 10.1080/03014223.1994.9517983. DOI

Schmidt JM, Sebastian P, Wilder SM, Rypstra AL. The nutritional content of prey affects the foraging of a generalist arthropod predator. PLOS ONE. 2012;7(11):e49223. doi: 10.1371/journal.pone.0049223. PubMed DOI PMC

Sentis A, Morisson J, Boukal DS. Thermal acclimation modulates the impacts of temperature and enrichment on trophic interaction strengths and population dynamics. Global Change Biology. 2015;21(9):3290–3298. doi: 10.1111/gcb.12931. PubMed DOI

Sherratt TN, Harvey IF. Frequency-dependent food selection by arthropods: a review. Biological Journal of the Linnean Society. 1993;48(2):167–186. doi: 10.1006/bijl.1993.1013. DOI

Sih A, Christensen B. Optimal diet theory: when does it work, and when and why does it fail? Animal Behaviour. 2001;61(2):379–390. doi: 10.1006/anbe.2000.1592. DOI

Stephens DW, Krebs JR. Foraging theory. New Jersey: Princeton University Press; 1986.

Sterner RW, Elser JJ. Ecological stoichiometry: the biology of elements from molecules to the biosphere. New Jersey: Princeton University Press; 2002.

Tinbergen L. The natural control of insects in pinewoods: I. factors influencing the intensity of predation by songbirds. Archives Neerlandaises de Zoologie. 1960;13(3):265–343.

Turner AM, Chislock MF. Dragonfly predators influence biomass and density of pond snails. Oecologia. 2007;153(2):407–415. doi: 10.1007/s00442-007-0736-9. PubMed DOI

Waldbauer G, Friedman S. Self-selection of optimal diets by insects. Annual Review of Entomology. 1991;36(1):43–63. doi: 10.1146/annurev.en.36.010191.000355. DOI

Wilder SM, Barnes CL, Hawlena D. Predicting predator nutrient intake from prey body contents. Frontiers in Ecology and Evolution. 2019;7:42. doi: 10.3389/fevo.2019.00042. DOI

Wilder SM, Eubanks MD. Might nitrogen limitation promote omnivory among carnivorous arthropods? Comment. Ecology. 2010;91(10):3114–3117. doi: 10.1890/09-2080.1. PubMed DOI

Woodward G, Hildrew AG. Body-size determinants of niche overlap and intraguild predation within a complex food web. Journal of Animal Ecology. 2002;71(6):1063–1074. doi: 10.1046/j.1365-2656.2002.00669.x. DOI

Woodward G, Warren PH. Body size and predatory interactions in freshwaters: scaling from individuals to communities. In: Hildrew AG, Raffaelli DG, Edmonds-Brown R, editors. Body Size: The Structure and Function of Aquatic Ecosystems. Cambridge: Cambridge University Press; 2007. pp. 98–117.

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