Abstract
Among defenses against predation, chemical defenses are possibly the most studied. However, when addressing the effectiveness of those chemical defenses, previous studies did not include properties of the chemical substances themselves. Lipophilicity, for instance, may facilitate crossing membranes, and boiling point may define the duration of the substances in the air. Moreover, other variables may also be relevant: the predator taxon; the prey model chosen to conduct experiments; whether the prey is presented grouped or not in experiments; and whether the chemical defense is a mixture of many substances or only one. To understand how those factors influence chemical defenses’ effectiveness, we conducted a multilevel meta-analysis with 43 studies (127 effect sizes), accounting for different types of dependence. We used Akaike Information Criterion (AICc) to select the best model. The model with the lowest AICc value included only the boiling point, which defines how quickly a chemical substance volatilizes. This model indicated that the most effective chemical defenses had lower boiling point values, i.e., higher volatility. Moreover, we did not find chemicals with very low boiling points, suggesting there might be an optimum range of volatility. Other models, including the intercept-only model, were also recovered among the best models, therefore further studies are needed to confirm the relationship between volatility and chemical defenses’ effectiveness. Our results highlight the value of incorporating physicochemical properties in the ecological and evolutionary study of chemical defense.
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All data generated or analyzed during this study are included in its supplementary information files, and in the OSF platform: https://osf.io/v7u8q/.
References
Abelian A, Dybek M, Wallach J, Gaye B, Adejare A (2021) Pharmaceutical chemistry. In: Adejare A, editor. Remington: The Science and Practice of Pharmay. 23rd ed. INC. p. 103–128. https://doi.org/10.1016/B978-0-12-820007-0.00006-4
Ache BW, Young JM (2005) Olfaction: diverse species, conserved principles. Neuron 48(3):417–430. https://doi.org/10.1016/j.neuron.2005.10.022
Barnett CA, Skelhorn J, Bateson M, Rowe C (2012) Educated predators make strategic decisions to eat defended prey according to their toxin content. Behav Ecol 23(2):418–424. https://doi.org/10.1093/beheco/arr206
Barnett CRA, Ringhofer M, Suzuki TN (2021) Differences in predatory behavior among three bird species when attacking chemically defended and undefended prey. J Ethol 39(1):29–37. https://doi.org/10.1007/s10164-020-00668-w
Barton K, Barton MK (2020) MuMIn: Multi-Model Inference. R Packag Version 14317(1):18. https://cran.r-project.org/package=MuMIn
Bland M (2015) Estimating Mean and Standard deviation from the sample size, three Quartiles, Minimum, and Maximum. Int J Stat Med Res 4(1):57–64. https://doi.org/10.6000/1929-6029.2015.04.01.6
Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to Meta-Analysis
Briolat ES, Burdfield-Steel ER, Paul SC, Rönkä KH, Seymoure BM, Stankowich T, Stuckert AMM (2019) Diversity in warning coloration: selective paradox or the norm? Biol Rev 94(2):388–414. https://doi.org/10.1111/brv.12460
Camarano S, González A, Rossini C (2006) Chemical defense of the ladybird beetle Epilachna paenulata. Chemoecology 16(4):179–184. https://doi.org/10.1007/s00049-006-0342-z
Carey FA (2000) Organic chemistry, 4th edn. McGraw Hill
ChemSpider | Search and share chemistry. [accessed 2021 Jun 21]. https://www.chemspider.com/
Clark L, Smeraski CA (2022) Chemesthesis and olfaction. Elsevier Inc. https://doi.org/10.1016/B978-0-12-819770-7.00035-9
Clark L, Hagelin J, Werner S (2015) The Chemical Senses in birds. Sixth Edit. Elsevier
Conner WE, Alley KM, Barry JR, Harper AE (2007) Has vertebrate chemesthesis been a selective agent in the evolution of arthropod chemical defenses? Biol Bull 213:267–273
Cronin MD (2006) The role of hydrophobicity in toxicity prediction. Curr Comput Aided-Drug Des 2(4):405–413. https://doi.org/10.2174/157340906778992346
Curley EAM, Rowley HE, Speed MP (2015) A field demonstration of the costs and benefits of group living to edible and defended prey. Biol Lett 11(6):20150152. https://doi.org/10.1098/rsbl.2015.0152
Debboun M, Fraces S, Strickman D (2006) In: Debboun M, Fraces S, Strickman D (eds) Insect repellents: principles, methods, and uses. Taylor & Francis
Drinkwater E, Allen WL, Endler JA, Hanlon RT, Holmes G, Homziak NT, Kang C, Leavell BC, Lehtonen J, Loeffler-Henry K et al (2022) A synthesis of deimatic behaviour. Biol Rev 3. https://doi.org/10.1111/brv.12891
Eisner T, Grant R (1981) Toxicity, odor aversion, and olfactory aposematism. Science 213(4506):476–476. https://doi.org/10.1126/science.7244647
Eisner T, Meinwald J, Monro A, Ghent R (1961) Defence mechanisms of arthropods - I the composition and function of the spray of the whipscorpion, Mastigoproctus giganteus (Lucas) (Arachnida, Pedipalpida). J Insect Physiol 6(4). https://doi.org/10.1016/0022-1910(61)90054-3
Eisner T, Eisner M, Rossini C, Iyengar VK, Roach BL, Benedikt E, Meinwald J (2000) Chemical defense against predation in an insect egg. Proc Natl Acad Sci U S A 97(4):1634–1639. https://doi.org/10.1073/pnas.030532797
Eisthen HL (2002) Why are olfactory systems of different animals so similar? Brain Behav Evol 59(5–6):273–293. https://doi.org/10.1159/000063564
Eliyahu D, Ceballos RA, Saeidi V, Becerra JX (2012) Synergy Versus Potency in the defensive secretions from Nymphs of two Pentatomomorphan families (Hemiptera: Coreidae and Pentatomidae). J Chem Ecol 38(11):1358–1365. https://doi.org/10.1007/s10886-012-0200-0
Elkinton JS, Cardé RT (1984) Odor dispersion. In: Bell WJ, Cardé RT, editors. Chemical Ecology of Insects. Chapman and Hall. p. 524
Fernández-Castilla B, Declercq L, Jamshidi L, Beretvas SN, Onghena P, Van den Noortgate W (2021) Detecting selection Bias in Meta-Analyses with multiple outcomes: a Simulation Study. J Exp Educ 89(1):125–144. https://doi.org/10.1080/00220973.2019.1582470
Fordyce JA, Malcolm SB (2000) Specialist weevil, Rhyssomatus lineaticollis, does not spatially avoid cardenolide defenses of common milkweed by ovipositing into pith tissue. J Chem Ecol 26(12):2857–2874. https://doi.org/10.1023/A:1026450112601
Fordyce JA, Nice CC (2008) Antagonistic, stage-specific selection on defensive chemical sequestration in a toxic butterfly. Evolution 62(7):1610–1617. https://doi.org/10.1111/j.1558-5646.2008.00388.x
Gangur AN, Smout M, Liddell MJ, Seymour JE, Wilson D, Northfield TD (2017) Changes in predator exposure, but not in diet, induce phenotypic plasticity in scorpion venom. Proc R Soc B: Biol Sci 284(1863):20171364. https://doi.org/10.1098/rspb.2017.1364
Glendinning JI (1990) Responses of three mouse species to deterrent chemicals in the monarch butterfly. II. Taste tests using intact monarchs. Chemoecology 1(3–4):124–130. https://doi.org/10.1007/BF01241653
Halpin CG, Skelhorn J, Rowe C (2014) Increased predation of nutrient-enriched aposematic prey. Proc R Soc B Biol Sci 281(1781):20133255. https://doi.org/10.1098/rspb.2013.3255
Hare JF, Eisner T (1993) Pyrrolizidine alkaloid deters ant predators of Utetheisa ornatrix eggs: effects of alkaloid concentration, oxidation state, and prior exposure of ants to alkaloid-laden prey. Oecologia 96(1):9–18. https://doi.org/10.1007/BF00318024
Heethoff M (2012) Regeneration of complex oil-gland secretions and its importance for chemical defense in an oribatid mite. J Chem Ecol 38:1116–1123. https://doi.org/10.1007/s10886-012-0169-8
Higginson AD, Ruxton GD (2009) Dynamic state-dependent modelling predicts optimal usage patterns of responsive defences. Oecologia 160:399–410. https://doi.org/10.1007/s00442-009-1296-y
John A, Weisberg S, Price B, Adler D, Bates D, Baud-bovy G, Bolker B, Ellison S, Graves S, Heiberger R et al (2022) Package ‘car.’
Johnson HL, Skinner WA (1968) Topical mosquito repellents. II. Repellent potency and duration in Ring-Substituted, N,N-DialkyI- and -Aminoalkylbenzamides. J Med Chem 11(6):1265–1268. https://doi.org/10.1021/jm00312a612
Jones RS, Speed MP, Mappes J (2016) Parameterising a public good: how experiments on predation can be used to predict cheat frequencies. Evol Ecol 30:825–840. https://doi.org/10.1007/s10682-016-9851-6
Kajita Y, Obrycki JJ, Sloggett JJ, Haynes KF (2010) Intraspecific alkaloid variation in ladybird eggs and its effects on con- and hetero-specific intraguild predators. Oecologia 163(2):313–322. https://doi.org/10.1007/s00442-009-1551-2
Kim S, Chen J, Cheng T, Gindulyte A, He J, He S, Li Q, Shoemaker BA, Thiessen PA, Yu B et al (2021) PubChem in 2021: New data content and improved web interfaces. Nucleic Acids Res 49(D1):D1388–D1395. https://doi.org/10.1093/nar/gkaa971
Lahti DC (2015) The limits of Artificial Stimuli in behavioral research: the Umwelt Gamble. Ethology 121(6):529–537. https://doi.org/10.1111/eth.12361
Lajeunesse MJ (2009) Meta-analysis and the comparative phylogenetic method. 174(3). https://doi.org/10.1086/603628
Marples NM, Speed MP, Thomas RJ (2018) An individual-based profitability spectrum for understanding interactions between predators and their prey. Biol J Linn Soc 125(1):1–13. https://doi.org/10.1093/BIOLINNEAN/BLY088
Mason JR, Bean NJ, Shah PS, Clark L (1991) Taxon-specific differences in responsiveness to capsaicin and several analogues: correlates between chemical structure and behavioral aversiveness. J Chem Ecol 17(12):2539–2551. https://doi.org/10.1007/BF00994601
Masterton WL, Hurley CN, Neth E (2011) Chemistry: principles and reactions. Brooks Cole
Nakagawa S, Santos ESA (2012) Methodological issues and advances in biological meta-analysis. Evol Ecol 26(5):1253–1274. https://doi.org/10.1007/s10682-012-9555-5
Nerio LS, Olivero-Verbel J, Stashenko E (2010) Repellent activity of essential oils: a review. Bioresour Technol 101(1):372–378. https://doi.org/10.1016/j.biortech.2009.07.048
Pasteels JM, Gregoire JC, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Annu Rev Entomol 28:1:263–289. https://doi.org/10.1146/annurev.en.28.010183.001403
Roth LM, Eisner T (1962) Chemical Defenses of Arthropods. Annu Rev Entomol 7(1):107–136. https://doi.org/10.1146/annurev.en.07.010162.000543
Rowland HM, Ruxton GD, Skelhorn J (2013) Bitter taste enhances predatory biases against aggregations of prey with warning coloration. Behav Ecol 24(4):942–948. https://doi.org/10.1093/beheco/art013
Schmidtberg H, Röhrich C, Vogel H, Vilcinskas A (2013) A switch from constitutive chemical defence to inducible innate immune responses in the invasive ladybird Harmonia axyridis. Biol Lett 9(3):20130006. https://doi.org/10.1098/rsbl.2013.0006
Silveira HC, Oliveira PS, Trigo JR (2010) Attracting predators without falling prey: chemical camouflage protects honeydew-producing treehoppers from ant predation. Am Nat 175(2):261–268. https://doi.org/10.1086/649580
Skelhorn J (2011) Colour biases are a question of conspecifics’ taste. Anim Behav 81(4):825–829. https://doi.org/10.1016/j.anbehav.2011.01.017
Skelhorn J, Rowe C (2007) Automimic frequency influences the foraging decisions of avian predators on aposematic prey. Anim Behav 74(5):1563–1572. https://doi.org/10.1016/j.anbehav.2007.03.021
Skelhorn J, Griksaitis D, Rowe C (2008) Colour biases are more than a question of taste. Anim Behav 75(3):827–835. https://doi.org/10.1016/j.anbehav.2007.07.003
Speed MP, Ruxton GD (2014) Ecological pharmacodynamics: prey toxin evolution depends on the physiological characteristics of predators. Anim Behav 98:53–67. https://doi.org/10.1016/j.anbehav.2014.09.011
Speed MP, Ruxton GD, Mappes J, Sherratt TN (2012) Why are defensive toxins so variable? An evolutionary perspective. Biol Rev 87(4):874–884. https://doi.org/10.1111/j.1469-185X.2012.00228.x
Speight JG (2017) Properties of Organic Compounds. In: Environmental Organic Chemistry for Engineers. Butterworth-Heinemann. p. 203–261
Startek JB, Voets T, Talavera K (2019) To flourish or perish: evolutionary TRiPs into the sensory biology of plant-herbivore interactions. Pflugers Arch Eur J Physiol 471(2):213–236. https://doi.org/10.1007/s00424-018-2205-1
Sugiura S, Sato T (2018) Successful escape of bombardier beetles from predator digestive systems. Biol Lett 14(2):20170647. https://doi.org/10.1098/rsbl.2017.0647
Tambe V, Ditani A, Rajpoot K, Tekade RK (2021) Pharmacokinetics aspects of structural modifications in drug design and therapy. In: Biopharmaceutics and Pharmacokinetics Considerations. INC p. 83–108
Tewksbury JJ, Nabhan GP, Norman D, Suzán H, Tuxill J, Donovan J (1999) In situ conservation of wild chiles and their biotic associates. Conserv Biol 13(1):98–107. https://doi.org/10.1046/j.1523-1739.1999.97399.x
Thompson CG, Kim RS, Aloe AM, Becker BJ (2017) Extracting the Variance inflation factor and other Multicollinearity Diagnostics from typical regression results. Basic Appl Soc Psych 39(2):81–90. https://doi.org/10.1080/01973533.2016.1277529
Tschinkel WR (1975) A comparative study of the chemical defensive system of tenebrionid beetles: Chemistry of the secretions. J Insect Physiol 21(4):753–783. https://doi.org/10.1016/0022-1910(75)90008-6
van Geem M, Harvey JA, Gols R (2014) Development of a generalist predator, Podisus maculiventris, on glucosinolate sequestering and nonsequestering prey. Sci Nat 101:707–714. https://doi.org/10.1007/s00114-014-1207-x
Viechtbauer W (2010) Conducting Meta-analyses in R with the metafor Package. J Stat Softw 36(3):1–48. https://doi.org/10.1103/PhysRevB.91.121108
Viechtbauer W (2020) Model checking in Meta-Analysis. In: Schmid CH (ed) Handbook of Meta-Analysis, 1st edn. CRC Press, pp 219–254
Vollhardt KP, Schore NE (2013) Química Orgânica: Estrutura e Função.Whitman DW, Andrés MF, Martínez-Díaz RA, Ibáñez-Escribano A, Olmeda AS, González-Coloma A 2019. Antiparasitic properties of cantharidin and the blister beetle Berberomeloe majalis (Coleoptera: Meloidae). Toxins, 11(4):234. https://doi.org/10.3390/toxins11040234
Wink M, Theile V (2002) Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Pharmacia 46:29–46. https://doi.org/10.1007/s00049-002-8324-2
Wyatt TD (2003) Animals in a Chemical World. Pheromones and animal Behaviour: communication by smell and taste. Cambridge University Press, pp 1021–1022
Zhang S, Koh TH, Seah WK, Lai YH, Elgar MA, Li D (2012) A novel property of spider silk: Chemical defence against ants. Proc R Soc B Biol Sci 279(1734):1824–1830
Züst T, Mou S, Agrawal AA (2018) What doesn’t kill you makes you stronger: the burdens and benefits of toxin sequestration in a milkweed aphid. Funct Ecol 32(8):1972–1981. https://doi.org/10.1111/1365-2435.13144
Zvereva EL, Kozlov MV (2016) The costs and effectiveness of chemical defenses in herbivorous insects: A meta‐analysis. Ecol Monogr 86(1):107–124. https://doi.org/10.1890/15-0911.1
Acknowledgements
We are grateful to Vítor Marques that kindly contributed to the figures’ design, Renato Chaves de Macedo Rego, Pedro Gnaspini and Daniel Pessoa for their comments on an early draft of this paper.
Funding
This work was supported by Coordenação de Aperfeicoamento de Pessoal de Nível Superior 88887.364513/2019-00; and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) 2021/02098-4 scholarships awarded to NGX; and by the Animal Behavior Society (ABS) Latin American Travel Award, which allowed NGX to present these results in the ABS in-person meeting. This study also benefited from FAPESP 2020/05158-5 and Conselho Nacional de Desenvolvimento Científico e Tecnológico 302879/2016-1 to RHW.
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All authors contributed to the study conception and design. Material preparation, and data collection were conducted by NGX and VSM. Statistical analyses were performed by NGX and reviewed by FMG. The first draft of the manuscript was written by NGX. RHW and FMG commented on versions of the manuscript. All authors read and approved the final manuscript.
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Nathalia, X., Vinicius, M., Danilo Brito, R. et al. The Influence of Substance Properties on Arthropod Chemical Defenses: A Meta-Analysis. J Chem Ecol 50, 42–51 (2024). https://doi.org/10.1007/s10886-023-01457-8
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DOI: https://doi.org/10.1007/s10886-023-01457-8